Renal hypoxia in kidney disease: Cause or consequence?

Acta Physiologica

Volumn 222, Issue 4, 2018, Pages

  Ow, C P C ^a   Ngo, J P ^a   Ullah, M M ^a   Hilliard, L M ^a   Evans, R G ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

acute kidney injury; chronic kidney disease; hypoxia; hypoxia inducible factors; oxygen consumption; oxygen delivery

Indexed keywords

ACUTE KIDNEY FAILURE; CHRONIC KIDNEY FAILURE; DISEASE EXACERBATION; HUMAN; HYPOXEMIA; IN VITRO STUDY; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY TUBULE DAMAGE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY; ANIMAL; CELL HYPOXIA; KIDNEY; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; CELL HYPOXIA; HUMANS; KIDNEY; KIDNEY DISEASES;

EID: 85039034769     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12999     Document Type: Review

References (205)

1. Eckardt K-U, Bernhardt WM, Weidermann A, et al. Role of hypoxia in the pathogenesis of renal disease. Kidney Int. 2005;68:S46-S51.
2. Heyman SN, Khamaisi M, Rosen S, Rosenberger C. Renal parenchymal hypoxia, hypoxia response and the progression of chronic kidney disease. Am J Nephrol. 2008;28:998-1006.
3. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol. 2006;17:17-25.
4. Fine LG, Orphanides C, Norman JT. Progressive renal disease: the chronic hypoxia hypothesis. Kidney Int Suppl. 1998;65:S74-S78.
5. Fine LG, Norman JT. Chronic hypoxia as a mechanism of progression of chronic kidney diseases: from hypothesis to novel therapeutics. Kidney Int. 2008;74:867-872.
6. Evans RG, Ince C, Joles JA, et al. Hemodynamic influences on kidney oxygenation: clinical implications of integrative physiology. Clin Exp Pharmacol Physiol. 2013;40:106-122.
7. Singh P, Ricksten S, Bragadottir G, Redfors B, Nordquist L. Renal oxygenation and haemodynamics in acute kidney injury and chronic kidney disease. Clin Exp Pharmacol Physiol. 2013;40:138-147.
8. Bellomo R, Kellum JA, Ronco C. Acute kidney injury. Lancet. 2012;380:756-766.
9. Kosieradzki M, Rowinski W. Ischemia/reperfusion injury in kidney transplantation: mechanisms and prevention. Transplant Proc. 2008;40:3279-3288.
10. O'Neal JB, Shaw AD, Billings FT 4th. Acute kidney injury following cardiac surgery: current understanding and future directions. Crit Care. 2016;20:187.
11. Secin FO. Importance and limits of ischemia in renal partial surgery: experimental and clinical research. Adv Urol. 2008;1–10:2008.
12. Munshi R, Hsu C, Himmelfarb J. Advances in understanding ischemic acute kidney injury. BMC Med. 2011;9:11-16.
13. Brezis M, Rosen S. Mechanisms of disease: hypoxia of the renal medulla - Its implications for disease. N Engl J Med. 1995;332:647-655.
14. Fry BC, Edwards A, Sgouralis I, Layton AT. Impact of renal medullary three-dimensional architecture on oxygen transport. Am J Physiol Renal Physiol. 2014;307:F263-F272.
15. Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol. 2006;17:1503-1520.
16. Tanaka T, Miyata T, Inagi R, et al. Hypoxia-induced apoptosis in cultured glomerular endothelial cells: involvement of mitochondrial pathways. Kidney Int. 2003;64:2020-2032.
17. Kim J, Seok YM, Jung K, Park KM. Reactive oxygen species/oxidative stress contributes to progression of kidney fibrosis following transient kidney injury in mice. Am J Physiol Renal Physiol. 2009;297:F461-F470.
18. Basile DP, Bonventre JV, Mehta RL, et al. Progression after AKI: understanding maladaptive repair processes to predict and identify therapeutic treatments. J Am Soc Nephrol. 2016;27:687-697.
19. Koch R. Die aetiologie der tuberculose. Berl Klin Wochenschr. 1882;19:221.
20. Evans RG, Gardiner BS, Smith DW, O'Connor PM. Methods for studying the physiology of kidney oxygenation. Clin Exp Pharmacol Physiol. 2008;35:1405-1412.
21. Hirakawa Y, Tanaka T, Nangaku M. Renal hypoxia in CKD; Pathophysiology and detecting methods. Front Physiol. 2017;8:99.
22. Clark LC, Mishrahy G, Fox RP. Chronically implanted polarographic electrodes. J Appl Physiol. 1958;13:85-91.
23. 2 at the cellular level. Br J Cancer. 1986;54:453-457.
24. 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;61:567-573.
25. Abdelkader A, Ho J, Ow CPC, et al. Renal oxygenation in acute renal ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2014;306:F1026-F1038.
26. Cobb LM, Hacker T, Nolan J. NAD(P)H nitroblue tetrazolium reductase levels in apparently normoxic tissues: a histochemical study correlating enzyme activity with binding of radiolabelled misonidazole. Br J Cancer. 1990;61:524-529.
