H3K9 Trimethylation Precedes DNA Methylation during Sheep Oogenesis: HDAC1, SUV39H1, G9a, HP1, and Dnmts Are Involved in These Epigenetic Events

Journal of Histochemistry and Cytochemistry

Volumn 61, Issue 1, 2013, Pages 75-89

  Russo, Valentina ^a   Bernabò, Nicola ^a   Di Giacinto, Oriana ^a   Martelli, Alessandra ^a   Mauro, Annunziata ^a   Berardinelli, Paolo ^a   Curini, Valentina ^a   Nardinocchi, Delia ^a   Mattioli, Mauro ^a   Barboni, Barbara ^a  

^a UNIVERSITY OF TERAMO   (Italy)

Author keywords

biological networks; Dnmt3a; G9a; global DNA methylation; H3K9me3; HDAC1; HP1; oogenesis; sheep; SUV39H1

Indexed keywords

DNMT3A ENZYME; ENZYME; G9A ENZYME; HISTONE DEACETYLASE 1; HP1 ENZYME; SUV39H1 ENZYME; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; LYSINE; NONHISTONE PROTEIN;

ANIMAL TISSUE; ARTICLE; DNA METHYLATION; EPIGENETICS; FLUORESCENCE IMAGING; GENE SILENCING; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; METHYLATION; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEEP; TRIMETHYLATION; ANIMAL; COMPUTER SIMULATION; GENETIC EPIGENESIS; METABOLISM;

OVIS ARIES;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; COMPUTER SIMULATION; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONE DEACETYLASE 1; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; IMMUNOHISTOCHEMISTRY; LYSINE; METHYLATION; OOGENESIS; SHEEP;

EID: 84874547365     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412463923     Document Type: Article

References (64)

