Substrate specificity of a peptidyl-aminoacyl-L/D-isomerase from frog skin

Amino Acids

Volumn 42, Issue 5, 2012, Pages 1757-1764

  Jilek, Alexander ^a,b   Mollay, Christa ^b   Lohner, Karl ^b   Kreil, Günther ^b,c  

^a JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Amphibian skin; Chirality; D amino acid; Peptide biosynthesis; Post translational modification

Indexed keywords

AMINO ACID; BOMBININ; ISOMERASE; PEPTIDE DERIVATIVE; PEPTIDYL AMINOACYL ISOMERASE; PHENYLALANINE; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; AMINO TERMINAL SEQUENCE; AMPHIBIA; ANURA; ARTICLE; CHIRALITY; ENZYME SPECIFICITY; FLUORESCENCE ANALYSIS; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SKIN;

AMINO ACID ISOMERASES; AMINO ACID SUBSTITUTION; AMINO ACIDS; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ANURA; MALE; PEPTIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SKIN; STEREOISOMERISM; SUBSTRATE SPECIFICITY;

AMPHIBIA; ANURA; BOMBINA; BOMBINA BOMBINA; MAMMALIA; VERTEBRATA;

EID: 84862754190     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-0890-6     Document Type: Article

References (51)

1. Amiche M, Delfour A, Nicolas P (1998) Opioid peptides from frog skin. EXS 85:57-71
2. Bai L, Sheeley S, Sweedler JV (2009) Analysis of endogenous D-amino acid-containing peptides in metazoa. Bioanal Rev 1(1):7-24. doi:10.1007/s12566- 009-0001-2
3. Bansal PS, Torres AM, Crossett B, Wong KK, Koh JM, Geraghty DP, Vandenberg JI, Kuchel PW (2008) Substrate specificity of platypus venom L-to-D-peptide isomerase. J Biol Chem 283(14): 8969-8975. doi:10.1074/jbc. M709762200
4. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2008) GenBank. Nucleic Acids Res 36 (Database issue):D25-D30. doi:10.1093/nar/gkm929 (Pubitemid 351149691)
5. Bozzi A, Mangoni ML, Rinaldi AC, Mignogna G, Aschi M (2008) Folding propensity and biological activity of peptides: the effect of a single stereochemical isomerization on the conformational properties of bombinins in aqueous solution. Biopolymers 89(9):769-778. doi:10.1002/bip.21006
6. Buczek O, Bulaj G, Olivera BM (2005a) Conotoxins and the posttranslational modification of secreted gene products. Cell Mol Life Sci 62(24):3067-3079. doi:10.1007/s00018-005-528 3-0 (Pubitemid 43004755)
7. Buczek O, Yoshikami D, Bulaj G, Jimenez EC, Olivera BM (2005b) Post-translational amino acid isomerization: a functionally important D-amino acid in an excitatory peptide. J Biol Chem 280(6):4247-4253. doi:10.1074/jbc.M405835200 (Pubitemid 40288591)
8. Buczek O, Yoshikami D, Watkins M, Bulaj G, Jimenez EC, Olivera BM (2005c) Characterization of D-amino-acid-containing excitatory conotoxins and redefinition of the I-conotoxin superfamily. FEBS J 272(16):4178-4188. doi:10.1111/j.1742-4658.2005. 04830.x (Pubitemid 41160924)
9. Castro MS, Ferreira TC, Cilli EM, Crusca E Jr, Mendes-Giannini MJ, Sebben A, Ricart CA, Sousa MV, Fontes W (2009) Hylin a1, the first cytolytic peptide isolated from the arboreal South American frog Hypsiboas albopunctatus ("spotted tree frog"). Peptides 30(2):291-296. doi:10.1016/j.peptides. 2008.11.003
