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Antimicrobial peptides from Phyllomedusa frogs: from biomolecular diversity to potential nanotechnologic medical applications

Abstract

Screening for new bioactive peptides in South American anurans has been pioneered in frogs of the genus Phyllomedusa. All frogs of this genus have venomous skin secretions, i.e., a complex mixture of bioactive peptides against potential predators and pathogens that presumably evolved in a scenario of predator–prey interaction and defense against microbial invasion. For every new anuran species studied new peptides are found, with homologies to hormones, neurotransmitters, antimicrobials, and several other peptides with unknown biological activity. From Vittorio Erspamer findings, this genus has been reported as a “treasure store” of bioactive peptides, and several groups focus their research on these species. From 1966 to 2009, more than 200 peptide sequences from different Phyllomedusa species were deposited in UniProt and other databases. During the last decade, the emergence of high-throughput molecular technologies involving de novo peptide sequencing via tandem mass spectrometry, cDNA cloning, pharmacological screening, and surface plasmon resonance applied to peptide discovery, led to fast structural data acquisition and the generation of peptide molecular libraries. Research groups on bioactive peptides in Brazil using these new technologies, accounted for the exponential increase of new molecules described in the last decade, much higher than in any previous decades. Recently, these secretions were also reported as a rich source of multiple antimicrobial peptides effective against multidrug resistant strains of bacteria, fungi, protozoa, and virus, providing instructive lessons for the development of new and more efficient nanotechnological-based therapies for infectious diseases treatment. Therefore, novel drugs arising from the identification and analysis of bioactive peptides from South American anuran biodiversity have a promising future role on nanobiotechnology.

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Abbreviations

ADR:

Adenoregulin

AFM:

Atomic force microscopy

AMP:

Antimicrobial peptide

CD:

Circular dichroism

DRP:

Dermaseptin related peptide

DRS:

Dermaseptin

DRT:

Dermatoxin

FSAP:

Frog skin active peptide

FTIR:

Fourier-transformed infrared spectroscopy

HIV-1:

Human immunodeficiency virus 1

HSV-1:

Herpes simplex virus 1

MALDI:

Matrix assisted laser desorption ionization

NMR:

Nuclear magnetic resonance

NPY:

Neuropeptide Y

PLS:

Phylloseptin

PLX:

Phylloxin

PM:

Plasmatic membrane

PTC:

Plasticin

PYY:

Polypeptide YY

SPYY:

Skin polypeptide YY

UniProt:

Universal protein resource

References

  1. Abu-Raddad LJ, Patnaik P, Kublin JG (2006) Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314:1603–1606

    CAS  PubMed  Article  Google Scholar 

  2. Amiche M, Ducancel F, Lajeunesse E, Boulain JC, Menez A, Nicolas P (1993) Molecular cloning of a cDNA encoding the precursor of adenoregulin from frog skin. Relationships with the vertebrate defensive peptides, dermaseptins. Biochem Biophys Res Commun 191:983–990

    CAS  PubMed  Article  Google Scholar 

  3. Amiche M, Ducancel F, Mor A, Boulain JC, Menez A, Nicolas P (1994) Precursors of vertebrate peptide antibiotics dermaseptin b and adenoreguhn have extensive sequence identities with precursors of opioid peptides dermorphin, dermenkephalin, and deltorphins. J Biol Chem 269:17847–17852

    CAS  PubMed  Google Scholar 

  4. Amiche M, Delfour A, Nicolas P (1998) Opioid peptides from frog skin. EXS 85:57–71

    Google Scholar 

  5. Amiche M, Seon AA, Pierre TN, 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

    CAS  PubMed  Article  Google Scholar 

  6. Amiche M, Seon AA, Wroblewski H, Nicolas P (2000) Isolation of dermatoxin from frog skin, an antibacterial peptide encoded by a novel member of the dermaseptin genes family. Eur J Biochem 267:4583–4592

    CAS  PubMed  Article  Google Scholar 

  7. Amiche M, Ladram A, Nicolas P (2008) A consistent nomenclature of antimicrobial peptides isolated from frogs of the subfamily Phyllomedusinae. Peptides 29:2074–2082

    CAS  PubMed  Article  Google Scholar 

  8. Ammar B, Perianin A, Mor A, Sarfat G, Tissot M, Nicolas P, Giroud JP, Roch-Arveiller M (1998) Dermaseptin, a peptide antibiotic, stimulates microbicidal activities of polymorphonuclear leukocytes. Biochem Biophys Res Commun 247:870–875

    CAS  PubMed  Article  Google Scholar 

  9. Anastasi A, Falconieri Erspamer G (1970) Occurrence of phyllomedusin, a physalaemin-like decapeptide, in the skin of Phyllomedusa bicolor. Experientia 26:866–867

    CAS  PubMed  Article  Google Scholar 

  10. Anastasi A, Bertaccini G, Erspamer V (1966) Pharmacological data on phyllokinin (bradykinyl-isoleucyl-tyrosine o-sulphate) and bradykinyl-isoleucyl-tyrosine. Br J Pharmacol 27:479–485

    CAS  Google Scholar 

  11. Anastasi A, Bertaccini G, Cei JM, De Caro G, Erspamer V, Impicciatore M (1969) Structure and pharmacological actions of phyllocaerulein, a caerulein-like nonapeptide: its occurrence in extracts of the skin of Phyllomedusa sauvagei and related Phyllomedusa species. Br J Pharmacol 37:198–206

    CAS  PubMed  Google Scholar 

  12. Andrä J, Monreal D, Martinez de Tejada G, Olak C, Brezesinski G, Sanchez Gomez S, Goldmann T, Bartels R, Brandenburg K, Moriyon I (2007) Rationale for the design of shortened derivatives of the NK-lysin-derived antimicrobial peptide NK-2 with improved activity against Gram-negative pathogens. J Biol Chem 282:14719–14728

    PubMed  Article  Google Scholar 

  13. Andreu D, Rivas L (1998) Animal antimicrobial peptides: an overview. Biopolymers 47:415–433

    CAS  PubMed  Article  Google Scholar 

  14. Barra D, Simmaco M (1995) Amphibian skin: a promising resource for antimicrobial peptides. Trends Biotechnol 13:205–209

    CAS  PubMed  Article  Google Scholar 

  15. Barra D, Falconieri Erspamer G, Simmaco M, Bossa F, Melchiorri P, Erspamer V (1985) Rohdei-litorin: a new peptide from the skin of Plyllomedusa rohdei. FEBS Lett 182:53–56

