Impact of Extracellular Matrix Remodeling on Ovulation and the Folliculo-Luteal Transition

ABSTRACT

Follicular rupture and the transformation of an estrogenic preovulatory follicle into a highly vascularized corpus luteum capable of producing large quantities of progesterone are required for the establishment of pregnancy. These processes are dependent upon the precise remodeling of the ovarian extracellular matrix (ECM). Such remodeling occurs both at the level of synthesis and/or proteolytic degradation of ECM proteins. Enzymes known to have important roles in ovarian ECM remodeling include matrix metalloproteinases, plasminogen activators/plasmin, and ADAMTS (a disintegrin and metalloproteinase with thrombospondin-like motifs). Each of the preceding proteases has corresponding inhibitors capable of regulating proteolytic activity temporally and spatially. This review focuses on recent contributions to our understanding of ovarian ECM remodeling that have furthered our appreciation of the role of proteinases in ovulation and the differentiation of follicular cells into the luteal phenotype.

KEYWORDS

Metalloproteinases - tissue inhibitors of metalloproteinases (TIMPs) - plasminogen - plasminogen activator (PA) - PA inhibitor - ADAMTS - cumulus - corpus luteum - ovary - review

REFERENCES

• 1 Espey L L, Lipner H. Ovulation. In: Knobil E, Neill J The Physiology of Reproduction. 2nd ed. New York; Raven Press 1994: 725-780
• 2 Downs S M, Longo F J. Prostaglandins and preovulatory follicular maturation in mice.  J Exp Zool. 1983;  228 99-108
• 3 Espey L L, Coons P J, Marsh J M, LeMaire W J. Effect of indomethacin on preovulatory changes in the ultrastructure of rabbit Graafian follicles.  Endocrinology. 1981;  108 1040-1048
• 4 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 2685-2695
• 5 Chen L, Mao S J, Larsen W J. 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 12380-12386
• 6 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 1154-1167
• 7 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 10501-10506
• 8 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 1020-1031
• 9 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;  394 173-181
• 10 Irving-Rodgers H F, Rodgers R J. Extracellular matrix in ovarian follicular development and disease.  Cell Tissue Res. 2005;  322 89-98
• 11 Richards J S. Ovulation: new factors that prepare the oocyte for fertilization.  Mol Cell Endocrinol. 2005;  234 75-79
• 12 Sato H, Kajikawa S, Kuroda S et al.. Impaired fertility in female mice lacking urinary trypsin inhibitor.  Biochem Biophys Res Commun. 2001;  281 1154-1160
• 13 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 7693-7696
• 14 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 2253-2261
• 15 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 EP2 null mice.  Endocrinology. 2003;  144 1008-1019
• 16 Curry Jr T E, Osteen K G. The matrix metalloproteinase system changes, regulation, and impact throughout the ovarian and uterine reproductive cycle.  Endocr Rev. 2003;  24 428-465
• 17 Smith M F, McIntush E W, Smith G W. Mechanisms associated with corpus luteum development.  J Anim Sci. 1994;  72 1857-1872
• 18 Stouffer R L, Brannian J D. The function and regulation of cell populations composing the corpus luteum of the ovarian cycle. In: Adashi EY, Leung PCK The Ovary. New York; Raven Press 1993: 245-259
• 19 Acosta T J, Miyamoto A. Vascular control of ovarian function: ovulation, corpus luteum formation and regression.  Anim Reprod Sci. 2004;  82-83 127-140
