See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/6393476

Nutrition of the Developing Embryo and Hatchling

Article  in  Poultry Science · June 2007

DOI: 10.1093/ps/86.5.1043 · Source: PubMed

CITATIONS READS
313 896

1 author:

Edwin Moran
Auburn University
221 PUBLICATIONS   5,466 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Retired View project

All content following this page was uploaded by Edwin Moran on 04 December 2014.

The user has requested enhancement of the downloaded file.

 Muscle Development in the Embryo and Hatchling1
S. G. Velleman2
Department of Animal Sciences, Ohio Agricultural Research and Development Center,
The Ohio State University, Wooster 44691
ABSTRACT Muscle cell proliferation, migration, adhe-
sion, and fusion are processes involved with the forma-
tion of multinucleated myotubes that will further differ-
entiate into mature muscle fibers. The process of muscle
fiber development is nearly complete at the time of hatch.
Muscle growth during the embryonic period of develop-
ment is characterized by an increase in myoblast cell num-
ber through hyperplasia. Posthatch muscle fiber growth
occurs through muscle fiber enlargement by the process
of hypertrophy, which results from the recruitment of
satellite cell nuclei. Hyperplasia and hypertrophy are reg-
ulated by factors extrinsic to the cell. These extrinsic ele-
ments include growth factors and the extracellular matrix.
The growth factors, hepatocyte growth factor, fibroblast
Key words: extracellular matrix, growth factor, hyperplasia, hypertrophy, muscle fiber
INTRODUCTION
Skeletal muscle comprises the largest proportion of ani-
mal mass. Understanding the mechanisms that regulate
muscle growth has significant agricultural implications.
Muscle is the major food product. One of the goals of the
poultry industry has been to select animals for increased
growth rate and increased muscle mass while main-
taining meat quality. For poultry breeders this maximiza-
tion of growth has focused on lean carcass development
especially for the breast muscles, the most valuable part
of the carcass.
Muscle cell proliferation, migration, adhesion, and fu-
sion are processes involved with the formation of multi-
nucleated myotubes that will further differentiate into
mature muscle fibers (Swartz et al., 1994). Not all muscle
fibers form simultaneously during the prenatal period of
muscle development. The first set of embryonic muscle
©2007 Poultry Science Association Inc.
Received August 7, 2006.
Accepted October 7, 2006.
1
Salaries and research support provided by state and federal funds
appropriated to the Ohio Agricultural Research and Development Cen-
ter, The Ohio State University. Presented as part of the Embryo Sympo-
sium: Managing the Embryo for Performance, July 19, 2006, at the
Poultry Science Association Annual Meeting, Edmonton, Alberta,
Canada.
2
Corresponding author: velleman.1@osu.edu
1050
growth factor 2, transforming growth factor-β, insulin-
like growth factor, and myostatin stimulate or inhibit
myoblast and satellite cell proliferation and differentia-
tion. Some of these growth factors like fibroblast growth
factor 2 must interact with a low affinity extracellular
Downloaded from http://ps.oxfordjournals.org/ at Poultry Science Association Member on December 4, 2014
matrix macromolecule to bind to their high affinity recep-
tor necessary for cell signaling. It is probable that the
expression of extracellular matrix proteins involved in
growth factor signaling will affect muscle growth proper-
ties during hyperplasia and hypertrophy. As signaling
pathways associated with muscle growth mechanisms
are further understood, the poultry industry may find it
beneficial to include the expression of key genes in their
selection strategies.
2007 Poultry Science 86:1050–1054
fibers to form is termed primary fibers that have centrally
located nuclei. Surrounding the primary fibers are mono-
nucleated myogenic cells that will differentiate into sec-
ondary fibers. The secondary muscle fibers position is
based on the location of the primary fibers. After the
secondary fibers form, the Z band of the sarcomere, the
contractile unit of muscle, will line up forming a mature
muscle fiber.
Mechanisms of Muscle Growth
The process of muscle fiber formation is nearly com-
plete at the time of hatch. Muscle growth can be separated
into 2 periods, hyperplasia and hypertrophy. Hyperplasia
refers to the embryonic increase in myoblast cell number.
During the embryonic period of muscle development,
myoblasts are proliferating, differentiating into multinu-
cleated myotubes, and forming muscle fibers. After the
prehatch formation of muscle fibers, fiber number is set
at hatch (Smith, 1963). How the prehatch period of muscle
growth affects posthatch muscle accretion has not re-
ceived significant research attention to date.
For posthatch muscle growth to occur there must be
an increase in protein synthesis, which is the direct conse-
quence of more DNA resulting in increased transcription
and translation. To acquire more DNA, there is a required
increase in nuclei number. Because nuclei number de-
rived from myoblasts is set at hatch, the new nuclei are
 EMBRYO SYMPOSIUM 1051
derived from another cell type. Mauro (1961) identified
the presence of a cell wedged between the plasma mem-
brane and basement of skeletal muscle fibers. These cells
were termed satellite cells because they have little cell
cytoplasm. Mauro (1961) hypothesized that the satellite
cells may be involved in postnatal muscle growth. Moss
and LeBlond (1971) demonstrated that when 3H-thymi-
dine was given to rats the label incorporated into the
nuclei of the satellite cells for the first hour. After this
time, the label was localized in the nuclei of the muscle
fiber. Allen et al. (1979) reported that most of the nuclei
in a mature muscle fiber are from satellite cells. After
hatch, the satellite cells fuse with existing muscle fibers,
causing an increase or hypertrophy in muscle fiber size.
Simply incorporating more satellite cell nuclei into a

