{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,10]],"date-time":"2026-04-10T06:30:57Z","timestamp":1775802657454,"version":"3.50.1"},"reference-count":52,"publisher":"Archives of Pathology and Laboratory Medicine","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2014,5]]},"abstract":"<jats:p>Context.\u2014The ability of intermediate trophoblasts to invade maternal tissue during placentation depends on how well they can degrade the extracellular matrix. Invasion into the extracellular matrix requires many complex proteases. A disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) is a novel family of secreted metalloproteinases. The ADAMTS-1, -4, -5, and -14 subtypes are known to be expressed in human placenta, but little is understood about their expression patterns.<\/jats:p>\n                  <jats:p>Objective.\u2014To examine the expression patterns of ADAMTS-1, -4, -5, and -14 in specific human placenta cell types during gestation and in gestational trophoblastic diseases.<\/jats:p>\n                  <jats:p>Design.\u2014Placental tissues were obtained from 25 pregnant women and 21 cases of gestational trophoblastic diseases (10 early complete moles, 3 placental site trophoblastic tumors, 4 invasive moles, and 4 choriocarcinomas). The expression of the 4 ADAMTS was analyzed by immunohistochemistry.<\/jats:p>\n                  <jats:p>Results.\u2014ADAMTS-1, -4, -5, and -14 were differentially expressed by the human placenta throughout gestation in a time-specific and cell type\u2013specific manner, as well as in gestational trophoblastic diseases. ADAMTS-1 showed gradually strong staining intensity in gestational trophoblastic diseases according to the invasive potential but showed consistent strong intensity throughout normal placenta. ADAMTS-4 and ADAMTS-5 exhibited higher and restricted expression in first-trimester intermediate trophoblasts. They also exhibited comparably strong expression in gestational trophoblastic diseases. However, ADAMTS-14 expression remained unchanged throughout gestation.<\/jats:p>\n                  <jats:p>Conclusions.\u2014The restricted expression pattern of ADAMTS-4 and ADAMTS-5 and their increased expression in gestational trophoblastic diseases suggest that these 2 ADAMTS subtypes are associated with a biological phenotype of trophoblasts involved in human placentation and the development of gestational trophoblastic diseases.<\/jats:p>","DOI":"10.5858\/arpa.2012-0227-oa","type":"journal-article","created":{"date-parts":[[2014,4,30]],"date-time":"2014-04-30T17:04:23Z","timestamp":1398877463000},"page":"643-650","source":"Crossref","is-referenced-by-count":27,"title":["Differential Expression Patterns of a Disintegrin and Metalloproteinase With Thrombospondin Motifs (ADAMTS) -1, -4, -5, and -14 in Human Placenta and Gestational Trophoblastic Diseases"],"prefix":"10.5858","volume":"138","author":[{"given":"So-Young","family":"Lee","sequence":"first","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hyang-Sin","family":"Lee","sequence":"additional","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Minchan","family":"Gil","sequence":"additional","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chong Jai","family":"Kim","sequence":"additional","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yong-Hee","family":"Lee","sequence":"additional","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kyu-Rae","family":"Kim","sequence":"additional","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chan-Sik","family":"Park","sequence":"additional","affiliation":[{"name":"From the Department of Pathology, Asan Medical Center (Drs S-Y. Lee, C. J. Kim, K-R. Kim, and C-S. Park), and Asan Institute for Life Science (Ms H-S. Lee and Dr Gil), University of Ulsan, College of Medicine, Seoul, and Department of Pathology, University of Ajou, College of Medicine, Ajou University Hospital, Su-won (Dr Y-H. Lee), Korea."}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"3906","reference":[{"issue":"12","key":"i1543-2165-138-5-643-b01","series-title":"Chin Sci Bull","first-page":"1169","article-title":"Matrix metalloproteinases and trophoblast invasion","volume":"50","author":"Li\n              J,","year":"2005","unstructured":"Li\n              J, \n            \n              Zhao\n              T, \n            \n              Duan\n              E. \n          \n          Matrix metalloproteinases and trophoblast invasion. Chin Sci Bull. 2005;50(12):1169\u20131173."},{"issue":"pt 4","key":"i1543-2165-138-5-643-b02","series-title":"J Cell Sci","first-page":"681","article-title":"Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro","volume":"99","author":"Aplin\n              JD.","year":"1991","unstructured":"Aplin\n              JD. \n          \n          Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. 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Philadelphia, PA: Saunders;2007."