Luminal flow regulates NO and O-2 along the nephron

American Journal of Physiology - Renal Physiology

Volumn 300, Issue 5, 2011, Pages 1047-1053

  Cabral, Pablo D ^a   Garvin, Jeffrey L ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ion delivery; Oxidative stress; Pressure; Reactive oxygen species; Shear stress; Stretch

Indexed keywords

BICARBONATE; CYCLIC GMP; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM CHLORIDE; SUPEROXIDE;

ARTICLE; HENLE LOOP; HYPERTENSION; INTESTINE BLOOD FLOW; KIDNEY DISTAL TUBULE; KIDNEY PROXIMAL TUBULE; MACULA DENSA; NEPHRON; NONHUMAN; PRIORITY JOURNAL; SODIUM TRANSPORT; URINE FLOW RATE; WATER ABSORPTION;

EID: 79955783370     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00724.2010     Document Type: Article

References (81)

1. Abe M, O'connor P, Kaldunski M, Liang M, Roman RJ, Cowley AW Jr. Effect of sodium delivery on superoxide and nitric oxide in the medullary thick ascending limb. Am J Physiol Renal Physiol 291: F350- F357, 2006.
2. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615, 2001.
3. Babior BM. NADPH oxidase: an update. Blood 93: 1464-1476, 1999.
4. Baer PG, Bianchi G, Liliana D. Renal micropuncture study of normotensive and Milan hypertensive rats before and after development of hypertension. Kidney Int 13: 452-466, 1978.
5. Bredt DS, Snyder SH. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 63: 175-95, 175-195, 1994.
6. Broadbelt NV, Stahl PJ, Chen J, Mizrahi M, Lal A, Bozkurt A, Poppas DP, Felsen D. Early upregulation of iNOS mRNA expression and increase in NO metabolites in pressurized renal epithelial cells. Am J Physiol Renal Physiol 293: F1877-F1888, 2007.
7. Cabral PD, Hong NJ, Garvin JL. Shear stress increases nitric oxide production in thick ascending limbs. Am J Physiol Renal Physiol 299: F1185-F1192, 2010.
8. Cabral PD, Garvin JL. ATP mediates flow-induced nitric oxide production in thick ascending limbs. FASEB J 24: 812, 2010.
9. Cai Z, Xin J, Pollock DM, Pollock JS. Shear stress-mediated NO production in inner medullary collecting duct cells. Am J Physiol Renal Physiol 279: F270-F274, 2000.
10. DiBona GF, Rios LL. Mechanism of exaggerated diuresis in spontaneously hypertensive rats. Am J Physiol 235: 409-416, 1978.
11. Dwyer TM, Schmidt-Nielsen B. The renal pelvis: machinery that concentrates urine in the papilla. News Physiol Sci 18: 1-6, 2003.
12. Feng Y, Venema VJ, Venema RC, Tsai N, Caldwell RB. VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun 256: 192-197, 1999.
13. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I. Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand 168: 81-88, 2000.
14. Fulton D, McGiff JC, Wolin MS, Kaminski P, Quilley J. Evidence against a cytochrome P450-derived reactive oxygen species as the mediator of the nitric oxide-independent vasodilator effect of bradykinin in the perfused heart of the rat. J Pharmacol Exp Ther 280: 702-709, 1997.
15. Gallis B, Corthals GL, Goodlett DR, Ueba H, Kim F, Presnell SR, Figeys D, Harrison DG, Berk BC, Aebersold R, Corson MA. Identification of flow-dependent endothelial nitric-oxide synthase phosphorylation sites by mass spectrometry and regulation of phosphorylation and nitric oxide production by the phosphatidylinositol 3-kinase inhibitor LY294002. J Biol Chem 274: 30101-30108, 1999.
16. Garvin JL, Hong NJ. Cellular stretch increases superoxide production in the thick ascending limb. Hypertension 51: 488-493, 2008.
17. Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 97: 8010-8014, 2000.
18. Gendron FP, Chalimoniuk M, Strosznajder J, Shen S, Gonzalez FA, Weisman GA, Sun GY. P2X7 nucleotide receptor activation enhances IFN gamma-induced type II nitric oxide synthase activity in BV-2 microglial cells. J Neurochem 87: 344-352, 2003.
