Heme Oxygenase 1 as a Therapeutic Target in Acute Kidney Injury

American Journal of Kidney Diseases

Volumn 69, Issue 4, 2017, Pages 531-545

  Bolisetty, Subhashini ^a,b,c   Zarjou, Abolfazl ^a,b   Agarwal, Anupam ^a,b,c,d  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Acute kidney injury (AKI); autophagic response; biomarker; cell cycle regulation; cytoprotection; heme oxygenase 1 (HO 1); HMOX1; inflammation; oxidative stress; pathophysiology; renal failure; review; translational research

Indexed keywords

HEME OXYGENASE 1; IRON; MICRORNA; HMOX1 PROTEIN, HUMAN;

ACUTE KIDNEY FAILURE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL MIGRATION; CELL PROTECTION; DNA POLYMORPHISM; ENDOTHELIUM CELL; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; ACUTE KIDNEY INJURY; ADULT; BLOOD; CASE REPORT; CELL CYCLE CHECKPOINT; COMPLICATION; ENZYME INDUCTION; LEG INJURY; MALE; OCCUPATIONAL ACCIDENT; PHYSIOLOGY; RHABDOMYOLYSIS; TRANSLATIONAL RESEARCH;

ACCIDENTS, OCCUPATIONAL; ACUTE KIDNEY INJURY; ADULT; AUTOPHAGY; CELL CYCLE CHECKPOINTS; ENZYME INDUCTION; HEME OXYGENASE-1; HUMANS; INFLAMMATION; LEG INJURIES; MALE; OXIDATIVE STRESS; RHABDOMYOLYSIS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 85010857604     PISSN: 02726386     EISSN: 15236838     Source Type: Journal    
DOI: 10.1053/j.ajkd.2016.10.037     Document Type: Article

References (145)

1. 1 Zarjou, A., Sanders, P.W., Mehta, R.L., Agarwal, A., Enabling innovative translational research in acute kidney injury. Clin Transl Sci 5:1 (2012), 93–101.
2. 2 Kaushal, G.P., Shah, S.V., Challenges and advances in the treatment of AKI. J Am Soc Nephrol 25:5 (2014), 877–883.
3. 3 Agarwal, A., Dong, Z., Harris, R., et al. Cellular and molecular mechanisms of AKI. J Am Soc Nephrol 27:5 (2016), 1288–1299.
4. 4 Agarwal, A., Nick, H.S., Renal response to tissue injury: lessons from heme oxygenase-1 gene ablation and expression. J Am Soc Nephrol 11:5 (2000), 965–973.
5. 5 Ryter, S.W., Choi, A.M., Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation. Transl Res 167:1 (2016), 7–34.
6. 6 Gozzelino, R., Jeney, V., Soares, M.P., Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 50 (2010), 323–354.
7. 7 Nath, K.A., Balla, G., Vercellotti, G.M., et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 90:1 (1992), 267–270.
8. 8 Agarwal, A., Balla, J., Alam, J., Croatt, A.J., Nath, K.A., Induction of heme oxygenase in toxic renal injury: a protective role in cisplatin nephrotoxicity in the rat. Kidney Int 48:4 (1995), 1298–1307.
9. 9 Shiraishi, F., Curtis, L.M., Truong, L., et al. Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis. Am J Physiol Renal Physiol 278:5 (2000), F726–F736.
10. -/- mice. Am J Pathol 170:6 (2007), 1820–1830.
11. 11 Blydt-Hansen, T.D., Katori, M., Lassman, C., et al. Gene transfer-induced local heme oxygenase-1 overexpression protects rat kidney transplants from ischemia/reperfusion injury. J Am Soc Nephrol 14:3 (2003), 745–754.
12. 12 Shimizu, H., Takahashi, T., Suzuki, T., et al. Protective effect of heme oxygenase induction in ischemic acute renal failure. Crit Care Med 28:3 (2000), 809–817.
13. 13 Leaf, D.E., Body, S.C., Muehlschlegel, J.D., et al. Length polymorphisms in heme oxygenase-1 and AKI after cardiac surgery. J Am Soc Nephrol 27:11 (2016), 3291–3297.
14. 14 Bywaters, E.G., Beall, D., Crush injuries with impairment of renal function. Br Med J 1:4185 (1941), 427–432.
