Thromboxane-induced renal vasoconstriction is mediated by the ADP-ribosyl cyclase CD38 and superoxide anion

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 6, 2013, Pages

  Moss, Nicholas G ^a   Vogel, Paul A ^a   Kopple, Tayler E ^a   Arendshorst, William J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Afferent arteriole; Kidney; Oxidative stress; Renal circulation; Renal vascular resistance; Superoxide dismutase; Tempol; Thromboxane prostanoid receptor; U 46619

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; ADENOSINE DIPHOSPHATE RIBOSYL CYCLASE; CD38 ANTIGEN; OXYGEN; PROSTANOID RECEPTOR; SUPEROXIDE; SUPEROXIDE DISMUTASE; TEMPOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTICLE; CONTROLLED STUDY; INTERNALIZATION; KIDNEY BLOOD FLOW; KIDNEY VASCULAR RESISTANCE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASOCONSTRICTION;

AFFERENT ARTERIOLE; KIDNEY; O2·- PRODUCTION; OXIDATIVE STRESS; RENAL CIRCULATION; RENAL VASCULAR RESISTANCE; SUPEROXIDE DISMUTASE; TEMPOL; THROMBOXANE PROSTANOID RECEPTOR; U-46619;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; ANIMALS; ANTIGENS, CD38; ARTERIOLES; CYCLIC N-OXIDES; KIDNEY; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; RECEPTORS, THROMBOXANE; SPIN LABELS; SUPEROXIDES; VASOCONSTRICTION;

EID: 84884222073     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00048.2013     Document Type: Article

References (57)

