ADAM12 and α9β1 integrin are instrumental in human myogenic cell differentiation

Molecular Biology of the Cell

Volumn 16, Issue 2, 2005, Pages 861-870

  Lafuste, Peggy ^a   Sonnet, Corinne ^a   Chazaud, Bénédicte ^a   Dreyfus, Patrick A ^a   Gherardi, Romain K ^a,b   Wewer, Ulla M ^c   Authier, François Jérôme ^a,b  

^a FACULTÉ DE MÉDECINE   (France)

^b HENRI MONDOR HOSPITAL   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; BLOCKING ANTIBODY; GLYCOPROTEIN; INTEGRIN; INTEGRIN ALPHA9BETA1; METALLOPROTEINASE; METALLOPROTEINASE ADAM 12; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4; 4',6 DIAMIDINO 2 PHENYLINDOLE; ADAM 12 PROTEIN; ADAM PROTEIN; ANTISENSE OLIGONUCLEOTIDE; FLUORESCEIN ISOTHIOCYANATE; FLUORESCENT DYE; INDOLE DERIVATIVE; INTEGRIN ALPHA 9 BETA 1; MEMBRANE PROTEIN; PROPIDIUM IODIDE; RHODAMINE; TETRAMETHYLRHODAMINE ISOTHIOCYANATE;

ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL INTERACTION; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MYOBLAST; MYOTUBE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CONFOCAL MICROSCOPY; DRUG ANTAGONISM; DRUG EFFECT; DRUG INTERACTION; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; KINETICS; MEMBRANE FUSION; METABOLISM; MUSCLE CELL; MUSCLE DEVELOPMENT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERODIAGNOSIS; SKELETAL MUSCLE;

ADAM PROTEINS; ANTIBODIES, BLOCKING; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DRUG INTERACTIONS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; HUMANS; IMMUNOBLOTTING; INDOLES; INTEGRINS; KINETICS; MEMBRANE FUSION; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICROSCOPY, CONFOCAL; MUSCLE DEVELOPMENT; MUSCLE FIBERS; MUSCLE, SKELETAL; OLIGONUCLEOTIDES, ANTISENSE; PRECIPITIN TESTS; PROPIDIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODAMINES;

EID: 12844277132     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-03-0226     Document Type: Article

References (80)