19. Goetz RM, Thatte HS, Prabhakar P, Cho MR, Michel T, Golan DE. Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 96: 2788-2793, 1999.
20. Gorren AC, Schrammel A, Schmidt K, Mayer B. Effects of pH on the structure and function of neuronal nitric oxide synthase. Biochem J 331: 801-807, 1998.
21. Govers R, Rabelink TJ. Cellular regulation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol 280: F193-F206, 2001.
22. Grote K, Flach I, Luchtefeld M, Akin E, Holland SM, Drexler H, Schieffer B. Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase- derived reactive oxygen species. Circ Res 92: e80-e86, 2003.
23. Hecker M, Mulsch A, Bassenge E, Busse R. Vasoconstriction and increased flow: two principal mechanisms of shear stress-dependent endothelial autacoid release. Am J Physiol Heart Circ Physiol 265: H828-H833, 1993.
24. -2 in the thick ascending limb in vivo (Abstract). Hypertension 56: e50-e166, 2010.
25. Herrera M, Silva GB, Garvin JL. A high-salt diet dissociates NO synthase-3 expression and NO production by the thick ascending limb. Hypertension 47: 95-101, 2006.
26. Hishikawa K, Luscher TF. Pulsatile stretch stimulates superoxide production in human aortic endothelial cells. Circulation 96: 3610-3616, 1997.
27. Holstein-Rathlou NH, Marsh DJ. Oscillations of tubular pressure, flow, and distal chloride concentration in rats. Am J Physiol Renal Fluid Electrolyte Physiol 256: F1007-F1014, 1989.
28. Holstein-Rathlou NH, Marsh DJ. A dynamic model of the tubuloglomerular feedback mechanism. Am J Physiol Renal Fluid Electrolyte Physiol 258: F1448-F1459, 1990.
29. Hong NJ, Garvin JL. Flow increases superoxide production by NADPH oxidase via activation of Na-K-2Cl cotransport and mechanical stress in thick ascending limbs. Am J Physiol Renal Physiol 292: F993-F998, 2007.
30. Hong NJ, Garvin JL. Nitric oxide reduces flow-induced superoxide production via cGMP-dependent protein kinase in thick ascending limbs. Am J Physiol Renal Physiol 296: F1061-F1066, 2009.
31. Hong NJ, Silva GB, Garvin JL. PKC-α mediates flow-stimulated superoxide production in thick ascending limbs. Am J Physiol Renal Physiol 298: F885-F891, 2010.
32. Huie RE, Padmaja S. The reaction of no with superoxide. Free Radic Res Commun 18: 195-199, 1993.
33. Ito S, Ren Y. Evidence for the role of nitric oxide in macula densa control of glomerular hemodynamics. J Clin Invest 92: 1093-1098, 1993.
34. 2+]i increase depends on nucleotide release and subsequent purinergic signaling in the intact nephron. J Am Soc Nephrol 18: 2062-2070, 2007.
35. Kontos HA, Wei EP, Ellis EF, Jenkins LW, Povlishock JT, Rowe GT, Hess ML. Appearance of superoxide anion radical in cerebral extracellular space during increased prostaglandin synthesis in cats. Circ Res 57: 142-151, 1985.
36. Kumar U, Chen J, Sapoznikhov V, Canteros G, White BH, Sidhu A. Overexpression of inducible nitric oxide synthase in the kidney of the spontaneously hypertensive rat. Clin Exp Hypertens 27: 17-31, 2005.
37. Leyssac PP, Karlsen FM, Holstein-Rathlou NH, Skøtt O. On determinants of glomerular filtration rate after inhibition of proximal tubular reabsorption. Am J Physiol Regul Integr Comp Physiol 266: R1544- R1550, 1994.
38. Li Y, Zheng J, Bird IM, Magness RR. Effects of pulsatile shear stress on nitric oxide production and endothelial cell nitric oxide synthase expression by ovine fetoplacental artery endothelial cells. Biol Reprod 69: 1053-1059, 2003.
