Structure and Biological Functions of β-Hairpin Antimicrobial Peptides

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Abstract

Antimicrobial peptides (AMPs) are evolutionarily ancient factors of the innate immune system that serve as a crucial first line of defense for humans, animals, and plants against infection. This review focuses on the structural organization, biosynthesis, and biological functions of AMPs that possess a β-hairpin spatial structure. Representatives of this class of AMPs are among the most active antibiotic molecules of animal origin. Due to their wide spectrum of activity and resistance to internal environmental factors, natural β-hairpin AMPbased compounds might become the most promising drug candidates.

About the authors

P. V. Panteleev

M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Email: ovch@ibch.ru
Russian Federation

I. A. Bolosov

M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Email: ovch@ibch.ru
Russian Federation

S. V. Balandin

M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Email: ovch@ibch.ru
Russian Federation

T. V. Ovchinnikova

M.M. Shemyakin and Yu.A. Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences

Author for correspondence.
Email: ovch@ibch.ru
Russian Federation

References

  1. Kokryakov V.N. // Ocherki o vrozhdennom immunitete (Essays on innate immunity). St. Petersburg: Nauka, 2006. 2006, P.261
  2. Zasloff M. // Nature 2002, V.415, №6870, P.389-395
  3. Oppenheim J.J., Biragyn A., Kwak L.W., Yang D. // Ann. Rheum. Dis. 2003, V.62, S2, P. ii17-ii21
  4. Bergquist D.C., Williams F.M., Fisher C.R. // Nature 2000, V.403, №6769, P.499-500
  5. Roscia G., Falciani C., Bracci L., Pini A. // Curr. Protein Pept. Sci. 2013, V.14, №8, P.641-649
  6. Zhao X., Wu H., Lu H., Li G., Huang Q. // PLoS One. 2013, V.8, №6, P.e66557
  7. Boman H.G. // Annu. Rev. Immunol. 1995, V.13, P.61-92
  8. Baumann G., Mueller P. J. // Supramol. Struct. 1974, V.2, №5-6, P.538-557
  9. Matsuzaki K., Yoneyama S., Fujii N., Miyajima K., Yamada K., Kirino Y., Anzai K. // Biochemistry. 1997, V.36, №32, P.9799-9806
  10. Yang L., Harroun T.A., Weiss T.M., Ding L., Huang H.W. // Biophys. J. 2001, V.81, №3, P.1475-1485
  11. Shai Y. // Biochim. Biophys. Acta. 1999, V.1462, №1-2, P.55-70
  12. Matsuzaki K. // Biochim. Biophys. Acta. 1999, V.1462, №1-2, P.1-10
  13. Yonezawa A., Kuwahara J., Fujii N., Sugiura Y. // Biochemistry. 1992, V.31, №11, P.2998-3004
  14. Osaki T., Omotezako M., Nagayama R., Hirata M., Iwanaga S., Kasahara J., Hattori J., Ito I., Sugiyama H., Kawabata S.J. // Biol. Chem. 1999, V.274, №37, P.26172-26178
  15. Fleischmann J., Selsted M., Lehrer R.I. // Diagn. Microbiol. Dis. 1985, V.3, №3, P.233-242
  16. Biragyn A., Surenhu M., Yang D., Ruffini P.A., Haines B.A., Klyushnenkova E., Oppenheim J.J., Kwak L.W. // J. Immunol. 2001, V.167, №11, P.6644-6653
  17. Niyonsaba F., Someya A., Hirata M., Ogawa H., Nagaoka I. // Eur. J. Immunol. 2001, V.31, №4, P.1066-1075