    CAS  PubMed  Article  Google Scholar 

  16. Barra D, Mignogna G, Simmaco M, Pucci P, Severini C, Falconieri Erspamer G, Negri L, Erspamer V (1994) [D-Leu2]deltorphin, a 17 amino acid opioid peptide from the skin of the Brazilian hylid frog, Phyllomedusa burmeisteri. Peptides 15:199–202

    CAS  PubMed  Article  Google Scholar 

  17. Batista CVF, Rosendo da Silva L, Sebben A, Scaloni A, Ferrara L, Paiva GR, Olamendi-Portugal T, Possani LD, Bloch C Jr (1999) Antimicrobial peptides from the Brazilian frog Phyllomedusa distincta. Peptides 20:679–686

    CAS  PubMed  Article  Google Scholar 

  18. Batista CVF, Scaloni A, Rigden DJ, Silva LR, Romero AR, Dukor R, Sebben A, Talamo F, Bloch C Jr (2001) A novel heterodimeric antimicrobial peptide from the tree-frog Phyllomedusa distincta. FEBS Lett 494:85–89

    CAS  PubMed  Article  Google Scholar 

  19. Bechinger B (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by solid-state NMR spectroscopy. Biochim Biophys Acta 1462:157–183

    CAS  PubMed  Article  Google Scholar 

  20. Bechinger B (2004) Membrane-lytic peptides. Crit Rev Plant Sci 23:271–292

    CAS  Article  Google Scholar 

  21. Bechinger B (2005) Detergent-like properties of magainin antibiotic peptides: a 31P solid-state NMR study. Biochim Biophys Acta 1712:101–108

    CAS  PubMed  Article  Google Scholar 

  22. Bechinger B, Lohner K (2006) Detergent-like action of linear cationic membrane-active antibiotic peptides. Biochim Biophys Acta 1758:1529–1539

    CAS  PubMed  Article  Google Scholar 

  23. Bechinger B, Skladnev DA, Ogrel A, Li X, Rogozhkina EV, Ovchinnikova TV, O’Neil JD, Raap J (2001) 15N and 31P solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes. Biochemistry 40:9428–9437

    CAS  PubMed  Article  Google Scholar 

  24. Belaid A, Aouni M, Khelifa R, Trabelsi A, Jemmali M, Hani K (2002) In vitro antiviral activity of dermaseptins against herpes simplex virus type 1. J Med Virol 66:229–234

    CAS  PubMed  Article  Google Scholar 

  25. Béven L, Helluin O, Molle G, Duclohier H, Wróblewski H (1999) Correlation between anti-bacterial activity and pore sizes of two classes of voltage-dependent channel-forming peptides. Biochim Biophys Acta 1421:53–63

    PubMed  Article  Google Scholar 

  26. Bevins CL, Zasloff M (1990) Peptides from frog skin. Annu Rev Biochem 59:395–414

    CAS  PubMed  Article  Google Scholar 

  27. Bisht GS, Rawat DS, Kumar A, Kumar R, Pasha S (2007) Antimicrobial activity of rationally designed amino terminal modified peptides. Bioorg Med Chem Lett 17:4343–4346

    CAS  PubMed  Article  Google Scholar 

  28. Blaylock LA, Ruibal R, Platt-Aloia K (1976) Skin structure and wiping behaviour of phyllomedusine frogs. Copeia 1976:283–295

    Article  Google Scholar 

  29. Boman HGJ (2003) Effect of peptide length on the interaction between consensus peptides and DOPC/DOPA bilayers. Intern Med 254:197–215

    CAS  Article  Google Scholar 

  30. Brand GD, Leite JRSA, Silva LP, Albuquerque S, Prates MV, Azevedo RB, Carregaro V, Silva JS, Sá VC, Brandao RA, Bloch C Jr (2002) Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta: anti-Trypanosoma cruzi activity without cytotoxicity to mammalian cells. J Biol Chem 277:49332–49340

    CAS  PubMed  Article  Google Scholar 

  31. Brand GD, Krause FC, Silva LP, Leite JRSA, Melo JAT, Prates MV, Pesquero JB, Santos EL, Nakaie CR, Costa-Neto CM, Bloch C Jr (2006a) Bradykinin-related peptides from Phyllomedusa hypochondrialis. Peptides 27:2137–2146

    CAS  PubMed  Article  Google Scholar 

  32. Brand GD, Leite JRSA, Mandel SMS, Mesquita DA, Silva LP, Prates MV, Barbosa EA, Vinecky F, Martins GR, Galasso JH, Kuckelhaus SAS, Sampaio RNR, Furtado JR, Andrade AC, Bloch C Jr (2006b) Novel dermaseptins from Phyllomedusa hypochondrialis (Amphibia). Biochem Biophys Res Commun 347:739–746

    CAS  PubMed  Article  Google Scholar 

  33. Broccardo M, Erspamer V, Falconieri Erspamer G, Improta G, Linaii G, Melchiorri P, Montecucchi PC (1981) Pharmacological data on dermorphins. A new class of potent opioid peptides from amphibian skin. Br J Pharmacol 73:625–631

    CAS  PubMed  Google Scholar 

  34. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250

    CAS  PubMed  Article  Google Scholar 

  35. Bruston F, Lacombe C, Zimmermann K, Piesse C, Nicolas P, El Amri C (2007) Structural malleability of plasticins: preorganized conformations in solution and relevance for antimicrobial activity. Biopolymers 86:42–56

    CAS  PubMed  Article  Google Scholar 

  36. Calderon LA, Silva-Jardim I, Zuliani JP, Silva AA, Ciancaglini P, Silva LHP, Stábeli RG (2009a) Amazonian biodiversity: a view of drug development for leishmaniasis and malaria. J Braz Chem Soc 20:1011–1023

    CAS  Google Scholar 

  37. Calderon LA, Messias MR, Serrano ROP, Zaqueo KD, Souza ED, Nienow SS, Cardozo-Filho JL, Diniz-Sousa R, Delaix-Zaqueo K, Stabeli RG (2009b) Amphibia, Anura, Hylidae, Phyllomedusinae, Phyllomedusa azurea: distribution extension and geographic distribution map. Check List 5(2):317–319

    Google Scholar 

  38. Caramaschi U (2006) Redefinição do grupo de Phyllomedusa hypochondrialis, com redescrição de P. megacephala (Miranda-Ribeiro, 1926), revalidação de P. azurea Cope, 1862 e descrição de uma nova espécie (Amphibia, Anura, Hylidae). Arq Mus Nac 64:159–179

    Google Scholar 

  39. Castanho LM, De Luca IMS (2001) Moulting behavior in leaf-frogs of the genus Phyllomedusa (Anura: Hylidae). Zool Anz 240:3–6

