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Published in: Pediatric Nephrology 7/2016

01-07-2016 | Review

Epigenetics mechanisms in renal development

Authors: Sylvia A. Hilliard, Samir S. El-Dahr

Published in: Pediatric Nephrology | Issue 7/2016

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Abstract

Appreciation for the role of epigenetic modifications in the diagnosis and treatment of diseases is fast gaining attention. Treatment of chronic kidney disease stemming from diabetes or hypertension as well as Wilms tumor will all profit from knowledge of the changes in the epigenomic landscapes. To do so, it is essential to characterize the epigenomic modifiers and their modifications under normal physiological conditions. The transcription factor Pax2 was identified as a major epigenetic player in the early specification of the kidney. Notably, the progenitors of all nephrons that reside in the cap mesenchyme display a unique bivalent histone signature (expressing repressive epigenetic marks alongside activation marks) on lineage-specific genes. These cells are deemed poised for differentiation and commitment to the nephrogenic lineage. In response to the appropriate inducing signal, these genes lose their repressive histone marks, which allow for their expression in nascent nephron precursors. Such knowledge of the epigenetic landscape and the resultant cell fate or behavior in the developing kidney will greatly improve the overall success in designing regenerative strategies and tissue reprogramming methodologies from pluripotent cells.
Literature
1.
go back to reference Chi P, Allis CD, Wang GG (2010) Covalent histone modifications—miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 10:457–469CrossRefPubMedPubMedCentral Chi P, Allis CD, Wang GG (2010) Covalent histone modifications—miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 10:457–469CrossRefPubMedPubMedCentral
3.
go back to reference Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473:43–49CrossRefPubMedPubMedCentral Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473:43–49CrossRefPubMedPubMedCentral
4.
go back to reference Gerstein MB, Bruce C, Rozowsky JS, Zheng D, Du J, Korbel JO, Emanuelsson O, Zhang ZD, Weissman S, Snyder M (2007) What is a gene, post-ENCODE? History and updated definition. Genome Res 17:669–681CrossRefPubMed Gerstein MB, Bruce C, Rozowsky JS, Zheng D, Du J, Korbel JO, Emanuelsson O, Zhang ZD, Weissman S, Snyder M (2007) What is a gene, post-ENCODE? History and updated definition. Genome Res 17:669–681CrossRefPubMed
6.
go back to reference Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322CrossRefPubMedPubMedCentral Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322CrossRefPubMedPubMedCentral
7.
go back to reference Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Carninci P, Cawley S, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Clee C, Collins FS, Cook LL, Copley RR, Coulson A, Couronne O, Cuff J, Curwen V, Cutts T, Daly M, David R, Davies J, Delehaunty KD, Deri J, Dermitzakis ET, Dewey C, Dickens NJ, Diekhans M, Dodge S, Dubchak I, Dunn DM, Eddy SR, Elnitski L, Emes RD, Eswara P, Eyras E, Felsenfeld A, Fewell GA, Flicek P, Foley K, Frankel WN, Fulton LA, Fulton RS, Furey TS, Gage D, Gibbs RA, Glusman G, Gnerre S, Goldman N, Goodstadt L, Grafham D, Graves TA, Green ED, Gregory S, Guigó R, Guyer M, Hardison RC, Haussler D, Hayashizaki Y, Hillier LW, Hinrichs A, Hlavina W, Holzer T, Hsu F, Hua A, Hubbard T, Hunt A, Jackson I, Jaffe DB, Johnson LS, Jones M, Jones