A requirement for fatty acid oxidation in the hormone-induced meiotic maturation of mouse oocytes

Biology of Reproduction

Volumn 89, Issue 2, 2013, Pages

  Valsangkar, Deepa ^a   Downs, Stephen M ^a  

^a Marquette University   (United States)

Author keywords

AMPK; Fatty acid oxidation; Meiotic resumption; Oocyte maturation; PRKA

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ACYL COENZYME A; AMPHIREGULIN; CARNITINE; CARNITINE PALMITOYLTRANSFERASE I; CHORIONIC GONADOTROPIN; EPIDERMAL GROWTH FACTOR; ETOMOXIR; FOLLITROPIN; MALONYL COENZYME A; PALMITIC ACID; THIOGLYCOLIC ACID; 2-MERCAPTOACETATE; 5 AMINO 4 IMIDAZOLECARBOXAMIDE; AICA RIBONUCLEOTIDE; AMINOPHENOL DERIVATIVE; DRUG DERIVATIVE; EPOXIDE; FATTY ACID; GLYCOPROTEIN; HYDRAZONE DERIVATIVE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RIBONUCLEOTIDE; RSVA405; SIGNAL PEPTIDE; THIOGLYCOLIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CUMULUS CELL; FATTY ACID OXIDATION; FEMALE; GERMINAL VESICLE; HORMONAL REGULATION; MEIOSIS; METABOLISM; MITOCHONDRION; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; AMPK; ANIMAL; DRUG EFFECT; MEIOTIC RESUMPTION; OVARY FOLLICLE; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PRKA;

AMPK; FATTY ACID OXIDATION; MEIOTIC RESUMPTION; OOCYTE MATURATION; PRKA;

ACYL COENZYME A; AMINOIMIDAZOLE CARBOXAMIDE; AMINOPHENOLS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CUMULUS CELLS; EPIDERMAL GROWTH FACTOR; EPOXY COMPOUNDS; FATTY ACIDS; FEMALE; FOLLICLE STIMULATING HORMONE; GLYCOPROTEINS; HYDRAZONES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALONYL COENZYME A; MEIOSIS; MICE; OOCYTES; OVARIAN FOLLICLE; OXIDATION-REDUCTION; RIBONUCLEOTIDES; THIOGLYCOLATES;

EID: 84886914149     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.109058     Document Type: Article

References (58)

