Reviews

Cite This: ACS Chem. Biol. 2018, 13, 26−35

Innovations in Undergraduate Chemical Biology Education

Aaron R. Van Dyke,* Daniel H. Gatazka, and Mariah M. Hanania
Department of Chemistry and Biochemistry, Fairfield University, Fairfield, Connecticut 06824, United States

ABSTRACT: Chemical biology derives intellectual vitality from its scientific interface: applying
chemical strategies and perspectives to biological questions. There is a growing need for chemical
biologists to synergistically integrate their research programs with their educational activities to
become holistic teacher−scholars. This review examines how course-based undergraduate research
experiences (CUREs) are an innovative method to achieve this integration. Because CUREs are
See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

course-based, the review first offers strategies for creating a student-centered learning
environment, which can improve students’ outcomes. Exemplars of CUREs in chemical biology
are then presented and organized to illustrate the five defining characteristics of CUREs:
Downloaded via IISER BERHAMPUR on January 23, 2024 at 12:21:15 (UTC).

significance, scientific practices, discovery, collaboration, and iteration. Finally, strategies to

overcome common barriers in CUREs are considered as well as future innovations in chemical
biology education.

B achelor degree recipients in chemistry, biochemistry, and

chemical biology join companies and graduate programs
that are increasingly globalized, interdisciplinary, and diversi-
fied. To better prepare students for these contexts, several
national reports have called for (1) cross-disciplinary courses
that give undergraduates a realistic sense of how science is
conducted, (2) meaningful implementation of active learning
strategies to create a student-centered learning environment,
and (3) substitution of traditional, verification laboratory
exercises with research-based laboratory experiences.1−5
These recommendations also recognize that undergraduate
research improves STEM graduation rates,6 boosts students’
self-confidence, and builds transformative mentoring relation-
ships.7,8 Research experiences are particularly beneficial for
retaining first-generation undergraduates, women, and under-
represented minorities in STEM fields. 9,10 The ACS
Committee on Professional Training (CPT) identifies under-
graduate research as a critical element of a bachelor’s
curriculum.11 Readers interested in different models of
undergraduate research as well as the broad opportunities
and challenges presented by it will find an excellent treatment
of the topic in publications by the National Academies of
Sciences, Engineering, and Medicine and the National Research
Council.5,12
Despite the benefits of undergraduate research and its
designation as a high-impact teaching practice,13 the reward
structures within academic institutions frequently tempt faculty
to pursue their teaching and scholarship as mutually exclusive
endeavors. The purpose of this review is to illustrate how
faculty can advance their research program by curricular
partnerships with undergraduate students, a model known as
course-based undergraduate research experiences (CUREs).
This review begins by discussing effective instructional practices
for creating a student-centered learning environment, an
important foundation for CUREs as they are course-based
experiences. The review then profiles innovative CUREs in
chemical biology, emphasizing those with undergraduate
coauthored publications. These exemplars have also been
selected and organized to illustrate the five defining character-
istics of CUREs: demonstrating significance beyond the
classroom, employing scientific practices, discovering new
knowledge, collaboration, and iteration.14 Finally, strategies to
overcome common barriers to the implementation of CUREs
will be discussed.
■ DESIGNING A STUDENT-CENTERED COURSE
Historically, undergraduate research experiences (UREs) have
mimicked the graduate apprenticeship model. The mentoring
relationships built in UREs can be transformative, inculcating
students with the habits of a scientific mind (i.e., patience,
independence, initiative)15 and making them more likely to
attend graduate school.16,17 Despite the power of UREs, they
are limited by scale (small student to faculty ratio) and often
privilege experienced over novice students (Figure 1). CUREs
represent a scalable solution, increasing access to undergraduate
research while simultaneously integrating a faculty member’s
teaching and scholarship.
Because CUREs are courses, it is important that they
maximize student learning. Discipline-based education research
(DBER) in the natural sciences reveals that students learn best
when instructors cultivate a student-centered environment.18,19
A chemical biology course designed around this principle
focuses less on what a chemical biologist knows and more on
how a chemical biologist thinks. The outcomes of student-
centered learning are significant, including greater student
engagement, better performance on summative assessments
(i.e., quizzes and exams), and a higher retention of STEM
majors.20,21 Importantly, no single activity or technology
creates a student-centered classroom. Rather, such classrooms
result when teacher−scholars (1) set learning objectives, (2)
Received: November 18, 2017
Accepted: December 1, 2017
Published: December 1, 2017

© 2017 American Chemical Society 26 DOI: 10.1021/acschembio.7b00986

ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
Figure 1. A comparison of two undergraduate research models:
undergraduate research experiences (UREs) and course-based under-
graduate research experiences (CUREs). Despite their organizational
differences, UREs and CUREs share many outcomes in common.
use formative assessments to gauge students’ comprehension,
(3) adopt active-learning strategies to scaffold students’
learning (Figure 2), and (4) evalute students’ mastery of
course content with summative assessments.18,22
Effective instructors set learning objectives for students,
specific competencies they will achieve by the end of an
experience (i.e., unit, lab, course). Learning objectives demystify
the purpose of the learning experience and support the
development of a schema for learning and students’ ability to
build comprehension. Because students’ prior knowledge affects
their level of comprehension, it is critical that instructors assess
this background in order to present material at an appropriate
level. Formative assessments are very useful in this respect,
providing feedback to both the student and the instructor
without affecting a student’s grade. Several of the active-
learning strategies in Figure 2 can become formative assessment
tools when used to check for student comprehension. For
example, an online video illustrating a laboratory technique
becomes formative assessment when punctuated with con-
ceptual checkpoints using the free-application EdPuzzle;23
students must demonstrate their comprehension by correctly
answering a checkpoint question before the video will resume.
Effective teacher−scholars also recognize that students are
not passive receptacles but rather learn best when they take an
active role in constructing knowledge.24,25 Thus, the highest
impact learning activities are those that are scaffolded, wherein
teachers provide instructional support to build on students’
prior knowledge, support their learning, and minimize
misconceptions. As student proficiency grows, the scaffolding
is removed. Scaffolding is commonly used in project-based
laboratory curricula where students begin with highly detailed
experimental procedures but evolve to develop their own
protocols by the end of the course. Examples of scaffolded
learning from CUREs profiled in this review include analyzing
published synthetic protocols to guide students through
limiting reagent calculations26 and practice problems to build
proficiency in genome annotation before annotating Drosophila
chromosomes.27 Finally, formal assessments such as quizzes
and exams reflect students’ mastery of learning objectives and
are one measure of students’ growth.
27
Reviews
The active learning methods in Figure 2 function best when
context factors such as class size and student background are
taken into consideration. For example, Process Oriented
Guided Inquiry Learning (POGIL) may be well suited to a
smaller sized course because of the need for frequent faculty
check-ins, while concept inventories or computer simulations
could easily be scaled to a course with over 200 students.
Additionally, case studies from the primary literature may work
well for upper division students, whereas case studies from the
popular media may be more appropriate for less experienced
first-year or nonmajor courses. Above all, pedagogical methods
require iterative testing, evaluation, and refinement, just like any
experimental method would be systematically optimized. A
student-centered course can evolve over time, by changing a
single unit or topic. These considerations are critical for
designing an effective course that moves students from content
memorization toward critical thinking, a core skill of successful
researchers.
