Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

Nutrient pathways regulating the nuclear maturation of mammalian oocytes

Stephen M. Downs
+ Author Affiliations
- Author Affiliations

Department of Biological Sciences, Marquette University, 530 N 15 St, Milwaukee, WI 53233, USA. Email: stephen.downs@marquette.edu

Reproduction, Fertility and Development 27(4) 572-582 https://doi.org/10.1071/RD14343
Submitted: 15 September 2014  Accepted: 10 January 2015   Published: 24 March 2015

Abstract

Oocyte maturation is defined as that phase of development whereby a fully grown oocyte reinitiates meiotic maturation, completes one meiotic division with extrusion of a polar body, then arrests at MII until fertilisation. Completion of maturation depends on many different factors, not the least of which is the proper provision of energy substrates to fuel the process. Interaction of the oocyte and somatic compartment of the follicle is critical and involves numerous signals exchanged between the two cell types in both directions. One of the prominent functions of the cumulus cells is the channelling of metabolites and nutrients to the oocyte to help stimulate germinal vesicle breakdown and direct development to MII. This entails the careful integration and coordination of numerous metabolic pathways, as well as oocyte paracrine signals that direct certain aspects of cumulus cell metabolism. These forces collaborate to produce a mature oocyte that, along with accompanying physiological changes called cytoplasmic maturation, which impart subsequent developmental competence to the oocyte, can be fertilised and develop to term. This review focuses on nuclear maturation and the metabolic interplay that regulates it, with special emphasis on data generated in the mouse.

Additional keywords: AMP-activated protein kinase, energy substrates, fatty acid oxidation, germinal vesicle breakdown.


References

Alvarez, G. M., Ferretti, E. L., Gutnisky, C., Dalvit, G. C., and Cetica, P. D. (2013). Modulation of lycolysis and the pentose phosphate pathway influences porcine oocyte in vitro maturation. Reprod. Domest. Anim. 48, 545–553.
Modulation of lycolysis and the pentose phosphate pathway influences porcine oocyte in vitro maturation.CrossRef | 1:CAS:528:DC%2BC3sXhsVersLjN&md5=f499033b43bb39b54c83fdd0b1745b99CAS | 23189959PubMed |

Bae, I.-H., and Chung, S.-O. (1975). The in vitro maturation of the mouse oocyte. Yonsei Med. J. 16, 18–28.
The in vitro maturation of the mouse oocyte.CrossRef | 1:STN:280:DyaE287otVSqsw%3D%3D&md5=4b2aa03f4dba6d396cbe203edf562737CAS | 1224637PubMed |

Bae, I.-H., and Foote, R. H. (1975). Carbohydrate and amino acid requirement and ammonia production of rabbit follicular oocytes matured in vitro. Exp. Cell Res. 91, 113–118.
Carbohydrate and amino acid requirement and ammonia production of rabbit follicular oocytes matured in vitro.CrossRef | 1:CAS:528:DyaE2MXhtV2lsb8%3D&md5=4a454323011f0af9c6c8f108f4f7bf9eCAS | 1169150PubMed |

Biggers, J. D., Whittingham, D. G., and Donahue, R. P. (1967). The pattern of energy metabolism in the mouse oocyte and zygote. Proc. Natl. Acad. Sci. USA 58, 560–567.
The pattern of energy metabolism in the mouse oocyte and zygote.CrossRef | 1:CAS:528:DyaF1cXitVaitw%3D%3D&md5=105f0132de02f2e6e3e05a34afdf2c94CAS | 5233459PubMed |

Bilodeau-Goeseels, S., Sasseville, M., Guillemette, C., and Richard, F. J. (2007). Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Mol. Reprod. Dev. 74, 1021–1034.
Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro.CrossRef | 1:CAS:528:DC%2BD2sXntVOhurY%3D&md5=6afe9a74f23660b7da1f14a4d1759e1aCAS | 17290417PubMed |

Brinster, R. L. (1971). Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J. Reprod. Fertil. 24, 187–191.
Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey.CrossRef | 1:CAS:528:DyaE3MXktlagu7w%3D&md5=8d180dabae462e34f140b1c243770befCAS | 4994572PubMed |

Brison, D. R., and Leese, H. J. (1994). Blastocoel cvity formation by preimplantation rat embryos in the presence of cyanide and other inhibitors of oxidative phosphorylation. J. Reprod. Fertil. 101, 305–309.
Blastocoel cvity formation by preimplantation rat embryos in the presence of cyanide and other inhibitors of oxidative phosphorylation.CrossRef | 1:CAS:528:DyaK2cXmvFOks7k%3D&md5=8f39fad46a856b0853fba902c4eb0c0eCAS | 7932362PubMed |

Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–681.
Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro.CrossRef | 1:CAS:528:DC%2BD3sXht1KksA%3D%3D&md5=b0e1f9983cc565b159bd2412be143d7aCAS | 12417006PubMed |

Chen, J., and Downs, S. M. (2008). AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev. Biol. 313, 47–57.
AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro.CrossRef | 1:CAS:528:DC%2BD1cXhsVOhsg%3D%3D&md5=99ee7500201a7e3e5b5dc3b303823cceCAS | 18048025PubMed |

