Эпигенетическое репрограммирование ДНК в гаметах и доимплантационных эмбрионах человека
Аннотация
В обзоре приведены новые данные об эпигенетическом репрограммировании генома в гаметогенезе и доимплантационном эмбриогенезе человека. Суммированы современные представления о динамических изменениях метилирования цитозина ДНК - ключевого механизма эпигенетической регуляции генома - в гаметах и у эмбрионов доимплантационных стадий развития. Рассмотрены различия в динамике и механизмах репрограммирования импринтированных и неимпринтированных участков ДНК в мужских и женских половых клетках.
Ключевые слова
метилирование ДНК,
5-метилцитозин,
5-гидроксиметилцитозин,
активное деметилирование ДНК,
эпигенетическое репрограммирование генома,
эмбриогенез человека,
DNA methylation 5-methylcytosine,
5-hydroxymethylcytosine,
active DNA demethylation,
epigenetic genome reprogramming,
human embryogenesis
Об авторах
А. В. Тихонов
НИИ акушерства, гинекологии и репродуктологии им. Д.О. Отта; Санкт-Петербургский государственный университет; Диагностический центр (медико-генетический)
Россия
Россия
О. А. Ефимова
НИИ акушерства, гинекологии и репродуктологии им. Д.О. Отта; Санкт-Петербургский государственный университет
Россия
Россия
А. А. Пендина
НИИ акушерства, гинекологии и репродуктологии им. Д.О. Отта; Санкт-Петербургский государственный университет; Диагностический центр (медико-генетический)
Россия
Россия
В. С. Баранов
НИИ акушерства, гинекологии и репродуктологии им. Д.О. Отта; Санкт-Петербургский государственный университет
Россия
Россия
Список литературы
1. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007; 447: 425-432.
2. Lange UC, Schneider R. What an epigenome remembers. Bioessays. 2010; 32(8): 659-668.
3. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001; 293: 1089-1093.
4. Пендина АА, Гринкевич ВВ, Кузнецова ТВ, Баранов ВС. Метилирование ДНК - универсальный механизм регуляции активности генов. Экологическая генетика. 2004; 1(II): 27-37.
5. Пендина АА, Ефимова ОА, Кузнецова ТВ, Баранов ВС. Болезни геномного импринтинга. Журнал акушерства и женских болезней. 2007; LVI(1): 76-83.
6. Ефимова ОА, Пендина АА, Тихонов АВ, и др. Метилирование ДНК - основной механизм репрограммирования и регуляции генома человека. Медицинская генетика. 2012; 11(4): 10-18.
7. Valinluck V, Sowers LC. Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res. 2007 Feb 1; 67(3): 946-950.
8. Tahiliani M, Koh KP, Shen Y. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009; 324: 930-935.
9. Ефимова ОА, Пендина АА, Тихонов АВ, и др. Гидроксильная форма 5-метилцитозина - 5-гидроксиметилцитозин: новый взгляд на биологическую роль в геноме млекопитающих. Экологическая генетика. 2014; XII(1): 3-13.
10. Ефимова ОА, Пендина АА, Тихонов АВ, Баранов ВС. Эволюция представлений о биологической роли кислородсодержащих производных 5-метилцитозина в геноме млекопитающих. Экологическая генетика. 2016; XVI(4): 14-25.
11. Bhutani N, Burns DM, Blau HM. DNA demethylation dynamics. Cell. 2011; 146(6): 866-872.
12. Ito S, D’Alessio AC, Taranova OV, et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010; 466: 1129-1133.
13. He YF, Li BZ, Li Z, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011; 333: 1303-1307.
14. Ito S, Shen L, Dai Q, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011; 333(6047): 1229-1230.
15. Maiti A, Drohat A. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem. 2011 Oct 14; 286(41): 35334-35338.
16. Iqbal K, Jin SG, Pfeifer GP, Szabо PE. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA. 2011; 108(9): 3642-3647.