1. Abe, E., Mocharla, H., Yamate, T., Taguchi, Y., and Manolagas, S. C. (1999). Meltrin-alpha, a fusion protein involved in multinucleated giant cell and osteoclast formation. Calcif. Tissue Int. 64, 508-515.
2. Abmayr, S. M., Balagopalan, L., Galletta, B. J., and Hong, S. J. (2003). Cell and molecular biology of myoblast fusion. Int. Rev. Cytol. 225, 33-89.
3. Asakura, M., et al. (2002). Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-epidermal growth factor: metalloproteinase inhibitors as a new therapy. Nat. Med. 8, 35-40.
4. Authier, F. J., Chazaud, B., Plonquet, A., Eliezer-Vanerot, M. C., Poron, F., Belec, L., Barlovatz-Meimon, G., and Gherardi, R. K. (1999). Differential expression of the IL-1 system components during in vitro myogenesis: implication of IL-1beta in induction of myogenic cell apoptosis. Cell Death Differ. 6, 1012-1021.
5. Barnoy, S., Glasner, T., and Kosower, N. S. (1996). The role of calpastatin (the specific calpain inhibitor) in myoblast differentiation and fusion. Biochem. Biophys. Res. Commun. 220, 933-938.
6. Baroffio, A., Aubry, J. P., Kaelin, A., Krause, R. M., Hamann, M., and Bader, C. R. (1993). Purification of human muscle satellite cells by flow cytometry. Muscle Nerve 16, 498-505.
7. Blanco-Bose, W. E., and Blau, H. M. (2001). Laminin-induced change in conformation of preexisting alpha7beta1 integrin signals secondary myofiber formation. Dev. Biol. 233, 148-160.
8. Blobel, C. P., Wolfsberg, T. G., Turck, C. W., Myles, D. G., Primakoff, P., and White, J. M. (1992). A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature 356, 248-252.
9. Borneman, A., Kuschel, R., and Fujisawa-Sehara, A. (2000). Analysis for transcript expression of meltrin alpha in normal, regenerating, and denervated rat muscle. J. Muscle Res. Cell Motil. 21, 475-480.
10. Burkin, D. J., and Kaufman, S. J. (1999). The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res. 296, 183-190.
11. Cao, Y., Kang, Q., Zhao, Z., and Zolkiewska, A. (2002). Intracellular processing of metalloprotease disintegrin ADAM12. J. Biol. Chem. 277, 26403-26411.
12. Cao, Y., Kang, Q., and Zolkiewska, A. (2001). Metalloprotease-disintegrin ADAM 12 interacts with alpha-actinin-1. Biochem. J. 357, 353-361.
13. Cao, Y., Zhao, Z., Gruszczynska-Biegala, J., and Zolkiewska, A. (2003). Role of metalloprotease disintegrin ADAM12 in determination of quiescent reserve cells during myogenic differentiation in vitro. Mol. Cell Biol. 23, 6725-6738.
14. Chazaud, B., Ricoux, R., Christov, C., Plonquet, A., Gherardi, R. K., and Barlovatz-Meimon, G. (2002). Promigratory effect of plasminogen activator inhibitor-1 on invasive breast cancer cell populations. Am. J. Pathol. 160, 237-246.
15. Chazaud, B., Sonnet, C., Lafuste, P., Bassez, G., Rimaniol, A. C., Poron, F., Authier, F. J., Dreyfus, P. A., and Gherardi, R. K. (2003). Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J. Cell Biol. 163, 1133-1143.
16. Choi, S. J., Han, J. H., and Roodman, G. D. (2001). ADAM 8, a novel osteoclast stimulating factor. J. Bone Miner. Res. 16, 814-822.
17. Crawley, S., Farrell, E. M., Wang, W., Gu, M., Huang, H. Y., Huynh, V., Hodges, B. L., Cooper, D. N., and Kaufman, S. J. (1997). The alpha7beta1 integrin mediates adhesion and migration of skeletal myoblasts on laminin. Exp. Cell Res. 235, 274-286.
18. De Rossi, M., Bernasconi, P., Baggi, F., de Waal, M. R., and Mantegazza, R. (2000). Cytokines and chemokines are both expressed by human myoblasts: possible relevance for the immune pathogenesis of muscle inflammation. Int. Immunol. 12, 1329-1335.
19. Dickson, G., Azad, A., Morris, G. E., Simon, H., Noursadeghi, M., and Walsh, F. S. (1992). Co-localization and molecular association of dystrophin with laminin at the surface of mouse and human myotubes. J. Cell Sci. 103, 1223-1233.
20. Doberstein, S. K., Fetter, R. D., Mehta, A. Y., and Goodman, C. S. (1997). Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J. Cell Biol. 136, 1249-1261.
