Absence of Maternal Methylation in Biparental Hydatidiform Moles from Women with Maternal-Effect Mutations Reveals Widespread Placenta-Specific Imprinting

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Complete hydatidiform moles (CHMs) are abnormal human conceptsus characterized by excessive trophoblast proliferation that commonly result from the absence of a maternal genetic contribution compensated by two copies of the paternal genome. In a few rare cases HMs maybe recurrent (RHM), characterized by a biparental genetic contribution and underlying NLRP7 mutations. It is speculated that aberrant genomic imprinting plays a key role in HM formation, but to date no studies have determined the extent of imprint defects in molar biopsies. By comparing the methylation profile of CHMs and RHMs with normal placentas, we confirm widespread absence of allelic methylation at imprinted loci and identify many aberrantly methylated regions, all of which have profiles consistent with imprinting.

Vyšlo v časopise: Absence of Maternal Methylation in Biparental Hydatidiform Moles from Women with Maternal-Effect Mutations Reveals Widespread Placenta-Specific Imprinting. PLoS Genet 11(11): e32767. doi:10.1371/journal.pgen.1005644
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005644

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1. Hoffner L, Surti U. The genetics of gestational trophoblastic disease: a rare complication of pregnancy. Cancer Genet. 2012;205 : 63–77. doi: 10.1016/j.cancergen.2012.01.004 22469506

2. Judson H, Hayward BE, Sheridan E, Bonthron DT. A global disorder of imprinting in the human female germ line. Nature. 2002;416 : 539–42. 11932746

3. Murdoch S, Djuric U, Mazhar B, Seoud M, Khan R, Kuick R, et al. Mutations in NALP7 cause recurrent hydatidiform moles and reproductive wastage in humans. Nat Genet. 2006;38 : 300–2. 16462743

4. Parry DA, Logan CV, Hayward BE, Shires M, Landolsi H, Diggle C, et al. Mutations causing familial biparental hydatidiform mole implicate c6orf221 as a possible regulator of genomic imprinting in the human oocyte. Am J Hum Genet. 2011;89 : 451–8. doi: 10.1016/j.ajhg.2011.08.002 21885028

5. Wang CM, Dixon PH, Decordova S, Hodges MD, Sebire NJ, Ozalp S, et al. Identification of 13 novel NLRP7 mutations in 20 families with recurrent hydatidiform mole; missense mutations cluster in the leucine-rich region. J Med Genet. 2009;46 : 569–75. doi: 10.1136/jmg.2008.064196 19246479

6. Dixon PH, Trongwongsa P, Abu-Hayyah S, Ng SH, Akbar SA, Khawaja NP, et al. Mutations in NLRP7 are associated with diploid biparental hydatidiform moles, but not androgenetic complete moles. J Med Genet 2012;49 : 206–11. doi: 10.1136/jmedgenet-2011-100602 22315435

7. Reddy R, Akoury E, Phuong Nguyen NM, Abdul-Rahman OA, Dery C, Gupta N, et al. Report of four new patients with protein-truncating mutations in C6orf221/KHDC3L and colocalization with NLRP7. Eur J Hum Genet. 2013;21 : 957–64. doi: 10.1038/ejhg.2012.274 23232697

8. Nguyen NM, Slim R. Genetics and Epigenetics of Recurrent Hydatidiform Moles: Basic Science and Genetic Counselling. Curr Obstet Gynecol Rep. 2014;3 : 55–64. 24533231

9. Fisher RA Lavery SA, Carby A, Abu-Hayyeh S, Swingler R, Sebire NJ, Seckl MJ. What a difference an egg makes. Lancet 2011;378 : 1974. doi: 10.1016/S0140-6736(11)61751-0 22130487

10. Zhang P, Dixon M, Zucchelli M, Hambiliki F, Levkov L, Hovatta O, et al. Expression analysis of the NLRP gene family suggests a role in human preimplantation development. PLoS One. 2008;3: e2755. doi: 10.1371/journal.pone.0002755 18648497

