The reduction of Na/H exchanger-3 protein and transcript expression in acute ischemia-reperfusion injury is mediated by extractable tissue factor(s)

Kidney International

Volumn 80, Issue 8, 2011, Pages 822-831

  Di Sole, Francesca ^a,b   Hu, Ming Chang ^a,b   Zhang, Jianning ^a   Babich, Victor ^a,b   Bobulescu, I Alexandru ^a,b   Shi, Mingjun ^b   McLeroy, Paul ^a   Rogers, Thomas E ^c   Moe, Orson W ^a,b,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

acute kidney injury; epithelial sodium transport; ischemia reperfusion; Na transport; proximal tubule

Indexed keywords

BINDING PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEASOME; RNA; SODIUM PROTON EXCHANGE PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; GENETIC TRANSCRIPTION; HOMOGENATE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; KIDNEY CELL; KIDNEY CORTEX; KIDNEY INJURY; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; NONHUMAN; NORTHERN BLOTTING; OPOSSUM; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; SODIUM TRANSPORT; UBIQUITINATION;

EID: 80053572127     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2011.229     Document Type: Article

References (70)

1. Ali T, Khan I, Simpson W et al. Incidence and outcomes in acute kidney injury: a comprehensive population-based study. J Am Soc Nephrol 2007; 18: 1292-1298. (Pubitemid 46536915)
2. Himmelfarb J, Ikizler TA. Acute kidney injury: changing lexicography, definitions, and epidemiology. Kidney Int 2007; 71: 971-976. (Pubitemid 46741995)
3. Thadhani R, Pascual M, Bonventre JV. Acute renal failure. N Engl J Med 1996; 334: 1448-1460. (Pubitemid 126590563)
4. Waikar SS, Bonventre JV. Biomarkers for the diagnosis of acute kidney injury. Curr Opin Nephrol Hypertens 2007; 16: 557-564. (Pubitemid 350293749)
5. Ferguson MA, Vaidya VS, Bonventre JV. Biomarkers of nephrotoxic acute kidney injury. Toxicology 2008; 245: 182-193.
6. Star RA. Treatment of acute renal failure. Kidney Int 1998; 54: 1817-1831. (Pubitemid 28533609)
7. Rosen S, Heyman SN. Difficulties in understanding human "acute tubular necrosis": limited data and flawed animal models. Kidney Int 2001; 60: 1220-1224. (Pubitemid 32960016)
8. Liu KD, Brakeman PR. Renal repair and recovery. Crit Care Med 2008; 36: S187-S192. (Pubitemid 351483050)
9. Jo SK, Rosner MH, Okusa MD. Pharmacologic treatment of acute kidney injury: why drugs havent worked and what is on the horizon. Clin J Am Soc Nephrol 2007; 2: 356-365.
10. Amemiya M, Loffing J, Lotscher M et al. Expression of NHE-3 in the apical membrane of rat renal proximal tubule and thick ascending limb. Kidney Int 1995; 48: 1206-1215.
11. Preisig PA, Ives HE, Cragoe Jr EJ et al. Role of the Na+/H+ antiporter in rat proximal tubule bicarbonate absorption. J Clin Invest 1987; 80: 970-978. (Pubitemid 18075630)
12. Preisig PA, Rector Jr FC. Role of Na+-H+ antiport in rat proximal tubule NaCl absorption. Am J Physiol 1988; 255: F461-F465.
13. Good DW, Watts III BA. Functional roles of apical membrane Na+/H+ exchange in rat medullary thick ascending limb. Am J Physiol 1996; 270: F691-F699.
14. Schultheis PJ, Clarke LL, Meneton P et al. Renal and intestinal absorptive defects in mice lacking the NHE3 Na+/H+ exchanger. Nat Genet 1998; 19: 282-285. (Pubitemid 28309344)
15. Lorenz JN, Schultheis PJ, Traynor T et al. Micropuncture analysis of singlenephron function in NHE3-deficient mice. Am J Physiol 1999; 277: F447-F453. (Pubitemid 29459657)
16. Noonan WT, Woo AL, Nieman ML et al. Blood pressure maintenance in NHE3-deficient mice with transgenic expression of NHE3 in small intestine. Am J Physiol Regul Integr Comp Physiol 2005; 288: R685-R691. (Pubitemid 40250580)
17. Wang Z, Rabb H, Craig T et al. Ischemic-reperfusion injury in the kidney: overexpression of colonic H+-K+-ATPase and suppression of NHE-3. Kidney Int 1997; 51: 1106-1115. (Pubitemid 27186536)
18. Kwon TH, Laursen UH, Marples D et al. Altered expression of renal AQPs and Na(+) transporters in rats with lithium-induced NDI. Am J Physiol Renal Physiol 2000; 279: F552-F564.
