Neural cell adhesion molecule (NCAM) marks adult myogenic cells committed to differentiation

Experimental Cell Research

Volumn 314, Issue 7, 2008, Pages 1553-1565

  Capkovic, Katie L ^a   Stevenson, Severin ^a,b   Johnson, Marc C ^a   Thelen, Jay J ^a,b   Cornelison, D D W ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

Adult myogenesis; Membrane raft; Muscle regeneration; Myogenic differentiation; Neural cell adhesion molecule; Satellite cell

Indexed keywords

CREATINE KINASE MM; MYOGENIN; NERVE CELL ADHESION MOLECULE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MOUSE; MUSCLE CELL; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SCANNING ELECTRON MICROSCOPY; TANDEM MASS SPECTROMETRY;

EID: 84881193992     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.01.021     Document Type: Article

References (75)

1. Christ B., and Brand-Saberi B. Limb muscle development. Int. J. Dev. Biol. 46 (2002) 905-914
2. Grounds M.D. Towards understanding skeletal-muscle regeneration. Pathol. Res. Pract. 187 (1991) 1-22
3. Hawke T.J., and Garry D.J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91 (2001) 534-551
4. Shi X., and Garry D.J. Muscle stem cells in development, regeneration, and disease. Genes Dev. 20 (2006) 1692-1708
5. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9 (1961) 493-498
6. Bischoff R. Analysis of muscle regeneration using single myofibers in culture. Med. Sci. Sports Exerc. 21 (1989) S164-S172
7. Grounds M.D. Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. "Towards Prolongation of the Healthy Life Span" (1998), New York Acad Sciences, New York
8. Schultz E., and McCormick K.M. Skeletal muscle satellite cells. Rev. Physiol., Biochem. Pharmacol. 123 (1994) 213-257
9. Kuang S., Kuroda K., Le Grand F., and Rudnicki M.A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129 (2007) 999-1010
10. Angello J.C., and Hauschka S.D. Skeletal muscle satellite cells: timelapse videomicroscopic evidence that renewal is stochastic. BAM 6 (1996) 491-502
11. Ferrari G., Cusella-DeAngelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., and Malvilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279 (1988) 1528-1530
12. Krauss R.S., Cole F., Gaio U., Takaesu G., Zhang W., and Kang J.S. Close encounters: regulation of vertebrate skeletal myogenesis by cell-cell contact. J. Cell Sci. 118 (2005) 2355-2362
13. Charge S.B., and Rudnicki M.A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84 (2004) 209-238
14. Maley M.A.L., Davies M.J., and Grounds M.D. Extracellular-matrix, growth-factors, genetics - their influence on cell proliferation and mytube formation in primary cultures of adult mouse skeletal muscle. Exp. Cell Res. 219 (1995) 169-179
15. Brown D.A., and London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14 (1998) 111-136
16. Pike L.J. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 47 (2006) 1597-1598
17. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat. Rev., Mol. Cell Biol. 1 (2000) 31-39
18. Parton R.G., and Richards A.A. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4 (2003) 724-738
19. Yamazaki S., Iwama A., Takayanagi S., Morita Y., Eto K., Ema H., and Nakauchi H. Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J. 25 (2006) 3515-3523
20. Yamazaki S., Iwama A., Morita Y., Eto K., Ema H., and Nakauchi H. Cytokine signaling, lipid raft clustering and HSC hibernation. Ann. N. Y. Acad. Sci. (2007) 54-63
21. Cornelison D.D., Wilcox-Adelman S.A., Goetinck P.F., Rauvala H., Rapraeger A.C., and Olwin B.B. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 18 (2004) 2231-2236
22. Larson D.R., Johnson M.C., Webb W.W., and Vogt V.M. Visualization of retrovirus budding with correlated light and electron microscopy. Proc. Natl. Acad. Sci. 102 (2005) 15453-15458
23. Linkhart T.A., Clegg C.H., and Hauschka S.D. Control of mouse myoblast commitment to terminal differentiation by mitogens. J. Supramol. Struct. 14 (1980) 483-498
24. Clegg C.H., Linkhart T.A., Olwin B.B., and Hauschka S.D. Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J. Cell Biol. 105 (1987) 949-956
25. Brown D.A., and Rose J.K. Sorting of Gpi-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell-surface. Cell 68 (1992) 533-544
26. Foster L.J., De Hoog C.L., and Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 5813-5818
27. Lagerholm B.C., Weinreb G.E., Jacobson K., and Thompson N.L. Detecting microdomains in intact cell membranes. Annu. Rev. Phys. Chem. 56 (2005) 309-336
