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Research Article

Proteolytic Mechanisms in the Ovulatory Folliculo-Luteal Transformation

William J. Murdoch Department of Animal Science and Reproductive Biology Program, University of Wyoming, Laramie, Wyoming, USA
&
Michelle L. Gottsch Department of Animal Science and Reproductive Biology Program, University of Wyoming, Laramie, Wyoming, USA
Pages 50-57 | Published online: 06 Aug 2009

  • McGee, E.A., and Hsueh, A.J.W. (2000). Initial and cyclic recruitment of ovarian follicles. Endo. Rev. 21:200-214.
  • Niswender, G.D., Juengel, J.L., Silva, P.J., Rollyson, M.K., and McIntush, E.W. (2000). Mechanisms controlling the function and life span of the corpus luteum. Physiol. Rev. 80:1-29.
  • Luck, M.R. (1994). The gonadal extracellular matrix. Oxf. Rev. Reprod. Biol. 16:34-85.
  • Eyre, D.R., Paz, M.A., and Gallop, P.M. (1984). Cross-linking in collagen and elastin. Ann. Rev. Biochem. 53:717-748.
  • Kühn, K. (1994). Basement membrane (type IV) collagen. Matrix Biol. 14:439-445.
  • Murdoch, W.J. (2000). Proteolytic and cellular death mechanisms in ovulatory ovarian rupture. Biol. Signals Recept. 9:102-114.
  • Andreasen, P.A., Egelund, R., and Petersen, H.H. (2000). The plasminogen activation system in tumor growth, invasion, and metastasis. Cell. MoI. Life Sct. 57:25-40.
  • Nagase, H., and Woessner, J.F., Jr. (1999). Matrix metalloproteinases. J. Biol. Chem. 274:21491-21494.
  • Roberts, A.J., Dunn, T.G., and Murdoch, W.J. (1985). Induction of ovulation in proestrous ewes: Identification of the ovulatory follicle and functional status of the corpus luteum. Domest. Anim. Endocrinol. 2: 207-210.
  • Murdoch, W.J. (1985). Follicular determinants of ovulation in the ewe. Domest. Anim. Endocrinol. 2:105-121.
  • Richards, J.S., Russell, D.L., Robker, R.L., Dajee, M., and Alliston, T.N. (1998). Molecular mechanisms of ovulation and luteinization. MoI. Cell Endocrinol. 145:47-54.
  • Murdoch, J., Van Kirk, E.A., and Murdoch, W.J. (1999). Hormonal control of urokinase plasminogen activator secretion by sheep ovarian surface epithelial cells. Biol. Reprod. 61:1487-1491.
  • Halterman, S.D., and Murdoch, W.J. (1986). Ovarian function in ewes treated with antihistamines. Endocrinology 119:2417-2421.
  • Cavender, J.L., and Murdoch, W.J. (1988). Morphological studies of the microcirculatory system of periovulatory ovine follicles. Biol. Reprod. 39:989-997.
  • Colgin, D.C., and Murdoch, W.J. (1997). 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. 47:197-204.
  • Murdoch, W.J. (1998). Regulation of collagenolysis and cell death by plasmin within the formative stigma of preovulatory ovine follicles. J. Reprod. Fertil. 113:331-336.
  • Smokovitis, A., Kokolis, N., and Alexaki-Tzivanidou, E. (1988). The plasminogen activator activity is markedly increased mainly at the area of the rupture of the follicular wall at the time of ovulation. Anim. Reprod. Sci. 16:285-294.
  • Peng, X.R., Hsueh, A.J.W., and Ny, T. (1993). Transient and cell-specific expression of tissue-type plasminogen activator and plasminogen-activator-inhibitor type 1 results in controlled and directed proteolysis during gonadotropin-induced ovulation. Eur. J. Biochem. 214: 147-156.
  • Tsafriri, A., and Reich, R. (1991). Plasminogen activators in the preovulatory follicle: Role in ovulation. In Plasminogen Activators: From Cloning to Therapy, R. Abbate, T. Barni, and A. Tsafriri (eds.), pp. 81-93. (Raven Press, New York).
