Granulosa cells (GCs) are somatic cells essential for establishing and maintaining bi-directional communication with the oocytes. This connection has a profound importance for the delivery of energy substrates, structural components and ions to the maturing oocyte through gap junctions. Cumulus cells, group of closely associated GCs, surround the oocyte and can diminished the effect of harmful environmental insults. Both GCs and oocytes prefer different energy substrates in their cellular metabolism: GCs are more glycolytic, whereas oocytes rely more on oxidative phosphorylation pathway. The interconnection of these cells is emphasized by the fact that GCs supply oocytes with intermediates produced in glycolysis. The number of GCs surrounding the oocyte and their age affect the energy status of oocytes. This review summarises available studies collaboration of cellular types in the ovarian follicle from the point of view of energy metabolism, signaling and protection of toxic insults. A deeper knowledge of the underlying mechanisms is crucial for better methods to prevent and treat infertility and to improve the technology of in vitro fertilization.

Department of Biochemistry Cell and Molecular Biology 3rd Faculty of Medicine Charles University Prague Czech Republic

Zobrazit více v PubMed

AALTONEN J, LAITINEN MP, VUOJOLAINEN K, JAATINEN R, HORELLI-KUITUNEN N, SEPPÄ L, LOUHIO H, TUURI T, SJÖBERG J, BÜTZOW R, HOVATA O, DALE L, RITVOS O. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab. 1999;84:2744–2750. doi: 10.1210/jc.84.8.2744. PubMed DOI

AARDEMA H, LOLICATO F, Van de LEST CHA, BROUWERS JF, VAANDRAGER AB, Van TOL HTA, ROELEN BAJ, VOS PLAM, HELMS JB, GADELLA BM. Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage. Biol Reprod. 2013;88:164–164. doi: 10.1095/biolreprod.112.106062. PubMed DOI

AARDEMA H, VOS PLAM, LOLICATO F, ROELEN BAJ, KNIJN HM, VAANDRAGER AB, HELMS JB, GADELLA BM. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol Reprod. 2011;85:62–69. doi: 10.1095/biolreprod.110.088815. PubMed DOI

ANDERSON E, ALBERTINI DF. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol. 1976;71:680–686. doi: 10.1083/jcb.71.2.680. PubMed DOI PMC

APPELTANT R, SOMFAI T, NAKAI M, BODÓ S, MAES D, KIKUCHI K, Van SOOM A. Interactions between oocytes and cumulus cells during in vitro maturation of porcine cumulus-oocyte complexes in a chemically defined medium: effect of denuded oocytes on cumulus expansion and oocyte maturation. Theriogenology. 2015;83:567–576. doi: 10.1016/j.theriogenology.2014.10.026. PubMed DOI

BARTMANN AK, ROMAO GS, RAMOS EDA S, FERRIANI RA. Why do older women have poor implantation rates? A possible role of the mitochondria. J Assist Reprod Genet. 2004;21:79–83. doi: 10.1023/B:JARG.0000027018.02425.15. PubMed DOI PMC

BAVISTER BD, SQUIRRELL JM. Mitochondrial distribution and function in oocytes and early embryos. Hum Reprod. 2000;15:189–198. doi: 10.1093/humrep/15.suppl_2.189. PubMed DOI

BUCCIONE R, SCHROEDER AC, EPPIG JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod. 1990;43:543–547. doi: 10.1095/biolreprod43.4.543. PubMed DOI

CAGLAR GS, HAMMADEH M, ASIMAKOPOULOS B, NIKOLETTOS N, DIEDRICH K, AL-HASSANI S. In vivo and In vitro decondensation of human sperm and assisted reproduction technologies. In Vivo. 2005;19:623–630. PubMed

CALVIN HI, GROSSHANS K, BLAKE EJ. Estimation and manipulation of glutathione levels in prepuberal mouse ovaries and ova: Relevance to sperm nucleus transformation in the fertilized egg. Gamete Res. 1986;14:265–275. doi: 10.1002/mrd.1120140310. DOI

