A novel peptide from the ACEI/BPP-CNP precursor in the venom of Crotalus durissus collilineatus

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 144, Issue 2, 2006, Pages 107-121

  Higuchi, Shigesada ^a,e   Murayama, Nobuhiro ^a   Saguchi, Ken ichi ^a   Ohi, Hiroaki ^a   Fujita, Yoshiaki ^a   da Silva Jr , Nelson Jorge ^b   de Siqueira, Rodrigo José Bezerra ^c   Lahlou, Saad ^c   Aird, Steven D ^d  

^a SHOWA UNIVERSITY   (Japan)

^b PONTIFÍCIA UNIVERSIDADE CATÓLICA DE GOIÁS   (Brazil)

^c DEPARTAMENTO DE MICOLOGIA   (Brazil)

^d NORFOLK STATE UNIVERSITY   (United States)

^e SOJO UNIVERSITY   (Japan)

Author keywords

Anaphylatoxin C3a; Angiotensin converting enzyme inhibitors; Bradykinin potentiating peptides; Crotalus durissus collilineatus; Crotalus viridis viridi; Hypotensive peptides; Rattlesnake venoms

Indexed keywords

ANAPHYLATOXIN; COMPLEMENT COMPONENT C3 RECEPTOR; COMPLEMENT COMPONENT C3A; COMPLEMENTARY DNA; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; NATRIURETIC PEPTIDE TYPE C; PEPTIDE; PROLINE; PYROGLUTAMIC ACID; SNAKE VENOM; SPACER DNA; THREONYLPROLYLPROLYLLANYLGLYCYLPROLYLASPARTYLGLYCYLGLYCLPROLYLARGININE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CROTALUS DURISSUS COLLILINEATUS; DNA DETERMINATION; FRACTIONATION; GENE SEQUENCE; HYPOTENSION; MALE; MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SNAKE; VALIDATION PROCESS;

BOTHROPS JARARACA; CROTALUS DURISSUS COLLILINEATUS; CROTALUS VIRIDIS; CROTALUS VIRIDIS VIRIDIS; GLOYDIUS BLOMHOFFI;

EID: 33751011324     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2006.04.006     Document Type: Article

References (90)

