{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T07:05:46Z","timestamp":1768287946686,"version":"3.49.0"},"reference-count":49,"publisher":"American Physiological Society","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["American Journal of Physiology-Cell Physiology"],"published-print":{"date-parts":[[2013,7,15]]},"abstract":"<jats:p> Matrix metalloproteinases (MMPs) are enzymes that regulate extracellular matrix composition and contribute to cell migration. Microarray studies in mouse placenta suggested that MMP-9 transcript abundance was dependent on distal-less 3 (Dlx3), a placental-specific transcriptional regulator; however, it was not clear if this was a direct or indirect effect. Here we investigate mechanism(s) for Dlx3-dependent MMP-9 gene transcription and gelatinase activity in placental trophoblasts. Initial studies confirmed that MMP-9 activity was reduced in placental explants from Dlx3<jats:sup>\u2212\/\u2212<\/jats:sup> mice and that murine MMP-9 promoter activity was induced by Dlx3 overexpression. Two binding sites within a murine MMP-9 promoter fragment bound Dlx3, and mutations in both elements reduced basal MMP-9-luciferase reporter activity and abolished regulation by Dlx3. Chromatin immunoprecipitation studies in JEG3 cells confirmed Dlx3 binding to the endogenous human MMP-9 promoter at three distinct sites and knockdown of human Dlx3 resulted in reduced endogenous MMP-9 transcripts and secreted activity. These studies provide novel evidence that Dlx3 is involved directly in the transcriptional regulation of mouse and human MMP-9 gene expression in placental trophoblasts. <\/jats:p>","DOI":"10.1152\/ajpcell.00205.2012","type":"journal-article","created":{"date-parts":[[2013,5,9]],"date-time":"2013-05-09T02:51:11Z","timestamp":1368067871000},"page":"C173-C181","source":"Crossref","is-referenced-by-count":4,"title":["Matrix metalloproteinase 9 is a distal-less 3 target-gene in placental trophoblast cells"],"prefix":"10.1152","volume":"305","author":[{"given":"Patricia A.","family":"Clark","sequence":"first","affiliation":[{"name":"Department of Biomedical Sciences, Cornell University, Ithaca, New York; and"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jianjun","family":"Xie","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Cornell University, Ithaca, New York; and"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sha","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Cornell University, Ithaca, New York; and"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xuesen","family":"Zhang","sequence":"additional","affiliation":[{"name":"Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, New York"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Scott","family":"Coonrod","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Cornell University, Ithaca, New York; and"},{"name":"Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, New York"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark S.","family":"Roberson","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Cornell University, Ithaca, New York; and"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"24","reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1471-4159.1995.64031312.x"},{"key":"B2","first-page":"5224","volume":"63","author":"Belotti D","year":"2003","journal-title":"Cancer Res"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1677\/joe.1.06217"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M603049200"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.103.026716"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1177\/1933719111434544"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1007\/s00109-009-0443-6"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7580.2005.00487.x"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1006\/mvre.1998.2142"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1038\/nm.1852"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1210\/en.2006-1356"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/dem303"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(17)35860-X"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(17)35859-3"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1172\/JCI113253"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2003.10.006"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.271.25.14657"},{"key":"B18","first-page":"881","volume":"10","author":"Kamochi J","year":"2003","journal-title":"Oncol Rep"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1007\/BF00219017"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1093\/embo-reports\/kve129"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.2353\/ajpath.2008.080128"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1016\/j.matbio.2009.01.001"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1084\/jem.193.7.793"},{"key":"B24","first-page":"73","volume":"42","author":"Li JK","year":"2007","journal-title":"Zhonghua Fu Chan Ke Za Zhi"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(00)00087-8"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.107.063743"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1369\/jhc.2008.952689"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2011.10.015"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-0528.1986.tb07933.x"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.1.162"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.135.6.1879"},{"key":"B32","first-page":"423","volume":"1","author":"Nakamura M","year":"2008","journal-title":"Mol Med Rep"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.108.071415"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1016\/j.clinbiochem.2008.04.015"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.274.37.26599"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1242\/dmm.008516"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-0528.1991.tb13450.x"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1016\/S0143-4004(83)80043-5"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2005.12.006"},{"key":"B40","first-page":"585","volume":"40","author":"Qiao C","year":"2005","journal-title":"Zhonghua Fu Chan Ke Za Zhi"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M007481200"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.15.7.3531"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.1038\/35080570"},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1016\/j.yexmp.2009.08.001"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1007\/s10555-007-9105-8"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deq350"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1152\/physiol.00043.2008"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1101\/gad.14.2.163"},{"key":"B49","first-page":"509","volume":"41","author":"Zhang H","year":"2006","journal-title":"Zhonghua Fu Chan Ke Za Zhi"}],"container-title":["American Journal of Physiology-Cell Physiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.physiology.org\/doi\/pdf\/10.1152\/ajpcell.00205.2012","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,17]],"date-time":"2024-06-17T16:46:09Z","timestamp":1718642769000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.physiology.org\/doi\/10.1152\/ajpcell.00205.2012"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,7,15]]},"references-count":49,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2013,7,15]]}},"alternative-id":["10.1152\/ajpcell.00205.2012"],"URL":"https:\/\/doi.org\/10.1152\/ajpcell.00205.2012","relation":{},"ISSN":["0363-6143","1522-1563"],"issn-type":[{"value":"0363-6143","type":"print"},{"value":"1522-1563","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,7,15]]}}}