    Article  Google Scholar 

  40. Castiglione-Morelli MA, Cristinziano P, Pepe A, Temussi PA (2005) Conformation–activity relationship of a novel peptide antibiotic: structural characterization of dermaseptin DS 01 in media that mimic the membrane environment. Biopolymers 80:688–696

    CAS  PubMed  Article  Google Scholar 

  41. Cerdá-Reverter JM, Larhammar D (2000) Neuropeptide Y family of peptides: structure, anatomical expression, function, and molecular evolution. Biochem Cell Biol 78:371–392

    PubMed  Article  Google Scholar 

  42. Chan DI, Prenner EJ, Vogel HJ (2006) Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim Biophys Acta 1758:1184–1202

    CAS  PubMed  Article  Google Scholar 

  43. Charpentier S, Amiche M, Mester J, Vouille V, Le Caer JP, Nicolas P, Delfour A (1998) Structure, synthesis, and molecular cloning of dermaseptins B, a family of skin peptide antibiotics. J Biol Chem 273:14690–14697

    CAS  PubMed  Article  Google Scholar 

  44. Chen T, Shaw C (2003) Cloning of the (Thr6)-phyllokinin precursor from Phyllomedusa sauvagei skin confirms a non-consensus tyrosine O-sulfation motif. Peptides 24:1123–1130

    CAS  PubMed  Article  Google Scholar 

  45. Chen T, Tang L, Shaw C (2003a) Identification of three novel Phyllomedusa sauvagei Dermaseptins (sVI-sVIII) by cloning from a skin secretion delivered cDNA library. Regul Pept 116:139–146

    CAS  PubMed  Article  Google Scholar 

  46. Chen T, Farragher S, Bjourson AJ, Orr DF, Rao P, Shaw C (2003b) Granular gland transcriptomes in stimulated amphibian skin secretions. Biochem J 371:125–130

    CAS  PubMed  Article  Google Scholar 

  47. Chen T, Walker B, Zhou M, Shaw C (2005a) Dermatoxin and Phylloxin from the waxy monkey frog, Phyllomedusa sauvagei: cloning of precursor cDNAs and structural characterization from lyophilized skin secretion. Regul Pept 129:103–108

    CAS  PubMed  Article  Google Scholar 

  48. Chen TB, Gagliardo R, Walker B, Zhou M, Shaw C (2005b) Partial structure of the phylloxin gene from the giant monkey frog Phyllomedusa bicolor: parallel cloning of precursor cDNA and genomic DNA from lyophilized skin secretion. Peptides 26:2624–2628

    CAS  PubMed  Article  Google Scholar 

  49. Chen TB, Zhou M, Gagliardo R, Walker B, Shaw C (2006) Elements of the granular gland peptidome and transcriptome persist in air-dried skin of the South American orange-legged leaf frog, Phyllomedusa hypochondrialis. Peptides 27:2129–2136

    CAS  PubMed  Article  Google Scholar 

  50. Coloma LA (2009) Anfibios de Ecuador 2005–2009. 2.0 Museo de Zoología, Pontificia Universidad Católica del Ecuador. Quito, Ecuador. http://www.puce.edu.ec/zoologia/vertebrados/amphibiawebec/anfibiosecuador/index.htm. Accessed 10 Jan 2010

  51. Conceição K, Konno K, Richardson M, Antonazzi MM, Jared C, Daffre S, Camargo ACM, Pimenta DC (2006) Isolation and biochemical characterization of peptides presenting antimicrobial activity from the skin of Phyllomedusa hypochondrialis. Peptides 27:3092–3099

    PubMed  Article  CAS  Google Scholar 

  52. Conceição K, Konno K, Melo RL, Antonazzi MM, Jared C, Sciani JM, Conceiçã IM, Prezoto BC, Camargo ACM, Pimenta DC (2007) Isolation and characterization of a novel bradykinin potentiating peptide (BPP) from the skin secretion. Peptides 28:515–523

    PubMed  Article  CAS  Google Scholar 

  53. Conceição K, Bruni FM, Sciani JM, Konno K, Melo RL, Antoniazzi MM, Jared C, Lopes-Ferreira M, Pimenta DC (2009) Identification of bradykinin-related peptides from Phyllomedusa nordestina skin secretion using electrospray ionization tandem mass spectrometry after a single-step liquid chromatography. J Venom Anim Toxins Incl Trop Dis 15:633–652

    Article  CAS  Google Scholar 

  54. Conlon JM, Chartrel N, Vaudry H (1992) Primary structure of frog PYY: implications for the molecular evolution of the pancreatic polypeptide family. Peptides 13:145–149

    CAS  PubMed  Article  Google Scholar 

  55. Dagan A, Efron L, Gaidukov L, Mor A, Ginsburg H (2002) In vitro antiplasmodium effects of dermaseptins S4 derivatives. Antimicrob Agents Chemother 46:1059–1066

    CAS  PubMed  Article  Google Scholar 

  56. Dalla SM, Cirioni O, Vitale RM, Renzone G, Coraiola M, Giacometti A, Potrich C, Baroni E, Guella G, Sanseverino M, De Luca S, Scalise G, Amodeo P, Scaloni A (2008) Structural features of distinctin affecting peptide biological and biochemical properties. Biochemistry 47:7888–7899

    Article  CAS  Google Scholar 

  57. Daly JW, Caceres J, Moni RW, Gusovsky F, Moos M Jr, Seamon KB, Milton K, Myers CW (1992) Frog secretions and hunting magic in the upper Amazon: identification of a peptide that interacts with an adenosine receptor. Proc Natl Acad Sci USA 89:10960–10963

    CAS  PubMed  Article  Google Scholar 

  58. Dathe M, Wieprecht T (1999) Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim Biophys Acta 1462:71–87

    CAS  PubMed  Article  Google Scholar 

  59. Delfino G (1991) Ultrastructural aspects of venom secretion in anuran cutaneous glands. In: Tu AT, Dekker M (eds) Reptile venoms and toxins. Handbook of natural toxins. Marcel Dekker Inc., New York, pp 777–802

  60. Delfino G, Brizzi R, Alvarez BB, Kracke-Berndorff R (1998) Serous cutaneous glands in Phyllomedusa hypochondrialis (Anura, Hylidae): secretory patterns during ontogenesis. Tissue Cell 30:30–40

    CAS  PubMed  Article  Google Scholar 

  61. Edwards P (2007) Combinatorial approaches to combating multidrug resistance. Drug Discov Today 12:786–787

    Article  Google Scholar 

  62. El Amri C, Lacombe C, Zimmerman K, Ladram A, Amiche M, Nicolas P, Bruston F (2006) The plasticins: membrane adsorption, lipid disorders, and biological activity. Biochemistry 45:14285–14297

