{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T21:31:28Z","timestamp":1792877488901,"version":"4.5.0"},"reference-count":71,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2024,7,17]],"date-time":"2024-07-17T00:00:00Z","timestamp":1721174400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["HD057446"],"award-info":[{"award-number":["HD057446"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["HD071875"],"award-info":[{"award-number":["HD071875"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Lalor Foundation Postdoctoral Fellowship"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,10,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The migratory and matrix-invading capacities of the cumulus\u2013oocyte complex have been shown to be important for the ovulatory process. In metastatic cancers, these capacities are due to increased expression of proteases, however, there is limited information on protease expression in the cumulus\u2013oocyte complexes. The present study examined cumulus\u2013oocyte complex expression of plasmins, matrix metalloproteases, and A Disintegrin and Metalloproteinase with Thrombospondin Motifs family members in the rat and human. In the rat, human chorionic gonadotropin (hCG) administration increased cumulus\u2013oocyte complex expression of Mmp2, Mmp9, Mmp13, Mmp14, Mmp16, Adamts1, and the protease inhibitors Timp1, Timp3, and Serpine1 by 8\u201312\u00a0h. This ovulatory induction of proteases in vivo could be mimicked by forskolin and ampiregulin treatment of cultured rat cumulus\u2013oocyte complexes with increases observed in Mmp2, Mmp13, Mmp14, Mmp16, Mmp19, Plat, and the protease inhibitors Timp1, Timp3, and Serpine1. Comparison of expression between rat cumulus\u2013oocyte complexes and granulosa cells at the time of ovulation showed decreased Mmp9 and increased Mmp13, Mmp14, Mmp16, Adamts1, Timp1, and Timp3 expression in the cumulus\u2013oocyte complexes. In human, comparison of expression between cumulus and granulosa cells at the time of in vitro fertilization retrieval showed decreased MMP1, MMP2, MMP9, and ADAMTS1, while expression of MMP16, TIMP1, and TIMP3 were increased. Treatment of expanding rat cumulus\u2013oocyte complexes with a broad spectrum matrix metalloproteases inhibitor, GM6001, significantly reduced the migration of cumulus cells in vitro. These data provide evidence that multiple proteases and their inhibitors are expressed in the cumulus\u2013oocyte complex and play an important role in imparting the migratory phenotype of the cumulus\u2013oocyte complex at the time of ovulation.<\/jats:p>\n               <jats:p>Summary Sentence\u00a0<\/jats:p>\n               <jats:p>Multiple proteases and their inhibitors are induced in the cumulus\u2013oocyte complex (COC) during the periovulatory period and potentially play an important role in imparting the migratory phenotype of the COC at the time of ovulation.<\/jats:p>","DOI":"10.1093\/biolre\/ioae108","type":"journal-article","created":{"date-parts":[[2024,7,16]],"date-time":"2024-07-16T22:15:57Z","timestamp":1721168157000},"page":"845-855","source":"Crossref","is-referenced-by-count":9,"title":["Protease expression in the human and rat cumulus\u2013oocyte complex during the periovulatory period: a role in cumulus\u2013oocyte complex migration"],"prefix":"10.1093","volume":"111","author":[{"given":"Ketan","family":"Shrestha","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muraly","family":"Puttabyatappa","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle A","family":"Wynn","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick R","family":"Hannon","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linah F","family":"Al-Alem","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine L","family":"Rosewell","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James","family":"Akin","sequence":"additional","affiliation":[{"name":"Bluegrass Fertility Center , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"Jr","given":"Thomas E","family":"Curry","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology , Chandler Medical Center, , Lexington, KY ,","place":["USA"]},{"name":"University of Kentucky , Chandler Medical Center, , Lexington, KY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,7,17]]},"reference":[{"key":"2024101506314978500_ref1","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1530\/rep.0.1220829","article-title":"Oocyte control of ovarian follicular development and function in mammals","volume":"122","author":"Eppig","year":"2001","journal-title":"Reproduction"},{"key":"2024101506314978500_ref2","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1093\/humupd\/dml062","article-title":"Molecular mechanisms of ovulation: co-ordination through the cumulus complex","volume":"13","author":"Russell","year":"2007","journal-title":"Hum Reprod Update"},{"key":"2024101506314978500_ref3","doi-asserted-by":"crossref","first-page":"2253","DOI":"10.1242\/dev.00422","article-title":"Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice","volume":"130","author":"Fulop","year":"2003","journal-title":"Development"},{"key":"2024101506314978500_ref4","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1210\/mend.16.6.0859","article-title":"Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility","volume":"16","author":"Varani","year":"2002","journal-title":"Mol