Compromised fertility disrupts Peg1 but not Snrpn and Peg3 imprinted methylation acquisition in mouse oocytes

Frontiers in Genetics

Volumn 3, Issue OCT, 2012, Pages

  Denomme, Michelle M ^a,b   White, Carlee R ^a,b   Gillio Meina, Carolina ^a,b   MacDonald, William A ^a,b   Deroo, Bonnie J ^a,b   Kidder, Gerald M ^a,b   Mann, Mellissa R W ^a,b  

^a CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^b WESTERN UNIVERSITY   (Canada)

Author keywords

Connexin37; DNA methylation; Estrogen receptor beta; Genomic imprinting; Imprint acquisition; Infertility; Oocyte; Oocyte diameter

Indexed keywords

MUS;

EID: 84867144848     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00129     Document Type: Article

References (54)

1. Anckaert, E., Adriaenssens, T., Romero, S., Dremier, S., and Smitz, J. (2009). Unaltered imprinting establishment of key imprinted genes in mouse oocytes after in vitro follicle culture under variable follicle-stimulating hormone exposure. Int. J. Dev. Biol. 53, 541-548.
2. Anckaert, E., Romero, S., Adriaenssens, T., and Smitz, J. (2010). Effects of low methyl donor levels in culture medium during mouse follicle culture on oocyte imprinting establishment. Biol. Reprod. 83, 377-386.
3. Azzi, S., Rossignol, S., Steunou, V., Sas, T., Thibaud, N., Dan-ton, F., Le Jule, M., Heinrichs, C., Cabrol, S., Gicquel, C., Le Bouc, Y., and Netchine, I. (2009). Multilocus methylation analysis in a large cohort of 11p15-related foetal growth disorders (Russell-Silver and Beckwith-Wiedemann syndromes) reveals simultaneous loss of methylation at paternal and maternal imprinted loci. Hum. Mol. Genet. 18, 4724-4733.
4. Barrett, S. L., and Albertini, D. F. (2010). Cumulus cell contact during oocyte maturation in mice regulates mei-otic spindle positioning and enhances developmental competence. J. Assist. Reprod. Genet. 27, 29-39.
5. Bartolomei, M. S., and Ferguson-Smith, A. C. (2011). Mammalian genomic imprinting. Cold Spring Harb. Per-spect. Biol. 3, pii: a002592.
6. Bliek, J., Verde, G., Callaway, J., Maas, S. M., De Crescenzo, A., Sparago, A., Cerrato, F., Russo, S., Ferraiuolo, S., Rinaldi, M. M., Fischetto, R., Lalatta, F., Giordano, L., Ferrari, P., Cubel-lis, M. V., Larizza, L., Temple, I. K., Mannens, M. M., Mackay D. J., and Riccio, A. (2009). Hypomethy-lation at multiple maternally methylated imprinted regions including PLAGL1 and GNAS loci in Beckwith-Wiedemann syndrome. Eur. J. Hum. Genet. 17,611-619.
7. Carabatsos, M. J., Sellitto, C., Good-enough, D. A., and Albertini, D. F. (2000). Oocyte-granulosa cell het-erologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev. Biol. 226, 167-179.
8. Chang, A. S., Moley, K. H., Wan-gler, M., Feinberg, A. P., and DeBaun, M. R. (2005). Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients. Fertil. Steril. 83, 349-354.
9. Couse, J. F., Curtis Hewitt, S., and Korach, K. S. (2000). Receptor null mice reveal contrasting roles for estrogen receptor alpha and beta in reproductive tissues. J. Steroid Biochem. Mol. Biol. 74, 287-296.
10. Couse, J. F., Yates, M. M., Deroo, B. J., and Korach, K. S. (2005). Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 146, 3247-3262.
11. Couse, J. F., Yates, M. M., Walker, V. R., and Korach, K. S. (2003). Characterization of the hypo-thalamic-pituitary-gonadal axis in estrogen receptor (ER) Null mice reveals hypergonadism and endocrine sex reversal in females lacking ERalpha but not ERbeta. Mol. Endocrinol. 17,1039-1053.
12. Cox, G. F., Burger, J., Lip, V., Mau, U. A., Sperling, K., Wu, B. L., and Hors-themke, B. (2002). Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am. J. Hum. Genet. 71, 162-164.
13. Davis, T. L., Trasler, J. M., Moss, S. B., Yang, G. J., and Bartolomei, M. S. (1999). Acquisition of the H19 methylation imprint occurs differentially on the parental alleles during spermatogenesis. Genomics 58, 18-28.
