A Disintegrin-like And Metalloproteinase with ThromboSpondin motifs—ADAMTSs—are a multi-domain, secreted, extracellular zinc metalloproteinase family with 19 members in humans. These extracellular metalloproteinases are known to cleave a wide range of substrates in the extracellular matrix. They have been implicated in various physiological processes, such as extracellular matrix turnover, melanoblast development, interdigital web regression, blood coagulation, ovulation, etc. ADAMTSs are also critical in pathological processes such as arthritis, atherosclerosis, cancer, angiogenesis, wound healing, etc. In the past few years, there has been an explosion of reports concerning the role of ADAMTS family members in angiogenesis and cancer. To date, 10 out of the 19 members have been demonstrated to be involved in regulating angiogenesis and/or cancer. The mechanism involved in their regulation of angiogenesis or cancer differs among different members. Both angiogenesis-dependent and -independent regulation of cancer have been reported. This review summarizes our current understanding on the roles of ADAMTS in angiogenesis and cancer and highlights their implications in cancer therapeutic development.
References
[1]
Koo, B.-H.; Longpré, J.-M.; Somerville, R.; Alexander, J.; Leduc, R.; Apte, S. Regulation of ADAMTS9 secretion and enzymatic activity by its propeptide. J. Biol. Chem. 2007, 282, 16146–16154.
[2]
Majerus, E.; Zheng, X.; Tuley, E.; Sadler, J. Cleavage of the ADAMTS13 propeptide is not required for protease activity. J. Biol. Chem. 2003, 278, 46643–46648.
[3]
Porter, S.; Clark, I.M.; Kevorkian, L.; Edwards, D.R. The ADAMTS metalloproteinases. Biochem. J. 2005, 386, 15–27, doi:10.1042/BJ20040424.
[4]
Apte, S. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: Functions and mechanisms. J. Biol. Chem. 2009, 284, 31493–31500, doi:10.1074/jbc.R109.052340.
[5]
Tortorella, M.; Malfait, F.; Barve, R.; Shieh, H.-S.; Malfait, A.-M. A review of the ADAMTS family, pharmaceutical targets of the future. Curr. Pharm. Des. 2009, 15, 2359–2374.
[6]
Stanton, H.; Melrose, J.; Little, C.; Fosang, A. Proteoglycan degradation by the ADAMTS family of proteinases. Biochim. Biophys. Acta 2011, 1812, 1616–1629, doi:10.1016/j.bbadis.2011.08.009.
[7]
Troeberg, L.; Nagase, H. Proteases involved in cartilage matrix degradation in osteoarthritis. Biochim. Biophys. Acta 2012, 1824, 133–145, doi:10.1016/j.bbapap.2011.06.020.
[8]
Wagstaff, L.; Kelwick, R.; Decock, J.; Edwards, D.R. The roles of ADAMTS metalloproteinases in tumorigenesis and metastasis. Front. Biosci. 2011, 16, 1861–1872.
[9]
Salter, R.; Ashlin, T.; Kwan, A.; Ramji, D. ADAMTS proteases: Key roles in atherosclerosis? J. Mol. Med. 2010, 88, 1203–1211, doi:10.1007/s00109-010-0654-x.
[10]
Lee, M.; Rodansky, E.; Smith, J.; Rodgers, G. ADAMTS13 promotes angiogenesis and modulates VEGF-induced angiogenesis. Microvasc. Res. 2012, 84, 109–115.
[11]
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, 556–618.
[12]
Vazquez, F.; Hastings, G.; Ortega, M.A.; Lane, T.F.; Oikemus, S.; Lombardo, M.; Iruela-Arispe, M.L. 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, 23349–23357.
[13]
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.
[14]
Thai, S.N.; Iruela-Arispe, M.L. Expression of ADAMTS1 during murine development. Mech. Dev. 2002, 115, 181–185, doi:10.1016/S0925-4773(02)00115-6.
[15]
Gustavsson, H.; Wang, W.; Jennbacken, K.; Welén, K.; Damber, J.-E. ADAMTS1, a putative anti-angiogenic factor, is decreased in human prostate cancer. BJU Int. 2009, 104, 1786–1790, doi:10.1111/j.1464-410X.2009.08676.x.
[16]
Hatipoglu, O.F.; Hirohata, S.; Yaykasli, K.O.; Cilek, M.Z.; Demircan, K.; Shinohata, R.; Yonezawa, T.; Oohashi, T.; Kusachi, S.; Ninomiya, Y. The 3'-untranslated region of ADAMTS1 regulates its mRNA stability. Acta Med. Okayama 2009, 63, 79–85.
[17]
Kalinski, T.; Krueger, S.; Sel, S.; Werner, K.; R？pke, M.; Roessner, A. ADAMTS1 is regulated by interleukin-1beta, not by hypoxia, in chondrosarcoma. Hum. Pathol. 2007, 38, 86–94, doi:10.1016/j.humpath.2006.06.012.
[18]
Lee, N.; Rodriguez-Manzaneque, J.; Thai, S.; Twal, W.; Luque, A.; Lyons, K.; Argraves, W.; Iruela-Arispe, M. Fibulin-1 acts as a cofactor for the matrix metalloprotease ADAMTS-1. J. Biol. Chem. 2005, 280, 34796–34804.
[19]
Shindo, T.; Kurihara, H.; Kuno, K.; Yokoyama, H.; Wada, T.; Kurihara, Y.; Imai, T.; Wang, Y.; Ogata, M.; Nishimatsu, H.; et al. DAMTS-1: A metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J. Clin. Invest. 2000, 105, 1345–1352.
[20]
Mittaz, L.; Russell, D.; Wilson, T.; Brasted, M.; Tkalcevic, J.; Salamonsen, L.; Hertzog, P.; Pritchard, M. Adamts-1 is essential for the development and function of the urogenital system. Biol. Reprod. 2004, 70, 1096–1105.
[21]
Yokoyama, H.; Wada, T.; Kobayashi, K.-I.; Kuno, K.; Kurihara, H.; Shindo, T.; Matsushima, K. A disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS)-1 null mutant mice develop renal lesions mimicking obstructive nephropathy. Nephrol. Dial. Transplant. 2002, 17, 39–41.
[22]
Rodríguez-Manzaneque, J.; Westling, J.; Thai, S.; Luque, A.; Knauper, V.; Murphy, G.; Sandy, J.; Iruela-Arispe, M. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors. Biochem. Biophys. Res. Commun. 2002, 293, 501–508.
[23]
Sandy, J.D.; Westling, J.; Kenagy, R.D.; Iruela-Arispe, M.L.; Verscharen, C.; Rodriguez-Mazaneque, J.C.; Zimmermann, D.R.; Lemire, J.M.; Fischer, J.W.; Wight, T.N.; et al. Versican V1 proteolysis in human aorta in vivo occurs at the Glu(441)-Ala(442) bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J. Biol. Chem. 2001, 276, 13372–13378.
[24]
Canals, F.; Colomé, N.; Ferrer, C.; Plaza-Calonge, M.; Rodríguez-Manzaneque, J. Identification of substrates of the extracellular protease ADAMTS1 by DIGE proteomic analysis. Proteomics 2006, 6, 35.
[25]
Torres-Collado, A.; Kisiel, W.; Iruela-Arispe, M.; Rodríguez-Manzaneque, J. ADAMTS1 interacts with, cleaves, and modifies the extracellular location of the matrix inhibitor tissue factor pathway inhibitor-2. J. Biol. Chem. 2006, 281, 17827–17837.
[26]
Krampert, M.; Kuenzle, S.; Thai, S.; Lee, N.; Iruela-Arispe, M.; Werner, S. ADAMTS1 proteinase is up-regulated in wounded skin and regulates migration of fibroblasts and endothelial cells. J. Biol. Chem. 2005, 280, 23844–23852.
[27]
Little, C.; Mittaz, L.; Belluoccio, D.; Rogerson, F.; Campbell, I.; Meeker, C.; Bateman, J.; Pritchard, M.; Fosang, A. ADAMTS-1-knockout mice do not exhibit abnormalities in aggrecan turnover in vitro or in vivo. Arthritis Rheum. 2005, 52, 1461–1472.