• 20 Schams D, Berisha B. Regulation of corpus luteum function in cattle-an overview.  Reprod Domest Anim. 2004;  39 241-251
• 21 Luck M R, Zhao Y. Identification and measurement of collagen in the bovine corpus luteum and its relationship with ascorbic acid and tissue development.  J Reprod Fertil. 1993;  99 647-652
• 22 Luck M R, Zhao Y. Identification and measurement of collagen in the bovine corpus luteum and its relationship with ascorbic acid and tissue development.  J Reprod Fertil. 1993;  99 647-652
• 23 Aten R F, Kolodecik T R, Behrman H R. A cell adhesion receptor antiserum abolishes, whereas laminin and fibronectin glycoprotein components of extracellular matrix promote, luteinization of cultured rat granulosa cells.  Endocrinology. 1995;  136 1753-1758
• 24 Ohnishi J, Ohnishi E, Shibuya H, Takahashi T. Functions for proteinases in the ovulatory process.  Biochim Biophys Acta. 2005;  1751 95-109
• 25 Ny T, Wahlberg P, Brandstrom I J. Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems.  Mol Cell Endocrinol. 2002;  187 29-38
• 26 Smith M F, Ricke W A, Bakke L J, Dow M PD, Smith G W. Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors.  Mol Cell Endocrinol. 2002;  191 45-56
• 27 Murdoch W J, Gottsch M L. Proteolytic mechanisms in the ovulatory folliculo-luteal transformation.  Connect Tissue Res. 2003;  44 50-57
• 28 Goldman S, Shalev E. MMPS and TIMPS in ovarian physiology and pathophysiology.  Front Biosci. 2004;  9 2474-2483
• 29 Birkedal-Hansen H, Moore W GI, Bodden M K. Matrix metalloproteinases: a review.  Crit Rev Oral Biol Med. 1993;  4 197-250
• 30 Nagase H, Woessner Jr J F. Matrix metalloproteinases.  J Biol Chem. 1999;  274 21491-21494
• 31 Woessner Jr J F, Nagase H. Matrix Metalloproteinases and TIMPs. New York; Oxford University Press 2000: 1-223
• 32 Murphy G, Knäuper V, Cowell S et al.. Evaluation of some newer matrix metalloproteinases.  Ann NY Acad Sci. 1999;  878 25-39
• 33 Kleiner Jr D E, Stetler-Stevenson W G. Structural biochemistry and activation of matrix metalloproteases.  Curr Opin Cell Biol. 1993;  5 891-897
• 34 Sternlicht M D, Werb Z. How matrix metalloproteinases regulate cell behavior.  Annu Rev Cell Dev Biol. 2001;  17 463-516
• 35 Gomez D E, Alonzo D F, Yoshiji H, Thorgeirsson U P. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions.  Eur J Cell Biol. 1997;  74 111-122
• 36 Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function.  Biochim Biophys Acta. 2000;  1477 267-283
• 37 Gaddy-Kurten D, Hickey G J, Fey G H, Gauldie J, Richards J S. Hormonal regulation and tissue-specific localization of α₂- macroglobulin in rat ovarian follicles and corpora lutea.  Endocrinology. 1989;  125 2985-2995
• 38 Dajee M, Kazansky A V, Raught B, Hocke G M, Fey G H, Richards J S. Prolactin induction of the alpha 2-macroglobulin gene in rat ovarian granulosa cells: stat 5 activation and binding to the interleukin-6 response element.  Mol Endocrinol. 1996;  10 171-184
• 39 Stetler-Stevenson W G, Krutzsch H C, Liotta L A. Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family.  J Biol Chem. 1989;  264 17374-17378
• 40 Leco K J, Hayden L J, Sharma R R, Rocheleau H, Greenberg A H, Edwards D R. Differential regulation of TIMP-1 and TIMP-2 mRNA expression in normal and Ha-ras-transformed murine fibroblasts.  Gene. 1992;  117 209-217
• 41 Pavloff N, Staskus P W, Kishnani N S, Hawkes S P. A new inhibitor of metalloproteinases from chicken: ChIMP-3. A third member of the TIMP family.  J Biol Chem. 1992;  267 17321-17326
