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Results and Problems in Cell Differentiation 63
Malgorzata Kloc Editor
Oocytes
Maternal Information and Functions
Results and Problems in Cell Differentiation
Volume 63
Series editors
Jacek Z. Kubiak, Rennes, France
Malgorzata Kloc, Houston, TX, USA
More information about this series at http://www.springer.com/series/400
Malgorzata Kloc
Editor
Oocytes
Maternal Information and Functions
Editor
Malgorzata Kloc
Department of Surgery
The Houston Methodist Hospital
Houston, TX
USA
The Houston Methodist Research Institute
Houston, TX
USA
Department of Genetics
MD Anderson Cancer Center
The University of Texas
Houston, TX
USA
ISSN 0080-1844 ISSN 1861-0412 (electronic)

Results and Problems in Cell Differentiation
ISBN 978-3-319-60854-9 ISBN 978-3-319-60855-6 (eBook)
DOI 10.1007/978-3-319-60855-6
Library of Congress Control Number: 2017948675
© Springer International Publishing AG 2017

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Preface
The oocytes are female germline cells that after maturation become fertilizable
female gametes/eggs. Animal oocytes are produced during a lengthy process of
oogenesis that manufactures and assembles highly specialized oocyte infrastructure
and culminates with entry into meiosis. Oocytes are very unique in combining
generic cellular features with specialized structures, maternal information and
functions, necessary to support the development of future embryo and ensuring
hereditary continuity of maternal nuclear and cytoplasmic information.
The first part of this volume describes how invertebrate and vertebrate oocytes
communicate and exchange information with somatic cells, extracellular environment
and symbiotic organisms. The second part describes how structural, cellular, organellar
and molecular polarity of oocytes is established and what the developmental
consequences of polar distribution of maternal information are. The third part concen-
trates on epigenetic, transcriptional and translational mechanisms regulating heredity
and expression of maternal information. The fourth part focuses on oocyte/egg-specific
features and functions of generic cellular organelles and components, such as
centrioles, mitochondria, lipids and vitellogenin, and the role of cohesin and condensin,
which convey proper topology of chromosomes through the ubiquitous cell cycle, in
the meiotic chromosomal events and age-related chromosome segregation errors.
Finally, the last part of the volume describes the origin and evolution of the
subpopulation of maternal genes and analyses how non-inheritable maternal informa-
tion present in the oocyte can be used for genetic manipulation and engineering.
Houston, TX Malgorzata Kloc
v
Abstract
This book combines the most recent knowledge on the maternal, i.e. oocyte/egg-
specific, molecules and processes. The volume covers the most recent advances in a
plethora of subjects such as maternal localized RNAs, functions and mechanisms of
RNA localization, transcriptional repression of maternal messages, maternal
inheritance and maternal role of CRISPR/Cas9-based genome editing (the
CRISPR/Cas system is a prokaryotic immune system that confers resistance to
foreign genetic elements such as plasmids and phages and provides a form of
acquired immunity), chromatin remodelling and epigenetic modifications, maternal
function of nucleosomes, maternal mitochondria and energy supply, role of bacterial
symbionts and their maternal transmission, acquisition of oocyte polarity and
evolution of maternal effect genes, germ plasm and oosome origin and functions,
mechanisms of oocyte activation and soma-germ cell communication. There is no
other book in existence, which would combine such a comprehensive list of subjects
in one volume. This book is also exceptional and unique in providing the information
that is a cross-section through oocytes from various invertebrate and vertebrate
species. This will give the readers a completely new and invaluable perspective on
all covered subjects.
vii
Contents
Part I Oocyte Interactions with Environment

1 Exogenous Molecule and Organelle Delivery in Oogenesis . . . . . . . 3
Malgorzata Kloc and Jacek Z. Kubiak
2 Control of Mammalian Oocyte Development by Interactions with
the Maternal Follicular Environment . . . . . . . . . . . . . . . . . . . . . . . 17
Hugh Clarke
3 Transovarial Transmission of Symbionts in Insects . . . . . . . . . . . . 43
Teresa Szklarzewicz and Anna Michalik
Part II Oocyte Polarity: Molecular and Organellar Aspects

and Developmental Consequences
4 Acquisition of Oocyte Polarity . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
Mara Clapp and Florence L. Marlow
5 The Pole (Germ) Plasm in Insect Oocytes . . . . . . . . . . . . . . . . . . . . 103
Szczepan M. Bilinski, Mariusz K. Jaglarz, and Waclaw Tworzydlo
6 Multiple Functions of the DEAD-Box Helicase Vasa
in Drosophila Oogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Mehrnoush Dehghani and Paul Lasko
7 The Role of Microtubule Motors in mRNA Localization
and Patterning Within the Drosophila Oocyte . . . . . . . . . . . . . . . . . 149
Chandler H. Goldman and Graydon B. Gonsalvez
8 Phosphoinositides and Cell Polarity in the Drosophila
Egg Chamber . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
Julie Jouette, Sandra Claret, and Antoine Guichet
ix
x Contents
9 RNA Localization in the Vertebrate Oocyte: Establishment

of Oocyte Polarity and Localized mRNA Assemblages . . . . . . . . . . 189
Denise Oh and Douglas W. Houston
Part III Epigenetic, Transcriptional and Translational

Regulation in Oocytes
10 DNA Methyltransferases in Mammalian Oocytes . . . . . . . . . . . . . . 211
Fatma Uysal and Saffet Ozturk
11 Accumulation of Chromatin Remodelling Enzyme and Histone
Transcripts in Bovine Oocytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
V. Lodde, A.M. Luciano, F. Franciosi, R. Labrecque, and M.A. Sirard
12 Translational Regulation in the Mammalian Oocyte . . . . . . . . . . . . 257
Andrej Susor and Michal Kubelka
13 Regulation of Translationally Repressed mRNAs in Zebrafish
and Mouse Oocytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297
Tomoya Kotani, Kaori Maehata, and Natsumi Takei
14 Switches in Dicer Activity During Oogenesis and Early
Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325
Mandy Yu Theng Lim and Katsutomo Okamura
Part IV Oocyte Specific Functions of Ubiquitous Molecules

and Organelles
15 The Regulation and Function of Cohesin and Condensin
in Mammalian Oocytes and Spermatocytes . . . . . . . . . . . . . . . . . . 355
Jibak Lee
16 Supply and Demand of Energy in the Oocyte and the Role
of Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 373
Wilding Martin
17 Functions of Vitellogenin in Eggs . . . . . . . . . . . . . . . . . . . . . . . . . . 389
Hongyan Li and Shicui Zhang
18 Lipids in Insect Oocytes: From the Storage Pathways to Their
Multiple Functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403
Leonardo L. Fruttero, Jimena Leyria, and Lilián E. Canavoso
19 Parthenogenesis in Insects: The Centriole Renaissance . . . . . . . . . . 435
Maria Giovanna Riparbelli, Marco Gottardo, and Giuliano Callaini
Contents xi
Part V Maternal Factors: Origin, Evolution and Application

in Genetic Engineering
20 The Origin and Evolution of Maternal Genes . . . . . . . . . . . . . . . . . 483
Antonio Marco
21 Noninheritable Maternal Factors Useful for Genetic Manipulation
in Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 495
Takayuki Sakurai, Takayuki Shindo, and Masahiro Sato
Part I
Oocyte Interactions with Environment
Chapter 1
Exogenous Molecule and Organelle Delivery
in Oogenesis
Malgorzata Kloc and Jacek Z. Kubiak
Abstract Recent discoveries on the delivery of small- and large-size molecules

and organelles to the oocytes/eggs from external sources, such as surrounding
somatic cells, body fluids, and sperm, change our understanding of female germ
cells’ (oocytes and eggs) self-containment and individuality. In this chapter, we will
summarize present-day knowledge on sources and presumptive functions of differ-
ent types of exogenous molecules and organelles delivered to the animal oocytes
and eggs.
1.1 Internal Versus External Source

