Comparative expression profiling identifies differential roles for Myogenin and p38α MAPK signaling in myogenesis

Journal of Molecular Cell Biology

Volumn 4, Issue 6, 2012, Pages 386-397

  Liu, Qi Cai ^a   Zha, Xiao Hui ^a,b   Faralli, Hervé ^a   Yin, Hang ^a   Louis Jeune, Caroline ^a   Perdiguero, Eusebio ^c   Pranckeviciene, Erinija ^a,b   Muñoz Cànoves, Pura ^c   Rudnicki, Michael A ^a,b   Brand, Marjorie ^a,b   Perez Iratxeta, Carol ^a   Dilworth, F Jeffrey ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

CD53; cell cycle exit; miRNA; myoblast fusion; myogenin; p38 MAPK

Indexed keywords

CD53 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 14; MYOGENIN; TETRASPANIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE PROGRESSION; CELL FUSION; CONTROLLED STUDY; DOWN REGULATION; EX VIVO STUDY; IN VIVO STUDY; MOUSE; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MYOTUBE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; ANTIGENS, CD53; CELL CYCLE; CELL DIFFERENTIATION; CELL FUSION; CELL LINE; CELL PROLIFERATION; DOWN-REGULATION; GENE EXPRESSION; MICE; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASE 14; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MYOBLASTS, SKELETAL; MYOGENIN; REGENERATION; SIGNAL TRANSDUCTION; UP-REGULATION;

MUS;

EID: 84871815845     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjs045     Document Type: Article

References (61)