15. 15 Courtney, A.E., Maxwell, A.P., Heme oxygenase 1: does it have a role in renal cytoprotection?. Am J Kidney Dis 51:4 (2008), 678–690.
16. 16 Nath, K.A., Heme oxygenase-1 and acute kidney injury. Curr Opin Nephrol Hypertens 23:1 (2014), 17–24.
17. 17 Nath, K.A., Heme oxygenase-1: a provenance for cytoprotective pathways in the kidney and other tissues. Kidney Int 70:3 (2006), 432–443.
18. 18 Jarmi, T., Agarwal, A., Heme oxygenase and renal disease. Curr Hypertens Rep 11:1 (2009), 56–62.
19. 19 Lever, J.M., Boddu, R., George, J.F., Agarwal, A., Heme oxygenase-1 in kidney health and disease. Antioxid Redox Signal 25:3 (2016), 165–183.
20. 20 Rabb, H., Griffin, M.D., McKay, D.B., et al. Inflammation in AKI: current understanding, key questions, and knowledge gaps. J Am Soc Nephrol 27:2 (2016), 371–379.
21. 21 Kinsey, G.R., Sharma, R., Okusa, M.D., Regulatory T cells in AKI. J Am Soc Nephrol 24:11 (2013), 1720–1726.
22. 22 Jang, H.R., Rabb, H., Immune cells in experimental acute kidney injury. Nat Rev Nephrol 11:2 (2015), 88–101.
23. 23 Akcay, A., Nguyen, Q., Edelstein, C.L., Mediators of inflammation in acute kidney injury. Mediators Inflamm, 2009, 2009, 137072.
24. 24 Kinsey, G.R., Li, L., Okusa, M.D., Inflammation in acute kidney injury. Nephron Exp Nephrol 109:4 (2008), e102–e107.
25. 25 Kovtunovych, G., Eckhaus, M.A., Ghosh, M.C., Ollivierre-Wilson, H., Rouault, T.A., Dysfunction of the heme recycling system in heme oxygenase 1-deficient mice: effects on macrophage viability and tissue iron distribution. Blood 116:26 (2010), 6054–6062.
26. 26 Hull, T.D., Agarwal, A., George, J.F., The mononuclear phagocyte system in homeostasis and disease: a role for heme oxygenase-1. Antioxid Redox Signal 20:11 (2014), 1770–1788.
27. 27 Kovtunovych, G., Ghosh, M.C., Ollivierre, W., et al. Wild-type macrophages reverse disease in heme oxygenase 1-deficient mice. Blood 124:9 (2014), 1522–1530.
28. 28 Ferenbach, D.A., Ramdas, V., Spencer, N., et al. Macrophages expressing heme oxygenase-1 improve renal function in ischemia/reperfusion injury. Mol Ther 18:9 (2010), 1706–1713.
29. 29 Ohta, K., Yachie, A., Fujimoto, K., et al. Tubular injury as a cardinal pathologic feature in human heme oxygenase-1 deficiency. Am J Kidney Dis 35:5 (2000), 863–870.
30. 30 Poss, K.D., Tonegawa, S., Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 94:20 (1997), 10919–10924.
31. 31 Kapturczak, M.H., Wasserfall, C., Brusko, T., et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 165:3 (2004), 1045–1053.
32. 32 Pittock, S.T., Norby, S.M., Grande, J.P., et al. MCP-1 is up-regulated in unstressed and stressed HO-1 knockout mice: pathophysiologic correlates. Kidney Int 68:2 (2005), 611–622.
33. 33 Hull, T.D., Kamal, A.I., Boddu, R., et al. Heme oxygenase-1 regulates myeloid cell trafficking in AKI. J Am Soc Nephrol 26:9 (2015), 2139–2151.
34. 34 Bolisetty, S., Zarjou, A., Hull, T.D., et al. Macrophage and epithelial cell H-ferritin expression regulates renal inflammation. Kidney Int 88:1 (2015), 95–108.
35. 35 Bolisetty, S., Traylor, A.M., Kim, J., et al. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 21:10 (2010), 1702–1712.
