[en] Epigenetic modifications are established during gametogenesis and preimplantation embryonic development. Any disturbance of the normal natural environment during these critical phases could cause alterations of the epigenetic signature. Histone acetylation is an important epigenetic modification involved in the regulation of chromatin organization and gene expression.
The present study was aimed to determine whether the proper establishment of post-translational histone H4 acetylation at lysine 8 (AcH4K8), 12 (AcH4K12), and 16 (AcH4K16) of equine oocytes is adversely affected during in vitro maturation when compared to in vivo matured oocytes collected from naturally cycling mares not undergoing ovarian hyperstimulation.
The acetylation patterns were investigated by means of indirect immunofluorescence staining with specific antibodies directed against the acetylated lysine residues. Our results indicate that the acetylation state of H4 is dependent on the chromatin configuration in immature GV stage oocytes and it changes in a residue-specific manner along with the increase of chromatin condensation. In particular, the levels of AcH4K8 and AcH4K12 increased significantly, while AcH4K16 decreased significantly from the fibrillar to the condensed state of chromatin configuration within the GV. Moreover, during meiosis K8 and K12 were substantially deacetylated without any differences between in vivo and in vitro conditions, while K16 displayed a strong acetylation in oocytes matured in vivo, and in contrast, it was markedly deacetylated following in vitro maturation.
Although the functional meaning of residue-specific acetylation during oocyte differentiation and meiotic resumption needs further investigation, our results support the hypothesis that in vitro maturation conditions can adversely affect oocyte ability to regulate the epigenetic reprogramming, critical for successful meiosis and subsequent embryonic development.
Disciplines :
Anatomy (cytology, histology, embryology...) & physiology Veterinary medicine & animal health Genetics & genetic processes
Author, co-author :
Franciosi, Federica; University of Milan > Dpt Animal Sciences, Faculty of Veterinary Medicine
Lodde, Valentina; University of Milan > Dpt of Animal Siences, Faculty of Veterinary Medicine
Goudet, Ghylène; Institut Scientifique de Recherche Agronomique - INRA > UMR 85 > Physiologie de la reproduction et des comportements
Duchamp, Guy; Institut Scientifique de Recherche Agronomique - INRA > UMR 85 > Physiologie de la Reproduction et des Comportements
Deleuze, Stefan ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Obstét. et path. de la reprod. des anim. de comp. et équidés
Douet, Cécile; Institut Scientifique de Recherche Agronomique - INRA > UMR85 > Physiologie de la Reproduction et des Comportements
Tessario, Irene; University of Milan > Dpt of Animal Siences, Faculty of Veterinary Medicine
Luciano, Alberto; University of Milan > Dpt of Animal Siences, Faculty of Veterinary Medicine
Language :
English
Title :
Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes
Abramoff MD, Magalhaes PJ, Ram SJ. Image processing with ImageJ. Biophot Int 2004;11:36-42.
Akiyama T, Kim JM, Nagata M, Aoki F. Regulation of histone acetylation during meiotic maturation in mouse oocytes. Mol Reprod Dev 2004; 69:222-227.
Akiyama T, Nagata M, Aoki F. Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc Natl Acad Sci USA 2006;103:7339-7344.
Borghol N, Lornage J, Blachere T, Sophie Garret A, Lefevre A. Epigenetic status of the H19 locus in human oocytes following in vitro maturation. Genomics 2006;87:417-426.
Christopikou D, Karamalegos C, Doriza S, Argyrou M, Sisi P, Davies S, Mastrominas M. Spindle and chromosome configurations of human oocytes matured in vitro in two different culture media. Reprod Biomed Online 2010;20:639-648.
Ciapa B, Arnoult C. Could modifications of signalling pathways activated after ICSI induce a potential risk of epigenetic defects? Int J Dev Biol 2011;55:143-152.
Ciccone DN, Chen T. Histone lysine methylation in genomic imprinting. Epigenetics 2009;4:216-220.
Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, Horsthemke B. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet 2002;71:162-164.
De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol 2006;292:1-12.
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;275:447-458.
De Rycke M, Liebaers I, Van Steirteghem A. Epigenetic risks related to assisted reproductive technologies: risk analysis and epigenetic inheritance. Hum Reprod 2002;17:2487-2494.
Dell'Aquila ME, Masterson M, Maritato F, Hinrichs K. Influence of oocyte collection technique on initial chromatin configuration, meiotic competence, and male pronucleus formation after intracytoplasmic sperm injection (ICSI) of equine oocytes. Mol Reprod Dev 2001;60:79-88.
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.
Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 2000;62:1526-1535.
Duchamp G, Bour B, Combarnous Y, Palmer E. Alternative solutions to hCG induction of ovulation in the mare. J Reprod Fertil Suppl 1987; 35:221-228.
Dupont C, Armant DR, Brenner CA. Epigenetics: definition, mechanisms and clinical perspective. Semin Reprod Med 2009;27:351-357.
