Therapeutic Potential and Application Prospects of Antimicrobial Peptides in the Era of Global Spread of Antibiotic Resistance

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Abstract

In the era of the growing global threat of antibiotic resistance, antimicrobial peptides (AMPs) are considered as new generation drugs for treatment of various infectious diseases. In this review, AMPs are seen as an alternative to traditional antibiotics, many of which have already lost or are gradually reducing their effectiveness against a number of critically important pathogenic microorganisms. Recent outbreaks of secondary infections during the COVID-19 pandemic have increased the interest in AMPs due to an acute shortage of effective agents against bacterial and fungal infections. The review summarized current data on clinical studies of AMPs, assembled a list of developed drugs based on AMPs at various stages of clinical trials, highlighted the urgency of study of new AMPs, and systematized the most relevant clinical data and application of AMPs.

About the authors

V. N. Safronova

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: arenicin@mail.ru
Russia, 117997, Moscow, ul. Miklukho-Maklaya 16/10

I. A. Bolosov

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: arenicin@mail.ru
Russia, 117997, Moscow, ul. Miklukho-Maklaya 16/10

P. V. Panteleev

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: arenicin@mail.ru
Russia, 117997, Moscow, ul. Miklukho-Maklaya 16/10

S. V. Balandin

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Author for correspondence.
Email: arenicin@mail.ru
Russia, 117997, Moscow, ul. Miklukho-Maklaya 16/10

T. V. Ovchinnikova

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: arenicin@mail.ru
Russia, 117997, Moscow, ul. Miklukho-Maklaya 16/10

