Proteome profile of functional mitochondria from human skeletal muscle using one-dimensional gel electrophoresis and HPLC-ESI-MS/MS

Journal of Proteomics

Volumn 72, Issue 6, 2009, Pages 1046-1060

  Lefort, Natalie ^a   Yi, Zhengping ^a,b   Bowen, Benjamin ^c   Glancy, Brian ^a   De Filippis, Eleanna A ^a   Mapes, Rebekka ^a   Hwang, Hyonson ^a   Flynn, Charles R ^a   Willis, Wayne T ^a   Civitarese, Anthony ^a   Højlund, Kurt ^d   Mandarino, Lawrence J ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c Arizona State University   (United States)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

HPLC ESI MS MS; Human skeletal muscle; Mitochondria; One dimensional gel electrophoresis; Proteome

Indexed keywords

MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; NUCLEOPROTEIN; RETINOL DEHYDROGENASE; SIRTUIN 5;

ADULT; ARTICLE; CATABOLISM; CELL DEATH; CITRIC ACID CYCLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ELECTROSPRAY MASS SPECTROMETRY; FATTY ACID OXIDATION; FUNCTIONAL PROTEOMICS; GEL ELECTROPHORESIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MASS SPECTROMETRY; MUSCLE BIOPSY; MUSCLE MITOCHONDRION; NORMAL HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; VASTUS LATERALIS MUSCLE;

AMINO ACIDS; ANIMALS; CELL NUCLEUS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTRON TRANSPORT; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FATTY ACIDS; HUMANS; MICE; MITOCHONDRIA; MUSCLE, SKELETAL; OXIDATIVE STRESS; PROTEINS; PROTEOMICS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 67651151024     PISSN: 18743919     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jprot.2009.06.011     Document Type: Article

References (79)