36. 36 Kim, J., Zarjou, A., Traylor, A.M., et al. In vivo regulation of the heme oxygenase-1 gene in humanized transgenic mice. Kidney Int 82:3 (2012), 278–291.
37. 37 Bolisetty, S., Traylor, A., Joseph, R., Zarjou, A., Agarwal, A., Proximal tubule-targeted heme oxygenase-1 in cisplatin-induced acute kidney injury. Am J Physiol Renal Physiol 310:5 (2016), F385–F394.
38. 38 Bolisetty, S., Traylor, A., Zarjou, A., et al. Mitochondria-targeted heme oxygenase-1 decreases oxidative stress in renal epithelial cells. Am J Physiol Renal Physiol 305:3 (2013), F255–F264.
39. 39 Dennery, P.A., McDonagh, A.F., Spitz, D.R., Rodgers, P.A., Stevenson, D.K., Hyperbilirubinemia results in reduced oxidative injury in neonatal Gunn rats exposed to hyperoxia. Free Radic Biol Med 19:4 (1995), 395–404.
40. 40 Leung, N., Croatt, A.J., Haggard, J.J., Grande, J.P., Nath, K.A., Acute cholestatic liver disease protects against glycerol-induced acute renal failure in the rat. Kidney Int 60:3 (2001), 1047–1057.
41. 41 Chen, S., Kapturczak, M.H., Wasserfall, C., et al. Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway. Proc Natl Acad Sci U S A 102:20 (2005), 7251–7256.
42. 42 Lee, T.S., Chau, L.Y., Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 mice. Nat Med 8:3 (2002), 240–246.
43. 43 Tracz, M.J., Juncos, J.P., Croatt, A.J., et al. Deficiency of heme oxygenase-1 impairs renal hemodynamics and exaggerates systemic inflammatory responses to renal ischemia. Kidney Int 72:9 (2007), 1073–1080.
44. 44 Chen, X., Wei, S.Y., Li, J.S., et al. Overexpression of heme oxygenase-1 prevents renal interstitial inflammation and fibrosis induced by unilateral ureter obstruction. PLoS One, 11(1), 2016, e0147084.
45. 45 Park, D.J., Agarwal, A., George, J.F., Heme oxygenase-1 expression in murine dendritic cell subpopulations: effect on CD8+ dendritic cell differentiation in vivo. Am J Pathol 176:6 (2010), 2831–2839.
46. 46 George, J.F., Braun, A., Brusko, T.M., et al. Suppression by CD4+CD25+ regulatory T cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. Am J Pathol 173:1 (2008), 154–160.
47. 47 Kotsch, K., Martins, P.N., Klemz, R., et al. Heme oxygenase-1 ameliorates ischemia/reperfusion injury by targeting dendritic cell maturation and migration. Antioxid Redox Signal 9:12 (2007), 2049–2063.
48. 48 Martins, P.N., Reutzel-Selke, A., Jurisch, A., et al. Induction of carbon monoxide in donor animals prior to organ procurement reduces graft immunogenicity and inhibits chronic allograft dysfunction. Transplantation 82:7 (2006), 938–944.
49. 49 Brusko, T.M., Wasserfall, C.H., Agarwal, A., Kapturczak, M.H., Atkinson, M.A., An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells. J Immunol 174:9 (2005), 5181–5186.
50. 50 Song, R., Mahidhara, R.S., Zhou, Z., et al. Carbon monoxide inhibits T lymphocyte proliferation via caspase-dependent pathway. J Immunol 172:2 (2004), 1220–1226.
51. 51 Gueler, F., Park, J.K., Rong, S., et al. Statins attenuate ischemia-reperfusion injury by inducing heme oxygenase-1 in infiltrating macrophages. Am J Pathol 170:4 (2007), 1192–1199.
52. 52 Jung, S.H., Kim, H.J., Oh, G.S., et al. Capsaicin ameliorates cisplatin-induced renal injury through induction of heme oxygenase-1. Mol Cells 37:3 (2014), 234–240.
53. 53 Cheng, C.F., Lian, W.S., Chen, S.H., et al. Protective effects of adiponectin against renal ischemia-reperfusion injury via prostacyclin-PPARalpha-heme oxygenase-1 signaling pathway. J Cell Physiol 227:1 (2012), 239–249.
