Nitric oxide-induced vasorelaxation in response to pntx2-6 toxin from phoneutria nigriventer spider in rat cavernosal tissue

Journal of Sexual Medicine

Volumn 7, Issue 12, 2010, Pages 3879-3888

  Nunes, Kenia P ^a,b   Cordeiro, Marta N ^c   Richardson, Michael ^c   Borges, Marcia N ^c   Diniz, Simone O F ^d   Cardoso, Valbert N ^d   Tostes, Rita ^b,e   De Lima, Maria Elena ^a   Webb, Robert Clinton ^b   Leite, Romulo ^f  

^a Department of Microbiology Biological Sciences Institute   (Brazil)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c Ezequiel Dias Foundation   (Brazil)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

Author keywords

Corpus Cavernosum; Erectile Physiology; Nitric Oxide; PnTx2 6 Toxin; Relaxation

Indexed keywords

ATROPINE; BRETYLIUM; NITRIC OXIDE; NITROPRUSSIDE SODIUM; OMEGA CONOTOXIN GVIA; PHENYLEPHRINE; PHOSPHODIESTERASE V; PNTX2 6 TOXIN; SILDENAFIL; SPIDER VENOM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS CAVERNOSUM; ELECTRIC FIELD; ELECTROSTIMULATION; MALE; NONHUMAN; PHONEUTRIA NIGRIVENTER; PRIAPISM; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE RELAXATION; SPIDER; SPIDER BITE; VASODILATATION;

EID: 78649825140     PISSN: 17436095     EISSN: 17436109     Source Type: Journal    
DOI: 10.1111/j.1743-6109.2010.01978.x     Document Type: Article

References (53)