■ DEFINING CHARACTERISTICS OF CURES
CUREsSignificance Beyond the Classroom. CUREs
provide teacher−scholars an opportunity to bring their research
into the curriculum and in so doing illustrate to students its
significance beyond the classroom’s walls. This can increase
students’ motivation and engagement in the laboratory,
particularly when paired with a tangible output of the research
project. While peer-reviewed publications are often a goal of
CUREs, many outcomes can extend beyond the classroom,
such as student presentations at scientific meetings, contribu-
tions to curated databases such as SEA-PHAGES28 or the
Minimum Information about a Biosynthetic Gene cluster
(MIBiG),29 as well as the generation of evidence-based
recommendations for community action.30 With outcomes
from publication to public engagement, CUREs can benefit
faculty research programs and positively contribute toward
promotion and/or tenure.31 The scientific significance of
CUREs has been recognized by private and public funding
agencies. The NSF has funded chemical-biology-related CUREs
including Bioorganic Chemistry of Eumelanin,32 Bioluminscent
Tools for Visualizing Disease,33 and Fluorinated Reporters of
Protein−Protein Interactions.34 The Howard Hughes Medical
Institute (HHMI) has also funded several chemical biology
CUREs: STEMCats,35 Endophyte and Natural Products
Discovery,36 and Chemical Biology for Sophomores.37 One of
the most extensive CURE programs is the HHMI-sponsored
SEA-PHAGES program, which served more than 3400 mostly
first-year students from over 140 different colleges and
universities in 2017.28 The SEA-PHAGES program has
generated 31 publications to date, 21 of which include
undergraduate coauthors. This program, in which students
isolate and characterize bacteriophages from local environments
and annotate the phage genomes, introduces biological and
genetic concepts relevant to chemical biology students across
the country early in their college careers. Thus, CUREs are a
gateway for students into research and provide valuable training
for subsequent UREs.
CUREsEmploying Scientific Practices. The second
hallmark of CUREs is their use of scientific practices: reading
the primary literature, proposing hypotheses, building and
testing models, gathering and analyzing data, navigating the
ambiguity of real-world data, as well as developing and
critiquing interpretations of one’s findings. A scaffolded
research experience can help undergraduates gain research
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
Figure 2. Eight active-learning strategies to engage students as part of a student-centered course. These practices, when thoughtfully implemented,
have the ability to improve student outcomes. In the primary literature, these strategies are also referred to as “evidenced-based practices.”
independence. Consequently, a CURE need not attempt to
cover all scientific practices with students but rather mean-
ingfully cultivate a few; the specific practices should be
communicated to students through the course’s learning
objectives.
Brandeis University has developed a CURE where students
have synthesized a library of peptide-based inhibitors for
metalloproteases,26 a class of enzymes involved in HIV,
Alzheimers’s disease, and Crohn’s disease.38 Diversity in the
library revolves around natural and unnatural amino acids,
joined to a metal chelating hydroxamic acid. As an example of
scaffolded learning, students were taught to write experimental
protocols through a guided exercise using successful examples
from the peer-reviewed literature. Students’ investment in
literature-based protocols resulted in more thoughtful and
independent work in the laboratory. They also honed structure
determination skills, using 1H NMR spectroscopy to character-
ize the products synthesized. Finally, students strengthened
interpersonal competencies including teamwork, writing ability,
and oral communication.
McMaster University redesigned an undergraduate labora-
tory to explore the plasticity of ActR regulation by a catalog of
28
Reviews
anthraquinone derivatives.39 ActR is a transcriptional repressor
in bacteria. The McMaster CURE is a tour de force for
undergraduate chemical biology laboratory techniques. Stu-
dents utilized a Diels−Alder cycloaddition to both construct
the anthraquinone core and generate diversity within their
chemical catalog (Figure 3A). After purifying and characterizing
the small molecules, students expressed and isolated ActR. Four
of the six anthraquinone derivatives exhibited modest binding
to ActR (Kd = 0.14 μM to 1.70 μM), in an in vitro fluorescence
assay.40 Hammett analysis indicated a subtle electronic effect
with the 4-methoxy derivative being the most active. Despite in
vitro binding, the anthraquinone catalog did not exhibit activity
in an in vivo bioluminescence assay. A lack of in vivo activity is a
common but unfortunate reality of researchespecially in
chemical biologyproviding students an opportunity to iterate
the project and teach resiliency, a lesson that should be learned
early in their development as scientists.41
CUREsDiscovering New Knowledge. The third hall-
mark of CUREs is the discovery of new knowledge. The
outcome of the project should be unknown for both the
student and the instructor. This differs from inquiry-based
laboratories where the outcome is only unknown to the student
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
Figure 3. Small molecule collections synthesized by undergraduates in
chemical biology CUREs. (A) Based on the anthraquinone scaffold.
(B) The combinatorial solid-phase synthesis approach used in
Distributed Drug Discovery (D3). (C) D3 synthesis of natural and
unnatural amino acid derivatives. (D) D3 synthesis of arylopeptoids.
or the research is of little interest to the scientific community.
CUREs require that students gather background knowledge on
their research topic and exercise evidence-based reasoning to
move the project forward.
Two CUREs, one at Yale University and one at Haverford
College, exemplify the discovery of new knowledge. Endo-
phytes are symbiotic fungi or bacteria that live within plants.
They offer a rich source of natural products, fueling
undergraduate discovery for Yale and its collaborators over
the past 15 years.36,42 Recently, students cultivated fungal
endophytes from Ecuador that produce unique unsaturated
hydrocarbons43 and hold promise for bioremediation.44
Bioactivity-guided fractionation of fungal isolates led to the
elucidation of two novel sesquiterpene-polyol natural prod-
29
Reviews
uctsStelliosphaerols A and Bwith activity against Staph-
ylococcus aureus.45 Yale undergraduates are also contributing to
our understanding of the biosynthetic machinery behind the
production of these secondary metabolites. They helped
discover the first fungal monoterpene synthase, important for
the biosynthesis of 1,8-cineole.46
While natural products can be discovered by their activity,47
genome mining is a companion strategy wherein candidate
biosynthetic gene clusters (BGCs) are identified, expressed, and
tested for the production of natural products.48 Undergraduate
researchers at Haverford College are providing new insights
into the evolution of BGCs. Focusing on type II polyketide
synthase (PKS), they discovered that five core genes expanded
and contracted during evolution.49 These changes inform our
understanding of the structural evolution of polyketide natural
products such as the tetracyclines. Studying gene swaps also
provides insight into the chemical diversity of natural product
space and is instructive for reengineering BGCs for the
production of “unnatural” natural products.50 Furthermore, this
evolutionary analysis could be applied to other BGCs or be
used to retrieve extinct natural products.
The success of future genome mining efforts depends on a
robust and curated catalog of BGCs for experimentally
validated natural products. While several databases connect
bacterial gene clusters with their resulting metabolites (e.g.,
DoBISCUIT51 and ClusterMine36052), similar resources for
fungi remain underdeveloped. Haverford undergraduates are
contributing to this unmet need, bringing fungal BGC curation
into the classroom. Students analyzed 217 peer-reviewed
articles and 779 nucleotide records, assigning 197 unique
fungal natural products.53 Genomics-based CUREs, as
exemplified by the Genomics Education Partnership,27 are
particularly well suited for undergraduates because next-
generation sequencing technologies have made the conversion
of data into knowledge the rate-limiting step.54 The Haverford-
generated data set was added to the recently established
Minimum Information about a Biosynthetic Gene cluster
(MIBiG) repository, yielding the largest collection of fungal
natural product gene clusters to date.29
CUREIteration. Bioorthogonal reactions are a corner-
stone of the chemical biology toolbox.55 This research area
highlights how science is inherently iterative and builds upon
existing knowledge. It is fitting then that the fourth character-
istic of CUREs is iteration. Iteration takes many forms.
