Skeletal muscle myogenesis is regulated by G protein-coupled receptor kinase 2

Journal of Molecular Cell Biology

Volumn 6, Issue 4, 2014, Pages 299-311

  Garcia Guerra, Lucia ^a,b,c,d   Vila Bedmar, Rocío ^e,f   Carrasco Rando, Marta ^g   Cruces Sande, Marta ^e,f   Martín, Mercedes ^g   Ruiz Gómez, Ana ^g   Ruiz Gómez, Mar ^g   Lorenzo, Margarita ^a,b   Fernández Veledo, Sonia ^b,h   Mayor, Federico ^e,f   Murga, Cristina ^e,f   Nieto Vázquez, Iria ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^e CSIC   (Spain)

^f INSTITUTO DE INVESTIGACIÓN SANITARIA DEL HOSPITAL CLÍNICO SAN CARLOS IDISSC   (Spain)

^g CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^h HOSPITAL UNIVERSITARI JOAN XXIII   (Spain)

Author keywords

Akt; GRK2; myogenesis; p38MAPK; skeletal muscle

Indexed keywords

CAVEOLIN 3; G PROTEIN COUPLED RECEPTOR KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MYOGENIN; MYOSIN HEAVY CHAIN; PROTEIN KINASE B; SYNAPTOPHYSIN; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; DOWN REGULATION; DROSOPHILA MELANOGASTER; EMBRYO; FLIGHT MUSCLE; IN VITRO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE MASS; MYOBLAST; NEWBORN; NONHUMAN; POINT MUTATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE MYOGENESIS; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; FLUORESCENCE MICROSCOPY; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; DROSOPHILA MELANOGASTER; G-PROTEIN-COUPLED RECEPTOR KINASE 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOBLASTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84905174926     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mju025     Document Type: Article

References (63)