28. Sotobori T., Ueda T., Myoui A., Yoshioka K., Nakasaki M., Yoshikawa H., and Itoh K. Bone morphogenetic protein-2 promotes the haptotactic migration of murine osteoblastic and osteosarcoma cells by enhancing incorporation of integrin beta 1 into lipid rafts. Exp. Cell Res. 312 (2006) 3927-3938
29. Pande G. The role of membrane lipids in regulation of integrin functions. Curr. Opin. Cell Biol. 12 (2000) 569-574
30. Thodeti C.K., Albrechtsen R., Grauslund M., Asmar M., Larsson C., Takada Y., Mercurio A.M., Couchman J.R., and Wewer U.M. ADAM12/syndecan-4 signaling promotes beta 1 integrin-dependent cell spreading through protein kinase Calpha and RhoA. J. Biol. Chem. 278 (2003) 9576-9584
31. Bass M.D., Morgan M.R., and Humphries M.J. Integrins and syndecan-4 make distinct, but critical, contributions to adhesion contact formation. Soft Matter 3 (2007) 372-376
32. Tkachenko E., and Simons M. Clustering induces redistribution of syndecan-4 core protein into raft membrane domains. J. Biol. Chem. 277 (2002) 19946-19951
33. Davis D.B., Doherty K.R., Delmonte A.J., and McNally E.M. Calcium-sensitive phospholipid binding properties of normal and mutant ferlin C2 domains. J. Biol. Chem. 277 (2002) 22883-22888
34. Lennon N.J., Kho A., Bacskai B.J., Perlmutter S.L., Hyman B.T., and Brown R.H. Dysferlin interacts with Annexins A1 and A2 and mediates sarcolemmal wound-healing. J. Biol. Chem. 278 (2003) 50466-50473
35. Matsuda C., Hayashi Y.K., Ogawa M., Aoki M., Murayama K., Nishino I., Nonaka I., Arahata K., and Brown R.H. The sarcolemmal proteins dysferlin and caveolin-3 interact in skeletal muscle. Hum. Mol. Genet. 10 (2001) 1761-1766
36. Hernandez-Deviez D.J., Martin S., Laval S.H., Lo H.P., Cooper S.T., North K.N., Bushby K., and Parton R.G. Aberrant dysferlin trafficking in cells lacking caveolin or expressing dystrophy mutants of caveolin-3. Hum. Mol. Genet. 15 (2006) 129-142
37. Inoue M., Wakayama Y., Kojima H., Shibuya S., Jimi T., Oniki H., Nishino I., and Nonaka I. Expression of myoferlin in skeletal muscles of patients with dysferlinopathy. Tohoku J. Exp. Med. 209 (2006) 109-116
38. Glover L., and Brown R.H. Dysferlin in membrane trafficking and patch repair. Traffic 8 (2007) 785-794
39. Galbiati F., Engelman J.A., Volonte D., Zhang X.L., Minetti C., Li M., Hou Jr. H., Kneitz B., Edelmann W., and Lisanti M.P. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J. Biol. Chem. 276 (2001) 21425-21433
40. Logan C.Y., and Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 781-810
41. Eastman Q., and Grosschedl R. Regulation of LEF-1/TCF transcription factors by Wnt and other signals. Curr. Opin. Cell Biol. 11 (1999) 233-240
42. Seale P., Polesskaya A., and Rudnicki M.A. Adult stem cell specification by Wnt signaling in muscle regeneration. Cell Cycle 2 (2003) 418-419
43. Rochat A., Fernandez A., Vandromme M., Moles J.P., Bouschet T., Carnac G., and Lamb N.J. Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol. Biol. Cell 15 (2004) 4544-4555
44. Steelman C.A., Recknor J.C., Nettleton D., and Reecy J.M. Transcriptional profiling of myostatin-knockout mice implicates Wnt signaling in postnatal skeletal muscle growth and hypertrophy. FASEB J. 20 (2006) 580-582
45. Brack A.S., Conboy M.J., Roy S., Lee M., Kuo C.J., Keller C., and Rando T.A. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317 (2007) 807-810
46. Novak A., Hsu S.C., Leung-Hagesteijn C., Radeva G., Papkoff J., Montesano R., Roskelley C., Grosschedl R., and Dedhar S. Cell adhesion and the integrin-linked kinase regulate the LEF-1 and beta-catenin signaling pathways. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 4374-4379
47. Galbiati F., Volonte D., Brown A.M., Weinstein D.E., Ben-Ze'ev A., Pestell R.G., and Lisanti M.P. Caveolin-1 expression inhibits Wnt/beta-catenin/Lef-1 signaling by recruiting beta-catenin to caveolae membrane domains. J. Biol. Chem. 275 (2000) 23368-23377
48. Mermelstein C.S., Portilho D.M., Medeiros R.B., Matos A.R., Einicker-Lamas M., Tortelote G.G., Vieyra A., and Costa M.L. Cholesterol depletion by methyl-beta-cyclodextrin enhances myoblast fusion and induces the formation of myotubes with disorganized nuclei. Cell Tissue Res. 319 (2005) 289-297
49. Mermelstein C.S., Portilho D.M., Mendes F.A., Costa M.L., and Abreu J.G. Wnt/beta-catenin pathway activation and myogenic differentiation are induced by cholesterol depletion. Differentiation 75 (2007) 184-192