Downloaded from http://ps.oxfordjournals.org/ at Poultry Science Association Member on December 4, 2014

muscle fiber alone does not result in muscle hypertrophy.
The balance between protein synthesis and degradation
will modulate the hypertrophy process. To have an in-
crease in muscle fiber size requires protein synthesis rates
being higher than the rate of protein degradation. Degra-
dation of muscle is largely regulated by the calpain system
(Goll et al., 2003). The calpains, ␮-calpain and m-calpain,
are calcium-dependent proteases that do not degrade pro-
teins to amino acids but disassemble the myofibril to
the point of the Z-band. The further degradation of the
myofibrillar structure is through the activity of the protea-
some system. Calpastatin is a protein whose only known
function is to inhibit the activity of the calpains.

Muscle Organization
Mature muscle fibers are surrounded and supported
by 3 layers of connective tissue: endomysium, perimy-
sium, and the epimysium. Connective tissue is composed
of cells and an extracellular matrix. The extracellular ma-
trix is composed of fibrous and nonfibrous proteins in-
cluding collagens and proteoglycans. Muscle should con-
tain well-defined muscle fibers as well as distinct endo-
mysial spacing between the muscle fibers and well-
defined perimysial spacing between the muscle fiber bun-
dles. Maintaining this spacing is critical in preventing
muscle fiber degeneration.
In broilers and turkeys selected for increased growth,
it is common to observe more muscle fiber degeneration
than in unimproved birds (Wilson et al., 1990; Dransfield
and Sosnicki, 1999; Velleman et al., 2003). Figure 1 shows
16 wk posthatch breast muscle from a turkey randombred
control line (RBC2) that is representative of a commercial
1967 turkey and 16 wk posthatch breast muscle from an
F line turkey developed from the RBC2 line by selection
for only increased 16-wk BW. The growth-selected F line
has significant muscle fiber degeneration. In birds with
increased muscle fiber degeneration, there is significantly
reduced endomysial and perimysial spacing between the
muscle fibers and the muscle fibers appear fragmented.
The breast muscle is composed of glycolytic type II muscle
fibers. The glycolytic mode of anaerobic respiration re-
sults in the formation of lactic acid. Lactic acid is largely
removed from the muscle by the circulatory system to be
Figure 1. The effect of growth selection on 16 wk posthatch turkey
breast muscle morphology. A) Randombred Control 2 Line (RBC2); and
B) F line.
converted into glycogen by the liver (Bangsbo et al., 1991).
Velleman et al. (2003) observed in turkey breast muscles
having increased muscle damage, there was a reduction
in the capillary supply in the perimysial connective layer.
A reduction in the blood supply to the muscle would
increase lactic acid concentration and lead to muscle dam-
age potentially associated with the pale, soft, and exuda-
tive condition. Turkey pale, soft, and exudative condition
is associated with an increase in lactic acid and a decrease
in pH (Sosnicki and Wilson, 1991).
Factors Regulating Muscle Growth
during Hyperplasia and Hypertrophy
Growth factors are strong stimulators or inhibitors of
myoblast and satellite cell proliferation and differentia-
tion. The following growth factors have been shown to
affect hyperplasia and hypertrophy: hepatocyte growth
1052 VELLEMAN
Table 1. Growth factors affecting myoblast and satellite cell proliferation
and differentiation1
Growth factor Proliferation Differentiation
Hepatocyte growth factor Stimulates Inhibits
Fibroblast growth factor 2 Stimulates Inhibits
Insulin-like growth factor Stimulates Stimulates
Transforming growth factor-beta Inhibits Inhibits
Myostatin Inhibits Inhibits
1
Proliferation and differentiation information is from Allen and Goll
(2003).
factor, fibroblast growth factor 2 (FGF2), insulin-like
growth factor, transforming growth factor beta (TGF-β),
and myostatin. Table 1 summarizes the effects of each of
these growth factors on muscle cell function.