1. Abmayr, S.M., and Pavlath, G.K. (2012). Myoblast fusion: lessons from flies and mice. Development (England) 139, 641-656.
2. Alonso-Chamorro, M., Nieto-Vazquez, I., Montori-Grau, M., et al. (2011). New emerging role of protein-tyrosine phosphatase 1B in the regulation of glycogen metabolism in basal and TNF-a-induced insulin-resistant conditions in an immortalised muscle cell line isolated from mice. Diabetologia 54, 1157-1168.
3. Avendaño, M.S., Lucas, E., Jurado-Pueyo, M., et al. (2014). Increased nitric oxide bioavailability in adult GRK2 hemizygous mice protects against angiotensin II-induced hypertension. Hypertension 63, 369-375.
4. Bernet, J.D., and Rudnicki, M.A. (2014). Rejuvenating aged muscle stem cells. Nat. Med. 20, 265-271.
5. Blau, H.M., Pavlath, G.K., Hardeman, E.C., et al. (1985). Plasticity of the differentiated state. Science 230, 758-766.
6. Buckingham, M. (2001). Skeletal muscle formation in vertebrates. Curr. Opin. Genet. Dev. 11, 440-448.
7. Buckingham, M., Bajard, L., Chang, T., et al. (2003). The formation of skeletal muscle: from somite to limb. J. Anat. 202, 59-68.
8. Conejo, R., and Lorenzo, M. (2001). Insulin signaling leading to proliferation, survival, and membrane ruffling in C2C12 myoblasts. J. Cell. Physiol. 187, 96-108.
9. Conejo, R., de Alvaro, C., Benito, M., et al. (2002). Insulin restores differentiation of Ras-transformed C2C12 myoblasts by inducing NF-kappaB through an AKT/P70S6K/p38-MAPK pathway. Oncogene 21, 3739-3753.
10. Cuenda, A., and Cohen, P. (1999). Stress-activated protein kinase-2/p38 and a rapamycin-sensitive pathway are required for C2C12 myogenesis. J. Biol. Chem. 274, 4341-4346.
11. de Alvaro, C., Martinez, N., Rojas, J.M., et al. (2005). Sprouty-2 overexpression in C2C12 cells confers myogenic differentiation properties in the presence of FGF2. Mol. Biol. Cell 16, 4454-4461.
12. De Alvaro, C., Nieto-Vazquez, I., Rojas, J.M., et al. (2008). Nuclear exclusion of forkhead box O and Elk1 and activation of nuclear factor-kappaB are required for C2C12-RasV12C40 myoblast differentiation. Endocrinology 149, 793-801.
13. de Angelis, L., Zhao, J., Andreucci, J.J., et al. (2005). Regulation of vertebrate myotome development by the p38 MAP kinase-MEF2 signaling pathway. Dev. Biol. 283, 171-179.
14. Duffy, J.B. (2002). GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34, 1-15.
15. Dutta, D., Anant, S., Ruiz-Gomez, M., et al. (2004). Founder myoblasts and fibre number during adult myogenesis in Drosophila. Development 131, 3761-3772.
16. Essers, J., Theil, A.F., Baldeyron, C., et al. (2005). Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25, 9350-9359.
17. Fernandes, J., Bate, M., and Vijayraghavan, K. (1991). Development of the indirect flight muscles of Drosophila. Development 113, 67-77.
18. Fujio, Y., Guo, K.,Mano, T., et al. (1999). Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol. Cell. Biol. 19, 5073-5082.
19. Galbiati, F., Razani, B., and Lisanti, M.P. (2001). Caveolae and caveolin-3 in muscular dystrophy. Trends Mol. Med. 7, 435-441.
20. Garcia-Guerra, L., Nieto-Vazquez, I., Vila-Bedmar, R., et al. (2010). G proteincoupled receptor kinase 2 plays a relevant role in insulin resistance and obesity. Diabetes 59, 2407-2417.
21. Glass, D.J. (2010a). PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr. Top. Microbiol. Immunol. 346, 267-278.
22. Glass, D.J. (2010b). Signaling pathways perturbing muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 13, 225-229.
23. Gonzalez, I., Tripathi, G., Carter, E.J., et al. (2004). Akt2, a novel functional link between p38 mitogen-activated protein kinase and phosphatidylinositol 3-kinase pathways in myogenesis. Mol. Cell. Biol. 24, 3607-3622.
24. Jansen, K.M., and Pavlath, G.K. (2008). Molecular control of mammalian myoblast fusion. Methods Mol. Biol. 475, 115-133.
25. Jiang, B.H., Aoki, M., Zheng, J.Z., et al. (1999). Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc. Natl Acad. Sci. USA 96, 2077-2081.
26. Katzemich, A., Kreiskother, N., Alexandrovich, A., et al. (2012). The function of the M-line protein obscurin in controlling the symmetry of the sarcomere in the flight muscle of Drosophila. J. Cell Sci. 125, 3367-3379.
27. Kelso, R. J., Buszczak, M., Quinones, A. T., et al. (2004). Flytrap, a database documenting a GFP protein-trap insertion screen in Drosophila melanogaster. Nucleic Acids Res. 32, D418-D420.
28. Keren, A., Bengal, E., and Frank, D. (2005). p38MAP kinase regulates the expression of XMyf5 and affects distinct myogenic programs during Xenopus development. Dev. Biol. 288, 73-86.
29. Krauss, R.S. (2010). Regulation of promyogenic signal transduction by cell-cell contact and adhesion. Exp. Cell Res. 316, 3042-3049.
30. Koopman, R., Ryall, J.G., Church, J.E., et al. (2009). The role of beta-adrenoceptor signaling in skeletal muscle: therapeutic implications for muscle wasting disorders. Curr. Opin. Clin. Nutr. Metab. Care 12, 601-606.
31. Lafarga,V., Aymerich, I., Tapia, O.,et al.(2012).AnovelGRK2/HDAC6 interaction modulates cell spreading and motility. EMBO J. 31,856-869.