1. Arendshorst WJ, Thai TL. Regulation of the renal microcirculation by ryanodine receptors and calcium-induced calcium release. Cur Opin Nephrol Hypertens 18: 40-49, 2009.
2. Ball SK, Field MC, Tippins JR. Regulation of thromboxane receptor signaling at multiple levels by oxidative stress-induced stabilization, relocation and enhanced responsiveness. PLos One 5: e12798, 2010.
3. Bauer J, Parekh N. Variations in cell signaling pathways for different vasoconstrictor agonists in renal circulation of the rat. Kidney Int 63: 2178-2186, 2003.
4. Baylis C. Effects of administered thromboxanes on the intact, normal rat kidney. Renal Physiol 10: 110-121, 1987.
5. Brannstrom K, Arendshorst WJ. Thromboxane A2 contributes to the enhanced tubuloglomerular feedback activity in young SHR. Am J Physiol Renal Physiol 276: F758-F766, 1999.
6. Chen YF, Cowley AW Jr, Zou AP. Increased H2O2 counteracts the vasodilator and natriuretic effects of superoxide dismutation by tempol in renal medulla. Am J Physiol Regul Integr Comp Physiol 285: R827-R833, 2003.
7. de Richeliew TT, Sorensen CM, Holstein-Rathlou NH, Salomonsson M. NO independent mechanism mediates tempol induced renal vasodilation in SHR. Am J Physiol Renal Physiol 289: F1227-F1234, 2005.
8. 2+ signaling in rat afferent arterioles: stimulation of cyclic ADP ribose and IP3 pathways. Am J Physiol Renal Physiol 288: F785-F791, 2005.
9. 2+ signaling in afferent arterioles. Am J Physiol Renal Physiol 289: F1012-F1019, 2005.
10. 2+ signaling in afferent arterioles. Am J Physiol Renal Physiol 292: F175-F184, 2007.
11. Francois H, Athirakul K, Mao L, Rockman H, Coffman TM. Role for thromboxane receptors in angiotensin-II-induced hypertension. Hypertension 43: 364-369, 2004.
12. Francois H, Makhanova N, Ruiz P, Ellison J, Mao L, Rockman HA, Coffman TM. A role for the thromboxane receptor in L-NAME hypertension. Am J Physiol Renal Physiol 295: F1096-F1102, 2008.
13. Geiger J, Zou AP, Campbell WB, Li PL. Inhibition of cADP-ribose formation produces vasodilation in bovine coronary arteries. Hypertension 35: 397-402, 2000.
14. 2+ channels and cyclic ADP-ribose. J Cardiovasc Pharmacol 36: 758-763, 2000.
15. Haque MZ, Majid DSA. Assessment of renal functional phenotype in mice lacking gp91phox subunit of NAD(P)H oxidase. Hypertension 43: 335-340, 2004.
16. Hayashi K, Loutzenhiser RD, Epstein M. Direct evidence that thromboxane mimetic U44069 preferentially constricts the afferent arteriole. J Am Soc Neprol 8: 25-31, 1997.
17. Hibino M, Okumura K, Iwama Y, Mokuno S, Osanai H, Matsui H, Toki Y, Ito T. Oxygen-derived free radical-induced vasoconstriction by thromboxane A2 in aorta of the spontaneously hypertensive rat. J Cardiovasc Pharmacol 33: 605-610, 1999.
18. Himmelstein SI, Klotman PE. The role of thromboxane in two-kidney, one-clip Goldblatt hypertension in rats. Am J Physiol Renal Fluid Electrolyte Physiol 257: F190-F196, 1989.
19. Hu L, Zhang Y, Lim PS, Miao Y, Tan C, McKenzie KU, Schyvens CG, Whitworth JA. Apocynin but not L-arginine prevents and reverses dexamethasone-induced hypertension in the rat. Am J Hypertens 19: 413-418, 2006.
20. Ichihara A, Hayashi M, Hirota N, Saruta T. Superoxide inhibits neuronal nitric oxide synthase influences on afferent arterioles in spontaneously hypertensive rats. Hypertension 37: 630-634, 2001.
21. Just A, Olson AJ, Whitten CL, Arendshorst WJ. Superoxide mediates acute renal vasoconstriction produced by angiotensin II and catecholamines by a mechanism independent of nitric oxide. Am J Physiol Heart Circ Physiol 292: H83-H92, 2007.
22. Just A, Whitten CL, Arendshorst WJ. Reactive oxygen species participate in acute renal vasoconstrictor responses induced by ETA-and ETB-receptors. Am J Physiol Renal Physiol 294: F719-F728, 2008.
23. 2+ signaling in the cardiovascular system. Am J Cardiol 78: 2-6, 1996.
24. Kaushal RD, Wilson TW. Effect of furegrelate on renal plasma flow after angiotensin II infusion. Can J Physiol Pharmacol 68: 500-504, 1990.
25. Kawada N, Dennehy K, Solis G, Modlinger P, Hamel R, Kawada JT, Aslam S, Moriyama T, Imai E, Welch WJ, Wilcox CS. TP receptors regulate renal hemodynamics during angiotensin II slow pressor response. Am J Physiol Renal Physiol 287: F753-F759, 2004.
26. Keen HL, Brands MW, Smith MJ Jr, Shek EW, Hall JE. Inhibition of thromboxane synthesis attenuates insulin hypertension in rats. Am J Hypertens 10: 1125-1131, 1997.
27. Keen HL, Brands MW, Smith MJ Jr, Shek EW, Hall JE. Thromboxane is required for full expression of angiotensin hypertension in rats. Hypertension 29: 310-314, 1997.
28. Kopkan L, Huskova Z, Vanourkova Z, Thumova M, Skaroupkova P, Cervenka L, Majid DSA. Superoxide and its interaction with nitric oxide modulates renal function in prehypertensive Ren-2 transgenic rats. J Hypertens 25: 2257-2265, 2007.
29. Lai EY, Wellstein A, Welch WJ, Wilcox CS. Superoxide modulates myogenic contractions of mouse afferent arterioles. Hypertension 58: 650-656, 2011.
30. Liu R, Ren Y, Garvin JL, Carretero OA. Superoxide enhances tubuloglomerular feedback by constricting the afferent arteriole. Kidney Int 66: 268-274, 2004.
31. Lopez B, Salom MG, Arregui B, Valero F, Fenoy FJ. Role of superoxide in modulating the renal effects of angiotensin II. Hypertension 42: 1150-1156, 2003.
