Regulation of hypoxia-inducible factor in kidney disease

Clinical and Experimental Pharmacology and Physiology

Volumn 40, Issue 2, 2013, Pages 148-157

  Nangaku, Masaomi ^a   Rosenberger, Christian ^b   Heyman, Samuel N ^d   Eckardt, Kai Uwe ^c  

^a UNIVERSITY OF TOKYO   (Japan)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Acute kidney injury; Chronic hypoxia; Chronic kidney disease; Hypoxia; Hypoxia indible factor; Kidney; Renal failure

Indexed keywords

ERYTHROPOIETIN; GLUCOSE TRANSPORTER; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEME OXYGENASE; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1; INDUCIBLE NITRIC OXIDE SYNTHASE; KELCH LIKE ECH ASSOCIATED PROTEIN 1;

ACUTE KIDNEY FAILURE; CELL PROTECTION; CHRONIC KIDNEY DISEASE; DEFENSE MECHANISM; DISEASE DURATION; GLOMERULUS FILTRATION RATE; GLUCOSE METABOLISM; HUMAN; HYDROXYLATION; HYPERKERATOSIS; HYPOXIA; IMMUNOHISTOCHEMISTRY; ISCHEMIA; KIDNEY DISEASE; KIDNEY DISTAL TUBULE; KIDNEY POLYCYSTIC DISEASE; KIDNEY PROXIMAL TUBULE; KIDNEY TRANSPLANTATION; NONHUMAN; OXYGEN TENSION; OXYGENATION; PODOCYTE; POLYCYTHEMIA; PROTEIN EXPRESSION; RENAL PROTECTION; REVIEW; SODIUM ABSORPTION; TENSION; VASOCONSTRICTION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; KIDNEY DISEASES;

EID: 84873104259     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12005     Document Type: Review

References (80)

