Altered versican cleavage in ADAMTS5 deficient mice; A novel etiology of myxomatous valve disease

Developmental Biology

Volumn 357, Issue 1, 2011, Pages 152-164

  Dupuis, Loren E ^a   McCulloch, Daniel R ^a   McGarity, Jessica D ^a   Bahan, Alexandria ^a   Wessels, Andy ^a   Weber, Deidra ^a   Diminich, A Megan ^a   Nelson, Courtney M ^a   Apte, Suneel S ^a   Kern, Christine B ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

ADAMTS5; Endocardial cushions; Extracellular matrix; Myxomatous valves; Versican

Indexed keywords

AGGRECANASE 2; BONE MORPHOGENETIC PROTEIN 2; TRANSCRIPTION FACTOR SOX9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; IMMUNOLOCALIZATION; INTRACELLULAR SPACE; MESENCHYME CELL; MOUSE; MYXOMATOUS VALVE DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VALVULAR HEART DISEASE;

MUS;

EID: 80051475089     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.06.041     Document Type: Article

References (86)

1. Aikawa E., Whittaker P., Farber M., Mendelson K., Padera R.F., Aikawa M., Schoen F.J. Human semilunar cardiac valve remodeling by activated cells from fetus to adult: implications for postnatal adaptation, pathology, and tissue engineering. Circulation 2006, 113:1344-1352.
2. Aikawa E., Nahrendorf M., Sosnovik D., Lok V.M., Jaffer F.A., Aikawa M., Weissleder R. Multimodality molecular imaging identifies proteolytic and osteogenic activities in early aortic valve disease. Circulation 2007, 115:377-386.
3. Akhtar S., Meek K.M., James V. Ultrastructure abnormalities in proteoglycans, collagen fibrils, and elastic fibers in normal and myxomatous mitral valve chordae tendineae. Cardiovasc. Pathol. 1999, 8:191-201.
4. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 2002, 16:2813-2828.
5. Angel P.M., Nusinow D., Brown C.B., Violette K., Barnett J.V., Zhang B., Baldwin H.S., Caprioli R.M. Networked-based characterization of extracellular matrix proteins from adult mouse pulmonary and aortic valves. J. Proteome Res. 2011, 10:812-823.
6. Apte S.S. A disintegrin-like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family. Int. J. Biochem. Cell. Biol. 2004, 36:981-985.
7. 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(46):31493-31497.
8. Aspberg A., Miura R., Bourdoulous S., Shimonaka M., Heinegard D., Schachner M., Ruoslahti E., Yamaguchi Y. The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc. Nat. Acad. Sci. U. S. A. 1997, 94:10116-10121.
9. Aspberg A., Adam S., Kostka G., Timpl R., Heinegard D. Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican. J. Biol. Chem. 1999, 274:20444-20449.
10. Aupperle H., Marz I., Thielebein J., Kiefer B., Kappe A., Schoon H.A. Immunohistochemical characterization of the extracellular matrix in normal mitral valves and in chronic valve disease (endocardiosis) in dogs. Res. Vet. Sci. 2009, 87:277-283.
11. Bondeson J., Wainwright S., Hughes C., Caterson B. The regulation of the ADAMTS4 and ADAMTS5 aggrecanases in osteoarthritis: a review. Clin. Exp. Rheumatol. 2008, 26:139-145.
12. Carta L., Pereira L., Arteaga-Solis E., Lee-Arteaga S.Y., Lenart B., Starcher B., Merkel C.A., Sukoyan M., Kerkis A., Hazeki N., Keene D.R., Sakai L.Y., Ramirez F. Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J. Biol. Chem. 2006, 281:8016-8023.
13. Carta L., Smaldone S., Zilberberg L., Loch D., Dietz H.C., Rifkin D.B., Ramirez F. p38 MAPK is an early determinant of promiscuous Smad2/3 signaling in the aortas of fibrillin-1 (Fbn1)-null mice. J. Biol. Chem. 2009, 284:5630-5636.