[28]
Wang, W.-M.; Lee, S.; Steiglitz, B.; Scott, I.; Lebares, C.; Allen, M.; Brenner, M.; Takahara, K.; Greenspan, D. Transforming growth factor-beta induces secretion of activated ADAMTS-2. A procollagen III N-proteinase. J. Biol. Chem. 2003, 278, 19549–19557.
[29]
Colige, A.; Sieron, A.; Li, S.; Schwarze, U.; Petty, E.; Wertelecki, W.; Wilcox, W.; Krakow, D.; Cohn, D.; Reardon, W.; et al. Human Ehlers-Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene. Am. J. Hum. Genet. 1999, 65, 308–317, doi:10.1086/302504.
[30]
Colige, A.; Ruggiero, F.; Vandenberghe, I.; Dubail, J.; Kesteloot, F.; van Beeumen, J.; Beschin, A.; Brys, L.; Lapière, C.; Nusgens, B. Domains and maturation processes that regulate the activity of ADAMTS-2, a metalloproteinase cleaving the aminopropeptide of fibrillar procollagens types I–III and V. J. Biol. Chem. 2005, 280, 34397–34408.
[31]
Li, S.; Arita, M.; Fertala, A.; Bao, Y.; Kopen, G.; L？ngsj？, T.; Hyttinen, M.; Helminen, H.; Prockop, D. Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem. J. 2001, 355, 271–278, doi:10.1042/0264-6021:3550271.
[32]
Tortorella, M.; Burn, T.; Pratta, M.; Abbaszade, I.; Hollis, J.; Liu, R.; Rosenfeld, S.; Copeland, R.; Decicco, C.; Wynn, R.; et al. Purification and cloning of aggrecanase-1: A member of the ADAMTS family of proteins. Science 1999, 284, 1664–1666, doi:10.1126/science.284.5420.1664.
[33]
Naito, S.; Shiomi, T.; Okada, A.; Kimura, T.; Chijiiwa, M.; Fujita, Y.; Yatabe, T.; Komiya, K.; Enomoto, H.; Fujikawa, K.; et al. Expression of ADAMTS4 (aggrecanase-1) in human osteoarthritic cartilage. Pathol. Int. 2007, 57, 703–711, doi:10.1111/j.1440-1827.2007.02167.x.
[34]
Matthews, R.; Gary, S.; Zerillo, C.; Pratta, M.; Solomon, K.; Arner, E.; Hockfield, S. Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J. Biol. Chem. 2000, 275, 22695–22703.
[35]
Ehlen, H.W.; Sengle, G.; Klatt, A.R.; Talke, A.; Muller, S.; Paulsson, M.; Wagener, R. Proteolytic processing causes extensive heterogeneity of tissue matrilin forms. J. Biol. Chem. 2009, 284, 21545–21556.
[36]
Weaver, M.S.; Workman, G.; Cardo-Vila, M.; Arap, W.; Pasqualini, R.; Sage, E.H. Processing of the matricellular protein hevin in mouse brain is dependent on ADAMTS4. J. Biol. Chem. 2010, 285, 5868–5877.
[37]
Hisanaga, A.; Morishita, S.; Suzuki, K.; Sasaki, K.; Koie, M.; Kohno, T.; Hattori, M. A disintegrin and metalloproteinase with thrombospondin motifs 4 (ADAMTS-4) cleaves Reelin in an isoform-dependent manner. FEBS Lett. 2012, 586, 3349–3353.
[38]
Glasson, S.S.; Askew, R.; Sheppard, B.; Carito, B.A.; Blanchet, T.; Ma, H.L.; Flannery, C.R.; Kanki, K.; Wang, E.; Peluso, D.; et al. Characterization of and osteoarthritis susceptibility in ADAMTS-4-knockout mice. Arthritis Rheum. 2004, 50, 2547–2558, doi:10.1002/art.20558.
[39]
Abbaszade, I.; Liu, R.; Yang, F.; Rosenfeld, S.; Ross, O.H.; Link, J.R.; Ellis, D.M.; Tortorella, M.D.; Pratta, MA.; Hollis, J.M.; et al. Cloning and characterization of ADAMTS11, an aggrecanase from the ADAMTS family. J. Biol. Chem. 1999, 274, 23443–23450.
[40]
Longpré, J.-M.; McCulloch, D.; Koo, B.-H.; Alexander, J.; Apte, S.; Leduc, R. Characterization of proADAMTS5 processing by proprotein convertases. Int. J. Biochem. Cell Biol. 2009, 41, 1116–1142.
[41]
Nakada, M.; Miyamori, H.; Kita, D.; Takahashi, T.; Yamashita, J.; Sato, H.; Miura, R.; Yamaguchi, Y.; Okada, Y. Human glioblastomas overexpress ADAMTS-5 that degrades brevican. Acta Neuropathol. 2005, 110, 239–246, doi:10.1007/s00401-005-1032-6.
[42]
Cross, N.; Chandrasekharan, S.; Jokonya, N.; Fowles, A.; Hamdy, F.; Buttle, D.; Eaton, C. The expression and regulation of ADAMTS-1, -4, -5, -9, and -15, and TIMP-3 by TGFbeta1 in prostate cells: Relevance to the accumulation of versican. Prostate 2005, 63, 269–275, doi:10.1002/pros.20182.
[43]
Glasson, S.; Askew, R.; Sheppard, B.; Carito, B.; Blanchet, T.; Ma, H.-L.; Flannery, C.; Peluso, D.; Kanki, K.; Yang, Z.; et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 2005, 434, 644–652.
[44]
Stanton, H.; Rogerson, F.; East, C.; Golub, S.; Lawlor, K.; Meeker, C.; Little, C.; Last, K.; Farmer, P.; Campbell, I.; et al. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 2005, 434, 648–700, doi:10.1038/nature03417.
[45]
McCulloch, D.; Nelson, C.; Dixon, L.; Silver, D.; Wylie, J.; Lindner, V.; Sasaki, T.; Cooley, M.; Argraves, W.; Apte, S. ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev. Cell 2009, 17, 687–785.
[46]
Velasco, J.; Li, J.; DiPietro, L.; Stepp, M.; Sandy, J.; Plaas, A. Adamts5 deletion blocks murine dermal repair through CD44-mediated aggrecan accumulation and modulation of transforming growth factor β1 (TGFβ1) signaling. J. Biol. Chem. 2011, 286, 26016–26043.
[47]
Majumdar, M.; Askew, R.; Schelling, S.; Stedman, N.; Blanchet, T.; Hopkins, B.; Morris, E.; Glasson, S. Double-knockout of ADAMTS-4 and ADAMTS-5 in mice results in physiologically normal animals and prevents the progression of osteoarthritis. Arthritis Rheum. 2007, 56, 3670–3674, doi:10.1002/art.23027.
[48]
Ilic, M.; East, C.; Rogerson, F.; Fosang, A.; Handley, C. Distinguishing aggrecan loss from aggrecan proteolysis in ADAMTS-4 and ADAMTS-5 single and double deficient mice. J. Biol. Chem. 2007, 282, 37420–37428, doi:10.1074/jbc.M703184200.
[49]
Collins-Racie, L.; Flannery, C.; Zeng, W.; Corcoran, C.; Annis-Freeman, B.; Agostino, M.; Arai, M.; DiBlasio-Smith, E.; Dorner, A.; Georgiadis, K.; et al. ADAMTS-8 exhibits aggrecanase activity and is expressed in human articular cartilage. Matrix Biol. 2004, 23, 219–230, doi:10.1016/j.matbio.2004.05.004.
[50]
Somerville, R.; Longpre, J.-M.; Jungers, K.; Engle, J.; Ross, M.; Evanko, S.; Wight, T.; Leduc, R.; Apte, S. 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.
[51]
Enomoto, H.; Nelson, C.; Somerville, R.; Mielke, K.; Dixon, L.; Powell, K.; Apte, S. Cooperation of two ADAMTS metalloproteases in closure of the mouse palate identifies a requirement for versican proteolysis in regulating palatal mesenchyme proliferation. Development 2010, 137, 4029–4038.
[52]
Koo, B.-H.; Coe, D.; Dixon, L.; Somerville, R.; Nelson, C.; Wang, L.; Young, M.; Lindner, D.; Apte, S. ADAMTS9 is a cell-autonomously acting, anti-angiogenic metalloprotease expressed by microvascular endothelial cells. Am. J. Pathol. 2010, 176, 1494–1504, doi:10.2353/ajpath.2010.090655.