1. Aird S.D. A quantitative assessment of variation in venom constituents within and between three nominal rattlesnake subspecies. Toxicon 23 (1985) 1000-1004
2. Aird S.D. Ophidian envenomation strategies and the role of purines. Toxicon 40 (2002) 335-393
3. Aird S.D. Taxonomic distribution and quantitative analysis of free purine and pyrimidine nucleosides in snake venoms. Comp. Biochem. Physiol. 140 (2005) 109-126
4. Bhoola K.D., Figueroa C.D., and Worthy K. Bioregulation of kinins: kallikreins, kininogens, and kininases. Physiol. Rev. 44 (1992) 1-80
5. Bjarnason J.B., and Tu A.T. Hemorrhagic toxins from Western diamondback rattlesnake (Crotalus atrox) venom: isolation and characterization of five toxins and the role of zinc in hemorrhagic toxin e. Biochemistry 17 (1978) 3395-3404
6. Bjarnason J.B., Barish A., Direnzo G.S., Campbell R., and Fox J.W. Kallikrein-like enzymes from Crotalus atrox venom. J. Biol. Chem. 258 (1983) 12566-12573
7. Bode-Böger S.M., Böger R.H., Creutzig A., Tsikas D., Gutzki F.M., Alexander K., and Frölich J.C. l-arginine infusion decreases peripheral arterial resistance and inhibits platelet aggregation in healthy subjects. Clin. Sci. (Lond.) 87 (1994) 303-310
8. Bokisch V.A., and Muller-Eberhard H.J. Anaphylatoxin inactivator of human plasma: its isolation and characterization as a carboxypeptidase. J. Clin. Invest. 49 (1970) 2427-2436
9. Bragança B.M., Patel N.T., and Badrinath P.G. Isolation and properties of a cobra venom factor selectively cytotoxic to Yoshida sarcoma cells. Biochim. Biophys. Acta 136 (1967) 508-520
10. Caporale L.H., Tippett P.S., Erickson B.W., and Hugli T.E. The active site of C3a anaphylatoxin. J. Biol. Chem. 255 (1980) 10758-10763
11. Chi C.W., Wang S.Z., Xu L.G., Wang M.Y., Lo S.S., and Huang W.D. Structure-function studies on the bradykinin potentiating peptide from Chinese snake venom (Agkistrodon halys Pallas). Peptides 6 Suppl. 3 (1985) 339-342
12. Cintra A.C., Vieira C.A., and Giglio J.R. Primary structure and biological activity of bradykinin potentiating peptides from Bothrops insularis snake venom. J. Protein Chem. 9 (1990) 221-227
13. Damas J., Garbacki N., and Lefèbvre P.J. Does insulin release kinins in rats?. Eur. J. Pharmacol. 525 (2005) 154-160
14. del Balzo U., Polley M.J., and Levi R. Activation of the third complement component (C3) and C3a generation in cardiac anaphylaxis: histamine release and associated inotropic and chronotropic effects. J. Pharmacol. Exp. Ther. 246 (1988) 911-916
15. del Balzo U., Polley M.J., and Levi R. C3a-induced contraction of guinea pig ileum consists of two components: fast histamine-mediated and slow prostanoid-mediated. J. Pharmacol. Exp. Ther. 248 (1989) 1003-1009
16. Ember J.A., and Hugli T.E. Complement factors and their receptors. Immunopharmacology 38 (1997) 3-15
17. Fabiano R.J., and Tu A.T. Purification and biochemical study of viriditoxin, tissue damaging toxin, from prairie rattlesnake venom. Biochemistry 20 (1981) 21-27
18. Ferreira S.H. A bradykinin-potentiating factor (BPF) present in the venom of Bothrops jararaca. Br. J. Pharmacol. 24 (1965) 163-169
19. Ferreira S.H., Bartelt D.C., and Greene L.J. Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 9 (1970) 2583-2593
20. Ferreira L.A., Henriques O.B., Lebrun I., Batista M.B., Prezoto B.C., Andreoni A.S., Zelnik R., and Habermehl G. Biologically active peptides from Bothrops jararacussu venom. Agents Actions Suppl. 36 (1992) 209-214
21. Ferreira L.A., Henriques O.B., Lebrun I., Batista M.B., Prezoto B.C., Andreoni A.S., Zelnik R., and Habermehl G. A new bradykinin-potentiating peptide (peptide P) isolated from the venom of Bothrops jararacussu (jararacuçu tapete, urutu dourado). Toxicon 30 (1992) 33-40