10. Chen H, Wang L, Zeller M, Hornshaw M, Wu Y, Zhou M, Li J, Hang X, Cai J, Chen T, Shaw C (2010) Kassorins: novel innate immune system peptides from skin secretions of the African hyperoliid frogs, Kassina maculata and Kassina senegalensis. Mol Immunol. doi:10.1016/j.molimm.2010.09.018
11. Conlon JM, Kolodziejek J, Nowotny N, Leprince J, Vaudry H, Coquet L, Jouenne T, King JD (2008) Characterization of antimicrobial peptides from the skin secretions of the Malaysian frogs, Odorrana hosii and Hylarana picturata (Anura:Ranidae). Toxicon 52(3):465-473. doi:10.1016/j.toxicon.2008.06.017
12. Conlon JM, Demandt A, Nielsen PF, Leprince J, Vaudry H, Woodhams DC (2009) The alyteserins: two families of antimicrobial peptides from the skin secretions of the midwife toad Alytes obstetricans (Alytidae). Peptides 30(6):1069-1073. doi: 10.1016/j.peptides.2009.03.004
13. Gößler-Schöfberger R, Hesser G, Muik M, Wechselberger C, Jilek A (2009) An orphan dermaseptin from frog skin reversibly assembles to amyloid-like aggregates in a pH-dependent fashion. FEBS J 276(20):5849-5859. doi:10.1111/j.1742-4658.2009.07266.x
14. Gudmundsson GH, Agerberth B, Odeberg J, Bergman T, Olsson B, Salcedo R (1996) The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur J Biochem 238(2):325-332 (Pubitemid 26188246)
15. Haldane JBS (1930) Enzymes. Longmans, Green and Co., London
16. Halverson T, Basir YJ, Knoop FC, Conlon JM (2000) Purification and characterization of antimicrobial peptides from the skin of the North American green frog Rana clamitans. Peptides 21(4):469-476. doi:S0196-9781(00)00178- 9[pii] (Pubitemid 30261563)
17. Harada N, Iijima S, Kobayashi K, Yoshida T, Brown WR, Hibi T, Oshima A, Morikawa M (1997) Human IgGFc binding protein (FcgammaBP) in colonic epithelial cells exhibits mucin-like structure. J Biol Chem 272(24):15232-15241 (Pubitemid 27255541)
18. Heck SD, Siok CJ, Krapcho KJ, Kelbaugh PR, Thadeio PF, Welch MJ, Williams RD, Ganong AH, Kelly ME, Lanzetti AJ, Gray WR, Phillips D, Parks TN, Jackson H, Ahlijanian MK, Saccomano NA, Volkmann RA (1994) Functional consequences of posttranslational isomerization of Ser46 in a calcium channel toxin. Science 266(5187):1065-1068
19. Heck SD, Faraci WS, Kelbaugh PR, Saccomano NA, Thadeio PF, Volkmann RA (1996) Posttranslational amino acid epimerization: enzyme-catalyzed isomerization of amino acid residues in peptide chains. Proc Natl Acad Sci USA 93(9):4036-4039 (Pubitemid 26144241)
20. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J, Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T, Khokha MK, Richardson PM, Rokhsar DS (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328(5978):633-636. doi:10.1126/science.1 183670
21. Jilek A, Kreil G (2008) D-amino acids in animal peptides. Chemical Monthly 139(1):1-5. doi:10.1007/s00706-007-0780-5
22. Jilek A, Mollay C, Tippelt C, Grassi J, Mignogna G, Müllegger J, Sander V, Fehrer C, Barra D, Kreil G (2005) Biosynthesis of a D-amino acid in peptide linkage by an enzyme from frog skin secretions. Proc Natl Acad Sci USA 102(12):4235-4239. doi: 10.1073/pnas.0500789102 (Pubitemid 40397095)
23. Kamatani Y, Minakata H, Kenny PT, Iwashita T, Watanabe K, Funase K, Sun XP, Yongsiri A, Kim KH, Novales-Li P et al (1989) Achatin-I, an endogenous neuroexcitatory tetrapeptide from Achatina fulica Ferussac containing a D-amino acid residue. Biochem Biophys Res Commun 160(3):1015-1020