of Oocyte-/Egg-Specific Molecules
One of the oldest and most firmly established paradigms of developmental biology
is a strict division between the germ line and soma. Such tenet assumes that the
germ cells, which form during lengthy process of gametogenesis, are transcription-
ally and translationally self-sufficient and independent from the surrounding
somatic cells. This concept of self-containment and self-reliance is especially
pronounced in female germ cells that have been believed to be the sole source of
maternally produced and inherited molecules, organelles, and maternal determi-
nants (Kloc et al. 1998, 2004, 2008, 2016a, b; Tworzydlo et al. 2010a, b). Although
in certain types of oogenesis (e.g., in mouse), the growing oocytes receive
M. Kloc (*)
The Houston Methodist Research Institute, Houston, TX, USA
Department of Surgery, The Houston Methodist Hospital, 6550 Fannin St., Houston, TX
77030, USA
e-mail: mkloc@houstonmethodist.org
J.Z. Kubiak
CNRS UMR 6290, Cell Cycle Group, Institute of Genetics and Development of Rennes,
Rennes, France
University of Rennes 1, Faculty of Medicine, Rennes, France
Department of Regenerative Medicine, Military Institute of Hygiene and Epidemiology
(WIHE), Warsaw, Poland
© Springer International Publishing AG 2017 3

M. Kloc (ed.), Oocytes, Results and Problems in Cell Differentiation 63,
DOI 10.1007/978-3-319-60855-6_1
4 M. Kloc and J.Z. Kubiak
Only one cystocyte becomes the oocyte

while sibling cystocytes become either
nurse cells or “aborted” oocytes
All
cystocytes
become
oocytes
mitoses
Cystoblast Fully grown oocyte
Cystocytes
Growth without division
Fig. 1.1 Cross talk between somatic cells and germ cells during oogenesis. Oogenesis starts with
the cystoblasts that originate from the primordial germ cells. There are three types of oogenesis
depending on the fate of the cystoblast. (1) The cystoblast does not divide but grows and develops
into a single oocyte/egg (some insect species with panoistic ovaries). (2) The cystoblast divides
several times with incomplete cytokinesis giving rise to the cyst of sister cystocytes connected by
intercellular bridges (ring canals). The cystocyte, which has the highest number of bridges and
inherited the oldest bridge, becomes the oocyte/egg, and the rest of the cystocytes become the
nurse cells (insects with meroistic ovaries) or “aborted” oocytes (mouse), which play a “nursing”
role by transferring their molecular and organellar components to the oocyte, and eventually
disintegrate. (3) All cystocytes become the oocytes/eggs (Xenopus). The cystoblast is located in
the somatic cell niche. The cystocytes are surrounded by prefollicular cells (dark blue) and the
oocyte is surrounded by follicular cells (light blue). The somatic cells exchange reciprocally with
the cystocytes and oocytes/eggs various molecules (see the main text). In addition nurse cells
and/or “aborted” oocytes deliver molecules and organelles to the cystocytes and oocyte via
cytoplasmic bridges
additional molecular and organellar supplies from the “aborted” oocytes (Lei and
Spradling 2016) or the accompanying nurse cells (e.g., in many insect species;
Jaglarz et al. 2008; Tworzydlo et al. 2010a, b), both the “aborted” oocytes and the
nurse cells are the oocyte’s siblings (cystocytes) derived from the division of a
common precursor cell (cystoblast; Brubacher and Huebner 2011; Kloc et al.
2016a, b; Lei and Spradling 2016; Fig. 1.1). Thus, all these cells belong to the
germ line, and the materials they produce and deliver to the oocyte are also germ
line-derived (Fig. 1.1). However, over the years, studies have shown various
instances of delivery of exogenous, somatic-derived molecules to the female and
male germ cells (El-Hayek and Clarke 2016; Kloc et al. 2016a, b; Chap. 2). In
addition, there are numerous examples of bidirectional communication between
female germ cells and surrounding somatic cells (Buccione et al. 1990; Gilchrist
1 Exogenous Molecule and Organelle Delivery in Oogenesis 5
et al. 2004; Guo et al. 2016; Monniaux 2016; Moussaddykine et al. 2012; Russell
et al. 2016; Wigglesworth et al. 2013). These discoveries blur the germ cell/soma
demarcation line forcing us to rethink the independence and individuality of germ
cells and to envisage the germ cells and surrounding somatic cells not as indepen-
dent entities but as a functional “syncytium.”
1.2 Exogenous Molecules, Their Sources and Routs

of Delivery to the Oocyte/Egg
During the whole process of oogenesis (oogonial divisions, formation of the oocyte,
subsequent oocyte growth, and egg maturation), the cells of female germ line
remain in intimate contact with somatic (prefollicular and follicular cells) compo-
nent (Fig. 1.2; Ackert et al. 2001; Buccione et al. 1990), and the ovary, as a whole,
is bathed with body fluids. These two milieus are constantly exchanging a multitude
of components with the germ cells. The routs employed in these exchanges are
determined by the size and identity of the cargo: small molecules are transferred
through the gap junctions, while large ones by endocytosis and/or gametic synapses
and tunneling nanotubes.
1.2.1 Exchange Through the Gap Junctions
The somatic cells are connected to the oocyte and between themselves by the gap
junctions. The gap junctions are the intercellular channels formed by the apposition
of two cylindrical hemichannels (composed of various connexin, innexin, or
pannexin proteins) situated in the neighboring cells (Fig. 1.2; Evans 2015). The gap
junctions transfer to the oocyte small molecules such as less than 1000 Da proteins,
small metabolites, ions, nucleotides, amino acids, and meiotic maturation regulatory
molecules and secondary messengers (e.g., cAMP and cGMP; Ackert et al. 2001;
Wigglesworth et al. 2013). Majority of data on gap junction transfer between the
somatic cells and oocyte comes from the studies of mammalian oocytes. It was shown
in mammals that the gap junctions between oocyte and cumulus cells participate in
transfer of ribonucleosides (Heller and Shultz 1980). The meiotic arrest of mamma-
lian oocyte is imposed by cGMP produced and delivered by somatic cells, while
reciprocally the oocyte transfers various paracrine factors to the somatic cells regu-
lating their cGMP levels (Wigglesworth et al. 2013). This interchange between germ
line and somatic cells plays a key role in regulation of mammalian reproduction.
It seems that the gap junctions play a similar role in invertebrate gametogen-
esis. In Drosophila ovary, the gap junctions between somatic cells contain
innexins 2 and 3, while those between follicular cells and germ line cells contain
innexins 2 and 4. The experimental interference with innexin 2 disrupts follicular
A B
Somatic cell
Small molecules
and ions
Germ cell
Long RNAs
Hemichannel Large proteins
Organelles
Gap Junction Gametic synapse (TZP)
C D
miRNAs
proteins
RNAs viruses
Large proteins
Somatic cell
Germ cell
Cumulus cells Theca
Follicular
Body fluids fluid
Tunneling nanotube Microvesicles and Exosomes
Fig. 1.2 Different routes of molecule and organelle delivery in oogenesis. (a) The gap junctions
are located between the germ cells and somatic cells and also between neighboring somatic cells.
Gap junctions are intercellular channels formed by the apposition of two cylindrical hemichannels
(composed of various connexin, innexin, or pannexin proteins). They transfer small molecules
such as ions, secondary messengers, and peptides between cells. (b) The gametic synapses
(transzonal projections, TZP) have been observed between cumulus cells in bovine oocytes
(Macaulay et al. 2014, 2016). They resemble synapse of neural cells. Gamete synapse has a
membrane; thus, there is no direct connection between the cytoplasm of oocyte and somatic cells.
The transfer of large-size molecules such as long noncoding (Lnc) RNAs and mRNAs and
potentially (this was not proven, marked in figure by “?”) organelles such as mitochondria occurs
through the vesicles budding from the end of the synapse. (c) Tunneling nanotubes (TNTs) have
been described between many different types of somatic cells. So far the only example of tunneling
nanotubes between somatic cells and oocytes are TNT-like projections in insect oogenesis
(Tworzydlo et al. 2010a, b). TNTs transfer molecules not larger than 200 nm (which is their
largest diameter). (d) Vesicular transport via microvesicles and exosomes from body fluids
(surrounding the whole ovary) or follicular fluid surrounding follicle (in mammals follicle is
composed of egg enveloped by cumulus/granulosa cells and multilayered theca outside) delivers
yolk proteins, enzymes, hormones, retrotransposons, and miRNAs
cell differentiation, oocyte growth, and choriogenesis and prevents dissipation of

