Cell and Tissue Research

, Volume 343, Issue 1, pp 201–212 | Cite as

The contribution of skin antimicrobial peptides to the system of innate immunity in anurans

Review

Abstract

Cationic peptides with the propensity to adopt an amphipathic α-helical conformation in a membrane-mimetic environment are synthesized in the skins of many species of anurans (frogs and toads). These peptides frequently display cytolytic activities against a range of pathogenic bacteria and fungi consistent with the idea that they play a role in the host's system of innate immunity. However, the importance of the peptides in the survival strategy of the animal is not clearly understood. It is a common misconception that antimicrobial peptides are synthesized in the skins of all anurans. In fact, the species distribution is sporadic suggesting that their production may confer some evolutionary advantage to the organism but is not necessary for survival. Although growth inhibitory activity against the chytrid fungus Batrachochytrium dendrobatidis, responsible for anuran population declines worldwide, has been demonstrated in vitro, the ability of frog skin antimicrobial peptides to protect the animal in the wild appears to be limited and there is no clear correlation between their production by a species and its resistance to fatal chytridiomycosis. The low potency of many frog skin antimicrobial peptides is consistent with the hypothesis that cutaneous symbiotic bacteria may provide the major system of defense against pathogenic microorganisms in the environment with antimicrobial peptides assuming a supplementary role in some species.

Keywords

Antimicrobial peptide Frog skin Host defense Chytridiomycosis Ranavirus Anura 

Notes

Acknowledgement

Work from my own laboratory that is cited in this review was supported by the Faculty Support Grants and Interdisciplinary Grants from the United Arab Emirates University.