1. Hyun D.H., Hunt N.D., Emerson S.S., Hernandez J.O., Mattson M.P., and de Cabo R. Up-regulation of plasma membrane-associated redox activities in neuronal cells lacking functional mitochondria. J Neurochem 100 (2007) 1364-1374
2. Da Cruz S., Parone P.A., and Martinou J.C. Building the mitochondrial proteome. Expert Rev Proteomics 2 (2005) 541-551
3. Johnson D.T., Harris R.A., Blair P.V., and Balaban R.S. Functional consequences of mitochondrial proteome heterogeneity. Am J Physiol Cell Physiol 292 (2007) C698-707
4. Johnson D.T., Harris R.A., French S., Blair P.V., You J., Bemis K.G., et al. Tissue heterogeneity of the mammalian mitochondrial proteome. Am J Physiol Cell Physiol 292 (2007) C689-C697
5. Forner F., Foster L.J., Campanaro S., Valle G., and Mann M. Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver. Mol Cell Proteomics 5 (2006) 608-619
6. Huttemann M., Lee I., Samavati L., Yu H., and Doan J.W. Regulation of mitochondrial oxidative phosphorylation through cell signaling. Biochim Biophys Acta 1773 (2007) 1701-1720
7. Taylor S.W., Fahy E., Zhang B., Glenn G.M., Warnock D.E., Wiley S., et al. Characterization of the human heart mitochondrial proteome. Nat Biotechnol 21 (2003) 281-286
8. Richly E., Chinnery P.F., and Leister D. Evolutionary diversification of mitochondrial proteomes: implications for human disease. Trends Genet 19 (2003) 356-362
9. Taylor S.W., Fahy E., and Ghosh S.S. Global organellar proteomics. Trends Biotechnol 21 (2003) 82-88
10. Everberg H., Leiding T., Schioth A., Tjerneld F., and Gustavsson N. Efficient and non-denaturing membrane solubilization combined with enrichment of membrane protein complexes by detergent/polymer aqueous two-phase partitioning for proteome analysis. J Chromatogr A 1122 (2006) 35-46
11. Reichert A.S., and Neupert W. Mitochondriomics or what makes us breathe. Trends Genet 20 (2004) 555-562
12. Szendroedi J., Schmid A.I., Chmelik M., Toth C., Brehm A., Krssak M., et al. Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 4 (2007) e154
13. Mogensen M., Sahlin K., Fernstrom M., Glintborg D., Vind B.F., Beck-Nielsen H., et al. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56 (2007) 1592-1599
14. Boushel R., Gnaiger E., Schjerling P., Skovbro M., Kraunsoe R., and Dela F. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50 (2007) 790-796
15. Phielix E., Schrauwen-Hinderling V.B., Mensink M., Lenaers E., Meex R., Hoeks J., et al. Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57 (2008) 2943-2949
16. Lopez M.F., Kristal B.S., Chernokalskaya E., Lazarev A., Shestopalov A.I., Bogdanova A., et al. High-throughput profiling of the mitochondrial proteome using affinity fractionation and automation. Electrophoresis 21 (2000) 3427-3440
17. Hanson B.J., Schulenberg B., Patton W.F., and Capaldi R.A. A novel subfractionation approach for mitochondrial proteins: a three-dimensional mitochondrial proteome map. Electrophoresis 22 (2001) 950-959
18. Fountoulakis M., Berndt P., Langen H., and Suter L. The rat liver mitochondrial proteins. Electrophoresis 23 (2002) 311-328
19. Da Cruz S., Xenarios I., Langridge J., Vilbois F., Parone P.A., and Martinou J.C. Proteomic analysis of the mouse liver mitochondrial inner membrane. J Biol Chem 278 (2003) 41566-41571
20. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134 (2008) 112-123
21. Rabilloud T., Kieffer S., Procaccio V., Louwagie M., Courchesne P.L., Patterson S.D., et al. Two-dimensional electrophoresis of human placental mitochondria and protein identification by mass spectrometry: toward a human mitochondrial proteome. Electrophoresis 19 (1998) 1006-1014
22. Taylor S.W., Warnock D.E., Glenn G.M., Zhang B., Fahy E., Gaucher S.P., et al. An alternative strategy to determine the mitochondrial proteome using sucrose gradient fractionation and 1D PAGE on highly purified human heart mitochondria. J Proteome Res 1 (2002) 451-458
23. Gaucher S.P., Taylor S.W., Fahy E., Zhang B., Warnock D.E., Ghosh S.S., et al. Expanded coverage of the human heart mitochondrial proteome using multidimensional liquid chromatography coupled with tandem mass spectrometry. J Proteome Res 3 (2004) 495-505
24. Jackman M.R., and Willis W.T. Characteristics of mitochondria isolated from type I and type IIb skeletal muscle. Am J Physiol 270 (1996) C673-C678
25. Yajid F., Mercier J.G., Mercier B.M., Dubouchaud H., and Prefaut C. Effects of 4 wk of hindlimb suspension on skeletal muscle mitochondrial respiration in rats. J Appl Physiol 84 (1998) 479-485
26. Milner D.J., Mavroidis M., Weisleder N., and Capetanaki Y. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol 150 (2000) 1283-1298
