Divide and Conquer: The application of organelle proteomics to heart failure

Circulation Research

Volumn 108, Issue 4, 2011, Pages 512-526

  Agnetti, Giulio ^a,b   Husberg, Cathrine ^a,c   Van Eyk, Jennifer E ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

Author keywords

communication; heart failure; organelle; posttranslational modifications; proteomics

Indexed keywords

PROTEOME;

BIOINFORMATICS; CELL COMMUNICATION; CELL FRACTIONATION; CELL FUNCTION; CELL ORGANELLE; GEL ELECTROPHORESIS; HEART FAILURE; HUMAN; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN TARGETING; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; SARCOMERE; SARCOPLASMIC RETICULUM; SEPARATION TECHNIQUE;

ANIMALS; ENERGY METABOLISM; HEART FAILURE; HUMANS; ORGANELLES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 79952057976     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.226910     Document Type: Review

References (167)

1. Diwan A, Dorn GW II. Decompensation of cardiac hypertrophy: cellular mechanisms and novel therapeutic targets. Physiology (Bethesda). 2007;22:56-64.
2. Houser SR, Margulies KB. Is depressed myocyte contractility centrally involved in heart failure? Circ Res. 2003;92:350-358.
3. Lehnart SE, Maier LS, Hasenfuss G. Abnormalities of calcium metabolism and myocardial contractility depression in the failing heart. Heart Fail Rev. 2009;14:213-224.
4. Rosca MG, Hoppel CL. Mitochondria in heart failure. Cardiovasc Res. 2010;88:40-50.
5. Capetanaki Y. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med. 2002;12:339-348. (Pubitemid 36092124)
6. Kaasik A, Veksler V, Boehm E, Novotova M, Minajeva A, Ventura- Clapier R. Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res. 2001;89:153-159. (Pubitemid 34135823)
7. Louch WE, Sejersted OM, Swift F. There goes the neighborhood: pathological alterations in T-tubule morphology and consequences for cardiomyocyte Ca2+ handling. J Biomed Biotechnol. 2010;2010:503906.
8. Dhalla NS, Saini-Chohan HK, Rodriguez-Leyva D, Elimban V, Dent MR, Tappia PS. Subcellular remodelling may induce cardiac dysfunction in congestive heart failure. Cardiovasc Res. 2009;81:429-438.
9. Periasamy M, Bhupathy P, Babu GJ. Regulation of sarcoplasmic reticulum Ca2+ ATPase pump expression and its relevance to cardiac muscle physiology and pathology. Cardiovasc Res. 2008;77:265-273. (Pubitemid 351197644)
10. Hamdani N, Kooij V, van Dijk S, Merkus D, Paulus WJ, Remedios CD, Duncker DJ, Stienen GJ, van der Velden J. Sarcomeric dysfunction in heart failure. Cardiovasc Res. 2008;77:649-658. (Pubitemid 351301859)
11. El-Armouche A, Eschenhagen T. Beta-adrenergic stimulation and myocardial function in the failing heart. Heart Fail Rev. 2009;14:225-241.
12. Hein S, Kostin S, Heling A, Maeno Y, Schaper J. The role of the cytoskeleton in heart failure. Cardiovasc Res. 2000;45:273-278. (Pubitemid 30069492)
13. Kueh HY, Mitchison TJ. Structural plasticity in actin and tubulin polymer dynamics. Science. 2009;325:960-963.
14. Leach RN, Desai JC, Orchard CH. Effect of cytoskeleton disruptors on L-type ca channel distribution in rat ventricular myocytes. Cell Calcium. 2005;38:515-526. (Pubitemid 41403668)
15. Capetanaki Y, Bloch RJ, Kouloumenta A, Mavroidis M, Psarras S. Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res. 2007;313:2063-2076. (Pubitemid 46842980)
16. Hollrigl A, Hofner M, Stary M, Weitzer G. Differentiation of cardiomyocytes requires functional serine residues within the amino-terminal domain of desmin. Differentiation. 2007;75:616-626. (Pubitemid 47301599)
17. Tannous P, Zhu H, Johnstone JL, Shelton JM, Rajasekaran NS, Benjamin IJ, Nguyen L, Gerard RD, Levine B, Rothermel BA, Hill JA. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci U S A. 2008;105:9745-9750. (Pubitemid 352031371)
18. Kim S, Coulombe PA. Emerging role for the cytoskeleton as an organizer and regulator of translation. Nat Rev Mol Cell Biol. 2010;11:75-81.
