Mitochondrial proteome design: From molecular identity to pathophysiological regulation

Journal of General Physiology

Volumn 139, Issue 6, 2012, Pages 395-406

  Zhang, Jun ^a,b   Lin, Amanda ^a,b   Powers, Jared ^a,b   Lam, Maggie P ^a,b   Lotz, Christopher ^a,b   Liem, David ^a,b   Lau, Edward ^a,b   Wang, Ding ^a,b   Deng, Ning ^c   Korge, Paavo ^a,b   Zong, Nobel C ^a,b   Cai, Hua ^a,b   Weiss, James ^a,b   Ping, Peipei ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME;

ANIMAL; ARTICLE; GENETICS; HOMEOSTASIS; HUMAN; METABOLISM; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY;

ANIMALS; HOMEOSTASIS; HUMANS; MITOCHONDRIA; PROTEOME;

EID: 84864011366     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210797     Document Type: Article

References (63)

1. Alonso, J., J.M. Rodriguez, L.A. Baena-López, and J.F. Santarén. 2005. Characterization of the Drosophila melanogaster mitochondrial proteome. J. Proteome Res. 4:1636-1645. http://dx.doi.org/10.1021/pr050130c
2. Balaban, R.S. 2010. The mitochondrial proteome: a dynamic functional program in tissues and disease states. Environ. Mol. Mutagen. 51:352-359.
3. Baseler, W.A., E.R. Dabkowski, C.L. Williamson, T.L. Croston, D. Thapa, M.J. Powell, T.T. Razunguzwa, and J.M. Hollander. 2011. Proteomic alterations of distinct mitochondrial subpopulations in the type 1 diabetic heart: contribution of protein import dysfunction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300:R186-R200. http://dx.doi.org/10.1152/ajpregu.00423.2010
4. Boja, E.S., D. Phillips, S.A. French, R.A. Harris, and R.S. Balaban. 2009. Quantitative mitochondrial phosphoproteomics using iTRAQ on an LTQ-Orbitrap with high energy collision dissociation. J. Proteome Res. 8:4665-4675. http://dx.doi.org/10.1021/pr900387b
5. Bulteau, A.L., and A. Bayot. 2011. Mitochondrial proteases and cancer. Biochim. Biophys. Acta. 1807:595-601. http://dx.doi.org/10.1016/j.bbabio.2010.12.011
6. Calvo, S.E., and V.K. Mootha. 2010. The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 11:25-44. http://dx.doi.org/10.1146/annurev-genom-082509-141720
7. Chen, C.H., G.R. Budas, E.N. Churchill, M.H. Disatnik, T.D. Hurley, and D. Mochly-Rosen. 2008. Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science. 321:1493-1495. http://dx.doi.org/10.1126/science.1158554
8. Choudhary, C., C. Kumar, F. Gnad, M.L. Nielsen, M. Rehman, T.C. Walther, J.V. Olsen, and M. Mann. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 325:834-840. http://dx.doi.org/10.1126/science.1175371
9. Cotter, D., P. Guda, E. Fahy, and S. Subramaniam. 2004. MitoProteome: mitochondrial protein sequence database and annotation system. Nucleic Acids Res. 32(Database issue):D463-D467. http://dx.doi.org/10.1093/nar/gkh048
10. Da Cruz, S., and J.C. Martinou. 2008. Purification and proteomic analysis of the mouse liver mitochondrial inner membrane. Methods Mol. Biol. 432:101-116. http://dx.doi.org/10.1007/978-1-59745-028-7_7
11. Das, S., R. Wong, N. Rajapakse, E. Murphy, and C. Steenbergen. 2008. Glycogen synthase kinase 3 inhibition slows mitochondrial adenine nucleotide transport and regulates voltage-dependent anion channel phosphorylation. Circ. Res. 103:983-991. http://dx.doi.org/10.1161/CIRCRESAHA.108.178970
12. Davidson, S.M. 2011. A needle in a haystack: focus on " Proteomic alterations of distinct mitochondrial subpopulations in the type 1 diabetic heart" Am. J. Physiol. Regul. Integr. Comp. Physiol. 300:R183-R185. http://dx.doi.org/10.1152/ajpregu.00751.2010
13. Deng, N., J. Zhang, C. Zong, Y. Wang, H. Lu, P. Yang, W. Wang, G.W. Young, Y. Wang, P. Korge, et al. 2011. Phosphoproteome analysis reveals regulatory sites in major pathways of cardiac mitochondria. Mol. Cell. Proteomics. 10:M110.000117.
14. DiMauro, S., and E.A. Schon. 2003. Mitochondrial respiratorychain diseases. N. Engl. J. Med. 348:2656-2668. http://dx.doi.org/10.1056/NEJMra022567
