Temporins, anti-infective peptides with expanding properties

Cellular and Molecular Life Sciences

Volumn 63, Issue 9, 2006, Pages 1060-1069

  Mangoni, M L ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Antimicrobial peptide; Frog skin secretion; Infectious disease; Innate immunity; Lipid peptide interaction; Membrane active peptide; Temporin

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT; TEMPORIN; TEMPORIN 1ARA; TEMPORIN 1AUA; TEMPORIN 1BYA; TEMPORIN 1CA; TEMPORIN 1CB; TEMPORIN 1CC; TEMPORIN 1CD; TEMPORIN 1CE; TEMPORIN 1EC; TEMPORIN 1GA; TEMPORIN 1GB; TEMPORIN 1GC; TEMPORIN 1GD; TEMPORIN 1JA; TEMPORIN 1LA; TEMPORIN 1LB; TEMPORIN 1LC; TEMPORIN A; TEMPORIN B; TEMPORIN C; TEMPORIN D; TEMPORIN E; TEMPORIN F; TEMPORIN G; TEMPORIN H; TEMPORIN K; TEMPORIN L; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AMINO ACID SEQUENCE; AMPHIBIA; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE RESPONSE; NONHUMAN; PROTEIN SYNTHESIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; REVIEW; SKIN SECRETION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANTI-INFECTIVE AGENTS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CONSENSUS SEQUENCE; ESCHERICHIA COLI; HOST-PARASITE RELATIONS; IMMUNITY, NATURAL; LEISHMANIA; PROTEINS; RANA TEMPORARIA; SEQUENCE HOMOLOGY, AMINO ACID; SKIN; STRUCTURE-ACTIVITY RELATIONSHIP;

AMPHIBIA; ANURA;

EID: 33744459976     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5536-y     Document Type: Review

References (100)

1. Guder A., Wiedemann I. and Sahl H. G. (2000) Posttranslationally modified bacteriocins - the lantibiotics. Biopolymers 55: 62-73
2. Marx F. (2004) Small, basic antifungal proteins secreted from filamentous ascomycetes: a comparative study regarding expression, structure, function and potential application. Appl. Microbiol. Biotechnol. 65: 133-142
3. Mygind P. H., Fischer R. L., Schnorr K. M., Hansen M. T., Sonksen C. P., Ludvigsen S. et al. (2005) Plectasin is apeptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437: 975-980
4. Lay F. T. and Anderson M. A. (2005) Defensins - components of the innate immune system in plants. Curr. Protein Pept. Sci. 6: 85-101
5. Zasloff M. (2002) Antimicrobial peptides of multicellular or ganisms. Nature 415: 389-395
6. Hoffmann J. A. (2003) The immune response of Drosophila. Nature 426: 33-38
7. Boman H. G. (2003) Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med. 254: 197-215
8. Lehrer R. I. (2004) Primate defensins. Nat. Rev. Microbiol. 2: 727-738
9. Sahl H. G., Pag U., Bonness S., Wagner S., Antcheva N. and Tossi A. (2005) Mammalian defensins: structures and mechanism of antibiotic activity. J. Leukoc. Biol. 77: 466-475
10. Boman H. G. (1995) Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13: 61-92
11. Kimbrell D. A. and Beutler B. (2001) The evolution and genetics of innate immunity. Nat. Rev. Genet. 2: 256-267
12. Ganz T. (2003) Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3: 710-720
13. Selsted M. E. and Ouellette A. J. (2005) Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6: 551-557
14. Zanetti M. (2005) The role of cathelicidins in the innate host defenses of mammals. Curr. Issues Mol. Biol. 7: 179-196
15. Glaser R., Harder J., Lange H., Bartels J., Christophers E. and Schroder J. M. (2005) Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat. Immunol. 6: 57-64
16. Muller C. A., Autenrieth I. B. and Peschel A. (2005) Innate defenses of the intestinal epithelial barrier. Cell. Mol. Life Sci. 62: 1297-1307
17. Wehkamp J., Salzman N. H., Porter E., Nuding S., Weichenthal M., Petras R. E. et al. (2005) Reduced Paneth cell α-defensins in ileal Crohn's disease. Proc. Natl. Acad. Sci. USA 102: 18129-18134
18. Hancock R. E. and Diamond G. (2000) The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol. 8: 402-410
19. Beisswenger C. and Bals R. (2005) Functions of antimicrobial peptides in host defense and immunity. Curr. Protein Pept. Sci. 6: 255-264