• 42 Leco K J, Khokha R, Pavloff N, Hawkes S P, Edwards D R. Tissue inhibitor of metalloproteinases-3 (TIMP-3) is an extracellular matrix-associated protein with a distinctive pattern of expression in mouse cells and tissues.  J Biol Chem. 1994;  269 9352-9360
• 43 Leco K J, Apte S, Taniguchi G T et al.. Murine tissue inhibitor of metalloproteinases-4 (Timp-4): cDNA isolation and expression in adult mouse tissues.  FEBS Lett. 1997;  401 213-217
• 44 Stratmann B, Farr M, Tschesche H. Characterization of C-terminally truncated human tissue inhibitor of metalloproteinases-4 expressed in Pichia pastoris.  Biol Chem. 2001;  382 987-991
• 45 Ny T, Wahlberg P, Brandstrom I J. Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems.  Mol Cell Endocrinol. 2002;  187 29-38
• 46 Raum D, Marcus D, Alper C A, Levey R, Taylor P D, Starzl T E. Synthesis of human plasminogen by the liver.  Science. 1980;  208 1036-1037
• 47 Sappino A P, Madani R, Huarte J et al.. Extracellular proteolysis in the adult murine brain.  J Clin Invest. 1993;  92 679-685
• 48 Alexander C M, Werb Z. Targeted disruption of the tissue inhibitor of metalloproteinases gene increases the invasive behavior of primitive mesenchymal cells derived from embryonic stem cells in vitro.  J Cell Biol. 1992;  118 727-739
• 49 Mignatti P, Robbins E, Rifkin D B. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade.  Cell. 1986;  47 487-498
• 50 DeClerck Y A, Laug W E. Cooperation between matrix metalloproteinases and the plasminogen activator-plasmin system in tumor progression.  Enzyme Protein. 1996;  49 72-84
• 51 Lijnen H R, Van H B, Lupu F, Moons L, Carmeliet P, Collen D. Function of the plasminogen/plasmin and matrix metalloproteinase systems after vascular injury in mice with targeted inactivation of fibrinolytic system genes.  Arterioscler Thromb Vasc Biol. 1998;  18 1035-1045
• 52 Makowski G S, Ramsby M L. Binding of latent matrix metalloproteinase 9 to fibrin: activation via a plasmin-dependent pathway.  Inflammation. 1998;  22 287-305
• 53 Murphy G, Cockett M I, Ward R V, Docherty A JP. Matrix metalloproteinase degradation of elastin, type IV collagen and proteoglycan. A quantitative comparison of the activities of 95 kDa and 72 kDa gelatinases, stromelysins-1 and -2 and punctuated metalloproteinase (PUMP).  Biochem J. 1991;  277 277-279
• 54 Aertgeerts K, De Bondt H L, De R C, Declerck P J. A model of the reactive form of plasminogen activator inhibitor-1.  J Struct Biol. 1994;  113 239-245
• 55 Petty H R, Worth R G, Todd III R F. Interactions of integrins with their partner proteins in leukocyte membranes.  Immunol Res. 2002;  25 75-95
• 56 Kjoller L. The urokinase plasminogen activator receptor in the regulation of the actin cytoskeleton and cell motility.  Biol Chem. 2002;  383 5-19
• 57 Ge Y, Elghetany M T. Urokinase plasminogen activator receptor (CD87): something old, something new.  Lab Hematol. 2003;  9 67-71
• 58 Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K. Molecular cloning of a gene encoding a new type of metalloproteinase- disintegrin family protein with thrombospondin motifs as an inflammation associated gene.  J Biol Chem. 1997;  272 556-562
• 59 Porter S, Clark I M, Kevorkian L, Edwards D R. The ADAMTS metalloproteinases.  Biochem J. 2005;  386 15-27
• 60 Somerville R P, Longpre J M, Jungers K A et al.. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1.  J Biol Chem. 2003;  278 9503-9513
