Abstract
In most mammals, oocyte maturation is the final process of oogenesis, from the prophase of the first meiosis (germinal vesicle stage) to the metaphase of the second meiosis (MII), during which the oocyte acquires fertilizable competence as well as post-fertilization development competence. The nuclear and cytoplasmic maturation processes occur in synchrony but independently. Cytoplasmic maturation entails biochemical and structural changes in the cytoplasm, which give rise to oocytes capable of being fertilized and developing into embryos. Herein we review the literature and results from our own experiments on the structural and molecular events regulating cytoplasmic maturation in oocytes, concentrating on (1) the appropriate reorganization of active mitochondria and the endoplasmic reticulum, a structural and functional feature of cytoplasmic maturation, and (2) factors involved in regulatory mechanisms such as cumulus cell–oocyte gap junctional signaling, cumulus cell–oocyte bidirectional paracrine signaling, and the complex interactions of these signaling processes and follicular fluid constituents in the follicle environment.
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Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool. 1974;187:383–6.
Dekel N, Beers WH. Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins. Proc Natl Acad Sci USA. 1978;75:4369–73.
Downs SM, Eppig JJ. Induction of mouse oocyte maturation in vivo by perturbants of purine metabolism. Biol Reprod. 1987;36:431–7.
Downs SM. Purine control of mouse oocyte maturation: evidence that nonmetabolized hypoxanthine maintains meiotic arrest. Mol Reprod Dev. 1993;35:82–94.
Eppig JJ, Ward-Bailey PF, Coleman DL. Hypoxanthine and adenosine in murine ovarian follicular fluid: concentrations and activity in maintaining oocyte meiotic arrest. Biol Reprod. 1985;33:1041–9.
Lindner HR, Tsafriri A, Lieberman ME, Zor U, Koch Y, Bauminger S, et al. Gonadotropin action on cultured Graafian follicles: induction of maturation division of the mammalian oocyte and differentiation of the luteal cell. Recent Prog Horm Res. 1974;30:79–138.
Eppig JJ. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fertil Dev. 1996;8:485–9.
Eppig JJ, Schultz RM, O’Brien M, Chesnel F. Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev Biol. 1994;164:1–9.
Kikuchi K, Nagai T, Ding J, Yamauchi N, Noguchi J, Izaike Y. Cytoplasmic maturation for activation of pig follicular oocytes cultured and arrested at metaphase I. J Reprod Fertil. 1999;116:143–56.
Combelles CM, Albertini DF. Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev Biol. 2001;239:281–94.
Brevini TA, Vassena R, Francisci C, Gandolfi F. Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol Reprod. 2005;72:1218–23.
Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, et al. 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;64:904–9.
Torner H, Brussow KP, Alm H, Ratky J, Pohland R, Tuchscherer A, et al. Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation. Theriogenology. 2004;61:1675–89.
Van Blerkom J, Davis PW, Lee J. ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum Reprod. 1995;10:415–24.
Brad AM, Bormann CL, Swain JE, Durkin RE, Johnson AE, Clifford AL, et al. Glutathione and adenosine triphosphate content of in vivo and in vitro matured porcine oocytes. Mol Reprod Dev. 2003;64:492–8.
Bavister BD, Squirrell JM. Mitochondrial distribution and function in oocytes and early embryos. Hum Reprod. 2000;15(Suppl 2):189–98.
Muggleton-Harris AL, Brown JJ. Cytoplasmic factors influence mitochondrial reorganization and resumption of cleavage during culture of early mouse embryos. Hum Reprod. 1988;3:1020–8.
Van Blerkom J, Runner MN. Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am J Anat. 1984;171:335–55.
Sun QY, Lai L, Wu GM, Park KW, Day BN, Prather RS, et al. Microtubule assembly after treatment of pig oocytes with taxol: correlation with chromosomes, gamma-tubulin, and MAP kinase. Mol Reprod Dev. 2001;60:481–90.
