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DOI: 10.1055/s-2006-948551
Extracellular Matrix of the Cumulus-Oocyte Complex
Publication History
Publication Date:
30 August 2006 (online)
ABSTRACT
The mammalian oocyte is surrounded by several layers of cumulus granulosa cells that nurture the oocyte during its development and actively participate in the process of ovulation. After the ovulatory luteinizing hormone surge, a distinctive program of extracellular matrix production is initiated in the cumulus-oocyte complex. This process known as cumulus expansion or mucification involves synthesis of a backbone of long hyaluronan oligosaccharide chains that are cross-linked by a complex of hyaluronan binding cell surface and extracellular matrix proteins and proteoglycans. Active components of the cumulus matrix are synthesized directly by cumulus cells under the control of endocrine- and oocyte-derived factors, secreted by mural granulosa cells, or enter the follicle in blood plasma. Appropriate composition and assembly of the cumulus matrix is essential for ovulation, efficient passage of the oocyte through the oviduct, and for fertilization. This review describes the critical components and their functional roles in the cumulus matrix, as well as the molecular regulation of cumulus matrix gene expression.
KEYWORDS
Cumulus expansion - ovulation - oocyte maturation
REFERENCES
- 1 Eppig J J. Regulation of cumulus oophorus expansion by gonadotropins in vivo and in vitro. Biol Reprod. 1980; 23(3) 545-552
- 2 Salustri A, Yanagishita M, Underhill C B, Laurent T C, Hascall V C. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle. Dev Biol. 1992; 151(2) 541-551
- 3 Salustri A, Yanagishita M, Hascall V. Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification. J Biol Chem. 1989; 264(23) 13840-13847
- 4 Zuelke K A, Brackett B G. Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology. 1992; 131(6) 2690-2696
- 5 Roy S K, Terada D M. Activities of glucose metabolic enzymes in human preantral follicles: In vitro modulation by follicle-stimulating hormone, luteinizing hormone, epidermal growth factor, insulin-like growth factor I, and transforming growth factor beta1. Biol Reprod. 1999; 60(3) 763-768
- 6 Tsafriri A, Lieberman M E, Ahren K, Lindner H R. Dissociation between lh-induced aerobic glycolysis and oocyte maturation in cultured graafian follicles of the rat. Acta Endocrinol (Copenh). 1976; 81(2) 362-366
- 7 Sutton M L, Gilchrist R B, Thompson J G. 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. 2003; 9(1) 35-48
- 8 Sutton-McDowall M L, Gilchrist R B, Thompson J G. Cumulus expansion and glucose utilisation by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction. 2004; 128(3) 313-319
- 9 Fulop C, Kamath R V, Li Y et al.. Coding sequence, exon-intron structure and chromosomal localization of murine TNF-stimulated gene 6 that is specifically expressed by expanding cumulus cell-oocyte complexes. Gene. 1997; 202(1-2) 95-102
- 10 Fulop C, Salustri A, Hascall V C. Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch Biochem Biophys. 1997; 337(2) 261-266
- 11 Schoenfelder M, Einspanier R. Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol Reprod. 2003; 69(1) 269-277
- 12 Kimura N, Konno Y, Miyoshi K, Matsumoto H, Sato E. Expression of hyaluronan synthases and CD44 messenger RNAs in porcine cumulus-oocyte complexes during in vitro maturation. Biol Reprod. 2002; 66(3) 707-717
- 13 Weigel P H, Hascall V C, Tammi M. Hyaluronan synthases. J Biol Chem. 1997; 272(22) 13997-14000
- 14 Itano N, Sawai T, Yashida M et al.. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J Biol Chem. 1999; 274(35) 25085-25092
