Proteome dynamics during C2C12 myoblast differentiation

Molecular and Cellular Proteomics

Volumn 4, Issue 7, 2005, Pages 887-901

  Kislinger, Thomas ^a   Gramolini, Anthony O ^a,b   Pan, Yan ^a,b,c   Rahman, Khaled ^a,d   MacLennan, David H ^a   Emili, Andrew ^a,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b HEART AND STROKE FOUNDATION OF CANADA   (Canada)

^c Protana Inc   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

^e CH Best Institute   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ALPHA5 INTEGRIN; BUTYRYL COENZYME A DEHYDROGENASE; COLECALCIFEROL RECEPTOR; CULLIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DESMIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA PRIMASE; EMERIN; FIBRONECTIN; FOCAL ADHESION KINASE; FUMARATE HYDRATASE; INITIATION FACTOR 3; ISOCITRATE DEHYDROGENASE; LONG CHAIN ACYL COENZYME A DEHYDROGENASE; MALATE DEHYDROGENASE; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; PLAKOGLOBIN; PROFILIN; PROTEIN KINASE C ALPHA; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SUPEROXIDE DISMUTASE; TATA BINDING PROTEIN ASSOCIATED FACTOR; TELOMERIC REPEAT BINDING FACTOR 2; VIMENTIN; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL METABOLISM; CONTROLLED STUDY; CYTOARCHITECTURE; DEVELOPMENTAL STAGE; GENETIC TRANSCRIPTION; LIQUID CHROMATOGRAPHY; MOLECULAR DYNAMICS; MOUSE; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MYOBLAST; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 24944559026     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M400182-MCP200     Document Type: Article

References (64)