References

  1. Ventola C.L. // P T. 2015. V. 40. P. 277–283.
  2. Ma Y., Wang C., Li Y., Li J., Wan Q., Chen J., Tay F.R., Niu L. // Adv. Sci. 2020. V. 7. P. 1901872. https://doi.org/10.1002/advs.201901872
  3. Lewis K. // Nat. Rev. Drug Dis. 2013. V. 12. P. 371–387. https://doi.org/10.1038/nrd3975
  4. Lloyd D.H. // Vet. Dermatol. 2012. V. 23. P. 299-e60. https://doi.org/10.1111/j.1365-3164.2012.01042.x
  5. Munguia J., Nizet V. // Trend. Pharmacol. Sci. 2017. V. 38. P. 473–488. https://doi.org/10.1016/j.tips.2017.02.003
  6. Johnson B.K., Abramovitch R.B. // Trend. Pharmacol. Sci. 2017. V. 38. P. 339–362. https://doi.org/10.1016/j.tips.2017.01.004
  7. Ventola C.L. // P T. 2015. V. 40. P. 344–352.
  8. Yeung A.T.Y., Gellatly S.L., Hancock R.E.W. // Cell. Mol. Life Sci. 2011. V. 68. P. 2161–2176. https://doi.org/10.1007/s00018-011-0710-x
  9. Peters B.M., Shirtliff M.E., Jabra-Rizk M.A. // PLoS Pathog. 2010. V. 6. P. e1001067. https://doi.org/10.1371/journal.ppat.1001067
  10. Zasloff M. // Nature. 2002. V. 415. P. 389–395. https://doi.org/10.1038/415389a
  11. de la Fuente-Núñez C., Cardoso M.H., de Souza Cândido E., Franco O.L., Hancock R.E.W. // Biochim. Biophys. Acta. 2016. V. 1858. P. 1061–1069. https://doi.org/10.1016/j.bbamem.2015.12.015
  12. Batoni G., Maisetta G., Brancatisano F.L., Esin S., Campa M. // Curr. Med. Chem. 2011. V. 18. P. 256–279. https://doi.org/10.2174/092986711794088399
  13. Lai Y., Gallo R.L. // Trend. Immunol. 2009. V. 30. P. 131–141. https://doi.org/10.1016/j.it.2008.12.003
  14. Pütsep K., Carlsson G., Boman H.G., Andersson M. // Lancet. 2002. V. 360. P. 1144–1149. https://doi.org/10.1016/S0140-6736(02)11201-3
  15. Wehkamp J., Salzman N.H., Porter E., Nuding S., Weichenthal M., Petras R.E., Shen B., Schaeffeler E., Schwab M., Linzmeier R. // Proc. Natl. Acad. Sci. USA. 2005. V. 102. P. 18129–18134. https://doi.org/10.1073/pnas.0505256102
  16. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.-H., Homey B., Cao W., Wang Y.-H., Su B., Nestle F.O. // Nature. 2007. V. 449. P. 564–569. https://doi.org/10.1038/nature06116
  17. Hancock R.E.W., Haney E.F., Gill E.E. // Nat. Rev. Immunol. 2016. V. 16. P. 321–334. https://doi.org/10.1038/nri.2016.29
  18. Cotter P.D., Ross R.P., Hill C. // Nat. Rev. Microbiol. 2013. V. 11. P. 95–105. https://doi.org/10.1038/nrmicro2937
  19. Ríos Colombo N.S., Chalón M.C., Navarro S.A., Bellomio A. // Curr. Genet. 2018. V. 64. P. 345–351. https://doi.org/10.1007/s00294-017-0757-9
  20. Chikindas M.L., Weeks R., Drider D., Chistyakov V.A., Dicks L.M. // Curr. Opin. Biotechnol. 2018. V. 49. P. 23–28. https://doi.org/10.1016/j.copbio.2017.07.011
  21. Teixeira V., Feio M.J., Bastos M. // Prog. Lipid Res. 2012. V. 51. P. 149–177. https://doi.org/10.1016/j.plipres.2011.12.005
  22. Joo H.-S., Fu C.-I., Otto M. // Philos. Trans. R Soc. Lond. B Biol. Sci. 2016. V. 371. P. 20150292. https://doi.org/10.1098/rstb.2015.0292
  23. Habets M.G.J.L., Brockhurst M.A. // Biol. Lett. 2012. V. 8. P. 416–418. https://doi.org/10.1098/rsbl.2011.1203
  24. Le C.-F., Fang C.-M., Sekaran S.D. // Antimicrob. Agents Chemother. 2017. V. 61. P. e02340-16. https://doi.org/10.1128/AAC.02340-16