    CAS  PubMed  Article  Google Scholar 

  63. Erspamer V (1992) The opioid peptides of the amphibian skin. Int J Dev Neurosci 10:3–30

    CAS  PubMed  Article  Google Scholar 

  64. Erspamer V, Bertaccini G, Cei JM (1962) Occurrence of an eledoisin-like polypeptide (physalaemin) in skin extracts of Physalaemus fuscumaculatus. Experientia 18:562–563

    CAS  Article  Google Scholar 

  65. Erspamer V, Melchiorri P, Broccardo M, Erspamer GF, Falaschi P, Improota G, Negri L, Renda T (1981) The brain–gut–skin triangle: new peptides. Peptides 2:7–16

    CAS  PubMed  Article  Google Scholar 

  66. Erspamer V, Melchiorri P, Falconieri Erspamer G, Montecucchi PC, De Castiglione R (1985) Phyllomedusa skin: a huge factory and store-house of a variety of active peptides. Peptides 6:7–12

    CAS  PubMed  Article  Google Scholar 

  67. Erspamer V, Melchiorri P, Falconieri-Erspamer G, Negri L, Corsi R, Severini C, Barra D, Simmaco M, Kreil G (1989) Deltorphins: a family of naturally occurring peptides with high affinity and selectivity for delta opioid binding sites. Proc Natl Acad Sci USA 86:5188–5192

    CAS  PubMed  Article  Google Scholar 

  68. Faivovich J, Haddad CFB, Garcia PCA, Frost DR, Campbell JA, Wheller WC (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bull Am Mus Nat Hist 294:1–240

    Article  Google Scholar 

  69. Feder R, Dagan A, Mor A (2000) Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerisation on selective cytotoxicity. J Biol Chem 275:4230–4238

    CAS  PubMed  Article  Google Scholar 

  70. Fleury Y, Dayem MA, Montagne JJ, Chaboisseau E, Le Caer JP, Nicolas P, Delfour A (1996) Covalent structure, synthesis, and structure-function studies of mesentericin Y105 (37), a defensive peptide from Gram-positive bacteria Leuconostoc mesenteroides. J Biol Chem 271:14421–14429

    CAS  PubMed  Article  Google Scholar 

  71. Fleury Y, Vouille V, Beven L, Amiche M, Wroblewski H, Delfour A, Nicolas P (1998) Synthesis, antimicrobial activity and gene structure of a novel member of the dermaseptin B family. Biochim Biophys Acta 1396:228–236

    CAS  PubMed  Google Scholar 

  72. Frost DR (2009) Amphibian species of the world: an online reference, Version 5.3. American Museum of Natural History, New York, USA. http://research.amnh.org/herpetology/amphibia/index.php. Accessed 2 Jan 2010

  73. Gaidukov L, Fish A, Mor A (2003) Analysis of membrane-binding properties of dermaseptin analogues: relationships between binding and cytotoxicity. Biochemistry 42:12866–12874

    CAS  PubMed  Article  Google Scholar 

  74. Ghosh JK, Shaool D, Guillaud P, Ciceron L, Mazier D, Kustanovich I, Shai Y, Mor A (1997) Selective cytotoxicity of dermaseptin S3 toward intraerythrocytic Plasmodium falciparum and the underlying molecular basis. J Biol Chem 272:31609–31616

    CAS  PubMed  Article  Google Scholar 

  75. Giacometti A, Cirioni O, Ghiselli R, Orlando F, Silvestri C, Renzone G, Testa I, Mocchegiani F, Della Vittoria A, Saba V, Scaloni A, Scalise G (2006) Distinctin improves the efficacies of glycopeptides and betalactams against staphylococcal biofilm in an experimental model of central venous catheter infection. J Biomed Mater Res A 81:233–239

    Google Scholar 

  76. Gomes A, Giri B, Saha A, Mishra R, Dasguta SC, Debnath A, Gomes A (2007) Bioactive molecules from amphibian skin: their biological activities with reference to therapeutic potential for possible drug development. Indian J Exp Biol 45:579–593

    CAS  PubMed  Google Scholar 

  77. Gozzini L, Montecucchi PC, Erspamer V, Melchiorri P (1985) Tryptophillins from extracts of Phyllomedusa rohdei skin: new tetra-, penta- and hepta-peptides. Int J Pept Protein Res 25:323–329

    CAS  Article  Google Scholar 

  78. Gregory SM, Cavenaugh A, Journigan V, Pokorny A, Almeida PFF (2008) A quantitative model for the all-or-none permeabilization of phospholipid vesicles by the antimicrobial peptide cecropin A. Biophys J 94:1667–1680

    CAS  PubMed  Article  Google Scholar 

  79. Hancock REW (1997) Peptide antibiotics. Lancet 349:418–422

    CAS  PubMed  Article  Google Scholar 

  80. Hancock REW, Lehrer R (1998) Cationic peptides: a new source of antibiotics. Trends Biotechnol 16:82–88

    CAS  PubMed  Article  Google Scholar 

  81. Harzer U, Bechinger B (2000) The alignment of lysine-anchored membrane peptides under conditions of hydrophobic mismatch: a CD, 15N and 31P solid-state NMR spectroscopy investigation. Biochemistry 39:13106–13114

    CAS  PubMed  Article  Google Scholar 

  82. Haug BE, Stensena W, Svendsen JS (2007) Application of the Suzuki–Miyaura cross-coupling to increase antimicrobial potency generates promising novel antibacterials. Bioorg Med Chem Lett 17:2361–2364

    CAS  PubMed  Article  Google Scholar 

  83. Hawrami A, Howe RA, Walsh TR, Dempsey CE (2008) Origin of low mammalian cell toxicity in a class of highly active antimicrobial amphipathic helical peptides. J Biol Chem 283:18636–18645

    Article  CAS  Google Scholar 

  84. Hernandez C, Mor A, Dagger F, Nicolas P, Hernandez A, Benedetti EL, Dunia I (1992) Functional and structural damage in Leishmania mexicana exposed to the cationic peptide dermaseptin. Eur J Cell Biol 59:414–424

    CAS  PubMed  Google Scholar 

  85. Hilpert K, Elliott MR, Volkmer-Engert R, Henklein P, Donini O, Zhou Q, Winkler DF, Hancock RE (2006) Sequence requirements and an optimization strategy for short antimicrobial peptides. Chem Biol 13:1101–1107

    CAS  PubMed  Article  Google Scholar 

  86. Huang HW, Chen FY, Lee MT (2004) Molecular mechanism of peptide-induced pores in membranes. Phys Rev Lett 92:198304–198307

