Bi-directional communication with the cumulus cells is involved in the deficiency of XY oocytes in the components essential for proper second meiotic spindle assembly

Developmental Biology

Volumn 385, Issue 2, 2014, Pages 242-252

  Xu, Baozeng ^a   Noohi, Saeid ^a   Shin, Jonghyun S ^a   Tan, Seang Lin ^a,b   Taketo, Teruko ^a,b  

^a ROYAL VICTORIA HOSPITAL   (Canada)

^b Montreal Reproductive Centre   (Canada)

Author keywords

ATP; Cumulus cells; Glycolysis; Meiotic spindle; Oocyte; XY female mouse

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; CUMULUS CELL; DEVELOPMENTAL GENE; DISORDER OF SEX DEVELOPMENT; DOWN REGULATION; FEMALE; GENE EXPRESSION REGULATION; GENE SEQUENCE; GLYCOLYSIS; LDH1 GENE; MEIOTIC SPINDLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PFKP GENE; PKM2 GENE; PRIORITY JOURNAL;

ATP; CUMULUS CELLS; GLYCOLYSIS; MEIOTIC SPINDLE; OOCYTE; XY FEMALE MOUSE;

ANIMALS; BASE SEQUENCE; CULTURE MEDIA; CUMULUS CELLS; DNA PRIMERS; GENE EXPRESSION; GLYCOLYSIS; MEIOSIS; MICE; MICROSCOPY, CONFOCAL; MILRINONE; OOCYTES; REAL-TIME POLYMERASE CHAIN REACTION; SPINDLE APPARATUS; X CHROMOSOME; Y CHROMOSOME;

EID: 84891632348     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.11.004     Document Type: Article

References (64)