19. Saffitz JE. Adhesion molecules: why they are important to the electro-physiologist. J Cardiovasc Electrophysiol. 2006;17:225-229. (Pubitemid 43344879)
20. Wasinger VC, Cordwell SJ, Cerpa-Poljak A, Yan JX, Gooley AA, Wilkins MR, Duncan MW, Harris R, Williams KL, Humphery-Smith I. Progress with gene-product mapping of the mollicutes: mycoplasma genitalium. Electrophoresis. 1995;16:1090-1094.
21. Hu P, Shimoji S, Hart GW. Site-specific interplay between O-GlcNAcylation and phosphorylation in cellular regulation. FEBS Lett. 2010;584:2526-2538.
22. Forner F, Foster LJ, Campanaro S, Valle G, Mann M. Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver. Mol Cell Proteomics. 2006;5:608-619.
23. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK. A mitochondrial protein compendium elucidates complex I disease biology. Cell. 2008;134:112-123. (Pubitemid 351916708)
24. Gomes AV, Venkatraman G, Davis JP, Tikunova SB, Engel P, Solaro RJ, Potter JD. Cardiac troponin T isoforms affect the Ca(2+) sensitivity of force development in the presence of slow skeletal troponin I: insights into the role of troponin T isoforms in the fetal heart. J Biol Chem. 2004;279:49579-49587.
25. Gorg A, Drews O, Luck C, Weiland F, Weiss W. 2-DE with IPGs. Electrophoresis. 2009;30(Suppl 1):S122-S132.
26. Righetti PG. Electrophoresis: the march of pennies, the march of dimes. J Chromatogr A. 2005;1079:24-40. (Pubitemid 40813185)
27. Wells L, Hart GW. O-GlcNAc turns twenty: functional implications for post-translational modification of nuclear and cytosolic proteins with a sugar. FEBS Lett. 2003;546:154-158. (Pubitemid 36782297)
28. Zachara NE. Detecting the "O-GlcNAc-ome"; detection, purification, and analysis of O-GlcNAc modified proteins. Methods Mol Biol. 2009;534:251-279.
29. Nita-Lazar A, Saito-Benz H, White FM. Quantitative phosphoproteomics by mass spectrometry: past, present, and future. Proteomics. 2008;8:4433-4443.
30. Lemeer S, Heck AJ. The phosphoproteomics data explosion. Curr Opin Chem Biol. 2009;13:414-420.
31. Grimsrud PA, Swaney DL, Wenger CD, Beauchene NA, Coon JJ. Phosphoproteomics for the masses. ACS Chem Biol. 2010;5:105-119.
32. Edwards AV, White MY, Cordwell SJ. The role of proteomics in clinical cardiovascular biomarker discovery. Mol Cell Proteomics. 2008;7:1824-1837.
33. Ping P. Getting to the heart of proteomics. N Engl J Med. 2009;360:532-534.
34. Didangelos A, Simper D, Monaco C, Mayr M. Proteomics of acute coronary syndromes. Curr Atheroscler Rep. 2009;11:188-195.
35. Agnetti G, Kane LA, Guarnieri C, Caldarera CM, Van Eyk JE. Proteomic technologies in the study of kinases: novel tools for the investigation of PKC in the heart. Pharmacol Res. 2007;55:511-522. (Pubitemid 46962311)
36. Faber MJ, Agnetti G, Bezstarosti K, Lankhuizen IM, Dalinghaus M, Guarnieri C, Caldarera CM, Helbing WA, Lamers JM. Recent developments in proteomics: implications for the study of cardiac hypertrophy and failure. Cell Biochem Biophys. 2006;44:11-29. (Pubitemid 43099568)
37. Schoenhoff FS, Fu Q, Van Eyk JE. Cardiovascular proteomics: implications for clinical applications. Clin Lab Med. 2009;29:87-99.
38. Leach C, Shenolikar S, Brautigan DL. Phosphorylation of phosphatase inhibitor-2 at centrosomes during mitosis. J Biol Chem. 2003;278:26015-26020. (Pubitemid 36835368)
39. Bisetto E, Di Pancrazio F, Simula MP, Mavelli I, Lippe G. Mammalian ATPsynthase monomer versus dimer profiled by blue native PAGE and activity stain. Electrophoresis. 2007;28:3178-3185. (Pubitemid 47506446)
40. Neverova I, Van Eyk JE. Role of chromatographic techniques in proteomic analysis. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;815:51-63. (Pubitemid 40136519)
41. Forrester MT, Foster MW, Stamler JS. Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J Biol Chem. 2007;282:13977- 13983. (Pubitemid 47100466)
42. Lopez-Sanchez LM, Muntane J, de la Mata M, Rodriguez-Ariza A. Unraveling the S-nitrosoproteome: tools and strategies. Proteomics. 2009;9:808-818.
