Lifelong exercise training modulates cardiac mitochondrial phosphoproteome in rats

Journal of Proteome Research

Volumn 13, Issue 4, 2014, Pages 2045-2055

  Ferreira, Rita ^a,c   Vitorino, Rui ^a,c   Padrão, Ana Isabel ^a   Espadas, Guadalupe ^b,c   Mancuso, Francesco M ^b,c   Moreira Gonçalves, Daniel ^d,e   Castro Sousa, Gonçalo ^e   Henriques Coelho, Tiago ^d   Oliveira, Paula A ^f   Barros, António S ^a   Duarte, José Alberto ^e   Sabidó, Eduard ^a,c   Amado, Francisco ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d Inst of Pharmacol and Therapeutics   (Portugal)

^e UNIVERSITY OF PORTO   (Portugal)

^f UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

Author keywords

kinases; mitochondria; phosphoproteomics; protein phosphorylation

Indexed keywords

PHOSPHOPROTEOME; PROTEOME; RAF PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN; PHOSPHOPROTEIN; PROTEIN KINASE;

ACCURACY; ANIMAL EXPERIMENT; ARTICLE; CARBOHYDRATE METABOLISM; CELL RESPIRATION; CONTROLLED STUDY; FEMALE; HEART FUNCTION; HEART MITOCHONDRION; MASS SPECTROMETRY; METABOLITE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT; SITTING; TREADMILL EXERCISE; WESTERN BLOTTING; ANIMAL; CHEMISTRY; HEART MUSCLE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION; SPRAGUE DAWLEY RAT;

ANIMALS; FEMALE; MITOCHONDRIAL PROTEINS; MYOCARDIUM; PHOSPHOPROTEINS; PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; PROTEIN INTERACTION MAPS; PROTEIN KINASES; PROTEOME; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84898762243     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4011926     Document Type: Article

References (47)