20. Zanetti M. (2004) Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 75: 39-48
21. Hancock R. E. W. and Patrzykat A. (2002) Clinical development of cationic antimicrobial peptides: from natural to novel antibiotics. Curr. Drug. Targets Infect. Disord. 2: 79-83
22. Papo N. and Shai Y. (2005) Host defense peptides as new weapons in cancer treatment. Cell. Mol. Life Sci. 62: 784-790
23. Wilson C. L., Ouellette A. J., Satchell D. P., Ayabe T., Lopez-Boado Y. S., Stratman J. L. et al. (1999) Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286: 113-117
24. Ayabe T., Ashida T., Kohgo Y. and Kono T. (2004) The role of Paneth cells and their antimicrobial peptides in innate host defense. Trends Microbiol. 12: 394-398
25. Yeaman M. R. and Yount N. Y. (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55: 27-55
26. Simmaco M., Mignogna G. and Barra D. (1998) Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers 47: 435-450
27. Rinaldi A. C. (2002) Antimicrobial peptides from amphibian skin: an expanding scenario. Curr. Opin. Chem. Biol. 6: 799-804
28. Conlon J. M., Kolodziejek J. and Nowotny N. (2004) Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim. Biophys. Acta 1696: 1-14
29. Simmaco M., Mangoni M. L., Boman A., Barra D. and Boman H. G. (1998) Experimental infections of Rana esculenta with Aeromonas hydrophila: a molecular mechanism for the control of the normal flora. Scand. J. Immunol. 48: 357-363
30. Boman H. G. (2000) Innate immunity and the normal microflora. Immunol. Rev. 173: 5-16
31. Miele R., Ponti D., Boman H. G., Barra D. and Simmaco M. (1998) Molecular cloning of a bombinin gene from Bombina orientalis: detection of NF-kappaB and NF-IL6 binding sites in its promoter. FEBS Lett. 431: 23-28
32. Mangoni M. L., Miele R., Renda T. G., Barra D. and Simmaco M. (2001) The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms. FASEB J. 15: 1431-1432
33. VanCompernolle S. E., Taylor R. J., Oswald-Richter K., Jiang J., Youree B. E., Bowie J. H. et al. (2005) Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J. Virol. 79: 11598-11606
34. Simmaco M., Mignogna G., Canofeni S., Miele R., Mangoni M. L. and Barra D. (1996) Temporins, antimicrobial peptides from the European red frog Rana temporaria. Eur. J. Biochem. 242: 788-792
35. Krishnakumari V. and Nagaraj R. (1997) Antimicrobial and hemolytic activities of crabrolin, a 13-residue peptide from the venom of the European hornet, Vespa crabro, and its analogs. J. Pept. Res. 50: 88-93
36. Argiolas A. and Pisano J. J. (1984) Isolation and characterization of two new peptides, mastoparan C and crabrolin, from the venom of the European hornet, Vespa crabro. J. Biol. Chem. 259: 10106-10111
37. Clark D. P., Durell S., Maloy W. L. and Zasloff M. (1994) Ranalexin: a novel antimicrobial peptide from bullfrog (Rana catesbeiana) skin, structurally related to the bacterial antibiotic, polymyxin. J. Biol. Chem. 269: 10849-10855
38. Amiche M., Ducancel F., Mor A., Boulain J. C., Menez A. and Nicolas P. (1994) Precursors of vertebrate peptide antibiotics dermaseptin b and adenoregulin have extensive sequence identities with precursors of opioid peptides dermorphin, dermenkephalin, and deltorphins. J. Biol. Chem. 269: 17847-17852
39. Kuchler K., Kreil G. and Sures I. (1989) The genes for the frog skin peptides GLa, xenopsin, levitide and caerulein contain a homologous export exon encoding a signal sequence and part of an amphiphilic peptide. Eur. J. Biochem. 179: 281-285
40. Simmaco M., Mignogna G., Barra D. and Bossa F. (1994) Antimicrobial peptides from skin secretions of Rana esculenta: molecular cloning of cDNAs encoding esculentin and brevinins and isolation of new active peptides. J. Biol. Chem. 269: 11956-11961
41. Amiche M., Seon A. A., Pierre T. N. and Nicolas P. (1999) The dermaseptin precursors: a protein family with a common preproregion and a variable C-terminal antimicrobial domain. FEBS Lett. 456: 352-356