43. O'Farrell PH. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975;250:4007-4021.
44. Bjellqvist B, Ek K, Righetti PG, Gianazza E, Gorg A, Westermeier R, Postel W. Isoelectric focusing in immobilized pH gradients: principle, methodology and some applications. J Biochem Biophys Methods. 1982;6:317-339.
45. Unlu M, Morgan ME, Minden JS. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis. 1997;18:2071-2077. (Pubitemid 27501267)
46. Gianazza E, Righetti PG. Immobilized pH gradients. Electrophoresis. 2009;30(Suppl 1):S112-S121.
47. Halligan BD, Ruotti V, Jin W, Laffoon S, Twigger SN, Dratz EA. ProMoST (protein modification screening tool): a web-based tool for mapping protein modifications on two-dimensional gels. Nucleic Acids Res. 2004;32:W638-W644. (Pubitemid 38997414)
48. Shirai A, Matsuyama A, Yashiroda Y, Hashimoto A, Kawamura Y, Arai R, Komatsu Y, Horinouchi S, Yoshida M. Global analysis of gel mobility of proteins and its use in target identification. J Biol Chem. 2008;283:10745-10752.
49. Dorfleutner A, Cho Y, Vincent D, Cunnick J, Lin H, Weed SA, Stehlik C, Flynn DC. Phosphorylation of AFAP-110 affects podosome lifespan in A7r5 cells. J Cell Sci. 2008;121:2394-2405.
50. Burre J, Wittig I, Schagger H. Non-classical 2-D electrophoresis. Methods Mol Biol. 2009;564:33-57.
51. Knoll R, Kostin S, Klede S, Savvatis K, Klinge L, Stehle I, Gunkel S, Kotter S, Babicz K, Sohns M, Miocic S, Didie M, Knoll G, Zimmermann WH, Thelen P, Bickeboller H, Maier LS, Schaper W, Schaper J, Kraft T, Tschope C, Linke WA, Chien KR. A common MLP (muscle LIM protein) variant is associated with cardiomyopathy. Circ Res. 2010;106:695-704.
52. Miyagi M, Rao KC. Proteolytic 18O-labeling strategies for quantitative proteomics. Mass Spectrom Rev. 2007;26:121-136. (Pubitemid 46061256)
53. Righetti PG, Sebastiano R, Citterio A. Isotope-coded two-dimensional maps: tagging with deuterated acrylamide and 2-vinylpyridine. Methods Mol Biol. 2008;424:87-99.
54. Friedman DB. Quantitative proteomics for two-dimensional gels using difference gel electrophoresis. Methods Mol Biol. 2007;367:219-239.
55. Santoni V, Molloy M, Rabilloud T. Membrane proteins and proteomics: un amour impossible? Electrophoresis. 2000;21:1054-1070.
56. Rabilloud T. Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis. 2009;30(Suppl 1):S174-S180.
57. Kane LA, Yung CK, Agnetti G, Neverova I, Van Eyk JE. Optimization of paper bridge loading for 2-DE analysis in the basic pH region: application to the mitochondrial subproteome. Proteomics. 2006;6:5683-5687. (Pubitemid 44764005)
58. Agnetti G, Kaludercic N, Kane LA, Elliott ST, Guo Y, Chakir K, Samantapudi D, Paolocci N, Tomaselli GF, Kass DA, Van Eyk JE. Modulation of mitochondrial proteome and improved mitochondrial function by biventricular pacing of dyssynchronous failing hearts. Circ Cardiovasc Genet. 2010;3:78-87.
59. Horvatovich P, Hoekman B, Govorukhina N, Bischoff R. Multidimensional chromatography coupled to mass spectrometry in analysing complex proteomics samples. J Sep Sci. 2010;33:1421-1437.
60. Sandra K, Moshir M, D'hondt F, Tuytten R, Verleysen K, Kas K, Francois I, Sandra P. Highly efficient peptide separations in proteomics. part 2: bi- and multidimensional liquid-based separation techniques. J Chromatogr B Analyt Technol Biomed Life Sci. 2009;877:1019-1039.
61. Zhang X, Fang A, Riley CP, Wang M, Regnier FE, Buck C. Multidimensional liquid chromatography in proteomics-a review. Anal Chim Acta. 2010;664:101-113.
62. Shen H, Li X, Bieberich CJ, Frey DD. Reducing sample complexity in proteomics by chromatofocusing with simple buffer mixtures. Methods Mol Biol. 2008;424:187-203.
63. Yates JR, Ruse CI, Nakorchevsky A. Proteomics by mass spectrometry: approaches, advances, and applications. Annu Rev Biomed Eng. 2009;11:49-79.
