Chemical strategies for the covalent modification of filamentous phage

Bernard, Jenna M.  L.; Francis, Matthew B.

doi:10.3389/fmicb.2014.00734

Title: Chemical strategies for the covalent modification of filamentous phage

Journal Article · 22 December 2014 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2014.00734 · OSTI ID:1628129

Bernard, Jenna M. L. ^[1]; Francis, Matthew B. ^[2]

Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; DOE/OSTI
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division

Historically filamentous bacteriophage have been known to be the workhorse of phage display due to their ability to link genotype to phenotype. More recently, the filamentous phage scaffold has proven to be powerful outside the realm of phage display technology in fields such as molecular imaging, cancer research and materials, and vaccine development. The ability of the virion to serve as a platform for a variety of applications heavily relies on the functionalization of the phage coat proteins with a wide variety of functionalities. Genetic modification of the coat proteins has been the most widely used strategy for functionalizing the virion; however, complementary chemical modification strategies can help to diversify the range of materials that can be developed. This review emphasizes the recent advances that have been made in the chemical modification of filamentous phage as well as some of the challenges that are involved in functionalizing the virion.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628129

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 5; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Virus-Templated Assembly of Porphyrins into Light-Harvesting Nanoantennae Nam, Yoon Sung; Shin, Taeho; Park, Heechul Journal of the American Chemical Society, Vol. 132, Issue 5 https://doi.org/10.1021/ja908812b	journal	February 2010
Genetically Engineered Nanofiber-Like Viruses For Tissue Regenerating Materials Merzlyak, Anna; Indrakanti, Shyam; Lee, Seung-Wuk Nano Letters, Vol. 9, Issue 2 https://doi.org/10.1021/nl8036728	journal	February 2009
N-Terminal Labeling of Filamentous Phage To Create Cancer Marker Imaging Agents Carrico, Zachary M.; Farkas, Michelle E.; Zhou, Yu ACS Nano, Vol. 6, Issue 8 https://doi.org/10.1021/nn301134z	journal	July 2012
Refactored M13 Bacteriophage as a Platform for Tumor Cell Imaging and Drug Delivery Ghosh, Debadyuti; Kohli, Aditya G.; Moser, Felix ACS Synthetic Biology, Vol. 1, Issue 12 https://doi.org/10.1021/sb300052u	journal	August 2012
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Sortagging: a versatile method for protein labeling Popp, Maximilian W.; Antos, John M.; Grotenbreg, Gijsbert M. Nature Chemical Biology, Vol. 3, Issue 11 https://doi.org/10.1038/nchembio.2007.31	journal	September 2007
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Ordering of Quantum Dots Using Genetically Engineered Viruses Lee, S. -W. Science, Vol. 296, Issue 5569 https://doi.org/10.1126/science.1068054	journal	May 2002
Virus-Based Toolkit for the Directed Synthesis of Magnetic and Semiconducting Nanowires Mao, C. Science, Vol. 303, Issue 5655 https://doi.org/10.1126/science.1092740	journal	January 2004
Virus-Enabled Synthesis and Assembly of Nanowires for Lithium Ion Battery Electrodes Nam, Ki Tae; Kim, Dong-Wan; Yoo, Pil J. Science, Vol. 312, Issue 5775, p. 885-888 https://doi.org/10.1126/science.1122716	journal	May 2006
Fabricating Genetically Engineered High-Power Lithium Ion Batteries Using Multiple Virus Genes Lee, Yun Jung; Yi, Hyunjung; Kim, Woo-Jae Science, Vol. 324, Issue 5930, p. 1051-1055 https://doi.org/10.1126/science.1171541	journal	April 2009
Targeting Antibacterial Agents by Using Drug-Carrying Filamentous Bacteriophages Yacoby, I.; Shamis, M.; Bar, H. Antimicrobial Agents and Chemotherapy, Vol. 50, Issue 6 https://doi.org/10.1128/aac.00169-06	journal	May 2006
Molecular Engineering of Viral Gene Delivery Vehicles Schaffer, David V.; Koerber, James T.; Lim, Kwang-il Annual Review of Biomedical Engineering, Vol. 10, Issue 1 https://doi.org/10.1146/annurev.bioeng.10.061807.160514	journal	August 2008
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M13 bacteriophage-polymer nanoassemblies as drug delivery vehicles Suthiwangcharoen, Nisaraporn; Li, Tao; Li, Kai Nano Research, Vol. 4, Issue 5 https://doi.org/10.1007/s12274-011-0104-2	journal	February 2011
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Monofunctional Near-Infrared Fluorochromes for Imaging Applications Hilderbrand, Scott A.; Kelly, Kimberley A.; Weissleder, Ralph Bioconjugate Chemistry, Vol. 16, Issue 5 https://doi.org/10.1021/bc0501799	journal	September 2005
