Novel Therapeutic Strategy With Hypoxia-Inducible Factors via Reversible Epigenetic Regulation Mechanisms in Progressive Tubulointerstitial Fibrosis

Seminars in Nephrology

Volumn 33, Issue 4, 2013, Pages 375-382

  Mimura, Imari ^a   Tanaka, Tetsuhiro ^a   Nangaku, Masaomi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Chromatin; Epigenetics; Histone; Hypoxia; Tubulointerstitium

Indexed keywords

AGENTS AFFECTING PROTEIN METABOLISM; DIMETHYLOXALYGLYCINE; ERYTHROPOIETIN; HISTONE DEMETHYLASE; HYPOXIA INDUCIBLE FACTOR 1; TRANSCRIPTION FACTOR RUNX3; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VALSARTAN;

AGING NEPHROPATHY; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHRONIC KIDNEY DISEASE; CONFORMATIONAL TRANSITION; DIABETIC NEPHROPATHY; DRUG MECHANISM; EPIGENETICS; ERYTHROPOIETIN GENE; GENE; GENE SILENCING; GENETIC REGULATION; GENOTYPE ENVIRONMENT INTERACTION; HISTONE MODIFICATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; KIDNEY DISEASE; KIDNEY FAILURE; KIDNEY FIBROSIS; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; RUNX3 GENE; UPREGULATION;

CHROMATIN; EPIGENETICS; HISTONE; HYPOXIA; TUBULOINTERSTITIUM;

CHROMATIN ASSEMBLY AND DISASSEMBLY; DIABETIC NEPHROPATHIES; EPIGENESIS, GENETIC; ERYTHROPOIETIN; FIBROSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; KIDNEY FAILURE, CHRONIC; KIDNEY TUBULES;

EID: 84883527272     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2013.05.009     Document Type: Article

References (70)