  • Carmeliet, P., Schoonjans, L., Kieckens, L., Ream, B., Degen, J., Bronson, R., De Vos, R., van den Oord, J.J., Collen, D., and Mulligan, R.C. (1994). Physiological consequences of loss of plasminogen activator function in mice. Nature 368:419-424.
  • Leonardsson, G., Peng, X.R., Liu, K., Nordström, L., Carmeliet, P., Mulligan, R., Collen, D., and Ny, T. (1995). Ovulation efficiency is reduced in mice that lack plasminogen activator gene function: Functional redundancy among physiological plasminogen activators. Proc. Natl. Acad. Sci. USA 92:12446-12450.
  • Hägglund, A.C., Ny, A., Liu, K., and Ny, T. (1996). Coordinated and cell-specific induction of both physiological plasminogen activators creates functionally redundant mechanisms for plasmin formation during ovulation. Endocrinology 137:5671-5677.
  • Curry, T.E., Jr., and Osteen, K.G. (2001). Cyclic changes in the matrix metalloproteinase system in the ovary and uterus. Biol. Reprod. 64:1285-1296.
  • Murdoch, W.J., Peterson, T.A., Van Kirk, E.A., Vincent, D.L., and Inskeep, E.K. (1986). Interactive roles of progesterone, prostaglandins and collagenase in the ovulatory mechanism of the ewe. Biol. Reprod. 35:1187-1194.
  • Murdoch, W.J., and McCormick, R.J. (1992). Enhanced degradation of collagen in apical vs. basal wall of ovulatory ovine follicle.Am. J. Physiol. 263:E221-225.
  • Fukumoto, M., Yajima, Y., Okamura, H., and Midorikawa, O. (1981). Collagenolytic enzyme activity in human ovary: An ovulatory enzyme system. Fertil. Steril. 36:746-750.
  • Bjersing, L., and Cajander, S. (1975). Ovulation and the role of the ovarian surface epithelium. Experentia 31:605-608.
  • Talbot, P., Martin, G.G., and Ashby, H. (1987). Formation of the rupture site in preovulatory hamster and mouse follicles: Loss of surface epithelium. Gamete Res. 17:287-302.
  • Reich, R., Daphna-Ilken, D., Chun, S.Y., Popliker, M., Slager, R., Adelmann-Grill, B.C., and Tsafriri, A. (1991). Preovulatory changes in ovarian expression of collagenases and tissue metalloproteinase inhibitor messenger ribonucleic acid: Role of eicosanoids. Endocrinology 129:1869-1875.
  • Tadakuma, H., Okamura, H., Kitaoka, M., Iyama, K., and Usuku, G. (1993). Association of immunolocalization of matrix metalloproteinase 1 with ovulation in hCG-treated rabbit ovary. J. Reprod. Fertil. 98:503-508.
  • Ichikawa, S., Ohta, M., Morioka, H., and Murao, S. (1983). Blockage of ovulation in the explanted hamster ovary by a collagenase inhibitor. J. Reprod. Fertil. 68:17-19.
  • Reich, R., Tsafriri, A., and Mechanic, G.L. (1985). The involvement of collagenolysis in ovulation in the rat. Endocrinology 116:522-527.
  • Brännström, M., Woessner, J.F., Jr., Koos, R.D., Sear, C.H., and LeMaire, W.J. (1988). Inhibitors of mammalian tissue collagenase and metalloproteinases suppress ovulation in the perfused rat ovary. Endocrinology 122:1715-1721.
  • Butler, T.A., Zhu, C., Mueller, R.A., Fuller, G.C., LeMaire, W.J., and Woessner, J.F., Jr. (1991). Inhibition of ovulation in the perfused rat ovary by the synthetic collagenase inhibitor SC 44463. Biol. Reprod. 44:1183-1188.
  • Liu, X., Wu, H., Byrne, M., Jeffrey, J., Krane, S., and Jaenisch, R. (1995). A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodelling. J. Cell Biol. 130:227-237.