1. Abmayr, S.M., and Pavlath, G.K. (2012). Myoblast fusion: lessons from flies and mice. Development 139, 641-656.
2. Andres, V., and Walsh, K. (1996). Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132, 657-666. (Pubitemid 26069245)
3. Aziz, A., Liu, Q.C., and Dilworth, F.J. (2010). Regulating a master regulator: Establishing tissue-specific gene expression in skeletal muscle. Epigenetics 5, 692-696.
4. Aziz, A., Sebastian, S., and Dilworth, F.J. (2012). The origin and fate of muscle satellite cells. Stem Cell Rev. 8, 609-622.
5. Biesiada, E., Hamamori, Y., Kedes, L., et al. (1999). Myogenic basic helix-loop-helix proteins and SP1 interact as components of a multiprotein transcriptional complex required for activity of the human cardiac alpha-actin promoter. Mol. Cell. Biol. 19, 2577-2584. (Pubitemid 29144501)
6. Blais, A., Tsikitis, M., Acosta-Alvear, D., et al. (2005). An initial blueprint for myogenic differentiation. Genes Dev. 19, 553-569. (Pubitemid 40314988)
7. Cabane, C., Englaro, W., Yeow, K., et al. (2003). Regulation of C2C12 myogenic terminal differentiation by MKK3/p38alpha pathway. Am. J. Physiol. Cell Physiol. 284, C658-C666. (Pubitemid 36237518)
8. Cabantous, S., and Waldo, G.S. (2006). In vivo and in vitro protein solubility assays using split GFP. Nat. Methods 3, 845-854. (Pubitemid 44445833)
9. Cao, Y., Kumar, R.M., Penn, B.H., et al. (2006). Global and gene-specific analyses show distinct roles for MyoD and Myog at a common set of promoters. EMBO J. 25, 502-511. (Pubitemid 43237657)
10. Charge, S.B., and Rudnicki, M.A. (2004). Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238. (Pubitemid 38049880)
11. Charrin, S., le Naour, F., Silvie, O., et al. (2009). Lateral organization of membrane proteins: tetraspanins spin their web. Biochem. J. 420, 133-154.
12. Chen, E.H., Grote, E., Mohler, W., et al. (2007). Cell-cell fusion. FEBS Lett. 581, 2181-2193. (Pubitemid 46722606)
13. Deneka, M., Pelchen-Matthews, A., Byland, R., et al. (2007). In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J. Cell Biol. 177, 329-341. (Pubitemid 46658643)
14. Dilworth, F.J., and Blais, A. (2011). Epigenetic regulation of satellite cell activation during muscle regeneration. Stem Cell Res. Ther. 2, 18.
15. Falcon, S., and Gentleman, R. (2007). Using GOstats to test gene lists for go term association. Bioinformatics 23, 257-258. (Pubitemid 46189622)
16. Gillespie, M.A., Le Grand, F., Scime, A., et al. (2009). P38-{gamma}-dependent gene silencing restricts entry into the myogenic differentiation program. J. Cell Biol. 187, 991-1005.
17. Glass, D.J. (2010). Signaling pathways perturbing muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 13, 225-229.
18. Hasty, P., Bradley, A., Morris, J.H., et al. (1993). Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506. (Pubitemid 23273093)
19. Huber, W., von Heydebreck, A., Sultmann, H., et al. (2002). Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl 1), S96-S104. (Pubitemid 41185642)
20. Irizarry, R.A., Bolstad, B.M., Collin, F., et al. (2003). Summaries of affymetrix genechip probe level data. Nucleic Acids Res. 31, e15.
21. Jang, Y.N., Lee, I.J., Park, M.C., et al. (2012). Role of JAK3 in myogenic differentiation. Cell. Signal. 24, 742-749.
22. Jegou, A., Ziyyat, A., Barraud-Lange, V., et al. (2011). CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. Proc. Natl Acad. Sci. USA 108, 10946-10951.
23. Joe, A.W., Yi, L., Natarajan, A., et al. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12, 153-163.
24. Junion, G., Bataille, L., Jagla, T., et al. (2007). Genome-wide view of cell fate specification: Ladybird acts at multiple levels during diversification of muscle and heart precursors. Genes Dev. 21, 3163-3180. (Pubitemid 350223532)
25. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., et al. (2004). Mrf4 determines skeletal muscle identity in Myf5:MyoD double-mutant mice. Nature 431, 466-471. (Pubitemid 39329587)
26. Keren, A., Tamir, Y., and Bengal, E. (2006). The p38 MAPK signaling pathway: A major regulator of skeletal muscle development. Mol. Cell. Endocrinol. 252, 224-230.
27. Lassar, A.B., Davis, R.L., Wright, W.E., et al. (1991). Functional activity of myo-genic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell 66, 305-315. (Pubitemid 121001368)
28. Lluis, F., Ballestar, E., Suelves, M., et al. (2005). E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle-specific gene transcription. EMBO J. 24, 974-984. (Pubitemid 40470146)
29. Luo, D., Renault, V.M., and Rando, T.A. (2005). The regulation of notch signaling in muscle stem cell activation and postnatal myogenesis. Semin. Cell Dev. Biol. 16, 612-622. (Pubitemid 41247884)
30. Ma, Q., Chirn, G.W., Szustakowski, J.D., et al. (2008). Uncovering mechanisms of transcriptional regulations by systematic mining of cis regulatory elements with gene expression profiles. Bio. Data Min. 1, 4.
31. Murre, C., McCaw, P.S., Vaessin, H., et al. (1989). Interactions between heter-ologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537-544. (Pubitemid 19203538)