[53]
Kern, C.; Wessels, A.; McGarity, J.; Dixon, L.; Alston, E.; Argraves, W.; Geeting, D.; Nelson, C.; Menick, D.; Apte, S. Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol. 2010, 29, 304–316.
[54]
Liu, C.-J.; Kong, W.; Xu, K.; Luan, Y.; Ilalov, K.; Sehgal, B.; Yu, S.; Howell, R.; di Cesare, P. ADAMTS-12 associates with and degrades cartilage oligomeric matrix protein. J. Biol. Chem. 2006, 281, 15800–15808.
[55]
Llamazares, M.; Obaya, A.; Moncada-Pazos, A.; Heljasvaara, R.; Espada, J.; López-Otín, C.; Cal, S. The ADAMTS12 metalloproteinase exhibits anti-tumorigenic properties through modulation of the Ras-dependent ERK signalling pathway. J. Cell Sci. 2007, 120, 3544–3552, doi:10.1242/jcs.005751.
[56]
El Hour, M.; Moncada-Pazos, A.; Blacher, S.; Masset, A.; Cal, S.; Berndt, S.; Detilleux, J.; Host, L.; Obaya, A.; Maillard, C.; et al. Higher sensitivity of Adamts12-deficient mice to tumor growth and angiogenesis. Oncogene 2010, 29, 3025–3032, doi:10.1038/onc.2010.49.
[57]
Moncada-Pazos, A.; Obaya, A.; Llamazares, M.; Heljasvaara, R.; Suárez, M.; Colado, E.; No？l, A.; Cal, S.; López-Otin, C. ADAMTS-12 metalloprotease is necessary for normal inflammatory response. J. Biol. Chem. 2012, 287, 39554–39563.
[58]
Fujikawa, K.; Suzuki, H.; McMullen, B.; Chung, D. Purification of human von Willebrand factor-cleaving protease and its identification as a new member of the metalloproteinase family. Blood 2001, 98, 1662–1666.
[59]
Banno, F.; Kokame, K.; Okuda, T.; Honda, S.; Miyata, S.; Kato, H.; Tomiyama, Y.; Miyata, T. Complete deficiency in ADAMTS13 is prothrombotic, but it alone is not sufficient to cause thrombotic thrombocytopenic purpura. Blood 2006, 107, 3161–3166, doi:10.1182/blood-2005-07-2765.
Yamaji, N.; Nishimura, K.; Abe, K.; Ohara, O.; Nagase, T.; Nomura, N. Novel metalloprotease having aggrecanase activity. EP1234875A1, 10 November 2000.
[62]
Fraser, F.W.; Dancevic, C.M.; Stupka, N.S.; Fosang, A.J.; Rogerson, F.; Ward, A.C.; McCulloch, D.R. The biosynthesis and expression of ADAMTS15; a novel versican-cleaving proteoglycanase, Matrix Biology Society of Australia and New Zealand Annual Meeting, Gold Coast, Australia, 7 September 2012.
[63]
Iruela-Arispe, M.; Carpizo, D.; Luque, A. ADAMTS1: A matrix metalloprotease with angioinhibitory properties. Ann. NY Acad. Sci. 2003, 995, 183–190.
[64]
Fu, Y.; Nagy, J.; Brown, L.; Shih, S.-C.; Johnson, P.; Chan, C.; Dvorak, H.; Wight, T. Proteolytic cleavage of versican and involvement of ADAMTS-1 in VEGF-A/VPF-induced pathological angiogenesis. J. Histochem. Cytochem. 2011, 59, 463–473, doi:10.1369/0022155411401748.
[65]
Obika, M.; Ogawa, H.; Takahashi, K.; Li, J.; Hatipoglu, O.; Cilek, M.; Miyoshi, T.; Inagaki, J.; Ohtsuki, T.; Kusachi, S.; et al. Tumor growth inhibitory effect of ADAMTS1 is accompanied by the inhibition of tumor angiogenesis. Cancer Sci. 2012, 103, 1889–1897.
[66]
Liu, Y.J.; Xu, Y.; Yu, Q. Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro- and antimetastatic activity, respectively. Oncogene 2006, 25, 2452–2467, doi:10.1038/sj.onc.1209287.
[67]
Nakamura, K.; Hirohata, S.; Murakami, T.; Miyoshi, T.; Demircan, K.; Oohashi, T.; Ogawa, H.; Koten, K.; Toeda, K.; Kusachi, S.; et al. Dynamic induction of ADAMTS1 gene in the early phase of acute myocardial infarction. J. Biochem. 2004, 136, 439–446, doi:10.1093/jb/mvh138.
[68]
Gustavsson, H.; Tesan, T.; Jennbacken, K.; Kuno, K.; Damber, J.-E.; Welén, K. ADAMTS1 alters blood vessel morphology and TSP1 levels in LNCaP and LNCaP-19 prostate tumors. BMC Cancer 2010, 10, 288, doi:10.1186/1471-2407-10-288.
[69]
Xu, Z.; Yu, Y.; Duh, E. Vascular endothelial growth factor upregulates expression of ADAMTS1 in endothelial cells through protein kinase C signaling. Invest. Ophthalmol. Vis. Sci. 2006, 47, 4059–4066.
[70]
Casal, C.; Torres-Collado, A.; Plaza-Calonge, M.D.C.; Martino-Echarri, E.; Ramón Y Cajal, S.; Rojo, F.; Griffioen, A.; Rodríguez-Manzaneque, J. ADAMTS1 contributes to the acquisition of an endothelial-like phenotype in plastic tumor cells. Cancer Res. 2010, 70, 4676–4686.
[71]
Dubail, J.; Kesteloot, F.; Deroanne, C.; Motte, P.; Lambert, V.; Rakic, J.M.; Lapière, C.; Nusgens, B.; Colige, A. ADAMTS-2 functions as anti-angiogenic and anti-tumoral molecule independently of its catalytic activity. Cell. Mol. Life Sci. 2010, 67, 4213–4232.
[72]
Rao, N.; Ke, Z.; Liu, H.; Ho, C.-J.; Kumar, S.; Xiang, W.; Zhu, Y.; Ge, R. ADAMTS4 and Its Proteolytic Fragments Differentially Affect Melanoma Growth and Angiogenesis in Mice. Int. J. Cancer 2012. submitted.
[73]
Karagiannis, E.D.; Popel, A.S. Anti-angiogenic peptides identified in thrombospondin type I domains. Biochem.Biophys. Res. Commun. 2007, 359, 63–69.
[74]
Hsu, Y.P.; Staton, C.A.; Cross, N.; Buttle, D.J. Anti-angiogenic properties of ADAMTS-4 in vitro. Int. J. Exp. Pathol. 2012, 93, 70–77, doi:10.1111/j.1365-2613.2011.00802.x.
[75]
Kumar, S.; Sharghi-Namini, S.; Rao, N.; Ge, R. ADAMTS5 Functions as an Anti-Angiogenic and Anti-Tumorigenic Protein Independent of Its Proteoglycanase Activity. Am. J. Pathol. 2012, 181, 1056–1068.
[76]
Sharghi-Namini, S.; Fan, H.; Sulochana, K.; Potturi, P.; Xiang, W.; Chong, Y.-S.; Wang, Z.; Yang, H.; Ge, R. The first but not the second thrombospondin type 1 repeat of ADAMTS5 functions as an angiogenesis inhibitor. Biochem. Biophys. Res. Commun. 2008, 371, 215–219, doi:10.1016/j.bbrc.2008.04.047.
Lee, N.; Sato, M.; Annis, D.; Loo, J.; Wu, L.; Mosher, D.; Iruela-Arispe, M. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J. 2006, 25, 5270–5283, doi:10.1038/sj.emboj.7601400.
[79]
Luque, A.; Carpizo, D.R.; Iruela-Arispe, M.L. ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J. Biol. Chem. 2003, 278, 23656–23665.