TA, Joy A, Kamal M, Karlsson EK, Karolchik D, Kasprzyk A, Kawai J, Keibler E, Kells C, Kent WJ, Kirby A, Kolbe DL, Korf I, Kucherlapati RS, Kulbokas EJ, Kulp D, Landers T, Leger JP, Leonard S, Letunic I, Levine R, Li J, Li M, Lloyd C, Lucas S, Ma B, Maglott DR, Mardis ER, Matthews L, Mauceli E, Mayer JH, McCarthy M, McCombie WR, McLaren S, McLay K, McPherson JD, Meldrim J, Meredith B, Mesirov JP, Miller W, Miner TL, Mongin E, Montgomery KT, Morgan M, Mott R, Mullikin JC, Muzny DM, Nash WE, Nelson JO, Nhan MN, Nicol R, Ning Z, Nusbaum C, O'Connor MJ, Okazaki Y, Oliver K, Overton-Larty E, Pachter L, Parra G, Pepin KH, Peterson J, Pevzner P, Plumb R, Pohl CS, Poliakov A, Ponce TC, Ponting CP, Potter S, Quail M, Reymond A, Roe BA, Roskin KM, Rubin EM, Rust AG, Santos R, Sapojnikov V, Schultz B, Schultz J, Schwartz MS, Schwartz S, Scott C, Seaman S, Searle S, Sharpe T, Sheridan A, Shownkeen R, Sims S, Singer JB, Slater G, Smit A, Smith DR, Spencer B, Stabenau A, Stange-Thomann N, Sugnet C, Suyama M, Tesler G, Thompson J, Torrents D, Trevaskis E, Tromp J, Ucla C, Ureta-Vidal A, Vinson JP, Von Niederhausern AC, Wade CM, Wall M, Weber RJ, Weiss RB, Wendl MC, West AP, Wetterstrand K, Wheeler R, Whelan S, Wierzbowski J, Willey D, Williams S, Wilson RK, Winter E, Worley KC, Wyman D, Yang S, Yang SP, Zdobnov EM, Zody MC, Lander ES (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562 Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Carninci P, Cawley S, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Clee C, Collins FS, Cook LL, Copley RR, Coulson A, Couronne O, Cuff J, Curwen V, Cutts T, Daly M, David R, Davies J, Delehaunty KD, Deri J, Dermitzakis ET, Dewey C, Dickens NJ, Diekhans M, Dodge S, Dubchak I, Dunn DM, Eddy SR, Elnitski L, Emes RD, Eswara P, Eyras E, Felsenfeld A, Fewell GA, Flicek P, Foley K, Frankel WN, Fulton LA, Fulton RS, Furey TS, Gage D, Gibbs RA, Glusman G, Gnerre S, Goldman N, Goodstadt L, Grafham D, Graves TA, Green ED, Gregory S, Guigó R, Guyer M, Hardison RC, Haussler D, Hayashizaki Y, Hillier LW, Hinrichs A, Hlavina W, Holzer T, Hsu F, Hua A, Hubbard T, Hunt A, Jackson I, Jaffe DB, Johnson LS, Jones M, Jones TA, Joy A, Kamal M, Karlsson EK, Karolchik D, Kasprzyk A, Kawai J, Keibler E, Kells C, Kent WJ, Kirby A, Kolbe DL, Korf I, Kucherlapati RS, Kulbokas EJ, Kulp D, Landers T, Leger JP, Leonard S, Letunic I, Levine R, Li J, Li M, Lloyd C, Lucas S, Ma B, Maglott DR, Mardis ER, Matthews L, Mauceli E, Mayer JH, McCarthy M, McCombie WR, McLaren S, McLay K, McPherson JD, Meldrim J, Meredith B, Mesirov JP, Miller W, Miner TL, Mongin E, Montgomery KT, Morgan M, Mott R, Mullikin JC, Muzny DM, Nash WE, Nelson JO, Nhan MN, Nicol R, Ning Z, Nusbaum C, O'Connor MJ, Okazaki Y, Oliver K, Overton-Larty E, Pachter L, Parra G, Pepin KH, Peterson J, Pevzner P, Plumb R, Pohl CS, Poliakov A, Ponce TC, Ponting CP, Potter S, Quail M, Reymond A, Roe BA, Roskin KM, Rubin EM, Rust AG, Santos R, Sapojnikov V, Schultz B, Schultz J, Schwartz MS, Schwartz S, Scott C, Seaman S, Searle S, Sharpe T, Sheridan A, Shownkeen R, Sims S, Singer JB, Slater G, Smit A, Smith DR, Spencer B, Stabenau A, Stange-Thomann N, Sugnet C, Suyama M, Tesler G, Thompson J, Torrents D, Trevaskis E, Tromp J, Ucla C, Ureta-Vidal A, Vinson JP, Von Niederhausern AC, Wade CM, Wall M, Weber RJ, Weiss RB, Wendl MC, West AP, Wetterstrand K, Wheeler R, Whelan S, Wierzbowski J, Willey D, Williams S, Wilson RK, Winter E, Worley KC, Wyman D, Yang S, Yang SP, Zdobnov EM, Zody MC, Lander ES (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562
8.