Sun QY, Wu GM, Lai L, Park KW, Cabot R, Cheong HT, et al. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction. 2001;122:155–63.
Brevini TA, Vassena R, Paffoni A, Francisci C, Fascio U, Gandolfi F. Exposure of pig oocytes to PCBs during in vitro maturation: effects on developmental competence, cytoplasmic remodelling and communications with cumulus cells. Eur J Histochem. 2004;48:347–56.
Liu L, Hammar K, Smith PJ, Inoue S, Keefe DL. Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium. 2001;30:423–33.
Knott JG, Kurokawa M, Fissore RA, Schultz RM, Williams CJ. Transgenic RNA interference reveals role for mouse sperm phospholipase Czeta in triggering Ca2+ oscillations during fertilization. Biol Reprod. 2005;72:992–6.
Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, et al. PLC zeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development. 2002;129:3533–44.
Swann K, Larman MG, Saunders CM, Lai FA. The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCzeta. Reproduction. 2004;127:431–9.
Larman MG, Saunders CM, Carroll J, Lai FA, Swann K. Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCzeta. J Cell Sci. 2004;117:2513–21.
Lee B, Yoon SY, Fissore RA. Regulation of fertilization-initiated [Ca2+]i oscillations in mammalian eggs: a multi-pronged approach. Semin Cell Dev Biol. 2006;17:274–84.
Miyazaki S, Yuzaki M, Nakada K, Shirakawa H, Nakanishi S, Nakade S, et al. Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science. 1992;257:251–5.
Yoda A, Oda S, Shikano T, Kouchi Z, Awaji T, Shirakawa H, et al. Ca2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev Biol. 2004;268:245–57.
Ducibella T, Schultz RM, Ozil JP. Role of calcium signals in early development. Semin Cell Dev Biol. 2006;17:324–32.
Xu Z, Kopf GS, Schultz RM. Involvement of inositol 1,4,5-trisphosphate-mediated Ca2+ release in early and late events of mouse egg activation. Development. 1994;120:1851–9.
Ozil JP, Banrezes B, Toth S, Pan H, Schultz RM. Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006;300:534–44.
Toth S, Huneau D, Banrezes B, Ozil JP. Egg activation is the result of calcium signal summation in the mouse. Reproduction. 2006;131:27–34.
Cheung A, Swann K, Carroll J. The ability to generate normal Ca2+ transients in response to spermatozoa develops during the final stages of oocyte growth and maturation. Hum Reprod. 2000;15:1389–95.
Jones KT, Carroll J, Whittingham DG. Ionomycin, thapsigargin, ryanodine, and sperm induced Ca2+ release increase during meiotic maturation of mouse oocytes. J Biol Chem. 1995;270:6671–7.
Carroll J, Swann K, Whittingham D, Whitaker M. Spatiotemporal dynamics of intracellular [Ca2+]i oscillations during the growth and meiotic maturation of mouse oocytes. Development. 1994;120:3507–17.
Mehlmann LM, Kline D. Regulation of intracellular calcium in the mouse egg: calcium release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol Reprod. 1994;51:1088–98.
Kline D. Attributes and dynamics of the endoplasmic reticulum in mammalian eggs. Curr Top Dev Biol. 2000;50:125–54.
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;305:133–44.
Mehlmann LM, Terasaki M, Jaffe LA, Kline D. Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte. Dev Biol. 1995;170:607–15.
Shiraishi K, Okada A, Shirakawa H, Nakanishi S, Mikoshiba K, Miyazaki S. Developmental changes in the distribution of the endoplasmic reticulum and inositol 1,4,5-trisphosphate receptors and the spatial pattern of Ca2+ release during maturation of hamster oocytes. Dev Biol. 1995;170:594–606.
Mallik R, Gross SP. Molecular motors: strategies to get along. Curr Biol. 2004;14:R971–82.