15. Distler, A.M., J. Kerner, and C.L. Hoppel. 2008. Proteomics of mitochondrial inner and outer membranes. Proteomics. 8:4066-4082. http://dx.doi.org/10.1002/pmic.200800102
16. Elstner, M., C. Andreoli, U. Ahting, I. Tetko, T. Klopstock, T. Meitinger, and H. Prokisch. 2008. MitoP2: an integrative tool for the analysis of the mitochondrial proteome. Mol. Biotechnol. 40:306-315. http://dx.doi.org/10.1007/s12033-008-9100-5
17. Ernster, L., and G. Schatz. 1981. Mitochondria: a historical review. J. Cell Biol. 91:227s-255s. http://dx.doi.org/10.1083/jcb.91.3.227s
18. Forner, F., L.J. Foster, S. Campanaro, G. Valle, and M. Mann. 2006. Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver. Mol. Cell. Proteomics. 5:608-619.
19. Gaucher, S.P., S.W. Taylor, E. Fahy, B. Zhang, D.E. Warnock, S.S. Ghosh, and B.W. Gibson. 2004. Expanded coverage of the human heart mitochondrial proteome using multidimensional liquid chromatography coupled with tandem mass spectrometry. J. Proteome Res. 3:495-505. http://dx.doi.org/10.1021/pr034102a
20. Glancy, B., and R.S. Balaban. 2012. Role of mitochondrial ca(2+) in the regulation of cellular energetics. Biochemistry. 51:2959-2973. http://dx.doi.org/10.1021/bi2018909
21. Gucek, M., and E. Murphy. 2010. What can we learn about cardioprotection from the cardiac mitochondrial proteome? Cardiovasc. Res. 88:211-218. http://dx.doi.org/10.1093/cvr/cvq277
22. Hart, G.W., C. Slawson, G. Ramirez-Correa, and O. Lagerlof. 2011. Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80:825-858. http://dx.doi.org/10.1146/annurev-biochem-060608-102511
23. Hogeboom, G.H., W.C. Schneider, and G.E. Pallade. 1948. Cytochemical studies of mammalian tissues; isolation of intact mitochondria from rat liver; some biochemical properties of mitochondria and submicroscopic particulate material. J. Biol. Chem. 172:619-635.
24. Hollander, J.M., W.A. Baseler, and E.R. Dabkowski. 2011. Proteomic remodeling of mitochondria in heart failure. Congest. Heart Fail. 17:262-268. http://dx.doi.org/10.1111/j.1751-7133.2011.00254.x
25. Hopper, R.K., S. Carroll, A.M. Aponte, D.T. Johnson, S. French, R.F. Shen, F.A. Witzmann, R.A. Harris, and R.S. Balaban. 2006. Mitochondrial matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry. 45:2524-2536. http://dx.doiorg/10.1021/bi052475e
26. Johnson, D.T., R.A. Harris, P.V. Blair, and R.S. Balaban. 2007a. Functional consequences of mitochondrial proteome heterogeneity. Am. J. Physiol. Cell Physiol. 292:C698-C707. http://dx.doi.org/10.1152/ajpcell.00109.2006
27. Johnson, D.T., R.A. Harris, S. French, P.V. Blair, J. You, K.G. Bemis, M. Wang, and R.S. Balaban. 2007b. Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell Physiol. 292:C689-C697. http://dx.doi.org/10.1152/ajpcell.00108.2006
28. Kane, L.A., M.J. Youngman, R.E. Jensen, and J.E. Van Eyk. 2010. Phosphorylation of the F(1)F(o) ATP synthase beta subunit: functional and structural consequences assessed in a model system. Circ. Res. 106:504-513. http://dx.doi.org/10.1161/CIRCRESAHA.109.214155
29. Kim, S.C., R. Sprung, Y. Chen, Y. Xu, H. Ball, J. Pei, T. Cheng, Y. Kho, H. Xiao, L. Xiao, et al. 2006. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell. 23:607-618. http://dx.doi.org/10.1016/j.molcel.2006.06.026
30. Kislinger, T., B. Cox, A. Kannan, C. Chung, P. Hu, A. Ignatchenko, M.S. Scott, A.O. Gramolini, Q. Morris, M.T. Hallett, et al. 2006. Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling. Cell. 125:173-186. http://dx.doi.org/10.1016/j.cell.2006.01.044
31. Lagranha, C.J., A. Deschamps, A. Aponte, C. Steenbergen, and E. Murphy. 2010. Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ. Res. 106:1681-1691. http://dx.doi.org/10.1161/CIRCRESAHA.109.213645