17. Wossidlo M, Nakamura T, Lepikhov K, et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun. 2011; 2: 241.
18. Beaujean N, Hartshorne G, Cavilla J, et al. Non-conservation of mammalian preimplantation methylation dynamics. Curr Biol. 2004; 14(7): R266-7.
19. Shi W, Dirim F, Wolf E, et al. Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos. Biol Reprod. 2004; 71: 340-347.
20. Hou J, Lei TH, Liu L, et al. DNA methylation patterns in in vitro-fertilized goat zygotes. Reprod Fert Devel. 2005; 17: 809-813.
21. Fulka J, Fulka H, Slavik T, et al. DNA methylation pattern in pig in vivo produced embryos. Histochem Cell Biol. 2006; 126: 213-217.
22. Carlson BM. Human embryology and developmental biology. 4th edition. USA. Mosby. 2009: 541 p.
23. Quenneville S, Verde G, Corsinotti A, et al. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Molecular Cell. 2011; 44: 361-372.
24. Walter M, Teissandier A, Perez-Palacios R, Bourc’his D. An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells. Elife. 2016; 5. doi: 10.7554/eLife.11418.
25. Bostick M, Kim JK, Esteve PO, et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science. 2007; 317: 1760-1764.
26. Rottach A, Frauer C, Pichler G, Bonapace IM, et al. The multi-domain protein Np95 connects DNA methylation and histone modification. Nucleic Acids Res. 2010; 38: 1796-1804.
27. Fang J, Cheng J, Wang J, et al. Hemi-methylated DNA opens a closed conformation of UHRF1 to facilitate its histone recognition. Nat Commun. 2016; 7: 11197.
28. Tang WWC, Dietmann S, Irie N, et al. A Unique Gene Regulatory Network Resets the Human Germline Epigenome for Development. Cell. 2015; 161: 1453-1467.
29. Guo F, Yan L, Guo H, et al. The Transcriptome and DNA Methylome Landscapes of Human Primordial Germ Cells. Cell. 2015; 161: 1437-1452.
30. Gkountela S, Zhang KX, Shafiq TA, et al. DNA Demethylation Dynamics in the Human Prenatal Germline. Cell. 2015; 161: 1425-1436.
31. von Meyenn F, Berrens RV, Andrews S, et al. Comparative principles of DNA methylation reprogramming during human and mouse in vitro primordial germ cell specification. Dev Cell. 2016; 39: 104-115.
32. Zhang W, Xia W, Wang Q, et al. Isoform switch of TET1 regulates DNA demethylation and mouse development. Mol Cell. 2016; 64(6): 1062-1073.
33. Gkountela S, Li Z, Vincent JJ, et al. The ontogeny of cKIT+ human primordial germ cells proves to be a resource for human germ line reprogramming, imprint erasure and in vitro differentiation. Nat Cell Biol. 2013; 15: 113-122.
34. Bartolomei MS, Ferguson-Smith AC. Mammalian genomic imprinting. Cold Spring Harb Perspect Biol. 2011 Jul 1; 3(7).
35. Macdonald WA, Mann MRW. Epigenetic regulation of genomic imprinting from germ line to preimplantation. Mol Reprod Dev. 2014; 81: 126-140.
36. Spahn L, Barlow DP. An ICE pattern crystallizes. Nat Genet 2003; 35: 11-12.
37. Kerjean A, Dupont JM, Vasseur C, et al. Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum Mol Genet. 2000; 9: 2183-2187.
38. Kagiwada S, Kurimoto K, Hirota T, et al. Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. Embo J. 2013; 32: 340-353.
39. Wermann H, Stoop H, Gillis AJM, et al. Global DNA methylation in fetal human germ cells and germ cell tumours: association with differentiation and cisplatin resistance. J Pathol. 2010; 221: 433-442.
40. Okae H, Chiba H, Hiura H, et al. Genome-wide analysis of DNA methylation dynamics during early human development. PLoS Genet. 2014; 10: e1004868.
