An orphan dermaseptin from frog skin reversibly assembles to amyloid-like aggregates in a pH-dependent fashion

FEBS Journal

Volumn 276, Issue 20, 2009, Pages 5849-5859

  Gößler Schöfberger, Ruth ^a   Hesser, Günter ^a   Muik, Martin ^a   Wechselberger, Christian ^b   Jilek, Alexander ^a  

^a JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

^b Upper Austrian Research GmbH   (Austria)

Author keywords

Amphibian skin; Amyloid; Bioactive peptide; Cytotoxicity; Self assembly

Indexed keywords

AMYLOID; ASPARTIC ACID; DERMASEPTIN; REACTIVE OXYGEN METABOLITE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DRUG EFFECT; DRUG STRUCTURE; FIBER; FROG; INNATE IMMUNITY; MOUSE; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SKIN;

AMPHIBIAN PROTEINS; ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; ANURA; CELL LINE; CELL SURVIVAL; CIRCULAR DICHROISM; HYDROGEN-ION CONCENTRATION; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MULTIPROTEIN COMPLEXES; NIH 3T3 CELLS; PROTEIN STRUCTURE, SECONDARY; REACTIVE OXYGEN SPECIES; SKIN; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPODOPTERA;

AMPHIBIA; ANURA;

EID: 70349481522     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07266.x     Document Type: Article

References (52)

