Chromatin dynamics in kidney development and function

Cell and Tissue Research

Volumn 356, Issue 3, 2014, Pages 601-608

  Bechtel Walz, Wibke ^a   Huber, Tobias B ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

DNA methylation; Epigenetics; Glomerulus; Histone acetylation; Histone methylation; Kidney development; Metanephric mesenchyme; Nephron; Podocyte

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; CHROMATIN;

CELL AGING; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL REGENERATION; CHROMATIN; CHROMATIN STRUCTURE; DISEASE COURSE; DNA METHYLATION; EPIGENETICS; EPITHELIUM CELL; GENETIC REGULATION; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; KIDNEY DEVELOPMENT; KIDNEY EPITHELIUM; KIDNEY FUNCTION; NEPHRON; PODOCYTE; PRIORITY JOURNAL; REVIEW; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHRONIC KIDNEY FAILURE; EMBRYOLOGY; GENETIC EPIGENESIS; GENETICS; KIDNEY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PRESCHOOL CHILD;

ANIMALS; CHILD, PRESCHOOL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; HUMANS; KIDNEY; RENAL INSUFFICIENCY, CHRONIC;

EID: 84902290862     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1884-y     Document Type: Review

References (94)

1. Anglin JL, Song Y (2013) A medicinal chemistry perspective for targeting histone H3 lysine-79 methyltransferase DOT1L. J Med Chem 56:8972-8983
2. Aoki M, Terada T, Kajiwara M, Ogasawara K, Ikai I, Ogawa O, Katsura T, Inui K (2008) Kidney-specific expression of human organic cation transporter 2 (OCT2/SLC22A2) is regulated by DNA methylation. Am J Physiol Ren Physiol 295:F165-F170
3. Bechtel W, McGoohan S, Zeisberg EM, Muller GA, Kalbacher H, Salant DJ, Muller CA, Kalluri R, Zeisberg M (2010) Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med 16:544-550
4. Bennett-Baker PE, Wilkowski J, Burke DT (2003) Age-associated activation of epigenetically repressed genes in the mouse. Genetics 165:2055-2062 (Pubitemid 38040289)
5. Bird AP (1986) CpG-rich islands and the function of DNA methylation. Nature 321:209-213
6. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6-21
7. Blackledge NP, Klose R (2011) CpG island chromatin: a platform for gene regulation. Epigenetics 6:147-152
8. Brenner BM, Garcia DL, Anderson S (1988) Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1:335-347
9. Brilli LL, Swanhart LM, de Caestecker MP, Hukriede NA (2013) HDAC inhibitors in kidney development and disease. Pediatr Nephrol 28: 1909-1921
10. Brunskill EW, Aronow BJ, Georgas K, Rumballe B, Valerius MT, Aronow J, Kaimal V, Jegga AG, Yu J, Grimmond S, McMahon AP, Patterson LT, Little MH, Potter SS (2008) Atlas of gene expression in the developing kidney at microanatomic resolution. Dev Cell 15:781-791
11. Bush EW, McKinsey TA (2010) Protein acetylation in the cardiorenal axis: the promise of histone deacetylase inhibitors. Circ Res 106:272-284
12. Cai Y, Lechner MS, Nihalani D, Prindle MJ, Holzman LB, Dressler GR (2002) Phosphorylation of Pax2 by the c-Jun N-terminal kinase and enhanced Pax2-dependent transcription activation. J Biol Chem 277:1217-1222 (Pubitemid 34968871)
13. Cai Y, Brophy PD, Levitan I, Stifani S, Dressler GR (2003) Groucho suppresses Pax2 transactivation by inhibition of JNK-mediated phosphorylation. EMBO J 22:5522-5529 (Pubitemid 37279961)
14. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP (2005) Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 9:283-292 (Pubitemid 41051746)
15. Chen S, Bellew C, Yao X, Stefkova J, Dipp S, Saifudeen Z, Bachvarov D, El-Dahr SS (2011) Histone deacetylase (HDAC) activity is critical for embryonic kidney gene expression, growth, and differentiation. J Biol Chem 286:32775-32789
16. Cheng X, Blumenthal RM (2010) Coordinated chromatin control: structural and functional linkage of DNA and histone methylation. Biochemistry 49:2999-3008
17. Cho YW, Hong T, Hong S, Guo H, Yu H, Kim D, Guszczynski T, Dressler GR, Copeland TD, Kalkum M, Ge K (2007) PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 282:20395-20406 (Pubitemid 47099985)
