Insights on ADAMTS proteases and ADAMTS-like proteins from mammalian genetics

Matrix Biology

Volumn 44-46, Issue , 2015, Pages 24-37

  Dubail, Johanne ^a   Apte, Suneel S ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

ADAMTS; ADAMTS like; Aggrecanase; Extracellular matrix; Forward genetics; Knockout; Metalloproteinase; Mouse; Procollagen; Reverse genetics

Indexed keywords

ADAMTS10 PROTEIN; ADAMTS17 PROTEIN; ADAMTS2 PROTEIN; ADAMTS3 PROTEIN; ADAMTSL2 PROTEIN; ADAMTSL4 PROTEIN; FIBRILLAR COLLAGEN; METALLOPROTEINASE; PROCOLLAGEN; PROTEINASE; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAM PROTEIN;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CONNECTIVE TISSUE DISEASE; DERMATOSPARAXIS; EMBRYO DEVELOPMENT; ENZYME STRUCTURE; ENZYME SUBSTRATE; GELEOPHYSIC DYSPLASIA; GENE INACTIVATION; GENE MUTATION; GENETIC DISORDER; GENETIC VARIABILITY; GENOMICS; HUMAN; MAMMALIAN GENETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RAT; REVIEW; WEILL MARCHESANI SYNDROME; ANIMAL; BOVINE; DOG; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MAMMAL; METABOLISM; MORPHOGENESIS; MULTIGENE FAMILY; MUTATION; TRANSGENIC ANIMAL;

ANIMALIA; BOVINAE; MAMMALIA; RODENTIA;

ADAM PROTEINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CATTLE; DOGS; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MAMMALS; MICE; MORPHOGENESIS; MULTIGENE FAMILY; MUTATION;

EID: 84930767729     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2015.03.001     Document Type: Review

References (150)

1. Colige A., Li S.W., Sieron A.L., Nusgens B.V., Prockop D.J., Lapiere C.M. 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 U S A 1997, 94:2374-2379.
2. Hurskainen T.L., Hirohata S., Seldin M.F., Apte S.S. ADAM-TS5, ADAM-TS6, and ADAM-TS7, novel members of a new family of zinc metalloproteases. General features and genomic distribution of the ADAM-TS family. J Biol Chem 1999, 274:25555-25563.
3. 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, 272:556-562.
4. Hirohata S., Wang L.W., Miyagi M., Yan L., Seldin M.F., Keene D.R., et al. Punctin, a novel ADAMTS-like molecule (ADAMTSL-1) in extracellular matrix. J Biol Chem 2002, 22:22.
5. Kramerova I.A., Kawaguchi N., Fessler L.I., Nelson R.E., Chen Y., Kramerov A.A., et al. Papilin in development; a pericellular protein with a homology to the ADAMTS metalloproteinases. Development 2000, 127:5475-5485.
6. Apte S.S. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem 2009, 284:31493-31497.
7. Abbaszade I., Liu R.Q., Yang F., Rosenfeld S.A., Ross O.H., Link J.R., et al. Cloning and characterization of ADAMTS11, an aggrecanase from the ADAMTS family. J Biol Chem 1999, 274:23443-23450.
8. Huxley-Jones J., Apte S.S., Robertson D.L., Boot-Handford R.P. The characterisation of six ADAMTS proteases in the basal chordate Ciona intestinalis provides new insights into the vertebrate ADAMTS family. Int J Biochem Cell Biol 2005, 37:1838-1845.
9. Nandadasa S., Foulcer S., Apte S.S. The multiple, complex roles of versican and its proteolytic turnover by ADAMTS proteases during embryogenesis. Matrix Biol 2014, 35:34-41.
10. Hubmacher D., Apte S.S. Genetic and functional linkage between ADAMTS superfamily proteins and fibrillin-1: a novel mechanism influencing microfibril assembly and function. Cell Mol Life Sci 2011, 68:3137-3148.
11. Zheng X., Majerus E.M., Sadler J.E. ADAMTS13 and TTP. Curr Opin Hematol 2002, 9:389-394.
12. Gross J., Lapiere C.M. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci U S A 1962, 48:1014-1022.
13. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 2005, 6:32-43.
14. Balbin M., Fueyo A., Knauper V., Lopez J.M., Alvarez J., Sanchez L.M., et al. Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J Biol Chem 2001, 276:10253-10262.
15. Schlondorff J., Blobel C.P. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J Cell Sci 1999, 112:3603-3617.
16. Sahin U., Weskamp G., Zheng Y., Chesneau V., Horiuchi K., Blobel C.P. A sensitive method to monitor ectodomain shedding of ligands of the epidermal growth factor receptor. Methods Mol Biol 2006, 327:99-113.
