Bj-PRO-5a, a natural angiotensin-converting enzyme inhibitor, promotes vasodilatation mediated by both bradykinin B2 and M1 muscarinic acetylcholine receptors

Biochemical Pharmacology

Volumn 81, Issue 6, 2011, Pages 736-742

  Morais, K L P ^a,b   Hayashi, M A F ^b   Bruni, F M ^a   Lopes Ferreira, M ^a   Camargo, A C M ^a,c   Ulrich, H ^c   Lameu, C ^a,c  

^a INSTITUTO BUTANTAN   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Bradykinin B2 receptor; Bradykinin potentiating peptides; Muscarinic acetylcholine receptor; Nitric oxide; Proline rich oligopeptide

Indexed keywords

BATROXOBIN; BOTHROPS JARARACA PROLINE RICH OLIGOPEPTIDE 5A; BRADYKININ B2 RECEPTOR; CALCIUM ION; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; MUSCARINIC M1 RECEPTOR; NITRIC OXIDE; UNCLASSIFIED DRUG;

ANALYZER; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CHEMOLUMINESCENCE; CONTROLLED STUDY; CREMASTER MUSCLE; DIAGNOSTIC IMAGING; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASODILATATION;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; BOTHROPS; CHO CELLS; CRICETINAE; CRICETULUS; CROTALID VENOMS; DOSE-RESPONSE RELATIONSHIP, DRUG; HEK293 CELLS; HUMANS; MALE; MICE; MICE, INBRED BALB C; PROLINE-RICH PROTEIN DOMAINS; RECEPTOR, BRADYKININ B2; RECEPTOR, MUSCARINIC M1; VASODILATION;

EID: 79951956746     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.12.016     Document Type: Article

References (58)