27. Janssen HLK, Hoebers FJ, Sprong D, et al. Differentiation-associated staining with anti-pimonidazole antibodies in head and neck tumors. Radiother Oncol. 2004;70:91-97.
28. Prasad PV. Evaluation of intra-renal oxygenation by BOLD MRI. Nephron Clin Pract. 2006;103:c58-c65.
29. Ahmad R, Kuppusamy P. Theory, instrumentation, and applications of EPR Oximetry. Chem Rev. 2010;110:3212-3236.
30. Khan N, Williams BB, Hou H, Li H, Swartz HM. Repetitive tissue PO2 measurements by electron paramagnetic resonance oximtery: current status and future potential for experimental and clinical studies. Antioxid Redox Signal. 2007;9:1169-1182.
31. Nangaku M, Eckardt K-U. Hypoxia and the HIF system in kidney disease. J Mol Med. 2007;85:1325-1330.
32. Calzavacca P, Evans RG, Bailey M, Bellomo R, May CN. Variable responses of regional renal oxygenation and perfusion to vasoactive agents in awake sheep. Am J Physiol Regul Integr Comp Physiol. 2015;309:R1226-R1233.
33. Calzavacca P, Evans RG, Bailey M, Lankadeva Y, Bellomo R, May CN. Long-term measurement of renal cortical and medullary tissue oxygenation and perfusion in unanesthetized sheep. Am J Physiol Regul Integr Comp Physiol. 2015;308:R832-R839.
34. Koeners MP, Ow CPC, Russell DM, et al. Telemetry-based oxygen sensor for continuous monitoring of kidney oxygenation in conscious rats. Am J Physiol Renal Physiol. 2013;304:F1471-F1480.
35. Koeners MP, Ow CPC, Russell DM, Evans RG, Malpas SC. Prolonged and continuos measurement of kidney oxygenation in conscious rats. Methods Mol Biol. 2016;1397:93-111.
36. Calzavacca P, Evans RG, Bailey M, Bellomo R, May CN. Cortical and medullary tissue perfusion and oxygenation in experimental septic acute kidney injury. Crit Care Med. 2015;43:e431-e439.
37. Emans TW, Janssen BJ, Pinkham MI, et al. Exogenous and endogenous angiotensin-II decrease renal cortical oxygen tension in conscious rats by limiting renal blood flow. J Physiol. 2016;594:6287-6300.
38. Lankadeva YR, Kosaka J, Evans RG, Bailey SR, Bellomo R, May CN. Intrarenal and urinary oxygenation during norepinephrine resuscitation in ovine septic acute kidney injury. Kidney Int. 2016;90:100-108.
39. Igarashi P, Somlo S. Genetics and pathogenesis of polycystic kidney disease. J Am Soc Nephrol. 2002;13:2384-2398.
40. Grantham JJ, Torres V, Chapman AB, et al. Volume progression in polycystic kidney disease. N Engl J Med. 2006;354:2122-2130.
41. Wei W, Popov V, Walocha JA, Wen J, Bello Reuss E. Evidence of angiogenesis and microvascular regression in autosomal-dominant polycystic kidney disease kidneys: a corrosion cast study. Kidney Int. 2006;70:1261-1268.
42. Ow CPC, Abdelkader A, Hilliard LM, Phillips JK, Evans RG. Determinants of renal tissue hypoxia in a rat model of polycystic kidney disease. Am J Physiol Regul Integr Comp Physiol. 2014;307:R1207-R1215.
43. Bernhardt W, Wiesener M, Weidemann A, et al. Involvement of hypoxia-inducible transcription factors in polycystic kidney disease. Am J Pathol. 2007;170:830-842.
44. Ding A, Kalaignanasundaram P, Ricardo SD, et al. Chronic treatment with tempol does not significantly ameliorate renal tissue hypoxia or disease progression in a rodent model of polycystic kidney disease. Clin Exp Pharmacol Physiol. 2012;39:917-929.
45. Lorenz G, Desai J, Anders H-J. Lupus nephritis: update on mechanisms of systemic autoimmunity and kidney immunopathology. Curr Opin Nephrol Hypertens. 2014;23:211-217.
46. Yung S, Tsang RCW, Leung JKH, Chan TM. Effect of human anti-DNA antibodies on proximal renal tubular epithelial cell cytokine expression: implications on tubulointerstitial inflammation in lupus nephritis. J Am Soc Nephrol. 2005;16:3281-3294.
47. Deng W, Ren Y, Feng X, et al. Hypoxia inducible factor-1 alpha promotes mesangial cell proliferation in lupus nephritis. Am J Nephrol. 2014;40:507-515.
48. Nechemia-Arbely Y, Khamaisi M, Rosenberger C, et al. In vivo evidence suggesting reciprocal renal hypoxia-inducible factor-1 upregulation and signal transducer and activator of transcription 3 activation in response to hypoxic and non-hypoxic stimuli. Clin Exp Pharmacol Physiol. 2013;40:262-272.
49. Rosenberger C, Khamaisi M, Abassi Z, et al. Adaptation to hypoxia in the diabetic rat kidney. Kidney Int. 2008;73:34-42.
50. Franzen S, Pihl L, Khan N, Gustafsson H, Palm F. Pronounced kidney hypoxia precedes albuminuria in type I diabetic mice. Am J Physiol Renal Physiol. 2016;310:F807-F809.