1. Balaban, R. S. Maintenance of the metabolic homeostasis of the heart: developing a systems analysis approach Ann. N.Y. Acad. Sci. 2006, 1080, 140-153
2. Gustafsson, A. B.; Gottlieb, R. A. Heart mitochondria: gates of life and death Cardiovasc. Res. 2008, 77, 334-343
3. Johannsen, D. L.; Ravussin, E. The role of mitochondria in health and disease Curr. Opin. Pharmacol. 2009, 9, 780-786
4. Frasier, C. R.; Moore, R. L.; Brown, D. A. Exercise-induced cardiac preconditioning: how exercise protects your achy-breaky heart J. Appl. Physiol. 2011, 111, 905-915
5. Ascensao, A.; Ferreira, R.; Magalhaes, J. Exercise-induced cardioprotection - biochemical, morphological and functional evidence in whole tissue and isolated mitochondria Int. J. Cardiol. 2007, 117, 16-30
6. Li, L.; Muhlfeld, C.; Niemann, B.; Pan, R.; Li, R.; Hilfiker-Kleiner, D.; Chen, Y.; Rohrbach, S. Mitochondrial biogenesis and PGC-1alpha deacetylation by chronic treadmill exercise: differential response in cardiac and skeletal muscle Basic Res. Cardiol. 2011, 106, 1221-1234
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. Koc, E. C.; Koc, H. Regulation of mammalian mitochondrial translation by post-translational modifications Biochim. Biophys. Acta 2012, 1819, 1055-1066
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. Deng, N.; Zhang, J.; Zong, C.; Wang, Y.; Lu, H.; Yang, P.; Wang, W.; Young, G. W.; Korge, P.; Lotz, C.; Doran, P.; Liem, D. A.; Apweiler, R.; Weiss, J. N.; Duan, H.; Ping, P. Phosphoproteome analysis reveals regulatory sites in major pathways of cardiac mitochondria Mol. Cell. Proteomics 2011, 10 M110 000117
11. Falcao-Pires, I.; Palladini, G.; Goncalves, N.; van der Velden, J.; Moreira-Goncalves, D.; Miranda-Silva, D.; Salinaro, F.; Paulus, W. J.; Niessen, H. W.; Perlini, S.; Leite-Moreira, A. F. Distinct mechanisms for diastolic dysfunction in diabetes mellitus and chronic pressure-overload Basic Res. Cardiol. 2011, 106, 801-814
12. Ascensao, A.; Magalhaes, J.; Soares, J. M.; Ferreira, R.; Neuparth, M. J.; Marques, F.; Oliveira, P. J.; Duarte, J. A. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis Am. J. Physiol. Heart Circ. Physiol. 2005, 289, H722-731
13. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent J. Biol. Chem. 1951, 193, 265-275
14. Simon, N.; Papa, K.; Vidal, J.; Boulamery, A.; Bruguerolle, B. Circadian rhythms of oxidative phosphorylation: effects of rotenone and melatonin on isolated rat brain mitochondria Chronobiol. Int. 2003, 20, 451-461
15. Schagger, H.; von Jagow, G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Anal. Biochem. 1991, 199, 223-231
16. Zerbetto, E.; Vergani, L.; Dabbeni-Sala, F. Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels Electrophoresis 1997, 18, 2059-2064
17. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970, 227, 680-685
18. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6, 359-362
19. Rappsilber, J.; Mann, M.; Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips Nat. Protoc. 2007, 2, 1896-906
20. Thingholm, T. E.; Larsen, M. R. The use of titanium dioxide micro-columns to selectively isolate phosphopeptides from proteolytic digests Methods Mol. Biol. 2009, 527, 57-66 xi.
21. Silva, J. C.; Gorenstein, M. V.; Li, G. Z.; Vissers, J. P.; Geromanos, S. J. Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition Mol. Cell. Proteomics 2006, 5, 144-156
22. Taus, T.; Köcher, T.; Pichler, P.; Paschke, C.; Schmidt, A.; Henrich, C.; Mechtler, K. Universal and confident phosphorylation site localization using phosphoRS J. Proteome Res. 2011, 10 (12) 5354-62
23. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing J. R. Stat. Soc. B 1995, 57, 289-300
24. Maere, S.; Heymans, K.; Kuiper, M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks Bioinformatics 2005, 21, 3448-3449
25. Locatelli, J.; de Assis, L. V.; Isoldi, M. C. Calcium handling proteins: structure, function, and modulation by exercise Heart Fail. Rev. 2013, 10.1007/s10741-013-9373-z
26. Pagliarini, D. J.; Dixon, J. E. Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem. Sci. 2006, 31, 26-34