• 61 Kashiwagi M, Enghild J J, Gendron C et al.. Altered proteolytic activities of ADAMTS-4 expressed by C-terminal processing.  J Biol Chem. 2004;  279 10109-10119
• 62 Kuno K, Matsushima K. ADAMTS-1 protein anchors at the extracellular matrix through the thrombospondin type I motifs and its spacing region.  J Biol Chem. 1998;  273 13912-13917
• 63 Blelloch R, Newman C, Kimble J. Control of cell migration during Caenorhabditis elegans development.  Curr Opin Cell Biol. 1999;  11 608-613
• 64 Nishiwaki K, Hisamoto N, Matsumoto K. A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans .  Science. 2000;  288 2205-2208
• 65 Fessler J H, Kramerova I, Kramerov A, Chen Y, Fessler L I. Papilin, a novel component of basement membranes, in relation to ADAMTS metalloproteases and ECM development.  Int J Biochem Cell Biol. 2004;  36 1079-1084
• 66 Kramerova I A, Kawaguchi N, Fessler L I et al.. Papilin in development; a pericellular protein with a homology to the ADAMTS metalloproteinases.  Development. 2000;  127 5475-5485
• 67 Kashiwagi M, Tortorella M, Nagase H, Brew K. TIMP-3 is a potent inhibitor of aggrecanase 1 (ADAM-TS4) and aggrecanase 2 (ADAM-TS5).  J Biol Chem. 2001;  276 12501-12504
• 68 Rodriguez-Manzaneque J C, Westling J, Thai S N et al.. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors.  Biochem Biophys Res Commun. 2002;  293 501-508
• 69 Tortorella M D, Arner E C, Hills R et al.. Alpha2-macroglobulin is a novel substrate for ADAMTS-4 and ADAMTS-5 and represents an endogenous inhibitor of these enzymes.  J Biol Chem. 2004;  279 17554-17561
• 70 Schochet S S. A suggestion as to the process of ovulation and ovarian cyst formation.  Anat Rec. 1916;  10 447-457
• 71 Bjersing L, Cajander S. Ovulation and the mechanism of follicle rupture. V. Ultrastructure of tunica albuginea and theca externa of rabbit graafian follicles prior to induced ovulation.  Cell Tissue Res. 1974;  153 15-30
• 72 Russell D L, Doyle K M, Ochsner S, 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
• 73 Morales T I, Woessner Jr J F, Marsh J M, LeMaire W J. Collagen, collagenase and collagenolytic activity in rat graafian follicles during follicular growth and ovulation.  Biochim Biophys Acta. 1983;  756 119-122
• 74 Murdoch W J, McCormick R J. Enhanced degradation of collagen within apical vs. basal wall of ovulatory ovine follicle.  Am J Physiol. 1992;  263 E221-E225
• 75 Fukumoto M, Yajima Y, Okamura H, Midorikawa O. Collagenolytic enzyme activity in human ovary: an ovulatory enzyme system.  Fertil Steril. 1981;  36 746-750
• 76 Reich R, Daphna-Iken D, Chun S Y et al.. Preovulatory changes in ovarian expression of collagenases and tissue metalloproteinase inhibitor messenger ribonucleic acid: Role of eicosanoids.  Endocrinology. 1991;  129 1869-1875
• 77 Curry Jr T E, Komar C M, Burns P D, Nothnick W B. Periovulatory changes in ovarian metalloproteinases and tissue inhibitors of metalloproteinases (TIMPs) following indomethacin treatment. In: Adashi EY Ovulation: Evolving Scientific and Clinical Concepts. New York; Springer Verlag 2000: 265-276
• 78 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-1and cathepsin L proteases.  Proc Natl Acad Sci USA. 2000;  97 4689-4694
• 79 Balbín M, Fueyo A, Lopez J M, Diez-Itza I, Velasco G, López-Otín C. Expression of collagenase-3 in the rat ovary during the ovulatory process.  J Endocrinol. 1996;  149 405-415
• 80 Jo M, Thomas L E, Wheeler S E, Curry Jr T E. Membrane-type 1 matrix metalloproteinase (MMP)-associated MMP-2 activation increases in the rat ovary in response to an ovulatory dose of human chorionic gonadotropin.  Biol Reprod. 2004;  70 1024-1033