1. Mimura I., Nangaku M. The suffocating kidney: tubulointerstitial hypoxia in end-stage renal disease. Nat Rev Nephrol 2010, 6:667-678.
2. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 2006, 17:17-25.
3. Tanaka T., Kato H., Kojima I., Ohse T., Son D., Tawakami T., et al. Hypoxia and expression of hypoxia-inducible factor in the aging kidney. J Gerontol A Biol Sci Med Sci 2006, 61:795-805.
4. Tanaka T., Matsumoto M., Inagi R., Miyata T., Kojima I., Ohse T., et al. Induction of protective genes by cobalt ameliorates tubulointerstitial injury in the progressive Thy1 nephritis. Kidney Int 2005, 68:2714-2725.
5. Tanaka T., Kojima I., Ohse T., Ingelfinger J.R., Adler S., Fujita T., et al. Cobalt promotes angiogenesis via hypoxia-inducible factor and protects tubulointerstitium in the remnant kidney model. Lab Invest 2005, 85:1292-1307.
6. Tanaka T., Kojima I., Ohse T., Inagi R., Miyata T., Ingelfinger J.R., et al. Hypoxia-inducible factor modulates tubular cell survival in cisplatin nephrotoxicity. Am J Physiol Renal Physiol 2005, 289:F1123-F1133.
7. Mimura I., Nangaku M., Nishi H., Inagi R., Tanaka T., Fujita T. Cytoglobin, a novel globin, plays an antifibrotic role in the kidney. Am J Physiol Renal Physiol 2010, 299:F1120-F1133.
8. Nishi H., Inagi R., Kawada N., Yoshizato K., Mimura I., Fujita T., et al. Cytoglobin, a novel member of the globin family, protects kidney fibroblasts against oxidative stress under ischemic conditions. Am J Pathol 2011, 178:128-139.
9. Wang G.L., Semenza G.L. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995, 270:1230-1237.
10. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008, 30:393-402.
11. Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004, 5:343-354.
12. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
13. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002, 16:6-21.
14. Zhou V.W., Goren A., Bernstein B.E. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 2011, 12:7-18.
15. Wolffe A.P., Pruss D. Targeting chromatin disruption: transcription regulators that acetylate histones. Cell 1996, 84:817-819.
16. Zofall M., Grewal S.I. HULC, a histone H2B ubiquitinating complex, modulates heterochromatin independent of histone methylation in fission yeast. J Biol Chem 2007, 282:14065-14072.
17. Rossetto D., Avvakumov N., Cote J. Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics 2012, 7:1098-1108.
18. Zager R.A., Johnson A.C. Renal ischemia-reperfusion injury upregulates histone-modifying enzyme systems and alters histone expression at proinflammatory/profibrotic genes. Am J Physiol Renal Physiol 2009, 296:F1032-F1041.
19. Kato M., Wang L., Putta S., Wang M., Yuan H., Sun G., et al. Post-transcriptional up-regulation of Tsc-22 by Ybx1, a target of miR-216a, mediates TGF-{beta}-induced collagen expression in kidney cells. J Biol Chem 2010, 285:34004-34015.
20. Patel V., Hajarnis S., Williams D., Hunter R., Huynh D., Igarashi P. MicroRNAs regulate renal tubule maturation through modulation of Pkd1. J Am Soc Nephrol 2012, 23:1941-1948.
21. Jin W., Reddy M.A., Chen Z., Putta S., Lanting L., Kato M., et al. Small RNA sequencing reveals microRNAs that modulate angiotensin II effects in vascular smooth muscle cells. J Biol Chem 2012, 287:15672-15683.
22. Putta S., Lanting L., Sun G., Lawson G., Kato M., Natarajan R. Inhibiting microRNA-192 ameliorates renal fibrosis in diabetic nephropathy. J Am Soc Nephrol 2012, 23:458-469.
23. Kato M., Putta S., Wang M., Yuan H., Lanting L., Nair I., et al. TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 2009, 11:881-889.
24. Kato M., Zhang J., Wang M., Lanting L., Yuan H., Rossi J.J., et al. MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 2007, 104:3432-3437.
25. Lee J.T. Epigenetic regulation by long noncoding RNAs. Science 2012, 338:1435-1439.
26. Kanki Y., Kohro T., Jiang S., Tsutsumi S., Mimura I., Suehiro J., et al. Epigenetically coordinated GATA2 binding is necessary for endothelium-specific endomucin expression. EMBO J 2011, 30:2582-2595.