1. Han SJ, Conti M. New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate. Cell Cycle 2006; 5: 227-231.
2. Hardie DG, Carling D, Carlson M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu Rev Biochem 1998; 67:821-855.
3. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 2011; 25:1895-1908.
4. Chen J, Hudson E, Chi MM, Chang AS, Moley KH, Hardie DG, Downs SM. AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev Biol 2006; 291:227-238.
5. Chen J, Downs SM. AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev Biol 2008; 313:47-57.
6. LaRosa C, Downs SM. Stress stimulates AMP-activated protein kinase and meiotic resumption in mouse oocytes. Biol Reprod 2006; 74:585-592.
7. LaRosa C, Downs SM. Meiotic induction by heat stress in mouse oocytes: involvement of AMP-activated protein kinase and MAPK family members. Biol Reprod 2007; 76:476-486.
8. Corton JM, Gillespie JG, Hawley SA, Hardie DG. 5-Aminoimidazole-4- carboxamide ribonucleoside. A specific method for activating AMPactivated protein kinase in intact cells? Eur J Biochem 1995; 229:558-565.
9. Vingtdeux V , Chandakkar P, Zhao H, d'Abramo C, Davies P, Marambaud P. Novel synthetic small-molecule activators of AMPK as enhancers of autophagy and amyloid-b peptide degradation. FASEB J 2011; 25: 219-231.
10. Downs SM, Hudson ER, Hardie DG. A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev Biol 2002; 245: 200-212.
11. Ya R, Downs SM. Perturbing microtubule integrity blocks AMP-activated protein kinase-induced meiotic resumption in cultured mouse oocytes. Zygote (in press), published online ahead of print 16 November 2012 as DOI:10.1017/S0967199412000457.
12. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, et al. Role of AMPactivated protein kinase in mechanism of metformin action. J Clin Invest 2001; 108:1167-1174.
13. Hardie DG, Pan DA. Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochem Soc Trans 2002; 30: 1064-1070.
14. Biggers JD, Whittingham DG, Donahue RP. The pattern of energy metabolism in the mouse oocyte and zygote. Proc Natl Acad Sci U S A 1967; 58:560-567.
15. Downs SM, Humpherson PG, Leese HJ. Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol Reprod Dev 2002; 62:113-123.
16. Harris SE, Leese HJ, Gosden RG, Picton HM. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol Reprod Dev 2009; 76:231-238.
17. Sutton-McDowall ML, Gilchrist RB, Thompson JG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction (Cambridge) 2010; 139:685-695.
18. Donahue RP , Stern S. Follicular cell support of oocyte maturation: production of pyruvate in vitro. J Reprod Fertil 1968; 17:395-398.
19. Leese HJ, Barton AM. Production of pyruvate by isolated mouse cumulus cells. J Exp Zool 1985; 234:231-236.
20. Fagbohun C F, Downs SM. Requirement for glucose in ligand-stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes. J Reprod Fertil 1992; 96:681-697.
21. Downs SM, Mastropolo AM. The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev Biol 1994; 162: 154-168.
22. Colton SA, Humpherson PG, Leese HJ, Downs SM. Physiological changes in oocyte-cumulus cell complexes from diabetic mice that potentially influence meiotic regulation. Biol Reprod 2003; 69:761-770.
23. Chang AS, Dale AN, Moley KH. Maternal diabetes adversely affects preovulatory oocyte maturation, development, and granulosa cell apoptosis. Endocrinology 2005; 146:2445-2453.
24. Ratchford AM , Chang AS, Chi MM-Y, Sheridan R, Moley KH. Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. Am J Physiol Endocrinol Metab 2007; 293:E1198-E1206.
25. Kim K, Kim CH, Moley KH, Cheon Y-P. Disordered meiotic regulation of oocytes by duration of diabetes mellitus in BBdp rat. Reprod Sci 2007; 14: 467-474.
26. Loewenstein JE, Cohen AI. Dry mass, lipid content and protein content of the intact and zona-free mouse ovum. J Embryol Exp Morphol 1964; 12: 113-121.
27. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 2000; 118:163-170.
28. Sturmey RG , Reis A, Leese HJ, McEvoy TG. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim 2009; 44(Suppl 3):50-58.
29. Songsasen N. Energy metabolism regulating mammalian oocyte maturation. In: Swan A (ed.), Meiosis - Molecular Mechanisms and Cytogenetic Diversity. InTech; 2012:174-186.
30. Cetica P, Pintos L, Dalvit G, Beconi M. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction (Cambridge) 2002; 124:675-681.