• 81 Jo M, Curry Jr T E. Regulation of matrix metalloproteinase-19 messenger RNA expression in the rat ovary.  Biol Reprod. 2004;  71 1796-1806
• 82 Smedts A M, Curry Jr T E. Expression of basigin, an inducer of matrix metalloproteinases, in the rat ovary.  Biol Reprod. 2005;  73 80-87
• 83 Bakke L J, Dow MPD, Cassar C A, Peters M W, Pursley J R, Smith G W. Effect of the preovulatory gonadotropin surge on matrix metalloproteinase (MMP)-14, MMP-2, and tissue inhibitor of metalloproteinase-2 expression within bovine periovulatory follicular and luteal tissue.  Biol Reprod. 2002;  66 1627-1634
• 84 Bakke L J, Li Q, Cassar C A, Dow M P, Pursley J R, Smith G W. Gonadotropin surge-induced differential upregulation of collagenase-1 (MMP-1) and collagenase-3 (MMP-13) mRNA and protein in bovine preovulatory follicles.  Biol Reprod. 2004;  71 605-612
• 85 Imai K, Khandoker M, Yonai M et al.. Matrix metalloproteinases-2 and -9 activities in bovine follicular fluid of different-sized follicles: relationship to intra-follicular inhibin and steroid concentrations.  Domest Anim Endocrinol. 2003;  24 171-183
• 86 Kim M, Hong M, Kim J et al.. Bovine follicular fluid and serum share a unique isoform of matrix metalloproteinase-2 that is degraded by the oviductal fluid.  Biol Reprod. 2001;  65 1726-1731
• 87 Murdoch W J. Regulation of collagenolysis and cell death by plasmin within the formative stigma of preovulatory ovine follicles.  J Reprod Fertil. 1998;  113 331-336
• 88 Black R A, Rauch C T, Kozlosky C J et al.. A metalloproteinase disintegrin that releases tumour-necrosis factor-α from cells.  Nature. 1997;  385 729-733
• 89 Johnson M L, Murdoch J, Van Kirk E A, Kaltenbach J E, Murdoch W J. Tumor necrosis factor alpha regulates collagenolytic activity in preovulatory ovine follicles: relationship to cytokine secretion by the oocyte-cumulus cell complex.  Biol Reprod. 1999;  61 1581-1585
• 90 Murdoch W J, Van Kirk E A, Murdoch J. Plasmin cleaves tumor necrosis factor α exodomain from sheep folliclular endothelium: implication in the ovulatory process.  Biol Reprod. 1999;  60 1166-1171
• 91 Colgin D C, Murdoch W J. Evidence for a role of the ovarian surface epithelium in the ovulatory mechanism of the sheep: secretion of urokinase-type plasminogen activator.  Anim Reprod Sci. 1997;  47 197-204
• 92 Gottsch M L, Van Kirk E A, Murdoch W J. Tumour necrosis factor alpha up-regulates matrix metalloproteinase-2 activity in periovulatory ovine follicles: metamorphic and endocrine implications.  Reprod Fertil Dev. 2000;  12 75-80
• 93 Murdoch W J, Colgin D C, Ellis J A. Role of tumor necrosis factor-alpha in the ovulatory mechanism of ewes.  J Anim Sci. 1997;  75 1601-1605
• 94 Gottsch M L, Van Kirk E A, Murdoch W J. Role of matrix metalloproteinase 2 in the ovulatory folliculo-luteal transition of ewes.  Reproduction. 2002;  124 347-352
• 95 Montgomery R V, Limback S D, Roby K F, Terranova P F. Differential responses of granulosa cells from small and large follicles to follicle stimulating hormone (FSH) during the menstrual cycle and acyclicity: effects of tumour necrosis factor-alpha.  Hum Reprod. 1998;  13 1285-1291
• 96 Zolti M, Meirom R, Shemesh M et al.. Granulosa cells as a source and target organ for tumor necrosis factor-alpha.  FEBS Lett. 1990;  261 253-255