Chen, J., Hudson, E., Chi, M. M., Chang, A. S., Moley, K. H., Hardie, D. G., and Downs, S. M. (2006). AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev. Biol. 291, 227–238.
AMPK regulation of mouse oocyte meiotic resumption in vitro.CrossRef | 1:CAS:528:DC%2BD28Xis1WisLk%3D&md5=b1e0e8c4db64fbed27491134f569c258CAS | 16443210PubMed |

Crawford, J. L., and McNatty, K. P. (2012). The ratio of growth differentiation factor 9: bone morphogenetic protein 15 mRNA expression is tightly coregulated and differs between species over a wide range of ovulation rates. Mol. Cell. Endocrinol. 348, 339–343.
The ratio of growth differentiation factor 9: bone morphogenetic protein 15 mRNA expression is tightly coregulated and differs between species over a wide range of ovulation rates.CrossRef | 21970812PubMed |

Davies, S. P., Carling, D., Munday, M. R., and Hardie, D. G. (1992). Diurnal rhythm of phosphorylation of rat liver acetyl-CoA carboxylase by the AMP-activated protein kinase, demonstrated using freeze-clamping. Effects of high fat diets. Eur. J. Biochem. 203, 615–623.
Diurnal rhythm of phosphorylation of rat liver acetyl-CoA carboxylase by the AMP-activated protein kinase, demonstrated using freeze-clamping. Effects of high fat diets.CrossRef | 1:CAS:528:DyaK38Xht1Gksbw%3D&md5=5642caab5704e188a7b6e8839836263eCAS | 1346520PubMed |

Dekel, N., Hultborn, R., Hillensjo, T., Hamberger, L., and Kraicer, P. (1976). Effect of luteinizing hormone on respiration of the preovulatory cumulus oophorus of the rat. Endocrinology 98, 498–504.
Effect of luteinizing hormone on respiration of the preovulatory cumulus oophorus of the rat.CrossRef | 1:CAS:528:DyaE28XhsVGht7c%3D&md5=1f1be29c54fead8f3d1e9c49ed92e412CAS | 1248457PubMed |

Donahue, R. P., and Stern, S. (1968). Follicular cell support of oocyte maturation: production of pyruvate in vitro. J. Reprod. Fertil. 17, 395–398.
Follicular cell support of oocyte maturation: production of pyruvate in vitro.CrossRef | 1:STN:280:DyaF1M%2FlsFagtQ%3D%3D&md5=56a14c24b476e9d890e0d7cf02224935CAS | 5723787PubMed |

Downs, S. M., Daniel, S. A. J., and Eppig, J. J. (1988). Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor. J. Exp. Zool. 245, 86–96.
Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor.CrossRef | 1:CAS:528:DyaL1cXht1Ghsr0%3D&md5=735c36780684afb8d8ab14a77cf1bb77CAS | 2832512PubMed |

Downs, S. M. (1998). Precursors of the purine backbone augment the inhibitory action of hypoxanthine and dibutyryl cAMP on mouse oocyte maturation. J. Exp. Zool. 282, 376–384.
Precursors of the purine backbone augment the inhibitory action of hypoxanthine and dibutyryl cAMP on mouse oocyte maturation.CrossRef | 1:CAS:528:DyaK1cXmtlOru74%3D&md5=47c76b4e5bffdfc1f01c225df18e7197CAS | 9755485PubMed |

Downs, S. M. (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.
The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte.CrossRef | 1:CAS:528:DyaK2MXktFagtb0%3D&md5=5048ff2e93b13c1d66d250e5d2ffc68aCAS | 7875374PubMed |

Downs, S. M. (1997a). Involvement of purine nucleotide synthetic pathways in gonadotropin-induced meiotic maturation in mouse cumulus cell-enclosed oocytes. Mol. Reprod. Dev. 46, 155–167.
Involvement of purine nucleotide synthetic pathways in gonadotropin-induced meiotic maturation in mouse cumulus cell-enclosed oocytes.CrossRef | 1:CAS:528:DyaK2sXoslWhuw%3D%3D&md5=0910c5a8c9b018a30c19256feeeb747eCAS | 9021747PubMed |

Downs, S. M. (1997b). Hypoxanthine regulation of oocyte maturation in the mouse: insights using hypoxanthine phosphoribosyltransferase-deficient animals. Biol. Reprod. 57, 54–62.
Hypoxanthine regulation of oocyte maturation in the mouse: insights using hypoxanthine phosphoribosyltransferase-deficient animals.CrossRef | 1:CAS:528:DyaK2sXktFCnur0%3D&md5=2f1c4671573bc5d9eae2c17247bc0fbcCAS | 9209080PubMed |

Downs, S. M. (1998). Precursors of the purine backbone augment the inhibitory action of hypoxanthine and dibuturyl cAMP on mouse oocyte maturation. J. Exp. Zool. 282, 376–384.
Precursors of the purine backbone augment the inhibitory action of hypoxanthine and dibuturyl cAMP on mouse oocyte maturation.CrossRef | 1:CAS:528:DyaK1cXmtlOru74%3D&md5=47c76b4e5bffdfc1f01c225df18e7197CAS | 9755485PubMed |

Downs, S. M. (2010). Regulation of the G2/M transition in rodent oocytes. Mol. Reprod. Dev. 77, 566–585.
Regulation of the G2/M transition in rodent oocytes.CrossRef | 1:CAS:528:DC%2BC3cXotVahsL8%3D&md5=5c8bfa1c5d5a1465977077a6a405b5f6CAS | 20578061PubMed |