nurse cells (Bohrmann and Zimmermann 2008). In addition, the centripetal
follicular cells (cFC) that reside at the anterior region of the oocyte contain
distinct subpopulation of innexin-3-containing gap junctions, which regulate ion
exchange and tension-dependent signaling that in turn regulates tissue integrity
(Kruger and Bohrmann 2015). Recent studies showed that similar to Drosophila,
the gonad of Caenorhabditis elegans has two different types of gap junctions with
different composition and functions. Gap junctions, which regulate proliferation

and differentiation of germ cells, are composed of innexins 8, 9, 14, and 21, and
those which regulate oocyte maturation contain innexins 8, 9, 14, and 22 (Starich
et al. 2014). Although genetic studies in C. elegans and Drosophila showed that
these differently composed gap junctions are necessary for their specific func-
tions, we still do not know why they require different molecular composition.
Interestingly, in Drosophila the gap junctions are also involved in the transmis-
sion of retrotransposons from somatic cells to the oocytes. Certain lines of
Drosophila flies contain retrovirus ZAM (belonging to the gypsy family of
retrotransposons) that is transferred from follicular cells to the oocyte using
exocytosis/endocytosis pathway involved in vitellogenin uptake (see below) and
also requires signaling through the gap junctions (Brasset et al. 2006).
1.2.2 Transfer from Body Fluids
In many invertebrates and vertebrates, the oocyte growth phase includes accumula-
tion of large amounts of yolk precursor proteins, such as vitellogenin, in the oocyte/
egg cytoplasm. After fertilization the yolk accumulated in the egg will be used to
support embryonic development. In vertebrates the vitellogenin is produced by the
liver, and after being released into the blood, it is endocytotically taken up by the
growing oocyte. In frog Xenopus laevis, the oocyte growth has been divided into six
stages: Stages I–II are previtellogenic oocytes and stages III–VI are vitellogenic
oocytes that accumulate vitellogenin and other yolk proteins (e.g., EP45, Marteil
et al. 2010). Experimental studies in frogs showed that follicular cells surrounding the
oocytes regulate their vitellogenin uptake and that defolliculated (denuded) oocytes
will uptake vitellogenin supplied in the culture medium indefinitely (Wallace et al.
1981). In frogs, insects, and crabs, the endocytic uptake of yolk protein during
vitellogenic phase of oocyte growth is regulated by the gap junctions and cAMP
signaling from the somatic cells (Anderson and Woodruff 2001; Luque et al. 2013;
Medeiros et al. 2004; Monaco et al. 2007). Interestingly, recent studies indicate that
yolk proteins such as vitellogenin, phosvitin (Pv), lipovitellin (Lv), and yolk-derived
small peptides that are stored in egg as the nutrients for embryo development have
also potent antimicrobial, antiviral, and immune defense activities in developing fish
embryos (Liu et al. 2011; Sun et al. 2013; Tong et al. 2010; Zhang et al. 2015),
Caenorhabditis elegans (Fischer et al. 2013), and metazoan coral Euphyllia ancora
(Du et al. 2016). They also regulate senescence and aging in honeybees (Aurori et al.
2014). In addition, in Drosophila, the vesicular trafficking of yolk granules during
vitellogenesis participates in transfer of retrotransposons ZAM (infectious entities
similar to vertebrate retrovirus) from the follicular cells to the oocyte (see above;
Leblanc et al. 2000). Minervini et al. (2010) showed experimentally that the sequence
located in the 50 UTR of the Drosophila ZAM plays a role of the “insulator”
(chromatin boundary DNA element) that organizes chromatin into regulatory
domains and modulates range of enhancer activity through a “positional-blocking
mechanism.” The most recent studies showed that in Caenorhabditis elegans double-
stranded RNA (dsRNA) present in extracellular space is transported within vesicles
into the oocytes along with yolk. Subsequently this extracellular dsRNA is transferred
between generations to cause gene silencing (Marré et al. 2016).
In mammals, ovarian follicles built of single oocyte surrounded by granulosa
cells are bathed in ovarian follicular fluid (Fig. 1.2). Follicular fluid contains
component of blood plasma and products secreted by surrounding the oocyte
granulosa and thecal cells. Beside various hormones (FSH, GH, LH, estrogens,
and androgens), proteins, peptides, amino acids, nucleotides, mucopolysaccha-
rides, and enzymes, the follicular fluid contains subpopulation of microvesicles
and exosomes rich in various microRNAs (Hung et al. 2015; Kloc et al. 2016a, b;
da Silveira et al. 2012; Sohel et al. 2013), which upon delivery to the oocytes and
eggs can affect their transcription, translation, and control the stability of mater-
nal transcripts (Dallaire and Simard 2016; Grossman and Shalgi 2016). Exosomes
are small (30–150 nm) endocytic membranous vesicles. They form inside the cell
through endosome/multivesicular body (MVB) pathway, in which they acquire
various cytoplasmic, membrane-bound, and/or nuclear components (Kloc et al.
2016a, b). Recently, the exosomal miRNAs, which can regulate ubiquitin,
neurotrophin, and insulin as well as MAPK signaling, have been found in bovine
follicular fluid. They had been shown to regulate levels of mRNAs in follicular
cells in vitro (Sohel et al. 2013). It is reasonable to assume that some of these
miRNA will end up in the oocytes and eggs where they can regulate maternal,
and following fertilization also zygotic, transcripts (Dallaire and Simard 2016;
Grossman and Shalgi 2016). Recently it has also been shown that mouse oocytes
reciprocally regulate, via paracrine signaling, expression of miRNAs in ovarian
granulosa cells (Sumitomo et al. 2016).
1.2.3 Transfer of Large-Size Molecules Through the Gametic

