Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

You’ve supercharged your research process with ACS and Mendeley!

STEP 1:
Click to create an ACS ID

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

MENDELEY PAIRING EXPIRED
Your Mendeley pairing has expired. Please reconnect
ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

Phage Display of Dynamic Covalent Binding Motifs Enables Facile Development of Targeted Antibiotics

  • Kelly A. McCarthy
    Kelly A. McCarthy
    Department of Chemistry, Merkert Chemistry Center, Boston College, Chestnut Hill, Massachusetts 02467, United States
  • Michael A. Kelly
    Michael A. Kelly
    Department of Chemistry, Merkert Chemistry Center, Boston College, Chestnut Hill, Massachusetts 02467, United States
  • Kaicheng Li
    Kaicheng Li
    Department of Chemistry, Merkert Chemistry Center, Boston College, Chestnut Hill, Massachusetts 02467, United States
    More by Kaicheng Li
  • Samantha Cambray
    Samantha Cambray
    Department of Chemistry, Merkert Chemistry Center, Boston College, Chestnut Hill, Massachusetts 02467, United States
  • Azade S. Hosseini
    Azade S. Hosseini
    Department of Chemistry, Merkert Chemistry Center, Boston College, Chestnut Hill, Massachusetts 02467, United States
  • Tim van Opijnen
    Tim van Opijnen
    Department of Biology, Boston College, Chestnut Hill, Massachusetts 02467, United States
  • , and 
  • Jianmin Gao*
    Jianmin Gao
    Department of Chemistry, Merkert Chemistry Center, Boston College, Chestnut Hill, Massachusetts 02467, United States
    *[email protected]
    More by Jianmin Gao
Cite this: J. Am. Chem. Soc. 2018, 140, 19, 6137–6145
Publication Date (Web):April 27, 2018
https://doi.org/10.1021/jacs.8b02461
Copyright © 2018 American Chemical Society

    Article Views

    7113

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (1)»

    Abstract

    Abstract Image

    Antibiotic resistance of bacterial pathogens poses an increasing threat to the wellbeing of our society and urgently calls for new strategies for infection diagnosis and antibiotic discovery. The antibiotic resistance problem at least partially arises from extensive use of broad-spectrum antibiotics. Ideally, for the treatment of infection, one would like to use a narrow-spectrum antibiotic that specifically targets and kills the disease-causing strain. This is particularly important considering the commensal bacterial species that are beneficial and sometimes even critical to the health of a human being. In this contribution, we describe a phage display platform that enables rapid identification of peptide probes for specific bacterial strains. The phage library described herein incorporates 2-acetylphenylboronic acid moieties to elicit dynamic covalent binding to the bacterial cell surface. Screening of the library against live bacterial cells yields submicromolar and highly specific binders for clinical strains of Staphylococcus aureus and Acinetobacter baumannii that display antibiotic resistance. We further show that the identified peptide probes can be readily converted to bactericidal agents that deliver generic toxins to kill the targeted bacterial strain with high specificity. The phage display platform described here is applicable to a wide array of bacterial strains, paving the way to facile diagnosis and development of strain-specific antibiotics.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/jacs.8b02461.

    • Small molecule synthesis, peptide synthesis and characterization, additional flow cytometry, and microscopy results (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 47 publications.

