Effects of lipopolysaccharide on the neuronal control of mesenteric vascular tone in rats: Mechanisms involved

Shock

Volumn 38, Issue 3, 2012, Pages 328-334

  Sastre, Esther ^a   Blanco Rivero, Javier ^a,b   Caracuel, Laura ^a   Lahera, Vicente ^c   Balfagón, Gloria ^a,c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

adrenergic innervation; LPS; nitrergic innervation; rat mesenteric artery

Indexed keywords

LIPOPOLYSACCHARIDE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PEROXYNITRITE; SUPEROXIDE;

ADRENERGIC NERVE; ANIMAL TISSUE; ARTERY CONSTRICTION; ARTERY DILATATION; ARTERY TONE; ARTICLE; BLOOD VESSEL INNERVATION; CONTROLLED STUDY; ELECTRIC FIELD; MALE; MESENTERIC ARTERY; NITRERGIC NERVE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT;

ANIMALS; ELECTRIC STIMULATION; HYDRAZINES; LIPOPOLYSACCHARIDES; MALE; MESENTERIC ARTERIES; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; NEURONS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE I; NOREPINEPHRINE; OXIDATIVE STRESS; PEROXYNITROUS ACID; POTASSIUM CHLORIDE; RATS; RATS, WISTAR; SUPEROXIDES; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATOR AGENTS; VASOMOTOR SYSTEM;

EID: 84865497148     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0b013e31826240ba     Document Type: Article

References (46)

