Proteomic technologies in the study of kinases: Novel tools for the investigation of PKC in the heart

Pharmacological Research

Volumn 55, Issue 6, 2007, Pages 511-522

  Agnetti, G ^a,b   Kane, L A ^c   Guarnieri, C ^a   Caldarera, C M ^a   Van Eyk, J E ^b,c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Heart; Mitochondria; PKC; Proteomics

Indexed keywords

CYTOSKELETON PROTEIN; MITOCHONDRIAL PROTEIN; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEIN KINASE C; TITANIUM DIOXIDE;

AFFINITY LABELING; ANTIBODY DETECTION; ANTIBODY LABELING; BIOTECHNOLOGY; CELLULAR DISTRIBUTION; CYTOSKELETON; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; GEL CHROMATOGRAPHY; GEL ELECTROPHORESIS; HEART DISEASE; HEART FAILURE; HEART PROTECTION; HUMAN; HYBRIDIZATION; HYPERTROPHY; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; METABOLIC DISORDER; MITOCHONDRION; MOLECULAR RECOGNITION; MYOFILAMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN QUALITY; PROTEOMICS; REVIEW; SEPARATION TECHNIQUE; STAINING;

ANIMALS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HEART DISEASES; HUMANS; MITOCHONDRIA, HEART; MYOCARDIUM; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS;

EID: 34250708974     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2007.04.012     Document Type: Review

References (98)

