Global relationship between the proteome and transcriptome of human skeletal muscle

Journal of Proteome Research

Volumn 7, Issue 8, 2008, Pages 3230-3241

  Yi, Zhengping ^a,b   Bowen, Benjamin P ^a,c   Hwang, Hyonson ^a   Jenkinson, Christopher P L ^d   Coletta, Dawn K ^d   Lefort, Natalie ^a   Bajaj, Mandeep ^d   Kashyap, Sangeeta ^d   Berria, Rachele ^d   De Filippis, Elena A ^a   Mandarino, Lawrence J ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c Arizona State University   (United States)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Gene ontology; HPLC ESI MS MS; Human skeletal muscle; Microarrays; Proteomic analysis; Tissue profiling; Transcriptome

Indexed keywords

LYASE; MUSCLE PROTEIN; PHOSPHOTRANSFERASE; PROTEOME; TRANSCRIPTOME;

ADULT; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; ELECTRON TRANSPORT; ENZYME ACTIVITY; GOLGI COMPLEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; VASTUS LATERALIS MUSCLE; COMPARATIVE STUDY; ELECTROSPRAY MASS SPECTROMETRY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MIDDLE AGED; SKELETAL MUSCLE; TANDEM MASS SPECTROMETRY;

ADULT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GENE EXPRESSION PROFILING; HUMANS; MIDDLE AGED; MUSCLE PROTEINS; MUSCLE, SKELETAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEOME; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 53049093175     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr800064s     Document Type: Article

References (50)

