Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle

Proteomics

Volumn 9, Issue 24, 2009, Pages 5509-5524

  O'Connell, Kathleen ^a   Ohlendieck, Kay ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Aging; Animal proteomics; DIGE; Mitochondria; Sarcopenia; Skeletal muscle proteomics

Indexed keywords

ACYL COENZYME A DEHYDROGENASE; MITOCHONDRIAL FISSION PROTEIN FIS1; MITOCHONDRIAL PROTEIN; MITOFILIN; MUSCLE PROTEIN; PEROXIREDOXIN; PORIN; PROHIBITIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SUCCINATE DEHYDROGENASE; SUCCINYL COENZYME A SYNTHETASE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ADOLESCENT; AEROBIC METABOLISM; AGED; ANIMAL TISSUE; ARTICLE; CELL AGING; COMPARATIVE ANATOMY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; IMMUNOBLOTTING; MUSCLE ATROPHY; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RAT; SKELETAL MUSCLE;

AGING; ANIMALS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PROTEOME; PROTEOMICS; RATS; RATS, WISTAR;

ANIMALIA; RATTUS;

EID: 73149108205     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200900472     Document Type: Article

References (78)

1. McBride, H. M., Neuspiel, M., Wasiak, S., Mitochondria: more than just a powerhouse. Curr. Biol. 2006, 16, R551-R560.
2. Distler, A. M., Kerner, J., Hoppel, C. L., Proteomics of mitochondrial inner and outer membranes. Proteomics 2008, 8, 4066-4082.
3. Brdiczka, D. G., Zorov, D. B., Sheu, S. S., Mitochondrial contact sites: their role in energy metabolism and apoptosis. Biochim. Biophys. Acta 2006, 1762, 148-163.
4. Dolder, M., Wendt, S., Wallimann, T., Mitochondrial creatine kinase in contact sites: interaction with porin and adenine nucleotide translocase, role in permeability transition and sensitivity to oxidative damage. Biol. Signals Recept. 2001, 10, 93-111.
5. Reichert, A. S., Neupert, W., Contact sites between the outer and inner membrane of mitochondria-role in protein transport. Biochim. Biophys. Acta 2002, 1592, 41-49.
6. Scheffler, I. E., A century of mitochondrial research: achievements and perspectives. Mitochondrion 2001, 1, 3-31.
7. Lee, C. P., Martens, M. E., in: Engel, A. G., Franzini-Armstrong, C. (Eds.), Myology, McGraw-Hill Inc., New York 1994, pp. 624-647.
8. Reifschneider, N. H., Goto, S., Nakamoto, H., Takahashi, R. et al., Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J. Proteome Res. 2006, 5, 1117-1132.
9. Johnson, D. T., Harris, R. A., French, S., Blair, P. V. et al., Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell Physiol. 2007, 292, C689-C697.
10. Johnson, D. T., Harris, R. A., Blair, P. V., Balaban, R. S., Functional consequences of mitochondrial proteome heterogeneity. Am. J. Physiol. Cell Physiol. 2007, 292, C698-C707
11. Forner, F., Foster, L. J., Campanaro, S., Valle, G., Mann, M., Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver. Mol. Cell Proteomics 2006, 5, 608-619.
12. Chan, D. C., Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006, 125, 1241-1252.
13. Gustafsson, A. B., Gottlieb, R. A., Heart mitochondria: gates of life and death. Cardiovasc. Res. 2008, 77, 334-343.
14. Siciliano, G., Volpi, L., Piazza, S., Ricci, G. et al., Functional diagnostics in mitochondrial diseases. Biosci. Rep. 2007, 27, 53-67.
15. Lin, M. T., Beal, M. F., Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443, 787-795.
16. Trifunovic, A., Larsson, N. G., Mitochondrial dysfunction as a cause of ageing. J. Intern. Med. 2008, 263, 167-178.