51. Palm F, Cederberg J, Hansell P, Liss P, Carlsson P-O. Reactive oxygen species cause diabetes-induced decrease in renal oxygen tension. Diabetologia. 2003;46:1153-1160.
52. Manotham K, Ongvilawan B, Urusopone P, et al. Angiotensin II receptor blocker partially ameliorated intrarenal hypoxia in chronic kidney disease patients: a pre/post-study. Intern Med J. 2012;42:e33-e37.
53. Yin W, Liu F, Li X, et al. Noninvasive evaluation of renal oxygenation in diabetic nephropathy by BOLD-MRI. Eur J Radiol. 2012;81:1426-1431.
54. Wang ZJ, Kumar R, Banerjee S, Hsu C-Y. Blood oxygen-level dependent (BOLD) MR imaging of diabetic nephropathy-preliminary experience. J Magn Reson Imaging. 2011;33:655-660.
55. Pruijm M, Hofmann L, Piskunowicz M, et al. Determinants of renal tissue oxygenation as measured with BOLD-MRI in chronic kidney disease and hypertension in humans. PLoS ONE. 2014;9:e95895.
56. Hostetter TH, Olson JL, Rennke HG, Venkatachalam MA, Brenner BM. Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. Am J Physiol Renal Physiol. 1981;241:F85-F93.
57. Nath KA, Croatt AJ, Hostetter TH. Oxygen consumption and oxidant stress in surviving nephrons. Am J Physiol Renal Physiol. 1990;27:F1354-F1362.
58. Takakuta K, Fujimori A, Chikanishi T, et al. Renoprotective properties of pirfenidone in subtotally nephrectomized rats. Eur J Pharmacol. 2010;629:118-124.
59. Yang B, Vohra P, Janardhanan R, Misra KD, Misra S. Expression of profibrotic genes in a murine remnant kidney model. J Vasc Interv Radiol. 2011;22:1765-1772.
60. Chen J-F, Liu H, Ni H-F, et al. Improved mitochondrial function underlies the protective effect of pirfenidone against tubulointerstitial fibrosis in 5/6 nephrectomized rats. PLoS ONE. 2013;8:e83593.
61. Lai EY, Luo Z, Onozato ML, et al. Effects of the antioxidant drug tempol on renal oxygenation in mice with reduced renal mass. Am J Physiol Renal Physiol. 2012;303:F64-F74.
62. 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;15:1277-1288.
63. Palm F, Nangaku M, Fasching A, et al. Uremia induces abnormal oxygen consumption in tubules and aggravates chronic hypoxia of the kidney via oxidative stress. Am J Physiol Renal Physiol. 2010;299:F380-F386.
64. Priyadarshi A, Periyasamy S, Burke TJ, Britton SL, Malhortra D, Shapiro JI. Effects of reduction of renal mass on renal oxygen tension and erythropoietin production in the rat. Kidney Int. 2002;61:542-546.
65. Schoenberg SO, Bock M, Kallinowski F, Just A. Correlation of hemodynamic impact and morphologic degree of renal artery stenosis in a canine model. J Am Soc Nephrol. 2000;11:2190-2198.
66. Palm F, Connors SG, Mendoca M, Welch WJ, Wilcox CS. Angiotensin II type 2 receptors and nitric oxide sustain oxygenation in the clipped kidney of early goldblatt hypertensive rats. Hypertension. 2008;51:345-351.
67. Welch WJ, Mendoca M, Aslam S, Wilcox CS. Roles of oxidative stress and AT1 receptors in renal hemodynamics and oxygenation in the postclipped 2K, 1C kidney. Hypertension. 2003;41:692-696.
68. Rognant N, Guebre-Egziabher F, Bacchetta J, et al. Evolution of renal oxygen content measured by BOLD MRI downstream a chronic renal artery stenosis. Nephrol Dial Transplt. 2011;26:1205-1210.
69. Gloviczki ML, Glockner JF, Lerman LO, et al. Preserved oxygenation despite reduced blood flow in poststenotic kidneys in human atherosclerotic renal artery stenosis. Hypertension. 2010;55:961-966.
70. Saad A, Crane JC, Glockner J, et al. Human renovascular disease: estimating fractional tissue hypoxia to analyze blood oxygen level-dependent MR. Radiology. 2013;268:770-778.
71. Saad A, Herrmann SMS, Crane J, et al. Stent revascularization restores cortical blood flow and reverses tissue hypoxia in atherosclerotic renal artery stenosis but fails to reverses inflammatory pathways or glomerular filtration rate. Circ Cardiovasc Interv. 2013;6:428-435.
72. Gloviczki ML, Glockner J, Crane JA, et al. Bloood oxygen level-dependent magnetic resonance imaging identifies cortical hypoxia in severe renovascular disease. Hypertension. 2011;58:1066-1072.
73. Babickova J, Klinkhammer BM, Buhl EM, et al. Regardless of etiology, progressive renal disease causes ultrastructural and functional alterations of peritubular capillaries. Kidney Int. 2017;91:70-85.
74. Hoste EAJ, Schurgers M. Epidemiology of acute kidney injury: how big is the problem? Crit Care Med. 2008;36:S146-S151.