• 97 Loret de Mola J R, Goldfarb J M, Hecht B R, Baumgardner G P, Babbo C J, Friedlander M A. Gonadotropins induce the release of interleukin-1 beta, interleukin-6 and tumor necrosis factor-alpha from the human preovulatory follicle.  Am J Reprod Immunol. 1998;  39 387-390
• 98 Brannstrom M, Bonello N, Wang L J, Norman R J. Effects of tumour necrosis factor alpha (TNF alpha) on ovulation in the rat ovary.  Reprod Fertil Dev. 1995;  7 67-73
• 99 Hales H A, Peterson C M, Mitchell M D, Jones K P, Hatasaka H H, Poulson A M. Tumor necrosis factor-alpha inhibits ovulation and steroidogenesis, but not prostaglandin production in the perfused rat ovary.  J Soc Gynecol Investig. 1994;  1 59-64
• 100 Yang W L, Godwin A K, Xu X X. Tumor necrosis factor-alpha-induced matrix proteolytic enzyme production and basement membrane remodeling by human ovarian surface epithelial cells: molecular basis linking ovulation and cancer risk.  Cancer Res. 2004;  64 1534-1540
• 101 Roland I H, Yang W L, Yang D H et al.. Loss of surface and cyst epithelial basement membranes and preneoplastic morphologic changes in prophylactic oophorectomies.  Cancer. 2003;  98 2607-2623
• 102 Chaffin C L, Stouffer R L. Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation.  Biol Reprod. 1999;  61 14-21
• 103 Duffy D M, Stouffer R L. Luteinizing hormone acts directly at granulosa cells to stimulate periovulatory processes: modulation of luteinizing hormone effects by prostaglandins.  Endocrine. 2003;  22 249-256
• 104 Shalev E, Goldman S, Ben-Shlomo I. The balance between MMP-9 and MMP-2 and their tissue inhibitor (TIMP)-1 in luteinized granulosa cells: comparison between women with PCOS and normal ovulatory women.  Mol Hum Reprod. 2001;  7 325-331
• 105 Lahav-Baratz S, Kraiem Z, Shiloh S, Koifman M. Decreased expression of tissue inhibitor of matrix metalloproteinases in follicular fluid from women with polycystic ovaries compared with normally ovulating patients undergoing in vitro fertilization.  Fertil Steril. 2003;  79 567-571
• 106 Lee D M, Lee T K, Song H B, Kim C H. The expression of matrix metalloproteinase-9 in human follicular fluid is associated with in vitro fertilisation pregnancy.  BJOG. 2005;  112 946-951
• 107 Nikolettos N, Asimakopoulos B, Tentes L, Schopper B, Al-Hasani S. Matrix metalloproteinases 2 and 9 in follicular fluids of patients undergoing controlled ovarian stimulation for ICSI/ET.  In Vivo. 2003;  17 201-204
• 108 D'Ascenzo S, Giusti I, Millimaggi D et al.. Intrafollicular expression of matrix metalloproteinases and their inhibitors in normally ovulating women compared with patients undergoing in vitro fertilization treatment.  Eur J Endocrinol. 2004;  151 87-91
• 109 Dow M P, Bakke L J, Cassar C A, Peters M W, Pursley J R, Smith G W. Gonadotropin surge-induced up-regulation of the plasminogen activators (tissue plasminogen activator and urokinase plasminogen activator) and the urokinase plasminogen activator receptor within bovine periovulatory follicular and luteal tissue.  Biol Reprod. 2002;  66 1413-1421
• 110 Dow M P, Bakke L J, Cassar C A, Peters M W, Pursley J R, Smith G W. Gonadotrophin surge-induced upregulation of mRNA for plasminogen activator inhibitors 1 and 2 within bovine periovulatory follicular and luteal tissue.  Reproduction. 2002;  123 711-719
• 111 Liu Y X, Liu K, Feng Q et al.. Tissue-type plasminogen activator and its inhibitor plasminogen activator inhibitor type 1 are coordinately expressed during ovulation in the rhesus monkey.  Endocrinology. 2004;  145 1767-1775
