Role of DNMT3B in the regulation of early neural and neural crest specifiers

Epigenetics

Volumn 7, Issue 1, 2012, Pages 71-82

  Martins Taylor, Kristen ^a   Schroeder, Diane I ^b   Lasalle, Janine M ^b   Lalande, Marc ^a   Xu, Ren He ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Centromere instability; DNA methylation; DNMT3B; Embryonic stem cells; EZH2; Facial anomalies (ICF) syndrome; Immunodeficiency; Methylome; Neural precursors

Indexed keywords

DNA METHYLTRANSFERASE 3B;

ARTICLE; CELL MATURATION; CENTROMERE; CONTROLLED STUDY; DNA METHYLATION; EMBRYONIC STEM CELL; FACE MALFORMATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; MILD COGNITIVE IMPAIRMENT; MISSENSE MUTATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEUROEPITHELIUM; RNA INTERFERENCE;

EID: 84930486044     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.7.1.18750     Document Type: Article

References (62)

1. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16:6-21; PMID:11782440; http://dx.doi.org/10.1101/gad.947102.
2. Ooi SK, O'Donnell AH, Bestor TH. Mammalian cytosine methylation at a glance. J Cell Sci 2009; 122:2787-91; PMID:19657014; http://dx.doi.org/10.1242/jcs.015123.
3. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462:315-22; PMID:19829295; http://dx.doi.org/10.1038/nature08514.
4. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G, et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011; 471:68-73; PMID:21289626; http://dx.doi.org/10.1038/nature09798.
5. Schroeder DI, Lott P, Korf I, Lasalle JM. Large-scale methylation domains mark a functional subset of neuronally expressed genes. Genome Res 2011; 21:1583-91; PMID:21784875; http://dx.doi.org/10.1101/gr.119131.110.
6. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005; 74:481-514; PMID:15952895; http://dx.doi.org/10.1146/annurev.biochem.74.010904.153721.
7. Chedin F, Lieber MR, Hsieh CL. The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a. Proc Natl Acad Sci USA 2002; 99:16916-21; PMID:12481029; http://dx.doi.org/10.1073/pnas.262443999.
8. Suetake I, Shinozaki F, Miyagawa J, Takeshima H, Tajima S. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J Biol Chem 2004; 279:27816-23; PMID:15105426; http://dx.doi.org/10.1074/jbc.M400181200.
9. Margot JB, Ehrenhofer-Murray AE, Leonhardt H. Interactions within the mammalian DNA methyltransferase family. BMC Mol Biol 2003; 4:7; PMID:12777184; http://dx.doi.org/10.1186/1471-2199-4-7.
10. Chen ZX, Mann JR, Hsieh CL, Riggs AD, Chedin F. Physical and functional interactions between the human DNMT3L protein and members of the de novo methyltransferase family. J Cell Biochem 2005; 95:902-17; PMID:15861382; http://dx.doi.org/10.1002/jcb.20447.
11. Xie ZH, Huang YN, Chen ZX, Riggs AD, Ding JP, Gowher H, et al. Mutations in DNA methyltransferase DNMT3B in ICF syndrome affect its regulation by DNMT3L. Hum Mol Genet 2006; 15:1375-85; PMID:16543361; http://dx.doi.org/10.1093/hmg/ddl059.
12. Kareta MS, Botello ZM, Ennis JJ, Chou C, Chedin F. Reconstitution and mechanism of the stimulation of de novo methylation by human DNMT3L. J Biol Chem 2006; 281:25893-902; PMID:16829525; http://dx.doi.org/10.1074/jbc.M603140200.
13. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 2007; 449:248-51; PMID:17713477; http://dx.doi.org/10.1038/nature06146.
14. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007; 448:714-7; PMID:17687327; http://dx.doi.org/10.1038/nature05987.
15. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99:247-57; PMID:10555141; http://dx.doi.org/10.1016/S0092-8674(00)81656-6.