41. Kobayashi H, Sakurai T, Imai M, et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 2012; 8: e1002440.
42. Smallwood SA, Tomizawa S-I, Krueger F, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011; 43: 811-814.
43. Guo H, Zhu P, Yan L, et al. The DNA methylation landscape of human early embryos. Nature. 2014; 511: 606-610.
44. Smith ZD, Chan MM, Humm KC, et al. DNA methylation dynamics of the human preimplantation embryo : Nature : Nature Publishing Group. Nature. 2014; 511: 611-615.
45. Marques CJ, Joаo Pinho M, Carvalho F, et al. DNA methylation imprinting marks and DNA methyltransferase expression in human spermatogenic cell stages. Epigenetics. 2011; 6: 1354-1361.
46. Kobayashi H, Sato A, Otsu E, et al. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet. 2007; 16: 2542-2551.
47. Marques CJ, Costa P, Vaz B, et al. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod. 2008; 14: 67-74.
48. Sato A, Hiura H, Okae H, et al. Assessing loss of imprint methylation in sperm from subfertile men using novel methylation polymerase chain reaction Luminex analysis. Fertil Steril. 2011; 95: 129-34- 134.e1-4.
49. Boissonnas CC, Abdalaoui HE, Haelewyn V, et al. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet. 2010; 18: 73-80.
50. Sato A, Otsu E, Negishi H, et al. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Human Reproduction. 2007; 22: 26-35.
51. Khoueiry R, Khoureiry R, Ibala-Rhomdane S, et al. Dynamic CpG methylation of the KCNQ1OT1 gene during maturation of human oocytes. J Med Genet. 2008; 45: 583-588.
52. Arima T, Wake N. Establishment of the primary imprint of the HYMAI/PLAGL1 imprint control region during oogenesis. Cytogenet Genome Res. 2006; 113: 247-252.
53. Geuns E, Hilven P, Van Steirteghem A, et al. Methylation analysis of KvDMR1 in human oocytes. J Med Genet. 2006; 44: 144-147.
54. Geuns E, De Temmerman N, Hilven P, et al. Methylation analysis of the intergenic differentially methylated region of DLK1-GTL2 in human. Eur J Hum Genet. 2007; 15: 352-361.
55. Geuns E, De Rycke M, Van Steirteghem A, Liebaers I. Methylation imprints of the imprint control region of the SNRPN-gene in human gametes and preimplantation embryos. Hum Mol Genet. 2003; 12: 2873-2879.
56. Anckaert E, De Rycke M, Smitz J. Culture of oocytes and risk of imprinting defects. Human Reproduction Update. 2013; 19: 52-66.
57. Petrussa L, Van de Velde H, De Rycke M. Dynamic regulation of DNA methyltransferases in human oocytes and preimplantation embryos after assisted reproductive technologies. Mol Hum Reprod. 2014; 20: 861-874.
58. Huntriss J, Hinkins M, Oliver B, et al. Expression of mRNAs for DNA methyltransferases and methyl-CpG-binding proteins in the human female germ line, preimplantation embryos, and embryonic stem cells. Mol Reprod Dev. 2004; 67: 323-336.
59. Yan L, Yang M, Guo H, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013; 20: 1131-1139.
60. Feng S, Jacobsen SE, Reik W. Epigenetic reprogramming in plant and animal development. Science. 2010; 330(6004): 622-627.
61. Ooi SL, Henikoff S. Germline histone dynamics and epigenetics. Curr Opin Cell Biol. 2007; 19: 257-265.
62. Fulka H, Mrazek M, Tepla O, Fulka J. DNA methylation pattern in human zygotes and developing embryos. Reproduction. 2004; 128: 703-708.
63. Fulka H, Barnetova I, Mosko T, Fulka J. Epigenetic analysis of human spermatozoa after their injection into ovulated mouse oocytes. Hum Reprod. 2008; 23: 627-634.