22. Ferreira L.A., Mollring T., Lebrun F.L., Raida M., Znottka R., and Habermehl G.G. Structure and effects of a kinin potentiating fraction F (AppF) isolated from Agkistrodon piscivorus piscivorus venom. Toxicon 33 (1995) 1313-1319
23. Ferreira L.A., Galle A., Raida M., Schrader M., Lebrun I., and Habermehl G. Isolation: analysis and properties of three bradykinin-potentiating peptides (BPP-II, BPP-III, and BPP-V) from Bothrops neuwiedi venom. J. Protein Chem. 17 (1998) 285-289
24. Ferreira L.A., Auer H., Haslinger E., Fedele C., and Habermehl G.G. Spatial structures of the bradykinin potentiating peptide F from Agkistrodon piscivorus piscivorus venom. Toxicon 37 (1999) 661-676
25. Giovanni de Simone S., Aguiar A.S., Gimenez A.R., Novellino K., and de Moura R.S. Purification, properties, and N-terminal amino acid sequence of a kallikrein-like enzyme from the venom of Lachesis muta rhombeata (Bushmaster). J. Protein Chem. 16 (1997) 809-818
26. Graham R.L.J., Graham C., McClean S., Chen T., O'Rourke M., Hirst D., Theakston D., and Shaw C. Identification and functional analysis of a novel bradykinin inhibitory peptide in the venoms of World Crotalinae pit vipers. Biochem. Biophys. Res. Commun. 338 (2005) 1587-1592
27. Greene L.J., Camargo A.C., Krieger E.M., Stewart J.M., and Ferreira S.H. Inhibition of the conversion of angiotensin I to II and potentiation of bradykinin by small peptides present in Bothrops jararaca venom. Circ. Res. 31 Suppl 2 (1972) 62-71
28. Harbeck H.T., and Mentlein R. Aminopeptidase P from rat brain. Purification and action on bioactive peptides. Eur. J. Biochem. 198 (1991) 451-458
29. Henriques O.B., Fichman M., and Beraldo W.T. Bradykinin releasing factor from Bothrops jararaca venom. Nature 187 (1960) 414-415
30. Higuchi S., Murayama N., Saguchi K., Ohi H., Fujita Y., Camargo A.C., Ogawa T., Deshimaru M., and Ohno M. Bradykinin-potentiating peptides and C-type natriuretic peptides from snake venom. Immunopharmacology 44 (1999) 129-135
31. Higuchi S., Murayama N., Saguchi K., Ohi H., Fujita Y., da Silva Jr. N.J., and Aird S.D. A novel peptide from the ACEI/BPP-CNP precursor in the venom of Crotalus durissus collilineatus. Abstracts of the 14th International Congress of the International Society on Toxinology, Adelaide (2003) 58
32. Higuchi S., Murayama N., Saguchi K., Ohi H., Fujita Y., da Silva N.J., and Aird S.D. Novel peptides from the ACEI/BPP-CNP precursor in crotaline snakes. In: Alewood P., Bulet P., Ganz T., Hoffman P., Menez A., Noukakis D., Offord R., Pennington M., Stocklin R., and Wells T. (Eds). Natural Peptides to Drugs - Abstracts of 1st International Congress, Dimitrios Noukakis and Reto Stocklin Associes, Switzerland (2004) 43-45
33. Higuchi S., Murayama N., Saguchi K., Ohi H., Fujita Y., da Silva N.J., and Aird S.D. Novel peptides in the venoms of crotaline snake. In: Shimohigashi Y. (Ed). Peptide Science 2004 (2005), The Japanese Peptide Society, Osaka 89-90
34. Hishikawa K., Nakaki T., Tsuda M., Esumi H., Ohshima H., Suzuki H., Saruta T., and Kato R. Effect of systemic l-arginine administration on hemodynamics and nitric oxide release in man. Jpn. Heart J. 33 (1992) 41-48
35. Hishikawa K., Nakaki T., Suzuki H., Kato R., and Saruta T. l-arginine as an antihypertensive agent. J. Cardiovasc. Pharmacol. 20 Suppl 12 (1992) S196-S197
36. 2-receptors mediate the pressor and renal hemodynamic effects of intravenous bradykinin in conscious rats. J. Auton. Nerv. Syst. 75 (1999) 7-15