    1. J. Trae Hampton, Wenshe Ray Liu. Diversification of Phage-Displayed Peptide Libraries with Noncanonical Amino Acid Mutagenesis and Chemical Modification. Chemical Reviews 2024, 124 (9) , 6051-6077. https://doi.org/10.1021/acs.chemrev.4c00004
    2. Mengmeng Zheng, Jianmin Gao. Phage Display of Two Distinct Warheads to Inhibit Challenging Proteins. ACS Chemical Biology 2023, 18 (10) , 2259-2266. https://doi.org/10.1021/acschembio.3c00297
    3. Sabrina E. Iskandar, Lilly F. Chiou, Tina M. Leisner, Devan J. Shell, Jacqueline L. Norris-Drouin, Cyrus Vaziri, Kenneth H. Pearce, Albert A. Bowers. Identification of Covalent Cyclic Peptide Inhibitors in mRNA Display. Journal of the American Chemical Society 2023, 145 (28) , 15065-15070. https://doi.org/10.1021/jacs.3c04833
    4. Rafael Alcala-Torano, Mariha Islam, Jaclyn Cika, Kwok Ho Lam, Rongsheng Jin, Konstantin Ichtchenko, Charles B. Shoemaker, James A. Van Deventer. Yeast Display Enables Identification of Covalent Single-Domain Antibodies against Botulinum Neurotoxin Light Chain A. ACS Chemical Biology 2022, 17 (12) , 3435-3449. https://doi.org/10.1021/acschembio.2c00574
    5. Mengmeng Zheng, Fa-Jie Chen, Kaicheng Li, Rahi M. Reja, Fredrik Haeffner, Jianmin Gao. Lysine-Targeted Reversible Covalent Ligand Discovery for Proteins via Phage Display. Journal of the American Chemical Society 2022, 144 (34) , 15885-15893. https://doi.org/10.1021/jacs.2c07375
    6. Rahi M. Reja, Wenjian Wang, Yuhan Lyu, Fredrik Haeffner, Jianmin Gao. Lysine-Targeting Reversible Covalent Inhibitors with Long Residence Time. Journal of the American Chemical Society 2022, 144 (3) , 1152-1157. https://doi.org/10.1021/jacs.1c12702
    7. Arunika I. Ekanayake, Lena Sobze, Payam Kelich, Jihea Youk, Nicholas J. Bennett, Raja Mukherjee, Atul Bhardwaj, Frank Wuest, Lela Vukovic, Ratmir Derda. Genetically Encoded Fragment-Based Discovery from Phage-Displayed Macrocyclic Libraries with Genetically Encoded Unnatural Pharmacophores. Journal of the American Chemical Society 2021, 143 (14) , 5497-5507. https://doi.org/10.1021/jacs.1c01186
    8. Bunty Sharma, Vipul Thakur, Gurpreet Kaur, Ganga Ram Chaudhary. Efficient Photodynamic Therapy against Gram-Positive and Gram-Negative Bacteria Using Rose Bengal Encapsulated in Metallocatanionic Vesicles in the Presence of Visible Light. ACS Applied Bio Materials 2020, 3 (12) , 8515-8524. https://doi.org/10.1021/acsabm.0c00901
    9. Sabrina E. Iskandar, Victoria A. Haberman, Albert A. Bowers. Expanding the Chemical Diversity of Genetically Encoded Libraries. ACS Combinatorial Science 2020, 22 (12) , 712-733. https://doi.org/10.1021/acscombsci.0c00179
    10. Michael Kelly, Samantha Cambray, Kelly A. McCarthy, Wenjian Wang, Edward Geisinger, Juan Ortiz-Marquez, Tim van Opijnen, Jianmin Gao. Peptide Probes of Colistin Resistance Discovered via Chemically Enhanced Phage Display. ACS Infectious Diseases 2020, 6 (9) , 2410-2418. https://doi.org/10.1021/acsinfecdis.0c00206
    11. Jia Song, Yuan Zheng, Mengjiao Huang, Lingling Wu, Wei Wang, Zhi Zhu, Yanling Song, Chaoyong Yang. A Sequential Multidimensional Analysis Algorithm for Aptamer Identification based on Structure Analysis and Machine Learning. Analytical Chemistry 2020, 92 (4) , 3307-3314. https://doi.org/10.1021/acs.analchem.9b05203