Synapses and Tunneling Nanotubes
Until recently the common belief was that only small-size molecules are delivered
from the somatic sources to developing oocytes and eggs. However, recent studies
indicate that also large-size molecules, such as messenger RNAs and long noncod-
ing (Lnc) RNAs, are transported from surrounding somatic cells to the oocyte
(Fig. 1.2; Kloc et al. 2016a, b; Macaulay et al. 2014, 2016). The long noncoding
(Lnc) RNAs have length greater than 200 nucleotides and presumably do not have
protein-coding potential and are non-translatable (Bassett et al. 2014; Hombach and
Kretz 2016). Because the LncRNAs do not produce proteins and are probably
multifunctional, their specific functions are very hard to authenticate experimen-
tally (Bassett et al. 2014). Some of the presumed functions of LncRNAs include
epigenetic regulation (Qiu et al. 2016); imprinting and X chromosome dosage
compensation (H19 and Xsist LncRNAs; Chen et al. 2016a, b; Gendrel and Heard
2014; Li et al. 2016); regulation of neighboring or distant gene expression in cis or

trans, respectively (Peschansky et al. 2016; Yu et al. 2016); being precursors of
certain classes of small RNAs (Bassett et al. 2014); sponging the miRNA and
competing with endogenous mRNA in transcriptional silencing (Zhang et al. 2016);
influencing chromatin conformation (Sun et al. 2016); or simply being a
nonfunctional by-product of transcription of LncRNA locus (Bassett et al. 2014).
Macaulay et al. (2014, 2016) have used combination of transmission electron
microscopy, confocal microscopy, and colored transcript detection to follow the
transfer of LncRNAs, mRNAs, and transfected synthetic transcripts (plasmids)
from the cumulus cells to the bovine oocytes. They showed that these transcripts
were transferred to the oocytes from surrounding cumulus cells via specialized
structures extending from cumulus cells toward the oocyte membrane, which they
named the transzonal projections (TZPs) or gametic synapses (Fig. 1.2; Chap. 2).
TZPs differ from the 50–200 nm diameter tunneling nanotubes (TNTs; Fig. 1.2),
which are known to connect and transfer large-size molecules and organelles
between various somatic cells (Kloc et al. 2016a, b). TZPs have larger diameter
(200 μm), and in contrast to the TNTs, their membrane is not fused with the oocyte
membrane. Instead, at the area of contact with the oocyte, the TZPs form the
vesicles reminiscent of synaptic vesicles between neural projections (Macaulay
et al. 2014, 2016). Using RNA-seq and bioinformatics analysis, these authors
showed that among hundreds of identified RNAs, there were H19 and Xsist
LncRNAs (which function in imprinting and X chromosome silencing) and 63 dif-
ferent mRNAs related to cytoskeletal and oocyte maturation functions. They also
showed that removal of cumulus cells, which are the sources of these transcripts,
reduces oocyte maturation rates (Macaulay et al. 2014, 2016). Although we still do
not know if such a transfer of large exogenous molecules occurs only during
preparation for oocyte maturation or also during earlier stages of oocyte develop-
ment, the discovery of TNT-like structures between follicular cells and oocyte in
developing insect ovaries (Tworzydlo et al. 2010a, b) suggests that the large-size
molecule exchange may occur in all stages of oogenesis to support consecutive
stages of oocyte development and growth.
1.3 Transfer of Sperm-Derived Components

and Epigenetic Heredity
Another unexpected source of delivery of exogenous molecules and organelles to

the egg is the sperm. The commonly accepted phenomenon of Mendelian heredity
is based on the transfer of genetic information contained within egg and sperm
DNA to the next generation. In Mendelian heredity scenario, the contribution from
the sperm is limited to the delivery of paternal DNA. However, there are many
examples of non-Mendelian heredity when various environmental factors induce
heritable phenotypic (epigenetic) variations that are not caused by mutations in
DNA sequence but depend on DNA methylation pattern and/or posttranslational

modification of histones (Rassoulzadegan and Cuzin 2015). There is also evidence
that the paternal contribution from sperm is not limited to DNA and that RNAs and
organelles present in the sperm may cause heritable epigenetic variations (Barroso
et al. 2009; Chen et al. 2016a, b; Rassoulzadegan and Cuzin 2015).
1.3.1 Sperm-Derived Mitochondria and Centrioles
It is known that in some animals, the sperm, during fertilization, delivers not only
genomic DNA but also mitochondria and centrioles (Fig. 1.3; Barroso et al. 2009).
Although in many animals sperm delivers many (up to 100 in mammals) mitochon-
dria, they usually contain “self-destruction switch” and are eliminated during, or
immediately after, fertilization through the process of mitophagy. However, if some
of the mitochondria or their DNA escape elimination, they can impose paternally
derived, and possibly epigenetic, effects on the egg and developing embryo
(Al Rawi et al. 2011; Baumann 2016; van der Bliek 2016).
Other organelles often delivered by sperm are the centrioles, which motile sperm
uses to produce axoneme. In the majority of animal species, female centrioles are
lost during oogenesis, and, at fertilization, sperm delivers one or two paternal
centrioles, which will be used to organize mitotic apparatus in the zygote. However,
in some insects, snails, and rodents, both sperm and egg do not have centrioles or
Egg
Sperm
nucleus acrosome
RNA
Centriole
Mitochondrium
Fig. 1.3 Delivery of sperm-derived molecules and organelles during fertilization. During fertil-
ization sperm delivers not only genetic information (DNA) but also mitochondria, centrioles, and
various coding and noncoding RNAs. Although majority of mitochondria reaching the egg
undergo mitophagy, the ones that survive and also mitochondrial DNA release from dying
mitochondria can cause epigenetic modification of the zygotic genome. It is possible that pater-
nally derived centrioles may also impose epigenetic changes on the embryonic genome. Some of
the sperm-derived mRNAs are transcribed in the zygote into protein, and those together with
sperm-derived noncoding RNAs may also influence developmental program of the embryo
the paternal centriole is rapidly degraded following fertilization, and zygote pro-
duces centriole de novo, from the maternal proteins (Pimenta-Marques et al. 2016;
Gueth-Hallonet et al. 1993; Manandhar et al. 2005; Ross and Normark 2015). For
decades scientists questioned whether centrioles contain their own heredity traits. If
they did then the paternal centrioles could theoretically impose their “heredity
program” on the zygote and developing embryos. However, after decades of
controversy, recent studies firmly established that centrioles do not contain their
own genetic material and that the old (providing template) “mother” centriole is not
necessary for the formation of a daughter centriole (Rodrigues-Martins et al. 2007).
In spite of these findings, some researchers believe that the paternal centrioles,
when delivered to the egg cytoplasm, may still somehow influence establishment of
paternally derived epigenetic traits in the zygote and developing embryo (Ross and
Normark 2015).
1.3.2 Sperm-Derived RNAs
It has been known for some time that sperm contains a multitude of noncoding
RNAs, coding mRNAs, and proteins that are delivered to the egg during fertiliza-
tion (Chen et al. 2016a, b; Jodar et al. 2016; Johnson et al. 2015; Stoeckius et al.
2014; Yan 2014). RNA analysis of the one-cell hybrid embryos originating from the
crosses of males and females from different C. elegans strains showed that they
expressed 160 paternal mRNAs and multiple paternal siRNAs and piRNAs
(Stoeckius et al. 2014). Fang et al. (2014) found that each mouse sperm contained
4885 mRNA transcripts. Some of these transcripts such as Wnt4 and Foxg1 were
delivered to the egg during fertilization, and Wnt4, but not Foxg1, was translated
into protein in zygotes. This suggests that the transmission of paternal (sperm-
derived) mRNAs may influence embryonic development.
Recently, Cropley et al. (2016) showed that in mice, the F1 generation sons of
obese males had defects in glucose and lipid metabolism that were transmitted to
their own, F2, sons. These authors prepared small RNA library from the sperm and
after its sequencing showed that sperm of F1 males had a unique profile of several
small RNA species, including the tRNA-derived (so-called diet-responsive) frag-
ments (Sharma et al. 2016). The authors postulate that this non-Mendelian inher-
itance of metabolic defects occurs via transmission of sperm-derived noncoding
RNA (Cropley et al. 2016; Sharma et al. 2016; Watson 2016).
In response to the accumulating data on the importance of sperm-derived RNAs
for non-Mendelian and epigenetic heredity, Schuster et al. (2016) developed a
simple method for isolation of sperm RNA from several mammalian species and
established SpermBase (www.spermbase.org) database, which contains informa-
tion on sperm-derived RNAs.
Studies presented above indicate that paternally derived coding and noncoding
RNAs can affect zygote and embryonic development (Liu et al. 2012) and also
participate in the establishment of epigenetic (non-Mendelian) transgenerational

