Induction of Tet3-dependent Epigenetic Remodeling by Low-dose Hydralazine Attenuates Progression of Chronic Kidney Disease

EBioMedicine

Volumn 2, Issue 1, 2015, Pages 19-36

  Tampe, Björn ^a,b   Tampe, Desiree ^a,b   Zeisberg, Elisabeth M ^a,b,c   Müller, Gerhard A ^a   Bechtel Walz, Wibke ^b,d   Koziolek, Michael ^a   Kalluri, Raghu ^b,e   Zeisberg, Michael ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

De methylation; DNA methylation; Epigenetics; Fibrosis; RASAL1; Ten Eleven Translocation (TET)

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AZACITIDINE; CALVASCULIN; DIHYDRALAZINE; DNA FRAGMENT; DOXYCYCLINE; HYDRALAZINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; RAS PROTEIN; RAS PROTEIN ACTIVATOR LIKE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; CPG ISLAND; CREATININE BLOOD LEVEL; DEMETHYLATION; DISEASE COURSE; DNA DEMETHYLATION; DNA EXTRACTION; DNA ISOLATION; EPIGENETICS; FOLIC ACID INDUCED NEPHROPATHY; GENE; GENE AMPLIFICATION; GENE SILENCING; GENETIC TRANSFECTION; HYPERTENSIVE NEPHROSCLEROSIS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; KIDNEY FIBROSIS; LOW DRUG DOSE; MOUSE; NEPHROSCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RENAL PROTECTION; RETROSPECTIVE STUDY; RNA EXTRACTION; TET METHYLCYTOSINE DIOXYGENASE 3; URETER OBSTRUCTION; URINARY EXCRETION; WESTERN BLOTTING;

EID: 84927720803     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2014.11.005     Document Type: Article

References (37)