24. Koh JM, Chow SJ, Crossett B, Kuchel PW (2010) Mammalian peptide isomerase: platypus-type activity is present in mouse heart. Chem Biodivers 7(6):1603-1611. doi:10.1002/cbdv.20090 0300
25. Kovacs JM, Mant CT, Kwok SC, Osguthorpe DJ, Hodges RS (2006) Quantitation of the nearest-neighbour effects of amino acid sidechains that restrict conformational freedom of the polypeptide chain using reversed-phase liquid chromatography of synthetic model peptides with L- and D-amino acid substitutions. J Chromatogr A 1123(2):212-224. doi:10.1016/j.chroma.2006.04.092 (Pubitemid 44118308)
26. Kreil G (1997) D-amino acids in animal peptides. Annu Rev Biochem 66:337-345. doi:10.1146/annurev.biochem.66.1.337 (Pubitemid 27274660)
27. Kreil G, Barra D, Simmaco M, Erspamer V, Erspamer GF, Negri L, Severini C, Corsi R, Melchiorri P (1989) Deltorphin, a novel amphibian skin peptide with high selectivity and affinity for delta opioid receptors. Eur J Pharmacol 162(1):123-128 (Pubitemid 19074884)
28. Lai R, Zheng YT, Shen JH, Liu GJ, Liu H, Lee WH, Tang SZ, Zhang Y (2002) Antimicrobial peptides from skin secretions of Chinese red belly toad Bombina maxima. Peptides 23(3):427-435. doi: S0196978101006416[pii] (Pubitemid 34143258)
29. Lazarus LH, Bryant SD, Cooper PS, Salvadori S (1999) What peptides these deltorphins be. Prog Neurobiol 57(4):377-420. doi:S0301-0082(98)00050-1[pii] (Pubitemid 29057110)
30. Mangoni ML, Grovale N, Giorgi A, Mignogna G, Simmaco M, Barra D (2000) Structure-function relationships in bombinins H, antimicrobial peptides from Bombina skin secretions. Peptides 21(11):1673-1679. doi:S0196-9781(00)00316- 8[pii]
31. Mangoni ML, Papo N, Saugar JM, Barra D, Shai Y, Simmaco M, Rivas L (2006) Effect of natural L- to D-amino acid conversion on the organization, membrane binding, and biological function of the antimicrobial peptides bombinins H. Biochemistry 45(13):4266-4276. doi:10.1021/bi052150y
32. Maselli VM, Brinkworth CS, Bowie JH, Tyler MJ (2004) Hostdefence skin peptides of the Australian Common Froglet Crinia signifera: sequence determination using positive and negative ion electrospray mass spectra. Rapid Commun Mass Spectrom 18(18):2155-2161. doi:10.1002/rcm.1602 (Pubitemid 39222457)
33. Mignogna G, Simmaco M, Kreil G, Barra D (1993) Antibacterial and haemolytic peptides containing D-alloisoleucine from the skin of Bombina variegata. EMBO J 12(12):4829-4832 (Pubitemid 23330289)
34. Montecucchi PC, de Castiglione R, Piani S, Gozzini L, Erspamer V (1981) Amino acid composition and sequence of dermorphin, a novel opiate-like peptide from the skin of Phyllomedusa sauvagei. Int J Pept Protein Res 17(3):275-283 (Pubitemid 11102452)
35. Mor A, Delfour A, Sagan S, Amiche M, Pradelles P, Rossier J, Nicolas P (1989) Isolation of dermenkephalin from amphibian skin, a high-affinity delta-selective opioid heptapeptide containing a D-amino acid residue. FEBS Lett 255(2):269-274. doi: 0014-5793(89)81104-4[pii] (Pubitemid 19234511)
36. Negri L, Melchiorri P, Lattanzi R (2000) Pharmacology of amphibian opiate peptides. Peptides 21(11):1639-1647. doi:S0196-9781 (00)00295-3[pii]