},{"issue":"4","key":"i1543-2165-138-5-643-b05","series-title":"PLoS One","article-title":"Regulated expression of ADAMTS-12 in human trophoblastic cells: a role for ADAMTS-12 in epithelial cell invasion","volume":"6","author":"Beristain\n              AG,","year":"2011","unstructured":"Beristain\n              AG, \n            \n              Zhu\n              H, \n            \n              Leung\n              PC. \n          \n          Regulated expression of ADAMTS-12 in human trophoblastic cells: a role for ADAMTS-12 in epithelial cell invasion? PLoS One. 2011;6(4):e18473.http:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC3073978\/. Accessed June 24, 2013."},{"issue":"2","key":"i1543-2165-138-5-643-b06","series-title":"Am J Reprod Immunol","first-page":"96","article-title":"Type 2 cadherins in the human endometrium and placenta: the putative roles in human implantation and placentation","volume":"39","author":"MacCalman\n              CD,","year":"1998","unstructured":"MacCalman\n              CD, \n            \n              Getsios\n              S, \n            \n              Chen\n              GT. \n          \n          Type 2 cadherins in the human endometrium and placenta: the putative roles in human implantation and placentation. Am J Reprod Immunol. 1998;39(2):96\u2013107."},{"issue":"8","key":"i1543-2165-138-5-643-b07","series-title":"Placenta","first-page":"783","article-title":"Metalloproteinases and human placental invasiveness","volume":"27","author":"Cohen\n              M,","year":"2006","unstructured":"Cohen\n              M, \n            \n              Meisser\n              A, \n            \n              Bischof\n              P. \n          \n          Metalloproteinases and human placental invasiveness. 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Human Reprod. 2006;21(8):1990\u20131999."},{"issue":"10","key":"i1543-2165-138-5-643-b09","series-title":"J Clin Invest","first-page":"1345","article-title":"ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function","volume":"105","author":"Shindo\n              T,","year":"2000","unstructured":"Shindo\n              T, \n            \n              Kurihara\n              H, \n            \n              Kuno\n              K, \n            et al\n          . ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest. 2000;105(10):1345\u20131352."},{"issue":"33","key":"i1543-2165-138-5-643-b10","series-title":"J Biol Chem","first-page":"23349","article-title":"METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity","volume":"274","author":"Vazquez\n              F,","year":"1999","unstructured":"Vazquez\n              F, \n            \n              Hastings\n              G, \n            \n              Ortega\n              MA, \n            et al\n          . METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity. J Biol Chem. 1999;274(33):23349\u201323357."},{"issue":"pt 1","key":"i1543-2165-138-5-643-b11","series-title":"Biochem J","first-page":"15","article-title":"The ADAMTS metalloproteinases","volume":"386","author":"Porter\n              S,","year":"2005","unstructured":"Porter\n              S, \n            \n              Clark\n              IM, \n            \n              Kevorkian\n              L, \n            \n              Edwards\n              DR. \n          \n          The ADAMTS metalloproteinases. Biochem J. 2005;386(pt 1):15\u201327."},{"issue":"6","key":"i1543-2165-138-5-643-b12","series-title":"Int J Biochem Cell Biol","first-page":"981","article-title":"A disintegrin-like and metalloproteinase (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family","volume":"36","author":"Apte\n              SS.","year":"2004","unstructured":"Apte\n              SS. \n          \n          A disintegrin-like and metalloproteinase (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family. Int J Biochem Cell Biol. 2004;36(6):981\u2013985."},{"issue":"33","key":"i1543-2165-138-5-643-b13","series-title":"J Biol Chem","first-page":"23443","article-title":"Cloning and characterization of ADAMTS11, an aggrecanase from the ADAMTS family","volume":"274","author":"Abbazade\n              I,","year":"1999","unstructured":"Abbazade\n              I, \n            \n              Liu\n              RQ, \n            \n              Yang\n              F, \n            et al\n          . Cloning and characterization of ADAMTS11, an aggrecanase from the ADAMTS family. J Biol Chem. 1999;274(33):23443\u201323450."},{"issue":"1","key":"i1543-2165-138-5-643-b14","series-title":"Hum Reprod","first-page":"63","article-title":"Expression of ADAMTS-5\/implantin in human decidual stromal cells: regulatory effects of cytokines","volume":"22","author":"Zhu\n              H,","year":"2007","unstructured":"Zhu\n              H, \n            \n              Leung\n              PC, \n            \n              MacCalman\n              CD. \n          \n          Expression of ADAMTS-5\/implantin in human decidual stromal cells: regulatory effects of cytokines. Hum Reprod. 