27. Johnson G., Roussel D., Dumas J.F., Douay O., Malthiery Y., Simard G., et al. Influence of intensity of food restriction on skeletal muscle mitochondrial energy metabolism in rats. Am J Physiol Endocrinol Metab 291 (2006) E460-E467
28. Kerner J., Turkaly P.J., Minkler P.E., and Hoppel C.L. Aging skeletal muscle mitochondria in the rat: decreased uncoupling protein-3 content. Am J Physiol Endocrinol Metab 281 (2001) E1054-E1062
29. Jackman M.R., Ravussin E., Rowe M.J., Pratley R., Milner M.R., and Willis W.T. Effect of a polymorphism in the ND1 mitochondrial gene on human skeletal muscle mitochondrial function. Obesity 16 (2008) 363-368 (Silver Spring)
30. Makinen M.W., and Lee C.P. Biochemical studies of skeletal muscle mitochondria. I. Microanalysis of cytochrome content, oxidative and phosphorylative activities of mammalian skeletal muscle mitochondria. Arch Biochem Biophys 126 (1968) 75-82
31. Nicholls DGaF S.J. Bioenergetics 3. 3rd ed. (2002), Academic Press
32. Hojlund K., Yi Z., Hwang H., Bowen B., Lefort N., Flynn C.R., et al. Characterization of the human skeletal muscle proteome by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. Mol Cell Proteomics 7 (2008) 257-267
33. Yi Z., Bowen B.P., Hwang H., Jenkinson C.P., Coletta D.K., Lefort N., et al. Global relationship between the proteome and transcriptome of human skeletal muscle. J Proteome Res 7 (2008) 3230-3241
34. Bizeau M.E., Willis W.T., and Hazel J.R. Differential responses to endurance training in subsarcolemmal and intermyofibrillar mitochondria. J Appl Physiol 85 (1998) 1279-1284
35. Krieger D.A., Tate C.A., McMillin-Wood J., and Booth F.W. Populations of rat skeletal muscle mitochondria after exercise and immobilization. J Appl Physiol 48 (1980) 23-28
36. Cogswell A.M., Stevens R.J., and Hood D.A. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol 264 (1993) C383-C389
37. Fernstrom M., Bakkman L., Tonkonogi M., Shabalina I.G., Rozhdestvenskaya Z., Mattsson C.M., et al. Reduced efficiency, but increased fat oxidation, in mitochondria from human skeletal muscle after 24-h ultraendurance exercise. J Appl Physiol 102 (2007) 1844-1849
38. Bakkman L., Sahlin K., Holmberg H.C., and Tonkonogi M. Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate. Acta Physiol (Oxf) 190 (2007) 243-251
39. Rasmussen U.F., and Rasmussen H.N. Human quadriceps muscle mitochondria: a functional characterization. Mol Cell Biochem 208 (2000) 37-44
40. Winkler-Stuck K., Kirches E., Mawrin C., Dietzmann K., Lins H., Wallesch C.W., et al. Re-evaluation of the dysfunction of mitochondrial respiratory chain in skeletal muscle of patients with Parkinson's disease. J Neural Transm 112 (2005) 499-518
41. Leek B.T., Mudaliar S.R., Henry R., Mathieu-Costello O., and Richardson R.S. Effect of acute exercise on citrate synthase activity in untrained and trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 280 (2001) R441-R447
42. Rasmussen U.F., and Rasmussen H.N. Human skeletal muscle mitochondrial capacity. Acta Physiol Scand 168 (2000) 473-480
43. Hojlund K., Yi Z., Hwang H., Bowen B., Lefort N., Flynn C.R., Langlais P., Weintraub S.T., and Mandarino L.J. Characterization of the human skeletal muscle proteome by one-dimensional Gel electrophoresis and HPLC-ESI-MS/MS. Mol Cell Proteomics 7 (2008) 257-267
44. Schwartz R., Ting C.S., and King J. Whole proteome pI values correlate with subcellular localizations of proteins for organisms within the three domains of life. Genome Res 11 (2001) 703-709
45. Paoletti A.C., Parmely T.J., Tomomori-Sato C., Sato S., Zhu D., Conaway R.C., et al. Quantitative proteomic analysis of distinct mammalian mediator complexes using normalized spectral abundance factors. Proc Natl Acad Sci USA 103 (2006) 18928-18933
46. Liu H., Sadygov R.G., and Yates III J.R. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76 (2004) 4193-4201
47. Wang Y., and Bogenhagen D.F. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J Biol Chem 281 (2006) 25791-25802
48. Zybailov B., Mosley A.L., Sardiu M.E., Coleman M.K., Florens L., and Washburn M.P. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res 5 (2006) 2339-2347
49. Guda C., Fahy E., and Subramaniam S. MITOPRED: a genome-scale method for prediction of nucleus-encoded mitochondrial proteins. Bioinformatics 20 (2004) 1785-1794
50. Guda C., Guda P., Fahy E., and Subramaniam S. MITOPRED: a web server for the prediction of mitochondrial proteins. Nucleic Acids Res 32 (2004) W372-W374
51. Carroll J., Altman M.C., Fearnley I.M., and Walker J.E. Identification of membrane proteins by tandem mass spectrometry of protein ions. Proc Natl Acad Sci USA 104 (2007) 14330-14335