1. Lazarus LH Attila M (1993) The toad, ugly and venomous, wears yet a precious jewel in his skin. Prog Neurobiol 41, 473 507.
2. Kreil G (1994) Antimicrobial peptides from amphibian skin: an overview. Ciba Found Symp 186, 77 90.
3. Olivera BM (2006) Conus peptides: biodiversity-based discovery and exogenomics. J Biol Chem 281, 31173 31177.
4. Wechselberger C, Severini C, Kreil G Negri L (1998) A new opioid peptide predicted from cloned cDNAs from skin of Pachymedusa dacnicolor and Agalychnis annae. FEBS Lett 429, 41 43.
5. Chen T, Orr DF, O'Rourke M, McLynn C, Bjourson AJ, McClean S, Hirst D, Rao P Shaw C (2004) Pachymedusa dacnicolor tryptophyllin-1: structural characterization, pharmacological activity and cloning of precursor cDNA. Regul Pept 117, 25 32.
6. Wechselberger C (1998) Cloning of cDNAs encoding new peptides of the dermaseptin-family. Biochim Biophys Acta 1388, 279 283.
7. 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.
8. Amiche M, Ladram A Nicolas P (2008) A consistent nomenclature of antimicrobial peptides isolated from frogs of the subfamily Phyllomedusinae. Peptides, 29, 2074 2082.
9. Shai Y (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66, 236 248.
10. Bechinger B Lohner K (2006) Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochim Biophys Acta 1758, 1529 1539.
11. Matsuzaki K (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim Biophys Acta 1462, 1 10.
12. Nilsson MR (2004) Techniques to study amyloid fibril formation in vitro. Methods 34, 151 160.
13. Jackson M Mantsch HH (1995) The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit Rev Biochem Mol Biol 30, 95 120.
14. Zandomeneghi G, Krebs MR, McCammon MG Fändrich M (2004) FTIR reveals structural differences between native beta-sheet proteins and amyloid fibrils. Protein Sci 13, 3314 3321.
15. Krull LH, Wall JS, Zobel H Dimler RJ (1965) Synthetic polypeptides containing side-chain amide groups: water-insoluble polymers. Biochemistry 4, 626 633.
16. Ferrone FA (2006) Nucleation: the connections between equilibrium and kinetic behavior. Methods Enzymol 412, 285 299.
17. Oosawa F Asakura S (1975) Thermodynamics of the Polymerization of Protein. Academic Press, London.
18. Lopez de la Paz M Serrano L (2004) Sequence determinants of amyloid fibril formation. Proc Natl Acad Sci USA 101, 87 92.
19. Kallberg Y, Gustafsson M, Persson B, Thyberg J Johansson J (2001) Prediction of amyloid fibril-forming proteins. J Biol Chem 276, 12945 12950.
20. Aggeli A, Bell M, Carrick LM, Fishwick CW, Harding R, Mawer PJ, Radford SE, Strong AE Boden N (2003) pH as a trigger of peptide beta-sheet self-assembly and reversible switching between nematic and isotropic phases. J Am Chem Soc 125, 9619 9628.
21. Spannhof L (1953) 54) Zur Genese, Morphologie und Physiologie der Hautdrüsen bei Xenopus laevis. Wiss Z Humboldt Universität Berlin 3, 295 305.
22. Lillywhite HB (2006) Water relations of tetrapod integument. J Exp Biol 209, 202 226.
23. Krebs MR, Bromley EH Donald AM (2005) The binding of thioflavin-T to amyloid fibrils: localisation and implications. J Struct Biol 149, 30 37.
24. Feder R, Dagan A 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.
25. Sal-Man N, Oren Z Shai Y (2002) Preassembly of membrane-active peptides is an important factor in their selectivity toward target cells. Biochemistry 41, 11921 11930.
26. 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.
27. Korzeniewski C Callewaert DM (1983) An enzyme-release assay for natural cytotoxicity. J Immunol Methods 64, 313 320.
28. Castle M, Nazarian A, Yi SS Tempst P (1999) Lethal effects of apidaecin on Escherichia coli involve sequential molecular interactions with diverse targets. J Biol Chem 274, 32555 32564.
29. Chiti F Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75, 333 366.
30. Skovronsky DM, Lee VM Trojanowski JQ (2006) Neurodegenerative diseases: new concepts of pathogenesis and their therapeutic implications. Annu Rev Pathol 1, 151 170.
31. Sipe JD (1992) Amyloidosis. Annu Rev Biochem 61, 947 975.
32. Pepys MB (2006) Amyloidosis. Annu Rev Med 57, 223 241.
33. Bucciantini M, Calloni G, Chiti F, Formigli L, Nosi D, Dobson CM Stefani M (2004) Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J Biol Chem 279, 31374 31382.
34. Gharibyan AL, Zamotin V, Yanamandra K, Moskaleva OS, Margulis BA, Kostanyan IA Morozova-Roche LA (2007) Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways. J Mol Biol 365, 1337 1349.
35. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307, 262 265.
36. Okada T, Wakabayashi M, Ikeda K Matsuzaki K (2007) Formation of toxic fibrils of Alzheimer's amyloid beta-protein-(1-40) by monosialoganglioside GM1, a neuronal membrane component. J Mol Biol 371, 481 489.
37. Fowler DM, Koulov AV, Balch WE Kelly JW (2007) Functional amyloid - from bacteria to humans. Trends Biochem Sci 32, 217 224.
38. Zhao H, Mattila JP, Holopainen JM Kinnunen PK (2001) Comparison of the membrane association of two antimicrobial peptides, magainin 2 and indolicidin. Biophys J 81, 2979 2991.
39. Sood R, Domanov Y, Pietiainen M, Kontinen VP Kinnunen PK (2008) Binding of LL-37 to model biomembranes: insight into target vs host cell recognition. Biochim Biophys Acta 1778, 983 996.
40. Auvynet C, El Amri C, Lacombe C, Bruston F, Bourdais J, Nicolas P Rosenstein Y (2008) Structural requirements for antimicrobial versus chemoattractant activities for dermaseptin S9. FEBS J 275, 4134 4151.
41. Simmaco M, Mangoni ML, Boman A, Barra D Boman HG (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.
42. Boman HG (2000) Innate immunity and the normal microflora. Immunol Rev 173, 5 16.
43. Miele R, Bjorklund G, Barra D, Simmaco M Engstrom Y (2001) Involvement of Rel factors in the expression of antimicrobial peptide genes in amphibia. Eur J Biochem 268, 443 449.
44. Poschner BC, Reed J, Langosch D Hofmann MW (2007) An automated application for deconvolution of circular dichroism spectra of small peptides. Anal Biochem 363, 306 308.
45. Fodera V, Groenning M, Vetri V, Librizzi F, Spagnolo S, Cornett C, Olsen L, van de Weert M Leone M (2008) Thioflavin T hydroxylation at basic pH and its effect on amyloid fibril detection. J Phys Chem B 112, 15174 15181.
46. Westermark GT, Engstrom U Westermark P (1992) The N-terminal segment of protein AA determines its fibrillogenic property. Biochem Biophys Res Commun 182, 27 33.
47. Moriarty DF Raleigh DP (1999) Effects of sequential proline substitutions on amyloid formation by human amylin20-29. Biochemistry 38, 1811 1818.
48. Zangger K, Gossler R, Khatai L, Lohner K Jilek A (2008) Structures of the glycine-rich diastereomeric peptides bombinin H2 and H4. Toxicon, 52, 246 254.
49. Byler DM Susi H (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25, 469 487.
50. Hultmark D, Steiner H, Rasmuson T Boman HG (1980) Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur J Biochem 106, 7 16.
51. Bulet P, Dimarcq JL, Hetru C, Lagueux M, Charlet M, Hegy G, Van Dorsselaer A Hoffmann JA (1993) A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J Biol Chem 268, 14893 14897.
52. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM Stefani M (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507 511.