- 15 Toole B P. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004; 4(7) 528-539
- 16 Bourguignon L YW, Zhu H, Zhou B, Diedrich F, Singleton P A, Hung M-C. Hyaluronan promotes CD44v3-Vav2 interaction with Grb2-p185(HER2) and induces Rac1 and Ras signaling during ovarian tumor cell migration and growth. J Biol Chem. 2001; 276(52) 48679-48692
- 17 Misra S, Ghatak S, Toole B P. Regulation of MDR1 expression and drug resistance by a positive feedback loop involving hyaluronan, phosphoinositide 3-kinase, and ErbB2. J Biol Chem. 2005; 280(21) 20310-20315
- 18 Ghatak S, Misra S, Toole B P. Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J Biol Chem. 2005; 280(10) 8875-8883
- 19 Yokoo M, Miyahayashi Y, Naganuma T, Kimura N, Sasada H, Sato E. Identification of hyaluronic acid-binding proteins and their expressions in porcine cumulus-oocyte complexes during in vitro maturation. Biol Reprod. 2002; 67(4) 1165-1171
- 20 Ohta N, Saito H, Kuzumaki T et al.. Expression of CD44 in human cumulus and mural granulosa cells of individual patients in in-vitro fertilization programmes. Mol Hum Reprod. 1999; 5(1) 22-28
- 21 Saito H, Kaneko T, Takahashi T, Kawachiya S, Saito T, Hiroi M. Hyaluronan in follicular fluids and fertilization of oocytes. Fertil Steril. 2000; 74(6) 1148-1152
- 22 Kaneko T, Saito H, Toya M, Satio T, Nakahara K, Hiroi M. Hyaluronic acid inhibits apoptosis in granulosa cells via CD44. J Assist Reprod Genet. 2000; 17(3) 162-167
- 23 Lee K, Joo B, Na Y, Yoon M, Choi O, Kim W. Clinical assisted reproduction: Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J Assist Reprod Genet. 2001; 18(9) 490-498
- 24 Host E, Gabrielsen A, Lindenberg S, Smidt-Jensen S. Apoptosis in human cumulus cells in relation to zona pellucida thickness variation, maturation stage, and cleavage of the corresponding oocyte after intracytoplasmic sperm injection. Fertil Steril. 2002; 77(3) 511-515
- 25 Yuan Y Q, Van Soom A, Leroy J LMR et al.. Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology. 2005; 63(8) 2147-2163
- 26 Schmits R, Filmus J, Gerwin N et al.. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood. 1997; 90(6) 2217-2233
- 27 Protin U, Schweighoffer T, Jochum W, Hilberg F. CD44-deficient mice develop normally with changes in subpopulations and recirculation of lymphocyte subsets. J Immunol. 1999; 163(9) 4917-4923
- 28 Turley E A, Noble P W, Bourguignon L YW. Signaling properties of hyaluronan receptors. J Biol Chem. 2002; 277(7) 4589-4592
- 29 Yudin A I, Cherr G N, Katz D F. Structure of the cumulus matrix and zona pellucida in the golden hamster: a new view of sperm interaction with oocyte-associated extracellular matrices. Cell Tissue Res. 1988; 251(3) 555-564
- 30 Cherr G N, Yudin A I, Katz D F. Organization of the hamster cumulus extracellular matrix: A hyaluronate-glicoprotein gel, which modulates sperm access to the oocyte. Dev Growth Differ. 1990; 32 353-365
- 31 Steinbauch M, Loeb J. Isolation of an alpha2-globulin from human plasma. Nature. 1961; 192 1196
- 32 Zhuo L, Salustri A, Kimata K. A physiological function of serum proteoglycan bikunin: the chondroitin sulfate moiety plays a central role. Glycoconj J. 2002; 19 241-247
- 33 Chen L, Mao S, Larsen W. Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-alpha-trypsin inhibitor family. J Biol Chem. 1992; 267(17) 12380-12386
- 34 Powers R W, Chen L, Russell P T, Larsen W J. Gonadotropin-stimulated regulation of blood-follicle barrier is mediated by nitric oxide. Am J Physiol. 1995; 269(2) E290-E298
- 35 Hess K, Chen L, Larsen W. The ovarian blood follicle barrier is both charge- and size-selective in mice. Biol Reprod. 1998; 58(3) 705-711