16. Chen T, Ueda Y, Dodge JE, Wang Z, Li E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol Cell Biol 2003; 23:5594-605; PMID:12897133; http://dx.doi.org/10.1128/MCB.23.16.5594-605.2003.
17. Watanabe D, Suetake I, Tada T, Tajima S. Stage- and cell-specific expression of Dnmt3a and Dnmt3b during embryogenesis. Mech Dev 2002; 118:187-90; PMID:12351185; http://dx.doi.org/10.1016/S0925-4773(02)00242-3.
18. Watanabe D, Suetake I, Tajima S, Hanaoka K. Expression of Dnmt3b in mouse hematopoietic progenitor cells and spermatogonia at specific stages. Gene Expr Patterns 2004; 5:43-9; PMID:15533817; http://dx.doi.org/10.1016/j.modgep.2004.06.008.
19. Feng J, Chang H, Li E, Fan G. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J Neurosci Res 2005; 79:734-46; PMID:15672446; http://dx.doi.org/10.1002/jnr.20404.
20. Watanabe D, Uchiyama K, Hanaoka K. Transition of mouse de novo methyltransferases expression from Dnmt3b to Dnmt3a during neural progenitor cell development. Neuroscience 2006; 142:727-37; PMID:16973295; http://dx.doi.org/10.1016/j.neuroscience.2006.07.053.
21. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 1999; 402:187-91; PMID:10647011; http://dx.doi.org/10.1038/46214.
22. Hansen RS, Wijmenga C, Luo P, Stanek AM, Canfield TK, Weemaes CM, et al. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc Natl Acad Sci USA 1999; 96:14412-7; PMID:10588719; http://dx.doi.org/10.1073/pnas.96.25.14412.
23. Robertson KD. DNA methylation, methyltransferases and cancer. Oncogene 2001; 20:3139-55; PMID:11420731; http://dx.doi.org/10.1038/sj.onc.1204341.
24. Ji W, Hernandez R, Zhang XY, Qu GZ, Frady A, Varela M, et al. DNA demethylation and pericentromeric rearrangements of chromosome 1. Mutat Res 1997; 379:33-41; PMID:9330620; http://dx.doi.org/10.1016/S0027-5107(97)00088-2.
25. Jeanpierre M, Turleau C, Aurias A, Prieur M, Ledeist F, Fischer A, et al. An embryonic-like methylation pattern of classical satellite DNA is observed in ICF syndrome. Hum Mol Genet 1993; 2:731-5; PMID:8102570; http://dx.doi.org/10.1093/hmg/2.6.731.
26. Tagarro I, Fernandez-Peralta AM, Gonzalez-Aguilera JJ. Chromosomal localization of human satellites 2 and 3 by a FISH method using oligonucleotides as probes. Hum Genet 1994; 93:383-8; PMID:8168808; http://dx.doi.org/10.1007/BF00201662.
27. Tuck-Muller CM, Narayan A, Tsien F, Smeets DF, Sawyer J, Fiala ES, et al. DNA hypomethylation and unusual chromosome instability in cell lines from ICF syndrome patients. Cytogenet Cell Genet 2000; 89:121-8; PMID:10894953; http://dx.doi.org/10.1159/000015590.
28. Hassan KM, Norwood T, Gimelli G, Gartler SM, Hansen RS. Satellite 2 methylation patterns in normal and ICF syndrome cells and association of hypomethylation with advanced replication. Hum Genet 2001; 109:452-62; PMID:11702227; http://dx.doi.org/10.1007/s004390100590.
29. Schuffenhauer S, Bartsch O, Stumm M, Buchholz T, Petropoulou T, Kraft S, et al. DNA, FISH and complementation studies in ICF syndrome: DNA hypomethylation of repetitive and single copy loci and evidence for a trans acting factor. Hum Genet 1995; 96:562-71; PMID:8530004; http://dx.doi.org/10.1007/BF00197412.
30. Kondo T, Bobek MP, Kuick R, Lamb B, Zhu X, Narayan A, et al. Whole-genome methylation scan in ICF syndrome: hypomethylation of non-satellite DNA repeats D4Z4 and NBL2. Hum Mol Genet 2000; 9:597-604; PMID:10699183; http://dx.doi.org/10.1093/hmg/9.4.597.
31. Miniou P, Jeanpierre M, Blanquet V, Sibella V, Bonneau D, Herbelin C, et al. Abnormal methylation pattern in constitutive and facultative (X inactive chromosome) heterochromatin of ICF patients. Hum Mol Genet 1994; 3:2093-102; PMID:7881405; http://dx.doi.org/10.1093/hmg/3.12.2093.
