Insulin increases phosphorylation of mitochondrial proteins in human skeletal muscle in vivo

Journal of Proteome Research

Volumn 13, Issue 5, 2014, Pages 2359-2369

  Zhao, Xiaolu ^a,b   Bak, Steffen ^a   Pedersen, Andreas J T ^c   Jensen, Ole Nørregaard ^a   Højlund, Kurt ^a,c,d  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b WUHAN UNIVERSITY   (China)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

human skeletal muscle; insulin stimulation in vivo; mitochondria; oxidative phosphorylation; phosphoproteomics

Indexed keywords

INSULIN; MITOCHONDRIAL PROTEIN; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; TITANIUM DIOXIDE; ANTIDIABETIC AGENT;

ADULT; ARTICLE; BODY MASS; CITRIC ACID CYCLE; ELECTROSPRAY MASS SPECTROMETRY; FATTY ACID METABOLISM; HUMAN; HUMAN CELL; HYDROPHILIC INTERACTION CHROMATOGRAPHY; IN VIVO STUDY; INSULIN INFUSION; MUSCLE MITOCHONDRION; NORMAL HUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; TANDEM MASS SPECTROMETRY; BINDING SITE; CLASSIFICATION; DRUG EFFECTS; LIQUID CHROMATOGRAPHY; METABOLISM; MIDDLE AGED; PHOSPHORYLATION; PROCEDURES; PROTEOMICS;

ADULT; BINDING SITES; CHROMATOGRAPHY, LIQUID; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN INFUSION SYSTEMS; MIDDLE AGED; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OXIDATIVE PHOSPHORYLATION; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84899824172     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401163t     Document Type: Article

References (58)