Students may repeat or revise previous work to address
challenges, gain a deeper level of understanding, or rule out
alternative hypotheses. Students may also be inspired by
previous research as a departure point for their own creative
scholarship.
Undergraduate researchers at the University of Utah have
enriched our understanding of the strain-promoted azide−
alkyne cycloaddition (SPAAC) reaction by thoroughly profiling
its reaction kinetics.56,57 Employing surfactants, they demon-
strated that micellar catalysis could accelerate the rate of
hydrophobic SPAAC substrates up to 179-fold.58 Through
iterative investigations, they determined that the SPAAC’s
second-order rate constant was generally insensitive to buffer
composition and ionic strength.59 However, it responded
differentially to organic cosolvents. These discoveries will
inform the community’s use of this important bioconjugation
reaction.
Undergraduate researchers at Fairfield University were
inspired by the fragmentation properties of the Staudinger
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
ligation60 to chemically label native enzymes. They prepared
“capture-tag-release” (CTR) probes by linking a competitive
enzyme inhibitor and benzophenone via the Staudinger’s aryl
phosphine ester.61 After UV-initiated capture of the enzyme,
addition of an azide-containing tag triggered the Staudinger
ligation, concomitantly labeling the enzyme and fragmenting
the CTR probe, restoring enzymatic activity. As a proof-of-
principle, the CTR strategy was used to biotinylate β-
galactosidase. Highlighting the iterative nature of this research,
the enzyme inhibitor could be replaced with any selective
protein-targeting small molecule, allowing labeling of other
protein targets by subsequent undergraduates.
In a new iteration of the Staudinger ligation, Bowdoin
College undergraduates are pairing the distinctive architecture
of bacterial glycomes with bioconjugation as a strategy for
therapeutic intervention.62 Students have shown that peracety-
lated N-azidoacetylglucosamine (Ac4GlcNAz) can be selectively
incorporated into the surface of the gastric pathogen
Helicobacter pylori (Hp) but not mammalian epithelial
cells.63,64 These azides were conjugated to 2,4-dinitrophenyl
(an immune stimulant) via a Staudinger ligation, resulting in
immune cell mediated destruction of Hp bacteria.64 The project
is well suited to iterative study as changing the cargo attached
to the Staudinger phosphine could enable new antibacterial
strategies: photosensitizers to induce oxidative damage,65
nanoparticles to induce thermal lysis,66 or peptides to breach
bacterial membranes.67 Bowdoin College redesigned a course
to investigate Hp urease, an enzyme critical for Hp
colonization.68 Data indicate that students enjoyed the freedom
of designing and implementing their own research projects;
they strengthened their command of biochemistry concepts
and gained a better understanding of how research impacts
human health.68
CURECollaboration. Collaboration is fittingly the final
characteristic of CUREs, as collaboration is one of the most
salient attributes of the chemical biology community. CUREs
should model how teams of specialized scientists contribute
their diverse skills to solve complex problems. This can be done
interdepartmentally as at Brandeis University, where under-
graduates in an organic chemistry laboratory synthesized
potential inhibitors or inducers of polyglutamine protein
aggregation.69 Biology laboratory undergraduates then tested
these compounds in model assays of Huntington’s disease.
Students in both courses gained a deeper appreciation of how
cross-disciplinary collaboration can yield scientifically signifi-
cant results.
Collaboration can also be global in scale, as pioneered by
Indiana University−Purdue University Indianapolis (IUPUI),
in which undergraduates distributed across institutions (e.g.,
multiple U.S. sites, Poland, Russia, Czech Republic, Cuba)
partner to discover drugs for neglected diseases. Distributed
Drug Discovery (D3) involves three stages: (1) computational
screening of virtual chemical catalogs, (2) chemical synthesis of
drug candidates, and (3) biological screening to determine drug
leads.70−73 A defining feature of D3 is reproducibility, both
within a site and among global sites. Reproducibility allows
students to discern between “failed” experiments and
opportunities for further investigation. For example, when
developing a synthesis for N-acylated amino acid amides,
undergraduates unexpectedlybut reproduciblyobserved
hydrolytic cleavage with electron-rich acyl groups. This led to
a systematic investigation of the structural elements contribu-
ting to this cleavage and ultimately conditions to minimize it.74
30
Reviews
Importantly, without reproducibility, these low yielding
reactions might have been dismissed as outliers. To date, D3
undergraduates have developed six robust solid-phase protocols
for combinatorially synthesizing (Figure 3B) natural and
unnatural amino acid derivatives (Figure 3C).75 They are
screening student-synthesized molecules against Pseudomonas
aeruginosa, a major cause of lung infections in people who have
cystic fibrosis.76 Excitingly, they have identified several potent
inhibitors, on par with the antibacterial agent tobramycin.77,78
Importantly, D3 is not limited to synthesizing amino acids and
their derivatives. Undergraduate researchers at Santa Clara
University have used the methodology to combinatorially
construct arylopeptoids (Figure 3D),79 a promising new class of
peroxisome proliferator-activated receptor (PPAR) γ agonists.80
As chemical biology continues to break down disciplinary
barriers, D3 is breaking down barriers to collaboration and
offers a transformative new model for undergraduate research.
■ OVERCOMING COMMON CURE BARRIERS
A significant barrier to implementing a CURE is selecting an
appropriate research project. It is instructive, therefore, to
consider the qualities of successful CUREs. First, they employ
reliable protocols that are easily learned and performed by
undergraduates. Examples from this review include robust
synthetic transformations (i.e., bioorthogonal reactions, peptide
coupling, Diels−Alder reaction), culturing phages, or genome
annotating procedures. Second, the laboratory protocols in a
CURE should be amenable to the time scale of undergraduates,
working in 3−4 h blocks per week with discrete stopping points
that yield stable and storable (physical or digital) intermediates.
Third, successful CUREs are designed to rapidly generate data
and scale well with student class size. Consequently, preparing
libraries (chemical or mutant) or contributing to information
libraries are ideal approaches because they give students
ownership over their individual contribution yet benefit from
the aggregate data generated by the larger group. Finally, an
entire project does not need to become a CURE, there may be
one aspect that is particularly well suited to undergraduate
adaptation. Once designed, it is ideal to pilot the CURE with a
small section of students. This “soft open” is an opportunity to
gather student feedback, troubleshoot aspects of the protocol,
and prepare activities to further scaffold students’ learning,
helping them make connections between the research and their
coursework. This extra investment of time will make the larger
rollout of the CURE more likely to meet with scientific success.
Not all barriers facing CUREs are purely scientific. For
example, limited institutional resources may prevent faculty
from making innovative changes to their curriculum. Joining a
CURE network (i.e., SEA-PHAGES, Genomics Education
Partnership) can be an effective strategy for overcoming this
barrier. CURE networks often provide training for new
members, practical resources like IRB approval letters and
assessment tools, as well as an online network of peer scientists
to help analyze data and troubleshoot problems. Faculty may
also have success targeting internal grants specifically ear-
marked for curricular innovation, as undergraduate research is a
high-impact teaching practice.13
A well-planned and well-funded CURE can still face barriers
from students, because it is an unfamiliar mode of learning.