32. Lam, M.P., S.B. Scruggs, T.Y. Kim, C. Zong, E. Lau, D. Wang, C.M. Ryan, K.F. Faull, and P. Ping. 2012. An MRM-based workflow for quantifying cardiac mitochondrial protein phosphorylation in murine and human tissue. J. Proteomics. In press.
33. Lau, E., D. Wang, J. Zhang, H. Yu, M.P. Lam, X. Liang, N. Zong, T.Y. Kim, and P. Ping. 2012. Substrate- and isoform-specific proteome stability in normal and stressed cardiac mitochondria. Circ. Res. 110:1174-1178. http://dx.doi.org/10.1161/CIRCRESAHA.112.268359
34. Lee, J., Y. Xu, Y. Chen, R. Sprung, S.C. Kim, S. Xie, and Y. Zhao. 2007. Mitochondrial phosphoproteome revealed by an improved IMAC method and MS/MS/MS. Mol. Cell. Proteomics. 6:669-676. http://dx.doi.org/10.1074/mcp.M600218-MCP200
35. Lesnefsky, E.J., and C.L. Hoppel. 2006. Oxidative phosphorylation and aging. Ageing Res. Rev. 5:402-433. http://dx.doi.org/10.1016/j.arr.2006.04.001
36. Lesnefsky, E.J., S. Moghaddas, B. Tandler, J. Kerner, and C.L. Hoppel. 2001. Mitochondrial dysfunction in cardiac disease: ischemia- reperfusion, aging, and heart failure. J. Mol. Cell. Cardiol. 33:1065-1089. http://dx.doi.org/10.1006/jmcc.2001.1378
37. Lin, J.S., Y.S. Chen, H.S. Chiang, and M.C. Ma. 2008. Hypoxic preconditioning protects rat hearts against ischaemia-reperfusion injury: role of erythropoietin on progenitor cell mobilization. J. Physiol. 586:5757-5769. http://dx.doi.org/10.1113/jphysiol.2008.160887
38. Lin, J., C. Steenbergen, E. Murphy, and J. Sun. 2009. Estrogen receptor-beta activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation. 120:245-254. http://dx.doi.org/10.1161/CIRCULATIONAHA.109.868729
39. McDonald, T., S. Sheng, B. Stanley, D. Chen, Y. Ko, R.N. Cole, P. Pedersen, and J.E. Van Eyk. 2006. Expanding the subproteome of the inner mitochondria using protein separation technologies: one- and two-dimensional liquid chromatography and twodimensional gel electrophoresis. Mol. Cell. Proteomics. 5:2392- 2411. http://dx.doi.org/10.1074/mcp.T500036-MCP200
40. Milano, G., P. Bianciardi, V. Rochemont, G. Vassalli, L.K. Segesser, A.F. Corno, M. Guazzi, and M. Samaja. 2011. Phosphodiesterase-5 inhibition mimics intermittent reoxygenation and improves cardioprotection in the hypoxic myocardium. PLoS ONE. 6:e27910. http://dx.doi.org/10.1371/journal.pone.0027910
41. Mootha, V.K., J. Bunkenborg, J.V. Olsen, M. Hjerrild, J.R. Wisniewski, E. Stahl, M.S. Bolouri, H.N. Ray, S. Sihag, M. Kamal, et al. 2003. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell. 115:629-640. http://dx.doi.org/10.1016/S0092-8674(03)00926-7
42. Neubauer, S. 2007. The failing heart-an engine out of fuel. N. Engl. J. Med. 356:1140-1151. http://dx.doi.org/10.1056/NEJMra063052
43. Pagliarini, D.J., S.E. Calvo, B. Chang, S.A. Sheth, S.B. Vafai, S.E. Ong, G.A. Walford, C. Sugiana, A. Boneh, W.K. Chen, et al. 2008. A mitochondrial protein compendium elucidates complex I disease biology. Cell. 134:112-123. http://dx.doi.org/10.1016/j.cell.2008.06.016
44. Phillips, D., R. Covian, A.M. Aponte, B. Glancy, J.F. Taylor, D.J. Chess, and R.S. Balaban. 2012. Regulation of oxidative phosphorylation complex activity: effects of tissue-specific metabolic stress within an allometric series and acute changes in workload. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302:R1034-R1048. http://dx.doi.org/10.1152/ajpregu.00596.2011
45. Rabilloud, T., S. Kieffer, V. Procaccio, M. Louwagie, P.L. Courchesne, S.D. Patterson, P. Martinez, J. Garin, and J. Lunardi. 1998. Two-dimensional electrophoresis of human placental mitochondria and protein identification by mass spectrometry: toward a human mitochondrial proteome. Electrophoresis. 19:1006-1014. http://dx.doi.org/10.1002/elps.1150190616
46. Rasola, A., M. Sciacovelli, F. Chiara, B. Pantic, W.S. Brusilow, and P. Bernardi. 2010. Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc. Natl. Acad. Sci. USA. 107:726-731. http://dx.doi.org/10.1073/pnas.0912742107