inheritance (Fig. 1.3; Chen et al. 2016a, b; Kumar et al. 2013).
1.4 Transfer from Somatic Cells and Testicular Fluid

to Sperm
Another phenomenon that abolishes the concept of a strict delineation between germ
line and soma is the transfer of information between somatic cells, testicular fluid,
and sperm. In the testes, developing male germ cells are in close contact with
somatic Sertoli cells, which are functional equivalent of follicular and nurse cells
in the ovary, and together they are bathed in testicular fluid. Both Sertoli cells and
male germ cells secrete various proteins into the testicular fluid. Analysis of this
“secrotome” using the “integrative omics” (combined proteomics, transcriptomics,
genomics, and interactomics analyses) methodology showed that, similar to the
follicular fluid in the ovaries, there is an extensive cross talk between the germ
and Sertoli cells mediated by the components of testicular fluid (Chalmel et al.
2014). Also, similar to the extensive physical contact between follicular cells and
oocyte/egg, the Sertoli cells form the tight junctions, adherent junctions,
tubulolobular complexes (TBC), and cytoplasmic bridges with the male germ
cells, and the assortment of these connections changes during different phases of
reproductive cycle (Ahmed et al. 2016; Segretain and Decrossas 1991).
1.5 Conclusions
Taken together, presented above studies indicate that there is bidirectional

exchange between germ line and soma and that paternally derived coding and
noncoding RNAs can affect both zygote and embryonic development and also
participate in the establishment of epigenetic (non-Mendelian) transgenerational
inheritance. This clearly shows striking mutual dependence of germ line and soma
and argues for the existence of functional germ/soma syncytium.
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Chapter 2
Control of Mammalian Oocyte Development by
Interactions with the Maternal Follicular
Environment
Hugh Clarke
Abstract Development of animal germ cells depends critically on continuous

contact and communication with the somatic compartment of the gonad. In females,
each oocyte is enclosed within a follicle, whose somatic cells supply nutrients that
sustain basal metabolic activity of the oocyte and send signals that regulate its
differentiation. This maternal microenvironment thus plays an indispensable role in
ensuring the production of fully differentiated oocytes that can give rise to healthy
embryos. The granulosa cells send signals, likely membrane-associated Kit ligand,
which trigger oocytes within resting-stage primordial follicles to initiate growth.
During growth, the granulosa cells feed amino acids, nucleotides, and glycolytic
substrates to the oocyte. These factors are necessary for the oocyte to complete its
growth and are delivered via gap junctions that couple the granulosa cells to the
oocyte. In a complementary manner, growing oocytes also release growth factors,
notably growth-differentiation factor 9 and bone morphogenetic protein 15, which
are necessary for proper differentiation of the granulosa cells and for these cells to
support oocyte growth. During the late stages of oocyte growth, cyclic GMP that is
synthesized by the granulosa cells and diffuses into the oocyte is required to prevent
its precocious entry into meiotic maturation. Finally, at the early stages of matura-
tion, granulosa cell signals promote the synthesis of a subset of proteins within the
oocyte that enhance their ability to develop as embryos. Thus, the maternal legacy
of the follicular microenvironment is witnessed by the fertilization of the ovulated
oocyte and subsequent birth of healthy offspring.
H. Clarke (*)
Department of Obstetrics and Gynecology, Research Institute of the McGill University Health
Centre, McGill University, Room E.M0.2218, Glen Research Building, 100 Boul Decarie,
Montreal, QC, Canada, H4A 3J1
e-mail: Hugh.clarke@mcgill.ca
© Springer International Publishing AG 2017 17

M. Kloc (ed.), Oocytes, Results and Problems in Cell Differentiation 63,
DOI 10.1007/978-3-319-60855-6_2
18 H. Clarke
2.1 Introduction
Maternal control of embryonic development typically describes the concept that

factors which accumulate in the oocyte during its growth and development before
fertilization influence the development of the embryo after fertilization. Many,
though by no means all, of these factors are messenger mRNAs, reflecting that
embryos are transcriptionally inactive during the early stages of postfertilization
development, so new protein synthesis relies entirely on mRNAs that were synthe-
sized by the oocyte. Thus, the maternal rather than embryonic genome determines
the mRNA population of the early embryo. Here we describe maternal control of a
different nature, focusing primarily on studies using the mouse as a model organ-
ism. Germ cells develop within a microenvironment that is created by the somatic
cells of the gonad. In females, the cells of the ovarian follicle—principally the
granulosa cells which surround and enclose the oocyte throughout its growth and
development—create this environment. Because individual oocytes and their folli-
cles undergo growth throughout reproductive life, and many aspects of growth can
be faithfully recapitulated in vitro, much has been learned about the interactions
between the female germ cell and its environment during this period. Such studies
have revealed a continuous and multidimensional exchange of signals that not only
drives oocyte development but also permits the oocyte to remodel the somatic
microenvironment to meet its evolving needs.
2.2 Generating Primordial Follicles
The early life histories of oocytes and the granulosa cells are separate stories,
reflecting their different embryological origin. Oocytes are descended from the
primordial germ cells (PGCs), which arise from posterior epiblast under the influ-
ence of signals sent by adjacent tissues, notably bone morphogenetic protein (BMP)
4 from the extra-embryonic ectoderm (Gunesdogan and Surani 2016). Following
migration to the genital ridge, the PGCs of female embryos differentiate into
oogonia, which undergo multiple rounds of mitotic proliferation before entering
meiosis (Pepling 2012; Jorgensen 2013; Grive and Freiman 2015). The granulosa
cells are not born so far from home but instead thought to be derived from cells at
the surface of the developing gonad (Mork et al. 2012; Hummitzsch et al. 2015). By
near the time of birth, each oocyte has become enclosed by a small number of
granulosa cells in a structure termed a primordial follicle. The signals that trigger
formation of the primordial follicles are not fully understood. However, when
oocytes lack the bHLH-type transcription factor, FIGLA, the follicles do not form
(Soyal et al. 2000). Similarly, when Sohlh2, which also encodes a bHLH transcrip-
tion factor, is deleted in oocytes, primordial follicles are able to form but disappear
shortly after birth (Choi et al. 2008). These and other reports (Reddy et al. 2009;
Saatcioglu et al. 2016) in which other genes have been deleted in the oocyte
2 Control of Mammalian Oocyte Development by Interactions with the Maternal. . . 19
highlight that, even at the primordial follicle stage, normal follicular structure and
function is not sustained in the absence of a healthy oocyte. Conversely, oocytes
that do not lie within a primordial follicle will undergo apoptosis (Pepling and
Spradling 2001). These observations underscore the indispensable role of signaling
between the germ line and soma in females, a mutual dependence that differs
strikingly different from the male, where seminiferous tubules can remain orga-
nized when no germ cells are present.
Within the primordial follicle, the oocyte and granulosa cells are closely apposed
as revealed by electron micrographs, and cell adhesion complexes appear to
physically couple the oocyte to the granulosa cells and the granulosa cells to each
other (Jorgensen 2013). Oocytes and granulosa cells express a variety of junctional
proteins, including cadherins and nectins that characterize adherens junctions
(Mora et al. 2012). Even at this early stage, oocytes express mainly E-cadherin,
whereas granulosa cells express mainly N-cadherin (Mora et al. 2012), meaning
that the intercellular complexes are likely heterotypic. In addition, gap junctional
structures have been detected using electron microscopy both between granulosa
cells and between oocytes and granulosa cells (Mitchell and Burghardt 1986). In
contrast, protein components of desmosomes have not been detected in the primor-
dial follicles (Mora et al. 2012). Desmosomes generate very strong intercellular
adhesion, and it was suggested that their absence facilitates the changes in the
association between the oocyte and granulosa cells that will occur when the
primordial follicle enters the growth phase, as described below (Mora et al. 2012).
2.3 Growth and Maturation of the Oocyte and Its Follicle
Prior to ovulation and fertilization, the oocyte undergoes a prolonged period of