Edwards RG. Are minimal stimulation IVF and IVM set to replace routine IVF? Reprod Biomed Online 2007;14:267-270.
Endo T, Kano K, Naito K. Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes. Biol Reprod 2008;78:1073-1080.
Endo T, Naito K, Aoki F, Kume S, Tojo H. Changes in histone modifications during in vitro maturation of porcine oocytes. Mol Reprod Dev 2005;71:123-128.
Felsenfeld G, Groudine M. Controlling the double helix. Nature 2003; 421:448-453.
Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol 2003;15:172-183.
Fulka H. Changes in global histone acetylation pattern in somatic cell nuclei after their transfer into oocytes at different stages of maturation. Mol Reprod Dev 2008;75:556-564.
Ginther OJ, Gastal EL, Gastal MO, Bergfelt DR, Baerwald AR, Pierson RA. Comparative study of the dynamics of follicular waves in mares and women. Biol Reprod 2004;71:1195-1201.
Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 2003; 361:1975-1977.
Goudet G, Belin F, MlodawskaW, Bezard J. Influence of epidermal growth factor on in vitro maturation of equine oocytes. J Reprod Fertil Suppl 2000; 56:483-492.
Grace KS, Sinclair KD. Assisted reproductive technology, epigenetics, and long-term health: a developmental time bomb still ticking. Semin Reprod Med 2009;27:409-416.
Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997;389:349-352.
Gu L, Wang Q, Sun QY. Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions. Cell Cycle 2010; 9:1942-1950.
Hinrichs K. The equine oocyte: factors affecting meiotic and developmental competence. Mol Reprod Dev 2010;77:651-661.
Hinrichs K, Schmidt AL. Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season. Biol Reprod 2000;62:1402-1408.
Hinrichs K, Williams KA. Relationships among oocyte-cumulus morphology, follicular atresia, initial chromatin configuration, and oocyte meiotic competence in the horse. Biol Reprod 1997; 57:377-384.
Hinrichs K, Choi YH, Love LB, Varner DD, Love CC, Walckenaer BE. Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence. Biol Reprod 2005;72:1142-1150.
Huang JC, Yan LY, Lei ZL, Miao YL, Shi LH, Yang JW, Wang Q, Ouyang YC, Sun QY, Chen DY. Changes in histone acetylation during postovulatory aging of mouse oocyte. Biol Reprod 2007; 77:666-670.
Huntriss J, Picton HM. Epigenetic consequences of assisted reproduction and infertility on the human preimplantation embryo. Hum Fertil (Camb) 2008;11:85-94.
Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000;403:795-800.
Imamura T, Kerjean A, Heams T, Kupiec JJ, Thenevin C, Paldi A. Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo. J Biol Chem 2005; 280:20171-20175.
Kageyama S, Liu H, Kaneko N, Ooga M, Nagata M, Aoki F. Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 2007;133:85-94.
Kerjean A, Couvert P, Heams T, Chalas C, Poirier K, Chelly J, Jouannet P, Paldi A, Poirot C. In vitro follicular growth affects oocyte imprinting establishment in mice. Eur J Hum Genet 2003;11:493-496.
Kim JM, Liu H, Tazaki M, Nagata M, Aoki F. Changes in histone acetylation during mouse oocyte meiosis. J Cell Biol 2003;162:37-46.
Kota SK, Feil R. Epigenetic transitions in germ cell development and meiosis. Dev Cell 2010;19:675-686.
Kruhlak MJ, Hendzel MJ, Fischle W, Bertos NR, Hameed S, Yang XJ, Verdin E, Bazett-Jones DP. Regulation of global acetylation in mitosis through loss of histone acetyltransferases and deacetylases from chromatin. J Biol Chem 2001;276:38307-38319.
Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002;3:662-673.
Liu J, Lu G, Qian Y, Mao Y, Ding W. Pregnancies and births achieved from in vitro matured oocytes retrieved from poor responders undergoing stimulation in in vitro fertilization cycles. Fertil Steril 2003; 80:447-449.
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;74:740-749.
Luciano AM, Goudet G, Perazzoli F, Lahuec C, Gerard N. Glutathione content and glutathione peroxidase expression in in vivo and in vitro matured equine oocytes. Mol Reprod Dev 2006;73:658-666.
Ludwig M, Katalinic A, Gross S, Sutcliffe A, Varon R, Horsthemke B. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J Med Genet 2005;42:289-291.
Maalouf WE, Alberio R, Campbell KH. Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics 2008; 3:199-209.
Manosalva I, Gonzalez A. Aging alters histone H4 acetylation and CDC2A in mouse germinal vesicle stage oocytes. Biol Reprod 2009; 81:1164-1171.
Market-Velker BA, Fernandes AD,MannMR. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biol Reprod 2010;83:938-950.
Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet 2005;14(Suppl 1):R47-58.
Mugnier S, Dell'Aquila ME, Pelaez J, Douet C, Ambruosi B, De Santis T, Lacalandra GM, Lebos C, Sizaret PY, Delaleu B et al. New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol Reprod 2009;81:856-870.