64. Motoyama A, Yates JR III. Multidimensional LC separations in shotgun proteomics. Anal Chem. 2008;80:7187-7193.
65. Chong BE, Yan F, Lubman DM, Miller FR. Chromatofocusing nonporous reversed-phase high-performance liquid chromatography/ electrospray ionization time-of-flight mass spectrometry of proteins from human breast cancer whole cell lysates: a novel two-dimensional liquid chromatography/mass spectrometry method. Rapid Commun Mass Spectrom. 2001;15:291-296. (Pubitemid 32201564)
66. Sheng S, Chen D, Van Eyk JE. Multidimensional liquid chromatography separation of intact proteins by chromatographic focusing and reversed phase of the human serum proteome: optimization and protein database. Mol Cell Proteomics. 2006;5:26-34. (Pubitemid 43169337)
67. Gundry RL, Tchernyshyov I, Sheng S, Tarasova Y, Raginski K, Boheler KR, Van Eyk JE. Expanding the mouse embryonic stem cell proteome: combining three proteomic approaches. Proteomics. 2010;10:2728-2732.
68. Wingren C, James P, Borrebaeck CA. Strategy for surveying the proteome using affinity proteomics and mass spectrometry. Proteomics. 2009;9:1511-1517.
69. Uhlen M. Affinity as a tool in life science. BioTechniques. 2008;44:649-654. (Pubitemid 351656284)
70. Forner F, Furlan S, Salvatori S. Mass spectrometry analysis of complexes formed by myotonic dystrophy protein kinase (DMPK). Biochim Biophys Acta. 2010;1804:1334-1341.
71. Gundry RL, White MY, Murray CI, Kane LA, Fu Q, Stanley BA, Van Eyk JE. Preparation of proteins and peptides for mass spectrometry analysis in a bottom-up proteomics workflow. Curr Protoc Mol Biol. 2009;Chapter 10:Unit10.25.
72. Fu Z, Wang M, Gucek M, Zhang J, Wu J, Jiang L, Monticone RE, Khazan B, Telljohann R, Mattison J, Sheng S, Cole RN, Spinetti G, Pintus G, Liu L, Kolodgie FD, Virmani R, Spurgeon H, Ingram DK, Everett AD, Lakatta EG, Van Eyk JE. Milk fat globule protein epidermal growth factor-8: a pivotal relay element within the angiotensin II and monocyte chemoattractant protein-1 signaling cascade mediating vascular smooth muscle cells invasion. Circ Res. 2009;104:1337-1346.
73. Liska AJ, Shevchenko A. Expanding the organismal scope of proteomics: cross-species protein identification by mass spectrometry and its implications. Proteomics. 2003;3:19-28. (Pubitemid 36151064)
74. Wright JC, Beynon RJ, Hubbard SJ. Cross species proteomics. Methods Mol Biol. 2010;604:123-135.
75. Zhou M, Veenstra T. Mass spectrometry: m/z 1983-2008. BioTechniques. 2008;44:667-668.
76. Tabet JC, Rebuffat S. Nobel prize 2002 for chemistry: mass spectrometry and nuclear magnetic resonance. Med Sci (Paris). 2003;19:865-872.
77. Pisitkun T, Hoffert JD, Yu MJ, Knepper MA. Tandem mass spectrometry in physiology. Physiology (Bethesda). 2007;22:390-400.
78. Raczynska ED, Gal JF, Maria PC, Zientara K, Szelag M. Application of FT-ICR-MS for the study of proton-transfer reactions involving biomolecules. Anal Bioanal Chem. 2007;389:1365-1380. (Pubitemid 350023662)
79. Siuti N, Kelleher NL. Decoding protein modifications using top-down mass spectrometry. Nat Methods. 2007;4:817-821. (Pubitemid 350055578)
80. Linscheid MW, Ahrends R, Pieper S, Kuhn A. Liquid chromatography- mass spectrometry-based quantitative proteomics. Methods Mol Biol. 2009;564:189-205.
81. Wang M, You J, Bemis KG, Tegeler TJ, Brown DP. Label-free mass spectrometry-based protein quantification technologies in proteomic analysis. Brief Funct Genomic Proteomic. 2008;7:329-339.
82. Aye TT, Scholten A, Taouatas N, Varro A, Van Veen TA, Vos MA, Heck AJ. Proteome-wide protein concentrations in the human heart. Mol Biosyst. 2010;6:1917-1927.
83. Kline KG, Sussman MR. Protein quantitation using isotope-assisted mass spectrometry. Annu Rev Biophys. 2010;39:291-308.