75. Coca SG, Singanamala S, Parikh CR. Chronic kidney disease after acute kidney injury: a systematic review and meta-analysis. Kidney Int. 2012;81:442-448.
76. Leung KCW, Tonelli M, James MT. Chronic kidney disease following acute kidney injury—risk and outcomes. Nat Rev Nephrol. 2013;9:77-85.
77. Lameire N, Bagga A, Cruz D, et al. Acute kidney injury: an increasing global concern. Lancet. 2013;382:170-179.
78. Legrand M, Almac E, Mik EG, et al. L-NIL prevents renal microvascular hypoxia and increase of renal oxygen consumption after ischemia-reperfusion in rats. Am J Physiol Renal Physiol. 2009;296:F1109-F1117.
79. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest. 2011;121:4210-4221.
80. Sheridan AM, Bonventre JV. Cell biology and molecular mechanisms of injury in ischemic acute renal failure. Curr Opin Nephrol Hypertens. 2000;9:427-434.
81. Sadowski EA, Djamali A, Wentland AL, et al. Blood oxygen level-dependent and perfusion magnetic resonance imaging: detecting differences in oxygen bioavailability and blood flow in transplanted kidney. Magn Reson Imaging. 2010;28:56-64.
82. Siegemund M, van Bommel J, Stegenga ME, et al. Aortic cross-clamping and reperfusion in pigs reduces microvascular oxygenation by altered systemic and regional blood flow distribution. Anesth Analg. 2010;111:345-353.
83. Conde E, Alegre L, Blanco-Sanchez I, et al. Hypoxia inducible factor 1-alpha (HIF-1 alpha) is induced during reperfusion after renal ischemia and is critical for proximal tubule cell survival. PLoS ONE. 2012;7:e33258.
84. Oostendorp M, de Vries EE, Slenter JMGM, Peutz-Koorstra CJ, Snoeijs MG, Post MJ. Ernest van Heurn LW, Backes WH: MRI of renal oxygenation and function after normothermic ischemia-reperfusion injury. NMR Biomed. 2011;24:194-200.
85. Pohlmann A, Hentschel J, Fechner M, et al. High temporal resolution parametric MRI monitoring of the initial ischemia/reperfusion phase in experimental acute kidney injury. PLoS ONE. 2013;8:e57411.
86. Lannemyr L, Bragadottir G, Krumbholz V, Redfors B, Sellgren J, Ricksten S-E. Effects of cardiopulmonary bypass on renal perfusion, filtration, and oxygenation in patients undergoing cardiac surgery. Anesthesiology. 2017;126:205-213.
87. Stafford-Smith M, Grocott HP. Renal medullary hypoxia during experimental cardiopulmonary bypass: a pilot study. Perfusion. 2005;20:53-58.
88. Darby PJ, Kim N, Hare GMT, et al. Anemia increases the risk of renal cortical and medullary hypoxia during cardiopulmonary bypass. Perfusion. 2013;28:504-511.
89. Sgouralis I, Evans RG, Gardiner BS, Smith JA, Fry B, Layton AT. Renal hemodynamics, function, and oxygenation during cardiac surgery performed on cardiopulmonary bypass: a modeling study. Physiol Rep. 2015;3:e12260.
90. Sgouralis I, Evans RG, Layton AT. Renal medullary and urinary oxygen tension during cardiopulmonary bypass in the rat. Math Med Biol. 2017;34:313-333.
91. Redfors B, Bragadottir G, Sellgren J, Sward K, Ricksten S. Acute renal failure is NOT an “acute renal success” - A clinical study on the renal oxygen supply/demand relationship in acute kidney injury. Crit Care Med. 2010;38:1695-1701.
92. Patel NN, Lin H, Toth T, et al. Reversal of anemia with allogenic RBC transfusion prevents post-cardiopulmonary bypass acute kidney injury in swine. Am J Physiol Renal Physiol. 2011;301:F605-F614.
93. Fahling M, Seeliger E, Patzak A, Persson PB. Understanding and preventing contrast-induced acute kidney injury. Nat Rev Nephrol. 2017;13:169-180.
94. Heyman SN, Brezis M, Epstein FH, Spokes K, Silva P, Rosen S. Early renal medullary hypoxic injury from radiocontrast and indomethacin. Kidney Int. 1991;40:632-642.
95. Liss P, Aukland K, Carlsson P-O, Palm F, Hansell P. Influence of iothalamate on renal medullary perfusion and oxygenation in the rat. Acta Radiol. 2005;8:823-929.
96. Liss P, Nygren A, Revsbech NP, Ulfendahl HR. Intrarenal oxygen tension measured by a modified Clark electrode at normal and low blood pressure and after injection of x-ray contrast media. Pflügers Arch. 1997;434:705-711.
97. Prasad PV, Priatna A, Spokes K, Epstein FH. Changes in intrarenal oxygenation as evaluated by BOLD MRI in a rat kidney model for radiocontrast nephropathy. J Magn Reson Imaging. 2001;13:744-747.
98. Zhang Y, Wang J, Yang X, et al. The serial effect of iodinated contrast media on renal hemodynamics and oxygenation as evaluated by ASL and BOLD MRI. Contrast Media Mol Imaging. 2012;7:418-425.