17. Lenaz, G., Bovina, C., D'Aurelio, M., Fato, R. et al., Role of mitochondria in oxidative stress and aging. Ann. NY Acad. Sci. 2002, 959, 199-213.
18. Chakravarti, B., Chakravarti, D. N., Oxidative modification of proteins: age-related changes. Gerontology 2007, 53, 128-139.
19. Friguet, B., Bulteau, A. L., Petropoulos, I., Mitochondrial protein quality control: implications in ageing. Biotechnol. J. 2008, 3, 757-764.
20. Figueiredo, P. A., Mota, M. P., Appell, H. J., Duarte, J. A., The role of mitochondria in aging of skeletal muscle. Biogerontology 2008, 9, 67-84.
21. Chabi, B., Ljubicic, V., Menzies, K. J., Huang, J. H. et al., Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 2008, 7, 2-12.
22. Figueiredo, P. A., Powers, S. K., Ferreira, R. M., Appell, H. J., Duarte, J. A., Aging impairs skeletal muscle mitochondrial bioenergetic function. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64, 21-33.
23. Janssen, I., Heymsfield, S. B., Ross, R., Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J. Am. Geriatr. Soc. 2002, 50, 889-896.
24. Hargreaves, M., Cameron-Smith, D., Exercise, diet, and skeletal muscle gene expression. Med. Sci. Sports Exerc. 2002, 34, 1505-1508.
25. Hood, D. A., Irrcher, I., Ljubicic, V., Joseph, A. M., Coordination of metabolic plasticity in skeletal muscle. J. Exp. Biol. 2006, 209, 2265-2275.
26. Doherty, T. J., Aging and sarcopenia. J. Appl. Physiol. 2003, 95, 1717-1727.
27. Thompson, L. V., Age-related muscle dysfunction. Exp. Gerontol. 2009, 44, 106-111.
28. Edstrom, E., Altun, M., Bergman, E., Johnson, H. et al., Factors contributing to neuromuscular impairment and sarcopenia during aging. Physiol. Behav. 2007, 92, 129-135.
29. Faulkner, J. A., Larkin, L. M., Claflin, D. R., Brooks, S. V., Age-related changes in the structure and function of skeletal muscles. Clin. Exp. Pharmacol. Physiol. 2007, 34, 1091-1096.
30. Campbell, W. W., Leidy, H. J., Dietary protein and resistance training effects on muscle and body composition in older persons. J. Am. Coll. Nutr. 2007, 26, 696S-703S.
31. Piec, I., Listrat, A., Alliot, J., Chambon, C. et al., Differential proteome analysis of aging in rat skeletal muscle. FASEB J. 2005, 19, 1143-1145.
32. Gelfi, C., Vigano, A., Ripamonti, M., Pontoglio, A. et al., The human muscle proteome in aging. J. Proteome Res. 2006, 5, 1344-1353.
33. O'Connell, K., Gannon, J., Doran, P., Ohlendieck, K., Proteomic profiling reveals a severely perturbed protein expression pattern in aged skeletal muscle. Int. J. Mol. Med. 2007, 20, 145-153.
34. Doran, P., O'Connell, K., Gannon, J., Kavanagh, M., Ohlendieck, K., Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis. Proteomics 2008, 8, 364-377.
35. Capitanio, D., Vasso, M., Fania, C., Moriggi, M. et al., Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE, Proteomics 2009, 9, 2004-2020.
36. Lombardi, A., Silvestri, E., Cioffi, F., Senese, R. et al., Defining the transcriptomic and proteomic profiles of rat ageing skeletal muscle by the use of a cDNA array, 2D- and Blue native-PAGE approach. J. Proteomics 2009, 72, 708-721.
37. Doran, P., Gannon, J., O'Connell, K., Ohlendieck, K., Aging skeletal muscle shows a drastic increase in the small heat shock proteins B-crystallin/HspB5 and cvHsp/HspB7. Eur. J. Cell Biol. 2007, 86, 629-640.
38. Doran, P., Donoghue, P., O'Connell, K., Gannon, J., Ohlendieck, K., Proteomics of skeletal muscle aging. Proteomics 2009, 9, 989-1003.