32. Loutzenhiser RD, Epstein M, Horton C, Sonke P. Reversal of renal and smooth muscle actions of the thromboxane mimetic U-44069 by diltiazem. Am J Physiol Renal Fluid Electrolyte Physiol 250: F619-F626, 1986.
33. Loutzenhiser RD, Van Breemen C. Mechanism of activation of isolated rabbit aorta by PGH2 analogue U-44069. Am J Physiol Cell Physiol 241: C243-C249, 1981.
34. Majid DSA, Nishiyama A, Jackson KE, Castillo A. Superoxide scavenging attenuates renal responses to ANG II during nitric oxide synthase inhibition in anesthetized dogs. Am J Physiol Renal Physiol 288: F412-F419, 2005.
35. 2+ handling of human small arteries. Am J Physiol Heart Circ Physiol 279: H1228-H1238, 2000.
36. Mistry M, Muirhead EE, Yamaguchi Y, Nasjletti A. Renal function in rats with angiotensin II-salt-induced hypertension: effect of thromboxane synthesis inhibition and receptor blockade. J Hypertens 8: 75-83, 1990.
37. Muzaffar S, Shukla N, Bond M, Sala-Newby G, Angelini GD, Newby AC, Jeremy JY. Acute inhibition of superoxide formation and Rac1 activation by nitric oxide and iloprost in human vascular smooth muscle cells in response to the thromboxane A2 analogue, U46619. Prostaglandins Leukot Essent Fatty Acids 78: 247-255, 2008.
38. Nishiyama A, Fukui T, Fujisawa Y, Rahman M, Tian RX, Kimura S, Abe Y. Systemic and regional hemodynamic responses to tempol in angiotensin II-infused hypertensive rats. Hypertension 37: 77-83, 2001.
39. Ogletree ML, Harris DN, Greenberg R, Haslanger MF, Nakane M. Pharmacological actions of SQ 29,548, a novel selective thromboxane antagonist. J Pharmacol Exp Ther 234: 435-441, 1985.
40. Ortiz MC, Sanabria E, Manriquez MC, Romero JC, Juncos LA. Role of endothelin and isoprostanes in slow pressor responses to angiotensin II. Hypertension 37: 505-510, 2001.
41. Perez-Vizcaino F, Villamor E, Duarte J, Tamargo J. Involvement of protein kinase C in reduced relaxant responses to the NO/cyclic GMP pathway in piglet pulmonary arteries contracted by the thromboxane A2-mimetic U46619. Br J Pharmacol 121: 1323-1333, 1997.
42. Pfister SL, Nithipatikom K, Campbell WB. Role of superoxide and thromboxane receptors in acute angiotensin II-induced vasoconstriction of rabbit vessels. Am J Physiol Heart Circ Physiol 300: H2064-H2071, 2011.
43. Schnackenberg CG, Welch WJ, Wilcox CS. TP receptor-mediated vasoconstriction in microperfused afferent arterioles: roles of O2 + and NO. Am J Physiol Renal Physiol 279: F302-F308, 2000.
44. 2+ release and vasoconstriction in small renal arteries. Microvasc Res 70: 65-75, 2005.
45. Thai TL, Arendshorst WJ. Mice lacking the ADP ribosyl cyclase CD38 exhibit attenauated renal vasoconstriction to angiotensin II, endothelin-1, and norepinephrine. Am J Physiol Renal Physiol 297: F169-F176, 2009.
46. Thai TL, Fellner SK, Arendshorst WJ. ADP-ribosyl cyclase and ryanodine receptor activity contribute to basal renal vasomotor tone and agonist-induced renal vasoconstriction in vivo. Am J Physiol Renal Physiol 293: F1107-F1114, 2007.
47. Tomida T, Numaguchi Y, Nishimoto Y, Tsuzuki M, Hayashi Y, Imai H, Matsui H, Okumura K. Inhibition of COX-2 prevents hypertension and proteinuria associated with a decrease of 8-iso-PGF2+ formation in L-NAME-treated rats. J Hypertens 21: 601-609, 2003.
48. Vagnes OB, Iversen BM, Arendshorst WJ. Short-term ANG II produces renal vasoconstriction independent of TP receptor activation and TxA2/ isoprostane production. Am J Physiol Renal Physiol 293: F860-F867, 2007.
49. Wang D, Chabrashvili T, Wilcox CS. Enhanced contractility of renal afferent arterioles from angiotensin-infused rabbits: roles of oxidative stress, thromboxane prostanoid receptors, and endothelium. Circ Res 94: 1436-1442, 2004.
50. Welch WJ, Ahlstrom NG, Wilcox CS. Mechanism of hypertension during prolonged infusion of thromboxane mimetic. Eur J Intern Med 2: 277-280, 1992.
51. Welch WJ, Wilcox CS, Folger WH. Mechanism of renal vasoconstriction with thromboxane mimetic: engagement of tubuloglomerular feedback. Adv Prostaglandin Thromboxane Leukot Res 21B: 693-696, 1991.
52. Wilson SJ, Cavanagh CC, Lesher AM, Frey AJ, Russell SE, Smyth EM. Activation-dependent stabilization of the human thromboxane receptor: role of reactive oxygen species. J Lipid Res 50: 1047-1056, 2009.
53. Yamagishi T, Yanagisawa T, Taira N. Activation of phospholipase C by the agonist U46619 is inhibited by cromakalim-induced hyperpolarization in porcine coronary artery. Biochem Biophys Res Commun 187: 1517-1522, 1992.
54. 2+ mobilization through cADP-ribose signaling in coronary arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 279: H873-H881, 2000.
55. 2+ mobilizing second messenger-cyclic ADP-ribose. J Cell Mol Med 10: 407-422, 2006.
56. Zhang AY, Yi F, Teggatz EG, Zou AP, Li PL. Enhanced production and action of cyclic ADP-ribose during oxidative stress in small bovine coronary arterial smooth muscle. Microvasc Res 67: 159-167, 2004.
57. 2+ signaling between inositol trisphosphate and ryanodine receptors. Am J Physiol Lung Cell Mol Physiol 285: L680-L690, 2003. This work was supported by National Heart, Lung, and Blood Institute Research Grant HL-02334.