64. Pendina AA, Efimova OA, Fedorova ID, et al. DNA methylation patterns of metaphase chromosomes in human preimplantation embryos. Cytogenet Genome Res. 2011; 132: 1-7.
65. Efimova OA, Pendina AA, Tikhonov AV, et al. Chromosome hydroxymethylation patterns in human zygotes and cleavage-stage embryos. Reproduction. 2015; 149: 223-233.
66. Iurlaro M, von Meyenn F, Reik W. DNA methylation homeostasis in human and mouse development. Curr Opin Genet Dev. 2017; 43: 101-109.
67. Morgan HD, Santos F, Green K, et al. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005; 14: R47-R58.
68. Xu Y, Zhang JJ, Grifo JA, Krey LC. DNA methylation patterns in human tripronucleate zygotes. Mol Hum Reprod. 2005; 11(3): 167-171.
69. Баранов ВС, Пендина АА, Кузнецова ТВ, и др. Некоторые особенности статуса метилирования метафазных хромосом у зародышей человека доимплантационных стадий развития. Цитология. 2005; 47(8): 723-730.
70. Saitou M, Kagiwada S, Kurimoto K. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development. 2012; 139: 15-31.
71. Payer B, Saitou M, Barton SC, et al. Stella is a maternal effect gene required for normal early development in mice. Curr Biol. 2003; 13: 2110-2117.
72. Bortvin A, Goodheart M, Liao M, Page DC. Dppa3 / Pgc7 / stella is a maternal factor and is not required for germ cell specification in mice. BMC Dev Biol. 2004; 4: 1-5.
73. Li X, Ito M, Zhou F, et al. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev Cell. 2008; 15: 547-557.
74. Li W, Liu M. Distribution of 5-hydroxymethylcytosine in different human tissues. J Nucleic Acids. 2011; 2011: 870726.
75. Wright FA, Lemon WJ, Zhao WD, et al. A draft annotation and overview of the human genome. Genome Biol. 2001: 2: 1-18.
76. Musio A, Mariani T, Vezzoni P, Frattini A. Heterogeneous gene distribution reflects human genome complexity as detected at the cytogenetic level. Cancer Genet Cytogenet. 2002; 134(2): 168-171.
77. Straussman R, Neiman D, Roberts D, et al. Developmental programming of CpG islands methylation profiles in the human genome. Net Struct Mol Biol. 2009; 16: 571-594.
78. Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG-binding proteins. Mol Cell Biol. 1998; 18: 6538-6547.
79. Пендина АА, Ефимова ОА, Каминская АН, и др. Иммуноцитохимический анализ статуса метилирования метафазных хромосом человека. Цитология. 2005; 47(8): 731-737.
80. Ефимова ОА, Пендина АА, Тихонов АВ, и др. Сравнительный иммуноцитохимический анализ профилей метилирования ДНК метафазных хромосом из лимфоцитов взрослых индивидов и плодов человека. Молекулярная медицина. 2015; 3: 17-21.
81. Santos F, Hyslop L, Stojkovic P, et al. Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Hum Reprod. 2010; 25(9): 2387-2395.
82. Robinson WP, Price EM. The human placental methylome. Cold Spring Harb Perspect Med. 2015. doi: 10.1101/cshperspect.a023044.
83. Inoue A, Zhang Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science. 2011; 334: 194.
84. Goto T, Jones GM, Lolatgis N, et al. Identification and characterisation of known and novel transcripts expressed during the final stages of human oocyte maturation. Mol Reprod Dev. 2002; 62: 13-28.
85. Anvar Z, Cammisa M, Riso V, et al. ZFP57 recognizes multiple and closely spaced sequence motif variants to maintain repressive epigenetic marks in mouse embryonic stem cells. Nucleic Acids Res. 2015.
86. Court F, Tayama C, Romanelli V, et al. Genome-wide parent-of-origin DNA methylation analysis reveals the intricacies of human imprinting and suggests a germline methylation-independent mechanism of establishment. Genome Res. 2014; 24: 554-569.