17. Foulcer S.J., Nelson C.M., Quintero M.V., Kuberan B., Larkin J., Dours-Zimmermann M.T., et al. Determinants of versican-V1 proteoglycan processing by the metalloproteinase ADAMTS5. J Biol Chem 2014, 289:27859-27873.
18. Gao W., Anderson P.J., Majerus E.M., Tuley E.A., Sadler J.E. Exosite interactions contribute to tension-induced cleavage of von Willebrand factor by the antithrombotic ADAMTS13 metalloprotease. Proc Natl Acad Sci U S A 2006, 103:19099-19104.
19. Gao W., Zhu J., Westfield L.A., Tuley E.A., Anderson P.J., Sadler J.E. Rearranging exosites in noncatalytic domains can redirect the substrate specificity of ADAMTS proteases. J Biol Chem 2012, 287:26944-26952.
20. Kashiwagi M., Enghild J.J., Gendron C., Hughes C., Caterson B., Itoh Y., et al. Altered proteolytic activities of ADAMTS-4 expressed by C-terminal processing. J Biol Chem 2004, 279:10109-10119.
21. 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.
22. Zheng X.L. Structure-function and regulation of ADAMTS-13 protease. J Thromb Haemost 2013, 11(Suppl. 1):11-23.
23. Goldstein J.L., Dana S.E., Brunschede G.Y., Brown M.S. Genetic heterogeneity in familial hypercholesterolemia: evidence for two different mutations affecting functions of low-density lipoprotein receptor. Proc Natl Acad Sci U S A 1975, 72:1092-1096.
24. Pendas A.M., Matilla T., Estivill X., Lopez-Otin C. The human collagenase-3 (CLG3) gene is located on chromosome 11q22.3 clustered to other members of the matrix metalloproteinase gene family. Genomics 1995, 26:615-618.
25. Koo B.H., Le Goff C., Jungers K.A., Vasanji A., O'Flaherty J., Weyman C.M., et al. ADAMTS-like 2 (ADAMTSL2) is a secreted glycoprotein that is widely expressed during mouse embryogenesis and is regulated during skeletal myogenesis. Matrix Biol 2007, 26:431-441.
26. Le Goff C., Morice-Picard F., Dagoneau N., Wang L.W., Perrot C., Crow Y.J., et al. ADAMTSL2 mutations in geleophysic dysplasia demonstrate a role for ADAMTS-like proteins in TGF-beta bioavailability regulation. Nat Genet 2008, 40:1119-1123.
27. Mosyak L., Georgiadis K., Shane T., Svenson K., Hebert T., McDonagh T., et al. Crystal structures of the two major aggrecan degrading enzymes, ADAMTS4 and ADAMTS5. Protein Sci 2008, 17:16-21.
28. Shieh H.S., Mathis K.J., Williams J.M., Hills R.L., Wiese J.F., Benson T.E., et al. High resolution crystal structure of the catalytic domain of ADAMTS-5 (aggrecanase-2). J Biol Chem 2008, 283:1501-1507.
29. Koo B.H., Longpre J.M., Somerville R.P., Alexander J.P., Leduc R., Apte S.S. Regulation of ADAMST9 secretion and enzymatic activity by its propeptide. J Biol Chem 2007, 282:16146-16154.
30. Majerus E.M., Zheng X., Tuley E.A., Sadler J.E. Cleavage of the ADAMTS13 propeptide is not required for protease activity. J Biol Chem 2003, 278:46643-46648.
31. Koo B.H., Longpre J.M., Somerville R.P., Alexander J.P., Leduc R., Apte S.S. Cell-surface processing of pro-ADAMTS9 by furin. J Biol Chem 2006, 281:12485-12494.
32. Longpre J.M., Leduc R. Identification of prodomain determinants involved in ADAMTS-1 biosynthesis. J Biol Chem 2004, 279:33237-33245.
33. Longpre J.M., McCulloch D.R., Koo B.H., Alexander J.P., Apte S.S., Leduc R. Characterization of proADAMTS5 processing by proprotein convertases. Int J Biochem Cell Biol 2009, 41:1116-1126.
34. Somerville R.P., Jungers K.A., Apte S.S. ADAMTS10: discovery and characterization of a novel, widely expressed metalloprotease and its proteolytic activation. J Biol Chem 2004, 279:51208-51217.
35. Somerville R.P., Longpre J.M., Apel E.D., Lewis R.M., Wang L.W., Sanes J.R., et al. ADAMTS7B, the full-length product of the ADAMTS7 gene, is a chondroitin sulfate proteoglycan containing a mucin domain. J Biol Chem 2004, 279:35159-35175.
