Oocytes isolated from dairy cows with reduced ovarian reserve have a high frequency of aneuploidy and alterations in the localization of progesterone receptor membrane component 1 and aurora kinase b

Biology of Reproduction

Volumn 88, Issue 3, 2013, Pages

  Luciano, Alberto Maria ^a   Franciosi, Federica ^a   Lodde, Valentina ^a   Tessaro, Irene ^a   Corbani, Davide ^a   Modina, Silvia Clotilde ^a   Peluso, John J ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Aneuploidy; Antral follicle count; AURKB; Infertility; Meiosis; Oocyte; Ovary; PGRMC1; Premature ovarian failure

Indexed keywords

AURORA B KINASE; MESSENGER RNA; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR MEMBRANE COMPONENT 1; UNCLASSIFIED DRUG;

ANEUPLOIDY; ANIMAL TISSUE; ARTICLE; CHROMOSOME; CONTROLLED STUDY; DAIRY CATTLE; FEMALE; IN VITRO STUDY; KARYOTYPE; NONHUMAN; OOCYTE; OOCYTE MATURATION; OVARIAN RESERVE; OVARY; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANEUPLOIDY; ANIMALS; CATTLE; CELLS, CULTURED; FEMALE; OOCYTES; OVARIAN FOLLICLE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, PROGESTERONE;

EID: 84877016023     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.106856     Document Type: Article

References (44)