References

  1. Abdel-Wahab YHA, Patterson S, Flatt PR, Conlon JM (2010) Brevinin-2-related peptide and its [D4K] analog stimulate insulin release in vitro and improve glucose tolerance in mice fed a high fat diet. Horm Metab Res (in press)Google Scholar
  2. Ali MF, Soto A, Knoop FC, Conlon JM (2001) Antimicrobial peptides isolated from skin secretions of the diploid frog, Xenopus tropicalis (Pipidae). Biochim Biophys Acta 1500:81–89Google Scholar
  3. Amiche M, Ladram A, Nicolas P (2008) A consistent nomenclature of antimicrobial peptides isolated from frogs of the subfamily Phyllomedusinae. Peptides 29:2074–2082PubMedGoogle Scholar
  4. Apponyi MA, Pukala TL, Brinkworth CS, Maselli VM, Bowie JH, Tyler MJ, Booker GW, Wallace JC, Carver JA, Separovic F, Doyle J, Llewellyn LE (2004) Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 25:1035–1054PubMedGoogle Scholar
  5. Ashcroft JW, Zalinger ZB, Bevier CR, Fekete FA (2007) Antimicrobial properties of two purified skin peptides from the mink frog (Rana septentrionalis) against bacteria isolated from the natural habitat. Comp Biochem Physiol C 146:325–330Google Scholar
  6. Banning JL, Weddle AL, Wahl GW 3rd, Simon MA, Lauer A, Walters RL, Harris RN (2008) Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum. Oecologia 156:423–429PubMedGoogle Scholar
  7. Bevier CR, Sonnevend A, Kolodziejek J, Nowotny N, Nielsen PF, Conlon JM (2004) Purification and characterization of antimicrobial peptides from the skin secretions of the mink frog (Rana septentrionalis). Comp Biochem Physiol C 139:31–38Google Scholar
  8. Boman HG (2000) Innate immunity and the normal microflora. Immunol Rev 173:5–16PubMedGoogle Scholar
  9. Bosch J, Rincon PA (2008) Chytridiomycosis-mediated expansion of Bufo bufo in a montane area of central Spain: an indirect effect of the disease. Divers Distrib 14:637–643Google Scholar
  10. Bradley GA, Rosen PC, Sredl MJ, Jones TR, Longcore JE (2002) Chytridiomycosis in native Arizona frogs. J Wildl Dis 38:206–212PubMedGoogle Scholar
  11. Brucker RM, Harris RN, Schwantes CR, Gallaher TN, Flaherty DC, Lam BA, Minbiole KP (2008) Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol 34:1422–1429PubMedGoogle Scholar
  12. Chen Q, Wade D, Kurosaka K, Wang ZY, Oppenheim JJ, Yang D (2004) Temporin A and related frog antimicrobial peptides use formyl peptide receptor-like 1 as a receptor to chemoattract phagocytes. J Immunol 173:2652–2659PubMedGoogle Scholar
  13. Chia BC, Carver JA, Mulhern TD, Bowie JH (1999) The solution structure of uperin 3.6, an antibiotic peptide from the granular dorsal glands of the Australian toadlet, Uperoleia mjobergii. J Pept Res 54:137–145PubMedGoogle Scholar
  14. Chinchar VG, Wang J, Murti G, Carey C, Rollins-Smith L (2001) Inactivation of frog virus 3 and channel catfish virus by esculentin-2P and ranatuerin-2P, two antimicrobial peptides isolated from frog skin. Virology 288:351–357PubMedGoogle Scholar
  15. Chinchar VG, Bryan L, Silphadaung U, Noga E, Wade D, Rollins-Smith L (2004) Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology 323:268–275PubMedGoogle Scholar
  16. Conlon JM (2004) The therapeutic potential of antimicrobial peptides from frog skin. Rev Med Micro 15:17–25Google Scholar
  17. Conlon JM (2008) Reflections on a systematic nomenclature for antimicrobial peptides from the skins of frogs of the family Ranidae. Peptides 29:1815–1819PubMedGoogle Scholar
  18. Conlon JM, Kim JB (2000) A protease inhibitor of the Kunitz family from skin secretions of the tomato frog, Dyscophus guineti (Microhylidae). Biochem Biophys Res Commun 279:961–964PubMedGoogle Scholar
  19. Conlon JM, Sonnevend A, Patel M, Davidson C, Nielsen PF, Pál T, Rollins-Smith LA (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 62:207–213PubMedGoogle Scholar
  20. Conlon JM, Kolodziejek J, Nowotny N (2004a) Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim Biophys Acta 1696:1–14PubMedGoogle Scholar
  21. Conlon JM, Sonnevend A, Davidson C, Smith DD, Nielsen PF (2004b) The ascaphins: a family of antimicrobial peptides from the skin secretions of the most primitive extant frog, Ascaphus truei. Biochem Biophys Res Commun 320:170–175PubMedGoogle Scholar