32. Bourc'his D, Miniou P, Jeanpierre M, Molina Gomes D, Dupont J, De Saint-Basile G, et al. Abnormal methylation does not prevent X inactivation in ICF patients. Cytogenet Cell Genet 1999; 84:245-52; PMID:10393442; http://dx.doi.org/10.1159/000015269.
33. Tao Q, Huang H, Geiman TM, Lim CY, Fu L, Qiu GH, et al. Defective de novo methylation of viral and cellular DNA sequences in ICF syndrome cells. Hum Mol Genet 2002; 11:2091-102; PMID:12189161; http://dx.doi.org/10.1093/hmg/11.18.2091.
34. Hansen RS. X inactivation-specific methylation of LINE-1 elements by DNMT3B: implications for the Lyon repeat hypothesis. Hum Mol Genet 2003; 12:2559-67; PMID:12925568; http://dx.doi.org/10.1093/hmg/ddg268.
35. Matarazzo MR, De Bonis ML, Gregory RI, Vacca M, Hansen RS, Mercadante G, et al. Allelic inactivation of the pseudoautosomal gene SYBL1 is controlled by epigenetic mechanisms common to the X and Y chromosomes. Hum Mol Genet 2002; 11:3191-8; PMID:12444103; http://dx.doi.org/10.1093/hmg/11.25.3191.
36. Sowinska A, Jagodzinski PP. RNA interference-mediated knockdown of DNMT1 and DNMT3B induces CXCL12 expression in MCF-7 breast cancer and AsPC1 pancreatic carcinoma cell lines. Cancer Lett 2007; 255:153-9; PMID:17532557; http://dx.doi.org/10.1016/j.canlet.2007.04.004.
37. Yeo S, Jeong S, Kim J, Han JS, Han YM, Kang YK. Characterization of DNA methylation change in stem cell marker genes during differentiation of human embryonic stem cells. Biochem Biophys Res Commun 2007; 359:536-42; PMID:17548060; http://dx.doi.org/10.1016/j.bbrc.2007.05.120.
38. Reubinoff BE, Itsykson P, Turetsky T, Pera MF, Reinhartz E, Itzik A, et al. Neural progenitors from human embryonic stem cells. Nat Biotechnol 2001; 19:1134-40; PMID:11731782; http://dx.doi.org/10.1038/nbt1201-134.
39. Hagleitner MM, Lankester A, Maraschio P, Hulten M, Fryns JP, Schuetz C, et al. Clinical spectrum of immunodeficiency, centromeric instability and facial dysmorphism (ICF syndrome). J Med Genet 2008; 45:93-9; PMID:17893117; http://dx.doi.org/10.1136/jmg.2007.053397.
40. Li XJ, Du ZW, Zarnowska ED, Pankratz M, Hansen LO, Pearce RA, et al. Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 2005; 23:215-21; PMID:15685164; http://dx.doi.org/10.1038/nbt1063.
41. Pankratz MT, Li XJ, Lavaute TM, Lyons EA, Chen X, Zhang SC. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 2007; 25:1511-20; PMID:17332508; http://dx.doi.org/10.1634/stemcells.2006-0707.
42. Li XJ, Zhang SC. In vitro differentiation of neural precursors from human embryonic stem cells. Methods Mol Biol 2006; 331:169-77; PMID:16881517.
43. Zhang X, Huang CT, Chen J, Pankratz MT, Xi J, Li J, et al. Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 2010; 7:90-100; PMID:20621053; http://dx.doi.org/10.1016/j.stem.2010.04.017.
44. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009; 27:275-80; PMID:19252484; http://dx.doi.org/10.1038/nbt.1529.
45. Zeng H, Guo M, Martins-Taylor K, Wang X, Zhang Z, Park JW, et al. Specification of region-specific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS ONE 2010; 5:11853; PMID:20686615; http://dx.doi.org/10.1371/journal.pone.0011853.
46. Martinez-Barbera JP, Beddington RS. Getting your head around Hex and Hesx1: forebrain formation in mouse. Int J Dev Biol 2001; 45:327-36; PMID:11291863.
47. Roybon L, Hjalt T, Stott S, Guillemot F, Li JY, Brundin P. Neurogenin2 directs granule neuroblast production and amplification while NeuroD1 specifies neuronal fate during hippocampal neurogenesis. PLoS ONE 2009; 4:4779; PMID:19274100; http://dx.doi.org/10.1371/journal.pone.0004779.