M13 Bacteriophage Display Framework That Allows Sortase-Mediated Modification of Surface-Accessible Phage Proteins Hess, Gaelen T.; Cragnolini, Juan J.; Popp, Maximilian W. Bioconjugate Chemistry, Vol. 23, Issue 7 https://doi.org/10.1021/bc300130z	journal	June 2012
Facile and Stabile Linkages through Tyrosine: Bioconjugation Strategies with the Tyrosine-Click Reaction Ban, Hitoshi; Nagano, Masanobu; Gavrilyuk, Julia Bioconjugate Chemistry, Vol. 24, Issue 4 https://doi.org/10.1021/bc300665t	journal	March 2013
Near Infrared Fluorescence-Based Bacteriophage Particles for Ratiometric pH Imaging Hilderbrand, Scott A.; Kelly, Kimberly A.; Niedre, Mark Bioconjugate Chemistry, Vol. 19, Issue 8 https://doi.org/10.1021/bc800188p	journal	August 2008
Chemical Modification of M13 Bacteriophage and Its Application in Cancer Cell Imaging Li, Kai; Chen, Yi; Li, Siqi Bioconjugate Chemistry, Vol. 21, Issue 7 https://doi.org/10.1021/bc900405q	journal	July 2010
Quantitative Synthesis of Genetically Encoded Glycopeptide Libraries Displayed on M13 Phage Ng, Simon; Jafari, Mohammad R.; Matochko, Wadim L. ACS Chemical Biology, Vol. 7, Issue 9 https://doi.org/10.1021/cb300187t	journal	June 2012
Discovery of Light-Responsive Ligands through Screening of a Light-Responsive Genetically Encoded Library Jafari, Mohammad R.; Deng, Lu; Kitov, Pavel I. ACS Chemical Biology, Vol. 9, Issue 2 https://doi.org/10.1021/cb4006722	journal	November 2013
M13 Bacteriophage as a Biological Scaffold for Magnetically-Recoverable Metal Nanowire Catalysts: Combining Specific and Nonspecific Interactions To Design Multifunctional Nanocomposites Avery, Kendra N.; Schaak, Janell E.; Schaak, Raymond E. Chemistry of Materials, Vol. 21, Issue 11 https://doi.org/10.1021/cm900869u	journal	June 2009
Filamentous Phage Display in the New Millennium Kehoe, John W.; Kay, Brian K. Chemical Reviews, Vol. 105, Issue 11 https://doi.org/10.1021/cr000261r	journal	November 2005
Phage Display Smith, George P.; Petrenko, Valery A. Chemical Reviews, Vol. 97, Issue 2 https://doi.org/10.1021/cr960065d	journal	April 1997
A Three-Component Mannich-Type Reaction for Selective Tyrosine Bioconjugation Joshi, Neel S.; Whitaker, Leanna R.; Francis, Matthew B. Journal of the American Chemical Society, Vol. 126, Issue 49 https://doi.org/10.1021/ja0439017	journal	December 2004
Tyrosine-Selective Protein Alkylation Using π-Allylpalladium Complexes Tilley, S. David; Francis, Matthew B. Journal of the American Chemical Society, Vol. 128, Issue 4 https://doi.org/10.1021/ja057106k	journal	February 2006
Phage Display Evolution of a Peptide Substrate for Yeast Biotin Ligase and Application to Two-Color Quantum Dot Labeling of Cell Surface Proteins Chen, Irwin; Choi, Yoon-Aa; Ting, Alice Y. Journal of the American Chemical Society, Vol. 129, Issue 20 https://doi.org/10.1021/ja071013g	journal	May 2007
Oxidative Modification of Native Protein Residues Using Cerium(IV) Ammonium Nitrate Seim, Kristen L.; Obermeyer, Allie C.; Francis, Matthew B. Journal of the American Chemical Society, Vol. 133, Issue 42 https://doi.org/10.1021/ja206324q	journal	October 2011
Site-Specific Protein Transamination Using N -Methylpyridinium-4-carboxaldehyde Witus, Leah S.; Netirojjanakul, Chawita; Palla, Kanwal S. Journal of the American Chemical Society, Vol. 135, Issue 45 https://doi.org/10.1021/ja408868a	journal	October 2013
Rapid, Hydrolytically Stable Modification of Aldehyde-Terminated Proteins and Phage Libraries Kitov, Pavel I.; Vinals, Daniel F.; Ng, Simon Journal of the American Chemical Society, Vol. 136, Issue 23 https://doi.org/10.1021/ja5023909	journal	May 2014
Optimization of a Biomimetic Transamination Reaction Scheck, Rebecca A.; Dedeo, Michel T.; Iavarone, Anthony T. Journal of the American Chemical Society, Vol. 130, Issue 35 https://doi.org/10.1021/ja802495w	journal	September 2008
Virus-Templated Assembly of Porphyrins into Light-Harvesting Nanoantennae Nam, Yoon Sung; Shin, Taeho; Park, Heechul Journal of the American Chemical Society, Vol. 132, Issue 5 https://doi.org/10.1021/ja908812b	journal	February 2010
Genetically Engineered Nanofiber-Like Viruses For Tissue Regenerating Materials Merzlyak, Anna; Indrakanti, Shyam; Lee, Seung-Wuk Nano Letters, Vol. 9, Issue 2 https://doi.org/10.1021/nl8036728	journal	February 2009
N-Terminal Labeling of Filamentous Phage To Create Cancer Marker Imaging Agents Carrico, Zachary M.; Farkas, Michelle E.; Zhou, Yu ACS Nano, Vol. 6, Issue 8 https://doi.org/10.1021/nn301134z	journal	July 2012