18. Colaneri A, Staffa N, Fargo DC, Gao Y, Wang T, Peddada SD, Birnbaumer L (2011) Expanded methyl-sensitive cut counting reveals hypomethylation as an epigenetic state that highlights functional sequences of the genome. Proc Natl Acad Sci USA 108:9715-9720
19. de Groh ED, Swanhart LM, Cosentino CC, Jackson RL, Dai W, Kitchens CA, Day BW, Smithgall TE, Hukriede NA (2010) Inhibition of histone deacetylase expands the renal progenitor cell population. J Am Soc Nephrol 21:794-802
20. Deaton AM, Webb S, Kerr AR, Illingworth RS, Guy J, Andrews R, Bird A (2011) Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res 21:1074-1086
21. DeLange RJ, Fambrough DM, Smith EL, Bonner J (1968) Calf and pea histone IV. I. Amino acid compositions and the identical COOH-terminal 19-residue sequence. J Biol Chem 243:5906-5913
22. Dressler GR (2008) Epigenetics, development, and the kidney. J Am Soc Nephrol 19:2060-2067
23. Dressler GR (2009) Advances in early kidney specification, development and patterning. Development 136:3863-3874
24. Dressler GR, Wilkinson JE, Rothenpieler UW, Patterson LT, Williams-Simons L, Westphal H (1993) Deregulation of Pax-2 expression in transgenic mice generates severe kidney abnormalities. Nature 362:65-67 (Pubitemid 23087291)
25. Ferguson-Smith AC, Surani MA (2001) Imprinting and the epigenetic asymmetry between parental genomes. Science 293:1086-1089 (Pubitemid 32758080)
26. Fraga MF, Esteller M (2007) Epigenetics and aging: the targets and the marks. Trends Genet 23:413-418 (Pubitemid 47088010)
27. Gershey EL, Vidali G, Allfrey VG (1968) Chemical studies of histone acetylation. The occurrence of epsilon-N-acetyllysine in the f2a1 histone. J Biol Chem 243:5018-5022
28. Goldknopf IL, Taylor CW, Baum RM, Yeoman LC, Olson MO, Prestayko AW, Busch H (1975) Isolation and characterization of protein A24, a "histone-like" non-histone chromosomal protein. J Biol Chem 250:7182-7187
29. Huang N, Tan L, Xue Z, Cang J, Wang H (2012) Reduction of DNA hydroxymethylation in the mouse kidney insulted by ischemia reperfusion. Biochem Biophys Res Commun 422:697-702
30. Illingworth R, Kerr A, Desousa D, Jorgensen H, Ellis P, Stalker J, Jackson D, Clee C, Plumb R, Rogers J, Humphray S, Cox T, Langford C, Bird A (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6:e22
31. Issaeva I, Zonis Y, Rozovskaia T, Orlovsky K, Croce CM, Nakamura T, Mazo A, Eisenbach L, Canaani E (2007) Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol Cell Biol 27:1889-1903
32. Jaenisch R (1997) DNA methylation and imprinting: why bother? Trends Genet 13:323-329
33. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074-1080 (Pubitemid 32758077)
34. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19:187-191 (Pubitemid 28248804)
35. Kikuchi R, Kusuhara H, Hattori N, Kim I, Shiota K, Gonzalez FJ, Sugiyama Y (2007) Regulation of tissue-specific expression of the human and mouse urate transporter 1 gene by hepatocyte nuclear factor 1 alpha/beta and DNAmethylation.Mol Pharmacol 72:1619-1625 (Pubitemid 350146099)
36. Kikuchi R, Yagi S, Kusuhara H, Imai S, Sugiyama Y, Shiota K (2010) Genome-wide analysis of epigenetic signatures for kidney-specific transporters. Kidney Int 78:569-577
37. Kim GD, Ni J, Kelesoglu N, Roberts RJ, Pradhan S (2002) Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J 21:4183-4195 (Pubitemid 34857450)
38. Kleinsmith LJ, Allfrey VG, Mirsky AE (1966) Phosphoprotein metabolism in isolated lymphocyte nuclei. Proc Natl Acad Sci USA 55:1182-1189
39. Kohli RM, Zhang Y (2013) TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502:472-479
40. Komohara Y, Suekane S, Noguchi M, Matsuoka K, Yamada A, Itoh K (2007) Expression of APOBEC3G in kidney cells. Tissue Antigens 69:95-98 (Pubitemid 46025343)
41. Kurdistani SK, Grunstein M (2003) Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 4:276-284 (Pubitemid 36383954)
42. Laird PW, Jaenisch R (1996) The role of DNA methylation in cancer genetic and epigenetics. Annu Rev Genet 30:441-464 (Pubitemid 27015267)