1. TIR sex-reversed mouse ovary. Reproduction 2008, 135:241-252.
2. TIR and XX cells. Biol. Reprod. 1998, 58:574-582.
3. DOM sex-reversed female mouse for maturation, fertilization, and embryonic development in vitro. Dev. Biol. 1996, 178:263-275.
4. TIR sex-reversed female mouse. Dev. Biol. 2000, 219:277-286.
5. Assidi M., Montag M., Van der Ven K., Sirard M.A. Biomarkers of human oocyte developmental competence expressed in cumulus cells before ICSI: a preliminary study. J. Assist. Reprod. Genet. 2011, 28:173-188.
6. Assou S., Haouzi D., Mahmoud K., Aouacheria A., Guillemin Y., Pantesco V., Reme T., Dechaud H., De Vos J., Hamamah S. A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol. Hum. Reprod. 2008, 14:711-719.
7. Ata B., Kaplan B., Danzer H., Glassner M., Opsahl M., Tan S.L., Munne S. Array CGH analysis shows that aneuploidy is not related to the number of embryos generated. Reprod. Biomed. Online 2012, 24:614-620.
8. Battaglia D.E., Goodwin P., Klein N.A., Soules M.R. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 1996, 11:2217-2222.
9. Biggers J.D., Whittingham D.G., Donahue R.P. The pattern of energy metabolism in the mouse oocyte and zygote. Proc. Nat. Acad. Sci. U.S.A. 1967, 58:560-567.
10. Broekmans F.J., Visser J.A., Laven J.S., Broer S.L., Themmen A.P., Fauser B.C. Anti-Mullerian hormone and ovarian dysfunction. Trends Endocrinol. Metab. 2008, 19:340-347.
11. Buccione R., Schroeder A.C., Eppig J.J. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol. Reprod. 1990, 43:543-547.
12. Buccione R., Vanderhyden B.C., Caron P.J., Eppig J.J. FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev. Biol. 1990, 138:16-25.
13. Cillo F., Brevini T.A., Antonini S., Paffoni A., Ragni G., Gandolfi F. Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 2007, 134:645-650.
14. Combelles C.M., Albertini D.F. Assessment of oocyte quality following repeated gonadotropin stimulation in the mouse. Biol. Reprod. 2003, 68:812-821.
15. Diaz F.J., Wigglesworth K., Eppig J.J. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J. Cell Sci. 2007, 120:1330-1340.
16. Donahue R.P., Stern S. Follicular cell support of oocyte maturation: production of pyruvate in vitro. J. Reprod. Fertil. 1968, 17:395-398.
17. Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N., Matzuk M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996, 383:531-535.
18. Downs S.M. The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev. Biol. 1995, 167:502-512.
19. Downs S.M., Utecht A.M. Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes. Biol. Reprod. 1999, 60:1446-1452.
20. Dube J.L., Wang P., Elvin J., Lyons K.M., Celeste A.J., Matzuk M.M. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 1998, 12:1809-1817.
21. Dumollard R., Campbell K., Halet G., Carroll J., Swann K. Regulation of cytosolic and mitochondrial ATP levels in mouse eggs and zygotes. Dev. Biol. 2008, 316:431-440.
22. Durlinger A.L., Kramer P., Karels B., de Jong F.H., Uilenbroek J.T., Grootegoed J.A., Themmen A.P. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 1999, 140:5789-5796.
23. Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Kumar T.R., Matzuk M.M., Rose U.M., de Jong F.H., Uilenbroek J.T., Grootegoed J.A., Themmen A.P. Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 2001, 142:4891-4899.
24. Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Ingraham H.A., Nachtigal M.W., Uilenbroek J.T., Grootegoed J.A., Themmen A.P. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002, 143:1076-1084.
25. Eicher E.M., Washburn L.L., Whitney J.B., Morrow K.E. Mus poschiavinus Y chromosome in the C57BL/6J murine genome causes sex reversal. Science 1982, 217:535-537.
26. Eppig J. Mouse oocytes control metabolic co-operativity between oocytes and cumulus cells. Reprod. Fertil. Dev. 2005, 17:1-2.
27. Eppig J.J. Analysis of mouse oogenesis in vitro. Oocyte isolation and the utilization of exogenous energy sources by growing oocytes. J. Exp. Zool. 1976, 198:375-382.
28. Eppig J.J. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001, 122:829-838.
29. Eppig J.J., Pendola F.L., Wigglesworth K., Pendola J.K. Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol. Reprod. 2005, 73:351-357.
30. Gosden R.G., Byatt-Smith J.G. Oxygen concentration gradient across the ovarian follicular epithelium: model, predictions and implications. Hum. Reprod. 1986, 1:65-68.
31. Goud A.P., Goud P.T., Van Oostveldt P., Diamond M.P., Dhont M. Dynamic changes in microtubular cytoskeleton of human postmature oocytes revert after ooplasm transfer. Fertil. Steril. 2004, 81:323-331.
32. Johnson M.T., Freeman E.A., Gardner D.K., Hunt P.A. Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol. Reprod. 2007, 77:2-8.
33. TIR sex reversal. Genesis 2001, 30:7-11.