• 112 Ohnishi J, Yokota J, Rajapakse R G et al.. Activity of an enzyme converting single-chain tissue-type plasminogen activator to the two-chain form in preovulatory human follicular fluid.  Mol Reprod Dev. 2004;  67 178-185
• 113 Tarkun I, Canturk Z, Arslan B C, Turemen E, Tarkun P. The plasminogen activator system in young and lean women with polycystic ovary syndrome.  Endocr J. 2004;  51 467-472
• 114 Diamanti-Kandarakis E, Palioniko G, Alexandraki K, Bergiele A, Koutsouba T, Bartzis M. The prevalence of 4G5G polymorphism of plasminogen activator inhibitor-1 (PAI-1) gene in polycystic ovarian syndrome and its association with plasma PAI-1 levels.  Eur J Endocrinol. 2004;  150 793-798
• 115 Reich R, Tsafriri A, Mechanic G L. The involvement of collagenolysis in ovulation in the rat.  Endocrinology. 1985;  116 522-527
• 116 Tsafriri A, Bicsak T A, Cajanders S B, Ny T, Hsueh AJW. Suppression of ovulation rat by antibodies to tissue-type plasminogen activator and α₂-antiplasmin.  Endocrinology. 1989;  124 415-421
• 117 Carmeliet P, Schoonjans L, Kieckens L et al.. Physiological consequences of loss of plasminogen activator gene function in mice.  Nature. 1994;  368 419-424
• 118 Leonardsson G, Peng X R, Liu K et al.. Ovulation efficiency is reduced in mice that lack plasminogen activator gene function: Functional redundancy among physiological plasminogen activators.  Proc Natl Acad Sci USA. 1995;  92 12446-12450
• 119 Shozu M, Minami N, Yokoyama H et al.. ADAMTS-1 is involved in normal follicular development, ovulatory process and organization of the medullary vascular network in the ovary.  J Mol Endocrinol. 2005;  35 343-355
• 120 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 1345-1352
• 121 Richards J S, Hernandez-Gonzalez I, Gonzalez-Robayna I et al.. Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation.  Biol Reprod. 2005;  72 1241-1255
• 122 Shimada M, Nishibori M, Yamashita Y, Ito J, Mori T, Richards J S. Down-regulated expression of A disintegrin and metalloproteinase with thrombospondin-like repeats-1 by progesterone receptor antagonist is associated with impaired expansion of porcine cumulus-oocyte complexes.  Endocrinology. 2004;  145 4603-4614
• 123 Boerboom D, Russell D L, Richards J S, Sirois J. Regulation of transcripts encoding ADAMTS-1 (a disintegrin and metalloproteinase with thrombospondin-like motifs-1) and progesterone receptor by human chorionic gonadotropin in equine preovulatory follicles.  J Mol Endocrinol. 2003;  31 473-485
• 124 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 1096-1105
• 125 Park J Y, Su Y Q, Ariga M, Law E, Jin S L, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle.  Science. 2004;  303 682-684
• 126 Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A. Epidermal growth factor family members: endogenous mediators of the ovulatory response.  Endocrinology. 2005;  146 77-84
• 127 Freimann S, Ben-Ami I, Dantes A et al.. Differential expression of genes coding for EGF-like factors and ADAMTS1 following gonadotropin stimulation in normal and transformed human granulosa cells.  Biochem Biophys Res Commun. 2005;  333 935-943
• 128 Madan P, Bridges P J, Komar C M et al.. Expression of messenger RNA for ADAMTS subtypes changes in the periovulatory follicle after the gonadotropin surge and during luteal development and regression in cattle.  Biol Reprod. 2003;  69 1506-1514
• 129 Niswender G D, Schwall R H, Fitz T A, Farin C E, Sawyer H R. Regulation of luteal function in domestic ruminants: new concepts.  Recent Prog Horm Res. 1985;  41 101-151