19. Wang Z, Rabb H, Haq M et al. A possible molecular basis of natriuresis during ischemic-reperfusion injury in the kidney. J Am Soc Nephrol 1998; 9: 605-613.
20. Anderson RJ, Schrier RW. Acute tubular necrosis. In: Schrier RW, Gottschalk C (eds). Diseases of the Kidney. Little, Brown and Co.: Boston/Toronto, 1988, pp 1413-1446.
21. Bobulescu IA, Moe OW. Luminal Na(+)/H (+) exchange in the proximal tubule. Pflugers Arch 2009; 458: 5-21.
22. Arroyo JD, Chevillet JR, Kroh EM et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011; 108: 5003-5008.
23. Blantz RC, Weir MR. Are the oxygen costs of kidney function highly regulated? Curr Opin Nephrol Hypertens 2004; 13: 67-71. (Pubitemid 39069901)
24. Kiil F, Sejersted OM, Steen PA. Energetics and specificity of transcellular NaCl transport in the dog kidney. Int J Biochem 1980; 12: 245-250. (Pubitemid 11246099)
25. Bagnasco S, Good D, Balaban R et al. Lactate production in isolated segments of the rat nephron. Am J Physiol 1985; 248: F522-F526. (Pubitemid 15056867)
26. Ruegg CE, Mandel LJ. Bulk isolation of renal PCT and PST. II. Differential responses to anoxia or hypoxia. Am J Physiol 1990; 259: F176-F185. (Pubitemid 20246431)
27. Thurau K, Dorge A, Mason J et al. Intracellular elemental concentrations in renal tubular cells. An electron microprobe analysis. Klin Wochenschr 1979; 57: 993-999. (Pubitemid 10194112)
28. Blantz RC, Deng A, Miracle CM et al. Regulation of kidney function and metabolism: a question of supply and demand. Trans Am Clin Climatol Assoc 2007; 118: 23-43.
29. Bobulescu IA, Moe OW. Na+/H+ exchangers in renal regulation of acidbase balance. Semin Nephrol 2006; 26: 334-344. (Pubitemid 44634900)
30. du Cheyron D, Daubin C, Poggioli J et al. Urinary measurement of Na+/H+ exchanger isoform 3 (NHE3) protein as new marker of tubule injury in critically ill patients with ARF. Am J Kidney Dis 2003; 42: 497-506. (Pubitemid 37048125)
31. Hu MC, Shi M, Zhang J et al. Klotho deficiency is an early biomarker of renal ischemia-reperfusion injury and its replacement is protective. Kidney Int 2010; 78: 1240-1251.
32. Yamashita J, Ohkita M, Takaoka M et al. Role of Na+/H+ exchanger in the pathogenesis of ischemic acute renal failure in mice. J Cardiovasc Pharmacol 2007; 49: 154-160. (Pubitemid 46579949)
33. Hropot M, Juretschke HP, Langer KH et al. S3226, a novel NHE3 inhibitor, attenuates ischemia-induced acute renal failure in rats. Kidney Int 2001; 60: 2283-2289. (Pubitemid 33070470)
34. Reuter S, Velic A, Edemir B et al. Protective role of NHE-3 inhibition in rat renal transplantation undergoing acute rejection. Pflugers Arch 2008; 456: 1075-1084.
35. Lieberthal W, Nigam SK. Acute renal failure. II. Experimental models of acute renal failure: imperfect but indispensable. Am J Physiol Renal Physiol 2000; 278: F1-F12. (Pubitemid 30106121)
36. Kinsey GR, Li L, Okusa MD. Inflammation in acute kidney injury. Nephron Exp Nephrol 2008; 109: e102-e107.
37. Bonventre JV, Zuk A. Ischemic acute renal failure: an inflammatory disease? Kidney Int 2004; 66: 480-485. (Pubitemid 38981982)
38. Schmidt C, Hocherl K, Schweda F et al. Regulation of renal sodium transporters during severe inflammation. J Am Soc Nephrol 2007; 18: 1072-1083. (Pubitemid 46536893)
39. Kohda Y, Chiao H, Star RA. alpha-Melanocyte-stimulating hormone and acute renal failure. Curr Opin Nephrol Hypertens 1998; 7: 413-417. (Pubitemid 28341754)
40. Gong H, Wang W, Kwon TH et al. EPO and alpha-MSH prevent ischemia/reperfusion-induced down-regulation of AQPs and sodium transporters in rat kidney. Kidney Int 2004; 66: 683-695. (Pubitemid 38982012)
41. Haase VH. Hypoxia-inducible factors in the kidney. Am J Physiol Renal Physiol 2006; 291: F271-F281. (Pubitemid 44148116)
42. Shimoda LA, Fallon M, Pisarcik S et al. HIF-1 regulates hypoxic induction of NHE1 expression and alkalinization of intracellular pH in pulmonary arterial myocytes. Am J Physiol Lung Cell Mol Physiol 2006; 291: L941-L949. (Pubitemid 44772056)
43. Bhatt K, Mi QS, Dong Z. microRNAs in kidneys: biogenesis, regulation, and pathophysiological roles. Am J Physiol Renal Physiol 2011; 300: F602-F610.