84. Ong SE, Foster LJ, Mann M. Mass spectrometric-based approaches in quantitative proteomics. Methods. 2003;29:124-130. (Pubitemid 36269199)
85. Coppinger JA, Cagney G, Toomey S, Kislinger T, Belton O, McRedmond JP, Cahill DJ, Emili A, Fitzgerald DJ, Maguire PB. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood. 2004;103:2096-2104. (Pubitemid 38326225)
86. Wiese S, Reidegeld KA, Meyer HE, Warscheid B. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics. 2007;7:340-350. (Pubitemid 46293976)
87. Yocum AK, Chinnaiyan AM. Current affairs in quantitative targeted proteomics: multiple reaction monitoring-mass spectrometry. Brief Funct Genomic Proteomic. 2009;8:145-157.
88. Cox DM, Zhong F, Du M, Duchoslav E, Sakuma T, McDermott JC. Multiple reaction monitoring as a method for identifying protein post-translational modifications. J Biomol Tech. 2005;16:83-90.
89. Domanski D, Murphy LC, Borchers CH. Assay development for the determination of phosphorylation stoichiometry using multiple reaction monitoring methods with and without phosphatase treatment: application to breast cancer signaling pathways. Anal Chem. 2010;82:5610-5620.
90. Blackburn K, Goshe MB. Challenges and strategies for targeted phosphorylation site identification and quantification using mass spectrometry analysis. Brief Funct Genomic Proteomic. 2009;8:90-103.
91. Boersema PJ, Mohammed S, Heck AJ. Phosphopeptide fragmentation and analysis by mass spectrometry. J Mass Spectrom. 2009;44:861-878.
92. Paradela A, Albar JP. Advances in the analysis of protein phosphorylation. J Proteome Res. 2008;7:1809-1818.
93. Rogers LD, Foster LJ. Phosphoproteomics-finally fulfilling the promise? Mol Biosyst. 2009;5:1122-1129.
94. Thingholm TE, Larsen MR. The use of titanium dioxide micro-columns to selectively isolate phosphopeptides from proteolytic digests. Methods Mol Biol. 2009;527:57-66, xi.
95. Block H, Maertens B, Spriestersbach A, Brinker N, Kubicek J, Fabis R, Labahn J, Schafer F. Immobilized-metal affinity chromatography (IMAC): a review. Methods Enzymol. 2009;463:439-473.
96. Gevaert K, Vandekerckhove J. Reverse-phase diagonal chromatography for phosphoproteome research. Methods Mol Biol. 2009;527:219-227.
97. McNulty DE, Annan RS. Hydrophilic interaction chromatography for fractionation and enrichment of the phosphoproteome. Methods Mol Biol. 2009;527:93-105.
98. Witze ES, Old WM, Resing KA, Ahn NG. Mapping protein post-translational modifications with mass spectrometry. Nat Methods. 2007;4:798-806. (Pubitemid 350055576)
99. Deutsch EW, Mendoza L, Shteynberg D, Farrah T, Lam H, Tasman N, Sun Z, Nilsson E, Pratt B, Prazen B, Eng JK, Martin DB, Nesvizhskii AI, Aebersold R. A guided tour of the trans-proteomic pipeline. Proteomics. 2010;10:1150-1159.
100. Creasy DM, Cottrell JS. Error tolerant searching of uninterpreted tandem mass spectrometry data. Proteomics. 2002;2:1426-1434. (Pubitemid 35340023)
101. Bell AW, Deutsch EW, Au CE, Kearney RE, Beavis R, Sechi S, Nilsson T, Bergeron JJ, HUPO Test Sample Working Group. A HUPO test sample study reveals common problems in mass spectrometry-based proteomics. Nat Methods. 2009;6:423-430.
102. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415:198-205. (Pubitemid 34059525)
103. Babu GJ, Wheeler D, Alzate O, Periasamy M. Solubilization of membrane proteins for two-dimensional gel electrophoresis: identification of sarcoplasmic reticulum membrane proteins. Anal Biochem. 2004;325:121-125. (Pubitemid 38050274)
104. Helbig AO, Heck AJ, Slijper M. Exploring the membrane proteome- challenges and analytical strategies. J Proteomics. 2010;73:868-878.
105. Donoghue PM, Hughes C, Vissers JP, Langridge JI, Dunn MJ. Nonionic detergent phase extraction for the proteomic analysis of heart membrane proteins using label-free LC-MS. Proteomics. 2008;8:3895-3905.
106. Pan Y, Kislinger T, Gramolini AO, Zvaritch E, Kranias EG, MacLennan DH, Emili A. Identification of biochemical adaptations in hyper- or hypocontractile hearts from phospholamban mutant mice by expression proteomics. Proc Natl Acad Sci U S A. 2004;101:2241-2246. (Pubitemid 38269296)
107. Andersson KB, Birkeland JA, Finsen AV, Louch WE, Sjaastad I, Wang Y, Chen J, Molkentin JD, Chien KR, Sejersted OM, Christensen G. Moderate heart dysfunction in mice with inducible cardiomyocyte-specific excision of the Serca2 gene. J Mol Cell Cardiol. 2009;47:180-187.