14. Clark T., Conway S., Scott I., Labosky P., Winnier G., Bundy J., Hogan B., Greenspan D. The mammalian tolloid-like 1 gene, Tll1, is necessary for normal septation and positioning of the heart. Deveopment 1999, 126:2631-2642.
15. Combs M.D., Yutzey K.E. Heart valve development: regulatory networks in development and disease. Circ. Res. 2009, 105:408-421.
16. Cooley M.A., Kern C.B., Fresco V.M., Wessels A., Thompson R.P., McQuinn T.C., Twal W.O., Mjaatvedt C.H., Drake C.J., Argraves W.S. Fibulin-1 is required for morphogenesis of neural crest-derived structures. Dev. Biol. 2008, 319:336-345.
17. Danielian P.S., Muccino D., Rowitch D.H., Michael S.K., McMahon A.P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 1998, 8:1323-1326.
18. de la Pompa J.L., Timmerman L.A., Takimoto H., Yoshida H., Elia A.J., Samper E., Potter J., Wakeham A., Marengere L., Langille B.L., Crabtree G.R., Mak T.W. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum [see comments]. Nature 1998, 392:182-186.
19. Delot E.C. Control of endocardial cushion and cardiac valve maturation by BMP signaling pathways. Mol. Genet. Metab. 2003, 80:27-35.
20. Delot E.C., Bahamonde M.E., Zhao M., Lyons K.M. BMP signaling is required for septation of the outflow tract of the mammalian heart. Development 2003, 130:209-220.
21. Derbali H., Bosse Y., Cote N., Pibarot P., Audet A., Pepin A., Arsenault B., Couture C., Despres J.P., Mathieu P. Increased biglycan in aortic valve stenosis leads to the overexpression of phospholipid transfer protein via Toll-like receptor 2. Am J Pathol. 2010, 176:2638-2645.
22. Enomoto H., Nelson C.M., Somerville R.P., Mielke K., Dixon L.J., Powell K., Apte S.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.
23. Galvin K.M., Donovan M.J., Lynch C.A., Meyer R.I., Paul R.J., Lorenz J.N., Fairchild-Huntress V., Dixon K.L., Dunmore J.H., Gimbrone M.A., Falb D., Huszar D. A role for smad6 in development and homeostasis of the cardiovascular system. Nat. Genet. 2000, 24:171-174.
24. Gupta V., Barzilla J.E., Mendez J.S., Stephens E.H., Lee E.L., Collard C.D., Laucirica R., Weigel P.H., Grande-Allen K.J. Abundance and location of proteoglycans and hyaluronan within normal and myxomatous mitral valves. Cardiovasc. Pathol. 2009, 18:191-197.
25. Gupta V., Tseng H., Lawrence B.D., Grande-Allen K.J. Effect of cyclic mechanical strain on glycosaminoglycan and proteoglycan synthesis by heart valve cells. Acta Biomater. 2009, 5:531-540.
26. Henderson D.J., Copp A.J. Versican expression is associated with chamber specification, septation, and valvulogenesis in the developing mouse heart. Circ. Res. 1998, 83:523-532.
27. Hinton R.B., Yutzey K.E. Heart valve structure and function in development and disease. Annu. Rev. Physiol. 2011, 73:29-46.
28. Hinton R.B., Lincoln J., Deutsch G.H., Osinska H., Manning P.B., Benson D.W., Yutzey K.E. Extracellular matrix remodeling and organization in developing and diseased aortic valves. Circ. Res. 2006, 98:1431-1438.
29. Hinton R.B., Alfieri C.M., Witt S.A., Glascock B.J., Khoury P.R., Benson D.W., Yutzey K.E. Mouse heart valve structure and function: echocardiographic and morphometric analyses from the fetus through the aged adult. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H2480-H2488.
30. Hoffman J.I., Kaplan S. The incidence of congenital heart disease. J. Am. Coll. Cardiol. 2002, 39:1890-1900.
31. Huang K., Wu L.D. Suppression of aggrecanase: a novel protective mechanism of dehydroepiandrosterone in osteoarthritis?. Mol. Biol. Rep. 2010, 37:1241-1245.