[80]
Hatipoglu, O.; Hirohata, S.; Cilek, M.; Ogawa, H.; Miyoshi, T.; Obika, M.; Demircan, K.; Shinohata, R.; Kusachi, S.; Ninomiya, Y. ADAMTS1 is a unique hypoxic early response gene expressed by endothelial cells. J. Biol. Chem. 2009, 284, 16325–16333.
[81]
Cilek, M.; Hirohata, S.; Faruk Hatipoglu, O.; Ogawa, H.; Miyoshi, T.; Inagaki, J.; Ohtsuki, T.; Harada, H.; Kamikawa, S.; Kusachi, S.; et al. AHR, a novel acute hypoxia-response sequence, drives reporter gene expression under hypoxia in vitro and in vivo. Cell Biol. Int. 2011, 35, 1–8.
[82]
Masui, T.; Hosotani, R.; Tsuji, S.; Miyamoto, Y.; Yasuda, S.; Ida, J.; Nakajima, S.; Kawaguchi, M.; Kobayashi, H.; Koizumi, M.; et al. Expression of METH-1 and METH-2 in pancreatic cancer. Clin. Cancer Res. 2001, 7, 3437–3443.
[83]
Choi, J.; Kim, D.; Kim, E.; Chae, M.; Cha, S.; Kim, C.; Jheon, S.; Jung, T.; Park, J. Aberrant methylation of ADAMTS1 in non-small cell lung cancer. Cancer Genet. Cytogenet. 2008, 187, 80–84.
[84]
Keightley, M.; Sales, K.; Jabbour, H. PGF2α-F-prostanoid receptor signalling via ADAMTS1 modulates epithelial cell invasion and endothelial cell function in endometrial cancer. BMC Cancer 2010, 10, 488.
[85]
Ricciardelli, C.; Frewin, K.; Tan, I.; Williams, E.; Opeskin, K.; Pritchard, M.; Ingman, W.; Russell, D. The ADAMTS1 protease gene is required for mammary tumor growth and metastasis. Am. J. Pathol. 2011, 179, 3075–3085.
[86]
Lu, X.; Wang, Q.; Hu, G.; van Poznak, C.; Fleisher, M.; Reiss, M.; Massagué, J.; Kang, Y. ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev. 2009, 23, 1882–1894.
[87]
Lee, Y.-J.; Koch, M.; Karl, D.; Torres-Collado, A.; Fernando, N.; Rothrock, C.; Kuruppu, D.; Ryeom, S.; Iruela-Arispe, M.; Yoon, S. Variable inhibition of thrombospondin 1 against liver and lung metastases through differential activation of metalloproteinase ADAMTS1. Cancer Res. 2010, 70, 948–956.
[88]
Rocks, N.; Paulissen, G.; Quesada-Calvo, F.; Munaut, C.; Gonzalez, M.-L. A.; Gueders, M.; Hacha, J.; Gilles, C.; Foidart, J.-M.; Noel, A.; et al. ADAMTS-1 metalloproteinase promotes tumor development through the induction of a stromal reaction in vivo. Cancer Res. 2008, 68, 9541–9550, doi:10.1158/0008-5472.CAN-08-0548.
[89]
Tyan, S.-W.; Hsu, C.-H.; Peng, K.-L.; Chen, C.-C.; Kuo, W.-H.; Lee, E.; Shew, J.-Y.; Chang, K.-J.; Juan, L.-J.; Lee, W.-H. Breast cancer cells induce stromal fibroblasts to secrete ADAMTS1 for cancer invasion through an epigenetic change. PLoS One 2012, 7, e35128.
[90]
Kuno, K.; Bannai, K.; Hakozaki, M.; Matsushima, K.; Hirose, K. The carboxyl-terminal half region of ADAMTS-1 suppresses both tumorigenicity and experimental tumor metastatic potential. Biochem. Biophys. Res. Commun. 2004, 319, 1327–1333.
[91]
Porter, S.; Scott, S.D.; Sassoon, E.M.; Williams, M.R.; Jones, J.L.; Girling, A.C.; Ball, R.Y.; Edwards, D.R. Dysregulated expression of adamalysin-thrombospondin genes in human breast carcinoma. Clin. Cancer Res. 2004, 10, 2429–2440.
[92]
Demircan, K.; Gunduz, E.; Gunduz, M.; Beder, L.B.; Hirohata, S.; Nagatsuka, H.; Cengiz, B.; Cilek, M.Z.; Yamanaka, N.; Shimizu, K.; et al. Increased mRNA expression of ADAMTS metalloproteinases in metastatic foci of head and neck cancer. Head Neck 2009, 31, 793–801, doi:10.1002/hed.21045.
[93]
Held-Feindt, J.; Paredes, E.B.; Blomer, U.; Seidenbecher, C.; Stark, A.M.; Mehdorn, H.M.; Mentlein, R. Matrix-degrading proteases ADAMTS4 and ADAMTS5 (disintegrins and metalloproteinases with thrombospondin motifs 4 and 5) are expressed in human glioblastomas. Int. J. Cancer 2006, 118, 55–61.
[94]
Minobe, K.; Ono, R.; Matsumine, A.; Shibata-Minoshima, F.; Izawa, K.; Oki, T.; Kitaura, J.; Iino, T.; Takita, J.; Iwamoto, S.; et al. Expression of ADAMTS4 in Ewing's sarcoma. Int. J. Oncol. 2010, 37, 569–581.
[95]
Kim, Y.-H.; Lee, H.; Kim, S.-Y.; Yeom, Y.; Ryu, K.; Min, B.-H.; Kim, D.-H.; Son, H.; Rhee, P.-L.; Kim, J.; et al. Epigenomic analysis of aberrantly methylated genes in colorectal cancer identifies genes commonly affected by epigenetic alterations. Ann. Surg. Oncol. 2011, 18, 2338–2347, doi:10.1245/s10434-011-1573-y.
[96]
Heighway, J.; Knapp, T.; Boyce, L.; Brennand, S.; Field, J.; Betticher, D.; Ratschiller, D.; Gugger, M.; Donovan, M.; Lasek, A.; et al. Expression profiling of primary non-small cell lung cancer for target identification. Oncogene 2002, 21, 7749–7763, doi:10.1038/sj.onc.1205979.
[97]
Dunn, J.; Panutsopulos, D.; Shaw, M.; Heighway, J.; Dormer, R.; Salmo, E.; Watson, S.; Field, J.; Liloglou, T. METH-2 silencing and promoter hypermethylation in NSCLC. Br. J. Cancer 2004, 91, 1149–1154.
[98]
Dunn, J.; Reed, J.; du Plessis, D.; Shaw, E.; Reeves, P.; Gee, A.; Warnke, P.; Walker, C. Expression of ADAMTS-8, a secreted protease with antiangiogenic properties, is downregulated in brain tumours. Br. J. Cancer 2006, 94, 1186–1193.
[99]
Lo, P.; Leung, A.C.; Kwok, C.; Cheung, W.; Ko, J.; Yang, L.; Law, S.; Wang, L.; Li, J.; Stanbridge, E.; et al. Identification of a tumor suppressive critical region mapping to 3p14.2 in esophageal squamous cell carcinoma and studies of a candidate tumor suppressor gene, ADAMTS9. Oncogene 2007, 26, 148–157.
[100]
Lung, H.; Lo, P.; Xie, D.; Apte, S.; Cheung, A.; Cheng, Y.; Law, E.; Chua, D.; Zeng, Y.-X.; Tsao, S.; et al. Characterization of a novel epigenetically-silenced, growth-suppressive gene, ADAMTS9, and its association with lymph node metastases in nasopharyngeal carcinoma. Int. J. Cancer 2008, 123, 401–408.
[101]
Zhang, C.; Shao, Y.; Zhang, W.; Wu, Q.; Yang, H.; Zhong, Q.; Zhang, J.; Guan, M.; Yu, B.; Wan, J. High-resolution melting analysis of ADAMTS9 methylation levels in gastric, colorectal, and pancreatic cancers. Cancer Genet. Cytogenet. 2010, 196, 38–44, doi:10.1016/j.cancergencyto.2009.08.016.
[102]
Du, W.; Wang, S.; Zhou, Q.; Li, X.; Chu, J.; Chang, Z.; Tao, Q.; Ng, E.; Fang, J.; Sung, J.; et al. ADAMTS9 is a functional tumor suppressor through inhibiting AKT/mTOR pathway and associated with poor survival in gastric cancer. Oncogene 2012, doi:10.1038/onc.2012.359.
