Immortalization of mouse myogenic cells can occur without loss of p16INK4a, p19ARF, or p53 and is accelerated by inactivation of Bax

BMC Cell Biology

Volumn 5, Issue , 2004, Pages

  Nowak, Jonathan A ^a   Malowitz, Jonathan ^a   Girgenrath, Mahasweta ^a   Kostek, Christine A ^a   Kravetz, Amanda J ^a   Dominov, Janice A ^a   Miller, Jeffrey Boone ^a  

^a BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESMIN; PROTEIN BAX; PROTEIN P16; PROTEIN P19; PROTEIN P53;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL IMMORTALIZATION; CELL LINE; CELL NUCLEUS; CELL STRUCTURE; CONTROLLED STUDY; FREQUENCY ANALYSIS; GENE INACTIVATION; IN VIVO STUDY; MOUSE; MULTINUCLEAR CELL; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE FIBRIL; MYOTUBE; NONHUMAN; NULL CELL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE;

ANIMALS; BCL-2-ASSOCIATED X PROTEIN; CELL DIVISION; CELL LINE; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; KINETICS; MICE; MICE, KNOCKOUT; MUSCLE FIBERS, SKELETAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53;

EID: 2342666611     PISSN: 14712121     EISSN: None     Source Type: Journal    
DOI: 10.1186/1471-2121-5-1     Document Type: Article

References (52)