1. Pownall, M. E., Gustafsson, M. K., and Emerson, C. P., Jr. (2002) Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747-783
2. Parker, M. H., Seale, P., and Rudnicki, M. A. (2003) Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat. Rev. Genet. 4, 497-507
3. Arnold, H. H., and Winter, B. (1998) Muscle differentiation: more complexity to the network of myogenic regulators. Curr. Opin. Genet. Dev. 8, 539-544
4. Black, B. L., and Olson, E. N. (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14, 167-196
5. Shen, X., Collier, J. M., Hlaing, M., Zhang, L., Delshad, E. H., Bristow, J., and Bernstein, H. S. (2003) Genome-wide examination of myoblast cell cycle withdrawal during differentiation. Dev. Dyn. 226, 128-138
6. Delgado, I., Huang, X., Jones, S., Zhang, L., Hatcher, R., Gao, B., and Zhang, P. (2003) Dynamic gene expression during the onset of myoblast differentiation in vitro. Genomics 82, 109-121
7. Tomczak, K. K., Marinescu, V. D., Ramoni, M. F., Sanoudou, D., Montanaro, F., Han, M., Kunkel, L. M., Kohane, I. S., and Beggs, A. H. (2004) Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J. 18, 403-405
8. Gygi, S. P., Rochon, Y., Franza, B. A., and Aebersold, R. (1999) Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730
9. Greenbaum, D., Colangelo, C., Williams, K., and Gerstein, M. (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol. http://genomebiology.com/2003/4/9/117
10. Hegde, P. S., White, I. R., and Debouck, C. (2003) Interplay of transcriptomics and proteomics. Curr. Opin. Biotechnol. 14, 647-651
11. Tannu, N. S., Rao, V. K., Chaudhary, R. M., Giorgianni, F., Saeed, A. E., Gao, Y., and Raghow, R. (2004) Comparative proteomes of the proliferating C2C12 myoblasts and fully differentiated myotubes reveal the complexity of the skeletal muscle differentiation program. Mol. Cell. Proteomics 3, 1065-1082
12. Griffin, T. J., Goodlett, D. R., and Aebersold, R. (2001) Advances in proteome analysis by mass spectrometry. Curr. Opin. Biotechnol. 12, 607-612
13. Gygi, S. P., Rist, B., and Aebersold, R. (2000) Measuring gene expression by quantitative proteome analysis. Curr. Opin. Biotechnol. 11, 396-401
14. Kislinger, T., and Emili, A. (2003) Going global: protein expression profiling using shotgun mass spectrometry. Curr. Opin. Mol. Ther. 5, 285-293
15. Aebersold, R., and Mann, M. (2003) Mass spectrometry-based proteomics. Nature 422, 198-207
16. Washburn, M. P., Wolters, D., and Yates, J. R., III (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247
17. Kislinger, T., Rahman, K., Radulovic, D., Cox, B., Rossant, J., and Emili, A. (2003) PRISM, a generic large scale proteomic investigation strategy for mammals. Mol. Cell. Proteomics 2, 96-106
18. Eng, J. K., McCormack, A. L., and Yates, J. R., III (1994) An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database. J. Am. Soc. Mass Spectrom. 11, 976-989
19. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
20. Liu, H., Sadygov, R. G., and Yates, J. R., III (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201
21. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95, 14863-14868
22. Robinson, M. D., Grigull, J., Mohammad, N., and Hughes, T. R. (2002) FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3, 35
23. Gramolini, A. O., and Jasmin, B. J. (1999) Expression of the utrophin gene during myogenic differentiation. Nucleic Acids Res. 27, 3603-3609
24. Corthals, G. L., Wasinger, V. C., Hochstrasser, D. F., and Sanchez, J. C. (2000) The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis 21, 1104-1115
25. Bairoch, A., and Apweiler, R. (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28, 45-48
26. Wu, L. F., Hughes, T. R., Davierwala, A. P., Robinson, M. D., Stoughton, R., and Altschuler, S. J. (2002) Large-scale prediction of Saccharomyces cerevisiae gene function using overlapping transcriptional clusters. Nat. Genet. 31, 255-265
27. Rida, P. C., Le Minh, N., and Jiang, Y. J. (2004) A Notch feeling of somite segmentation and beyond. Dev. Biol. 265, 2-22
28. Sheffield-Moore, M., and Urban, R. J. (2004) An overview of the endocrinology of skeletal muscle. Trends Endocrinol. Metab. 15, 110-115
29. Guttridge, D. C. (2004) Signaling pathways weigh in on decisions to make or break skeletal muscle. Curr. Opin. Clin. Nutr. Metab. Care 7, 443-450
30. Le Roch, K. G., Johnson, J. R., Florens, L., Zhou, Y., Santrosyan, A., Grainger, M., Yan, S. F., Williamson, K. C., Holder, A. A., Carucci, D. J., Yates, J. R., III, and Winzeler, E. A. (2004) Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 14, 2308-2318
31. Schulz, R. A., and Yutzey, K. E. (2004) Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev. Biol. 266, 1-16
32. Martin, P. T. (2003) Role of transcription factors in skeletal muscle and the potential for pharmacological manipulation. Curr. Opin. Pharmacol. 3, 300-308
33. Solloway, M. J., and Harvey, R. P. (2003) Molecular pathways in myocardial development: a stem cell perspective. Cardiovasc. Res. 58, 264-277
34. Baylies, M. K., and Michelson, A. M. (2001) Invertebrate myogenesis: looking back to the future of muscle development. Curr. Opin. Genet. Dev. 11, 431-439
35. Walsh, K., and Perlman, H. (1997) Cell cycle exit upon myogenic differentiation. Curr. Opin. Genet. Dev. 7, 597-602
36. Wei, Q., and Paterson, B. M. (2001) Regulation of MyoD function in the dividing myoblast. FEBS Lett. 490, 171-178
37. Purl, P. L., and Sartorelli, V. (2000) Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J. Cell. Physiol. 185, 155-173