[103]
Moncada-Pazos, A.; Obaya, A.; Fraga, M.; Viloria, C.; Capellá, G.; Gausachs, M.; Esteller, M.; López-Otín, C.; Cal, S. The ADAMTS12 metalloprotease gene is epigenetically silenced in tumor cells and transcriptionally activated in the stroma during progression of colon cancer. J. Cell. Sci. 2009, 122, 2906–2913.
[104]
Oleksowicz, L.; Bhagwati, N.; DeLeon-Fernandez, M. Deficient activity of von Willebrand’s factor-cleaving protease in patients with disseminated malignancies. Cancer Res. 1999, 59, 2244–2250.
[105]
Koo, B.-H.; Oh, D.; Chung, S.; Kim, N.; Park, S.; Jang, Y.; Chung, K.-H. Deficiency of von Willebrand factor-cleaving protease activity in the plasma of malignant patients. Thromb. Res. 2002, 105, 471–476, doi:10.1016/S0049-3848(02)00053-1.
[106]
B？hm, M.; Gerlach, R.; Beecken, W.-D.; Scheuer, T.; Stier-Brück, I.; Scharrer, I. ADAMTS-13 activity in patients with brain and prostate tumors is mildly reduced, but not correlated to stage of malignancy and metastasis. Thromb. Res. 2003, 111, 33–37.
[107]
Viloria, C.; Obaya, A.; Moncada-Pazos, A.; Llamazares, M.; Astudillo, A.; Capellá, G.; Cal, S.; López-Otín, C. Genetic inactivation of ADAMTS15 metalloprotease in human colorectal cancer. Cancer Res. 2009, 69, 4926–4934.
[108]
Jones, S.; Zhang, X.; Parsons, D.; Lin, J.; Leary, R.; Angenendt, P.; Mankoo, P.; Carter, H.; Kamiyama, H.; Jimeno, A.; et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321, 1801–1806.
[109]
Connolly, K.; Gabra, H.; Millwater, C.; Taylor, K.; Rabiasz, G.; Watson, J.; Smyth, J.; Wyllie, A.; Jodrell, D. Identification of a region of frequent loss of heterozygosity at 11q24 in colorectal cancer. Cancer Res. 1999, 59, 2806–2809.
[110]
Li, Z.; Zhang, W.; Shao, Y.; Zhang, C.; Wu, Q.; Yang, H.; Wan, X.; Zhang, J.; Guan, M.; Wan, J.; et al. High-resolution melting analysis of ADAMTS18 methylation levels in gastric, colorectal and pancreatic cancers. Med. Oncol. 2010, 27, 998–1004.
[111]
Wood, L.D.; Parsons, D.W.; Jones, S.; Lin, J.; Sjoblom, T.; Leary, R.J.; Shen, D.; Boca, S.M.; Barber, T.; Ptak, J.; et al. The genomic landscapes of human breast and colorectal cancers. Science 2007, 318, 1108–1113.
[112]
Wei, X.; Prickett, T.D.; Viloria, C.G.; Molinolo, A.; Lin, J.C.; Cardenas-Navia, I.; Cruz, P.; Rosenberg, S.A.; Davies, M.A.; Gershenwald, J.E.; et al. Mutational and functional analysis reveals ADAMTS18 metalloproteinase as a novel driver in melanoma. Mol. Cancer Res. 2010, 8, 1513–1525.
[113]
Lapière, C.; Lenaers, A.; Kohn, L. Procollagen peptidase: An enzyme excising the coordination peptides of procollagen. Proc. Natl. Acad. Sci. USA 1971, 68, 3054–3058.
[114]
Hojima, Y.; van der Rest, M.; Prockop, D. Type I procollagen carboxyl-terminal proteinase from chick embryo tendons. Purification and characterization. J. Biol. Chem. 1985, 260, 15996–16003.
[115]
Hanset, R.; Ansay, M. Dermatosparaxie (peau déchirée) chez le veau: Un défaut général du tissu conjonctif, de nature héréditaire. Ann. Med. Vet. 1967, 7, 451–470.
[116]
Smith, L.; Wertelecki, W.; Milstone, L.; Petty, E.; Seashore, M.; Braverman, I.; Jenkins, T.; Byers, P. Human dermatosparaxis: A form of Ehlers-Danlos syndrome that results from failure to remove the amino-terminal propeptide of type I procollagen. Am. J. Hum. Genet. 1992, 51, 235–244.
[117]
Nusgens, B.; Verellen-Dumoulin, C.; Hermanns-Lê, T.; de Paepe, A.; Nuytinck, L.; Piérard, G.; Lapière, C. Evidence for a relationship between Ehlers-Danlos type VII C in humans and bovine dermatosparaxis. Nat. Genet. 1992, 1, 214–217.
[118]
Colige, A.; Li, S.; Sieron, A.; Nusgens, B.; Prockop, D.; Lapière, C. cDNA cloning and expression of bovine procollagen I N-proteinase: A new member of the superfamily of zinc-metalloproteinases with binding sites for cells and other matrix components. Proc. Natl. Acad. Sci. USA 1997, 94, 2374–2379, doi:10.1073/pnas.94.6.2374.
[119]
Nardi, J.; Martos, R.; Walden, K.; Lampe, D.; Robertson, H. Expression of lacunin, a large multidomain extracellular matrix protein, accompanies morphogenesis of epithelial monolayers in Manduca sexta. Insect Biochem. Mol. Biol. 1999, 29, 883–897, doi:10.1016/S0965-1748(99)00064-8.
[120]
Colige, A.; Nuytinck, L.; Hausser, I.; van Essen, A.; Thiry, M.; Herens, C.; Adès, L.; Malfait, F.; Paepe, A.; Franck, P.; et al. Novel types of mutation responsible for the dermatosparactic type of Ehlers-Danlos syndrome (Type VIIC) and common polymorphisms in the ADAMTS2 gene. J. Invest. Dermatol. 2004, 123, 656–663, doi:10.1111/j.0022-202X.2004.23406.x.
[121]
De Coster, P.; Cornelissen, M.; de Paepe, A.; Martens, L.; Vral, A. Abnormal dentin structure in two novel gene mutations [COL1A1, Arg134Cys] and [ADAMTS2, Trp795-to-ter] causing rare type I collagen disorders. Arch. Oral Biol. 2007, 52, 101–109, doi:10.1016/j.archoralbio.2006.08.007.
[122]
Zhou, H.; Hickford, J.; Fang, Q. A premature stop codon in the ADAMTS2 gene is likely to be responsible for dermatosparaxis in Dorper sheep. Anim. Genet. 2012, 43, 471–473.
[123]
Tolsma, S.; Volpert, O.; Good, D.; Frazier, W.; Polverini, P.; Bouck, N. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J. Cell Biol. 1993, 122, 497–511.
[124]
Arner, E.C.; Pratta, M.A.; Trzaskos, J.M.; Decicco, C.P.; Tortorella, M.D. Generation and characterization of aggrecanase. A soluble, cartilage-derived aggrecan-degrading activity. J. Biol. Chem. 1999, 274, 6594–6601.
[125]
Wang, P.; Tortorella, M.; England, K.; Malfait, A.M.; Thomas, G.; Arner, E.C.; Pei, D. Proprotein convertase furin interacts with and cleaves pro-ADAMTS4 (Aggrecanase-1) in the trans-Golgi network. J. Biol. Chem. 2004, 279, 15434–15440.
Gao, G.; Plaas, A.; Thompson, V.P.; Jin, S.; Zuo, F.; Sandy, J.D. ADAMTS4 (aggrecanase-1) activation on the cell surface involves C-terminal cleavage by glycosylphosphatidyl inositol-anchored membrane type 4-matrix metalloproteinase and binding of the activated proteinase to chondroitin sulfate and heparan sulfate on syndecan-1. J. Biol. Chem. 2004, 279, 10042–10051.
[128]
Boerboom, D.; Lafond, J.-F.; Zheng, X.; Lapointe, E.; Mittaz, L.; Boyer, A.; Pritchard, M.; DeMayo, F.; Mort, J.; Drolet, R.; et al. Partially redundant functions of Adamts1 and Adamts4 in the perinatal development of the renal medulla. Dev. Dyn. 2011, 240, 1806–1814.