1. Hojlund, K.; Beck-Nielsen, H. Impaired glycogen synthase activity and mitochondrial dysfunction in skeletal muscle. Markers or mediators in type 2 diabetes. Curr. Diabetes Rev. 2006, 2, 375-395.
2. Krebs, M.; Roden, M. Molecular mechanisms of lipid-induced insulin resistance in muscle, liver and vasculature. Diabetes Obes. Metab. 2005, 7 (6), 621-32.
3. Lowell, B. B.; Shulman, G. I. Mitochondrial dysfunction and type 2 diabetes. Science 2005, 307 (5708), 384-387.
4. Pirola, L.; Johnston, A. M.; Van Obberghen, E. Modulation of insulin action. Diabetologia 2004, 47 (2), 170-184.
5. Kelley, D. E.; Mandarino, L. J. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 2000, 49 (5), 677-683.
6. Giresi, P. G.; Stevenson, E. J.; Theilhaber, J.; Koncarevic, A.; Parkington, J.; Fielding, R. A.; Kandarian, S. C. Identification of a molecular signature of sarcopenia. Physiol. Genomics 2005, 21 (2), 253-263.
7. Patti, M. E.; Butte, A. J.; Crunkhorn, S.; Cusi, K.; Berria, R.; Kashyap, S.; Miyazaki, Y.; Kohane, I.; Costello, M.; Saccone, R.; Landaker, E. J.; Goldfine, A. B.; Mun, E.; DeFronzo, R.; Finlayson, J.; Kahn, C. R.; Mandarino, L. J. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. U.SA. 2003, 100 (14), 8466-8471.
8. Mootha, V. K.; Lindgren, C. M.; Eriksson, K. F.; Subramanian, A.; Sihag, S.; Lehar, J.; Puigserver, P.; Carlsson, E.; Ridderstrale, M.; Laurila, E.; Houstis, N.; Daly, M. J.; Patterson, N.; Mesirov, J. P.; Golub, T. R.; Tamayo, P.; Spiegelman, B.; Lander, E. S.; Hirschhorn, J. N.; Altshuler, D.; Groop, L. C. PGC-1 alpha-responsive genes involved in oxidative phosphorylation are coordinately downregu-lated in human diabetes. Nat. Genet. 2003, 34 (3), 267-273.
9. Sreekumar, R.; Halvatsiotis, P.; Schimke, J. C.; Nair, K. S. Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes 2002, 51 (6), 1913-1920.
10. Richardson, D. K.; Kashyap, S.; Bajaj, M.; Cusi, K.; Mandarino, S. J.; Finlayson, J.; DeFronzo, R. A.; Jenkinson, C. P.; Mandarino, L. J. Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J. Biol. Chem. 2005, 280 (11), 10290-10297.
11. Winokur, S. T.; Chen, Y. W.; Masny, P. S.; Martin, J. FL; Ehmsen, J. T.; Tapscott, S. J.; van der Maarel, S. M.; Hayashi, Y.; Flanigan, K. M. Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum. Mol. Genet. 2003, 12 (22), 2895-2907.
12. Batt, J.; Bain, J.; Goncalves, J.; Michalski, B.; Plant, P.; Fahnestock, M.; Woodgett, J. Differential gene expression profiling of short and long term denervated muscle. FASEB J. 2006, 20 (1), 115-117.
13. Teran-Garcia, M.; Rankinen, T.; Koza, R. A.; Rao, D. C.; Bouchard, C. Endurance training-induced changes in insulin sensitivity and gene expression. Am. J. Physiol. Endocrinol. Metab. 2005, 288 (6), El 168-1178.
14. Anderson, L.; Seilhamer, J. A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 1997, 18 (3-4), 533-537.
15. Gygi, S. P.; Rochon, Y.; Franza, B. R.; Aebersold, R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 1999, 19 (3), 1720-1730.
16. Hojlund, K.; Wrzesinski, K.; Larsen, P. M.; Fey, S. J.; Roepstorff, P.; Handberg, A.; Dela, F.; Vinten, J.; McCormack, J. G.; Reynet, C.; Beck-Nielsen, H. Proteome analysis reveals phosphorylation of ATP synthase beta-subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes. J. Biol. Chem. 2003, 278 (12), 10436-10442.
17. Hittel, D. S.; Hathout, Y.; Hoffman, E. P.; Houmard, J. A. Proteome analysis of skeletal muscle from obese and morbidly obese women. Diabetes 2005, 54 (5), 1283-1288.
18. Gelfi, C.; Vigano, A.; Ripamonti, 'M.; Pontoglio, A.; Begum, S.; Pellegrino, M. A.; Grassi, B.; Bottinelli, R.; Wait, R.; Cerretelli, P. The human muscle proteome in aging. J. Proteome Res. 2006, 5 (6), 1344-1353.
19. Capitanio, D.; Vigano, A.; Ricci, E.; Cerretelli, P.; Wait, R.; Gelfi, C. Comparison of protein expression in human deltoideus and vastus lateralis muscles using two-dimensional gel electrophoresis. Proteomics 2005, 5 (10), 2577-2586.
20. Gelfi, C.; De Palma, S.; Cerretelli, P.; Begum, S.; Wait, R. Two-dimensional protein map of human vastus lateralis muscle. Electrophoresis 2003, 24 (1-2), 286-295.
21. Gelfi, C.; De Palma, S.; Ripamonti, M.; Eberini, I.; Wait, R.; Bajracharya, A.; Marconi, C.; Schneider, A.; Hoppeler, H.; Cerretelli, P. New aspects of altitude adaptation in Tibetans: a proteomic approach. FASEB J. 2004, 18 (3), 612-614.
22. Adachi, J.; Kumar, C.; Zhang, Y.; Mann, M. In-depth analysis of the adipocyte proteome by mass spectrometry and bioinformatics. Mol. Cell. Proteomics 2007, 6 (7), 1257-1273.
23. Brockmann, R.; Beyer, A.; Heinisch, J. J.; Wilhelm, T. Posttran-scriptional expression regulation: what determines translation rates. PLoS Comput. Biol. 2007, 3 (3), e57.
24. Chen, Y. R.; Juan, H. F.; Huang, H. C.; Huang, H. H.; Lee, Y. J.; Liao, M. Y.; Tseng, C. W.; Lin, L. L.; Chen, J. Y.; Wang, M. J.; Chen, J. H.; Chen, Y. J. Quantitative proteomic and genomic profiling reveals metastasis-related protein expression patterns in gastric cancer cells. J. Proteome Res. 2006, 5 (10), 2727-2742.