  • Vilcek, J., and Lee, T.H. (1991). Tumor necrosis factor. J. Biol. Chem. 266:7313-7316.
  • Vandenabeele, P., Declercq, W., Beyaert, R., and Fiers, W. (1995). Two tumour necrosis factor receptors: Structure and function. Trends Cell Biol. 5:392-399.
  • Terranova, P.F. (1997). Potential roles of tumor necrosis factor-a in follicular development, ovulation, and the life span of the corpus luteum. Domest. Anim. Endocrinol. 14:1-15.
  • Bazzoni, F., and Beutler, B. (1995). How do tumor necrosis factor receptors work. J. Inflam. 45:221-238.
  • Baker, T., and Reddy, E. (1996). Transducers of life and death: TNF receptor superfamily and associated proteins. Oncogene 12:1-9.
  • Zhivotovsky, B., Burgess, D.H., and Orrenius, S. (1996). Proteases and apoptosis. Experentia 52:968-978.
  • Alnemri, E.S. (1997). Mammalian cell death proteases: A family of highly conserved asperate specific cysteine proteases. J. Cell Biochem. 64:33-42.
  • Warzocha, K., and Salles, G. (1998). The tumor necrosis factor signaling complex: Choosing pathway toward cell death or cell proliferation. Leak Lymph. 29:81-92.
  • Larrick, J.W., and Wright, S.C. (1990). Cytotoxic mechanism of tumor necrosis factor-a. FASEB J. 4:3215-3223.
  • Murdoch, W.J., Colgin, D.C., and Ellis, J.A. (1997). Role of tumor necrosis factor-a in the ovulatory mechanism of ewes. J. Anim. Sci. 75:1601-1605.
  • Murdoch, W.J., Van Kirk, E.A., and Murdoch, J. (1999). Plasmin cleaves tumor necrosis factor a exodomain from sheep follicular endothelium: Implication in the ovulatory process. Biol. Reprod. 60:1166-1171.
  • Zolti, M., Meirom, R., Shemesh, M., Wollach, D., Mashiach, S., Shore, L., and Ben-Rafael, Z. (1990). Granulosa cells as a source and target organ for tumor necrosis factor-a. FEBS Lett. 261:253-255.
  • Brännström, M., Norman, R.J., Seamark, R.F., and Robertson, S.A. (1994). Rat ovary produces cytokines during ovulation. Biol. Reprod. 50:88-94.
  • deMola, J.R.L., Goldfarb, J.M., Hecht, B.R., Baumgardner, G.P., Babbo, C.J., and Friedlander, M.A. (1998). Gonadotropins induce the release of interleukin-1ß, interleukin-6 and tumor necrosis factor-a from the human preovulatory follicle. Am. J. Reprod. Immunol. 39:387-390.
  • Montgomery-Rice, V., Limback, S.D., Roby, K.F., and Terranova, P.F. (1998). Changes in circulating and ovarian concentrations of bioactive tumour necrosis factor a during the first ovulation at puberty in rats and in gonadotrophin-treated immature rats. J. Reprod. Fertil. 113: 337-341.
  • Black, R.A., Rauch, C.T., Kozlosky, C.J., Peschon, J.J., Slack, J.L., Wolfson, M.F., Castner, B.J., Stocking, K.L., Reddy, P., Srinivasan, S., Nelson, N., Boiani, N., Schooley, K.A., Gerhart, M., Davis, R., Fitzner, J.N., Johnson, R.S., Paxton, R.J., March, C.J., and Cerretti, O.P. (1997). A metalloproteinase disintegrin that releases tumour necrosis factor-a from cells. Nature 385:729-733.
  • Johnson, M.L., Murdoch, J., Van Kirk, E.A., Kaltenbach, J.E., and Murdoch, W.J. (1999). Tumor necrosis factor a regulates collagenolytic activity in preovulatory ovine follicles: Relationship to cytokine secretion by the oocyte-cumulus cell complex. Biol. Reprod. 61:1581-1585.