    PubMed  Article  CAS  Google Scholar 

  87. Huguenin F, Zucolotto V, Carvalho AJF, Gonzalez ER, Oliveira ON (2005) Layer-by-layer hybrid films incorporating WO3, TiO2 and chitosan. Chem Mater 17:6739–6745

    CAS  Article  Google Scholar 

  88. Hwang PM, Vogel HJ (1998) Structure–function relationships of antimicrobial peptides. Biochem Cell Biol 76:235–246

    CAS  PubMed  Article  Google Scholar 

  89. Jones AJS, Epand RM, Lin KF, Walton D, Vail WJ (1978) Size and shape of the model lipoprotein complex formed between glucagon and dimyristolglycerophosphocholine. Biochemistry 17:2301–2307

    CAS  PubMed  Article  Google Scholar 

  90. Koczulla AR, Bals R (2003) Antimicrobial peptides—current status and therapeutic potential. Drugs 63:389–406

    CAS  PubMed  Article  Google Scholar 

  91. Kohri K, Nata K, Yonekura H, Nagai A, Konno K, Okamoto H (1993) Cloning and structural determination of human peptide YY cDNA and gene. Biochim Biophys Acta 1173:345–349

    CAS  PubMed  Google Scholar 

  92. Krugliak M, Feder R, Zolotarev VY, Gaidukov L, Dagan A, Ginsburg H, Mor A (2000) Antimalarial activities of dermaseptin S4 derivatives. Antimicrob Agents Chemother 44:2442–2451

    CAS  PubMed  Article  Google Scholar 

  93. Kückelhaus SAS, Leite JRSA, Neves MP, Frota KS, Abdala LF, Muniz-Junqueira MI, Bloch C Jr, Tosta CE (2006) Toxicity evaluation to mice of phylloseptin-1, an antimicrobial peptide from the skin secretion of Phyllomedusa hypochondrialis (Amphibia). Int J Pept Res Ther 13:423–429

    Article  CAS  Google Scholar 

  94. Kückelhaus SAS, Leite JRSA, Muniz-Junqueira MI, Sampaio RN, Bloch C Jr, Tosta CE (2009) Antiplasmodial and antileishmanial activities of phylloseptin-1, an antimicrobial peptide from the skin secretion of Phyllomedusa azurea (Amphibia). Exp Parasitol 123:11–16

    PubMed  Article  CAS  Google Scholar 

  95. Kustanovich I, Shalev DE, Mikhlin M, Gaidukov L, Mor A (2002) Structural requirements for potent versus selective cytotoxicity for antimicrobial dermaseptin S4 derivatives. J Biol Chem 277:16941–16951

    CAS  PubMed  Article  Google Scholar 

  96. Kwong PD, McDonald NQ, Singler PB, Hendrickson WA (1995) Structure of beta 2-bungarotoxin: potassium channel binding by Kunitz modules and targeted phospholipase action. Structure 3:1109–1119

    CAS  PubMed  Article  Google Scholar 

  97. Lacombe C, Cifuentes-Diasz C, Dunia I, Auber-Thomay M, Nicolas P, Amiche M (2000) Peptide secretion in the cutaneous gland of South American tree frog Phyllomedusa bicolor: an ultrastructural study. Eur J Cell Biol 79:631–641

    CAS  PubMed  Article  Google Scholar 

  98. Lazarus LH, Attila M (1993) The toad, ugly and venomous, wears yet a precious jewel in his skin. Progr Neurobiol 41:473–507

    CAS  Article  Google Scholar 

  99. Lazarus LH, Bryant SD, Cooper PS, Salvadori S (1999) What peptides these deltorphins be. Prog Neurobiol 57:377–420

    CAS  PubMed  Article  Google Scholar 

  100. Leite JRSA, Silva LP, Rodrigues MI, Prates MV, Brand GD, Lacava BM, Azevedo RB, Bocca AL, Albuquerque S, Bloch C Jr (2005) Phylloseptins: a novel class of anti-bacterial and anti-protozoan peptides from the Phyllomedusa genus. Peptides 26:565–573

    CAS  PubMed  Article  Google Scholar 

  101. Leite JRSA, Brand GD, Silva LP, Kückelhaus SAS, Bento WRC, Araújo ALT, Martins GR, Lazzari AM, Carlos Bloch Jr C (2008) Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta: secondary structure, antimicrobial activity, and mammalian cell toxicity. Comp Biochem Physiol A Mol Integr Physiol 151:336–343

  102. Lequin O, Bruston F, Convert O, Chassaing G, Nicolas P (2003) Helical structure of dermaseptin B2 in a membrane-mimetic environment. Biochemistry 42:10311–10323

    CAS  PubMed  Article  Google Scholar 

  103. Lequin O, Ladram A, Chabbert L, Bruston F, Convert O, Vanhoye D, Chassaing G, Nicolas P, Amiche M (2006) Dermaseptin S9, an α-helical antimicrobial peptide with a hydrophobic core and cationic termini. Biochemistry 45:468–480

    CAS  PubMed  Article  Google Scholar 

  104. Li J, Nation RL, Turnidge JD, Milne RW, Coulthard K, Rayner CR, Paterson DL (2006) Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect Dis 6:589–601

    CAS  PubMed  Article  Google Scholar 

  105. Lorin C, Saidi H, Belaid A, Zairi A, Baleux F, Hocini H (2005) The antimicrobial peptide dermaseptin S4 inhibits HIV-1 infectivity in vitro. Virology 334:264–275

    CAS  PubMed  Article  Google Scholar 

  106. Mandel SMS (2008) Prospecção de peptídeos antimicrobianos da secreção cutânea de anfíbios do gênero Phyllomedusa. Dissertation. Universidade de Brasília

  107. Marenah L, McClean S, Flatt PR, Orr DF, Shaw C, Abdel-Wahab YH (2004) Novel insulin-releasing peptides in the skin of Phyllomedusa trinitatis frog include 28 amino acid peptide from dermaseptin BIV precursor. Pancreas 29:110–115

    CAS  PubMed  Article  Google Scholar 

  108. Marr AK, Gooderham WJ, Hancock REW (2006) Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr Opin Pharmacol 6:468–472

    CAS  PubMed  Article  Google Scholar 

  109. Matsuzaki K (1998) Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim Biophys Acta 1376:391–400

    CAS  PubMed  Google Scholar 

  110. Matsuzaki K (2009) Control of cell selectivity of antimicrobial peptides. Biochim Biophys Acta 1788:1687–1692

    CAS  PubMed  Article  Google Scholar 

  111. Mignogna G, Severini C, Simmaco M, Negri L, Falconieri Erspamer G, Kreil G, Barra D (1992) Identification and characterization of two dermorphins from skin extracts of the Amazonian frog Phyllomedusa bicolor. FEBS Lett 302:151–154

