Metalloproteinases and their inhibitors in the pathophysiology of heritable connective tissue disorders: current evidence

References

• Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol. 2007;8(3):221–233.
   PubMed Web of Science ®Google Scholar
• Maskos K. Crystal structures of MMPs in complex with physiological and pharmacological inhibitors. Biochimie. 2005;87(3–4):249–263.
   PubMed Web of Science ®Google Scholar
• Birkedal-Hansen H, Moore WG, Bodden MK, et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med. 1993;4(2):197–250.
   PubMedGoogle Scholar
• Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14(2):163–176.
   PubMed Web of Science ®Google Scholar
• Apte SS. A disintegrin–like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family. Intern J Biochem Cell Biol. 2004;36:981–985.
   Web of Science ®Google Scholar
• Apte SS. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem. 2009;284:31493–31497.
   PubMed Web of Science ®Google Scholar
• Bekhouche M, Colige A. The procollagen N-proteinases ADAMTS2, 3 and 14 in pathophysiology. Matrix Biol. 2015;44–46:46–53.
   Web of Science ®Google Scholar
• Stanton H, Rogersoon FM, East CJ, et al. ADAMTS5 is the major aggreganase in mouse cartilage in vivo and in vitro. Nature. 2005;434:648–652.
   PubMed Web of Science ®Google Scholar
• Sandy JD, Verscharen C. Analysis of aggregan in human knee cartilage and synovial indicates that aggreganase (ADAMTS) activity is responsible for the catabolic turnover and loss of whole aggregan whereas other protease activity is required for C-terminal processing in vivo. Biochem J. 2001;358:615–626.
   PubMed Web of Science ®Google Scholar
• Asada Y, Sumiyoshi A, Hayashi T, Suzumiya J, Kaketami K. Immunohistochemistry of vascular lesion in thrombotic thromcytopenic purpura with special reference to factor VIII related antigen. Thromb Res. 1985;38:469–479.
   PubMed Web of Science ®Google Scholar
• Luan Y, Kong L, Howell DR, et al. Inhibition of ADAMTS-7 and ADAMTS-12 degradation of cartilage oligomeric matrix protein by alpha-2-macroglobulin. Osteoarthritis Cartilage. 2008;16(11):1413–1420.
   Web of Science ®Google Scholar
• Liu CJ, Kong W, Ilalov K, et al ADAMTS-7: a metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein. FASEB J. 2006;20(7):988–990.
   Web of Science ®Google Scholar
• Hirohata S, Wang LW, Miyagi M, et al. Punctin, a novel ADAMTS-like molecule, ADAMTSL-1, in extracellular matrix. J Biol Chem. 2002;277:12182–12189.
   Web of Science ®Google Scholar
• Hall NG, Klenotic P, Anand-Apte B, Apte SS. ADAMTSL-3/punctin-2, a novel glycoprotein in extracellular matrix related to the ADAMTS family of metalloproteases. Matrix Biol. 2003;22:501–510.
   Web of Science ®Google Scholar
• Koo BH, Le Goff C, Jungers KA, 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.
   PubMed Web of Science ®Google Scholar
• Tsutsui K, Manabe R, Yamada T, et al. 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.
   PubMed Web of Science ®Google Scholar
• Kramerova IA, Kawaguchi N, Fessler LI, et al. Papilin in development; a pericellular protein with a homology to the ADAMTS metalloproteinases. Development. 2000;127:5475–5485.
   PubMed Web of Science ®Google Scholar
• Fessler JH, Kramerova I, Kramerov A, Chen Y, Fessler LI. Papilin, a novel component of basement membranes, in relation to ADAMTS metalloproteases and ECM development. Int J Biochem Cell Biol. 2004;36(6):1079–1084.
   PubMed Web of Science ®Google Scholar
• Maroteaux P, Verloes A, Stanescu V, Stanescu R. Metaphysealanadysplasia: a metaphyseal dysplasia of early onset with radiological regression and benign course. Am J Med Genet. 1991;39:4–10.
   Web of Science ®Google Scholar
• Wiedemann H-R, Spranger J. Chondrodysplasia metaphysaria (Dysostosismetaphysaria) – ein neuer Typ? Z Kinderheilk. 1970;108:171–186.
   Google Scholar
• Lausch E, Keppler R, Hilbert K. Mutations in MMP9 and MMP13 determine the mode of inheritance and the clinical spectrum of metaphysealanadysplasia. Am J Hum Genet. 2009;85:168–178.
