Summary
The expression of the CD24 molecule, a glycoprotein expressed at the surface of most B lymphocytes and differentiating neuroblasts, was studied in developing nerve and muscle (after 16 weeks of gestation), normal adult and various diseased human muscles using immunohistochemistry and Western blot analysis. Immunohistochemical studies demonstrated that: (1) in developing muscles, fibers did not express CD24, whereas only some mesenchymal areas, also expressing neural cell adhesion molecule (N.CAM) and vimentin, and developing nerves were positive; (2) in normal adult muscles, CD24 immunoreactivity was observed only in some unmyelinated nerve fibers-intra and extra fusal muscle fibers, satellite cells and neuromuscular junctions were negative; and (3) in all diseased muscles studied here, CD24 expression was always associated with a subpopulation of regenerative fibers. These fibers also expressed vimentin, desmin, developmental myosin heavy chain, N.CAM and its polysialylated isoforms (PSA-N.CAM). The number of CD24-positive fibers was always lower than that of PSA-N.CAM-positive fibers. Denervated fibers and vacuolated muscle fibers never expressed CD24. Western blot analysis indicated that the apparent molecular mass of CD24 antigen was different between muscle and developing nervous tissues, suggesting that CD24 glycosylation is tissue specific. Since the molecule was not expressed in developing human muscle fibers, it strongly suggests that regenerative and fetal myotubes are different with respect to the CD24 molecule expression.
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Boisseau S, Nedelec J, Poirier V, Rougon G, Simonneau M (1991) Analysis of high PSA-N.CAM expression during mammalian spinal cord and peripheral nervous system development. Development 112: 69–82
Bornemann A, Schmalbruch H (1992) Desmin and vimentin in regenerating muscles. Muscle Nerve 15: 14–20
Brocks L, Jap PHK, Ramaekers FCS, Stadhouders AM (1991) Vimentin and desmin expression in degenerating and regenerating dystrophic muscles. Virchows Arch [B] 61: 89–96
Carlsson M, Nilsson K (1989) Reactivity of workshop B-cell antibodies with B-CLL cells induced to differentiate with or without concomitant proliferation. In: W Knapp, et al (eds) Leucocyte typing IV. Oxford University Press, Oxford, pp 206–218
Cashman N, Covault J, Wollman R, Sanes J (1987) Neural cell adhesion molecule in normal, denervated and myopathic human muscle. Ann Neurol 21: 481–489
Cossu G, Molinaro M (1987) Cell heterogeneity in the myogenic lineage. Curr Top Dev Biol 23: 185–208
Covault J, Merlie JP, Goridis C, Sanes JR (1986) Molecular forms of N.CAM and its RNA in developing and denervated skeletal muscle. J Cell Biol 102: 731–739
Cros D, Pearson C, Verity MA (1980) Polymyositis-Dermatomyositis. Diagnosis and prognostic significance of muscle alkaline phosphatase. Am J Pathol 101: 159–176
Draeger A, Weeds AG, Fitzsimons B (1987) Primary, secondary and tertiary myotubes in developing skeletal muscle: a new approach to the analysis of human myogenesis. J Neurol Sci 81: 19–43
Engel P, Ingles J, Gallart T, Vives J (1987) Changes in the expression of B cell surface antigen detected by the workshop CD 24 monoclonal antibodies following in vitro activation. In: McMichael AJ, et al (eds) Leucocyte typing III. Oxford University Press, Oxford, pp 368–382
Figarella-Branger D, Nedelec J, Pelissier JF, Boucraut J, Bianco N, Rougon G (1990) Expression of various isoforms of neural cell adhesion molecules and their highly polysialylated counterparts in diseased human muscles. J Neurol Sci 98: 21–36
Figarella-Branger D, Pellissier JF, Bianco N, Pons F, Leger JJ; Rougon G (1992) Expression of various N.CAM isoforms in human embryonic muscles: correlation with myosin heavy chain phenotypes. J Neurol Exp Pathol 51: 12–23
Figarella-Branger D, Calore EE, Boucraut J, Bianco N, Rougon G and Pellissier JF (1992) Expression of cell surface and cytoskeleton developmentally regulated proteins in adult centronuclear myopathies. J Neurol Sci 109: 69–76
Hartley RS, Brandman E, Yablonka-Reuveni Z (1991) Myoblasts from fetal and adult skeletal muscle regulate myosin expression differently. Dev Biol 148: 249–260
Kay R, Takei F, Humphries RK (1990) Expression cloning of a cDNA encoding M1/69-J11d heat-stable antigens. J Immunol 145: 1952–1959
Kay R, Rosten PM, Humphries RK (1991) CD 24, a signal transducer modulating B cell activation response, is a very short peptide with a glycosyl phosphatidylinositol membrane anchor. J Immunol 147: 1412–1416
