Register      Login
Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
RESEARCH ARTICLE

Fluorescent Reporters for Antimicrobial Peptides

Yuning Hong https://orcid.org/0000-0002-8085-1651 A C and Wenyi Li https://orcid.org/0000-0003-3584-0301 B C
+ Author Affiliations
- Author Affiliations

A Department of Chemistry and Physics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Vic. 3086, Australia.

B Bio21 Institute, Melbourne Dental School, University of Melbourne, Melbourne, Vic. 3010, Australia.

C Corresponding authors. Email: y.hong@latrobe.edu.au; wenyi.li@unimelb.edu.au




Dr Wenyi Li obtained his doctoral degree from The University of Melbourne in 2016, working with Professors John Wade and Frances Separovic. His thesis on antimicrobial peptide development won the Graham Johnston Best Thesis Award from the RACI and the University of Melbourne’s Monica Reum Memorial Prize. He then worked with Professor Christian Hackenberger at the Leibniz Institute of Molecular Pharmacology, Germany, as a Leibniz-DAAD post-doctoral fellow conducting research in protein semisynthesis and chemical ligation. In 2018, he returned to The University of Melbourne to work on antibacterial polymers and peptides in the groups of Professors Neil O’Brien-Simpson and Greg Qiao.

Australian Journal of Chemistry 75(2) 2-8 https://doi.org/10.1071/CH21070
Submitted: 15 March 2021  Accepted: 31 May 2021   Published: 16 June 2021

Abstract

Antimicrobial peptides (AMPs), a part of the natural defence against pathogens, have been considered as alternative antibiotics to combat the increase of antimicrobial resistance (AMR). Given the advanced development of fluorescent probes, extensive research has been focussed on understanding the physiological processes of the interaction between AMPs and bacteria. To better guide the choice of suitable fluorescent reporters for the mechanism study of AMPs, in this review, we summarise a toolbox of commonly used fluorescent reporters for AMP studies, including intrinsic fluorescent reporters, conventional fluorophores, and recently developed aggregation-induced emission (AIE) fluorogens.

Keywords: antimcirobial peptide, peptide labelling, fluorescent probes, mode of action, intrinsic fluorescence, conventional fluorophores, aggregation-induced emission fluorogens, antimicrobial resistance.


References

[1]  (a) B. N. G. Giepmans, S. R. Adams, M. H. Ellisman, R. Y. Tsien, Science 2006, 312, 217.
         | Crossref | GoogleScholarGoogle Scholar |
      (b) E. C. Jensen, Anat. Rec. 2012, 295, 2031.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) H. Singh, K. Tiwari, R. Tiwari, S. K. Pramanik, A. Das, Chem. Rev. 2019, 119, 11718.
         | Crossref | GoogleScholarGoogle Scholar |
      (d) E. A. Specht, E. Braselmann, A. E. Palmer, Annu. Rev. Physiol. 2017, 79, 93.
         | Crossref | GoogleScholarGoogle Scholar |
      (e) D. Choquet, M. Sainlos, J.-B. Sibarita, Nat. Rev. Neurosci. 2021, 22, 237.

[2]  (a) L. Malacrida, S. Astrada, A. Briva, M. Bollati-Fogolín, E. Gratton, L. A. Bagatolli, Biochim. Biophys. Acta Biomembr. 2016, 1858, 2625.
         | Crossref | GoogleScholarGoogle Scholar |
      (b) T. C. Owyong, P. Subedi, J. Deng, E. Hinde, J. J. Paxman, J. M. White, et al. Angew. Chem. Int. Ed. 2020, 59, 10129.
         | Crossref | GoogleScholarGoogle Scholar |

[3]  (a) S. Chen, Y. Hong, Y. Zeng, Q. Sun, Y. Liu, E. Zhao, et al. Chem. – Eur. J. 2015, 21, 4315.
         | Crossref | GoogleScholarGoogle Scholar | 25645956PubMed |
      (b) K. Suhling, J. A. Levitt, P.-H. Chung, M. K. Kuimova, G. Yahioglu, J. Vis. Exp. 2012, 60, e2925.