   Web of Science ®Google Scholar
• Bonafe L, Liang J, Gorna MW, et al. MMP13 mutations are the cause of recessive metaphyseal dysplasia, Spahr type. Am J Med Genet. 2014;164A:1175–1179.
   Google Scholar
• Ortega N, Behonick DJ, Colnot C, Cooper DN, Werb Z. Galectin-3 is a downstream regulator of matrix metalloproteinase-9 function during endochondral bone formation. Mol Biol Cell. 2005;16(6):3028–3039.
   Web of Science ®Google Scholar
• Vu TH, Shipley JM, Bergers G, et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 1998;93:411–422.
   PubMed Web of Science ®Google Scholar
• Chung AWY, Yeung KA, Sandor GG, et al. Loss of elastic fiber integrity and reduction of vascular smooth muscle contraction resulting from the upregulated activities of matrix metalloproteinase-2 and -9 in the thoracic aortic aneurysm in Marfan syndrome. Circ Res. 2007;101:512–522.
   PubMed Web of Science ®Google Scholar
• Dubois B, Masure S, Hurtenbach U, et al. Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions. J Clin Invest. 1999;104:1507–1515.
   PubMed Web of Science ®Google Scholar
• Engsig MT, Chen QJ, Vu TH, et al. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol. 2000;151(4):879–889.
   PubMed Web of Science ®Google Scholar
• Mitchell PG, Magna HA, Reeves LM, et al. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J Clin Invest. 1996;97:761–768.
   PubMed Web of Science ®Google Scholar
• Reboul P, Pelletier J-P, Tardif G, Cloutier J-M, Martel-Pelletier J. The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes: a role in osteoarthritis. J Clin Invest. 1996;97:2011–2019.
   PubMed Web of Science ®Google Scholar
• Stickens D, Behonick DJ, Ortega N, et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development. 2004;131(23):5883–5895.
   Web of Science ®Google Scholar
• Borochowitz ZU, Scheffer D, Adir V, Dagoneau N, Munnich A, Cormier-Daire V. Spondylo-epi-metaphyseal dysplasia (SEMD) matrilin 3 type: homozygote matrilin 3 mutation in a novel form of SEMD. J Med Genet. 2004;41:366–372.
   PubMed Web of Science ®Google Scholar
• Kennedy AM, Inada M, Krane SM, et al. MMP13 mutation causes spondyloepimetaphyseal dysplasia, Missouri type (SEMD(MO)). J Clin Invest. 2005;115:2832–2842.
   PubMed Web of Science ®Google Scholar
• Patel AC, McAlister WH, Whyte MP. Spondyloepimetaphyseal dysplasia: clinical and radiologic investigation of a large kindred manifesting autosomal dominant inheritance, and a review of the literature. Medicine. 1993;72:326–342.
   Web of Science ®Google Scholar
• Winchester P, Grossman H, Lim WN, Danes BS. A new acid mucopolysaccharidosis with skeletal deformities simulating rheumatoid arthritis. Am J Roentgen. 1969;106:121–128.
   Web of Science ®Google Scholar
• Evans BR, Mosig RA, Lobl M, et al. Mutation of membrane type-1 metalloproteinase, MT1-MMP, causes the multicentric osteolysis and arthritis disease Winchester syndrome. Am J Hum Genet. 2012;91:572–576.
   Web of Science ®Google Scholar
• Holmbeck K, Bianco P, Caterina J, et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell. 1999;99:81–92.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Apte SS, Soininen R, et al. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A. 2000;97(8):4052–4057.
   PubMed Web of Science ®Google Scholar
• Zankl A, Pachman L, Poznanski A, et al. Torg syndrome is caused by inactivating mutations in MMP2 and is allelic to NAO and Winchester syndrome. J Bone Miner Res. 2007;22:329–333.
   Web of Science ®Google Scholar
• Torg JS, DiGeorge AM, Kirkpatrick JA Jr, Trujillo MM. Hereditary multicentric osteolysis with recessive transmission: a new syndrome. J Pediat. 1969;75:243–252.
   Web of Science ®Google Scholar
• Eisenstein DM, Poznanski AK, Pachman LM. Torgosteolysis syndrome. Am J Med Genet. 1998;80:207–212.
   PubMed Web of Science ®Google Scholar
• Inoue K, Mikuni-Takagaki Y, Oikawa K, et al. A crucial role for matrix metalloproteinase 2 in osteocyticcanalicular formation and bone metabolism. J Biol Chem. 2006;281(44):33814–33824.
   Web of Science ®Google Scholar
• Oh J, Takahashi R, Adachi E, et al. Mutations in two matrix metalloproteinase genes, MMP-2 and MT1-MMP, are synthetic lethal in mice. Oncogene. 2004;23(29):5041–5048.