108. Haghighi K, Gregory KN, Kranias EG. Sarcoplasmic reticulum ca-ATPase-phospholamban interactions and dilated cardiomyopathy. Biochem Biophys Res Commun. 2004;322:1214-1222. (Pubitemid 39164651)
109. Pan C, Olsen JV, Daub H, Mann M. Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics. Mol Cell Proteomics. 2009;8:2796-2808.
110. Husberg C, Agnetti G, Nygaard S, Andersson KB, Christensen G, Van Eyk J. Abstract 2944: activation of heat shock proteins and shifts in cytoskeleton composition in a cardiac-specific SERCA2 KO mouse. Circulation. 2009;120:S717.
111. Solaro RJ, Sheehan KA, Lei M, Ke Y. The curious role of sarcomeric proteins in control of diverse processes in cardiac myocytes. J Gen Physiol. 2010;136:13-19.
112. Morimoto S. Sarcomeric proteins and inherited cardiomyopathies. Cardiovasc Res. 2008;77:659-666. (Pubitemid 351301864)
113. Metzger JM, Westfall MV. Covalent and noncovalent modification of thin filament action: the essential role of troponin in cardiac muscle regulation. Circ Res. 2004;94:146-158. (Pubitemid 38197446)
114. Solaro RJ, Rosevear P, Kobayashi T. The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation. Biochem Biophys Res Commun. 2008;369:82-87.
115. Solaro RJ, van der Velden J. Why does troponin I have so many phosphorylation sites? fact and fancy. J Mol Cell Cardiol. 2010;48:810-816.
116. Ayaz-Guner S, Zhang J, Li L, Walker JW, Ge Y. In vivo phosphorylation site mapping in mouse cardiac troponin I by high resolution top-down electron capture dissociation mass spectrometry: Ser22/23 are the only sites basally phosphorylated. Biochemistry. 2009;48:8161-8170.
117. Torres CR, Hart GW. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. evidence for O-linked GlcNAc. J Biol Chem. 1984;259:3308-3317. (Pubitemid 14130544)
118. Ramirez-Correa GA, Jin W, Wang Z, Zhong X, Gao WD, Dias WB, Vecoli C, Hart GW, Murphy AM. O-linked GlcNAc modification of cardiac myofilament proteins: a novel regulator of myocardial contractile function. Circ Res. 2008;103:1354-1358.
119. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med. 2007;356:1140-1151. (Pubitemid 46425598)
120. Lopaschuk GD, Rebeyka IM, Allard MF. Metabolic modulation: a means to mend a broken heart. Circulation. 2002;105:140-142. (Pubitemid 34084307)
121. Neubert D, Wojtczak AB, Lehninger AL. Purification and enzymatic identity of mitochondrial contraction-factors I and II. Proc Natl Acad Sci U S A. 1962;48:1651-1658.
122. Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, Murphy AN, Gaucher SP, Capaldi RA, Gibson BW, Ghosh SS. Characterization of the human heart mitochondrial proteome. Nat Biotechnol. 2003;21:281-286.
123. Elstner M, Andreoli C, Ahting U, Tetko I, Klopstock T, Meitinger T, Prokisch H. MitoP2: an integrative tool for the analysis of the mitochondrial proteome. Mol Biotechnol. 2008;40:306-315.
124. Schwartz R, Ting CS, King J. Whole proteome pI values correlate with subcellular localizations of proteins for organisms within the three domains of life. Genome Res. 2001;11:703-709. (Pubitemid 32447858)
125. Kavazis AN, Alvarez S, Talbert E, Lee Y, Powers SK. Exercise training induces a cardioprotective phenotype and alterations in cardiac subsarcolemmal and intermyofibrillar mitochondrial proteins. Am J Physiol Heart Circ Physiol. 2009;297:H144-52.