2007;22(1):63\u201374."},{"issue":"4","key":"i1543-2165-138-5-643-b15","series-title":"Biol Reprod","first-page":"1096","article-title":"ADAMTS-1 is essential for the development and function of the urogenital system","volume":"70","author":"Mittaz\n              L,","year":"2004","unstructured":"Mittaz\n              L, \n            \n              Russell\n              DL, \n            \n              Wilson\n              T, \n            et al\n          . ADAMTS-1 is essential for the development and function of the urogenital system. Biol Reprod. 2004;70(4):1096\u20131105."},{"issue":"1\u20132","key":"i1543-2165-138-5-643-b16","series-title":"Cancer Metastasis Rev","first-page":"159","article-title":"Endogenous regulators of angiogenesis: emphasis on proteins with thrombospondin: type 1 motifs","volume":"19","author":"Carpizo\n              D,","year":"2000","unstructured":"Carpizo\n              D, \n            \n              Iruela-Arispe\n              ML. \n          \n          Endogenous regulators of angiogenesis: emphasis on proteins with thrombospondin: type 1 motifs. 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Clin Cancer Res. 2004;10(7):2429\u20132440."},{"issue":"1","key":"i1543-2165-138-5-643-b18","series-title":"Placenta","first-page":"53","article-title":"Expression and activity of matrix metalloproteinase 2 and 9 in human trophoblasts","volume":"24","author":"Isaka\n              K,","year":"2003","unstructured":"Isaka\n              K, \n            \n              Usuda\n              S, \n            \n              Ito\n              H, \n            et al\n          . Expression and activity of matrix metalloproteinase 2 and 9 in human trophoblasts. Placenta. 2003;24(1):53\u201364."},{"issue":"5","key":"i1543-2165-138-5-643-b19","series-title":"J Clin Pathol","first-page":"399","article-title":"Comparison of ADAMTS-1, -4, and -5 expression in culprit plaques between acute myocardial infarction and stable angina","volume":"64","author":"Lee\n              CW,","year":"2011","unstructured":"Lee\n              CW, \n            \n              Hwang\n              I, \n            \n              Park\n              CS, \n            et al\n          . Comparison of ADAMTS-1, -4, and -5 expression in culprit plaques between acute myocardial infarction and stable angina. J Clin Pathol. 2011;64(5):399\u2013404."},{"issue":"3","key":"i1543-2165-138-5-643-b20","series-title":"Osteoarthritis Cartilage","first-page":"321","article-title":"Association of a nsSNP in ADAMTS-14 to some osteoarthritis phenotypes","volume":"17","author":"Rodriguez-Lopez\n              J,","year":"2009","unstructured":"Rodriguez-Lopez\n              J, \n            \n              Pombo-Suarez\n              M, \n            \n              Loughlin\n              J, \n            et al\n          . Association of a nsSNP in ADAMTS-14 to some osteoarthritis phenotypes. Osteoarthritis Cartilage. 2009;17(3):321\u2013327."},{"issue":"3","key":"i1543-2165-138-5-643-b21","series-title":"Acta Neuropathol","first-page":"239","article-title":"Human glioblastomas overexpress ADAMTS-5 that degrades brevican","volume":"110","author":"Nakada\n              M,","year":"2005","unstructured":"Nakada\n              M, \n            \n              Miyamori\n              H, \n            \n              Kita\n              D, \n            et al\n          . Human glioblastomas overexpress ADAMTS-5 that degrades brevican. Acta Neuropathol. 2005;110(3):239\u2013246."},{"issue":"5","key":"i1543-2165-138-5-643-b22","series-title":"Int J Cancer","first-page":"1241","article-title":"ADAMTS8 and ADAMTS15 expression predicts survival in human breast carcinoma","volume":"118","author":"Porter\n              S,","year":"2006","unstructured":"Porter\n              S, \n            \n              Span\n              PN, \n            \n              Sweep\n              FC, \n            et al\n          . ADAMTS8 and ADAMTS15 expression predicts survival in human breast carcinoma. 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Int J Cancer. 2006;118(1):55\u201361."},{"issue":"10","key":"i1543-2165-138-5-643-b24","series-title":"J Clin Invest","first-page":"1335","article-title":"The new kids on the block: ADAMTSs, potentially multifunctional metalloproteinases of the ADAM family","volume":"105","author":"Kaushal\n              GP,","year":"2000","unstructured":"Kaushal\n              GP, \n            \n              Shah\n              SV. \n          \n          The new kids on the block: ADAMTSs, potentially multifunctional metalloproteinases of the ADAM family. J Clin Invest. 2000;105(10):1335\u20131337."