Lessons from bacteriophages part 1: Deriving utility from protein structure, function, and evolution
Abstract
Historically, some of the most fundamental discoveries of modern molecular biology were revealed by examination of phage-infected cells. Some examples include the use of bacteriophage T2 to show that DNA, not protein, was the genetic material by Hershey and Chase in 1952. Crick and colleagues showed that codons are degenerate and encode for single amino acids by making use of T4 bacteriophage. Brenner and colleagues discovered that mRNA acts as the messenger in relaying the information from DNA to ribosomes with the aid of bacteriophage T2. Szybalski and colleagues demonstrated the semiconservative mechanism of DNA replication using λ phage. Restriction modification, a bacterial innate immune system that evolved as protection against invading mobile genetic elements such as plasmids and phages, was discovered in bacteriophage-infected cells. Restriction mapping was crucial for the completion of the human genome project. The mechanism of action of heat shock genes—which encode for molecular chaperones such as dnaK, dnaJ, and grpE, as well as the groE gene locus, which encodes for the molecular chaperones GroES and GroEL—were discovered in λ phage–infected Escherichia coli. The first capsid assembly inhibitor, the fluorescent dye 4,4’–bis(1-anilinonaphthalene-8-sulfonic acid) (bisANS), was discovered in experiments investigating assembly of phage P22. These are justmore »
- Authors:
-
- Univ. of Connecticut, Storrs, CT (United States). Dept. of Molecular and Cell Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1560552
- Grant/Contract Number:
- AC02-05CH11231; R01 GM076661
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Pathogens
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 5; Journal ID: ISSN 1553-7374
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Asija, Kunica, Teschke, Carolyn M., and Dutch, Rebecca Ellis. Lessons from bacteriophages part 1: Deriving utility from protein structure, function, and evolution. United States: N. p., 2018.
Web. doi:10.1371/journal.ppat.1006971.
Asija, Kunica, Teschke, Carolyn M., & Dutch, Rebecca Ellis. Lessons from bacteriophages part 1: Deriving utility from protein structure, function, and evolution. United States. https://doi.org/10.1371/journal.ppat.1006971
Asija, Kunica, Teschke, Carolyn M., and Dutch, Rebecca Ellis. Thu .
"Lessons from bacteriophages part 1: Deriving utility from protein structure, function, and evolution". United States. https://doi.org/10.1371/journal.ppat.1006971. https://www.osti.gov/servlets/purl/1560552.
@article{osti_1560552,
title = {Lessons from bacteriophages part 1: Deriving utility from protein structure, function, and evolution},
author = {Asija, Kunica and Teschke, Carolyn M. and Dutch, Rebecca Ellis},
abstractNote = {Historically, some of the most fundamental discoveries of modern molecular biology were revealed by examination of phage-infected cells. Some examples include the use of bacteriophage T2 to show that DNA, not protein, was the genetic material by Hershey and Chase in 1952. Crick and colleagues showed that codons are degenerate and encode for single amino acids by making use of T4 bacteriophage. Brenner and colleagues discovered that mRNA acts as the messenger in relaying the information from DNA to ribosomes with the aid of bacteriophage T2. Szybalski and colleagues demonstrated the semiconservative mechanism of DNA replication using λ phage. Restriction modification, a bacterial innate immune system that evolved as protection against invading mobile genetic elements such as plasmids and phages, was discovered in bacteriophage-infected cells. Restriction mapping was crucial for the completion of the human genome project. The mechanism of action of heat shock genes—which encode for molecular chaperones such as dnaK, dnaJ, and grpE, as well as the groE gene locus, which encodes for the molecular chaperones GroES and GroEL—were discovered in λ phage–infected Escherichia coli. The first capsid assembly inhibitor, the fluorescent dye 4,4’–bis(1-anilinonaphthalene-8-sulfonic acid) (bisANS), was discovered in experiments investigating assembly of phage P22. These are just some of the examples of contributions made by bacteriophage research in the past few decades. Here, we discuss additional discoveries derived from studies of phages.},
doi = {10.1371/journal.ppat.1006971},
journal = {PLoS Pathogens},
number = 5,
volume = 14,
place = {United States},
year = {2018},
month = {5}
}
Web of Science
Figures / Tables:

Works referenced in this record:
A Molecular Staple: D-Loops in the I Domain of Bacteriophage P22 Coat Protein Make Important Intercapsomer Contacts Required for Procapsid Assembly
journal, August 2015
- D'Lima, Nadia G.; Teschke, Carolyn M.