In recent years, myostatin has received significant re-
search attention from the biomedical and agricultural
communities. Myostatin is a member of the TGF-β family
and is a strong inhibitor of myoblast and satellite cell
proliferation and differentiation. Inhibiting the expres-
sion of myostatin results in a significant increase in muscle
mass. In addition to the increase in muscle mass, meat
quality is good from animals with inhibited myostatin
expression, and intramuscular fat and connective tissue
are decreased with improved feed efficiency.
Fibroblast growth factor 2 is a major growth factor
involved in the regulation of muscle growth. It is a potent
stimulator of myoblast and satellite cell proliferation and
an intense inhibitor of differentiation (Dollenmeier et al.,
1981). One biological effect of FGF2 during myogenesis is
to inhibit the transcription of myogenin, a muscle specific
transcriptional regulatory factor required for the initia-
tion of myotube formation (Brunetti and Goldfine, 1990).
By suppressing myogenin expression, FGF2 maintains
the skeletal muscle cells in a state of proliferation. The
turkey F line when compared with the RBC2 line that it
was selected from has been shown to have higher FGF2
expression during satellite cell proliferation and embry-
onic stages of development (Liu et al., 2003). Increased
FGF2 expression during the hyperplasia period of muscle
growth would result in the formation of more muscle
fibers prior to hatch. If more muscle fibers are present at
time of hatch, this would provide more fiber availability
for satellite cell fusion and muscle growth by hypertro-
phy. Fibroblast growth factor 2 is also a strong stimulator
of satellite cell proliferation. The activation of satellite
cell proliferation is critical in muscle hypertrophy. Feed-
deprived turkey poults and chicks exhibit reduced satel-
lite cell mitotic activity (Halevy et al., 2000; Mozdziak et
al., 2002). The activity of the myoblasts and satellite cells is
further influenced by the extrinsic or extracellular matrix
environment surrounding the cells.
The extracellular matrix is composed of an organized
network of proteins and polysaccharides, which are se-
creted by the muscle cells and localized in the connective
layers surrounding the muscle fibers. The extracellular
matrix consists mainly of collagens, proteoglycans, and
glycoproteins like fibronectin. The extracellular matrix is
a dynamic structure that changes in expression with the
developmental age of the tissue and is cell type specific.
The extracellular matrix communicates information back
to the cell and regulates cellular gene expression. Certain
extracellular matrix macromolecules, especially the pro-
teoglycans, interact with growth factors and are required
for the cell to elicit a response to the growth factor. Proteo-
glycans contain a central core protein with one or more
attached carbohydrate residues called glycosaminogly-
cans. Glycosaminoglycans covalently attached to the core
protein include chondroitin sulfate, keratan sulfate, der-
matan sulfate, and heparan sulfate. Based on this defini-
tion, the proteoglycans are a diverse family of macromole-
cules that exhibit developmental and tissue specificity in
terms of their expression.
Downloaded from http://ps.oxfordjournals.org/ at Poultry Science Association Member on December 4, 2014
In skeletal muscle, the proteoglycans play a major role
in regulating myoblast and satellite cell responsiveness
to the growth factors FGF2 and TGF-β, and recent data
suggest a role in myostatin responsiveness (Miura et al.,
2006). The interaction of FGF2 with its high affinity recep-
tor is mediated by the interaction of FGF2 with the he-
paran sulfate chains of heparan sulfate containing mem-
brane-associated proteoglycans. Yayon et al. (1991) dem-
onstrated that cells deficient in heparan sulfate
proteoglycans and transfected to express the FGF2 recep-
tor were unable to bind FGF2. The treatment of cells with
chlorate to prevent glycosaminoglycan sulfation de-
creased the binding of FGF2 to its high affinity receptor