  25. Vetterli S.U., Zerbe K., Müller M., Urfer M., Mondal M., Wang S.-Y., Moehle K., Zerbe O., Vitale A., Pessi G. // Sci. Adv. 2018. V. 4. P. eaau2634. https://doi.org/10.1126/sciadv.aau2634
  26. Seefeldt A.C., Graf M., Pérébaskine N., Nguyen F., Arenz S., Mardirossian M., Scocchi M., Wilson D.N., Innis C.A. // Nucleic Acids Res. 2016. V. 44. P. 2429–2438. https://doi.org/10.1093/nar/gkv1545
  27. Cassone M., Otvos L. // Expert Rev. Anti-Infect. Ther. 2010. V. 8. P. 703–716. https://doi.org/10.1586/eri.10.38
  28. Zharkova M.S., Orlov D.S., Golubeva O.Yu., Chakchir O.B., Eliseev I.E., Grinchuk T.M., Shamova O.V. // Front. Cell. Infect. Microbiol. 2019. V. 9. P. 128. https://doi.org/10.3389/fcimb.2019.00128
  29. Ma B., Fang C., Lu L., Wang M., Xue X., Zhou Y., Li M., Hu Y., Luo X., Hou Z. // Nat. Commun. 2019. V. 10. P. 3517. https://doi.org/10.1038/s41467-019-11503-3
  30. Dobias J., Poirel L., Nordmann P. // Clin. Microbiol. Infect. 2017. V. 23. P. 676.e1–676.e5. https://doi.org/10.1016/j.cmi.2017.03.015
  31. Theuretzbacher U., Outterson K., Engel A., Karlén A. // Nat. Rev. Microbiol. 2020. V. 18. P. 275–285. https://doi.org/10.1038/s41579-019-0288-0
  32. Andersson D.I., Hughes D., Kubicek-Sutherland J.Z. // Drug Resist. Updat. 2016. V. 26. P. 43–57. https://doi.org/10.1016/j.drup.2016.04.002
  33. Mahlapuu M., Håkansson J., Ringstad L., Björn C. // Front. Cell. Infect. Microbiol. 2016. V. 6. P. 194. https://doi.org/10.3389/fcimb.2016.00194
  34. Atefyekta S., Blomstrand E., Rajasekharan A.K., Svensson S., Trobos M., Hong J., Webster T.J., Thomsen P., Andersson M. // ACS Biomater. Sci. Eng. 2021. V. 7. P. 1693–1702. https://doi.org/10.1021/acsbiomaterials.1c00029
  35. Luong H.X., Thanh T.T., Tran T.H. // Life Sci. 2020. V. 260. P. 118407. https://doi.org/10.1016/j.lfs.2020.118407
  36. Fosgerau K., Hoffmann T. // Drug Dis. Today. 2015. V. 20. P. 122–128. https://doi.org/10.1016/j.drudis.2014.10.003
  37. Greco I., Molchanova N., Holmedal E., Jenssen H., Hummel B.D., Watts J.L., Håkansson J., Hansen P.R., Svenson J. // Sci. Rep. 2020. V. 10. P. 13206. https://doi.org/10.1038/s41598-020-69995-9
  38. Ahmed T.A.E., Hammami R. // J. Food Biochem. 2019. V. 43. P. e12546. https://doi.org/10.1111/jfbc.12546
  39. Edwards I.A., Elliott A.G., Kavanagh A.M., Zuegg J., Blaskovich M.A.T., Cooper M.A. // ACS Infect. Dis. 2016. V. 2. P. 442–450. https://doi.org/10.1021/acsinfecdis.6b00045
  40. Schmitt P., Rosa R.D., Destoumieux-Garzón D. // Biochim. Biophys. Acta. 2016. V. 1858. P. 958–970. https://doi.org/10.1016/j.bbamem.2015.10.011
  41. Marr A., Gooderham W., Hancock R. // Curr. Opin. Pharmacol. 2006. V. 6. P. 468–472. https://doi.org/10.1016/j.coph.2006.04.006
  42. Cao J., de la Fuente-Nunez C., Ou R.W., Torres M.D.T., Pande S.G., Sinskey A.J., Lu T.K. // ACS Synth. Biol. 2018. V. 7. P. 896–902. https://doi.org/10.1021/acssynbio.7b00396
  43. Dijksteel G.S., Ulrich M.M.W., Middelkoop E., Boekema B.K.H.L. // Front. Microbiol. 2021. V. 12. P. 616979. https://doi.org/10.3389/fmicb.2021.616979
  44. Divyashree M., Mani M.K., Reddy D., Kumavath R., Ghosh P., Azevedo V., Barh D. // Protein Pept. Lett. 2020. V. 27. P. 120–134. https://doi.org/10.2174/0929866526666190925152957