1. Nangaku M, Eckardt KU. Hypoxia and the HIF system in kidney disease. J. Mol. Med. 2007; 85: 1325-30.
2. Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011; 16: 123-40.
3. Pergola PE, Raskin P, Toto RD et al. Bardoxolone methyl and kidney function in CKD with Type 2 diabetes. N. Engl. J. Med. 2011; 365: 327-36.
4. Wakabayashi N, Itoh K, Wakabayashi J et al. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat. Genet. 2003; 35: 238-45.
5. Rosenberger C, Mandriota S, Jürgensen JS et al. Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys. J. Am. Soc. Nephrol. 2002; 13: 1721-32.
6. Wiesener MS, Jürgensen JS, Rosenberger C et al. Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 2003; 17: 271-3.
7. Rosenberger C, Griethe W, Gruber G et al. Cellular responses to hypoxia after renal segmental infarction. Kidney Int. 2003; 64: 874-86.
8. Aprelikova O, Chandramouli GV, Wood M et al. Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J. Cell. Biochem. 2004; 92: 491-501.
9. Appelhoff RJ, Tian YM, Raval RR et al. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 2004; 279: 38 458-65.
10. Schödel J, Klanke B, Weidemann A et al. HIF-prolyl hydroxylases in the rat kidney: Physiologic expression patterns and regulation in acute kidney injury. Am. J. Pathol. 2009; 174: 1663-74.
11. Schödel J, Bohr D, Klanke B et al. Factor inhibiting HIF limits the expression of hypoxia-inducible genes in podocytes and distal tubular cells. Kidney Int. 2010; 78: 857-67.
12. Koivunen P, Hirsilä M, Günzler V, Kivirikko KI, Myllyharju J. Catalytic properties of the asparaginyl hydroxylase (FIH) in the oxygen sensing pathway are distinct from those of its prolyl 4-hydroxylases. J. Biol. Chem. 2004; 279: 9899-904.
13. Jewell UR, Kvietikova I, Scheid A, Bauer C, Wenger RH, Gassmann M. Induction of HIF-1α in response to hypoxia is instantaneous. FASEB J. 2001; 15: 1312-4.
14. Heldmaier G, Ortmann S, Elvert R. Natural hypometabolism during hibernation and daily torpor in mammals. Respir. Physiol. Neurobiol. 2004; 141: 317-29.
15. Gross MW, Karbach U, Groebe K, Franko AJ, Mueller-Klieser W. Calibration of misonidazole labeling by simultaneous measurement of oxygen tension and labeling density in multicellular spheroids. Int. J. Cancer 1995; 61: 567-73.
16. Rosenberger C, Heyman SN, Rosen S et al. Upregulation of HIF in acute renal failure: Evidence for a protective transcriptional response to hypoxia. Kidney Int. 2005; 67: 531-42.
17. Rosenberger C, Goldfarb M, Shina A et al. Evidence for sustained renal hypoxia and transient hypoxia adaptation in experimental rhabdomyolysis-induced acute kidney injury. Nephrol. Dial. Transplant. 2008; 23: 1135-43.
18. Wahlberg J. The renal response to ureteral obstruction. Scand. J. Urol. Nephrol. Suppl. 1983; 73: 1-30.
19. Nørregaard R, Bødker T, Jensen BL, Stødkilde L, Nielsen S, Frøkiaer J. Increased renal adrenomedullin expression in rats with ureteral obstruction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009; 296: R185-92.
20. Zhang S, Han CH, Chen XS et al. Transient ureteral obstruction prevents against kidney ischemia/reperfusion injury via hypoxia-inducible factor (HIF)-2a activation. PLoS ONE 2012; 7: e29876.
21. Rosenberger C, Shina A, Rosen S, Goldfarb M, Eckardt K, Heyman SN. Hypoxia inducible factors and tubular cell survival in isolated perfused kidneys. Kidney Int. 2006; 70: 60-70.
22. Rosenberger C, Rosen S, Shina A et al. Activation of hypoxia inducible factors (HIF) ameliorates hypoxic distal tubular injury in the isolated perfused rat kidney. Nephrol. Dial. Transplant. 2008; 23: 3472-8.
23. Heyman SN, Rosenberger C, Rosen S. Experimental ischemia-reperfusion: Biases and myths. The proximal vs. distal hypoxic tubular injury debate revisited. Kidney Int. 2010; 77: 9-16.
24. Tanaka T, Kojima I, Ohse T et al. Hypoxia-inducible factor modulates tubular cell survival in cisplatin nephrotoxicity. Am. J. Physiol. Renal Physiol. 2005; 289: F1123-33.
25. Weidemann A, Bernhardt WM, Klanke B et al. HIF activation protects from acute kidney injury. J. Am. Soc. Nephrol. 2008; 19: 486-94.
26. Rosenberger C, Pratschke J, Rudolph B et al. Immunohistochemical detection of hypoxia-inducible factor-1alpha in human renal allograft biopsies. J. Am. Soc. Nephrol. 2007; 18: 343-51.
27. Conde E, Alegre L, Blanco-Sanchez I et al. Hypoxia inducible factor 1-alpha (HIF-1alpha) is induced during reperfusion after renal ischemia and is critical for proximal tubule cell survival. PLoS ONE 2012; 7: e33258.
28. Rich MW, Crecelius CA. Incidence, risk factors, and clinical course of acute renal insufficiency after cardiac catheterization in patients 70 years of age or older. A prospective study. Arch. Intern. Med. 1990; 150: 1237-42.