(Olwin and Rapraeger, 1992). These studies have demon-
strated that heparan sulfate functions as a low affinity
coreceptor for FGF2. Because commercial poultry have
been selected for enhanced muscling based on phenotype
not by biological mechanisms involved in regulating mus-
cle growth, it is not clear how growth selection has af-
fected the expression of extracellular matrix macromole-
cules critical to the regulation of muscle growth during
hyperplasia and hypertrophy.
To study how selection for growth and muscling has
affected the expression of heparan sulfate proteoglycans
during the embryonic and posthatch periods of develop-
ment, research is in progress comparing the expression
profiles of heparan sulfate proteoglycans in the RBC2 and
F lines. During the embryonic and posthatch periods of
age, heparan sulfate proteoglycan expression was higher
in the growth selected F line compared with the unse-
lected RBC2 line (Liu et al., 2002). The expression of FGF2
mRNA was higher earlier in embryonic development for
the F line compared with the RBC2 line (Liu et al., 2003).
This suggests that the growth-selected F line has the po-
tential for increased FGF2 signaling, which would stimu-
late the proliferation of muscle cells leading to enhanced
muscle development and growth. In a related study,
McFarland et al. (2003) showed that fast growing turkey
satellite cell populations were more responsive to FGF2,
expressed more FGF2 mRNA, and had higher levels of
heparan sulfate proteoglycans compared with slower
growing satellite cell populations.
In muscle, 2 predominant groups of heparan sulfate
proteoglycans expressed are the syndecans and glypi-
 EMBRYO SYMPOSIUM
cans. The syndecan family is composed of 4 members,
syndecan-1 through -4, which have all been identified in
skeletal muscle. The syndecans have a membrane span-
ning core protein possessing highly conserved cyto-
plasmic and transmembrane domains and a diverse ecto-
domain to which the glycosaminoglycan chains are
attached (Carey, 1997; Rapraeger, 2001). Glypicans 1
through 6 have a core protein that contains conserved
cysteine residues and glycosaminoglycan attachment
sites. The glypicans are attached to the cell plasma mem-
brane through a glycosylphosphatidyl-inositol anchor
(David et al., 1990). Only glypican-1 has been reported
in skeletal muscle. In vitro studies with C2C12 myoblasts
have shown that syndecan-1, -3, and -4 expression are
downregulated during skeletal muscle differentiation
(Larraı́n et al., 1997; Fuentealba et al., 1999), whereas syn-
decan-2 remained unchanged (Brandan and Larráın,
1998). In contrast, glypican-1 expression increased sig-
nificantly during cell differentiation (Brandan et al., 1996).
Syndecans and glypicans mediate FGF2 binding to fibro-
blast growth factor receptors and regulated FGF2 activity
(Steinfeld et al., 1996; Filla et al., 1998). The different
expression patterns of syndecan-1 and glypican imply
that these 2 proteoglycans may have functional differ-
ences in regulating cellular responsiveness to FGF2. To
investigate the expression of syndecan-1 and glypican-1
as it relates to muscle development, studies have been
ongoing in the author’s laboratory measuring the expres-
sion of syndecan-1 and glypican-1 in the F and RBC2
lines during embryonic and posthatch development (Liu
et al., 2004, 2006).
Embryonic expression of syndecan-1 is higher at d 14
and 16 in the growth-selected F line compared with the
RBC2 line. Glypican-1 expression is higher in the F line
compared with the RBC2 line beginning at d 18. These
results support the findings that syndecan-1 and glypi-
can-1 are differentially expressed. Elevated syndecan-1
expression coincides with the period of muscle cell prolif-
eration and is followed directly by high levels of glypican-
1 expression. This expression profile of syndecan-1 and
glypican-1 in the F line may lead to more myoblast prolif-
eration and the formation of more muscle fibers by hyper-
plasia. With more muscle fibers present at hatch, the op-
