Differentiation of human rhabdomyosarcoma RD cells is regulated by reciprocal, functional interactions between myostatin, p38 and extracellular regulated kinase signalling pathways

European Journal of Cancer

Volumn 47, Issue 7, 2011, Pages 1095-1105

  Rossi, Stefania ^a   Stoppani, Elena ^a   Puri, Pier Lorenzo ^b,c   Fanzani, Alessandro ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^c BURNHAM INSTITUTE   (United States)

Author keywords

Activin receptor; ERK; Myostatin; p38; Rhabdomyosarcoma; SMAD

Indexed keywords

ACTIVIN RECEPTOR 2; ACTIVIN RECEPTOR 2B; ACTIVIN RECEPTOR LIKE KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOSTATIN; SMAD2 PROTEIN; SMAD3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RHABDOMYOSARCOMA;

ACTIVIN RECEPTORS; CELL DIFFERENTIATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, DOMINANT; HUMANS; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; MYOSTATIN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 79953687657     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejca.2010.12.010     Document Type: Article

References (50)

1. Tonin PN, Scrable H, Shimada H, Cavenee WK. Muscle-specific gene expression in rhabdomyosarcomas and stages of human fetal skeletal muscle development. Cancer Res 1991;51:5100-6.
2. Loh EWJ, Scrable HJ, Livanos E, et al. Human chromosome 11 contains two different growth suppresser genes for embryonal rhabdomyosarcoma. Proc Natl Acad Sci USA 1992;89:1755-9.
3. Galili N, Davis RJ, Fredericks WJ, et al. Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993;5:230-5. (Pubitemid 23330384)
4. Anderson J, Gordon A, McManus A, Shipley J, Pritchard-Jones K. Disruption of imprinted genes at chromosome region 11p15.5 in paediatric rhabdomyosarcoma. Neoplasia 1999;1:340-8.
5. Barr FG. Gene fusions involving PAX and FOX family members in alveolar rhabdomyosarcoma. Oncogene 2001;20:5736-46 [review].
6. Ricaud S, Vernus B, Duclos M, et al. Inhibition of autocrine secretion of myostatin enhances terminal differentiation in human rhabdomyosarcoma cells. Oncogene 2003;22:8221-32. (Pubitemid 37485515)
7. Langley B, Thomas M, McFarlane C, et al. Myostatin inhibits rhabdomyosarcoma cell proliferation through an Rb-independent pathway. Oncogene 2004;23:524-34. (Pubitemid 38175007)
8. Yang Z, Zhang J, Cong H, et al. A retrovirus-based system to stably silence GDF-8 expression and enhance myogenic differentiation in human rhabdomyosarcoma cells. J Gene Med 2008;8:825-33.
9. Chardin P, Yeramian P, Madaule P, Tavitian A. N-ras gene activation in the RD human rhabdomyosarcoma cell line. Int J Cancer 1985;35:647-52. (Pubitemid 15019802)
10. Stratton MR, Fisher C, Gusterson BA, Cooper CS. Detection of point mutations in N-ras and K-ras genes of human embryonal rhabdomyosarcomas using oligonucleotide probes and the polymerase chain reaction. Cancer Res 1989;49:6324-7. (Pubitemid 20000931)
11. Tsumura H, Yoshida T, Saito H, Imanaka-Yoshida K, Suzuki N. Cooperation of oncogenic K-ras and p53 deficiency in pleomorphic rhabdomyosarcoma development in adult mice. Oncogene 2006;25:7673-9. (Pubitemid 44967962)
12. Puri PL, Wu Z, Zhang P, et al. Induction of terminal differentiation by constitutive activation of p38 MAP kinase in human rhabdomyosarcoma cells. Genes Dev 2000;14:574-84. (Pubitemid 30159776)
13. Mauro A, Ciccarelli C, De Cesaris P, et al. PKCalpha-mediated ERK, JNK and p38 activation regulates the myogenic program in human rhabdomyosarcoma cells. J Cell Sci 2002;115:3587-99.
14. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997;387:83-90. (Pubitemid 27202654)
15. Lee SJ, Reed LA, Davies MV, et al. Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc Natl Acad Sci USA 2005;102:18117-22. (Pubitemid 41798511)
16. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003;425:577-84 [review].
17. Massaguè J, Gomis RR. The logic of TGFbeta signaling. FEBS Lett 2006;580:2811-20 [review].
18. Langley B, Thomas M, Bishop A, et al. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 2002;277:49831-40. (Pubitemid 36014431)
19. Zhu X, Topouzis S, Liang LF, Stotish RL. Myostatin signaling through Smad2, Smad3 and Smad4 is regulated by the inhibitory Smad7 by a negative feedback mechanism. Cytokine 2004;26:262-72.
20. Huang Z, Chen D, Zhang K, et al. Regulation of myostatin signaling by c-Jun N-terminal kinase in C2C12 cells. Cell Signal 2007;19:2286-95. (Pubitemid 47361684)
21. Yang W, Chen Y, Zhang Y, et al. Extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase pathway is involved in myostatin-regulated differentiation repression. Cancer Res 2006;66:1320-6. (Pubitemid 43259910)
22. Lee SJ, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 2001;98(16):9306-11. (Pubitemid 32743912)
23. Donoghue M, Merlie J, Rosenthal N, Sanes J. Rostrocaudal gradient of transgene expression in adult skeletal muscle. Proc Natl Acad Sci USA 1991;88:5847-51. (Pubitemid 21914843)