1. Parrillo JE, Parker MM, Natanson C, Suffredini AF, Danner RL, Cunnion RE, Ognibene FP: Septic shock in humans. Advances in the understanding of pathogenesis, cardiovascular dysfunction, and therapy. Ann Intern Med 113: 227-242, 2005.
2. Sorrentino R, d'Emmanuele di Villa Bianca R, Lippolis L, Sorrentino L, Autore G, Pinto A: Involvement of ATP-sensitive potassium channels in a model of a delayed vascular hyporeactivity induced by lipopolysaccharide in rats. Br J Pharmacol 127:1447-1453, 1999. (Pubitemid 29358946)
3. Lange M, Nakano Y, Traber DL, Hamahata A, Esechie A, Jonkam C, Bansal K, Traber LD, Enkhbaatar P: Role of different nitric oxide synthase isoforms in a murine model of acute lung injury and sepsis. Biochem Biophys Res Commun 399:286-291, 2010.
4. Carnio EC, Stabile AM, Batalhão ME, Silva JS, Antunes-Rodrigues J, Branco LG, Magder S: Vasopressin release during endotoxaemic shock in mice lacking inducible nitric oxide synthase. Pflugers Arch 450:390-394, 2005. (Pubitemid 41380697)
5. Ohlmann P, Mart?́nez MC, Bucher B, Andriantsitohaina R, Muller B, Schneider F, Stoclet JC: Effect of lipopolysaccharide treatment on neurogenic contraction and noradrenaline release in rat arteries. Fundam Clin Pharmacol 14:593-600, 2000. (Pubitemid 32052556)
6. Yilmaz MS, Goktalay G, Millington WR, Myer BS, Cutrera RA, Feleder C: Lipopolysaccharide-induced hypotension is mediated by a neural pathway involving the vagus nerve, the nucleus tractus solitarius and alpha-adrenergic receptors in the preoptic anterior hypothalamic area. J Neuroimmunol 203: 39-49, 2008.
7. Kirkebøen KA, Strand OA: The role of nitric oxide in sepsisVan overview. Acta Anaesthesiol Scand 43:275-288, 1999. (Pubitemid 29109473)
8. Holmqvist B, Olsson CF, Svensson ML, Svanborg C, Forsell J, Alm P: Expression of nitric oxide synthase isoforms in the mouse kidney: cellular localization and influence by lipopolysaccharide and Toll-like receptor 4. J Mol Histol 36:499-516, 2005. (Pubitemid 43829389)
9. Nava E, Palmer RM, Moncada S: Inhibition of nitric oxide synthesis in septic shock: how much is beneficial? Lancet 338:1555-1557, 1991.
10. Lange M, Hamahata A, Traber DL, Nakano Y, Traber LD, Enkhbaatar P: Specific inhibition of nitric oxide synthases at different time points in a murine model of pulmonary sepsis. Biochem Biophys Res Commun 404:877-881, 2011.
11. Petros A, Lamb G, Leone A, Moncada S, Bennett D, Vallance P: Effects of a nitric oxide synthase inhibitor in humans with septic shock. Cardiovasc Res 28:34-39, 1994.
12. Briones AM, Alonso MJ, Maŕn J, Balfagón G, Salaices M: Influence of hypertension on nitric oxide synthase expression and vascular effects of lipopolysaccharide in rat mesenteric arteries. Br J Pharmacol 131:185-194, 2000.
13. Scicluna JK, Mansart A, Ross JJ, Reilly CS, Brown NJ, Brookes ZL: Reduced vascular response to phenylephrine during exposure to lipopolysaccharide in vitro involves nitric oxide and endothelin 1. Shock 29:417-421, 2008. (Pubitemid 351278376)
14. Panayiotou CM, Baliga R, Stidwill R, Taylor V, Singer M, Hobbs AJ: Resistance to endotoxic shock in mice lacking natriuretic peptide receptor-A. Br J Pharmacol 160:2045-2054, 2010.
15. Grasa L, Arruebo MP, Plaza MA, Murillo MD: A downregulation of nNOS is associated to dysmotility evoked by lipopolysaccharide in rabbit duodenum. J Physiol Pharmacol 59:511-524, 2008.
16. Gocan NC, Scott JA, Tyml K: Nitric oxide produced via neuronal NOS may impair vasodilatation in septic rat skeletal muscle. Am J Physiol Heart Circ Physiol 278:1480-1489, 2000.
17. Harada S, Imaki T, Chikada N, Naruse M, Demura H: Distinct distribution and time-course changes in neuronal nitric oxide synthase and inducible NOS in the paraventricular nucleus following lipopolysaccharide injection. Brain Res 821: 322-332, 1999. (Pubitemid 29222795)
18. Enkhbaatar P, Lange M, Nakano Y, Hamahata A, Jonkam C, Wang J, Jaroch S, Traber L, Herndon D, Traber D: Role of neuronal nitric oxide synthase in ovine sepsis model. Shock 32:253-257, 2009.
19. Javenshghani D, Magder S: Regional changes in constitutive nitric oxide synthase and the hemodynamic consequences of its inhibition in lipopolysaccharide-treated pigs. Shock 16:232-238, 2001. (Pubitemid 33598203)
20. Loesch A: Perivascular nerves and vascular endothelium: recent advances. Histol Histopathol 17:591-597, 2002. (Pubitemid 34411213)
21. Li YJ, Duckles SP: Effect of endothelium on the actions of sympathetic and sensory nerves in the perfused rat mesentery. Eur J Pharmacol 210:23-40, 1992.
22. Boeckxstaens GE, Pelckmans PA: Nitric oxide and the non-adrenergic noncholinergic neurotransmission. Comp Biochem Physiol A Physiol 118:925-937, 1997. (Pubitemid 28087950)
23. Maŕn J, Balfagón G: Effect of clenbuterol on non-endothelial nitric oxide release in rat mesenteric arteries and the involvement of "-adrenoceptors. Br J Pharmacol 124:473-478, 1998. (Pubitemid 28254502)