43. Lefevre GM, Patel SR, Kim D, Tessarollo L, Dressler GR (2010) Altering a histone H3K4 methylation pathway in glomerular podocytes promotes a chronic disease phenotype. PLoS Genet 6:e1001142
44. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13:1192-1200 (Pubitemid 36872941)
45. Liang P, Song F, Ghosh S, Morien E, Qin M, Mahmood S, Fujiwara K, Igarashi J, Nagase H, Held WA (2011) Genome-wide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. BMC Genomics 12:231
46. Ling C, Groop L (2009) Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 58:2718-2725
47. Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G (2001) Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293:2453-2455 (Pubitemid 32917326)
48. Little MH, McMahon AP (2012) Mammalian kidney development: principles, progress, and projections. Cold Spring Harb Perspect Biol 4
49. Manke IA, Lowery DM, Nguyen A, Yaffe MB (2003) BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636-639 (Pubitemid 37310918)
50. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, Turecki G, Delaney A, Varhol R, Thiessen N, Shchors K, Heine VM, Rowitch DH, Xing X, Fiore C, Schillebeeckx M, Jones SJ, Haussler D, Marra MA, Hirst M, Wang T, Costello JF (2010) Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466:253-257
51. McLaughlin N, Wang F, Saifudeen Z, El-Dahr SS (2013a) In situ histone landscape of nephrogenesis. Epigenetics 9:222-235
52. McLaughlin N, Yao X, Li Y, Saifudeen Z, El-Dahr SS (2013b) Histone signature of metanephric mesenchyme cell lines. Epigenetics 8:970-978
53. Monk M (1990) Changes in DNA methylation during mouse embryonic development in relation to X-chromosome activity and imprinting. Philos Trans R Soc Lond B 326:299-312
54. Murray K (1964) The Occurrence of Epsilon-N-Methyl Lysine in Histones. Biochemistry 3:10-15
55. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389 (Pubitemid 28269714)
56. Ord MG, Stocken LA (1967) Phosphate and thiol groups in histone f3 from rat liver and thymus nuclei. Biochem J 102:631-636
57. O'Sullivan L, Combes AN, Moritz KM (2012) Epigenetics and developmental programming of adult onset diseases. Pediatr Nephrol 27:2175-2182
58. Patel SR, Kim D, Levitan I, Dressler GR (2007) The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev Cell 13:580-592 (Pubitemid 47500812)
59. Quaggin SE, Kreidberg JA (2008) Development of the renal glomerulus: good neighbors and good fences. Development 135:609-620 (Pubitemid 351405014)
60. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593-599 (Pubitemid 30641039)
61. Reddy MA, Natarajan R (2011) Epigenetics in diabetic kidney disease. J Am Soc Nephrol 22:2182-2185
62. Reidy KJ, Rosenblum ND (2009) Cell and molecular biology of kidney development. Semin Nephrol 29:321-337
63. Reik W, Walter J (2001) Evolution of imprinting mechanisms: the battle of the sexes begins in the zygote. Nat Genet 27:255-256 (Pubitemid 32201843)
64. Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh ST, Lee HB (2005) Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 16:667-675 (Pubitemid 41725103)
65. Riggs AD,Porter TN(1996)Overviewofepigeneticmechanisms.In:Russo VEA,Martienssen RA,Riggs AD(eds)Epigeneticmechanismsofgeneregulation. ColdSpringHarborLaboratory,ColdSpringHarbor, pp29-45
66. Ritz E, Amann K, Koleganova N, Benz K (2011) Prenatal programming-effects on blood pressure and renal function. Nat Rev Nephrol 7:137-144
67. Rosenberg SL, Chen S, McLaughlin N, El-Dahr SS (2011) Regulation of kidney development by histone deacetylases. Pediatr Nephrol 26:1445-1452
68. Rusche LN, Kirchmaier AL, Rine J (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72:481-516 (Pubitemid 36930453)
69. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419:407-411
70. Saxen L, Sariola H (1987) Early organogenesis of the kidney. Pediatr Nephrol 1:385-392 (Pubitemid 18016633)
71. Sharma M, Brantley JG, Vassmer D, Chaturvedi G, Baas J, Vanden Heuvel GB (2009) The homeodomain protein Cux1 interacts with Grg4 to repress p27 kip1 expression during kidney development. Gene 439:87-94
