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Discovery of Catalytic Phages by Biocatalytic Self-Assembly

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Department of Chemistry and Biochemistry, Hunter College, City University of New York, 695 Park Avenue, New York, New York 10065, United States
WestCHEM, Department of Pure & Applied Chemistry, University of Strathclyde, 295 Cathedral Street, Glasgow G1 1XL, U.K.
§ Department of Civil and Environmental Engineering, University of Strathclyde, 75 Montrose Street, Glasgow G1 1XJ, U.K.
Advanced Science Research Centre, City University of New York, 85 St Nicholas Terrace, New York, New York 10031, United States
Cite this: J. Am. Chem. Soc. 2014, 136, 45, 15893–15896
Publication Date (Web):October 24, 2014
https://doi.org/10.1021/ja509393p
Copyright © 2014 American Chemical Society

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    Abstract

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    Discovery of new catalysts for demanding aqueous reactions is challenging. Here, we describe methodology for selection of catalytic phages by taking advantage of localized assembly of the product of the catalytic reaction that is screened for. A phage display library covering 109 unique dodecapeptide sequences is incubated with nonassembling precursors. Phages which are able to catalyze formation of the self-assembling reaction product (via amide condensation) acquire an aggregate of reaction product, enabling separation by centrifugation. The thus selected phages can be amplified by infection of Escherichia coli. These phages are shown to catalyze amide condensation and hydrolysis. Kinetic analysis shows a minor role for substrate binding. The approach enables discovery and mass-production of biocatalytic phages.

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    Optimization of phage elution, selected sequences, additional TEM analysis, amide condensation, FRET peptide hydrolysis, and detailed methods. This material is available free of charge via the Internet at http://pubs.acs.org.

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    11. Melissa J. MacDonald, Luke D. Lavis, Donald Hilvert, and Samuel H. Gellman . Evaluation of the Ser-His Dipeptide, a Putative Catalyst of Amide and Ester Hydrolysis. Organic Letters 2016, 18 (15) , 3518-3521. https://doi.org/10.1021/acs.orglett.6b01279
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    14. Yurii S. Moroz, Tiffany T. Dunston, Olga V. Makhlynets, Olesia V. Moroz, Yibing Wu, Jennifer H. Yoon, Alissa B. Olsen, Jaclyn M. McLaughlin, Korrie L. Mack, Pallavi M. Gosavi, Nico A. J. van Nuland, and Ivan V. Korendovych . New Tricks for Old Proteins: Single Mutations in a Nonenzymatic Protein Give Rise to Various Enzymatic Activities. Journal of the American Chemical Society 2015, 137 (47) , 14905-14911. https://doi.org/10.1021/jacs.5b07812
    15. Jing Chen, Ke Shi, Rongjing Chen, Zhaoyi Zhai, Peiyong Song, Lesley W. Chow, Rona Chandrawati, E. Thomas Pashuck, Fang Jiao, Yiyang Lin. Supramolecular Hydrolase Mimics in Equilibrium and Kinetically Trapped States. Angewandte Chemie 2024, 136 (9) https://doi.org/10.1002/ange.202317887
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    17. Patrizia Janković, Erik Otović, Goran Mauša, Daniela Kalafatovic. Manually curated dataset of catalytic peptides for ester hydrolysis. Data in Brief 2023, 48 , 109290. https://doi.org/10.1016/j.dib.2023.109290
    18. Sara Carvalho, David Q. Peralta Reis, Sara V. Pereira, Daniela Kalafatovic, Ana Sofia Pina. Catalytic Peptides: the Challenge between Simplicity and Functionality. Israel Journal of Chemistry 2022, 62 (9-10) https://doi.org/10.1002/ijch.202200029
    19. Marina Kurbasic, Ana M. Garcia, Simone Viada, Silvia Marchesan. Heterochiral tetrapeptide self‐assembly into hydrogel biomaterials for hydrolase mimicry. Journal of Peptide Science 2022, 28 (1) https://doi.org/10.1002/psc.3304
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    35. O. Zozulia, M. A. Dolan, I. V. Korendovych. Catalytic peptide assemblies. Chemical Society Reviews 2018, 47 (10) , 3621-3639. https://doi.org/10.1039/C8CS00080H
    36. Niels ten Brummelhuis, Patrick Wilke, Hans G. Börner. Identification of Functional Peptide Sequences to Lead the Design of Precision Polymers. Macromolecular Rapid Communications 2017, 38 (24) https://doi.org/10.1002/marc.201700632
    37. Christopher C. Moser, Nathan M. Ennist, Joshua A. Mancini, P. L. Dutton. Making Maquette Models of Bioenergetic Structures. 2017, 1-24. https://doi.org/10.1039/9781788010405-00001
    38. Olga V. Makhlynets, Pallavi M. Gosavi, Ivan V. Korendovych. Short Self‐Assembling Peptides Are Able to Bind to Copper and Activate Oxygen. Angewandte Chemie 2016, 128 (31) , 9163-9166. https://doi.org/10.1002/ange.201602480
    39. Olga V. Makhlynets, Pallavi M. Gosavi, Ivan V. Korendovych. Short Self‐Assembling Peptides Are Able to Bind to Copper and Activate Oxygen. Angewandte Chemie International Edition 2016, 55 (31) , 9017-9020. https://doi.org/10.1002/anie.201602480
    40. Takuya Machida, Som Dutt, Nicolas Winssinger. Allosterically Regulated Phosphatase Activity from Peptide–PNA Conjugates Folded Through Hybridization. Angewandte Chemie 2016, 128 (30) , 8737-8740. https://doi.org/10.1002/ange.201602751
    41. Takuya Machida, Som Dutt, Nicolas Winssinger. Allosterically Regulated Phosphatase Activity from Peptide–PNA Conjugates Folded Through Hybridization. Angewandte Chemie International Edition 2016, 55 (30) , 8595-8598. https://doi.org/10.1002/anie.201602751
    42. Yoshiaki Maeda, Olga V. Makhlynets, Hiroshi Matsui, Ivan V. Korendovych. Design of Catalytic Peptides and Proteins Through Rational and Combinatorial Approaches. Annual Review of Biomedical Engineering 2016, 18 (1) , 311-328. https://doi.org/10.1146/annurev-bioeng-111215-024421
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    46. Yoshiaki Maeda, Justin Fang, Yasuhiro Ikezoe, Douglas H. Pike, Vikas Nanda, Hiroshi Matsui, . Molecular Self-Assembly Strategy for Generating Catalytic Hybrid Polypeptides. PLOS ONE 2016, 11 (4) , e0153700. https://doi.org/10.1371/journal.pone.0153700
    47. Ignacio Alfonso. From simplicity to complex systems with bioinspired pseudopeptides. Chemical Communications 2016, 52 (2) , 239-250. https://doi.org/10.1039/C5CC07596C
    48. Angelique N. Besold, Leland R. Widger, Frances Namuswe, Jamie L. Michalek, Sarah L. J. Michel, David P. Goldberg. Revisiting and re-engineering the classical zinc finger peptide: consensus peptide-1 (CP-1). Molecular BioSystems 2016, 12 (4) , 1183-1193. https://doi.org/10.1039/C5MB00796H
    49. Chengbiao Yang, Xinrui Ren, Dan Ding, Ling Wang, Zhimou Yang. Enzymatic induction of supramolecular order and bioactivity. Nanoscale 2016, 8 (20) , 10768-10773. https://doi.org/10.1039/C6NR02330D
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