Action mechanism and structural requirements of the antimicrobial peptides, gaegurins

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 8, 2009, Pages 1620-1629

  Won, Hyung Sik ^a   Kang, Su Jin ^b   Lee, Bong Jin ^b  

^a Konkuk University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Antimicrobial peptide; Geagurin; Membrane binding; Nomenclature; Rana box; Structure activity relationship

Indexed keywords

CYSTEINE; GAEGURIN 4; GAEGURIN 5; GAEGURIN 6; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTIMICROBIAL ACTIVITY; ARTIFICIAL MEMBRANE; CARBOXY TERMINAL SEQUENCE; DRUG IDENTIFICATION; DRUG ISOLATION; DRUG STRUCTURE; FROG; HUMAN; MEMBRANE BINDING; MEMBRANE TRANSPORT; NONHUMAN; NUCLEAR PORE; PRIORITY JOURNAL; REVIEW; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ION CHANNELS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN PRECURSORS; STRUCTURE-ACTIVITY RELATIONSHIP; TERMINOLOGY AS TOPIC;

ANURA; GLANDIRANA; RANA RUGOSA;

EID: 67649277614     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.10.021     Document Type: Review

References (62)

1. Nascimento A.C., Fontes W., Sebben A., and Castro M.S. Antimicrobial peptides from anurans skin secretions. Prot. Peptide Letters 10 (2003) 227-238
2. Rinaldi A.C. Antimicrobial peptides from amphibian skin: an expanding scenario. Curr. Opin. Chem. Biol. 6 (2002) 799-804
3. Simmaco M., Mignogna G., and Barra D. Antimicrobial peptides from amphibian skin: what do they tell us?. Biopolymers 47 (1998) 435-450
4. Jenssen H., Hamill P., and Hancock R.E.W. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19 (2006) 491-511
5. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
6. Apponyi M.A., Pukala T.L., Brinkworth C.S., Maselli V.M., Bowie J.H., Tyler M.J., Booker G.W., Wallace J.C., Carver J.A., Separovic F., Doyle J., and Llewellyn L.E. Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 25 (2004) 11035-11054
7. Park J.M., Jung J.-E., and Lee B.J. Antimicrobial peptides from the skin of a Korean frog, Rana rugosa. Biochem. Biophys. Res. Commun. 205 (1994) 948-954 [Erratum in: Biochem. Biophys. Res. Commun. 209 (1995) 775.]
8. Kim S.S., Kim S., Kim E., Hyun B., Kim K.K., and Lee B.J. Synergistic inhibitory effect of cationic peptides and antimicrobial agents on the growth of oral streptococci. Caries Res. 37 (2003) 425-430
9. Won H.-S., Seo M.-D., Jung S.-J., Lee S.-J., Kang S.-J., Son W.-S., Kim H.-J., Park T.-K., Park S.-J., and Lee B.-J. Structural determinants for the membrane interaction of novel bioactive undecapeptides derived from gaegurin 5. J. Med. Chem. 49 (2006) 4886-4895
10. Kim S., Kim S.S., Bang Y.-J., Kim S.-J., and Lee B.J. In vitro activities of native and designed peptide antibiotics against drug sensitive and resistant tumor cell lines. Peptides 24 (2003) 945-953
11. J.M. Conlon, Reflections on a systematic nomenclature for antimicrobial peptides from the skins of frogs of the family Ranidae, Peptides 29 (2008) 1815-1819.
12. Park J.M., Lee J.Y., Moon H.M., and Lee B.J. Molecular cloning of cDNAs encoding precursors of frog skin antimicrobial peptides from Rana Rugos. Biochim. Biophys. Acta 1264 (1995) 23-25
13. Kwon S.Y., Carlson B.A., Park J.M., and Lee B.J. Structural organization and expression of the gaegurins 4 gene of Rana rugosa. Biochim. Biophys. Acta 1492 (2000) 185-190
14. Suzuki S., Ohe Y., Okubo T., Kakegawa T., and Tatemoto K. Isolation and characterization of novel antimicrobial peptides, rugosins A, B and C, from the skin of the frog, Rana rugosa. Biochem. Biophys. Res. Commun. 212 (1995) 249-254
15. Ali M.F., Knoop F.C., Vaudry H., and Conlon J.M. Characterization of novel antimicrobial peptides from the skins of frogs of the Rana esculenta complex. Peptides 24 (2003) 955-961
16. Won H.-S., Kim S.S., Jung S.-J., Son W.-S., Lee B., and Lee B.-J. Structure-activity relationships of antimicrobial peptides from the skin of Rana esculenta inhabiting in Korea. Mol. Cells 17 (2004) 469-476
17. Che J., Pang J., Zhao H., Wu G., Zhao E., and Zhang Y. Phylogeny of Raninae (Anura: Ranidae) inferred from mitochondrial and nuclear sequences. Mol. Phylogenet. Evol. 43 (2007) 1-13