CAVILLA JL, KENNEDY CR, BYSKOV AG, HARTSHORNE GM. Human immature oocytes grow during culture for IVM. Hum Reprod. 2008;23:37–45. doi: 10.1093/humrep/dem178. PubMed DOI

CHAPPEL S. The role of mitochondria from mature oocyte to viable blastocyst. Obstet Gynecol Int. 2013;2013:1–10. doi: 10.1155/2013/183024. PubMed DOI PMC

CLARK AR, STOKES YM, LANE M, THOMPSON JG. Mathematical modelling of oxygen concentration in bovine and murine cumulus-oocyte complexes. Reproduction. 2006;131:999–1006. doi: 10.1530/rep.1.00974. PubMed DOI

DALTON CM, SZABADKAI G, CARROLL J. Measurement of ATP in single oocytes: impact of maturation and cumulus cells on levels and consumption. J Cell Physiol. 2014;229:353–361. doi: 10.1002/jcp.24457. PubMed DOI

DEBEY P, SZÖLLÖSI MS, SZÖLLÖSI D, VAUTIER D, GIROUSSE A, BESOMBES D. Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol Reprod Dev. 1993;36:59–74. doi: 10.1002/mrd.1080360110. PubMed DOI

De la FUENTE R, EPPIG JJ. Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. Dev Biol. 2001;229:224–236. doi: 10.1006/dbio.2000.9947. PubMed DOI

De la FUENTE R, VIVEIROS MM, BURNS KH, ADASHI EY, MATZUK MM, EPPIG JJ. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol. 2004;75:447–458. doi: 10.1016/j.ydbio.2004.08.028. PubMed DOI

De MATOS DG, FURNUS CC, MOSES DF. Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol Reprod. 1997;57:1420–1425. doi: 10.1095/biolreprod57.6.1420. PubMed DOI

DIAZ FJ, O’BRIEN MJ, WIGGLESWORTH K, EPPIG JJ. The preantral granulosa cell to cumulus cell transition in the mouse ovary: development of competence to undergo expansion. Dev Biol. 2006;299:91–104. doi: 10.1016/j.ydbio.2006.07.012. PubMed DOI

DIAZ FJ, WIGGLESWORTH K, EPPIG JJ. Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice. Dev Biol. 2007;305:300–311. doi: 10.1016/j.ydbio.2007.02.019. PubMed DOI PMC

DONAHUE RP, STERN S. Follicular cell support of oocyte maturation: production of pyruvate in vitro. J Reprod Fertil. 1968;17:395–398. doi: 10.1530/jrf.0.0170395. PubMed DOI

DOWNS SM, DANIEL SAJ, EPPIG JJ. Induction of maturation in cumulus cell-enclosed 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. doi: 10.1002/jez.1402450113. PubMed DOI

DOWNS SM, HUDSON ED. Energy substrates and the completion of spontaneous meiotic maturation. Zygote. 2000;8:339–351. doi: 10.1017/S0967199400001131. PubMed DOI

DOWNS SM. The influence of glucose, cumulus cells, and metabolic coupling on the ATP levels and meiotic control in the isolated mouse oocyte. Dev Biol. 1995;167:502–512. doi: 10.1006/dbio.1995.1044. PubMed DOI

DRÖGE W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95. doi: 10.1152/physrev.00018.2001. PubMed DOI

DUBE JL, WANG P, ELVIN J, LYONS KM, CELESTE AJ, MATZUK MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol. 1998;12:1809–1817. doi: 10.1210/mend.12.12.0206. PubMed DOI

DUNNING KR, ANASTASI MR, ZHANG VJ, RUSSELL DL, ROBKER RL. Regulation of fatty acid oxidation in mouse cumulus-oocyte complexes during maturation and modulation by PPAR agonists. PLoS One. 2014a;9:e87327. doi: 10.1371/journal.pone.0087327. PubMed DOI PMC

