E2F5 and LEK1 translocation to the nucleus is an early event demarcating myoblast quiescence

Journal of Cellular Biochemistry

Volumn 101, Issue 6, 2007, Pages 1394-1408

  Reed, Sarah A ^a   Ouellette, Sara E ^a   Liu, Xiaosong ^b   Allen, Ronald E ^b   Johnson, Sally E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

E2F5; LEK1; Myoblast; Quiescent; Satellite cell

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN; PROTEIN LEK1; PROTEIN P107; PROTEIN P130; RAF PROTEIN; TRANSCRIPTION FACTOR E2F5; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEOMICS; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL CYCLE; CELL NUCLEUS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; E2F5 TRANSCRIPTION FACTOR; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE KINASE KINASES; MICE; MYOBLASTS; RAF KINASES; RETINOBLASTOMA PROTEIN; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION;

EID: 34547745912     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21256     Document Type: Article

References (66)

1. Allen RE, Boxhorn LK. 1989. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138:311-315.
2. Apostolova MD, Ivanova IA, Dagnino C, D'Souza SJ, Dagnino L. 2002. Active nuclear import and export pathways regulate E2F-5 subcellular localization. J Biol Chem 277:34471-34479.
3. Ashe M, Pabon-Pena L, Dees E, Price KL, Bader D. 2004. LEK1 is a potential inhibitor of pocket protein-mediated cellular processes. J Biol Chem 279:664-676.
4. Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS. 2000. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221-1234.
5. Becker JR, Dorman CM, McClafferty TM, Johnson SE. 2001. Characterization of a dominant inhibitory E47 protein that suppresses C2C12 myogenesis. Exp Cell Res 267:135-143.
6. Bischoff R. 1990a. Cell cycle commitment of rat muscle satellite cells. J Cell Biol 111:201-207.
7. Bischoff R. 1990b. Control of satellite cell proliferation. Adv Exp Med Biol 280:147-157.
8. Buck V, Allen KE, Sorensen T, Bybee A, Hijmans EM, Voorhoeve PM, Bernards R, La Thangue NB. 1995. Molecular and functional characterisation of E2F-5, a new member of the E2F family. Oncogene 11:31-38.
9. Carnac G, Fajas L, L'honore A, Sardet C, Lamb NJ, Fernandez A. 2000. The retinoblastoma-like protein p130 is involved in the determination of reserve cells in differentiating myoblasts. Curr Biol 10:543-546.
10. Chen CR, Kang Y, Siegel PM, Massague J. 2002. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 110:19-32.
11. Cobrinik D. 2005. Pocket proteins and cell cycle control. Oncogene 24:2796-2809.
12. Coller HA, Sang L, Roberts JM. 2006. A new description of cellular quiescence. PLoS Biol 4:e83.
13. Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB. 2001. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239:79-94.
14. Cornelison DD, Wilcox-Adelman SA, Goetinck PF, Rauvala H, Rapraeger AC, Olwin BB. 2004. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18:2231-2236.
15. Dasgupta P, Sun J, Wang S, Fusaro G, Betts V, Padmanabhan J, Sebti SM, Chellappan SP. 2004. Disruption of the Rb-Raf-1 interaction inhibits tumor growth and angiogenesis. Mol Cell Biol 24:9527-9541.
16. DeChant AK, Dee K, Weyman CM. 2002. 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 21:5268-5279.
17. Dhawan J, Rando TA. 2005. Stem cells in postnatal myogenesis: Molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15:666-673.
18. Dorman CM, Johnson SE. 2000. Activated Raf inhibits myogenesis through a mechanism independent of activator protein 1-mediated myoblast transformation. J Biol Chem 275:27481-27487.