27. Mimura I., Nangaku M., Kanki Y., Tsutsumi S., Inoue T., Kohro T., et al. Dynamic change of chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of hypoxia-inducible factor 1 and KDM3A. Mol Cell Biol 2012, 32:3018-3032.
28. Woroniecki R., Gaikwad A.B., Susztak K. Fetal environment, epigenetics, and pediatric renal disease. Pediatr Nephrol 2011, 26:705-711.
29. Kanno Y., Vahedi G., Hirahara K., Singleton K., O'Shea J.J. Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity. Ann Rev Immunol 2012, 30:707-731.
30. Hirahara K., Vahedi G., Ghoreschi K., Yang X.P., Nakayamada S., Kanno Y., et al. Helper T-cell differentiation and plasticity: insights from epigenetics. Immunology 2011, 134:235-245.
31. 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, 115:453-458.
32. Villeneuve L.M., Reddy M.A., Natarajan R. Epigenetics: deciphering its role in diabetes and its chronic complications. Clin Exp Pharmacol Physiol 2011, 38:451-459.
33. Yang J., Ledaki I., Turley H., Gatter K.C., Montero J.C., Li J.L., et al. Role of hypoxia-inducible factors in epigenetic regulation via histone demethylases. Ann N Y Acad Sci 2009, 1177:185-197.
34. Perez-Perri J.I., Acevedo J.M., Wappner P. Epigenetics: new questions on the response to hypoxia. Int J Mol Sci 2011, 12:4705-4721.
35. Chen S., Bellew C., Yao X., Stefkova J., Dipp S., Saifudeen Z., et al. Histone deacetylase (HDAC) activity is critical for embryonic kidney gene expression, growth, and differentiation. J Biol Chem 2011, 286:32775-32789.
36. Beyer S., Kristensen M.M., Jensen K.S., Johansen J.V., Staller P. The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF. J Biol Chem 2008, 283:36542-36552.
37. Pollard P.J., Loenarz C., Mole D.R., McDonough M.A., Gleadle J.M., Schofield C.J., et al. Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha. Biochem J 2008, 416:387-394.
38. Wellmann S., Bettkober M., Zelmer A., Seeger K., Faigle M., Eltzschig H.K., et al. Hypoxia upregulates the histone demethylase JMJD1A via HIF-1. Biochem Biophys Res Commun 2008, 372:892-897.
39. Krieg A.J., Rankin E.B., Chan D., Razorenova O., Fernandez S., Giaccia A.J. Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 alpha enhances hypoxic gene expression and tumor growth. Mol Cell Biol 2010, 30:344-353.
40. Lee S.H., Kim J., Kim W.H., Lee Y.M. Hypoxic silencing of tumor suppressor RUNX3 by histone modification in gastric cancer cells. Oncogene 2009, 28:184-194.
41. Chen H., Yan Y., Davidson T.L., Shinkai Y., Costa M. Hypoxic stress induces dimethylated histone H3 lysine 9 through histone methyltransferase G9a in mammalian cells. Cancer Res 2006, 66:9009-9016.
42. Sun G., Reddy M.A., Yuan H., Lanting L., Kato M., Natarajan R. Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol 2010, 21:2069-2080.
43. Yuan H., Reddy M.A., Sun G., Lanting L., Wang M., Kato M., et al. Involvement of p300/CBP and epigenetic histone acetylation in TGF-beta1 mediated gene transcription in mesangial cells. Am J Physiol Renal Physiol 2013, 304:F601-F613.
44. Miao F., Chen Z., Zhang L., Liu Z., Wu X., Yuan Y.C., et al. Profiles of epigenetic histone post-translational modifications at type 1 diabetes susceptible genes. J Biol Chem 2012, 287:16335-16345.
45. Gaikwad A.B., Gupta J., Tikoo K. Epigenetic changes and alteration of Fbn1 and Col3A1 gene expression under hyperglycaemic and hyperinsulinaemic conditions. Biochem J 2010, 432:333-341.
46. Villeneuve L.M., Natarajan R. The role of epigenetics in the pathology of diabetic complications. Am J Physiol Renal Physiol 2010, 299:F14-F25.
47. Tonna S., El-Osta A., Cooper M.E., Tikellis C. Metabolic memory and diabetic nephropathy: potential role for epigenetic mechanisms. Nat Rev Nephrol 2010, 6:332-341.
48. Reddy M.A., Natarajan R. Epigenetic mechanisms in diabetic vascular complications. Cardiovasc Res 2011, 90:421-429.
49. Villeneuve L.M., Reddy M.A., Lanting L.L., Wang M., Meng L., Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci U S A 2008, 105:9047-9052.