54. 54 Kamimoto, M., Mizuno, S., Matsumoto, K., Nakamura, T., Hepatocyte growth factor prevents multiple organ injuries in endotoxemic mice through a heme oxygenase-1-dependent mechanism. Biochem Biophys Res Commun 380:2 (2009), 333–337.
55. 55 Li, Y., Xie, K., Chen, H., Wang, G., Yu, Y., Hydrogen gas inhibits high-mobility group box 1 release in septic mice by upregulation of heme oxygenase 1. J Surg Res 196:1 (2015), 136–148.
56. 56 Ferenbach, D.A., Kluth, D.C., Hughes, J., Hemeoxygenase-1 and renal ischaemia-reperfusion injury. Nephron Exp Nephrol 115:3 (2010), e33–e37.
57. 57 Wu, Q.Q., Wang, Y., Senitko, M., et al. Bardoxolone methyl (BARD) ameliorates ischemic AKI and increases expression of protective genes Nrf2, PPARgamma, and HO-1. Am J Physiol Renal Physiol 300:5 (2011), F1180–F1192.
58. 58 Wu, J., Liu, X., Fan, J., et al. Bardoxolone methyl (BARD) ameliorates aristolochic acid (AA)-induced acute kidney injury through Nrf2 pathway. Toxicology 318 (2014), 22–31.
59. 59 Gao, Z., Han, Y., Hu, Y., et al. Targeting HO-1 by epigallocatechin-3-gallate reduces contrast-induced renal injury via anti-oxidative stress and anti-inflammation pathways. PLoS One, 11(2), 2016, e0149032.
60. 60 Wang, Y., Wang, B., Du, F., et al. Epigallocatechin-3-gallate attenuates oxidative stress and inflammation in obstructive nephropathy via NF-kappaB and Nrf2/HO-1 signalling pathway regulation. Basic Clin Pharmacol Toxicol 117:3 (2015), 164–172.
61. 61 Gonzalez-Michaca, L., Farrugia, G., Croatt, A.J., Alam, J., Nath, K.A., Heme: a determinant of life and death in renal tubular epithelial cells. Am J Physiol Renal Physiol 286:2 (2004), F370–F377.
62. 62 Iwata, M., Zager, R.A., Myoglobin inhibits proliferation of cultured human proximal tubular (HK-2) cells. Kidney Int 50:3 (1996), 796–804.
63. 63 Wang, L., Zhang, Y., Yuan, L., Liu, C., Fu, L., Mei, C., Cyclin-dependent kinase inhibitor p18INK4c is involved in protective roles of heme oxygenase-1 in cisplatin-induced acute kidney injury. Int J Mol Med 34:3 (2014), 911–917.
64. 64 Banerjee, P., Basu, A., Wegiel, B., et al. Heme oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis- and autophagy-regulating molecules. J Biol Chem 287:38 (2012), 32113–32123.
65. 65 Demirogullari, B., Ekingen, G., Guz, G., et al. A comparative study of the effects of hemin and bilirubin on bilateral renal ischemia reperfusion injury. Nephron Exp Nephrol 103:1 (2006), e1–e5.
66. 66 Katavetin, P., Inagi, R., Miyata, T., et al. Erythropoietin induces heme oxygenase-1 expression and attenuates oxidative stress. Biochem Biophys Res Commun 359:4 (2007), 928–934.
67. 67 Mori, K., Lee, H.T., Rapoport, D., et al. Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest 115:3 (2005), 610–621.
68. 68 Adin, C.A., Croker, B.P., Agarwal, A., Protective effects of exogenous bilirubin on ischemia-reperfusion injury in the isolated, perfused rat kidney. Am J Physiol Renal Physiol 288:4 (2005), F778–F784.
69. 69 Goebel, U., Siepe, M., Schwer, C.I., et al. Inhaled carbon monoxide prevents acute kidney injury in pigs after cardiopulmonary bypass by inducing a heat shock response. Anesth Analg 111:1 (2010), 29–37.
70. 70 Wang, P., Huang, J., Li, Y., et al. Exogenous carbon monoxide decreases sepsis-induced acute kidney injury and inhibits NLRP3 inflammasome activation in rats. Int J Mol Sci 16:9 (2015), 20595–20608.
