A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis

Cell Metabolism

Volumn 16, Issue 5, 2012, Pages 672-683

  Grimsrud, Paul A ^a   Carson, Joshua J ^a   Hebert, Alex S ^a,b   Hubler, Shane L ^a,b   Niemi, Natalie M ^a   Bailey, Derek J ^a,b   Jochem, Adam ^a   Stapleton, Donald S ^a   Keller, Mark P ^a   Westphall, Michael S ^b   Yandell, Brian S ^a   Attie, Alan D ^a   Coon, Joshua J ^a,b   Pagliarini, David J ^a  

^a Department of Biochemistry ^*  (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN; PROTEOME; SERINE;

ANIMAL CELL; ARTICLE; CATALYSIS; FUNCTIONAL PROTEOMICS; KETOGENESIS; LIVER MITOCHONDRION; MALE; MASS SPECTROMETRY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PLASTICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS;

EID: 84871461508     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.10.004     Document Type: Article

References (48)

1. Acin-Perez, R., Salazar, E., Kamenetsky, M., Buck, J., Levin, L.R., and Manfredi, G. (2009). Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab. 9, 265-276.
2. Andrew Skaff, D., and Miziorko, H.M. (2010). A visible wavelength spectrophotometric assay suitable for high-throughput screening of 3-hydroxy-3-methylglutaryl- CoA synthase. Anal. Biochem. 396, 96-102.
3. Berry, M.N., Clark, D.G., Grivell, A.R., and Wallace, P.G. (1983). The calorigenic nature of hepatic ketogenesis: an explanation for the stimulation of respiration induced by fatty acid substrates. Eur. J. Biochem. 131, 205-214.
4. Boja, E.S., Phillips, D., French, S.A., Harris, R.A., and Balaban, R.S. (2009). Quantitative mitochondrial phosphoproteomics using iTRAQ on an LTQOrbitrap with high energy collision dissociation. J. Proteome Res. 8, 4665-4675.
5. Bonet, M.L., Ribot, J., and Palou, A. (2012). Lipid metabolism in mammalian tissues and its control by retinoic acid. Biochim. Biophys. Acta 1821, 177-189.
6. Buchner, D.A., Yazbek, S.N., Solinas, P., Burrage, L.C., Morgan, M.G., Hoppel, C.L., and Nadeau, J.H. (2011). Increased mitochondrial oxidative phosphorylation in the liver is associated with obesity and insulin resistance. Obesity (Silver Spring) 19, 917-924.
7. Calvo, S.E., and Mootha, V.K. (2010). The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 11, 25-44.
8. Chen, Y.Q., Zhu, J., Lum, P.Y., Yang, X., Pinto, S., MacNeil, D.J., Zhang, C.S., Lamb, J., Edwards, S., Sieberts, S.K., et al. (2008). Variations in DNA elucidate molecular networks that cause disease. Nature 452, 429-435.
9. Deng, W.J., Nie, S., Dai, J., Wu, J.R., and Zeng, R. (2010). Proteome, phosphoproteome, and hydroxyproteome of liver mitochondria in diabetic rats at early pathogenic stages. Mol. Cell. Proteomics 9, 100-116.
10. Fang, X., Yu, S.X., Lu, Y., Bast, R.C., Jr., Woodgett, J.R., and Mills, G.B. (2000). Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc. Natl. Acad. Sci. USA 97, 11960-11965.
11. Foster, L.J., de Hoog, C.L., Zhang, Y., Zhang, Y., Xie, X., Mootha, V.K., and Mann, M. (2006). A mammalian organelle map by protein correlation profiling. Cell 125, 187-199.
12. Gnad, F., Gunawardena, J., and Mann, M. (2011). PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res. 39(Database issue), D253-D260.
13. Grimsrud, P.A., den Os, D., Wenger, C.D., Swaney, D.L., Schwartz, D., Sussman, M.R., Ané, J.M., and Coon, J.J. (2010a). Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol. 152, 19-28.
14. Grimsrud, P.A., Swaney, D.L., Wenger, C.D., Beauchene, N.A., and Coon, J.J. (2010b). Phosphoproteomics for the masses. ACS Chem. Biol. 5, 105-119.