growth, followed by a briefer stage termed meiotic maturation (Fig. 2.1). Because
available evidence indicates that no new functional oocytes are created after birth
under physiological conditions (Zhang et al. 2012, 2015; Lei and Spradling 2013;
Zarate-Garcia et al. 2016), the entry of primordial follicles into the growth phase
must be regulated. Thus, some primordial follicles will remain in this arrested
condition for up to decades before initiating growth. Oocytes from aged females,
however, develop poorly as embryos (Nelson et al. 2013; Ben-Meir et al. 2015;
Haverfield et al. 2016; Meldrum et al. 2016). Whether this reduced oocyte quality
reflects damage that accumulates during its prolonged arrest within the primordial
follicle or arises during the growth and maturation process is unclear; however, in
both mice and humans, primordial follicles of aged females show increased DNA
damage as reflected by immunological detection of γH2A.X (Titus et al. 2013).
This suggests that there may be an age-associated loss of oocyte quality within the
primordial follicles.
The growth phase of oogenesis lasts about 3 weeks in the mouse and 3–4 months
in human. The most obvious feature of the growth phase is the enormous
increase—greater than 100-fold—in the volume of the oocyte. This increase
20 H. Clarke
OOCYTE AND FOLLICULAR GROWTH mural

granulosa
antrum
cumulus
thecal basement
granulosa
cells membrane
zona
granulosa pellucida
oocyte
cells
Primordial Primary Secondary Early antral Late antral

follicle follicle follicle follicle (Graafian) follicle
~3 weeks (mouse); ~4 months (human)
MEIOTIC MATURATION
germinal vesicle germinal vesicle metaphase II

metaphase I
stage (immature) breakdown (mature)
~12 h (mouse); ~36 h (human)
Fig. 2.1 Oocyte and follicular growth and meiotic maturation. Upper Near the time of birth, each
oocyte becomes surrounded by a small number of squamous granulosa cells in a primordial
follicle. During reproductive life, individual follicles enter the growth phase and are termed
primary follicles. The granulosa cells assume a cuboidal morphology and begin to proliferate
mitotically, continuing to fully cover the surface of the growing oocyte. At this stage, the
oocyte elaborates the zona pellucida, which physically separates it from the granulosa cell bodies.
A basement membrane appears outside the granulosa cell layer and thecal cells are recruited
external to this membrane. As the granulosa cells continue to proliferate, they generate multiple
layers. A fluid-filled cavity appears, which separates the granulosa into the cumulus granulosa,
adjacent to the oocyte, and the mural granulosa, adjacent to the follicle wall. Preovulatory follicles
contain a large antrum and may be termed Graafian. Lower Luteinizing hormone, which binds to
receptors on the mural granulosa cells, triggers meiotic maturation of the oocyte. The nuclear
(germinal vesicle) membrane breaks down and the chromosomes condense and become assembled
on the first meiotic spindle. After translocation of the spindle to the oocyte cortex, the first meiotic
division occurs and half of the chromosomes are discarded in the first polar body. The oocyte
chromosomes become aligned on the second meiotic spindle (metaphase II). Fertilization will
trigger the completion of the second meiotic division. Not shown are cytoplasmic events that occur
during maturation. Adapted from Res Probl Cell Diff 58:191–224
reflects the accumulation of mitochondria and other organelles, mRNA, and pro-
teins that will support early embryonic development after fertilization (Sánchez
and Smitz 2012). The growing oocyte also undergoes major ultrastructural
rearrangements, including the accumulation of cortical granules that will play an
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Fig.
267
The picture above (Fig. 266) shows you a daisy cut in two, and
next you have one of the white outer flowers (Fig. 267). This flower,
as we must call it, has a pistil, but no stamens. The pollen is brought
by flies from the yellow central flowers to this pistil.
Fig.
268
Here (Fig. 268) you see a picture of one of those yellow flowers
which have both stamens and pistil inside its tube.
If you children once make yourselves well acquainted with the
make-up of the daisy, seeing with your own bright eyes (not believing
it just because I tell you it is so) that there are many little flowers
where most people think they see only one big one, you will never
forget it as long as you live; and you will know something that many
of the big people about you do not know. Some day while walking
across the fields I think you will enjoy surprising them by pulling to
pieces a daisy, and explaining to them this favorite flower trick.
ROBIN’S PLANTAIN, GOLDEN-ROD, AND
ASTER
A LONG the roadsides, in the month of May, grows a flower which

you children call a blue daisy. This has the yellow center of the
field daisy; but the narrow outer flowers which surround the yellow
center are not white, they are blue.
Fig. 269
The real name of this flower is “robin’s plantain.” It is not a daisy,

though it belongs to the same big family. Here, too, the yellow center
is made up of many little tube-shaped flowers.
Later in the year the fields are white and purple with beautiful
asters (Fig. 269). It is easy to see that these asters are own cousins
to robin’s plantain. Their flower heads are put together in the same
way, and many of the asters wear the same blue or purple dress
(Fig. 269).
Fig. 270
When once you have become acquainted with the secret of

dandelion and daisy and aster and robin’s plantain, you will find it
quite easy to discover their little separate flowers. All these plants
have large, plain flower heads that you cannot mistake.
But with some members of this great Composite family you are
going to have more trouble, unless you take your time and keep your
wits about you.
Fig.
271
Just when the asters begin to border the roadsides in the month of
August, the golden-rod (Fig. 270) hangs out its bright yellow flowers.
This golden-rod is one of the plants which you may find a little
troublesome; for its little flowers are so tiny, that even when a
number of them are fastened together in a bunch, the whole bunch
looks like a very small blossom (Fig. 271).
Fig.
272
In each of these little bunches or heads (for when a number of

flowers are packed together in this way, we call the whole bunch a
“head”) there are a few of the strap flowers (Fig. 272) on the outside,
and a few tube flowers (Fig. 273) in the center; but the outer strap
flowers are so small that you can hardly believe they are really
flowers, and the tube flowers look hardly larger than ordinary
stamens. To see them at all clearly, you must use a good magnifying
glass.
Fig.
273
And you must search very patiently for the tiny bunch (Fig. 271)
which is the head of the golden-rod. Next you must pick to pieces
this little head, separating the outer from the inner flowers.
In hunting for a single head in this great yellow flower cluster, you
must look for the little cup-like arrangement, the tiny greenish or
yellowish leaves; for each head is held in one of these small cups.
Although the golden-rod is one of the most difficult of all the
flowers to understand, once you have seen for yourselves how each
little head is held in its tiny cup, you will find it easy enough to pick
out its single flowers, and then you will have mastered the secret of
the golden-rod.
THE LAST OF THE FLOWERS
W E found, you remember, that the dandelion head was made up