38. Ornatsky, O. I., and McDermott, J. C. (1996) MEF2 protein expression, DNA binding specificity and complex composition, and transcriptional activity in muscle and non-muscle cells. J. Biol. Chem. 271, 24927-24933
39. Di Lisi, R., Millino, C., Calabria, E., Altruda, F., Schiaffino, S., and Ausoni, S. (1998) Combinatorial cis-acting elements control tissue-specific activation of the cardiac troponin I gene in vitro and in vivo. J. Biol. Chem. 273, 25371-25380
40. Spitz, F., Demignon, J., Porteu, A., Kahn, A., Concordet, J. P., Daegelen, D., and Maire, P. (1998) Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc. Natl. Acad. Sci. U. S. A. 95, 14220-14225
41. Parmacek, M. S., Ip, H. S., Jung, F., Shen, T., Martin, J. F., Vora, A. J., Olson, E. N., and Leiden, J. M. (1994) A novel myogenic regulatory circuit controls slow/cardiac troponin C gene transcription in skeletal muscle. Mol. Cell. Biol. 14, 1870-1885
42. Himeda, C. L., Ranish, J. A., Angello, J. C., Maire, P., Aebersold, R., and Hauschka, S. D. (2004) Quantitative proteomic identification of six4 as the trex-binding factor in the muscle creatine kinase enhancer. Mol. Cell. Biol. 24, 2132-2143
43. Joh, K., Takano, K., Mukai, T., and Hori, K. (1991) Analysis of upstream regulatory regions required for the activities of two promoters of the rat aldolase A gene. FEBS Lett. 292, 128-132
44. Spitz, F., Salminen, M., Demignon, J., Kahn, A., Daegelen, D., and Maire, P. (1997) A combination of MEF3 and NF1 proteins activates transcription in a subset of fast-twitch muscles. Mol. Cell. Biol. 17, 656-666
45. Bassel-Duby, R., Hernandez, M. D., Yang, Q., Rochelle, J. M., Seldin, M. F., and Williams, R. S. (1994) Myocyte nuclear factor, a novel winged-helix transcription factor under both developmental and neural regulation in striated myocytes. Mol. Cell. Biol. 14, 4596-4605
46. Yang, Q., Bassel-Duby, R., and Williams, R. S. (1997) Transient expression of a winged-helix protein, MNF-β, during myogenesis. Mol. Cell. Biol. 17, 5236-5243
47. Lai, E., Clark, K. L., Burley, S. K., and Darnell, J. E., Jr. (1993) Hepatocyte nuclear factor 3/fork head or "winged helix" proteins: a family of transcription factors of diverse biologic function. Proc. Natl. Acad. Sci. U. S. A. 90, 10421-10423
48. Scita, G., Tenca, P., Frittoli, E., Tocchetti, A., Innocenti, M., Giardina, G., and Di Fiore, P. P. (2000) Signaling from Ras to Rac and beyond: not just a matter of GEFs. EMBO J. 19, 2393-2398
49. Molkentin, J. D., and Dorn, I. G., II (2001) Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu. Rev. Physiol. 63, 391-426
50. Presslauer, S., Hinterhuber, G., Cauza, K., Horvat, R., Rappersberger, K., Wolff, K., and Foedinger, D. (2003) RasGAP-like protein IQGAP1 is expressed by human keratinocytes and recognized by autoantibodies in association with bullous skin disease. J. Investig. Dermatol. 120, 365-371
51. Dahlqvist, C., Blokzijl, A., Chapman, G., Falk, A., Dannaeus, K., Ibanez, C. F., and Lendahl, U. (2003) Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130, 6089-6099
52. Wilson-Rawls, J., Molkentin, J. D., Black, B. L., and Olson, E. N. (1999) Activated notch inhibits myogenic activity of the MADS-box transcription factor myocyte enhancer factor 2C. Mol. Cell. Biol. 19, 2853-2862
53. Conboy, I. M., and Rando, T. A. (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3, 397-409
54. Zhu, S., Goldschmidt-Clermont, P. J., and Dong, C. (2004) Transforming growth factor-β-induced inhibition of myogenesis is mediated through Smad pathway and is modulated by microtubule dynamic stability. Circ. Res. 94, 617-625
55. Zhu, S., Goldschmidt-Clermont, P. J., and Dong, C. (1997) Smad1 and Smad5 act downstream of intracellular signalings of BMP-2 that inhibits myogenic differentiation and induces osteoblast differentiation in C2C12 myoblasts. Biochem. Biophys. Res. Commun. 238, 574-580
56. Moresco, E. M., and Koleske, A. J. (2003) Regulation of neuronal morphogenesis and synaptic function by Abl family kinases. Curr. Opin. Neurobiol. 13, 535-544
57. Burgess, H. A., and Reiner, O. (2000) Doublecortin-like kinase is associated with microtubules in neuronal growth cones. Mol. Cell. Neurosci. 16, 529-541
58. Caudell, E. G., Caudell, J. J., Tang, C. H., Yu, T. K., Frederick, M. J., and Grimm, E. A. (2000) Characterization of human copine III as a phospho-protein with associated kinase activity. Biochemistry 39, 13034-13043
59. Clark, K. A., McElhinny, A. S., Beckerle, M. C., and Gregorio, C. C. (2002) Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18, 637-706
60. MacLennan, D. H., and Kranias, E. G. (2003) Phospholamban: a crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell. Biol. 4, 566-577
61. Sartorelli, V., and Fulco, M. (2004) Molecular and cellular determinants of skeletal muscle atrophy and hypertrophy. Sci. STKE 2004, re11
62. Lapidos, K. A., Kakkar, R., and McNally, E. M. (2004) The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ. Res. 94, 1023-1031
63. Tian, Q., Stepaniants, S. B., Mao, M., Weng, L., Feetham, M. C., Doyle, M. J., Yi, E. C., Dai, H., Thorsson, V., Eng, J., Goodlett, D., Berger, J. P., Gunter, B., Linseley, P. S., Stoughton, R. B., Aebersold, R., Collins, S. J., Hanlon, W. A., and Hood, L. E. (2004) Integrated genomic and proteomic analyses of gene expression in mammalian cells. Mol. Cell. Proteomics 3, 960-969
64. Koller, A., Washburn, M. P., Lange, B. M., Andon, N. L., Deciu, C., Haynes, P. A., Hays, L., Schieltz, D., Ulaszek, R., Wei, J., Wolters, D., and Yates, J. R., III (2002) Proteomic survey of metabolic pathways in rice. Proc. Natl. Acad. Sci. U. S. A. 99, 11969-11974