Versican processing by a disintegrin-like and metalloproteinase domain with thrombospondin-1 repeats proteinases-5 and-15 facilitates myoblast fusion

Journal of Biological Chemistry

Volumn 288, Issue 3, 2013, Pages 1907-1917

  Stupka, Nicole ^a,b   Kintakas, Christopher ^b,c   White, Jason D ^b,c   Fraser, Fiona W ^a   Hanciu, Michael ^a   Aramaki Hattori, Noriko ^d   Martin, Sheree ^a   Coles, Chantal ^b   Collier, Fiona ^e   Ward, Alister C ^a   Apte, Suneel S ^d   McCulloch, Daniel R ^a  

^a DEAKIN UNIVERSITY   (Australia)

^b MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d LERNER RESEARCH INSTITUTE   (United States)

^e GEELONG HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

C2C12 CELLS; CANCER CACHEXIA; ENZYMATIC PROTEOLYSIS; HYALURONAN; IN-VITRO; IN-VIVO; METALLOPROTEINASES; MULTINUCLEATED MYOTUBES; MUSCLE FIBER; MUSCULAR DYSTROPHY; MYOBLASTS; MYOGENESIS; PERICELLULAR MATRIX; REGENERATIVE CAPACITY; SARCOPENIA; SKELETAL MUSCLE; SKELETAL MUSCLE FIBERS; TRANSGENIC MICE;

CELL MEMBRANES; CYTOLOGY;

MUSCLE;

ADAMTS15 PROTEIN; AGGRECANASE 2; HYALURONIC ACID; MESSENGER RNA; METALLOPROTEINASE; UNCLASSIFIED DRUG; VERSICAN;

ADAMTS15 GENE; ADAMTS5 GENE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ADAM PROTEINS; ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; MICE; MICE, TRANSGENIC; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MYOBLASTS; REGENERATION; RNA, MESSENGER; THROMBOSPONDINS; VERSICANS;

MUS MUSCULUS;

EID: 84872692374     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.429647     Document Type: Article

References (48)