Endocrinol"},{"key":"2024101506314978500_ref5","doi-asserted-by":"crossref","first-page":"7693","DOI":"10.1074\/jbc.C000899200","article-title":"Defect in SHAP-hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice","volume":"276","author":"Zhuo","year":"2001","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref6","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1055\/s-2006-948551","article-title":"Extracellular matrix of the cumulus\u2013oocyte complex","volume":"24","author":"Russell","year":"2006","journal-title":"Semin Reprod Med"},{"key":"2024101506314978500_ref7","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1095\/biolreprod.111.097345","article-title":"Transient invasive migration in mouse cumulus oocyte complexes induced at ovulation by luteinizing hormone","volume":"86","author":"Akison","year":"2012","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref8","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1002\/path.4586","article-title":"Current mechanistic insights into the roles of matrix metalloproteinases in tumour invasion and metastasis","volume":"237","author":"Brown","year":"2015","journal-title":"J Pathol"},{"key":"2024101506314978500_ref9","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.biopha.2016.12.021","article-title":"Role of protease and protease inhibitors in cancer pathogenesis and treatment","volume":"86","author":"Eatemadi","year":"2017","journal-title":"Biomed Pharmacother"},{"key":"2024101506314978500_ref10","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1210\/er.2002-0005","article-title":"The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle","volume":"24","author":"Curry","year":"2003","journal-title":"Endocr Rev"},{"key":"2024101506314978500_ref11","doi-asserted-by":"crossref","first-page":"3356","DOI":"10.2741\/1487","article-title":"Plasminogen activator\/plasminogen activator inhibitors in ovarian physiology","volume":"9","author":"Liu","year":"2004","journal-title":"Front Biosci"},{"key":"2024101506314978500_ref12","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0303-7207(01)00711-0","article-title":"Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems","volume":"187","author":"Ny","year":"2002","journal-title":"Mol Cell Endocrinol"},{"key":"2024101506314978500_ref13","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.matbio.2015.03.007","article-title":"ADAMTS proteases in fertility","volume":"44-46","author":"Russell","year":"2015","journal-title":"Matrix Biol"},{"key":"2024101506314978500_ref14","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/S0303-7207(02)00054-0","article-title":"Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors","volume":"191","author":"Smith","year":"2002","journal-title":"Mol Cell Endocrinol"},{"key":"2024101506314978500_ref15","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1095\/biolreprod.111.095588","article-title":"Ovarian expression and regulation of the stromelysins during the periovulatory period in the human and the rat","volume":"86","author":"McCord","year":"2012","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref16","doi-asserted-by":"crossref","first-page":"3903","DOI":"10.1210\/en.2008-1141","article-title":"Regulation and function of tissue inhibitor of metalloproteinase (TIMP) 1 and TIMP3 in periovulatory rat granulosa cells","volume":"150","author":"Li","year":"2009","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref17","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1095\/biolreprod.113.115717","article-title":"Ovarian membrane-type matrix metalloproteinases: induction of MMP14 and MMP16 during the periovulatory period in the rat, macaque, and human","volume":"91","author":"Puttabyatappa","year":"2014","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref18","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.fertnstert.2014.11.017","article-title":"Induction of proteinases in the human preovulatory follicle of the menstrual cycle by human chorionic gonadotropin","volume":"103","author":"Rosewell","year":"2015","journal-title":"Fertil Steril"},{"key":"2024101506314978500_ref19","doi-asserted-by":"crossref","first-page":"3963","DOI":"10.1210\/en.2011-1172","article-title":"Systematic analysis of protease gene expression in the rhesus macaque ovulatory follicle: metalloproteinase involvement in follicle rupture","volume":"152","author":"Peluffo","year":"2011","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref20","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/S0015-0282(16)54430-6","article-title":"Intrabursal administration of protein kinase or proteinase inhibitors: effects on ovulation in the rat","volume":"56","author":"Guerre","year":"1991","journal-title":"Fertil Steril"},{"key":"2024101506314978500_ref21","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1210\/endo-124-1-415","article-title":"Suppression of ovulation rate by antibodies to tissue-type plasminogen activator and alpha 2-antiplasmin","volume":"124","author":"Tsafriri","year":"1989","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref22","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1095\/biolreprod.103.023911","article-title":"Adamts-1 