15. Guan, K.L., and Xiong, Y. (2011). Regulation of intermediary metabolism by protein acetylation. Trends Biochem. Sci. 36, 108-116.
16. Holmström, M.H., Iglesias-Gutierrez, E., Zierath, J.R., and Garcia-Roves, P.M. (2012). Tissue-specific control of mitochondrial respiration in obesity-related insulin resistance and diabetes. Am. J. Physiol. Endocrinol. Metab. 302, E731-E739.
17. Huttlin, E.L., Jedrychowski, M.P., Elias, J.E., Goswami, T., Rad, R., Beausoleil, S.A., Villén, J., Haas, W., Sowa, M.E., and Gygi, S.P. (2010). A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189.
18. Johnson, D.T., Harris, R.A., French, S., Blair, P.V., You, J., Bemis, K.G., Wang, M., and Balaban, R.S. (2007). Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell Physiol. 292, C689-C697.
19. Keller, M.P., Choi, Y., Wang, P., Davis, D.B., Rabaglia, M.E., Oler, A.T., Stapleton, D.S., Argmann, C., Schueler, K.L., Edwards, S., et al. (2008). A gene expression network model of type 2 diabetes links cell cycle regulation in islets with diabetes susceptibility. Genome Res. 18, 706-716.
20. Kostiuk, M.A., Corvi, M.M., Keller, B.O., Plummer, G., Prescher, J.A., Hangauer, M.J., Bertozzi, C.R., Rajaiah, G., Falck, J.R., and Berthiaume, L.G. (2008). Identification of palmitoylated mitochondrial proteins using a bio-orthogonal azido-palmitate analogue. FASEB J. 22, 721-732.
21. Lea, W., Abbas, A.S., Sprecher, H., Vockley, J., and Schulz, H. (2000). Longchain acyl-CoA dehydrogenase is a key enzyme in the mitochondrial betaoxidation of unsaturated fatty acids. Biochim. Biophys. Acta 1485, 121-128.
22. Lee, J., Xu, Y., Chen, Y., Sprung, R., Kim, S.C., Xie, S., and Zhao, Y. (2007). Mitochondrial phosphoproteome revealed by an improved IMAC method and MS/MS/MS. Mol. Cell. Proteomics 6, 669-676.
23. Lee, M.V., Topper, S.E., Hubler, S.L., Hose, J., Wenger, C.D., Coon, J.J., and Gasch, A.P. (2011). A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol. Syst. Biol. 7, 514.
24. McAlister, G.C., Russell, J.D., Rumachik, N.G., Hebert, A.S., Syka, J.E., Geer, L.Y., Westphall, M.S., Pagliarini, D.J., and Coon, J.J. (2012). Analysis of the acidic proteome with negative electron-transfer dissociation mass spectrometry. Anal. Chem. 84, 2875-2882.
25. Monetti, M., Nagaraj, N., Sharma, K., and Mann, M. (2011). Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nat. Methods 8, 655-658.
26. Nunnari, J., and Suomalainen, A. (2012). Mitochondria: in sickness and in health. Cell 148, 1145-1159.
27. Olsen, J.V., Macek, B., Lange, O., Makarov, A., Horning, S., and Mann, M. (2007). Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 4, 709-712.
28. O'Rourke, B., Van Eyk, J.E., and Foster, D.B. (2011). Mitochondrial protein phosphorylation as a regulatory modality: implications for mitochondrial dysfunction in heart failure. Congest. Heart Fail. 17, 269-282.
29. Pagliarini, D.J., and Dixon, J.E. (2006). Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem. Sci. 31, 26-34.
30. Pagliarini, D.J., Calvo, S.E., Chang, B., Sheth, S.A., Vafai, S.B., Ong, S.E., Walford, G.A., Sugiana, C., Boneh, A., Chen, W.K., et al. (2008). A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123.
31. Phanstiel, D.H., Brumbaugh, J., Wenger, C.D., Tian, S., Probasco, M.D., Bailey, D.J., Swaney, D.L., Tervo, M.A., Bolin, J.M., Ruotti, V., et al. (2011). Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat. Methods 8, 821-827.