Furthermore, the unpredictable nature of research and the
possibility of research “failure” can be worrisome for students
who want to cultivate a high GPA for competitive fellowships
and graduate programs.5 Three strategies to address students’
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
research anxieties include articulating learning objectives,
building undergraduate research teams, and deploying con-
ceptual checkpoints. First, recall that creating a student-
centered learning environment begins by setting learning
objectives. Part of a learning objective is explaining to students
the course’s relevance. Articulate why the course is designed as
a CURE. The benefits may be self-evident to the instructor, but
they are likely obscure to the student. Second, graduate
students work collaboratively, drawing intellectual enrichment
from their research group. Therefore, model this by putting
undergraduates into research teams with specific responsibil-
ities. When undergraduates collaborate in a meaningful way
with peers, it can be a formative experience, teaching them to
work as part of a diverse team. Finally, deploy conceptual
checkpoints throughout the course, to assess student under-
standing and increase student confidence. Examples may
include literature searches or written reports on background
information, guided activities to check students’ mastery of a
research topic or skill, as well as brief group presentations.
These strategies can help students discover the exciting and
transformative nature of research, enabling them to fully
embrace the CURE.
■ DIGITAL LITERACY AND THE FUTURE OF
CHEMICAL BIOLOGY
ACS Chemical Biology includes the byline “the community of
chemical biologists” on its cover. As mentioned above,
collaboration is a distinguishing characteristic of CUREs and
of chemical biologists. Interestingly, today’s chemical biology
undergraduates have grown up immersed in social media
technologies, yet they may not realize the power of their digital
devices for scientific collaboration and learning. To capitalize
on this unrealized potential, an outcome of chemical biology
CUREs should be cultivating digital literacy: the ability to use
digital and information technologies to discover, create,
critique, and communicate information. The University of
WisconsinEau Claire is engaging digital literacy with
undergraduates, using two free Web-based programs:81
SWISS-MODEL (for homology modeling)82 and WEBnm@
(for normal-mode analysis).83 With these tools, students
hypothesized that aminoacyl-tRNA synthetases (AARSs),
which are classified based on sequence and structural
homology,84 could also be discriminated based on their
intrinsic dynamics. Indeed, they discovered that class I and
class II AARSs exhibit distinct patterns of motion within their
catalytic and anticodon binding domains.85 In a separate series
of investigations, students discovered that cytochrome P450
(CYP) superfamily proteins possess strong dynamic similarities,
despite low sequence identity.86 The University of Warwick is
also advancing digital literacy, developing a protocol that allows
undergraduates to rapidly dock chemical libraries to a target
protein.87
Trends in device ownership among undergraduates nation-
wide indicate that the future of digital literacyand thus
chemical biology educationlies in mobile devices: laptops,
smartphones, and tablet computers.88 These devices have the
potential to transform student learning. In the laboratory,
mobile devices are already being used as digital laboratory
notebooks,89 spectrophotometers,90 and luminometers.91 In the
classroom, student feedback is collected in real-time using
mobile devices and the Web site PollEverwhere, obviating the
need for clickers.92 Mobile devices are even being used to
orient undergraduates to ACS national meetings.93 Under-
31
Reviews
graduates want more meaningful and creative learning
experiences with mobile devices, yet a significant percentage
of faculty ban or discourage their use in the classroom.88
Instead of banning devices and sending the message they are
not useful tools for learning, faculty may wish to reflect on why
students are tempted to use mobile devices for nonclass
activities. Is it due to disrespect or a lack of engagement? If the
former, such behavior should never be tolerated and handled
appropriately. If the latter, however, it is worth considering how
these devices can be leveraged to create a more student-
centered learning environment. Chemical biologists and DBER
faculty will benefit by collaborating, to understand how mobile
devices can further improve learning.
This raises an intriguing question, “Do chemical biology
undergraduates possess distinctive competencies?” While the
biology community1,2 and the ACS CPT11 have outlined core
competencies for their undergraduates, the chemical biology
community has yet to do the same. Might modern chemical
biologists distinguish themselves through digital literacy and its
ability to enhance collaboration? While collaboration is not a
new concept, it has undergone a digital paradigm shift.
Collaboration is no longer facilitated by proximity but rather
connectivity, transformed by cloud-based resources like Drop-
box 94 and Google Drive. 95 Chemical biology, as an
interdisciplinary field, is uniquely situated to model scientific
collaborations enabled by digital literacy. Regardless of the
specific competencies enumerated for chemical biologists, the
community must continue to innovatively integrate teaching
and scholarship. In this Review, we have profiled CUREs as one
bridge between these interfaces. Several institutions are building
another bridge in the form of convergent curricula, which
emphasize interdisciplinary connections in introductory
courses.96 Supporting and building new bridges will require
collaboration, particularly partnerships between research
intensive (R1) universities and primarily undergraduate
institutions (PUI). PUI faculty are uniquely positioned to
support the pedagogical growth of R1 faculty. Similarly, R1
faculty can provide instrumentation and subdisciplinary overlap
that is rare in small departments. The fruits of these
collaborations could spur the next wave of innovation in
undergraduate chemical biology education.
■
AUTHOR INFORMATION
Corresponding Author
*Address: 1073 N. Benson Road, Fairfield University −
BNW315, Fairfield, CT 06824. Phone: 203-254-4000. E-mail:
avandyke@fairfield.edu.
ORCID
Aaron R. Van Dyke: 0000-0002-6989-4394
Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS
The authors gratefully acknowledge support from the Fairfield
University College of Arts and Sciences and a Hardiman
Fellowship (to D.H.G.). The authors also thank J. Belitsky, M.
Kubasik, E. Smith and J. Smith-Carpenter for insightful
discussions.
■ KEYWORDS
Committee on Professional Training (CPT): A committee
of the American Chemical Society that promotes excellence
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
in postsecondary education. The CPT also furthers effective
practices and innovations in chemistry education.
Course-based Undergraduate Research Experience
(CURE): Integrating faculty-driven research questions into
an undergraduate course, CUREs are defined by five
characteristics: significance, scientific practices, discovery,
collaboration, and iteration.
Digital Literacy: The ability to use digital and information
technologies to discover, create, critique, and communicate
information.
Distributed Drug Discovery (D3): Undergraduates dis-
tributed across institutions partner to discover drugs for
neglected diseases. D3 involves three stages: (1) computa-
tional screening, (2) chemical synthesis, and (3) biological
screening.
Formative Assessment: Also known as “low-stakes” assess-
ment; a method of assessment that provides the student and
instructor with feedback on the student’s level of
comprehension, generally without affecting the student’s
grade.
Learning Objective: A specific skill or competency the
student should master after completing a learning experi-
ence. Often beginning of the form, “At the end of this
experience, students will be able to...” followed by a specific
action verb or task.
Student-Centered Learning: An environment that focuses
less on transmitting factual information, uses active-learning
strategies and frequent formative assessment so students
build an understanding of the methods and principles of a
discipline.
Summative Assessment: A method of assessment that
measures that student’s mastery of course material and used
to determine the student’s grade (i.e., quizzes, exams, course
projects).