[4]  A. J. Boersma, I. S. Zuhorn, B. Poolman, Nat. Methods 2015, 12, 227.
         | Crossref | GoogleScholarGoogle Scholar | 25643150PubMed |

[5]  H. Soleimaninejad, M. Z. Chen, X. Lou, T. A. Smith, Y. Hong, Chem. Commun. 2017, 53, 2874.
         | Crossref | GoogleScholarGoogle Scholar |

[6]  C. Brives, J. Pourraz, Palgrave Commun. 2020, 6, 100.
         | Crossref | GoogleScholarGoogle Scholar |

[7]  C. Ghose, C. W. Euler, Antibiotics 2020, 9, 74.

[8]  E. Pelfrene, M. Mura, A. Cavaleiro Sanches, M. Cavaleri, Clin. Microbiol. Infect. 2019, 25, 60.
         | Crossref | GoogleScholarGoogle Scholar | 29715552PubMed |

[9]  D. R. Silva, J. C. O. Sardi, N. S. Pitangui, S. M. Roque, A. C. B. d. Silva, P. L. Rosalen, J. Funct. Foods 2020, 73, 104080.
         | Crossref | GoogleScholarGoogle Scholar |

[10]  L. Czaplewski, R. Bax, M. Clokie, M. Dawson, H. Fairhead, V. A. Fischetti, et al. Lancet Infect. Dis. 2016, 16, 239.
         | Crossref | GoogleScholarGoogle Scholar | 26795692PubMed |

[11]  J. O’Neill, Antimicrobial Resistance: Tackling a Crisis for the Health and Wealth of Nations 2014 (Grande-Bretagne: London).

[12]  (a) W. Li, J. Tailhades, N. O’Brien-Simpson, F. Separovic, L. Otvos, M. A. Hossain, et al. Amino Acids 2014, 46, 2287.
         | Crossref | GoogleScholarGoogle Scholar | 25141976PubMed |
      (b) A. Peschel, H.-G. Sahl, Nat. Rev. Microbiol. 2006, 4, 529.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) W. Li, F. Separovic, N. M. O’Brien-Simpson, J. D. Wade, Chem. Soc. Rev. 2021, 50, 4932.
         | Crossref | GoogleScholarGoogle Scholar |

[13]  L. Miao, W. Liu, Q. Qiao, X. Li, Z. Xu, J. Pharm. Anal. 2020, 10, 444.
         | Crossref | GoogleScholarGoogle Scholar | 33133728PubMed |

[14]  (a) R. I. Lehrer, A. Barton, K. A. Daher, S. S. Harwig, T. Ganz, M. E. Selsted, J. Clin. Invest. 1989, 84, 553.
         | Crossref | GoogleScholarGoogle Scholar | 2668334PubMed |
      (b) A. da Silva, O. Teschke, Biochim. Biophys. Acta Mol. Cell Res. 2003, 1643, 95.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) M. Hartmann, M. Berditsch, J. Hawecker, M. F. Ardakani, D. Gerthsen, A. S. Ulrich, Antimicrob. Agents Chemother. 2010, 54, 3132.
         | Crossref | GoogleScholarGoogle Scholar |

[15]  (a) G. Boix-Lemonche, M. Lekka, B. Skerlavaj, Antibiotics 2020, 9, 92.
         | Crossref | GoogleScholarGoogle Scholar |
      (b) A. H. Benfield, S. T. Henriques, Front Med Technol. 2020, 2, 610997.
         | Crossref | GoogleScholarGoogle Scholar |

[16]  (a) H. Sträuber, S. Müller, Cytometry A 2010, 77A, 623.
         | Crossref | GoogleScholarGoogle Scholar |
      (b) S. Langsrud, G. Sundheim, J. Appl. Bacteriol. 1996, 81, 411.
         | Crossref | GoogleScholarGoogle Scholar |