FitzHarris G, Marangos P, Carroll J. Cell cycle-dependent regulation of structure of endoplasmic reticulum and inositol 1,4,5-trisphosphate-induced Ca2+ release in mouse oocytes and embryos. Mol Biol Cell. 2003;14:288–301.
Fissore RA, Longo FJ, Anderson E, Parys JB, Ducibella T. Differential distribution of inositol trisphosphate receptor isoforms in mouse oocytes. Biol Reprod. 1999;60:49–57.
Parrington J, Brind S, De Smedt H, Gangeswaran R, Lai FA, Wojcikiewicz R, et al. Expression of inositol 1,4,5-trisphosphate receptors in mouse oocytes and early embryos: the type I isoform is upregulated in oocytes and downregulated after fertilization. Dev Biol. 1998;203:451–61.
Mehlmann LM, Mikoshiba K, Kline D. Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev Biol. 1996;180:489–98.
Goud PT, Goud AP, Van Oostveldt P, Dhont M. Presence and dynamic redistribution of type I inositol 1,4,5-trisphosphate receptors in human oocytes and embryos during in-vitro maturation, fertilization and early cleavage divisions. Mol Hum Reprod. 1999;5:441–51.
Kline D, Mehlmann L, Fox C, Terasaki M. The cortical endoplasmic reticulum (ER) of the mouse egg: localization of ER clusters in relation to the generation of repetitive calcium waves. Dev Biol. 1999;215:431–42.
Dekel N, Beers WH. Development of the rat oocyte in vitro: inhibition and induction of maturation in the presence or absence of the cumulus oophorus. Dev Biol. 1980;75:247–54.
Dekel N. Regulation of oocyte maturation. The role of cAMP. Ann N Y Acad Sci. 1988;541:211–6.
Eppig JJ. The participation of cyclic adenosine monophosphate (cAMP) in the regulation of meiotic maturation of oocytes in the laboratory mouse. J Reprod Fertil Suppl. 1989;38:3–8.
Eppig JJ. Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte–granulosa cell complexes developed in vitro from preantral follicles. Biol Reprod. 1991;45:824–30.
Eppig JJ, Freter RR, Ward-Bailey PF, Schultz RM. Inhibition of oocyte maturation in the mouse: participation of cAMP, steroid hormones, and a putative maturation-inhibitory factor. Dev Biol. 1983;100:39–49.
Aktas H, Wheeler MB, Rosenkrans CF Jr, First NL, Leibfried-Rutledge ML. Maintenance of bovine oocytes in prophase of meiosis I by high [cAMP]i. J Reprod Fertil. 1995;105:227–35.
Sirard MA, First NL. In vitro inhibition of oocyte nuclear maturation in the bovine. Biol Reprod. 1988;39:229–34.
Thomas RE, Armstrong DT, Gilchrist RB. Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev Biol. 2002;244:215–25.
Thomas RE, Armstrong DT, Gilchrist RB. Bovine cumulus cell–oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosphate levels. Biol Reprod. 2004;70:548–56.
Horner K, Livera G, Hinckley M, Trinh K, Storm D, Conti M. Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev Biol. 2003;258:385–96.
Mehlmann LM, Jones TL, Jaffe LA. Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science. 2002;297:1343–5.
Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, Pendola FL, et al. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science. 2004;306:1947–50.
Dekel N, Lawrence TS, Gilula NB, Beers WH. Modulation of cell-to-cell communication in the cumulus–oocyte complex and the regulation of oocyte maturation by LH. Dev Biol. 1981;86:356–62.
Sherizly I, Galiani D, Dekel N. Regulation of oocyte maturation: communication in the rat cumulus–oocyte complex. Hum Reprod. 1988;3:761–6.
Gilula NB, Epstein ML, Beers WH. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J Cell Biol. 1978;78:58–75.
Sela-Abramovich S, Chorev E, Galiani D, Dekel N. Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology. 2005;146:1236–44.