Downs, S. M. (2011). Mouse versus rat: profound differences in meiotic regulation at the level of the isolated oocyte. Mol. Reprod. Dev. 78, 778–794.
Mouse versus rat: profound differences in meiotic regulation at the level of the isolated oocyte.CrossRef | 1:CAS:528:DC%2BC3MXhtlagu7vN&md5=b32dc35b9f97595e20b6e81b92f5618cCAS | 21953615PubMed |

Downs, S. M., and Hudson, E. D. (2000). Energy substrates and the completion of spontaneous meiotic maturation. Zygote 8, 339–351.
Energy substrates and the completion of spontaneous meiotic maturation.CrossRef | 1:CAS:528:DC%2BD3cXovF2hsbs%3D&md5=c5c0417194c384c14cf05155dc4a1acfCAS | 11108555PubMed |

Downs, S. M., and Mastropolo, A. M. (1994). The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162, 154–168.
The participation of energy substrates in the control of meiotic maturation in murine oocytes.CrossRef | 1:CAS:528:DyaK2cXhvVyitLs%3D&md5=2810bb97abf7681fce1bb1ef60576930CAS | 8125183PubMed |

Downs, S. M., and Mastropolo, A. M. (1997). Culture conditions affect meiotic regulation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 46, 551–566.
Culture conditions affect meiotic regulation in cumulus cell-enclosed mouse oocytes.CrossRef | 1:CAS:528:DyaK2sXit1aisLk%3D&md5=b56f4d6403477814b2e8653227739100CAS | 9094102PubMed |

Downs, S. M., and Utecht, A. M. (1999). Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes. Biol. Reprod. 60, 1446–1452.
Metabolism of radiolabeled glucose by mouse oocytes and oocyte–cumulus cell complexes.CrossRef | 1:CAS:528:DyaK1MXjsVeisLs%3D&md5=61ffb61e79949557bc72522c89cf3df1CAS | 10330104PubMed |

Downs, S. M., and Verhoeven, A. (2003). Glutamine and the maintenance of meiotic arrest in mouse oocytes: influence of culture medium, glucose, and cumulus cells. Mol. Reprod. Dev. 66, 90–97.
Glutamine and the maintenance of meiotic arrest in mouse oocytes: influence of culture medium, glucose, and cumulus cells.CrossRef | 1:CAS:528:DC%2BD3sXmt1Giu7g%3D&md5=df6c24ae28a14849bd48b96a723b10d2CAS | 12874804PubMed |

Downs, S. M., Humpherson, P. G., Martin, K. L., and Leese, H. J. (1996). Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 44, 121–131.
Glucose utilization during gonadotropin-induced meiotic maturation in cumulus cell-enclosed mouse oocytes.CrossRef | 1:CAS:528:DyaK28XivV2mt7g%3D&md5=edbff842293afae3179f1ba11935bb26CAS | 8722700PubMed |

Downs, S. M., Houghton, F. D., Humpherson, P. G., and Leese, H. J. (1997). Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction. J. Reprod. Fertil. 110, 1–10.
Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction.CrossRef | 1:CAS:528:DyaK2sXksVagu7Y%3D&md5=59a6a134d1d52534a62e6019b33a67f4CAS | 9227351PubMed |

Downs, S. M., Humpherson, P. G., and Leese, H. J. (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58, 1084–1094.
Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway.CrossRef | 1:CAS:528:DyaK1cXit1KhtL0%3D&md5=4046251410f98d275eae874a665548a3CAS | 9546744PubMed |

Downs, S. M., Hudson, E. R., and Hardie, D. G. (2002a). A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev. Biol. 245, 200–212.
A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes.CrossRef | 1:CAS:528:DC%2BD38XjtVegurg%3D&md5=a24cedb5c4a3a6bdd5bba5e1262b2edeCAS | 11969266PubMed |

Downs, S. M., Humpherson, P. G., and Leese, H. J. (2002b). Pyuruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol. Reprod. Dev. 62, 113–123.
Pyuruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus.CrossRef | 1:CAS:528:DC%2BD38XivVChu7s%3D&md5=ddaa22ff872344cc6dfa884bbf220a69CAS | 11933168PubMed |

Downs, S. M., Mosey, J. L., and Klinger, J. (2009). Fatty acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 76, 844–853.
Fatty acid oxidation and meiotic resumption in mouse oocytes.CrossRef | 1:CAS:528:DC%2BD1MXptleht7c%3D&md5=3b14836c82b9bafe20052faa496b7360CAS | 19455666PubMed |

Downs, S. M., Ya, R., and Davis, C. C. (2010). Role of AMPK throughout meiotic maturation in the mouse oocyte: evidence for promotion of polar body formation and suppression of premature activation. Mol. Reprod. Dev. 77, 888–899.
Role of AMPK throughout meiotic maturation in the mouse oocyte: evidence for promotion of polar body formation and suppression of premature activation.CrossRef | 1:CAS:528:DC%2BC3cXhtleqsL3F&md5=e9c7de517d3cdf7a77844f1e40452b49CAS | 20830737PubMed |

Dumollard, R., Ward, Z., Carroll, J., and Duchen, M. R. (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455–465.
Regulation of redox metabolism in the mouse oocyte and embryo.CrossRef | 1:CAS:528:DC%2BD2sXjtlWgs7g%3D&md5=d77b17285158c4c0a7bb0574441c7e1aCAS | 17185319PubMed |