44. Godwin JG, Ge X, Stephan K et al. Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci USA 2010; 107: 14339-14344.
45. Bobulescu IA. Renal lipid metabolism and lipotoxicity. Curr Opin Nephrol Hypertens 2010; 19: 393-402.
46. Bobulescu IA, Di Sole F, Moe OW. Na+/H+ exchangers: physiology and link to hypertension and organ ischemia. Curr Opin Nephrol Hypertens 2005; 14: 485-494. (Pubitemid 41152713)
47. Zachos NC, Kovbasnjuk O, Donowitz M. Regulation of intestinal electroneutral sodium absorption and the brush border Na+/H+ exchanger by intracellular calcium. Ann NY Acad Sci 2009; 1165: 240-248.
48. Yang X, Amemiya M, Peng Y et al. Acid incubation causes exocytic insertion of NHE3 in OKP cells. Am J Physiol Cell Physiol 2000; 279: C410-C419.
49. Ambuhl PM, Amemiya M, Danczkay M et al. Chronic metabolic acidosis increases NHE3 protein abundance in rat kidney. Am J Physiol 1996; 271: F917-F925.
50. Amemiya M, Yamaji Y, Cano A et al. Acid incubation increases NHE-3 mRNA abundance in OKP cells. Am J Physiol 1995; 269: C126-C133.
51. Baum M, Amemiya M, Dwarakanath V et al. Glucocorticoids regulate NHE-3 transcription in OKP cells. Am J Physiol 1996; 270: F164-F169.
52. Olson TS, Dice JF. Regulation of protein degradation rates in eukaryotes. Curr Opin Cell Biol 1989; 1: 1194-1200. (Pubitemid 20110927)
53. Lee DH, Goldberg AL. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 1998; 8: 397-403. (Pubitemid 28458705)
54. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998; 67: 425-479. (Pubitemid 28411135)
55. Hicke L. Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J 1997; 11: 1215-1226. (Pubitemid 27527885)
56. Hicke L. Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2001; 2: 195-201. (Pubitemid 33675744)
57. Ward CL, Omura S, Kopito RR. Degradation of CFTR by the ubiquitinproteasome pathway. Cell 1995; 83: 121-127.
58. Coux O, Tanaka K, Goldberg AL. Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem 1996; 65: 801-847. (Pubitemid 26255262)
59. Mitch WE, Goldberg AL. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 1996; 335: 1897-1905. (Pubitemid 26419198)
60. Jeffers M, Taylor GA, Weidner KM et al. Degradation of the Met tyrosine kinase receptor by the ubiquitin-proteasome pathway. Mol Cell Biol 1997; 17: 799-808. (Pubitemid 27044379)
61. Malik B, Yue Q, Yue G et al. Role of Nedd4-2 and polyubiquitination in epithelial sodium channel degradation in untransfected renal A6 cells expressing endogenous ENaC subunits. Am J Physiol Renal Physiol 2005; 289: F107-F116. (Pubitemid 40863578)
62. Simonin A, Fuster D. Nedd4-1 and beta-arrestin-1 are key regulators of Na+/H+ exchanger 1 ubiquitylation, endocytosis, and function. J Biol Chem 2010; 285: 38293-38303.
63. Di Sole F, Cerull R, Babich V et al. Acute regulation of Na/H exchanger NHE3 by adenosine A(1) receptors is mediated by calcineurin homologous protein. J Biol Chem 2004; 279: 2962-2974. (Pubitemid 38114289)
64. Di Sole F, Babich V, Moe OW. The calcineurin homologous protein-1 increases Na(+)/H(+) -exchanger 3 trafficking via ezrin phosphorylation. J Am Soc Nephrol 2009; 20: 1776-1786.
65. Wiederkehr MR, Di Sole F, Collazo R et al. Characterization of acute inhibition of Na/H exchanger NHE-3 by dopamine in opossum kidney cells. Kidney Int 2001; 59: 197-209. (Pubitemid 32063018)
66. Currie MG, Geller DM, Cole BR et al. Bioactive cardiac substances: potent vasorelaxant activity in mammalian atria. Science 1983; 221: 71-73. (Pubitemid 13061693)
67. Robenek H, Hofnagel O, Buers I et al. Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. J Cell Sci 2006; 119: 4215-4224. (Pubitemid 44774028)
68. Smith DW, Brown DM, Carnes WH. Preparation and properties of saltsoluble elastin. J Biol Chem 1972; 247: 2427-2432.
69. Di Sole F, Cerull R, Babich V et al. Short- and long-term A3 adenosine receptor activation inhibits the Na+/H+ exchanger NHE3 activity and expression in opossum kidney cells. J Cell Physiol 2008; 216: 221-233. (Pubitemid 351813113)
70. Di Sole F, Cerull R, Casavola V et al. Molecular aspects of acute inhibition of Na(+)-H(+) exchanger NHE3 by A(2)-adenosine receptor agonists. J Physiol 2002; 541: 529-543. (Pubitemid 35190218)