39. Lin MI, Fulton D, Babbitt R, Fleming I, Busse R, Pritchard KA Jr, WC Sessa. Phosphorylation of threonine 497 in endothelial nitric-oxide synthase coordinates the coupling of L-arginine metabolism to efficient nitric oxide production. J Biol Chem 278: 44719-44726, 2003.
40. Liu R, Carretero OA, Ren Y, Garvin JL. Increased intracellular pH at the macula densa activates nNOS during tubuloglomerular feedback. Kidney Int 67: 1837-1843, 2005.
41. Liu R, Carretero OA, Ren Y, Wang H, Garvin JL. Intracellular pH regulates superoxide production by the macula densa. Am J Physiol Renal Physiol 295: F851-F856, 2008.
42. Liu R, Garvin JL, Ren Y, Pagano PJ, Carretero OA. Depolarization of the macula densa induces superoxide production via NAD(P)H oxidase. Am J Physiol Renal Physiol 292: F1867-F1872, 2007.
43. Liu R, Juncos LA. GTPase-Rac enhances depolarization-induced superoxide production by the macula densa during tubuloglomerular feedback. Am J Physiol Regul Integr Comp Physiol 298: R453-R458, 2010.
44. Liu R, Ren Y, Garvin JL, Carretero OA. Superoxide enhances tubuloglomerular feedback by constricting the afferent arteriole. Kidney Int 66: 268-274, 2004.
45. Lyon-Roberts B, Strait KA, van Peursem E, Kittikulsuth W, Pollock JS, Pollock DM, Kohan DE. Flow regulation of collecting duct endothelin- 1 production. Am J Physiol Renal Physiol 300: F650-F666, 2011.
46. Majid DS, Nishiyama A. Nitric oxide blockade enhances renal responses to superoxide dismutase inhibition in dogs. Hypertension 39: 293-297, 2002.
47. Mozaffari MS, Jirakulsomchok S, Shao ZH, Wyss JM. High-NaCl diets increase natriuretic and diuretic responses in salt-resistant but not salt-sensitive SHR. Am J Physiol Renal Fluid Electrolyte Physiol 260: F890-F897, 1991.
48. Nakano D, Pollock JS, Pollock DM. Renal medullary ETB receptors produce diuresis and natriuresis via NOS1. Am J Physiol Renal Physiol 294: F1205-F1211, 2008.
49. Ortiz PA, Garvin JL. NO inhibits NaCl absorption by rat thick ascending limb through activation of cGMP-stimulated phosphodiesterase. Hypertension 37: 467-471, 2001.
50. -2 and NO in the thick ascending limb. Hypertension 39: 591-596, 2002.
51. Ortiz PA, Garvin JL. Superoxide stimulates NaCl absorption by the thick ascending limb. Am J Physiol Renal Physiol 283: F957-F962, 2002.
52. - cotransporter activity. Am J Physiol Renal Physiol 281: F819-F825, 2001.
53. Ortiz PA, Hong NJ, Garvin JL. Luminal flow induces eNOS activation and translocation in the rat thick ascending limb. Am J Physiol Renal Physiol 287: F274-F280, 2004.
54. Ortiz PA, Hong NJ, Garvin JL. Luminal flow induces eNOS activation and translocation in the rat thick ascending limb. II. Role of PI3-kinase and Hsp90. Am J Physiol Renal Physiol 287: F281-F288, 2004.
55. Ortiz PA, Hong NJ, Wang D, Garvin JL. Gene transfer of eNOS to the thick ascending limb of eNOS-KO mice restores the effects of L-arginine on NaCl absorption. Hypertension 42: 674-679, 2003.
56. Parks DA, Granger DN. Xanthine oxidase: biochemistry, distribution and physiology. Acta Physiol Scand Suppl 548: 87-99, 1986.
57. Plato CF, Shesely EG, Garvin JL. eNOS mediates L-arginine-induced inhibition of thick ascending limb chloride flux. Hypertension 35: 319-323, 2000.
58. Plato CF, Stoos BA, Wang D, Garvin JL. Endogenous nitric oxide inhibits chloride transport in the thick ascending limb. Am J Physiol Renal Physiol 276: F159-F163, 1999.
59. Pollock CA, Lawrence JR, Field MJ. Tubular sodium handling and tubuloglomerular feedback in experimental diabetes mellitus. Am J Physiol Renal Fluid Electrolyte Physiol 260: F946-F952, 1991.
60. Pou S, Keaton L, Surichamorn W, Rosen GM. Mechanism of superoxide generation by neuronal nitric-oxide synthase. J Biol Chem 274: 9573-9580, 1999.