Dunning, K. R., and Robker, R. L. (2012). Promoting lipid utilizataion with l-carnitine to improve oocyte quality. Anim. Reprod. Sci. 134, 69–75.
Promoting lipid utilizataion with l-carnitine to improve oocyte quality.CrossRef | 1:CAS:528:DC%2BC38Xht1eku7jM&md5=b037ce3f34ce65dd0f14af0792effd5eCAS | 22917873PubMed |

Dunning, K. R., Cashman, K., Russell, D. L., Thompson, J. G., Norman, R. J., and Robker, R. L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–918.
Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.CrossRef | 1:CAS:528:DC%2BC3cXhsFahurfN&md5=d2b87b938fd1b9207ccd0d890a41f1beCAS | 20686180PubMed |

Dunning, K. R., Akison, L. K., Russell, D. L., Norman, R. J., and Robker, R. L. (2011). Increased beta- oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice. Biol. Reprod. 85, 548–555.
Increased beta- oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice.CrossRef | 1:CAS:528:DC%2BC3MXhtV2gtLjN&md5=b596b79bfa2373bc4077d0a18bc42acfCAS | 21613630PubMed |

Dunning, K. R., Russell, D. L., and Robker, R. L. (2014). Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation. Reproduction 148, R15–R27.
Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation.CrossRef | 1:CAS:528:DC%2BC2cXhtFyrtrnE&md5=165dea5bbc533770beafa05b87509710CAS | 24760880PubMed |

Eppig, J. J. (1976). Analysis of mouse oogenesis in vitro: oocyte isolation and the utilization of exogenous energy sources by growing oocytes. J. Exp. Zool. 198, 375–381.
Analysis of mouse oogenesis in vitro: oocyte isolation and the utilization of exogenous energy sources by growing oocytes.CrossRef | 1:STN:280:DyaE2s%2FntlWrsA%3D%3D&md5=c1beaf3567a09feae66a51325cc1f889CAS | 1003146PubMed |

Fagbohun, C. F., and Downs, S. M. (1992). Requirement for glucose in ligand-stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes. J. Reprod. Fertil. 96, 681–697.
Requirement for glucose in ligand-stimulated meiotic maturation of cumulus cell-enclosed mouse oocytes.CrossRef | 1:CAS:528:DyaK3sXpvVyqsw%3D%3D&md5=519197178cb7a5d25d4f732c3c810c68CAS | 1339848PubMed |

Ferguson, E. M., and Leese, H. J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–378.
Triglyceride content of bovine oocytes and early embryos.CrossRef | 1:CAS:528:DyaK1MXkslOltbc%3D&md5=7dcf1ca4e4190921db5a3506b5f051d8CAS | 10615263PubMed |

Ferguson, E. M., and Leese, H. J. (2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 73, 1195–1201.
A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development.CrossRef | 1:CAS:528:DC%2BD28XnvFahtr0%3D&md5=f2578182c56ab88a367fbfe61db95607CAS | 16804881PubMed |

Gilchrist, R. B., and Thompson, J. G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.
Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro.CrossRef | 17092551PubMed |

Gutnisky, C., Dalvit, G. C., Thompson, J. G., and Cetica, P. D. (2014). Pentose phosphate pathway activity: effect on in vitro maturation and oxidative status of bovine oocytes. Reprod. Fertil. Dev. 26, 931–942.
Pentose phosphate pathway activity: effect on in vitro maturation and oxidative status of bovine oocytes.CrossRef | 1:CAS:528:DC%2BC2cXhsVClsLvN&md5=5dac80e1d2639a325febf130ab466798CAS | 23859479PubMed |

Gwatkin, R. B. L., and Haidri, A. A. (1973). Requirements for the maturation of hamster oocytes in vitro. Exp. Cell Res. 76, 1–7.
Requirements for the maturation of hamster oocytes in vitro.CrossRef | 1:CAS:528:DyaE3sXlsF2htQ%3D%3D&md5=d6312669c18040761037bdd44b741b39CAS |

Haidri, A. A., Miller, I. M., and Gwatkin, R. B. L. (1971). Culture of mouse oocytes in vitro, using a system without oil or protein. J. Reprod. Fertil. 26, 409–411.
Culture of mouse oocytes in vitro, using a system without oil or protein.CrossRef | 1:STN:280:DyaE3M3os1CqsQ%3D%3D&md5=0782b8ac1c3b239b9f63f0c76f6e752bCAS | 5569659PubMed |

Hardie, D. G., Ross, F. A., and Hawley, S. A. (2012). AMP-activated protein kinase: a target for drugs both ancient and modern. Chem. Biol. 19, 1222–1236.
AMP-activated protein kinase: a target for drugs both ancient and modern.CrossRef | 1:CAS:528:DC%2BC38XhsF2hsbfF&md5=02ae6482985d460caf518ae158baf5ccCAS | 23102217PubMed |

Harris, S. E., Gopichandran, N., Picton, H. M., Leese, H. J., and Orsi, N. M. (2005). Nutrient concentrations inmuring follicular fluid and the female reproductive tract. Theriogenology 64, 992–1006.
Nutrient concentrations inmuring follicular fluid and the female reproductive tract.CrossRef | 1:CAS:528:DC%2BD2MXmvVGjsbw%3D&md5=db1f2f1a68a9adb86a5fd5e4c851f3c3CAS | 16054501PubMed |