    12. Mengjiao Huang, Jia Song, Peifeng Huang, Xiaofeng Chen, Wei Wang, Zhi Zhu, Yanling Song, Chaoyong Yang. Molecular Crowding Evolution for Enabling Discovery of Enthalpy-Driven Aptamers for Robust Biomedical Applications. Analytical Chemistry 2019, 91 (16) , 10879-10886. https://doi.org/10.1021/acs.analchem.9b02697
    13. Yuanwei Dai, Jiaping Weng, Justin George, Huan Chen, Qishan Lin, Jun Wang, Maksim Royzen, Qiang Zhang. Three-Component Protein Modification Using Mercaptobenzaldehyde Derivatives. Organic Letters 2019, 21 (10) , 3828-3833. https://doi.org/10.1021/acs.orglett.9b01294
    14. Sébastien Ulrich. Growing Prospects of Dynamic Covalent Chemistry in Delivery Applications. Accounts of Chemical Research 2019, 52 (2) , 510-519. https://doi.org/10.1021/acs.accounts.8b00591
    15. Yu Zhou, Chen Li, Jianzhao Peng, Liangxu Xie, Ling Meng, Qingrong Li, Jianfu Zhang, Xiang David Li, Xin Li, Xuhui Huang, Xiaoyu Li. DNA-Encoded Dynamic Chemical Library and Its Applications in Ligand Discovery. Journal of the American Chemical Society 2018, 140 (46) , 15859-15867. https://doi.org/10.1021/jacs.8b09277
    16. Samantha Cambray, Jianmin Gao. Versatile Bioconjugation Chemistries of ortho-Boronyl Aryl Ketones and Aldehydes. Accounts of Chemical Research 2018, 51 (9) , 2198-2206. https://doi.org/10.1021/acs.accounts.8b00154
    17. Elena Marone Fassolo, Shaodong Guo, Yachen Wang, Stefano Rosa, Volker Herzig. Genetically encoded libraries and spider venoms as emerging sources for crop protective peptides. Journal of Peptide Science 2024, https://doi.org/10.1002/psc.3600
    18. Bunty Sharma, Gurpreet Kaur, Ganga Ram Chaudhary. Eradication of E. coli using synergistic eosin loaded metallocatanionic vesicle formulation in presence of visible light. Colloids and Surfaces A: Physicochemical and Engineering Aspects 2024, 686 , 133331. https://doi.org/10.1016/j.colsurfa.2024.133331
    19. Shang Wu, Lina Sheng, Xin Lu, Yongli Ye, Jiadi Sun, Jian Ji, Jingdong Shao, Yinzhi Zhang, Xiulan Sun. Screening of bio-recognition elements by phage display and their application in the detection of foodborne pathogens. TrAC Trends in Analytical Chemistry 2024, 171 , 117481. https://doi.org/10.1016/j.trac.2023.117481
    20. Jack G. Haggett, Dylan W. Domaille. ortho ‐Boronic Acid Carbonyl Compounds and Their Applications in Chemical Biology**. Chemistry – A European Journal 2024, 30 (7) https://doi.org/10.1002/chem.202302485
    21. Semra Tasdurmazli, Senanur Dokuz, Berna Erdogdu, Isil Var, John Yu‐Shen Chen, Tulin Ozbek. The evaluation of biotechnological potential of Gp144, the key molecule of natural predator bacteriophage K in Staphylococcus aureus hunting mechanism. Biotechnology Journal 2023, 18 (10) https://doi.org/10.1002/biot.202300145
    22. Khushal Khambhati, Gargi Bhattacharjee, Nisarg Gohil, Gurneet K. Dhanoa, Antonia P. Sagona, Indra Mani, Nhat Le Bui, Dinh‐Toi Chu, Janardhan Keshav Karapurkar, Su Hwa Jang, Hee Yong Chung, Rupesh Maurya, Khalid J. Alzahrani, Suresh Ramakrishna, Vijai Singh. Phage engineering and phage‐assisted CRISPR‐Cas delivery to combat multidrug‐resistant pathogens. Bioengineering & Translational Medicine 2023, 8 (2) https://doi.org/10.1002/btm2.10381
    23. Hui Zhao, Dan Nie, Yue Hu, Zhou Chen, Zheng Hou, Mingkai Li, Xiaoyan Xue. Phage Display-Derived Peptides and Antibodies for Bacterial Infectious Diseases Therapy and Diagnosis. Molecules 2023, 28 (6) , 2621. https://doi.org/10.3390/molecules28062621