32. Hutson M.R., Kirby M.L. Neural crest and cardiovascular development: a 20-year perspective. Birth Defects Res. C Embryo Today 2003, 69:2-13.
33. Ito K., Shinomura T., Zako M., Ujita M., Kimata K. Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J. Biol. Chem. 1995, 270:958-965.
34. Jackson L.F., Qiu T.H., Sunnarborg S.W., Chang A., Zhang C., Patterson C., Lee D.C. Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. EMBO J. 2003, 22:2704-2716.
35. Jang G.H., Park I.S., Yang J.H., Bischoff J., Lee Y.M. Differential functions of genes regulated by VEGF-NFATc1 signaling pathway in the migration of pulmonary valve endothelial cells. FEBS Lett. 2010, 584:141-146.
36. Jian B., Narula N., Li Q.Y., Mohler E.R., Levy R.J. Progression of aortic valve stenosis: TGF-beta1 is present in calcified aortic valve cusps and promotes aortic valve interstitial cell calcification via apoptosis. Ann. Thorac. Surg. 2003, 75:457-465. discussion 465-6.
37. Jonsson-Rylander A.C., Nilsson T., Fritsche-Danielson R., Hammarstrom A., Behrendt M., Andersson J.O., Lindgren K., Andersson A.K., Wallbrandt P., Rosengren B., Brodin P., Thelin A., Westin A., Hurt-Camejo E., Lee-Sogaard C.H. Role of ADAMTS-1 in atherosclerosis: remodeling of carotid artery, immunohistochemistry, and proteolysis of versican. Arterioscler. Thromb. Vasc. Biol. 2005, 25:180-185.
38. Jungers K.A., Le Goff C., Somerville R.P., Apte S.S. Adamts9 is widely expressed during mouse embryo development. Gene. Expr. Patterns. 2005, 5:609-617.
39. Kantola A.K., Keski-Oja J., Koli K. Fibronectin and heparin binding domains of latent TGF-beta binding protein (LTBP)-4 mediate matrix targeting and cell adhesion. Exp. Cell Res. 2008, 314:2488-2500.
40. Kenagy R.D., Fischer J.W., Lara S., Sandy J.D., Clowes A.W., Wight T.N. Accumulation and loss of extracellular matrix during shear stress-mediated intimal growth and regression in baboon vascular grafts. J. Histochem. Cytochem. 2005, 53:131-140.
41. Kenagy R.D., Plaas A.H., Wight T.N. Versican degradation and vascular disease. Trends Cardiovasc. Med. 2006, 16:209-215.
42. Kenagy R.D., Min S.K., Clowes A.W., Sandy J.D. Cell death-associated ADAMTS4 and versican degradation in vascular tissue. J. Histochem. Cytochem. 2009, 57:889-897.
43. Kern C.B., Twal W.O., Mjaatvedt C.H., Fairey S.E., Toole B.P., Iruela-Arispe M.L., Argraves W.S. Proteolytic cleavage of versican during cardiac cushion morphogenesis. Dev. Dyn. 2006, 235:2238-2247.
44. Kern C.B., Norris R.A., Thompson R.P., Argraves W.S., Fairey S.E., Reyes L., Hoffman S., Markwald R.R., Mjaatvedt C.H. Versican proteolysis mediates myocardial regression during outflow tract development. Dev. Dyn. 2007, 236:671-683.
45. Kern C.B., Wessels A., McGarity J., Dixon L.J., Alston E., Argraves W.S., Geeting D., Nelson C.M., Menick D.R., Apte S.S. Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol. 2010, 29:304-316.
46. Kim R.Y., Robertson E.J., Solloway M.J. Bmp6 and Bmp7 are required for cushion formation and septation in the developing mouse heart. Dev. Biol. 2001, 235:449-466.
47. Kim L., Kim do, K., Yang W.I., Shin D.H., Jung I.M., Park H.K., Chang B.C. Overexpression of transforming growth factor-beta 1 in the valvular fibrosis of chronic rheumatic heart disease. J. Korean Med. Sci. 2008, 23:41-48.
48. Lee N.V., Sato M., Annis D.S., Loo J.A., Wu L., Mosher D.F., Iruela-Arispe M.L. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J. 2006, 25:5270-5283.
49. Lincoln J., Alfieri C.M., Yutzey K.E. Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev. Dyn. 2004, 230:239-250.