Harris, S. E., Adriaens, I., Leese, H. J., Gosden, R. G., and Picton, H. M. (2007). Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro. Reproduction 134, 415–424.
Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro.CrossRef | 1:CAS:528:DC%2BD2sXhtFKnur3O&md5=5cc02aab8900231649a5bf49a03ca2a5CAS | 17709560PubMed |

Herrick, J. R., Brad, A. M., and Krisher, R. L. (2006). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289–298.
Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.CrossRef | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=28fc1b0f4d415406b10f4d5615d8c6d9CAS | 16452722PubMed |

Homa, S. T., Racowsky, C., and McGaughey, R. W. (1986). Lipid analysis of immature pig oocytes. J. Reprod. Fertil. 77, 425–434.
Lipid analysis of immature pig oocytes.CrossRef | 1:CAS:528:DyaL28XltFamtrs%3D&md5=89e41c05a601d855773e43e7b0cabc16CAS | 3735242PubMed |

Jaffe, L. A., and Norris, R. P. (2010). Initiation of the meiotic prophase-to-metaphase transition in mammalian oocytes. In: ‘Oogenesis: The Universal Process’. (Eds M.-H. Verlhac and A. Villenuve.) pp. 181–198. (Wiley: New York.)

Johnson, M. T., Freeman, E. A., Gardner, D. K., and Hunt, P. A. (2007). Oxidative metabolism of pyruvate is required for meiotic maturation of muring oocytes in vivo. Biol. Reprod. 77, 2–8.
Oxidative metabolism of pyruvate is required for meiotic maturation of muring oocytes in vivo.CrossRef | 1:CAS:528:DC%2BD2sXntV2gsbw%3D&md5=8a79de1c8fac9d097615949ca894194fCAS | 17314311PubMed |

Kane, M. T. (1972). Energy substrates and culture of single cell rabbit ova to blastocysts. Nature 238, 468–469.
Energy substrates and culture of single cell rabbit ova to blastocysts.CrossRef | 1:CAS:528:DyaE38Xlt1Cht7k%3D&md5=549ba672b9bcf97703a178b3b5f724adCAS | 4561860PubMed |

Kim, J. Y., Kinoshita, M., Ohnishi, M., and Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–138.
Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes.CrossRef | 1:CAS:528:DC%2BD3MXlsVGis70%3D&md5=2b5049110598d7946e58d5859cdefa02CAS | 11425337PubMed |

Kim, Y., Kim, E.-Y., Seo, Y.-M., Yoon, T. K., Lee, W.-S., and Lee, K.-A. (2012). Function of the pentose phosphate pathway and its key enzyme, transketolase, in the regulation of the meiotic cell cycle in oocytes. Clin. Exp. Reprod. Med. 39, 58–67.
Function of the pentose phosphate pathway and its key enzyme, transketolase, in the regulation of the meiotic cell cycle in oocytes.CrossRef | 22816071PubMed |

Krisher, R. L., and Bavister, B. D. (1998). Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.
Responses of oocytes and embryos to the culture environment.CrossRef | 1:CAS:528:DyaK1cXnsFCrtQ%3D%3D&md5=7313a95018e89eac1d456d7c670dd2a5CAS | 10732124PubMed |

Krisher, R. L., and Prather, R. S. (2012). A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Mol. Reprod. Dev. 79, 311–320.
A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation.CrossRef | 1:CAS:528:DC%2BC38XlsFygs7Y%3D&md5=c0eff42a155facc9c59aef5762dc984fCAS | 22431437PubMed |

Krisher, R. L., Brad, A. M., Herrick, J. R., Sparman, M. L., and Swain, J. E. (2007). A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation. Anim. Reprod. Sci. 98, 72–96.
A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation.CrossRef | 1:CAS:528:DC%2BD2sXhs1Sksrw%3D&md5=50e49e8fe6b3dc243fd05b25ff6ca931CAS | 17110061PubMed |

Leese, H. J. (2002). Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays 24, 845–849.
Quiet please, do not disturb: a hypothesis of embryo metabolism and viability.CrossRef | 12210521PubMed |

Leese, H. J., and Barton, A. M. (1984). Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J. Reprod. Fertil. 72, 9–13.
Pyruvate and glucose uptake by mouse ova and preimplantation embryos.CrossRef | 1:CAS:528:DyaL2cXmt1Ols7k%3D&md5=62c31203db7257d1525bf1cbe7d36e21CAS | 6540809PubMed |

Loewenstein, J. E., and Cohen, A. I. (1964). Dry mass, lipid content and protein content of the intact and zona-free mouse ovum. J. Embryol. Exp. Morphol. 12, 113–121.
| 1:CAS:528:DyaF2cXkt1ShtL4%3D&md5=b40a6bfffc0ba8420a36076db323c8f8CAS | 14155399PubMed |

Magnusson, C., Hillensjo, T., Tsafriri, A., Hultborn, R., and Ahren, K. (1977). Oxygen consumption of maturing rat oocytes. Biol. Reprod. 17, 9–15.
| 1:CAS:528:DyaE2sXlslyitbY%3D&md5=b003097a9ecfc17702aed67bb4061ddeCAS | 884190PubMed |