126. Rich PR. The molecular machinery of keilin's respiratory chain. Biochem Soc Trans. 2003;31:1095-1105. (Pubitemid 38030918)
127. Fearnley IM, Carroll J, Walker JE. Proteomic analysis of the subunit composition of complex I (NADH:Ubiquinone oxidoreductase) from bovine heart mitochondria. Methods Mol Biol. 2007;357:103-125. (Pubitemid 350183242)
128. Schilling B, Murray J, Yoo CB, Row RH, Cusack MP, Capaldi RA, Gibson BW. Proteomic analysis of succinate dehydrogenase and ubiquinol-cytochrome c reductase (complex II and III) isolated by immunoprecipitation from bovine and mouse heart mitochondria. Biochim Biophys Acta. 2006;1762:213-222. (Pubitemid 43006027)
129. Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J, Walker JE. Bovine complex I is a complex of 45 different subunits. J Biol Chem. 2006;281:32724-32727. (Pubitemid 46036828)
130. Palmisano G, Sardanelli AM, Signorile A, Papa S, Larsen MR. The phosphorylation pattern of bovine heart complex I subunits. Proteomics. 2007;7:1575-1583. (Pubitemid 46841820)
131. Pocsfalvi G, Cuccurullo M, Schlosser G, Scacco S, Papa S, Malorni A. Phosphorylation of B14.5a subunit from bovine heart complex I identified by titanium dioxide selective enrichment and shotgun proteomics. Mol Cell Proteomics. 2007;6:231-237. (Pubitemid 46359512)
132. Gottlieb RA. Identification of targets of phosphorylation in heart mitochondria. Methods Mol Biol. 2007;357:127-137. (Pubitemid 350183243)
133. Kane LA, Youngman MJ, Jensen RE, Van Eyk JE. Phosphorylation of the F(1)F(o) ATP synthase beta subunit: functional and structural consequences assessed in a model system. Circ Res. 2010;106:504-513.
134. Deng N, Zhang J, Zong C, Wang Y, Lu H, Yang P, Wang W, Young GW, Wang Y, Korge P, Lotz C, Doran P, Liem DA, Apweiler R, Weiss JN, Duan H, Ping P. Phosphoproteome analysis reveals regulatory sites in major pathways of cardiac mitochondria. Mol Cell Proteomics. 2010.
135. McDonald T, Sheng S, Stanley B, Chen D, Ko Y, Cole RN, Pedersen P, Van Eyk JE. 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. (Pubitemid 46040643)
136. McDonald TG, Van Eyk JE. Mitochondrial proteomics. undercover in the lipid bilayer. Basic Res Cardiol. 2003;98:219-227. (Pubitemid 36874020)
137. Distler AM, Kerner J, Hoppel CL. Proteomics of mitochondrial inner and outer membranes. Proteomics. 2008;8:4066-4082.
138. Lukyanenko V, Chikando A, Lederer WJ. Mitochondria in cardiomyocyte Ca2+ signaling. Int J Biochem Cell Biol. 2009;41:1957-1971.
139. Mudd JO, Kass DA. Tackling heart failure in the twenty-first century. Nature. 2008;451:919-928.
140. Fiedler B, Wollert KC. Interference of antihypertrophic molecules and signaling pathways with the Ca2+-calcineurin-NFAT cascade in cardiac myocytes. Cardiovasc Res. 2004;63:450-457. (Pubitemid 38970189)
141. Lima B, Forrester MT, Hess DT, Stamler JS. S-nitrosylation in cardiovascular signaling. Circ Res. 2010;106:633-646.
142. Gonzalez DR, Treuer AV, Castellanos J, Dulce RA, Hare JM. Impaired S-nitrosylation of the ryanodine receptor due to xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem. 2010.
143. Feil R, Lohmann SM, de Jonge H, Walter U, Hofmann F. Cyclic GMP-dependent protein kinases and the cardiovascular system: insights from genetically modified mice. Circ Res. 2003;93:907-916. (Pubitemid 37433228)
144. Lee DI, Vahebi S, Tocchetti CG, Barouch LA, Solaro RJ, Takimoto E, Kass DA. PDE5A suppression of acute beta-adrenergic activation requires modulation of myocyte beta-3 signaling coupled to PKG-mediated troponin I phosphorylation. Basic Res Cardiol. 2010;105:337-347.
145. Burley DS, Ferdinandy P, Baxter GF. Cyclic GMP and protein kinase-G in myocardial ischaemia-reperfusion: opportunities and obstacles for survival signaling. Br J Pharmacol. 2007;152:855-869. (Pubitemid 350100488)
146. Grimm M, Brown JH. Beta-adrenergic receptor signaling in the heart: role of CaMKII. J Mol Cell Cardiol. 2010;48:322-330.
147. Nediani C, Raimondi L, Borchi E, Cerbai E. No/ros generation and Nitroso/redox imbalance in heart failure: from molecular mechanisms to therapeutic implications. Antioxid Redox Signal. 2010.
148. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal. 2010;3:ra3.
149. Choudhary C, Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol. 2010;11:427-439.
150. Goldfarb LG, Dalakas MC. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest. 2009;119:1806-1813.
151. Francalanci P, Gallo P, Bernucci P, Silver MD, d'Amati G. The pattern of desmin filaments in myocardial disarray. Hum Pathol. 1995;26:262-266.