25. Greenbaum, D.; Jansen, R.; Gerstein, M. Analysis of mRNA expression and protein abundance data: an approach for the comparison of the enrichment of features in the cellular population of proteins and transcripts. Bioinformatics 2002, 18 (4), 585- 596.
26. Ideker, T.; Thorsson, V.; Ranish, J. A.; Christmas, R.; Buhler, J.; Eng, J. K.; Bumgarner, R.; Goodlett, D. R.; Aebersold, R.; Hood, L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 2001, 292 (5518), 929-934.
27. Nissom, P. M.; Sanny, A.; Kok, Y. J.; Hiang, Y. T.; Chuah, S. H.; Shing, T. K.; Lee, Y. Y.; Wong, K. T.; Hu, W. S.; Sim, M. Y.; Philp, R. Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Mol. Biotechnol. 2006, 34 (2), 125-140.
28. Schmidt, M. W.; Houseman, A.; Ivanov, A. R.; Wolf, D. A. Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe. Mol. Syst. Biol. 2007, 3, 79.
29. Unwin, R. D.; Whetton, A. D. Systematic proteome and transcriptome analysis of stem cell populations. Cell Cycle 2006, 5 (15), 1587-1591.
30. Yin, L.; Tao, Y.; Zhao, K.; Shao, J.; Li, X.; Liu, G.; Liu, S.; Zhu, L. Proteomic and transcriptomic analysis of rice mature seed-derived callus differentiation. Proteomics 2007, 7 (5), 755-768.
31. Joosen, R.; Cordewener, J.; Supena, E. D.; Vorst, O.; Lammers, M.; Maliepaard, C.; Zeilmaker, T.; Miki, B.; America, T.; Custers, J.; Boutilier, K. Combined transcriptome and proteome analysis identifies pathways and markers associated with the establishment of rapeseed microspore-derived embryo development. Plant Physiol. 2007, 144 (1), 155-12.
32. Cox, B.; Kislinger, T.; Emili, A. Integrating gene and protein expression data: pattern analysis and profile mining. Methods 2005, 35 (3), 303-314.
33. Mootha, V. K.; Bunkenborg, J.; Olsen, J. V.; Hjerrild, M.; Wisniewski, J. R.; Stahl, E.; Bolouri, M. S.; Ray, H. N.; Sihag, S.; Kamal, M.; Patterson, N.; Lander, E. S.; Mann, M. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 2003, 115 (5), 629-440.
34. 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.; Hood, L. E. Integrated genomic and proteomic analyses of gene expression in Mammalian cells. Mol. Cell. Proteomics 2004, 3 (10), 960-969.
35. McNicoll, F.; Drummelsmith, J.; Muller, M.; Madore, E.; Boilard, N.; Ouellette, M.; Papadopoulou, B. A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics 2006, 6 (12), 3567-3581.
36. Xun, Z.; Sowell, R. A.; Kaufman, T. C.; Clemmer, D. E. Protein expression in a Drosophila model of Parkinson's disease. J. Proteome Res. 2007, 6 (1), 348-357.
37. Habermann, J. K.; Paulsen, U.; Roblick, U. J.; Upender, M. B.; McShane, L. M.; Korn, E. L.; Wangsa, D.; Kruger, S.; Duchrow, M.; Bruch, H. P.; Auer, G.; Ried, T. Stage-specific alterations of the genome, transcriptome, and proteome during colorectal carcinogenesis. Genes, Chromosomes Cancer 2007, 46 (1), 10-26.
38. Lorenz, P.; Ruschpler, P.; Koczan, D.; Stiehl, P.; Thiesen, H. J. From transcriptome to proteome: differentially expressed proteins identified in synovial tissue of patients suffering from rheumatoid arthritis and osteoarthritis by an initial screen with a panel of 791 antibodies. Proteomics 2003, 3 (6), 991-1002.
39. Ruse, C. I.; Tan, F. L.; Kinter, M.; Bond, M. Intregrated analysis of the human cardiac transcriptome, proteome and phosphopro- teome. Proteomics 2004, 4 (5), 1505-1516.
40. Hojlund, K.; Yi, Z.; Hwang, H,; Bowen, B,; Lefort, N.; Flynn, C. R.; Langlais, P.; Weintraub, S. T.; Mandarino, L. J. Characterization of the human skeletal muscle proteome by one-dimensional Gel electrophoresis and HPLC-ESI-MS/MS. Mol. Cell. Proteomics 2008, 7 (2), 257-267.
41. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193 (1), 265-275.
42. Foster, L. J.; Rudich, A.; Talior, I.; Patel, N.; Huang, X.; Furtado, L. M.; Bilan, P. J.; Mann, M.; Klip, A. Insulin-dependent interactions of proteins with GLUT4 revealed through stable isotope labeling by amino acids in cell culture (SILAC). J. Proteome Res. 2006, 5 (1), 64-75.
43. Bolstad, B. M.; Irizarry, R. A.; Astrand, M.; Speed, T. P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19 (2), 185-193.
44. Irizarry, R. A.; Hobbs, B.; Collin, F.; Beazer-Barclay, Y. D.; Antonellis, K. J.; Scherf, U.; Speed, T. P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4 (2), 249-264.
45. Davison, A. C.; Hinkley, D. V.; Schechtman, E. Efficient Bootstrap Simulation. Biometrika 1986, 73 (3), 555-566.
46. Davison, A. C.; Hinkley, D. V.; Young, G. A. Recent developments in bootstrap methodology. Statist. Sci. 2003, 18 (2), 141-157.
47. Cavelier, C.; Lorenzi, I.; Rohrer, L.; von Eckardstein, A. Lipid efflux by the ATP-binding cassette transporters ABCA1 and ABCG1. Biochim. Biophys. Acta 2006, 1761 (7), 655-666.
48. Dullens, S. P.; Plat, J.; Mensink, R. P. Increasing apoA-I production as a target for CHD risk reduction. Nutr. Metab. Cardiovasc. Dis. 2007, 17 (8), 616-528.
49. Guda, C.; Fahy, E.; Subramaniam, S. MITOPRED: a genome-scale method for prediction of nucleus-encoded mitochondrial proteins. Bioinformatics 2004, 20 (11), 1785-1794.
50. Urso, M. L.; Scrimgeour, A. G.; Chen, Y. W.; Thompson, P. D.; Clarkson, P. M. Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J. Appl. Physiol. 2006, 101 (4), 1136-1148.