Mayes, M. A., Laforest, M. F., Guillemette, C., Gilchrist, R. B., and Richard, F. J. (2007). Adenosine 5′-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Biol. Reprod. 76, 589–597.
Adenosine 5′-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes.CrossRef | 1:CAS:528:DC%2BD2sXjsFCnu7w%3D&md5=0e243e26b8af40311adff8f8ff4840e9CAS | 17167165PubMed |

McEvoy, T. G., Coull, G. D., Broadbent, P. J., and Hutchinson, J. S. M. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–170.
| 1:CAS:528:DC%2BD3cXpsl2msA%3D%3D&md5=69d15be9addb3c72b6286e9f90ee7c96CAS | 10793638PubMed |

Ménézo, Y., Lichtblau, I., and Elder, K. (2013). New insights into human pre-implantation metabolism in vivo and in vitro. J. Assist. Reprod. Genet. 30, 293–303.
New insights into human pre-implantation metabolism in vivo and in vitro.CrossRef | 23430228PubMed |

Montjean, D., Entezami, F., Lichtblau, I., Belloc, S., Gurgan, T., and Menezo, Y. (2012). Carnitine content in the follicular fluid and expression of the enzymes involved in beta oxidation in oocytes and cumulus cells. J. Assist. Reprod. Genet. 29, 1221–1225.
Carnitine content in the follicular fluid and expression of the enzymes involved in beta oxidation in oocytes and cumulus cells.CrossRef | 23054356PubMed |

Paczkowski, M., Silva, E., Schoolcraft, W. B., and Krisher, R. L. (2013). Comparative importance of fatty acid beta-oidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes. Biol. Reprod. 88, 111.
Comparative importance of fatty acid beta-oidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes.CrossRef | 23536372PubMed |

Park, J.-Y., Su, Y.-Q., Ariga, M., Law, E., Jin, S.-E. C., and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
EGF-like growth factors as mediators of LH action in the ovulatory follicle.CrossRef | 1:CAS:528:DC%2BD2cXmvVKlsg%3D%3D&md5=5d954a7ad7a1fe0e2878c16ac4ee2563CAS | 14726596PubMed |

Rafaeloff-Phail, R., Ding, L., Conner, L., Yeh, W. K., McClure, D., Guo, H., Emerson, K., and Brooks, H. (2004). Biochemical regulation of mammalian AMP-activated protein kinase activity by NAD and NADH. J. Biol. Chem. 279, 52 934–52 939.
Biochemical regulation of mammalian AMP-activated protein kinase activity by NAD and NADH.CrossRef | 1:CAS:528:DC%2BD2cXhtVKqurrK&md5=74cba136165be6ee3c24eec8691aff9fCAS |

Richani, D., Ritter, L. J., Thompson, J. G., and Gilchrist, R. B. (2013). Mode of oocyte maturation affects EGF-like peptide function and oocyte competence. Mol. Hum. Reprod. 19, 500–509.
Mode of oocyte maturation affects EGF-like peptide function and oocyte competence.CrossRef | 1:CAS:528:DC%2BC3sXhtFOgt7fL&md5=9d1ef8022a5ee6d702988e0d0a848fc9CAS | 23594928PubMed |

Richani, D., Sutton-McDowall, M. L., Frank, L. A., Gilchrist, R. B., and Thompson, J. G. (2014). Effect of epidermal growth factor-like peptides on the metabolism of in vitro-matured mouse oocytes and cumulus cells. Biol. Reprod. 90, 49.
Effect of epidermal growth factor-like peptides on the metabolism of in vitro-matured mouse oocytes and cumulus cells.CrossRef | 24451986PubMed |

Rieger, D., and Loskutoff, N. M. (1994). Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. J. Reprod. Fertil. 100, 257–262.
Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro.CrossRef | 1:CAS:528:DyaK2cXjt1Sjurs%3D&md5=982a655123e470c7d0a7782c0d53bcd5CAS | 8182598PubMed |

Roberts, R., Franks, S., and Hardy, K. (2002). Culture environment modultes maturation and metabolism of human oocytes. Hum. Reprod. 17, 2950–2956.
Culture environment modultes maturation and metabolism of human oocytes.CrossRef | 12407055PubMed |

Ruderman, N., and Prentki, M. (2004). AMP kinase and malonyl-CoA: targets for therapy of the metabolic syndrome. Nat. Rev. Drug Discov. 3, 340–351.
AMP kinase and malonyl-CoA: targets for therapy of the metabolic syndrome.CrossRef | 1:CAS:528:DC%2BD2cXis1Gktrc%3D&md5=5e803209790eef18d5f16a66b7e72e3eCAS | 15060529PubMed |

Rushmer, R. A., and Brinster, R. L. (1973). Carbon dioxide production from pyruvate and glucose by bovine oocytes. Exp. Cell Res. 82, 252–254.
Carbon dioxide production from pyruvate and glucose by bovine oocytes.CrossRef | 1:CAS:528:DyaE2cXks1SqsQ%3D%3D&md5=abc56935c9718da3257f16cadac0e201CAS | 4203065PubMed |

Saito, T., Hiroi, M., and Kate, T. (1994). Development of glucose utilization studied in single oocytes and preimplantation embryos from mice. Biol. Reprod. 50, 266–270.
Development of glucose utilization studied in single oocytes and preimplantation embryos from mice.CrossRef | 1:CAS:528:DyaK2cXhvVOqtbo%3D&md5=185adad0ad7130f251a90be3184c6a4fCAS | 8142545PubMed |