1. Wasinger V.C., Cordwell S.J., Cerpa-Poljak A., Yan J.X., Gooley A.A., Wilkins M.R., et al. Progress with gene-product mapping of the Mollicutes: Mycoplasma genitalium. Electrophoresis 16 (1995) 1090-1094
2. Gygi S.P., Rochon Y., Franza B.R., and Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19 (1999) 1720-1730
3. Pandey A., and Mann M. Proteomics to study genes and genomes. Nature 405 (2000) 837-846
4. Neverova I., and Van Eyk J.E. Role of chromatographic techniques in proteomic analysis. J Chromatogr B: Analyt Technol Biomed Life Sci 815 (2005) 51-63
5. O'Donovan C., Apweiler R., and Bairoch A. The human proteomics initiative (HPI). Trends Biotechnol 19 (2001) 178-181
6. Arrell D.K., Neverova I., Fraser H., Marban E., and Van Eyk J.E. Proteomic analysis of pharmacologically preconditioned cardiomyocytes reveals novel phosphorylation of myosin light chain 1. Circ Res 89 (2001) 480-487
7. Arrell D.K., Elliott S.T., Kane L.A., Guo Y., Ko Y.H., Pedersen P.L., et al. Proteomic analysis of pharmacological preconditioning: novel protein targets converge to mitochondrial metabolism pathways. Circ Res 99 (2006) 706-714
8. Yuan C., Guo Y., Ravi R., Przyklenk K., Shilkofski N., Diez R., et al. Myosin binding protein C is differentially phosphorylated upon myocardial stunning in canine and rat hearts-evidence for novel phosphorylation sites. Proteomics 6 (2006) 4176-4186
9. Pawson Tand Nash P. Protein-protein interactions define specificity in signal transduction. Genes Dev 14 (2000) 1027-1047
10. Ping P. Identification of novel signaling complexes by functional proteomics. Circ Res 93 (2003) 595-603
11. Ping P., Zhang J., Pierce Jr. W.M., and Bolli R. Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ Res 88 (2001) 59-62
12. Vondriska T.M., Zhang J., Song C., Tang X.L., Cao X., Baines C.P., et al. Protein kinase C epsilon-Src modules direct signal transduction in nitric oxide-induced cardioprotection: complex formation as a means for cardioprotective signaling. Circ Res 88 (2001) 1306-1313
13. Anderson N.G., Matheson A., and Anderson N.L. Back to the future: the human protein index (HPI) and the agenda for post-proteomic biology. Proteomics 1 (2001) 3-12
14. Guo Y., Ma S.F., Grigoryev D., Van Eyk J., and Garcia J.G. 1DE MS and 2D LC-MS analysis of the mouse bronchoalveolar lavage proteome. Proteomics 5 (2005) 4608-4624
15. McDonald T., Sheng S., Stanley B., Chen D., Ko Y., Cole R.N., et al. 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)
16. O'Farrell P.H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250 (1975) 4007-4021
17. Klose J. Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutations in mammals. Humangenetik 26 (1975) 231-243
18. Scheele G.A. Two-dimensional gel analysis of soluble proteins. Charaterization of guinea pig exocrine pancreatic proteins. J Biol Chem 250 (1975) 5375-5385
19. Bjellqvist B., Pasquali C., Ravier F., Sanchez J.C., and Hochstrasser D. A nonlinear wide-range immobilized pH gradient for two-dimensional electrophoresis and its definition in a relevant pH scale. Electrophoresis 14 (1993) 1357-1365
20. Gorg A., Obermaier C., Boguth G., Harder A., Scheibe B., Wildgruber R., et al. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21 (2000) 1037-1053
21. Westbrook J.A., Wheeler J.X., Wait R., Welson S.Y., and Dunn M.J. The human heart proteome: two-dimensional maps using narrow-range immobilised pH gradients. Electrophoresis 27 (2006) 1547-1555
22. Faber M.J., Agnetti G., Bezstarosti K., Lankhuizen I.M., Dalinghaus M., Guarnieri C., et al. Recent developments in proteomics: implications for the study of cardiac hypertrophy and failure. Cell Biochem Biophys 44 (2006) 11-29
23. Santoni V., Molloy M., and Rabilloud T. Membrane proteins and proteomics: un amour impossible?. Electrophoresis 21 (2000) 1054-1070
24. Kane L.A., Yung C.K., Agnetti G., Neverova I., and Van Eyk J.E. Optimization of paper bridge loading for 2-DE analysis in the basic pH region: application to the mitochondrial subproteome. Proteomics (2006)
25. Rabilloud T. Solubilization of proteins for electrophoretic analyses. Electrophoresis 17 (1996) 813-829
26. Luche S., Santoni V., and Rabilloud T. Evaluation of nonionic and zwitterionic detergents as membrane protein solubilizers in two-dimensional electrophoresis. Proteomics 3 (2003) 249-253