50. Niethammer P., Delling M., Sytnyk V., Dityatev A., Fukami K., and Schachner M. Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J. Cell Biol. 157 (2002) 521-532
51. Simson R., Yang B., Moore S.E., Doherty P., Walsh F.S., and Jacobson K.A. Structural mosaicism on the submicron scale in the plasma membrane. Biophys. J. 74 (1998) 297-308
52. Leshchyns'ka I., Sytnyk V., Morrow J.S., and Schachner M. Neural cell adhesion molecule (NCAM) association with PKCbeta2 via betaI spectrin is implicated in NCAM-mediated neurite outgrowth. J. Cell Biol. 161 (2003) 625-639
53. Hurko O., and Walsh F.S. Human fetal muscle-specific antigen is restricted to regenerating myofibers in diseased adult muscle. Neurology 33 (1983) 737-743
54. Fidzianska A., and Kaminska A. Neural cell adhesion molecule (N-CAM) as a marker of muscle tissue alternations. Review of the literature and own observations. Folia Neuropathol. 33 (1995) 125-128
55. Covault J., and Sanes J.R. Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J. Cell Biol. 102 (1986) 716-730
56. Moore S.E., Thompson J., Kirkness V., Dickson J.G., and Walsh F.S. Skeletal muscle neural cell adhesion molecule (N-CAM): changes in protein and mRNA species during myogenesis of muscle cell lines. J. Cell Biol. 105 (1987) 1377-1386
57. Kubo Y. Comparison of initial stages of muscle differentiation in rat and mouse myoblastic and mouse mesodermal stem cell lines. J. Physiol. 442 (1991) 743-759
58. Irintchev A., Zeschnigk M., Starzinski-Powitz A., and Wernig A. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 199 (1994) 326-337
59. Grounds M.D. Towards understanding skeletal muscle regeneration. Pathol. Res. Pract. 187 (1991) 1-22
60. Irintchev A., Zeschnigk M., Starzinski-Powitz A., and Wernig A. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 199 (1994) 326-337
61. Walmod P.S., Kolkova K., Berezin V., and Bock E. Zippers make signals: NCAM-mediated molecular interactions and signal transduction. Neurochem. Res. 29 (2004) 2015-2035
62. Harder T., Scheiffele P., Verkade P., and Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141 (1998) 929-942
63. Parton R.G., and Simons K. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8 (2007) 185-194
64. Cornelison D.D., Filla M.S., Stanley H.M., Rapraeger A.C., and Olwin B.B. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 239 (2001) 79-94
65. Volonte D., Liu Y., and Galbiati F. The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J. 19 (2005) 237-239
66. Cornelison D.D.W. Gene Expression in wild-type and MyoD-null satellite cells: regulation of activation, proliferation, and myogenesis (1998), California Institute of Technology, Pasadena
67. Dubois C., Figarellabranger D., Pastoret C., Rampini C., Karpati G., and Rougon G. Expression of Ncam and its polysialylated isoforms during Mdx mouse muscle regeneration and in-vitro myogenesis. Neuromuscul. Disord. 4 (1994) 171-182
68. Lyons G.E., Moore R., Yahara O., Buckingham M.E., and Walsh F.S. Expression of NCAM isoforms during skeletal myogenesis in the mouse embryo. Dev. Dyn. 194 (1992) 94-104
69. Glaser T., Brose C., Franceschini I., Hamann K., Smorodchenko A., Zipp F., Dubois-Dalcq M., and Brustle O. NCAM polysialylation enhances the sensitivity of ES cell-derived neural precursors to migration guidance cues. Stem Cells (2007) 3016-3025
70. Johnson C.P., Fujimoto I., Rutishauser U., and Leckband D.E. Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem. 280 (2005) 137-145
71. Suzuki M., Angata K., Nakayama J., and Fukuda M. Polysialic acid and mucin type o-glycans on the neural cell adhesion molecule differentially regulate myoblast fusion. J. Biol. Chem. 278 (2003) 49459-49468
72. Dickson G., Peck D., Moore S.E., Barton C.H., and Walsh F.S. Enhanced myogenesis in NCAM-transfected mouse myoblasts. Nature 344 (1990) 348-351
73. Peck D., and Walsh F.S. Differential effects of over-expressed neural cell adhesion molecule isoforms on myoblast fusion. J. Cell Biol. 123 (1993) 1587-1595
74. Fazeli S., Wells D.J., Hobbs C., and Walsh F.S. Altered secondary myogenesis in transgenic animals expressing the neural cell adhesion molecule under the control of a skeletal muscle alpha-actin promoter. J. Cell Biol. 135 (1996) 241-251
75. Charlton C.A., Mohler W.A., and Blau H.M. Neural cell adhesion molecule (NCAM) and myoblast fusion. Dev. Biol. 221 (2000) 112-119