Sela-Abramovich S, Edry I, Galiani D, Nevo N, Dekel N. Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology. 2006;147:2280–6.
Bagg MA, Nottle MB, Grupen CG, Armstrong DT. Effect of dibutyryl cAMP on the cAMP content, meiotic progression, and developmental potential of in vitro matured pre-pubertal and adult pig oocytes. Mol Reprod Dev. 2006;73:1326–32.
Funahashi H, Cantley TC, Day BN. Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol Reprod. 1997;57:49–53.
Luciano AM, Pocar P, Milanesi E, Modina S, Rieger D, Lauria A, et al. Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol Reprod Dev. 1999;54:86–91.
Merriman JA, Whittingham DG, Carroll J. The effect of follicle stimulating hormone and epidermal growth factor on the developmental capacity of in vitro matured mouse oocytes. Hum Reprod. 1998;13:690–5.
Nogueira D, Cortvrindt R, De Matos DG, Vanhoutte L, Smitz J. Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol Reprod. 2003;69:2045–52.
Schoevers EJ, Kidson A, Verheijden JH, Bevers MM. Effect of follicle-stimulating hormone on nuclear and cytoplasmic maturation of sow oocytes in vitro. Theriogenology. 2003;59:2017–28.
Thomas RE, Thompson JG, Armstrong DT, Gilchrist RB. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol Reprod. 2004;71:1142–9.
Luciano AM, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod. 2004;70:465–72.
Salustri A, Siracusa G. Metabolic coupling, cumulus expansion and meiotic resumption in mouse cumuli oophori cultured in vitro in the presence of FSH or dcAMP, or stimulated in vivo by hCG. J Reprod Fertil. 1983;68:335–41.
Edwards RG. Follicular fluid. J Reprod Fertil. 1974;37:189–219.
Artini PG, Battaglia C, D’Ambrogio G, Barreca A, Droghini F, Volpe A, et al. Relationship between human oocyte maturity, fertilization and follicular fluid growth factors. Hum Reprod. 1994;9:902–6.
Driancourt MA, Thuel B. Control of oocyte growth and maturation by follicular cells and molecules present in follicular fluid. A review. Reprod Nutr Dev. 1998;38:345–62.
Ali A, Coenen K, Bousquet D, Sirard MA. Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes. Theriogenology. 2004;62:1596–606.
Lonergan P, Monaghan P, Rizos D, Boland MP, Gordon I. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol Reprod Dev. 1994;37:48–53.
Sirard MA, Roy B, Patrick P, Mermillod P, Gullbault LA. Origin of the follicular fluid added to the media during bovine IVM influences embryonic development. Theriogenology. 1995;44:85–94.
Carolan C, Lonergan P, Monget P, Monniaux D, Mermillod P. Effect of follicle size and quality on the ability of follicular fluid to support cytoplasmic maturation of bovine oocytes. Mol Reprod Dev. 1996;43:477–83.
Romero-Arredondo A, Seidel GE Jr. Effects of follicular fluid during in vitro maturation of bovine oocytes on in vitro fertilization and early embryonic development. Biol Reprod. 1996;55:1012–6.
Ayoub MA, Hunter AG. Inhibitory effect of bovine follicular fluid on in vitro maturation of bovine oocytes. J Dairy Sci. 1993;76:95–100.
Choi YH, Takagi M, Kamishita H, Wijayagunawardane MP, Acosta TJ, Miyazawa K, et al. Developmental capacity of bovine oocytes matured in two kinds of follicular fluid and fertilized in vitro. Anim Reprod Sci. 1998;50:27–33.
Kim K, Mitsumizo N, Fujita K, Utsumi K. The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos. Theriogenology. 1996;45:787–99.
Ikeda S, Azuma T, Hashimoto S, Yamada M. In vitro maturation of bovine oocytes with fractions of bovine follicular fluid separated by heparin affinity chromatography. J Reprod Dev. 1999;45:397–404.