Refactored M13 Bacteriophage as a Platform for Tumor Cell Imaging and Drug Delivery Ghosh, Debadyuti; Kohli, Aditya G.; Moser, Felix ACS Synthetic Biology, Vol. 1, Issue 12 https://doi.org/10.1021/sb300052u	journal	August 2012
Phage display: practicalities and prospects Willats, William G. T. Plant Molecular Biology, Vol. 50, Issue 6, p. 837-854 https://doi.org/10.1023/A:1021215516430	journal	December 2002
Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly Whaley, Sandra R.; English, D. S.; Hu, Evelyn L. Nature, Vol. 405, Issue 6787 https://doi.org/10.1038/35015043	journal	June 2000
Phage-encoded combinatorial chemical libraries based on bicyclic peptides Heinis, Christian; Rutherford, Trevor; Freund, Stephan Nature Chemical Biology, Vol. 5, Issue 7 https://doi.org/10.1038/nchembio.184	journal	May 2009
Sortagging: a versatile method for protein labeling Popp, Maximilian W.; Antos, John M.; Grotenbreg, Gijsbert M. Nature Chemical Biology, Vol. 3, Issue 11 https://doi.org/10.1038/nchembio.2007.31	journal	September 2007
Introducing genetically encoded aldehydes into proteins Carrico, Isaac S.; Carlson, Brian L.; Bertozzi, Carolyn R. Nature Chemical Biology, Vol. 3, Issue 6, p. 321-322 https://doi.org/10.1038/nchembio878	journal	April 2007
Genetically modified filamentous phage as bactericidal agents: a pilot study Hagens, S.; Blasi, U. Letters in Applied Microbiology, Vol. 37, Issue 4 https://doi.org/10.1046/j.1472-765X.2003.01400.x	journal	October 2003
Protein evolution with an expanded genetic code Liu, C. C.; Mack, A. V.; Tsao, M. -L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 46 https://doi.org/10.1073/pnas.0809543105	journal	November 2008
A method for directed evolution and functional cloning of enzymes Pedersen, H.; Holder, S.; Sutherlin, D. P. Proceedings of the National Academy of Sciences, Vol. 95, Issue 18 https://doi.org/10.1073/pnas.95.18.10523	journal	September 1998
Selection of optical biosensors from chemisynthetic antibody libraries Jespers, L.; Bonnert, T. P.; Winter, G. Protein Engineering Design and Selection, Vol. 17, Issue 10 https://doi.org/10.1093/protein/gzh083	journal	November 2004
Ordering of Quantum Dots Using Genetically Engineered Viruses Lee, S. -W. Science, Vol. 296, Issue 5569 https://doi.org/10.1126/science.1068054	journal	May 2002
Virus-Based Toolkit for the Directed Synthesis of Magnetic and Semiconducting Nanowires Mao, C. Science, Vol. 303, Issue 5655 https://doi.org/10.1126/science.1092740	journal	January 2004
Virus-Enabled Synthesis and Assembly of Nanowires for Lithium Ion Battery Electrodes Nam, Ki Tae; Kim, Dong-Wan; Yoo, Pil J. Science, Vol. 312, Issue 5775, p. 885-888 https://doi.org/10.1126/science.1122716	journal	May 2006
Fabricating Genetically Engineered High-Power Lithium Ion Batteries Using Multiple Virus Genes Lee, Yun Jung; Yi, Hyunjung; Kim, Woo-Jae Science, Vol. 324, Issue 5930, p. 1051-1055 https://doi.org/10.1126/science.1171541	journal	April 2009
Targeting Antibacterial Agents by Using Drug-Carrying Filamentous Bacteriophages Yacoby, I.; Shamis, M.; Bar, H. Antimicrobial Agents and Chemotherapy, Vol. 50, Issue 6 https://doi.org/10.1128/AAC.00169-06	journal	May 2006
GENE THERAPY: Twenty-First Century Medicine Verma, Inder M.; Weitzman, Matthew D. Annual Review of Biochemistry, Vol. 74, Issue 1 https://doi.org/10.1146/annurev.biochem.74.050304.091637	journal	June 2005
Molecular Engineering of Viral Gene Delivery Vehicles Schaffer, David V.; Koerber, James T.; Lim, Kwang-il Annual Review of Biomedical Engineering, Vol. 10, Issue 1 https://doi.org/10.1146/annurev.bioeng.10.061807.160514	journal	August 2008
Killing cancer cells by targeted drug-carrying phage nanomedicines Bar, Hagit; Yacoby, Iftach; Benhar, Itai BMC Biotechnology, Vol. 8, Issue 1 https://doi.org/10.1186/1472-6750-8-37	journal	January 2008
In vivo characteristics of targeted drug-carrying filamentous bacteriophage nanomedicines Vaks, Lilach; Benhar, Itai Journal of Nanobiotechnology, Vol. 9, Issue 1 https://doi.org/10.1186/1477-3155-9-58	journal	January 2011
Site directed biotinylation of filamentous phage structural proteins Smelyanski, Larisa; Gershoni, Jonathan M. Virology Journal, Vol. 8, Issue 1 https://doi.org/10.1186/1743-422X-8-495	journal	November 2011
A generalized kinetic model for amine modification of proteins with application to phage display Jin, Xiaofang; Newton, Jessica Rose; Montgomery-Smith, Stephen BioTechniques, Vol. 46, Issue 3 https://doi.org/10.2144/000113074	journal	March 2009