[17]  (a) D. E. Epps, M. L. Wolfe, V. Groppi, Chem. Phys. Lipids 1994, 69, 137.
         | Crossref | GoogleScholarGoogle Scholar | 8181103PubMed |
      (b) H. M. Shapiro, Methods 2000, 21, 271.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) M. Wu, E. Maier, R. Benz, R. E. W. Hancock, Biochemistry 1999, 38, 7235.
         | Crossref | GoogleScholarGoogle Scholar |

[18]  (a) N. M. O’Brien-Simpson, W. Li, N. Pantarat, M. A. Hossain, F. Separovic, J. D. Wade, et al. Aust. J. Chem. 2017, 70, 220.
         | Crossref | GoogleScholarGoogle Scholar |
      (b) N. M. O’Brien-Simpson, N. Pantarat, T. J. Attard, K. A. Walsh, E. C. Reynolds, PLoS One 2016, 11, e0151694.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) W. Li, N. M. O’Brien-Simpson, S. Yao, J. Tailhades, E. C. Reynolds, R. M. Dawson, et al. Chem. – Eur. J. 2017, 23, 390.
         | Crossref | GoogleScholarGoogle Scholar |
      (d) W. Li, M.-A. Sani, E. Jamasbi, L. Otvos, M. A. Hossain, J. D. Wade, et al. Biochim. Biophys. Acta 2016, 1858, 1236.
         | Crossref | GoogleScholarGoogle Scholar |

[19]  (a) M. M. Welling, A. W. Hensbergen, A. Bunschoten, A. H. Velders, H. Scheper, W. K. Smits, et al. Clin. Transl. Imaging 2019, 7, 125.
         | Crossref | GoogleScholarGoogle Scholar |
      (b) M. R. L. Stone, M. S. Butler, W. Phetsang, M. A. Cooper, M. A. T. Blaskovich, Trends Biotechnol. 2018, 36, 523.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) M. R. L. Stone, W. Phetsang, M. A. Cooper, M. A. T. Blaskovich, J. Vis. Exp. 2020, 157, e60743.

[20]  (a) C. A. Royer, Chem. Rev. 2006, 106, 1769.
         | Crossref | GoogleScholarGoogle Scholar | 16683754PubMed |
      (b) A. Ghisaidoobe, S. Chung, Int. J. Mol. Sci. 2014, 15, 22518.
         | Crossref | GoogleScholarGoogle Scholar |

[21]  F. W. J. Teale, G. Weber, Biochem. J. 1957, 65, 476.
         | Crossref | GoogleScholarGoogle Scholar |

[22]     (a) M. Arias, H. J. Vogel, in Antimicrobial Peptides: Methods and Protocols (Ed. P. R. Hansen) 2017, pp. 141–157 (Springer: New York, NY).
      (b) N. G. Park, S. Lee, O. Oishi, H. Aoyagi, S. Iwanaga, S. Yamashita, et al. Biochemistry 1992, 31, 12241.
         | Crossref | GoogleScholarGoogle Scholar |

[23]  A. J. Mason, I. N. H. Chotimah, P. Bertani, B. Bechinger, Mol. Membr. Biol. 2006, 23, 185.
         | Crossref | GoogleScholarGoogle Scholar | 16754361PubMed |

[24]  X. Bi, C. Wang, L. Ma, Y. Sun, D. Shang, J. Appl. Microbiol. 2013, 115, 663.
         | Crossref | GoogleScholarGoogle Scholar | 23710779PubMed |

[25]  H. Schröder-Borm, R. Willumeit, K. Brandenburg, J. Andrä, Biochim. Biophys. Acta Biomembr. 2003, 1612, 164.
         | Crossref | GoogleScholarGoogle Scholar |

[26]  O. K. Abou-Zied, A. Barbour, N. A. Al-Sharji, K. Philip, RSC Adv. 2015, 5, 14214.
         | Crossref | GoogleScholarGoogle Scholar |

[27]  G. Manzo, M. A. Scorciapino, P. Wadhwani, J. Bürck, N. P. Montaldo, M. Pintus, et al. PLoS One 2015, 10, e0116379.
         | Crossref | GoogleScholarGoogle Scholar | 25617899PubMed |