  22. Conlon JM, Abraham B, Sonnevend A, Jouenne T, Cosette P, Leprince J, Vaudry H, Bevier CR (2005) Purification and characterization of antimicrobial peptides from the skin secretions of the carpenter frog Rana virgatipes (Ranidae, Aquarana). Regul Pept 131:38–45PubMedGoogle Scholar
  23. Conlon JM, Al-Ghafari N, Coquet L, Leprince J, Jouenne T, Vaudry H, Davidson C (2006) Evidence from peptidomic analysis of skin secretions that the red-legged frogs, Rana aurora draytonii and Rana aurora aurora, are distinct species. Peptides 27:1305–1312PubMedGoogle Scholar
  24. Conlon JM, Al-Ghaferi N, Abraham B, Leprince J (2007a) Strategies for transformation of naturally-occurring amphibian antimicrobial peptides into therapeutically valuable anti-infective agents. Methods 42:349–357PubMedGoogle Scholar
  25. Conlon JM, Bevier CR, Coquet L, Leprince J, Jouenne T, Vaudry H, Hossack BR (2007b) Peptidomic analysis of skin secretions supports separate species status for the tailed frogs, Ascaphus truei and Ascaphus montanus. Comp Biochem Physiol 2D:121–125Google Scholar
  26. Conlon JM, Woodhams DC, Raza H, Coquet L, Leprince J, Jouenne T, Vaudry H, Rollins-Smith LA (2007c) Peptides with differential cytolytic activity from skin secretions of the lemur leaf frog Hylomantis lemur (Hylidae: Phyllomedusinae). Toxicon 50:498–506PubMedGoogle Scholar
  27. Conlon JM, Galadari S, Raza H, Condamine E (2008) Design of potent, non-toxic antimicrobial agents based upon the naturally occurring frog skin peptides, ascaphin-8 and peptide XT-7. Chem Biol Drug Des 72:58–64PubMedGoogle Scholar
  28. Conlon JM, Ahmed E, Condamine E (2009a) Antimicrobial properties of brevinin-2-related peptide and its analogs: efficacy against multidrug-resistant Acinetobacter baumannii. Chem Biol Drug Des 74:488–493PubMedGoogle Scholar
  29. Conlon JM, Demandt A, Nielsen PF, Leprince J, Vaudry H, Woodhams DC (2009b) The alyteserins: two families of antimicrobial peptides from the skin secretions of the midwife toad Alytes obstetricans (Alytidae). Peptides 30:1069–1073PubMedGoogle Scholar
  30. Conlon JM, Iwamuro S, King JD (2009c) Dermal cytolytic peptides and the system of innate immunity in anurans. Ann NY Acad Sci 1163:75–82PubMedGoogle Scholar
  31. Conlon JM, Kolodziejek J, Nowotny N (2009d) Antimicrobial peptides from the skins of North American frogs. Biochim Biophys Acta 1788:1556–1563PubMedGoogle Scholar
  32. Conlon JM, Al-Ghaferi N, Ahmed E, Meetani MA, Leprince J, Nielsen PF (2010) Orthologs of magainin, PGLa, procaerulein-derived, and proxenopsin-derived peptides from skin secretions of the octoploid frog Xenopus amieti (Pipidae). Peptides 31:989–994PubMedGoogle Scholar
  33. Cunningham AA, Hyatt AD, Russell P, Bennett PM (2007) Experimental transmission of a ranavirus disease of common toads (Bufo bufo) to common frogs (Rana temporaria). Epidemiol Infect 135:1213–1216PubMedGoogle Scholar
  34. Dasak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150Google Scholar
  35. Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R (1999) Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 5:735–748PubMedGoogle Scholar
  36. Daszak P, Scott DE, Kilpatrick AM, Faggioni C, Gibbons JW, Porter D (2005) Amphibian population declines at Savannah river site are linked to climate not chytridiomycosis. Ecology 86:3232–3237Google Scholar
  37. Davidson C, Benard MF, Shaffer HB, Parker JM, O'Leary C, Conlon JM, Rollins-Smith LA (2007) Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ Sci Technol 41:1771–1776PubMedGoogle Scholar
  38. Diamond G, Beckloff N, Weinberg A, Kisich KO (2009) The roles of antimicrobial peptides in innate host defense. Curr Pharm Des 15:2377–2392PubMedGoogle Scholar
  39. Fellers GM, Green DE, Longcore JE (2001) Oral chytridiomycosis in the mountain yellow-legged frog (Rana muscosa). Copeia 2001:945–953Google Scholar
  40. Fisher MC, Garner TW, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310PubMedGoogle Scholar
  41. Frost DR (2010) Amphibian Species of the World: an Online Reference. Version 5.4. Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.php. American Museum of Natural History, New York, USA
  42. Garcia TS, Romansic JM, Blaustein AR (2006) Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatidis. Dis Aquat Organ 72:163–169PubMedGoogle Scholar