    24. Komal Sharma, Krishna K. Sharma, Anku Sharma, Rahul Jain. Peptide-based drug discovery: Current status and recent advances. Drug Discovery Today 2023, 28 (2) , 103464. https://doi.org/10.1016/j.drudis.2022.103464
    25. Dong Lu, Xin Yu, Hanfeng Lin, Ran Cheng, Erika Y. Monroy, Xiaoli Qi, Meng C. Wang, Jin Wang. Applications of covalent chemistry in targeted protein degradation. Chemical Society Reviews 2022, 51 (22) , 9243-9261. https://doi.org/10.1039/D2CS00362G
    26. Jianping Xie. Grand challenge of antibiotics resistance: A global, multidisciplinary effort is needed. Frontiers in Antibiotics 2022, 1 https://doi.org/10.3389/frabi.2022.984076
    27. Mengmeng Zheng, Fredrik Haeffner, Jianmin Gao. N-Terminal cysteine mediated backbone-side chain cyclization for chemically enhanced phage display. Chemical Science 2022, 13 (28) , 8349-8354. https://doi.org/10.1039/D2SC03241D
    28. Mingkang Li, Guize Li, Hongwei Wang, Lin Yuan. The chemodynamic antibacterial effect of MnO X nanosheet decorated silicon nanowire arrays. Materials Advances 2022, 3 (1) , 526-533. https://doi.org/10.1039/D1MA00794G
    29. Yahong Tan, Junjie Wu, Lulu Song, Mengmeng Zhang, Christopher John Hipolito, Changsheng Wu, Siyuan Wang, Youming Zhang, Yizhen Yin. Merging the Versatile Functionalities of Boronic Acid with Peptides. International Journal of Molecular Sciences 2021, 22 (23) , 12958. https://doi.org/10.3390/ijms222312958
    30. Shuli Chou, Qiuke Li, Hua Wu, Jinze Li, Yung-Fu Chang, Lu Shang, Jiawei Li, Zhihua Wang, Anshan Shan. Selective Antifungal Activity and Fungal Biofilm Inhibition of Tryptophan Center Symmetrical Short Peptide. International Journal of Molecular Sciences 2021, 22 (15) , 8231. https://doi.org/10.3390/ijms22158231
    31. João P. M. António, Hélio Faustino, Pedro M. P. Gois. A 2-formylphenylboronic acid (2FPBA)-maleimide crosslinker: a versatile platform for Cys-peptide–hydrazine conjugation and interplay. Organic & Biomolecular Chemistry 2021, 19 (28) , 6221-6226. https://doi.org/10.1039/D1OB00917F
    32. Ming Lei, Arul Jayaraman, James A. Van Deventer, Kyongbum Lee. Engineering Selectively Targeting Antimicrobial Peptides. Annual Review of Biomedical Engineering 2021, 23 (1) , 339-357. https://doi.org/10.1146/annurev-bioeng-010220-095711
    33. Sarah R. Herschede, Hassan Gneid, Taylor Dent, Ellen B. Jaeger, Louise B. Lawson, Nathalie Busschaert. Bactericidal urea crown ethers target phosphatidylethanolamine membrane lipids. Organic & Biomolecular Chemistry 2021, 19 (17) , 3838-3843. https://doi.org/10.1039/D1OB00263E
    34. Hanna Dotter, Melanie Boll, Matthias Eder, Ann-Christin Eder. Library and post-translational modifications of peptide-based display systems. Biotechnology Advances 2021, 47 , 107699. https://doi.org/10.1016/j.biotechadv.2021.107699
    35. Armin Ahmadi, V. S. S. Abhinav Ayyadevara, Jerome Baudry, Kyung-Ho Roh. Calcium signaling on Jurkat T cells induced by microbeads coated with novel peptide ligands specific to human CD3ε. Journal of Materials Chemistry B 2021, 9 (6) , 1661-1675. https://doi.org/10.1039/D0TB02235G