14. Davis, T. L., Yang, G. J., McCarrey, J. R., and Bartolomei, M. S. (2000). The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum. Mol. Genet. 9,2885-2894.
15. DeBaun, M. R., Niemitz, E. L., and Feinberg, A. P. (2003). Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epige-netic alterations of LIT1 and H19. Am. J. Hum. Genet. 72,156-160.
16. Denomme, M. M., Zhang, L., and Mann, M. R. (2011). Embryonic imprinting perturbations do not originate from superovulation-induced defects in DNA methylation acquisition. Fertil. Steril. 96, 734-738.e732.
17. Deroo, B. J., Rodriguez, K. F., Couse, J. E, Hamilton, K. J., Collins, J. B., Gris-som, S. F., and Korach, K. S. (2009). Estrogen receptor beta is required for optimal cAMP production in mouse granulosa cells. Mol. Endocrinol. 23, 955-965.
18. Doornbos, M. E., Maas, S. M., Mcdon-nell, J., Vermeiden, J. P., and Hen-nekam, R. C. (2007). Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Hum. Reprod. 22, 2476-2480.
19. Drummond, A. E., and Fuller, P. J. (2011). Activin and inhibin, estrogens and NFΚB, play roles in ovarian tumourigenesis is there crosstalk? Mol. Cell. Endocrinol. 359, 85-91.
20. Dupont, S., Krust, A., Gansmuller, A., Dierich, A., Chambon, P., and Mark, M. (2000). Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127, 4277-4291.
21. Eggermann, T. (2010). Russell-Silver syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 154C, 355-364.
22. Emmen, J. M., Couse, J. F., Elmore, S. A., Yates, M. M., Kissling, G. E., and Korach, K. S. (2005). In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER) {alpha} and ER{beta} null mice indicate a role for ER{beta} in follic-ular maturation. Endocrinology 146, 2817-2826.
23. Gicquel, C., Gaston, V., Mandelbaum, J., Siffroi, J. P., Flahault, A., and Le Bouc, Y. (2003). In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am. J. Hum. Genet. 72, 1338-1341.
24. Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159-177.
25. Halliday, J., Oke, K., Breheny, S., Algar, E., and Amor, D. J. (2004). Beckwith-Wiedemann syndrome and IVF: a case-control study. Am. J. Hum. Genet. 75, 526-528.
26. Harris, A. L. (2001). Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 34, 325-472.
27. Hiura, H., Obata, Y., Komiyama, J., Shirai, M., and Kono, T. (2006). Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11, 353-361.
28. Inzunza, J., Morani, A., Cheng, G., Warner, M., Hreinsson, J., Gustafsson, J. A., and Hovatta, O. (2007). Ovarian wedge resection restores fertility in estrogen receptor beta knockout (ERbeta-/-) mice. Proc. Natl. Acad. Sci. U.S.A. 104, 600-605.
29. Kafri, T., Ariel, M., Brandeis, M., She-mer, R., Urven, L., Mccarrey, J., Cedar, H., and Razin, A. (1992). Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 6, 705-714.
30. Kerjean, A., Couvert, P., Heams, T., Chalas, C., Poirier, K., Chelly, J., Jouannet, P., Paldi, A., and Poirot, C. (2003). In vitro follicular growth affects oocyte imprinting establishment in mice. Eur. J. Hum. Genet. 11, 493-496.
31. Kidder, G. M., and Mhawi, A. A. (2002). Gap junctions and ovarian folliculogenesis. Reproduction 123, 613-620.
32. Kidder, G. M., and Vanderhyden, B. C. (2010). Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can. J. Physiol. Pharmacol. 88, 399-413.
33. Krege, J. H., Hodgin, J. B., Couse, J. F., Enmark, E., Warner, M., Mahler, J. F., Sar, M., Korach, K. S., Gustafsson, J. A., and Smithies, O. (1998). Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc. Natl. Acad. Sci. U.S.A. 95, 15677-15682.
34. Lennerz, J. K., Timmerman, R. J., Grange, D. K., DeBaun, M. R., Feinberg, A. P., and Zehn-bauer, B. A. (2010). Addition of H19 'loss of methylation testing' for Beckwith-Wiedemann syndrome (BWS) increases the diagnostic yield. J. Mol. Diagn. 12, 576-588.