27. Graham D.R., Garnham C.P., Fu Q., Robbins J., and Van Eyk J.E. Improvements in two-dimensional gel electrophoresis by utilizing a low cost "in-house" neutral pH sodium dodecyl sulfate-polyacrylamide gel electrophoresis system. Proteomics 5 (2005) 2309-2314
28. Neuhoff V., Stamm R., Pardowitz I., Arold N., Ehrhardt W., and Taube D. Essential problems in quantification of proteins following colloidal staining with coomassie brilliant blue dyes in polyacrylamide gels, and their solution. Electrophoresis 11 (1990) 101-117
29. Switzer III R.C., Merril C.R., and Shifrin S. A highly sensitive silver stain for detecting proteins and peptides in polyacrylamide gels. Anal Biochem 98 (1979) 231-237
30. Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., et al. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25 (2004) 1327-1333
31. Chevallet M., Diemer H., Luche S., van Dorsselaer A., Rabilloud T., and Leize-Wagner E. Improved mass spectrometry compatibility is afforded by ammoniacal silver staining. Proteomics 6 (2006) 2350-2354
32. Gharbi S., Gaffney P., Yang A., Zvelebil M.J., Cramer R., Waterfield M.D., et al. Evaluation of two-dimensional differential gel electrophoresis for proteomic expression analysis of a model breast cancer cell system. Mol Cell Proteomics 1 (2002) 91-98
33. Liu H., Lin D., and Yates III J.R. Multidimensional separations for protein/peptide analysis in the post-genomic era. Biotechniques 32 (2002) 898 900, 902 passim
34. Wolters D.A., Washburn M.P., and Yates III J.R. An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 73 (2001) 5683-5690
35. Washburn M.P., Wolters D., and Yates III J.R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19 (2001) 242-247
36. Gevaert K., Goethals M., Martens L., Van Damme J., Staes A., Thomas G.R., et al. Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nat Biotechnol 21 (2003) 566-569
37. Gevaert K., Van Damme J., Goethals M., Thomas G.R., Hoorelbeke B., Demol H., et al. Chromatographic isolation of methionine-containing peptides for gel-free proteome analysis: identification of more than 800 Escherichia coli proteins. Mol Cell Proteomics 1 (2002) 896-903
38. Adamczyk M., Gebler J.C., and Wu J. Selective analysis of phosphopeptides within a protein mixture by chemical modification, reversible biotinylation and mass spectrometry. Rapid Commun Mass Spectrom 15 (2001) 1481-1488
39. Adamczyk M., Gebler J.C., and Wu J. Identification of phosphopeptides by chemical modification with an isotopic tag and ion trap mass spectrometry. Rapid Commun Mass Spectrom 16 (2002) 999-1001
40. Lubman D.M., Kachman M.T., Wang H., Gong S., Yan F., Hamler R.L., et al. Two-dimensional liquid separations-mass mapping of proteins from human cancer cell lysates. J Chromatogr B: Analyt Technol Biomed Life Sci 782 (2002) 183-196
41. Wang H., and Hanash S. Intact-protein based sample preparation strategies for proteome analysis in combination with mass spectrometry. Mass Spectrom Rev 24 (2005) 413-426
42. Sheng S., Chen D., and Van Eyk J.E. 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 5 (2006) 26-34
43. Karas M., and Hillenkamp F. Laser desorption ionization of proteins with molecular masses exceeding 10,000 Da. Anal Chem 60 (1988) 2299-2301
44. Fenn J.B., Mann M., Meng C.K., Wong S.F., and Whitehouse C.M. Electrospray ionization for mass spectrometry of large biomolecules. Science 246 (1989) 64-71
45. Domon B., and Aebersold R. Mass spectrometry and protein analysis. Science 312 (2006) 212-217
46. Olsen J.V., and Mann M. Improved peptide identification in proteomics by two consecutive stages of mass spectrometric fragmentation. Proc Natl Acad Sci USA 101 (2004) 13417-13422
47. Oda Y., Huang K., Cross F.R., Cowburn D., and Chait B.T. Accurate quantitation of protein expression and site-specific phosphorylation. Proc Natl Acad Sci USA 96 (1999) 6591-6596
48. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1 (2002) 376-386
49. Gygi S.P., Rist B., Gerber S.A., Turecek F., Gelb M.H., and Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17 (1999) 994-999
50. Ross P.L., Huang Y.N., Marchese J.N., Williamson B., Parker K., Hattan S., et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3 (2004) 1154-1169
51. Yao X., Afonso C., and Fenselau C. Dissection of proteolytic 18O labeling: endoprotease-catalyzed 16O-to-18O exchange of truncated peptide substrates. J Proteome Res 2 (2003) 147-152