Undergraduate Research Experience (URE): Student
research that follows the apprenticeship model in a faculty
member’s lab. A student typically works in close collabo-
ration with a mentor (i.e., faculty, postdoc or graduate
student).
■
REFERENCES
(1) National Research Council. (2003) BIO2010: Transforming
undergraduate education for future research biologists (Whitacre, P. T.,
Ed.), The National Academies Press, Washington, DC.
(2) Vision and Change in Undergraduate Biology Education. http://
visionandchange.org/files/2011/03/Revised-Vision-and-Change-Final-
Report.pdf (accessed November 2017).
(3) Holdren, J. P., and Lander, E. (2012) Engage to excel: Producing
one million additional college graduates with degrees in science, technology,
engineering, and mathematics, President’s Council of Advisors on
Science and Technology, Washington, DC.
(4) National Research Council. (2015) Reaching Students: What
Research Says About Effective Instruction in Undergraduate Science and
Engineering (Kober, L., Ed.), The National Academies Press,
Washington, DC.
(5) National Research Council. (2015) Integrating Discovery-Based
Research into the Undergraduate Curriculum: Report of a Convocation,
The National Academies Press, Washington, DC.
(6) Rodenbusch, S. E., Hernandez, P. R., Simmons, S. L., and Dolan,
E. L. (2016) Early engagement in course-based research increases
graduation rates and completion of science, engineering and
mathematics degrees. CBE Life Sci. Educ. 15, ar20.
(7) Seymour, E., Hunter, A.-B., Laursen, S. L., and DeAntoni, T.
(2004) Establishing the benefits of research experiences for under-
32
Reviews
graduates in the sciences: First findings from a three-year study. Sci.
Educ. 88, 493−534.
(8) Linn, M. C., Palmer, E., Baranger, A., Gerard, E., and Stone, E.
(2015) Undergraduate research experiences: Impacts and opportu-
nities. Science 347, 1261757.
(9) Estrada, M., Burnett, M., Campbell, A., Campbell, P., Denetclaw,
W., Gutierrez, C., Hurtado, S., Gilbert, J., Matsui, J., McGee, R.,
Okpodu, C., Robinson, T., Summers, M., Werner-Washburne, M., and
Zavala, M. (2016) Improving underrepresented minority student
persistence in STEM. CBE Life Sci. Educ 15, es5.
(10) Bangera, G., and Brownell, S. (2014) Course-based under-
graduate research experiences can make scientific research more
inclusive. CBE Life Sci. Educ 13, 602−606.
(11) Undergraduate Professional Education in Chemistry − ACS
Guidelines and Evaluation Procedures for Bachelor’s Degree
Programs. https://www.acs.org/content/dam/acsorg/about/
governance/committees/training/2015-acs-guidelines-for-bachelors-
degree-programs.pdf (accessed November 2017).
(12) The National Academies of Sciences. (2017) Engineering,
Medicine. Undergraduate Research Experiences for STEM Students:
Successes, Challenges and Opportunities (Gentile, J., Brenner, K., and
Stephens, A., Eds.), The National Academies Press, Washington, DC.
(13) Kuh, G., and Schneider, C. (2008) High-impact educational
practices: what they are, who has access to them, and why they matter,
Association of American Colleges and Universities, Washington, DC.
(14) Auchincloss, L. C., Laursen, S. L., Branchaw, J. L., Eagan, K.,
Graham, M., Hanauer, D. I., Lawrie, G., McLinn, C. Ml, Pelaez, N.,
Rowland, S., Towns, M., Trautmann, N. M., Varma-Nelson, P.,
Weston, T. J., and Dolan, E. L. (2014) Assessment of course-based
undergraduate research experiences: A meeting report. CBE Life Sci.
Educ. 13, 29−40.
(15) Thiry, H., Weston, T. J., Laursen, S. L., and Hunter, A. B.
(2012) The benefits of multi-year research experiences: Differences in
novice and experienced students’ reported gains from undergraduate
research. CBE Life Sci. Educ 11, 260−272.
(16) Eagan, M. K., Jr, Hurtado, S., Chang, M. J., Garcia, G. A.,
Herrera, F. A., and Garibay, J. C. (2013) Making a difference in science
education: The impact of undergraduate research programs. Am. Educ.
Res. J. 50, 683−713.
(17) Taraban, R., and Logue, E. (2012) Academic factors that affect
undergraduate research experiences. J. Educ. Psychol 104, 499.
(18) National Research Council. (2012) Discipline-Based Education
Research: Understanding and Improving Learning in Undergraduate
Science and Engineering (Singer, S. R., Nielsen, N. R., and
Schweingruber, H. A., Eds.), The National Academies Press,
Washington, DC.
(19) Kober, N. (2015) Reaching students: What research says about
effective instruction in undergraduate science and engineering, National
Research Council, Washington, DC.
(20) Freeman, S., Eddy, S., McDonough, M., Smith, M., Okoroafor,
N., Jordt, H., and Wenderoth, M. (2014) Active learning increases
student performance in science, engineering and mathematics. Proc.
Natl. Acad. Sci. U. S. A. 111, 8410−8415.
(21) Watkins, J., and Mazur, E. (2013) Retaining Students in Science,
Technology, Engineering, and Mathematics (STEM) majors. J. Coll.
Sci. Tech 42, 36−41.
(22) Feldon, D. (2010) Why Magic Bullets Don’t Work. Change 42,
15−21.
(23) EdPuzzle. https://edpuzzle.com/ (accessed November 2017).
(24) Freire, P. (1972) Pedagogy of the Oppressed, Herder & Herder,
New York.
(25) Vygotsky, L. (1978) Mind in Society: The Development of Higher
Psychological Processes, Harvard University Press: Cambridge.
(26) Pontrello, J. K. (2015) Metalloprotease Peptide Inhibitors: A
Semester-Long Organic Synthetic Research Project for the Introduc-
tory Laboratory Course. J. Chem. Educ. 92, 811−818.
(27) Genomics Education Partnership. http://gep.wustl.edu (ac-
cessed November 2017).
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
(28) Science Education Alliance (SEA) PHAGES. https://seaphages.
org (accessed November 2017).
(29) Medema, M. H., Kottmann, R., Yilmaz, P., Cummings, M.,
Biggins, J. B., Blin, K., de Bruijn, I., Chooi, Y. H., Claesen, J., Coates, R.
C., Cruz-Morales, P., Duddela, S., Düsterhus, S., Edwards, D. J., Fewer,
D. P., Garg, N., Geiger, C., Gomez-Escribano, J. P., Greule, A.,
Hadjithomas, M., Haines, A. S., Helfrich, E. J. N., Hillwig, M. L., Ishida,
K., Jones, A. C., Jones, C. S., Jungmann, K., Kegler, C., Kim, H. U.,
Kötter, P., Krug, D., Masschelein, J., Melnik, A. V., Mantovani, S. M.,
Monroe, E. A., Moore, M., Moss, N., Nützmann, H.-W., Pan, G., Pati,
A., Petras, D., Reen, F. J., Rosconi, F., Rui, Z., Tian, Z., Tobias, N. J.,
Tsunematsu, Y., Wiemann, P., Wyckoff, E., Yan, X., Yim, G., Yu, F.,
Xie, Y., Aigle, B., Apel, A. K., Balibar, C. J., Balskus, E. P., Barona-
Gómez, F., Bechthold, A., Bode, H. B., Borriss, R., Brady, S. F.,
Brakhage, A. A., Caffrey, P., Cheng, Y.-Q., Clardy, J., Cox, R. J., De
Mot, R., Donadio, S., Donia, M. S., van der Donk, W. A., Dorrestein, P.