48. Boutin C, Hardt O, de Chevigny A, Core N, Goebbels S, Seidenfaden R, et al. NeuroD1 induces terminal neuronal differentiation in olfactory neurogenesis. Proc Natl Acad Sci USA 2010; 107:1201-6; PMID:20080708; http://dx.doi.org/10.1073/pnas.0909015107.
49. Gao Z, Ure K, Ables JL, Lagace DC, Nave KA, Goebbels S, et al. Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci 2009; 12:1090-2; PMID:19701197; http://dx.doi.org/10.1038/nn.2385.
50. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, Lie DC, et al. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci 2009; 12:1097-105; PMID:19701198; http://dx.doi.org/10.1038/nn.2360.
51. Lee G, Kim H, Elkabetz Y, Al Shamy G, Panagiotakos G, Barberi T, et al. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 2007; 25:1468-75; PMID:18037878; http://dx.doi.org/10.1038/nbt1365.
52. Sauka-Spengler T, Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 2008; 9:557-68; PMID:18523435; http://dx.doi.org/10.1038/nrm2428.
53. Martins-Taylor K, Nisler BS, Taapken SM, Compton T, Crandall L, Montgomery KD, et al. Recurrent copy number variations in human induced pluripotent stem cells. Nat Biotechnol 2011; 29:488-91; PMID:21654665; http://dx.doi.org/10.1038/nbt.1890.
54. Jin B, Tao Q, Peng J, Soo HM, Wu W, Ying J, et al. DNA methyltransferase 3B (DNMT3B) mutations in ICF syndrome lead to altered epigenetic modifications and aberrant expression of genes regulating development, neurogenesis and immune function. Hum Mol Genet 2008; 17:690-709; PMID:18029387; http://dx.doi.org/10.1093/hmg/ddm341.
55. Fisher CL, Fisher AG. Chromatin states in pluripotent, differentiated and reprogrammed cells. Curr Opin Genet Dev 2011; 21:140-6; PMID:21316216; http://dx.doi.org/10.1016/j.gde.2011.01.015.
56. Chamberlain SJ, Chen PF, Ng KY, Bourgois-Rocha F, Lemtiri-Chlieh F, Levine ES, et al. Induced pluripotent stem cell models of the genomic imprinting disorders Angelman and Prader-Willi syndromes. Proc Natl Acad Sci USA 2010; 107:17668-73; PMID:20876107; http://dx.doi.org/10.1073/pnas.1004487107.
57. Wang L, Menendez P, Shojaei F, Li L, Mazurier F, Dick JE, et al. Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med 2005; 201:1603-14; PMID:15883170; http://dx.doi.org/10.1084/jem.20041888.
58. Unger C, Karner E, Treschow A, Stellan B, Felldin U, Concha H, et al. Lentiviral-mediated HoxB4 expression in human embryonic stem cells initiates early hematopoiesis in a dose-dependent manner but does not promote myeloid differentiation. Stem Cells 2008; 26:2455-66; PMID:18617691; http://dx.doi.org/10.1634/stemcells.2007-0876.
59. Jefferson A, Colella S, Moralli D, Wilson N, Yusuf M, Gimelli G, et al. Altered intra-nuclear organisation of heterochromatin and genes in ICF syndrome. PLoS ONE 2010; 5:11364; PMID:20613881; http://dx.doi.org/10.1371/journal.pone.0011364.
60. Wang X, Lin G, Martins-Taylor K, Zeng H, Xu RH. Inhibition of caspase-mediated anoikis is critical for bFGF-sustained culture of human pluripotent stem cells. J Biol Chem 2009; 16:16.
61. Gatto S, Della Ragione F, Cimmino A, Strazzullo M, Fabbri M, Mutarelli M, et al. Epigenetic alteration of microRNAs in DNMT3B-mutated patients of ICF syndrome. Epigenetics 2010; 5:427-43; PMID:20448464; http://dx.doi.org/10.4161/epi.5.5.11999.
62. Chen PY, Cokus SJ, Pellegrini MBS. Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 2010; 11:203; PMID:20416082; http://dx.doi.org/10.1186/1471-2105-11-203.