1. Shamloul R. Natural aphrodisiacs. J Sex Med 2010;7(1 Pt 1):39-49.
2. Costa C, Virag R. The endothelial-erectile dysfunction connection: An essential update. J Sex Med 2009;6:2390-404.
3. Aversa A, Bruzziches R, Francomano D, Natali M, Gareri P, Spera G. Endothelial dysfunction and erectile dysfunction in the aging man. Int J Urol 2010;17:38-47.
4. Ayta IA, McKinlay JB, Krane RJ. The likely worldwide increase in erectile dysfunction between 1995 and 2025 and some possible policy consequences. BJU Int 1999;84:50-6.
5. Teixeira CE, De Oliveira JF, Baracat JS, Priviero FB, Okuyama CE, Rodrigues Netto N Jr, Fregonesi A, Antunes E, De Nucci G. Nitric oxide release from human corpus cavernosum induced by a purified scorpion toxin. Urology 2004;63:184-9.
6. Andrade E, Villanova F, Borra P, Leite K, Troncone L, Cortez I, Messina L, Paranhos M, Claro J, Srougi M. Penile erection induced in vivo by a purified toxin from the Brazilian spider Phoneutria nigriventer. BJU Int 2008;102:835-7.
7. Nunes KP, Cardoso FL, Cardoso HC, Jr., Pimenta AMC, De Lima ME. Animal toxins as potential pharmacological tools for treatment of erectile dysfunction. In: De Lima ME, Pimenta AMC, Martin-Eauclaire MF, Zingali R, Rochat H, eds. Animal toxins: State of the art perspectives in health and biotechnology, vol. 2. 2009:314-22.
8. Bucaretchi F, Deus Reinaldo CR, Hyslop S, Madureira PR, De Capitani EM, Vieira RJ. A clinico-epidemiological study of bites by spiders of the genus Phoneutria. Rev Inst Med Trop Sao Paulo 2000;42:17-21.
9. Bucaretchi F, Mello SM, Vieira RJ, Mamoni RL, Blotta MH, Antunes E, Hyslop S. Systemic envenomation caused by the wandering spider Phoneutria nigriventer, with quantification of circulating venom. Clin Toxicol (Phila) 2008;46:885-9.
10. Lopes-Martins RA, Antunes E, Oliva ML, Sampaio CA, Burton J, De Nucci G. Pharmacological characterization of rabbit corpus cavernosum relaxation mediated by the tissue kallikrein-kinin system. Br J Pharmacol 1994;113:81-6.
11. Cordeiro Mdo N, Diniz CR, Valentim Ado C, Von Eickstedt VR, Gilroy J, Richardson M. The purification and amino acid sequences of four Tx2 neurotoxins from the venom of the Brazilian "armed" spider Phoneutria nigriventer (Keys). FEBS Lett 1992;310:153-6.
12. Cordeiro MN, Richardson M, Gilroy J, Figueiredo SGD, Beirão PSL, Diniz CR. Properties of the venom from the south american armed spider Phoneutria nigriventer (Keyserling, 1891). J Toxicol Toxin Rev 1995;14:309-26.
13. Richardson M, Pimenta AM, Bemquerer MP, Santoro MM, Beirao PS, Lima ME, Figueiredo SG, Bloch C Jr, Vasconcelos EA, Campos FA, Gomes PC, Cordeiro MN. Comparison of the partial proteomes of the venoms of Brazilian spiders of the genus Phoneutria. Comp Biochem Physiol C Toxicol Pharmacol 2006;142:173-87.
14. Schenberg S, Lima FA. Pharmacology of the polypeptides from the venom of the spider Phoneutria fera. Mem Inst Butantan 1966;33:627-38.
15. Cordeiro MN. Properties of the venom from the south american armed spider Phoneutria nigriventer (Keyserling, 1891). J Toxicol Toxin Rev 1995;14:309-26.
16. Gomez MV, Kalapothakis E, Guatimosim C, Prado MA. Phoneutria nigriventer venom: A cocktail of toxins that affect ion channels. Cell Mol Neurobiol 2002;22:579-88.
17. Araujo DA, Cordeiro MN, Diniz CR, Beirao PS. Effects of a toxic fraction, PhTx2, from the spider Phoneutria nigriventer on the sodium current. Naunyn Schmiedebergs Arch Pharmacol 1993;347:205-8.
18. Matavel A, Cruz JS, Penaforte CL, Araujo DA, Kalapothakis E, Prado VF, Diniz CR, Cordeiro MN, Beirao PS. Electrophysiological characterization and molecular identification of the Phoneutria nigriventer peptide toxin PnTx2-6. FEBS Lett 2002;523:219-23.
19. Martin-Moutot N, Mansuelle P, Alcaraz G, Dos Santos RG, Cordeiro MN, De Lima ME, Seagar M, Van Renterghem C. Phoneutria nigriventer toxin 1: A novel, state-dependent inhibitor of neuronal sodium channels that interacts with micro conotoxin binding sites. Mol Pharmacol 2006;69:1931-7.
20. De Lima ME, Figueiredo SG, Pimenta AM, Santos DM, Borges MH, Cordeiro MN, Richardson M, Oliveira LC, Stankiewicz M, Pelhate M. Peptides of arachnid venoms with insecticidal activity targeting sodium channels. Comp Biochem Physiol C Toxicol Pharmacol 2007;146:264-79.
21. Borges MH, De Lima ME, Stankiewicz M, Pelhate M, Cordeiro MN, Beirão PS. Structural and functional diversity in the venom of spiders of the genus Phoneutria. In: De Lima ME, Pimenta AMC, Martin-Eauclaire MF, Zingali R, Rochat H, eds. Animal toxins: State of the art perspectives in health and biotechnology, vol. 2. 2009:291-312.
22. Matavel A, Fleury C, Oliveira LC, Molina F, De Lima ME, Cruz JS, Cordeiro MN, Richardson M, Ramos CH, Beirao PS. Structure and activity analysis of two spider toxins that alter sodium channel inactivation kinetics. Biochemistry 2009;48:3078-88.
23. Yonamine CM, Troncone LR, Camillo MA. Blockade of neuronal nitric oxide synthase abolishes the toxic effects of Tx2-5, a lethal Phoneutria nigriventer spider toxin. Toxicon 2004;44:169-72.