C., Doyle, S., Driessen, A. J. M., Ehling-Schulz, M., Entian, K.-D.,
Fischbach, M. A., Gerwick, L., Gerwick, W. H., Gross, H., Gust, B.,
Hertweck, C., Höfte, M., Jensen, S. E., Ju, J., Katz, L., Kaysser, L.,
Klassen, J. L., Keller, N. P., Kormanec, J., Kuipers, O. P., Kuzuyama, T.,
Kyrpides, N. C., Kwon, H.-J., Lautru, S., Lavigne, R., Lee, C. Y.,
Linquan, B., Liu, X., Liu, W., Luzhetskyy, A., Mahmud, T., Mast, Y.,
Méndez, C., Metsä-Ketelä, M., Micklefield, J., Mitchell, D. A., Moore,
B. S., Moreira, L. M., Müller, R., Neilan, B. A., Nett, M., Nielsen, J.,
O’Gara, F., Oikawa, H., Osbourn, A., Osburne, M. S., Ostash, B.,
Payne, S. M., Pernodet, J.-L., Petricek, M., Piel, J., Ploux, O.,
Raaijmakers, J. M., Salas, J. A., Schmitt, E. K., Scott, B., Seipke, R. F.,
Shen, B., Sherman, D. H., Sivonen, K., Smanski, M. J., Sosio, M.,
Stegmann, E., Süssmuth, R. D., Tahlan, K., Thomas, C. M., Tang, Y.,
Truman, A. W., Viaud, M., Walton, J. D., Walsh, C. T., Weber, T., van
Wezel, G. P., Wilkinson, B., Willey, J. M., Wohlleben, W., Wright, G.
D., Ziemert, N., Zhang, C., Zotchev, S. B., Breitling, R., Takano, E., and
Glöckner, F. O. (2015) Minimum Information about a Biosynthetic
Gene cluster. Nat. Chem. Biol. 11, 625−631.
(30) Savan, B., and Sider, D. (2003) Contrasting approaches to
community based research and a case study of community
sustainability in Toronto, Canada. Local Environ 8, 303−316.
(31) Shortlidge, E. E., Bangera, G., and Brownell, S. E. (2016)
Faculty perspectives on developing and teaching course-based
undergraduate research experiences. BioScience 66, 54−62.
(32) Award Abstract #1305919 NSF RUI: Bioorganic chemistry of
eumelanin. https://www.nsf.gov/awardsearch/showAward?AWD_
ID=1305919&HistoricalAwards=false (accessed November 2017).
(33) Award Abstract #1351302 NSF CAREER: Engineered bio-
luminescent tools for visualizing metastatic disease. https://www.nsf.
gov/awardsearch/showAward?AWD_ID=
1351302&HistoricalAwards=false (accessed November 2017).
(34) Award Abstract #1352091 NSF CAREER: Teflon proteins for
protein-protein interaction ligand discovery. https://www.nsf.gov/
awardsearch/showAward?AWD_ID=1352091&HistoricalAwards=
false (accessed November 2017).
(35) Swanson, H. I., Sarge, O-K. P., Rodrigo-Peiris, T., Xiang, L., and
Cassone, V. M. (2016) Development of a course-based undergraduate
research experience to introduce drug-receptor concepts. J. Med. Educ.
Curr. Dev. 3, 57−66.
(36) Strobel, S. A., and Strobel, G. A. (2007) Plant endophytes as a
platform for discovery-based undergraduate science education. Nat.
Chem. Biol. 3, 356−359.
(37) Schepartz Laboratory − Chemical Biology for Sophomores.
http://schepartzlab.yale.edu/chembiolsoph/index.html (accessed No-
vember 2017).
(38) Moss, M. L., White, J. M., Lambert, M. H., and Andrews, R. C.
(2001) TACE and Other ADAM Proteases as Targets for Drug
Discovery. Drug Discovery Today 6, 417−426.
(39) Tahlan, K., Yu, Z., Xu, Y., Davidson, A. R., and Nodwell, J. R.
(2008) Ligand recognition by ActR, a TetR-like regulator of
actinorhodin export. J. Mol. Biol. 383, 753−761.
(40) McKenzie, N., McNulty, J., McLeod, D., McFadden, M., and
Balachandran, N. (2012) Synthesizing novel anthraquinone natural
33
Reviews
product-like compounds to investigate protein-ligand interactions in
both an in vitro and in vivo assay: an integrated research-based third-
year chemical biology laboratory course. J. Chem. Educ. 89, 743−749.
(41) Hernandez, P. R., Schultz, P., Estrada, M., Woodcock, A., and
Chance, R. C. (2013) Sustaining optimal motivation: A longitudinal
analysis of interventions to broaden participation of underrepresented
students in STEM. J. Educ. Psychol. 105, 89−107.
(42) Bascom-Slack, C. A., Arnold, A. E., and Strobel, S. A. (2012)
Student-directed discovery of the plant microbiome and its products.
Science 338, 485−486.
(43) Shaw, J. J., Spakowicz, D. J., Dalal, R. S., Davis, J. H., Lehr, N. A.,
Dunican, B. F., Orellana, E. A., Narvaez-Trujillo, A., and Strobel, S. A.
(2015) Biosynthesis and genomic analysis of medium-chain hydro-
carbon production by the endophytic fungal isolate Nigrograna
mackinnonii E5202H. Appl. Microbiol. Biotechnol. 99, 3715−3728.
(44) Russell, J. R., Huang, J., Anand, P., Kucera, K., Sandoval, A. G.,
Dantzler, K. W., Hickman, D., Jee, J., Kimovec, F. M., Koppstein, D.,
Marks, D. H., Mittermiller, P. A., Nunez, S. J., Santiago, M., Townes,
M. A., Vishnevetsky, M., Williams, N. E., Vargas, M. P., Boulanger, L.
A., Bascom-Slack, C., and Strobel, S. A. (2011) Biodegradation of
Polyester Polyurethane by Endophytic Fungi. Appl. Environ. Microb 77,
6076−6084.
(45) Forcina, G. C., Castro, A., Bokesch, H. R., Spakowicz, D. J.,
Legaspi, M. E., Kucera, K., Villota, S., Narvaez-Trujillo, A., McMahon,
J. B., Gustafson, K., and Strobel, S. A. (2015) Stelliosphaerols A and B,
sesquiterpene-polyol conjugates from an Ecuadorian fungal endophyte.
J. Nat. Prod. 78, 3005−3010.
(46) Shaw, J. J., Berbasova, T., Sasaki, T., Jefferson-George, K.,
Spakowicz, D. J., Dunican, B. F., Portero, C. E., Narvaez-Trujillo, A.,
and Strobel, S. A. (2015) Identification of a fungal 1,8-cineole synthase
from Hypoxylon sp. with specificity determinants in common with the
plant synthases. J. Biol. Chem. 290, 8511−8526.
(47) Harvey, A. L., Edrada-Ebel, R., and Quinn, R. J. (2015) The re-
emergence of natural products for drug discovery in the genomics era.