portunity for muscle fiber growth by hypertrophy exists.
Implications for the Poultry Industry
In summary, a number of factors are involved in the
molecular regulation of muscle growth. Developing a
comprehensive understanding of the mechanisms of hy-
perplasia and hypertrophy is critical to the improvement
and maintenance of poultry meat quality. The poultry
industry has largely selected animals based on pheno-
typic growth rate and muscling and by using this ap-
proach has likely favored selection based on hypertrophy
rather than hyperplasia. Hypertrophy will result in larger
muscle fibers that have been observed in broiler breast
meat (Dransfield and Sosnicki, 1999). In the case of skele-
tal muscle, this type of selection regimen will alter muscle
1053
fiber proportions (Dransfield and Sosnicki, 1999). As well
as muscle fiber proportions being modified, the connec-
tive tissue spacing surrounding the muscle fibers will be
changed resulting in a situation that could be detrimental
to muscle health and subsequently meat quality.
The extracellular matrix macromolecules especially the
proteoglycans will affect a number of properties critical to
muscle growth and meat quality including water-holding
capacity and growth factor regulation. The growth factor
FGF2, for example, is a potent stimulator of muscle
growth and a strong inhibitor of differentiation. For the
muscle cells to elicit a response to FGF2, the FGF2 must
bind to heparan sulfate containing proteoglycans. Selec-
tion for increased 16-wk BW in turkeys has been shown
to increase FGF2 and heparan sulfate proteoglycan ex-
Downloaded from http://ps.oxfordjournals.org/ at Poultry Science Association Member on December 4, 2014
pression during the embryonic phase of growth (Liu et al.,
2002, 2003). These changes in FGF2 and heparan sulfate
proteoglycan expression would prolong the period of
proliferation and likely result in muscle growth through
hyperplasia. Perhaps the poultry industry should develop
strategies to include screening for the expression of key
genes related to muscle growth by hyperplasia and hyper-
trophy.
REFERENCES
Allen, R. E., and D. E. Goll. 2003. Cellular and developmental
biology of skeletal muscle as related to muscle growth. Pages
148–169 in Biology of Growth of Domestic Animals. Colin
Scanes, ed. Iowa State Press, Ames.
Allen, R. E., R. A. Merkel, and R. B. Young. 1979. Cellular aspects
of muscle growth: Myogenic cell proliferation. J. Anim. Sci.
49:115–127.
Bangsbo, J., P. D. Gollnick, T. E. Graham, and B. Saltin. 1991.
Substrates for muscle glycogen synthesis in recovery from
intense exercise in man. J. Physiol. 434:423–440.
Brandan, E., D. J. Carey, J. Larráın, F. Melo, and A. Campos.
1996. Synthesis and processing of glypican during differenti-
ation of skeletal muscle cells. Eur. J. Cell Biol. 71:170–176.
Brandan, E., and J. Larraı́n. 1998. Heparan sulfate proteoglycans
during terminal skeletal muscle differentiation. Possible
functions and regulation of their expression. Basic Appl.
Myol. 8:107–114.
Brunetti, A., and I. D. Goldfine. 1990. Role of myogenin in
myoblast differentiation and its regulation by fibroblast
growth factor. J. Biol. Chem. 265:5960–5963.
Carey, D. J. 1997. Syndecans: Multifunctional cell surface co-
receptors. Biochem. J. 327:1–16.
David, G., V. Lories, B. Decock, P. Marynen, J.-J. Cassiman, and
H. Van Den Berghe. 1990. Molecular cloning of a phosphati-
dylinositol-anchored membrane heparan sulfate proteogly-
can from human lung fibroblasts. J. Cell Biol. 111:3165–3176.
Dollenmeier, P., D. C. Turner, and H. M. Eppenberger. 1981.
Proliferation and differentiation of chick skeletal muscle cells
cultured in a chemically defined medium. Exp. Cell Res.
135:47–61.
Dransfield, E., and A. A. Sosnicki. 1999. Relationship between
muscle growth and poultry meat quality. Poult. Sci.
78:743–746.
Filla, M. S., P. Dam, and A. C. Rapraeger. 1998. The cell surface
proteoglycan syndecan-1 mediates fibroblast growth factor-
2 binding and activity. J. Cell. Physiol. 174:310–321.
Fuentealba, L., D. J. Carey, and E. Brandan. 1999. Antisense
