Activation of kinin B1 receptor evokes hyperthermia through a vagal sensory mechanism in the rat

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Talbot, Sébastien ^a   De Brito Gariépy, Helaine ^a   Saint Denis, Julien ^a   Couture, Réjean ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Bradykinin; Diabetes; Hyperthermia; Inflammation; Kinin B1 receptor; NO; Sensory C fibers; Thermoregulation

Indexed keywords

BRADYKININ B1 RECEPTOR; BRADYKININ B1 RECEPTOR AGONIST; BRADYKININ B2 RECEPTOR AGONIST; CALCITONIN GENE RELATED PEPTIDE; CYCLOOXYGENASE 2; INDOMETACIN; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NIFLUMIC ACID; NITRIC OXIDE; PROSTAGLANDIN; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORE TEMPERATURE; HYPERTHERMIA; HYPOTHALAMUS; MALE; NERVE LIGATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; RECTUM TEMPERATURE; SENSORY NERVE; VAGUS NERVE; VAGUS NERVE STIMULATION;

EID: 84866130622     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-214     Document Type: Article

References (49)

1. Dinarello CA. Infection, fever, and exogenous and endogenous pyrogens: some concepts have changed. J Endotoxin Res 2004, 10:201-222.
2. Nakamura K. Central circuitries for body temperature regulation and fever. Am J Physiol Regul Integr Comp Physiol 2011, 301:R1207-1228. 10.1152/ajpregu.00109.2011, 21900642.
3. Hansen MK, O'Connor KA, Goehler LE, Watkins LR, Maier SF. The contribution of the vagus nerve in interleukin-1beta-induced fever is dependent on dose. Am J Physiol Regul Integr Comp Physiol 2001, 280:R929-934.
4. Werner MF, Fraga D, Melo MC, Souza GE, Zampronio AR. Importance of the vagus nerve for fever and neutrophil migration induced by intraperitoneal LPS injection. Inflamm Res 2003, 52:291-296.
5. Watkins LR, Goehler LE, Relton JK, Tartaglia N, Silbert L, Martin D, Maier SF. Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune-brain communication. Neurosci Lett 1995, 183:27-31. 10.1016/0304-3940(94)11105-R, 7746479.
6. Laye S, Bluthe RM, Kent S, Combe C, Medina C, Parnet P, Kelley K, Dantzer R. Subdiaphragmatic vagotomy blocks induction of IL-1 beta mRNA in mice brain in response to peripheral LPS. Am J Physiol 1995, 268:R1327-1331.
7. Dias JP, Talbot S, Senecal J, Carayon P, Couture R. Kinin B1 receptor enhances the oxidative stress in a rat model of insulin resistance: outcome in hypertension, allodynia and metabolic complications. PLoS One 2010, 5:e12622. 10.1371/journal.pone.0012622, 2935380, 20830306.
8. Couture R, Harrisson M, Vianna RM, Cloutier F. Kinin receptors in pain and inflammation. Eur J Pharmacol 2001, 429:161-176. 10.1016/S0014-2999(01)01318-8, 11698039.
9. Couture R, Girolami JP. Putative roles of kinin receptors in the therapeutic effects of angiotensin 1-converting enzyme inhibitors in diabetes mellitus. Eur J Pharmacol 2004, 500:467-485. 10.1016/j.ejphar.2004.07.045, 15464053.
10. Talbot S, Chahmi E, Dias JP, Couture R. Key role for spinal dorsal horn microglial kinin B1 receptor in early diabetic pain neuropathy. J Neuroinflammation 2010, 7:36. 10.1186/1742-2094-7-36, 2913947, 20587056.
11. Talbot S, Couture R. Emerging role of microglial kinin B1 receptor in diabetic pain neuropathy. Exp Neurol 2012, 234:373-381. 10.1016/j.expneurol.2011.11.032, 22154922.
12. Talbot S, Dias JP, Lahjouji K, Bogo MR, Campos MM, Gaudreau P, Couture R. Activation of TRPV1 by capsaicin induces functional kinin B(1) receptor in rat spinal cord microglia. J Neuroinflammation 2012, 9:16. 10.1186/1742-2094-9-16, 3282640, 22264228.
13. Calixto JB, Medeiros R, Fernandes ES, Ferreira J, Cabrini DA, Campos MM. Kinin B1 receptors: key G-protein-coupled receptors and their role in inflammatory and painful processes. Br J Pharmacol 2004, 143:803-818. 10.1038/sj.bjp.0706012, 1575942, 15520046.
14. Regoli D, Barabe J. Pharmacology of bradykinin and related kinins. Pharmacol Rev 1980, 32:1-46.