47. Reifschneider, N.H., S. Goto, H. Nakamoto, R. Takahashi, M. Sugawa, N.A. Dencher, and F. Krause. 2006. Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J. Proteome Res. 5:1117-1132. http://dx.doi.org/10.1021/pr0504440
48. Richly, E., P.F. Chinnery, and D. Leister. 2003. Evolutionary diversification of mitochondrial proteomes: implications for human disease. Trends Genet. 19:356-362. http://dx.doi.org/10.1016/S0168-9525(03)00137-9
49. Rosca, M.G., and C.L. Hoppel. 2010. Mitochondria in heart failure. Cardiovasc. Res. 88:40-50. http://dx.doi.org/10.1093/cvr/cvq240
50. Sickmann, A., J. Reinders, Y. Wagner, C. Joppich, R. Zahedi, H.E. Meyer, B. Schönfisch, I. Perschil, A. Chacinska, B. Guiard, et al. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA. 100:13207-13212. http://dx.doi.org/10.1073/pnas.2135385100
51. Smith, A.C., and A.J. Robinson. 2009. MitoMiner, an integrated database for the storage and analysis of mitochondrial proteomics data. Mol. Cell. Proteomics. 8:1324-1337. http://dx.doi.org/10.1074/mcp.M800373-MCP200
52. Sun, J., M. Morgan, R.F. Shen, C. Steenbergen, and E. Murphy. 2007. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ. Res. 101:1155-1163. http://dx.doi.org/10.1161/CIRCRESAHA.107.155879
53. Taurino, F., E. Stanca, L. Siculella, R. Trentadue, S. Papa, F. Zanotti, and A. Gnoni. 2012. Mitochondrial proteome analysis reveals depression of the Ndufs3 subunit and activity of complex I in diabetic rat brain. J. Proteomics. 75:2331-2341. http://dx.doi.org/10.1016/j.jprot.2012.02.002
54. Taylor, S.W., E. Fahy, B. Zhang, G.M. Glenn, D.E. Warnock, S. Wiley, A.N. Murphy, S.P. Gaucher, R.A. Capaldi, B.W. Gibson, and S.S. Ghosh. 2003. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21:281-286. http://dx.doi.org/10.1038/nbt793
55. UniProt Consortium. 2012. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40:D71-D75. http://dx.doi.org/10.1093/nar/gkr981
56. Wallace, D.C. 2010. Mitochondrial DNA mutations in disease and aging. Environ. Mol. Mutagen. 51:440-450.
57. Wang, Z., N.D. Udeshi, M. O'Malley, J. Shabanowitz, D.F. Hunt, and G.W. Hart. 2010. Enrichment and site mapping of O-linked N-acetylglucosamine by a combination of chemical/enzymatic tagging, photochemical cleavage, and electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics. 9:153-160. http://dx.doi.org/10.1074/mcp.M900268-MCP200
58. Weiss, J.N., P. Korge, H.M. Honda, and P. Ping. 2003. Role of the mitochondrial permeability transition in myocardial disease. Circ. Res. 93:292-301. http://dx.doi.org/10.1161/01.RES.0000087542.26971.D4
59. Wu, R., W. Haas, N. Dephoure, E.L. Huttlin, B. Zhai, M.E. Sowa, and S.P. Gygi. 2011. A large-scale method to measure absolute protein phosphorylation stoichiometries. Nat. Methods. 8:677- 683. http://dx.doi.org/10.1038/nmeth.1636
60. Zahedi, R.P., A. Sickmann, A.M. Boehm, C. Winkler, N. Zufall, B. Schönfisch, B. Guiard, N. Pfanner, and C. Meisinger. 2006. Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol. Biol. Cell. 17:1436-1450. http://dx.doi.org/10.1091/mbc.E05-08-0740
61. Zhang, J., X. Li, M. Mueller, Y. Wang, C. Zong, N. Deng, T.M. Vondriska, D.A. Liem, J.I. Yang, P. Korge, et al. 2008. Systematic characterization of the murine mitochondrial proteome using functionally validated cardiac mitochondria. Proteomics. 8:1564- 1575. http://dx.doi.org/10.1002/pmic.200700851
62. Zhang, Z., M. Tan, Z. Xie, L. Dai, Y. Chen, and Y. Zhao. 2011. Identification of lysine succinylation as a new post-translational modification. Nat. Chem. Biol. 7:58-63. http://dx.doi.org/10.1038/nchembio.495
63. Zhu, W.Z., X.F. Wu, Y. Zhang, and Z.N. Zhou. 2012. Proteomic analysis of mitochondrial proteins in cardiomyocytes from rats subjected to intermittent hypoxia. Eur. J. Appl. Physiol. 112:1037- 1046. http://dx.doi.org/10.1007/s00421-011-2050-9