Beyond genetics: Epigenetic code in chronic kidney disease

Kidney International

Volumn 79, Issue 1, 2011, Pages 23-32

  Dwivedi, Rama S ^a   Herman, James G ^b   McCaffrey, Timothy A ^c   Raj, Dominic S C ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

chronic kidney disease; ESRD; genetics and development; mRNA; obesity

Indexed keywords

MICRORNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; UREMIC TOXIN;

ATHEROSCLEROSIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHRONIC KIDNEY DISEASE; CPG ISLAND; DIABETIC NEPHROPATHY; DNA METHYLATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; HUMAN; HYPERHOMOCYSTEINEMIA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION;

EID: 78650270964     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2010.335     Document Type: Review

References (123)

1. Collins FS, Patrinos A, Jordan E et al. New goals for the U.S. Human Genome Project: 1998-2003. Science 1998; 282: 682-689.
2. Kruglyak L. The road to genome-wide association studies. Nat Rev Genet 2008; 9: 314-318.
3. Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3000 shared controls. Nature 2007; 447: 661-678.
4. Waddington CH. The Strategy of the Genes. Geo Allen & Unwin: London, 1957.
5. Feinberg AP. Genome-scale approaches to the epigenetics of common human disease. Virchows Arch 2010; 456: 13-21.
6. Egger G, Liang G, Aparicio A et al. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004; 429: 457-463.
7. Callinan PA, Feinberg AP. The emerging science of epigenomics. Hum Mol Genet 2006; 15(Spec No 1): R95-101.
8. Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci USA 2002; 99: 3740-3745.
9. Bird AP, Wolffe AP. Methylation-induced repression-belts, braces, and chromatin. Cell 1999; 99: 451-454.
10. Graff JR, Herman JG, Lapidus RG et al. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res 1995; 55: 5195-5199.
11. Jarrard DF, Bova GS, Ewing CM et al. Deletional, mutational, and methylation analyses of CDKN2 (p16/MTS1) in primary and metastatic prostate cancer. Genes Chromosomes Cancer 1997; 19: 90-96.
12. Dwivedi RS, Wang LJ, Mirkin BL. S-adenosylmethionine synthetase is overexpressed in murine neuroblastoma cells resistant to nucleoside analogue inhibitors of S-adenosylhomocysteine hydrolase: a novel mechanism of drug resistance. Cancer Res 1999; 59: 1852-1856.
13. Qiu YY, Mirkin BL, Dwivedi RS. MDR1 hypermethylation contributes to the progression of neuroblastoma. Mol Cell Biochem 2007; 301: 131-135.
14. Wolffe AP, Matzke MA. Epigenetics: regulation through repression. Science 1999; 286: 481-486.
15. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349: 2042-2054.
16. Rountree MR, Bachman KE, Herman JG et al. DNA methylation, chromatin inheritance, and cancer. Oncogene 2001; 20: 3156-3165.
17. Peterson CL, Laniel MA. Histones and histone modifications. Curr Biol 2004; 14: R546-R551.
18. Jenuwein T. Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol 2001; 11: 266-273.
19. Jiang YH, Bressler J, Beaudet AL. Epigenetics and human disease. Annu Rev Genomics Hum Genet 2004; 5: 479-510.
20. Fire A, Xu S, Montgomery MK et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391: 806-811. (Pubitemid 28099681)
21. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9: 102-114.
22. Suzuki M, Sunaga N, Shames DS et al. RNA interference-mediated knockdown of DNA methyltransferase 1 leads to promoter demethylation and gene re-expression in human lung and breast cancer cells. Cancer Res 2004; 64: 3137-3143.
23. Lippman Z, Martienssen R. The role of RNA interference in heterochromatic silencing. Nature 2004; 431: 364-370.
24. Bernstein E, Kim SY, Carmell MA et al. Dicer is essential for mouse development. Nat Genet 2003; 35: 215-217.
25. Meister G, Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004; 431: 343-349.
26. Esau C, Kang X, Peralta E et al. MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 2004; 279: 52361-52365.
27. Poy MN, Eliasson L, Krutzfeldt J et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004; 432: 226-230.
28. Chen CZ, Li L, Lodish HF et al. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303: 83-86.
29. Zilberman D, Henikoff S. Genome-wide analysis of DNA methylation patterns. Development 2007; 134: 3959-3965.
30. Murrell A, Rakyan VK, Beck S. From genome to epigenome. Hum Mol Genet 2005; 14(Spec No 1): R3-R10.
31. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003; 3: 253-266.
32. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 1997; 25: 2532-2534.
33. Gonzalgo ML, Jones PA. Rapid quantitation of methylation differences at specific sites using methylation-sensitive single nucleotide primer extension (Ms-SNuPE). Nucleic Acids Res 1997; 25: 2529-2531.
34. Herman JG, Graff JR, Myohanen S et al. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996; 93: 9821-9826.
35. Uhlmann K, Brinckmann A, Toliat MR et al. Evaluation of a potential epigenetic biomarker by quantitative methyl-single nucleotide polymorphism analysis. Electrophoresis 2002; 23: 4072-4079.
36. Cross SH, Charlton JA, Nan X et al. Purification of CpG islands using a methylated DNA binding column. Nat Genet 1994; 6: 236-244.
37. Rauch T, Li H, Wu X et al. MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res 2006; 66: 7939-7947.
38. Bentley DR. Whole-genome re-sequencing. Curr Opin Genet Dev 2006; 16: 545-552.
39. Braslavsky I, Hebert B, Kartalov E et al. Sequence information can be obtained from single DNA molecules. Proc Natl Acad Sci USA 2003; 100: 3960-3964.
40. Fuks F, Hurd PJ, Wolf D et al. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 2003; 278: 4035-4040.
41. Ren B, Robert F, Wyrick JJ et al. Genome-wide location and function of DNA binding proteins. Science 2000; 290: 2306-2309.
42. Schubeler D, MacAlpine DM, Scalzo D et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 2004; 18: 1263-1271.
43. Morgan HD, Santos F, Green K et al. Epigenetic reprogramming in mammals. Hum Mol Genet 2005; 14(Spec No 1): R47-R58.
44. De Bustos C, Ramos E, Young JM et al. Tissue-specific variation in DNA methylation levels along human chromosome 1. Epigenetics Chromatin 2009; 2: 7.
45. Ball MP, Li JB, Gao Y et al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 2009; 27: 361-368.
46. Eckhardt F, Lewin J, Cortese R et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 2006; 38: 1378-1385.
47. Esteller M. Aberrant DNA methylation as a cancer-inducing mechanism. Annu Rev Pharmacol Toxicol 2005; 45: 629-656.
48. Fraga MF, Ballestar E, Paz MF et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 2005; 102: 10604-10609.
49. Mikkelsen TS, Hanna J, Zhang X et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 2008; 454: 49-55.
50. Romano G. Artificial reprogramming of human somatic cells to generate pluripotent stem cells: a possible alternative to the controversial use of human embryonic stem cells. Drug News Perspect 2008; 21: 440-445.
51. Brodie JC, Humes HD. Stem cell approaches for the treatment of renal failure. Pharmacol Rev 2005; 57: 299-313.
52. Zhang TY, Meaney MJ. Epigenetics and the environmental regulation of the genome and its function. Annu Rev Psychol 2010; 61: 439-443.
53. Friso S, Choi SW. Gene-nutrient interactions in one-carbon metabolism. Curr Drug Metab 2005; 6: 37-46.
54. Rampersaud GC, Kauwell GP, Hutson AD et al. Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr 2000; 72: 998-1003.
55. Heller H, Kammer C, Wilgenbus P et al. Chromosomal insertion of foreign (adenovirus type 12, plasmid, or bacteriophage lambda) DNA is associated with enhanced methylation of cellular DNA segments. Proc Natl Acad Sci USA 1995; 92: 5515-5519.
56. Holliday R. Genomic imprinting and allelic exclusion. Dev Suppl 1990; 108: 125-129.
57. Kim DH, Nelson HH, Wiencke JK et al. p16(INK4a) and histology-specific methylation of CpG islands by exposure to tobacco smoke in non-small cell lung cancer. Cancer Res 2001; 61: 3419-3424.
58. Sutherland JE, Costa M. Epigenetics and the environment. Ann N Y Acad Sci 2003; 983: 151-160.
59. Feil R. Environmental and nutritional effects on the epigenetic regulation of genes. Mutat Res 2006; 600: 46-57.
60. Fenech M. The role of folic acid and vitamin B12 in genomic stability of human cells. Mutat Res 2001; 475: 57-67.
61. Bjornsson HT, Fallin MD, Feinberg AP. An integrated epigenetic and genetic approach to common human disease. Trends Genet 2004; 20: 350-358.
62. Feinberg AP. Epigenetics at the epicenter of modern medicine. JAMA 2008; 299: 1345-1350.
63. Bjornsson HT, Sigurdsson MI, Fallin MD et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA 2008; 299: 2877-2883.
64. Harvey SJ, Jarad G, Cunningham J et al. Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 2008; 19: 2150-2158.