go back to reference Larsen F, Gundersen G, Lopez R, Prydz H (1992) CpG islands as gene markers in the human genome. Genomics 13:1095–1107CrossRefPubMed Larsen F, Gundersen G, Lopez R, Prydz H (1992) CpG islands as gene markers in the human genome. Genomics 13:1095–1107CrossRefPubMed
9.
go back to reference Zhu J, He F, Hu S, Yu J (2008) On the nature of human housekeeping genes. Trends Genet 24:481–484CrossRefPubMed Zhu J, He F, Hu S, Yu J (2008) On the nature of human housekeeping genes. Trends Genet 24:481–484CrossRefPubMed
11.
12.
go back to reference Fouse SD, Shen Y, Pellegrini M, Cole S, Meissner A, Van Neste L, Jaenisch R, Fan G (2008) Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2:160–169CrossRefPubMedPubMedCentral Fouse SD, Shen Y, Pellegrini M, Cole S, Meissner A, Van Neste L, Jaenisch R, Fan G (2008) Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2:160–169CrossRefPubMedPubMedCentral
13.
go back to reference Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789CrossRefPubMedPubMedCentral Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789CrossRefPubMedPubMedCentral
14.
go back to reference Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159CrossRefPubMed Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159CrossRefPubMed
15.
go back to reference Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323CrossRefPubMedPubMedCentral Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323CrossRefPubMedPubMedCentral
16.
go back to reference Lee JT, Bartolomei MS (2013) X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 152:1308–1323CrossRefPubMed Lee JT, Bartolomei MS (2013) X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 152:1308–1323CrossRefPubMed
17.
18.
19.
go back to reference Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, Farnham PJ, Hirst M, Lander ES, Mikkelsen TS, Thomson JA (2010) The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28:1045–1048CrossRefPubMedPubMedCentral Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, Farnham PJ, Hirst M, Lander ES, Mikkelsen TS, Thomson JA (2010) The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28:1045–1048CrossRefPubMedPubMedCentral
20.
go back to reference Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan KK, Cheng C, Mu XJ, Khurana E, Rozowsky J, Alexander R, Min R, Alves P, Abyzov A, Addleman N, Bhardwaj N, Boyle AP, Cayting P, Charos A, Chen DZ, Cheng Y, Clarke D, Eastman C, Euskirchen G, Frietze S, Fu Y, Gertz J, Grubert F, Harmanci A, Jain P, Kasowski M, Lacroute P, Leng J, Lian J, Monahan H, O'Geen H, Ouyang Z, Partridge EC, Patacsil D, Pauli F, Raha D, Ramirez L, Reddy TE, Reed B, Shi M, Slifer T, Wang J, Wu L, Yang X, Yip KY, Zilberman-Schapira G, Batzoglou S, Sidow A, Farnham PJ, Myers RM, Weissman SM, Snyder M (2012) Architecture of the human regulatory network derived from ENCODE data. Nature 489:91–100CrossRefPubMedPubMedCentral Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan KK, Cheng C, Mu XJ, Khurana E, Rozowsky J, Alexander R, Min R, Alves P, Abyzov A, Addleman N, Bhardwaj N, Boyle AP, Cayting P, Charos A, Chen DZ, Cheng Y, Clarke D, Eastman C, Euskirchen G, Frietze S, Fu Y, Gertz J, Grubert F, Harmanci A, Jain P, Kasowski M, Lacroute P, Leng J, Lian J, Monahan H, O'Geen H, Ouyang Z, Partridge EC, Patacsil D, Pauli F, Raha D, Ramirez L, Reddy TE, Reed B, Shi M, Slifer T, Wang J, Wu L, Yang X, Yip KY, Zilberman-Schapira G, Batzoglou S, Sidow A, Farnham PJ, Myers RM, Weissman SM, Snyder M (2012) Architecture of the human regulatory network derived from ENCODE data. Nature 489:91–100CrossRefPubMedPubMedCentral
21.
