Haploinsufficiency of the paternal-effect gene Dnmt3L results in transient DNA hypomethylation in progenitor cells of the male germline

Human Reproduction

Volumn 28, Issue 2, 2013, Pages 519-530

  Niles, K M ^a,b   Yeh, J R ^a,c   Chan, D ^a,b   Landry, M ^b   Nagano, M C ^a,c   Trasler, J M ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MONTREAL CHILDREN S HOSPITAL   (Canada)

^c ROYAL VICTORIA HOSPITAL   (Canada)

Author keywords

DNA methylation; Dnmt3L; epigenetics; paternal effect; spermatogonial stem cells

Indexed keywords

DNA METHYLTRANSFERASE 1; DNMT3L PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CHROMOSOME 9; CONTROLLED STUDY; CPG ISLAND; CROSS-SECTIONAL STUDY; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; GENE; GENE LOCUS; GENOME; GENOTYPE; GERM CELL; HAPLOINSUFFICIENCY; HETEROZYGOTE; MALE; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPERMATOGONIUM; X CHROMOSOME;

EID: 84872529915     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/des395     Document Type: Article

References (59)

1. Allegrucci C, Wu YZ, Thurston A, Denning CN, Priddle H, Mummery CL, Ward-van Oostwaard D, Andrews PW, Stojkovic M, Smith N et al. Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Hum Mol Genet 2007;16: 1253-1268.
2. Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004; 431: 96-99.
3. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC, Beisel C, Schubeler D, Stadler MB, Peters AH. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 2010;17: 679-687.
4. 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: 16916-16921.
5. Chong S, Vickaryous N, Ashe A, Zamudio N, Youngson N, Hemley S, Stopka T, Skoultchi A, Matthews J, Scott HS et al. Modifiers of epigenetic reprogramming show paternal effects in the mouse. Nat Genet 2007;39: 614-622.
6. Delaval K, Govin J, Cerqueira F, Rousseaux S, Khochbin S, Feil R. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J 2007;26: 720-729.
7. Dindot SV, Person R, Strivens M, Garcia R, Beaudet AL. Epigenetic profiling at mouse imprinted gene clusters reveals novel epigenetic and genetic features at differentially methylated regions. Genome Res 2009;19: 1374-1383.
8. Ebata KT, Zhang X, Nagano MC. Expression patterns of cell-surface molecules on male germ line stem cells during postnatal mouse development. Mol Reprod Dev 2005;72: 171-181.
9. Ebata KT, Yeh JR, Zhang X, Nagano MC. Soluble growth factors stimulate spermatogonial stem cell divisions that maintain a stem cell pool and produce progenitors in vitro. Exp Cell Res 2011;317: 1319-1329.
10. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, Burton J, Cox TV, Davies R, Down TA et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 2006;38: 1378-1385.
11. Fournier C, Goto Y, Ballestar E, Delaval K, Hever AM, Esteller M, Feil R. Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes. EMBO J 2002;21: 6560-6570.
12. Galetzka D, Weis E, Tralau T, Seidmann L, Haaf T. Sex-specific windows for high mRNA expression of DNA methyltransferases 1 and 3A and methyl-CpG-binding domain proteins 2 and 4 in human fetal gonads. Mol Reprod Dev 2007;74: 233-241.
13. Godmann M, Auger V, Ferraroni-Aguiar V, Di Sauro A, Sette C, Behr R, Kimmins S. Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis. Biol Reprod 2007;77: 754-764.
14. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005;74: 481-514.
15. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009;460: 473-478.
16. Hata K, Kusumi M, Yokomine T, Li E, Sasaki H. Meiotic and epigenetic aberrations in Dnmt3L-deficient male germ cells. Mol Reprod Dev 2006;73: 116-122.
17. Hayashi K, Yoshida K, Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 2005; 438: 374-378.
18. Henckel A, Nakabayashi K, Sanz LA, Feil R, Hata K, Arnaud P. Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum Mol Genet 2009; 18: 3375-3383.
19. Hu YG, Hirasawa R, Hu JL, Hata K, Li CL, Jin Y, Chen T, Li E, Rigolet M, Viegas-Pequignot E et al. Regulation of DNA methylation activity through Dnmt3L promoter methylation by Dnmt3 enzymes in embryonic development. Hum Mol Genet 2008;17: 2654-2664.
20. Hu JL, Zhou BO, Zhang RR, Zhang KL, Zhou JQ, Xu GL. The N-terminus of histone H3 is required for de novo DNA methylation in chromatin. Proc Natl Acad Sci USA 2009;106: 22187-22192.
21. Huang JX, Scott MB, Pu XY, Zhou-Cun A. Association between single-nucleotide polymorphisms of DNMT3L and infertility with azoospermia in Chinese men. Reprod Biomed Online 2012;24: 66-71.
22. 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: 248-251.
23. Kanatsu-Shinohara M, Ogonuki N, Iwano T, Lee J, Kazuki Y, Inoue K, Miki H, Takehashi M, Toyokuni S, Shinkai Y et al. Genetic and epigenetic properties of mouse male germline stem cells during long-term culture. Development 2005;132: 4155-4163.
24. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004;429: 900-903.
25. Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y, Okano M, Li E, Nozaki M, Sasaki H. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet 2007;16: 2272-2280.
26. Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, Sasaki H, Yaegashi N, Arima T. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 2007;16: 2542-2551.