71. 71 Lanone, S., Bloc, S., Foresti, R., et al. Bilirubin decreases nos2 expression via inhibition of NAD(P)H oxidase: implications for protection against endotoxic shock in rats. FASEB J 19:13 (2005), 1890–1892.
72. 72 Seta, F., Bellner, L., Rezzani, R., et al. Heme oxygenase-2 is a critical determinant for execution of an acute inflammatory and reparative response. Am J Pathol 169:5 (2006), 1612–1623.
73. 73 Bellner, L., Martinelli, L., Halilovic, A., et al. Heme oxygenase-2 deletion causes endothelial cell activation marked by oxidative stress, inflammation, and angiogenesis. J Pharmacol Exp Ther 331:3 (2009), 925–932.
74. 74 Bellner, L., Marrazzo, G., van Rooijen, N., Dunn, M.W., Abraham, N.G., Schwartzman, M.L., Heme oxygenase-2 deletion impairs macrophage function: implication in wound healing. FASEB J 29:1 (2015), 105–115.
75. 75 Bellner, L., Wolstein, J., Patil, K.A., Dunn, M.W., Laniado-Schwartzman, M., Biliverdin rescues the HO-2 null mouse phenotype of unresolved chronic inflammation following corneal epithelial injury. Invest Ophthalmol Vis Sci 52:6 (2011), 3246–3253.
76. 76 Megyesi, J., Safirstein, R.L., Price, P.M., Induction of p21WAF1/CIP1/SDI1 in kidney tubule cells affects the course of cisplatin-induced acute renal failure. J Clin Invest 101:4 (1998), 777–782.
77. 77 Megyesi, J., Andrade, L., Vieira, J.M. Jr., Safirstein, R.L., Price, P.M., Positive effect of the induction of p21WAF1/CIP1 on the course of ischemic acute renal failure. Kidney Int 60:6 (2001), 2164–2172.
78. 78 Inguaggiato, P., Gonzalez-Michaca, L., Croatt, A.J., Haggard, J.J., Alam, J., Nath, K.A., Cellular overexpression of heme oxygenase-1 up-regulates p21 and confers resistance to apoptosis. Kidney Int 60:6 (2001), 2181–2191.
79. 79 Nath, K.A., Haggard, J.J., Croatt, A.J., Grande, J.P., Poss, K.D., Alam, J., The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am J Pathol 156:5 (2000), 1527–1535.
80. 80 Kumar, D., Bhaskaran, M., Alagappan, L., et al. Heme oxygenase-1 modulates mesangial cell proliferation by p21 Waf1 upregulation. Ren Fail 32:2 (2010), 254–258.
81. 81 Kim, S.Y., Kang, H.T., Choi, H.R., Park, S.C., Biliverdin reductase A in the prevention of cellular senescence against oxidative stress. Exp Mol Med 43:1 (2011), 15–23.
82. 82 Zhang, Y., Yuan, L., Fu, L., Liu, C., Liu, D., Mei, C., Overexpression of p18INK(4)C in LLC-PK1 cells increases resistance to cisplatin-induced apoptosis. Pediatr Nephrol 26:8 (2011), 1291–1301.
83. 83 Kashani, K., Al-Khafaji, A., Ardiles, T., et al. Discovery and validation of cell cycle arrest biomarkers in human acute kidney injury. Crit Care, 17(1), 2013, R25.
84. 84 Yang, L., Besschetnova, T.Y., Brooks, C.R., Shah, J.V., Bonventre, J.V., Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 16:5 (2010), 535–543 531p following 143.
85. 85 Levine, B., Klionsky, D.J., Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:4 (2004), 463–477.
86. 86 Mizushima, N., Autophagy: process and function. Genes Dev 21:22 (2007), 2861–2873.
87. 87 He, L., Livingston, M.J., Dong, Z., Autophagy in acute kidney injury and repair. Nephron Clin Pract 127:1-4 (2014), 56–60.
88. 88 Kaushal, G.P., Shah, S.V., Autophagy in acute kidney injury. Kidney Int 89:4 (2016), 779–791.
89. 89 Suzuki, C., Isaka, Y., Takabatake, Y., et al. Participation of autophagy in renal ischemia/reperfusion injury. Biochem Biophys Res Commun 368:1 (2008), 100–106.