52. Sharer J.D., Shern J.F., Van Valkenburgh H., Wallace D.C., and Kahn R.A. ARL2 and BART enter mitochondria and bind the adenine nucleotide transporter. Mol Biol Cell 13 (2002) 71-83
53. Pfanner N., Wiedemann N., Meisinger C., and Lithgow T. Assembling the mitochondrial outer membrane. Nat Struct Mol Biol 11 (2004) 1044-1048
54. Alam T.I., Kanki T., Muta T., Ukaji K., Abe Y., Nakayama H., et al. Human mitochondrial DNA is packaged with TFAM. Nucleic Acids Res 31 (2003) 1640-1645
55. Holt I.J., He J., Mao C.C., Boyd-Kirkup J.D., Martinsson P., Sembongi H., et al. Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 7 (2007) 311-321
56. Bogenhagen D.F., Wang Y., Shen E.L., and Kobayashi R. Protein components of mitochondrial DNA nucleoids in higher eukaryotes. Mol Cell Proteomics 2 (2003) 1205-1216
57. Sharma M.R., Koc E.C., Datta P.P., Booth T.M., Spremulli L.L., and Agrawal R.K. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115 (2003) 97-108
58. Zhang Z., and Gerstein M. Identification and characterization of over 100 mitochondrial ribosomal protein pseudogenes in the human genome. Genomics 81 (2003) 468-480
59. O'Brien T.W., O'Brien B.J., and Norman R.A. Nuclear MRP genes and mitochondrial disease. Gene 354 (2005) 147-151
60. Beugnet A., Tee A.R., Taylor P.M., and Proud C.G. Regulation of targets of mTOR (mammalian target of rapamycin) signalling by intracellular amino acid availability. Biochem J 372 (2003) 555-566
61. Tremblay F., and Marette A. Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J Biol Chem 276 (2001) 38052-38060
62. Khamzina L., Veilleux A., Bergeron S., and Marette A. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 146 (2005) 1473-1481
63. Cunningham J.T., Rodgers J.T., Arlow D.H., Vazquez F., Mootha V.K., and Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450 (2007) 736-740
64. Katz A. Modulation of glucose transport in skeletal muscle by reactive oxygen species. J Appl Physiol 102 (2007) 1671-1676
65. Yakes F.M., and Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 94 (1997) 514-519
66. Dawson T.L., Gores G.J., Nieminen A.L., Herman B., and Lemasters J.J. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am J Physiol 264 (1993) C961-C967
67. Chabi B., Ljubicic V., Menzies K.J., Huang J.H., Saleem A., and Hood D.A. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell (2007)
68. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341 Pt 2 (1999) 233-249
69. Tonkonogi M., Walsh B., Svensson M., and Sahlin K. Mitochondrial function and antioxidative defence in human muscle: effects of endurance training and oxidative stress. J Physiol 528 Pt 2 (2000) 379-388
70. Wiley S.E., Murphy A.N., Ross S.A., van der Geer P., and Dixon J.E. MitoNEET is an iron-containing outer mitochondrial membrane protein that regulates oxidative capacity. Proc Natl Acad Sci USA 104 (2007) 5318-5323
71. Paddock M.L., Wiley S.E., Axelrod H.L., Cohen A.E., Roy M., Abresch E.C., et al. MitoNEET is a uniquely folded 2Fe 2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc Natl Acad Sci USA 104 (2007) 14342-14347
72. Michishita E., Park J.Y., Burneskis J.M., Barrett J.C., and Horikawa I. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 16 (2005) 4623-4635
73. Xie J., Marusich M.F., Souda P., Whitelegge J., and Capaldi R.A. The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11. FEBS Lett 581 (2007) 3545-3549
74. Kim J.Y., Tillison K.S., Zhou S., Lee J.H., and Smas C.M. Differentiation-dependent expression of Adhfe1 in adipogenesis. Arch Biochem Biophys 464 (2007) 100-111
75. Belyaeva O.V., Korkina O.V., Stetsenko A.V., and Kedishvili N.Y. Human retinol dehydrogenase 13 (RDH13) is a mitochondrial short-chain dehydrogenase/reductase with a retinaldehyde reductase activity. FEBS J 275 (2007) 138-147
76. Fukada K., Zhang F., Vien A., Cashman N.R., and Zhu H. Mitochondrial proteomic analysis of a cell line model of familial amyotrophic lateral sclerosis. Mol Cell Proteomics 3 (2004) 1211-1223
77. Calvo S., Jain M., Xie X., Sheth S.A., Chang B., Goldberger O.A., et al. Systematic identification of human mitochondrial disease genes through integrative genomics. Nat Genet 38 (2006) 576-582
78. Hajek P., Chomyn A., and Attardi G. Identification of a novel mitochondrial complex containing mitofusin 2 and stomatin-like protein 2. J Biol Chem 282 (2007) 5670-5681
79. Mootha V.K., Bunkenborg J., Olsen J.V., Hjerrild M., Wisniewski J.R., Stahl E., et al. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115 (2003) 629-640