15. Leeb-Lundberg LM, Marceau F, Muller-Esterl W, Pettibone DJ, Zuraw BL. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev 2005, 57:27-77. 10.1124/pr.57.1.2, 15734727.
16. Marceau F, Regoli D. Bradykinin receptor ligands: therapeutic perspectives. Nat Rev Drug Discov 2004, 3:845-852. 10.1038/nrd1522, 15459675.
17. de Blois D, Horlick RA. Endotoxin sensitization to kinin B(1) receptor agonist in a non-human primate model: haemodynamic and pro-inflammatory effects. Br J Pharmacol 2001, 132:327-335. 10.1038/sj.bjp.0703748, 1572522, 11156593.
18. Abdouh M, Talbot S, Couture R, Hassessian HM. Retinal plasma extravasation in streptozotocin-diabetic rats mediated by kinin B(1) and B(2) receptors. Br J Pharmacol 2008, 154:136-143. 10.1038/bjp.2008.48, 2438974, 18311190.
19. Ismael MA, Talbot S, Carbonneau CL, Beausejour CM, Couture R. Blockade of sensory abnormalities and kinin B(1) receptor expression by N-acetyl-L-cysteine and ramipril in a rat model of insulin resistance. Eur J Pharmacol 2008, 589:66-72. 10.1016/j.ejphar.2008.05.006, 18555989.
20. Blatteis CM. The onset of fever: new insights into its mechanism. Prog Brain Res 2007, 162:3-14.
21. Romanovsky AA, Almeida MC, Aronoff DM, Ivanov AI, Konsman JP, Steiner AA, Turek VF. Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front Biosci 2005, 10:2193-2216. 10.2741/1690, 15970487.
22. Coelho MM, Oliveira CR, Pajolla GP, Calixto JB, Pela IR. Central involvement of kinin B1 and B2 receptors in the febrile response induced by endotoxin in rats. Br J Pharmacol 1997, 121:296-302. 10.1038/sj.bjp.0701110, 1564670, 9154340.
23. Silva TC A, Pela IR. Changes in rectal temperature of the rabbit by intracerebroventricular injection of bradykinin and related kinins. Agents Actions 1978, 8:102-107. 10.1007/BF01972410, 636933.
24. Rao PJ, Bhattacharya SK. Hyperthermic effect of centrally administered bradykinin in the rat: role of prostaglandins and serotonin. Int J Hyperthermia 1988, 4:183-189. 10.3109/02656738809029308, 3361165.
25. Caldeira JC, Franci CR, Pela IR. Bilateral lesion of hypothalamic paraventricular nucleus abolishes fever induced by endotoxin and bradykinin in rats. Ann N Y Acad Sci 1998, 856:294-297. 10.1111/j.1749-6632.1998.tb08342.x, 9917894.
26. Pouliot M, Talbot S, Senecal J, Dotigny F, Vaucher E, Couture R. Ocular application of the kinin B1 receptor antagonist LF22-0542 inhibits retinal inflammation and oxidative stress in streptozotocin-diabetic rats. PLoS One 2012, 7:e33864. 10.1371/journal.pone.0033864, 3314679, 22470485.
27. Regoli D, Dion S, Rhaleb NE, Drapeau G, D'Orleans-Juste P. Vasoactive peptides and their receptors. Blood Vessels 1990, 27:137-145.
28. Regoli D, Jukic D, Gobeil F, Rhaleb NE. Receptors for bradykinin and related kinins: a critical analysis. Can J Physiol Pharmacol 1993, 71:556-567. 10.1139/y93-079, 8306193.
29. Zuccollo A, Cueva F, Frontera M, Navarro M, Catanzaro O. The role of the kallikrein-kinin system in type I diabetes (insulitis). Immunopharmacology 1996, 33:349-350. 10.1016/0162-3109(96)00095-1, 8856183.
30. Campos MM, Ongali B. De Souza Buck H, Schanstra JP, Girolami JP, Chabot JG, Couture R: Expression and distribution of kinin B1 receptor in the rat brain and alterations induced by diabetes in the model of streptozotocin. Synapse 2005, 57:29-37. 10.1002/syn.20150, 15858836.
31. Talbot S, Theberge-Turmel P, Liazoghli D, Senecal J, Gaudreau P, Couture R. Cellular localization of kinin B1 receptor in the spinal cord of streptozotocin-diabetic rats with a fluorescent [Nalpha-Bodipy]-des-Arg9-bradykinin. J Neuroinflammation 2009, 6:11. 10.1186/1742-2094-6-11, 2667487, 19323833.
32. Morissette G, Sabourin T, Adam A, Marceau F. Inhibition of human and rabbit arterial smooth muscle cell migration mediated by the kinin B1 receptor: role of receptor density and released mediators. Can J Physiol Pharmacol 2006, 84:1107-1119. 10.1139/y06-031, 17218975.