31. Ferguson E M, Leese HJ. A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev 2006; 73:1195-1201.
32. Downs SM, Mosey JL, Klinger J. Fatty acid oxidation and meiotic resumption in mouse oocytes. Mol Reprod Dev 2009; 76:844-853.
33. Declercq PE, Falck JR, Kuwajima M, Tyminski H, Foster DW, McGarry JD. Characterization of the mitochondrial carnitine palmitoyltransferase enzyme system. I. Use of inhibitors. J Biol Chem 1987; 262:9812-9821.
34. Bauché F, Sabourault D, Giudicelli Y, Nordmann J, Nordmann R. 2- Mercaptoacetate administration depresses the beta-oxidation pathway through an inhibition of long-chain acyl-CoA dehydrogenase activity. Biochem J 1981; 196:803-809.
35. Thupari JN , Landree LE, Ronnett GV, Kuhajda FP. C75 increases peripheral energy utilization and fatty acid oxidation in diet-induced obesity. Proc Natl Acad Sci U S A 2002; 99:9498-9502.
36. Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol Reprod 2010; 83: 909-918.
37. Sturmey RG, Leese HJ. Energy metabolism in pig oocytes and early embryos. Reproduction (Cambridge) 2003; 126:197-204.
38. Dunning KR , Akison LK, Russell DL, Norman RJ, Robker RL. Increased beta-oxidation and improved oocyte developmental competence in response to L-carnitine during ovarian in vitro follicle development in mice. Biol Reprod 2011; 85:548-555.
39. Abdelrazik H, Sharma R, Mahfouz R, Agarwal A. L-Carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos. Fertil Steril 2009; 91:589-596.
40. Wu G-Q, Jia B-Y, Li J-J, Fu X-W, Zhou G-B, Hou Y-P, Zhu S-E. LCarnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs. Theriogenology 2011; 76:785-793.
41. Somfai T, Kaneda M, Akagi S, Watanabe S, Haraguchi S, Mizutani E, Dang-Nguyen TQ, Geshi M, Kikuchi K, Nagai T. Enhancement of lipid metabolism with L-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes. Reprod Fertil Dev 2011; 23:912-920.
42. You J, Lee J, Hyun S-H, Lee E. L-Carnitine treatment during oocyte maturation improves in vitro development of cloned pig embryos by influencing intracellular glutathione synthesis and embryonic gene expression. Theriogenology 2012; 78:235-243.
43. Ye J, Li J , Yu Y, Wei Q, Deng W, Yu L. L-Carnitine attenuates oxidant injury in HK-2 cells via ROS-mitochondria pathway. Regul Pept 2010; 161:58-66.
44. Dunning KR, Robker RL. Promoting lipid utilization with L-carnitine to improve oocyte quality. Anim Reprod Sci 2012; 134:69-75.
45. Kane MT. Fatty acids as energy sources for culture of one-cell rabbit ova to viable morulae. Biol Reprod 1979; 20:323-332.
46. Ya R, Downs SM. Suppression of chemically induced and spontaneous mouse oocyte activation by AMP-activated protein kinase. Biol Reprod 2013; 88:70.
47. Cho W K, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool 1974; 187:383-386.
48. Weis BC, Cowan AT, Brown N, Foster DW, McGarry JD. Use of a selective inhibitor of liver carnitine palmitoyltransferase I (CPT I) allows quantification of its contribution to total CPT I activity in rat heart. Evidence that the dominant cardiac CPT I isoform is identical to the skeletal muscle enzyme. J Biol Chem 1994; 269:26443-26448.
49. McGarry JD, Leatherman GF, Foster DW. Carnitine palmitoyltransferase I. The site of inhibition of hepatic fatty acid oxidation by malonyl-CoA. J Biol Chem 1978; 253:4128-4136.
50. Downs SM, Daniel SA, Eppig JJ. Induction of maturation in cumulus cellenclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J Exp Zool 1988; 245:86-96.
51. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004; 303:682-684.
52. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 2006; 20:1352-1365.
53. Downs SM, Chen J. EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 2008; 75: 105-114.
54. Downs SM. R egulation of the G2/M transition in rodent oocytes. Mol Reprod Dev 2010; 77:566-585.
55. Hardie DG, Hawley SA, Scott JW. AMP-activated protein kinasedevelopment of the energy sensor concept. J Physiol (Lond) 2006; 574: 7-15.
56. Downs SM . Mouse versus rat: profound differences in meiotic regulation at the level of the isolated oocyte. Mol Reprod Dev 2011; 78:778-794.
57. Sturmey RG , O'Toole PJ, Leese HJ. Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction (Cambridge) 2006; 132:829-837.
58. Wang H, Fang J, Kuang X, Miao L, Wang C, Xia G, King ML, Zhang J. Activity of long-chain acyl-CoA synthetase is required for maintaining meiotic arrest in Xenopus laevis. Biol Reprod 2012; 87:74.