- 36 Nagyova E, Camaioni A, Prochazka R, Salustri A. Covalent transfer of heavy chains of inter-{alpha}-trypsin inhibitor family proteins to hyaluronan in in vivo and in vitro expanded porcine oocyte-cumulus complexes. Biol Reprod. 2004; 71(6) 1838-1843
- 37 Eppig J J. Gonadotropin stimulation of the expansion of cumulus oophori isolated from mice: general conditions for expansion in vitro. J Exp Zool. 1979; 208(1) 111-120
- 38 Camaioni A, Hascall V, Yanagishita M, Salustri A. Effects of exogenous hyaluronic acid and serum on matrix organization and stability in the mouse cumulus cell-oocyte complex. J Biol Chem. 1993; 268(27) 20473-20481
- 39 Chen L, Zhang H, Powers R W, Russell P T, Larsen W J. Covalent linkage between proteins of the inter-alpha-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells. J Biol Chem. 1996; 271(32) 19409-19414
- 40 Zhuo L, Yoneda M, Zhao M et al.. Defect in SHAP-hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice. J Biol Chem. 2001; 276(11) 7693-7696
- 41 Sato H, Kajikawa S, Kuroda S et al.. Impaired fertility in female mice lacking urinary trypsin inhibitor. Biochem Biophys Res Commun. 2001; 281(5) 1154-1160
-
42 Zhuo L, Salustri A.
Role of serum-derived hyaluronan-associated protein in the construction of cumulus matrix and oocyte maturation . In: BEA, HVC Hyaluronan: Structure, Metabolism, Biological Activities, Therapeutic Applications. Matrix Biology Institute 2005: 731-735 - 43 Chen L, Mao S, McLean L, Powers R, Larsen W. Proteins of the inter-alpha-trypsin inhibitor family stabilize the cumulus extracellular matrix through their direct binding with hyaluronic acid. J Biol Chem. 1994; 269(45) 28282-28287
- 44 Yoshioka S, Ochsner S, Russell D L et al.. Expression of tumor necrosis factor-stimulated gene-6 in the rat ovary in response to an ovulatory dose of gonadotropin. Endocrinology. 2000; 141(11) 4114-4119
- 45 Carrette O, Nemade R V, Day A J, Brickner A, Larsen W J. TSG-6 is concentrated in the extracellular matrix of mouse cumulus oocyte complexes through hyaluronan and inter-alpha-inhibitor binding. Biol Reprod. 2001; 65(1) 301-308
- 46 Mukhopadhyay D, Hascall V C, Day A J, Salustri A, Fulop C. Two distinct populations of tumor necrosis factor-stimulated gene-6 protein in the extracellular matrix of expanded mouse cumulus cell-oocyte complexes. Arch Biochem Biophys. 2001; 394(2) 173-181
- 47 Ochsner S A, Day A J, Rugg M S, Breyer R M, Gomer R H, Richards J S. Disrupted function of tumor necrosis factor-α-stimulated gene 6 blocks cumulus cell-oocyte complex expansion. Endocrinology. 2003; 144(10) 4376-4384
- 48 Varani S, Elvin J A, Yan C et al.. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol. 2002; 16(6) 1154-1167
- 49 Kahmann J D, O'Brien R, Werner J M et al.. Localization and characterization of the hyaluronan-binding site on the link module from human TSG-6. Structure. 2000; 8 763-774
- 50 Fulop C, Szanto S, Mukhopadhyay D et al.. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development. 2003; 130(10) 2253-2261
- 51 Jessen T, Odum L. Role of tumour necrosis factor stimulated gene 6 (tsg-6) in the coupling of inter-alpha-trypsin inhibitor to hyaluronan in human follicular fluid. Reproduction. 2003; 125(1) 27-31
- 52 Rugg M S, Willis A C, Mukhopadhyay D et al.. Characterization of complexes formed between TSG-6 and inter-α-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J Biol Chem. 2005; 280(27) 25674-25686
- 53 Sanggaard K W, Karring H, Valnickova Z, Thogersen I B, Enghild J J. The TSG-6 I alpha I interaction promotes a transesterification cleaving the protein-glycosaminoglycan-protein (PGP) cross-link. J Biol Chem. 2005; 280(12) 11936-11942
