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DEER/PELDOR Study of the Effect of Extremely Low Concentrations of the Antimicrobial Peptide Chalciporin A on the Membrane Lipid Organization

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Abstract

Antimicrobial peptides (AMPs) are promising therapeutic agents against drug-resistant bacteria. Many AMPs can directly interact with bacterial membranes, disturbing their integrity and/or functionality. Chalciporin A is a naturally occurring 14-mer AMP, belonging to the class of peptaibiotic. Spin-label electron paramagnetic resonance in its pulsed versions is a suitable tool to study intermolecular interactions in biological media. Here, we applied double electron–electron resonance (DEER, also known as PELDOR) and electron spin echo envelope modulation, to study model membranes of palmitoyl-oleoyl-glycero-phosphocholine in the presence of chalciporin A. The spin-labeled molecules were either chalciporin A or doxyl-spin-labeled stearic acids (DSAs). We observed that chalciporin A influences DSA clustering, disturbing the formation of the alternative sub-clusters in two opposing leaflets that was recently found in peptide-free membranes (Smorygina et al. in Langmuir 37:13909–13916, 2021). The intriguing point of this influence is that it takes place for peptide concentrations as small as 0.01 mol% (1/10,000 peptide-to-lipid ratio). The possible reasons for this membrane perturbation at extremely low concentrations are discussed.

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References

  1. C.L. Ventola, Pharm. Ther. 40, 277 (2015)

    Google Scholar 

  2. C.L. Ventola, Pharm. Ther. 40, 344 (2015)

    Google Scholar 

  3. M.D. Seo, H.S. Won, J.H. Kim, T.B. Mishig-Ochir, J. Le, Molecules 17, 2276 (2012)

    Article  Google Scholar 

  4. M. Rima, M. Rima, Z. Fajloun, J.M. Sabatier, B. Bechinger, T. Naas, Antibiotics 10, 1095 (2021)

    Article  Google Scholar 

  5. A.A. Bahar, D. Ren, Pharmaceuticals 6, 1543 (2013)

    Article  Google Scholar 

  6. M. Zasloff, Nature 415, 389 (2002)

    Article  ADS  Google Scholar 

  7. T. Neuhof, A. Berg, H. Besl, T. Schwecke, R. Dieckmann, H. von Doehren, Chem. Biodiv. 4, 1103 (2007)

    Article  Google Scholar 

  8. P.G. Lima, J.T.A. Oliveira, J.L. Amaral, C.D.T. Freitas, P.F.N. Souza, Life Sci. 278, 119647 (2021)

    Article  Google Scholar 

  9. E. Randal, Future Microbiol. 6, 635 (2011)

    Article  Google Scholar 

  10. W.L. Zhu, Y.M. Song, Y. Park, K.H. Park, S.T. Yang, J.I. Kim, I.S. Park, K.S. Hahm, S.Y. Shin, Biochim. Biophys. Acta-Biomembr 1768, 1506 (2007)

    Article  Google Scholar 

  11. M. Gobbo, M. Benincasa, G. Bertoloni, B. Biondi, R. Dosselli, E. Papini, E. Reddi, R. Rochhi, R. Tavano, R. Gennaro, J. Med. Chem. 52, 5197 (2009)