  • Gottsch, M.L., Van Kirk, E.A., and Murdoch, W.J. (2000). Tumour necrosis factor a upregulates matrix metalloproteinase-2 activity in periovulatory ovine follicles: Metamorphic and endocrine implications. Reprod. Fertil. Dev. 12:75-80.
  • Murdoch, W.J. (1994). Ovarian surface epithelium during ovulatory and anovulatory ovine estrous cycles. Anat. Rec. 240:322-326.
  • Murdoch, W.J. (1995). Programmed cell death in preovulatory ovine follicles. Biol. Reprod. 53:8-12.
  • Murdoch, W.J. (1995). Endothelial cell death in preovulatory ovine follicles: Possible implication in the biomechanics of rupture. J. Reprod. Fertil. 105:161-164.
  • Murdoch, W.J., Wilken, C., and Young, D.A. (1999). Sequence of apoptosis and inflammatory necrosis within the formative ovulatory site of sheep follicles. J. Reprod. Fertil. 117:325-329.
  • Brännström, M., Bonello, N., Wang, L.J., and Norman, R.J. (1995). Effects of tumour necrosis factor a (TNFa) on ovulation in the rat ovary. Reprod. Fertil. Dev. 7:67-73.
  • Roby, K.F., Son, D-S., and Terranova, P.F. (1999). Alterations of events related to ovarian function in tumor necrosis factor receptor type I knockout mice. Biol. Reprod. 61:1616-1621.
  • Murdoch, W.J., Hansen, T.R., and McPherson, L.A. (1993). Role of eicosanoids in vertebrate ovulation. Prostaglandins 46:85-115.
  • Espey, L.L. (1994). Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol. Reprod. 50:233-238.
  • Murdoch, W.J., and Lund, S.A. (1999). Prostaglandin-independent anovulatory mechanism of indomethacin action: Inhibition of tumor necrosis factor a-induced sheep ovarian cell apoptosis. Biol. Reprod. 61:1655-1659.
  • Smith, M.F., McIntush, E.W., and Smith, G.W. (1994). Mechanisms associated with corpus luteum development. J. Anim. Sci. 72:1857-1872.
  • Smith, M.F., McIntush, E.W., Ricke, W.A., Kojima, F.N., and Smith, G.W. (1999). Regulation of ovarian matrix remodelling by metalloproteinases and their tissue inhibitors: Effects on follicular development, ovulation and luteal function. J. Reprod. Fertil. Suppl. 54:367-381.
  • Puistola, U., SaIo, T., Martikainen, H., and Ronnberg, L. (1986). Type IV collagenolytic activity in human preovulatory follicular fluid. Ferttl. Steril. 45:578-580.
  • Curry, T.E., Jr., Mann, J.S., Huang, M.H., and Keeble, S.C. (1992). Gelatinase and proteoglycanase activity during the periovulatory period in the rat. Biol. Reprod. 46:256-264.
  • Bagavandoss, P. (1998). Differential distribution of gelatinases and tissue inhibitor of metalloproteinase-1 in the rat ovary. J. Endocrinol. 158:221-228.
  • Liu, K., Wahlberg, P., and Ny, T. (1998). Coordinated and cell-specific regulation of membrane type matrix metalloproteinase 1 (MTl-MMP) and its substrate matrix metalloproteinase 2 (MMP-2) by physiological signals during follicular development and ovulation. Endocrinology 139:4735-4738.
  • Liu, K., Olofsson, J.I., Wahlberg, P., and Ny, T. (1999). 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 140:5330-5338.
  • Chaffin, C.L., and Stouffer, R.L. (1999). Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: Time course and steroid regulation. Biol. Reprod. 61:14-21.
  • Pitzel, L., Lüdemann, S., and Wuttke, W. (2000). Secretion and gene expression of metalloproteinases and gene expression of their inhibitors in porcine corpora lutea at different stages of the luteal phase. Biol. Reprod. 62:1121-1127.
  • Corcoran, M.L., Hewitt, R.E., Kleiner, D.E., and Stetler-Stevenson, W.G. (1996). MMP-2: Expression, activation and inhibition. Enz. Prot. 49: 7-19.
