Live imaging reveals the link between decreased glucose uptake in ovarian cumulus cells and impaired oocyte quality in female diabetic mice

Endocrinology

Volumn 153, Issue 4, 2012, Pages 1984-1989

  Wang, Qiang ^a   Chi, Maggie M ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 [N (7 NITROBENZ 2 OXA 1,3 DIAZOL 4 YL)AMINO] 6 DEOXYGLUCOSE; ADENOSINE TRIPHOSPHATE; GLUCOSE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMOSOME; CONTROLLED STUDY; CUMULUS CELL; EMBRYO; FEMALE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; IMAGING SYSTEM; LIVE IMAGING; MATERNAL DIABETES MELLITUS; MOUSE; NONHUMAN; OOCYTE MATURATION; OOCYTE QUALITY; OVARY; PRIORITY JOURNAL; QUALITY CONTROL; SPINDLE CELL;

ADENOSINE TRIPHOSPHATE; ANIMALS; CUMULUS CELLS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FEMALE; GLUCOSE; MEIOSIS; MICE; MICE, INBRED STRAINS; MICROSCOPY, FLUORESCENCE; MITOTIC SPINDLE APPARATUS; OOCYTES; OVARY; STREPTOZOCIN;

EID: 84859398172     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1815     Document Type: Article

References (34)

1. Doblado M, Moley KH 2007 Glucose metabolism in pregnancy and embryogenesis. Curr Opin Endocrinol Diabetes Obes 14:488-493 (Pubitemid 350059361)
2. Greene MF 1999 Spontaneous abortions and major malformations in women with diabetes mellitus. Semin Reprod Endocrinol 17:127-136 (Pubitemid 29477720)
3. Amaral S, Oliveira PJ, Ramalho-Santos J 2008 Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev 4:46-54 (Pubitemid 351210972)
4. Colton SA, Pieper GM, Downs SM 2002 Altered meiotic regulation in oocytes from diabetic mice. Biol Reprod 67:220-231 (Pubitemid 34680657)
5. Ratchford AM, Chang AS, Chi MM, Sheridan R, Moley KH 2007 Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. Am J Physiol Endocrinol Metab 293:E1198-E1206 (Pubitemid 350106585)
6. Wang Q, Ratchford AM, Chi MM, Schoeller E, Frolova A, Schedl T, Moley KH 2009 Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol Endocrinol 23:1603-1612
7. Gilchrist RB, Lane M, Thompson JG 2008 Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 14:159-177 (Pubitemid 351321110)
8. Biggers JD, Whittingham DG, Donahue RP 1967 The pattern of energy metabolism in the mouse oocyte and zygote. Proc Natl Acad Sci USA 58:560-567
9. Sugiura K, Eppig JJ 2005 Society for Reproductive Biology Founders' Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reprod Fertil Dev 17:667-674 (Pubitemid 43225310)
10. Chen L, Wert SE, Hendrix EM, Russell PT, Cannon M, Larsen WJ 1990 Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Mol Reprod Dev 26:236-247 (Pubitemid 20199282)
11. Sutton-McDowall ML, Gilchrist RB, Thompson JG 2010 The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139:685-695
12. Sutton-McDowall ML, Gilchrist RB, Thompson JG 2004 Cumulus expansion and glucose utilisation by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128:313-319 (Pubitemid 39242707)
13. Sutton-McDowall ML, Mitchell M, Cetica P, Dalvit G, Pantaleon M, Lane M, Gilchrist RB, Thompson JG 2006 Glucosamine supplementation during in vitro maturation inhibits subsequent embryo development: possible role of the hexosamine pathway as a regulator of developmental competence. Biol Reprod 74:881-888
14. Wang Q, Frolova AI, Purcell S, Adastra K, Schoeller E, Chi MM, Schedl T, Moley KH 2010 Mitochondrial dysfunction and apoptosis in cumulus cells of type I diabetic mice. PLoS One 5:e15901
15. Yamada K, Saito M, Matsuoka H, Inagaki N 2007 A real-time method of imaging glucose uptake in single, living mammalian cells. Nat Protoc 2:753-762 (Pubitemid 47040036)
16. Chi MM, Hoehn A, Moley KH 2002 Metabolic changes in the glucose-induced apoptotic blastocyst suggest alterations in mitochondrial physiology. Am J Physiol Endocrinol Metab 283:E226-E232 (Pubitemid 34827436)
17. Miao YL, Shi LH, Lei ZL, Huang JC, Yang JW, Ouyang YC, Sun QY, Chen DY 2007 Effects of caffeine on in vivo and in vitro oocyte maturation in mice. Theriogenology 68:640-645
18. Hutt KJ, Albertini DF 2007 An oocentric view of folliculogenesis and embryogenesis. Reprod Biomed Online 14:758-764 (Pubitemid 46951711)
19. Colton SA, Humpherson PG, Leese HJ, Downs SM 2003 Physiological changes in oocyte-cumulus cell complexes from diabetic mice that potentially influence meiotic regulation. Biol Reprod 69:761-770 (Pubitemid 37064604)
20. Quinn P, Wales RG 1973 The relationships between the ATP content of preimplantation mouse embryos and their development in vitro during culture. J Reprod Fertil 35:301-309
21. Van Blerkom J, Davis PW, Lee J 1995 ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod 10:415-424
22. Dumollard R, Duchen M, Carroll J 2007 The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol 77:21-49
23. Su YQ, Sugiura K, Eppig JJ 2009 Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 27:32-42
24. Stokes YM, Clark AR, Thompson JG 2008 Mathematical modeling of glucose supply toward successful in vitro maturation of mammalian oocytes. Tissue Eng Part A 14:1539-1547
25. Clark AR, Stokes YM, Thompson JG 2011 Estimation of glucose uptake by ovarian follicular cells. Ann Biomed Eng 39:2654-2667
26. Downs SM 1995 The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev Biol 167:502-512
27. Baird DT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J, Crosignani PG, Devroey P, Diedrich K, Fauser BC, Fraser L, Glasier A, Liebaers I, Mautone G, Penney G, Tarlatzis B 2005 Fertility and ageing. Hum Reprod Update 11:261-276 (Pubitemid 40668111)
28. Johnson MT, Freeman EA, Gardner DK, Hunt PA 2007 Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol Reprod 77:2-8 (Pubitemid 46986390)
29. Zeng HT, Ren Z, Yeung WS, Shu YM, Xu YW, Zhuang GL, Liang XY 2007 Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum Reprod 22:1681-1686 (Pubitemid 47055160)
30. Pan H, Ma P, Zhu W, Schultz RM 2008 Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol 316:397-407
31. Selesniemi K, Lee HJ, Muhlhauser A, Tilly JL 2011 Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc Natl Acad Sci USA 108:12319-12324
32. Li Q, Miao DQ, Zhou P, Wu YG, Gao D, Wei DL, Cui W, Tan JH 2011 Glucose metabolism in mouse cumulus cells prevents oocyte aging by maintaining both energy supply and the intracellular redox potential. Biol Reprod 84:1111-1118
33. Hunt PA, Hassold TJ 2008 Human female meiosis: what makes a good egg go bad? Trends Genet 24:86-93
34. Downs SM, Humpherson PG, Leese HJ 1998 Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol Reprod 58:1084-1094 (Pubitemid 28145002)