99. Hofmann L, Simon Zoula SC, Nowak A, et al. BOLD-MRI for the assessment of renal oxygenation in humans: acute effect of nephrotoxic xenobiotics. Kidney Int. 2006;70:144-150.
100. Haller C, Hizoh I. The cytotoxicity of iodinated radiocontrast agents on renal cells in vitro. Invest Radiol. 2004;39:149-154.
101. Uchino S, Kellum JA, Bellomo R, et al. Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA. 2005;294:813-818.
102. Neveu H, Kleinknecht D, Brivet F, Loirat P, Landais P. Prognostic factors in acute renal failure due to sepsis: results of a prospective multicentre study. Nephrol Dial Transplt. 1996;11:293-299.
103. Kaukonen K-M, Bailey M, Suzuki S, Pilcher D, Bellomo R. Mortality related to severe sepsis and septic shock among critically ill patients in Australia and New Zealand, 2000-2012. JAMA. 2014;311:1308-1316.
104. Schrier RW, Wang W. Acute renal failure and sepsis. N Engl J Med. 2004;351:159-169.
105. Doi K, Leelahavanichkul A, Yuen PST, Star RA. Animal models of sepsis and sepsis-induced kidney injury. J Clin Invest. 2009;119:2868-2878.
106. Dyson A, Bezemer R, Legrand M, Balestra G, Singer M, Ince C. Microvascular and interstitial oxygen tension in the renal cortex and medulla studied in a 4-H rat model of LPS-induced endotoxemia. Shock. 2011;36:83-89.
107. 2 , measured by in vivo electron paramagnetic resonance oximetry and magnetic resonance imaging. Free Radic Biol Med. 1996;21:25-34.
108. Legrand M, Bezemer R, Kandil A, Demirci C, Payen D, Ince C. The role of renal hypoperfusion in development of renal microcirculatory dysfunction in endotoxemic rats. Intensive Care Med. 2011;37:1534-1542.
109. Wang Z, Holthoff JH, Seely KA, et al. Development of oxidative stress in the peritubular capillary microenvironment mediates sepsis-induced renal microcirculatory failure and acute kidney injury. Am J Pathol. 2012;180:505-516.
110. Yasuda H, Yuen PST, Hu X, Zhou H, Star RA. Simvastatin improves sepsis-induced mortality and acute kidney injury via renal vascular effects. Kidney Int. 2006;69:1535-1542.
111. Tran M, Tam D, Bardia A, et al. PGC-1α promotes recovery after acute kidney injury during systemic inflammation in mice. J Clin Invest. 2011;121:4003-4014.
112. Bouglé A, Duranteau J. Pathophysiology of sepsis-induced acute kidney injury: the role of global renal blood flow and renal vascular resistance. Contrib Nephrol. 2011;174:89-97.
113. Neusser MA, Lindenmeyer MT, Moll AG, et al. Human nephrosclerosis triggers a hypoxia-related glomerulopathy. Am J Pathol. 2010;176:594-607.
114. Rosenberger C, Pratschke J, Rudolph B, et al. Immunohistochemical detection of hypoxia-inducible factor-1α in human renal allograft biopsies. J Am Soc Nephrol. 2007;18:343-351.
115. Belibi F, Zafar I, Ravichandran K, et al. Hypoxia-inducible factor-1α (HIF-1α) and autophagy in polycystic kidney disease (PKD). Am J Physiol Renal Physiol. 2011;300:F1235-F1243.
116. Rosenberger C, Madriota S, Jurgensen JS, et al. Expression of hypoxia-induced factor-1-alpha and -2alpha in hypoxic and ischemic rat kidneys. J Am Soc Nephrol. 2002;13:1721-1732.
117. Haase VH. Hypoxia-inducible factors in the kidney. Am J Physiol Renal Physiol. 2006;291:F271-F281.
118. Greer SN, Metcalf JL, Wang Y, Ohh M. The updated biology of hypoxia-inducible factor. EMBO J. 2012;31:2448-2460.
119. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol. 2006;70:1469-1480.
120. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3:721-732.
121. Gunaratnam L, Bonventre JV. HIF in kidney disease and development. J Am Soc Nephrol. 2009;20:1877-1887.
122. Donnelly S. Why is erythropoietin made in the kidney? The kidney functions as a ‘critmeter’ to regulate the hematocrit. Am J Kidney Dis. 2001;38:415-425.
123. Lee FS, Percy MJ. The HIF pathway and erythrocytosis. Annu Rev Pathol. 2011;6:165-192.
124. Farsijani NM, Liu Q, Kobayashi H, et al. Renal epithelium regulates erythropoiesis via HIF-dependent suppression of erythropoietin. J Clin Invest. 2016;126:1425-1437.
125. Stockmann C, Fandrey J. Hypoxia-induced erythropoietin production: a paradigm for oxygen-regulated gene expression. Clin Exp Pharmacol Physiol. 2006;33:968-979.
126. Sharples E, Patel NN, Brown P, et al. Erythropoietin protects the kidney against the injury and dysfunction caused by ischemia-reperfusion. J Am Soc Nephrol. 2004;15:2115-2124.