Ling NR, Maclennan ICM, Mason DY (1987) B-cell and plasma cell antigens: new and previously defined clusters. In: McMichael AJ, et al (eds) Leucocyte typing III. Oxford University Press, Oxford, pp 302–315
Linton PJ, Decker DJ, Klinman NR (1989) Primary antibodyforming cells and secondary B cells are generated from separate precursor cell subpopulations. Cell 59: 1049–1059
Marini JF, Pons F, Anoal F, Fardeau M, Léger JJ (1990) Immunocytochemical study of myosin changes in muscle fibers of DMD boys and symptomatic carriers of DMD identified by antidystrophin monoclonal antibodies (abstract). J Neurol Sci 98: 420
Miller JB (1992) Myoblast diversity in skeletal myogenesis: how much and to what end? Cell 69: 1–3
Mittler RS, Talle MA, Carpenter K, Rao PE, Goldstein G (1983) Generation and characterization of monoclonal antibodies reactive with human B lymphocytes. J Immunol 131: 1754–1761
Montarras D, Chelly J, Bober E, Arnold H, Ott MO, Gros F, Pinset C (1991) Developmental pattern in the expression of myf 5, myo D, myogenin, and mrf4 during myogenesis. New Biologist 3: 592–600
Nedelec J, Pierres M, Moreau H, Barbet J, Naquet P, Faivre-Sarrailh C, Rougon G (1992) Isolation and characterization of a novel glycosyl-phosphatidyl inositol anchored glycoconjugate expressed by developing neurons. Eur J Biochem 203: 433–442
Pezzutto A, Behur F, Callard RE (1989) Flow cytometry analysis of the B-cell panel: joint report. In: Knapp W, et al (eds) Leucocyte typing IV. Oxford University Press, Oxford, pp 165–181
Pirruccello ST, Lebien TW (1986) The human B cell-associated antigen CD24 is a single chain sialoglycoprotein. J Immunol 136: 3779–3784
Pons F, Leger J, Chevallay M, Tomé FMS, Fardeau M, Léger JJ (1986) Immunocytochemical analysis of myosin heavy chain in human fetal skeletal muscles. J Neurol Sci 76: 151–163
Rougon G, Marshak D (1986) Structural and immunological characterization of the amino-terminal domain of mammalian neural cell adhesion molecules. J Biol Chem 261: 3396–3401
Rougon G, Deagostini-Bazin H, Hirn M, Goridis C (1982) Tissue and developmental stage specific forms of a neural cell surface antigen linked to differences in glycosylation of a common polypeptide. EMBO J 1: 1239–1244
Rougon G, Dubois C, Buckley N, Magnani J, Zollinger W (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N.CAM. J Cell Biol 103: 2429–2437
Rougon G, Alterman LA, Dennis K, Guo XJ, Kinnon C (1991) The murine heat-stable antigen: a different antigen expressed in both the hematolymphoid and neural cell lineages. Eur J Immunol 21: 1397–1402
Sarnat HB (1990) Myotubular myopathy: arrest of morphogenesis of myofibers associated with persistence of fetal vimentin and desmin. Four cases compared with fetal and neonatal muscle. Can J Neurol Sci 17: 109–123
Stockinger H, Majdic O, Koller U, Knapp M (1987) Subclustering of the CD24 cluster. In: McMichael AJ, et al (eds) Leucocyte typing III. Oxford University Press, Oxford, pp 367–375
Vater R, Cullen MJ, Nicholson LVB, Harris JB (1992) The fate of desmin and titin during the degeneration and regeneration of the soleus muscle of the rat. Acta Neuropathol 84: 278–288
Walsh F, Moore S (1985) Expression of cell adhesion molecule N.CAM in diseases of human adult skeletal muscle. Neurosci Lett 59: 73–78
Wang CY, Azzo W, Al-Katib A, Chiorrazzi N, Knowles DM (1984) Preparation and characterization of monoclonal antibodies recognizing three distinct differentiation antigens (BL1, BL2, BL3) on human lymphocytes. J Immunol 133: 684–688
Yablonka-Reuveni Z, Maneroff M (1990) Temporal differences in desmin expression between myoblasts from embryonic and adult chicken skeletal muscle. Differentiation 45: 21–28
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Supported by the Assistance Publique de Marseille (to D.F.B.) institutional grants from CNRS (to G.R.) and University (to G.R. and D.F.B.), grants from Fédération des Centres de Lutte contre le Cancer (to G.R.), from the Ligue Départementale du Var contre le Cancer (to D.F.B.), and from Association Française contre les Myopathies (to G.R.).
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Figarella-Branger, D., Moreau, H., Pellissier, J.F. et al. CD24, a signal-transducing molecule expressed on human B lymphocytes, is a marker for human regenerating muscle. Acta Neuropathol 86, 275–284 (1993). https://doi.org/10.1007/BF00304142
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DOI: https://doi.org/10.1007/BF00304142