42. Bradbury A. F. and Smyth D. G. (1991) Peptide amidation. Trends Biochem. Sci. 16: 112-115
43. Skerlavaj B., Benincasa M., Risso A., Zanetti M. and Gennaro R. (1999) SMAP-29: a potent antibacterial and antifungal peptide from sheep leukocytes. FEBS Lett. 463: 58-62
44. Oren Z., Lerman J. C., Gudmundsson G. H., Agerberth B. and Shai Y. (1999) Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem. J. 341: 501-513
45. Chen Q., Wade D., Kurosaka K., Wang Z. Y., Oppenheim J. J. and Yang D. (2004) Temporin A and related frog antimicrobial peptides use formyl peptide receptor-like 1 as a receptor to chemoattract phagocytes. J. Immunol. 173: 2652-2659
46. Mangoni M. L., Saugar J. M., Dellisanti M., Barra D., Simmaco M. and Rivas L. (2005) Temporins, small antimicrobial peptides with leishmanicidal activity. J. Biol. Chem. 280: 984-990
47. Ghiselli R., Giacometti A., Cirioni O., Mocchegiani F., Orlando F., Kamysz W. et al. (2002) Temporin A as a prophylactic agent against methicillin sodium-susceptible and methicillin sodium-resistant Staphylococcus epidermidis vascular graft infection. J. Vasc. Surg. 36: 1027-1030
48. Cirioni O., Giacometti A., Ghiselli R., Dell'Acqua G., Gov Y., Kamysz W. et al. (2003) Prophylactic efficacy of topical temporin A and RNAIII-inhibiting peptide in a subcutaneous rat Pouch model of graft infection attributable to staphylococci with intermediate resistance to glycopeptides. Circulation 108: 767-771
49. Wade D., Silberring J., Soliymani R., Heikkinen S., Kilpelainen I., Lankinen H. et al. (2000) Antibacterial activities of temporin A analogs. FEBS Lett. 479: 6-9
50. Giacometti A., Cirioni O., Kamysz W., D'Amato G., Silvestri C., Del Prete M. S. et al. (2005) In vitro activity and killing effect of temporin A on nosocomial isolates of Enterococcus faecalis and interactions with clinically used antibiotics. J. Antimicrob. Chemother. 55: 272-274
51. Rollins-Smith L. A., Carey C., Conlon J. M., Reinert L. K., Doersam J. K., Bergman T. et al. (2003) Activities of temporin family peptides against the chytrid fungus (Batrachochytrium dendrobatidis) associated with global amphibian declines. Antimicrob. Agents. Chemother. 47: 1157-1160
52. Rinaldi A. C., Mangoni M. L., Rufo A., Luzi C., Barra D., Zhao H. et al. (2002) Temporin L: antimicrobial, haemolytic and cytotoxic activities, and effects on membrane permeabilization in lipid vesicles. Biochem. J. 368: 91-100
53. Isaacson T., Soto A., Iwamuro S., Knoop F. C. and Conlon J. M. (2002) Antimicrobial peptides with atypical structural features from the skin of the Japanese brown frog Rana japonica. Peptides 23: 419-425
54. Conlon J. M., Sonnevend A., Davidson C., Demandt A. and Jouenne T. (2005) Host-defense peptides isolated from the skin secretions of the Northern red-legged frog Rana aurora aurora. Dev. Comp. Immunol. 29: 83-90
55. Conlon J. M., Sonnevend A., Patel M., Al-Dhaheri K., Nielsen P. F., Kolodziejek J. et al. (2004) A family of brevinin-2 peptides with potent activity against Pseudomonas aeruginosa from the skin of the Hokkaido frog, Rana pirica. Regul. Pept. 118: 135-141
56. Kim J. B., Iwamuro S., Knoop F. C. and Conlon J. M. (2001) Antimicrobial peptides from the skin of the Japanese mountain brown frog, Rana ornativentris. J. Pept. Res. 58: 349-356
57. Mangoni M. L., Rinaldi A. C., Di Giulio A., Mignogna G., Bozzi A., Barra D. et al. (2000) Structure-function relationships of temporins, small antimicrobial peptides from amphibian skin. Eur. J. Biochem. 267: 1447-1454
58. Chinchar V. G., Bryan L., Silphadaung U., Noga E., Wade D. and Rollins-Smith L. (2004) Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology 323: 268-275
59. Vizioli J. and Salzet M. (2002) Antimicrobial peptides versus parasitic infections? Trends Parasitol. 18: 475-476