18. Chen T., Li L., Zhou M., Rao P., Walker B., and Shaw C. Amphibian skin peptides and their corresponding cDNAs from single lyophilized secretion samples: identification of novel brevinins from three species of Chinese frogs. Peptides 27 (2006) 42-48
19. Goraya J., Wang Y., Li Z., O'Flaherty M., Knoop F.C., Platz J.E., and Conlon J.M. Peptides with antimicrobial activity from four different families isolates from the skins of the North American frogs Rana luteiventris, Rana berlandieri and Rana pipiens. Eur. J. Biochem. 267 (2000) 894-900
20. D.R. Frost, Amphibian Species of the World: an Online Reference, Version 5.2 (2008) Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.php. American Museum of Natural History, New York, USA
21. Conlon J.M., Kolodziejek J., and Nowotny N. Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim. Biophys. Acta 1696 (2004) 1-14
22. Vanhoye D., Bruston F., Nicolas P., and Amiche M. Antimicrobial peptides from hylid and ranin frogs originated from a 150-million-year-old ancestral precursor with a conserved signal peptide but a hypermutable antimicrobial domain. Eur. J. Biochem. 270 (2003) 2068-2081
23. Simmaco M., Mignogna G., Barra D., and Bossa F. Novel antimicrobial peptides from skin secretion of the European frog Rana esculenta. FEBS Lett. 324 (1993) 159-161
24. Simmaco M., Mignogna G., Barra D., and Bossa F. Antimicrobial peptides from skin secretions of Rana esculenta. J. Biol. Chem. 269 (1994) 11956-11961
25. Morikawa N., Hagiwara K., and Nakajima T. Brevinin-1 and -2, unique antimicrobial peptides from the skin of the frog, Rana brevipoda porsa. Biochem. Biophys. Res. Commun. 189 (1992) 184-190
26. Park S., Park S.-H., Ahn H.-C., Kim S., Kim S.S., Lee B.J., and Lee B.-J. Structural study of novel antimicrobial peptides, nigrocins, isolated from Rana nigromaculata. FEBS Lett. 507 (2001) 95-100
27. 15N nuclear magnetic resonance spectroscopy. Eur. J. Biochem. 267 (2000) 2695-2704
28. Park S.-H., Kim H.-E., Kim C.-M., Yun H.-J., Choi E.-C., and Lee B.-J. Role of proline, cysteine and a disulphide bridge in the structure and activity of the anti-microbial peptide gaegurin 5. Biochem. J. 368 (2002) 171-182
29. Chi S.-W., Kim J.-S., Kim D.-H., Lee S.-H., Park Y.-H., and Han K.-H. Solution structure and membrane interaction mode of an antimicrobial peptide gaegurin 4. Biochem. Biophys. Res. Commun. 352 (2007) 592-597
30. Park S.H., Son W.-S., Kim Y.-J., Kwon A.-R., and Lee B.-J. NMR spectroscopic assessment of the structure and dynamic properties of an amphibian antimicrobial peptide (gaegurin 4) bound to SDS micelles. J. Biochem. Mol. Biol. 40 (2007) 261-269
31. Won H.-S., Jung S.-J., Kim H.E., Seo M.-D., and Lee B.-J. Systematic peptide engineering and structural characterization to search for the shortest antimicrobial peptide analogue of gaegurin 5. J. Biol. Chem. 279 (2004) 14784-14791
32. Won H.-S., Park S.-H., Kim H.E., Hyun B., Kim M., Lee B.J., and Lee B.-J. Effects of a tryptophanyl substitution on the structure and antimicrobial activity of C-terminally truncated gaegurin 4. Eur. J. Biochem. 269 (2002) 4367-4374
33. Sitaram N. Antimicrobial peptides with unusual amino acid compositions and unusual structures. Curr. Med. Chem. 13 (2006) 679-696
34. Epand R.M., and Vogel H.J. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462 (1999) 11-28
35. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev., Microbiol. 3 (2005) 238-250
36. Yeaman M.R., and Yount N.Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55 (2003) 27-55
37. Oren Z., and Shai Y. Mode of action of linear amphipathic α-helical antimicrobial peptides. Biopolymers 47 (1998) 451-463
38. Shai Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by a-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochimica. Biophys. Acta 1462 (1999) 55-70
39. Giangaspero A., Sandri L., and Tossi A. Amphipathic α helical antimicrobial peptides. Eur. J. Biochem. 268 (2001) 5589-5600
40. Blondelle S.E., Lohner K., and Aguilar M.-I. Lipid-induced conformation and lipid-binding properties of cytolytic and antimicrobial peptides: determination and biological specificity. Biochim. Biophys. Acta 1462 (1999) 89-108
41. Tossi A., Sandri L., and Giangspero A. Amphipathic, α-helical antimicrobial peptides. Biopolymers 55 (2000) 4-30