entirely of strap flowers; and we saw that the daisy and aster
and golden-rod were made up partly of strap flowers, and partly of
tube flowers.
And here you have a great thistle head (Fig. 274). If you should
pull it to pieces, you would find only tube flowers.
The Composite family always makes up its head in one of these
three ways, using either nothing but strap flowers, or nothing but
tube flowers, or else using tube flowers for the center of the head,
and strap flowers for the outside.
Fig. 274
Now, I hope you will remember these three ways in which this
important family puts together its little flowers.
Fig. 275
When you go into the garden where a big sunflower (Fig. 275) is
trying to peep into your neighbor’s yard, I hope your eyes will be
sharp enough to see that this sunflower is a cousin to the field daisy,
and that, although its brown center is much larger than the daisy’s
golden eyes, it is made up of tube flowers (Fig. 276) shaped much
like the tube flowers of the daisy.
And you will notice, I am sure, that the yellow circle about this
brown center is made up of strap flowers (Fig. 277) just like the circle
about the daisy center.
Fig.
276
And what is that which falls like a golden shower from the great
brown center of the sunflower? Ah, you know well that that is the
precious pollen which powders thickly the visiting bees and
butterflies, and goes to make new sunflower plants.
The picture at the head of this chapter shows the wild sister of the
garden sunflower.
Fig.
277
When you come across the bright blue flower of the chicory, you
will be reminded, I hope, of your dear old friend the dandelion; for the
chicory head, like that of the dandelion, is made up entirely of strap
flowers.
But when you pick a spray of everlasting, whose white and yellow
clusters you find on the rocky hillsides, you will have to use your
eyes with great care if you are to discover that here, as in the great
purple thistle head, are nothing but tube flowers.
Part VII—Learning to See
A BAD HABIT
I N fact, if you are to see any of the things that are really worth
seeing, you must study the art of using your eyes. You must learn
to see.
This world is full of things that are beautiful and interesting, things
that do not cost money, that can be had for the seeing.
School is nearly over now, and during the weeks that lie before
you there will be many hours which you children can call your own.
I wonder what you will do with these holiday hours?
Of course, you will play a great deal; at least, I hope you will, for
we need play almost as much as we need work. But one does not
play every minute, even in the holidays. I hope that all of you will
spend a part of your holidays in trying to be a little useful to your
mothers.
But even then there will be some time left for other things,—things
that are not work, and that are not exactly play, yet that are a little of
each, and so perhaps better than either play or work alone.
Among these “other things” I hope “learning to see” will find its
place. I wish that every child who reads this book would make a
resolution that during these coming holiday weeks he will “learn to
see.”
There are many different ways of doing this. The children in the
city can learn this great lesson as well as those who live in the
country. There is much to be seen in the city besides people and
houses, and horses and wagons. There are the clouds of the sky by
day, and its stars by night. There are the trees in the squares, the
birds and flowers in the parks, and much besides.
The children who live by the sea do not have the great forest trees
that grow among the mountains; but for this loss they can comfort
themselves by the beautiful rose mallows (see the picture at the
head of this chapter) that grow in the marsh, by the sea pinks along
the creek, by the pretty shells and seaweeds on the beach.
But perhaps you think I am quite wrong in taking it for granted that
you need to “learn to see.” What gives me the idea that you ought to
learn any such lesson?
Well, nine times out of ten, if I hand a flower to a child and ask him
to look at it and then to tell me about it, he will stare at it, oh, very
hard indeed, for some moments, and then he will have nothing to
say.
Now, this cannot be the fault of the flower; for we have seen that
the flower is made up of so many different things that to tell about
them all takes some time. It must be the fault of the child; or at least
the fault of his eyes and brain, both of which are needed for really
seeing, and which probably he does not know how to use.
It must be that he has never “learned to see.” Perhaps he has
used his eyes well enough, and has really seen a great many things
in the flower; but his brain may not be able to put them together in
the right way, and to find the words that are needed.
If this is the only trouble, a little practice will make it all right. He
will find that his brain works better after each trial, just as a new pair
of scissors works better after it has been used several times.
But often the eyes do not seem to do their share of the work; and if
they do not, there is no chance for the brain to come to their help.
That is a sad state of affairs, because, if when we are young we let
our eyes form bad habits, such as not seeing the things they ought
to see, we are likely to be half blind all the rest of our lives.
It would be a terrible thing, would it not, to be told that you were
about to become blind, that soon you would be unable to see the
things about you?
Now, while I trust that none of you will ever become altogether
blind, I tell you honestly, I greatly fear that some of you are in danger
of becoming partly so,—of becoming blind to many of the things
about you that would please you greatly if you only saw them. And I
know that this sort of blindness must take from your lives much
happiness.
But still you may wonder how I know this about children whom I
have never seen. How can I know whether the boys and girls who
read this are in any danger of losing their power to see?
Well, the only way I know about you boys and girls, whom I have
never seen, is by watching very carefully the ones I do see.
You children who live in New York, say, have never seen the
children who live in California; yet you feel sure that they have eyes
and ears just as you have, do you not?
And you are pretty confident that most of them like to play far
better than they like to work; that sometimes they are good-natured,
and that again they are quarrelsome; and that in many ways they are
like the boys and girls who live near you.
In just the same way I am able to guess that you children whom I
do not know are more or less like the ones I do know.
Now, among these children only a few, as I have said before,
seem to have the full use of their eyes. This troubles me, because
the evil is one that grows greater as the children grow older. Perhaps
you know that if you stop using any part of your body, that part soon
begins to lose its power of doing the things it was meant to do.
If you should not use your legs for a long time, they would grow so
weak that they could hardly carry you. It would be much as if you
had no legs, or at least as if you had legs that could not do the work
they were meant to do.
If you stopped using your hands, you would find your fingers
growing stiffer and stiffer, so that at last they could not take a good
hold of things.
And if your eyes are not used for seeing clearly the things before
them, they will grow less and less able to see clearly.
A COUNTRY ROAD
I HAVE taken a walk along a country road which was bright with
flowers of many kinds, where lovely-colored butterflies and
buzzing bees were hard at work hunting for sweet stuff, where birds
were singing in the trees as they watched their nests, where a rabbit
would dart from the bushes close by, and a squirrel would scold at
me from overhead,—where, in short, there was so much to look at
and delight in, that I could hardly make up my mind to keep on to my
journey’s end, instead of stopping to see if I knew the names of all
the flowers, to admire the queer, bright-colored little patterns on the
wing of the butterfly which was resting on a neighboring blossom,
and to find out what sort of eggs were in the nest that I knew must be
near at hand, for the mother bird let out her secret by her frightened
clucking.
Well, I have taken just such a walk; and on going into the house I
have felt as if I were obliged to put aside a book of enchanting fairy
stories, or rather as if I were turning my back on fairyland itself, with
all its wonderful sights and sounds and adventures.
And then what has happened?
Why, some child (it has not always been a child) has come in, and
I have said, “Was not that a fine walk? What did you see along that
lovely road?”
Now, if he was a boy (for I want to be quite fair), he probably had
seen the rabbit and given it chase; and it is more than likely that he
had stopped long enough to chuck a stone at the squirrel; and if the
mother bird had not finished with her foolish chatter, I fear he gave
her some evil moments by hunting for her nest, with no good
intentions. But if, fortunately for them, he had met none of these
creatures, he probably looked at me in surprise, and answered by
look, if not by words, “No, I thought it a long, stupid walk. I did not
see a thing.”
And if it was a girl, I fear the answer, silent or spoken, was much
the same.
Now, I say that boy or girl must have been partly blind to have
missed seeing those wonderful flowers, and butterflies, and bees,
and birds, and many other interesting things which I have not time
here to tell about. Certainly they were not using their eyes properly;
and the longer they go about in such a way, more worthy of a bat
than of a well-made child, the more useless and bat-like will their
eyes become.
It is really more natural for a child to use his eyes constantly than it
is for an older person. The grown-up man or woman is likely to have
so many things to think about, that eyes and brain do not always
work together, and so the surroundings are not noticed.
For every boy knows that if his head is full of the ball game he is
going to play, he runs along without eyes or thoughts for other
things.
And every girl knows that if she is on her way to some friend to
whom she has a secret to tell, she is in such haste to reach her
journey’s end, and is so busy thinking what her friend will have to
say about it all, that of course there is no time to pay attention to
anything else. Her eyes may be in good working order, yet they are
not of much use unless her brain is ready to help them; and that little
brain just now is too busy with its secret.
No, by the people who are half blind I mean only those who much
of the time use neither eyes nor brain, who can neither tell you what
they have seen nor what they have been thinking about. Sometimes
it seems as if such people were not only half blind, it seems as if
they were only half alive.
A HOLIDAY LESSON
B UT I am in hopes that some of the children who read this book