- 54 Salustri A, Garlanda C, Hirsch E et al.. Ptx3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development. 2004; 131(7) 1577-1586
- 55 Bottazzi B, Vouret-Craviari V, Bastone A et al.. Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins c-reactive protein and serum amyloid p component. J Biol Chem. 1997; 272(52) 32817-32823
- 56 Eisenbach M, Tur-Kaspa I. Do human eggs attract spermatozoa?. Bioessays. 1999; 21(3) 203-210
- 57 LeBaron R G, Zimmermann D R, Ruoslahti E. Hyaluronate binding properties of versican. J Biol Chem. 1992; 267(14) 10003-10010
- 58 Camaioni A, Salustri A, Yanagishita M, Hascall V C. Proteoglycans and proteins in the extracellular matrix of mouse cumulus cell-oocyte complexes. Arch Biochem Biophys. 1996; 325(2) 190-198
- 59 Russell D L, Ochsner S A, Hsieh M, Mulders S, Richards J S. Hormone-regulated expression and localization of versican in the rodent ovary. Endocrinology. 2003; 144(3) 1020-1031
- 60 Mjaatvedt C H, Yamamura H, Capehart A A, Turner D, Markwald R R. The Cspg2 should be gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev Biol. 1998; 202(1) 56-66
- 61 Sandy J D, Westling J, Kenagy R D et al.. Versican V1 proteolysis in human aorta in vivo occurs at the glu441-ala442 bond, a site that is cleaved by recombinant adamts-1 and adamts-4. J Biol Chem. 2001; 276(16) 13372-13378
- 62 Doyle K MH, Russell D L, Sriraman V, Richards J S. Coordinate transcription of the Adamts-1 gene by luteinizing hormone and progesterone receptor. Mol Endocrinol. 2004; 18(10) 2463-2478
- 63 Robker R L, Russell D L, Espey L L, Lydon J P, O'Malley B W, Richards J S. Progesterone-regulated genes in the ovulation process: Adamts-1 and cathepsin l proteases. Proc Natl Acad Sci USA. 2000; 97(9) 4689-4694
- 64 Russell D L, Doyle K H, Ochsner S A, Sandy J D, Richards J S. Processing and localization of adamts-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J Biol Chem. 2003; 278 42330-42339
- 65 Mittaz L, Russell D L, Wilson T et al.. Adamts-1 is essential for the development and function of the urogenital system. Biol Reprod. 2004; 70(4) 1096-1105
- 66 Shindo T, Kurihara H, Kuno K et al.. Adamts-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest. 2000; 105(10) 1345-1352
- 67 Kawashima H, Hirose M, Hirose J, Nagakubo D, Plaas A HK, Miyasaka M. Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. J Biol Chem. 2000; 275(45) 35448-35456
- 68 Familiari G, Verlengia C, Nottola S A et al.. Heterogeneous distribution of fibronectin, tenascin-C, and laminin immunoreactive material in the cumulus-corona cells surrounding mature human oocytes from IVF-ET protocols-evidence that they are composed of different subpopulations: An immunohistochemical study using scanning confocal laser and fluorescence microscopy. Mol Reprod Dev. 1996; 43(3) 392-402
- 69 Relucenti M, Heyn R, Correr S, Familiari G. Cumulus oophorus extracellular matrix in the human oocyte: a role for adhesive proteins. Ital J Anat Embryol. 2005; 110(suppl 1) 219-224
- 70 Kobayashi H, Sun G W, Hirashima Y, Terao T. Identification of link protein during follicle development and cumulus cell cultures in rats. Endocrinology. 1999; 140(8) 3835-3842
- 71 Sun G W, Kobayashi H, Suzuki M, Kanayama N, Terao T. Follicle-stimulating hormone and insulin-like growth factor I synergistically induce up-regulation of cartilage link protein (Crtl1) via activation of phosphatidylinositol-dependent kinase/Akt in rat granulosa cells. Endocrinology. 2003; 144(3) 793-801
- 72 Sun G W, Kobayashi H, Suzuki M, Kanayama N, Terao T. Link protein as an enhancer of cumulus cell-oocyte complex expansion. Mol Reprod Dev. 2002; 63(2) 223-231