is essential for the development and function of the urogenital system","volume":"70","author":"Mittaz","year":"2004","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref23","doi-asserted-by":"crossref","first-page":"1715","DOI":"10.1210\/endo-122-5-1715","article-title":"Inhibitors of mammalian tissue collagenase and metalloproteinases suppress ovulation in the perfused rat ovary","volume":"122","author":"Brannstrom","year":"1988","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref24","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1095\/biolreprod44.6.1183","article-title":"Inhibition of ovulation in the perfused rat ovary by the synthetic collagenase inhibitor SC 44463","volume":"44","author":"Butler","year":"1991","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref25","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1007\/s00018-010-0566-5","article-title":"The plasmin-antiplasmin system: structural and functional aspects","volume":"68","author":"Schaller","year":"2011","journal-title":"Cell Mol Life Sci"},{"key":"2024101506314978500_ref26","doi-asserted-by":"crossref","first-page":"5121","DOI":"10.1016\/S0021-9258(18)89187-6","article-title":"Plasminogen activator in the rat ovary. Production and gonadotropin regulation of the enzyme in granulosa and thecal cells","volume":"260","author":"Canipari","year":"1985","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref27","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1095\/biolreprod61.1.14","article-title":"Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation","volume":"61","author":"Chaffin","year":"1999","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref28","doi-asserted-by":"crossref","first-page":"1767","DOI":"10.1210\/en.2003-1327","article-title":"Tissue-type plasminogen activator and its inhibitor plasminogen activator inhibitor type 1 are coordinately expressed during ovulation in the rhesus monkey","volume":"145","author":"Liu","year":"2004","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref29","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.semcdb.2016.07.010","article-title":"The hidden side of SERPINB1\/leukocyte elastase inhibitor","volume":"62","author":"Torriglia","year":"2017","journal-title":"Semin Cell Dev Biol"},{"key":"2024101506314978500_ref30","first-page":"820","article-title":"Coordinated regulation of tissue type plasminogen activator and plasminogen activator inhibitor type-1 gene expression in hypophysectomized rat ovaries during GnRHa-induced ovulation","volume":"37","author":"Liu","year":"1994","journal-title":"Sci China B"},{"key":"2024101506314978500_ref31","first-page":"271","article-title":"Hormonal regulation of expression of tissue type plasminogen activator and plasminogen activator inhibitor type 1 in cultured rat granulosa cells","volume":"37","author":"Liu","year":"1994","journal-title":"Sci China B"},{"key":"2024101506314978500_ref32","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1210\/en.2016-1544","article-title":"Induction of tissue factor pathway inhibitor 2 by hCG regulates periovulatory gene expression and plasmin activity","volume":"158","author":"Puttabyatappa","year":"2017","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref33","doi-asserted-by":"crossref","first-page":"1796","DOI":"10.1095\/biolreprod.104.031823","article-title":"Regulation of matrix metalloproteinase-19 messenger RNA expression in the rat ovary","volume":"71","author":"Jo","year":"2004","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref34","doi-asserted-by":"crossref","first-page":"21491","DOI":"10.1074\/jbc.274.31.21491","article-title":"Matrix metalloproteinases","volume":"274","author":"Nagase","year":"1999","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref35","doi-asserted-by":"crossref","first-page":"31493","DOI":"10.1074\/jbc.R109.052340","article-title":"A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms","volume":"284","author":"Apte","year":"2009","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref36","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1095\/biolreprod.110.084434","article-title":"ADAMTS1 cleavage of versican mediates essential structural remodeling of the ovarian follicle and cumulus-oocyte matrix during ovulation in mice","volume":"83","author":"Brown","year":"2010","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref37","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.1095\/biolreprod.104.038083","article-title":"Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation","volume":"72","author":"Richards","year":"2005","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref38","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1530\/REP-13-0005","article-title":"Differences in the transcriptional profiles of human cumulus cells isolated from MI and MII oocytes of patients with polycystic ovary syndrome","volume":"145","author":"Huang","year":"2013","journal-title":"Reproduction"},{"key":"2024101506314978500_ref39","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1186\/gb-2011-12-11-233","article-title":"Tissue inhibitors of metalloproteinases","volume":"12","author":"Murphy","year":"2011","journal-title":"Genome