42. Sai K.P., Jagannadham M.V., Vairamani M., Raju N.P., Devi A.S., Nagaraj R., and Sitaram N. Tigerinins: novel antimicrobial peptides from the Indian frog Rana tigerina. J. Biol. Chem. 276 (2001) 2701-2707
43. Vignal E., Chavanieu A., Roch P., Chiche L., Grassy G., Calas B., and Aumelas A. Solution structure of the antimicrobial peptide ranalexin and a study of its interaction with perdeuterated dodecylphosphocholine micelles. Eur. J. Biochem. 253 (1998) 221-228
44. Clark D.P., Durell S., Maloy W.L., and Zasloff M. Ranalexin: a novel antimicrobial peptide from bullfrog (Rana catesbeiana) skin, structurally related to the bacterial antibiotic, polymyxin. J. Biol. Chem. 269 (1994) 10849-10855
45. Kim S., Kim J.-Y., Lee B.-J., and Kim S.-J. Synthesis and characterization of GGN4 and its tryptophan substituted analogue peptides. J. Biochem. Mol. Biol. 32 (1999) 12-19
46. Kwon M.-Y., Hong S.-Y., and Lee K.-H. Structure-activity analysis of brevinin 1E amide, an antimicrobial peptide from Rana esculenta. Biochim. Biophys. Acta 1387 (1998) 239-248
47. Kumari V.K., and Nagarj R. Structure-function studies on the amphibian peptide brevinin 1E: translocating the cationic segment from the C-terminal end to a central position favors selective antibacterial activity. J. Pept. Res. 58 (2001) 433-441
48. Lee K.-H., Hong S.-Y., Oh J.-E., Lee B.-J., and Choi B.-S. Antimicrobial activity and conformation of gaegurin-6 amide and its analogs. Peptides 19 (1998) 1653-1658
49. Suh J.-Y., Lee Y.-T., Park C.-B., Lee K.-H., Kim S.-C., and Choi B.-S. Structural and functional implications of a proline residue in the antimicrobial peptide gaegurin. Eur. J. Biochem. 266 (1999) 665-674
50. Suh J.-Y., Lee K.-H., Chi S.-W., Hong S.-Y., Choi B.-W., Moon H.-M., and Choi B.-S. Unusually stable helical kink in the antimicrobial peptide - a derivative of gaegurin. FEBS Lett. 392 (1996) 309-312
51. Ponti D., Mignogna G., Mangoni M.L., De Biase D., Simmaco M., and Barra D. Expression and activity of cyclic and linear analogues of esculentin-1, an anti-microbial peptide from amphibian skin. Eur. J. Biochem. 263 (1999) 921-927
52. Buchko G.W., Rozek A., Hoyt D.W., Cushley R.J., and Kennedy M.A. The use of sodium dodecyl sulfate to model the apolipoprotein environment: evidence for peptide-SDS complexes using pulsed-field-gradient NMR spectroscopy. Biochim. Biophys. Acta 1392 (1998) 101-108
53. Ambroggio E.E., Separovic F., Bowie J.H., Fidelio G.D., and Bagatolli L.A. Direct visualization of membrane leakage induced by the antibiotic peptides: maculatin, citropin, and aurein. Biophys. J. 89 (2005) 1874-1881
54. Kim H.J., Han S.K., Park J.B., Baek H.J., Lee B.J., and Ryu P.D. Gaegurin 4, a peptide antibiotic of frog skin, forms voltage-dependent channels in planar lipid bilayers. J. Pept. Res. 53 (1999) 1-7
55. Eun S.-Y., Jang H.-K., Han S.-K., Ryu P.-D., Lee B.-J., Han K.-H., and Kim S.-J. A helix-induced oligomeric transition of gaegurin 4, an antimicrobial peptide isolated from a Korean frog. Mol. Cells 21 (2006) 229-236
56. Kim H.J., Kim S.S., Lee M.H., Lee B.J., and Ryu P.D. Role of C-terminal heptapeptide in pore-forming activity of antimicrobial agent gaegurin 4. J. Pept. Res. 64 (2004) 151-158
57. Marsh D. Peptide models for membrane channels. Biochem. J. 315 (1996) 345-361
58. Lau S.Y., Taneja A.K., and Hodges R.S. Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and formation of two-stranded alpha-helical coiled-coils. J. Biol. Chem. 259 (1984) 13253-13261
59. Zhou N.E., Zhu B.-Y., Sykes B.D., and Hodges R.S. Relationship between amide proton chemical shifts and hydrogen bonding in amphipathic α-helical peptides. J. Am. Chem. Soc. 114 (1992) 4320-4326
60. Lam Y.-H., Wassall S.R., Morton C.J., Smith R., and Separovic F. Solid-state NMR structure determination of melittin in a lipid environment. Biophys. J. (2001) 2752-2761
61. Boland M.P., and Separovic F. Membrane interactions of antimicrobial peptides from Australian tree frogs. Biochim. Biophys. Acta 1758 (2006) 1178-1183
62. Woolfson D.N., Mortishire-Smith R.J., and Williams D.H. Conserved positioning of proline residues in membrane-spanning helices of ion-channel proteins. Biochem. Biophys. Res. Commun. 175 (1991) 733-737