33. Pilon M, Wu R, Huot-Marchand JE, de Blois D, Champlain J, Couture R. Effect of chronic inhibition of nitric oxide on hypertension, insulin resistance, and cardiovascular remodeling in glucose-fed rats. J Cardiovasc Pharmacol 2009, 53:405-413. 10.1097/FJC.0b013e3181a1d88a, 19333132.
34. Brueggemeier RW, Diaz-Cruz ES, Li PK, Sugimoto Y, Lin YC, Shapiro CL. Translational studies on aromatase, cyclooxygenases, and enzyme inhibitors in breast cancer. J Steroid Biochem Mol Biol 2005, 95:129-136. 10.1016/j.jsbmb.2005.04.013, 15964185.
35. Gougat J, Ferrari B, Sarran L, Planchenault C, Poncelet M, Maruani J, Alonso R, Cudennec A, Croci T, Guagnini F, Urban-Szabo K, Martinolle JP, Soubrié P, Finance O, Le Fur G. SSR240612 [(2R)-2-[((3R)-3-(1,3-benzodioxol-5-yl)-3-[[(6-methoxy-2-naphthyl)sulfonyl]amino] propanoyl)amino]-3-(4-[[2R,6S)-2,6-dimethylpiperidinyl]methyl]phenyl)-N-isopropyl -N-methylpropanamide hydrochloride], a new nonpeptide antagonist of the bradykinin B1 receptor: biochemical and pharmacological characterization. J Pharmacol Exp Ther 2004, 309:661-669. 10.1124/jpet.103.059527, 14747609.
36. Kwon HY, Chang TM, Lee KY, Chey WY. Vagus nerve modulates secretin binding sites in the rat forestomach. Am J Physiol 1999, 276:G1052-1058.
37. Lin JC, Talbot S, Lahjouji K, Roy JP, Senecal J, Couture R, Morin A. Mechanism of cigarette smoke-induced kinin B(1) receptor expression in rat airways. Peptides 2010, 31:1940-1945. 10.1016/j.peptides.2010.07.008, 20637817.
38. Loiola RA, Reis FC, Kawamoto EM, Scavone C, Abdalla DS, Fernandes L, Pesquero JB. Role of vascular Kinin B1 and B2 receptors in endothelial nitric oxide metabolism. Peptides 2011, 32:1700-1705. 10.1016/j.peptides.2011.06.010, 21704095.
39. Lungu C, Dias JP, Franca CE, Ongali B, Regoli D, Moldovan F, Couture R. Involvement of kinin B1 receptor and oxidative stress in sensory abnormalities and arterial hypertension in an experimental rat model of insulin resistance. Neuropeptides 2007, 41:375-387. 10.1016/j.npep.2007.09.005, 17988733.
40. Gabra BH, Merino VF, Bader M, Pesquero JB, Sirois P. Absence of diabetic hyperalgesia in bradykinin B1 receptor-knockout mice. Regul Pept 2005, 127:245-248. 10.1016/j.regpep.2004.12.003, 15680494.
41. Campos MM, Cabrini DA, Cardozo AH, Rae GA, Toro JH, Calixto JB. Changes in paw oedema triggered via bradykinin B(1) and B(2) receptors in streptozotocin-diabetic rats. Eur J Pharmacol 2001, 416:169-177. 10.1016/S0014-2999(01)00883-4, 11282127.
42. Vianna RM, Ongali B, Regoli D, Calixto JB, Couture R. Up-regulation of kinin B1 receptor in the lung of streptozotocin-diabetic rat: autoradiographic and functional evidence. Br J Pharmacol 2003, 138:13-22. 10.1038/sj.bjp.0704999, 1573626, 12522068.
43. Catanzaro O, Labal E, Andornino A, Capponi JA, Di Martino I, Sirois P. Blockade of early and late retinal biochemical alterations associated with diabetes development by the selective bradykinin B1 receptor antagonist R-954. Peptides 2012, 34:349-352. 10.1016/j.peptides.2012.02.008, 22369720.
44. Lawson SR, Gabra BH, Nantel F, Battistini B, Sirois P. Effects of a selective bradykinin B1 receptor antagonist on increased plasma extravasation in streptozotocin-induced diabetic rats: distinct vasculopathic profile of major key organs. Eur J Pharmacol 2005, 514:69-78. 10.1016/j.ejphar.2005.03.023, 15878326.
45. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA. The neutrophil as a cellular source of chemokines. Immunol Rev 2000, 177:195-203. 10.1034/j.1600-065X.2000.17706.x, 11138776.
46. Conti B, Tabarean I, Andrei C, Bartfai T. Cytokines and fever. Front Biosci 2004, 9:1433-1449.
47. Blatteis CM. The afferent signalling of fever. J Physiol 2000, 526:470.
48. Souza GEP, Piza AM, Peroza EA, Couture R, Lindsey CJ. Vagotomy blocks LPS-induced fever and bradykinin B1 receptor gene expression in rat hypothalamus. Brain Res 2000, 848:39. Abstract.
49. Roth J, Souza GEP. Fever induction pathways: evidence from responses to systemic or local cytokine formation. Braz J Med Biol Res 2001, 34:301-314.