• 130 Luck M R, Münker M. Beta adrenoceptors mediate the catecholamine-induced stimulation of oxytocin secretion from cultured bovine granulosa cells.  Reprod Fertil Dev. 1991;  3 715-723
• 131 Hwang D H, Kee S H, Kim K, Cheong K S, Yoo Y B, Lee B L. Role of reconstituted basement membrane in human granulosa cell culture.  Endocr J. 2000;  47 177-183
• 132 Nothnick W B, Keeble S C, Curry Jr T E. Collagenase, gelatinase, and proteoglycanase mRNA expression and activity during luteal development, maintenance, and regression in the pseudopregnant rat ovary.  Biol Reprod. 1996;  54 616-624
• 133 Li Q L, Wang H M, Lin H Y et al.. Expression of gelatinases and their tissue inhibitors in rat corpus luteum during pregnancy and postpartum.  Mol Reprod Dev. 2002;  63 273-281
• 134 Liu K, Olofsson J I, Wahlberg P, Ny T. Distinct expression of gelatinase A [matrix metalloproteinase (MMP)-2], collagenase-3 (MMP-13), membrane type MMP 1 (MMP-14), and tissue inhibitor of MMPs type 1 mediated by physiological signals during formation and regression of the rat corpus luteum.  Endocrinology. 1999;  140 5330-5338
• 135 Ricke W A, Smith G W, Reynolds L P, Redmer D A, Smith M F. Matrix metalloproteinase (2, 9, and 14) expression, localization, and activity in ovine copora lutea throughout the estrous cycle.  Biol Reprod. 2002;  66 1083-1094
• 136 Goldberg M J, Moses M A, Tsang P C. Identification of matrix metalloproteinases and metalloproteinase inhibitors in bovine corpora lutea and their variation during the estrous cycle.  J Anim Sci. 1996;  74 849-857
• 137 Duncan W C, McNeilly A S, Illingworth P J. The effect of luteal “rescue” on the expression and localization of matrix metalloproteinases and their tissue inhibitors in the human corpus luteum.  J Clin Endocrinol Metab. 1998;  83 2470-2478
• 138 Curry Jr T E, Song L, Wheeler S E. Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation and early luteal formation in the rat.  Biol Reprod. 2001;  65 855-865
• 139 Ricke W A, Smith G W, Smith M F. Matrix metalloproteinase expression and activity following prostaglandin F_2α induced luteolysis.  Biol Reprod. 2002;  66 685-691
• 140 Liu K, Wahlberg P, Hagglund A C, Ny T. Expression pattern and functional studies of matrix degrading proteases and their inhibitors in the mouse corpus luteum.  Mol Cell Endocrinol. 2003;  205 131-140
• 141 Smith G W, Gentry P C, Bao B, Long D K, Roberts R M, Smith M F. Control of extracellular matrix remodelling within ovarian tissues: localization and regulation of gene expression of plasminogen activator inhibitor type-1 within the ovine corpus luteum.  J Reprod Fertil. 1997;  110 107-114
• 142 O'Shea J D, Cran D G, Hay M F. The small luteal cell of the sheep.  J Anat. 1979;  128 239-251
• 143 Young K A, Hennebold J D, Stouffer R L. Dynamic expression of mRNAs and proteins for matrix metalloproteinases and their tissue inhibitors in the primate corpus luteum during the menstrual cycle.  Mol Hum Reprod. 2002;  8 833-840
• 144 Duffy D M, Stouffer R L. Luteinizing hormone acts directly at granulosa cells to stimulate periovulatory processes: modulation of luteinizing hormone effects by prostaglandins.  Endocrine. 2003;  22 249-256
• 145 Richardson M C, Slack C, Stewart I J. Rearrangement of extracellular matrix during cluster formation by human luteinising granulosa cells in culture.  J Anat. 2000;  196(pt 2) 243-248
• 146 Curry Jr T E, Song L, Wheeler S E. Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation and early luteal formation in the rat.  Biol Reprod. 2001;  65 855-865