37. Ohta N, Kubota I, Takao T, Shimonishi Y, Yasuda-Kamatani Y, Minakata H, Nomoto K, Muneoka Y, Kobayashi M (1991) Fulicin, a novel neuropeptide containing a D-amino acid residue isolated from the ganglia of Achatina fulica. Biochem Biophys Res Commun 178(2):486-493. doi:0006-291X(91)90133-R[pii]
38. Ollivaux C, Gallois D, Amiche M, Boscameric M, Soyez D (2009) Molecular and cellular specificity of post-translational aminoacyl isomerization in the crustacean hyperglycaemic hormone family. FEBS J 276(17):4790-4802. doi:10.1111/j.1742-4658. 2009.07180.x
39. Perry SJ, Yi-Kung Huang E, Cronk D, Bagust J, Sharma R, Walker RJ, Wilson S, Burke JF (1997) A human gene encoding morphine modulating peptides related to NPFF and FMRFamide. FEBS Lett 409(3):426-430. doi:S0014-5793(97)00557-7[pii] (Pubitemid 27285899)
40. Schonwetter BS, Stolzenberg ED, Zasloff MA (1995) Epithelial antibiotics induced at sites of inflammation. Science 267(5204): 1645-1648
41. Simmaco M, Kreil G, Barra D (2009) Bombinins, antimicrobial peptides from Bombina species. Biochim Biophys Acta 1788(8):1551-1555. doi:10.1016/j.bbamem. 2009.01.004
42. Smith GG, Reddy GV (2002) Effect of the side chain on the racemization of amino acids in aqueous solution. J Org Chem 54(19):4529-4535. doi:10.1021/jo00280a017
43. Soyez D, Van Herp F, Rossier J, Le Caer JP, Tensen CP, Lafont R (1994) Evidence for a conformational polymorphism of invertebrate neurohormones. D-amino acid residue in crustacean hyperglycemic peptides. J Biol Chem 269 (28):18295-18298 (Pubitemid 24224051)
44. Soyez D, Toullec JY, Ollivaux C, Geraud G (2000) L to D amino acid isomerization in a peptide hormone is a late post-translational event occurring in specialized neurosecretory cells. J Biol Chem 275(48):37870-37875. doi:10.1074/jbc.M007302200[pii] (Pubitemid 32004905)
45. Tang YQ, Selsted ME (1993) Characterization of the disulfide motif in BNBD-12, an antimicrobial beta-defensin peptide from bovine neutrophils. J Biol Chem 268(9):6649-6653 (Pubitemid 23099369)
46. Torres AM, Tsampazi C, Geraghty DP, Bansal PS, Alewood PF, Kuchel PW (2005) D-amino acid residue in a defensin-like peptide from platypus venom: effect on structure and chromatographic properties. Biochem J 391(Pt 2):215-220. doi:10.1042/BJ20050900 (Pubitemid 41532417)
47. Torres AM, Tsampazi M, Tsampazi C, Kennett EC, Belov K, Geraghty DP, Bansal PS, Alewood PF, Kuchel PW (2006) Mammalian L-to-D-amino-acid-residue isomerase from platypus venom. FEBS Lett 580(6):1587-1591. doi:10.1016/j. febslet. 2006.01.089 (Pubitemid 43290355)
48. Torres AM, Tsampazi M, Kennett EC, Belov K, Geraghty DP, Bansal PS, Alewood PF, Kuchel PW (2007) Characterization and isolation of L-to-D-amino-acid-residue isomerase from platypus venom. Amino Acids 32(1):63-68. doi:10.1007/s00726-006- 0346-6 (Pubitemid 44866569)
49. Wechselberger C (1998) Cloning of cDNAs encoding new peptides of the dermaseptin-family. Biochim Biophys Acta 1388(1):279-283. doi:S0167-4838(98) 00202-7[pii] (Pubitemid 28468629)
50. 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(1):41-43. doi: S0014-5793(98)00545-6[pii] (Pubitemid 28281242)
51. Zangger K, Gößler R, Khatai L, Lohner K, Jilek A (2008) Structures of the glycine-rich diastereomeric peptides bombinin H2 and H4. Toxicon 52(2):246-254. doi:10.1016/j.toxicon.2008.05.011