  18. Davidson D.J., Currie A.J., Reid G.S., Bowdish D.M., Mac-Donald K.L., Ma R.C., Hancock R.E., Speert D.P. // Immunol. 2004, V.172, №2, P.1146-1156
  19. Li J., Post M., Volk R., Gao Y., Li M., Metais C., Sato K., Tsai J., Aird W., Rosenberg R. // Nat. Med. 2000, V.6, №1, P.49-55
  20. Zhu Q.Z., Hu J., Mulay S., Esch F., Shimasaki S., Solomon S. // Proc. Natl. Acad. Sci. USA. 1988, V.85, №2, P.592-596
  21. Saito T., Miyakawa H., Tamura Y.J. // Dairy Sci. 1991, V.74, №11, P.3724-3730
  22. Bellamy W., Takase M., Yamauchi K., Wakabayashi H., Kawase K., Tomita M. // Biochem. Biophys. Acta. 1992. V. 1121. № 1-2. 1992, V.1121, №1-2, P.130-136
  23. Hwang P.M., Zhou N., Shan X., Arrowsmith C.H., Vogel H.J. // Biochemistry. 1998, V.37, №12, P.4288-4298
  24. Yamauchi K., Tomita M., Giehl T.J., Ellison R.T. // Infect. Immun. 1993, V.61, №2, P.719-728
  25. Jenssen H., Andersen J.H., Uhlin-Hansen L., Gutteberg T.J., Rekdal O. // Antiviral Res. 2004, V.61, №2, P.101-109
  26. Bellamy W., Yamauchi K., Wakabayashi H., Takase M., Takakura N., Shimamura S., Tomita M. // Lett. Appl. Microbiol. 2008, V.18, P.230-233
  27. Yoo Y., Watanabe S., Watanabe R., Hata K., Shimazaki K., Azuma I. // Jpn. J. Cancer Res. 1997, V.88, №2, P.184-190
  28. Eliassen L.T., Berge G., Leknessund A., Wikman M., Lindin I., Løkke C., Ponthan F., Johnsen J.I., Sveinbjørnsson B., Kogner P. // Int. J. Cancer. 2006, V.119, №3, P.493-500
  29. Mader J.S., Salsman J., Conrad D.M., Hoskin D.W. // Mol. Cancer. Ther. 2005, V.4, №4, P.612-624
  30. Mattsby-Baltzer I., Roseanu A., Motas C., Elverfors J., Engberg I., Hanson L.A. // Pediatr. Res. 1996, V.40, №2, P.257-262
  31. Britigan B.E., Lewis T.S., Waldshcmidt M., McCormick M.L., Krieg A.M. // J. Immunol. 2001, V.167, №5, P.2921-2928
  32. Ellison R. 3rd., Giehl T. // J. Clin. Invest. 1991, V.88, №8, P.1080-1091
  33. Velden W.J., van Iersel T.M., Blijlevens N.M., Donnelly J.P. // BMC Med. 2009, V.7, P.44
  34. Romeo D., Skerlavaj B., Bolognesi M., Gennaro R. // J. Biol. Chem. 1988, V.263, №20, P.9573-9575
  35. Wu M., Hancock R. // Antimicrob. Agents Chemother. 1999, V.43, №5, P.1274-1276
  36. Shestakov A., Jenssen H., Hancock R.E., Nordström I., Eriksson K. // Antiviral Res. Nov. 2013, V.100, №2, P.455-459
  37. Sai K.P., Jagannadham M.V., Vairamani M., Raju N.P., Devi A.S., Nagaraj R., Sitaram N. // J. Biol. Chem. 2001, V.276, №4, P.2701-2707
  38. Sitaram N., Purna Sai K., Singh S., Sankaran K., Nagaraj R. // Antimicrob. Agents Chemother. 2002, V.46, №7, P.2279-2283
  39. Ojo O., Abdel-Wahab Y., Flatt P., Mechkarska M., Conlon J. // Diabetes Obes. Metab. 2011, V.13, №12, P.1114-1122
  40. Fehlbaum P., Bulet P., Chernysh S., Briand J.P., Roussel J.P., Letellier L., Hetru C., Hoffmann J.A. // Proc. Natl. Acad. Sci. 1996, V.93, №3, P.1221-1225
  41. Morikawa N., Hagiwara K., Nakajima T. // Biochem. Biophys. Res. Commun. 1992, V.189, №1, P.184-190
  42. Mandard N., Sodano P., Labbe H., Bonmatin J.M., Bulet P., Hetru C., Ptak M., Vovelle F. // Eur. J. Biochem. 1998, V.256, №2, P.404-410
  43. Pages J.M., Dimarcq J.L., Quenin S., Hetru C. // Int. J. Antimicrob. Agents. 2003, V.22, №3, P.265-269