1. Arce C., Segura-Pacheco B., Perez-Cardenas E., Taja-Chayeb L., Candelaria M., Duennas-Gonzalez A. Hydralazine target: from blood vessels to the epigenome. J. Transl. Med. 2006, 4:10.
2. Bechtel W., McGoohan S., Zeisberg E.M., et al. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat. Med. 2010, 16:544-550.
3. Bhutani N., Burns D.M., Blau H.M. DNA demethylation dynamics. Cell 2011, 146:866-872.
4. Chavez-Blanco A., Perez-Plasencia C., Perez-Cardenas E., et al. Antineoplastic effects of the DNA methylation inhibitor hydralazine and the histone deacetylase inhibitor valproic acid in cancer cell lines. Cancer Cell Int. 2006, 6:2.
5. Chuang J.C., Yoo C.B., Kwan J.M., et al. Comparison of biological effects of non-nucleoside DNA methylation inhibitors versus 5-aza-2'-deoxycytidine. Mol. Cancer Ther. 2005, 4:1515-1520.
6. Coronel J., Cetina L., Pacheco I., et al. A double-blind, placebo-controlled, randomized phase III trial of chemotherapy plus epigenetic therapy with hydralazine valproate for advanced cervical cancer. Preliminary results. Med. Oncol. 2011, 28(Suppl. 1):S540-S546.
7. Djukanovic L., Susic D., Jovanovic D., et al. Effects of captopril and hydralazine on progression of adriamycin nephropathy in spontaneously hypertensive rats. Isr. J. Med. Sci. 1994, 30:742-746.
8. Druey, inventor Ciba Pharm Prod Inc., assignee. 1,4-hydrazo-phtalazine and its acid salts. USA patent US2484785A. 1949.
9. Fern R.J., Yesko C.M., Thornhill B.A., Kim H.S., Smithies O., Chevalier R.L. Reduced angiotensinogen expression attenuates renal interstitial fibrosis in obstructive nephropathy in mice. J. Clin. Invest. 1999, 103:39-46.
10. Foulks J.M., Parnell K.M., Nix R.N., et al. Epigenetic drug discovery: targeting DNA methyltransferases. J. Biomol. Screen. 2012, 17:2-17.
11. Heagerty A.M., Russell G.I., Bing R.F., Thurston H., Swales J.D. The addition of prazosin to standard triple therapy in the treatment of severe hypertension. Br. J. Clin. Pharmacol. 1982, 13:539-541.
12. Hollander W., Judson W.E., Wilkins R.W. The effects of intravenous apresoline (hydralazine) on cardiovascular and renal function in patients with and without congestive heart failure. Circulation 1956, 13:664-674.
13. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
14. James P.A., Oparil S., Carter B.L., et al. 2014 evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). JAMA 2014, 311:507-520.
15. Knowles H.J., Tian Y.M., Mole D.R., Harris A.L. Novel mechanism of action for hydralazine: induction of hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and angiogenesis by inhibition of prolyl hydroxylases. Circ. Res. 2004, 95:162-169.
16. LeBleu V., Sugimoto H., Mundel T.M., et al. Stem cell therapies benefit Alport syndrome. J. Am. Soc. Nephrol. 2009, 20:2359-2370.
17. Leonetti G., Cuspidi C., Sampieri L., et al. Evaluation of the efficacy and safety of enalapril plus hydrochlorothiazide plus methyldopa vs standard triple therapy in the treatment of moderate to severe hypertension: results from a multicentre study. J. Hum. Hypertens. 1990, 4:5-11.
18. Ma L.J., Yang H., Gaspert A., et al. Transforming growth factor-beta-dependent and -independent pathways of induction of tubulointerstitial fibrosis in beta6(-/-) mice. Am. J. Pathol. 2003, 163:1261-1273.
19. Manucha W., Oliveros L., Carrizo L., Seltzer A., Valles P. Losartan modulation on NOS isoforms and COX-2 expression in early renal fibrogenesis in unilateral obstruction. Kidney Int. 2004, 65:2091-2107.
20. Mogensen C.E. Progression of nephropathy in long-term diabetics with proteinuria and effect of initial anti-hypertensive treatment. Scand. J. Clin. Lab. Invest. 1976, 36:383-388.
21. Parving H.H., Smidt U.M., Hommel E., et al. Effective antihypertensive treatment postpones renal insufficiency in diabetic nephropathy. Am. J. Kidney Dis. 1993, 22:188-195.
22. Pierpont G.L., Brown D.C., Franciosa J.A., Cohn J.N. Effect of hydralazine on renal failure in patients with congestive heart failure. Circulation 1980, 61:323-327.
23. Rayner H.C., Baharani J., Dasgupta I., et al. Does community-wide chronic kidney disease management improve patient outcomes?. Nephrol. Dial. Transplant. 2014, 29:644-649.
24. Schwarzenbach H., Hoon D.S., Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 2011, 11:426-437.
25. Science JMECfCDaC Management of chronic kidney disease stages 1-3. Comparative Effectiveness Review Summary Guide for Clinicians 2012, Agency for Research and Quality, US.
26. Soto K., Gomez-Garre D., Largo R., et al. Tight blood pressure control decreases apoptosis during renal damage. Kidney Int. 2004, 65:811-822.
27. Sugimoto H., LeBleu V.S., Bosukonda D., et al. Activin-like kinase 3 is important for kidney regeneration and reversal of fibrosis. Nat. Med. 2012, 18:396-404.
28. Sugiyama H., Kobayashi M., Wang D.H., et al. Telmisartan inhibits both oxidative stress and renal fibrosis after unilateral ureteral obstruction in acatalasemic mice. Nephrol. Dial. Transplant. 2005, 20:2670-2680.
29. Tahiliani M., Koh K.P., Shen Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
30. Tampe D., Zeisberg M. A primer on the epigenetics of kidney fibrosis. Minerva Med. 2012, 103:267-278.
31. Tampe D., Zeisberg M. Potential approaches to reverse or repair renal fibrosis. Nat. Rev. Nephrol. 2014, 10:226-237.
32. Tampe B., Zeisberg M. Evidence for the involvement of epigenetics in the progression of renal fibrogenesis. Nephrol. Dial. Transplant. 2014, 29(Suppl. 1):i1-i8.
33. Tampe B., Tampe D., Müller C.A., et al. Tet3-mediated hydroxymethylation of epigenetically silenced genes contributes to bone morphogenic protein 7-induced reversal of kidney fibrosis. J. Am. Soc. Nephrol. 2014, 25:905-912.
34. Velasquez M.T., Striffler J.S., Abraham A.A., OEt Michaelis, Scalbert E., Thibault N. Perindopril ameliorates glomerular and renal tubulointerstitial injury in the SHR/N-corpulent rat. Hypertension 1997, 30:1232-1237.
35. Xu Y., Xu C., Kato A., et al. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 2012, 151:1200-1213.
36. Zambrano P., Segura-Pacheco B., Perez-Cardenas E., et al. A phase I study of hydralazine to demethylate and reactivate the expression of tumor suppressor genes. BMC Cancer 2005, 5:44.
37. Zeisberg E.M., Zeisberg M. The role of promoter hypermethylation in fibroblast activation and fibrogenesis. J. Pathol. 2013, 229:264-273.