  45. Browne K., Chakraborty S., Chen R., Willcox M.D., Black D.S., Walsh W.R., Kumar N. // Int. J. Mol. Sci. 2020. V. 21. P. 7047. https://doi.org/10.3390/ijms21197047
  46. Magana M., Pushpanathan M., Santos A.L., Leanse L., Fernandez M., Ioannidis A., Giulianotti M.A., Apidianakis Y., Bradfute S., Ferguson A.L. // Lancet Infect. Dis. 2020. V. 20. P. e216–e230. https://doi.org/10.1016/S1473-3099(20)30327-3
  47. Erdem Büyükkiraz M., Kesmen Z. // J. Appl. Microbiol. 2022. V. 132. P. 1573–1596. https://doi.org/10.1111/jam.15314
  48. Mercer D.K., O’Neil D.A. // Front. Immunol. 2020. V. 11. P. 2177. https://doi.org/10.3389/fimmu.2020.02177
  49. Mookherjee N., Anderson M.A., Haagsman H.P., Davidson D.J. // Nat. Rev. Drug. Discov. 2020. V. 19. P. 311–332. https://doi.org/10.1038/s41573-019-0058-8
  50. Jiang Y., Chen Y., Song Z., Tan Z., Cheng J. // Adv. Drug Deliv. Rev. 2021. V. 170. P. 261–280. https://doi.org/10.1016/j.addr.2020.12.016
  51. Lesiuk M., Paduszyńska M., Greber K.E. // Antibiotics. 2022. V. 11. P. 1062. https://doi.org/10.3390/antibiotics11081062
  52. Moretta A., Scieuzo C., Petrone A.M., Salvia R., Manniello M.D., Franco A., Lucchetti D., Vassallo A., Vogel H., Sgambato A. // Front. Cell. Infect. Microbiol. 2021. V. 11. P. 668632. https://doi.org/10.3389/fcimb.2021.668632
  53. Boakes S., Appleyard A.N., Cortés J., Dawson M.J. // J. Antibiot. (Tokyo). 2010. V. 63. P. 351–358. https://doi.org/10.1038/ja.2010.48
  54. Crowther G.S., Baines S.D., Todhunter S.L., Freeman J., Chilton C.H., Wilcox M.H. // J. Antimicrob. Chemother. 2013. V. 68. P. 168–176. https://doi.org/10.1093/jac/dks359
  55. Li X.S., Reddy M.S., Baev D., Edgerton M. // J. Biol. Chem. 2003. V. 278. P. 28553–28561. https://doi.org/10.1074/jbc.M300680200
  56. Jang W.S., Li X.S., Sun J.N., Edgerton M. // Antimicrob. Agents Chemother. 2008. V. 52. P. 497–504. https://doi.org/10.1128/AAC.01199-07
  57. Cheng K.-T., Wu C.-L., Yip B.-S., Chih Y.-H., Peng K.-L., Hsu S.-Y., Yu H.-Y., Cheng J.-W. // Int. J. Mol. Sci. 2020. V. 21. P. 2654. https://doi.org/10.3390/ijms21072654
  58. Nell M.J., Tjabringa G.S., Wafelman A.R., Verrijk R., Hiemstra P.S., Drijfhout J.W., Grote J.J. // Peptides. 2006. V. 27. P. 649–660. https://doi.org/10.1016/j.peptides.2005.09.016
  59. Chen Y., Mant C.T., Farmer S.W., Hancock R.E.W., Vasil M.L., Hodges R.S. // J. Biol. Chem. 2005. V. 280. P. 12316–12329. https://doi.org/10.1074/jbc.M413406200
  60. Zhang L., Benz R., Hancock R.E. // Biochemistry. 1999. V. 38. P. 8102–8111. https://doi.org/10.1021/bi9904104
  61. AB Naafs M. // Biomed. J. Sci. Tech. Res. 2018. V. 7. P. 6038–6042. https://doi.org/10.26717/BJSTR.2018.07.001536
  62. Wei Y., Wu J., Chen Y., Fan K., Yu X., Li X., Zhao Y., Li Y., Lv G., Song G. // Ann. Surg. 2022. V. 277(1). P. 43–49. https://doi.org/10.1097/SLA.0000000000005508
  63. Schmidtchen A., Pasupuleti M., Mörgelin M., Davoudi M., Alenfall J., Chalupka A., Malmsten M. // J. Biol. Chem. 2009. V. 284. P. 17584–17594. https://doi.org/10.1074/jbc.M109.011650