- Journal of Virology, Vol. 89, Issue 20
Engineering virus-like particles as vaccine platforms
journal, June 2016
- Frietze, Kathryn M.; Peabody, David S.; Chackerian, Bryce
- Current Opinion in Virology, Vol. 18
Escherichia coli-derived virus-like particles in vaccine development
journal, February 2017
- Huang, Xiaofen; Wang, Xin; Zhang, Jun
- npj Vaccines, Vol. 2, Issue 1
Nature׳s favorite building block: Deciphering folding and capsid assembly of proteins with the HK97-fold
journal, May 2015
- Suhanovsky, Margaret M.; Teschke, Carolyn M.
- Virology, Vol. 479-480
Development of virus-like particles for diagnostic and prophylactic biomedical applications: Development of virus-like particles
journal, February 2015
- Schwarz, Benjamin; Douglas, Trevor
- Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, Vol. 7, Issue 5
Contractile injection systems of bacteriophages and related systems: Conserved features of a contractile sheath-rigid tube mechanism
journal, February 2018
- Taylor, Nicholas M. I.; van Raaij, Mark J.; Leiman, Petr G.
- Molecular Microbiology, Vol. 108, Issue 1
‘Let the phage do the work’: Using the phage P22 coat protein structures as a framework to understand its folding and assembly mutants
journal, June 2010
- Teschke, Carolyn M.; Parent, Kristin N.
- Virology, Vol. 401, Issue 2
Comparison of a bacteriophage-delivered DNA vaccine and a commercially available recombinant protein vaccine against hepatitis B
journal, March 2011
- Clark, Jason R.; Bartley, Kathryn; Jepson, Catherine D.
- FEMS Immunology & Medical Microbiology, Vol. 61, Issue 2
Processing of Filamentous Bacteriophage Virions in Antigen-Presenting Cells Targets Both HLA Class I and Class II Peptide Loading Compartments
journal, January 2003
- Gaubin, Muriel; Fanutti, Cristina; Mishal, Zohar
- DNA and Cell Biology, Vol. 22, Issue 1
An Unstable Intermediate Carrying Information from Genes to Ribosomes for Protein Synthesis
journal, May 1961
- Brenner, S.; Jacob, F.; Meselson, M.
- Nature, Vol. 190, Issue 4776
Extensive subunit contacts underpin herpesvirus capsid stability and interior-to-exterior allostery
journal, April 2016
- Huet, Alexis; Makhov, Alexander M.; Huffman, Jamie B.
- Nature Structural & Molecular Biology, Vol. 23, Issue 6
A century of phage research: Bacteriophages and the shaping of modern biology: Cause to reflect
journal, December 2014
- Keen, Eric C.
- BioEssays, Vol. 37, Issue 1
The pyocins of Pseudomonas aeruginosa
journal, May 2002
- Michel-Briand, Yvon; Baysse, Christine
- Biochimie, Vol. 84, Issue 5-6
The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage
journal, October 2000
- Nakayama, Keisuke; Takashima, Kayoko; Ishihara, Hiroshi
- Molecular Microbiology, Vol. 38, Issue 2
Accurate model annotation of a near-atomic resolution cryo-EM map
journal, March 2017
- Hryc, Corey F.; Chen, Dong-Hua; Afonine, Pavel V.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
Flexible Connectors between Capsomer Subunits that Regulate Capsid Assembly
journal, August 2017
- Hasek, Mary L.; Maurer, Joshua B.; Hendrix, Roger W.