  43. Garner TW, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol Lett 2:455–459PubMedGoogle Scholar
  44. Goraya J, Wang Y, Li Z, O’Flaherty M, Knoop FC, Platz JE, Conlon JM (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 267:894–900PubMedGoogle Scholar
  45. Hale SF, Rosen PC, Jarchow JL, Bradley GA (2005) Effects of the chytrid fungus on the Tarahumara frog (Rana tarahumarae) in Arizona and Sonora, Mexico. USDA Forest Service Proc 407–411Google Scholar
  46. Harris RN, Lauer A, Simon MA, Banning JL, Alford RA (2009a) Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Dis Aquat Organ 83:11–16PubMedGoogle Scholar
  47. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT, Minbiole KP (2009b) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818–824PubMedGoogle Scholar
  48. Hayes MP, Rombough CJ, Padgett-Flohr G, Hallock LA, Johnson JE, Wagner RS, Engler JD (2009) Amphibian chytridiomycosis in the Oregon spotted frog (Rana pretiosa) in Washington State, USA. Northwest Nat 90:148–151Google Scholar
  49. Hossack BR, Adams MJ, Campbell Grant EH, Pearl CA, Bettaso JB, Barichivich WJ, Lowe WH, True K, Ware JL, Corn PS (2010) Low prevalence of chytrid fungus (Batrachochytrium dendrobatidis) in amphibians of U.S. headwater streams. J Herpetol 44:253–260Google Scholar
  50. James TY, Litvintseva AP, Vilgalys R, Morgan JA, Taylor JW, Fisher MC, Berger L, Weldon C, du Preez L, Longcore JE (2009) Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog 5:e1000458PubMedGoogle Scholar
  51. Jancovich JK, Davidson EW, Parameswaran N, Mao J, Chinchar VG, Collins JP, Jacobs BL, Storfer A (2005) Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Mol Ecol 14:213–224PubMedGoogle Scholar
  52. Kawasaki H, Isaacson T, Iwamuro S, Conlon JM (2003) A protein with antimicrobial activity in the skin of Schlegel’s green tree frog Rhacophorus schlegelii (Rhacophoridae) identified as histone H2B. Biochem Biophys Res Commun 312:1082–1086PubMedGoogle Scholar
  53. Kawasaki H, Iwamuro S, Goto Y, Nielsen PF, Conlon JM (2008) Characterization of a hemolytic protein, identified as histone H4, from the skin of the Japanese tree frog Hyla japonica (Hylidae). Comp Biochem Physiol B 149:120–125PubMedGoogle Scholar
  54. Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25:109–118PubMedGoogle Scholar
  55. Kim JB, Halverson T, Basir YJ, Dulka J, Knoop FC, Abel PW, Conlon JM (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 90:53–60PubMedGoogle Scholar
  56. Lips K, Reeve JD, Witters LR (2003) Ecological traits predicting amphibian population declines in Central America. Conserv Biol 17:1078–1088Google Scholar
  57. Mangoni ML, Rinaldi AC, Di Giulio A, Mignogna G, Bozzi A, Barra D, Simmaco M (2000) Structure-function relationships of temporins, small antimicrobial peptides from amphibian skin. Eur J Biochem 267:1447–1454PubMedGoogle Scholar
  58. Mattute B, Knoop FC, Conlon JM (2000) Kassinatuerin-1: a peptide with broad-spectrum antimicrobial activity isolated from the skin of the hyperoliid frog, Kassina senegalensis. Biochem Biophys Res Commun 268:433–436PubMedGoogle Scholar
  59. Mazzoni R (2003) Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade. Emerg Infect Dis 9:995–998PubMedGoogle Scholar
  60. Morgan JA, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, Bingham RE, Parker JM, Longcore JE, Moritz C, Briggs CJ, Taylor JW (2007) Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proc Natl Acad Sci USA 104:13845–13850PubMedGoogle Scholar
  61. Morikawa N, Hagiwara K, Nakajima T (1992) Brevinin-1 and -2, unique antimicrobial peptides from the skin of the frog, Rana brevipoda porsa. Biochem Biophys Res Commun 189:184–190PubMedGoogle Scholar
  62. Murphy PJ, St-Hilaire S, Bruer S, Corn PS, Peterson CR (2009) Distribution and pathogenicity of Batrachochytrium dendrobatidis in boreal toads from the Grand Teton area of western Wyoming. EcoHealth 6:109–120PubMedGoogle Scholar
  63. Muths E, Corn PS, Pessier AP, Green DE (2003) Evidence for disease-related amphibian decline in Colorado. Biol Conserv 110:357–365Google Scholar
  64. Nascimento AC, Zanotta LC, Kyaw CM, Schwartz EN, Schwartz CA, Sebben A, Sousa MV, Fontes W, Castro MS (2004) Ocellatins: new antimicrobial peptides from the skin secretion of the South American frog Leptodactylus ocellatus (Anura: Leptodactylidae). Protein J 23:501–508PubMedGoogle Scholar