34. Leese H.J., Barton A.M. Production of pyruvate by isolated mouse cumulus cells. J. Exp. Zool. 1985, 234:231-236.
35. MacArthur C.A., Lawshe A., Xu J., Santos-Ocampo S., Heikinheimo M., Chellaiah A.T., Ornitz D.M. FGF-8 isoforms activate receptor splice forms that are expressed in mesenchymal regions of mouse development. Development 1995, 121:3603-3613.
36. McGrath S.A., Esquela A.F., Lee S.J. Oocyte-specific expression of growth differentiation factor-9. Mol. Endocrinol. 1995, 9:131-136.
37. Nagamine C.M., Taketo T., Koo G.C. Studies on the genetics of tda-1 XY sex reversal in the mouse. Differentiation 1987, 33:223-231.
38. Obata Y., Villemure M., Kono T., Taketo T. Transmission of Y chromosomes from XY female mice was made possible by the replacement of cytoplasm during oocyte maturation. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:13918-13923.
39. Piko L., Chase D.G. Role of the mitochondrial genome during early development in mice: effects of ethidium bromide and chloramphenicol. J. Cell Biol. 1973, 58:357-378.
40. Simon A.M., Goodenough D.A., Li E., Paul D.L. Female infertility in mice lacking connexin 37. Nature 1997, 385:525-529.
41. Stojkovic M., Machado S.A., Stojkovic P., Zakhartchenko V., Hutzler P., Goncalves P.B., Wolf E. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 2001, 64:904-909.
42. Su Y.Q., Sugiura K., Wigglesworth K., O'Brien M.J., Affourtit J.P., Pangas S.A., Matzuk M.M., Eppig J.J. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 2008, 135:111-121.
43. Su Y.Q., Sugiura K., Eppig J.J. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin. Reprod. Med. 2009, 27:32-42.
44. Sugiura K., Eppig J.J. Society for Reproductive Biology Founders' Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reprod. Fertil. Dev. 2005, 17:667-674.
45. Sugiura K., Pendola F.L., Eppig J.J. Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 2005, 279:20-30.
46. Sugiura K., Su Y.Q., Diaz F.J., Pangas S.A., Sharma S., Wigglesworth K., O'Brien M.J., Matzuk M.M., Shimasaki S., Eppig J.J. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007, 134:2593-2603.
47. Sun Q.Y., Schatten H. Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 2006, 131:193-205.
48. Sutton-McDowall M.L., Gilchrist R.B., Thompson J.G. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 2010, 139:685-695.
49. DOM sex-reversed female mouse. Development 1989, 107:95-105.
50. Tsafriri A., Chun S.Y., Zhang R., Hsueh A.J., Conti M. Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 1996, 178:393-402.
51. Valve E., Penttila T.L., Paranko J., Harkonen P. FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem. Biophys. Res. Commun. 1997, 232:173-177.
52. Van Blerkom J., Davis P.W., Lee J. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 1995, 10:415-424.
53. Van Blerkom J., Sinclair J., Davis P. Mitochondrial transfer between oocytes: potential applications of mitochondrial donation and the issue of heteroplasmy. Hum. Reprod. 1998, 13:2857-2868.
54. Villemure M., Chen H.Y., Kurokawa M., Fissore R.A., Taketo T. The presence of X- and Y-chromosomes in oocytes leads to impairment in the progression of the second meiotic division. Dev. Biol. 2007, 301:1-13.
55. Visser J.A., Schipper I., Laven J.S., Themmen A.P. Anti-Mullerian hormone: an ovarian reserve marker in primary ovarian insufficiency. Nat. Rev. Endocrinol. 2012, 8:331-341.
56. Wadsworth P., Salmon E.D. Spindle microtubule dynamics: modulation by metabolic inhibitors. Cell Motil. Cytoskeleton 1988, 11:97-105.
57. Wang Q., Ratchford A.M., Chi M.M., Schoeller E., Frolova A., Schedl T., Moley K.H. Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol. Endocrinol. 2009, 23:1603-1612.
58. Wilding M., Dale B., Marino M., di Matteo L., Alviggi C., Pisaturo M.L., Lombardi L., De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 2001, 16:909-917.
59. Wilding M., Coppola G., Dale B., Di Matteo L. Mitochondria and human preimplantation embryo development. Reproduction 2009, 137:619-624.
60. Xu B., Obata Y., Cao F., Taketo T. The presence of the Y-chromosome, not the absence of the second X-chromosome, alters the mRNA levels stored in the fully grown XY mouse oocyte. PLoS One 2012, 7:e40481.
61. Yan C., Wang P., DeMayo J., DeMayo F.J., Elvin J.A., Carino C., Prasad S.V., Skinner S.S., Dunbar B.S., Dube J.L., Celeste A.J., Matzuk M.M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 2001, 15:854-866.
62. Yu Y., Dumollard R., Rossbach A., Lai F.A., Swann K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell Physiol. 2010, 224:672-680.
63. Zeng H.T., Ren Z., Yeung W.S., Shu Y.M., Xu Y.W., Zhuang G.L., Liang X.Y. Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum. Reprod. 2007, 22:1681-1686.
64. Zhang X., Wu X.Q., Lu S., Guo Y.L., Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 2006, 16:841-850.