will say, “I do not think it fair to call children half blind and only
half alive. I know I am not half blind. I saw all those things that Mrs.
Dana saw along that country road, and” (perhaps some of them may
add) “a good deal more too. I know all the different flowers by sight,
and the sunny hollows where the first ones come. I know where ever
so many of the birds build their nests, and how their different eggs
are marked and colored. Often I go down to the little pool in the
woods where they come for their bath. I know how the caterpillars
wrap themselves in leaves and come out beautiful butterflies. I have
peeped into the hollow of the tree where the red squirrel is bringing
up its family; and I have seen how the pretty green katydid scrapes
his wings along his sides, and makes the sound, ‘Katy did, Katy
didn’t,’ and oh, so many more things that I have not time to tell them
all.”
Ah! that is just it. The child that knows how to use his eyes can
see so much, so many wonderful things!
That is why I am so anxious that he or she should not miss
through carelessness the revelations that come to the child alone.
It seems as though the woods and fields were more ready to tell
their stories, to whisper their secrets, to children than to grown
people. If people learn to use their eyes and ears only after they are
grown, I hardly think that they will ever read quite the same stories,
ever listen to quite such wonderful secrets, as if they had begun to
look and to listen when they were little children.
If fairy godmothers came now, as the stories tell us they did once
upon a time, to the christenings of our little ones, offering whatever
gifts the parents should choose, it seems to me one of the wisest
selections would be the power to see.
And so when I ask you children, now that you are putting by your
lesson books for many weeks, to learn one lesson this holiday time,
—to learn to see,—I am asking you to do something that will make
your lives far happier than they could be were this lesson left
unlearned.
INDEX
(For the convenience of teachers and other older readers, technical

terms avoided in the body of the book are given in the index.)
A
Above-ground roots, 106-111.
Acorn, seed of oak, 68.
seed leaves of, 87.
a fruit, 95.
Adder’s tongue, yellow, 203, 216, 219.
Air, composition of, 151.
Air roots, 107.
Alder, black, 49.
Alder, speckled, 173.
Alder, swamp, 173.
Alder tassels, 207-209.
Almond seed, a food, 91.
Amphibious knotweed, 119, 123.
Anemone, 203, 209, 216, 219.
Animals and plants, difference between, 154, 155.
Anthers, see “dust boxes.”
Apple, study of, 11-19.
seed of, 20, 24, 27, 29, 93.
signs of ripeness of, 28, 29.
Apple blossom, parts of, 14, 15, 32.
buds of, 129.
Ash, seed of, 62.
Aster puffball, 59.
Asters, 251, 252, 254.
B
Baneberry, red, 49.
Baneberry, white, 49.
Barberry, 49.
stamens of, 193.
Bark, defined, 120, 121.
Basswood, leaves of, 165.
Bean, planting of seed of, 80.
seed leaves of, 81.
development of seed, 81-83, 96-98.
root of, 99.
stem of, 115, 117.
Bee, a pollen carrier, 17, 18, 189, 207, 226, 227, 233.
Beech tree, 215.
Beet, root of, 102, 103.
Birch tassels, 208, 209.
Birds, as seed transporters, 72, 73.
Bittersweet berries, 42.
Black alder, 49.
Blackberry, development of, 235-237.
Bladderwort, 179, 180.
Bloodroot, 106.
Bloom, 173.
Blue daisy, 251.
Blue flag, classified, 88.
Bristles, 175.
Bryophyllum, 132, 133, 150.
Buckwheat seed, a food, 91.
Buds, 125-133.
protection of, 126, 127, 131.
position of, 128, 132.
unprotected, 130.
on leaves, 132, 133.
Bulb, described, 105, 106.
an underground stem, 216, 217.
Bulblets, defined, 132.
Burdock burr, 35, 36, 52, 53, 95.
Burrs, description of, 52.
use of, to plant, 53.
as seed cases, 67, 68.
Buttercup, pistils and stamens of, 201
Buttonwood buds, 130, 131.
C
Cabbage leaves, 173.
Cabbage, skunk, 204.
Caladium, 163, 164.
Calyx (cup), described, 15.
position of, 18.
function of, 188.
defined, 189.
Carrion vine, 230, 231.
Carrot root, 102.
Carrot, wild, 246, 247.

Textbook Oocytes Maternal Information and Functions 1St Edition Kloc Ebook All Chapter PDF

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Oocytes.

Maternal Information and

Marine Organisms as Model Systems in Biology and

Maternal grief in the Hebrew bible 1st Edition Kozlova

Maternal Effect Genes in Development 1st Edition

Maternal-Fetal and Neonatal Endocrinology Christopher

RN Maternal Newborn Nursing 11th Edition Archer Knippa

Ridge Functions 1st Edition Allan Pinkus

Nutraceuticals for Prenatal Maternal and Offspring s

Maternal Sentencing and the Rights of the Child Shona

Malgorzata Kloc Editor

ISSN 0080-1844 ISSN 1861-0412 (electronic)

Library of Congress Control Number: 2017948675

© Springer International Publishing AG 2017

Printed on acid-free paper

This Springer imprint is published by Springer Nature

Houston, TX Malgorzata Kloc

Part I Oocyte Interactions with Environment

Part II Oocyte Polarity: Molecular and Organellar Aspects

9 RNA Localization in the Vertebrate Oocyte: Establishment

Part III Epigenetic, Transcriptional and Translational

Part IV Oocyte Specific Functions of Ubiquitous Molecules

Part V Maternal Factors: Origin, Evolution and Application

Malgorzata Kloc and Jacek Z. Kubiak

Abstract Recent discoveries on the delivery of small- and large-size molecules

1.1 Internal Versus External Source

© Springer International Publishing AG 2017 3

Only one cystocyte becomes the oocyte

Cystoblast Fully grown oocyte

Growth without division

1.2 Exogenous Molecules, Their Sources and Routs

1.2.1 Exchange Through the Gap Junctions

Gap Junction Gametic synapse (TZP)

Cumulus cells Theca

Tunneling nanotube Microvesicles and Exosomes

cell differentiation, oocyte growth, and choriogenesis and prevents dissipation of

different composition and functions. Gap junctions, which regulate proliferation

1.2.2 Transfer from Body Fluids

1.2.3 Transfer of Large-Size Molecules Through the Gametic

2014; Li et al. 2016); regulation of neighboring or distant gene expression in cis or

1.3 Transfer of Sperm-Derived Components

Another unexpected source of delivery of exogenous molecules and organelles to

DNA sequence but depend on DNA methylation pattern and/or posttranslational

1.3.1 Sperm-Derived Mitochondria and Centrioles

1.3.2 Sperm-Derived RNAs

participate in the establishment of epigenetic (non-Mendelian) transgenerational

1.4 Transfer from Somatic Cells and Testicular Fluid

Taken together, presented above studies indicate that there is bidirectional

Al Rawi S, Louvet-Vallée S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V

Abstract Development of animal germ cells depends critically on continuous

© Springer International Publishing AG 2017 17

Maternal control of embryonic development typically describes the concept that

2.2 Generating Primordial Follicles

2.3 Growth and Maturation of the Oocyte and Its Follicle

Prior to ovulation and fertilization, the oocyte undergoes a prolonged period of

OOCYTE AND FOLLICULAR GROWTH mural

Primordial Primary Secondary Early antral Late antral

~3 weeks (mouse); ~4 months (human)

germinal vesicle germinal vesicle metaphase II

~12 h (mouse); ~36 h (human)

A LONG the roadsides, in the month of May, grows a flower which

The real name of this flower is “robin’s plantain.” It is not a daisy,

When once you have become acquainted with the secret of