},{"issue":"1","key":"i1543-2165-138-5-643-b25","series-title":"Int J Biochem Cell Biol","first-page":"33","article-title":"ADAMTS: a novel family of extracellular matrix proteases","volume":"33","author":"Tang\n              BL.","year":"2001","unstructured":"Tang\n              BL. \n          \n          ADAMTS: a novel family of extracellular matrix proteases. Int J Biochem Cell Biol. 2001;33(1):33\u201344."},{"issue":"22","key":"i1543-2165-138-5-643-b26","series-title":"EMBO J","first-page":"5270","article-title":"ADAMTS-1 mediates the release of antiangiogenic polypeptides from TSP1 and 2","volume":"25","author":"Lee\n              NV,","year":"2006","unstructured":"Lee\n              NV, \n            \n              Sato\n              M, \n            \n              Annis\n              DS, \n            et al\n          . ADAMTS-1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J. 2006;25(22):5270\u20135283."},{"issue":"12","key":"i1543-2165-138-5-643-b01","series-title":"Chin Sci Bull","first-page":"1169","article-title":"Matrix metalloproteinases and trophoblast invasion","volume":"50","author":"Li\n              J,","year":"2005","unstructured":"Li\n              J, \n            \n              Zhao\n              T, \n            \n              Duan\n              E. \n          \n          Matrix metalloproteinases and trophoblast invasion. 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Philadelphia, PA: Saunders;2007."},{"issue":"4","key":"i1543-2165-138-5-643-b05","series-title":"PLoS One","article-title":"Regulated expression of ADAMTS-12 in human trophoblastic cells: a role for ADAMTS-12 in epithelial cell invasion","volume":"6","author":"Beristain\n              AG,","year":"2011","unstructured":"Beristain\n              AG, \n            \n              Zhu\n              H, \n            \n              Leung\n              PC. \n          \n          Regulated expression of ADAMTS-12 in human trophoblastic cells: a role for ADAMTS-12 in epithelial cell invasion? PLoS One. 2011;6(4):e18473.http:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC3073978\/. Accessed June 24, 2013."},{"issue":"2","key":"i1543-2165-138-5-643-b06","series-title":"Am J Reprod Immunol","first-page":"96","article-title":"Type 2 cadherins in the human endometrium and placenta: the putative roles in human implantation and placentation","volume":"39","author":"MacCalman\n              CD,","year":"1998","unstructured":"MacCalman\n              CD, \n            \n              Getsios\n              S, \n            \n              Chen\n              GT. \n          \n          Type 2 cadherins in the human endometrium and placenta: the putative roles in human implantation and placentation. Am J Reprod Immunol. 1998;39(2):96\u2013107."},{"issue":"8","key":"i1543-2165-138-5-643-b07","series-title":"Placenta","first-page":"783","article-title":"Metalloproteinases and human placental invasiveness","volume":"27","author":"Cohen\n              M,","year":"2006","unstructured":"Cohen\n              M, \n            \n              Meisser\n              A, \n            \n              Bischof\n              P. \n          \n          Metalloproteinases and human placental invasiveness. 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Human Reprod. 2006;21(8):1990\u20131999."},{"issue":"10","key":"i1543-2165-138-5-643-b09","series-title":"J Clin Invest","first-page":"1345","article-title":"ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function","volume":"105","author":"Shindo\n              T,","year":"2000","unstructured":"Shindo\n              T, \n            \n              Kurihara\n              H, \n            \n              Kuno\n              K, \n            et al\n          . ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest. 2000;105(10):1345\u20131352."},{"issue":"33","key":"i1543-2165-138-5-643-b10","series-title":"J Biol Chem","first-page":"23349","article-title":"METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity","volume":"274","author":"Vazquez\n              F,","year":"1999","unstructured":"Vazquez\n              F, \n            \n              Hastings\n              G, \n            \n              Ortega\n              MA, \n            et al\n          . METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity. J Biol Chem. 1999;274(33):23349\u201323357."},{"issue":"pt 1","key":"i1543-2165-138-5-643-b11","series-title":"Biochem J","first-page":"15","article-title":"The ADAMTS metalloproteinases","volume":"386","author":"Porter\n              S,","year":"2005","unstructured":"Porter\n              S, \n            \n              Clark\n              IM, \n            \n              Kevorkian\n              L, \n            \n              Edwards\n              DR. \n          \n          The ADAMTS metalloproteinases. 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