60. Feder R., Dagan A. and Mor A. (2000) Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerization on selective cytotoxicity. J. Biol. Chem. 275: 4230-4238
61. Vouldoukis I., Shai Y., Nicolas P. and Mor A. (1996) Broad spectrum antibiotic activity of the skin-PYY. FEBS Lett. 380: 237-240
62. Bera A., Singh S., Nagaraj R. and Vaidya T. (2003) Induction of autophagic cell death in Leishmania donovani by antimicrobial peptides. Mol. Biochem. Parasitol. 127: 23-35
63. Silva P. I. Jr, Daffre S. and Bulet P. (2000) Isolation and characterization of gomesin, an 18-residue cysteine-rich defense peptide from the spider Acanthoscurria gomesiana hemocytes with sequence similarities to horseshoe crab antimicrobial peptides of the tachyplesin family. J. Biol. Chem. 275: 33464-33470
64. Chicharro C., Granata C., Lozano R., Andreu D. and Rivas L. (2001) N-terminal fatty acid substitution increases the leishmanicidal activity of CA(1-7)M(2-9), a cecropin-melittin hybrid peptide. Antimicrob. Agents Chemother. 45: 2441-2449
65. Luque-Ortega J. R., Saugar J. M., Chiva C., Andreu D. and Rivas L. (2003) Identification of new leishmanicidal peptide lead structures by automated real-time monitoring of changes in intracellular ATP. Biochem. J. 375: 221-230
66. Mantyla T., Sirola H., Kansanen E., Korjamo T., Lankinen H., Lappalainen K. et al. (2005) Effect of temporin A modifications on its cytotoxicity and antimicrobial activity. Apmis 113: 497-505
67. Wade D., Flock J. I., Edlund C., Lofving-Arvholm I., Sallberg M., Bergman T. et al. (2002) Antibiotic properties of novel synthetic temporin A analogs and a cecropin A-temporin A hybrid peptide. Protein Pept. Lett. 9: 533-543
68. Ammar B., Perianin A., Mor A., Sarfati G., Tissot M., Nicolas P. et al. (1998) Dermaseptin, a peptide antibiotic, stimulates microbicidal activities of polymorphonuclear leukocytes. Biochem. Biophys. Res. Commun. 247: 870-875
69. Yang D., Chertov O. and Oppenheim J. J. (2001) Participation of mammalian defensins and cathelicidins in anti-microbial immunity: receptors and activities of human defensins and cathelicidin (LL-37). J. Leukoc. Biol. 69: 691-697
70. De Y., Chen Q., Schmidt A. P., Anderson G. M., Wang J. M., Wooters J. et al. (2000) LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192: 1069-1074
71. Kim J. B., Halverson T., Basir Y. J., Dulka J., Knoop F. C., Abel P. W. et al. (2000) Purification and characterization of antimicrobial and vasorelaxant peptides from skin extracts and skin secretions of the North American pig frog Rana grylio. Regul. Pept. 90: 53-60
72. Zhao H. and Kinnunen P. K. (2003) Modulation of the activity of secretory phospholipase A2 by antimicrobial peptides. Antimicrob. Agents Chemother. 47: 965-971
73. Op den Kamp J. A. (1979) Lipid asymmetry in membranes. Annu. Rev. Biochem. 48: 47-71
74. Shai Y. (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66: 236-248
75. Shai Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta. 1462: 55-70
76. Matsuzaki K., Sugishita K. and Miyajima K. (1999) Interactions of an antimicrobial peptide, magainin 2, with lipopolysaccharide-containing liposomes as a model for outer membranes of gram-negative bacteria. FEBS Lett. 449: 221-224
77. Scott M. G., Yan H. and Hancock R. E. (1999) Biological properties of structurally related alpha-helical cationic antimicrobial peptides. Infect. Immun. 67: 2005-2009
78. Mangoni M. L., Papo N., Barra D., Simmaco M., Bozzi A., Di Giulio A. et al. (2004) Effects of the antimicrobial peptide temporin L on cell morphology, membrane permeability and viability of Escherichia coli. Biochem. J. 380: 859-865
79. Oren Z., Hong J. and Shai Y. (1997) A repertoire of novel antibacterial diastereomeric peptides with selective cytolytic activity. J. Biol. Chem. 272: 14643-14649
80. Oren Z. and Shai Y. (1997) Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study. Biochemistry 36: 1826-1835