- 73 Shi S, Grothe S, Zhang Y et al.. Link protein has greater affinity for versican than aggrecan. J Biol Chem. 2004; 279(13) 12060-12066
- 74 Matsumoto K, Shionyu M, Go M et al.. Distinct interaction of versican/PG-M with hyaluronan and link protein. J Biol Chem. 2003; 278(42) 41205-41212
- 75 Hernandez-Gonzalez I, Gonzalez-Robayna I, Shimada M et al.. Gene expression profiles of cumulus cell oocyte complexes (COC) during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process?. Mol Endocrinol. 2006; 20 1300-1321
- 76 Aspberg A, Miura R, Bourdoulous S et al.. The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc Natl Acad Sci USA. 1997; 94(19) 10116-10121
- 77 Sirois J, Richards J S. Purification and characterization of a novel, distinct isoform of prostaglandin endoperoxide synthase induced by human chorionic gonadotropin in granulosa cells of rat preovulatory follicles. J Biol Chem. 1992; 267(9) 6382-6388
- 78 Wong W Y, Richards J S. Induction of prostaglandin H synthase in rat preovulatory follicles by gonadotropin-releasing hormone. Endocrinology. 1992; 130(6) 3512-3521
- 79 Sirois J, Simmons D, Richards J. Hormonal regulation of messenger ribonucleic acid encoding a novel isoform of prostaglandin endoperoxide h synthase in rat preovulatory follicles. Induction in vivo and in vitro. J Biol Chem. 1992; 267(16) 11586-11592
- 80 Eppig J J. Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol Reprod. 1981; 25(1) 191-195
- 81 Espey L L, Richards J S. Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biol Reprod. 2002; 67(6) 1662-1670
- 82 Mikuni M, Pall M, Peterson C M et al.. The selective prostaglandin endoperoxide synthase-2 inhibitor, NS-398, reduces prostaglandin production and ovulation in vivo and in vitro in the rat. Biol Reprod. 1998; 59(5) 1077-1083
- 83 Athanasiou S, Bourne T H, Khalid A et al.. Effects of indomethacin on follicular structure, vascularity, and function over the periovulatory period in women. Fertil Steril. 1996; 65(3) 556-560
- 84 Davis B J, Lennard D E, Lee C A et al.. Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta. Endocrinology. 1999; 140(6) 2685-2695
- 85 Ochsner S A, Russell D L, Day A J, Breyer R M, Richards J S. Decreased expression of tumor necrosis factor-alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP-2 null mice. Endocrinology. 2003; 144(3) 1008-1019
- 86 Dinchuk J E, Car B D, Focht R J et al.. Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase ii. Nature. 1995; 378(6555) 406-409
- 87 Lim H, Paria B C, Das S K et al.. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell. 1997; 91(2) 197-208
- 88 Wang H, Ma W-G, Tejada L et al.. Rescue of female infertility from the loss of cyclooxygenase-2 by compensatory up-regulation of cyclooxygenase-1 is a function of genetic makeup. J Biol Chem. 2004; 279(11) 10649-10658
- 89 Hizaki H, Segi E, Sugimoto Y et al.. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin e receptor subtype ep(2). Proc Natl Acad Sci USA. 1999; 96(18) 10501-10506
- 90 Tilley S L, Audoly L P, Hicks E H et al.. Reproductive failure and reduced blood pressure in mice lacking the EP2 prostaglandin E2 receptor. J Clin Invest. 1999; 103(11) 1539-1545
- 91 Downs S. Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol Reprod. 1989; 41(2) 371-379
- 92 Salustri A, Ulisse S, Yanagishita M, Hascall V. Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J Biol Chem. 1990; 265(32) 19517-19523
- 93 Tirone E, D'Alessandris C, Hascall V C, Siracusa G, Salustri A. Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocyte factor (or transforming growth factor beta 1). J Biol Chem. 1997; 272(8) 4787-4794