Das K, Stout LE, Hensleigh HC, Tagatz GE, Phipps WR, Leung BS. Direct positive effect of epidermal growth factor on the cytoplasmic maturation of mouse and human oocytes. Fertil Steril. 1991;55:1000–4.
De La Fuente R, O’Brien MJ, Eppig JJ. Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod. 1999;14:3060–8.
Kobayashi K, Yamashita S, Hoshi H. Influence of epidermal growth factor and transforming growth factor-alpha on in vitro maturation of cumulus cell-enclosed bovine oocytes in a defined medium. J Reprod Fertil. 1994;100:439–46.
Lonergan P, Carolan C, Van Langendonckt A, Donnay I, Khatir H, Mermillod P. Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol Reprod. 1996;54:1420–9.
Park KW, Iga K, Niwa K. Exposure of bovine oocytes to EGF during maturation allows them to develop to blastocysts in a chemically-defined medium. Theriogenology. 1997;48:1127–35.
Silva CC, Knight PG. Modulatory actions of activin-A and follistatin on the developmental competence of in vitro-matured bovine oocytes. Biol Reprod. 1998;58:558–65.
Stock AE, Woodruff TK, Smith LC. Effects of inhibin A and activin A during in vitro maturation of bovine oocytes in hormone- and serum-free medium. Biol Reprod. 1997;56:1559–64.
Marin Bivens CL, Grondahl C, Murray A, Blume T, Su YQ, Eppig JJ. Meiosis-activating sterol promotes the metaphase I to metaphase II transition and preimplantation developmental competence of mouse oocytes maturing in vitro. Biol Reprod. 2004;70:1458–64.
Cioffi JA, Van Blerkom J, Antczak M, Shafer A, Wittmer S, Snodgrass HR. The expression of leptin and its receptors in pre-ovulatory human follicles. Mol Hum Reprod. 1997;3:467–72.
Craig J, Zhu H, Dyce PW, Petrik J, Li J. Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology. 2004;145:5355–63.
Ikeda S, Nishikimi A, Ichihara-Tanaka K, Muramatsu T, Yamada M. cDNA cloning of bovine midkine and production of the recombinant protein, which affects in vitro maturation of bovine oocytes. Mol Reprod Dev. 2000;57:99–107.
Kadomatsu K, Huang RP, Suganuma T, Murata F, Muramatsu T. A retinoic acid responsive gene MK found in the teratocarcinoma system is expressed in spatially and temporally controlled manner during mouse embryogenesis. J Cell Biol. 1990;110:607–16.
Kadomatsu K, Tomomura M, Muramatsu T. cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem Biophys Res Commun. 1988;151:1312–8.
Tomomura M, Kadomatsu K, Matsubara S, Muramatsu T. A retinoic acid-responsive gene, MK, found in the teratocarcinoma system. Heterogeneity of the transcript and the nature of the translation product. J Biol Chem. 1990;265:10765–70.
Fabri L, Maruta H, Muramatsu H, Muramatsu T, Simpson RJ, Burgess AW, et al. Structural characterisation of native and recombinant forms of the neurotrophic cytokine MK. J Chromatogr. 1993;646:213–25.
Muramatsu H, Shirahama H, Yonezawa S, Maruta H, Muramatsu T. Midkine, a retinoic acid-inducible growth/differentiation factor: immunochemical evidence for the function and distribution. Dev Biol. 1993;159:392–402.
Hirota Y, Osuga Y, Nose E, Koga K, Yoshino O, Hirata T, et al. The presence of midkine and its possible implication in human ovarian follicles. Am J Reprod Immunol. 2007;58:367–73.
Ohyama Y, Miyamoto K, Minamino N, Matsuo H. Isolation and identification of midkine and pleiotrophin in bovine follicular fluid. Mol Cell Endocrinol. 1994;105:203–8.