32. Nabeshima, Y., Hanaoka, K., Hayasaka, M., et al. (1993). Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532-535. (Pubitemid 23273098)
33. Nagel, S., Venturini, L., Przybylski, G.K., et al. (2009). Activation of mir-17-92 by NK-like homeodomain proteins suppresses apoptosis via reduction of E2F1 in T-cell acute lymphoblastic leukemia. Leuk. Lymphoma 50, 101-108.
34. Neville, C.M., Choe, Y.H., Lee, Y.S., et al. (1998). The E protein CTF4 and acetyl-choline receptor expression in development and denervation supersensitiv-ity. J. Biol. Chem. 273, 14046-14052. (Pubitemid 28268462)
35. O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., et al. (2005). c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839-843. (Pubitemid 40839736)
36. Palacios, D., Mozzetta, C., Consalvi, S., et al. (2010). TNF/p38alpha/Polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7, 455-469.
37. Penn, B.H., Bergstrom, D.A., Dilworth, F.J., et al. (2004). A MyoD-generated feed forward circuit temporally patterns gene expression during skeletal muscle differentiation. Genes Dev. 18, 2348-2353. (Pubitemid 39304681)
38. Perdiguero, E., Ruiz-Bonilla, V., Gresh, L., et al. (2007). Genetic analysis of p38 map kinases in myogenesis: Fundamental role of p38alpha in abrogating myoblast proliferation. EMBO J. 26, 1245-1256. (Pubitemid 46398710)
39. Rampalli, S., Li, L., Mak, E., et al. (2007). p38 MAPK signaling regulates recruitment of Ash2L-containing methyltransferase complexes to specific genes during differentiation. Nat. Struct. Mol. Biol. 14, 1150-1156. (Pubitemid 350223328)
40. Rochlin, K., Yu, S., Roy, S., et al. (2010). Myoblast fusion: When it takes more to make one. Dev. Biol. 341, 66-83.
41. Rudnicki, M.A., Braun, T., Hinuma, S., et al. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390.
42. Rudnicki, M.A., Schnegelsberg, P.N., Stead, R.H., et al. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359. (Pubitemid 24021909)
43. Seenundun, S., Rampalli, S., Liu, Q.C., et al. (2010). UTX mediates demethyla-tion of H3K27me3 at muscle-specific genes during myogenesis. EMBO J. 29, 1401-1411.
44. Simone, C., Forcales, S.V., Hill, D.A., et al. (2004). p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat. Genet. 36, 738-743. (Pubitemid 38886636)
45. Smyth, G.K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3.
46. Spinner, D.S., Liu, S., Wang, S.W., et al. (2002). Interaction of the myogenic determination factor myogenin with E12 and a DNA target: Mechanism and kinetics. J. Mol. Biol. 317, 431-445. (Pubitemid 34722181)
47. Subramanian, A., Tamayo, P., Mootha, V.K., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550. (Pubitemid 41528093)
48. Sylvestre, Y., De Guire, V., Querido, E., et al. (2007). An E2F/mir-20a autoregu-latory feedback loop. J. Biol. Chem. 282, 2135-2143.
49. Szklarczyk, D., Franceschini, A., Kuhn, M., et al. (2011). The string database in 2011: Functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568.
50. Tachibana, I., and Hemler, M.E. (1999). Role of transmembrane 4 superfamily (tm4sf) proteins CD9 and CD81 in muscle cell fusion and myotube maintenance. J. Cell Biol. 146, 893-904. (Pubitemid 29408913)
51. Takeda, Y., Tachibana, I., Miyado, K., et al. (2003). Tetraspanins CD9 and CD81 function to prevent the fusion of mononuclear phagocytes. J. Cell Biol. 161, 945-956. (Pubitemid 36718427)
52. Tapscott, S.J. (2005). The circuitry of a master switch: MyoD and the regulation of skeletal muscle gene transcription. Development 132, 2685-2695. (Pubitemid 40932860)
53. Tschop, K., Conery, A.R., Litovchick, L., et al. (2011). A kinase shrna screen links Lats2 and the prb tumor suppressor. Genes Dev. 25, 814-830.
54. Ustanina, S., Carvajal, J., Rigby, P., et al. (2007). The myogenic factor Myf5 supports efficient skeletal muscle regeneration by enabling transient myoblast amplification. Stem Cells 25, 2006-2016. (Pubitemid 47258178)
55. Wang, Y., and Jaenisch, R. (1997). Myogenin can substitute for Myf5 in promoting myogenesis but less efficiently. Development 124, 2507-2513. (Pubitemid 27341751)
56. Wang, J., and Conboy, I. (2010). Embryonic vs. Adult myogenesis: Challenging the 'regeneration recapitulates development' paradigm. J. Mol. Cell Biol. 2, 1-4.
57. Wu, Z., Woodring, P.J., Bhakta, K.S., et al. (2000). p38 and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol. Cell. Biol. 20, 3951-3964. (Pubitemid 30314494)
58. Yaffe, D., and Saxel, O. (1977). Serial passaging and differentiation of myogen-ic cells isolated from dystrophic mouse muscle. Nature 270, 725-727. (Pubitemid 8239246)
59. Zetser, A., Gredinger, E., and Bengal, E. (1999). p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J. Biol. Chem. 274, 5193-5200.
60. Zhang, K., Sha, J., and Harter, M.L. (2010). Activation of cdc6 by MyoD is associated with the expansion of quiescent myogenic satellite cells. J. Cell Biol. 188, 39-48.
61. Zhao, M., New, L., Kravchenko, V.V., et al. (1999). Regulation of the Mef2 family of transcription factors by p38. Mol. Cell. Biol. 19, 21-30. (Pubitemid 29018406)