- 94 Park J-Y, Su Y-Q, Ariga M, Law E, Jin S-LC, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science. 2004; 303(5658) 682-684
- 95 Tsafriri A, Cao X, Ashkenazi H, Motola S, Popliker M, Pomerantz S H. Resumption of oocyte meiosis in mammals: On models, meiosis activating sterols, steroids and EGF-like factors. Mol Cell Endocrinol. 2005; 234(1-2) 37-45
- 96 Su Y-Q, Wigglesworth K, Pendola F L, O'Brien M J, Eppig J J. Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology. 2002; 143(6) 2221-2232
- 97 Elvin J A, Clark A T, Wang P, Wolfman N M, Matzuk M M. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol. 1999; 13(6) 1035-1048
- 98 Sirois J, Sayasith K, Brown K A, Stock A E, Bouchard N, Dore M. Cyclooxygenase-2 and its role in ovulation: a 2004 account. Hum Reprod Update. 2004; 10(5) 373-385
- 99 Salustri A, Yanagishita M, Hascall V C. Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol. 1990; 138(1) 26-32
- 100 Buccione R, Vanderhyden B C, Caron P J, Eppig J J. Fsh-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev Biol. 1990; 138(1) 16-25
- 101 Eppig J J, Wigglesworth K, Chesnel F. Secretion of cumulus expansion enabling factor by mouse oocytes: relationship to oocyte growth and competence to resume meiosis. Dev Biol. 1993; 158(2) 400-409
- 102 Singh B, Zhang X, Armstrong D. Porcine oocytes release cumulus expansion-enabling activity even though porcine cumulus expansion in vitro is independent of the oocyte. Endocrinology. 1993; 132(4) 1860-1862
- 103 Vanderhyden B C, Caron P J, Buccione R, Eppig J J. Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol. 1990; 140(2) 307-317
- 104 Ralph J H, Telfer E E, Wilmut I. Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol Reprod Dev. 1995; 42(2) 248-253
- 105 Hussein T S, Froiland D A, Amato F, Thompson J G, Gilchrist R B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci. 2005; 118 5257-5268
- 106 Vanderhyden B C, Macdonald E A, Nagyova E, Dhawan A. Evaluation of members of the TGFbeta superfamily as candidates for the oocyte factors that control mouse cumulus expansion and steroidogenesis. Reproduction. 2003; 61 55-70
- 107 Dragovic R A, Ritter L J, Schulz S J, Amato F, Armstrong D T, Gilchrist R B. Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology. 2005; 146(6) 2798-2806
- 108 Gui L-M, Joyce I M. RNA interference evidence that growth differentiation factor-9 mediates oocyte regulation of cumulus expansion in mice. Biol Reprod. 2005; 72(1) 195-199
- 109 Elvin J A, Yan C, Wang P, Nishimori K, Matzuk M M. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol. 1999; 13(6) 1018-1034
- 110 Juengel J L, Hudson N L, Heath D A et al.. Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol Reprod. 2002; 67(6) 1777-1789
- 111 Di Pasquale E, Rossetti R, Marozzi A et al.. Identification of new variants of human bmp-15 gene in a large cohort of women with premature ovarian failure. J Clin Endocrinol Metab. 2006; 91 1976-1979
- 112 Di Pasquale E, Beck-Peccoz P, Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (Bmp15) gene. Am J Hum Genet. 2004; 75(1) 106-111
- 113 Erickson G F, Shimasaki S. The role of the oocyte in folliculogenesis. Trends Endocrinol Metab. 2000; 11(5) 193-198
- 114 McNatty K P, Juengel J L, Reader K L et al.. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction. 2005; 129(4) 481-487
- 115 Mazerbourg S, Klein C, Roh J et al.. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol. 2004; 18(3) 653-665
- 116 Kaivo-Oja N, Mottershead D G, Mazerbourg S et al.. Adenoviral gene transfer allows smad-responsive gene promoter analyses and delineation of type I receptor usage of transforming growth factor-β family ligands in cultured human granulosa luteal cells. J Clin Endocrinol Metab. 2005; 90(1) 271-278