Karino S, Minegishi T, Ohyama Y, Tano M, Nakamura K, Miyamoto K, et al. Regulation and localization of midkine in rat ovary. FEBS Lett. 1995;362:147–50.
Minegishi T, Karino S, Tano M, Ibuki Y, Miyamoto K. Regulation of midkine messenger ribonucleic acid levels in cultured rat granulosa cells. Biochem Biophys Res Commun. 1996;229:799–805.
Owada K, Sanjo N, Kobayashi T, Mizusawa H, Muramatsu H, Muramatsu T, et al. Midkine inhibits caspase-dependent apoptosis via the activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase in cultured neurons. J Neurochem. 1999;73:2084–92.
Maeda N, Ichihara-Tanaka K, Kimura T, Kadomatsu K, Muramatsu T, Noda M. A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J Biol Chem. 1999;274:12474–9.
Sato W, Kadomatsu K, Yuzawa Y, Muramatsu H, Hotta N, Matsuo S, et al. Midkine is involved in neutrophil infiltration into the tubulointerstitium in ischemic renal injury. J Immunol. 2001;167:3463–9.
Muramatsu T. Midkine (MK), the product of a retinoic acid responsive gene, and pleiotrophin constitute a new protein family regulating growth and differentiation. Int J Dev Biol. 1993;37:183–8.
Muramatsu T. Midkine and pleiotrophin: two related proteins involved in development, survival, inflammation and tumorigenesis. J Biochem. 2002;132:359–71.
Muramatsu H, Zou P, Kurosawa N, Ichihara-Tanaka K, Maruyama K, Inoh K, et al. Female infertility in mice deficient in midkine and pleiotrophin, which form a distinct family of growth factors. Genes Cells. 2006;11:1405–17.
Ikeda S, Saeki K, Imai H, Yamada M. Abilities of cumulus and granulosa cells to enhance the developmental competence of bovine oocytes during in vitro maturation period are promoted by midkine; a possible implication of its apoptosis suppressing effects. Reproduction. 2006;132:549–57.
Anderson RA, Bayne RA, Gardner J, De Sousa PA. Brain-derived neurotrophic factor is a regulator of human oocyte maturation and early embryo development. Fertil Steril. 2010;93:1394–406.
Kawamura K, Kawamura N, Mulders SM, Sollewijn Gelpke MD, Hsueh AJ. Ovarian brain-derived neurotrophic factor (BDNF) promotes the development of oocytes into preimplantation embryos. Proc Natl Acad Sci USA. 2005;102:9206–11.
Lee E, Jeong YI, Park SM, Lee JY, Kim JH, Park SW, et al. Beneficial effects of brain-derived neurotropic factor on in vitro maturation of porcine oocytes. Reproduction. 2007;134:405–14.
Martins da Silva SJ, Gardner JO, Taylor JE, Springbett A, De Sousa PA, Anderson RA. Brain-derived neurotrophic factor promotes bovine oocyte cytoplasmic competence for embryo development. Reproduction. 2005;129:423–34.
Ge L, Han D, Lan GC, Zhou P, Liu Y, Zhang X, et al. Factors affecting the in vitro action of cumulus cells on the maturing mouse oocytes. Mol Reprod Dev. 2008;75:136–42.
Hussein TS, Thompson JG, Gilchrist RB. Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol. 2006;296:514–21.
McNatty KP, Moore LG, Hudson NL, Quirke LD, Lawrence SB, Reader K, et al. The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology. Reproduction. 2004;128:379–86.
Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci. 2005;118:5257–68.
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Yamada, M., Isaji, Y. Structural and functional changes linked to, and factors promoting, cytoplasmic maturation in mammalian oocytes. Reprod Med Biol 10, 69–79 (2011). https://doi.org/10.1007/s12522-011-0079-4
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DOI: https://doi.org/10.1007/s12522-011-0079-4