  44. Lee M.K., Cha L., Lee S.H., Hahm K.S. // J. Biochem. Mol. Biol. 2002, V.35, №3, P.291-296
  45. Hou Z., Da F., Liu B., Xue X., Xu X., Zhou Y., Li M., Li Z., Ma X., Meng J. // Antimicrob. Agents Chemother. 2013, V.57, №10, P.5045-5052
  46. Wu G., Deng X., Wu P., Shen Z., Xu H. // Peptides. 2012, V.36, №1, P.109-113
  47. Wu G., Wu P., Xue X., Yan X., Liu S., Zhang C., Shen Z., Xi T. // Peptides. 2013, V.45, P.73-77
  48. Wu T., Tang D., Chen W., Huang H., Wang R., Chen Y. // Gene. 2013, V.527, №1, P.235-242
  49. Imamura T., Yasuda M., Kusano H., Nakashita H., Ohno Y., Kamakura T., Taguchi S., Shimada H. // Transgenic Res. 2010, V.19, №3, P.415-424
  50. Ovchinnikova T.V., Aleshina G.M., Balandin S.V., Krasnosdembskaya A.D., Markelov M.L., Frolova E.I., Leonova Y.F., Tagaev A.A., Krasnodembsky E.G., Kokryakov V.N. // FEBS Lett. 2004. V. 577. № 1-2. 2004, V.577, №1-2, P.209-214
  51. Andrä J., Jakovkin I., Grötzinger J., Hecht O., Krasnosdembskaya A.D., Goldmann T., Gutsmann T., Leippe M. // Biochem. J. 2008, V.410, №1, P.113-122
  52. Cho J., Lee D.G. // Biochim. Biophys. Acta. 2011, V.1810, №12, P.1246-1251
  53. Diachenko I.A., Murashev A.N., Yakimenko Z.A., Balandin S.V., Ovchinnikova T.V. // Toksikologicheskii vestnik. (Toxicological review). 2012, V.112, №1, P.40-43
  54. Ovchinnikova T.V., Shenkarev Z.O., Nadezhdin K.D., Balandin S.V., Zhmak M.N., Kudelina I.A., Finkina E.I., Kokryakov V.N., Arseniev A.S. // Biochem. Biophys. Res. Commun. 2007, V.360, №1, P.156-162
  55. Stavrakoudis A., Tsoulos I.G., Shenkarev Z.O., Ovchinnikova T.V. // Biopolymers. 2009, V.92, №3, P.143-155
  56. Ovchinnikova T.V., Shenkarev Z.O., Balandin S.V., Nadezhdin K.D., Paramonov A.S., Kokryakov V.N., Arseniev A.S. // Biopolymers. 2008, V.89, №5, P.455-464
  57. Salnikov E.S., Aisenbrey C., Balandin S.V., Zhmak M.N., Ovchinnikova T.V., Bechinger B. // Biochemistry. 2011, V.50, №18, P.3784-3795
  58. Shenkarev Z.O., Balandin S.V., Trunov K.I., Paramonov A.S., Sukhanov S.V., Barsukov L.I., Arseniev A.S., Ovchinnikova T.V. // Biochemistry. 2011, V.50, №28, P.6255-6265
  59. Mani R., Cady S.D., Tang M., Waring A.J., Lehrer R.I., Hong M. // Proc. Natl. Acad. Sci. USA. 2006, V.103, №44, P.16242-16247
  60. Hoegenhaug H.H.K., Mygind P.H., Kruse T., Segura D.R., Sandvang D., Neve S. // PCT/ EP2011/059,6896. // WO Patent App. 2011
  61. Fox J.L. // Nat. Biotechnol. 2013, V.31, №5, P.379-382
  62. Nakamura T., Furunaka H., Miyata T., Tokunaga F., Muta T., Iwanaga S., Niwa M., Takao T., Shimonishi Y. // J. Biol. Chem. 1988, V.263, №32, P.16709-16713
  63. Miyata T., Tokunaga F., Yoneya T., Yoshikawa K., Iwanaga S., Niwa M., Takao T., Shimonishi Y. // J. Biochem. 1989, V.106, №4, P.663-668
  64. Shigenaga T., Takayenoki Y., Kawasaki S., Seki N., Muta T., Toh Y., Ito A., Iwanaga S. // J. Biochem. 1993, V.114, №3, P.307-316
  65. Oishi O., Yamashita S., Nishimoto E., Lee S., Sugihara G., Ohno M. // Biochemistry. 1997, V.36, №14, P.4352-4359