1. Ferreira SH, Barteld DC, Greene LJ. Isolation of bradykinin potentiating peptides from Bothrops jararaca venom. Biochemistry 1970;9(13):2583-93.
2. Ondetti MA, Cushman DW. Angiontesin-converting enzyme inhibitions: biochemical properties and biological actions. CRC Crit Rev Biochem 1984;16(4):381-411.
3. Stewart JM, Ferreira SH, Greene LJ. Bradykinin potentiating peptide PCA-Lys-Trp-Ala-Pro: an inhibitor of the pulmonary inactivation of bradykinin and conversion of angiotensin I to II. Biochem Pharmacol 1971;20:1557-67.
4. Cushman DW, Cheung HS, Sabo EF, Ondetti MA. Design of potent competitive inhibitors of angiotensin-converting enzyme. Carboxyalkanoyl and mercaptoalkanoyl amino acids. Biochemistry 1977;16(25):5484-91.
5. Ondetti MA, Cushman DW. Inhibition of the renin-angiotensin system. A new approach to the therapy of hypertension. J Med Chem 1981;24(4):355-61. (Pubitemid 11151637)
6. Smith CG, Vane JR. The discovery of captopril. FASEB J 2003;17(8):788-9. (Pubitemid 36538651)
7. Ondetti MA,Williams NJ, Sabo EF, Pluscec J, Weaver ER, Kocy O. Angiotensins-converting enzyme inhibitors from the venom of Bothrops jararaca. Isolation, elucidation of structure, and synthesis. Biochemistry 1971;19(22):4033-9.
8. Murayama N, Hayashi MA, Ohi H, Ferreira LA, Fernandes BL, Yamane T, et al. Cloning and sequence of a Bothrops jararaca cDNA encoding a precursor of seven bradykinin-potentiating peptides and a C-type natriuretic peptide. Proc Natl Acad Sci USA 1997;94:1189-93. (Pubitemid 27087826)
9. Hayashi MAF, Camargo AC. The Bradykinin-potentiating peptides from venom gland and brain of Bothrops jararaca contain highly site specific inhibitors of the somatic angiotensin-converting enzyme. Toxicon 2005;45(8):1163-70. (Pubitemid 40732588)
10. Wei L, Alhenc-Gelas F, Corvol P, Clauser E. The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J Biol Chem 1991;266(14):9002-8. (Pubitemid 21906610)
11. Coates D. The angiotensin converting enzyme (ACE). Int J Biochem Cell Biol 2003;35(6):769-73. (Pubitemid 36379317)
12. Ianzer D, Santos RAS, Etelvino GM, Xavier CH, de Almeida Santos J, Mendes EP, et al. Do the cardiovascular effects of angiotensina-converting enzyme (ACE) I involve ACE-independent mechanisms? New insights from proline-rich peptides of Bothrops jararaca. J Pharm Exp Ther 2007;322:795-805. (Pubitemid 47105778)
13. Guerreiro JR, Lameu C, Oliveira EF, Klitzke CF, Linares E, Ohara A, et al. Argininosuccinate synthetase is a novel functional target for a snake venom anti-hypertensive peptide: role in arginine and nitric oxide production. J Biol Chem 2009;30(284):20022-33.
14. Lameu C, Hayashi MA, Guerreiro JR, Oliveira EF, Lebrun I, Pontieri V, et al. The central nervous system as target for antihypertensive actions of a proline-rich peptide from Bothrops jararaca venom. Cytometry A 2010;77(3):220-30.
15. Umans JG, Levi R. Nitric oxide in the regulation of blood flow and arterial pressure. Annu Rev Physiol 1995;57:771-90.
16. Busse R, Fleming I. Regulation and functional consequences of endothelial nitric oxide formation. Ann Med 1995;27(3):331-71.
17. Rowe J, Campbell S, Gallery ED. Nitric oxide production by decidual endothelial cells is not reduced in preeclampsia. Hypertens Pregnancy 2003;22(1):63-75.
18. Solomonson LP, Flam BR, Pendleton LC, Goodwin BL, Eichler DC. The caveolar nitric oxide synthase/arginine regeneration system for NO production in endothelial cells. J Exp Biol 2003;206:2083-7. (Pubitemid 36761811)
19. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci 1990;87(2):682-5.
20. Schmidt HH, Pollock JS, Nakane M, Gorsky LD, Förstermann U, Murad F. Purification of a soluble isoform of guanylyl cyclase-activating-factor synthase. Proc Natl Acad Sci USA 1991;88(2):365-9. (Pubitemid 21915465)
21. Flam BR, Eichler DC, Solomonson LP. Endothelial nitric oxide production is tightly coupled to the citrulline-NO cycle. Nitric Oxide 2007;17:115-21. (Pubitemid 47513850)
22. Ryberg AT, Selberg H, Soukup O, Gradin K, Tobin G. Cholinergic submandibular effects and muscarinic receptor expression in blood vessels of the rat. Arch Oral Biol 2008;53(7):605-16.
23. Gomes CL, Konno K, Conceição IM, Ianzer D, Yamanouye N, Prezoto BC, et al. Identification of novel bradykinin-potentiating peptides (BPPs) in the venom gland of a rattlesnake allowed the evaluation of the structure-function relationship of BPPs. Biochem Pharmacol 2007;74:1350-60. (Pubitemid 47445446)
24. Feelisch M, Rassaf T, Mnaimneh S, Singh N, Bryan NS, Jourd'Heuil D, et al. Concomitant S-, N-, and heme-nitros(yl)ation in biological tissues and fluids: implications for the fate of NO in vivo. FASEB J 2002;16:1775-85.
25. Baez S. An open cremaster muscle preparation for the study of blood vessels by in vivo microscopy. Microvasc Res 1973;5:384-96.
26. Lomonte B, Lundgren J, Johansson B, Bagge U. The dynamics of local tissue damage induced by Bothrops asper snake venom and myotoxin II on the mouse cremaster muscle: an intravital and electron microscopic study. Toxicon 1994;34:41-55. (Pubitemid 24047960)
27. Mundell SJ, Benovic JL. Selective regulation of endogenous G protein-coupled receptors by arrestins in HEK293 cells. J Biol Chem 2000;275(17):12900-8. (Pubitemid 30241446)
28. Kramarenko II, Bunni MA, Morinelli TA, Raymond JR, Garnovskaya MN. Identification of functional bradykinin B(2) receptors endogenously expressed in HEK293 cells. Biochem Pharmacol 2009;77(2):269-76.
29. Martins AH, Alves JM, Trujillo CA, Schwindt TT, Barnabé GF, Motta FL, et al. Kinin-B2 receptor expression and activity during differentiation of embryonic rat neurospheres. Cytometry A 2008;73(4):361-8. (Pubitemid 351522119)