DUNNING KR, RUSSELL DL, ROBKER RL. Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation. Reproduction. 2014b;148:R15–R27. doi: 10.1530/REP-13-0251. PubMed DOI

EPPIG JJ. FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature. 1979;281:483–484. doi: 10.1038/281483a0. PubMed DOI

EPPIG JJ. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays. 1991;13:569–574. doi: 10.1002/bies.950131105. PubMed DOI

EPPIG JJ. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fertil Dev. 1996;8:485–489. doi: 10.1071/RD9960485. PubMed DOI

FITZHARRIS G, MARANGOS P, CARROLL J. Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev Biol. 2007;305:133–144. doi: 10.1016/j.ydbio.2007.02.006. PubMed DOI

FORMAN HJ, ZHANG H, RINNA A. Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med. 2009;30:1–12. doi: 10.1016/j.mam.2008.08.006. PubMed DOI PMC

FUNAHASHI H, KOIKE T, SAKAI R. Effect of glucose and pyruvate on nuclear and cytoplasmic maturation of porcine oocytes in a chemically defined medium. Theriogenology. 2008;70:1041–1047. doi: 10.1016/j.theriogenology.2008.06.025. PubMed DOI

GILCHRIST RB, LANE M, THOMPSON JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14:159–177. doi: 10.1093/humupd/dmm040. PubMed DOI

GILCHRIST RB, RITTER LJ, ARMSTRONG DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci. 2004;82–83:431–446. doi: 10.1016/j.anireprosci.2004.05.017. PubMed DOI

GILULA NB, REEVES OR, STEINBACH A. Metabolic coupling, ionic coupling and cell contacts. Nature. 1972;235:262–265. doi: 10.1038/235262a0. PubMed DOI

HAMDAN M, JONES KT, CHEONG Y, LANE SIR. The sensitivity of the DNA damage checkpoint prevents oocyte maturation in endometriosis. Sci Rep. 2016;6:36994. doi: 10.1038/srep36994. PubMed DOI PMC

HÉRUBEL F, El MOUATASSIM S, GUÉRIN P, FRYDMAN R, MÉNÉZO Y. Genetic expression of monocarboxylate transporters during human and murine oocyte maturation and early embryonic development. Zygote. 2002;10:175–181. doi: 10.1017/S096719940200223X. PubMed DOI

HSU AL, TOWNSEND PM, OEHNINGER S, CASTORA FJ. Endometriosis may be associated with mitochondrial dysfunction in cumulus cells from subjects undergoing in vitro fertilization-intracytoplasmic sperm injection, as reflected by decreased adenosine triphosphate production. Fertil Steril. 2015;103:347–352. doi: 10.1016/j.fertnstert.2014.11.002. PubMed DOI

INOUE A, NAKAJIMA R, NAGATA M, AOKI F. Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum Reprod. 2008;23:1377–1384. doi: 10.1093/humrep/den096. PubMed DOI

IKAWA M, INOUE N, BENHAM AM, OKABE M. Fertilization: a sperm’s journey to and interaction with the oocyte. J Clin Invest. 2010;120:984–994. doi: 10.1172/JCI41585. PubMed DOI PMC

ITAMI N, SHIRATSUKI S, SHIRASUNA K, KUWAYAMA T, IWATA H. Mitochondrial biogenesis and degradation are induced by CCCP treatment of porcine oocytes. Reproduction. 2015;150:97–104. doi: 10.1530/REP-15-0037. PubMed DOI

IWATA H, GOTO H, TANAKA H, SAKAGUCHI Y, KIMURA K, KUWAYAMA T, MONJI Y. Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod Fertil Dev. 2011;23:424–432. doi: 10.1071/RD10133. PubMed DOI

JERUSS JS, WOODRUFF TK. Preservation of fertility in patients with cancer. N Engl J Med. 2009;360:902–911. doi: 10.1056/NEJMra0801454. PubMed DOI PMC