[28]  M. Bagheri, H. Nikolenko, S. Arasteh, N. Rezaei, M. Behzadi, M. Dathe, et al. ACS Appl. Mater. Interfaces 2020, 12, 26852.
         | Crossref | GoogleScholarGoogle Scholar | 32422035PubMed |

[29]  H. Raghuraman, A. Chattopadhyay, Biophys. J. 2004, 87, 2419.
         | Crossref | GoogleScholarGoogle Scholar | 15454440PubMed |

[30]  M. Makowski, M. R. Felício, I. C. M. Fensterseifer, O. L. Franco, N. C. Santos, S. Gonçalves, Int. J. Mol. Sci. 2020, 21, 9104.
         | Crossref | GoogleScholarGoogle Scholar |

[31]  (a) A. Bhunia, H. Mohanram, P. N. Domadia, J. Torres, S. Bhattacharjya, J. Biol. Chem. 2009, 284, 21991.
         | Crossref | GoogleScholarGoogle Scholar | 19520860PubMed |
      (b) H. Mohanram, S. Bhattacharjya, Antimicrob. Agents Chemother. 2014, 58, 1987.
         | Crossref | GoogleScholarGoogle Scholar |

[32]  (a) A. K. Buck, D. E. Elmore, L. E. Darling, Future Med. Chem. 2019, 11, 2445.
         | Crossref | GoogleScholarGoogle Scholar | 31517514PubMed |
      (b) H. Choi, N. Rangarajan, J. C. Weisshaar, Trends Microbiol. 2016, 24, 111.
         | Crossref | GoogleScholarGoogle Scholar |

[33]  H. R. Chileveru, S. A. Lim, P. Chairatana, A. J. Wommack, I. L. Chiang, E. M. Nolan, Biochemistry 2015, 54, 1767.
         | Crossref | GoogleScholarGoogle Scholar | 25664683PubMed |

[34]  (a) B.-H. Gan, T. N. Siriwardena, S. Javor, T. Darbre, J.-L. Reymond, ACS Infect. Dis. 2019, 5, 2164.
         | Crossref | GoogleScholarGoogle Scholar | 31618574PubMed |
      (b) A. R. Akram, N. Avlonitis, E. Scholefield, M. Vendrell, N. McDonald, T. Aslam, et al. Sci. Rep. 2019, 9, 8422.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) M. Benincasa, S. Pacor, R. Gennaro, M. Scocchi, Antimicrob. Agents Chemother. 2009, 53, 3501.
         | Crossref | GoogleScholarGoogle Scholar |
      (d) F. Hossain, M. M. R. Moghal, M. Z. Islam, M. Moniruzzaman, M. Yamazaki, J. Biol. Chem. 2019, 294, 10449.
         | Crossref | GoogleScholarGoogle Scholar |
      (e) J. Deng, J. H. Viel, J. Chen, O. P. Kuipers, ACS Synth. Biol. 2020, 9, 2525.
         | Crossref | GoogleScholarGoogle Scholar |

[35]  A. Lossouarn, P.-Y. Renard, C. Sabot, Bioconjug. Chem. 2021, 32, 63.
         | Crossref | GoogleScholarGoogle Scholar | 33232599PubMed |

[36]  C. Zhao, A. Fernandez, N. Avlonitis, G. Vande Velde, M. Bradley, N. D. Read, et al. ACS Comb. Sci. 2016, 18, 689.
         | Crossref | GoogleScholarGoogle Scholar | 27723293PubMed |

[37]  (a) W. Li, N. M. O’Brien-Simpson, J. Tailhades, N. Pantarat, R. M. Dawson, L. Otvos, et al. Chem. Biol. 2015, 22, 1250.
         | Crossref | GoogleScholarGoogle Scholar | 26384569PubMed |
      (b) S. J. Lam, N. M. O’Brien-Simpson, N. Pantarat, A. Sulistio, E. H. H. Wong, Y.-Y. Chen, et al. Nat. Microbiol. 2016, 1, 16162.
         | Crossref | GoogleScholarGoogle Scholar |