  66. Fjell C.D., Hiss J.A., Hancock R.E., Schneider G. // Nat. Rev. Drug. Discov. 2011, V.11, №1, P.37-51
  67. Ozaki A., Ariki S., Kawabata S. // FEBS J. 2005, V.272, №15, P.3863-3871
  68. Tamamura H., Kuroda M., Masuda M., Otaka A., Funakoshi S., Nakashima H., Yamamoto N., Waki M., Matsumoto A., Lancelin J.M. // Biochim. Biophys. Acta. 1993, V.1163, №2, P.209-216
  69. Chen Y., Xu X., Hong S., Chen J., Liu N., Underhill C.B., Creswell K., Zhang L. // Cancer Research 2001, V.61, №6, P.2434-2438
  70. Shi S.L., Wang Y.Y., Liang Y., Li Q.F. // World J. Gastroenterol. 2006, V.12, №11, P.1694-1698
  71. Chen J., Xu X.M., Underhill C.B., Yang S., Wang L., Chen Y., Hong S., Creswell K., Zhang L. // Cancer Research 2005, V.65, №11, P.4614-4622
  72. Silva P. Jr., Daffre S., Bulet P. // J. Biol. Chem. 2000, V.275, №43, P.33464-33470
  73. Mandard N., Bulet P., Caille A., Daffre S., Vovelle F. // Eur. J. Biochem. 2002, V.269, №4, P.1190-1198
  74. Barbosa F.M., Daffre S., Maldonado R.A., Miranda A., Nimrichter L., Rodrigues M.L. // FEMS Microbiol Lett. 2007, V.274, №2, P.279-286
  75. Rodrigues E.G., Dobroff A.S., Cavarsan C.F., Paschoalin T., Nimrichter L., Mortara R.A., Santos E.L., Fázio M.A., Miranda A., Daffre S. // Neoplasia. 2008, V.10, №1, P.61-68
  76. Ehret-Sabatier L., Loew D., Goyffon M., Fehlbaum P., Hoffmann J.A., van Dorsselaer A., Bulet P. // J. Biol. Chem. 1996, V.271, №47, P.29537-29544
  77. Mandard N., Sy D., Maufrais C., Bonmatin J.M., Bulet P., Hetru C., Vovelle F. // J. Biomol. Struct. Dyn. 1999, V.17, №2, P.367-380
  78. Hetru C., Letellier L., Oren Z., Hoffmann J.A., Shai Y. // Biochem J. 2000, V.345, Pt3, P.653-664
  79. Kokryakov V.N., Harwig S.S.L., Panyutich E.A., Shevchenko A.A., Aleshina G.M., Shamova O.V., Korneva H.A., Lehrer R.I. // FEBS Lett. 1993, V.327, №2, P.231-236
  80. Fahrner R.L., Dieckmann T., Harwig S.S., Lehrer R.I., Eisenberg D., Feigon J. // Chem. Biol. 1996, V.3, №7, P.543-550
  81. Panyutich A., Shi J., Boutz P.L., Zhao C., Ganz T. // Infect Immun. 1997, V.65, №3, P.978-985
  82. Steinberg D.A., Hurst M.A., Fujii C.A., Kung A.H., Ho J.F., Cheng F.C., Loury D.J., Fiddes J.C. // Antimicrob. Agents Chemother. 1997, V.41, №8, P.1738-1742
  83. Ge Y.G., MacDonald D.L., Holroyd K.J., Thornsberry C., Wexler H., Zasloff M. // Antimicrob. Agents Chemother. 1999, V.43, №4, P.782-788
  84. Shamova O.V., Sakuta G.A., Orlov D.S., Zenin V.V., Shtein G.I., Kolodkin N.I., Afonina I.V., Kokriakov V.N. // Cell Tissue Biology. 2007, V.1, №6, P.524-533
  85. Paredes-Gamero E.J., Martins M.N., Cappabianco F.A., Ide J.S., Miranda A. // Biochim. Biophys. Acta. 2012, V.1820, №7, P.1062-1072
  86. Rothan H.A., Abdulrahman A.Y., Sasikumer P.G., Othman S., Rahman N.A., Yusof R. // J. Biomed. Biotechnol. 2012, V.2012, P.P. ID 251482
  87. Chen J., Falla T.J., Liu H., Hurst M.A., Fujii C.A., Mosca D.A., Embree J.R., Loury D.J., Radel P.A., Cheng Chang C. // Biopolymers. 2000, V.55, №1, P.88-98
  88. Giles F.J., Redman R., Yazji S., Bellm L. // Expert. Opin. Investig. Drugs. 2002, V.11, №8, P.1161-1170