19. Ebisuya M, Kondoh K, Nishida E. 2005. The duration, magnitude and compartmentalization of ERK MAP kinase activity: Mechanisms for providing signaling specificity. J Cell Sci 118:2997-3002.
20. Garry DJ, Yang Q, Bassel-Duby R, Williams RS. 1997. Persistent expression of MNF identifies myogenic stem cells in postnatal muscles. Dev Biol 188:280-294.
21. Gaubatz S, Lindeman GJ, Ishida S, Jakoi L, Nevins JR, Livingston DM, Rempel RE. 2000. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol Cell 6:729-735.
22. Goodwin RL, Pabon-Pena LM, Foster GC, Bader D. 1999. The cloning and analysis of LEK1 identifies variations in the LEK/centromere protein F/mitosin gene family. J Biol Chem 274:18597-18604.
23. Gos M, Miloszewska J, Swoboda P, Trembacz H, Skierski J, Janik P. 2005. Cellular quiescence induced by contact inhibition or serum withdrawal in C3H10T1/2 cells. Cell Prolif 38:107-116.
24. Gu W, Schneider JW, Condorelli G, Kaushal S, Mahdavi V, Nadal-Ginard B. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
25. Guo CS, Degnin C, Fiddler TA, Stauffer D, Thayer MJ. 2003. Regulation of MyoD activity and muscle cell differentiation by MDM2, pRb, and Sp1. J Biol Chem 278:22615-22622.
26. Horst D, Ustanina S, Sergi C, Mikuz G, Juergens H, Braun T, Vorobyov E. 2006. Comparative expression analysis of Pax3 and Pax7 during mouse myogenesis. Int J Dev Biol 50:47-54.
27. Huh MS, Parker MH, Scime A, Parks R, Rudnicki MA. 2004. Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J Cell Biol 166:865-876.
28. Ishido M, Kami K, Masuhara M. 2004a. In vivo expression patterns of MyoD, p21, and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle. Am J Physiol Cell Physiol 287:C484-C493.
29. Ishido M, Kami K, Masuhara M. 2004b. Localization of MyoD, myogenin and cell cycle regulatory factors in hypertrophying rat skeletal muscles. Acta Physiol Scand 180:281-289.
30. Johnson SE, Allen RE. 1993. Proliferating cell nuclear antigen (PCNA) is expressed in activated rat skeletal muscle satellite cells. J Cell Physiol 154:39-43.
31. Johnson SE, Allen RE. 1995. Activation of skeletal muscle satellite cells and the role of fibroblast growth factor receptors. Exp Cell Res 219:449-453.
32. Kerkhoff E, Rapp UR. 1998. High-intensity Raf signals convert mitotic cell cycling into cellular growth. Cancer Res 58:1636-1640.
33. Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA. 2006. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol 172:103-113.
34. Li FQ, Coonrod A, Horwitz M. 1996. Preferential MyoD homodimer formation demonstrated by a general method of dominant negative mutation employing fusion with a lysosomal protease. J Cell Biol 135:1043-1057.
35. Mauro A. 1961. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493-495.
36. Myers TK, Andreuzza SE, Franklin DS. 2004. p18INK4c and p27KIP1 are required for cell cycle arrest of differentiated myotubes. Exp Cell Res 300:365-378.
37. Oustanina S, Hause G, Braun T. 2004. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 23:3430-3439.
38. Papadimou E, Menard C, Grey C, Puceat M. 2005. Interplay between the retinoblastoma protein and LEK1 specifies stem cells toward the cardiac lineage. EMBO J 24:1750-1761.
39. Puceat M. 2005. Rb and LE K1: A "Pas de Deux" in cardiogenesis. Cell Cycle 4.
40. Ravi RK, Weber E, McMahon M, Williams JR, Baylin S, Mal A, Harter ML, Dillehay LE, Claudio PP, Giordano A, Nelkin BD, Mabry M. 1998. Activated Raf-1 causes growth arrest in human small cell lung cancer cells. J Clin Invest 101:153-159.
41. Ravi RK, McMahon M, Yangang Z, Williams JR, Dillehay LE, Nelkin BD, Mabry M. 1999. Raf-1-induced cell cycle arrest in LNCaP human prostate cancer cells. J Cell Biochem 72:458-469.