65. Ho JJ, Marsden PA. Dicer cuts the kidney. J Am Soc Nephrol 2008; 19: 2043-2046.
66. Shi S, Yu L, Chiu C et al. Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 2008; 19: 2159-2169.
67. Harvey SJ, Jarad G, Cunningham J et al. Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 2008; 19: 2150-2158.
68. Ho J, Ng KH, Rosen S et al. Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol 2008; 19: 2069-2075.
69. Cerda J, Lameire N, Eggers P et al. Epidemiology of acute kidney injury. Clin J Am Soc Nephrol 2008; 3: 881-886.
70. Yang L, Besschetnova TY, Brooks CR et al. Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 2010; 16: 535-543, 1p.
71. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003; 112: 1776-1784.
72. Rashid A, Issa JP. CpG island methylation in gastroenterologic neoplasia: a maturing field. Gastroenterology 2004; 127: 1578-1588.
73. Bechtel W, McGoohan S, Zeisberg EM et al. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med 2010; 16: 544-550.
74. Liu Y. New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol 2010; 21: 212-222.
75. Perna AF, Ingrosso D, Satta E et al. Homocysteine metabolism in renal failure. Curr Opin Clin Nutr Metab Care 2004; 7: 53-57.
76. Kottgen A, Kao WH, Hwang SJ et al. Genome-wide association study for renal traits in the Framingham Heart and Atherosclerosis Risk in Communities Studies. BMC Med Genet 2008; 9: 49.
77. Perna AF, Ingrosso D, Zappia V et al. Enzymatic methyl esterification of erythrocyte membrane proteins is impaired in chronic renal failure. Evidence for high levels of the natural inhibitor S-adenosylhomocysteine. J Clin Invest 1993; 91: 2497-2503.
78. Stenvinkel P, Karimi M, Johansson S et al. Impact of inflammation on epigenetic DNA methylation-a novel risk factor for cardiovascular disease? J Intern Med 2007; 261: 488-499.
79. Rao M, Wong C, Kanetsky P et al. Cytokine gene polymorphism and progression of renal and cardiovascular diseases. Kidney Int 2007; 72: 549-556.
80. Nanayakkara PW, Kiefte-de Jong JC, Stehouwer CD et al. Association between global leukocyte DNA methylation, renal function, carotid intima-media thickness and plasma homocysteine in patients with stage 2-4 chronic kidney disease. Nephrol Dial Transplant 2008; 23: 2586-2592.
81. Hodge DR, Xiao W, Clausen PA et al. Interleukin-6 regulation of the human DNA methyltransferase (HDNMT) gene in human erythroleukemia cells. J Biol Chem 2001; 276: 39508-39511.
82. Raj DSC, Dominic EA, Pai A et al. Skeletal muscle, cytokines and oxidative stress in end-stage renal disease. Kidney Int 2005; 68: 2338-2344.
83. Fitzpatrick DR, Wilson CB. Methylation and demethylation in the regulation of genes, cells, and responses in the immune system. Clin Immunol 2003; 109: 37-45.
84. Bergman Y, Cedar H. A stepwise epigenetic process controls immunoglobulin allelic exclusion. Nat Rev Immunol 2004; 4: 753-761.
85. Wilson CB, Makar KW, Perez-Melgosa M. Epigenetic regulation of T cell fate and function. J Infect Dis 2002; 185(Suppl 1): S37-S45.
86. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005; 122: 947-956.
87. Avni O, Lee D, Macian F et al. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat Immunol 2002; 3: 643-651.
88. Armenante F, Merola M, Furia A et al. Repression of the IL-6 gene is associated with hypermethylation. Biochem Biophys Res Commun 1999; 258: 644-647.
89. He B, You L, Uematsu K et al. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci USA 2003; 100: 14133-14138.
90. Liu Y, Freedman BI. Genetics of progressive renal failure in diabetic kidney disease. Kidney Int Suppl 2005; 99: S94-S97.
91. Dabelea D, Hanson RL, Lindsay RS et al. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 2000; 49: 2208-2211.
92. Yokomori N, Tawata M, Onaya T. DNA demethylation during the differentiation of 3T3-L1 cells affects the expression of the mouse GLUT4 gene. Diabetes 1999; 48: 685-690. (Pubitemid 29153065)
93. Carretero MV, Torres L, Latasa U et al. Transformed but not normal hepatocytes express UCP2. FEBS Lett 1998; 439: 55-58.
94. Goh KP, Sum CF. Connecting the dots: molecular and epigenetic mechanisms in type 2 diabetes. Curr Diabetes Rev 2010; 6: 255-265.
95. Ling C, Poulsen P, Simonsson S et al. Genetic and epigenetic factors are associated with expression of respiratory chain component NDUFB6 in human skeletal muscle. J Clin Invest 2007; 117: 3427-3435.