  • Matrisian, L.M. (1996). Matrix metalloproteinase gene expression. Ann. NY Acad. Sci. 732:42-50.
  • Gotlieb, W.H., Watson, J.M., and Rezai, B.A. (1994). Cytokine-induced modulation of tumor suppressor gene expression in ovarian cancer cells: Up-regulation of p53 gene expression and induction of apoptosis by tumor necrosis factor-a. Am. J. Obstet. Gynecol. 170:1121-1130.
  • Yeung, M.C., and Lau, A.S. (1998). Tumor suppressor p53 as a component of the tumor necrosis factor-induced, protein kinase PKR-mediated apoptotic pathway in human promonocytic U937 cells. J. Biol. Chem. 273:25198-25202.
  • Rokhlin, O.W., Gudkov, A.V., Kwek, S., Glover, R.A., Gewies, A.S., and Cohen, M.B. (2000). p53 is involved in tumor necrosis factor a-induced apoptosis in the human prostatic carcinoma cell line LNCaP. Oncogene 19:1959-1968.
  • Bian, J., and Sun, Y. (1997). Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase-2) promoter. MoI. Cell Biol. 17:6330-6338.
  • Bortolussi, M., Zanchetta, R., Doliana, R., Castellani, I., Bressan, G.M., and Lauria, A. (1989). Changes in the organization of the extracellular matrix in ovarian follicles during the preovulatory phase and atresia. Basic Appl. Histochem. 33:31-38.
  • Matsushima, T, Fukuda, Y., Tsukada, K., and Yamanaka, N. (1996). The extracellular matrices and vascularization of the developing corpus luteum in rats. J. Submicrosc. Cytol. Pathol. 28:441-445.
  • Silvester, L.M., and Luck, M.R. (1999). Distribution of extracellular matrix components in the developing ruminant corpus luteum: A wound repair hypothesis. J. Reprod. Ferttl. 116:187-198.
  • Fata, J.E., Ho, A.T.V., Leco, K.J., Moorehead, R.A., and Khokha, R. (2000). Cellular turnover and extracellular matrix remodeling in female reproductive tissues: Functions of metalloproteinases and their inhibitors. Cell MoI. Life Sci. 57:77-95.
  • Jablonka-Shariff, A., Grazul-Bilska, A.T., Redmer, D.A., and Reynolds, L.P. (1993). Growth and cellular proliferation of ovine corpora lutea throughout the estrous cycle. Endocrinology 133:1871-1879.
  • Sang, Q.X.A. (1998). Complex role of matrix metalloproteinases in angiogenesis. Cell Res. 8:171-177.
  • Hass, T.L., and Madri, J.A. (1999). Extracellular matrix-driven matrix metalloproteinase production in endothelial cells: Implications for angiogenesis. Trends Cardiovasc. Med. 9:70-77.
  • Sato, H., and Seiki, M. (1996). Membrane-type matrix metalloproteinases (MT-MMPs) in tumor metastasis. J. Biochem. 119:209-215.
  • Stack, M.S., Ellerbroek, S.M., and Fishman, D.A. (1998). The role of proteolytic enzymes in the pathology of epithelial ovarian carcinoma. Int. J. Oncol. 12:569-576.
  • Nelson, A.R., Fingleton, B., Rothenberg, M.L., and Matrisian, L.M. (2000). Matrix metalloproteinases: Biologic activity and clinical implications. J. Clin. Oncol. 18:1135-1149.
  • Woessner, J.F., Jr. (1991). Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5:2145-2154.
  • Birkedal-Hansen, H. (1995). Proteolytic remodeling of extracellular matrix. Curr. Opin. Cell Biol. 7:728-735.
  • Borkakoti, N. (1998). Matrix metalloproteinases: Variations on a theme. Prog. Biophys. MoI. Biol. 70:73-94.
