Bcl-2 expression identifies an early stage of myogenesis and promotes clonal expansion of muscle cells

Journal of Cell Biology

Volumn 142, Issue 2, 1998, Pages 537-544

  Dominov, Janice A ^a,b   Dunn, Jonathan J ^a   Miller, Jeffrey Boone ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Bcl 2; Myoblast; Myogenin; Skeletal muscle

Indexed keywords

DESMIN; HYBRID PROTEIN; MYOGENIC FACTOR; STAUROSPORINE;

ANIMAL CELL; ARTICLE; CELL ADHESION; GENE EXPRESSION; MOLECULAR CLONING; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; DESMIN; DNA PRIMERS; DNA-BINDING PROTEINS; GENE EXPRESSION; GENES, BCL-2; GENETIC MARKERS; MICE; MICE, KNOCKOUT; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; POLYMERASE CHAIN REACTION; STAUROSPORINE; TRANS-ACTIVATORS;

EID: 0032572533     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.2.537     Document Type: Article

References (53)

1. Baroffio, A., M. Hamann, L. Bernheim, M.L. Bochatonpiallat, G. Gabbiani, and C.R. Bader. 1996. Identification of self-renewing myoblasts in the progeny of single human muscle satellite cells. Differentiation (Camb.). 60:47-57.
2. Bischoff, R., and C. Heintz. 1994. Enhancement of skeletal muscle regeneration. Dev. Dyn. 201:41-54.
3. Blau, H.M., G.K. Pavlath, E.C. Hardeman, C.-P. Chiu, L. Silberstein, S.B. Webster, S.C. Miller, and C. Webster. 1985. Plasticity of the differentiated state. Science. 230:758-766.
4. Block, N.E., Z. Zhu, A.M. Kachinsky, J.A. Dominov, and J.B. Miller. 1996. Acceleration of somitic myogenesis in embryos of myogenin promoter-MRF4 transgenic mice. Dev. Dyn. 207:382-394.
5. Brown, R.H., and J.B. Miller. 1996. Progress, problems and prospects for gene therapy in muscle. Curr. Opin. Rheum. 8:539-543.
6. Clegg, C.H., and S.D. Hauschka. 1987. Heterokaryon analysis of muscle differentiation: regulation of the postmitotic state. J. Cell Biol. 105:937-947.
7. Cornelison, D.D.W., and B.J. Wold. 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:270-283.
8. Dominov, J.A., and J.B. Miller. 1996. POU homeodomain genes in myogenesis. Dev. Genet. 19:108-118.
9. George-Weinstein, M., R.F. Foster, J.V. Gerhart, and S.J. Kaufman. 1993. In vitro and in vivo expression of α7 integrin and desmin define the primary and secondary myogenic lineages. Dev. Biol. 156:209-229.
10. Haldar, S., J. Chintapalli, and C.M. Croce. 1996. Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res. 56:1253-1255.
11. Hauschka, S.D., T.A. Linkhart, C. Clegg, and G. Merrill. 1979. Clonal studies of human and mouse muscle. In Muscle Regeneration. A. Mauro, editor. Raven Press Ltd., New York. 311-322.
12. Ibi, T., K. Sahashi, L. Jing, G. Zhang, and T. Mitsuma. 1996. Immunostaining of anti-Bcl-2 antibody in diseased human muscles [Japanese]. Clin. Neurol. 36: 735-740.
13. Irintchev, A., M. Zeschnigk, A. Starzinski-Powitz, and A. Wernig. 1994. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 199:326-337.
14. Jacobsen, M.D., J.F. Burne, and M.C. Raff. 1994. Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO (Eur. Mol. Biol. Organ.) J. 13:1899-1910.
15. Jacobsen, M.D., M. Weil, and M.C. Raff. 1996. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell Biol. 133: 1041-1051.
16. Kachinsky, A.M., J.A. Dominov, and J.B. Miller. 1994. Myogenesis and the intermediate filament protein, nestin. Dev. Biol. 165:216-228.
17. Kamada, S., A. Shimono, Y. Shinto, T. Tsujimura, T. Takahasi, T. Noda, Y. Kitamura, H. Kondoh, and Y. Tsujimoto. 1995. bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res. 55:354-359.
18. Kirschenbaum, L.A., and D. de Moissac. 1997. The bcl-2 gene product prevents programmed cell death of ventricular myocytes. Circulation. 96:1580-1585.
19. Korsmeyer, S.J. 1995. Regulators of cell death. Trends Genet. 11:101-105.
20. Krajewski, S., A. Tanaka, S. Takayama, M.J. Schibler, W. Fenton, and J.C. Reed. 1993. Investigations of the subcellular distribution of the Bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum and outer mitochondrial membranes. Cancer Res. 53:4701-4714.
21. Krajewski, S., M. Krajewska, A. Shabaik, H.-G. Wang, S. Irie, L. Fong, and J.C. Reed. 1994. Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res. 54:5501-5507.
22. Krajewski, S., S. Bodrug, M. Krajewska, A. Shabaik, R. Gascoyne, K. Berean, and J.C. Reed. 1995. Immunohistochemical analysis of Mcl-1 protein in human tissues. Am. J. Pathol. 146:1309-1319.
23. Kroemer, G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3:614-620.
24. Mampuru, L., S.-J. Chen, J. Kalenick, M.E. Bradley, and T. -C. Lee. 1996. Analysis of events associated with serum deprivation-induced apoptosis in C3H/Sol8 muscle satellite cells. Exp. Cell Res. 226:372-380.
25. Matsuda, R., A. Nishikawa, and H. Tanaka. 1995. Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans Blue: evidence for apoptosis in dystrophin-deficient muscle. Biochem. J. 118:959-964.