1. Albert R.Scale-free networks in cell biology.J Cell Sci. 2005;118:4947-4957.
2. Arney KL,Erhardt S,Drewell RA,Surani MA.Epigenetic reprogramming of the genome-from the germ line to the embryo and back again.Int J Dev Biol. 2001;45 (3): 533-540.
3. Bannister AJ,Zegerman P,Partridge JF,Miska EA,Thomas JO,Allshire RC,Kouzarides T.Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain.Nature. 2001;410 (6824): 120-124.
4. Barboni B,Russo V,Cecconi S,Curini V,Colosimo A,Garofalo ML,Capacchietti G,Di Giacinto O,Mattioli M.In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation.PLoS One. 2011;6 (11): e27550.
5. Bártová E,Krejcí J,Harnicarová A,Galiová G,Kozubek S.Histone modifications and nuclear architecture: a review.J Histochem Cytochem. 2008;56 (8): 711-721.
6. Bestor TH.Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain.EMBO J. 1992;11:2611-2617.
7. Bestor TH.The DNA methyltransferases of mammals.Hum Mol Genet. 2000;9 (16): 2395-2402.
8. Bollobás BNew York: Springer Verlag; 1979:.
9. Bouniol-Baly C,Hamraoui L,Guibert J,Beaujean N,Szollosi MS,Debey P.Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes.Biol Reprod. 1999;60 (3): 580-587.
10. Cecconi S,Barboni B,Coccia M,Mattioli M.In vitro development of sheep preantral follicles.Biol Reprod. 1999;60 (3): 594-601.
11. Cheng X,Blumenthal RM.Coordinated chromatin control: structural and functional linkage of DNA and histone methylation.Biochemistry. 2010;49 (14): 2999-3008.
12. Colosimo A,Di Rocco G,Curini V,Russo V,Capacchietti G,Berardinelli P,Mattioli M,Barboni B.Characterization of the methylation status of five imprinted genes in sheep gametes.Anim Genet. 2009;40 (6): 900-908.
13. De La Fuente R.Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes.Dev Biol. 2006;292 (1): 1-12.
14. De La Fuente R,Viveiros MM,Burns KH,Adashi EY,Matzuk MM,Eppig JJ.Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function.Dev Biol. 2004;275 (2): 447-458.
15. Dean W,Lucifero D,Santos F.DNA methylation in mammalian development and disease.Birth Defects Res C Embryo Today. 2005;75 (2): 98-111.
16. Espada J,Ballestar E,Fraga MF,Villar-Garea A,Juarranz A,Stockert JC,Robertson KD,Fuks F,Esteller M.Human DNA methyltransferase 1 is required for maintenance of the histone H3 modification pattern.J Biol Chem. 2004;279 (35): 37175-37184.
17. Estève PO,Chin HG,Smallwood A,Feehery GR,Gangisetty O,Karpf AR,Carey MF,Pradhan S.Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication.Genes Dev. 2006;20 (22): 3089-3103.
18. Fuks F.DNA methylation and histone modifications: teaming up to silence genes.Curr Opin Genet Dev. 2005;15 (5): 490-495.
19. Gu L,Wang Q,Sun QY.Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions.Cell Cycle. 2010;9 (10): 1942-1950.
20. He XJ,Chen T,Zhu JK.Regulation and function of DNA methylation in plants and animals.Cell Res. 2011 2011;21 (3): 442-465.
21. Hiura H,Obata Y,Komiyama J,Shirai M,Kono T.Oocyte growth-dependent progression of maternal imprinting in mice.Genes Cells. 2006;11 (4): 353-361.
22. Hou J,Liu L,Zhang J,Cui XH,Yan FX,Guan H,Chen YF,An XR.Epigenetic modification of histone 3 at lysine 9 in sheep zygotes and its relationship with DNA methylation.BMC Dev Biol. 2008;8:60.
23. Huang J,Li T,Ding CH,Brosens J,Zhou CQ,Wang HH,Xu YW.Insufficient histone-3 lysine-9 deacetylation in human oocytes matured in vitro is associated with aberrant meiosis.Fertil Steril. 2012;97 (1): 178-184.e3.
24. Jones PA,Baylin SB.The fundamental role of epigenetic events in cancer.Nat Rev Genet. 2002;3 (6): 415-428.
25. Kageyama S,Liu H,Kaneko N,Ooga M,Nagata M,Aoki F.Alterations in epigenetic modifications during oocyte growth in mice.Reproduction. 2007;133 (1): 85-94.
26. 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 (6994): 900-903.
27. Kono T.Influence of epigenetic changes during oocyte growth on nuclear reprogramming after nuclear transfer.Reprod Fertil Dev. 1998;10 (7-8): 593-598.
28. Lachner M,O'Carroll D,Rea S,Mechtler K,Jenuwein T.Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins.Nature. 2001;410 (6824): 116-120.
29. Lehnertz B,Ueda Y,Derijck AA,Braunschweig U,Perez-Burgos L,Kubicek S,Chen T,Li E,Jenuwein T,Peters AH.Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin.Curr Biol. 2003;13 (14): 1192-1200.
30. Li E.Chromatin modification and epigenetic reprogramming in mammalian development.Nat Rev Genet. 2002;3 (9): 662-673.
31. Lodde V,Modina S,Galbusera C,Franciosi F,Luciano AM.Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence.Mol Reprod Dev. 2007;74 (6): 740-749.
32. Lucifero D,Mann MR,Bartolomei MS,Trasler JM.Gene-specific timing and epigenetic memory in oocyte imprinting.Hum Mol Genet. 2004;13 (8): 839-849.
33. Mager J,Bartolomei MS.Strategies for dissecting epigenetic mechanisms in the mouse.Nat Genet. 2005;37 (11): 1194-1200.
34. Mattioli M,Barboni B,Turriani M,Galeati G,Zannoni A,Castellani G,Berardinelli P,Scapolo PA.Follicle activation involves vascular endothelial growth factor production and increased blood vessel extension.Biol Reprod. 2001;65 (4): 1014-1019.
35. Mattson BA,Albertini DF.Oogenesis: chromatin and microtubule dynamics during meiotic prophase.Mol Reprod Dev. 1990;25 (4): 374-383.