  65. Nicolas P, El Amri C (2009) The dermaseptin superfamily: a gene-based combinatorial library of antimicrobial peptides. Biochim Biophys Acta 1788:1537–1550PubMedGoogle Scholar
  66. Nieto NC, Camann MA, Foley JE, Reiss JO (2007) Disease associated with integumentary and cloacal parasites in tadpoles of northern red-legged frog Rana aurora aurora. Dis Aquat Organ 78:61–71PubMedGoogle Scholar
  67. Ohnuma A, Conlon JM, Iwamuro S (2010) Differential expression of genes encoding preprobrevinin-2, prepropalustrin-2, and preproranatuerin-2 in developing larvae and adult tissues of the mountain brown frog Rana ornativentris. Comp Biochem Physiol C 151:122–130Google Scholar
  68. Olson L 3rd, Soto AM, Knoop FC, Conlon JM (2001) Pseudin-2: an antimicrobial peptide with low hemolytic activity from the skin of the paradoxical frog. Biochem Biophys Res Commun 288:1001–1005PubMedGoogle Scholar
  69. Ouellet M, Mikaelian I, Pauli BD, Rodrigue J (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conserv Biol 19:1431–1440Google Scholar
  70. Padgett-Flohr GE, Goble ME (2007) Evaluation of tadpole mouthpart depigmentation as a diagnostic test for infection by Batrachochytrium dendrobatidis for four California anurans. J Wildl Dis 43:690–699PubMedGoogle Scholar
  71. Padgett-Flohr GE, Hopkins RL 2nd (2009) Batrachochytrium dendrobatidis, a novel pathogen approaching endemism in central California. Dis Aquat Organ 83:1–9PubMedGoogle Scholar
  72. Pál T, Sonnevend A, Galadari S, Conlon JM (2005) Design of potent, non-toxic antimicrobial agents based upon the structure of the frog skin peptide, pseudin-2. Regul Pept 129:85–91PubMedGoogle Scholar
  73. Parker JM, Mikaelian I, Hahn N, Diggs HE (2002) Clinical diagnosis and treatment of epidermal chytridiomycosis in African clawed frogs (Xenopus tropicalis). Comp Med 52:265–268PubMedGoogle Scholar
  74. Pearl CA, Bull EL, Green DE, Bowerman J, Adams MJ, Hyatt A, Wente WH (2007) Occurrence of the amphibian pathogen Batrachochytrium dendrobatidis in the Pacific northwest. J Herpetol 41:145–149Google Scholar
  75. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15PubMedGoogle Scholar
  76. Powers JP, Hancock RE (2003) The relationship between peptide structure and antibacterial activity. Peptides 24:1681–1691PubMedGoogle Scholar
  77. Pukala TL, Bowie JH, Maselli VM, Musgrave IF, Tyler MJ (2006) Host-defence peptides from the glandular secretions of amphibians: structure and activity. Nat Prod Rep 23:368–393PubMedGoogle Scholar
  78. Rachowicz LJ, Vredenburg VT (2004) Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis Aquat Org 61:75–83PubMedGoogle Scholar
  79. Rachowicz LJ, Knapp RA, Morgan JA, Stice MJ, Vredenburg VT, Parker JM, Briggs CJ (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683PubMedGoogle Scholar
  80. Rollins-Smith LA, Conlon JM (2005) Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev Comp Immunol 29:589–598PubMedGoogle Scholar
  81. Rollins-Smith LA, Carey C, Longcore J, Doersam JK, Boutte A, Bruzgal JE, Conlon JM (2002a) Activity of antimicrobial skin peptides from Ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev Comp Immunol 26:471–479PubMedGoogle Scholar
  82. Rollins-Smith LA, Reinert LK, Miera V, Conlon JM (2002b) Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem Biophys Res Commun 297:361–367PubMedGoogle Scholar
  83. Rollins-Smith LA, Carey C, Conlon JM, Reinert LK, Doersam JK, Bergman T, Silberring J, Lankinen H, Wade D (2003) Activities of temporin family peptides against the chytrid fungus (Batrachochytrium dendrobatidis) associated with global amphibian declines. Antimicrob Agents Chemother 47:1157–1160PubMedGoogle Scholar
  84. Rollins-Smith LA, Woodhams DC, Reinert LK, Vredenburg VT, Briggs CJ, Nielsen PF, Conlon JM (2006) Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev Comp Immunol 30:831–842PubMedGoogle Scholar
  85. Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC, Livo LJ, Carey C (2009) Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front Biosci (Schol Ed) 1:68–91Google Scholar
  86. Rosenblum EB, Poorten TJ, Settles M, Murdoch GK, Robert J, Maddox N, Eisen MB (2009) Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS One 4:e6494Google Scholar