27. O'Rourke, B.; Van Eyk, J. E.; Foster, D. B. Mitochondrial protein phosphorylation as a regulatory modality: implications for mitochondrial dysfunction in heart failure Congest. Heart Fail. 2011, 17, 269-282
28. Kadaja, L.; Eimre, M.; Paju, K.; Roosimaa, M.; Podramagi, T.; Kaasik, P.; Pehme, A.; Orlova, E.; Mudist, M.; Peet, N.; Piirsoo, A.; Seene, T.; Gellerich, F. N.; Seppet, E. K. Impaired oxidative phosphorylation in overtrained rat myocardium Exp. Clin. Cardiol. 2010, 15, e116-127
29. Fillmore, N.; Lopaschuk, G. D. Targeting mitochondrial oxidative metabolism as an approach to treat heart failure Biochim. Biophys. Acta 2013, 1833, 857-865
30. Li, X.; Arslan, F.; Ren, Y.; Adav, S. S.; Poh, K. K.; Sorokin, V.; Lee, C. N.; de Kleijn, D.; Lim, S. K.; Sze, S. K. Metabolic adaptation to a disruption in oxygen supply during myocardial ischemia and reperfusion is underpinned by temporal and quantitative changes in the cardiac proteome J. Proteome Res. 2012, 11, 2331-2346
31. Lee, J.; Xu, Y.; Chen, Y.; Sprung, R.; Kim, S. C.; Xie, S.; Zhao, Y. Mitochondrial phosphoproteome revealed by an improved IMAC method and MS/MS/MS Mol. Cell. Proteomics 2007, 6, 669-676
32. Covian, R.; Balaban, R. S. Cardiac mitochondrial matrix and respiratory complex protein phosphorylation Am. J. Physiol. Heart Circ. Physiol. 2012, 303, H940-966
33. He, L.; Kim, T.; Long, Q.; Liu, J.; Wang, P.; Zhou, Y.; Ding, Y.; Prasain, J.; Wood, P. A.; Yang, Q. Carnitine palmitoyltransferase-1b deficiency aggravates pressure overload-induced cardiac hypertrophy caused by lipotoxicity Circulation 2012, 126, 1705-1716
34. Kerner, J.; Distler, A. M.; Minkler, P.; Parland, W.; Peterman, S. M.; Hoppel, C. L. Phosphorylation of rat liver mitochondrial carnitine palmitoyltransferase-I: effect on the kinetic properties of the enzyme J. Biol. Chem. 2004, 279, 41104-41113
35. Medeiros, A.; Rolim, N. P.; Oliveira, R. S.; Rosa, K. T.; Mattos, K. C.; Casarini, D. E.; Irigoyen, M. C.; Krieger, E. M.; Krieger, J. E.; Negrao, C. E.; Brum, P. C. Exercise training delays cardiac dysfunction and prevents calcium handling abnormalities in sympathetic hyperactivity-induced heart failure mice J. Appl. Physiol. 2008, 104, 103-109
36. Artal-Sanz, M.; Tavernarakis, N. Prohibitin and mitochondrial biology Trends Endocrinol. Metab. 2009, 20, 394-401
37. Mishra, S.; Ande, S. R.; Nyomba, B. L. The role of prohibitin in cell signaling FEBS J. 2010, 277, 3937-3946
38. Yao, Z.; Seger, R. The ERK signaling cascade - views from different subcellular compartments Biofactors 2009, 35, 407-416
39. Kuznetsov, A. V.; Smigelskaite, J.; Doblander, C.; Janakiraman, M.; Hermann, M.; Wurm, M.; Scheidl, S. F.; Sucher, R.; Deutschmann, A.; Troppmair, J. Survival signaling by C-RAF: mitochondrial reactive oxygen species and Ca2+ are critical targets Mol. Cell. Biol. 2008, 28, 2304-2313
40. Muslin, A. J. Role of raf proteins in cardiac hypertrophy and cardiomyocyte survival Trends Cardiovasc. Med. 2005, 15, 225-229
41. Rose, B. A.; Force, T.; Wang, Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale Physiol. Rev. 2010, 90, 1507-1546
42. Iemitsu, M.; Maeda, S.; Jesmin, S.; Otsuki, T.; Kasuya, Y.; Miyauchi, T. Activation pattern of MAPK signaling in the hearts of trained and untrained rats following a single bout of exercise J. Appl. Physiol. 2006, 101, 151-163
43. Chang, Z.; Zhang, Q.; Feng, Q.; Xu, J.; Teng, T.; Luan, Q.; Shan, C.; Hu, Y.; Hemmings, B. A.; Gao, X.; Yang, Z. Deletion of Akt1 causes heart defects and abnormal cardiomyocyte proliferation Dev. Biol. 2010, 347, 384-391
44. Matsui, T.; Li, L.; Wu, J. C.; Cook, S. A.; Nagoshi, T.; Picard, M. H.; Liao, R.; Rosenzweig, A. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart J. Biol. Chem. 2002, 277, 22896-22901
45. Bindea, G.; Mlecnik, B.; Hackl, H.; Charoentong, P.; Tosolini, M.; Kirilovsky, A.; Fridman, W. H.; Pages, F.; Trajanoski, Z.; Galon, J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks Bioinformatics 2009, 25, 1091-1093
46. Zhang, B.; Kirov, S.; Snoddy, J. WebGestalt: an integrated system for exploring gene sets in various biological contexts Nucleic Acids Res. 2005, 33, W741-W748
47. Bindea, G.; Galon, J.; Mlecnik, B. CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data Bioinformatics 2013, 29 (5) 661-663