   Web of Science ®Google Scholar
• Witkop CJ Jr. Amelogenesis imperfecta, dentinogenesis imperfecta and dentin dysplasia revisited: problems in classification. J Oral Path. 1989;17:547–553.
   Google Scholar
• Kim J-W, Simmer JP, Hart TC, et al. MMP-20 mutation in autosomal recessive pigmented hypomaturation amelogenesis imperfecta. J Med Genet. 2005;42:271–275.
   PubMed Web of Science ®Google Scholar
• Ozdemir D, Hart PS, Ryu OH, et al. MMP20 active-site mutation in hypomaturation amelogenesis imperfecta. J Dent Res. 2005;84:1031–1035.
   PubMed Web of Science ®Google Scholar
• Caterina JJ, Skobe Z, Shi J, et al. Enamelysin (matrix metalloproteinase 20)-deficient mice display an amelogenesis imperfecta phenotype. J Biol Chem. 2002;277:49598–49604.
   PubMed Web of Science ®Google Scholar
• Shin M, Hu Y, Tye CE. Matrix metalloproteinase-20 over-expression is detrimental to enamel development: a Mus musculus model. PLoS One. 2014;9(1):e86774.
   Web of Science ®Google Scholar
• Lapiere CM, Nusgens BV. Ehlers DAnlos type VIIC or human dermatosparaxis. The offspring of a union between basic and clinical research. Arch Dermatol. 1993;129:1316–1319.
   Google Scholar
• Nusgens BV, Verellen-Dumoulin C, Hermanns-Le T, et al. Evidence for a relationship between Ehlers-Danlos type VII C in humans and bovine dermatosparaxis. Nat Genet. 1992;1:214–217.
   PubMed Web of Science ®Google Scholar
• Malfait F, De Paepe A. The Ehlers-Danlos syndrome. Adv Exp Med Biol. 2014;802:129–143.
   PubMed Web of Science ®Google Scholar
• Colige A, Sieron AL, Li SW, et al. Human Ehlers-Danlos syndrome type VIIc and bovine dermatosparaxis are caused by mutations in the procollagen I N proteinase gene. Am J Hum Genet, 1999;65:308–317.
   PubMed Web of Science ®Google Scholar
• Le Goff C, Somerville RP, Kesteloot F. 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.
   PubMed Web of Science ®Google Scholar
• Li SW, Arita M, Fertala A, et al. Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem J. 2001;355(Pt 2):271–278.
   Google Scholar
• Le Goff C, Cormier-Daire V. Genetic and molecular aspects of acromelic dysplasia. Pediatr Endocrinol Rev. 2009;6(3):418–423.
   Google Scholar
• Weill G. Ectopie du cristallin et malformations générales. Ann Occul. 1932;169:21–44.
   Google Scholar
• Marchesani O. Brachydaktylie und angerobene kugellines als systemerkrnakung. Klin Mibl Augenheilk. 1939;103:392–406.
   Google Scholar
• Dagoneau N, Benoist-Lasselin C, Huber C, et al. ADAMTS 10 mutations in autosomal recessive Weill-Marchesani syndrome. Am J Hum Genet. 2004;75:801–806.
   PubMed Web of Science ®Google Scholar
• Faivre L, Gorlin RJ, Wirtz MW, et al. In-frame fibrillin-1 gene deletion in autosomal dominant Weill-Marchesani syndrome. J Med Genet. 2003;240:34–35.
   Google Scholar
• Haji-Seyed-Javadi R, Jelodari-Mamaghani S, Paylakhi SH. LTBP2 mutations cause Weill-Marchesani and Weill-Marchesani-like syndrome and affect disruptions in the extracellular matrix. Hum Mutat. 2012;33(8):1182–1187.
   Web of Science ®Google Scholar
• Somerville RP, Jungers KA, Apte SS. Discovery and characterization of a novel, widely expressed metalloprotease, ADAMTS10, and its proteolytic activation J Biol Chem. 2004;279(49):51208–51217.
   PubMed Web of Science ®Google Scholar
• Kutz WE, Wang LW, Bader HL, 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.
   PubMed Web of Science ®Google Scholar
• Morales J, Al-Sharif L, Khalil DS, et al. Homozygous mutations in ADAMTS10 and ADAMTS17 cause lenticular myopia, ectopialentis, glaucoma, spherophakia, and short stature. Am J Hum Genet. 2009;85:558–568.