36. Somerville R.P., Longpre J.M., Jungers K.A., Engle J.M., Ross M., Evanko S., et al. 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.
37. Tortorella M.D., Arner E.C., Hills R., Gormley J., Fok K., Pegg L., et al. ADAMTS-4 (aggrecanase-1): N-terminal activation mechanisms. Arch Biochem Biophys 2005, 444:34-44.
38. Koo B.H., Apte S.S. Cell-surface processing of the metalloprotease pro-ADAMTS9 is influenced by the chaperone GRP94/gp96. J Biol Chem 2010, 285:197-205.
39. Ricketts L.M., Dlugosz M., Luther K.B., Haltiwanger R.S., Majerus E.M. O-fucosylation is required for ADAMTS13 secretion. J Biol Chem 2007, 282:17014-17023.
40. Wang L.W., Dlugosz M., Somerville R.P., Raed M., Haltiwanger R.S., Apte S.S. O-fucosylation of thrombospondin type 1 repeats in ADAMTS-like-1/punctin-1 regulates secretion: implications for the ADAMTS superfamily. J Biol Chem 2007, 282:17024-17031.
41. Wang L.W., Leonhard-Melief C., Haltiwanger R.S., Apte S.S. Post-translational modification of thrombospondin type-1 repeats in ADAMTS-like 1/punctin-1 by C-mannosylation of tryptophan. J Biol Chem 2009, 284:30004-30015.
42. Kozma K., Keusch J.J., Hegemann B., Luther K.B., Klein D., Hess D., et al. Identification and characterization of abeta1,3-glucosyltransferase that synthesizes the Glc-beta1,3-Fuc disaccharide on thrombospondin type 1 repeats. J Biol Chem 2006, 281:36742-36751.
43. Luo Y., Koles K., Vorndam W., Haltiwanger R.S., Panin V.M. Protein O-fucosyltransferase 2 adds O-fucose to thrombospondin type 1 repeats. J Biol Chem 2006, 281:9393-9399.
44. Wang W.M., Ge G., Lim N.H., Nagase H., Greenspan D.S. TIMP-3 inhibits the procollagen N-proteinase ADAMTS-2. Biochem J 2006, 398:515-519.
45. 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.
46. Tortorella M.D., Arner E.C., Hills R., Easton A., Korte-Sarfaty J., Fok K., et al. Alpha2-macroglobulin is a novel substrate for ADAMTS-4 and ADAMTS-5 and represents an endogenous inhibitor of these enzymes. J Biol Chem 2004, 279:17554-17561.
47. Li Z., Nardi M.A., Li Y.S., Zhang W., Pan R., Dang S., et al. 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.
48. Troeberg L., Mulloy B., Ghosh P., Lee M.H., Murphy G., Nagase H. Pentosan polysulfate increases affinity between ADAMTS-5 and TIMP-3 through formation of an electrostatically driven trimolecular complex. Biochem J 2012, 443:307-315.
49. Yamamoto K., Owen K., Parker A.E., Scilabra S.D., Dudhia J., Strickland D.K., et al. Low density lipoprotein receptor-related protein 1 (LRP1)-mediated endocytic clearance of a disintegrin and metalloproteinase with thrombospondin motifs-4 (ADAMTS-4): functional differences of non-catalytic domains of ADAMTS-4 and ADAMTS-5 in LRP1 binding. J Biol Chem 2014, 289:6462-6474.
50. Yamamoto K., Troeberg L., Scilabra S.D., Pelosi M., Murphy C.L., Strickland D.K., et al. LRP-1-mediated endocytosis regulates extracellular activity of ADAMTS-5 in articular cartilage. FASEB J 2013, 27:511-521.
51. Jeltsch M., Jha S.K., Tvorogov D., Anisimov A., Leppanen V.M., Holopainen T., et al. CCBE1 enhances lymphangiogenesis via A disintegrin and metalloprotease with thrombospondin motifs-3-mediated vascular endothelial growth factor-C activation. Circulation 2014, 129:1962-1971.
52. Counts D.F., Byers P.H., Holbrook K.A., Hegreberg G.A. Dermatosparaxis in a Himalayan cat: I. Biochemical studies of dermal collagen. J Invest Dermatol 1980, 74:96-99.
53. Hanset R., Lapiere C.M. Inheritance of dermatosparaxis in the calf. A genetic defect of connective tissues. J Hered 1974, 65:356-358.
54. Ramshaw J.A., Peters D.E., Jones L.N., Badman R.T., Brodsky B.B. Ovine dermatosparaxis. Aust Vet J 1983, 60:149-151.
55. Lapiere C.M., Lenaers A., Kohn L.D. Procollagen peptidase: an enzyme excising the coordination peptides of procollagen. Proc Natl Acad Sci U S A 1971, 68:3054-3058.