KANSAKU K, ITAMI N, KAWAHARA-MIKI R, SHIRASUNA K, KUWAYAMA T, IWATA H. Differential effects of mitochondrial inhibitors on porcine granulosa cells and oocytes. Theriogenology. 2017a;103:98–103. doi: 10.1016/j.theriogenology.2017.07.049. PubMed DOI

KANSAKU K, TAKEO S, ITAMI N, KIN A, SHIRASUNA K, KUWAYAMA T, IWATA H. Maternal aging affects oocyte resilience to carbonyl cyanide-m-chlorophenylhydrazone-induced mitochondrial dysfunction in cows. PLoS One. 2017b;12:e0188099. doi: 10.1371/journal.pone.0188099. PubMed DOI PMC

KIDDER GM, MHAWI AA. Gap junctions and ovarian folliculogenesis. Reproduction. 2002;123:613–620. doi: 10.1530/reprod/123.5.613. PubMed DOI

KOLATOROVA L, VITKU J, VAVROUS R, HAMPL R, ADAMCOVA K, SIMKOVA M, PARIZEK A, STARKA L, DUSKOVA M. Phthalate metabolites in maternal and cord plasma and their relations to other selected endocrine disruptors and steroids. Physiol Res. 2018;67(Suppl 3):S473–S487. doi: 10.33549/physiolres.933962. PubMed DOI

KOLESAROVA A, SIROTKIN AV, MELLEN M, ROYCHOUDHURY S. Possible intracellular regulators of female sexual maturation. Physiol Res. 2015;64:379–386. doi: 10.33549/physiolres.932838. PubMed DOI

LARSEN WJ, WERT SE. Roles of cell junctions in gametogenesis and in early embryonic development. Tissue Cell. 1988;20:809–848. doi: 10.1016/0040-8166(88)90025-0. PubMed DOI

LEESE HJ, BARTON AM. Production of pyruvate by isolated mouse cumulus cells. J Exp Zool. 1985;234:231–236. doi: 10.1002/jez.1402340208. PubMed DOI

LI D, REDDING GP, BRONLUND JE. Oxygen consumption by bovine granulosa cells with prediction of oxygen transport in preantral follicles. Reprod Fertil Dev. 2013;25:1158–1164. doi: 10.1071/RD12283. PubMed DOI

LUBERDA Z. The role of glutathione in mammalian gametes. Reprod Biol. 2005;5:5–17. PubMed

LU J, WANG Z, CAO J, CHEN Y, DONG Y. A novel and compact review on the role of oxidative stress in female reproduction. Reprod Biol Endocrinol. 2018;16:80. doi: 10.1186/s12958-018-0391-5. PubMed DOI PMC

MADGWICK S, JONES KT. How eggs arrest at metaphase II: MPF stabilisation plus APC/C inhibition equals cytostatic factor. Cell Div. 2007;2:4. doi: 10.1186/1747-1028-2-4. PubMed DOI PMC

MAREI WF, WATHES DC, FOULADI-NASHTA AA. The effect of linolenic Acid on bovine oocyte maturation and development. Biol Reprod. 2009;81:1064–1072. doi: 10.1095/biolreprod.109.076851. PubMed DOI

MARO B, JOHNSON MH, PICKERING SJ, FLACH G. Changes in actin distribution during fertilization of the mouse egg. J Embryol Exp Morphol. 1984;81:211–237. PubMed

MARO B, VERLHAC M-H. Polar body formation: new rules for asymmetric divisions. Nat Cell Biol. 2002;4:E281–E283. doi: 10.1038/ncb1202-e281. PubMed DOI

MEISTER A. Selective modification of glutathione metabolism. Science. 1983;220:472–477. doi: 10.1126/science.6836290. PubMed DOI

MOLINA JR, BARTON DL, LOPRINZI CL. Chemotherapy-induced ovarian failure. Drug Saf. 2005;28:401–416. doi: 10.2165/00002018-200528050-00004. PubMed DOI