127. Yang B, Hosgood S, Bagul A, Waller H, Nicholson M. Erythropoietin regulates apoptosis, inflammation and tissue remodelling via caspase-3 and IL-β in isolated hemoperfused kidneys. Eur J Pharmacol. 2011;660:420-430.
128. Hu L, Yang C, Zhao T, et al. Erythropoietin ameliorates renal ischemia and reperfusion injury via inhibiting tubulointerstitial inflammation. J Surg Res. 2012;176:260-266.
129. Gobe GC, Bennett NC, West M, et al. Increased progression to kidney fibrosis after erythropoietin is used as a treatment for acute kidney injury. Am J Physiol Renal Physiol. 2014;306:F681-F692.
130. Genovese F, Manresa AA, Leeming DJ, Karsdal MA, Boor P. The extracellular matrix in the kidney: a source of novel non-invasive biomarkers of kidney fibrosis? Fibrogenesis Tissue Repair. 2014;7:4.
131. Norman JT, Orphanides C, Garcia P, Fine LG. Hypoxia-induced changes in extracellular matrix metabolism in renal cells. Exp Nephrol. 1999;7:463-469.
132. Norman JT, Clark IM, Garcia PL. Hypoxia promotes fibrogenesis in human renal fibroblasts. Kidney Int. 2000;58:2351-2366.
133. Rana MK, Srivasta J, Yang M, Chen CS, Barber DL. Hypoxia increases extracellular fibronectin abundance but not the assembly of extracellular fibronectin during epithelial cell transdifferentiation. J Cell Sci. 2015;128:1083-1089.
134. Strutz F, Zeisberg M, Ziyadeh FN, et al. Role of basic fibroblast growth factor-2 in epithelial-mesenchymal transformation. Kidney Int. 2002;61:1717-1728.
135. Tan TK, Zheng G, Hsu TT, et al. Matrix metalloproteinase-9 of tubular and macrophage origin contributes to the pathogenesis of renal fibrosis via macrophage recruitment through osteopontin cleavage. Lab Invest. 2013;93:434-449.
136. Catania JM, Chen G, Parrish AR. Role of matrix metalloproteinases in renal pathophysiologies. Am J Physiol Renal Physiol. 2007;292:F905-F911.
137. 1 -independent mechanism. Kidney Int. 1997;52:637-647.
138. Rama I, Bruene B, Torras J, et al. Hypoxia stimulus: an adaptive immune response during dendritic cell maturation. Kidney Int. 2008;73:816-825.
139. Kuhlicke J, Frick JS, Morote-Garcia JC, Rosenberger P, Eltzschig HK. Hypoxia inducible factor (HIF)-1 coordinates induction of toll-like receptors TLR2 and TLR6 during hypoxia. PLoS ONE. 2007;2:e1364.
140. Rius J, Guma M, Schachtrup C, et al. NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α. Nature. 2008;453:807-811.
141. Walmsley SR, Print C, Farahi N, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1α-dependent NF-κB activity. J Exp Med. 2005;201:105-115.
142. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol. 2005;175:6257-6263.
143. Baud L, Ardaillou R. Tumor necrosis factor in renal injury. Miner Electrolyte Metab. 1995;21:336-341.
144. Burke B, Giannoudis A, Corke KP, et al. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol. 2003;463:1233-1243.
145. Hall AM, Molitoris BA. Dynamic multiphoton microscopy: focusing light on acute kidney injury. Physiology. 2014;29:334-342.
146. Small DM, Sanchez WY, Gobe GC. Intravital multiphoton imaging of the kidney: tubular structure and metabolism. Methods Mol Biol. 2016;1397:155-172.
147. Sharfuddin AA, Sandoval RM, Berg DT, et al. Soluble thrombomodulin protects ischemic kidneys. J Am Soc Nephrol. 2009;20:524-534.
148. Hall AM, Rhodes GJ, Sandoval RM, Corridon PR, Molitoris BA. In vivo multiphoton imaging of mitochondrial structure and function during acute kidney injury. Kidney Int. 2013;83:72-83.
149. Hato T, Winfree S, Kalakeche R, et al. The macrophage mediates the renoprotective effects of endotoxin preconditioning. J Am Soc Nephrol. 2014;26:1347-1362.
150. Camirand G, Li Q, Demetris AJ, et al. Multiphoton intravital microscopy of the transplanted mouse kidney. Am J Transplant. 2011;11:2067-2074.
151. Schuh CD, Haenni D, Craigie E, et al. Long wavelength multiphoton excitation is advantageous for intravital kidney imaging. Kidney Int. 2016;89:712-719.
152. 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;15:1574-1581.
153. Nakagawa T, Lan HY, Kang D-K, Schreiner GF, Johnson RJ. Differential regulation of VEGF by TGF-β and hypoxia in rat proximal tubular cells. Am J Physiol Renal Physiol. 2004;287:F658-F664.
154. Grone H-J, Simon MC, Grone EF. Expression of vascular endothelial growth factor in renal vascular disease and renal allografts. J Pathol. 1995;177:259-267.
155. Kairaitis LK, Wang Y, Gassman M, Tay Y-C, Harris CH. HIF-1α expression follows microvascular loss in advanced murine adriamycin nephrosis. Am J Physiol Renal Physiol. 2005;288:F198-F206.
