Depolarization of the macula densa induces superoxide production via NAD(P)H oxidase

American Journal of Physiology - Renal Physiology

Volumn 292, Issue 6, 2007, Pages

  Liu, Ruisheng ^a   Garvin, Jeffrey L ^a   Ren, YiLin ^a   Pagano, Patrick J ^a   Carretero, Oscar A ^a  

^a HENRY FORD HOSPITAL   (United States)

Author keywords

Tubuloglomerular feedback

Indexed keywords

APOCYNIN; FLUORESCENT DYE; FUROSEMIDE; HYDROETHIDINE; OXYETHIDIUM; POTASSIUM CHLORIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM CHLORIDE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SUPEROXIDE; SUPEROXIDE DISMUTASE; TEMPOL; UNCLASSIFIED DRUG; VALINOMYCIN; AMINE OXIDE; DIURETIC AGENT; NITRIC OXIDE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2 PROTEIN; SODIUM-POTASSIUM CHLORIDE COTRANSPORTER 2 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEPOLARIZATION; FEEDBACK SYSTEM; GENE INACTIVATION; GLOMERULAR STRUCTURE; HENLE LOOP; KIDNEY PARENCHYMA; MACULA DENSA; MALE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; RABBIT; ANIMAL; ARTERIOLE; GLOMERULUS; IN VITRO STUDY; KIDNEY TUBULE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPIN LABELING;

ANIMALS; ARTERIOLES; CYCLIC N-OXIDES; DIURETICS; FEEDBACK; FUROSEMIDE; KIDNEY GLOMERULUS; KIDNEY TUBULES; LOOP OF HENLE; MALE; NADPH OXIDASE; NITRIC OXIDE; POTASSIUM CHLORIDE; RABBITS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SPIN LABELS; SUPEROXIDES; VALINOMYCIN;

EID: 34447624146     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00515.2006     Document Type: Article

References (59)