MORENO RD, SCHATTEN G, RAMALHO-SANTOS J. Golgi apparatus dynamics during mouse oocyte in vitro maturation: effect of the membrane trafficking inhibitor brefeldin A. Biol Reprod. 2002;66:1259–1266. doi: 10.1095/biolreprod66.5.1259. PubMed DOI

MOTTA PM, NOTTOLA SA, MAKABE S, HEYN R. Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod. 2000;15:129–147. doi: 10.1093/humrep/15.suppl_2.129. PubMed DOI

MUNAKATA Y, ICHINOSE T, OGAWA K, ITAMI N, TASAKI H, SHIRASUNA K, KUWAYAMA T, IWATA H. Relationship between the number of cells surrounding oocytes and energy states of oocytes. Theriogenology. 2016a;86:1789–1798. doi: 10.1016/j.theriogenology.2016.05.036. PubMed DOI

MUNAKATA Y, KAWAHARA-MIKI R, SHIRATSUKI S, TASAKI H, ITAMI N, SHIRASUNA K, KUWAYAMA T, IWATA H. Gene expression patterns in granulosa cells and oocytes at various stages of follicle development as well as in in vitro grown oocyte-and-granulosa cell complexes. J Reprod Dev. 62:359–366. doi: 10.1262/jrd.2016-022. PubMed DOI PMC

ORISAKA M, TAJIMA K, TSANG BK, KOTSUJI F. Oocyte-granulosa-theca cell interactions during preantral follicular development. J Ovarian Res. 2009;2:9. doi: 10.1186/1757-2215-2-9. PubMed DOI PMC

OZAWA M, NAGAI T, SOMFAI T, NAKAI M, MAEDOMARI N, FAHRUDIN M, KARJA NWK, KANEKO H, NOGUCHI J, OHNUMA K, YOSHIMI N, MIYAZAKI H, KIKUCHI K. Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap junctional communication, LH-receptor expression, and meiotic maturation of cumulus-oocyte complexes in pigs. Mol Reprod Dev. 2008;75:857–866. doi: 10.1002/mrd.20820. PubMed DOI

PANTOS K, ATHANASIOU V, STEFANIDIS K, STAVROU D, VAXEVANOGLOU T, CHRONOPOULOU M. Influence of advanced age on the blastocyst development rate and pregnancy rate in assisted reproductive technology. Fertil Steril. 1999;71:1144–1146. doi: 10.1016/S0015-0282(99)00121-1. PubMed DOI

PERREAULT SD, BARBEE RR, SLOTT VL. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol. 1988;125:181–186. doi: 10.1016/0012-1606(88)90070-X. PubMed DOI

PICTON H, BRIGGS D, GOSDEN R. The molecular basis of oocyte growth and development. Mol Cell Endocrinol. 1998;145:27–37. doi: 10.1016/S0303-7207(98)00166-X. PubMed DOI

RACEDO SE, RAWE VY, NIEMANN H. Dynamic changes of the Golgi apparatus during bovine in vitro oocyte maturation. Reproduction. 2012;143:439–447. doi: 10.1530/REP-11-0492. PubMed DOI

RAMBAGS BP, Van BOXTEL DC, THARASANIT T, LENSTRA JA, COLENBRANDER B, STOUT TA. Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology. 2014;81:959–965. doi: 10.1016/j.theriogenology.2014.01.020. PubMed DOI

REDDING GP, BRONLUND JE, HART AL. Theoretical investigation into the dissolved oxygen levels in follicular fluid of the developing human follicle using mathematical modelling. Reprod Fertil Dev. 2008;20:408–417. doi: 10.1071/RD07190. PubMed DOI

REYES R, ROSADO A, HERNÁNDEZ O, DELGADO NM. Heparin and glutathione: physiological decondensing agents of human sperm nuclei. Gamete Res. 1989;23:39–47. doi: 10.1002/mrd.1120230105. PubMed DOI