72. Shiio Y, Eisenman RN (2003) Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci USA 100:13225-13230 (Pubitemid 37444723)
73. Song F, Mahmood S, Ghosh S, Liang P, Smiraglia DJ, Nagase H, Held WA (2009) Tissue specific differentially methylated regions (TDMR): changes in DNA methylation during development. Genomics 93:130-139
74. Song R, Van Buren T, Yosypiv IV (2010) Histone deacetylases are critical regulators of the renin-angiotensin system during ureteric bud branching morphogenesis. Pediatr Res 67:573-578
75. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, Tiwari VK, Schubeler D (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480:490-495
76. Staruschenko A (2013) Aldosterone-dependent trans-activation and epigenetic derepression of ENaC: where is the balance? Am J Physiol Ren Physiol 305:F968-F969
77. Suetake I, Shinozaki F, Miyagawa J, Takeshima H, Tajima S (2004) DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J Biol Chem279:27816-27823 (Pubitemid 38812623)
78. Sun W, Guan M, Li X (2014) 5-hydroxymethylcytosine-mediated DNA demethylation in stem cells and development. Stem Cells Dev (in press)
79. Surendran K, Kopan R (2011) Chromatin-based mechanisms of renal epithelial differentiation. J Am Soc Nephrol 22:1208-1212
80. Szemes M, Dallosso AR, Melegh Z, Curry T, Li Y, Rivers C, Uney J, Magdefrau AS, Schwiderski K, Park JH, Brown KW, Shandilya J, Roberts SG, Malik K (2013) Control of epigenetic states by WT1 via regulation of de novo DNA methyltransferase 3A. Hum Mol Genet 22:74-83
81. Takano K, Kawasaki Y, Imaizumi T, Matsuura H, Nozawa R, Tannji M, Suyama K, Isome M, Suzuki H, Hosoya M (2007) Development of glomerular endothelial cells, podocytes and mesangial cells in the human fetus and infant. Tohoku J Exp Med 212:81-90 (Pubitemid 46711729)
82. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34:75-79 (Pubitemid 36548794)
83. Tonna S, El-Osta A, Cooper ME, Tikellis C (2010) Metabolic memory and diabetic nephropathy: potential role for epigenetic mechanisms. Nat Rev Nephrol 6:332-341
84. Ueda K, Omachi A, Kawaichi M, Hayaishi O (1975) Natural occurrence of poly(ADP-ribosyl) histones in rat liver. Proc Natl Acad Sci USA 72:205-209
85. Vidali G, Gershey EL, Allfrey VG (1968) Chemical studies of histone acetylation. The distribution of epsilon-N-acetyllysine in calf thymus histones. J Biol Chem 243:6361-6366
86. Villeneuve LM, Natarajan R (2010) The role of epigenetics in the pathology of diabetic complications. Am J Physiol Ren Physiol 299:F14-F25
87. Vincent A, Van Seuningen I (2009) Epigenetics, stem cells and epithelial cell fate. Differentiation 78:99-107
88. Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 23:62-66 (Pubitemid 29418789)
89. Wiggins JE, Goyal M, Sanden SK, Wharram BL, Shedden KA, Misek DE, Kuick RD, Wiggins RC (2005) Podocyte hypertrophy, "adaptation," and "decompensation" associated with glomerular enlargement and glomerulosclerosis in the aging rat: prevention by calorie restriction. J Am Soc Nephrol 16:2953-2966 (Pubitemid 44743493)
90. Wiggins JE, Goyal M, Wharram BL, Wiggins RC (2006) Antioxidant ceruloplasmin is expressed by glomerular parietal epithelial cells and secreted into urine in association with glomerular aging and high-calorie diet. J Am Soc Nephrol 17:1382-1387 (Pubitemid 43673418)
91. Wing MR, Devaney JM, Joffe MM, Xie D, Feldman HI, Dominic EA, Guzman NJ, Ramezani A, Susztak K, Herman JG, Cope L, Harmon B, Kwabi-Addo B, Gordish-Dressman H, Go AS, He J, Lash JP, Kusek JW, Raj DS (2014) DNA methylation profile associated with rapid decline in kidney function: findings from the CRIC Study. Nephrol Dial Transplant 29(4):864-872
92. Wu H, Zhang Y (2014) Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156:45-68
93. Yokote S, Yamanaka S, Yokoo T (2012) De novo kidney regeneration with stem cells. J Biomed Biotechnol 2012:453519
94. Yosypiv IV, Boh MK, Spera MA, El-Dahr SS (2008) Downregulation of Spry-1, an inhibitor of GDNF/Ret, causes angiotensin II-induced ureteric bud branching. Kidney Int 74:1287-1293