50. Lincoln J., Alfieri C.M., Yutzey K.E. BMP and FGF regulatory pathways control cell lineage diversification of heart valve precursor cells. Dev. Biol. 2006, 292:292-302.
51. 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.
52. Margolis R., Margolis R. Aggrecan-versican-neurocan family proteoglycans. Methods Enzymol. 1994, 245:105-126.
53. McCulloch D.R., Le Goff C., 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.
54. McCulloch D.R., Nelson C.M., Dixon L.J., Silver D.L., Wylie J.D., Lindner V., Sasaki T., Cooley M.A., Argraves W.S., Apte S.S. ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev. Cell. 2009, 17:687-698.
55. Melching L.I., Fisher W.D., Lee E.R., Mort J.S., Roughley P.J. The cleavage of biglycan by aggrecanases. Osteoarthr. Cartil. 2006, 14:1147-1154.
56. Merryman W.D., Liao J., Parekh A., Candiello J.E., Lin H., Sacks M.S. Differences in tissue-remodeling potential of aortic and pulmonary heart valve interstitial cells. Tissue Eng. 2007, 13:2281-2289.
57. Mjaatvedt C.H., Yamamura H., Capehart A.A., Turner D., Markwald R.R. The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev. Biol. 1998, 202:56-66.
58. Mjaatvedt C.H., Nakaoka T., Moreno-Rodriguez R., Norris R.A., Kern M.J., Eisenberg C.A., Turner D., Markwald R.R. The outflow tract of the heart is recruited from a novel heart-forming field. Dev. Biol. 2001, 238:97-109.
59. Morales A.R., Romanelli R., Boucek R.J., Tate L.G., Alvarez R.T., Davis J.T. Myxoid heart disease: an assessment of extravalvular cardiac pathology in severe mitral valve prolapse. Hum. Pathol. 1992, 23:129-137.
60. Ng C.M., Cheng A., Myers L.A., Martinez-Murillo F., Jie C., Bedja D., Gabrielson K.L., Hausladen J.M., Mecham R.P., Judge D.P., Dietz H.C. TGF-beta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. J. Clin. Invest. 2004, 114:1586-1592.
61. Ohno-Jinno A., Isogai Z., Yoneda M., Kasai K., Miyaishi O., Inoue Y., Kataoka T., Zhao J.S., Li H., Takeyama M., Keene D.R., Sakai L.Y., Kimata K., Iwaki M., Zako M. Versican and fibrillin-1 form a major hyaluronan-binding complex in the ciliary body. Invest Ophthalmol. Vis. Sci. 2008, 49:2870-2877.
62. Peacock J.D., Levay A.K., Gillaspie D.B., Tao G., Lincoln J. Reduced sox9 function promotes heart valve calcification phenotypes in vivo. Circ. Res. 2010, 106:712-719.
63. Rabkin-Aikawa E., Aikawa M., Farber M., Kratz J.R., Garcia-Cardena G., Kouchoukos N.T., Mitchell M.B., Jonas R.A., Schoen F.J. Clinical pulmonary autograft valves: pathologic evidence of adaptive remodeling in the aortic site. J. Thorac. Cardiovasc. Surg. 2004, 128:552-561.
64. Rabkin-Aikawa E., Mayer J.E., Schoen F.J. Heart valve regeneration. Adv. Biochem. Eng. Biotechnol. 2005, 94:141-179.
65. Ranger A.M., Grusby M.J., Hodge M.R., Gravallese E.M., de la Brousse F.C., Hoey T., Mickanin C., Baldwin H.S., Glimcher L.H. The transcription factor NF-ATc is essential for cardiac valve formation. Nature 1998, 392:186-190.
66. Roberts W.C., Ko J.M., Hamilton C. Comparison of valve structure, valve weight, and severity of the valve obstruction in 1849 patients having isolated aortic valve replacement for aortic valve stenosis (with or without associated aortic regurgitation) studied at 3 different medical centers in 2 different time periods. Circulation 2005, 112:3919-3929.
67. Rogerson F.M., Stanton H., East C.J., Golub S.B., Tutolo L., Farmer P.J., Fosang A.J. Evidence of a novel aggrecan-degrading activity in cartilage: Studies of mice deficient in both ADAMTS-4 and ADAMTS-5. Arthritis Rheum. 2008, 58:1664-1673.