32. Li, Y., Jiang, B., Ensign,W.Y., et al. (2000). Myogenic differentiation requires signalling through both phosphatidylinositol 3-kinase and p38 MAP kinase. Cell. Signal. 12, 751-757.
33. Liu, C.J., Ding, B., Wang, H., et al. (2002). The MyoD-inducible p204 protein overcomes the inhibition of myoblast differentiation by Id proteins. Mol. Cell. Biol. 22, 2893-2905.
34. Lluis, F., Perdiguero, E., Nebreda, A.R., et al. (2006). Regulation of skeletal muscle gene expression by p38 MAP kinases. Trends Cell Biol. 16, 36-44.
35. Lynch, G.S., and Ryall, J.G. (2008). Role of beta-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol. Rev. 88, 729-767.
36. Molnar, C., Holguin, H.,Mayor, F., Jr, et al. (2007). TheGprotein-coupled receptor regulatory kinase GPRK2 participates in Hedgehog signaling in Drosophila. Proc. Natl Acad. Sci. USA 104, 7963-7968.
37. Nebreda, A.R., and Porras, A. (2000). p38 MAP kinases: beyond the stress response. Trends Biochem. Sci. 25, 257-260.
38. Niu, A., Wen, Y., Liu, H., et al. (2013). Src mediates the mechanical activation of myogenesis by activating TNFalpha-converting enzyme. J. Cell Sci. 126, 4349-4357.
39. 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.
40. Penela, P., Ribas, C., and Mayor, F., Jr. (2003). Mechanisms of regulation of the expression and function of G protein-coupled receptor kinases. Cell. Signal. 15, 973-981.
41. Penela, P., Murga, C., Ribas, C., et al. (2010). The complex G protein-coupled receptor kinase 2 (GRK2) interactome unveils new physiopathological targets. Br. J. Pharmacol. 160, 821-832.
42. Penn, B.H., Bergstrom, D.A., Dilworth, F.J., et al. (2004). A MyoD-generated feedforward circuit temporally patterns gene expression during skeletal muscle differentiation. Genes Dev. 18, 2348-2353.
43. Perdiguero, E., Ruiz-Bonilla, V., Gresh, L., et al. (2007a). Genetic analysis of p38 MAPkinases in myogenesis: fundamental role of p38alpha in abrogating myoblast proliferation. EMBO J. 26, 1245-1256.
44. Perdiguero, E., Ruiz-Bonilla, V., Serrano, A.L., et al. (2007b). Genetic deficiency of p38alpha reveals its critical role in myoblast cell cycle exit: the p38alpha-JNK connection. Cell Cycle 6, 1298-1303.
45. Peregrin, S., Jurado-Pueyo, M., Campos, P.M., et al. (2006). Phosphorylation of p38MAPKbyGRK2 at the docking groove unveils a novel mechanism for inactivating p38MAPK. Curr. Biol. 16, 2042-2047.
46. Poznic, M. (2009). Retinoblastoma protein: a central processing unit. J. Biosci. 34, 305-312.
47. Ribas, C., Penela, P., Murga, C., et al. (2007). The G protein-coupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim. Biophys. Acta 1768, 913-922.
48. Roy, S., and VijayRaghavan, K. (1998). Patterning muscles using organizers: larval muscle templates and adult myoblasts actively interact to pattern the dorsal longitudinal flight muscles of Drosophila. J. Cell Biol. 141, 1135-1145.
49. Sabourin, L.A., Girgis-Gabardo, A., Seale, P., et al. (1999). Reduced differentiation potential of primary MyoD-/-myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144, 631-643.
50. Salcedo, A., Mayor, F., Jr, and Penela, P. (2006). Mdm2 is involved in the ubiquitination and degradation of G-protein-coupled receptor kinase 2. EMBO J. 25, 4752-4762.
51. Schuster-Gossler, K., Cordes, R., and Gossler, A. (2007).Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc. Natl Acad. Sci. USA 104, 537-542.
52. Serrano, A.L., Baeza-Raja, B., Perdiguero, E., et al. (2008). Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 7, 33-44.
53. Shen, X., Collier, J.M., Hlaing, M., et al. (2003). Genome-wide examination of myoblast cell cycle withdrawal during differentiation. Dev. Dyn. 226, 128-138.
54. Simionescu, A., and Pavlath, G.K. (2011). Molecular mechanisms of myoblast fusion across species. Adv. Exp. Med. Biol. 713, 113-135.
55. Soler, C., and Taylor, M.V. (2009). The Him gene inhibits the development of Drosophila flight muscles during metamorphosis. Mech. Dev. 126, 595-603.
56. Soler, C., Daczewska, M., Da Ponte, J.P., et al. (2004). Coordinated development of muscles and tendons of the Drosophila leg. Development 131, 6041-6051.
57. Stoker, M., and Gherardi, E. (1991). Regulation of cell movement: the motogenic cytokines. Biochim. Biophys. Acta 1072, 81-102.
58. Suelves, M., Lluis, F., Ruiz, V., et al. (2004). Phosphorylation of MRF4 transactivation domain by p38MAPK mediates repression of specific myogenic genes. EMBO J. 23, 365-375.
59. Vrailas-Mortimer, A., del Rivero, T., Mukherjee, S., et al. (2011). A musclespecific p38MAPK MAPK/Mef2/MnSOD pathway regulates stress, motor function, and life span in Drosophila. Dev. Cell 21, 783-795.
60. Weintraub, H. (1993). The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241-1244.
61. Wu, Z., Woodring, P.J., Bhakta, K.S., et al. (2000). p38MAPK and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol. Cell. Biol. 20, 3951-3964.
62. Zarubin, T., and Han, J. (2005). Activation and signaling of the p38 MAP kinase pathway. Cell Res. 15, 11-18.
63. 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.