39. Gibson, B. W., The human mitochondrial proteome: oxidative stress, protein modifications and oxidative phosphorylation. Int. J. Biochem. Cell Biol. 2005, 37, 927-934.
40. Da Cruz, S., Parone, P.A., Martinou, J. C., Building the mitochondrial proteome. Expert Rev. Proteomics 2005, 2, 541-551.
41. Dimmer, K. S., Rapaport, D., Proteomic view of mitochondrial function. Genome Biol. 2008, 9, 209.
42. Taylor, S. W., Fahy, E., Zhang, B., Glenn, G. M. et al., Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 2003, 21, 281-286.
43. Gaucher, S. P., Taylor, S. W., Fahy, E., Zhang, B. et al., Expanded coverage of the human heart mitochondrial proteome using multidimensional liquid chromatography coupled with tandem mass spectrometry. J. Proteome Res. 2004, 3, 495-505.
44. White, M. Y., Edwards, A. V. G., Cordwell, S. J., Van Eyk, J. E., Mitochondria: a mirror into cellular dysfunction in heart disease. Proteomics Clin. Appl. 2008, 2, 845-861.
45. McDonald, T., Sheng, S., Stanley, B., Chen, D. et al., Expanding the subproteome of the inner mitochondria using protein separation technologies: one- and two-dimensional liquid chromatography and two-dimensional gel electrophoresis. Mol. Cell Proteomics 2006, 5, 2392-2411.
46. Da Cruz, S., Martinou, J. C., Purification and proteomic analysis of the mouse liver mitochondrial inner membrane. Methods Mol. Biol. 2008, 432, 101-116.
47. Pesce, V., Cormio, A., Fracasso, F., Vecchiet, J. et al., Age-related mitochondrial genotypic and phenotypic alterations in human skeletal muscle. Free Radic. Biol. Med. 2001, 30, 1223-1233.
48. Chang, J., Van Remmen, H., Cornell, J., Richardson, A., Ward, W. F., Comparative proteomics: characterization of a two-dimensional gel electrophoresis system to study the effect of aging on mitochondrial proteins. Mech. Ageing Dev. 2003, 124, 33-41.
49. Dencher, N. A., Goto, S., Reifschneider, N. H., Sugawa, M., Krause, F., Unraveling age-dependent variation of the mitochondrial proteome. Ann. NY Acad. Sci. 2006, 1067, 116-119.
50. Dencher, N. A., Frenzel, M., Reifschneider, N. H., Sugawa, M., Krause, F., Proteome alterations in rat mitochondria caused by aging. Ann. NY Acad. Sci. 2007, 1100, 291-298.
51. Chang, J., Cornell, J. E., Van Remmen, H., Hakala, K. et al., Effect of aging and caloric restriction on the mitochondrial proteome. J. Gerontol. A Biol. Sci. Med. Sci. 2007, 62, 223-234.
52. Viswanathan, S., Unlu, M., Minden, J. S., Two-dimensional difference gel electrophoresis. Nat. Protoc. 2006, 1, 1351-1358.
53. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S. et al., Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 2001, 1, 377-396.
54. Marouga, R., David, S., Hawkins, E., The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382, 669-678.
55. Doran, P., Gannon, J., O'Connell, K., Ohlendieck, K., Proteomic profiling of animal models mimicking skeletal muscle disorders. Proteomics Clin. Appl. 2007, 1, 1169-1184.
56. O'Connell, K., Doran, P., Gannon, J., Ohlendieck, K., Lectin-based proteomic profiling of aged skeletal muscle: decreased pyruvate kinase isozyme M1 exhibits drastically increased levels of N-glycosylation. Eur. J. Cell Biol. 2008, 87, 793-805.
57. Bradford, M. M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
58. Kane, L. A., Yung, C. K., Agnetti, G., Neverova, I., Van Eyk, J. E., Optimization of paper bridge loading for 2-DE analysis in the basic pH region: application to the mitochondrial subproteome. Proteomics. 2006, 6, 5683-5687.