90. 90 Kim, H.P., Wang, X., Chen, Z.H., et al. Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy 4:7 (2008), 887–895.
91. 91 Nath, K.A., Balla, J., Croatt, A.J., Vercellotti, G.M., Heme protein-mediated renal injury: a protective role for 21-aminosteroids in vitro and in vivo. Kidney Int 47:2 (1995), 592–602.
92. 92 Dhar, G.J., Bossenmaier, I., Cardinal, R., Petryka, Z.J., Watson, C.J., Transitory renal failure following rapid administration of a relatively large amount of hematin in a patient with acute intermittent porphyria in clinical remission. Acta Med Scand 203:5 (1978), 437–443.
93. 93 Tracz, M.J., Alam, J., Nath, K.A., Physiology and pathophysiology of heme: implications for kidney disease. J Am Soc Nephrol 18:2 (2007), 414–420.
94. 94 Yachie, A., Niida, Y., Wada, T., et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 103:1 (1999), 129–135.
95. 95 Stocker, R., Antioxidant activities of bile pigments. Antioxid Redox Signal 6:5 (2004), 841–849.
96. 96 Kaur, H., Hughes, M.N., Green, C.J., Naughton, P., Foresti, R., Motterlini, R., Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 543:1-3 (2003), 113–119.
97. 97 Baranano, D.E., Rao, M., Ferris, C.D., Snyder, S.H., Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci U S A 99:25 (2002), 16093–16098.
98. 98 Matsumoto, H., Ishikawa, K., Itabe, H., Maruyama, Y., Carbon monoxide and bilirubin from heme oxygenase-1 suppresses reactive oxygen species generation and plasminogen activator inhibitor-1 induction. Mol Cell Biochem 291:1-2 (2006), 21–28.
99. 99 Kirkby, K.A., Adin, C.A., Products of heme oxygenase and their potential therapeutic applications. Am J Physiol Renal Physiol 290:3 (2006), F563–F571.
100. 100 Kawashima, A., Oda, Y., Yachie, A., Koizumi, S., Nakanishi, I., Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol 33:1 (2002), 125–130.
101. 101 Radhakrishnan, N., Yadav, S.P., Sachdeva, A., et al. Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia. J Pediatr Hematol Oncol 33:1 (2011), 74–78.
102. 102 Tzima, S., Victoratos, P., Kranidioti, K., Alexiou, M., Kollias, G., Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. J Exp Med 206:5 (2009), 1167–1179.
103. 103 Sikorski, E.M., Hock, T., Hill-Kapturczak, N., Agarwal, A., The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol 286:3 (2004), F425–F441.
104. 104 Lee, R.C., Feinbaum, R.L., Ambros, V., The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:5 (1993), 843–854.
105. 105 Wightman, B., Ha, I., Ruvkun, G., Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:5 (1993), 855–862.
106. 106 Erson, A.E., Petty, E.M., MicroRNAs in development and disease. Clin Genet 74:4 (2008), 296–306.
107. 107 Gomez, I.G., Nakagawa, N., Duffield, J.S., MicroRNAs as novel therapeutic targets to treat kidney injury and fibrosis. Am J Physiol Renal Physiol 310:10 (2016), F931–F944.
108. 108 Bhatt, K., Kato, M., Natarajan, R., Mini-review: emerging roles of microRNAs in the pathophysiology of renal diseases. Am J Physiol Renal Physiol 310:2 (2016), F109–F118.
109. 109 Yang, H., Wang, Q., Li, S., MicroRNA-218 promotes high glucose-induced apoptosis in podocytes by targeting heme oxygenase-1. Biochem Biophys Res Commun 471:4 (2016), 582–588.
110. 110 Stachurska, A., Ciesla, M., Kozakowska, M., et al. Cross-talk between microRNAs, nuclear factor E2-related factor 2, and heme oxygenase-1 in ochratoxin A-induced toxic effects in renal proximal tubular epithelial cells. Mol Nutr Food Res 57:3 (2013), 504–515.
111. 111 Schrottmaier, W.C., Oskolkova, O.V., Schabbauer, G., Afonyushkin, T., MicroRNA miR-320a modulates induction of HO-1, GCLM and OKL38 by oxidized phospholipids in endothelial cells. Atherosclerosis 235:1 (2014), 1–8.