56. Nusgens B.V., Verellen-Dumoulin C., Hermanns-Le T., De Paepe A., Nuytinck L., Pierard G.E., et al. Evidence for a relationship between Ehlers-Danlos type VII C in humans and bovine dermatosparaxis. Nat Genet 1992, 1:214-217.
57. Colige A., Sieron A.L., Li S.W., Schwarze U., Petty E., Wertelecki 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.
58. Colige A., Ruggiero F., Vandenberghe I., Dubail J., Kesteloot F., Van Beeumen J., et al. Domains and maturation processes that regulate the activity of ADAMTS-2, a metalloproteinase cleaving the aminopropeptide of fibrillar procollagens type I, II, III and V. J Biol Chem 2005, 280:34397-34408.
59. Colige A., Vandenberghe I., Thiry M., Lambert C.A., Van Beeumen J., Li S.W., et al. Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem 2002, 277:5756-5766.
60. Fernandes R.J., Hirohata S., Engle J.M., Colige A., Cohn D.H., Eyre D.R., et al. Procollagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J Biol Chem 2001, 276:31502-31509.
61. Le Goff C., Somerville R.P., Kesteloot F., Powell K., Birk D.E., Colige A.C., et al. Regulation of procollagen amino-propeptide processing during mouse embryogenesis by specialization of homologous ADAMTS proteases: insights on collagen biosynthesis and dermatosparaxis. Development 2006, 133:1587-1596.
62. Dagoneau N., Benoist-Lasselin C., Huber C., Faivre L., Megarbane A., Alswaid A., et al. ADAMTS10 mutations in autosomal recessive Weill-Marchesani syndrome. Am J Hum Genet 2004, 75:801-806.
63. Faivre L., Gorlin R.J., Wirtz M.K., Godfrey M., Dagoneau N., Samples J.R., et al. In frame fibrillin-1 gene deletion in autosomal dominant Weill-Marchesani syndrome. J Med Genet 2003, 40:34-36.
64. Kutz W.E., Wang L.W., Bader H.L., Majors A.K., Iwata K., Traboulsi E.I., et al. ADAMTS10 protein interacts with fibrillin-1 and promotes its deposition in extracellular matrix of cultured fibroblasts. J Biol Chem 2011, 286:17156-17167.
65. Gabriel L.A., Wang L.W., Bader H., Ho J.C., Majors A.K., Hollyfield J.G., et al. ADAMTSL4, a secreted glycoprotein widely distributed in the eye, binds fibrillin-1 microfibrils and accelerates microfibril biogenesis. Invest Ophthalmol Vis Sci 2012, 53:461-469.
66. Tsutsui K., Manabe R.I., Yamada T., Nakano I., Oguri Y., Keene D.R., et al. A disintegrin and metalloproteinase with thrombospondin motifs-like-6 (ADAMTSL-6) is a novel extracellular matrix protein that binds to fibrillin-1 and promotes fibrillin-1 fibril formation. J Biol Chem 2010, 285:4870-4882.
67. Farias F.H., Johnson G.S., Taylor J.F., Giuliano E., Katz M.L., Sanders D.N., et al. An ADAMTS17 splice donor site mutation in dogs with primary lens luxation. Invest Ophthalmol Vis Sci 2010, 51:4716-4721.
68. Morales J., Al-Sharif L., Khalil D.S., Shinwari J.M., Bavi P., Al-Mahrouqi R.A., et al. Homozygous mutations in ADAMTS10 and ADAMTS17 cause lenticular myopia, ectopia lentis, glaucoma, spherophakia, and short stature. Am J Hum Genet 2009, 85:558-568.
69. Aragon-Martin J.A., Ahnood D., Charteris D.G., Saggar A., Nischal K.K., Comeglio P., et al. Role of ADAMTSL4 mutations in FBN1 mutation-negative ectopia lentis patients. Hum Mutat 2010, 31:E1622-E1631.
70. Chandra A., Aragon-Martin J.A., Hughes K., Gati S., Reddy M.A., Deshpande C., et al. A genotype-phenotype comparison of ADAMTSL4 and FBN1 in isolated ectopia lentis. Invest Ophthalmol Vis Sci 2012, 53:4889-4896.
71. Christensen A.E., Fiskerstrand T., Knappskog P.M., Boman H., Rodahl E. A novel ADAMTSL4 mutation in autosomal recessive ectopia lentis et pupillae. Invest Ophthalmol Vis Sci 2010, 51:6369-6373.
72. Chandra A., Jones M., Cottrill P., Eastlake K., Limb G.A., Charteris D.G. Gene expression and protein distribution of ADAMTSL-4 in human iris, choroid and retina. Br J Ophthalmol 2013, 97:1208-1212.