1. Newmeyer, D. D.; Ferguson-Miller, S. Mitochondria: releasing power for life and unleashing the machineries of death Cell 2003, 112, 481-490
2. Szendroedi, J.; Phielix, E.; Roden, M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus Nat. Rev. Endocrinol. 2012, 8, 92-103
3. Balaban, R. S. The mitochondrial proteome: a dynamic functional program in tissues and disease states Environ. Mol. Mutagen 2010, 51, 352-359
4. Nunnari, J.; Suomalainen, A. Mitochondria: in sickness and in health Cell 2012, 148, 1145-1159
5. Covian, R.; Balaban, R. S. Cardiac mitochondrial matrix and respiratory complex protein phosphorylation Am. J. Physiol. Heart Circ. Physiol. 2012, 303, H940-966
6. Feng, J.; Zhu, M.; Schaub, M. C.; Gehrig, P.; Roschitzki, B.; Lucchinetti, E.; Zaugg, M. Phosphoproteome analysis of isoflurane-protected heart mitochondria: phosphorylation of adenine nucleotide translocator-1 on Tyr194 regulates mitochondrial function Cardiovasc. Res. 2008, 80, 20-29
7. Grimsrud, P. A.; Carson, J. J.; Hebert, A. S.; Hubler, S. L.; Niemi, N. M.; Bailey, D. J.; Jochem, A.; Stapleton, D. S.; Keller, M. P.; Westphall, M. S.; Yandell, B. S.; Attie, A. D.; Coon, J. J.; Pagliarini, D. J. A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis Cell Metab. 2012, 16, 672-683
8. Pagliarini, D. J.; Dixon, J. E. Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem. Sci. 2006, 31, 26-34
9. Zhao, X.; Leon, I. R.; Bak, S.; Mogensen, M.; Wrzesinski, K.; Hojlund, K.; Jensen, O. N. Phosphoproteome analysis of functional mitochondria isolated from resting human muscle reveals extensive phosphorylation of inner membrane protein complexes and enzymes Mol. Cell. Proteomics 2011, 10 M110 000299
10. Mottram, R. F. The oxygen consumption of human skeletal muscle in vivo J. Physiol. 1955, 128, 268-276
11. Hojlund, K.; Beck-Nielsen, H. Impaired glycogen synthase activity and mitochondrial dysfunction in skeletal muscle: markers or mediators of insulin resistance in type 2 diabetes? Curr. Diabetes Rev. 2006, 2, 375-395
12. Diamanti-Kandarakis, E.; Dunaif, A. Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications Endocr. Rev. 2012, 33, 981-1030
13. Hojlund, K.; Glintborg, D.; Andersen, N. R.; Birk, J. B.; Treebak, J. T.; Frosig, C.; Beck-Nielsen, H.; Wojtaszewski, J. F. Impaired insulin-stimulated phosphorylation of Akt and AS160 in skeletal muscle of women with polycystic ovary syndrome is reversed by pioglitazone treatment Diabetes 2008, 57, 357-366
14. Vind, B. F.; Pehmoller, C.; Treebak, J. T.; Birk, J. B.; Hey-Mogensen, M.; Beck-Nielsen, H.; Zierath, J. R.; Wojtaszewski, J. F.; Hojlund, K. Impaired insulin-induced site-specific phosphorylation of TBC1 domain family, member 4 (TBC1D4) in skeletal muscle of type 2 diabetes patients is restored by endurance exercise-training Diabetologia 2011, 54, 157-167
15. Vind, B. F.; Birk, J. B.; Vienberg, S. G.; Andersen, B.; Beck-Nielsen, H.; Wojtaszewski, J. F.; Hojlund, K. Hyperglycaemia normalises insulin action on glucose metabolism but not the impaired activation of AKT and glycogen synthase in the skeletal muscle of patients with type 2 diabetes Diabetologia 2012, 55, 1435-1445
16. Hojlund, K.; Mogensen, M.; Sahlin, K.; Beck-Nielsen, H. Mitochondrial dysfunction in type 2 diabetes and obesity Endocrinol. Metab. Clin. North Am. 2008, 37, 713-731
17. Skov, V.; Glintborg, D.; Knudsen, S.; Tan, Q.; Jensen, T.; Kruse, T. A.; Beck-Nielsen, H.; Hojlund, K. Pioglitazone enhances mitochondrial biogenesis and ribosomal protein biosynthesis in skeletal muscle in polycystic ovary syndrome PLoS One 2008, 3, e2466
18. Phielix, E.; Schrauwen-Hinderling, V. B.; Mensink, M.; Lenaers, E.; Meex, R.; Hoeks, J.; Kooi, M. E.; Moonen-Kornips, E.; Sels, J. P.; Hesselink, M. K.; Schrauwen, P. Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients Diabetes 2008, 57, 2943-2949
19. Sleigh, A.; Raymond-Barker, P.; Thackray, K.; Porter, D.; Hatunic, M.; Vottero, A.; Burren, C.; Mitchell, C.; McIntyre, M.; Brage, S.; Carpenter, T. A.; Murgatroyd, P. R.; Brindle, K. M.; Kemp, G. J.; O'Rahilly, S.; Semple, R. K.; Savage, D. B. Mitochondrial dysfunction in patients with primary congenital insulin resistance J. Clin. Invest. 2011, 121, 2457-2461