  64. Boge L., Umerska A., Matougui N., Bysell H., Ringstad L., Davoudi M., Eriksson J., Edwards K., Andersson M. // Int. J. Pharm. 2017. V. 526. P. 400–412. https://doi.org/10.1016/j.ijpharm.2017.04.082
  65. Nordström R., Nyström L., Andrén O.C.J., Malkoch M., Umerska A., Davoudi M., Schmidtchen A., Malmsten M. // J. Colloid Interface Sci. 2018. V. 513. P. 141–150. https://doi.org/10.1016/j.jcis.2017.11.014
  66. Mercer D.K., Stewart C.S., Miller L., Robertson J., Duncan V.M.S., O’Neil D.A. // Antimicrob. Agents Chemother. 2019. V. 63. P. e02117-18. https://doi.org/10.1128/AAC.02117-18
  67. Turner J., Cho Y., Dinh N.-N., Waring A.J., Lehrer R.I. // Antimicrob. Agents Chemother. 1998. V. 42. P. 2206–2214.
  68. Kos S., Vanvarenberg K., Dolinsek T., Cemazar M., Jelenc J., Préat V., Sersa G., Vandermeulen G. // Bioelectrochemistry. 2017. V. 114. P. 33–41. https://doi.org/10.1016/j.bioelechem.2016.12.002
  69. Kowalski R.P., Romanowski E.G., Yates K.A., Mah F.S. // J. Ocul. Pharmacol. Ther. 2016. V. 32. P. 23–27. https://doi.org/10.1089/jop.2015.0098
  70. Isaksson J., Brandsdal B.O., Engqvist M., Flaten G.E., Svendsen J.S.M., Stensen W. // J. Med. Chem. 2011. V. 54. P. 5786–5795. https://doi.org/10.1021/jm200450h
  71. Saravolatz L.D., Pawlak J., Johnson L., Bonilla H., Saravolatz L.D., Fakih M.G., Fugelli A., Olsen W.M. // Antimicrob. Agents Chemother. 2012. V. 56. P. 4478–4482. https://doi.org/10.1128/AAC.00194-12
  72. Saravolatz L.D., Pawlak J., Martin H., Saravolatz S., Johnson L., Wold H., Husbyn M., Olsen W.M. // Lett. Appl. Microbiol. 2017. V. 65. P. 410–413. https://doi.org/10.1111/lam.12792
  73. Bojsen R., Torbensen R., Larsen C.E., Folkesson A., Regenberg B. // PLoS One. 2013. V. 8. P. e69483. https://doi.org/10.1371/journal.pone.0069483
  74. Tew G.N., Liu D., Chen B., Doerksen R.J., Kaplan J., Carroll P.J., Klein M.L., DeGrado W.F. // Proc. Natl. Acad. Sci. USA. 2002. V. 99. P. 5110–5114. https://doi.org/10.1073/pnas.082046199
  75. Kaplan C.W., Sim J.H., Shah K.R., Kolesnikova-Kaplan A., Shi W., Eckert R. // Antimicrob. Agents Chemother. 2011. V. 55. P. 3446–3452. https://doi.org/10.1128/AAC.00342-11
  76. Melo M., Dugourd D., Castanho M. // Recent Patents Anti-Infect. Drug Discov. 2006. V. 1. P. 201–207. https://doi.org/10.2174/157489106777452638
  77. Lorenzi T., Trombettoni M.M.C., Ghiselli R., Paolinelli F., Gesuita R., Cirioni O., Provinciali M., Kamysz W., Kamysz E., Piangatelli C. // Am. J. Transl. Res. 2017. V. 9. P. 3374–3386.
  78. Sader H.S., Fedler K.A., Rennie R.P., Stevens S., Jones R.N. // Antimicrob. Agents Chemother. 2004. V. 48. P. 3112–3118. https://doi.org/10.1128/AAC.48.8.3112-3118.2004
  79. Butler M.S., Blaskovich M.A., Cooper M.A. // J. Antibiot. 2013. V. 66. P. 571–591. https://doi.org/10.1038/ja.2013.86
  80. Martin-Loeches I., Dale G.E., Torres A. // Exp. Rev. Anti-Infect. Ther. 2018. V. 16. P. 259–268. https://doi.org/10.1080/14787210.2018.1441024
  81. Srinivas N., Jetter P., Ueberbacher B.J., Werneburg M., Zerbe K., Steinmann J., Van der Meijden B., Bernardini F., Lederer A., Dias R.L.A. // Science. 2010. V. 327. P. 1010–1013. https://doi.org/10.1126/science.1182749