24. Sastre E, Márquez-Rodas I, Blanco-Rivero J, Balfagón G: Perivascular innervation of the superior mesenteric artery: pathophysiological implications. Rev Neurol 50:727-737, 2010.
25. Hernanz R, Alonso MJ, Zibrandtsen H, Alvarez Y, Salaices M, Simonsen U: Measurements of nitric oxide concentration and hyporeactivity in rat superior mesenteric artery exposed to endotoxin. Cardiovasc Res 62:202-211, 2004. (Pubitemid 38326826)
26. Yao SY, Ljunggren-Rose A, Chandramohan N, Whetsell WO Jr, Sriram S: In vitro and in vivo induction and activation of nNOS by LPS in oligodendrocytes. J Neuroimmunol 229:146-156, 2010.
27. Mitchell JA, Kohlhaas KL, Sorrentino R, Warner TD, Murad F, Vane JR: Induction by endotoxin of nitric oxide synthase in the rat mesentery: lack of effect on action of vasoconstrictors. Br J Pharmacol 109:265-270, 1993. (Pubitemid 23113832)
28. Holzmann A: Nitric oxide and sepsis. Respir Care Clin N Am 3:537-550, 1997.
29. Farmer MR, Roberts RE, Gardiner SM, Ralevic V: Effects of in vivo lipopolysaccharide infusion on vasoconstrictor function of rat isolated mesentery, kidney, and aorta. J Pharmacol Exp Ther 306:538-545, 2003. (Pubitemid 36886152)
30. Nielsen KC, Owman C: Contractile response and amine receptor mechanisms in isolated middle cerebral artery of the cat. Brain Res 27:33-42, 1971.
31. Blanco-Rivero J, de las Heras N, Mart́n-Fernández B, Cachofeiro V, Lahera V, Balfagón G: Rosuvastatin restored adrenergic and nitrergic function in mesenteric arteries from obese rats. Br J Pharmacol 162:271-285, 2011.
32. Blanco-Rivero J, Furieri LB, Vassallo DV, Saláces M, Balfagón G: Chronic HgCl2 treatment increases vasoconstriction induced by electrical field stimulation. Role of adrenergic and nitrergic innervation. Clin Sci (Lond) 121: 331-341, 2010.
33. Ferrer M, Maŕn J, Balfagón G: Diabetes alters neuronal nitric oxide release from rat mesenteric arteries. Role of protein kinase C. Life Sci 66: 337-345, 2000. (Pubitemid 30025486)
34. Balfagón G, Márquez-Rodas I, Alvarez Y, Alonso MJ, Cachofeiro V, Salaices M, Lahera V. Aldosterone modulates neural vasomotor response in hypertension: role of calcitonin gene-related peptide. Regul Pept 120:253-260, 2004. (Pubitemid 38726214)
35. Quintana E, Hernández C, Moran AP, Esplugues JV, Barrachina MD: Transcriptional up-regulation of nNOS in the dorsal vagal complex during low endotoxemia. Life Sci 77:1044-1054, 2005. (Pubitemid 40814639)
36. Comini L, Boraso A, Bachetti T, Bernocchi P, Pasini E, Bastianon D, Curello S, Terracciano CM, Ceconi C, Ferrari R: Effects of endotoxic shock on neuronal NOS and calcium transients in rat cardiac myocytes. Pharmacol Res 51: 409-417, 2005. (Pubitemid 40326192)
37. Xavier FE, Salaices M, Márquez-Rodas I, Alonso MJ, Rossoni LV, Vassallo DV, Balfagón G: Neurogenic nitric oxide release increases in mesenteric arteries from ouabain hypertensive rats. J Hypertens 22:949-957, 2004. (Pubitemid 38680470)
38. Arden WA, Fiscus RR, Wang X, Maley R, Lanzo S, Gross DR: Early endotoxic shock results in enhanced vasodilator responses to nitroglycerin but unaltered responses to neuropeptides calcitonin gene-related peptide and substance P. Shock 1:425-431, 1994.
39. Ralevic V, Farmer MR, Gardiner SM: Vasoconstrictor responsiveness of tail arteries from endotoxaemic rats. Eur J Pharmacol 460:145-153, 2003. (Pubitemid 36139982)
40. Mart́nez MC, Muller B, Stoclet JC, Andriantsitohaina R: Alteration by lipopolysaccharide of the relationship between intracellular calcium levels and contraction in rat mesenteric artery. Br J Pharmacol 118:1218-1222, 1996. (Pubitemid 26235621)
41. Müller-Schweinitzer E, Gilles H, Grapow M, Kern T, Reineke D, Zerkowski HR: Attenuation of lipopolysaccharide-induced hyperreactivity of human internal mammary arteries by melatonin. J Pinel Res 37:92-97, 2004. (Pubitemid 39120212)
42. Kamisaki Y, Wada K, Ataka M, Yamada Y, Nakamoto K, Ashida K, Kishimoto Y: Lipopolysaccharide-induced increase in plasma nitrotyrosine concentrations in rats. Biochim Biophys Acta 1362:24-28, 1997. (Pubitemid 28027108)
43. Brandes RP, Koddenberg G, Gwinner W, Kim D, Kruse HJ, Busse R, Mügge A: Role of increased production of superoxide anions by NAD(P)H oxidase and xanthine oxidase in prolonged endotoxemia. Hypertension 33: 1243-1249, 1999. (Pubitemid 29230981)
44. Cuzzocrea S, Mazzon E, Di Paola R, Esposito E, Macarthur H, Matuschak GM, Salvemini D: A role for nitric oxide-mediated peroxynitrite formation in a model of endotoxin-induced shock. J Pharmacol Exp Ther 319:73-81, 2006. (Pubitemid 44455112)
45. Mart́n MC, Balfagón G, Minoves N, Blanco-Rivero J, Ferrer M: Androgen deprivation increases neuronal nitric oxide metabolism and its vasodilator effect in rat mesenteric arteries. Nitric Oxide 12:163-176, 2005. (Pubitemid 40432136)
46. Kang YM, He RL, Yang LM, Qin DN, Guggilam A, Elks C, Yan N, Guo Z, Francis J: Brain tumour necrosis factor-! modulates neurotransmitters in hypothalamic paraventricular nucleus in heart failure. Cardiovasc Res 83:737-746, 2009.