Brain nitric oxide production by a proline-rich decapeptide from Bothrops jararaca venom improves baroreflex sensitivity of spontaneously hypertensive rats

Hypertension Research

Volumn 33, Issue 12, 2010, Pages 1283-1288

  Lameu, Claudiana ^a,b   Pontieri, Vera ^b   Guerreiro, Juliano R ^a   Oliveira, Eduardo F ^b,c   Da Silva, Carlos Alberto ^d   Giglio, Joyce M ^b   Melo, Robson L ^b   Campos, Ruy R ^c   De Camargo, Antonio Carlos Martins ^a   Ulrich, Henning ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d Natural and Human Sciences Center   (Brazil)

Author keywords

argininosuccinate synthase; baroreflex sensitivity; Bothrops jararaca venom; nitric oxide; proline rich oligopeptide

Indexed keywords

ARGININOSUCCINATE SYNTHASE; BATROXOBIN; METABOTROPIC RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROLINE RICH DECAPEPTIDE; PROLINE RICH PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CALCIUM TRANSPORT; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; GENE ACTIVATION; GENE EXPRESSION; HEART RATE; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; PRESSORECEPTOR REFLEX; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ARGININOSUCCINATE SYNTHASE; BAROREFLEX; BLOOD PRESSURE; BOTHROPS; BRAIN; CELLS, CULTURED; CROTALID VENOMS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION; HEART RATE; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, INBRED SHR; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 78649862205     PISSN: 09169636     EISSN: 13484214     Source Type: Journal    
DOI: 10.1038/hr.2010.208     Document Type: Article

References (40)