21. Engvall, E., and Wewer, U. M. (2003). The new frontier in muscular dystrophy research: booster genes. FASEB J. 17, 1579-1584.
22. Eto, K., Huet, C., Tarui, T., Kupriyanov, S., Liu, H. Z., Puzon-McLaughlin, W., Zhang, X. P., Sheppard, D., Engvall, E., and Takada, Y. (2002). Functional classification of ADAMs based on a conserved motif for binding to integrin alpha 9beta 1, implications for sperm-egg binding and other cell interactions. J. Biol. Chem. 277, 17804-17810.
23. Eto, K., Puzon-McLaughlin, W., Sheppard, D., Sehara-Fujisawa, A., Zhang, X. P., and Takada, Y. (2000). RGD-independent binding of integrin alpha9beta1 to the ADAM-12 and -15 disintegrin domains mediates cell-cell interaction. J. Biol. Chem. 275, 34922-34930.
24. Friday, B. B., Mitchell, P. O., Kegley, K. M., and Pavlath, G. K. (2003). Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD. Differentiation 71, 217-227.
25. Fujio, Y., Guo, K., Mano, T., Mitsuuchi, Y., Testa, J. R., and Walsh, K. (1999). Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol. Cell. Biol. 19, 5073-5082.
26. Galliano, M. F., Huet, C., Frygelius, J., Polgren, A., Wewer, U. M., and Engvall, E. (2000). Binding of ADAM12, a marker of skeletal muscle regeneration, to the muscle-specific actin-binding protein, alpha-achnin-2, is required for myoblast fusion. J. Biol. Chem. 275, 13933-13939.
27. Gilpin, B. J., Loechel, F., Mattei, M. G., Engvall, E., Albrechtsen, R., and Wewer, U. M. (1998). A novel, secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo. J. Biol. Chem. 273, 157-166.
28. Gorza, L., and Vitadello, M. (2000). Reduced amount of the glucose-regulated protein GRP94 in skeletal myoblasts results in loss of fusion competence. FASEB J. 14, 461-475.
29. Hawke, T. J., and Garry, D. J. (2001). Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 92, 534-551.
30. He, Z. Y., Brakebusch, C., Fassler, R., Kreidberg, J. A., Primakoff, P., and Myles, D. G. (2003). None of the integrins known to be present on the mouse egg or to be ADAM receptors are essential for sperm-egg binding and fusion. Dev. Biol. 254, 226-237.
31. Hemler, M. E. (2001). Specific tetraspanin functions. J. Cell Biol. 155, 1103-1107.
32. Hirasawa, N., Sato, Y., Fujita, Y., and Ohuchi, K. (2000). Involvement of a phosphatidylinositol 3-kinase-p38 mitogen activated protein kinase pathway in antigen-induced IL-4 production in mast cells. Biochim. Biophys. Acta 1456, 45-55.
33. Hirsch, E., Lohikangas, L., Gullberg, D., Johansson, S., and Fassler, R. (1998). Mouse myoblasts can fuse and form a normal sarcomere in the absence of beta1 integrin expression. J. Cell Sci. 111, 2397-2409.
34. Hooft van Huijsduijnen, R. (1998). ADAM 20 and 21; two novel human testis-specific membrane metalloproteases with similarity to fertilin-alpha. Gene 206, 273-282.
35. Horsley, V., Friday, B. B., Matteson, S., Kegley, K. M., Gephart, J., and Pavlath, G. K. (2001). Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J. Cell Biol. 153, 329-338.
36. 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.
37. Horsley, V., and Pavlath, G. K. (2003). Prostaglandin F2(alpha) stimulates growth of skeletal muscle cells via an NFATC2-dependent pathway. J. Cell Biol. 161, 111-118.
38. Hougaard, S., Loechel, F., Xu, X., Tajima, R., Albrechtsen, R., and Wewer, U. M. (2000). Trafficking of human ADAM 12-L: retention in the trans-Golgi network. Biochem. Biophys. Res. Commun. 275, 261-267.
39. Huovila, A. P., Almeida, E. A., and White, J. M. (1996). ADAMs and cell fusion. Curr. Opin. Cell Biol. 8, 692-699.
40. Husmann, I., Soulet, L., Gautron, J., Martelly, I., and Barritault, D. (1996). Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev. 7, 249-258.
41. Iba, K., et al. (2000). The cysteine-rich domain of human ADAM 12 supports cell adhesion through syndecans and triggers signaling events that lead to betal integrin-dependent cell spreading. J. Cell Biol. 149, 1143-1156.