1. Aviv A, Hollenberg NK, Weder AB. Sodium glomerulopathy: tubuloglomerular feedback and renal injury in African Americans. Kidney Int 65: 361-368, 2004.
2. Babior BM, Lambeth JD, Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys 397: 342-344, 2002.
3. + channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 287: 138-142, 2000.
4. 2+-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 276: 37594-37601, 2001.
5. Bell PD, Lapointe JY, Sabirov R, Hayashi S, Peti-Peterdi J, Manabe K, Kovacs G, Okada Y. Macula densa cell signaling involves ATP release through a maxi anion channel. Proc Natl Acad Sci USA 100: 4322-4327, 2003.
6. Chabrashvili T, Tojo A, Onozato ML, Kitiyakara C, Quinn MT, Fujita T, Welch WJ, Wilcox CS. Expression and cellular localization of classic NADPH oxidase subunits in the spontaneously hypertensive rat kidney. Hypertension 39: 269-274, 2002.
7. De Deken X, Wang D, Many MC, Costagliola S, Libert F, Vassart G, Dumont JE, Miot F. Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J Biol Chem 275: 23227-23233, 2000.
8. Dobrian AD, Schriver SD, Khraibi AA, Prewitt RL. Pioglitazone prevents hypertension and reduces oxidative stress in diet-induced obesity. Hypertension 43: 48-56, 2004.
9. Dupuy C, Ohayon R, Valent A, Noel-Hudson MS, Deme D, Virion A. Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cDNAs. J Biol Chem 274: 37265-37269, 1999.
10. Edens WA, Sharling L, Cheng G, Shapira R, Kinkade JM, Lee T, Edens HA, Tang X, Sullards C, Flaherty DB, Benian GM, Lambeth JD. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol 154: 879-891, 2001.
11. Ergul A, Johansen JS, Strømhaug C, Harris AK, Hutchinson J, Tawfik A, Rahimi A, Rhim E, Wells B, Caldwell RW, Anstadt MP. Vascular dysfunction of venous bypass conduits is mediated by reactive oxygen species in diabetes: role of endothelin-1. J Pharmacol Exp Ther 313: 70-77, 2004.
12. Fink B, Laude K, McCann L, Doughan A, Harrison DG, Dikalov S. Detection of intracellular superoxide formation in endothelial cells and intact tissues using dihydroethidium and an HPLC-based assay. Am J Physiol Cell Physiol 287: C895-C902, 2004.
13. Fujii S, Zhang L, Igarashi J, Kosaka H. L-Arginine reverses p47phox and gp91phox expression induced by high salt in Dahl rats. Hypertension 42: 1014-1020, 2003.
14. Gao WD, Liu Y, Marban E. Selective effects of oxygen free radicals on excitation-contraction coupling in ventricular muscle. Implications for the mechanism of stunned myocardium. Circulation 94: 2597-2604, 1996.
15. Geiszt M, Kopp JB, PVárnai, Leto TL. Identification of Renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 97: 8010-8014, 2000.
16. Herrera M, Silva G, Garvin JL. A high-salt diet dissociates NO synthase-3 expression and NO production by the thick ascending limb. Hypertension 47: 95-101, 2006.
17. Higashi Y, Sasaki S, Nakagawa K, Matsuura H, Oshima T, Chayama K. Endothelial dysfunction and oxidative stress in renovascular hypertension. N Engl J Med 346: 1954-1962, 2002.
18. 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 In press.
19. Huang CL, Cogan MG. Atrial natriuretic factor inhibits maximal tubuloglomerular feedback response. Am J Physiol Renal Fluid Electrolyte Physiol 252: F825-F828, 1987.
20. Inscho EW, Ohishi K, Navar LG. Effects of ATP on pre- and postglomerular juxtamedullary microvasculature. Am J Physiol Renal Fluid Electrolyte Physiol 263: F886-F893, 1992.
21. Kikuchi H, Hikage M, Miyashita H, Fukumoto M. NADPH oxidase subunit, 6p91(phox) homologue, preferentially expressed in human colon epithelial cells. Gene 254: 237-243, 2000.
22. Kishi T, Hirooka Y, Kimura Y, Ito K, Shimokawa H, Takeshita A. Increased reactive oxygen species in rostral ventrolateral medulla contribute to neural mechanisms of hypertension in stroke-prone spontaneously hypertensive rats. Circulation 109: 2357-2362, 2004.
23. Kotchen TA, Piering AW, Cowley AW, Grim CE, Gaudet D, Hamet P, Kaldunski ML, Kotchen JM, Roman RJ. Glomerular hyperfiltration in hypertensive African Americans. Hypertension 35: 822-826, 2000.
24. Kurtz A, Pfeilschifter J, Brown CD, Bauer C. NaCl transport stimulates prostaglandin release in cultured renal epithelial (MDCK) cells. Am J Physiol Cell Physiol 250: C676-C681, 1986.
25. Landmesser U, Cai H, Dikalov S, McCann L, Hwang J, Jo H, Holland SM, Harrison DG. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension 40: 511-515, 2002.
26. Lee VM, Quinn PA, Jennings SC, Ng LL. Neutrophil activation and production of reactive oxygen species in pre-eclampsia. J Hypertens 21: 395-402, 2003.
27. Lip GY, Edmunds E, Nuttall SL, Landray MJ, Blann AD, Beevers DG. Oxidative stress in malignant and non-malignant phase hypertension. J Hum Hypertens 16: 333-336, 2002.
28. 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, 2004.
29. Liu R, Persson AE. Simultaneous changes of cell volume and cytosolic calcium concentration in macula densa cells caused by alterations of luminal NaCl concentration. J Physiol 563: 895-901, 2005.