Nagashima T, Maruyama T, Furuya M, Kajitani T, Uchida H, Masuda H, Ono M, Arase T, Ozato K, Yoshimura Y. Histone acetylation and subcellular localization of chromosomal protein BRD4 during mouse oocyte meiosis and mitosis. Mol Hum Reprod 2007;13:141-148.
Ola SI, Wang Q, Ai JS, Yin S, Liang CG, Chen DY, Sun QY. Meiotic competence and acetylation pattern of UV light classified mouse antral oocytes after meiotic arrest with isobutylmethylxanthine. Mol Reprod Dev 2007;74:591-599.
Qiao J, Chen Y, Yan LY, Yan J, Liu P, Sun QY. Changes in histone methylation during human oocyte maturation and IVF- or ICSI-derived embryo development. Fertil Steril 2010;93:1628-1636.
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;21:738-748.
Rea S, Xouri G, Akhtar A. Males absent on the first (MOF): from flies to humans. Oncogene 2007;26:5385-5394.
Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007;447:425-432.
Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001;293:1089-1093.
Requena A, Bronet F, Guillen A, Agudo D, Bou C, Garcia-Velasco JA. The impact of in-vitro maturation of oocytes on aneuploidy rate. Reprod Biomed Online 2009;18:777-783.
Sagirkaya H, Misirlioglu M, Kaya A, First NL, Parrish JJ, Memili E. Developmental and molecular correlates of bovine preimplantation embryos. Reproduction 2006;131:895-904.
Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
Schultz RM, Davis W Jr, Stein P, Svoboda P. Reprogramming of gene expression during preimplantation development. J Exp Zool 1999; 285:276-282.
Smith CM, Gafken PR, Zhang Z, Gottschling DE, Smith JB, Smith DL. Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone H4. Anal Biochem 2003; 316:23-33.
Spinaci M, Seren E, Mattioli M. Maternal chromatin remodeling during maturation and after fertilization in mouse oocytes. Mol Reprod Dev 2004;69:215-221.
Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403:41-45.
Suo L, Meng QG, Pei Y, Yan CL, Fu XW, Bunch TD, Zhu SE. Changes in acetylation on lysine 12 of histone H4 (AcH4K12) of murine oocytes during maternal aging may affect fertilization and subsequent embryo development. Fertil Steril 2010;93:945-951.
Tang LS, Wang Q, Xiong B, Hou Y, Zhang YZ, Sun QY, Wang SY. Dynamic changes in histone acetylation during sheep oocyte maturation. J Reprod Dev 2007;53:555-561.
Thompson JG, Kind KL, Roberts CT, Robertson SA, Robinson JS. Epigenetic risks related to assisted reproductive technologies: shortand long-term consequences for the health of children conceived through assisted reproduction technology: more reason for caution? Hum Reprod 2002;17:2783-2786.
Turner BM, Fellows G. Specific antibodies reveal ordered and cell-cycle-related use of histone-H4 acetylation sites in mammalian cells. Eur J Biochem 1989;179:131-139.
van den Berg IM, Eleveld C, van der Hoeven M, Birnie E, Steegers EA, Galjaard RJ, Laven JS, van Doorninck JH. Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment. Hum Reprod 2011; 26:1181-1190.
van der Heijden GW, van den Berg IM, Baart EB, Derijck AA, Martini E, de Boer P. Parental origin of chromatin in human monopronuclear zygotes revealed by asymmetric histone methylation patterns, differs between IVF and ICSI. Mol Reprod Dev 2009;76:101-108.
Vaquero A, Sternglanz R, Reinberg D. NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs. Oncogene 2007; 26:5505-5520.
Wang Q, Wang CM, Ai JS, Xiong B, Yin S, Hou Y, Chen DY, Schatten H, Sun QY. Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 2006a;5:1974-1982.
Wang Q, Yin S, Ai JS, Liang CG, Hou Y, Chen DY, Schatten H, Sun QY. Histone deacetylation is required for orderly meiosis. Cell Cycle 2006b; 5:766-774.
Wang N, Le F, Zhan QT, Li L, Dong MY, Ding GL, Xu CM, Jiang SW, Huang HF, Jin F. Effects of in vitro maturation on histone acetylation in metaphase II oocytes and early cleavage embryos. Obstet Gynecol Int 2010;2010:989278.
Xu YW, Peng YT, Wang B, Zeng YH, Zhuang GL, Zhou CQ. High follicle-stimulating hormone increases aneuploidy in human oocytes matured in vitro. Fertil Steril 2010;95:99-104.
Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod 1998;3:155-163.
Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, Broadbent PJ, Robinson JJ, Wilmut I, Sinclair KD. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet 2001;27:153-154.
Zuccotti M, Giorgi Rossi P, Martinez A, Garagna S, Forabosco A, Redi CA. Meiotic and developmental competence of mouse antral oocytes. Biol Reprod 1998;58:700-704.