35. Li, T. Y., Colley, D., Barr, K. J., Yee, S. P., and Kidder, G. M. (2007). Rescue of oogenesis in Cx37-null mutant mice by oocyte-specific replacement with Cx43.J. Cell Sci. 120,4117-4125.
36. Li, Y., and Sasaki, H. (2011). Genomic imprinting in mammals: its life cycle, molecular mechanisms and repro-gramming. Cell Res. 21, 466-473.
37. Lim, D., Bowdin, S. C., Tee, L., Kirby, G. A., Blair, E., Fryer, A., Lam, W., Oley, C., Cole, T., Brue-ton, L. A., Reik, W., Macdonald, E, and Maher, E. R. (2009). Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies. Hum. Reprod. 24, 741-747.
38. Lucifero, D., Mann, M. R., Bartolomei, M. S., and Trasler, J. M. (2004). Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet. 13, 839-849.
39. Ludwig, M., Katalinic, A., Gross, S., Sut-cliffe, A., Varon, R., and Horsthemke, B. (2005). Increased prevalence of imprinting defects in patients with Angelman syndrome born to sub-fertile couples. J. Med. Genet. 42, 289-291.
40. Mabb, A. M., Judson, M. C., Zylka, M. J., and Philpot, B. D. (2011). Angelman syndrome: insights into genomic imprinting and neurodevel-opmental phenotypes. Trends Neu-rosci. 34, 293-303.
41. Maher, E. R., Brueton, L. A., Bowdin, S. C., Luharia, A., Cooper, W., Cole, T. R., Macdonald, F., Sampson, J. R., Barratt, C. L., Reik, W., and Hawkins, M. M. (2003). Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J. Med. Genet. 40, 62-64.
42. Market-Velker, B. A., Zhang, L., Magri, L. S., Bonvissuto, A. C., and Mann, M. R. (2010). Dual effects of super-ovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum. Mol. Genet. 19,36-51.
43. Matzuk, M. M., Burns, K. H., Viveiros, M. M., and Eppig, J. J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178-2180.
44. Orstavik, K. H., Eiklid, K., Van Der Hagen, C. B., Spetalen, S., Kierulf, K., Skjeldal, O., and Buiting, K. (2003). Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am. J. Hum. Genet. 72,218-219.
45. Rossignol, S., Steunou, V., Chalas, C., Kerjean, A., Rigolet, M., Viegas-Pequignot, E., Jouannet, P., Le Bouc, Y., and Gicquel, C. (2006). The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region. J. Med. Genet. 43, 902-907.
46. Sato, A., Otsu, E., Negishi, H., Utsunomiya, T., and Arima, T. (2007). Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum. Reprod. 22, 26-35.
47. Simon, A. M., Goodenough, D. A., Li, E., and Paul, D. L. (1997). Female infertility in mice lacking connexin 37. Nature 385, 525-529.
48. Song, Z., Min, L., Pan, Q., Shi, Q., and Shen, W. (2009). Maternal imprinting during mouse oocyte growth in vivo and in vitro. Biochem. Biophys. Res. Commun. 387, 800-805.
49. Su, Y Q., Sugiura, K., and Eppig, J. J. (2009). Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin. Reprod. Med. 27, 32-42.
50. Trapphoff, T., El Hajj, N., Zechner, U., Haaf, T., and Eichenlaub-Ritter, U. (2010). DNA integrity, growth pattern, spindle formation, chromosomal constitution and imprinting patterns of mouse oocytes from vitrified pre-antral follicles. Hum. Reprod. 25,3025-3042.
51. Turner, C. L., Mackay, D. M., Call-away, J. L., Docherty, L. E., Poole, R. L., Bullman, H., Lever, M., Castle, B. M., Kivuva, E. C., Turnpenny, P. D., Mehta, S. G., Man-sour, S., Wakeling, E. L., Mathew, V., Madden, J., Davies, J. H., and Temple, I. K. (2010). Methylation analysis of 79 patients with growth restriction reveals novel patterns of methylation change at imprinted loci. Eur. J. Hum. Genet. 18, 648-655.
52. Ueda, T., Abe, K., Miura, A., Yuzuriha, M., Zubair, M., Noguchi, M., Niwa, K., Kawase, Y., Kono, T., Mat-suda, Y., Fujimoto, H., Shibata, H., Hayashizaki, Y., and Sasaki, H. (2000). The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 5, 649-659.
53. Verona, R. I., Mann, M. R., and Bar-tolomei, M. S. (2003). Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu. Rev. Cell Dev. Biol. 19,237-259.
54. Weksberg, R., Shuman, C., and Beckwith, J. B. (2010). Beckwith-Wiedemann syndrome. Eur. J. Hum. Genet. 18,8-14.