81. Hancock R. E. (2001) Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1: 156-164
82. Wassef M. K., Fioretti T. B. and Dwyer D. M. (1985) Lipid analyses of isolated surface membranes of Leishmania donovani promastigotes. Lipids 20: 108-115
83. Turco S. J., Hull S. R., Orlandi P. A. Jr, Shepherd S. D., Homans S. W., Dwek R. A. et al. (1987) Structure of the major carbohydrate fragment of the Leishmania donovani lipophosphoglycan. Biochemistry 26: 6233-6238
84. Epand R. M. and Vogel H. J. (1999) Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462: 11-28
85. Park C. B., Kim H. S. and Kim S. C. (1998) Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 244: 253-257
86. Zhao H., Rinaldi A. C., Di Giulio A., Simmaco M. and Kinnunen P. K. (2002) Interactions of the antimicrobial peptides temporins with model biomembranes: comparison of temporins B and L. Biochemistry 41: 4425-4436
87. Ladokhin A. S., Selsted M. E. and White S. H. (1997) Sizing membrane pores in lipid vesicles by leakage of co-encapsulated markers: pore formation by melittin. Biophys. J. 72: 1762-1766
88. Rinaldi A. C., Di Giulio A., Liberi M., Gualtieri G., Oratore A., Bozzi A. et al. (2001) Effects of temporins on molecular dynamics and membrane permeabilization in lipid vesicles. J. Pept. Res. 58: 213-220
89. Zhao H. and Kinnunen P. K. (2002) Binding of the antimicrobial peptide temporin L to liposomes assessed by Trp fluorescence. J. Biol. Chem. 277: 25170-25177
90. Kovacs F., Quine J. and Cross T. A. (1999) Validation of the single-stranded channel conformation of gramicidin A by solid-state NMR Proc. Natl. Acad. Sci. USA 96: 7910-7915
91. Ali M. F., Lips K. R., Knoop F. C. Fritzsch B., Miller C. and Conlon J. M. (2002) Antimicrobial peptides and protease inhibitors in the skin secretions of the crawfish frog, Rana areolata. Biochim. Biophys. Acta 1601: 55-63
92. Conlon J. M., Sonnevend A., Patel M., Davidson C., Nielsen P. F., Pal T. et al. (2003) Isolation of peptides of the brevinin-1 family with potent candidacidal activity from the skin secretions of the frog Rana boylii. J. Pept. Res. 62: 207-213
93. Halverson T., Basir Y. J., Knoop F. C. and Conlon J. M. (2000) Purification and characterization of antimicrobial peptides from the skin of the North American green frog Rana clamitans. Peptides 21: 469-476
94. Ali M. F., Knoop F. C., Vaudry H. and Conlon J. M. (2003) Characterization of novel antimicrobial peptides from the skins of frogs of the Rana esculenta complex. Peptides 24: 955-961
95. Goraya J., Wang Y., Li Z., O'Flaherty M., Knoop F. C., Platz J. E. et al. (2000) Peptides with antimicrobial activity from four different families isolated from the skins of the North American frogs Rana luteiventris, Rana berlandieri and Rana pipiens. Eur. J. Biochem. 267: 894-900
96. Basir Y. J., Knoop F. C., Dulka J. and Conlon J. M. (2000) Multiple antimicrobial peptides and peptides related to bradykinin and neuromedin N isolated from skin secretions of the pickerel frog, Rana palustris. Biochim. Biophys. Acta 1543: 95-105
97. Conlon J. M., Sonnevend A., Patel M., Camasamudram V., Nowotny N., Zilahi E. et al. (2003) A melittin-related peptide from the skin of the Japanese frog, Rana tagoi, with antimicrobial and cytolytic properties. Biochem. Biophys. Res. Commun. 306: 496-500
98. Conlon J. M., Abraham B., Sonnevend A., Jouenne T., Cosette P., Leprince J. et al. (2005) Purification and characterization of antimicrobial peptides from the skin secretions of the carpenter frog Rana virgatipes (Ranidae, Aquarana). Regul. Pept. 131: 38-45
99. Goraya J., Knoop F. C. and Conlon J. M. (1998) Ranatuerins: antimicrobial peptides isolated from the skin of the American bullfrog, Rana catesbeiana. Biochem. Biophys. Res. Commun. 250: 589-592
100. Hultmark D., Engstrom A., Andersson K., Steiner H., Bennich H. and Boman H. G. (1983) Insect immunity: attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO J. 2: 571-576