73. Chandra A., Aragon-Martin J.A., Sharif S., Parulekar M., Child A., Arno G. Craniosynostosis with ectopia lentis and a homozygous 20-base deletion in ADAMTSL4. Ophthalmic Genet 2013, 34:78-82.
74. Buchner D.A., Meisler M.H. TSRC1, a widely expressed gene containing seven thrombospondin type I repeats. Gene 2003, 307:23-30.
75. Cal S., Obaya A.J., Llamazares M., Garabaya C., Quesada V., Lopez-Otin 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.
76. Bader H.L., Ruhe A.L., Wang L.W., Wong A.K., Walsh K.F., Packer R.A., et al. An ADAMTSL2 founder mutation causes Musladin-Lueke syndrome, a heritable disorder of beagle dogs, featuring stiff skin and joint contractures. PLoS One 2010, 5:e12817.
77. Le Goff C., Mahaut C., Wang L.W., Allali S., Abhyankar A., Jensen S., et al. Mutations in the TGFbeta binding-protein-like domain 5 of FBN1 are responsible for acromicric and geleophysic dysplasias. Am J Hum Genet 2011, 89:7-14.
78. Shi Y., Tu Y., De Maria A., Mecham R.P., Bassnett S. Development, composition, and structural arrangements of the ciliary zonule of the mouse. Invest Ophthalmol Vis Sci 2013, 54:2504-2515.
79. Beene L.C., Wang L.W., Hubmacher D., Keene D.R., Reinhardt D.P., Annis D.S., et al. Nonselective assembly of fibrillin 1 and fibrillin 2 in the rodent ocular zonule and in cultured cells: implications for marfan syndrome. Invest Ophthalmol Vis Sci 2013, 54:8337-8344.
80. Zheng X.L. ADAMTS13 and von Willebrand factor in thrombotic thrombocytopenic purpura. Annu Rev Med 2015, 66:211-225.
81. Levy G.G., Nichols W.C., Lian E.C., Foroud T., McClintick J.N., McGee B.M., et al. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 2001, 413:488-494.
82. Aldahmesh M.A., Alshammari M.J., Khan A.O., Mohamed J.Y., Alhabib F.A., Alkuraya F.S. The syndrome of microcornea, myopic chorioretinal atrophy, and telecanthus (MMCAT) is caused by mutations in ADAMTS18. Hum Mutat 2013, 34:1195-1199.
83. Peluso I., Conte I., Testa F., Dharmalingam G., Pizzo M., Collin R.W., et al. The ADAMTS18 gene is responsible for autosomal recessive early onset severe retinal dystrophy. Orphanet J Rare Dis 2013, 8:16.
84. Rao C., Foernzler D., Loftus S.K., Liu S., McPherson J.D., Jungers K.A., et al. A defect in a novel ADAMTS family member is the cause of the belted white-spotting mutation. Development 2003, 130:4665-4672.
85. Silver D.L., Hou L., Somerville R., Young M.E., Apte S.S., Pavan W.J. The secreted metalloprotease ADAMTS20 is required for melanoblast survival. PLoS Genet 2008, 4:1-15.
86. Shindo T., Kurihara H., Kuno K., Yokoyama H., Wada T., Kurihara Y., et al. ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest 2000, 105:1345-1352.
87. Mittaz L., Russell D.L., Wilson T., Brasted M., Tkalcevic J., Salamonsen L.A., et al. Adamts-1 is essential for the development and function of the urogenital system. Biol Reprod 2004, 70:1096-1105.
88. Brown H.M., Dunning K.R., Robker R.L., Boerboom D., Pritchard M., Lane M., et al. ADAMTS1 cleavage of versican mediates essential structural remodeling of the ovarian follicle and cumulus-oocyte matrix during ovulation in mice. Biol Reprod 2010, 83:549-557.
89. Brown H.M., Dunning K.R., Robker R.L., Pritchard M., Russell D.L. Requirement for ADAMTS-1 in extracellular matrix remodeling during ovarian folliculogenesis and lymphangiogenesis. Dev Biol 2006, 300:699-709.
90. Russell D.L., Doyle K.M., Ochsner S.A., Sandy J.D., Richards J.S. Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J Biol Chem 2003, 278:42330-42339.
91. Stankunas K., Hang C.T., Tsun Z.Y., Chen H., Lee N.V., Wu J.I., et al. Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev Cell 2008, 14:298-311.
92. Fosang A.J., Little C.B. Drug insight: aggrecanases as therapeutic targets for osteoarthritis. Nat Clin Pract Rheumatol 2008, 4:420-427.