inhibition of syndecan-3 expression during skeletal muscle
differentiation accelerates myogenesis through a basic fibro-
1054 VELLEMAN
blast growth factor-dependent mechanism. J. Biol. Chem.
274:37876–37884.
Goll, D. E., V. F. Thompson, H. Li, W. Wei, and J. Cong. 2003.
The calpain system. Physiol. Rev. 83:731–801.
Halevy, O., A. Geyra, M. Barak, Z. Uni, and D. Sklan. 2000. Early
posthatch starvation decreases satellite cell proliferation and
skeletal muscle growth in chicks. J. Nutr. 130:858–864.
Larraı́n, J., G. Cizmeci-Smith, V. Troncoso, R. C. Stahl, D. J.
Carey, and E. Brandan. 1997. Syndecan-1 expression is down-
regulated during myoblast terminal differentiation. Modula-
tion by growth factors and retinoic acid. J. Biol. Chem.
272:18418–18424.
Liu, X., D. C. McFarland, K. E. Nestor, and S. G. Velleman.
2003. Expression of fibroblast growth factor 2 and its receptor
during skeletal muscle development from turkeys with dif-
ferent growth rates. Domest. Anim. Endocrinol. 25:215–229.
Liu, X., D. C. McFarland, K. E. Nestor, and S. G. Velleman.
2004. Developmental regulated expression of syndecan-1 and
glypican in pectoralis major muscle in turkeys with different
growth rates. Dev. Growth Differ. 46:37–51.
Liu, C., D. C. McFarland, and S. G. Velleman. 2006. Membrane-
associated heparan sulfate proteoglycans are differentially
expressed in the skeletal muscle of turkeys with different
growth rates. Poult. Sci. 85:422–428.
Liu, X., K. E. Nestor, D. C. McFarland, and S. G. Velleman. 2002.
Developmental expression of skeletal muscle heparan sulfate
proteoglycans in turkeys with different growth rates. Poult.
Sci. 81:1621–1628.
Mauro, A. 1961. Satellite cells of skeletal muscle fibers. J. Bio-
phys. Biochem. Cytol. 9:493–495.
McFarland, D. C., X. Liu, S. G. Velleman, C. Zeng, C. S. Coy,
and J. E. Pesall. 2003. Variation in fibroblast growth factor
response and heparan sulfate proteoglycan production in
satellite cell populations. Comp. Biochem. Physiol. C
134:341–351.
View publication stats
Miura, T., Y. Kishioka, J. Wakamatsu, A. Hattori, A. Hennebry,
C. J. Berry, M. Sharam, R. Kambadur, and T. Nishimura.
2006. Decorin binds myostatin and modulates its activity to
muscle cells. Biochem. Biophys. Res. Commun. 340:675–680.
Moss, F. P., and C. P. LeBlond. 1971. Satellite cells are source
of nuclei in muscles of growing rats. Anat. Rec. 170:421–436.
Mozdziak, P. E., T. J. Walsh, and D. W. McCoy. 2002. The effect
of early posthatch nutrition on satellite cell mitotic activity.
Poult. Sci. 81:1703–1708.
Olwin, B. B., and A. Rapraeger. 1992. Repression of myogenic
differentiation by aFGF, bFGF, and K-FGF is dependent on
cellular heparan sulfate. J. Cell Biol. 118:631–639.
Rapraeger, A. C. 2001. Molecular interactions of syndecans dur-
ing development. Semin. Cell Dev. Biol. 12:107–116.
Smith, J. H. 1963. Relation of body size to muscle cell size and
number in the chicken. Poult. Sci. 42:283–290.
Sosnicki, A. A., and B. W. Wilson. 1991. Pathology of turkey
skeletal muscle: Implications for the poultry industry. Food
Downloaded from http://ps.oxfordjournals.org/ at Poultry Science Association Member on December 4, 2014
Struct. 10:317–326.
Steinfeld, R., H. Van Den Berghe, and G. David. 1996. Stimula-
tion of fibroblast growth factor receptor-1 occupancy and
signaling by cell surface-associated syndecans and glypican.
J. Cell Biol. 133:405–416.
Swartz, D. R., S.-S. Lim, and T. Faseel, and M. L. Greaser. 1994.
Mechanisms of myofibril assembly. Reciprocal Meat Conf.
Proc. 47:141–153.
Velleman, S. G., J. W. Anderson, C. S. Coy, and K. E. Nestor.
2003. Effect of selection for growth rate on muscle damage
during turkey breast muscle development. Poult. Sci.
82:1069–1074.
Wilson, B. W., P. S. Nieberg, and R. J. Buhr. 1990. Turkey muscle
growth and focal myopathy. Poult. Sci. 69:1553–1562.
Yayon, B. L., M. Klagsburn, J. D. Esko, P. Leder, and D. M.
Oritz. 1991. Cell surface heparin-like molecules are required
for binding of basic fibroblast growth factors to its high affin-
ity receptors. Cell 64:841–848.