156. Kang D-H, Joly AH, Oh S-W, et al. Impaired angiogenesis in the remnant kidney model: I. potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol. 2001;12:1434-1447.
157. Kang D-H, Hughes J, Mazzali M, Schreiner GF, Johnson RJ. Impaired angiogenesis in the remnant kidney model: II. vascular endothelial growth factor administration reduces renal fibrosis and stabilizes renal function. J Am Soc Nephrol. 2001;12:1448-1457.
158. Basile DP, Friedrich JL, Spahic J, et al. Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am J Physiol Renal Physiol. 2011;300:F721-F733.
159. Hakroush S, Moeller MJ, Theilig F, et al. Effects of increased renal tubular vascular endothelial growth factor (VEGF) on fibrosis, cyst formation, and glomerular disease. Am J Pathol. 2009;175:1883-1898.
160. Bernhardt WM, Gottmann 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. 2009;106:21276-21281.
161. Bernhardt WM, Campean V, Kany S, et al. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol. 2006;17:1970-1978.
162. Wang Z, Schley G, Turkoglu 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 Transplt. 2012;27:929-936.
163. Nordquist L, Friederich-Persson M, Fasching A, et al. Activation of hypoxia-inducible factors prevents diabetic nephropathy. J Am Soc Nephrol. 2015;26:328-338.
164. Tanaka S, Tanaka T, Nangaku M. Hypoxia as a key player in the AKI-to-CKD transition. Am J Physiol Renal Physiol. 2014;307:F1187-F1195.
165. Dallatu MK, Choi M, Oyekan AO. Inhibition of prolyl hydroxylase domain-containing protein on hypertension/renal injury induced by high salt diet and nitric oxide withdrawal. J Hypertens. 2013;31:2043-2049.
166. Friederich-Persson M, Persson P, Fasching A, Hansell P, Nordquist L, Palm F. Increased kidney metabolism as a pathway to kidney tissue hypoxia and damage: effects of triiodothyronine and dinitrophenol in normoglycemic rats. Adv Exp Med Biol. 2013;789:9-14.
167. Friederich-Persson M, Thorn E, Hansell P, Nangaku M, Levin M, Palm F. Kidney hypoxia, attributable to increased oxygen consumption, induces nephropathy independently of hyperglycemia and oxidative stress. Hypertension. 2013;62:914-919.
168. Johannes T, Mik EG, Nohe B, Unertl KE, Ince C. Acute decrease in renal microvascular PO2 during acute normovolemic hemodilution. Am J Physiol Renal Physiol. 2007;292:F796-F803.
169. Cody JD, Hodson EM. Recombinant human erythropoietin versus placebo or no treatment for the anaemia of chronic kidney disease in people not requiring dialysis. Cochrane Database Syst Rev. 2016:CD003266.
170. Franzen S, Friederich-Persson M, Fasching A, Hansell P, Nangaku M, Palm F. Differences in susceptibility to develop parameters of diabetic nephropathy in four mouse strains with type 1 diabetes. Am J Physiol Renal Physiol. 2014;306:F1171-F1178.
171. Heijnen BFJ, Peutz-Koorstra CJ, Mullins JJ, Janssen BJ, Struijker-Boudier HA. Transient renin–angiotensin system stimulation in an early stage of life causes sustained hypertension in rats. J Hypertens. 2011;29:2369-2380.
172. Heijnen BFJ, Nelissen J, van Essen H, et al. Irreversible renal damage after transient renin-angiotensin system stimulation: involvement of an AT1-receptor mediated immune response. PLoS ONE. 2013;8:e57815.
173. Evans RG, Ow CPC, Bie P. The chronic hypoxia hypothesis: the search for the smoking gun goes on. Am J Physiol Renal Physiol. 2015;308:F101-F102.
174. Jankovic B, Aquino-Parsons C, Raleigh JA, et al. Comparison between pimonidazole binding, oxygen electrode measurements, and expression of endogenous hypoxia markers in cancer of the uterine cervix. Cytometry B Clin Cytom. 2006;70B:45-55.
175. Varghese AJ, Gulyas S, Mohindra JK. Hypoxia-dependent reduction of 1-(2-nitro-1-imidazolyl)-3-methoxy-2-propanol by chinese hamster ovary cells and KHT tumor cells in vitro and in vivo. Cancer Res. 1976;36:3761-3765.
176. Rosenberger C, Rosen S, Paliege A, Heyman SN. Pimonidazole adduct immunohistochemistry in the rat kidney: detection of tissue hypoxia. Methods Mol Biol. 2009;466:161-174.
177. Rosenberger C, Heyman SN, Rosen S, et al. Up-regulation of HIF in experimental acute renal failure: evidence for a protective transcriptional response to hypoxia. Kidney Int. 2005;67:531-542.
178. Efrati S, Berman S, Aharon GB, Siman-Tov Y, Averbukh Z, Weissgarten J. Application of normobaric hyperoxia therapy for amelioration of haemorrhagic shock-induced acute renal failure. Nephrol Dial Transplt. 2008;23:2213-2222.
179. Edremitlioğlu M, Kiliç D, Oter S, et al. The effect of hyperbaric oxygen treatment on the renal functions in septic rats: relation to oxidative damage. Surg Today. 2005;35:653-661.