Biol"},{"key":"2024101506314978500_ref40","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/S0167-4838(99)00279-4","article-title":"Tissue inhibitors of metalloproteinases: evolution, structure and function","volume":"1477","author":"Brew","year":"2000","journal-title":"Biochim Biophys Acta"},{"key":"2024101506314978500_ref41","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1080\/00016340601033741","article-title":"Collagens in the human ovary and their changes in the perifollicular stroma during ovulation","volume":"85","author":"Lind","year":"2006","journal-title":"Acta Obstet Gynecol Scand"},{"key":"2024101506314978500_ref42","doi-asserted-by":"crossref","first-page":"42330","DOI":"10.1074\/jbc.M300519200","article-title":"Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation","volume":"278","author":"Russell","year":"2003","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref43","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.mce.2010.07.019","article-title":"ADAMTS-1: a new human ovulatory gene and a cumulus marker for fertilization capacity","volume":"328","author":"Yung","year":"2010","journal-title":"Mol Cell Endocrinol"},{"key":"2024101506314978500_ref44","doi-asserted-by":"crossref","first-page":"4603","DOI":"10.1210\/en.2004-0542","article-title":"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\u2013oocyte complexes","volume":"145","author":"Shimada","year":"2004","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref45","doi-asserted-by":"crossref","first-page":"6164","DOI":"10.1210\/en.2007-0195","article-title":"Hormone-induced expression of tumor necrosis factor alpha-converting enzyme\/a disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor","volume":"148","author":"Yamashita","year":"2007","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref46","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1210\/en.2013-1655","article-title":"Protein kinase C (PKC) increases TACE\/ADAM17 enzyme activity in porcine ovarian somatic cells, which is essential for granulosa cell luteinization and oocyte maturation","volume":"155","author":"Yamashita","year":"2014","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref47","doi-asserted-by":"crossref","first-page":"6815","DOI":"10.1038\/s41598-017-07039-5","article-title":"Transcriptomic signature of the follicular somatic compartment surrounding an oocyte with high developmental competence","volume":"7","author":"Sugimura","year":"2017","journal-title":"Sci Rep"},{"key":"2024101506314978500_ref48","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1210\/endo-124-1-187","article-title":"Tissue-type plasminogen activator in rat oocytes: expression during the periovulatory period, after fertilization, and during follicular atresia","volume":"124","author":"Bicsak","year":"1989","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref49","doi-asserted-by":"crossref","first-page":"922","DOI":"10.1093\/humrep\/den466","article-title":"Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring","volume":"24","author":"Eppig","year":"2009","journal-title":"Hum Reprod"},{"key":"2024101506314978500_ref50","doi-asserted-by":"crossref","first-page":"3358","DOI":"10.1210\/en.2014-1874","article-title":"Chemokine ligand 20: a signal for leukocyte recruitment during human ovulation?","volume":"156","author":"Al-Alem","year":"2015","journal-title":"Endocrinology"},{"key":"2024101506314978500_ref51","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.1172\/JCI117578","article-title":"Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases","volume":"94","author":"Gijbels","year":"1994","journal-title":"J Clin Invest"},{"key":"2024101506314978500_ref52","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1095\/biolreprod.107.062539","article-title":"Timing of nuclear maturation and postovulatory aging in oocytes of in vitro-grown mouse follicles with or without oil overlay","volume":"78","author":"Segers","year":"2008","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref53","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1016\/j.fertnstert.2018.01.030","article-title":"Matrix metalloproteinases and their inhibitors in human cumulus and granulosa cells as biomarkers for oocyte quality estimation","volume":"109","author":"Luddi","year":"2018","journal-title":"Fertil Steril"},{"key":"2024101506314978500_ref54","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.theriogenology.2018.02.020","article-title":"Lysophosphatidic acid increases in vitro maturation efficiency via uPA-uPAR signaling pathway in cumulus cells","volume":"113","author":"Hwang","year":"2018","journal-title":"Theriogenology"},{"key":"2024101506314978500_ref55","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1007\/s00418-006-0194-1","article-title":"Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis","volume":"126","author":"Berkholtz","year":"2006","journal-title":"Histochem Cell Biol"},{"key":"2024101506314978500_ref56","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1046\/j.1432-0436.1998.6330125.x","article-title":"Differential distribution of type IV collagen chains in the developing rat testis and