Nat. Rev. Drug Discovery 14, 111−129.
(48) Ziemert, N., Alanjary, M., and Weber, T. (2016) The evolution
of genome mining in microbes − a review. Nat. Prod. Rep. 33, 988−
1005.
(49) Hillenmeyer, M. E., Vandova, G. A., Berlew, E. E., and
Charkoudian, L. K. (2015) Evolution of chemical diversity by
coordinated gene swaps in type II polyketide gene clusters. Proc.
Natl. Acad. Sci. U. S. A. 112, 13952−13957.
(50) Lane, A. L., and Moore, B. S. (2011) A sea of biosynthesis:
marine natural products meet the molecular age. Nat. Prod. Rep. 28,
411−428.
(51) Ichikawa, N., Sasagawa, M., Yamamoto, M., Komaki, H.,
Yoshida, Y., Yamazaki, S., and Fujita, N. (2012) DoBISCUIT: A
database of secondary metabolite biosynthetic gene clusters. Nucleic
Acids Res. 41, D408−D414.
(52) Conway, K. R., and Boddy, C. N. (2012) ClusterMine360: A
database of microbial PKS/NRPS biosynthesis. Nucleic Acids Res. 41,
D402−D407.
(53) Li, Y. F., Tsai, K. J. S., Harvey, C. J. B., Li, J. J., Ary, B. E., Berlew,
E. E., Boehman, B. L., Findley, D. M., Friant, A. G., Gardner, C. A.,
Gould, M. P., Ha, J. H., Lilley, B. K., McKinstry, E. L., Nawal, S., Parry,
R. C., Rothchild, K. W., Silbert, S. D., Tentilucci, M. D., Thurston, A.
M., Wai, R. B., Yoon, Y., Aiyar, R. S., Medema, M. H., Hillenmeyer, M.
E., and Charkoudian, L. K. (2016) Comprehensive curation and
analysis of fungal biosynthetic gene clusters of published natural
products. Fungal Genet. Biol. 89, 18−28.
(54) Goodwin, S., McPherson, J. D., and McCombie, W. R. (2016)
Coming of age: ten years of next-generation sequencing technologies.
Nat. Rev. Genet. 17, 333−351.
(55) Chen, X., and Wu, Y. (2016) Selective chemical labeling of
proteins. Org. Biomol. Chem. 14, 5417−5439.
(56) Debets, M. F., van Berkel, S. S., Schoffelen, S., Rutjes, F. P J. T.,
van Hest, J. C. M., and van Delft, F. L. (2010) Aza-
dibenzocyclooctynes for fast and efficient enzyme PEGylation via
copper-free (3 + 2) cycloaddition. Chem. Commun. 46, 97−99.
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology
(57) Jewett, J. C., Sletten, E. M., and Bertozzi, C. R. (2010) Rapid
Cu-free click chemistry with readily synthesized biarylazacycloocty-
nones. J. Am. Chem. Soc. 132, 3688−3690.
(58) Anderton, G. I., Bangerter, A. S., Davis, T. C., Feng, Z., Furtak,
A. J., Larsen, J. O., Scroggin, T. L., and Heemstra, J. M. (2015)
Accelerating strain-promoted azide-alkyne cycloaddition using micellar
catalysis. Bioconjugate Chem. 26, 1687−1691.
(59) Davis, D. L., Price, E. K., Aderibigbe, S. O., Larkin, M. X.,
Barlow, E. D., Chen, R., Ford, L. C., Gray, Z. T., Gren, S. H., Jin, Y.,
Keddington, K. S., Kent, A. D., Kim, D., Lewis, A., Marrouche, R. S.,
O’Dair, M. K., Powell, D. R., Scadden, M. H. C., Session, C. B., Tao, J.,
Trieu, J., Whiteford, K. N., Yuan, Z., Yun, G., Zhu, J., and Heemstra, J.
M. (2016) Effect of buffer conditions and organic cosolvents on the
rate of strain-promoted azide-alkyne cycloaddition. J. Org. Chem. 81,
6816−6819.
(60) Saxon, E., and Bertozzi, C. R. (2000) Cell surface engineering by
a modified staudinger reaction. Science 287, 2007−2010.
(61) Van Dyke, A. R., Etemad, L. S., Vessicchio, M. J., Naclerio, G. A.,
and Jedson, V. (2016) Capture-Tag-Release: A strategy for small
molecule labeling of native enzymes. ChemBioChem 17, 1602−1605.
(62) Tra, V. N., and Dube, D. H. (2014) Glycans in pathogenic
bacteria − potential for targeted covalent therapeutics and imaging
agents. Chem. Commun. 50, 4659−4673.
(63) Champasa, K., Longwell, S. A., Eldridge, A. M., Stemmler, E. A.,
and Dube, D. H. (2013) Targeted identification of glycosylated
proteins in the gastric pathogen Helicobacter pylori (Hp). Mol. Cell.
Proteomics 12, 2568−2586.
(64) Kaewsapsak, P., Esonu, O., and Dube, D. (2013) Recruiting the
host’s immune system to target Helicobacter pylori’s surface glycans.
ChemBioChem 14, 721−726.
(65) Sperandio, F. F., Huang, Y.-Y., and Hamblin, M. R. (2013)
Antimicrobial photodynamic therapy to kill gram-negative bacteria.
Recent Pat. Anti-Infect. Recent Pat. Anti-Infect. Drug Discovery 8, 108−
120.
(66) Norman, R. S., Stone, J. W., Gole, A., Murphy, C. J., and Sabo-
Attwood, T. L. (2008) Targeted photothermal lysis of the pathogenic
bacteria, Pseudomonas aeruginosa, with gold nanorods. Nano Lett. 8,
302−306.
(67) Cruz, J., Ortiz, C., Guzman, F., Fernandez-Lafuente, R., and
Torres, R. (2014) Antimicrobial peptides: promising compounds
against pathogenic microorganisms. Curr. Med. Chem. 21, 2299−2321.
(68) Farnham, K. R., and Dube, D. H. (2015) A semester-long
project-oriented biochemistry laboratory based on Helicobacter pylori
Urease. Biochem. Mol. Biol. Educ. 43, 333−340.
(69) Boltax, A. L., Armanious, S., Kosinski-Collins, M. S., and
Pontrello, J. K. (2015) Connecting biology and organic chemistry
introductory laboratory courses through a collaborative research
project. Biochem. Mol. Biol. Educ. 43, 233−244.
(70) Scott, W. L., and O'Donnell, M. J. (2009) Distributed Drug
Discovery, Part 1: Linking Academia and Combinatorial Chemistry to
Find Drug Leads for Developing World Diseases. J. Comb. Chem. 11,
3−13.
(71) Scott, W. L., Alsina, J., Audu, C. O., Babaev, E., Cook, L., Dage,
J. L., Goodwin, L. A., Martynow, J. G., Matosiuk, D., Royo, M., Smith,
J. G., Strong, A. T., Wickizer, K., Woerly, E. M., Zhou, Z., and
O’Donnell, M. J. (2009) Distributed Drug Discovery, Part 2: Global
Rehearsal of Alkylating Agents for the Synthesis of Resin-Bound
Unnatural Amino Acids and Virtual D3 Catalog Construction. J. Comb.
Chem. 11, 14−33.