20. Taniguchi, C. M.; Emanuelli, B.; Kahn, C. R. Critical nodes in signalling pathways: insights into insulin action Nat. Rev. Mol. Cell. Biol. 2006, 7, 85-96
21. Szendroedi, J.; Schmid, A. I.; Chmelik, M.; Toth, C.; Brehm, A.; Krssak, M.; Nowotny, P.; Wolzt, M.; Waldhausl, W.; Roden, M. Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes PLoS Med. 2007, 4, e154
22. Stump, C. S.; Short, K. R.; Bigelow, M. L.; Schimke, J. M.; Nair, K. S. Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 7996-8001
23. Hojlund, K.; Yi, Z.; Lefort, N.; Langlais, P.; Bowen, B.; Levin, K.; Beck-Nielsen, H.; Mandarino, L. J. Human ATP synthase beta is phosphorylated at multiple sites and shows abnormal phosphorylation at specific sites in insulin-resistant muscle Diabetologia 2010, 53, 541-551
24. Bijur, G. N.; Jope, R. S. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation J. Neurochem. 2003, 87, 1427-1435
25. Yang, J. Y.; Yeh, H. Y.; Lin, K.; Wang, P. H. Insulin stimulates Akt translocation to mitochondria: implications on dysregulation of mitochondrial oxidative phosphorylation in diabetic myocardium J. Mol. Cell. Cardiol. 2009, 46, 919-926
26. Hey-Mogensen, M.; Hojlund, K.; Vind, B. F.; Wang, L.; Dela, F.; Beck-Nielsen, H.; Fernstrom, M.; Sahlin, K. Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes Diabetologia 2010, 53, 1976-1985
27. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6, 359-362
28. Savitski, M. M.; Lemeer, S.; Boesche, M.; Lang, M.; Mathieson, T.; Bantscheff, M.; Kuster, B. Confident phosphorylation site localization using the Mascot Delta Score Mol. Cell. Proteomics 2011, 10 M110 003830
29. Taus, T.; Kocher, T.; Pichler, P.; Paschke, C.; Schmidt, A.; Henrich, C.; Mechtler, K. Universal and confident phosphorylation site localization using phosphoRS J. Proteome Res. 2011, 10, 5354-5362
30. Linding, R.; Jensen, L. J.; Ostheimer, G. J.; van Vugt, M. A.; Jorgensen, C.; Miron, I. M.; Diella, F.; Colwill, K.; Taylor, L.; Elder, K.; Metalnikov, P.; Nguyen, V.; Pasculescu, A.; Jin, J.; Park, J. G.; Samson, L. D.; Woodgett, J. R.; Russell, R. B.; Bork, P.; Yaffe, M. B.; Pawson, T. Systematic discovery of in vivo phosphorylation networks Cell 2007, 129, 1415-1426
31. Hojlund, K.; Bowen, B. P.; Hwang, H.; Flynn, C. R.; Madireddy, L.; Thangiah, G.; Meyer, C.; Mandarino, L. J.; Yi, Z. In vivo phosphoproteome of human skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS J. Proteome Res. 2009, 8, 4954-4965
32. Lefort, N.; Yi, Z.; Bowen, B.; Glancy, B.; De Filippis, E. A.; Mapes, R.; Hwang, H.; Flynn, C. R.; Willis, W. T.; Civitarese, A.; Hojlund, K.; Mandarino, L. J. Proteome profile of functional mitochondria from human skeletal muscle using one-dimensional gel electrophoresis and HPLC-ESI-MS/MS J. Proteomics 2009, 72, 1046-1060
33. 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, 257-267
34. Kelley, D. E.; Mandarino, L. J. Fuel selection in human skeletal muscle in insulin resistance: a reexamination Diabetes 2000, 49, 677-683
35. Linn, T. C.; Pettit, F. H.; Reed, L. J. Alpha-keto acid dehydrogenase complexes. X. Regulation of the activity of the pyruvate dehydrogenase complex from beef kidney mitochondria by phosphorylation and dephosphorylation Proc. Natl. Acad. Sci. U.S.A. 1969, 62, 234-241
36. Harris, R. A.; Hawes, J. W.; Popov, K. M.; Zhao, Y.; Shimomura, Y.; Sato, J.; Jaskiewicz, J.; Hurley, T. D. Studies on the regulation of the mitochondrial alpha-ketoacid dehydrogenase complexes and their kinases Adv. Enzyme Regul. 1997, 37, 271-293
37. Patel, M. S.; Korotchkina, L. G. Regulation of mammalian pyruvate dehydrogenase complex by phosphorylation: complexity of multiple phosphorylation sites and kinases Exp. Mol. Med. 2001, 33, 191-197
38. Mandarino, L. J.; Wright, K. S.; Verity, L. S.; Nichols, J.; Bell, J. M.; Kolterman, O. G.; Beck-Nielsen, H. Effects of insulin infusion on human skeletal muscle pyruvate dehydrogenase, phosphofructokinase, and glycogen synthase. Evidence for their role in oxidative and nonoxidative glucose metabolism J. Clin. Invest. 1987, 80, 655-663