93. Gilbert A.M., Bursavich M.G., Lombardi S., Georgiadis K.E., Reifenberg E., Flannery C.R., et al. 5-((1H-pyrazol-4-yl)methylene)-2-thioxothiazolidin-4-one inhibitors of ADAMTS-5. Bioorg Med Chem Lett 2007, 17:1189-1192.
94. McCulloch D.R., Goff C.L., Bhatt S., Dixon L.J., Sandy J.D., Apte S.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, 9:314-323.
95. Dupuis L.E., McCulloch D.R., McGarity J.D., Bahan A., Wessels A., Weber D., et al. Altered versican cleavage in ADAMTS5 deficient mice; a novel etiology of myxomatous valve disease. Dev Biol 2011, 357:152-164.
96. Dupuis L.E., Osinska H., Weinstein M.B., Hinton R.B., Kern C.B. Insufficient versican cleavage and Smad2 phosphorylation results in bicuspid aortic and pulmonary valves. J Mol Cell Cardiol 2013, 60:50-59.
97. Dubail J., Aramaki-Hattori N., Bader H.L., Nelson C.M., Katebi N., Matuska B., et al. A new Adamts9 conditional mouse allele identifies its non-redundant role in interdigital web regression. Genesis 2014, 52:702-712.
98. Kern C.B., Wessels A., McGarity J., Dixon L.J., Alston E., Argraves W.S., et al. Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol 2010, 29:304-316.
99. Koo B.H., Coe D.M., Dixon L.J., Somerville R.P., Nelson C.M., Wang L.W., et al. ADAMTS9 is a cell-autonomously acting, anti-angiogenic metalloprotease expressed by microvascular endothelial cells. Am J Pathol 2010, 176:1494-1504.
100. Enomoto H., Nelson C., Somerville R.P.T., Mielke K., Dixon L., Powell K., et al. 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.
101. McCulloch D.R., Nelson C.M., Dixon L.J., Silver D.L., Wylie J.D., Lindner V., et al. ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev Cell 2009, 17:687-698.
102. Abdul-Majeed S., Mell B., Nauli S.M., Joe B. Cryptorchidism and infertility in rats with targeted disruption of the Adamts16 locus. PLoS One 2014, 9:e100967.
103. Gopalakrishnan K., Kumarasamy S., Abdul-Majeed S., Kalinoski A.L., Morgan E.E., Gohara A.F., et al. Targeted disruption of Adamts16 gene in a rat genetic model of hypertension. Proc Natl Acad Sci U S A 2012, 109:20555-20559.
104. Jacobi C.L., Rudigier L.J., Scholz H., Kirschner K.M. Transcriptional regulation by the Wilms tumor protein, Wt1, suggests a role of the metalloproteinase Adamts16 in murine genitourinary development. J Biol Chem 2013, 288:18811-18824.
105. Boesgaard T.W., Gjesing A.P., Grarup N., Rutanen J., Jansson P.A., Hribal M.L., et al. Variant near ADAMTS9 known to associate with type 2 diabetes is related to insulin resistance in offspring of type 2 diabetes patients-EUGENE2 study. PLoS One 2009, 4:e7236.
106. de Jong E.K., Breukink M.B., Schellevis R.L., Bakker B., Mohr J.K., Fauser S., et al. Chronic central serous chorioretinopathy is associated with genetic variants implicated in age-related macular degeneration. Ophthalmology 2014, 122:562-570.
107. Dong K., Yao N., Pu Y., He X., Zhao Q., Luan Y., et al. Genomic scan reveals loci under altitude adaptation in Tibetan and Dahe pigs. PLoS One 2014, 9:e110520.
108. Heid I.M., Jackson A.U., Randall J.C., Winkler T.W., Qi L., Steinthorsdottir V., et al. Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution. Nat Genet 2010, 42:949-960.
109. Helisalmi S., Immonen I., Losonczy G., Resch M.D., Benedek S., Balogh I., et al. ADAMTS9 locus associates with increased risk of wet AMD. Acta Ophthalmol 2014, 92:e410.
110. Zeggini E., Scott L.J., Saxena R., Voight B.F., Marchini J.L., Hu T., et al. Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 2008, 40:638-645.
111. Chaemsaithong P., Madan I., Romero R., Than N.G., Tarca A.L., Draghici S., et al. Characterization of the myometrial transcriptome in women with an arrest of dilatation during labor. J Perinat Med 2013, 41:665-681.
112. Pyun J.A., Kim S., Cho N.H., Koh I., Lee J.Y., Shin C., et al. Genome-wide association studies and epistaxis analyses of candidate genes related to age at menarche and age at natural menopause in a Korean population. Menopause 2014, 21:522-529.