61. Prabhakar P, Thatte HS, Goetz RM, Cho MR, Golan DE, Michel T. Receptor-regulated translocation of endothelial nitric-oxide synthase. J Biol Chem 273: 27383-27388, 1998.
62. Ramseyer V, Garvin JL. Angiotensin II decreases NOS3 expression via nitric oxide and superoxide in the thick ascending limb. Hypertension 53: 313-318, 2008.
63. Ren Y, Carretero OA, Garvin JL. Mechanism by which superoxide potentiates tubuloglomerular feedback. Hypertension 39: 624-628, 2002.
64. Ren Y, Garvin JL, Liu R, Carretero OA. Crosstalk between the connecting tubule and the afferent arteriole regulates renal microcirculation. Kidney Int 71: 1116-1121, 2007.
65. Ren Y, Garvin JL, Liu R, Carretero OA. Cross-talk between arterioles and tubules in the kidney. Pediatr Nephrol 24: 31-35, 2009.
66. Ren YL, Garvin JL, Carretero OA. Role of macula densa nitric oxide and cGMP in the regulation of tubuloglomerular feedback. Kidney Int 58: 2053-2060, 2000.
67. Roczniak A, Zimpelmann J, Burns KD. Effect of dietary salt on neuronal nitric oxide synthase in the inner medullary collecting duct. Am J Physiol Renal Physiol 275: F46-F54, 1998.
68. Sakai T, Craig DA, Wexler AS, Marsh DJ. Fluid waves in renal tubules. Biophys J 50: 805-813, 1986.
69. Schmidt-Nielsen B. The renal concentrating mechanism in insects and mammals: a new hypothesis involving hydrostatic pressures. Am J Physiol Regul Integr Comp Physiol 268: R1087-R1100, 1995.
70. Seney FD Jr, Persson EG, Wright FS. Modification of tubuloglomerular feedback signal by dietary protein. Am J Physiol Renal Fluid Electrolyte Physiol 252: F83-F90, 1987.
71. Shin SJ, Lai FJ, Wen JD, Lin SR, Hsieh MC, Hsiao PJ, Tsai JH. Increased nitric oxide synthase mRNA expression in the renal medulla of water-deprived rats. Kidney Int 56: 2191-2202, 1999.
72. Silva GB, Beierwaltes WH, Garvin JL. Extracellular ATP stimulates NO production in rat thick ascending limb. Hypertension 47: 563-567, 2006.
73. Silva GB, Ortiz PA, Hong NJ, Garvin JL. Superoxide stimulates NaCl absorption in the thick ascending limb via activation of protein kinase C. Hypertension 48: 467-472, 2006.
74. Sipos A, Vargas SL, Toma I, Hanner F, Willecke K, Peti-Peterdi J. Connexin 30 deficiency impairs renal tubular ATP release and pressure natriuresis. J Am Soc Nephrol 20: 1724-1732, 2009.
75. Stoos BA, Garcia NH, Garvin JL. Nitric oxide inhibits sodium reabsorption in the isolated perfused cortical collecting duct. J Am Soc Nephrol 6: 89-94, 1995.
76. Thorup C, Erik A, Persson G. Macula densa derived nitric oxide in regulation of glomerular capillary pressure. Kidney Int 49: 430-436, 1996.
77. Wang H, Garvin JL, D'Ambrosio MA, Ren Y, Carretero OA. Connecting tubule glomerular feedback antagonizes tubuloglomerular feedback in vivo. Am J Physiol Renal Physiol 299: F1374-F1378, 2010.
78. Welch WJ, Tojo A, Wilcox CS. Roles of NO and oxygen radicals in tubuloglomerular feedback in SHR. Am J Physiol Renal Physiol 278: F769-F776, 2000.
79. Yip KP, Holstein-Rathlou NH, Marsh DJ. Mechanisms of temporal variation in single-nephron blood flow in rats. Am J Physiol Renal Fluid Electrolyte Physiol 264: F427-F434, 1993.
80. Zhang Y, Mircheff AK, Hensley CB, Magyar CE, Warnock DG, Chambrey R, Yip KP, Marsh DJ, Holstein-Rathlou NH, McDonough AA. Rapid redistribution and inhibition of renal sodium transporters during acute pressure natriuresis. Am J Physiol Renal Fluid Electrolyte Physiol 270: F1004-F1014, 1996.
81. Zhu X, Lu D, Fu Y, Liu H, Lu Y, Juncos LA, Liu R. Shear stress at the macula densa blunts tubuloglomerular feedback via primary cilia-dependent increases in MD nNOS activity (Abstract). Hypertension 56: e50-e166. 2010.