27. Kobayashi H, Hiura H, John RM, Sato A, Otsu E, Kobayashi N, Suzuki R, Suzuki F, Hayashi C, Utsunomiya T et al. DNA methylation errors at imprinted loci after assisted conception originate in the parental sperm. Eur J Hum Genet 2009;17: 1582-1591.
28. Kubota H, Brinster RL. Culture of rodent spermatogonial stem cells, male germline stem cells of the postnatal animal. Methods Cell Biol 2008; 86: 59-84.
29. Kubota H, Avarbock MR, Brinster RL. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 2004a;71: 722-731.
30. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 2004b;101: 16489-16494.
31. Kumaki Y, Oda M, Okano M. QUMA: quantification tool for methylation analysis. Nucleic Acids Res 2008;36: W170-W175.
32. La Salle S, Oakes CC, Neaga OR, Bourc'his D, Bestor TH, Trasler JM. Loss of spermatogonia and wide-spread DNA methylation defects in newborn male mice deficient in DNMT3L. BMC Dev Biol 2007; 7: 104-121.
33. Lee J, Kanatsu-Shinohara M, Ogonuki N, Miki H, Inoue K, Morimoto T, Morimoto H, Ogura A, Shinohara T. Heritable imprinting defect caused by epigenetic abnormalities in mouse spermatogonial stem cells. Biol Reprod 2009;80: 518-527.
34. Lee DH, Singh P, Tsai SY, Oates N, Spalla A, Spalla C, Brown L, Rivas G, Larson G, Rauch TA et al. CTCF-dependent chromatin bias constitutes transient epigenetic memory of the mother at the H19-Igf2 imprinting control region in prospermatogonia. PLoS Genet 2010;6: e1001224.
35. Marques CJ, Francisco T, Sousa S, Carvalho F, Barros A, Sousa M. Methylation defects of imprinted genes in human testicular spermatozoa. Fertil Steril 2009;94: 585-594.
36. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008;454: 766-770.
37. Nagano M. Spermatogonial transplantation. In: Gardner DK, Lane MWA (eds). A Laboratory Guide to the Mammalian Embryo. Oxford: Oxford University Press, 2004,334-351.
38. Niles KM, Chan D, La Salle S, Oakes CC, Trasler JM. Critical period of nonpromoter DNA methylation acquisition during prenatal male germ cell development. PLoS One 2011;6: e24156.
39. Oakes CC, La Salle S, Robaire B, Trasler JM. Evaluation of a quantitative DNA methylation analysis technique using methylation-sensitive/dependent restriction enzymes and real-time PCR. Epigenetics 2006; 1: 146-152.
40. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci USA 2007a;104: 228-233.
41. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol 2007b;307: 368-379.
42. Oakes CC, La Salle S, Trasler JM, Robaire B. Restriction digestion and real-time PCR (qAMP). Methods Mol Biol 2009;507: 271-280.
43. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 2008;24: 263-286.
44. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 2006;103: 9524-9529.
45. O'Doherty AM, Rutledge CE, Sato S, Thakur A, Lees-Murdock DJ, Hata K, Walsh CP. DNA methylation plays an important role in promoter choice and protein production at the mouse Dnmt3L locus. Dev Biol 2011;356: 411-420.
46. Ogawa T, Arechaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 1997;41: 111-122.
47. Okazaki Y, Okuizumi H, Sasaki N, Ohsumi T, Kuromitsu J, Hirota N, Muramatsu M, Hayashizaki Y. An expanded system of restriction landmark genomic scanning (RLGS Ver. 1.8). Electrophoresis 1995; 16: 197-202.
48. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007; 448: 714-717.
49. Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M, Shirakawa M. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep 2009;10: 1235-1241.
50. Ryu BY, Kubota H, Avarbock MR, Brinster RL. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci USA 2005;102: 14302-14307.
51. Suetake I, Morimoto Y, Fuchikami T, Abe K, Tajima S. Stimulation effect of Dnmt3L on the DNA methylation activity of Dnmt3a2. J Biochem (Tokyo) 2006;140: 553-559.
52. Vu TH, Li T, Hoffman AR. Promoter-restricted histone code, not the differentially methylated DNA regions or antisense transcripts, marks the imprinting status of IGF2R in human and mouse. Hum Mol Genet 2004;13: 2233-2245.
53. Webster KE, O'Bryan MK, Fletcher S, Crewther PE, Aapola U, Craig J, Harrison DK, Aung H, Phutikanit N, Lyle R et al. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci USA 2005;102: 4068-4073.
54. Yeh JR, Zhang X, Nagano MC. Establishment of a short-term in vitro assay for mouse spermatogonial stem cells. Biol Reprod 2007;77: 897-904.
55. Yeh JR, Zhang X, Nagano MC. Wnt5a is a cell-extrinsic factor that supports self-renewal of mouse spermatogonial stem cells. J Cell Sci 2011;124: 2357-2366.
56. Yeh JR, Zhang X, Nagano MC. Indirect effects of Wnt3a/beta-catenin signalling support mouse spermatogonial stem cells in vitro. PLoS One 2012;7: e40002.
57. Yoshimizu T, Sugiyama N, De Felice M, Yeom YI, Ohbo K, Masuko K, Obinata M, Abe K, Scholer HR, Matsui Y. Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev Growth Differ 1999;41: 675-684.
58. Zamudio NM, Scott HS, Wolski K, Lo CY, Law C, Leong D, Kinkel SA, Chong S, Jolley D, Smyth GK et al. DNMT3L is a regulator of X chromosome compaction and post-meiotic gene transcription. PLoS One 2011;6: e18276.
59. Zhang Y, Jurkowska R, Soeroes S, Rajavelu A, Dhayalan A, Bock I, Rathert P, Brandt O, Reinhardt R, Fischle W et al. Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res 2010;38: 4246-4253.