    Article  Google Scholar 

  12. M. De Zotti, B. Biondi, Y. Park, K.S. Hahm, M. Crisma, C. Toniolo, F. Formaggio, Amino Acids 43, 1761 (2012)

    Article  Google Scholar 

  13. A.J. Krauson, O.M. Hall, T. Fuselier, C.G. Starr, W.B. Kauffman, W.C. Wimley, J. Am. Chem. Soc. 137, 16144 (2015)

    Article  Google Scholar 

  14. F.G. Avci, B.S. Akbulut, E. Ozkirimli, Biomolecules 8, 77 (2018)

    Article  Google Scholar 

  15. M.F. Brown, Biochem. 51, 9782 (2012)

    Article  Google Scholar 

  16. D. Marsch, Biochim. Biophys. Acta Biomembr 1778, 1545 (2008)

    Article  Google Scholar 

  17. V.K. Sharma, E. Mamontov, M. Tyagi, S. Qian, D.K. Rai, V.S.K. Urban, J. Phys. Chem. Lett. 7, 2394 (2016)

    Article  Google Scholar 

  18. J.B. Mitra, V.K. Sharma, A. Mukherjee, V.G. Sakai, A. Dash, M. Kumar, Langmuir 36, 397 (2019)

    Article  Google Scholar 

  19. V.K. Sharma, S. Qian, Langmuir 35, 4152 (2019)

    Article  Google Scholar 

  20. R.M. Epand, S. Rotem, A. Mor, B. Berno, R.F. Epand, J. Am. Chem. Soc. 130, 14346 (2008)

    Article  Google Scholar 

  21. P. Wadhwani, R.F. Epand, N. Heidenreich, J. Bürck, A.S. Ulrich, R.M. Epand, Biophys. J. 103, 265 (2012)

    Article  ADS  Google Scholar 

  22. S. Qian, D. Rai, W.T. Heller, J. Phys. Chem. B 118, 11200 (2014)

    Article  Google Scholar 

  23. K. Hammond, M.G. Ryadnov, B.W. Hoogenboom, Biochim. Biophys. Acta Biomembr 1863, 183447 (2021)

    Article  Google Scholar 

  24. S.J. Archer, J.F. Ellena, D.S. Cafiso, Biophys. J. 60, 389 (1991)

    Article  Google Scholar 

  25. J. Pan, S. Tristram-Nagle, J.F. Nagle, J. Membr. Biol. 231, 11 (2009)

    Article  Google Scholar 

  26. R. Seyfi, F.A. Kahaki, T. Ebrahimi, S. Montazersaheb, S. Eyvazi, V. Babaeipour, V. Tarhriz, Int. J. Peptide Res. Ther. 26, 1451 (2020)

    Article  Google Scholar 

  27. V. Teixeira, M.J. Feio, M. Bastos, Progr. Lipid Res. 51, 149 (2012)

    Article  Google Scholar 

  28. E.F. Afanasyeva, V.N. Syryamina, S.A. Dzuba, J. Chem. Phys. 146, 011103 (2017)

    Article  ADS  Google Scholar 

  29. E.F. Afanasyeva, V.N. Syryamina, M. De Zotti, F. Formaggio, C. Toniolo, S.A. Dzuba, Biochim. Biophys. Acta Biomembr 1862, 524 (2019)

    Article  Google Scholar 

  30. B. Biondi, C. Peggion, M. De Zotti, C. Pignaffo, A. Dalzini, M. Bortolus, S. Oancea, G. Hilma, A. Bortolotti, L. Stella, J.Z. Pedersen, V.N. Syryamina, Y.D. Tsvetkov, S.A. Dzuba, C. Toniolo, F. Formaggio, Peptide Sci. 110, e23083 (2018)

    Article  Google Scholar 

  31. V.N. Syryamina, E.F. Afanasyeva, S.A. Dzuba, F. Formaggio, M. De Zotti, Biochim. Biophys. Acta Biomembr. 1864, 183978 (2022)

  32. K. Fa, H. Liu, H. Gong, L. Zhang, M. Liao, X. Hu, D. Ciumac, P. Li, J. Webster, J. Petkov, R.K. Thomas, J.R. Lu, Langmuir 38, 6623 (2022)

    Article  Google Scholar 

  33. S.S. Funari, F. Barceló, P.V. Escribá, J. Lipid Res. 44, 567 (2003)

    Article  Google Scholar 

  34. C.C. De Carvalho, M.J. Caramujo, Molecules 23, 2583 (2018)

    Article  Google Scholar 

  35. A.P. Desbois, V.J. Smith, Appl. Microbiol. Biotechnol. 85, 1629 (2010)

    Article  Google Scholar 

  36. R.F. Epand, P.B. Savage, R.M. Epand, Biochim. Biophys. Acta Biomembr. 1768, 2500 (2007)

    Article  Google Scholar 

  37. C. Sohlenkamp, O. Geiger, FEMS Microbiol. Rev. 40, 133 (2016)

    Article  Google Scholar 

  38. A.S. Smorygina, E.A. Golysheva, S.A. Dzuba, Langmuir 37, 13909 (2021)

    Article  Google Scholar 

  39. A.D. Milov, K.M. Salikhov, M.D. Shirov, Fiz. Tverd. Tela 23, 975 (1981)

    Google Scholar 

  40. A.D. Milov, A.G. Maryasov, Yu.D. Tsvetkov, Appl. Magn. Reson. 15, 107 (1998)

    Article  Google Scholar 

  41. G. Jeschke, G. Panek, A. Godt, A. Bender, H. Paulsen, Appl. Magn. Reson. 26, 223 (2004)

    Article  Google Scholar 

  42. G. Jeschke, Biomolecules 12, 1369 (2022)

    Article  Google Scholar 

  43. K.M. Salikhov, I.T. Khairuzhdinov, R.B. Zaripov, Appl. Magn. Reson. 45, 573 (2014)

    Article  Google Scholar 

  44. D.A. Erilov, R. Bartucci, R. Guzzi, A.A. Shubin, A.G. Maryasov, D. Marsh, S.A. Dzuba, L. Sportelli, J. Phys. Chem. B 109, 12003 (2005)