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Modified TMV particles as beneficial scaffolds to present sensor enzymes Koch, Claudia; Wabbel, Katrin; Eber, Fabian J. Universität Stuttgart https://doi.org/10.18419/opus-9220	collection	January 2015
Immunocontraception: Filamentous Bacteriophage as a Platform for Vaccine Development Samoylova, Tatiana I.; Braden, Timothy D.; Spencer, Jennifer A. Current Medicinal Chemistry, Vol. 24, Issue 35 https://doi.org/10.2174/0929867324666170911160426	journal	November 2017
Exploring the Secretomes of Microbes and Microbial Communities Using Filamentous Phage Display Gagic, Dragana; Ciric, Milica; Wen, Wesley X. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00429	journal	April 2016
Novel roles for well-known players: from tobacco mosaic virus pests to enzymatically active assemblies Koch, Claudia; Eber, Fabian J.; Azucena, Carlos Beilstein Journal of Nanotechnology, Vol. 7 https://doi.org/10.3762/bjnano.7.54	journal	January 2016
Application of filamentous phages in environment: A tectonic shift in the science and practice of ecorestoration Sharma, Radhey Shyam; Karmakar, Swagata; Kumar, Pankaj Ecology and Evolution, Vol. 9, Issue 4 https://doi.org/10.1002/ece3.4743	journal	January 2019
Virus-derived materials: bury the hatchet with old foes Wu, Jiahe; Wu, Honghui; Nakagawa, Shinsaku Biomaterials Science, Vol. 8, Issue 4 https://doi.org/10.1039/c9bm01383k	journal	January 2020
Modified TMV particles as beneficial scaffolds to present sensor enzymes Koch, Claudia; Wabbel, Katrin; Eber, Fabian J. Universität Stuttgart https://doi.org/10.18419/opus-9220	collection	January 2015
Modified TMV Particles as Beneficial Scaffolds to Present Sensor Enzymes Koch, Claudia; Wabbel, Katrin; Eber, Fabian J. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01137	journal	December 2015
Novel roles for well-known players: from tobacco mosaic virus pests to enzymatically active assemblies Koch, Claudia; Eber, Fabian J.; Azucena, Carlos Beilstein Journal of Nanotechnology, Vol. 7 https://doi.org/10.3762/bjnano.7.54	journal	January 2016
Novel roles for well-known players: from tobacco mosaic virus pests to enzymatically active assemblies Koch, Claudia; Eber, Fabian J.; Azucena, Carlos Karlsruhe https://doi.org/10.5445/ir/1000058793	text	January 2016

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59 BASIC BIOLOGICAL SCIENCES
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