37. Huey R., Fukuoka Y., Hoeprich Jr. P.D., and Hugli T.E. Cellular receptors to the anaphylatoxins C3a and C5a. Biochem. Soc. Symp. 51 (1986) 69-81
38. Hugli T.E. Structure and function of C3a anaphylatoxin. Curr. Top. Microbiol. Immunol. 153 (1990) 181-208
39. Hugli T.E., and Müller-Eberhard H.J. Anaphylatoxins: C3a and C5a. Adv. Immunol. 26 (1978) 1-53
40. Hugli T.E., Stimler N.P., Gerard C., and Moon K.E. Possible role of serum anaphylatoxins in hypersensitivity reactions. Int. Arch. Allergy Appl. Immunol. 66 Suppl 1 (1981) 113-120
41. Ianzer D., Konno K., Marques-Porto R., Vieira Portaro F.C., Stöcklin R., Martins de Camargo A.C., and Carvalho Pimenta D. Identification of five new bradykinin potentiating peptides (BPPs) from Bothrops jararaca crude venom by using electrospray ionization tandem mass spectrometry after a two-step liquid chromatography. Peptides 25 (2004) 1085-1092
42. Juillerat-Jeanneret L., Roth M., and Bargetzi J.P. Some properties of porcine carboxypeptidase N. Hoppe-Seyler Z. Physiol. Chem. 363 (1982) 51-58
43. Kato H., and Suzuki T. Bradykinin-potentiating peptides from the venom of Agkistrodon halys blomhoffii. Experientia 25 (1969) 694-695
44. Kato H., and Suzuki T. Structure of bradykinin-potentiating peptide containing tryptophan from the venom of Agkistrodon halys blomhoffii. Experientia 26 (1970) 1205-1206
45. Kato H., and Suzuki T. Bradykinin-potentiating peptides from the venom of Agkistrodon halys blomhoffii. Isolation of five bradykinin potentiators and the amino acid sequences of two of them, potentiators B and C. Biochemistry 10 (1971) 972-980
46. Kato H., Iwanaga S., and Suzuki T. The isolation and amino acid sequences of new pyroglutamylpeptides from snake venoms. Experientia 22 (1966) 49-50
47. Kato H., Suzuki T., Okada K., Kimura T., and Sakakibara S. Structure of potentiator A, one of the five bradykinin potentiating peptides from the venom of Agkistrodon halys blomhoffii. Experientia 29 (1973) 574-575
48. Kitamura S., Carbini L.A., Carretero O.A., Simmons W.H., and Scicli A.G. Potentiation by aminopeptidase P of blood pressure response to bradykinin. Br. J. Pharmacol. 114 (1995) 6-7
49. Komori Y., and Sugihara H. Characterization of a new inhibitor for angiotensin converting enzyme from the venom of Vipera aspis aspis. Int. J. Biochem. 22 (1990) 767-771
50. Komori Y., Nikai T., and Sugihara H. Biochemical and physiological studies on a kallikrein-like enzyme from the venom of Crotalus viridis viridis (prairie rattlesnake). Biochim. Biophys. Acta 967 (1988) 92-102
51. Korthuis R.J., and Granger D.N. Reactive oxygen metabolites, neutrophils, and the pathogenesis of ischemic-tissue/reperfusion. Clin. Cardiol. 16 (1993) I19-I26
52. Legler D.F., Loetscher M., Jones S.A., Dahinden C.A., Arock M., and Moser B. Expression of high- and low-affinity receptors for C3a on the human mast cell line, HMC-1. Eur. J. Immunol. 26 (1996) 753-758
53. Lepow I.H., Willms-Kretschmer K., Patrick R.A., and Rosen F.S. Gross and ultrastructural observations on lesions produced by intradermal injection of human C3a in man. Am. J. Pathol. 61 (1970) 13-23
54. Maia L.G., Ramos M.C., Fernandes L., de Carvalho M.H.C., Campagnole-Santos M.J., and dos Santos R.A.S. Angiotensin-(1-7) antagonist A-779 attenuates the potentiation of bradykinin by captopril in rats. J. Cardiovasc. Pharmacol. 43 (2004) 685-691
55. Markland F.S., Kettner C., Schiffman S., Shaw E., Bajwa S.S., Reddy K.N., Kirakossian H., Patkos G.B., Theodor I., and Pirkle H. Kallikrein-like activity of crotalase, a snake venom enzyme that clots fibrinogen. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 1688-1692