  89. Tang Y.Q., Yuan J., Osapay G., Osapay K., Tran D., Miller C.J., Ouellette A.J., Selsted M.E. // Science. 1999, V.286, №5439, P.498-502
  90. Lehrer R.I., Cole A.M., Selsted M.E. // J. Biol. Chem. 2012, V.287, №32, P.27014-27019
  91. Nguyen T.X., Cole A.M., Lehrer R.I. // Peptides. 2003, V.24, №11, P.1647-1654
  92. Cole A.M., Hong T., Boo L.M., Nguyen T., Zhao C., Bristol G., Zack J.A., Waring A.J., Yang O.O., Lehrer R.I. // Proc. Natl. Acad. Sci. USA. 2002, V.99, №4, P.1813-1818
  93. Trabi M., Schirra H.J., Craik D.J. // Biochemistry. 2001, V.40, №14, P.4211-4221
  94. Garcia A.E., Osapay G., Tran P.A., Yuan J., Selsted M.E. // Infect. Immun. 2008, V.76, №12, P.5883-5891
  95. Wang W., Mulakala C., Ward S.C., Jung G., Luong H., Pham D., Waring A.J., Kaznessis Y., Lu W., Bradley K.A. // J. Biol. Chem. 2006, V.281, №43, P.32755-32764
  96. Arnett E., Lehrer R.I., Pratikhya P., Lu W., Seveau S. // Cell Microbiol. 2011, V.13, №4, P.635-651
  97. Doss M., White M.R., Tecle T., Gantz D., Crouch E.C., Jung G., Ruchala P., Waring A.J., Lehrer R.I., Hartshorn K.L. // J. Immunol. 2009, V.182, №12, P.7878-7887
  98. Yasin B., Wang W., Pang M., Cheshenko N., Hong T., Waring A.J., Herold B.C., Wagar E.A., Lehrer R.I. // Virology Journal 2004, V.78, №10, P.5147-5156
  99. Schaal J.B., Tran D., Tran P., Ösapay G., Trinh K., Roberts K.D., Brasky K.M., Tongaonkar P., Ouellette A.J., Selsted M.E. // PLoS One. 2012, V.7, №12, P.e51337
  100. Krause A., Neitz S., Mägert H.J., Schulz A., Forssmann W.G., Schulz-Knappe P., Adermann K. // FEBS Lett. 2000, V.480, №2-3, P.147-150
  101. Park C.H., Valore E.V., Waring A.J., Ganz T. J. // Biol. Chem. 2001, V.276, №11, P.7806-7810
  102. Shike H., Lauth X., Westerman M.E., Ostland V.E., Carlberg J.M., van Olst J.C., Shimizu C., Bulet P., Burns J.C. // Eur. J. Biochem. 2002, V.269, №8, P.2232-2237
  103. Hunter H.N., Fulton D.B., Ganz T., Vogel H.J. // J. Biol. Chem. 2002, V.277, №40, P.37597-37603
  104. Hocquellet A., Odaert B., Cabanne C., Noubhani A., Dieryck W., Joucla G., Le Senechal C., Milenkov M., Chaignepain S., Schmitter J.M. // Peptides. 2010, V.31, №1, P.58-66
  105. Hocquellet A., Le Senechal C., Garbay B. // Peptides. 2012, V.36, №2, P.303-307
  106. Ganz T. // Blood. 2003, V.102, №3, P.783-788
  107. Nicolas G., Bennoun M., Devaux I., Beaumont C., Grandchamp B., Kahn A., Vaulont S. // Proc. Natl. Acad. Sci. USA. 2001, V.98, №15, P.8780-8785
  108. Ganz T., Nemeth E. // Annu. Rev. Med. 2011, V.62, P.347-360
  109. Nguyen L.T., Chau J.K., Perry N.A., de Boer L., Zaat S.A.J., Vogel H.J. // PLoS One. 2010, V.5, №9, P.e12684
  110. Nan Y., Jacob B., Kim Y., Shin S. // J. Pept. Sci. 2012, V.18, №12, P.740-747
  111. Fazio M.A., Oliveira V.X., Bulet P., Miranda M.T.M., Daffre S., Miranda A. // Biopolymers. 2006, V.84, №2, P.205-218
  112. Conibear A.C., Rosengren K.J., Daly N.L., Henriques S.T., Craik D.J. // J. Biol. Chem. 2013, V.188, №15, P.10830-10840
  113. Peschel A., Sahl H.G. // Nat. Rev. Microbiol. 2006, V.4, №7, P.529-536

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