112. 112 Pulkkinen, K.H., Yla-Herttuala, S., Levonen, A.L., Heme oxygenase 1 is induced by miR-155 via reduced BACH1 translation in endothelial cells. Free Radic Biol Med 51:11 (2011), 2124–2131.
113. 113 Beckman, J.D., Chen, C., Nguyen, J., et al. Regulation of heme oxygenase-1 protein expression by miR-377 in combination with miR-217. J Biol Chem 286:5 (2011), 3194–3202.
114. 114 Kozakowska, M., Szade, K., Dulak, J., Jozkowicz, A., Role of heme oxygenase-1 in postnatal differentiation of stem cells: a possible cross-talk with microRNAs. Antioxid Redox Signal 20:11 (2014), 1827–1850.
115. 115 Go, H., La, P., Namba, F., et al. MiR-196a regulates heme oxygenase-1 by silencing Bach1 in the neonatal mouse lung. Am J Physiol Lung Cell Mol Physiol 311:2 (2016), L400–411.
116. 116 Lin, S.H., Song, W., Cressatti, M., Zukor, H., Wang, E., Schipper, H.M., Heme oxygenase-1 modulates microRNA expression in cultured astroglia: implications for chronic brain disorders. Glia 63:7 (2015), 1270–1284.
117. 117 Kozakowska, M., Ciesla, M., Stefanska, A., et al. Heme oxygenase-1 inhibits myoblast differentiation by targeting myomirs. Antioxid Redox Signal 16:2 (2012), 113–127.
118. 118 Exner, M., Minar, E., Wagner, O., Schillinger, M., The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic Biol Med 37:8 (2004), 1097–1104.
119. 119 Daenen, K.E., Martens, P., Bammens, B., Association of HO-1 (GT)n promoter polymorphism and cardiovascular disease: a reanalysis of the literature. Can J Cardiol 32:2 (2016), 160–168.
120. 120 Qiao, H., Sai, X., Gai, L., et al. Association between heme oxygenase 1 gene promoter polymorphisms and susceptibility to coronary artery disease: a HuGE review and meta-analysis. Am J Epidemiol 179:9 (2014), 1039–1048.
121. 121 Bao, W., Song, F., Li, X., et al. Association between heme oxygenase-1 gene promoter polymorphisms and type 2 diabetes mellitus: a HuGE review and meta-analysis. Am J Epidemiol 172:6 (2010), 631–636.
122. 122 Hirai, H., Kubo, H., Yamaya, M., et al. Microsatellite polymorphism in heme oxygenase-1 gene promoter is associated with susceptibility to oxidant-induced apoptosis in lymphoblastoid cell lines. Blood 102:5 (2003), 1619–1621.
123. 123 Taha, H., Skrzypek, K., Guevara, I., et al. Role of heme oxygenase-1 in human endothelial cells: lesson from the promoter allelic variants. Arterioscler Thromb Vasc Biol 30:8 (2010), 1634–1641.
124. 124 Chen, Y.H., Lin, S.J., Lin, M.W., et al. Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients. Hum Genet 111:1 (2002), 1–8.
125. 125 Chin, H.J., Cho, H.J., Lee, T.W., et al. The heme oxygenase-1 genotype is a risk factor to renal impairment of IgA nephropathy at diagnosis, which is a strong predictor of mortality. J Korean Med Sci 24:1 (2009), S30–S37.
126. 126 Baan, C., Peeters, A., Lemos, F., et al. Fundamental role for HO-1 in the self-protection of renal allografts. Am J Transplant 4:5 (2004), 811–818.
127. 127 Exner, M., Bohmig, G.A., Schillinger, M., et al. Donor heme oxygenase-1 genotype is associated with renal allograft function. Transplantation 77:4 (2004), 538–542.
128. 128 Lin, C.C., Yang, W.C., Lin, S.J., et al. Length polymorphism in heme oxygenase-1 is associated with arteriovenous fistula patency in hemodialysis patients. Kidney Int 69:1 (2006), 165–172.