180. Hering D, Zdrojewski Z, Krol E, et al. Tonic chemoreflex activation contributes to the elevated muscle sympathetic nerve activity in patients with chronic renal failure. J Hypertens. 2007;25:157-161.
181. van der Bel R, Caliskan M, van Hulst RA, van Lieshout JJ, Stroes ESG, Krediet CTP. Blood pressure increase during oxygen supplementation in chronic kidney disease patients is mediated by vasoconstriction independent of baroreflex function. Front Physiol. 2017;8:186.
182. Jamieson D. Oxygen toxicity and reactive oxygen metabolites in mammals. Free Radic Biol Med. 1998;7:87-108.
183. Brezis M, Agmon Y, Epstein FH. Determinants of intrarenal oxygenation I. Effects of diuretics. Am J Physiol. 1994;36:F1059-F1062.
184. Brezis M, Rosen S, Silva P, Epstein FH. Transport activity modifies thick ascending limb damage in the isolated perfused kidney. Kidney Int. 1984;25:65-72.
185. Heyman SN, Brezis M, Greenfeld Z, Rosen S. Protective role of furosemide and saline in radiocontrast-induced acute renal failure in the rat. Am J Kidney Dis. 1989;14:377-385.
186. Fouque D, Laville M. Low protein diets for chronic kidney disease in non diabetic adults. Cochrane Database Syst Rev. 2009:CD001892.
187. Heyman SN, Brezis M, Epstein FH, Spokes K, Rosen S. Effect of glycine and hypertrophy on renal outer medullary hypoxic injury in ischemia reflow and contrast nephropathy. Am J Kidney Dis. 1992;19:578-586.
188. Rui T, Feng Q, Lei M, et al. Erythropoietin prevents the acute myocardial inflammatory response induced by ischemia/reperfusion via induction of AP-1. Cardiovasc Res. 2005;65:719-727.
189. Shanley PF, Rosen MD, Brezis M, Silva P, Epstein FH, Rosen S. Topography of focal proximal tubular necrosis after ischemia with reflow in the rat kidney. Am J Pathol. 1986;122:462-468.
190. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. 2003;9:677-684.
191. Reinders MEJ, Sho M, Izawa A, et al. Proinflammatory functions of vascular endothelial growth factor in alloimmunity. J Clin Invest. 2003;112:1655-1665.
192. Basu RK, Hubchak S, Hayashida T, Runyan CE, Schumacker PT, Schnaper HW. Interdependence of HIF-1α and TGF-β/Smad3 signaling in normoxic and hypoxic renal epithelial cell collagen expression. Am J Physiol Renal Physiol. 2011;300:F898-F905.
193. Grimshaw MJ. Endothelins and hypoxia-inducible factor in cancer. Endocr Relat Cancer. 2007;14:233-244.
194. Morishita Y, Ookawara S, Hirahara I, Muto S, Nagata D. HIF-1α mediates hypoxia-induced epithelial–mesenchymal transition in peritoneal mesothelial cells. Ren Fail. 2016;38:282-289.
195. Jing S-W, Wang Y-D, Kuroda M, et al. HIF-1α contributes to hypoxia-induced invasion and metastasis of esophageal carcinoma via inhibiting E-cadherin and promoting MMP-2 expression. Acta Med Okayama. 2012;66:399-407.
196. Olson N, van der Vliet A. Interactions between nitric oxide and hypoxia-inducible factor signaling pathways in inflammatory disease. Nitric Oxide. 2011;25:125-137.
197. Wilkinson-Berka JL, Wraight C, Werther G. The role of growth hormone, insulin-like growth factor and somatostatin in diabetic retinopathy. Curr Med Chem. 2006;13:3307-3317.
198. Pricci F, Pugliese G, Romano G, et al. Insulin-like growth factors I and II stimulate extracellular matrix production in human glomerular mesangial cells. Comparison with transforming growth factor-β. Endocrinology. 1996;137:879-885.
199. Feld SM, Hirschberg R, Artishevsky A, Nast C, Adler SG. Insulin-like growth factor I induces mesangial proliferation and increases mRNA and secretion of collagen. Kidney Int. 1995;49:45-51.
200. Lee SC, Han SH, Li JJ, et al. Induction of heme oxygenase-1 protects against podocyte apoptosis under diabetic conditions. Kidney Int. 2009;76:838-848.
201. Bolisetty S, Traylor AM, Kim J, et al. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol. 2010;21:1702-1712.
202. Lee PJ, Alam J, Wiegand GW, Choi AK. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci. 1996;93:10393-10398.
203. Lum JJ, Bui T, Gruber M, et al. The transcription factor HIF-1α plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev. 2013;21:1037-1049.
204. Linden KC, DeHaan CL, Zhang Y, et al. Renal expression and localization of the facilitating glucose transporters GLUT1 and GLUT12 in animal models of hypertension and diabetic nephropathy. Am J Physiol Renal Physiol. 2006;290:F205-F213.
205. Patel NN, Toth T, Jones C, et al. Prevention of post-cardiopulmonary bypass acute kidney injury by endothelin A receptor blockade. Crit Care Med. 2011;39:793-802.