S100B protein in myoblasts modulates myogenic differentiation via NF-κB-dependent inhibition of MyoD expression

Journal of Cellular Physiology

Volumn 223, Issue 1, 2010, Pages 270-282

  Tubaro, Claudia ^a   Arcuri, Cataldo ^a   Giambanco, Ileana ^a   Donato, Rosario ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYOD PROTEIN; MYOGENIN; MYOSIN HEAVY CHAIN; PROTEIN S100B; TRANSCRIPTION FACTOR YY1;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; GENE SILENCING; MOUSE; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SKELETAL MUSCLE;

ANIMALS; CATTLE; CELL DIFFERENTIATION; CELL LINE; I-KAPPA B KINASE; MICE; MUSCLE DEVELOPMENT; MYOBLASTS; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; MYOGENIN; MYOSIN HEAVY CHAINS; NERVE GROWTH FACTORS; NF-KAPPA B; RATS; RECOMBINANT PROTEINS; RNA INTERFERENCE; S100 PROTEINS; TIME FACTORS; TRANSFECTION; YY1 TRANSCRIPTION FACTOR;

EID: 75749099822     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22035     Document Type: Article

References (59)

1. Acharyya S, Ladner KJ, Nelsen LL, Damrauer J, Reiser PJ, Swoap S, Guttridge DC. 2004. Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J Clin Invest 114:370-378.
2. Acharyya S, Villalta SA, Bakkar N, Bupha-Intr T, Janssen PM, Carathers M, Li ZW, Beg AA, Ghosh S, Sahenk Z, Weinstein M, Gardner KL, Rafael-Fortney JA, Karin M, Tidball JG, Baldwin AS, Guttridge DC. 2007. Interplay of IKK/NF-κB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest 117:889-901.
3. Arcuri C, Bianchi R, Brozzi F, Donato R. 2005. S100B increases proliferation in PC12 neuronal cells and reduces their responsiveness to NGF via Akt activation. J Biol Chem 280:4402-4414.
4. Arcuri C, Giambanco I, Bianchi R, Donato R. 2002. Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience 109:371-388.
5. Baeza-Raja B, Munoz-Canoves P. 2004. p38 MAPK-induced nuclear factor-κB activity is required for skeletal muscle differentiation: role of interleukin-6. Mol Biol Cell 15:2013-2026.
6. Bakkar N, Wang J, Ladner KJ, Wang H, Dahlman JM, Carathers M, Acharyya S, Rudnicki MA, Hollenbach AD, Guttridge DC. 2008. IKK/NF-κB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promotemitochondrial biogenesis. J Cell Biol 180:787-802.
7. Batra RK, Guttridge DC, Brenner DA, Dubinett SM, Baldwin AS, Boucher RC. 1999. IkBa gene transfer is cytotoxic to squamous-cell lung cancer cells and sensitizes them to tumor necrosis factor-a-mediated cell death. Am J Respir Cell Mol Biol 21:238-245.
8. Bennett AM, Tonks NK. 1997. Regulation of distinct stages of skeletal muscle differentiation by mitogen-activated protein kinases. Science 278:1288-1291.
9. Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA. 2008. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2:50-59.
10. Brozzi F, Arcuri C, Giambanco I, Donato R. 2009. S100B protein regulates astrocyte shape and migration via interaction with Src kinase: implications for astrocyte development, activation and tumor growth. J Biol Chem 284:8797-8811.
11. Buckingham M. 2006. Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Curr Opin Genet Dev 16:525-532.
12. Carnac G, Primig M, Kitzmann M, Chafey P, Tuil D, Lamb N, Fernandez A. 1998. RhoA GTPase and serum response factor control selectively the expression of MyoD without affecting Myf5 in mouse myoblasts. Mol Biol Cell 9:1891-1902.
13. Castellani L, Salvati E, Alemà S, Falcone G. 2006. Fine regulation of RhoA and Rock is required for skeletal muscle differentiation. J Biol Chem 281:15249-15257.
14. Chargé SB, Rudnicki MA. 2004. Cellular and molecular regulation of muscle regeneration. Physiol Rev 8:209-238.
15. Charrasse S, Comunale F, Grumbach Y, Poulat F, Blangy A, Gauthier-Rouviere C. 2006. RhoA GTPase regulates M-cadherin activity and myoblast fusion. Mol Biol Cell 17:749-759.
16. Charrasse S, Comunale F, Fortier M, Portales-Casamar E, Debant A, Gauthier-Rouviere C. 2007. M-Cadherin activates Rac1 GTPase through the Rho-GEF Trio during myoblast fusion. Mol Biol Cell 18:1734-1743.
17. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR. 1997. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 272:6653-6662.