(72) Scott, W. L., Audu, C. O., Dage, J. L., Goodwin, L. A.,
Martynow, J. G., Platt, L. K., Smith, J. G., Strong, A. T., Wickizer, K.,
Woerly, E. M., and O’Donnell, M. J. (2009) Distributed Drug
Discovery, Part 3: Using D3Methodology to Synthesize Analogs of an
Anti-Melanoma Compound. J. Comb. Chem. 11, 34−43.
(73) Abraham, M., Denton, R., Harper, R., Scott, W., O’Donnell, M.,
and Durrant, J. (2017) Documenting and harnessing the biological
potential of molecules in Distributed Drug Discovery (D3) virtual
catalogs. Chem. Biol. Drug Des. 90, 909−918.
34
Reviews
(74) Samaritoni, J. G., Copes, A. T., Crews, D. K., Glos, C.,
Thompson, A. L., Wilson, C., O’Donnell, M. J., and Scott, W. L.
(2014) Unexpected Hydrolytic Instability of N-Acylated Amino Acid
Amides and Peptides. J. Org. Chem. 79, 3140−3151.
(75) Scott, W. L., Denton, R. E., Marrs, K. A., Durrant, J. D.,
Samaritoni, J. G., Abraham, M. M., Brown, S. P., Carnahan, J. M.,
Fischer, L. G., Glos, C. E., Sempsrott, P. J., and O’Donnell, M. J.
(2015) Distributed Drug Discovery: Advancing Chemical Education
through Contextualized Combinatorial Solid-Phase Organic Labo-
ratories. J. Chem. Educ. 92, 819−826.
(76) Hassett, D. J., Cuppoletti, J., Trapnell, B., Lymar, S., Rowe, J.,
Sun Yoon, S., Hilliard, G., Parvatiyar, K., Kamani, M., Wozniak, D.,
Hwang, S., McDermott, T., and Ochsner, U. (2002) Anaerobic
metabolism and quorum sensing by Pseudomonas aeruginosa biofilms
in chronically infected cystic fibrosis airways: rethinking antibiotic
treatment strategies and drug targets. Adv. Drug Delivery Rev. 54,
1425−1443.
(77) Scott, W., Samaritoni, J., Anderson, G., Marrs, K., Colglazier, S.,
Hitchens, J., Burris, S., Ware, M., and O’Donnell, M. (2016)
Distributed drug discovery (D3) in action: Finding inhibitors of P.
aeruginosa, Abstracts of Papers, 252nd National Meeting of the American
Chemical Society, Philadelphia, PA, August 21−25, 2016, MEDI 27,
American Chemical Society, Washington, DC.
(78) Scott, W. L., Denton, R. E., Anderson, G., Kathleen, M.,
Samaritoni, J. G., Colglazier, S., Lacombe, J., Phillips, M., and
O’Donnell, M. J. (2016) Identifying a potent inhibitor of Pseudomonas
aeruginosa through the Distributed Drug Discovery (D3) process,
Abstracts of Papers, 250th National Meeting of the American Chemical
Society, Boston, MA, August 16−20, 2015, MEDI 52, American
Chemical Society, Washington, DC.
(79) Fuller, A. A. (2016) Combinatorial solid-phase synthesis of
aromatic oligoamides: A research-based laboratory module for
undergraduate organic chemistry. J. Chem. Educ. 93, 953−957.
(80) Worm-Leonhard, K., Hjelmgaard, T., Petersen, R. K.,
Kristiansen, K., and Nielsen, J. (2013) Discovery of New PPARγ
Agonists Based on Arylopeptoids. Bioorg. Med. Chem. Lett. 23, 4162−
4165.
(81) Pirhadi, S., Sunseri, J., and Koes, D. R. (2016) Open source
molecular modeling. J. Mol. Graphics Modell. 69, 127−143.
(82) SWISS-MODEL. https://swissmodel.expasy.org (accessed
November 2017).
(83) WEBnm@ − Webtool for Normal Mode Analysis. http://apps.
cbu.uib.no/webnma/home (accessed November 2017).
(84) O’Donoghue, P., and Luthey-Schulten, Z. (2003) On the
evolution of structure in aminoacyl-tRNA synthetases. Microbiol. Mol.
Biol. Rev. 67, 550−571.
(85) Warren, N., Strom, A., Nicolet, B., Albin, K., Albrecht, J., Bausch,
B., Dobbe, M., Dudek, M., Firgens, S., Fritsche, C., Gunderson, A.,
Heimann, J., Her, C., Hurt, J., Konorev, D., Lively, M., Meacham, S.,
Rodriguez, V., Tadayon, S., Trcka, D., Yang, Y., Bhattacharyya, S., and
Hati, S. (2014) Comparison of the intrinsic dynamics of aminoacyl-
tRNA synthetases. Protein J. 33, 184−198.
(86) Dorner, M. E., McMunn, R. D., Bartholow, T. G., Calhoon, B.
E., Conlon, M. R., Dulli, J. M., Fehling, S. C., Fisher, C. R., Hodgson,
S. W., Keenan, S. W., Kruger, A. N., Mabin, J. W., Mazula, D. L.,
Monte, C. A., Olthafer, A., Sexton, A. E., Soderholm, B. R., Strom, A.
M., and Hati, S. (2015) Comparison of Intrinsic Dynamics of
Cytochrome P450 Proteins Using Normal Mode Analysis. Protein Sci.
24, 1495−1507.
(87) Price, G. W., Gould, P. S., and Marsh, A. (2014) Use of freely
available and open source tools for in silico screening in chemical
biology. J. Chem. Educ. 91, 602−604.
(88) Study of Undergraduate Students and Information Technology,
2017. https://library.educause.edu/~/media/files/library/2017/10/
studentitstudy2017.pdf (accessed November 2017).
(89) Van Dyke, A. R., and Smith-Carpenter, J. (2017) Bring Your
Own Device: A Digital Notebook for Undergraduate Biochemistry
Laboratory Using a Free, Cross-Platform Application. J. Chem. Educ.
94, 656−661.
DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35
ACS Chemical Biology Reviews

(90) Grasse, E. K., Torcasio, M. H., and Smith, A. W. (2016)

Teaching UV-Vis spectroscopy with a 3D-printable smartphone
spectrophotometer. J. Chem. Educ. 93, 146−151.
(91) Arts, R., den Hartog, I., Zijlema, S. E., Thijssen, V., van der
Beelen, S. H. E., and Merkx, M. (2016) Detection of antibodies in
blood plasma using bioluminescent sensor proteins and a smartphone.
Anal. Chem. 88, 4525−4532.
(92) PollEverywhere. https://www.polleverywhere.com (accessed
November 2017).
(93) Kubasik, M. A., Van Dyke, A. R., Harper-Leatherman, A. S.,
Miecznikowski, J. R., Steffen, L. K., and Smith-Carpenter, J. (2016) A
cloud-based scavenger hunt: Orienting undergraduates to ACS
national meetings. J. Chem. Educ. 93, 1957−1960.
(94) Dropbox. https://www.dropbox.com/ (accessed November
2017).
(95) Evernote Corporation. https://evernote.com/ (accessed No-
vember 2017).
(96) Boarding up the tunnel: Innovations in introductory chemistry
curricula. http://sites.tufts.edu/convergentchemistry/ (accessed No-
vember 2017).

35 DOI: 10.1021/acschembio.7b00986
ACS Chem. Biol. 2018, 13, 26−35