[38]  (a) A. T. Krueger, B. Imperiali, ChemBioChem 2013, 14, 788.
         | Crossref | GoogleScholarGoogle Scholar | 23609944PubMed |
      (b) L. Mendive-Tapia, R. Subiros-Funosas, C. Zhao, F. Albericio, N. D. Read, R. Lavilla, et al. Nat. Protoc. 2017, 12, 1588.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) Z. Cheng, E. Kuru, A. Sachdeva, M. Vendrell, Nat. Rev. Chem. 2020, 4, 275.
         | Crossref | GoogleScholarGoogle Scholar |

[39]  (a) Y. Hong, J. W. Y. Lam, B. Z. Tang, Chem. Soc. Rev. 2011, 40, 5361.
         | Crossref | GoogleScholarGoogle Scholar | 21799992PubMed |
      (b) S. Ding, Y. Hong, Chem. Soc. Rev. 2020, 49, 8354.
         | Crossref | GoogleScholarGoogle Scholar |

[40]  J. Mei, Y. Hong, J. W. Y. Lam, A. Qin, Y. Tang, B. Z. Tang, Adv. Mater. 2014, 26, 5429.
         | Crossref | GoogleScholarGoogle Scholar | 24975272PubMed |

[41]  J. Mei, N. L. C. Leung, R. T. K. Kwok, J. W. Y. Lam, B. Z. Tang, Chem. Rev. 2015, 115, 11718.
         | Crossref | GoogleScholarGoogle Scholar | 26492387PubMed |

[42]  (a) A. C. Sedgwick, K.-C. Yan, D. N. Mangel, Y. Shang, A. Steinbrueck, H.-H. Han, et al. J. Am. Chem. Soc. 2021, 142, 1278.
      (b) M. Kang, C. Zhou, S. Wu, B. Yu, Z. Zhang, N. Song, et al. J. Am. Chem. Soc. 2019, 141, 16781.
         | Crossref | GoogleScholarGoogle Scholar |
         (c) Wei  H.Zheng  Z.Haotian  B.Ling-Hong  X.Lei  W.Yinghui  L.et al.ChemRxiv. 2020 .

[43]  (a) H. Bai, W. He, J. H. C. Chau, Z. Zheng, R. T. K. Kwok, J. W. Y. Lam, et al. Biomaterials 2021, 268, 120598.
         | Crossref | GoogleScholarGoogle Scholar | 33321291PubMed |
      (b) X. He, L.-H. Xiong, Z. Zhao, Z. Wang, L. Luo, J. W. Y. Lam, et al. Theranostics 2019, 9, 3223.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) I. M. Khan, S. Niazi, M. K. Iqbal Khan, I. Pasha, A. Mohsin, J. Haider, et al. Trends Analyt. Chem. 2019, 119, 115637.
         | Crossref | GoogleScholarGoogle Scholar |

[44]  T. Luu, W. Li, N. M. O’Brien-Simpson, Y. Hong, Chem. Asian J. 2021, 16, 1027.
         | Crossref | GoogleScholarGoogle Scholar | 33723926PubMed |

[45]  J. Chen, M. Gao, L. Wang, S. Li, J. He, A. Qin, et al. ACS Appl. Mater. Interfaces 2018, 10, 11436.
         | Crossref | GoogleScholarGoogle Scholar | 29564898PubMed |

[46]  (a) Y. Shi, G. Yin, Z. Yan, P. Sang, M. Wang, R. Brzozowski, et al. J. Am. Chem. Soc. 2019, 141, 12697.
         | Crossref | GoogleScholarGoogle Scholar | 31335135PubMed |
      (b) P. Bao, C. Li, H. Ou, S. Ji, Y. Chen, J. Gao, et al. Biomater. Sci. 2021, 9, 437.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) C. Yang, F. Hu, X. Zhang, C. Ren, F. Huang, J. Liu, et al. Biomaterials 2020, 244, 119972.
         | Crossref | GoogleScholarGoogle Scholar |

[47]  A.-B. Schäfer, M. Wenzel, Front Cell Infect. 2020, 10, 610.