[129]
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.
[130]
Hashimoto, G.; Aoki, T.; Nakamura, H.; Tanzawa, K.; Okada, Y. Inhibition of ADAMTS4 (aggrecanase-1) by tissue inhibitors of metalloproteinases (TIMP-1, 2, 3 and 4). FEBS Lett. 2001, 494, 192–195, doi:10.1016/S0014-5793(01)02323-7.
[131]
Wayne, G.; Deng, S.-J.; Amour, A.; Borman, S.; Matico, R.; Carter, H.; Murphy, G. TIMP-3 inhibition of ADAMTS-4 (Aggrecanase-1) is modulated by interactions between aggrecan and the C-terminal domain of ADAMTS-4. J. Biol. Chem. 2007, 282, 20991–20998.
[132]
Pratta, M.A.; Scherle, P.A.; Yang, G.; Liu, R.Q.; Newton, R.C. Induction of aggrecanase 1 (ADAM-TS4) by interleukin-1 occurs through activation of constitutively produced protein. Arthritis Rheum. 2003, 48, 119–133.
Thirunavukkarasu, K.; Pei, Y.; Moore, T.; Wang, H.; Yu, X.-P.; Geiser, A.; Chandrasekhar, S. Regulation of the human ADAMTS-4 promoter by transcription factors and cytokines. Biochem. Biophys. Res. Commun. 2006, 345, 197–204, doi:10.1016/j.bbrc.2006.04.023.
[135]
W？gs？ter, D.; Bj？rk, H.; Zhu, C.; Bj？rkegren, J.; Valen, G.; Hamsten, A.; Eriksson, P. ADAMTS-4 and -8 are inflammatory regulated enzymes expressed in macrophage-rich areas of human atherosclerotic plaques. Atherosclerosis 2008, 196, 514–522, doi:10.1016/j.atherosclerosis.2007.05.018.
[136]
Wainwright, S.; Bondeson, J.; Hughes, C. An alternative spliced transcript of ADAMTS4 is present in human synovium from OA patients. Matrix Biol. 2006, 25, 317–320.
[137]
Richards, J.; Hernandez-Gonzalez, I.; Gonzalez-Robayna, I.; Teuling, E.; Lo, Y.; Boerboom, D.; Falender, A.; Doyle, K.; LeBaron, R.; Thompson, V.; 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, doi:10.1095/biolreprod.104.038083.
[138]
Hamel, M.; Ajmo, J.; Leonardo, C.; Zuo, F.; Sandy, J.; Gottschall, P. Multimodal signaling by the ADAMTSs (a disintegrin and metalloproteinase with thrombospondin motifs) promotes neurite extension. Exp. Neurol. 2008, 210, 428–440.
[139]
Tauchi, R.; Imagama, S.; Natori, T.; Ohgomori, T.; Muramoto, A.; Shinjo, R.; Matsuyama, Y.; Ishiguro, N.; Kadomatsu, K. The endogenous proteoglycan-degrading enzyme ADAMTS-4 promotes functional recovery after spinal cord injury. J. Neuroinflammation 2012, 9, 53.
[140]
Tortorella, M.D.; Malfait, A.M.; Deccico, C.; Arner, E. The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation. Osteoarthr. Cartil. 2001, 9, 539–552.
[141]
Tortorella, M.; Pratta, M.; Liu, R.; Austin, J.; Ross, O.; Abbaszade, I.; Burn, T.; Arner, E. Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4). J. Biol. Chem. 2000, 275, 18566–18573.
[142]
Nagase, H.; Kashiwagi, M. Aggrecanases and cartilage matrix degradation. Arthritis Res. Ther. 2003, 5, 94–103.
[143]
Iruela-Arispe, M.L.; Vazquez, F.; Ortega, M.A. Antiangiogenic domains shared by thrombospondins and metallospondins, a new family of angiogenic inhibitors. Ann. NY Acad. Sci. 1999, 886, 58–66.
[144]
Kahn, J.; Mehraban, F.; Ingle, G.; Xin, X.; Bryant, J.; Vehar, G.; Schoenfeld, J.; Grimaldi, C.; Peale, F.; Draksharapu, A.; et al. Gene expression profiling in an in vitro model of angiogenesis. Am. J. Pathol. 2000, 156, 1887–1900.
[145]
Kintakas, C.; McCulloch, D. Emerging roles for ADAMTS5 during development and disease. Matrix Biol. 2011, 30, 311–318.
[146]
Fosang, A.; Rogerson, F.; East, C.J.; Stanton, H. ADAMTS-5: The story so far. Eur. Cell Mater. 2008, 15, 11–26.
[147]
Mosyak, L.; Georgiadis, K.; Shane, T.; Svenson, K.; Hebert, T.; McDonagh, T.; Mackie, S.; Olland, S.; Lin, L.; Zhong, X.; et al. Crystal structures of the two major aggrecan degrading enzymes, ADAMTS4 and ADAMTS5. Protein Sci. 2008, 17, 16–37, doi:10.1110/ps.073287008.
[148]
Shieh, H.-S.; Mathis, K.; Williams, J.; Hills, R.; Wiese, J.; Benson, T.; Kiefer, J.; Marino, M.; Carroll, J.; Leone, J.; et al. High resolution crystal structure of the catalytic domain of ADAMTS-5 (aggrecanase-2). J. Biol. Chem. 2008, 283, 1501–1508.
[149]
Maingot, L.; Leroux, F.; Landry, V.; Dumont, J.; Nagase, H.; Villoutreix, B.; Sperandio, O.; Deprez-Poulain, R.; Deprez, B. New non-hydroxamic ADAMTS-5 inhibitors based on the 1,2,4-triazole-3-thiol scaffold. Bioorg. Med. Chem. Lett. 2010, 20, 6213–6219.
[150]
Longpré, J.-M.; Leduc, R. Identification of prodomain determinants involved in ADAMTS-1 biosynthesis. J. Biol. Chem. 2004, 279, 33237–33282.
[151]
Koo, B.-H.; Longpré, J.-M.; Somerville, R.; Alexander, J.; Leduc, R.; Apte, S. Cell-surface processing of pro-ADAMTS9 by furin. J. Biol. Chem. 2006, 281, 12485–12494.
[152]
Zeng, W.; Corcoran, C.; Collins-Racie, L.; Lavallie, E.; Morris, E.; Flannery, C. Glycosaminoglycan-binding properties and aggrecanase activities of truncated ADAMTSs: Comparative analyses with ADAMTS-5, -9, -16 and -18. Biochim. Biophys. Acta 2006, 1760, 517–541, doi:10.1016/j.bbagen.2006.01.013.
[153]
Gendron, C.; Kashiwagi, M.; Lim, N.; Enghild, J.; Th？gersen, I.; Hughes, C.; Caterson, B.; Nagase, H. Proteolytic activities of human ADAMTS-5: Comparative studies with ADAMTS-4. J. Biol. Chem. 2007, 282, 18294–18600.
[154]
McCulloch, D.; Le Goff, C.; Bhatt, S.; Dixon, L.; Sandy, J.; Apte, S. Adamts5, the gene encoding a proteoglycan-degrading metalloprotease, is expressed by specific cell lineages during mouse embryonic development and in adult tissues. Gene Expr. Patterns 2009, 9, 314–337, doi:10.1016/j.gep.2009.02.006.
[155]
Fosang, A.; Rogerson, F. Identifying the human aggrecanase. Osteoarthr. Cartil. 2010, 18, 1109–1116.
[156]
Koshy, P.; Lundy, C.; Rowan, A.; Porter, S.; Edwards, D.; Hogan, A.; Clark, I.; Cawston, T. The modulation of matrix metalloproteinase and ADAM gene expression in human chondrocytes by interleukin-1 and oncostatin M: A time-course study using real-time quantitative reverse transcription-polymerase chain reaction. Arthritis Rheum. 2002, 46, 961–967.