go back to reference Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, Zhang X, Durham T, Miri M, Deshpande V, De Jager PL, Bennett DA, Houmard JA, Muoio DM, Onder TT, Camahort R, Cowan CA, Meissner A, Epstein CB, Shoresh N, Bernstein BE (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152:642–654CrossRefPubMedPubMedCentral Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, Zhang X, Durham T, Miri M, Deshpande V, De Jager PL, Bennett DA, Houmard JA, Muoio DM, Onder TT, Camahort R, Cowan CA, Meissner A, Epstein CB, Shoresh N, Bernstein BE (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152:642–654CrossRefPubMedPubMedCentral
22.
go back to reference Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837CrossRefPubMed Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837CrossRefPubMed
23.
go back to reference Thompson RF, Fazzari MJ, Niu H, Barzilai N, Simmons RA, Greally JM (2010) Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats. J Biol Chem 285:15111–15118CrossRefPubMedPubMedCentral Thompson RF, Fazzari MJ, Niu H, Barzilai N, Simmons RA, Greally JM (2010) Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats. J Biol Chem 285:15111–15118CrossRefPubMedPubMedCentral
24.
go back to reference Matoba S, Liu Y, Lu F, Iwabuchi KA, Shen L, Inoue A, Zhang Y (2014) Embryonic Development following Somatic Cell Nuclear Transfer Impeded by Persisting Histone Methylation. Cell 159:884–895CrossRefPubMedPubMedCentral Matoba S, Liu Y, Lu F, Iwabuchi KA, Shen L, Inoue A, Zhang Y (2014) Embryonic Development following Somatic Cell Nuclear Transfer Impeded by Persisting Histone Methylation. Cell 159:884–895CrossRefPubMedPubMedCentral
25.
go back to reference Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108–112CrossRefPubMedPubMedCentral Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108–112CrossRefPubMedPubMedCentral
26.
go back to reference Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279–283CrossRefPubMedPubMedCentral Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279–283CrossRefPubMedPubMedCentral
28.
go back to reference Burney MJ, Johnston C, Wong KY, Teng SW, Beglopoulos V, Stanton LW, Williams BP, Bithell A, Buckley NJ (2013) An epigenetic signature of developmental potential in neural stem cells and early neurons. Stem Cells 31:1868–1880CrossRefPubMed Burney MJ, Johnston C, Wong KY, Teng SW, Beglopoulos V, Stanton LW, Williams BP, Bithell A, Buckley NJ (2013) An epigenetic signature of developmental potential in neural stem cells and early neurons. Stem Cells 31:1868–1880CrossRefPubMed
29.
go back to reference Foret MR, Sandstrom RS, Rhodes CT, Wang Y, Berger MS, Lin CH (2014) Molecular targets of chromatin repressive mark H3K9me3 in primate progenitor cells within adult neurogenic niches. Front Genet 5:1–11CrossRef Foret MR, Sandstrom RS, Rhodes CT, Wang Y, Berger MS, Lin CH (2014) Molecular targets of chromatin repressive mark H3K9me3 in primate progenitor cells within adult neurogenic niches. Front Genet 5:1–11CrossRef
30.
go back to reference Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP (2009) Large organized chromatin K9-modifications (LOCKs) distinguish differentiated from embryonic stem cells. Nat Genet 41:246–250CrossRefPubMedPubMedCentral Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP (2009) Large organized chromatin K9-modifications (LOCKs) distinguish differentiated from embryonic stem cells. Nat Genet 41:246–250CrossRefPubMedPubMedCentral
31.
go back to reference 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 13:580–592CrossRefPubMedPubMedCentral 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 13:580–592CrossRefPubMedPubMedCentral
32.
go back to reference Dressler GR, Patel SR (2015) Epigenetics in kidney development and renal disease. Trans Res 165:166–176CrossRef Dressler GR, Patel SR (2015) Epigenetics in kidney development and renal disease. Trans Res 165:166–176CrossRef
33.
go back to reference Patel SR, Ranghini E, Dressler GR (2014) Mechanisms of gene activation and repression by Pax proteins in the developing kidney. Pediatr Nephrol 29:589–595CrossRefPubMedPubMedCentral Patel SR, Ranghini E, Dressler GR (2014) Mechanisms of gene activation and repression by Pax proteins in the developing kidney. Pediatr Nephrol 29:589–595CrossRefPubMedPubMedCentral
34.
go back to reference Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3:169–181CrossRefPubMedPubMedCentral Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3:169–181CrossRefPubMedPubMedCentral
35.