1. Monget P, Bobe J, Gougeon A, Fabre S, Monniaux D, Dalbies-Tran R. The ovarian reserve in mammals: a functional and evolutionary perspective. Mol Cell Endocrinol 2012; 356:2-12.
2. Ireland JJ, Smith GW, Scheetz D, Jimenez-Krassel F, Folger JK, Ireland JL, Mossa F, Lonergan P, Evans AC. Does size matter in females? An overview of the impact of the high variation in the ovarian reserve on ovarian function and fertility, utility of anti-Mullerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod Fertil Dev 2011; 23:1-14.
3. Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian nongrowing follicle number from birth to menopause. Hum Reprod 2008; 23:699-708.
4. Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev 2009; 30:465-493.
5. De Vos M, Devroey P, Fauser BC. Primary ovarian insufficiency. Lancet 2010; 376:911-921.
6. Rosen MP, Johnstone E, Addauan-Andersen C, Cedars MI. A lower antral follicle count is associated with infertility. Fertil Steril 2011; 95:1950-1954.
7. Modina SC, Tessaro I, Lodde V, Franciosi F, Corbani D, Luciano AM. Reductions in the number of mid-sized antral follicles are associated with markers of premature ovarian senescence in dairy cows. Reprod Fertil Dev 2013; (in press). Published online 18 January 2013; http://dx.doi.org/10.1071/RD12295.
8. Modina S, Borromeo V, Luciano AM, Lodde V, Franciosi F, Secchi C. Relationship between growth hormone concentrations in bovine oocytes and follicular fluid and oocyte developmental competence. Eur J Histochem 2007; 51:173-180.
9. Tessaro I, Luciano AM, Franciosi F, Lodde V, Corbani D, Modina SC. The endothelial nitric oxide synthase/nitric oxide system is involved in the defective quality of bovine oocytes from low mid-antral follicle count ovaries. J Anim Sci 2011; 89:2389-2396.
10. Handel MA, Schimenti JC. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 2010; 11:124-136.
11. Yanowitz J. Meiosis: making a break for it. Curr Opin Cell Biol 2010; 22:744-751.
12. Fragouli E, Wells D, Delhanty JD. Chromosome abnormalities in the human oocyte. Cytogenet Genome Res 2011; 133:107-118.
13. Jones KT, Lane SI. Chromosomal, metabolic, environmental, and hormonal origins of aneuploidy in mammalian oocytes. Exp Cell Res 2012; 318:1394-1399.
14. Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 2007; 8:379-393.
15. Sun SC, Kim NH. Spindle assembly checkpoint and its regulators in meiosis. Hum Reprod Update 2012; 18:60-72.
16. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, van Meel J, Rieder CL, Peters JM. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 2003; 161:281-294.
17. Carmena M, Earnshaw WC. The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 2003; 4:842-854.
18. Ota T, Suto S, Katayama H, Han ZB, Suzuki F, Maeda M, Tanino M, Terada Y, Tatsuka M. Increased mitotic phosphorylation of histone H3 attributable to AIM-1/Aurora-B overexpression contributes to chromosome number instability. Cancer Res 2002; 62:5168-5177.
19. Fu J, Bian M, Jiang Q, Zhang C. Roles of Aurora kinases in mitosis and tumorigenesis. Mol Cancer Res 2007; 5:1-10.
20. Luciano AM, Lodde V, Franciosi F, Ceciliani F, Peluso JJ. Progesterone receptor membrane component 1 expression and putative function in bovine oocyte maturation, fertilization, and early embryonic development. Reproduction 2010; 140:663-672.
21. Luciano AM, Franciosi F, Modina SC, Lodde V. Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol Reprod 2011; 85:1252-1259.
22. Luciano AM, Lodde V, Beretta MS, Colleoni S, Lauria A, Modina S. Developmental capability of denuded bovine oocyte in a Co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 30, 50-monophosphate, and glutathione. Mol Reprod Dev 2005; 71:389-397.
23. Takeuchi T, Ergun B, Huang TH, Rosenwaks Z, Palermo GD. A reliable technique of nuclear transplantation for immature mammalian oocytes. Hum Reprod 1999; 14:1312-1317.
24. Lundsteen C, Lind AM. A test of a climate room for preparation of chromosome slides. Clin Genet 1985; 28:260-262.
25. Modina S, Beretta M, Lodde V, Lauria A, Luciano AM. Cytoplasmic changes and developmental competence of bovine oocytes cryopreserved without cumulus cells. Eur J Histochem 2004; 48:337-346.
26. Lazzari G, Tessaro I, Crotti G, Galli C, Hoffmann S, Bremer S, Pellizzer C. Development of an in vitro test battery for assessing chemical effects on bovine germ cells under the ReProTect umbrella. Toxicol Appl Pharmacol 2008; 233:360-370.
27. Luciano AM, Franciosi F, Lodde V, Corbani D, Lazzari G, Crotti G, Galli C, Pellizzer C, Bremer S, Weimer M, Modina SC. Transferability and inter-laboratory variability assessment of the in vitro bovine oocyte maturation (IVM) test within ReProTect. Reprod Toxicol 2010; 30:81-88.
28. Shuda K, Schindler K, Ma J, Schultz RM, Donovan PJ. Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol Reprod Dev 2009; 76:1094-1105.
29. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 2003; 161:267-280.
30. Hassold T, Hall H, Hunt P. The origin of human aneuploidy: where we have been, where we are going. Hum Mol Genet 2007; 16(Spec No. 2): R203-R208.
31. Pellestor F, Anahory T, Hamamah S. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet Genome Res 2005; 111:206-212.
32. Tatone C, Amicarelli F, Carbone MC, Monteleone P, Caserta D, Marci R, Artini PG, Piomboni P, Focarelli R. Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update 2008; 14:131-142.
33. Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R. The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 2002; 157:219-229.
34. Revenkova E, Jessberger R. Keeping sister chromatids together: cohesins in meiosis. Reproduction 2005; 130:783-790.
35. Vogt E, Kipp A, Eichenlaub-Ritter U. Aurora kinase B, epigenetic state of centromeric heterochromatin and chiasma resolution in oocytes. Reprod Biomed Online 2009; 19:352-368.
36. Uzbekova S, Arlot-Bonnemains Y, Dupont J, Dalbies-Tran R, Papillier P, Pennetier S, Thelie A, Perreau C, Mermillod P, Prigent C, Uzbekov R. Spatio-temporal expression patterns of aurora kinases a, B, and C and cytoplasmic polyadenylation-element-binding protein in bovine oocytes during meiotic maturation. Biol Reprod 2008; 78:218-233.
37. Neubauer H, Adam G, Seeger H, Mueck AO, Solomayer E, Wallwiener D, Cahill MA, Fehm T. Membrane-initiated effects of progesterone on proliferation and activation of VEGF in breast cancer cells. Climacteric 2009; 12:230-239.
38. Neubauer H, Clare SE, Wozny W, Schwall GP, Poznanovic S, Stegmann W, Vogel U, Sotlar K, Wallwiener D, Kurek R, Fehm T, Cahill MA. Breast cancer proteomics reveals correlation between estrogen receptor status and differential phosphorylation of PGRMC1. Breast Cancer Res 2008; 10:R85.
39. Nousiainen M, Sillje HH, Sauer G, Nigg EA, Korner R. Phosphoproteome analysis of the human mitotic spindle. Proc Natl Acad Sci U S A 2006; 103:5391-5396.
40. Lodde V, Peluso JJ. A novel role for progesterone and progesterone receptor membrane component 1 in regulating spindle microtubule stability during rat and human ovarian cell mitosis. Biol Reprod 2011; 84:715-722.
41. Vader G, Lens SM. The Aurora kinase family in cell division and cancer. Biochim Biophys Acta 2008; 1786:60-72.
42. Peluso JJ, Lodde V, Liu X. Progesterone regulation of progesterone receptor membrane component 1 (PGRMC1) sumoylation and transcriptional activity in spontaneously immortalized granulosa cells. Endocrinology 2012; 153:3929-3939.
43. Geiss-Friedlander R, Melchior F. Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 2007; 8:947-956.
44. Wang ZB, Ou XH, Tong JS, Li S, Wei L, Ouyang YC, Hou Y, Schatten H, Sun QY. The SUMO pathway functions in mouse oocyte maturation. Cell Cycle 2010; 9:2640-2646.