39. Feng, J.; Lucchinetti, E.; Enkavi, G.; Wang, Y.; Gehrig, P.; Roschitzki, B.; Schaub, M. C.; Tajkhorshid, E.; Zaugg, K.; Zaugg, M. Tyrosine phosphorylation by Src within the cavity of the adenine nucleotide translocase 1 regulates ADP/ATP exchange in mitochondria Am. J. Physiol. Cell. Physiol. 2010, 298, C740-748
40. Sanderson, T. H.; Mahapatra, G.; Pecina, P.; Ji, Q.; Yu, K.; Sinkler, C.; Varughese, A.; Kumar, R.; Bukowski, M. J.; Tousignant, R. N.; Salomon, A. R.; Lee, I.; Hüttemann, M. Cytochrome C is tyrosine 97 phosphorylated by neuroprotective insulin treatment PLoS One 2013, 8, e78627
41. Zerbes, R. M.; Bohnert, M.; Stroud, D. A.; von der Malsburg, K.; Kram, A.; Oeljeklaus, S.; Warscheid, B.; Becker, T.; Wiedemann, N.; Veenhuis, M.; van der Klei, I. J.; Pfanner, N.; van der Laan, M. Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains J. Mol. Biol. 2012, 422, 183-191
42. van der Laan, M.; Bohnert, M.; Wiedemann, N.; Pfanner, N. Role of MINOS in mitochondrial membrane architecture and biogenesis Trends Cell Biol. 2012, 22, 185-192
43. Xie, J.; Marusich, M. F.; Souda, P.; Whitelegge, J.; 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. 2007, 581, 3545-3549
44. Darshi, M.; Mendiola, V. L.; Mackey, M. R.; Murphy, A. N.; Koller, A.; Perkins, G. A.; Ellisman, M. H.; Taylor, S. S. ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function J. Biol. Chem. 2011, 286, 2918-2932
45. Ott, C.; Ross, K.; Straub, S.; Thiede, B.; Gotz, M.; Goosmann, C.; Krischke, M.; Mueller, M. J.; Krohne, G.; Rudel, T.; Kozjak-Pavlovic, V. Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes Mol. Cell. Biol. 2012, 32, 1173-1188
46. Weber, T. A.; Koob, S.; Heide, H.; Wittig, I.; Head, B.; van der Bliek, A.; Brandt, U.; Mittelbronn, M.; Reichert, A. S. APOOL is a cardiolipin-binding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria PloS One 2013, 8, e63683
47. Kontro, H.; Hulmi, J. J.; Rahkila, P.; Kainulainen, H. Cellular and tissue expression of DAPIT, a phylogenetically conserved peptide Eur. J. Histochem. 2012, 56, e18
48. Ohsakaya, S.; Fujikawa, M.; Hisabori, T.; Yoshida, M. Knockdown of DAPIT (diabetes-associated protein in insulin-sensitive tissue) results in loss of ATP synthase in mitochondria J. Biol. Chem. 2011, 286, 20292-20296
49. Meyer, B.; Wittig, I.; Trifilieff, E.; Karas, M.; Schagger, H. Identification of two proteins associated with mammalian ATP synthase Mol. Cell. Proteomics 2007, 6, 1690-1699
50. Kelley, D. E.; He, J.; Menshikova, E. V.; Ritov, V. B. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes Diabetes 2002, 51, 2944-2950
51. Hwang, H.; Bowen, B. P.; Lefort, N.; Flynn, C. R.; De Filippis, E. A.; Roberts, C.; Smoke, C. C.; Meyer, C.; Hojlund, K.; Yi, Z.; Mandarino, L. J. Proteomics analysis of human skeletal muscle reveals novel abnormalities in obesity and type 2 diabetes Diabetes 2010, 59, 33-42
52. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 2006, 127, 635-648
53. Boersema, P. J.; Mohammed, S.; Heck, A. J. Hydrophilic interaction liquid chromatography (HILIC) in proteomics Anal. Bioanal. Chem. 2008, 391, 151-159
54. McNulty, D. E.; Annan, R. S. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection Mol. Cell. Proteomics 2008, 7, 971-980
55. Engholm-Keller, K.; Hansen, T. A.; Palmisano, G.; Larsen, M. R. Multidimensional strategy for sensitive phosphoproteomics incorporating protein prefractionation combined with SIMAC, HILIC, and TiO(2) chromatography applied to proximal EGF signaling J. Proteome Res. 2011, 10, 5383-5397
56. Engholm-Keller, K.; Birck, P.; Storling, J.; Pociot, F.; Mandrup-Poulsen, T.; Larsen, M. R. TiSH - a robust and sensitive global phosphoproteomics strategy employing a combination of TiO2, SIMAC, and HILIC J. Proteomics 2012, 75, 5749-5761
57. Picard, M.; Taivassalo, T.; Ritchie, D.; Wright, K. J.; Thomas, M. M.; Romestaing, C.; Hepple, R. T. Mitochondrial structure and function are disrupted by standard isolation methods PLoS One 2011, 6, e18317
58. Perry, C. G.; Kane, D. A.; Lanza, I. R.; Neufer, P. D. Methods for assessing mitochondrial function in diabetes Diabetes 2013, 62 (4) 1041-1053