Sekiguchi, T., Mizutani, T., Yamada, K., Kajitani, T., Yazawa, T., Yoshino, M., and Miyamoto, K. (2004). Expression of epiregulin and amphiregulin in the rat ovary. J. Mol. Endocrinol. 33, 281–291.
Expression of epiregulin and amphiregulin in the rat ovary.CrossRef | 1:CAS:528:DC%2BD2cXntFOltLo%3D&md5=9735b10d3a12c5f02d17997ccb25003eCAS | 15291759PubMed |

Songsasen, N., Yu, I., and Leibo, S. P. (2002). Nuclear maturation of canine oocytes cultured in protein-free media. Mol. Reprod. Dev. 62, 407–415.
Nuclear maturation of canine oocytes cultured in protein-free media.CrossRef | 1:CAS:528:DC%2BD38XktlWrsr0%3D&md5=1043b42afb55a148d64ffdcf2a09bdfeCAS | 12112606PubMed |

Songsasen, N., Spindler, R. E., and Wildt, D. E. (2007). Requirement for, and patterns of, pyruvate and glutamine metabolism in the domestic dog oocyte in vitro. Mol. Reprod. Dev. 74, 870–877.
Requirement for, and patterns of, pyruvate and glutamine metabolism in the domestic dog oocyte in vitro.CrossRef | 1:CAS:528:DC%2BD2sXmtlKlsbY%3D&md5=6fef518dd8a651325b1e6e13e16fc0d4CAS | 17186552PubMed |

Spindler, R. E., Pukazhenthi, B. S., and Wildt, D. E. (2000). Oocyte metabolism predicts the development of cat embryos to blastocyst in vitro. Mol. Reprod. Dev. 56, 163–171.
Oocyte metabolism predicts the development of cat embryos to blastocyst in vitro.CrossRef | 1:CAS:528:DC%2BD3cXjtFyrtb4%3D&md5=ff21c620392e6574350693738d132c3eCAS | 10813848PubMed |

Steeves, T. E., and Gardner, D. K. (1999). Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows. Mol. Reprod. Dev. 54, 92–101.
Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows.CrossRef | 1:CAS:528:DyaK1MXkvFanurg%3D&md5=f6857612f195687082d73466b941a4eeCAS | 10423304PubMed |

Steinberg, G. R., and Kemp, B. E. (2009). AMPK in health and disease. Physiol. Rev. 89, 1025–1078.
AMPK in health and disease.CrossRef | 1:CAS:528:DC%2BD1MXpslyjsb4%3D&md5=b2af08cdf449fdd209d6059d858aed1fCAS | 19584320PubMed |

Sturmey, R. G., and Leese, H. J. (2003). Energy metabolism in pig oocytes and early embryos. Reproduction 126, 197–204.
Energy metabolism in pig oocytes and early embryos.CrossRef | 1:CAS:528:DC%2BD3sXntFyjtr4%3D&md5=64ce8e53c53d9e7b3d87d6e095fa23a0CAS | 12887276PubMed |

Sturmey, R. G., and Leese, H. J. (2008). Role of glucose and fatty acid metabolism in porcine early embryo development. Reprod. Fertil. Dev. 20, 149.
Role of glucose and fatty acid metabolism in porcine early embryo development.CrossRef |

Sturmey, R. G., O’Toole, P. J., and Leese, H. J. (2006). Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 132, 829–837.
Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte.CrossRef | 1:CAS:528:DC%2BD2sXmsF2isw%3D%3D&md5=41804fc5d2cbb5f9dfe8f86c072f1501CAS | 17127743PubMed |

Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50–58.
Role of fatty acids in energy provision during oocyte maturation and early embryo development.CrossRef | 19660080PubMed |

Sugiura, K., Pendola, F. L., and Eppig, J. J. (2005). Oocyte control of metabolic cooperativity between ooytes and companion granulosa cells: energy metabolism. Dev. Biol. 279, 20–30.
Oocyte control of metabolic cooperativity between ooytes and companion granulosa cells: energy metabolism.CrossRef | 1:CAS:528:DC%2BD2MXhtlemtb4%3D&md5=0c245fcd2980dff7f2c163e4f86744f9CAS | 15708555PubMed |

Sugiura, K., Su, Y. Q., Diaz, F. J., Pangas, S.A., Sharma, S., Wigglesworth, K., O’Brien, M. J., Matzuk, M. M., Shimasaki, S., and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593–2603.
Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells.CrossRef | 1:CAS:528:DC%2BD2sXpsFeju7k%3D&md5=df54766b689a7f23fed934c7886c6656CAS | 17553902PubMed |

Sutton, M. L., Gilchrist, R. B., and Thompson, J. G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 9, 35–48.
Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity.CrossRef | 1:CAS:528:DC%2BD3sXjtVelt7Y%3D&md5=75859ff3ff369af7cc6bb67f34275966CAS | 12638780PubMed |

Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2005). Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle fluid medium. Reprod. Fertil. Dev. 17, 407–415.
Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle fluid medium.CrossRef | 1:CAS:528:DC%2BD2MXjtFOktbs%3D&md5=170504fab222fe9dedd77be7e4580cfbCAS | 15899152PubMed |

Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
The pivotal role of glucose metabolism in determining oocyte developmental competence.CrossRef | 1:CAS:528:DC%2BC3cXltFajtr0%3D&md5=72e1531d06ee8b60f71467945f41f3c0CAS | 20089664PubMed |

Sutton-McDowall, M. L., Mottershead, D. G., Gardner, D. K., Gilchrist, R. B., and Thompson, J. G. (2012). Metabolic differences in bovine cumulus–oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol. Reprod. 87, 87.
Metabolic differences in bovine cumulus–oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15.CrossRef | 22895854PubMed |

Tong, L. (2005). Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell. Mol. Life Sci. 62, 1784–1803.
Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery.CrossRef | 1:CAS:528:DC%2BD2MXhtFCgsL3I&md5=3814ad523b3a2c85c8adf2d1a9053434CAS | 15968460PubMed |

Tosca, L., Uzbekova, S., Chabrolle, C., and Dupont, J. (2007). Possible role of 5′AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Biol. Reprod. 77, 452–465.
Possible role of 5′AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation.CrossRef | 1:CAS:528:DC%2BD2sXpvFCrtbk%3D&md5=0bced3d871600fb17c5006de7a5072c9CAS | 17567959PubMed |

Tsafriri, A., Lieberman, M. E., Ahren, K., and Lindner, H. R. (1976). Dissociation between LH-induced aerobic glycolysis and oocyte maturation in cultured Graafian follicles of the rat. Acta Endocrinol. (Copenh.) 81, 362–366.
| 1:CAS:528:DyaE28XosVGksQ%3D%3D&md5=dd5a4c9adc28092c7fc2079aa371df03CAS | 946152PubMed |

Tsutsumi, O., Satoh, K., Taketanim, Y., and Kato, T. (1992). Determination of enzyme activities of energy metabolism in the maturing rat oocyte. Mol. Reprod. Dev. 33, 333–337.
Determination of enzyme activities of energy metabolism in the maturing rat oocyte.CrossRef | 1:CAS:528:DyaK3sXhsVChsb4%3D&md5=c4fb950023d3ab8bb9a904eb598fd6ecCAS | 1449800PubMed |

Urner, F., and Sakkas, D. (1999). Characterization of glycolysis and pentose phosphate pathway activity during sperm entry into the mouse oocyte. Biol. Reprod. 60, 973–978.
Characterization of glycolysis and pentose phosphate pathway activity during sperm entry into the mouse oocyte.CrossRef | 1:CAS:528:DyaK1MXitVGqtLc%3D&md5=70a1589c02f2f81376a2d59c828e0626CAS | 10084974PubMed |

Urner, F., and Sakkas, D. (2005). Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse. Mol. Reprod. Dev. 70, 494–503.
Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse.CrossRef | 1:CAS:528:DC%2BD2MXit1Sls7Y%3D&md5=85c29924895ddb7fd4603daa5690046cCAS | 15685628PubMed |

Valsangkar, D., and Downs, S. M. (2013). A requirement for fatty acid oxidation in the hormone-induced meiotic maturation of mouse oocytes. Biol. Reprod. 89, 43.
A requirement for fatty acid oxidation in the hormone-induced meiotic maturation of mouse oocytes.CrossRef | 23863407PubMed |

Wigglesworth, K., Lee, K.-B., O’Brien, M. J., Peng, J., Matzuk, M. M., and Eppig, J. J. (2013). Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammaoian oocytes. Proc. Natl Acad. Sci. USA 110, E3723–E3729.
Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammaoian oocytes.CrossRef | 1:CAS:528:DC%2BC3sXhs1WlurfE&md5=04081d6ca3a4bbd58007fb438ce40ee6CAS | 23980176PubMed |

Wongsrikeao, P., Otoi, T., Taniguchi, M., Karja, N. W. K., Agung, B., Nii, M., and Nagai, T. (2006). Effects of hexoses on in vitro oocyte maturation and embryo development in pigs. Theriogenology 65, 332–343.
Effects of hexoses on in vitro oocyte maturation and embryo development in pigs.CrossRef | 1:CAS:528:DC%2BD2MXhtlCqtb%2FI&md5=d24a052d97062f4b4cb682b8a2bc45b1CAS | 15967489PubMed |

Ya, R., and Downs, S. M. (2013). Suppression of chemically induced and spontaneous mouse oocyte activation by AMP-activated protein kinase. Biol. Reprod. 88, 70.
Suppression of chemically induced and spontaneous mouse oocyte activation by AMP-activated protein kinase.CrossRef | 23390161PubMed |

Zeilmaker, G. H., and Verhamme, C. M. P. M. (1974). Observations on rat oocyte maturation in vitro: morphology and energy requirements. Biol. Reprod. 11, 145–152.
Observations on rat oocyte maturation in vitro: morphology and energy requirements.CrossRef | 1:CAS:528:DyaE2MXlsV2ltQ%3D%3D&md5=809508a1fb36b4a0362191dfb71e60a9CAS | 4457130PubMed |

Zuelke, K. A., and Brackett, B. G. (1992). Efects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 131, 2690–2696.
| 1:CAS:528:DyaK3sXlt1OltA%3D%3D&md5=39ca93a02ce6c6f8b4a7e913a7cacdb2CAS | 1446610PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (7)