11. Akoury E, Zhang L, Ao A, Slim R.NLRP7 and KHDC3L, the two maternal-effect proteins responsible for recurrent hydatidiform moles, co-localize to the oocyte cytoskeleton. Hum Reprod. 2015;30 : 159–69. doi: 10.1093/humrep/deu291 25358348

12. Court F, Martin-Trujillo A, Romanelli V, Garin I, Iglesias-Platas I, Salafsky I, et al. Genome-wide allelic methylation analysis reveals disease-specific susceptibility to multiple methylation defects in imprinting syndromes. Hum Mutat. 2013;34 : 595–602. doi: 10.1002/humu.22276 23335487

13. Kou YC, Shao L, Peng HH, Rosetta R, del Gaudio D, Wagner AF, et al. A recurrent intragenic genomic duplication, other novel mutations in NLRP7 and imprinting defects in recurrent biparental hydatidiform moles. Mol Hum Reprod 2008;14 : 33–40. 18039680

14. Hayward BE, De Vos M, Talati N, Abdollahi MR, Taylor GR, Meyer E, et al. Genetic and epigenetic analysis of recurrent hydatidiform mole. Hum Mutat. 2009;30: E629–39 doi: 10.1002/humu.20993 19309689

15. Ferguson-Smith AC. Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet. 2011;12 : 565–75. doi: 10.1038/nrg3032 21765458

16. Duéñez-Guzmán EA, Haig D. The evolution of reproduction-related NLRP genes. J Mol Evol. 2014;78 : 194–201. doi: 10.1007/s00239-014-9614-3 24615281

17. Meyer E, Lim D, Pasha S, Tee LJ, Rahman F, Yates JR, et al. Germline mutation in NLRP2 (NALP2) in a familial imprinting disorder (Beckwith-Wiedemann Syndrome). PLoS Genet. 2009;5: e1000423. doi: 10.1371/journal.pgen.1000423 19300480

18. Court F, Tayama C, Romanelli V, Martin-Trujillo A, Iglesias-Platas I, Okamura K, 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 : 554–69. doi: 10.1101/gr.164913.113 24402520

19. Okae H, Chiba H, Hiura H, Hamada H, Sato A, Utsunomiya T, et al. Genome-wide analysis of DNA methylation dynamics during early human development. PloS Genet. 2014;10: e1004868. doi: 10.1371/journal.pgen.1004868 25501653

20. Camprubí C, Iglesias-Platas I, Martin-Trujillo A, Salvador-Alarcon C, Rodriguez MA, Barredo DR, et al. Stability of genomic imprinting and gestational-age dynamic methylation in complicated pregnancies conceived following assisted reproductive technologies. Biol Reprod. 2013;89 : 50. doi: 10.1095/biolreprod.113.108456 23884645

21. Metsalu T, Viltrop T, Tiirats A, Rajashekar B, Reimann E, Kõks S, et al. Using RNA sequencing for identifying gene imprinting and random monoallelic expression in human placenta. Epigenetics. 2014;9 : 1397–409. doi: 10.4161/15592294.2014.970052 25437054

22. Pozharny Y, Lambertini L, Ma Y, Ferrara L, Litton CG, Diplas A, et al. Genomic loss of imprinting in first-trimester human placenta. Am J Obstet Gynecol. 2010;202 : 391.e1–8.

23. Kobayashi H, Yanagisawa E, Sakashita A, Sugawara N, Kumakura S, Ogawa H, et al. Epigenetic and transcriptional features of the novel human imprinted lncRNA GPR1AS suggest it is a functional orthology to mouse Zdbf2linc. Epigenetics. 2013;8 : 635–45. doi: 10.4161/epi.24887 23764515

24. Duffié R, Ajjan S, Greenberg M, Zamudio N, Secamilla del Arenal M, Iranzo J, et al. The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals. Genes & Dev. 2014;28 : 463–78.