30. Resende RR, Gomes KN, Adhikari A, Britto LR, Ulrich H. Mechanism of acetylcholine-induced calcium signaling during neuronal differentiation of P19 embryonal carcinoma cells in vitro. Cell Calcium 2008;43(2):107-21.
31. Tzemos N, Lim PO, Macdonald TM. Exercise blood pressure and endothelial dysfunction in hypertension. Int J Clin Pract 2009;63(2):202-6.
32. Erdös EG, Marcic BM. Kinins, receptors, kininases and inhibitors-where did they lead us? Biol Chem 2001;382(1):43-7.
33. Mueller S, Gothe R, Siems WD, Vietinghoff G, Paegelow I, Reissmann S. Potentiation of bradykinin actions by analogues of the bradykinin potentiating nonapeptide BPP9alpha. Peptides 2005;26(7):1235-47.
34. Antonaccio MJ, Rubin B, Horovitz ZP, Laffan RJ, Goldberg ME, High JP, et al. Effects of chronic treatment with Captopril (SQ 14,225), an orally active inhibitor of angiotensin I-converting enzyme, in spontaneously hypertensive rats. Jpn J Pharmacol 1979;29:285-94.
35. Marks ES, Bing RF, Thurston H, Swales JD. Vasodepressor property of the converting enzyme inhibitor captopril (SQ 14 225): the role of factors other than renin-angiotensin blockade in the rat. Clin Sci 1980;58:1-6.
36. Mittra S, Singh M. Possible mechanism of captopril induced endothelium-dependent relaxation in isolated rabbit aorta. Mol Cell Biochem 1998;183(1-2):63-7. (Pubitemid 28263888)
37. Houben AJ, Kroon AA, de Haan CH, Fuss-Lejeune MJ, de Leeuw PW. Quinaprilat-induced vasodilatation in forearm vasculature of patients with essential hypertension: comparison with enalaprilat. Cardiovasc Drugs Ther 2000;14:657-63. (Pubitemid 32217189)
38. Mueller S, Paegelow I, Reissmann S. Hypothesized and found mechanisms for potentiation of bradykinin actions. Signal Transduct 2006;6:5-18. (Pubitemid 43374161)
39. Negraes PD, Lameu C, Hayashi MA, Melo RL, Camargo AC, Ulrich H. The snake venom peptide Bj-PRO-7a is a M1 muscarinic acetylcholine receptor agonist. Cytometry A 2011;79(1):77-83.
40. Shen LJ, Beloussow K, Shen WC. Accessibility of endothelial and inducible nitric oxide synthase to the intracellular citrulline-arginine regeneration pathway. Biochem Pharmacol 2005;69:97-104. (Pubitemid 39592876)
41. Noda M, Kariura Y, Amano T, Manago Y. Kinin receptors in cultured rat microglia. Neurochem Int 2004;45:437-42. (Pubitemid 38625633)
42. Vanhoutte PM. Endothelial adrenoceptors. J Cardiovasc Pharmacol 2001;38(5):796-808. (Pubitemid 32983286)
43. Wess J. Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 2004;44:423-50. (Pubitemid 38263848)
44. Padley JR, Overstreet DH, Pilowsky PM, Goodchild AK. Impaired cardiac and sympathetic autonomic control in rats differing in acetylcholine receptor sensitivity. Am J Physiol Heart Circ Physiol 2005;289(5):1985-92.
45. LanzafameAA, Christopoulos A, Mitchelson F. Cellular signalingmechanisms for muscarinic acetylcholine receptors. Receptors Channels 2003;9(4):241-60. (Pubitemid 37069446)
46. Servent D, Fruchart-Gaillard C. Muscarinic toxins: tools for the study of the pharmacological and functional properties of muscarinic receptors. J Neurochem 2009;109(5):1193-202.
47. Turner AJ, Hooper NM. The angiotensin-converting enzyme gene family: genomics and pharmacology. Trends Pharmacol Sci 2002;23(4):177-83. (Pubitemid 34270600)
48. Bachvarov DR, Houle S, Bachvarova M, Bouthillier J, Adam A, Marceau F. Bradykinin B2 receptor endocytosis, recycling, and down-regulation assessed using green fluorescent protein conjugates. J Pharmacol Exp Ther 2001;297:19-26. (Pubitemid 32242559)
49. Silva CA, Portaro FC, Fernandes BL, Ianzer DA, Guerreiro JR, Gomes CL, et al. Tissue distribution in mice of BPP 10c, a potent proline-rich anti-hypertensive peptide of Bothrops jararaca. Toxicon 2008;51:515-23.
50. Minshall RD, Tan F, Nakamura F, Rabito SF, Becker RP, Marcic B, et al. Potentiation of the actions of bradykinin by angiotensin I-converting enzyme inhibitors. The role of expressed human bradykinin B2 receptors and angiotensin I-converting enzyme in CHO cells. Circ Res 1997;81(5):848-56.
51. Prezeau L, Rives ML, Comps-Agrar L, Maurel D, Kniazeff J, Pin JP. Functional crosstalk between GPCRs: with or without oligomerization. Curr Opin Pharmacol 2010;10(1):6-13.
52. Fernandez JH, Hayashi MA, Camargo AC, Neshich G. Structural basis of the lisinopril-binding specificity in N- and C-domains of human somatic ACE. Biochem Biophys Res Commun 2003;308(2):219-26. (Pubitemid 36937169)
53. Fernandez JH, Neshich G, Camargo AC. Using bradykinin-potentiating peptide structures to develop new antihypertensive drugs. Genet Mol Res 2004;3(4):554-63. (Pubitemid 40318049)
54. Marcic B, Deddish PA, Jackman HL, Erdös EG. Enhancement of bradykinin and resensitization of its B2 receptor. Hypertension 1999;33(3):835-43. (Pubitemid 29140443)
55. Caccamo A, Oddo S, Billings LM, Green KN, Martinez-Coria H, Fisher A, et al. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 2006;49(5):671-82. (Pubitemid 43290127)
56. Sheffler DJ, Williams R, Bridges TM, Xiang Z, Kane AS, Byun NE, et al. A novel selective muscarinic acetylcholine receptor subtype 1 antagonist reduces seizures without impairing hippocampus-dependent learning. Mol Pharmacol 2009;76(2):356-68.
57. Conn PJ, Jones CK, Lindsley CW. Subtype-selective allosteric modulators of muscarinic receptors for the treatment of CNS disorders. Trends Pharmacol Sci 2009;30(3):148-55.
58. Langmead CJ, Watson J, Reavill C. Muscarinic acetylcholine receptors as CNS drug targets. Pharmacol Ther 2008;117(2):232-43.