    36. Ahmed Ragab, Sawsan A. Fouad, Ola A. Abu Ali, Entsar M. Ahmed, Abeer M. Ali, Ahmed A. Askar, Yousry A. Ammar. Sulfaguanidine Hybrid with Some New Pyridine-2-One Derivatives: Design, Synthesis, and Antimicrobial Activity against Multidrug-Resistant Bacteria as Dual DNA Gyrase and DHFR Inhibitors. Antibiotics 2021, 10 (2) , 162. https://doi.org/10.3390/antibiotics10020162
    37. Kyle E Murphy, Grace F Sloan, Grace V Lawhern, Grace E Volk, Jacob T Shumate, Amanda L Wolfe. Advances in Antibiotic Drug Discovery: Reducing the Barriers for Antibiotic Development. Future Medicinal Chemistry 2020, 12 (22) , 2067-2087. https://doi.org/10.4155/fmc-2020-0247
    38. Narendra Kumar, Wenjian Wang, Juan C. Ortiz-Marquez, Matthew Catalano, Mason Gray, Nadia Biglari, Kitadai Hikari, Xi Ling, Jianmin Gao, Tim van Opijnen, Kenneth S. Burch. Dielectrophoresis assisted rapid, selective and single cell detection of antibiotic resistant bacteria with G-FETs. Biosensors and Bioelectronics 2020, 156 , 112123. https://doi.org/10.1016/j.bios.2020.112123
    39. Matthew N. Idso, Ajay Suresh Akhade, Mario L. Arrieta-Ortiz, Bert T. Lai, Vivek Srinivas, James P. Hopkins, Ana Oliveira Gomes, Naeha Subramanian, Nitin Baliga, James R. Heath. Antibody-recruiting protein-catalyzed capture agents to combat antibiotic-resistant bacteria. Chemical Science 2020, 11 (11) , 3054-3067. https://doi.org/10.1039/C9SC04842A
    40. Hang Chen, Hebo Ye, Yu Hai, Ling Zhang, Lei You. n → π* interactions as a versatile tool for controlling dynamic imine chemistry in both organic and aqueous media. Chemical Science 2020, 11 (10) , 2707-2715. https://doi.org/10.1039/C9SC05698J
    41. Yan Zhang, Yunchuan Qi, Sébastien Ulrich, Mihail Barboiu, Olof Ramström. Dynamic covalent polymers for biomedical applications. Materials Chemistry Frontiers 2020, 4 (2) , 489-506. https://doi.org/10.1039/C9QM00598F
    42. Hyun Kim, Ju Hye Jang, Sun Chang Kim, Ju Hyun Cho. Development of a novel hybrid antimicrobial peptide for targeted killing of Pseudomonas aeruginosa. European Journal of Medicinal Chemistry 2020, 185 , 111814. https://doi.org/10.1016/j.ejmech.2019.111814
    43. Adriana Barreto-Santamaría, Manuel E. Patarroyo, Hernando Curtidor. Designing and optimizing new antimicrobial peptides: all targets are not the same. Critical Reviews in Clinical Laboratory Sciences 2019, 56 (6) , 351-373. https://doi.org/10.1080/10408363.2019.1631249
    44. Ratmir Derda, Simon Ng. Genetically encoded fragment-based discovery. Current Opinion in Chemical Biology 2019, 50 , 128-137. https://doi.org/10.1016/j.cbpa.2019.03.014
    45. Daniel Ferrer Vinals, Pavel I. Kitov, Zhijay Tu, Chunxia Zou, Christopher W. Cairo, Hans Chun‐Hung Lin, Ratmir Derda. Selection of galectin‐3 ligands derived from genetically encoded glycopeptide libraries. Peptide Science 2019, 111 (1) https://doi.org/10.1002/pep2.24097
    46. Miriam Corredor, Daniel Carbajo, Cecilia Domingo, Yolanda Pérez, Jordi Bujons, Angel Messeguer, Ignacio Alfonso. Dynamic Covalent Identification of an Efficient Heparin Ligand. Angewandte Chemie 2018, 130 (37) , 12149-12153. https://doi.org/10.1002/ange.201806770
    47. Miriam Corredor, Daniel Carbajo, Cecilia Domingo, Yolanda Pérez, Jordi Bujons, Angel Messeguer, Ignacio Alfonso. Dynamic Covalent Identification of an Efficient Heparin Ligand. Angewandte Chemie International Edition 2018, 57 (37) , 11973-11977. https://doi.org/10.1002/anie.201806770