1. Grounds, M. D., Sorokin, L., and White, J. (2005) Strength at the extracellular matrix-muscle interface. Scand. J. Med. Sci. Sports 15, 381-391 (Pubitemid 41752307)
2. Reed, U. C. (2009) Congenital muscular dystrophy. Part I. A review of phenotypical and diagnostic aspects. Arq. Neuropsiquiatr. 67, 144-168
3. Horsley, V., and Pavlath, G. K. (2004) Forming a multinucleated cell. Molecules that regulate myoblast fusion. Cells Tissues Organs 176, 67-78 (Pubitemid 38199420)
4. Abmayr, S. M., and Pavlath, G. K. (2012) Myoblast fusion. Lessons from flies and mice. Development 139, 641-656
5. Melo, F., Carey, D. J., and Brandan, E. (1996) Extracellular matrix is required for skeletal muscle differentiation but not myogenin expression. J. Cell Biochem. 62, 227-239 (Pubitemid 26287207)
6. Calve, S., and Simon, H. G. (2012) Biochemical and mechanical environment cooperatively regulate skeletal muscle regeneration. FASEB J. 26, 2538-2545
7. Landolt, R. M., Vaughan, L., Winterhalter, K. H., and Zimmermann, D. R. (1995) Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development 121, 2303-2312
8. Wu, Y. J., La Pierre, D. P., Wu, J., Yee, A. J., and Yang, B. B. (2005) The interaction of versican with its binding partners. Cell Res. 15, 483-494 (Pubitemid 41653919)
9. Knudson, C. B., and Toole, B. P. (1987) Hyaluronate-cell interactions during differentiation of chick embryo limb mesoderm. Dev. Biol. 124, 82-90
10. Snow, H. E., Riccio, L. M., Mjaatvedt, C. H., Hoffman, S., and Capehart, A. A. (2005) 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. 282, 95-105 (Pubitemid 40223531)
11. Ermakova, I. I., Sakuta, G. A., Potekhina, M. A., Fedorova, M. A., Hoffmann, R., and Morozov, V. I. (2011) Major chondroitin sulfate proteoglycans identified in L6J1 myoblast culture. Biochemistry 76, 359-365
12. 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., and Clowes, A. W. (2001) 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. 276, 13372-13378
13. Apte, S. S. (2009) A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily. Functions and mechanisms. J. Biol. Chem. 284, 31493-31497
14. Kintakas, C., and McCulloch, D. R. (2011) Emerging roles for ADAMTS5 during development and disease. Matrix Biol. 30, 311-317
15. McCulloch, D. R., Le Goff, C., Bhatt, S., Dixon, L. J., Sandy, J. D., and Apte, S. S. (2009) 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 9, 314-323
16. Longpré, J. M., McCulloch, D. R., Koo, B. H., Alexander, J. P., Apte, S. S., and Leduc, R. (2009) Characterization of proADAMTS5 processing by proprotein convertases. Int. J. Biochem. Cell Biol. 41, 1116-1126
17. Malfait, A. M., Arner, E. C., Song, R. H., Alston, J. T., Markosyan, S., Staten, N., Yang, Z., Griggs, D. W., and Tortorella, M. D. (2008) Proprotein convertase activation of aggrecanases in cartilage in situ. Arch. Biochem. Biophys. 478, 43-51
18. Glasson, S. S., Askew, R., Sheppard, B., Carito, B., Blanchet, T., Ma, H. L., Flannery, C. R., Peluso, D., Kanki, K., Yang, Z., Majumdar, M. K., and Morris, E. A. (2005) Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 434, 644-648 (Pubitemid 40488556)
19. Stanton, H., Rogerson, F. M., East, C. J., Golub, S. B., Lawlor, K. E., Meeker, C. T., Little, C. B., Last, K., Farmer, P. J., Campbell, I. K., Fourie, A. M., and Fosang, A. J. (2005) ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 434, 648-652 (Pubitemid 40488557)
20. 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., and Apte, S. S. (2009) ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev. Cell 17, 687-698
21. McCulloch, D. R., Akl, P., Samaratunga, H., Herington, A. C., and Odorico, D. M. (2004) Expression of the disintegrin metalloprotease, ADAM-10, in prostate cancer and its regulation by dihydrotestosterone, insulin-like growth factor I, and epidermal growth factor in the prostate cancer cell model LNCaP. Clin. Cancer Res. 10, 314-323 (Pubitemid 38114194)
22. McCulloch, D. R., Wylie, J. D., Longpre, J. M., Leduc, R., and Apte, S. S. (2010) 10 mM Glucosamine prevents activation of proADAMTS5 (aggrecanase-2) in transfected cells by interference with post-translational modification of furin. Osteoarthritis Cartilage 18, 455-463
23. Koo, B. H., Longpré, J. M., Somerville, R. P., Alexander, J. P., Leduc, R., and Apte, S. S. (2007) Regulation of ADAMTS9 secretion and enzymatic activity by its propeptide. J. Biol. Chem. 282, 16146-16154 (Pubitemid 47100362)
24. Horsley, V., Jansen, K. M., Mills, S. T., and Pavlath, G. K. (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113, 483-494 (Pubitemid 36588751)
25. Jansen, K. M., and Pavlath, G. K. (2006) Mannose receptor regulates myoblast motility and muscle growth. J. Cell Biol. 174, 403-413 (Pubitemid 44156770)
26. Park, I. H., and Chen, J. (2005) Mammalian target of rapamycin (mTOR) signaling is required for a late-stage fusion process during skeletal myotube maturation. J. Biol. Chem. 280, 32009-32017 (Pubitemid 41291952)