29. Manotham K, Tanaka T, Ohse T et al. A biologic role of HIF-1 in the renal medulla. Kidney Int. 2005; 67: 1428-39.
30. Tanaka T, Kato H, Kojima I et al. Hypoxia and expression of hypoxia-inducible factor in the aging kidney. J. Gerontol. A Biol. Sci. Med. Sci. 2006; 61: 795-805.
31. Rosenberger C, Khamaisi M, Abassi Z et al. Adaptation to hypoxia in the diabetic rat kidney. Kidney Int. 2008; 73: 34-42.
32. Goldfarb M, Rosenberger C, Abassi Z et al. Acute-on-chronic renal failure in the rat: Functional compensation and hypoxia tolerance. Am. J. Nephrol. 2006; 26: 22-33.
33. Yeo EJ, Chun YS, Cho YS et al. YC-1: A potential anticancer drug targeting hypoxia-inducible factor 1. J. Natl Cancer Inst. 2003; 95: 516-25.
34. Hill P, Shukla D, Tran MGB et al. Inhibition of hypoxia inducible factor hydroxylases protects against renal ischemia-reperfusion injury. J. Am. Soc. Nephrol. 2008; 19: 39-46.
35. Kojima I, Tanaka T, Inagi R et al. Protective role of hypoxia-inducible factor-2a against ischemic damage and oxidative stress in the kidney. J. Am. Soc. Nephrol. 2007; 18: 1218-26.
36. Zhang L, Huang H, Cheng J et al. Pre-treatment with isoflurane ameliorates renal ischemic-reperfusion injury in mice. Life Sci. 2011; 88: 1102-7.
37. Bernhardt WM, Campean V, Kany S et al. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J. Am. Soc. Nephrol. 2006; 17: 1970-8.
38. Faleo G, Seda Neto J, Kohmoto J et al. Carbon monoxide ameliorates renal cold ischemia-reperfusion injury with an upregulation of vascular endothelial growth factor by activation of hypoxia-inducible factor. Transplantation 2008; 85: 1833-40.
39. Yang CC, Lin LC, Wu MS, Chien CT, Lai MK. Repetitive hypoxic preconditioning attenuates renal ischemia/reperfusion induced oxidative injury via upregulating HIF-1 alpha-dependent bcl-2 signaling. Transplantation 2009; 88: 1251-60.
40. Matsumoto M, Makino Y, Tanaka T et al. Induction of renoprotective gene expression by cobalt ameliorates ischemic injury of the kidney in rats. J. Am. Soc. Nephrol. 2003; 14: 1825-32.
41. Tanaka T, Kojima I, Ohse T et al. Cobalt promotes angiogenesis via hypoxia-inducible factors and protects ischemic tubulointerstitium in the remnant kidney. Lab. Invest. 2005; 85: 1292-307.
42. Tanaka T, Matsumoto M, Inagi R et al. Induction of renoprotective gene expression by cobalt ameliorates tubulointerstitial injury in the progressive Thy1 nephritis model. Kidney Int. 2005; 68: 2714-25.
43. Bernhardt WM, Gottmannb U, Doyon F et al. Donor treatment with a PHD-inhibitor activating HIFs prevents graft injury and prolongs survival in an allogenic kidney transplant model. Proc. Natl Acad. Sci. USA. 2009; 106: 21 276-81.
44. Kapitsinou PP, Jaffe J, Michael M et al. Preischemic targeting of HIF prolyl hydroxylation inhibits fibrosis associated with acute kidney injury. Am. J. Physiol. Renal Physiol. 2012; 302: F1172-9.
45. Wang Z, Schley G, Türkoglu G et al. The protective effect of prolyl-hydroxylase inhibition against renal ischaemia requires application prior to ischaemia but is superior to EPO treatment. Nephrol. Dial. Transplant. 2012; 27: 929-36.
46. Schley G, Klanke B, Schödel J et al. Hypoxia-inducible transcription factors stabilization in the thick ascending limb protects against ischemic acute kidney injury. J. Am. Soc. Nephrol. 2011; 22: 2004-15.
47. Iguchi M, Kakinuma Y, Kurabayashi A et al. Acute inactivation of the VHL gene contributes to protective effects of ischemic preconditioning in the mouse kidney. Nephron Exp. Nephrol. 2008; 110: e82-90.
48. Yeh CH, Hsu SP, Yang CC, Chien CT, Wang NP. Hypoxic preconditioning reinforces HIF-alpha-dependent HSP70 signaling to reduce ischemic renal failure-induced renal tubular apoptosis and autophagy. Life Sci. 2010; 86: 115-23.
49. Zhang XL, Yan ZW, Sheng WW, Xiao J, Zhang ZX, Ye ZB. Activation of hypoxia-inducible factor-1 ameliorates postischemic renal injury via inducible nitric oxide synthase. Mol. Cell. Biochem. 2011; 358: 287-95.
50. Nangaku M. Chronic hypoxia and tubulointerstitial injury: A final common pathway to end-stage renal failure. J. Am. Soc. Nephrol. 2006; 17: 17-25.
51. Mimura I, Nangaku M. The suffocating kidney: Tubulointerstitial hypoxia in end-stage renal disease. Nat. Rev. Nephrol. 2010; 6: 667-78.
52. Palm F, Cederberg J, Hansell P, Liss P, Carlsson PO. Reactive oxygen species cause diabetes-induced decrease in renal oxygen tension. Diabetologia 2003; 46: 1153-60.
53. Matsumoto M, Tanaka T, Yamamoto T et al. Hypoperfusion of peritubular capillaries induces chronic hypoxia before progression of tubulointerstitial injury in a progressive model of rat glomerulonephritis. J. Am. Soc. Nephrol. 2004; 15: 1574-81.