24. Dennler S, Itoh S, Vivien D, et al. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998;17(11):3091-100. (Pubitemid 28254381)
25. Knudsen ES, Pazzagli C, Born TL, et al. Elevated cyclins and cyclin-dependent kinase activity in the rhabdomyosarcoma cell line RD. Cancer Res 1998;58(9):2042-9. (Pubitemid 28217485)
26. Xia Y, Schneyer AL. The biology of activin: recent advances in structure, regulation and function. J Endocrinol 2009;202:1-12 [review].
27. Andersson O, Reissmann E, Ibáñez CF. Growth differentiation factor 11 signals through the transforming growth factor-beta receptor ALK5 to regionalize the anterior-posterior axis. EMBO Rep 2006;7:831-7. (Pubitemid 44275403)
28. Ciccarelli C, Marampon F, Scoglio A, et al. p21WAF1 expression induced by MEK/ERK pathway activation or inhibition correlates with growth arrest, myogenic differentiation, onco-phenotype reversal in rhabdomyosarcoma cells. Mol Cancer 2005;4:41.
29. Marampon F, Ciccarelli C, Zani BM. Down-regulation of c-Myc following MEK/ERK inhibition halts the expression of malignant phenotype in rhabdomyosarcoma and in non muscle-derived human tumors. Mol Cancer 2006;5:31.
30. Marampon F, Bossi G, Ciccarelli C, et al. MEK/ERK inhibitor U0126 affects in vitro and in vivo growth of embryonal rhabdomyosarcoma. Mol Cancer Ther 2009;8:543-51.
31. Bouché M, Senni MI, Grossi AM, et al. TPA-induced differentiation of human rhabdomyosarcoma cells: expression of the myogenic regulatory factors. Exp Cell Res 1993;208:209-17. (Pubitemid 23274506)
32. Bouché M, Canipari R, Melchionna R, et al. TGF-beta autocrine loop regulates cell growth and myogenic differentiation in human rhabdomyosarcoma cells. FASEB J 2000;14:1147-58. (Pubitemid 30350397)
33. Joulia D, Bernardi H, Garandel V, et al. Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp Cell Res 2003;286:263-75. (Pubitemid 36566439)
34. Lee MK, Pardoux C, Hall MC, et al. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J 2007;26:3957-67. (Pubitemid 47367487)
35. Wu Z, Woodring PJ, Bhakta KS, et al. P38 and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol Cell Biol 2000;20(11):3951-64. (Pubitemid 30314494)
36. Chen G, Hitomi M, Han J, Stacey DW. The p38 pathway provides negative feedback for Ras proliferative signaling. J Biol Chem 2000;275(50):38973-80. (Pubitemid 32058908)
37. Schaaf G, Hamdi M, Zwijnenburg D, et al. Silencing of SPRY1 triggers complete regression of rhabdomyosarcoma tumors carrying a mutated RAS gene. Cancer Res 2010;70(2):762-71.
38. Bulavin DV, Fornace Jr AJ. p38 MAP kinase's emerging role as a tumor suppressor. Adv Cancer Res 2004;92:95-118 [review].
39. Lluís F, Perdiguero E, Nebreda AR, Muñoz-Cánoves P. Regulation of skeletal muscle gene expression by p38 MAP kinases. Trends Cell Biol 2006;16(1):36-44 [review].
40. Guasconi V, Puri PL. Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends Cell Biol 2009;19(6):286-94 [review].
41. Lluís F, Ballestar E, Suelves M, Esteller M, Muñoz- Cánoves P. E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle-specific gene transcription. EMBO J 2005;24(5):974-84. (Pubitemid 40470146)
42. Simone C, Forcales SV, Hill DA, et al. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat Genet 2004;36(7):738-43. (Pubitemid 38886636)
43. Serra C, Palacios D, Mozzetta C, et al. Functional interdependence at the chromatin level between the MKK6/ p38 and IGF1/PI3K/AKT pathways during muscle differentiation. Mol Cell 2007;28(2):200-13. (Pubitemid 47599998)
44. Rampalli S, Li L, Mak E, et al. p38 MAPK signaling regulates recruitment of Ash2L-containing methyltransferase complexes to specific genes during differentiation. Nat Struct Mol Biol 2007;14(12):1150-6. (Pubitemid 350223328)
45. Yang Z, MacQuarrie KL, Analau E, et al. MyoD and E-protein heterodimers switch rhabdomyosarcoma cells from an arrested myoblast phase to a differentiated state. Genes Dev 2009;23:694-707.
46. Li ZY, Yang J, Gao X, et al. Sequential recruitment of PCAF and BRG1 contributes to myogenin activation in 12-O-tetradecanoylphorbol- 13-acetate-induced early differentiation of rhabdomyosarcoma-derived cells. J Biol Chem 2007;282(26):18872-8. (Pubitemid 47100136)
47. Decristofaro MF, Betz BL, Rorie CJ, et al. Characterization of SWI/SNF protein expression in human breast cancer cell lines and other malignancies. J Cell Physiol 2001;186(1):136-45.
48. Decristofaro MF, Betz BL, Wang W, Weissman BE. Alteration of hSNF5/INI1/BAF47 detected in rhabdoid cell lines and primary rhabdomyosarcomas but not Wilms' tumors. Oncogene 1999;18(52):7559-65. (Pubitemid 30035057)
49. Perry RL, Parker MH, Rudnicki MA. Activated MEK1 binds the nuclear MyoD transcriptional complex to repress transactivation. Mol Cell 2001;8(2):291-301. (Pubitemid 32831547)
50. Philip B, Lu Z, Gao Y. Regulation of GDF-8 signaling by the p38 MAPK. Cell Signal 2005;17:365-75. (Pubitemid 39574697)