59. Srere, P. A., Citrate synthase.Methods Enzymol. 1969, 13, 3-11.
60. Heukeshoven, J., Dernick, R., Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis, 1985, 6, 103-112.
61. Bradd, S. J., Dunn, M. J., Analysis of membrane proteins by western blotting and enhanced chemiluminescence. Methods Mol. Biol. 1993, 19, 211-218.
62. Doran, P., Martin, G., Dowling, P., Jockusch, H., Ohlendieck, K., Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 2006, 6, 4610-4621.
63. Donoghue, P., Doran, P., Wynne, K., Pedersen, K. et al., Proteomic profiling of chronic low-frequency stimulated fast muscle. Proteomics 2007, 7, 3417-3430.
64. Doran, P., Wilton, S. D., Fletcher, S., Ohlendieck, K., Proteomic profiling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 2009, 9, 671-685.
65. Karp, N. A., Lilley, K. S., Maximising sensitivity for detecting changes in protein expression: experimental design using minimal CyDyes. Proteomics 2005, 5, 3105-3115.
66. Karp, N. A., Feret, R., Rubtsov, D. V., Lilley, K. S., Comparison of DIGE and post-stained gel electrophoresis with both traditional and SameSpots analysis for quantitative proteomics. Proteomics 2008, 8, 946-948.
67. Karp, N. A., Lilley, K. S., Investigating sample pooling strategies for DIGE experiments to address biological variability. Proteomics 2009, 9, 388-397.
68. Fang, J., Beattie, D. S., Novel FMN-containing rotenone-insensitive NADH dehydrogenase from Trypanosoma brucei mitochondria: isolation and characterization. Biochemistry 2002, 41, 3065-3072.
69. Drechsler, E. R., Boyer, P. D., Kowalsky, A. G., The catalytic activity of carboxypeptidase-degraded aldolase. J. Biol. Chem. 1959, 234, 2627-2634.
70. Krahenbuhl, S., Chang, M., Brass, E. P., Hoppel, C. L., Decreased activities of ubiquinol:ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin[c-lactam]-induced methylmalonic aciduria. J. Biol. Chem. 1991, 266, 20998-21003.
71. Dudkina, N. V., Sunderhaus, S., Boekema, E. J., Braun, H. P., The higher level of organization of the oxidative phosphorylation system: mitochondrial supercomplexes. J. Bioenerg. Biomembr. 2008, 40, 419-424.
72. John, G. B., Shang, Y., Li, L., Renken, C. et al., The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell. 2005, 16, 1543-1554.
73. Serasinghe, M. N., Yoon, Y., The mitochondrial outer membrane protein hFis1 regulates mitochondrial morphology and fission through self-interaction. Exp. Cell Res. 2008, 314, 3494-3507.
74. Liu, X. H., Qian, L. J., Gong, J. B., Shen, J. et al., Proteomic analysis of mitochondrial proteins in cardiomyocytes from chronic stressed rat. Proteomics 2004, 4, 3167-3176.
75. Cao, Z., Bhella, D., Lindsay, J. G., Reconstitution of the mitochondrial PrxIII antioxidant defence pathway: general properties and factors affecting PrxIII activity and oligomeric state. J. Mol. Biol. 2007, 372, 1022-1033.
76. Bonifati, V., Oostra, B. A., Heutink, P., Linking DJ-1 to neurodegeneration offers novel insights for understanding the pathogenesis of Parkinson's disease. J. Mol. Med. 2004, 82, 163-174.
77. De Pinto, V., Reina, S., Guarino, F., Messina, A., Structure of the voltage dependent anion channel: state of the art. J. Bioenerg. Biomembr. 2008, 40, 139-147.
78. Marziliano, N., Mannarino, S., Nespoli, L., Diegoli, M. et al., Barth syndrome associated with compound hemizygosity and heterozygosity of the TAZ and LDB3 genes. Am. J. Med. Genet. 2007, 143A, 907-915.