ovary","volume":"63","author":"Frojdman","year":"1998","journal-title":"Differentiation"},{"key":"2024101506314978500_ref57","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1093\/molehr\/5.7.607","article-title":"Human granulosa cells express integrin alpha2 and collagen type IV: possible involvement of collagen type IV in granulosa cell luteinization","volume":"5","author":"Yamada","year":"1999","journal-title":"Mol Hum Reprod"},{"key":"2024101506314978500_ref58","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1083\/jcb.200408028","article-title":"Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP","volume":"167","author":"Sabeh","year":"2004","journal-title":"J Cell Biol"},{"key":"2024101506314978500_ref59","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1095\/biolreprod.103.023499","article-title":"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","volume":"70","author":"Jo","year":"2004","journal-title":"Biol Reprod"},{"key":"2024101506314978500_ref60","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0070-2153(03)54004-2","article-title":"Membrane type-matrix metalloproteinases (MT-MMP)","volume":"54","author":"Zucker","year":"2003","journal-title":"Curr Top Dev Biol"},{"key":"2024101506314978500_ref61","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1262\/jrd.2015-177","article-title":"Developmental consequences of supplementing with matrix metallopeptidase-9 during in vitro maturation of heat-stressed bovine oocytes","volume":"62","author":"Goodwin","year":"2016","journal-title":"J Reprod Dev"},{"key":"2024101506314978500_ref62","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1006\/cbir.2001.0759","article-title":"Effect of hyaluronan on MMP expression and activation","volume":"25","author":"Isnard","year":"2001","journal-title":"Cell Biol Int"},{"key":"2024101506314978500_ref63","first-page":"3962","article-title":"Hyaluronan-CD44s signaling regulates matrix metalloproteinase-2 secretion in a human lung carcinoma cell line QG90","volume":"62","author":"Zhang","year":"2002","journal-title":"Cancer Res"},{"key":"2024101506314978500_ref64","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1093\/molehr\/5.1.22","article-title":"Expression of CD44 in human cumulus and mural granulosa cells of individual patients in in-vitro fertilization programmes","volume":"5","author":"Ohta","year":"1999","journal-title":"Mol Hum Reprod"},{"key":"2024101506314978500_ref65","doi-asserted-by":"crossref","first-page":"48679","DOI":"10.1074\/jbc.M106759200","article-title":"Hyaluronan promotes CD44v3-Vav2 interaction with Grb2-p185(HER2) and induces Rac1 and Ras signaling during ovarian tumor cell migration and growth","volume":"276","author":"Bourguignon","year":"2001","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref66","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1055\/s-0028-1108010","article-title":"Epidermal growth factor-like growth factors in the follicular fluid: role in oocyte development and maturation","volume":"27","author":"Hsieh","year":"2009","journal-title":"Semin Reprod Med"},{"key":"2024101506314978500_ref67","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1042\/BJ20150758","article-title":"Antibody-based exosite inhibitors of ADAMTS-5 (aggrecanase-2)","volume":"471","author":"Santamaria","year":"2015","journal-title":"Biochem J"},{"key":"2024101506314978500_ref68","doi-asserted-by":"crossref","first-page":"786","DOI":"10.1038\/nrm3904","article-title":"Remodelling the extracellular matrix in development and disease","volume":"15","author":"Bonnans","year":"2014","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2024101506314978500_ref69","doi-asserted-by":"crossref","first-page":"10814","DOI":"10.1074\/jbc.M606991200","article-title":"Formation of hyaluronan- and versican-rich pericellular matrix by prostate cancer cells promotes cell motility","volume":"282","author":"Ricciardelli","year":"2007","journal-title":"J Biol Chem"},{"key":"2024101506314978500_ref70","doi-asserted-by":"crossref","first-page":"3075","DOI":"10.1016\/j.ajpath.2011.08.021","article-title":"The ADAMTS1 protease gene is required for mammary tumor growth and metastasis","volume":"179","author":"Ricciardelli","year":"2011","journal-title":"Am J Pathol"},{"key":"2024101506314978500_ref71","first-page":"1553","article-title":"ADAMTS1 promotes adhesion to extracellular matrix proteins and predicts prognosis in early stage breast cancer patients","volume":"52","author":"Tan","year":"2019","journal-title":"Cell Physiol Biochem"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioae108\/58660609\/ioae108.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/111\/4\/845\/59742811\/ioae108.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/111\/4\/845\/59742811\/ioae108.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,15]],"date-time":"2024-10-15T06:32:22Z","timestamp":1728973942000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/111\/4\/845\/7715931"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,17]]},"references-count":71,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,7,17]]},"published-print":{"date-parts":[[2024,10,14]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioae108","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,10]]},"published":{"date-parts":[[2024,7,17]]}}}