18. Cossu G, Borrello U. 1999. Wnt signaling and the activation of myogenesis in mammals. EMBO J 18:6867-6872.
19. Di Marco S, Mazroui R, Dallaire P, Chittur S, Tenenbaum SA, Radzioch D, Marette A, Gallouzi IE. 2005. NF-κB-mediated MyoD decay during muscle wasting requires nitric oxide synthasem RNA stabilization, HuR protein, and nitric oxide release. Mol Cell Biol 25:6533-6545.
20. Dogra C, Changotra H, Mohan S, Kumar A. 2006. Tumor necrosis factor-like weak inducer of apoptosis inhibits skeletal myogenesis through sustained activation of nuclear factor-κB and degradation of MyoD protein. J Biol Chem 281:10327-10336.
21. Donato R. 1988. Calcium-independent, pH regulated effects of S-100 proteins on assemblydisassembly of brain microtubule protein in vitro. J Biol Chem 263:106-110.
22. Donato R. 2001. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33:637-668.
23. Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F, Tubaro C, Giambanco I. 2009. S100B's double life: intracellular regulator and extracellular signal. Biochim Biophys Acta (Molecular Cell Research) 1793:1008-1022.
24. Guttridge DC, Mayo MW, Madrid LV, Wang CY, Baldwin AS Jr. 2000. NF-κB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289:2363-2366.
25. Heizmann CW, Fritz G, Schaefer BW. 2002. S100 proteins: structure, functions and pathology. Front Biosci 7:d1356-d1368.
26. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H. 2000. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through RAGE activation. J Biol Chem 275:40096-40105.
27. Komati H, Naro F, Mebarek S, De Arcangelis V, Adamo S, Lagarde M, Prigent AF, Nemoz G. 2005. Phospholipase D is involved in myogenic differentiation through remodeling of actin cytoskeleton. Mol Biol Cell 16:1232-1244.
28. Kumar A, Murphy R, Robinson P, Wei L, Boriek AM. 2004. Cyclic mechanical strain inhibits skeletal myogenesis through activation of focal adhesion kinase, Rac-1 GTPase, and NF-κB transcription factor. FASEB J 18:1524-1535.
29. Kuwahara K, Barrientos T, Pipes GC, Li S, Olson EN. 2005. Muscle-specific signaling mechanism that links actin dynamics to serum response factor. Mol Cell Biol 25:3173-3181.
30. Langen RC, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM. 2001. Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-B. FASEB J 15:1169-1180.
31. Langen RC, Van Der Velden JL, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM. 2004. Tumor necrosis factor-a inhibits myogenic differentiation through MyoD protein destabilization. FASEB J 18:227-237.
32. Lin J, Yang Q, Yan Z, Markowitz J, Wilder PT, Carrier F, Weber DJ. 2004. Inhibiting S100B restores p53 levels in primary malignant melanoma cancer cells. J Biol Chem 279:34071-34077.
33. Lluis F, Perdiguero E, Nebreda AR, Munoz-Canoves P. 2006. Regulation of skeletal muscle gene expression by p38 MAP kinases. Trends Cell Biol 16:36-44.
34. Lovett FA, Gonzalez I, Salih DA, Cobb LJ, Tripathi G, Cosgrove RA, Murrell A, Kilshaw PJ, Pell JM. 2006. Convergence of Igf2 expression and adhesion signalling via RhoA and p38 MAPK enhances myogenic differentiation. J Cell Sci 119:4828-4840.
35. Marenholz I, Heizmann CW, Fritz G. 2004. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322:1111-1122.
36. Meriane M, Roux P, Primig M, Fort P, Gauthier-Rouviere C. 2000. Critical activities of Rac1 and Cdc42Hs in skeletal myogenesis: antagonistic effects of JNK and p38 pathways. Mol Biol Cell 11:2513-2528.
37. Mourkioti F, Kratsios P, Luedde T, Song YH, Delafontaine P, Adami R, Parente V, Bottinelli R, Pasparakis M, Rosenthal N. 2006. Targeted ablation of IKK2 improves skeletal muscle strength, maintains mass, and promotes regeneration. J Clin Invest 116:2945-2954.
38. Neville C, Rosenthal N, McGrew M, Tsakiris T, Parthimos N, Hauschka S. 1997. Skeletal muscle cultures. Method Cell Biol 52:85-116.
39. Nishiyama T, Kii I, Kudo A. 2004. Inactivation of Rho/ROCK signaling is crucial for the nuclear accumulation of FKHR and myoblast fusion. J Biol Chem 279:47311-47319.