  82. Kong Q., Yang Y. // Bioorg. Med. Chem. Lett. 2021. V. 35. P. 127799. https://doi.org/10.1016/j.bmcl.2021.127799
  83. Sader H.S., Dale G.E., Rhomberg P.R., Flamm R.K. // Antimicrob. Agents Chemother. 2018. V. 62. P. e00311-18. https://doi.org/10.1128/AAC.00311-18
  84. Sader H.S., Flamm R.K., Dale G.E., Rhomberg P.R., Castanheira M. // J. Antimicrob. Chemother. 2018. V. 73. P. 2400–2404. https://doi.org/10.1093/jac/dky227
  85. Giles F.J., Redman R., Yazji S., Bellm L. // Exp. Opin. Invest. Drugs. 2002. V. 11. P. 1161–1170. https://doi.org/10.1517/13543784.11.8.1161
  86. Gottler L.M., Ramamoorthy A. // Biochim. Biophys. Acta. 2009. V. 1788. P. 1680–1686. https://doi.org/10.1016/j.bbamem.2008.10.009
  87. Chalekson C.P., Neumeister M.W., Jaynes J. // J. Trauma. 2003. V. 54. P. 770–774. https://doi.org/10.1097/01.TA.0000047047.79701.6D
  88. Ballweber L.M., Jaynes J.E., Stamm W.E., Lampe M.F. // Antimicrob. Agents Chemother. 2002. V. 46. P. 34–41. https://doi.org/10.1128/AAC.46.1.34-41.2002
  89. Chalekson C.P., Neumeister M.W., Jaynes J. // Plast. Reconstr. Surg. 2002. V. 109. P. 1338–1343. https://doi.org/10.1097/00006534-200204010-00020
  90. Sandiford S.K. // Exp. Opin. Drug Dis. 2019. V. 14. P. 71–79. https://doi.org/10.1080/17460441.2019.1549032
  91. de la Fuente-Núñez C., Reffuveille F., Mansour S.C., Reckseidler-Zenteno S.L., Hernández D., Brackman G., Coenye T., Hancock R.E.W. // Chem. Biol. 2015. V. 22. P. 196–205. https://doi.org/10.1016/j.chembiol.2015.01.002
  92. Han Y., Zhang M., Lai R., Zhang Z. // Peptides. 2021. V. 146. P. 170666. https://doi.org/10.1016/j.peptides.2021.170666
  93. Henninot A., Collins J.C., Nuss J.M. // J. Med. Chem. 2018. V. 61. P. 1382–1414. https://doi.org/10.1021/acs.jmedchem.7b00318
  94. Lazzaro B.P., Zasloff M., Rolff J. // Science. 2020. V. 368. P. eaau5480. https://doi.org/10.1126/science.aau5480
  95. Mercer D.K., Torres M.D.T., Duay S.S., Lovie E., Simpson L., von Köckritz-Blickwede M., de la Fuente-Nunez C., O’Neil D.A., Angeles-Boza A.M. // Front. Cell. Infect. Microbiol. 2020. V. 10. P. 326. https://doi.org/10.3389/fcimb.2020.00326
  96. Murugaiyan J., Kumar P.A., Rao G.S., Iskandar K., Hawser S., Hays J.P., Mohsen Y., Adukkadukkam S., Awuah W.A., Jose R.A.M. // Antibiotics. 2022. V. 11. P. 200. https://doi.org/10.3390/antibiotics11020200
  97. Gan B.H., Gaynord J., Rowe S.M., Deingruber T., Spring D.R. // Chem. Soc. Rev. 2021. V. 50. P. 7820–7880. https://doi.org/10.1039/D0CS00729C
  98. Duong L., Gross S.P., Siryaporn A. // Front. Med. Technol. 2021. V. 3. P. 640981. https://doi.org/10.3389/fmedt.2021.640981
  99. Czaplewski L., Bax R., Clokie M., Dawson M., Fairhead H., Fischetti V.A., Foster S., Gilmore B.F., Hancock R.E.W., Harper D. // Lancet Infect. Dis. 2016. V. 16. P. 239–251. https://doi.org/10.1016/S1473-3099(15)00466-1
  100. Nang S.C., Li J., Velkov T. // Crit. Rev. Microbiol. 2019. V. 45. P. 131–161. https://doi.org/10.1080/1040841X.2018.1492902
  101. Han J.E., Alvarez J.A., Jones J.L., Tangpricha V., Brown M.A., Hao L., Brown L.A.S., Martin G.S., Ziegler T.R. // Nutrition. 2017. V. 38. P. 102–108. https://doi.org/10.1016/j.nut.2017.02.002

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