    CAS  PubMed  Article  Google Scholar 

  112. Moellering RC Jr (2003) New approaches to developing antimicrobials for resistant bacteria. J Infect Chemother 9:8–11

    PubMed  Article  Google Scholar 

  113. Montecucchi PC, Henschen A, Erspamer V (1979) Structure of sauvagine, a vasoactive peptide from the skin of a frog. Hoppe-Seylers Z Physiol Chem 360:1178

    Google Scholar 

  114. Montecucchi PC, Anastasi A, De Castiglione R, Erspamer V (1980) Isolation and amino acid composition of sauvagine, an active polypeptide from methanol extracts of the skin of the South American frog Phyllomedusa sauvagei. Int J Pept Protein Res 16:191–199

    CAS  PubMed  Article  Google Scholar 

  115. Montecucchi PC, De Castiglione R, Piani S, Gozzini L, Erspamer V (1981a) Amino acid composition and sequence of dermorphin, a novel opiate-like peptide from the skin of Phyllomedusa sauvagei. Int J Pept Protein Res 17:275–283

    CAS  PubMed  Article  Google Scholar 

  116. Montecucchi PC, De Castiglione R, Erspamer V (1981b) Identification of dermorphin and Hyp δ-dermorphin in skin extracts of the Brazilian frog Phyllomedusa rhodei. Int J Pept Protein Res 17:316–321

    CAS  PubMed  Article  Google Scholar 

  117. Montecucchi PC, Gozzini L, Erspamer V (1986) Primary structure determination of a tryptophan-containing tridecapeptide from Phyllomedusa rohdei. Int J Pept Protein Res 27:175–182

    CAS  Article  Google Scholar 

  118. Mor A, Nicolas P (1994a) Isolation and structure of novel defensive peptides from frog skin. Eur J Biochem 219:145–154

    CAS  PubMed  Article  Google Scholar 

  119. Mor A, Nicolas P (1994b) The NH2-terminal α-helical domain 1–18 of dermaseptin is responsible for antimicrobial activity. J Biol Chem 269:1934–1939

    CAS  PubMed  Google Scholar 

  120. Mor A, Delfour A, Nicolas P (1991a) Identification of a d-alanine-containing polypeptide precursor for the peptide opioid, dermorphin. J Biol Chem 266:6264–6270

    CAS  PubMed  Google Scholar 

  121. Mor A, Nguyen VH, Delfour A, Migliore D, Nicolas P (1991b) Isolation, amino acid sequence, and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry 30:8824–8830

    CAS  PubMed  Article  Google Scholar 

  122. Mor A, Amiche M, Nicolas P (1994a) Structure, synthesis, and activity of dermaseptin B. A novel vertebrate defensive peptide from frog skin: relationship with adenoregulin. Biochemistry 33:6642–6650

    CAS  PubMed  Article  Google Scholar 

  123. Mor A, Chartrel N, Vaudry H, Nicolas P (1994b) Skin peptide tyrosine-tyrosine, a member of the pancreatic polypeptide family: Isolation, structure, synthesis, and endocrine activity. Proc Natl Acad Sci USA 91:10295–10299

    CAS  PubMed  Article  Google Scholar 

  124. Mor A, Hani K, Nicolas P (1994c) The vertebrate peptide antibiotics dermaseptins have overlapping structural features but target specific microorganisms. J Biol Chem 269:31635–31641

    CAS  PubMed  Google Scholar 

  125. Mundim NCCR (2008) Prospecção de bradicininas de anfibios do gênero Phyllomedusa. Dissertation. Universidade de Brasília

  126. Navon-Venezia S, Feder R, Gaidukov L, Carmeli Y, Mor A (2002) Antibacterial properties of dermaseptin S4 derivatives with in vivo activity. Antimicrob Agents Chemother 46:689–694

    CAS  PubMed  Article  Google Scholar 

  127. Nicolas P, El Amri C (2009) The dermaseptin superfamily: A gene-based combinatorial library of antimicrobial peptides. Biochim Biophys Acta 1788:1537–1550

    CAS  PubMed  Article  Google Scholar 

  128. Nicolas P, Vanhoye D, Amiche M (2003) Molecular strategies in biological evolution of antimicrobial peptides. Peptides 24:1669–1680

    CAS  PubMed  Article  Google Scholar 

  129. Papo N, Shai Y (2003) Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes? Peptides 24:1693–1703

    CAS  PubMed  Article  Google Scholar 

  130. Perron GG, Zasloff M, Bell G (2006) Experimental evolution of resistance to an antimicrobial peptide. Proc Roy Soc Lond B 273:251–256

    CAS  Article  Google Scholar 

  131. Peschel A, Sahl HG (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4:529–536

    CAS  PubMed  Article  Google Scholar 

  132. Pierre TP, Seon AA, Amiche M, Nicolas P (2000) Phylloxin, a novel peptide antibiotic of the dermaseptin family of antimicrobial/opioid peptide precursors. Eur J Biochem 267:370–378

    CAS  PubMed  Article  Google Scholar 

  133. Poulter L, Terry AS, Williams DH, Giovannini MG, Moore CH, Gibson BW (1988) Levitide, a new hormone-like peptide from the skin of Xenopus laevis. Peptide and peptide precursor cDNA sequence. J Biol Chem 263:3279–3283

    CAS  PubMed  Google Scholar 

  134. Pouny Y, Rapaport D, Mor A, Nicolas P, Shai Y (1992) Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31:12416–12423

    CAS  PubMed  Article  Google Scholar 

  135. Pukkila-Worley R, Mylonakis E (2008) Epidemiology and management of cryptococcal meningitis: developments and challenges. Expert Opin Pharmacother 9:551–560

    CAS  PubMed  Article  Google Scholar 

  136. Resende JM, Moraes CM, Prates MV, Cesar A, Almeida FCL, Mundim NCCR, Valente AP, Bemquerer MP, Piló-Veloso DA, Bechinger B (2008) Solution NMR structures of the antimicrobial peptides phylloseptin-1, -2, and -3 and biological activity: the role of charges and hydrogen bonding interactions in stabilizing helix conformations. Peptides 29:1633–1644

    CAS  PubMed  Article  Google Scholar 

  137. Richter K, Egger R, Kreil G (1987) d-Alanine in the frog skin peptide dermorphin is derived from l-alanine in the precursor. Science 238:200–202

    CAS  PubMed  Article  Google Scholar 

  138. Richter K, Egger R, Negri L, Corsi R, Severini C, Kreil G (1990) cDNAs encoding [D-Ala2]deltorphin precursors from skin of Phyllomedusa bicolor also contain genetic information for three dermorphin-related opioid peptides. Proc Natl Acad Sci USA 87:4836–4839