129. 129 Lin, C.C., Chung, M.Y., Yang, W.C., Lin, S.J., Lee, P.C., Length polymorphisms of heme oxygenase-1 determine the effect of far-infrared therapy on the function of arteriovenous fistula in hemodialysis patients: a novel physicogenomic study. Nephrol Dial Transplant 28:5 (2013), 1284–1293.
130. 130 Chen, Y.H., Kuo, K.L., Hung, S.C., Hsu, C.C., Chen, Y.H., Tarng, D.C., Length polymorphism in heme oxygenase-1 and risk of CKD among patients with coronary artery disease. J Am Soc Nephrol 25:11 (2014), 2669–2677.
131. 131 Holweg, C.T., Balk, A.H., Uitterlinden, A.G., et al. Functional heme oxygenase-1 promoter polymorphism in relation to heart failure and cardiac transplantation. J Heart Lung Transplant 24:4 (2005), 493–497.
132. 132 Courtney, A.E., McNamee, P.T., Heggarty, S., Middleton, D., Maxwell, A.P., Association of functional haem oxygenase-1 gene promoter polymorphism with polycystic kidney disease and IgA nephropathy. Nephrol Dial Transplant 23:2 (2008), 608–611.
133. 133 Courtney, A.E., McNamee, P.T., Middleton, D., Heggarty, S., Patterson, C.C., Maxwell, A.P., Association of functional heme oxygenase-1 gene promoter polymorphism with renal transplantation outcomes. Am J Transplant 7:4 (2007), 908–913.
134. 134 Martines, A.M., Masereeuw, R., Tjalsma, H., Hoenderop, J.G., Wetzels, J.F., Swinkels, D.W., Iron metabolism in the pathogenesis of iron-induced kidney injury. Nat Rev Nephrol 9:7 (2013), 385–398.
135. 135 Walker, V.J., Agarwal, A., Targeting iron homeostasis in acute kidney injury. Semin Nephrol 36:1 (2016), 62–70.
136. 136 Leaf, D.E., Rajapurkar, M., Lele, S.S., Mukhopadhyay, B., Waikar, S.S., Plasma catalytic iron, AKI, and death among critically ill patients. Clin J Am Soc Nephrol 9:11 (2014), 1849–1856.
137. 137 Leaf, D.E., Rajapurkar, M., Lele, S.S., et al. Increased plasma catalytic iron in patients may mediate acute kidney injury and death following cardiac surgery. Kidney Int 87:5 (2015), 1046–1054.
138. 138 Scindia, Y., Dey, P., Thirunagari, A., et al. Hepcidin mitigates renal ischemia-reperfusion injury by modulating systemic iron homeostasis. J Am Soc Nephrol 26:11 (2015), 2800–2814.
139. 139 Zarjou, A., Bolisetty, S., Joseph, R., et al. Proximal tubule H-ferritin mediates iron trafficking in acute kidney injury. J Clin Invest 123:10 (2013), 4423–4434.
140. 140 Gunnerson, K.J., Shaw, A.D., Chawla, L.S., et al. TIMP2*IGFBP7 biomarker panel accurately predicts acute kidney injury in high-risk surgical patients. J Trauma Acute Care Surg 80:2 (2016), 243–249.
141. 141 Gocze, I., Koch, M., Renner, P., et al. Urinary biomarkers TIMP-2 and IGFBP7 early predict acute kidney injury after major surgery. PLoS One, 10(3), 2015, e0120863.
142. 142 Pajenda, S., Ilhan-Mutlu, A., Preusser, M., Roka, S., Druml, W., Wagner, L., NephroCheck data compared to serum creatinine in various clinical settings. BMC Nephrol, 16, 2015, 206.
143. 143 Zager, R.A., Johnson, A.C., Becker, K., Plasma and urinary heme oxygenase-1 in AKI. J Am Soc Nephrol 23:6 (2012), 1048–1057.
144. 144 Li, Z., Xu, Y., Liu, X., Nie, Y., Zhao, Z., Urinary heme oxygenase-1 as a potential biomarker for early diabetic nephropathy. Nephrology (Carlton) 22:1 (2016), 58–64.
145. 145 Billings, F.T. 4th, Yu, C., Byrne, J.G., Petracek, M.R., Pretorius, M., Heme oxygenase-1 and acute kidney injury following cardiac surgery. Cardiorenal Med 4:1 (2014), 12–21.