40. Pajcini KV, Pomerantz JH, Alkan O, Doyonnas R, Blau HM. 2008. Myoblasts andmacrophages share molecular components that contribute to cell-cell fusion. J Cell Biol 180:1005-1019.
41. Palacios D, Puri PL. 2006. The epigenetic network regulating muscle development and regeneration. J Cell Physiol 207:1-11.
42. Pelosi M, Marampon F, Zani BM, Prudente S, Perlas E, Caputo V, Cianetti L, Berno V, Narumiya S, Kang SW, Musarò A, Rosenthal N. 2007. ROCK2 and its alternatively spliced isoform ROCK2m positively control the maturation of the myogenic program. Mol Cell Biol 27:6163-6176.
43. Perdiguero E, Ruiz-Bonilla V, Gresh L, Hui L, Ballestar E, Sousa-Victor P, Baeza-Raja B, JardíM, Bosch-Comas A, Esteller M, Caelles C, Serrano AL, Wagner EF, Muñoz-Cánoves P. 2007. Genetic analysis of p38 MAP kinases inmyogenesis: fundamental role of p38a in abrogating myoblast proliferation. EMBO J 26:1245-1256.
44. Riuzzi F, Sorci G, Donato R. 2006a. S100B stimulates myoblast proliferation and inhibits myoblast differentiation by independently stimulating ERK1/2 and inhibiting p38 MAPK. J Cell Physiol 207:461-470.
45. Riuzzi F, Sorci G, Donato R. 2006b. The amphoterin/RAGE pair modulates myoblast proliferation, apoptosis, adhesiveness, migration and invasiveness. Functional inactivation of RAGE in L6 myoblasts results in tumor formation in vivo. J Biol Chem 281:8242-8253.
46. Rochat A, Fernandez A, Vandromme M, Moles JP, Bouschet T, Carnac G, Lamb NJ. 2004. Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol Biol Cell 15:4544-4555.
47. Saito T, Ikeda T, Nakamura K, Chung UI, Kawaguchi H. 2007. S100A1 and S100B, transcriptional targets of SOX trio, inhibit terminal differentiation of chondrocytes.EMBO Rep 8:504-509.
48. Serra C, Palacios D, Mozzetta C, Forcales SV, Morante I, Ripani M, Jones DR, Du K, Jhala US, Simone C, Puri PL. 2007. Functional interdependence at the chromatin level between the MKK6/p38 and IGF1/PI3K/AKT pathways during muscle differentiation. Mol Cell 28:200-213.
49. Simone C, Forcales SV, Hill DA, Imbalzano AN, Latella L, Puri PL. 2004. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat Genet 36:738-743.
50. Sorci G, Bianchi R, Giambanco I, Rambotti MG, Donato R. 1999. Replicating myoblasts and fused myotubes express the calcium-regulated proteins S100A1 and S100B. Cell Calcium 25:93-106.
51. Sorci G, Agneletti AL, Riuzzi F, Marchetti C, Donato R. 2003. S100B inhibits myogenic differentiation and myotube formation in a RAGE-independent manner. Mol Cell Biol 23:4870-4881.
52. Sorci G, Riuzzi F, Arcuri C, Giambanco I, Donato R. 2004. Amphoterin stimulates myogenesis and counteracts the antimyogenic factors basic fibroblast growth factor and S100B via RAGE binding. Mol Cell Biol 24:4880-4894.
53. Takano H, Komuro I, Oka T, Shiojima I, Hiroi Y, Mizuno T, Yazaki Y. 1998. The Rho family G proteins play a critical role in muscle differentiation. Mol Cell Biol 18:1580-1589.
54. van der Velden JL, Langen RC, Kelders MC, Wouters EF, Janssen-Heininger YM, Schols AM. 2006. Inhibition of glycogen synthase kinase-3beta activity is sufficient to stimulate myogenic differentiation. Am J Physiol Cell Physiol 290:C453-462.
55. van der Velden JL, Schols AM, Willems J, Kelders MC, Langen RC. 2008. Glycogen synthase kinase 3 suppresses myogenic differentiation through negative regulation of NFATc3. J Biol Chem 283:358-366.
56. Wang H, Hertlein E, Bakkar N, Sun H, Acharyya S, Wang J, Carathers M, Davuluri R, Guttridge DC. 2007. NF-κB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol 27:4374-4387.
57. Wei L, Zhou W, Croissant JD, Johansen FE, Prywes R, Balasubramanyam A, Schwartz RJ. 1998. RhoA signaling via serum response factor plays an obligatory role in myogenic differentiation. J Biol Chem 273:30287-30294.
58. Winter B, Arnold H-H. 2000. Activated raf kinase inhibits muscle cell differentiation through a MEF2-dependent mechanism. J Cell Sci 113:4211-4220.
59. Zhan M, Jin B, Chen SE, Reecy JM, Li YP. 2007. TACE release of TNF-α mediates mechanotransduction-induced activation of p38 MAPK and myogenesis. J Cell Sci 120:692-701.