27. Hattori, N., Carrino, D. A., Lauer, M. E., Vasanji, A., Wylie, J. D., Nelson, C. M., and Apte, S. S. (2011) Pericellular versican regulates the fibroblastmyofibroblast transition. A role for ADAMTS5 protease-mediated proteolysis. J. Biol. Chem. 286, 34298-34310
28. Brown, H. M., Dunning, K. R., Robker, R. L., Pritchard, M., and Russell, D. L. (2006) Requirement for ADAMTS-1 in extracellular matrix remodeling during ovarian folliculogenesis and lymphangiogenesis. Dev. Biol. 300, 699-709 (Pubitemid 44909111)
29. Somerville, R. P., Longpre, J. M., Jungers, K. A., Engle, J. M., Ross, M., Evanko, S., Wight, T. N., Leduc, R., and Apte, S. S. (2003) Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J. Biol. Chem. 278, 9503-9513 (Pubitemid 36800443)
30. White, R. B., Biérinx, A. S., Gnocchi, V. F., and Zammit, P. S. (2010) Dynamics of muscle fiber growth during postnatal mouse development. BMC Dev. Biol. 10, 21
31. Bains, W., Ponte, P., Blau, H., and Kedes, L. (1984) Cardiac actin is the major actin gene product in skeletal muscle cell differentiation in vitro. Mol. Cell Biol. 4, 1449-1453 (Pubitemid 15131903)
32. Orkin, R. W., Knudson, W., and Toole, B. P. (1985) Loss of hyaluronatedependent coat during myoblast fusion. Dev. Biol. 107, 527-530
33. Raganathan, S., and Datta, K. (1995) Presence of hyaluronan binding protein in cardiac myoblasts and its altered level during myogenesis. Cell Biol. Int. 19, 161-165
34. Carrino, D. A., Sorrell, J. M., and Caplan, A. I. (1999) Dynamic expression of proteoglycans during chicken skeletal muscle development and maturation. Poult. Sci. 78, 769-777 (Pubitemid 129555221)
35. Jungers, K. A., Le Goff, C., Somerville, R. P., and Apte, S. S. (2005) Adamts9 is widely expressed during mouse embryo development. Gene Expr. Patterns 5, 609-617 (Pubitemid 40796606)
36. Stewart, M. C., Fosang, A. J., Bai, Y., Osborn, B., Plaas, A., and Sandy, J. D. (2006) ADAMTS5-mediated aggrecanolysis in murine epiphyseal chondrocyte cultures. Osteoarthritis Cartilage 14, 392-402
37. Demircan, K., Hirohata, S., Nishida, K., Hatipoglu, O. F., Oohashi, T., Yonezawa, T., Apte, S. S., and Ninomiya, Y. (2005) ADAMTS-9 is synergistically induced by interleukin-1α and tumor necrosis factor α in OUMS-27 chondrosarcoma cells and in human chondrocytes. Arthritis Rheum. 52, 1451-1460 (Pubitemid 40663937)
38. Velleman, S. G., Sporer, K. R., Ernst, C. W., Reed, K. M., and Strasburg, G. M. (2012) Versican, matrix Gla protein, and death-associated protein expression affect muscle satellite cell proliferation and differentiation. Poult. Sci. 91, 1964-1973
39. Velasco, J., Li, J., DiPietro, L., Stepp, M. A., Sandy, J. D., and Plaas, A. (2011) Adamts5 deletion blocks murine dermal repair through CD44-mediated aggrecan accumulation and modulation of transforming growth factor α1 (TGFα1) signaling. J. Biol. Chem. 286, 26016-26027
40. Kashiwagi, M., Tortorella, M., Nagase, H., and Brew, K. (2001) TIMP-3 is a potent inhibitor of aggrecanase 1 (ADAM-TS4) and aggrecanase 2 (ADAM-TS5). J. Biol. Chem. 276, 12501-12504
41. Liu, H., Chen, S. E., Jin, B., Carson, J. A., Niu, A., Durham, W., Lai, J. Y., and Li, Y. P. (2010) TIMP3. A physiological regulator of adult myogenesis. J. Cell Sci. 123, 2914-2921
42. Goldspink, G., and Ward, P. S. (1979) Changes in rodent muscle fibre types during postnatal growth, undernutrition and exercise. J. Physiol. 296, 453-469
43. Dupuis, L. E., McCulloch, D. R., McGarity, J. D., Bahan, A., Wessels, A., Weber, D., Diminich, A. M., Nelson, C. M., Apte, S. S., and Kern, C. B. (2011) Altered versican cleavage in ADAMTS5-deficient mice. A novel etiology of myxomatous valve disease. Dev. Biol. 357, 152-164
44. Enomoto, H., Nelson, C. M., Somerville, R. P., Mielke, K., Dixon, L. J., Powell, K., and Apte, S. S. (2010) Cooperation of two ADAMTS metalloproteases in closure of the mouse palate identifies a requirement for versican proteolysis in regulating palatal mesenchyme proliferation. Development 137, 4029-4038
45. Mittaz, L., Russell, D. L., Wilson, T., Brasted, M., Tkalcevic, J., Salamonsen, L. A., Hertzog, P. J., and Pritchard, M. A. (2004) Adamts-1 is essential for the development and function of the urogenital system. Biol. Reprod. 70, 1096-1105 (Pubitemid 38387721)
46. Russell, D. L., Doyle, K. M., Ochsner, S. A., Sandy, J. D., and Richards, J. S. (2003) Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J. Biol. Chem. 278, 42330-42339 (Pubitemid 37310502)
47. Rogerson, F. M., Stanton, H., East, C. J., Golub, S. B., Tutolo, L., Farmer, P. J., and Fosang, A. J. (2008) Evidence of a novel aggrecan-degrading activity in cartilage. Studies of mice deficient in both ADAMTS-4 and ADAMTS-5. Arthritis Rheum. 58, 1664-1673 (Pubitemid 351847519)
48. Tajbakhsh, S. (2009) Skeletal muscle stem cells in developmental versus regenerative myogenesis. J. Internal. Med. 266, 372-389