56. Masuda K., Yoshioka M., Hinode D., and Nakamura R. Purification and characterization of arginine carboxypeptidase produced by Porphyromonas gingivalis. Infect. Immun. 70 (2002) 1807-1815
57. Michel G.H., Murayama N., Sada T., Nozaki M., Saguchi K., Ohi H., Fujita Y., Koike H., and Higuchi S. Two N-terminally truncated forms of C-type natriuretic peptide from habu snake venom. Peptides 21 (2000) 609-615
58. Monsinjon T., Gasque P., Chan P., Ischenko A., Brady J.J., and Fontaine M.C. Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. FASEB J. 17 (2003) 1003-1014
59. Murayama N., Hayashi M.A., Ohi H., Ferreira L.A., Hermann V.V., Saito H., Fujita Y., Higuchi S., Fernandes B.L., Yamane T., and de Camargo A.C. Cloning and sequence analysis of a Bothrops jararaca cDNA encoding a precursor of seven bradykinin-potentiating peptides and a C-type natriuretic peptide. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 1189-1193
60. Murayama N., Michel G.H., Yanoshita R., Samejima Y., Saguchi K., Ohi H., Fujita Y., and Higuchi S. cDNA cloning of bradykinin-potentiating peptides-C-type natriuretic peptide precursor, and characterization of the novel peptide Leu3-blomhotin from the venom of Agkistrodon blomhoffi. Eur. J. Biochem. 267 (2000) 4075-4080
61. Navar L.G., Inscho E.W., Majid S.A., Imig J.D., Harrison-Bernard L.M., and Mitchell K.D. Paracrine regulation of the renal microcirculation. Physiol. Rev. 76 (1996) 426-520
62. Ondetti M.A., Williams N.J., Sabo E.F., Pluscec J., Weaver E.R., and Kocy O. Angiotensin-converting enzyme inhibitors from the venom of Bothrops jararaca. Isolation, elucidation of structure, and synthesis. Biochemistry 10 (1971) 4033-4039
63. Orawski A.T., and Simmons W.H. Purification and properties of membrane-bound aminopeptidase P from rat lung. Biochemistry 34 (1995) 11227-11236
64. Orawski A.T., Susz J.P., and Simmons W.H. Aminopeptidase P from bovine lung: solubilization, properties, and potential role in bradykinin degradation. Mol. Cell. Biochem. 75 (1987) 123-132
65. Ownby C.L., and Colberg T.R. Characterization of the biological and immunological properties of fractions of prairie rattlesnake (Crotalus viridis viridis) venom. Toxicon 25 (1987) 1329-1342
66. Politi V., De Luca G., Di Stazio G., Schinina E., and Bossa F. A new peptide from Crotalus atrox snake venom. Peptides 6 Suppl. 3 (1985) 343-346
67. Polley M.J., and Nachman R.L. Human platelet activation by C3a and C3a des-arg. J. Exp. Med. 158 (1983) 603-615
68. Puri V.N., and Saha S. Comparison of acute cardiovascular effects of cadmium and captopril in relation to oxidant and angiotensin-converting enzyme activity in rats. Drug Chem. Toxicol. 26 (2003) 213-218
69. Ryan J.W., Berryer P., Chung A.Y., and Sheffy D.H. Characterization of rat pulmonary vascular aminopeptidase P in vivo: role in the inactivation of bradykinin. J. Pharmacol. Exp. Ther. 269 (1994) 941-947
70. Sacks T., Moldow C.F., Craddock P.R., Bowers T.K., and Jacob H.S. Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes. An in vitro model of immune vascular damage. J. Clin. Invest. 61 (1978) 1161-1167
71. Samejima Y., Iwasaki E., and Yanoshita R. Pharmacological characterization of contraction induced by blomhotin, a novel peptide from the venom of Agkistrodon halys blomhoffi, in rat fundus. Abstracts of the 6th Asia-Pacific Congress on Animal, Plant and Microbial Toxins (2002) 117
72. Schaeffer Jr. R.C., Pattabhiraman T.R., Carlson R.W., Russell F.E., and Weil M.H. Cardiovascular failure produced by a peptide from the venom of the southern Pacific rattlesnake, Crotalus viridis helleri. Toxicon 17 (1979) 447-453