36. Milutinovic S,D'Alessio AC,Detich N,Szyf M.Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes.Carcinogenesis. 2007;28 (3): 560-571.
37. Morgan HD,Santos F,Green K,Dean W,Reik W.Epigenetic reprogramming in mammals.Hum Mol Genet. 2005;14 (Spec No. 1): R47-R58.
38. Munari F,Soeroes S,Zenn HM,Schomburg A,Kost N,Schroeder S,Klingberg R,Rezaei-Ghaleh N,Stuetzer A,Gelato KA, et al.Methylation of K9 in histone H3 directs alternative modes of highly dynamic interaction of heterochromatin protein hHP1β with the nucleosome.J Biol Chem. 2012;287 (40): 33746-33765.
39. Nagase H,Ghosh S.Epigenetics: differential DNA methylation in mammalian somatic tissues.FEBS J. 2008;275 (8): 1617-1623.
40. Nowak-Imialek M,Wrenzycki C,Herrmann D,Lucas-Hahn A,Lagutina I,Lemme E,Lazzari G,Galli C,Niemann H.Messenger RNA expression patterns of histone-associated genes in bovine preimplantation embryos derived from different origins.Mol Reprod Dev. 2008;75 (5): 731-743.
41. Ogawa H,Ishiguro K,Gaubatz S,Livingston DM,Nakatani Y.A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells.Science. 2002;296:1132-1136.
42. Okano M,Bell DW,Haber DA,Li E.DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development.Cell. 1999;99:247-257.
43. Ou JN,Torrisani J,Unterberger A,Provençal N,Shikimi K,Karimi M,Ekström TJ,Szyf M.Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines.Biochem Pharmacol. 2007;73 (9): 1297-1307.
44. Prokhortchouk A,Hendrich B,Jørgensen H,Ruzov A,Wilm M,Georgiev G,Bird A,Prokhortchouk E.The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor.Genes Dev. 2001;15 (13): 1613-1618.
45. Racedo SE,Wrenzycki C,Lepikhov K,Salamone D,Walter J,Niemann H.Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation.Reprod Fertil Dev. 2009;21 (6): 738-748.
46. Raynal NJ,Si J,Taby RF,Gharibyan V,Ahmed S,Jelinek J,Estécio MR,Issa JP.DNA methylation does not stably lock gene expression but instead serves as a molecular mark for gene silencing memory.Cancer Res. 2012;72 (5): 1170-1181.
47. Rea S,Eisenhaber F,O'Carroll D,Strahl BD,Sun ZW,Schmid M,Opravil S,Mechtler K,Ponting CP,Allis CD, et al.Regulation of chromatin structure by site-specific histone H3 methyltransferases.Nature. 2000;406 (6796): 593-599.
48. Riccio A,Aaltonen LA,Godwin AK,Loukola A,Percesepe A,Salovaara R,Masciullo V,Genuardi M,Paravatou-Petsotas M,Bassi DE, et al.The DNA repair gene MBD4 (MED1) is mutated in human carcinomas with microsatellite instability.Nat Genet. 1999;23 (3): 266-268.
49. Russo V,Berardinelli P,Martelli A,Di Giacinto O,Nardinocchi D,Fantasia D,Barboni B.Expression of telomerase reverse transcriptase subunit (TERT) and telomere sizing in pig ovarian follicles.J Histochem Cytochem. 2006;54 (4): 443-455.
50. Russo V,Martelli A,Berardinelli P,Di Giacinto O,Bernabò N,Fantasia D,Mattioli M,Barboni B.Modifications in chromatin morphology and organization during sheep oogenesis.Microsc Res Tech. 2007;70 (8): 733-744.
51. Schultz DC,Ayyanathan K,Negorev D,Maul GG,Rauscher FJ.SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zincfinger proteins.Genes Dev. 2002;16:919-932.
52. Smallwood A,Estève PO,Pradhan S,Carey M.Functional cooperation between HP1 and DNMT1 mediates gene silencing.Genes Dev. 2007;21 (10): 1169-1178.
53. Swales AK,Spears N.Genomic imprinting and reproduction.Reproduction. 2005;130 (4): 389-399.
54. Tachibana M,Sugimoto K,Nozaki M,Ueda J,Ohta T,Ohki M,Fukuda M,Takeda N,Niida H,Kato H, et al.G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis.Genes Dev. 2002;16 (14): 1779-1791.
55. Tan JH,Wang HL,Sun XS,Liu Y,Sui HS,Zhang J.Chromatin configurations in the germinal vesicle of mammalian oocytes.Mol Hum Reprod. 2009;15 (1): 1-9.
56. Vaissière T,Sawan C,Herceg Z.Epigenetic interplay between histone modifications and DNA methylation in gene silencing.Mutat Res. 2008;659 (1-2): 40-48.
57. Vespignani A.Evolution thinks modular.Nat Genet. 2003;35 (2): 118-119.
58. Wade PA,Gegonne A,Jones PL,Ballestar E,Aubry F,Wolffe AP.Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation.Nat Genet. 1999;23 (1): 62-66.
59. Wong CM,Wong CC,Ng YL,Au SL,Ko FC,Ng IO.Transcriptional repressive H3K9 and H3K27 methylations contribute to DNMT1-mediated DNA methylation recovery.PLoS One. 2011;8;6 (2): e16702.
60. Yang L,Xia L,Wu DY,Wang H,Chansky HA,Schubach WH,Hickstein DD,Zhang Y.Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor.Oncogene. 2002;21 (1): 148-152.
61. Zhang Y,Ng HH,Erdjument-Bromage H,Tempst P,Bird A,Reinberg D.Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation.Genes Dev. 1999;13 (15): 1924-1935.
62. Zhang Y,Reinberg D.Transcriptional regulation by histone methylation: interplay between different covalent modifications of the core histone tails.Genes Dev. 2001;15:2343-2360.
63. Zuccotti M,Garagna S,Merico V,Monti M,Alberto Redi C.Chromatin organisation and nuclear architecture in growing mouse oocytes.Mol Cell Endocrinol. 2005;234 (1-2): 11-17.
64. Zuccotti M,Piccinelli A,Giorgi Rossi P,Garagna S,Redi CA.Chromatin organization during mouse oocyte growth.Mol Reprod Dev. 1995;41 (4): 479-485.