- 117 Su Y-Q, Denegre J M, Wigglesworth K, Pendola F L, O'Brien M J, Eppig J J. Oocyte-dependent activation of mitogen-activated protein kinase (Erk1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus cell complex. Dev Biol. 2003; 263(1) 126-138
- 118 Van Soom A, Tanghe S, De Pauw I, Maes D, de Kruif A. Function of the cumulus oophorus before and during mammalian fertilization. Reprod Domest Anim. 2002; 37(3) 144-151
- 119 Hong S J, Chiu P C, Lee K F, Tse J MY, Ho P C, Yeung W SB. Establishment of a capillary-cumulus model to study the selection of sperm for fertilization by the cumulus oophorus. Hum Reprod. 2004; 19(7) 1562-1569
- 120 Drahorad J, Tesarik J, Cechova D, Vilim V. Proteins and glycosaminoglycans in the intercellular matrix of the human cumulus-oophorus and their effect on conversion of proacrosin to acrosin. J Reprod Fertil. 1991; 93(2) 253-262
- 121 Tesarik J, Pilka L, Drahorad J, Cechova D, Veselsky L. The role of cumulus cell-secreted proteins in the development of human sperm fertilizing ability: implication IVF. Hum Reprod. 1988; 3(1) 129-132
- 122 Lam X, Gieseke C, Knoll M, Talbot P. Assay and importance of adhesive interaction between hamster (Mesocricetus auratus) oocyte-cumulus complexes and the oviductal epithelium. Biol Reprod. 2000; 62(3) 579-588
- 123 Talbot P, Shur B D, Myles D G. Cell adhesion and fertilization: steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion. Biol Reprod. 2003; 68(1) 1-9
- 124 Odor D L, Blandau R J. Egg transport over the fimbrial surface of the rabbit oviduct under experimental conditions. Fertil Steril. 1973; 24(4) 292-300
- 125 Mahi-Brown C A, Yanagimachi R. Parameters influencing ovum pick-up by. Gamete Res. 1983; 8 1-10
-
126 Harper J K.
Gamete and zygote transport . In: Knobil E, Neill JD The Physiology of Reproduction. New York; Raven Press 1994: 123-185 - 127 Suzuki M, Kobayashi H, Tanaka Y, Kanayama N, Terao T. Reproductive failure in mice lacking inter-alpha-trypsin inhibitor (iti)-iti target genes in mouse ovary identified by microarray analysis. J Endocrinol. 2004; 183(1) 29-38
- 128 Fatehi A N, Roelen B A, Colenbrander B et al.. Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development. Zygote. 2005; 13(2) 177-185
- 129 Luciano A M, Lodde V, Beretta M S, Colleoni S, Lauria A, Modina S. Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 3′5′-monophosphate, and glutathione. Mol Reprod Dev. 2005; 71(3) 389-397
- 130 Wu Y, Wu J, Lee D Y et al.. Versican protects cells from oxidative stress-induced apoptosis. Matrix Biol. 2005; 24(1) 3-13
- 131 Ball G, Leibfried M, Lenz R, Ax R, Bavister B, First N. Factors affecting successful in vitro fertilization of bovine follicular oocytes. Biol Reprod. 1983; 28(3) 717-725
- 132 Laufer N, Tarlatzis B C, Naftolin F. In vitro fertilization: state of the art. Semin Reprod Endocrinol. 1984; 2 197-219
- 133 Foote R H. In vitro fertilization and embryo transfer in domestic animals: Applications in animals and implications for humans. J In Vitro Fert Embryo Transf. 1987; 4(2) 73-88
- 134 McKenzie L J, Pangas S A, Carson S A et al.. Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod. 2004; 19(12) 2869-2874
- 135 Zhang X, Jafari N, Barnes R B, Confino E, Milad M, Kazer R R. Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil Steril. 2005; 83(4, suppl 1) 1169-1179
Darryl L RussellPh.D.
School of Paediatrics and Reproductive Health, Research Centre for Reproductive Health, The University of Adelaide
Adelaide, South Australia 5005, Australia
Email: darryl.russell@adelaide.edu.au