96. Wren JD, Garner HR. Data-mining analysis suggests an epigenetic pathogenesis for type 2 diabetes. J Biomed Biotechnol 2005; 2005: 104-112.
97. Jiang MH, Fei J, Lan MS et al. Hypermethylation of hepatic Gck promoter in ageing rats contributes to diabetogenic potential. Diabetologia 2008; 51: 1525-1533.
98. Nathan DM, Cleary PA, Backlund JY et al. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005; 353: 2643-2653.
99. Engerman RL, Kern TS. Progression of incipient diabetic retinopathy during good glycemic control. Diabetes 1987; 36: 808-812.
100. El-Osta A, Brasacchio D, Yao D et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008; 205: 2409-2417.
101. Brasacchio D, Okabe J, Tikellis C et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 2009; 58: 1229-1236.
102. Culleton BF, Larson MG, Evans JC et al. Prevalence and correlates of elevated serum creatinine levels: the Framingham Heart Study. Arch Intern Med 1999; 159: 1785-1790.
103. Newman PE. Can reduced folic acid and vitamin B12 levels cause deficient DNA methylation producing mutations which initiate atherosclerosis? Med Hypotheses 1999; 53: 421-424.
104. Lund G, Andersson L, Lauria M et al. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J Biol Chem 2004; 279: 29147-29154.
105. Zaina S, Lindholm MW, Lund G. Nutrition and aberrant DNA methylation patterns in atherosclerosis: more than just hyperhomocysteinemia? J Nutr 2005; 135: 5-8.
106. Brattstrom L, Wilcken DE. Homocysteine and cardiovascular disease: cause or effect? Am J Clin Nutr 2000; 72: 315-323.
107. Castro R, Rivera I, Struys EA et al. Increased homocysteine and S-adenosylhomocysteine concentrations and DNA hypomethylation in vascular disease. Clin Chem 2003; 49: 1292-1296.
108. Laukkanen MO, Mannermaa S, Hiltunen MO et al. Local hypomethylation in atherosclerosis found in rabbit ec-sod gene. Arterioscler Thromb Vasc Biol 1999; 19: 2171-2178.
109. Ying AK, Hassanain HH, Roos CM et al. Methylation of the estrogen receptor-alpha gene promoter is selectively increased in proliferating human aortic smooth muscle cells. Cardiovasc Res 2000; 46: 172-179.
110. Zhu S, Goldschmidt-Clermont PJ, Dong C. Inactivation of monocarboxylate transporter MCT3 by DNA methylation in atherosclerosis. Circulation 2005; 112: 1353-1361.
111. D'Cruz LG, Baboonian C, Phillimore HE et al. Cytosine methylation confers instability on the cardiac troponin T gene in hypertrophic cardiomyopathy. J Med Genet 2000; 37: E18.
112. Ikeuchi M, Matsusaka H, Kang D et al. Overexpression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 2005; 112: 683-690.
113. Choi YS, Kim S, Pak YK. Mitochondrial transcription factor A (mtTFA) and diabetes. Diabetes Res Clin Pract 2001; 54(Suppl 2): S3-S9.
114. Ingrosso D, Cimmino A, Perna AF et al. Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinaemia in patients with uraemia. Lancet 2003; 361: 1693-1699.
115. Ptak C, Petronis A. Epigenetics and complex disease: from etiology to new therapeutics. Annu Rev Pharmacol Toxicol 2008; 48: 257-276.
116. Griffiths EA, Gore SD. DNA methyltransferase and histone deacetylase inhibitors in the treatment of myelodysplastic syndromes. Semin Hematol 2008; 45: 23-30.
117. Fukuda N. Development of gene therapies for cardiovascular and renal diseases by nucleic acid medicines. Med Chem 2006; 2: 13-19.
118. Esteller M, Sanchez-Cespedes M, Rosell R et al. Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients. Cancer Res 1999; 59: 67-70.
119. Muller HM, Widschwendter A, Fiegl H et al. DNA methylation in serum of breast cancer patients: an independent prognostic marker. Cancer Res 2003; 63: 7641-7645.
120. Garcia-Olmo D, Garcia-Olmo DC. Functionality of circulating DNA: the hypothesis of genometastasis. Ann N Y Acad Sci 2001; 945: 265-275.
121. Sharma P, Senthilkumar RD, Brahmachari V et al. Mining literature for a comprehensive pathway analysis: a case study for retrieval of homocysteine related genes for genetic and epigenetic studies. Lipids Health Dis 2006; 5: 1.
122. Ulrich CM, Curtin K, Samowitz W et al. MTHFR variants reduce the risk of G:C-4A:T transition mutations within the p53 tumor suppressor gene in colon tumors. J Nutr 2005; 135: 2462-2467.
123. Murrell A, Heeson S, Cooper WN et al. An association between variants in the IGF2 gene and Beckwith-Wiedemann syndrome: interaction between genotype and epigenotype. Hum Mol Genet 2004; 13: 247-255.