42. Relaix F, Rocancourt D, Mansouri A, Buckingham M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948-953.
43. Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M. 2006. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172:91-102.
44. Renault V, Thornell LE, Butler-Browne G, Mouly V. 2002. Human skeletal muscle satellite cells: Aging, oxidative stress and the mitotic clock. Exp Gerontol 37:1229-1236.
45. Sajko S, Kubinova L, Cvetko E, Kreft M, Wernig A, Erzen I. 2004. Frequency of M-cadherin-stained satellite cells declines in human muscles during aging. J Histochem Cytochem 52:179-185.
46. Sardet C, Vidal M, Cobrinik D, Geng Y, Onufryk C, Chen A, Weinberg RA. 1995. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc Natl Acad Sci USA 92:2403-2407.
47. Schneider JW, Gu W, Zhu L, Mahdavi V, Nadal-Ginard B. 1994. Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells. Science 264:1467-1471.
48. Schultz E. 1989. Satellite cell behavior during skeletal muscle growth and regeneration. Med Sci Sports Exerc 21:S181-S186.
49. Schultz E, Gibson MC, Champion T. 1978. Satellite cells are mitotically quiescent in mature mouse muscle: An EM and radioautographic study. J Exp Zool 206:451-456.
50. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777-786.
51. Sewing A, Wiseman B, Lloyd AC, Land H. 1997. High-intensity Raf signal causes cell cycle arrest mediated by p21Cip1. Mol Cell Biol 17:5588-5597.
52. Smith CK, Janney MJ, Allen RE. 1994. Temporal expression of myogenic regulatory genes during activation, proliferation, differentiation of rat skeletal muscle satellite cells. J Cell Physiol 159:379-385.
53. Smith EJ, Leone G, DeGregori J, Jakoi L, Nevins JR. 1996. The accumulation of an E2F-p130 transcriptional repressor distinguishes a G0 cell state from a G1 cell state. Mol Cell Biol 16:6965-6976.
54. Smith EJ, Leone G, Nevins JR. 1998. Distinct mechanisms control the accumulation of the Rb-related p107 and p130 proteins during cell growth. Cell Growth Differ 9:297-303.
55. Snow MH. 1977a. Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. I. A fine structural study. Anat Rec 188:181-199.
56. Snow MH. 1977b. Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. II. An autoradiographic study. Anat Rec 188:201-217.
57. Stevens C, La Thangue NB. 2003. E2F and cell cycle control: A double-edged sword. Arch Biochem Biophys 412:157-169.
58. Trimarchi JM, Fairchild B, Verona R, Moberg K, Andon N, Lees JA. 1998. E2F-6, a member of the E2F family that can behave as a transcriptional repressor. Proc Natl Acad Sci USA 95:2850-2855.
59. Vaccarello G, Figliola R, Cramerotti S, Novelli F, Maione R. 2006. p57Kip2 is induced by MyoD through a p73-dependent pathway. J Mol Biol 356:578-588.
60. Walsh K. 1997. Coordinate regulation of cell cycle and apoptosis during myogenesis. Prog Cell Cycle Res 3:53-58.
61. Wang X, Thomson SR, Starkey JD, Page JL, Ealy AD, Johnson SE. 2004. Transforming growth factor beta1 is up-regulated by activated Raf in skeletal myoblasts but does not contribute to the differentiation-defective phenotype. J Biol Chem 279:2528-2534.
62. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, McMahon M. 1997. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 17:5598-5611.
63. Wozniak AC, Anderson JE. 2005. Single-fiber isolation and maintenance of satellite cell quiescence. Biochem Cell Biol 83:674-676.
64. Yablonka-Reuveni Z, Seger R, Rivera AJ. 1999. Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47:23-42.
65. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR. 2006. Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824-1832.
66. Zhu J, Woods D, McMahon M, Bishop JM. 1998. Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev 12:2997-3007.