[157]
Cortial, D.; Gouttenoire, J.; Rousseau, C.; Ronzière, M.C.; Piccardi, N.; Msika, P.; Herbage, D.; Mallein-Gerin, F.; Freyria, A.M. Activation by IL-1 of bovine articular chondrocytes in culture within a 3D collagen-based scaffold. An in vitro model to address the effect of compounds with therapeutic potential in osteoarthritis. Osteoarthr. Cartil. 2006, 14, 631–640.
[158]
Arai, M.; Anderson, D.; Kurdi, Y.; Annis-Freeman, B.; Shields, K.; Collins-Racie, L.; Corcoran, C.; DiBlasio-Smith, E.; Pittman, D.; Dorner, A.; et al. Effect of adenovirus-mediated overexpression of bovine ADAMTS-4 and human ADAMTS-5 in primary bovine articular chondrocyte pellet culture system. Osteoarthr. Cartil. 2004, 12, 599–613.
[159]
Bondeson, J.; Lauder, S.; Wainwright, S.; Amos, N.; Evans, A.; Hughes, C.; Feldmann, M.; Caterson, B. Adenoviral gene transfer of the endogenous inhibitor IkappaBalpha into human osteoarthritis synovial fibroblasts demonstrates that several matrix metalloproteinases and aggrecanases are nuclear factor-kappaB-dependent. J. Rheumatol. 2007, 34, 523–533.
[160]
Moulharat, N.; Lesur, C.; Thomas, M.; Rolland-Valognes, G.; Pastoureau, P.; Anract, P.; de Ceuninck, F.; Sabatini, M. Effects of transforming growth factor-beta on aggrecanase production and proteoglycan degradation by human chondrocytes in vitro. Osteoarthr. Cartil. 2004, 12, 296–305.
[161]
Yamanishi, Y.; Boyle, D.; Clark, M.; Maki, R.; Tortorella, M.; Arner, E.; Firestein, G. Expression and regulation of aggrecanase in arthritis: The role of TGF-beta. J. Immunol. 2002, 168, 1405–1412.
[162]
Didangelos, A.; Mayr, U.; Monaco, C.; Mayr, M. Novel role of ADAMTS-5 protein in proteoglycan turnover and lipoprotein retention in atherosclerosis. J. Biol. Chem. 2012, 287, 19341–19346.
[163]
Chia, S.-L.; Sawaji, Y.; Burleigh, A.; McLean, C.; Inglis, J.; Saklatvala, J.; Vincent, T. Fibroblast growth factor 2 is an intrinsic chondroprotective agent that suppresses ADAMTS-5 and delays cartilage degradation in murine osteoarthritis. Arthritis Rheum. 2009, 60, 2019–2027.
[164]
Yamamoto, K.; Troeberg, L.; Scilabra, S.; Pelosi, M.; Murphy, C.; Strickland, D.; Nagase, H. LRP-1-mediated endocytosis regulates extracellular activity of ADAMTS-5 in articular cartilage. FASEB J. 2012, doi:10.1096/fj.12-216671.
[165]
Hattori, N.; Carrino, D.; Lauer, M.; Vasanji, A.; Wylie, J.; Nelson, C.; Apte, S. Pericellular versican regulates the fibroblast-myofibroblast transition: A role for ADAMTS5 protease-mediated proteolysis. J. Biol. Chem. 2011, 286, 34298–34310.
[166]
Nissinen, L.; K？h？ri, V.-M. ADAMTS5: A New Player in the Vascular Field. Am. J. Pathol. 2012, 181, 743–745, doi:10.1016/j.ajpath.2012.07.002.
[167]
Frischknecht, R.; Seidenbecher, C. Brevican: A key proteoglycan in the perisynaptic extracellular matrix of the brain. Int. J. Biochem. Cell Biol. 2012, 44, 1051–1054.
[168]
Georgiadis, K.; Hirohata, S.; Seldin, M.; Apte, S. ADAM-TS8, a novel metalloprotease of the ADAM-TS family located on mouse chromosome 9 and human chromosome 11. Genomics 1999, 62, 312–315.
[169]
Porter, S.; Span, P.; Sweep, F.; Tjan-Heijnen, V.; Pennington, C.; Pedersen, T.; Johnsen, M.; Lund, L.; R？mer, J.; Edwards, D. ADAMTS8 and ADAMTS15 expression predicts survival in human breast carcinoma. Int. J. Cancer 2006, 118, 1241–1247.
[170]
Clark, M.; Kelner, G.; Turbeville, L.; Boyer, A.; Arden, K.; Maki, R. ADAMTS9, a novel member of the ADAM-TS/ metallospondin gene family. Genomics 2000, 67, 343–350.
[171]
Blelloch, R.; Kimble, J. Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans. Nature 1999, 399, 586–590.
[172]
Jungers, K.; Le Goff, C.; Somerville, R.; Apte, S. Adamts9 is widely expressed during mouse embryo development. Gene Expr. Patterns 2005, 5, 609–617, doi:10.1016/j.modgep.2005.03.004.
[173]
Demircan, K.; Hirohata, S.; Nishida, K.; Hatipoglu, O.; Oohashi, T.; Yonezawa, T.; Apte, S.; Ninomiya, Y. ADAMTS-9 is synergistically induced by interleukin-1beta and tumor necrosis factor alpha in OUMS-27 chondrosarcoma cells and in human chondrocytes. Arthritis Rheum. 2005, 52, 1451–1460.
[174]
Yaykasli, K.; Oohashi, T.; Hirohata, S.; Hatipoglu, O.; Inagawa, K.; Demircan, K.; Ninomiya, Y. ADAMTS9 activation by interleukin 1 beta via NFATc1 in OUMS-27 chondrosarcoma cells and in human chondrocytes. Mol. Cell. Biochem. 2009, 323, 69–79, doi:10.1007/s11010-008-9965-4.
[175]
Bevitt, D.; Mohamed, J.; Catterall, J.; Li, Z.; Arris, C.; Hiscott, P.; Sheridan, C.; Langton, K.; Barker, M.; Clarke, M.; McKie, N. Expression of ADAMTS metalloproteinases in the retinal pigment epithelium derived cell line ARPE-19: Transcriptional regulation by TNFalpha. Biochim. Biophys. Acta 2003, 1626, 83–91.
[176]
Silver, D.; Hou, L.; Somerville, R.; Young, M.; Apte, S.; Pavan, W. The secreted metalloprotease ADAMTS20 is required for melanoblast survival. PLoS Genet. 2008, 4, e1000003.
[177]
Coughlan, T.; Crawford, A.; Goldring, M.; Hatton, P.; Barker, M. Lentiviral shRNA knock-down of ADAMTS-5 and -9 restores matrix deposition in 3D chondrocyte culture. J. Tissue Eng. Regen. Med. 2010, 4, 611–618, doi:10.1002/term.275.
[178]
Cal, S.; Arguelles, J.; Fernandez, P.; López-Otín, C. Identification, characterization, and intracellular processing of ADAM-TS12, a novel human disintegrin with a complex structural organization involving multiple thrombospondin-1 repeats. J. Biol. Chem. 2001, 276, 17932–17940.
[179]
Beristain, A.; Zhu, H.; Leung, P. Regulated expression of ADAMTS-12 in human trophoblastic cells: A role for ADAMTS-12 in epithelial cell invasion? PLoS One 2011, 6, e18473, doi:10.1371/journal.pone.0018473.
[180]
Tseng, S.; Reddi, A.; di Cesare, P. Cartilage Oligomeric Matrix Protein (COMP): A Biomarker of Arthritis. Biomark. Insights 2009, 4, 33–44.
[181]
Luan, Y.; Kong, L.; Howell, D.; Ilalov, K.; Fajardo, M.; Bai, X.H.; di Cesare, P.; Goldring, M.; Abramson, S.; Liu, C.J. Inhibition of ADAMTS-7 and ADAMTS-12 degradation of cartilage oligomeric matrix protein by alpha-2-macroglobulin. Osteoarthr. Cartil. 2008, 16, 1413–1420.
[182]
Guo, F.; Lai, Y.; Tian, Q.; Lin, E.; Kong, L.; Liu, C. Granulin-epithelin precursor binds directly to ADAMTS-7 and ADAMTS-12 and inhibits their degradation of cartilage oligomeric matrix protein. Arthritis Rheum. 2010, 62, 2023–2036.