42. Iba, K., Albrechtsen, R., Gilpin, B. J., Loechel, F., and Wewer, U. M. (1999). Cysteine-rich domain of human ADAM 12 (meltrin alpha) supports tumor cell adhesion. Am. J. Pathol. 154, 1489-1501.
43. Jascur, T., Gilman, J., and Mustelin, T. (1997). Involvement of phosphatidylinositol 3-kinase in NFAT activation in T cells. J. Biol. Chem. 272, 14483-14488.
44. Jiang, B. H., Zheng, J. Z., and Vogt, P. K. (1998). An essential role of phosphatidylinositol 3-kinase in myogenic differentiation. Proc. Natl. Acad. Sci. USA 95, 14179-14183.
45. Kadota, N., Suzuki, A., Nakagami, Y., Izrani, T., and Endo, T. (2000). Endogenous meltrin alpha is ubiquitously expressed and associated with the plasma membrane but exogenous meltrin alpha is retained in the endoplasmic reticulum. J. Biochem. (Tokyo) 128, 941-949.
46. Kaliman, P., Vinals, F., Testar, X., Palacin, M., and Zorzano, A. (1996). Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J. Biol. Chem. 271, 19146-19151.
47. Kang, Q., Cao, Y., and Zolkiewska, A. (2001). Direct interaction between the cytoplasmic tail of ADAM 12 and the Src homology 3 domain of p85alpha activates phosphatidylinositol 3-kinase in C2C12 cells. J. Biol. Chem. 276, 24466-24472.
48. Kawaguchi, N., et al. (2003). ADAM12 induces actin cytoskeleton and extracellular matrix reorganization during early adipocyte differentiation by regulating {beta}1 integrin function. J. Cell Sci. 116, 3893-3904.
49. Kawaguchi, N., Xu, X., Tajima, R., Kronqvist, P., Sundberg, C., Loechel, F., Albrechtsen, R., and Wewer, U. M. (2002). ADAM 12 protease induces adipogenesis in transgenic mice. Am. J. Pathol. 160, 1895-1903.
50. Kratzschmar, J., Lum, L., and Blobel, C. P. (1996). Metargidin, a membrane-anchored metalloprotease-disintegrin protein with an RGD integrin binding sequence. J. Biol Chem. 271, 4593-4596.
51. Kronqvist, P., Kawaguchi, N., Albrechtsen, R., Xu, X., Schroder, H. D., Moghadaszadeh, B., Nielsen, F. C., Frohlich, C., Engvall, E., and Wewer, U. M. (2002). ADAM12 alleviates the skeletal muscle pathology in mdx dystrophic mice. Am. J. Pathol. 161, 1535-1540.
52. Kurisaki, T., Masuda, A., Osumi, N., Nabeshima, Y., and Fujisawa-Sehara, A. (1998), Spatially- and temporally-restricted expression of meltrin alpha (ADAM12) and beta (ADAM19) in mouse embryo. Mech. Dev. 73, 211-215.
53. Li, Y., Jiang, B., Ensign, W. Y., Vogt, P. K., and Han, J. (2000). Myogenic differentiation requires signalling through both phosphatidylinositol 3-kinase and p38 MAP kinase. Cell Signal. 12, 751-757.
54. Loechel, F., Fox, J. W., Murphy, G., Albrechtsen, R., and Wewer, U. M. (2000). ADAM 12-S cleaves IGFBP-3 and IGFBP-5 and is inhibited by TIMP-3. Biochem. Biophys. Res. Commun. 278, 511-515.
55. Loechel, F., Gilpin, B. J., Engvall, E., Albrechtsen, R., and Wewer, U. M. (1998). Human ADAM 12 (meltrin alpha) is an active metalloprotease. J. Biol. Chem. 273, 16993-16997.
56. Marcinkiewicz, C., Taooka, Y., Yokosaki, Y., Calvete, J. J., Marcinkiewicz, M. M., Lobb, R. R., Niewiarowski, S., and Sheppard, D. (2000). Inhibitory effects of MLDG-containing heterodimeric disintegrins reveal distinct structural requirements for interaction of the integrin alpha 9beta 1 with VCAM-1, tenascin-C, and osteopontin. J. Biol. Chem. 275, 31930-31937.
57. Mayer, U. (2003). Integrins: redundant or important players in skeletal muscle? J. Biol. Chem. 278, 14587-14590.
58. Moghadaszadeh, B., et al. (2003). Compensation for dystrophin-deficiency: ADAM12 overexpression in skeletal muscle results in increased alpha 7 integrin, utrophin and associated glycoproteins. Hum. Mol. Genet. 12, 2467-2479.
59. Nawrotzki, R., Willem, M., Miosge, N., Brinkmeier, H., and Mayer, U. (2003). Defective integrin switch and matrix composition at alpha 7-deficient myotendinous junctions precede the onset of muscular dystrophy in mice. Hum. Mol. Genet. 12, 483-495.