113. Fritsche L.G., Chen W., Schu M., Yaspan B.L., Yu Y., Thorleifsson G., et al. Seven new loci associated with age-related macular degeneration. Nat Genet 2013, 45:433-439.
114. Padang R., Bagnall R.D., Tsoutsman T., Bannon P.G., Semsarian C. Comparative transcriptome profiling in human bicuspid aortic valve disease using RNA-sequencing. Physiol Genomics 2015, 47:75-87.
115. Arning A., Hiersche M., Witten A., Kurlemann G., Kurnik K., Manner D., et al. A genome-wide association study identifies a gene network of ADAMTS genes in the predisposition to pediatric stroke. Blood 2012, 120:5231-5236.
116. Weedon M.N., Lango H., Lindgren C.M., Wallace C., Evans D.M., Mangino M., et al. Genome-wide association analysis identifies 20 loci that influence adult height. Nat Genet 2008, 40:575-583.
117. Dow D.J., Huxley-Jones J., Hall J.M., Francks C., Maycox P.R., Kew J.N., et al. ADAMTSL3 as a candidate gene for schizophrenia: gene sequencing and ultra-high density association analysis by imputation. Schizophr Res 2011, 127:28-34.
118. Reilly M.P., Li M., He J., Ferguson J.F., Stylianou I.M., Mehta N.N., et al. Identification of ADAMTS7 as a novel locus for coronary atherosclerosis and association of ABO with myocardial infarction in the presence of coronary atherosclerosis: two genome-wide association studies. Lancet 2011, 377:383-392.
119. Pu X., Xiao Q., Kiechl S., Chan K., Ng F.L., Gor S., et al. ADAMTS7 cleavage and vascular smooth muscle cell migration is affected by a coronary-artery-disease-associated variant. Am J Hum Genet 2013, 92:366-374.
120. Rodriguez-Manzaneque J.C., Carpizo D., Plaza-Calonge Mdel C., Torres-Collado A.X., Thai S.N., Simons M., et al. Cleavage of syndecan-4 by ADAMTS1 provokes defects in adhesion. Int J Biochem Cell Biol 2009, 41:800-810.
121. Rodriguez-Manzaneque J.C., Westling J., Thai S.N., Luque A., Knauper V., Murphy G., et al. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors. Biochem Biophys Res Commun 2002, 293:501-508.
122. Torres-Collado A.X., Kisiel W., Iruela-Arispe M.L., Rodriguez-Manzaneque J.C. 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.
123. 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.
124. Canals F., Colome N., Ferrer C., Plaza-Calonge Mdel C., Rodriguez-Manzaneque J.C. Identification of substrates of the extracellular protease ADAMTS1 by DIGE proteomic analysis. Proteomics 2006, 6(Suppl. 1):S28-S35.
125. Lee N.V., Sato M., Annis D.S., Loo J.A., Wu L., Mosher D.F., et al. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J 2006, 25:5270-5283.
126. Lind T., Birch M.A., McKie N. Purification of an insect derived recombinant human ADAMTS-1 reveals novel gelatin (type I collagen) degrading activities. Mol Cell Biochem 2006, 281:95-102.
127. Sandy J.D., Westling J., Kenagy R.D., Iruela-Arispe M.L., Verscharen C., Rodriguez-Mazaneque J.C., et al. Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 2001, 276:13372-13378.
128. Stupka N., Kintakas C., White J.D., Fraser F.W., Hanciu M., Aramaki-Hattori N., et al. Versican processing by a disintegrin-like and metalloproteinase domain with thrombospondin-1 repeats proteinases-5 and -15 facilitates myoblast fusion. J Biol Chem 2013, 288:1907-1917.
129. Kessler T., Zhang L., Liu Z., Yin X., Huang Y., Wang Y., et al. ADAMTS-7 inhibits re-endothelialization of injured arteries and promotes vascular remodeling via cleavage of thrombospondin-1. Circulation 2015 Feb 20, [Epub ahead of print, pii: CIRCULATIONAHA.114.014072].
130. Wang L., Zheng J., Bai X., Liu B., Liu C.J., Xu Q., et al. ADAMTS-7 mediates vascular smooth muscle cell migration and neointima formation in balloon-injured rat arteries. Circ Res 2009, 104:688-698.
131. Little C.B., Meeker C.T., Golub S.B., Lawlor K.E., Farmer P.J., Smith S.M., et al. Blocking aggrecanase cleavage in the aggrecan interglobular domain abrogates cartilage erosion and promotes cartilage repair. J Clin Invest 2007, 117:1627-1636.
132. Yokoyama H., Wada T., Kobayashi K., Kuno K., Kurihara H., Shindo T., et al. A disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS)-1 null mutant mice develop renal lesions mimicking obstructive nephropathy. Nephrol Dial Transplant 2002, 17(Suppl. 9):39-41.