[183]
Denis, C.; Lenting, P. von Willebrand factor: At the crossroads of bleeding and thrombosis. Int. J. Hematol. 2012, 95, 353–361.
[184]
Levy, G.; Nichols, W.; Lian, E.; Foroud, T.; McClintick, J.; McGee, B.; Yang, A.; Siemieniak, D.; Stark, K.; Gruppo, R.; et al. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 2001, 413, 488–494.
[185]
Sadler, J. Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood 2008, 112, 11–18, doi:10.1182/blood-2008-02-078170.
[186]
Zheng, X.; Chung, D.; Takayama, T.; Majerus, E.; Sadler, J.; Fujikawa, K. Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura. J. Biol. Chem. 2001, 276, 41059–41063.
[187]
Shomron, N.; Hamasaki-Katagiri, N.; Hunt, R.; Hershko, K.; Pommier, E.; Geetha, S.; Blaisdell, A.; Dobkin, A.; Marple, A.; Roma, I.; et al. A splice variant of ADAMTS13 is expressed in human hepatic stellate cells and cancerous tissues. Thromb. Haemost. 2010, 104, 531–535, doi:10.1160/TH09-12-0860.
[188]
Majerus, E.; Anderson, P.; Sadler, J. Binding of ADAMTS13 to von Willebrand factor. J. Biol. Chem. 2005, 280, 21773–21778.
[189]
Gao, W.; Zhu, J.; Westfield, L.; Tuley, E.; Anderson, P.; Sadler, J. Rearranging Exosites in Noncatalytic Domains Can Redirect the Substrate Specificity of ADAMTS Proteases. J. Biol. Chem. 2012, 287, 26944–26952.
[190]
Gerritsen, H.; Robles, R.; L？mmle, B.; Furlan, M. Partial amino acid sequence of purified von Willebrand factor-cleaving protease. Blood 2001, 98, 1654–1661.
[191]
Uemura, M.; Tatsumi, K.; Matsumoto, M.; Fujimoto, M.; Matsuyama, T.; Ishikawa, M.; Iwamoto, T.-A.; Mori, T.; Wanaka, A.; Fukui, H.; et al. Localization of ADAMTS13 to the stellate cells of human liver. Blood 2005, 106, 922–924.
[192]
Zhou, W.; Inada, M.; Lee, T.-P.; Benten, D.; Lyubsky, S.; Bouhassira, E.; Gupta, S.; Tsai, H.-M. ADAMTS13 is expressed in hepatic stellate cells. Lab. Invest. 2005, 85, 780–788.
[193]
Plaimauer, B.; Zimmermann, K.; V？lkel, D.; Antoine, G.; Kerschbaumer, R.; Jenab, P.; Furlan, M.; Gerritsen, H.; L？mmle, B.; Schwarz, H.; et al. Cloning, expression, and functional characterization of the von Willebrand factor-cleaving protease (ADAMTS13). Blood 2002, 100, 3626–3632, doi:10.1182/blood-2002-05-1397.
Tauchi, R.; Imagama, S.; Ohgomori, T.; Natori, T.; Shinjo, R.; Ishiguro, N.; Kadomatsu, K. ADAMTS-13 is produced by glial cells and upregulated after spinal cord injury. Neurosci. Lett. 2012, 517, 1–6.
[196]
Turner, N.; Nolasco, L.; Tao, Z.; Dong, J.F.; Moake, J. Human endothelial cells synthesize and release ADAMTS‐13. J. Thromb. Haemost. 2006, 4, 1396–1404.
[197]
Ruggeri, Z. The role of von Willebrand factor in thrombus formation. Thromb. Res. 2007, 120, 9.
[198]
De Meyer, S.; Savchenko, A.; Haas, M.; Schatzberg, D.; Carroll, M.; Schiviz, A.; Dietrich, B.; Rottensteiner, H.; Scheiflinger, F.; Wagner, D. Protective anti-inflammatory effect of ADAMTS13 on myocardial ischemia/reperfusion injury in mice. Blood 2012. PMID:22915644.
[199]
Gandhi, C.; Motto, D.; Jensen, M.; Lentz, S.; Chauhan, A. ADAMTS13 deficiency exacerbates VWF-dependent acute myocardial ischemia/reperfusion injury in mice. Blood 2012, doi:10.1182/blood-2012-06-440255.
Cal, S.; Obaya, A.; Llamazares, M.; Garabaya, C.; Quesada, V.; López-Otín, C. Cloning, expression analysis, and structural characterization of seven novel human ADAMTSs, a family of metalloproteinases with disintegrin and thrombospondin-1 domains. Gene 2002, 283, 49–62.
[202]
Molokwu, C.; Adeniji, O.; Chandrasekharan, S.; Hamdy, F.; Buttle, D. Androgen regulates ADAMTS15 gene expression in prostate cancer cells. Cancer Invest. 2010, 28, 698–710.
[203]
Sjoblom, T.; Jones, S.; Wood, L.D.; Parsons, D.W.; Lin, J.; Barber, T.D.; Mandelker, D.; Leary, R.J.; Ptak, J.; Silliman, N.; et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006, 314, 268–274, doi:10.1126/science.1133427.
[204]
Wagstaff, L.; Kelwick, R.; Decock, J.; Pennington, C.; Jaworski, D.; Edwards, D. ADAMTS15 Metalloproteinase Inhibits Breast Cacer Cell Migration. Breast Cancer Res. 2010, 12, P15.
[205]
Jin, H.; Wang, X.; Ying, J.; Wong, A.; Li, H.; Lee, K.; Srivastava, G.; Chan, A.; Yeo, W.; Ma, B.; et al. Epigenetic identification of ADAMTS18 as a novel 16q23.1 tumor suppressor frequently silenced in esophageal, nasopharyngeal and multiple other carcinomas. Oncogene 2007, 26, 7490–7498.
[206]
Wang, J.; Zhang, W.; Yi, Z.; Wang, S.; Li, Z. Identification of a thrombin cleavage site and a short form of ADAMTS-18. Biochem. Biophys. Res. Commun. 2012, 419, 692–697.
[207]
Li, Z.; Nardi, M.A.; Li, Y.S.; Zhang, W.; Pan, R.; Dang, S.; Yee, H.; Quartermain, D.; Jonas, S.; Karpatkin, S. C-terminal ADAMTS-18 fragment induces oxidative platelet fragmentation, dissolves platelet aggregates, and protects against carotid artery occlusion and cerebral stroke. Blood 2009, 113, 6051–6060, doi:10.1182/blood-2008-07-170571.
[208]
Aldahmesh, M.A.; Khan, A.O.; Mohamed, J.Y.; Alkuraya, H.; Ahmed, H.; Bobis, S.; Al-Mesfer, S.; Alkuraya, F.S. Identification of ADAMTS18 as a gene mutated in Knobloch syndrome. J. Med. Genet. 2011, 48, 597–601.
[209]
Balsara, B.; Pei, J.; de Rienzo, A.; Simon, D.; Tosolini, A.; Lu, Y.; Shen, F.; Fan, X.; Lin, W.; Buetow, K.; et al. Human hepatocellular carcinoma is characterized by a highly consistent pattern of genomic imbalances, including frequent loss of 16q23.1-24.1. Genes Chromosomes Cancer 2001, 30, 245–253, doi:10.1002/1098-2264(2000)9999:9999<::AID-GCC1083>3.0.CO;2-M.
[210]
Lo, K.; Teo, P.; Hui, A.; To, K.; Tsang, Y.; Chan, S.; Mak, K.; Lee, J.; Huang, D. High resolution allelotype of microdissected primary nasopharyngeal carcinoma. Cancer Res. 2000, 60, 3348–3353.
[211]
Mori, Y.; Matsunaga, M.; Abe, T.; Fukushige, S.; Miura, K.; Sunamura, M.; Shiiba, K.; Sato, M.; Nukiwa, T.; Horii, A. Chromosome band 16q24 is frequently deleted in human gastric cancer. Br. J. Cancer 1999, 80, 556–562, doi:10.1038/sj.bjc.6690391.
[212]
Riegman, P.; Vissers, K.; Alers, J.; Geelen, E.; Hop, W.; Tilanus, H.; van Dekken, H. Genomic alterations in malignant transformation of Barrett’s esophagus. Cancer Res. 2001, 61, 3164–3170.