RONESS H, KALICH-PHILOSOPH L, MEIROW D. Prevention of chemotherapy-induced ovarian damage: possible roles for hormonal and non-hormonal attenuating agents. Hum Reprod Update. 2014;20:759–774. doi: 10.1093/humupd/dmu019. PubMed DOI

SALUSTRI A, GARLANDA C, HIRSCH E, De ACETIS M, MACCAGNO A, BOTTAZZI B, DONI A, BASTONE A, MANTOVANI G, BECK PECCOZ P, SALVATORI G, MAHONEY DJ, DAY AJ, SIRACUSA G, ROMANI L, MANTOVANI A. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development. 2004;131:1577–1586. doi: 10.1242/dev.01056. PubMed DOI

SALUSTRI A, YANAGISHITA M, HASCALL VC. Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol. 1990;138:26–32. doi: 10.1016/0012-1606(90)90173-G. PubMed DOI

SALUSTRI A, YANAGISHITA M, UNDERHILL CB, LAURENT TC, HASCALL VC. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle. Dev Biol. 1992;151:541–551. doi: 10.1016/0012-1606(92)90192-J. PubMed DOI

SÁNCHEZ F, SMITZ J. Molecular control of oogenesis. Biochim Biophys Acta. 2012;1822:1896–1912. doi: 10.1016/j.bbadis.2012.05.013. PubMed DOI

SCHATTEN H, SUN QY, PRATHER R. The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility. Reprod Biol Endocrinol. 2014;12:111. doi: 10.1186/1477-7827-12-111. PubMed DOI PMC

SHAEIB F, KHAN SN, ALI I, THAKUR M, SAED MG, DAI J, AWONUGA AO, BANERJEE J, ABU-SOUD HM. The defensive role of cumulus cells against reactive oxygen species insult in metaphase II mouse oocytes. Reprod Sci. 2016;23:498–507. doi: 10.1177/1933719115607993. PubMed DOI PMC

SHIRATSUKI S, HARA T, MUNAKATA Y, SHIRASUNA K, KUWAYAMA T, IWATA H. Low oxygen level increases proliferation and metabolic changes in bovine granulosa cells. Mol Cell Endocrinol. 2016;437:75–85. doi: 10.1016/j.mce.2016.08.010. PubMed DOI

SIMERMAN AA, HILL DL, GROGAN TR, ELASHOFF D, CLARKE NJ, GOLDSTEIN EH, MANRRIQUEZ AN, CHAZENBALK GD, DUMESIC DA. Intrafollicular cortisol levels inversely correlate with cumulus cell lipid content as a possible energy source during oocyte meiotic resumption in women undergoing ovarian stimulation for in vitro fertilization. Fertil Steril. 2015;103:249–257. doi: 10.1016/j.fertnstert.2014.09.034. PubMed DOI PMC

SIMSEK DURAN F, LI F, FORD W, SWANSON RJ, JONES HW, JR, CASTORA FJ. Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS One. 2013;8:e64955. doi: 10.1371/journal.pone.0064955. PubMed DOI PMC

STOJKOVIC M, MACHADO SA, STOJKOVIC P, ZAKHARTCHENKO V, HUTZLER P, GONÇALVES PB, 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. doi: 10.1095/biolreprod64.3.904. PubMed DOI

STROUD JS, MUTCH D, RADER J, POWELL M, THAKER PH, GRIGSBY PW. Effects of cancer treatment on ovarian function. Fertil Steril. 2009;92:417–427. doi: 10.1016/j.fertnstert.2008.07.1714. PubMed DOI

SUGIYAMA M, SUMIYA M, SHIRASUNA K, KUWAYAMA T, IWATA H. Addition of granulosa cell mass to the culture medium of oocytes derived from early antral follicles increases oocyte growth, ATP content, and acetylation of H4K12. Zygote. 2016;24:848–856. doi: 10.1017/S0967199416000198. PubMed DOI

SUN F, BAHAT A, GAKAMSKY A, GIRSH E, KATZ N, GIOJALAS LC, TUR-KASPA I, EISENBACH M. Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum Reprod. 2005;20:761–767. doi: 10.1093/humrep/deh657. PubMed DOI