24. Nunes KP, Costa-Goncalves A, Lanza LF, Cortes SF, Cordeiro MN, Richardson M, Pimenta AM, Webb RC, Leite R, De Lima ME. Tx2-6 toxin of the Phoneutria nigriventer spider potentiates rat erectile function. Toxicon 2008;51:1197-206.
25. Villanova FE, Andrade E, Leal E, Andrade PM, Borra RC, Troncone LR, Magalhaes L, Leite KR, Paranhos M, Claro J, Srougi M. Erection induced by Tx2-6 toxin of Phoneutria nigriventer spider: Expression profile of genes in the nitric oxide pathway of penile tissue of mice. Toxicon 2009;54:793-801.
26. Barker TH, Baneyx G, Cardo-Vila M, Workman GA, Weaver M, Menon PM, Dedhar S, Rempel SA, Arap W, Pasqualini R, Vogel V, Sage EH. SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J Biol Chem 2005;280:36483-93.
27. Yonamine CM, Costa H, Silva JAA, Muramoto E, Rogero JR, Troncone LRP, Camillo MAP. Biodistribuition studies of bee venom and spider toxin using radiotracers. J Venom Anim Toxins Incl Trop Dis 2005;11:39-50.
28. Burnett AL, Lowenstein CJ, Bredt DS, Chang TS, Snyder SH. Nitric oxide: A physiologic mediator of penile erection. Science 1992;257:401-3.
29. Hayashida H, Okamura T, Tomoyoshi T, Toda N. Neurogenic nitric oxide mediates relaxation of canine corpus cavernosum. J Urol 1996;155:1122-7.
30. Toda N, Ayajiki K, Okamura T. Nitric oxide and penile erectile function. Pharmacol Ther 2005;106:233-66.
31. Prieto D. Physiological regulation of penile arteries and veins. Int J Impot Res 2008;20:17-29.
32. Angulo J, Gonzalez-Corrochano R, Cuevas P, Fernandez A, Fuente JM, Rolo F, Allona A, Saenz de Tejada I. Diabetes exacerbates the functional deficiency of nO/cGMP pathway associated with erectile dysfunction in human corpus cavernosum and penile arteries. J Sex Med 2010;7:758-68.
33. Vicari E, La Vignera S, Condorelli R, Calogero AE. Endothelial antioxidant administration ameliorates the erectile response to PDE5 regardless of the extension of the atherosclerotic process. J Sex Med 2010;7:1247-53.
34. Priviero FB, Leite R, Webb RC, Teixeira CE. Neurophysiological basis of penile erection. Acta Pharmacol Sin 2007;28:751-5.
35. Saenz de Tejada I, Angulo J, Cellek S, Gonzalez-Cadavid N, Heaton J, Pickard R, Simonsen U. Physiology of erectile function. J Sex Med 2004;1:254-65.
36. Cirino G, Fusco F, Imbimbo C, Mirone V. Pharmacology of erectile dysfunction in man. Pharmacol Ther 2006;111:400-23.
37. Lin CS. Phosphodiesterase type 5 regulation in the penile corpora cavernosa. J Sex Med 2009;6(suppl 3):203-9.
38. Dean RC, Lue TF. Physiology of penile erection and pathophysiology of erectile dysfunction. Urol Clin North Am 2005;32:379-95.
39. Burnett AL. Novel nitric oxide signaling mechanisms regulate the erectile response. Int J Impot Res 2004;16(suppl 1):S15-9.
40. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 1990;87:682-5.
41. Okamura T, Fujioka H, Ayajiki K. Effects of calcium antagonists on the nitrergic nerve function in canine corpus cavernosum. Jpn J Pharmacol 2001;87:208-13.
42. Cordeiro MN. The purification and amino acid sequences of four Tx2 neurotoxins from the venom of the Brazilian "armed" spider Phoneutria nigriventer (keys). FEBS Lett 1995;32:153-6.
43. Nunan EA, Cardoso VN, Moraes-Santos T. Technetium-99m labeling of tityustoxin and venom from the scorpion Tityus serrulatus. Appl Radiat Isot 2002;57:849-52.
44. Pauwels EK, Welling MM, Feitsma RI, Atsma DE, Nieuwenhuizen W. The labeling of proteins and LDL with 99mTc: A new direct method employing KBH4 and stannous chloride. Nucl Med Biol 1993;20:825-33.
45. Andersson KE. Pharmacology of penile erection. Pharmacol Rev 2001;53:417-50.
46. Andersson KE, Wagner G. Physiology of penile erection. Physiol Rev 1995;75:191-236.
47. Moura JR, Prado MA, Gomez MV, Kalapothakis E, Diniz CR, Cordeiro MN, Romano-Silva MA. Investigation of the effect of PhTx2, from the venom of the spider Phoneutria nigriventer, on the release of [3H]-acetylcholine from rat cerebrocortical synaptosomes. Toxicon 1998;36:1189-92.
48. Leite R, Giachini FR, Carneiro FS, Nunes KP, Tostes RC, Webb RC. Targets for the treatment of erectile dysfunction: Is NO/cGMP still the answer? Recent Pat Cardiovas Drug Discov 2007;2:119-32.
49. Derouet H, Osterhage J, Sittinger H. [Erectile function disorders. Epidemiology, physiology, etiology, diagnosis and therapy]. Nervenarzt 2004;75:595-605.
50. Burnett AL. The role of nitric oxide in erectile dysfunction: Implications for medical therapy. J Clin Hypertens (Greenwich) 2006;8(12 suppl 4):53-62.
51. Fernandes de Oliveira J, Teixeira CE, Arantes EC, De Nucci G, Antunes E. Relaxation of rabbit corpus cavernosum by selective activators of voltage-gated sodium channels: Role of nitric oxide-cyclic guanosine monophosphate pathway. Urology 2003;62:581-8.
52. Vlachopoulos C, Ioakeimidis N, Rokkas K, Stefanadis C. Cardiovascular effects of phosphodiesterase type 5 inhibitors. J Sex Med 2009;6:658-74.
53. Becher EF, Toblli JE, Castronuovo C, Nolazco C, Rosenfeld C, Grosman H, Vazquez E, Mazza ON. Expression of caveolin-1 in penile cavernosal tissue in a denervated animal model after treatment with sildenafil citrate. J Sex Med 2009;6:1587-93.