152. Gard JJ, Yamada K, Green KG, Eloff BC, Rosenbaum DS, Wang X, Robbins J, Schuessler RB, Yamada KA, Saffitz JE. Remodeling of gap junctions and slow conduction in a mouse model of desmin-related cardiomyopathy. Cardiovasc Res. 2005;67:539-547. (Pubitemid 41019561)
153. Maloyan A, Gulick J, Glabe CG, Kayed R, Robbins J. Exercise reverses preamyloid oligomer and prolongs survival in {alpha}B-crystallin-based desmin-related cardiomyopathy. Proc Natl Acad Sci U S A. 2007;104:5995-6000. (Pubitemid 47175647)
154. Otten E, Asimaki A, Maass A, van Langen IM, Wal AV, de Jonge N, van den Berg MP, Saffitz JE, Wilde AA, Jongbloed JD, van Tintelen JP. Desmin mutations as a cause of right ventricular heart failure affect the intercalated disks. Heart Rhythm. 2010.
155. Agnetti G, Bezstarosti K, Dekkers DH, Verhoeven AJ, Giordano E, Guarnieri C, Caldarera CM, Van Eyk JE, Lamers JM. Proteomic profiling of endothelin-1-stimulated hypertrophic cardiomyocytes reveals the increase of four different desmin species and alpha-B-crystallin. Biochim Biophys Acta. 2008;1784:1068-1076.
156. Panagopoulou P, Davos CH, Milner DJ, Varela E, Cameron J, Mann DL, Capetanaki Y. Desmin mediates TNF-alpha-induced aggregate formation and intercalated disk reorganization in heart failure. J Cell Biol. 2008;181:761-775. (Pubitemid 351786982)
157. Agnetti G, Halperin-Kuhns V, Guo Y, Sheng S, Fu Z, Nicolini F, Gherli T, Guarnieri C, Caldarera CM, Kass DA, Tomaselli GF, Van Eyk JE. Abstract 1809: novel human and canine desmin phosphorylations as potential regulators of oligomer formation and disease in heart failure. Circulation. 2009;120:S559-c.
158. Faber MJ, Dalinghaus M, Lankhuizen IM, Bezstarosti K, Dekkers DH, Duncker DJ, Helbing WA, Lamers JM. Proteomic changes in the pressure overloaded right ventricle after 6 weeks in young rats: correlations with the degree of hypertrophy. Proteomics. 2005;5:2519-2530. (Pubitemid 40966479)
159. Huang X, Li J, Foster D, Lemanski SL, Dube DK, Zhang C, Lemanski LF. Protein kinase C-mediated desmin phosphorylation is related to myofibril disarray in cardiomyopathic hamster heart. Exp Biol Med (Maywood). 2002;227:1039-1046. (Pubitemid 36008313)
160. Corbett JM, Why HJ, Wheeler CH, Richardson PJ, Archard LC, Yacoub MH, Dunn MJ. Cardiac protein abnormalities in dilated cardiomyopathy detected by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis. 1998;19:2031-2042. (Pubitemid 28392250)
161. Rappaport L, Contard F, Samuel JL, Delcayre C, Marotte F, Tome F, Fardeau M. Storage of phosphorylated desmin in a familial myopathy. FEBS Lett. 1988;231:421-425.
162. Bar H, Goudeau B, Walde S, Casteras-Simon M, Mucke N, Shatunov A, Goldberg YP, Clarke C, Holton JL, Eymard B, Katus HA, Fardeau M, Goldfarb L, Vicart P, Herrmann H. Conspicuous involvement of desmin tail mutations in diverse cardiac and skeletal myopathies. Hum Mutat. 2007;28:374-386. (Pubitemid 46542924)
163. Di Somma S, Di Benedetto MP, Salvatore G, Agozzino L, Ferranti F,
164. Heling A, Zimmermann R, Kostin S, Maeno Y, Hein S, Devaux B, Bauer E, Klovekorn WP, Schlepper M, Schaper W, Schaper J. Increased expression of cytoskeletal, linkage, and extracellular proteins in failing human myocardium. Circ Res. 2000;86:846-853. (Pubitemid 30246981)
165. Han G, Ye M, Liu H, Song C, Sun D, Wu Y, Jiang X, Chen R, Wang C, Wang L, Zou H. Phosphoproteome analysis of human liver tissue by long-gradient nanoflow LC coupled with multiple stage MS analysis. Electrophoresis. 2010;31:1080-1089.
166. Nelson WJ, Traub P. Proteolysis of vimentin and desmin by the Ca2+- activated proteinase specific for these intermediate filament proteins. Mol Cell Biol. 1983;3:1146-1156. (Pubitemid 13038523)
167. Inagaki M, Gonda Y, Matsuyama M, Nishizawa K, Nishi Y, Sato C. Intermediate filament reconstitution in vitro. the role of phosphorylation on the assembly-disassembly of desmin. J Biol Chem. 1988;263:5970-5978.