SUTOVSKY P, SCHATTEN G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod. 1997;56:1503–1512. doi: 10.1095/biolreprod56.6.1503. PubMed DOI

SUTTON-McDOWALL ML, GILCHRIST RB, THOMPSON JG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction. 2010;139:685–695. doi: 10.1530/REP-09-0345. PubMed DOI

SU Y-Q, SUGIURA K, EPPIG J. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med. 2009;27:32–42. doi: 10.1055/s-0028-1108008. PubMed DOI PMC

TAKAHASHI N, DAVY PM, GARDNER LH, MATHEWS J, YAMAZAKI Y, ALLSOPP RC. Hypoxia inducible factor 1 alpha is expressed in germ cells throughout the murine life cycle. PLoS One. 2016;11:e0154309. doi: 10.1371/journal.pone.0154309. PubMed DOI PMC

TANGHE S, Van SOOM A, NAUWYNCK H, CORYN M, De KRUIF A. Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61:414–424. doi: 10.1002/mrd.10102. PubMed DOI

TEIXEIRA FILHO FL, BARACAT EC, LEE TH, SUH CS, MATSUI M, CHANG RJ, SHIMASAKI S, ERICKSON GF. Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2002;87:1337–1344. doi: 10.1210/jcem.87.3.8316. PubMed DOI

TEVES ME, BARBANO F, GUIDOBALDI HA, SANCHEZ R, MISKA W, GIOJALAS LC. Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil Steril. 2006;86:745–749. doi: 10.1016/j.fertnstert.2006.02.080. PubMed DOI

THOMPSON JG, SIMPSON AC, PUGH PA, WRIGHT RW, JR, TERVIT HR. Glucose utilization by sheep embryos derived in vivo and in vitro. Reprod Fertil Dev. 1991;3:571–576. doi: 10.1071/RD9910571. PubMed DOI

TILLY JL, SINCLAIR DA. Germline energetics, aging, and female infertility. Cell Metab. 2013;17:838–850. doi: 10.1016/j.cmet.2013.05.007. PubMed DOI PMC

UHDE K, Van TOL HTA, STOUT TAE, ROELEN BAJ. Metabolomic profiles of bovine cumulus cells and cumulus-oocyte-complex-conditioned medium during maturation in vitro. Sci Rep. 2018;8:9477. doi: 10.1038/s41598-018-27829-9. PubMed DOI PMC

VALKO M, LEIBFRITZ D, MONCOL J, CRONIN MT, MAZUR M, TELSER J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84. doi: 10.1016/j.biocel.2006.07.001. PubMed DOI

VIRANT-KLUN I, BAUER C, STÅHLBERG A, KUBISTA M, SKUTELLA T. Human oocyte maturation in vitro is improved by co-culture with cumulus cells from mature oocytes. Reprod Biomed Online. 2018;36:508–523. doi: 10.1016/j.rbmo.2018.01.011. PubMed DOI

WAI T, AO A, ZHANG X, CYR D, DUFORT D, SHOUBRIDGE EA. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod. 2010;83:52–62. doi: 10.1095/biolreprod.109.080887. PubMed DOI PMC

WALES RG, WHITTINGHAM DG, HARDY K, CRAFT IL. Metabolism of glucose by human embryos. J Reprod Fertil. 1987;79:289–297. doi: 10.1530/jrf.0.0790289. PubMed DOI

WANG Q, CHI MM, SCHEDL T, MOLEY KH. An intercellular pathway for glucose transport into mouse oocytes. Am J Physiol Endocrinol Metab. 2012;302:E1511–E1518. doi: 10.1152/ajpendo.00016.2012. PubMed DOI PMC

WARNE GL, FAIRLEY KF, HOBBS JB, MARTIN FIR. Cyclophosphamide-induced ovarian failure. N Engl J Med. 1973;289:1159–1162. doi: 10.1056/NEJM197311292892202. PubMed DOI