  87. Rosenfeld Y, Barra D, Simmaco M, Shai Y, Mangoni ML (2006) A synergism between temporins toward Gram-negative bacteria overcomes resistance imposed by the lipopolysaccharide protective layer. J Biol Chem 281:28565–28574PubMedGoogle Scholar
  88. Simmaco M, Mignogna G, Canofeni S, Miele R, Magnoni ML, Barra D (1996) Temporins, antimicrobial peptides from the European red frog Rana temporaria. Eur J Biochem 242:788–792PubMedGoogle Scholar
  89. Simmaco M, Kreil G, Barra D (2009) Bombinins, antimicrobial peptides from Bombina species. Biochim Biophys Acta 1788:1551–1555PubMedGoogle Scholar
  90. Stice MJ, Briggs CJ (2010) Immunization is ineffective at preventing infection and mortality due to the amphibian chytrid fungus Batrachochytrium dendrobatidis. J Wildl Dis 46:70–77PubMedGoogle Scholar
  91. Tennessen JA, Blouin MS (2007) Selection for antimicrobial peptide diversity in frogs leads to gene duplication and low allelic variation. J Mol Evol 65:605–615PubMedGoogle Scholar
  92. Tennessen JA, Woodhams DC, Chaurand P, Reinert LK, Billheimer D, Shyr Y, Caprioli RM, Blouin MS, Rollins-Smith LA (2009) Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Dev Comp Immunol 33:1247–1257PubMedGoogle Scholar
  93. VanCompernolle SE, Taylor RJ, Oswald-Richter K, Jiang J, Youree BE, Bowie JH, Tyler MJ, Conlon JM, Wade D, Aiken C, Dermody TS, Kewal Ramani VN, Rollins-Smith LA, Unutmaz D (2005) Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J Virol 79:11598–11606PubMedGoogle Scholar
  94. Voordouw MJ, Adama D, Houston B, Govindarajulu P, Robinson J (2010) Prevalence of the pathogenic chytrid fungus, Batrachochytrium dendrobatidis, in an endangered population of northern leopard frogs, Rana pipiens. BMC Ecol 10:6PubMedGoogle Scholar
  95. Voyles J, Berger L, Young S, Speare R, Webb R, Warner J, Rudd D, Campbell R, Skerratt LF (2007) Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Dis Aquat Organ 77:113–118PubMedGoogle Scholar
  96. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–585PubMedGoogle Scholar
  97. Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci USA 105(Suppl 1):11466–11473PubMedGoogle Scholar
  98. Waldman B, van de Wolfshaar KE, Klena JD, Andjic V, Bishop PJ, de Norman RJB (2001) Chytridiomycosis in new Zealand frogs. Surveillance 28(3):9–11Google Scholar
  99. Weldon C, du Preez LH, Hyatt AD, Muller R, Spears R (2004) Origin of the amphibian chytrid fungus. Emerg Infect Dis 10:2100–2105PubMedGoogle Scholar
  100. Woodhams DC, Rollins-Smith LA, Carey C, Reinert L, Tyler MJ, Alford RA (2006) Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146:531–540PubMedGoogle Scholar
  101. Woodhams DC, Ardipraja K, Alford RA, Marantelli G, Reinert LK, Rollins-Smith LA (2007a) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv 10:409–417Google Scholar
  102. Woodhams DC, Vredenburg VT, Simon M-A, Billheimer D, Shakhtour B, Shyr Y, Briggs CJ, Rollins-Smith LA, Harris RN (2007b) Symbiotic bacteria contribute to innate immune defences of the threatened mountain yellow-legged frog, Rana muscosa. Biol Conserv 138:390–398Google Scholar
  103. Yasin B, Pang M, Turner JS, Cho Y, Dinh NN, Waring AJ, Lehrer RI, Wagar EA (2000) Evaluation of the inactivation of infectious Herpes simplex virus by host-defense peptides. Eur J Clin Microbiol Infect Dis 19:187–194PubMedGoogle Scholar
  104. Yeaman MR, Yount NY (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55:27–55PubMedGoogle Scholar
  105. Zaiou M (2007) Multifunctional antimicrobial peptides: therapeutic targets in several human diseases. J Mol Med 85:317–329PubMedGoogle Scholar
  106. Zasloff M (1987) Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms and partial cDNA sequence of a precursor. Proc Natl Acad Sci USA 84:5449–5453PubMedGoogle Scholar
  107. Zhao H, Kinnunen PK (2003) Modulation of the activity of secretory phospholipase A2 by antimicrobial peptides. Antimicrob Agents Chemother 47:965–971PubMedGoogle Scholar

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© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Faculty of Medicine and Health Sciences, Department of BiochemistryUnited Arab Emirates UniversityAl-AinUnited Arab Emirates

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