32. Quant, P.A., Tubbs, P.K., and Brand, M.D. (1990). Glucagon activates mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase in vivo by decreasing the extent of succinylation of the enzyme. Eur. J. Biochem. 187, 169-174.
33. Reed, W.D., Clinkenbeard, D., and Lane, M.D. (1975). Molecular and catalytic properties of mitochondrial (ketogenic) 3-hydroxy-3-methylglutaryl coenzyme A synthase of liver. J. Biol. Chem. 250, 3117-3123.
34. Ross, P.L., Huang, Y.N., Marchese, J.N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., et al. (2004). Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169.
35. Schmidt, O., Harbauer, A.B., Rao, S., Eyrich, B., Zahedi, R.P., Stojanovski, D., Schönfisch, B., Guiard, B., Sickmann, A., Pfanner, N., and Meisinger, C. (2011). Regulation of mitochondrial protein import by cytosolic kinases. Cell 144, 227-239.
36. Schwartz, D., and Gygi, S.P. (2005). An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398.
37. Sengupta, S., Peterson, T.R., Laplante, M., Oh, S., and Sabatini, D.M. (2010). mTORC1 controls fasting-induced ketogenesis and its modulation by ageing. Nature 468, 1100-1104.
38. Shimazu, T., Hirschey, M.D., Hua, L., Dittenhafer-Reed, K.E., Schwer, B., Lombard, D.B., Li, Y., Bunkenborg, J., Alt, F.W., Denu, J.M., et al. (2010). SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab. 12, 654-661.
39. Syka, J.E., Coon, J.J., Schroeder, M.J., Shabanowitz, J., and Hunt, D.F. (2004). Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 101, 9528-9533.
40. Szendroedi, J., Phielix, E., and Roden, M. (2012). The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat. Rev. Endocrinol. 8, 92-103.
41. Thompson, A., Schäfer, J., Kuhn, K., Kienle, S., Schwarz, J., Schmidt, G., Neumann, T., Johnstone, R., Mohammed, A.K., and Hamon, C. (2003). Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 75, 1895-1904.
42. Villén, J., Beausoleil, S.A., Gerber, S.A., and Gygi, S.P. (2007). Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. USA 104, 1488-1493.
43. Wang, C.Y., Stapleton, D.S., Schueler, K.L., Rabaglia, M.E., Oler, A.T., Keller, M.P., Kendziorski, C.M., Broman, K.W., Yandell, B.S., Schadt, E.E., and Attie, A.D. (2012a). Tsc2, a positional candidate gene underlying a quantitative trait locus for hepatic steatosis. J. Lipid Res. 53, 1493-1501.
44. Wang, Y., Li, G., Goode, J., Paz, J.C., Ouyang, K., Screaton, R., Fischer, W.H., Chen, J., Tabas, I., and Montminy, M. (2012b). Inositol-1,4,5-trisphosphate receptor regulates hepatic gluconeogenesis in fasting and diabetes. Nature 485, 128-132.
45. Wenger, C.D., Lee, M.V., Hebert, A.S., McAlister, G.C., Phanstiel, D.H., Westphall, M.S., and Coon, J.J. (2011a). Gas-phase purification enables accurate, multiplexed proteome quantification with isobaric tagging. Nat. Methods 8, 933-935.
46. Wenger, C.D., Phanstiel, D.H., Lee, M.V., Bailey, D.J., and Coon, J.J. (2011b). COMPASS: a suite of pre- and post-search proteomics software tools for OMSSA. Proteomics 11, 1064-1074.
47. Zhao, E., Keller, M.P., Rabaglia, M.E., Oler, A.T., Stapleton, D.S., Schueler, K.L., Neto, E.C., Moon, J.Y., Wang, P., Wang, I.M., et al. (2009). Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm. Genome 20, 476-485.
48. Zhao, X., Leon, I.R., Bak, S., Mogensen, M., Wrzesinski, K., Hojlund, K., and Jensen, O.N. (2011). Phosphoproteome analysis of functional mitochondria isolated from resting human muscle reveals extensive phosphorylation of inner membrane protein complexes and enzymes. Mol. Cell. Proteomics 10. http://dx.doi.org/10.1074/mcp.M110.000299, M110 000299.