WERT SE, LARSEN WJ. Preendocytotic alterations in cumulus cell gap junctions precede meiotic resumption in the rat cumulus-oocyte complex. Tissue Cell. 1990;22:827–851. doi: 10.1016/0040-8166(90)90047-D. PubMed DOI

WILDING M, DALE B, MARINO M, Di MATTEO L, ALVIGGI C, PISATURO ML, LOMBARDI L, De PLACIDO G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod. 2001;16:909–917. doi: 10.1093/humrep/16.5.909. PubMed DOI

WINSHIP AL, STRINGER JM, LIEW SH, HUTT KJ. The importance of DNA repair for maintaining oocyte quality in response to anti-cancer treatments, environmental toxins and maternal ageing. Hum Reprod Update. 2018;24:119–134. doi: 10.1093/humupd/dmy002. PubMed DOI

XIE H-L, WANG Y-B, JIAO G-Z, KONG D-L, LI Q, LI H, ZHENG L-L, TAN J-H. Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Sci Rep. 2016;6:20764. doi: 10.1038/srep20764. PubMed DOI PMC

XU J, OSUGA Y, YANO T, MORITA Y, TANG X, FUJIWARA T, TAKAI Y, MATSUMI H, KOGA K, TAKETANI Y, TSUTSUMI O. Bisphenol A induces apoptosis and G2-to-M arrest of ovarian granulosa cells. Biochem Biophys Res Commun. 2002;292:456–462. doi: 10.1006/bbrc.2002.6644. PubMed DOI

YAMAMOTO T, IWATA H, GOTO H, SHIRATUKI S, TANAKA H, MONJI Y, KUWAYAMA T. Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol Reprod Dev. 2010;77:595–604. doi: 10.1002/mrd.21188. PubMed DOI

YEO CX, GILCHRIST RB, THOMPSON JG, LANE M. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum Reprod. 2008;23:67–73. doi: 10.1093/humrep/dem140. PubMed DOI

YOSHIDA M. Role of glutathione in the maturation and fertilization of pig oocytes in vitro. Mol Reprod Dev. 1993;35:76–81. doi: 10.1002/mrd.1080350113. PubMed DOI

YOUNGLAI EV, FOSTER WG, HUGHES EG, TRIM K, JARRELL JF. Levels of environmental contaminants in human follicular fluid, serum, and seminal plasma of couples undergoing in vitro fertilization. Arch Environ Contam Toxicol. 2002;43:121–126. doi: 10.1007/s00244-001-0048-8. PubMed DOI

YU Y, DUMOLLARD R, ROSSBACH A, LAI FA, SWANN K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol. 2010;224:672–680. doi: 10.1002/jcp.22171. PubMed DOI PMC

ŽALMANOVÁ T, HOŠKOVÁ K, NEVORAL J, ADÁMKOVÁ K, KOTT T, ŠULC M, KOTÍKOVÁ Z, PROKEŠOVÁ Š, JÍLEK F, KRÁLÍČKOVÁ M, PETR J. Bisphenol S negatively affects the meotic maturation of pig oocytes. Sci Rep. 2017;7:485. doi: 10.1038/s41598-017-00570-5. PubMed DOI PMC

ZHANG D, KEILTY D, ZHANG ZF, CHIAN RC. Mitochondria in oocyte aging: current understanding. Facts Views Vis Obgyn. 2017;9:29–38. PubMed PMC

ZUELKE KA, JEFFAY SC, ZUCKER RM, PERREAULT SD. Glutathione (GSH) concentrations vary with the cell cycle in maturing hamster oocytes, zygotes, and pre-implantation stage embryos. Mol Reprod Dev. 2003;64:106–112. doi: 10.1002/mrd.10214. PubMed DOI

The bisphenol S contamination level observed in human follicular fluid affects the development of porcine oocytes

The role of connexin 37 polymorphism in spontaneous abortion

Fennel affects ovarian cell proliferation, apoptosis, and response to ghrelin