26. McClearn, D., R. Medville, and D. Noden. 1995. Muscle cell death during the development of head and neck muscles in the chick embryo. Dev. Dyn. 202: 365-377.
27. Merritt, A.J., C.S. Potten, A.J. Watson, D.Y. Loh, K. Nakayama, K. Nakayama, and J.A. Hickman. 1995. Differential expression of bcl-2 in intestinal epithelia. Correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia. J. Cell Sci. 108:2261-2271.
28. Michaelidis, T.M., M. Sendtner, J.D. Cooper, M.S. Airaksinen, B. Holtmann, M. Meyer, and H. Thoenen. 1996. Inactivation of Bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron. 17:75-89.
29. Miller, J.B. 1990. Myogenic programs of mouse muscle cell lines: expression of myosin heavy chain isoforms, MyoD1, and myogenin. J. Cell Biol. 111:1149-1160.
30. Miller, J.B. 1992. Myoblast diversity in skeletal myogenesis: how much and to what end? Cell. 69:1-3.
31. Miller, J.B., and F.E. Stockdale. 1986. Developmental regulation of the multiple myogenic cell lineages of the avian embryo. J. Cell Biol. 103:2197-2208.
32. Montarras, D., J. Chelly, E. Bober, H. Arnold, M.O. Ott, F. Gros, and C. Pinset. 1991. Developmental patterns in the expression of Myf5, MyoD, myogenin, and MRF4 during myogenesis. New Biol. 3:592-600.
33. Nakayama, K., K.-I. Nakayama, I. Negishi, I. Kuida, H. Sawa, and D.Y. Loh. 1994. Targeted disruption of Bcl-2aβ in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc. Nat. Acad. Sci. USA. 91: 3700-3704.
34. Negrini, M., E. Silini, C. Kozak, Y. Tsujimoto, and C.M. Croce. 1987. Molecular analysis of mbcl-2: structure and expression of the murine gene homologous to the human gene involved in follicular lymphoma. Cell. 49:455-463.
35. Peck, D., and F.S. Walsh. 1993. Differential effects of over-expressed neural cell adhesion molecule isoforms on myoblast fusion. J. Cell Biol. 123:1587-1595.
36. Polakowska, R.R., M. Piacentini, R. Bartlett, L.A. Goldsmith, and A.R. Haake. 1994. Apoptosis in human skin development: morphogenesis, periderm, and stem cells. Dev. Dyn. 199:176-188.
37. Rastinejad, F., and H.M. Blau. 1993. Genetic complementation reveals a novel regulatory role for 3′ untranslated regions in growth and differentiation. Cell. 72:903-917.
38. Reed, J.C. 1997. Double identity for proteins of the Bcl-2 family. Nature. 387: 773-776.
39. Rutz, R., C. Haney, and S.D. Hauschka. 1982. Spatial analysis of limb bud myogenesis: a proximodistal gradient of muscle colony-forming cells in chick embryo leg buds. Dev. Biol. 90:399-411.
40. Sandri, M., M. Podhorska-okolow, V. Geromel, C. Rizzi, P. Arslan, C. Franceshci, and U. Carraro. 1997. Exercise induces myonuclear ubiquitination and apoptosis in dystrophin-deficient muscle of mice. J. Neuropathol. Exp. Neurol. 56:45-57.
41. Skapek, S.X., J. Rhee, D.B. Spicer, and A.B. Lassar. 1995. Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science. 267:1022-1024.
42. Smith, T.H., and J.B. Miller. 1992. Distinct myogenic programs of embryonic and fetal mouse muscle cells: expression of the perinatal myosin heavy chain isoform in vitro. Dev. Biol. 149:16-26.
43. Smith, T.H., N.E. Block, S.J. Rhodes, S.F. Konieczny, and J.B. Miller. 1993. A unique pattern of expression of the four muscle regulatory factors distinguishes somitic from embryonic, fetal, and newborn mouse myogenic cells. Development (Camb.). 117:1125-1133.
44. Smith, T.H., A.M. Kachinsky, and J.B. Miller. 1994. Somite subdomains, muscle cell origins, and the four muscle regulatory factor proteins. J. Cell Biol. 127: 95-105.
45. Stockdale, F.E. 1992. Myogenic cell lineages. Dev. Biol. 154:284-298.
46. Tews, D.S., and H.H. Goebel. 1997. Apoptosis-related proteins in skeletal muscle fibers of spinal muscular atrophy. J. Neuropath. Exp. Neurol. 56:150-156.
47. Tidball, J.G., D.E. Albrecht, B.E. Lokensgard, and M.J. Spencer. 1995. Apoptosis precedes necrosis of dystrophin-deficient muscle. J. Cell Sci. 108:2197-2204.
48. Vachon, P.H., H. Xu, L. Liu, F. Loechel, Y. Hayashi, K. Arahata, J.C. Reed, U.M. Wewer, and E. Engvall. 1997. Integrins (α7β1) in muscle function and survival. Disrupted expression in merosin-deficient congenital muscular dystrophy. J. Clin. Invest. 100:1870-1881.
49. Veis, D.J., C.M. Sorenson, J.R. Shutter, and S.J. Korsmeyer. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell. 75:229-240.
50. Wang, J., and K. Walsh. 1996. Resistance to apoptosis conferred by cdk inhibitors during myocyte differentiation. Science. 273:359-361.
51. Webster, C., and H.M. Blau. 1990. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat. Cell Mol. Genet. 16:557-565.
52. Wright, W.E. 1984. Control of differentiation in heterokaryons and hybrids involving differentiation-defective myoblast variants. J. Cell Biol. 98:436-443.
53. Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:725-727.