30. Liu R, Pittner J, Persson AEG. The changes of nitric oxide concentration in macula densa cells caused by changes in luminal NaCl concentration. J Am Soc Nephrol 13: 2688-2696, 2002.
31. Liu R, Ren Y, Garvin JL, Carretero OA. Superoxide enhances tubuloglomerular feedback by constricting the afferent arteriole. Kidney Int 66: 268-274, 2004.
32. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared with other NADPH oxidases. Cell Signal 18: 69-82, 2006.
33. Meyer JW, Schmitt ME. A central role for the endothelial NADPH oxidase in atherosclerosis. FEBS Lett 472: 1-4, 2000.
34. Mori T, Cowley AW Jr. Renal oxidative stress in medullary thick ascending limbs produced by elevated NaCl and glucose. Hypertension 43: 341-346, 2004.
35. Navar LG, Bell PD, Thomas CE, Ploth DW. Influence of perfusate osmolality on stop-flow pressure feedback responses in the dog. Am J Physiol Renal Fluid Electrolyte Physiol 235: F352-F358, 1978.
36. Nishiyama A, Yao L, Nagai Y, Miyata K, Yoshizumi M, Kagami S, Kondo S, Kiyomoto H, Shokoji T, Kimura S, Kohno M, Abe Y. Possible contributions of reactive oxygen species and mitogen-activated protein kinase to renal injury in alsosterone/salt-induced hypertensive rats. Hypertension 24: 841-848, 2004.
37. 2+] signaling pathway in macula densa cells. Am J Physiol Renal Physiol 277: F472-F476, 1999.
38. Price DA, Fisher ND, Lansang MC, Stevanovic R, Williams GH, Hollenberg NK. Renal perfusion in blacks: alterations caused by insuppressibility of intrarenal renin with salt. Hypertension 40: 186-189, 2002.
39. Ren Y, Carretero OA, Garvin JL. Mechanism by which superoxide potentiates tubuloglomerular feedback. Hypertension 39: 624-628, 2002.
40. Ren Y, Garvin JL, Carretero OA. Vasodilator action of angiotensin-(1-7) on isolated rabbit afferent arterioles. Hypertension 39: 799-802, 2002.
41. Ren Y, Garvin JL, Liu R, Carretero OA. Role of macula densa adenosine triphosphate (ATP) in tubuloglomerular feedback. Kidney Int 66: 1479-1485, 2004.
42. Ren Y, Yu H, Wang H, Carretero OA, Garvin JL. Nystatin and valinomycin induce tubuloglomerular feedback. Am J Physiol Renal Physiol 281: F1102-F1108, 2001.
43. + cotransport. Pflügers Arch 414: 286-290, 1989.
44. Shiose A, Kuroda J, Tsuruya K, Hirai M, Hirakata H, Naito S, Hattori M, Sakaki Y, Sumimoto H. A novel superoxide-producing NAD(P)H oxidase in kidney. J Biol Chem 276: 1417-1423, 2001.
45. Sohn HY, Keller M, Gloe T, Morawietz H, Rueckschloss U, Pohl U. The small G-protein Rac mediates depolarization-induced superoxide formation in human endothelial cells. J Biol Chem 275: 18745-18750, 2000.
46. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401: 79-82, 1999.
47. Sun D, Samuelson LC, Yang T, Huang Y, Paliege A, Saunders T, Briggs J, Schnermann J. Mediation of tubuloglomerular feedback by adenosine: evidence from mice lacking adenosine 1 receptors. Proc Natl Acad Sci USA 98: 9983-9988, 2001.
48. Terada LS. Specificity in reactive oxidant signaling: think globally, act locally. J Cell Biol 174: 615-623, 2006.
49. Vaziri ND, Wang XQ, Oveisi F, Rad B. Induction of oxidative stress by glutathione depletion causes severe hypertension in normal rats. Hypertension 36: 142-146, 2000.
50. Virdis A, Neves MF, Amiri F, Viel E, Touyz RM, Schiffrin EL. Spironolactone improves angiotensin-induced vascular changes and oxidative stress. Hypertension 40: 504-510, 2002.
51. Wallwork CJ, Parks DA, Schmid-Schonbein GW. Xanthine oxidase activity in the dexamethasone-induced hypertensive rat. Microvasc Res 66: 30-37, 2003.
52. Ward NC, Hodgson JM, Puddey IB, Mori TA, Beilin LJ, Croft KD. Oxidative stress in human hypertension: association with antihypertensive treatment, gender, nutrition, and lifestyle. Free Radic Biol Med 36: 226-232, 2004.
53. Welch WJ, Tojo A, Lee JU, Kang DG, Schnackenberg CG, Wilcox CS. Nitric oxide synthase in the JGA of the SHR: expression and role in tubuloglomerular feedback. Am J Physiol Renal Physiol 277: F130-F138, 1999.
54. 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.
55. Whitin JC, Chapman CE, Simons ER, Chovaniec ME, Cohen HJ. Correlation between membrane potential changes and superoxide production in human granulocytes stimulated by phorbol myristate acetate. Evidence for defective activation in chronic granulomatous disease. J Biol Chem 255: 1874-1878, 1980.
56. Wilcox CS, Welch WJ, Murad F, Gross SS, Taylor G, Levi R, Schmidt HHW. Nitric oxide synthase in macula densa regulates glomerular capillary pressure. Proc Natl Acad Sci USA 89: 11993-11997, 1992.
57. Zhang Z, Dmitrieva NI, Park JH, Levine RL, Burg MB. High urea and NaCl carbonylate proteins in renal cells in culture and in vivo, and high urea causes 8-oxoguanine lesions in their DNA. Proc Natl Acad Sci USA 101: 9491-9496, 2004.
58. Zhao H, Kalivendi S, Zhang H, Joseph J, Nithipatikom K, Vásquez-Vivar, Kalyanaraman B. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 34: 1359-1368, 2003.
59. Zhou X, Ferraris JD, Cai Q, Agarwal A, Burg MB. Increased reactive oxygen species contribute to high NaCl-induced activation of the osmoregulatory transcription factor TonEBP/OREBP. Am J Physiol Renal Physiol 289: F377-F385, 2005.