  • Liu, K., Brandstom, A., Liu, X.X., Ny, T., and Selstam, G. (1996). Coordinated expression of tissue-type plasminogen activator and plasminogen activator inhibitor type 1 during corpus luteum formation and luteolysis in the adult pseudopregnant rat. Endocrinology 137:2126-2132.
  • Morgunova, E., Tuuttila, A., Bergmann, U., Isupov, M., Lindqvist, Y., Schneider, G., and Tryggvason, K. (1999). Structure of human pro-matrix metalloproteinase-2: Activation mechanism revealed. Science 284:1667-1670.
  • Gottsch, M.L., Van Kirk, E.A., and Murdoch, W.J. (2002). Role of matrix metalloproteinase-2 in the ovulatory folliculo-luteal transition of ewes. Reproduction 124:347-352.
  • Russell, D.L., Salamonsen, L.A., and Findlay, J.K. (1995). Immunization against the N-terminal peptide of the inhibin a43-subunit (a N) disrupts tissue remodeling and the increase in matrix metalloproteinase-2 during ovulation. Endocrinology 136:3657-3664.
  • Driancourt, M.A., Quesnel, H., Meduri, G., Prunier, A., and Hermier, D. (1998). Luteinization and proteolysis in ovarian follicles of Meishan and Large White gilts during the preovulatory period. J. Reprod. Ferttl. 114:287-297.
  • Riley, S.C., Gibson, A.H., Leask, R., Mauchline, D.J.W., Pedersen, H.G., and Watson, E.D. (2001). Secretion of matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases into follicular fluid during follicle development in equine ovaries. Reproduction 121:553-560.
  • Nothnick, W.B., Keeble, S.C., and Curry, T.E., Jr. (1996). Collagenase, gelatinase, and proteoglycanase messenger ribonucleic acid expression and activity during luteal development, maintenance, and regression in the pseudopregnant rat ovary. Biol. Reprod. 54:616-624.
  • Goldberg, M.J., Moses, M.A., and Tsang, P.C. (1996). Identification of matrix metalloproteinases and metalloproteinase inhibitors in bovine corpora lutea and their variation during the estrous cycle. J. AnIm. Sci. 74:849-857.
  • Zhao, Y., and Luck, M.R. (1996). Bovine granulöse cells express extracellular matrix proteins and their regulators during luteinization in culture. Reprod. Fertil. Dev. 8:259-266.
  • Duncan, W.C., McNeilly, A.S., and Illingworth, P.J. (1998). The effect of luteal "rescue" on the expression and localization of matrix metalloproteinases and their inhibitors in the human corpus luteum. J. Clin. Endocrinol. Metab. 83:2470-2478.
  • Baibin, M., Fueyo, A., Lopez, J.M., Diez-Itza, I., Velasco, G., and Lopez-Otin, C. (1996). Expression of collagenase-3 in the rat ovary during the ovulatory process. J. Endocrinol. 149:405-415.
  • Komar, C.M., Matousek, M., Mitsube, K., Mikuni, M., Brânnstrom, M., and Curry, T.E., Jr. (2001). Effects of genistein on the periovulatory expression of messenger ribonucleic acid for matrix metalloproteinases and tissue inhibitors of metalloproteinases in the rat ovary. Reproduction 121:259-265.
  • Robker, R.L., Russell, D.L., Yoshioka, S., Sharma, S.C., Lyndon, J.P., O'Malley, B.W., Espey, L.L., and Richards, J.S. (2000). Ovulation: A multi-gene, multi-step process. Steroids 65:559-570.
  • Endo, H.H.T., Nagasawa, K., Hayashi, T., Chida, M., Akutagawa, N., Iwasaki, M., Kitajima, Y., Kiya, T., Nishikawa, A., Manase, K., and Kudo, R. (2001). Lysyl oxidase and MMP-2 expression in dehydroepiandrosterone-induced polycystic ovary in rats. Biol. Reprod. 64:157-162.
  • Boujrad, N., Ogwuegbu, S.O., Gamier, M., Lee, C.H., Martin, B.M., and Papadopoulos, V. (1995). Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 286:1609-1612.

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