60. Palmer, E. L., Ruegg, C., Ferrando, R., Pytela, R., and Sheppard, D. (1993). Sequence and tissue distribution of the integrin alpha 9 subunit, a novel partner of beta 1 that is widely distributed in epithelia and muscle. J. Cell Biol. 123, 1289-1297.
61. Pavlath, G. K., and Horsley, V. (2003). Cell fusion in skeletal muscle-central role of NFATC2 in regulating muscle cell size. Cell Cycle 2, 420-423.
62. Primakoff, P., and Myles, D. G. (2002). Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science 296, 2183-2185.
63. Rau, A., Buttgereit, D., Holz, A., Fetter, R., Doberstein, S. K., Paululat, A., Staudt, N., Skeath, J., Michelson, A. M., and Renkawitz-Pohl, R. (2001). Rolling pebbles (rols) is required in Drosophila muscle precursors for recruitment of myoblasts for fusion. Development 128, 5061-5073.
64. Rosen, G. D., Sanes, J. R., LaChance, R., Cunningham, J. M., Roman, J., and Dean, D. C. (1992). Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis. Cell 69, 1107-1119.
65. Sanchez-Madrid, F., De Landazuri, M. O., Morago, G., Cebrian, M., Acevedo, A., and Bernabeu, C. (1986). VLA-3, a novel polypeptide association within the VLA molecular complex: cell distribution and biochemical characterization. Eur. J. Immunol. 16, 1343-1349.
66. Schwander, M., Leu, M., Stumm, M., Dorchies, O. M., Ruegg, U. T., Schittny, J., and Muller, U. (2003). Beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev. Cell 4, 673-685.
67. Shi, Z., Xu, W., Loechel, F., Wewer, U. M., and Murphy, L. J. (2000). ADAM 12, a disintegrin metalloprotease, interacts with insulin-like growth factor-binding protein-3. J. Biol. Chem. 275, 18574-18580.
68. Skuk, D., and Tremblay, J. P. (2000). Progress in myoblast transplantation: a potential treatment of dystrophies. Microsc. Res. Tech. 48, 213-222.
69. Tachibana, I., and Hemler, M. E. (1999). Role of transmembrane 4 superfamily (TM4SF) proteins CD9 and CD81 in muscle cell fusion and myotube maintenance. J. Cell Biol. 146, 893-904.
70. Taylor, M. V. (2003). Muscle differentiation: signalling cell fusion. Curr. Biol. 13, R964-R966.
71. Thodeti, C. K., et al. (2003). ADAM12/syndecan-4 signaling promotes beta 1 integrin-dependent cell spreading through protein kinase Calpha and RhoA. J. Biol. Chem. 278, 9576-9584.
72. Thornhill, M. H., Wellicome, S. M., Mahiouz, D. L., Lanchbury, J. S., Kyan-Aung, U., and Haskard, D. O. (1991). Tumor necrosis factor combines with IL-4 or IFN-gamma to selectively enhance endothelial cell adhesiveness for T cells. The contribution of vascular cell adhesion molecule-1-dependent and -independent binding mechanisms. J. Immunol. 146, 592-598.
73. Wang, A., Patrone, L., McDonald, J. A., and Sheppard, D. (1995). Expression of the integrin subunit alpha 9 in the murine embryo. Dev. Dyn. 204, 421-431.
74. Weskamp, G., Kratzschmar, J., Reid, M. S., and Blobel, C. P. (1996). MDC9, a widely expressed cellular disintegrin containing cytoplasmic SH3 ligand domains. J. Cell Biol. 132, 717-726.
75. White, J. M. (2003). ADAMs: modulators of cell-cell and cell-matrix interactions. Curr. Opin. Cell Biol. 15, 598-606.
76. Wolfsberg, T. G., and White, J. M. (1996). ADAMs in fertilization and development. Dev. Biol. 180, 389-401.
77. Yagami-Hiromasa, T., Sato, T., Kurisaki, T., Kamijo, K., Nabeshima, Y., and Fujisawa-Sehara, A. (1995). A metalloprotease-disintegrin participating in myoblast fusion. Nature 377, 652-656.
78. Yao, C. C., Ziober, B. L., Squillace, R. M., and Kramer, R. H. (1996). Alpha7 integrin mediates cell adhesion and migration on specific laminin isoforms. J. Biol. Chem. 271, 25598-25603.
79. Zhao, Z., Gruszczynska-Biegala, J., Cheuvront, T., Yi, H., von der, M. H., von der, M. K., Kaufman, S. J., and Zolkiewska, A. (2004). Interaction of the disintegrin and cysteine-rich domains of ADAM12 with integrin alpha7beta1. Exp. Cell Res. 298, 28-37.
80. Zolkiewska, A. (1999). Disintegrin-like/cysteine-rich region of ADAM 12 is an active cell adhesion domain. Exp. Cell Res. 252, 423-431.