go back to reference Park JS, Ma W, O'Brien LL, Chung E, Guo JJ, Cheng JG, Valerius MT, McMahon JA, Wong WH, McMahon AP (2012) Six2 and Wnt Regulate Self-Renewal and Commitment of Nephron Progenitors through Shared Gene Regulatory Networks. Dev Cell 23:637–651CrossRefPubMedPubMedCentral Park JS, Ma W, O'Brien LL, Chung E, Guo JJ, Cheng JG, Valerius MT, McMahon JA, Wong WH, McMahon AP (2012) Six2 and Wnt Regulate Self-Renewal and Commitment of Nephron Progenitors through Shared Gene Regulatory Networks. Dev Cell 23:637–651CrossRefPubMedPubMedCentral
36.
go back to reference 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 9:283–292CrossRefPubMed 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 9:283–292CrossRefPubMed
38.
go back to reference Xu CR, Cole PA, Meyers DJ, Kormish J, Dent S, Zaret KS (2011) Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas. Science 332:963–966CrossRefPubMedPubMedCentral Xu CR, Cole PA, Meyers DJ, Kormish J, Dent S, Zaret KS (2011) Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas. Science 332:963–966CrossRefPubMedPubMedCentral
40.
go back to reference Biron VL, McManus KJ, Hu N, Hendzel MJ, Underhill DA (2004) Distinct dynamics and distribution of histone methyl-lysine derivatives in mouse development. Dev Biol 276:337–351CrossRefPubMed Biron VL, McManus KJ, Hu N, Hendzel MJ, Underhill DA (2004) Distinct dynamics and distribution of histone methyl-lysine derivatives in mouse development. Dev Biol 276:337–351CrossRefPubMed
41.
42.
go back to reference 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 21:794–802CrossRefPubMedPubMedCentral 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 21:794–802CrossRefPubMedPubMedCentral
43.
go back to reference 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 286:32775–32789CrossRefPubMedPubMedCentral 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 286:32775–32789CrossRefPubMedPubMedCentral
44.
45.
go back to reference Chen S, Yao X, Li Y, Saifudeen Z, Bachvarov D, El-Dahr SS (2015) Histone deacetylase 1 and 2 regulate Wnt and p53 pathways in the ureteric bud epithelium. Development 142:1180–1192CrossRefPubMedPubMedCentral Chen S, Yao X, Li Y, Saifudeen Z, Bachvarov D, El-Dahr SS (2015) Histone deacetylase 1 and 2 regulate Wnt and p53 pathways in the ureteric bud epithelium. Development 142:1180–1192CrossRefPubMedPubMedCentral
46.
go back to reference Aiden AP, Rivera MN, Rheinbay E, Ku M, Coffman EJ, Truong TT, Vargas SO, Lander ES, Haber DA, Bernstein BE (2010) Wilms tumor chromatin profiles highlight stem cell properties and a renal developmental network. Cell Stem Cell 6:591–602CrossRefPubMedPubMedCentral Aiden AP, Rivera MN, Rheinbay E, Ku M, Coffman EJ, Truong TT, Vargas SO, Lander ES, Haber DA, Bernstein BE (2010) Wilms tumor chromatin profiles highlight stem cell properties and a renal developmental network. Cell Stem Cell 6:591–602CrossRefPubMedPubMedCentral
47.
go back to reference 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 16:544–550CrossRefPubMedPubMedCentral 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 16:544–550CrossRefPubMedPubMedCentral
48.
go back to reference Van Beneden K, Mannaerts I, Pauwels M, Van den Branden C, van Grunsven LA (2013) HDAC inhibitors in experimental liver and kidney fibrosis. Fibrogenesis Tissue Repair 6:1CrossRefPubMedPubMedCentral Van Beneden K, Mannaerts I, Pauwels M, Van den Branden C, van Grunsven LA (2013) HDAC inhibitors in experimental liver and kidney fibrosis. Fibrogenesis Tissue Repair 6:1CrossRefPubMedPubMedCentral
Metadata
Title
Epigenetics mechanisms in renal development
Authors
Sylvia A. Hilliard
Samir S. El-Dahr
Publication date
01-07-2016
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Nephrology / Issue 7/2016
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-015-3228-x

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