    Article  Google Scholar 

  45. E.S. Salnikov, D.A. Erilov, A.D. Milov, Yu.D. Tsvetkov, C. Peggion, F. Formaggio, C. Toniolo, J. Raap, S.A. Dzuba, Biophys. J. 91, 1532 (2006)

    Article  ADS  Google Scholar 

  46. A.D. Milov, R.I. Samoilova, A.A. Shubin, Y.A. Grishin, S.A. Dzuba, Appl. Magn. Reson. 35, 73 (2008)

    Article  Google Scholar 

  47. S.A. Dzuba, D. Marsh, ESEEM of spin labels to study intermolecular interactions, molecular assembly and conformation. in A Specialist Periodic Report, Electron Paramagnetic Resonance, vol. 24, ed. by C. Gilbert, V. Chechik, D.M. Murphy (RSC Publishing, 2015), pp. 102–121

  48. G. Pabst, S. Danner, R. Podgornik, J. Katsaras, Langmuir 23, 11705 (2007)

    Article  Google Scholar 

  49. A.D. Milov, Y.A. Grishin, S.A. Dzuba, Yu.D. Tsvetkov, Appl. Magn. Reson. 41, 59 (2011)

    Article  Google Scholar 

  50. T.I. Smirnova, A.I. Smirnov, Methods Enzym. 564, 219 (2015)

    Article  Google Scholar 

  51. D. Marsh, Spin-Label Electron Paramagnetic Resonance Spectroscopy (CRC Press, Boca Raton, 2020)

    Google Scholar 

  52. H.J. Steinhoff, N. Radzwill, W. Thevis, V. Lenz, D. Brandenburg, A. Antson, G. Dodson, A. Wollmer, Biophys. J. 73, 3287 (1997)

    Article  Google Scholar 

  53. M.E. Kardash, S.A. Dzuba, J. Phys. Chem. B 121, 5209 (2017)

    Article  Google Scholar 

  54. E.A. Golysheva, A.S. Smorygina, S.A. Dzuba, Appl. Magn. Reson. 53, 685 (2022)

    Article  Google Scholar 

  55. A.S. Kashnik, D.S. Baranov, S.A. Dzuba, Membranes 12, 1077 (2022)

    Article  Google Scholar 

  56. D. Poger, A.E. Mark, J. Chem. Theory Comput. 6, 325 (2010)

    Article  Google Scholar 

  57. N. Kučerka, M.P. Nieh, J. Katsaras, Biochim. Biophys. Acta 1808, 2761 (2011)

    Article  Google Scholar 

  58. D.S. Baranov, A.S. Smorygina, S.A. Dzuba, Molecules 27, 4127 (2022)

    Article  Google Scholar 

  59. K.B. Konov, N.P. Isaev, S.A. Dzuba, Mol. Phys. 111, 2882 (2013)

    Article  ADS  Google Scholar 

  60. L. Janosi, A.A. Gorfe, J. Chem. Theory Comput. 6, 3267 (2010)

    Article  Google Scholar 

  61. G.E. Schulz, R.H. Schirmer, Principles of Protein Structure (Springer Science & Business Media, Berlin, 2013)

    Google Scholar 

  62. B. Bechinger, J. Pept. Sci. 21, 346 (2015)

    Article  Google Scholar 

  63. V.N. Syryamina, N.E. Sannikova, M. De Zotti, M. Gobbo, F. Formaggio, S.A. Dzuba, Biochim. Biophys. Acta Biomembr. 1863, 183585 (2021)

    Article  Google Scholar 

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Funding

ASK, VNS and SAD, Russian Science Foundation, project # 21-13-00025, BB, CP and FF Fresenius Kabi iPSUM and the University of Padova (Grant Uni-Impresa 2019).

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Investigation, ASK; data processing, VNS, synthesis, BB, CP and FF, editing, FF, conceptualization and writing, SAD. All authors read and approved the final manuscript.

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Correspondence to Sergei A. Dzuba.

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Kashnik, A.S., Syryamina, V.N., Biondi, B. et al. DEER/PELDOR Study of the Effect of Extremely Low Concentrations of the Antimicrobial Peptide Chalciporin A on the Membrane Lipid Organization. Appl Magn Reson 54, 401–414 (2023). https://doi.org/10.1007/s00723-023-01526-x

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