   PubMed Web of Science ®Google Scholar
• Spranger JW, Gilbert EF, Tuffli GA, Rossiter FP, Opitz JM. Geleophysic dwarfism – a “focal” mucopolysaccharidosis? Lancet. 1971;10:97–98.
   Google Scholar
• Allali S, Le Goff C, Pressac-Diebold I, et al. Molecular screening of ADAMTSL2 gene in 33 patients reveals the genetic heterogeneity of geleophysic dysplasia. J Med Genet. 2011;48:417–421.
   PubMed Web of Science ®Google Scholar
• Le Goff C, Morice-Picard F, Dagoneau N, 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.
   PubMed Web of Science ®Google Scholar
• Le Goff C, Mahaut C, Wang LW, et al. Mutations in the TGFβ binding-protein-like domain 5 of FBN1 are responsible for acromicric and geleophysic dysplasias. Am J Hum Genet. 2011;89:7–14.
   PubMed Web of Science ®Google Scholar
• Ramirez F, Sakai LY. Biogenesis and function of fibrillin assemblies. Cell Tissue Res. 2010;339(1):71–82.
   PubMed Web of Science ®Google Scholar
• Cain SA, McGovern A, Baldwin AK, Baldock C, Kielty CM. Fibrillin-1 mutations causing Weill-Marchesani syndrome and acromicric and geleophysicdysplasias disrupt heparan sulfate interactions. PLoS One. 2012;7(11):e48634.
   Web of Science ®Google Scholar
• Hubmacher D, Wang LW, Mecham RP, Reinhardt DP, Apte SS. Adamtsl2 deletion results in bronchial fibrillin microfibril accumulation and bronchial epithelial dysplasia – a novel mouse model providing insights into geleophysic dysplasia. Dis Model Mech. 2015;8(5):487–499.
   Web of Science ®Google Scholar
• Ahram D, Sato TS, Kohilan A, et al. A homozygous mutation in ADAMTSL4 causes autosomal-recessive isolated ectopialentis. Am J Hum Genet. 2009;84:274–278.
   PubMed Web of Science ®Google Scholar
• Lonqvist L, Child A, Kainulainen K, Davidson R, Puhakka L, Peltonen L. A novel mutation of the fibrillin gene causing ectopialentis. Genomics. 1994;19:573–576.
   Web of Science ®Google Scholar
• Dietz HC, Cutting GR, Pyeritz RE, et al. Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature. 1991;352:337–339.
   PubMed Web of Science ®Google Scholar
• Chandra A, Aragon-Martin JA, Sharif S, Parulekar M, Child A, Arno G. Craniosynostosis with ectopialentis and a homozygous 20-base deletion in ADAMTSL4. Ophthalmic Genet. 2013;34(1–2):78–82.
   PubMed Web of Science ®Google Scholar
• Gabriel LA, Wang LW, Bader H. ADAMTSL4, a secreted glycoprotein widely distributed in the eye, binds fibrillin-1 microfibrils and accelerates microfibril biogenesis. Invest Ophthalmol Vis Sci. 2012;53(1):461–469.
   Web of Science ®Google Scholar
• Khan AO. Microcornea with myopic chorioretinal atrophy, telecanthus and posteriorly-rotated ears: a distinct clinical syndrome. Ophthalmic Genet. 2012;33:196–199.
   PubMed Web of Science ®Google Scholar
• Aldahmesh MA, Alshammari MJ, Khan AO, Mohamed JY, Alhabib FA, Alkuraya FS. The syndrome of microcornea, myopic chorioretinal atrophy, and telecanthus (MMCAT) is caused by mutations in ADAMTS18. Hum Mutat. 2013;34:1195–1199.
   PubMed Web of Science ®Google Scholar
• Peluso I, Conte I, Testa F. The ADAMTS18 gene is responsible for autosomal recessive early onset severe retinal dystrophy. Orphanet J Rare Dis. 2013;8:16.
   PubMed Web of Science ®Google Scholar
• Sorsby A, Mason MEJ, Gardner N. A fundus dystrophy with unusual features (late onset and dominant inheritance of a central retinal lesion showing oedema, haemorrhage and exudates developing into generalized choroidal atrophy with massive pigment proliferation). Brit J Ophthal. 1949;33:67–97.
   PubMed Web of Science ®Google Scholar
• Weber, BHF, Vogt G, Pruett RC, Stohr H, Felbor U. Mutations in the tissue inhibitor metalloproteinases-3 (TIMP3) in patients with Sorsby’s fundus dystrophy. Nature Genet. 1994;8:352–356.
   PubMed Web of Science ®Google Scholar