1. Hauschka SD, Linkhart TA, Clegg C, Merrill G: Clonal studies of human and mouse muscle. In Muscle Regeneration Edited by: Mauro A. Raven Press NY; 1979:311-322.
2. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, Grosveld G, Sherr CJ: Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997, 91:649-659.
3. Yaffe D, Saxel O: Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977, 270:725-727.
4. Dominov JA, Houlihan-Kawamoto CA, Swap CJ, Miller JB: Pro- and anti-apoptotic members of the Bcl-2 family in skeletal muscle: A role for Bcl-2 in later stages of myogenesis. Dev Dyn 2001, 220:18-26.
5. Dominov JA, Dunn JJ, Miller JB: Bcl-2 expression identifies an early stage of myogenesis and promotes clonal expansion of muscle cells. J Cell Biol 1998, 142:537-544.
6. Primeau AJ, Adhihetty PJ, Hood DA: Apoptosis in heart and skeletal muscle. Can J Appl Physiol 2002, 27:349-395.
7. Tews DS: Apoptosis and muscle fibre loss in neuromuscular disorders. Neuromuscul Disord 2002, 12:613-622.
8. Wright WE, Shay JW: Telomere dynamics in cancer progression and prevention: fundamental differences in human and mouse telomere biology. Nat Med 2000, 6:849-851.
9. Loo DT, Fuquay JI, Rawson CL, Barnes DW: Extended culture of mouse embryo cells without senescence: Inhibition by serum. Science 1987, 236:200-202.
10. Mathon NF, Malcolm DS, Harrisingh MC, Cheng L, Lloyd AC: Lack of replicative senescence in normal rodent glia. Science 2001, 291:872-875.
11. Tang DG, Tokumoto YM, Apperly JA, Lloyd AC, Raff MC: Lack of replicative senescence in cultured rat oligodendrocyte precursor cells. Science 2001, 291:868-871.
12. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, Wright WE: Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 2001, 15:398-403.
13. Wright WE, Shay JW: Historical claims and current interpretations of replicative aging. Nat Biotechnol 2002, 20:682-688.
14. Harvey M, Sand AT, Weiss RS, Hegri ME, Wiseman RW, Pantazis P, Giovanella BC, Tainsky MA, Bradly A, Donehower LA: In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 1993, 8:2457-2467.
15. Randle DH, Zindy F, Sherr CJ, Roussel MF: Differential effects of p19(Arf) and p16(Ink4a) loss on senescence of murine bone marrow-derived preB cells and macrophages. Proc Natl Acad Sci U S A 2001, 98:9654-9659.
16. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA: Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996, 85:27-37.
17. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, Aguirre AJ, Wu EA, Horner JW, DePinho RA: Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 2001, 413:86-91.
18. White JD, Rachel C, Vermeulen R, Davies M, Grounds MD: The role of p53 in vivo during skeletal muscle post-natal development and regeneration: studies in p53 knockout mice. Int J Dev Biol 2002, 46:577-582.
19. Porrello A, Cerone MA, Coen S, Gurtner A, Fontemaggi G, Cimino L, Piaggio G, Sacchi A, Soddu S: p53 regulates myogenesis by triggering the differentiation activity of pRb. J Cell Biol 2000, 151:1295-1304.
20. Zacksenhaus E, Jiang Z, Chung D, Marth JD, Phillips RA, Gallie BL: pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev 1996, 10:3051-3064.
21. Takahashi C, Bronson RT, Socolovsky M, Contreras B, Lee KY, Jacks T, Noda M, Kucherlapati R, Ewen ME: Rb and N-ras function together to control differentiation in the mouse. Mol Cell Biol 2003, 23:5256-5268.
22. Soddu S, Blandino G, Scardigli R, Coen S, Marchetti A, Rizzo MG, Bossi G, Cimino L, Crescenzi M, Sacchi A: Interference with p53 protein inhibits hematopoietic and muscle differentiation. J Cell Biol 1996, 134:193-204.
23. Wagner M, Hampel B, Bernhard D, Hala M, Zwerschke W, Jansen-Durr P: Replicative senescence of human endothelial cells in vitro involves G1 arrest, polyploidization and senescence-associated apoptosis. Exp Gerontol 2001, 36:1327-1347.
24. Raffo AJ, Kim AL, Fine RL: Formation of nuclear Bax/p53 complexes is associated with chemotherapy induced apoptosis. Oncogene 2000, 19:6216-6228.
25. Morris EJ, Keramaris E, Rideout HJ, Slack RS, Dyson NJ, Stefanis L, Park DS: Cyclin-dependent kinases and P53 pathways are activated independently and mediate Bax activation in neurons after DNA damage. J Neurosci 2001, 21:5017-5026.
26. Knudson CM, Johnson GM, Lin Y, Korsmeyer SJ: Bax accelerates tumorigenesis in p53-deficient mice. Cancer Res 2001, 61:659-665.
27. Eischen CM, Rehg JE, Korsmeyer SJ, Cleveland JL: Loss of Bax alters tumor spectrum and tumor numbers in ARF-deficient mice. Cancer Res 2002, 62:2184-2191.
28. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA: Myogenic specification of side population cells in skeletal muscle. J Cell Biol 2002, 159:123-134.
29. Howell JC, Yoder MC, Srour EF: Hematopoietic potential of murine skeletal muscle-derived CD45(-)Sca-1(+)c-kit(-) cells. Exp Hematol 2002, 30:915-924.
30. Lee JY, Qu-Petersen Z, Cao B, Kimura S, Jankowski R, Cummins J, Usas A, Gates C, Robbins P, Wernig A, Huard J: Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 2000, 150:1085-1100.
31. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA: Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Aca Sci USA 2002, 99:1341-1346.
32. Torrente Y, Tremblay JP, Pisati F, Belicchi M, Rossi B, Sironi M, Fortunato F, El Fahime M, D'Angelo MG, Caron NJ, Constantin G, Paulin D, Scarlato G, Bresolin N: Intraarterial injection of musclederived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol 2001, 152:335-348.
33. Cerone MA, Marchetti A, Bossi G, Blandino G, Sacchi A, Soddu S: p53 is involved in the differentiation but not in the differentiation-associated apoptosis of myoblasts. Cell Death Differ 2000, 7:506-508.
34. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ, Roussel MF: Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 1998, 12:2424-2433.
35. Mazzaro G, Bossi G, Coen S, Sacchi A, Soddu S: The role of wild-type p53 in the differentiation of primary hemopoietic and muscle cells. Oncogene 1999, 18:5831-5835.
36. McDoniels-Silvers AL, Herzog CR, Tyson FL, Malkinson AM, You M: Inactivation of both Rb and p53 pathways in mouse lung epithelial cell lines. Exp Lung Res 2001, 27:297-318.
37. Obata M, Imamura E, Yoshida Y, Goto J, Kishibe K, Yasuda A, Ogawa K: Resistance of primary cultured mouse hepatic tumor cells to cellular senescence despite expression of p16(Ink4a), p19(Arf), p53, and p21(Waf1/Cip1). Mol Carcinog 2001, 32:9-18.
38. Hardwick JM, Polster BM: Bax, along with lipid conspirators, allows cytochrome c to escape mitochondria. Mol Cell 2002, 10:963-965.
39. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH: Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 2000, 7:1166-1173.
40. DeChant AK, Dee K, Weyman CM: Raf-induced effects on the differentiation and apoptosis of skeletal myoblasts are determined by the level of Raf signaling: abrogation of apoptosis by Raf is downstream of caspase 3 activation. Oncogene 2002, 21:5268-5279.
41. Kamradt MC, Chen F, Sam S, Cryns VL: The small heat shock protein alpha B-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation. J Biol Chem 2002, 77:38731-38736.
42. Shiokawa D, Kobayashi T, Tanuma S: Involvement of DNase gamma in apoptosis associated with myogenic differentiation of C2C12 cells. J Biol Chem 2002, 277:31031-31037.
43. Wang J, Guo K, Wills KN, Walsh K: Rb functions to inhibit apoptosis during myocyte differentiation. Cancer Res 1997, 57:351-354.
44. Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC: Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 1999, 401:390-394.
45. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ: Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 1995, 270:96-99.
46. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, Snider WD: Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 1998, 18:1428-1239.
47. Grounds MD: Reasons for the degeneration of ageing skeletal muscle: a central role for IGF-1 signalling.Biogerontology 2002, 3:19-24.
48. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM Jr, Snider WD, Korsmeyer SJ: BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 1996, 17:401-411.
49. Bischoff R, Heintz C: Enhancement of skeletal muscle regeneration. Dev Dyn 1994, 201:41-54.
50. Bischoff FZ, Yim SO, Pathak S, Grant G, Siciliano MJ, Giovanella BC, Strong LC, Tainsky MA: Spontaneous abnormalities in normal fibroblasts from patients with Li-Fraumeni cancer syndrome: aneuploidy and immortalization. Cancer Res 1990, 50:7979-7984.
51. Zhu Z, Miller JB: MRF4 can substitute for myogenin during early myogenesis. Dev Dyn 1997, 209:233-241.
52. Cumming WJK, Fulthorpe J, Hudgson P, Mahon M: Color Atlas of Muscle Pathology London: Mosby-Wolfe; 1994.