68. Runyan R.B., Markwald R.R. Invasion of mesenchyme into three-dimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue. Dev. Biol. 1983, 95:108-114.
69. Sandy J.D. Proteoglycan core proteins and catabolic fragments present in tissues and fluids. Methods Mol. Biol. 2001, 171:335-345.
70. 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., Clowes A.W. 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.
71. Seidelmann S.B., Kuo C., Pleskac N., Molina J., Sayers S., Li R., Zhou J., Johnson P., Braun K., Chan C., Teupser D., Breslow J.L., Wight T.N., Tall A.R., Welch C.L. Athsq1 is an atherosclerosis modifier locus with dramatic effects on lesion area and prominent accumulation of versican. Arterioscler. Thromb. Vasc. Biol. 2008, 28:2180-2186.
72. Shelton E.L., Yutzey K.E. Tbx20 regulation of endocardial cushion cell proliferation and extracellular matrix gene expression. Dev. Biol. 2007, 302:376-388.
73. Shepard J.B., Krug H.A., LaFoon B.A., Hoffman S., Capehart A.A. Versican expression during synovial joint morphogenesis. Int. J. Biol. Sci. 2007, 3:380-384.
74. Shibata S., Fukada K., Imai H., Abe T., Yamashita Y. In situ hybridization and immunohistochemistry of versican, aggrecan and link protein, and histochemistry of hyaluronan in the developing mouse limb bud cartilage. J. Anat. 2003, 203:425-432.
75. Snarr B.S., Kern C.B., Wessels A. Origin and fate of cardiac mesenchyme. Dev. Dyn. 2008, 237:2804-2819.
76. Snow H.E., Riccio L.M., Mjaatvedt C.H., Hoffman S., Capehart A.A. Versican expression during skeletal/joint morphogenesis and patterning of muscle and nerve in the embryonic mouse limb. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2005, 282A:95-105.
77. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
78. Stankunas K., Hang C.T., Tsun Z.Y., Chen H., Lee N.V., Wu J.I., Shang C., Bayle J.H., Shou W., Iruela-Arispe M.L., Chang C.P. Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev. Cell. 2008, 14:298-311.
79. Theocharis A.D. Versican in health and disease. Connect Tissue Res. 2008, 49:230-234.
80. Weismann C.G., Gelb B.D. The genetics of congenital heart disease: a review of recent developments. Curr. Opin. Cardiol. 2007, 22:200-206.
81. Wight T.N. Arterial remodeling in vascular disease: a key role for hyaluronan and versican. Front. Biosci. 2008, 13:4933-4937.
82. Wirrig E.E., Snarr B.S., Chintalapudi M.R., O'Neal J.L., Phelps A.L., Barth J.L., Fresco V.M., Kern C.B., Mjaatvedt C.H., Toole B.P., Hoffman S., Trusk T.C., Argraves W.S., Wessels A. Cartilage link protein 1 (Crtl1), an extracellular matrix component playing an important role in heart development. Dev. Biol. 2007, 310:291-303.
83. Wu Y.J., La Pierre D.P., Wu J., Yee A.J., Yang B.B. The interaction of versican with its binding partners. Cell Res. 2005, 15:483-494.
84. Yamamura H., Zhang M., Markwald R., Mjaatvedt C. A heart segmental defect in the anterior-posterior axis of a transgenic mutant mouse. Dev. Biol. 1997, 186:58-72.
85. Yatabe T., Mochizuki S., Takizawa M., Chijiiwa M., Okada A., Kimura T., Fujita Y., Matsumoto H., Toyama Y., Okada Y. Hyaluronan inhibits expression of ADAMTS4 (aggrecanase-1) in human osteoarthritic chondrocytes. Ann. Rheum. Dis. 2009, 68:1051-1058.
86. Zako M., Shinomura T., Ujita M., Ito K., Kimata K. Expression of PG-M(V3), an alternatively spliced form of PG-M without a chondroitin sulfate attachment in region in mouse and human tissues. J. Biol. Chem. 1995, 270:3914-3918.