    CAS  PubMed  Article  Google Scholar 

  139. Rivas L, Luque-Ortega JR, Andreu D (2009) Amphibian antimicrobial peptides and protozoa: lessons from parasites. Biochim Biophys Acta 1788:1570–1581

    CAS  PubMed  Article  Google Scholar 

  140. Rotem S, Mor A (2009) Antimicrobial peptide mimics for improved therapeutic properties. Biochim Biophys Acta 1788:1582–1592

    CAS  PubMed  Article  Google Scholar 

  141. Rydlo T, Sotem S, Mor A (2006) Antibacterial properties of dermaseptin S4 derivatives under extreme incubation conditions. Antimicrob Agents Chemother 50:490–507

    CAS  PubMed  Article  Google Scholar 

  142. SBH (2009) Lista de espécies de anfíbios do Brasil. Sociedade Brasileira de Herpetologia (SBH).http://www.sbherpetologia.org.br/checklist/anfibios.htm. Accessed 12 Jan 2010

  143. Sengupta D, Leontiadou H, Mark AE, Marrink SJ (2008) Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim Biophys Acta 1778:2308–2317

    CAS  PubMed  Article  Google Scholar 

  144. Seon AA, Pierre TN, Redeker V, Lacombe C, Delfour A, Nicolas P, Amiche M (2000) Isolation, structure, synthesis, and activity of a new member of the calcitonin gene-related peptide family from frog skin and molecular cloning of its precursor. J Biol Chem 275:5934–5940

    CAS  PubMed  Article  Google Scholar 

  145. Serra MD, Cirioni O, Vitale RM, Renzone G, Coraiola M, Giacometti A, Potrich C, Baroni E, Guella G, Sanseverino M, De Luca S, Scalise G, Amodeo P, Scaloni A (2008) Structural features of distinctin affecting peptide biological and biochemical properties. Biochemistry 47:7888–7899

    Google Scholar 

  146. Shai Y (1995) Molecular recognition between membrane-spanning polypeptides. Trends Biochem Sci 20:460–464

    CAS  PubMed  Article  Google Scholar 

  147. Shai Y (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66:236–248

    CAS  PubMed  Article  Google Scholar 

  148. Shalev DE, Mor A, Kustanovich I (2002) Structural consequences of carboxyamidation of dermaseptin S3. Biochemistry 41:7312–7317

    CAS  PubMed  Article  Google Scholar 

  149. Shaw C (2009) Advancing drug discovery with reptile and amphibian venom peptides, venom-based medicines. Biochem Soc 31:34–37

    Google Scholar 

  150. Shin Y, Moni RW, Lueders JE, Daly JW (1994) Effects of the amphiphilic peptides mastoparan and adenoregulin on receptor binding, G proteins, phosphoinositide breakdown, cyclic AMP generation, and calcium influx. Cell Mol Neurobiol 14:133–157

    CAS  PubMed  Article  Google Scholar 

  151. Shukla A, Fleming KE, Chuang HF, Chau TM, Loose CR, Stephanopoulos GN, Hammond PT (2009) Controlling the release of peptide antimicrobial agents from surfaces. Biomaterials 31(8):2348–2357

    PubMed  Article  CAS  Google Scholar 

  152. Silva LR, Batista CVF, Prates MV, Gordo M, Bloch C Jr (2000) A new antimicrobial peptide homologous to the dermaseptins isolated from Phyllomedusa tarsius. Toxicon 38:554–555

    Article  Google Scholar 

  153. Silva LP, Leite JR, Brand GD, Regis WB, Tedesco AC, Azevedo RB, Freitas SM, Bloch C Jr (2008) Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta: liposomes fusion and/or lysis investigated by fluorescence and atomic force microscopy. Comp Biochem Physiol A Mol Integr Physiol 151:329–335

    PubMed  Article  CAS  Google Scholar 

  154. Siqueira JR Jr, Gasparotto LHS, Crespilho FN, Carvalho AJF, Zucolotto V, Oliveira ON Jr (2006) Physicochemical properties and sensing ability of metallophthalocyanines/chitosan nanocomposites. J Phys Chem B 110:22690–22694

    CAS  PubMed  Article  Google Scholar 

  155. Strahilevitz J, Mor A, Nicolas P, Shai Y (1994) Spectrum of antimicrobial activity and assembly of dermaseptin B and its precursor form in phospholipid membranes. Biochemistry 33:10951–10960

    CAS  PubMed  Article  Google Scholar 

  156. Thompson AH (2006) A genomic/proteomic approach to isolating and identifying bioactive peptides from the skin secretions of Phyllomedusa hypochondrialis azurea. Thesis. University of Ulster Coleraine

  157. Thompson AH, Bjourson AJ, Shaw C, McClean S (2006) Bradykinin-related peptides from Phyllomedusa hypochondrialis azurea: Mass spectrometric structural characterisation and cloning of precursor cDNAs. Rapid Commun Mass Spectr 20:3780–3788

    CAS  Article  Google Scholar 

  158. Thompson AH, Bjourson AJ, Orr DF, Shaw C, Mcclean S (2007a) A combined mass spectrometric and cDNA sequencing approach to the isolation and characterization of novel antimicrobial peptides from the skin secretions of Phyllomedusa hypochondrialis azurea. Peptides 28:1331–1343

    CAS  PubMed  Article  Google Scholar 

  159. Thompson AH, Bjourson AJ, Orr DF, Shaw C, McClean S (2007b) Amphibian skin secretomics: application of parallel quadrupole time- of-flight mass spectrometry and peptide precursor cDNA cloning to rapidly characterize the skin secretory peptidome of Phyllomedusa hypochondrialis azurea: discovery of a novel peptide family, the hyposins. J Proteome Res 6:3604–3613

    CAS  PubMed  Article  Google Scholar 

  160. Toledo RC, Jared C (1993) Cutaneous adaptations to water balance in amphibians. Comp Biochem Physiol 105:593–608

    Article  Google Scholar 

  161. Toledo RC, Jared C (1995) Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol 111:1–29

    Article  Google Scholar 

  162. UniProt (2009) The UniProt Consortium. The Universal Protein Resource (UniProt). Nucl Acids Res 37:D169–D174

    Article  CAS  Google Scholar 

  163. Vaara M (2009) New approaches in peptide antibiotics. Curr Opin Pharmacol 9(5):571–576

    CAS  PubMed  Article  Google Scholar 

  164. van’t HW, Veerman EC, Helmerhorst EJ, Amerongen AV (2001) Antimicrobial peptides: properties and applicability. Biol Chem 382:597–619

    Article  Google Scholar 

  165. Vanhoye D, Bruston F, Nicolas P, Amiche M (2003) 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 270:2068–2081