- Journal of Molecular Biology, Vol. 429, Issue 16
Filamentous phage as an immunogenic carrier to elicit focused antibody responses against a synthetic peptide
journal, May 2006
- Vanhouten, N.; Zwick, M.; Menendez, A.
- Vaccine, Vol. 24, Issue 19
Topologically Linked Protein Rings in the Bacteriophage HK97 Capsid
journal, September 2000
- Wikoff, W. R.
- Science, Vol. 289, Issue 5487
Toothpicks, Serendipity and the Emergence of the Escherichia coli DnaK (Hsp70) and GroEL (Hsp60) Chaperone Machines
journal, December 2006
- Georgopoulos, Costa
- Genetics, Vol. 174, Issue 4
The phage major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system
journal, February 2009
- Pell, L. G.; Kanelis, V.; Donaldson, L. W.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 11
Asymmetric distribution of the transcribing regions on the complementary strands of coliphage lambda DNA.
journal, June 1967
- Taylor, K.; Hradecna, Z.; Szybalski, W.
- Proceedings of the National Academy of Sciences, Vol. 57, Issue 6
Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry
journal, May 2005
- Fokine, A.; Leiman, P. G.; Shneider, M. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 20
Structural biology of type VI secretion systems
journal, April 2012
- Cascales, Eric; Cambillau, Christian
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1592
Lambda phage-based vaccine induces antitumor immunity in hepatocellular carcinoma
journal, September 2017
- Iwagami, Yoshifumi; Casulli, Sarah; Nagaoka, Katsuya
- Heliyon, Vol. 3, Issue 9
Architecture and assembly of the Type VI secretion system
journal, August 2014
- Zoued, Abdelrahim; Brunet, Yannick R.; Durand, Eric
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 8
Structure Unifies the Viral Universe
journal, July 2012
- Abrescia, Nicola G. A.; Bamford, Dennis H.; Grimes, Jonathan M.
- Annual Review of Biochemistry, Vol. 81, Issue 1
Type VI secretion and bacteriophage tail tubes share a common assembly pathway
journal, January 2014
- Brunet, Y. R.; Henin, J.; Celia, H.
- EMBO reports, Vol. 15, Issue 3
General Nature of the Genetic Code for Proteins
journal, December 1961
- Crick, F. H. C.; Barnett, Leslie; Brenner, S.
- Nature, Vol. 192, Issue 4809
Double-stranded DNA bacteriophage prohead protease is homologous to herpesvirus protease
journal, August 2004
- Cheng, Hua; Shen, Nan; Pei, Jimin
- Protein Science, Vol. 13, Issue 8
Herpesvirus capsid assembly: insights from structural analysis
journal, August 2011
- Brown, Jay C.; Newcomb, William W.
- Current Opinion in Virology, Vol. 1, Issue 2
Common Evolutionary Origin of Procapsid Proteases, Phage Tail Tubes, and Tubes of Bacterial Type VI Secretion Systems
journal, November 2016
- Fokine, Andrei; Rossmann, Michael G.
- Structure, Vol. 24, Issue 11
Inhibition of viral capsid assembly by 1,1'-bis(4-anilinonaphthalene-5-sulfonic acid)
journal, October 1993
- Teschke, Carolyn M.; King, Jonathan; Prevelige, Peter E.
- Biochemistry, Vol. 32, Issue 40
Works referencing / citing this record:
Phage penetration of eukaryotic cells: practical implications
journal, November 2019
- Żaczek, Maciej; Górski, Andrzej; Skaradzińska, Aneta
- Future Virology, Vol. 14, Issue 11
The phage L capsid decoration protein has a novel OB-fold and an unusual capsid binding strategy
journal, April 2019
- Newcomer, Rebecca L.; Schrad, Jason R.; Gilcrease, Eddie B.
- eLife, Vol. 8