54. Manotham K, Tanaka T, Matsumoto M et al. Evidence of tubular hypoxia in the early phase in the remnant kidney model. J. Am. Soc. Nephrol. 2004; 15: 1277-88.
55. Izuhara YNangaku M, Inagi R et al. Renoprotective properties of angiotensin receptor blockers beyond blood pressure lowering. J. Am. Soc. Nephrol. 2005; 16: 3631-41.
56. Ries M, Basseau F, Tyndal B et al. Renal diffusion and BOLD MRI in experimental diabetic nephropathy. Blood oxygen level-dependent. J. Magn. Reson. Imaging 2003; 17: 104-13.
57. dos Santos EA, Li LP, Ji L, Prasad PV. Early changes with diabetes in renal medullary hemodynamics as evaluated by fiberoptic probes and BOLD magnetic resonance imaging. Invest. Radiol. 2007; 42: 157-62.
58. Tanaka T, Miyata T, Inagi R, Fujita T, Nangaku M. Hypoxia in renal disease with proteinuria and/or glomerular hypertension. Am. J. Pathol. 2004; 165: 1979-92.
59. Inoue T, Kozawa E, Okada H et al. Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging. J. Am. Soc. Nephrol. 2011; 22: 1429-34.
60. Wang ZJ, Kumar R, Banerjee S, Hsu CY. Blood oxygen level-dependent (BOLD) MRI of diabetic nephropathy: Preliminary experience. J. Magn. Reson. Imaging 2011; 33: 655-60.
61. Yin WJ, Liu F, Li XM et al. Noninvasive evaluation of renal oxygenation in diabetic nephropathy by BOLD-MRI. Eur. J. Radiol. 2012; 81: 1426-31.
62. Singh P, Blantz RC, Rosenberger C, Gabbai FB, Schoeb TR, Thomson SC. Aberrant tubuloglomerular feedback and HIF-1α confer resistance to ischemia after subtotal nephrectomy. J. Am. Soc. Nephrol. 2012; 23: 483-93.
63. Katavetin P, Miyata T, Inagi R et al. High glucose blunts vascular endothelial growth factor response to hypoxia via the oxidative stress-regulated hypoxia-inducible factor/hypoxia-responsible element pathway. J. Am. Soc. Nephrol. 2006; 17: 1405-13.
64. Yu X, Fang Y, Ding X et al. Transient hypoxia-inducible factor activation in rat renal ablation and reduced fibrosis with 1-mimosine. Nephrology 2012; 17: 58-67.
65. Bernhardt WM, Wiesener MS, Weidemann A et al. Involvement of hypoxia-inducible transcription factors in polycystic kidney disease. Am. J. Pathol. 2007; 170: 830-42.
66. Bernhardt WM, Wiesener MS, Scigalla P et al. Inhibition of prolyl hydroxylases increases erythropoietin production in ESRD. J. Am. Soc. Nephrol. 2010; 21: 2151-6.
67. Ohtomo S, Nangaku M, Izuhara Y, van Ypersele de Strihou C, Miyata T. Induction of hypoxia inducible factor (HIF)-regulated genes by cobalt ameliorates renal injury in an obese, hypertensive Type 2 diabetes rat model. Nephrol. Dial. Transplant. 2008; 23: 1166-72.
68. Song YR, You SJ, Lee YM et al. Activation of hypoxia-inducible factor attenuates renal injury in rat remnant kidney. Nephrol. Dial. Transplant. 2009; 25: 77-85.
69. Yu X, Fang Y, Liu H et al. The balance of beneficial and deleterious effects of hypoxia-inducible factor activation by prolyl hydroxylase inhibitor in rat remnant kidney depends on the timing of administration. Nephrol. Dial. Transplant. 2012; 27: 3110-9.
70. Schietke R, Warnecke C, Wacker I et al. The lysyl oxidases LOX and LOXL2 are necessary and sufficient to repress E-cadherin in hypoxia: Insights into cellular transformation processes mediated by HIF-1. J. Biol. Chem. 2010; 285: 6658-69.
71. Higgins DF, Kimura K, Bernhardt WM et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J. Clin. Invest. 2007; 117: 3810-20.
72. Humphreys BD, Lin SL, Kobayashi A et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 2010; 176: 85-97.
73. Asada N, Takase M, Nakamura J et al. Dysfunction of fibroblasts of extrarenal origin underlies renal fibrosis and renal anemia in mice. J. Clin. Invest. 2011; 121: 3981-90.
74. Schietke RE, Hackenbeck T, Tran M et al. Renal tubular HIF-2α expression requires VHL inactivation and causes fibrosis and cysts. PLoS ONE 2012; 7: e31034.
75. Simonson TS, Yang Y, Huff CD et al. Genetic evidence for high-altitude adaptation in Tibet. Science 2010; 329: 72-5.
76. Yi X, Liang Y, Huerta-Sanchez E et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 2010; 329: 75-8.
77. Bigham A, Bauchet M, Pinto D et al. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 2010; 6: e1001116.
78. Rosenberger C, Khamaisi M, Goldfarb M et al. Acute kidney injury in the diabetic rat: Studies in the isolated perfused and intact kidney. Am. J. Nephrol. 2008; 28: 831-9.
79. Mimura I, Nangaku M, Kanki Y et al. Dynamic change of the chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of HIF1 and KDM3A. Mol. Cell. Biol. 2012; 32: 3018-32.
80. Mimura I, Tanaka T, Wada Y, Kodama T, Nangaku M. Pathophysiological response to hypoxia: From the molecular mechanisms of malady to drug discovery: Epigenetic regulation of the hypoxic response via hypoxia-inducible factor and histone modifying enzymes. J. Pharmacol. Sci. 2011; 115: 453-8.