1. Umans JG, Levi R. Nitric oxide in the regulation of blood flow and arterial pressure. Annu Rev Physiol 1995; 57: 771-790.
2. Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 1995; 57: 683-706.
3. Souza HC, De Araújo JE, Martins-Pinge MC, Cozza IC, Martins-Dias DP. Nitric oxide synthesis blockade reduced the baroreflex sensitivity in trained rats. Auton Neurosci 2009; 150: 38-44.
4. Martins-Pinge MC, Garcia MR, Zoccal DB, Crestani CC, Pinge-Filho P. Differential influence of iNOS and nNOS inhibitors on rostral ventrolateralmedullary mediated cardiovascular control in conscious rats. Auton Neurosci 2007; 131: 65-69.
5. Galea E, Feinstein DL, Reis DJ. Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc Natl Acad Sci USA 1992; 89: 10945-10949.
6. Husson A, Brasse-Lagnel C, Fairand A, Renouf S, Lavoinne A. Argininosuccinate synthetase from the urea cycle to the citrulline-NO cycle. Eur J Biochem 2003; 270: 1987-1999.
7. Flam BR, Hartmann PJ, Harrell-Booth M, Solomonson LP, Eichler DC. Caveolar localization of arginine regeneration enzymes, argininosuccinate sythase, and lyase, with endothelial nitric oxide synthase. Nitric Oxide 2001; 5: 187-197.
8. Murayama N, Hayashi MA, Ohi H, Ferreira LA, Hermann VV, Saito H, Fujita Y, Higuchi S, Fernandes BL, Yamane T, de Camargo AC. 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 USA 1997; 94: 1189-1193.
9. Hayashi MA, Murbach AF, Ianzer D, Portaro FC, Prezoto BC, Fernandes BL, Silveira PF, Silva CA, Pires RS, Britto LR, Dive V, Camargo AC. The C-type natriuretic peptide precursor of snake brain contains highly specific inhibitors of the angiotensin-convert-ing enzyme. J Neurochem 2003; 85: 969-977.
10. Ianzer D, Santos RA, Etelvino GM, Xavier CH, de Almeida Santos J, Mendes EP, Machado LT, Prezoto BC, Dive V, de Camargo AC. Do the cardiovascular effects of angiotensin-converting enzyme (ACE) I involve ACE-independent mechanisms? new insights from proline-rich peptides of Bothrops jararaca. J Pharmacol Exp Ther 2007; 322: 795-805.
11. Guerreiro JR, Lameu C, Oliveira EF, Linares E, Augusto O, Lebrun I, Serrano SMT, Camargo ACM. Argininosuccninate synthase (AsS) is a novel target for a snake venom anti-hypertensive oligopeptide. J Biol Chem 2009; 284: 20022-20033.
12. Bunag RD, Walaszek EJ, Mueting N. Sex differences in reflex tachycardia induced by hypotensive drugs in unanesthetized rats. Am J Physiol 1975; 229: 652-656.
13. Silva CA, Portaro FC, Fernandes BL, Ianzer DA, Guerreiro JR, Gomes CL, Konno K, Serrano SM, Nascimento N, Camargo AC. Tissue distribution in mice of BPP 10c, a potent proline-rich anti-hypertensive peptide of Bothrops jararaca. Toxicon 2008; 51: 515-523.
14. Lameu C, Hayashi MA, Guerreiro JR, Oliveira EF, Lebrun I, Pontieri V, Morais KL, Camargo AC, Ulrich H. The central nervous system as target for antihypertensive actions of a proline-rich peptide from Bothrops jararaca venom. Cytometry A 2010; 77: 220-230.
15. Hayashi J, Takeda K, Kuwabara T, Takesako T, Itoh H, Hirata M, Tanabe S, Nakata T, Sasaki S, Nakagawa M. Clonidine improves central attenuation og the baroreflex in spontaneously hypertensive rats. Jpn Heart J 1993; 34: 333-339.
16. Szabo B, Fritz T, Wedzony K. Effects of imidazoline antihypertensive drugs on sympathetic tone and noradrenaline release in the prefrontal cortex. Br J Pharmacol 2001; 134: 295-304.
17. La Rovere MT, Pinna GD, Raczak G. Baroreflex sensitivity: measurement and clinical implications. Ann Noninvasive Electrocardiol 2008; 13: 191-207.
18. Pontieri V, Venezuela MK, Scavone C, Michelini LC. Role of endogenous nitric oxide in the nucleus tractus solitarii on baroreflex control of heart rate in spontaneously hypertensive rats. J Hypertens 1998; 16: 1993-1999.
19. Gomes CL, Konno K, Conceicao IM, Ianzer D, Yamanouye N, Prezoto BC, Assakura MT, Rádis-Baptista G, Yamane T, Santos RA, de Camargo AC, Hayashi MA. 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: 1350-1360.
20. Raizada MK, Lu D, Sumners C. AT1 receptors and angiotensin actions in the brain and neuronal cultures of normotensive and hypertensive rats. Adv Exp Med Biol 1995; 377: 331-348.
21. Martins AH, Resende RR, Majumder P, Faria M, Casarini DE, Tárnok A, Colli W, Pesquero JB, Ulrich H. Neuronal differentiation of P19 embryonal carcinoma cells modulates kinin B2 receptor gene expression and function. J Biol Chem 2005; 280: 19576-19586.
22. Feelisch M, Rassaf T, Mnaimneh S, Singh N, Bryan NS, Jourd'Heuil D, Kelm M. Concomitant S-, N-, and heme-nitros(yl)ation in biological tissues and fluids: implications for the fate of NO in vivo. FA SE B J 2002; 16: 1775-1785.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25: 402-408.
24. Irigoyen MC, Lacchini S, De Angelis K, Michelini LC. Fisiopatologia da hipertensão: O que avançamos? Ver Soc Cardiol Estado de São Paulo 2003; 1: 20-45.
25. Thastrup O, Dawson AP, Scharff O, Foder B, Cullen PJ, Drobak BK, Bjerrum PJ, Christensen SB, Hanley MR. Thapsigargin, a novel molecular probe for studying intracellular calcium release and storage. Agents Actions 1989; 27: 17-23.
26. Krieger EM, Da Silva GJ, Negrão CE. Effects of exercise training on baroreflex control of the cardiovascular system. Ann N Y Acad Sci 2001; 940: 338-347.
27. Patel KP, Li YF, Hirooka Y. Role of nitric oxide in central sympathetic outflow. Exp Biol Med (Maywood) 2001; 226: 814-824.
28. Hauser GJ, Dayao EK, Zukowska-Grojec Z. Effect of pentobarbital anesthesia on the pressor response to agonists in vivo in normal and endotoxemic rats. Res Commun Mol Pathol Pharmacol 1995; 90: 289-300.
29. Lanfranchi PA, Somers VK. Arterial baroreflex function and cardiovascular variability: interactions and implications. Am J Physiol Regul Integr Comp Physiol 2002; 283: R815-R826.
30. Ducher M, Fauvel JP, Cerutti C. Risk profile in hypertension genesis: a five-year follow-up study. Am J Hypertens 2006; 19: 775-780.
31. Xing-Sheng Y, Yong-Zhi L, Jie-Xin L, Yu-Qing G, Zhang-Huang C, Chong-Fa Z, Zhi-Zhong T, Shu-Zheng L. genetic influence on baroreflex sensitivity in normotensive young men. Am J Hypertens 2010; 23: 655-659.
32. Bristow JD, Honour AJ, Pickering GW, Sleight P, Smyth HS. Diminished baroreflex sensitivity in high blood pressure. Circulation 1969; 39: 48-54.
33. Grassi G, Trevano FQ, Seravalle G, Scopelliti F, Mancia G. Baroreflex function in hypertension: consequences for antihypertensive therapy. Prog Cardiovasc Dis 2006; 48: 407-415.
34. Gordon FJ, Sved AF. Neurotransmitters in central cardiovascular regulation: glutamate and GABA. Clin Exp Pharmacol Physiol 2002; 29: 522-524.
35. Parmer RJ, Cervenka JH, Stone RA. Baroreflex sensitivity and heredity in essential hypertension. Circulation 1992; 85: 497-503.
36. Lameu C, de Camargo AC, Faria M. L-arginine signalling potential in the brain: the peripheral gets central. Recent Pat CNS Drug Discov 2009; 4: 137-142.
37. Nakamura H, Saheki T, Ichiki H, Nakata K, Nakagawa S. Immunocytochemical localization of argininosuccinate synthetase in the rat brain. J Comp Neurol 1991; 312: 652-679.
38. Kishi T, Hirooka Y, Sakai K, Shigematsu H, Shimokawa H, Takeshita A. Overexpression of eNOS in the RVLM causes hypotension and bradycardia via GABA release. Hypertension 2001; 38: 896-901.
39. Hirooka Y, Sakai K, Kishi T, Ito K, Shimokawa H, Takeshita A. Enhanced depressor response to endothelial nitric oxide synthase gene transfer into the nucleus tractus solitarii of spontaneously hypertensive rats. Hypertens Res 2003; 26: 325-331.
40. Kishi T, Hirooka Y, Kimura Y, Sakai K, Ito K, Shimokawa H, Takeshita A. Overexpression of eNOS in RVLM improves impaired baroreflex control of heart rate in SHRSP. Rostral ventrolateral medulla. Stroke-prone spontaneously hypertensive rats. Hypertension 2003; 41: 255-260.