133. Shozu M., Minami N., Yokoyama H., Inoue M., Kurihara H., Matsushima K., et al. ADAMTS-1 is involved in normal follicular development, ovulatory process and organization of the medullary vascular network in the ovary. J Mol Endocrinol 2005, 35:343-355.
134. Howell M.D., Torres-Collado A.X., Iruela-Arispe M.L., Gottschall P.E. Selective decline of synaptic protein levels in the frontal cortex of female mice deficient in the extracellular metalloproteinase ADAMTS1. PLoS One 2012, 7:e47226.
135. Boerboom D., Lafond J.F., Zheng X., Lapointe E., Mittaz L., Boyer A., et al. Partially redundant functions of Adamts1 and Adamts4 in the perinatal development of the renal medulla. Dev Dyn 2011, 240:1806-1814.
136. Li S.W., Arita M., Fertala A., Bao Y., Kopen G.C., Langsjo T.K., et al. Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem J 2001, 355:271-278.
137. Glasson S.S., Askew R., Sheppard B., Carito B.A., Blanchet T., Ma H.L., et al. Characterization of and osteoarthritis susceptibility in ADAMTS-4-knockout mice. Arthritis Rheum 2004, 50:2547-2558.
138. Demircan K., Topcu V., Takigawa T., Akyol S., Yonezawa T., Ozturk G., et al. ADAMTS4 and ADAMTS5 knockout mice are protected from versican but not aggrecan or brevican proteolysis during spinal cord injury. Biomed Res Int 2014, 2014:693746.
139. Glasson S.S., Askew R., Sheppard B., Carito B., Blanchet T., Ma H.L., et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 2005, 434:644-648.
140. Botter S.M., Glasson S.S., Hopkins B., Clockaerts S., Weinans H., van Leeuwen J.P., et al. ADAMTS5-/- mice have less subchondral bone changes after induction of osteoarthritis through surgical instability: implications for a link between cartilage and subchondral bone changes. Osteoarthritis Cartilage 2009, 17:636-645.
141. Li J., Anemaet W., Diaz M.A., Buchanan S., Tortorella M., Malfait A.M., et al. Knockout of ADAMTS5 does not eliminate cartilage aggrecanase activity but abrogates joint fibrosis and promotes cartilage aggrecan deposition in murine osteoarthritis models. J Orthop Res 2011, 29:516-522.
142. Dancevic C.M., Fraser F.W., Smith A.D., Stupka N., Ward A.C., McCulloch D.R. Biosynthesis and expression of a disintegrin-like and metalloproteinase domain with thrombospondin-1 repeats-15: a novel versican-cleaving proteoglycanase. J Biol Chem 2013, 288:37267-37276.
143. Velasco J., Li J., Dipietro L., Stepp M.A., Sandy J.D., Plaas A. ADAMTS5 ablation blocks murine dermal repair through CD44-mediated aggrecan accumulation and modulation of TGFbeta1 signaling. J Biol Chem 2011, 286:26016-26027.
144. Wang V.M., Bell R.M., Thakore R., Eyre D.R., Galante J.O., Li J., et al. Murine tendon function is adversely affected by aggrecan accumulation due to the knockout of ADAMTS5. J Orthop Res 2012, 30:620-626.
145. Majumdar M.K., Askew R., Schelling S., Stedman N., Blanchet T., Hopkins B., et al. 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.
146. El Hour M., Moncada-Pazos A., Blacher S., Masset A., Cal S., Berndt S., et al. Higher sensitivity of Adamts12-deficient mice to tumor growth and angiogenesis. Oncogene 2010, 29:3025-3032.
147. Moncada-Pazos A., Obaya A.J., Llamazares M., Heljasvaara R., Suarez M.F., Colado E., et al. ADAMTS-12 metalloprotease is necessary for normal inflammatory response. J Biol Chem 2012, 287:39554-39563.
148. Paulissen G., El Hour M., Rocks N., Gueders M.M., Bureau F., Foidart J.M., et al. Control of allergen-induced inflammation and hyperresponsiveness by the metalloproteinase ADAMTS-12. J Immunol 2012, 189:4135-4143.
149. Motto D.G., Chauhan A.K., Zhu G., Homeister J., Lamb C.B., Desch K.C., et al. Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice. J Clin Invest 2005, 115:2752-2761.
150. De Meyer S.F., Savchenko A.S., Haas M.S., Schatzberg D., Carroll M.C., Schiviz A., et al. Protective anti-inflammatory effect of ADAMTS13 on myocardial ischemia/reperfusion injury in mice. Blood 2012, 120:5217-5223.