73. Schmidt H.H., Klein M.M., Niroomand F., and Bohme E. Is arginine a physiological precursor of endothelium-derived nitric oxide?. Eur. J. Pharmacol. 148 (1988) 293-295
74. Shah S.V., Baricos W.H., and Basci A. Degradation of human glomerular basement membrane by stimulated neutrophils. Activation of a metalloproteinase(s) by reactive oxygen metabolites. J. Clin. Invest. 79 (1987) 25-31
75. 2 bond of bradykinin by a human lung peptidase: isolation, characterization, and inhibition by several beta-lactam antibiotics. Proc. Soc. Exp. Biol. Med. 175 (1984) 503-509
76. Soares M.R., Oliveira-Carvalho A.L., Wermelinger L.S., Zingali R.B., Ho P.L., Junqueira-de-Azevedo I.D., and Vasconcelos Diniz M.R. Identification of novel bradykinin-potentiating peptides and C-type natriuretic peptide from Lachesis muta venom. Toxicon 46 (2005) 31-38
77. Stimler N.P., Hugli T.E., and Bloor C.M. Pulmonary injury induced by C3a and C5a anaphylatoxins. Am. J. Pathol. 100 (1980) 327-338
78. Suzuki M., and Satoh S. Converting enzyme inhibition and modulation of plasma renin activity with captopril in anesthetized rats. Arch. Int. Pharmacodyn. Ther. 253 (1981) 121-136
79. Tabrizchi R., and Lupichuk S.M. The effects of losartan and captopril on vasopressor actions of cirazoline in the absence and presence of SZL-49 and nifedipine. J. Cardiovasc. Pharmacol. 26 (1995) 137-144
80. Till G.O., Johnson K.J., Kunkel R., and Ward P.A. Intravascular activation of complement and acute lung injury. Dependency on neutrophils and toxic oxygen metabolites. J. Clin. Invest. 69 (1982) 1126-1135
81. Unson C.G., Erickson B.W., and Hugli T.E. Active site of C3a anaphylatoxin: contributions of the lipophilic and orienting residues. Biochemistry 23 (1984) 585-589
82. Ward P.E., Chow A., and Drapeau G. Metabolism of bradykinin agonists and antagonists by plasma aminopeptidase P. Biochem. Pharmacol. 42 (1991) 721-727
83. Watson J.W., Drazen J.M., and Stimler-Gerard N.P. Synergism between inflammatory mediators in vivo. Induction of airway hyperresponsiveness to C3a in the guinea pig. Am. Rev. Respir. Dis. 137 (1988) 636-640
84. Wermelinger L.S., Dutra D.L.S., Oliveira-Carvalho A.L., Soares M.R., Bloch Jr. C., and Zingali R.B. Fast analysis of low molecular mass compounds present in snake venom: identification of ten new pyroglutamate-containing peptides. Rapid Commun. Mass Spectrom. 19 (2005) 1703-1708
85. Yanoshita R. Structure and biological activities of peptides in the venom of snakes and sea anemones. Seikagaku 75 (2003) 133-137
86. Yanoshita R., Kasuga A., Inoue S., Ikeda K., and Samejima Y. Blomhotin: a novel peptide with smooth muscle contractile activity identified in the venom of Agkistrodon halys blomhoffii. Toxicon 37 (1999) 1761-1770
87. Yanoshita R., Iwasaki E., Kambe T., and Samejima Y. Structure-activity studies of analogues of blomhotin mediating contraction of rat fundus. Biol. Pharm. Bull. 23 (2000) 1379-1381
88. Yanoshita R., Doi Y., and Samejima Y. Blomhotin-related peptides increase vascular permeability through mast cell activation. Abstracts of the 6th Asia-Pacific Congress on Animal, Plant and Microbial Toxins (2002) 118
89. Yoshimoto T., Orawski A.T., and Simmons W.H. Substrate specificity of aminopeptidase P from Escherichia coli: comparison with membrane-bound forms from rat and bovine lung. Arch. Biochem. Biophys. 311 (1994) 28-34
90. Younger J.G., Sasaki N., Delgado J., Ko A.A.C., Nghiem T.X., Waite M.D., Till G.O., and Ward P.A. Systemic and lung physiological changes in rats after intravascular activation of complement. J. Appl. Physiol. 90 (2001) 2289-2295