25. Yuen RK, Jiang R, Peñaherrera MS, McFadden DE, Robinson WP (2011) Genome-wide mapping of imprinted differentially methylated regions by DNA methylation profiling of human placentas from triploidies. Epigenetics Chromatin 4(1):10. doi: 10.1186/1756-8935-4-10 21749726

26. Herse F, Lamarca B, Hubel CA, Kaartokallio T, Lokki AI, Ekholm E, et al. Cytochrome P450 subfamily 2J polypeptide 2 expression and circulating epoxyeicosatrienoic metabolites in preeclampsia. Circulation 2012;126 : 2990–9. doi: 10.1161/CIRCULATIONAHA.112.127340 23155181

27. Kuo MW, Wang CH, Wu HC, Chang SJ, Chuang YJ. Soluble THSD7A is an N-glycoprotein that promotes endothelial cell migration and tube formation in angiogenesis. PLoS One. 2011;6: e29000. doi: 10.1371/journal.pone.0029000 22194972

28. Noguer-Dance M, Abu-Amero S, Al-Khtib M, Lefèvre A, Coullin P, et al. The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. Hum Mol Genet 2010;19 : 3566–82. doi: 10.1093/hmg/ddq272 20610438

29. Xie L, Mouillet JF, Chu T, Parks WT, Sadovsky E, Knöfler M, et al. C19MC MicroRNAs Regulate the Migration of Human Trophoblasts. Endocrinology. 2014;155 : 4975–85. doi: 10.1210/en.2014-1501 25211593

30. Guo H, Zhu P, Yan L, Li R, Hu B, Lian Y, et al. The DNA methylation landscape of human early embryos. Nature. 2014;511 : 606–10. doi: 10.1038/nature13544 25079557

31. Smith ZD, Chan MM, Humm KC, Karnik R, Mekhoubad S, Regev A, et al. (2014) DNA methylation dynamics of the human preimplantation embryo. Nature 2014;511 : 611–5. doi: 10.1038/nature13581 25079558

32. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P, et al. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev Cell. 2008;15 : 547–57. doi: 10.1016/j.devcel.2008.08.014 18854139

33. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol. 2007;9 : 64–71. 17143267

34. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, Boiani M, et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun. 2011;2 : 241. doi: 10.1038/ncomms1240 21407207

35. 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 : 861–74. doi: 10.1093/molehr/gau049 24994815

36. Mahadevan S, Wen S, Wan YW, Peng HH, Otta S, Liu Z, et al. NLRP7 affects trophoblast lineage differentiation, binds to overexpressed YY1 and alters CpG methylation. Hum Mol Genet. 2014;23 : 706–16. doi: 10.1093/hmg/ddt457 24105472

37. Singer H, Biswas A, Nuesgen N, Oldenburg J, El-Maarri O. NLRP7, Involved in hydatidiform molar pregnancy (HYDM1), interacts with the transcriptional repressor ZBTB16. PLoS One. 2015: e0130416. doi: 10.1371/journal.pone.0130416 26121690

38. Messaed C, Akoury E, Djuric U, Zeng J, Saleh M, Gilbert L, et al. NLRP7, a nucleotide oligomerization domain-like receptor protein, is required for normal cytokine secretion and co-localizes with Golgi and the microtubule-organizing center. J Biol Chem. 2011;286 : 43313–23. doi: 10.1074/jbc.M111.306191 22025618

39. Caillaud M, Duchamp G, Gérard N. In vivo effect of interleukin-1beta and interleukin-1RA on oocyte cytoplasmic maturation, ovulation, and early embryonic development in the mare. Reprod Biol Endocrinol. 2005;3 : 26. 15972098

40. Gkountela S, Li Z, Vincent JJ, Zhang KX, Chen A, Pellegrini M, 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 : 113–22. doi: 10.1038/ncb2638 23242216

41. Nakabayashi K, Trujillo AM, Tayama C, Camprubi C, Yoshida W, Lapunzina P, et al. Methylation screening of reciprocal genome-wide UPDs identifies novel human-specific imprinted genes. Hum Mol Genet. 2011;20 : 3188–97. doi: 10.1093/hmg/ddr224 21593219