    CAS  PubMed  Article  Google Scholar 

  166. Vanhoye D, Bruston F, El Amri S, Ladram A, Amiche M, Nicolas P (2004) Membrane Association, electrostatic sequestration, and cytotoxicity of gly-leu-rich peptide orthologs with differing functions. Biochemistry 43:8391–8409

    CAS  PubMed  Article  Google Scholar 

  167. Verly RM, Rodrigues MA, Daghastanli KR, Denadai AM, Cuccovia IM, Bloch C Jr, Frézard F, Santoro MM, Piló-Veloso D, Bemquerer MP (2008) Effect of cholesterol on the interaction of the amphibian antimicrobial peptide DD K with liposomes. Peptides 29:15–24

    CAS  PubMed  Article  Google Scholar 

  168. Verly RM, Moraes CM, Resende JM, Aisenbrey C, Bemquerer MP, Piló-Veloso D, Valente AP, Almeida FCL, Bechinge B (2009) Structure and membrane interactions of the antibiotic peptide dermadistinctin K by multidimensional solution and oriented 15N and 31P solid-state NMR spectroscopy. Biophys J 96:2194–2203

    CAS  PubMed  Article  Google Scholar 

  169. Vouille V, Amiche M, Nicolas P (1997) Structure of genes for dermaseptins B, antimicrobial peptides from frog skin. FEBS Lett 414:27–31

    CAS  PubMed  Article  Google Scholar 

  170. Vouldoukis I, Shai Y, Nicolas P, Mor A (1996) Broad spectrum antibiotic activity of the skin-PYY. FEBS Lett 380:237–240

    CAS  PubMed  Article  Google Scholar 

  171. Wang L, Zhou M, Zhou Z, Chen T, Walker B, Shaw C (2009) Sauvatide—a novel amidated myotropic decapeptide from the skin secretion of the waxy monkey frog, Phyllomedusa sauvagei. Bioch Biophy Res Commun 383:240–244

    CAS  Article  Google Scholar 

  172. Wang H, Xu K, Liu L, Tan JPK, Chen Y, Li Y, Fan W, Wei Z, Sheng J, Yang YY, Li L (2010) The efficacy of self-assembled cationic antimicrobial peptide nanoparticles against Cryptococcus neoformans for the treatment of meningitis. Biomaterials 31(10):2874–2881

    CAS  PubMed  Article  Google Scholar 

  173. Wieprecht T, Dathe M, Krause E, Beyermann M, Maloy WL, MacDonald DL, Bienert M (1997) Modulation of membrane activity of amphipathic, antibacterial peptides by slight modifications of the hydrophobic moment. FEBS Lett 417:135–140

    CAS  PubMed  Article  Google Scholar 

  174. Yasuhara T, Nakajima T, Falconieri Erspamer G, Erspamer V (1981) New tachykinins Glu2, Pro5-kassinin (Hylambates-kassinin) and hylambatin in the skin of the African rhacophorid frog Hylambates maculates. Biomed Res 2:613–617

    CAS  Google Scholar 

  175. Yasuhara T, Nakajima T, Nokihara K, Yanaihara C, Yanaihara N, Erspamer V, Falconieri Erspamer G (1983) Two new, frog skin peptides, phyllolitorins, of the bombesin-ranatensin family. Biomed Res 4:407–412

    CAS  Google Scholar 

  176. Yeaman MR, Yount NY (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55:27–55

    CAS  PubMed  Article  Google Scholar 

  177. Zairi A, Tangy F, Saadi S, Hani K (2008) In vitro activity of dermaseptin S4 derivatives against genital infections pathogens. Regul Toxicol Pharmacol 50:353–358

    CAS  PubMed  Article  Google Scholar 

  178. Zairi A, Tangy F, Bouassida K, Hani K (2009) Dermaseptins and magainins: antimicrobial peptides from frogs’ skin—new sources for a promising spermicides microbicides. J Biomed Biotechnol 2009:1–8

    Article  CAS  Google Scholar 

  179. Zampa MF, de Brito AC, Kitagawa IL, Constantino CJ, Oliveira ON Jr, da Cunha HN, Zucolotto V, dos Santos JR Jr, Eiras C (2007) Natural gum-assisted phthalocyanine immobilization in electroactive nanocomposites: physicochemical characterization and sensing applications. Biomacromolecules 8:3408–3413

    CAS  PubMed  Article  Google Scholar 

  180. Zampa MF, Araújo IMS, Costa V, Costa CHN, Santos JR Jr, Zucolotto V, Eiras C, Leite JRSA (2009) Leishmanicidal Activity and Immobilization of dermaseptin 01 antimicrobial peptides in ultrathin films for nanomedicine applications. Nanomedicine 5:352–358

    CAS  PubMed  Google Scholar 

  181. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395

    CAS  PubMed  Article  Google Scholar 

  182. Zhang L, Parente J, Harris SM, Woods DE, Hancock REW, Falla TJ (2005) Antimicrobial peptide therapeutics for cystic fibrosis. Antimicrob Agents Chemother 49:2921–2927

    CAS  PubMed  Article  Google Scholar 

  183. Zucolotto V, Pinto AP, Tumolo T, Moraes ML, Baptista MS, Riul A Jr, Araújo AP, Oliveira ON Jr (2006) Catechol biosensing using a nanostructured layer-by-layer film containing Cl-catechol 1, 2 dioxygenase. Biosens Bioelectron 21:1320–1326

    CAS  PubMed  Article  Google Scholar 

  184. Zucolotto V, Daghastanli KRP, Hayasaka CO, Riul A Jr, Ciancaglini P, Oliveira ON Jr (2007) Using capacitance measurements as the detection method in antigen-containing layer-by-layer films for biosensing. Anal Chem 79:2163–2167

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

The authors are grateful to the Ministry of Science and Technology (MCT), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP), Fundação de Tecnologia do Acre (FUNTAC/FDCT), Coordenação de Aperfeiçoamento de Nível Superior (CAPES) – Projeto NanoBiotec, Secretary of Development of the Rondonia State (PRONEX/CNPq) for financial support and Priscila Cerviglieri for linguistic advice.

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Azevedo Calderon, L., Silva, A.A.E., Ciancaglini, P. et al. Antimicrobial peptides from Phyllomedusa frogs: from biomolecular diversity to potential nanotechnologic medical applications. Amino Acids 40, 29–49 (2011). https://doi.org/10.1007/s00726-010-0622-3

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Keywords

  • Phyllomedusa
  • Bioprospection
  • Antimicrobial peptide
  • Dermaseptin
  • Infection disease
  • New drugs
  • Nanobiotechnology