87. Takikawa S, Wang X, Ray C, et al. Human and mouse ZFP57 proteins are functionally interchangeable in maintaining genomic imprinting at multiple imprinted regions in mouse ES cells. Epigenetics. 2013; 8: 1268-1279.
88. Tian X, Pascal G, Monget P. Evolution and functional divergence of NLRP genes in mammalian reproductive systems. BMC Evol Biol. 2009; 9: 202.
89. Murdoch S, Djuric U, Mazhar B, et al. Mutations in NALP7 cause recurrent hydatidiform moles and reproductive wastage in humans. Nat Genet. 2006; 38: 300-302.
90. Nguyen NM, Slim R. Genetics and epigenetics of recurrent hydatidiform moles: Basic science and genetic counselling. Curr Obstet Gynecol Rep. 2014; 3: 55-64.
91. Mahadevan S, Wen S, Wan YW, et al. NLRP7 affects trophoblast lineage differentiation, binds to overexpressed YY1 and alters CpG methylation. Hum Mol Genet. 2013; 23(3): 706-716.
92. Soellner L, Begemann M, Mackay DJ, et al. Recent Advances in Imprinting Disorders. Clin Genet. 2017; 91(1): 3-13.
93. Gicquel C, Gaston V, Mandelbaum J, et al. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am J Hum Genet. 2003; 72: 1338-1341.
94. Maher ER, Brueton LA, Bowdin SC, et al. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet. 2003; 40: 62-64.
95. Sutcliffe AG, Peters CJ, Bowdin S, et al. Assisted reproductive therapies and imprinting disorders-a preliminary British survey. Human Reproduction. 2006; 21: 1009-1011.
96. Doornbos ME, Maas SM, McDonnell J, Vermeiden JPW, Hennekam RCM. Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Human Reproduction. 2007; 22: 2476-2480.
97. Vermeiden JPW, Bernardus RE. Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection? Fertil Steril. 2013; 99: 642-651.
98. Ludwig M, Katalinic A, Gross S, et al. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J Med Genet. 2005; 42: 289-291.
99. Chiba H, Hiura H, Okae H, et al. DNA methylation errors in imprinting disorders and assisted reproductive technology. Pediatr Int. 2013; 55: 542-549.
100. Bliek J, Terhal P, van den Bogaard M-J, et al. Hypomethylation of the H19 gene causes not only Silver-Russell syndrome (SRS) but also isolated asymmetry or an SRS-like phenotype. Am J Hum Genet. 2006; 78: 604-614.
101. Chopra M, Amor DJ, Sutton L, et al. Russell-Silver syndrome due to paternal H19/IGF2 hypomethylation in a patient conceived using intracytoplasmic sperm injection. Reprod Biomed Online. 2010; 20: 843-847.
102. Hiura H, Okae H, Miyauchi N, et al. Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Hum Reprod. 2012; 27: 2541-2548.
103. Cocchi G, Marsico C, Cosentino A, et al. Silver-Russell syndrome due to paternal H19/IGF2 hypomethylation in a twin girl born after in vitro fertilization. Am J Med Genet A. 2013; 161A: 2652-2655.
104. Talaulikar VS, Arulkumaran S. Reproductive outcomes after assisted conception. Obstet Gynecol Surv. 2012; 67: 566-583.
105. Okun N, Sierra S. Pregnancy outcomes after assisted human reproduction. J Obstet Gynaecol Can 2014; 36: 64-83.
Рецензия
Для цитирования:
Тихонов А.В., Ефимова О.А., Пендина А.А., Баранов В.С. Эпигенетическое репрограммирование ДНК в гаметах и доимплантационных эмбрионах человека. Медицинская генетика. 2017;16(5):17-25.
For citation:
Tikhonov A.V., Efimova O.A., Pendina A.A., Baranov V.S. Epigenetic reprogramming in human gametes and preimplantation embryos. Medical Genetics. 2017;16(5):17-25. (In Russ.)
Просмотров: 810
Послать статью по эл. почте 