50. Villeneuve L.M., Kato M., Reddy M.A., Wang M., Lanting L., Natarajan R. Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes 2010, 59:2904-2915.
51. Caramori M.L., Kim Y., Moore J.H., Rich S.S., Mychaleckyj J.C., Kikyo N., et al. Gene expression differences in skin fibroblasts in identical twins discordant for type 1 diabetes. Diabetes 2012, 61:739-744.
52. Abrass C.K., Hansen K., Popov V., Denisenko O. Alterations in chromatin are associated with increases in collagen III expression in aging nephropathy. Am J Physiol Renal Physiol 2011, 300:F531-F539.
53. Sataranatarajan K., Feliers D., Mariappan M.M., Lee H.J., Lee M.J., Day R.T., et al. Molecular events in matrix protein metabolism in the aging kidney. Aging Cell 2012, 11:1065-1073.
54. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008, 22:894-907.
55. Lan Y.F., Chen H.H., Lai P.F., Cheng C.F., Huang Y.T., Lee Y.C., et al. MicroRNA-494 reduces ATF3 expression and promotes AKI. J Am Soc Nephrol 2012, 23:2012-2023.
56. Wang G.L., Semenza G.L. Molecular basis of hypoxia-induced erythropoietin expression. Curr Opin Hematol 1996, 3:156-162.
57. Warnecke C., Zaborowska Z., Kurreck J., Erdmann V.A., Frei U., Wiesener M., et al. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J 2004, 18:1462-1464.
58. Semenza G.L., Nejfelt M.K., Chi S.M., Antonarakis S.E. Hypoxia-inducible nuclear factors bind to an enhancer element located 3' to the human erythropoietin gene. Proc Natl Acad Sci U S A 1991, 88:5680-5684.
59. Suzuki N., Obara N., Pan X., Watanabe M., Jishage K., Minegishi N., et al. Specific contribution of the erythropoietin gene 3' enhancer to hepatic erythropoiesis after late embryonic stages. Mol Cell Biol 2011, 31:3896-3905.
60. Steinmann K., Richter A.M., Dammann R.H. Epigenetic silencing of erythropoietin in human cancers. Genes Cancer 2011, 2:65-73.
61. Lee J.S., Kim Y., Bhin J., Shin H.J., Nam H.J., Lee S.H., et al. Hypoxia-induced methylation of a pontin chromatin remodeling factor. Proc Natl Acad Sci U S A 2011, 108:13510-13515.
62. Lee J.S., Kim Y., Kim I.S., Kim B., Choi H.J., Lee J.M., et al. Negative regulation of hypoxic responses via induced reptin methylation. Mol Cell 2010, 39:71-85.
63. Schodel J., Oikonomopoulos S., Ragoussis J., Pugh C.W., Ratcliffe P.J., Mole D.R. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 2011, 117:e207-e217.
64. Mole D.R., Blancher C., Copley R.R., Pollard P.J., Gleadle J.M., Ragoussis J., et al. Genome-wide association of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha DNA binding with expression profiling of hypoxia-inducible transcripts. J Biol Chem 2009, 284:16767-16775.
65. Kobayashi H., Gilbert V., Liu Q., Kapitsinou P.P., Unger T.L., Rha J., et al. Myeloid cell-derived hypoxia-inducible factor attenuates inflammation in unilateral ureteral obstruction-induced kidney injury. J Immunol 2012, 188:5106-5115.
66. Song Y.R., You S.J., Lee Y.M., Chin H.J., Chae D.W., Oh Y.K., et al. Activation of hypoxia-inducible factor attenuates renal injury in rat remnant kidney. Nephrol Dial Transplant 2010, 25:77-85.
67. Higgins D.F., Kimura K., Bernhardt W.M., Shrimanker N., Akai Y., Hohenstein B., et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 2007, 117:3810-3820.
68. Takiyama Y., Harumi T., Watanabe J., Fujita Y., Honjo J., Shimizu N., et al. Tubular injury in a rat model of type 2 diabetes is prevented by metformin: a possible role of HIF-1alpha expression and oxygen metabolism. Diabetes 2011, 60:981-992.
69. Tang L., Yi R., Yang B., Li H., Chen H., Liu Z. Valsartan inhibited HIF-1alpha pathway and attenuated renal interstitial fibrosis in streptozotocin-diabetic rats. Diabetes Res Clin Pract 2012, 97:125-131.
70. Kapitsinou P.P., Jaffe J., Michael M., Swan C.E., Duffy K.J., Erickson-Miller C.L., et al. Preischemic targeting of HIF prolyl hydroxylation inhibits fibrosis associated with acute kidney injury. Am J Physiol Renal Physiol 2012, 302:F1172-F1179.