52. Murray J., Marusich M.F., Capaldi R.A., and Aggeler R. Focused proteomics: monoclonal antibody-based isolation of the oxidative phosphorylation machinery and detection of phosphoproteins using a fluorescent phosphoprotein gel stain. Electrophoresis 25 (2004) 2520-2525
53. Hopper R.K., Carroll S., Aponte A.M., Johnson D.T., French S., Shen R.F., et al. Mitochondrial matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry 45 (2006) 2524-2536
54. Agrawal G.K., and Thelen J.J. Large-scale identification and quantitative profiling of phosphoproteins expressed during seed filling in oilseed rape. Mol Cell Proteomics (2006)
55. Gronborg M., Kristiansen T.Z., Stensballe A., Andersen J.S., Ohara O., Mann M., et al. A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: identification of a novel protein, Frigg, as a protein kinase A substrate. Mol Cell Proteomics 1 (2002) 517-527
56. Steen H., Kuster B., Fernandez M., Pandey A., and Mann M. Tyrosine phosphorylation mapping of the epidermal growth factor receptor signaling pathway. J Biol Chem 277 (2002) 1031-1039
57. Chen R., Fearnley I.M., Peak-Chew S.Y., and Walker J.E. The phosphorylation of subunits of complex I from bovine heart mitochondria. J Biol Chem 279 (2004) 26036-26045
58. Delom F., and Chevet E. Phosphoprotein analysis: from proteins to proteomes. Proteome Sci 4 (2006) 15
59. Mann M., Ong S.E., Gronborg M., Steen H., Jensen O.N., and Pandey A. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20 (2002) 261-268
60. Carr S.A., Annan R.S., and Huddleston M.J. Mapping posttranslational modifications of proteins by MS-based selective detection: application to phosphoproteomics. Methods Enzymol 405 (2005) 82-115
61. Corthals G.L., Aebersold R., and Goodlett D.R. Identification of phosphorylation sites using microimmobilized metal affinity chromatography. Methods Enzymol 405 (2005) 66-81
62. Ficarro S.B., McCleland M.L., Stukenberg P.T., Burke D.J., Ross M.M., Shabanowitz J., et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20 (2002) 301-305
63. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., and Jorgensen T.J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4 (2005) 873-886
64. Larsen M.R., Sorensen G.L., Fey S.J., Larsen P.M., and Roepstorff P. Phospho-proteomics: evaluation of the use of enzymatic de-phosphorylation and differential mass spectrometric peptide mass mapping for site specific phosphorylation assignment in proteins separated by gel electrophoresis. Proteomics 1 (2001) 223-238
65. Huang X.P., Pi Y., Lokuta A.J., Greaser M.L., and Walker J.W. Arachidonic acid stimulates protein kinase C-epsilon redistribution in heart cells. J Cell Sci 110 Pt 14 (1997) 1625-1634
66. Murphy S., and Frishman W.H. Protein kinase C in cardiac disease and as a potential therapeutic target. Cardiol Rev 13 (2005) 3-12
67. Baines C.P., Song C.X., Zheng Y.T., Wang G.W., Zhang J., Wang O.L., et al. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92 (2003) 873-880
68. Burkart E.M., Sumandea M.P., Kobayashi T., Nili M., Martin A.F., Homsher E., et al. Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J Biol Chem 278 (2003) 11265-11272
69. Labugger R., McDonough J.L., Neverova I., and Van Eyk J.E. Solubilization, two-dimensional separation and detection of the cardiac myofilament protein troponin T. Proteomics 2 (2002) 673-678
70. van der Velden J., Narolska N.A., Lamberts R.R., Boontje N.M., Borbely A., Zaremba R., et al. Functional effects of protein kinase C-mediated myofilament phosphorylation in human myocardium. Cardiovasc Res 69 (2006) 876-887
71. van der Velden J., Merkus D., Klarenbeek B.R., James A.T., Boontje N.M., Dekkers D.H., et al. Alterations in myofilament function contribute to left ventricular dysfunction in pigs early after myocardial infarction. Circ Res 95 (2004) e85-e95
72. Hein S., Kostin S., Heling A., Maeno Y., and Schaper J. The role of the cytoskeleton in heart failure. Cardiovasc Res 45 (2000) 273-278
73. Wang X., Osinska H., Gerdes A.M., and Robbins J. Desmin filaments and cardiac disease: establishing causality. J Card Fail 8 (2002) S287-S292
74. Huang X., Li J., Foster D., Lemanski S.L., Dube D.K., Zhang C., et al. Protein kinase C-mediated desmin phosphorylation is related to myofibril disarray in cardiomyopathic hamster heart. Exp Biol Med (Maywood) 227 (2002) 1039-1046
75. Kitamura S., Ando S., Shibata M., Tanabe K., Sato C., and Inagaki M. Protein kinase C phosphorylation of desmin at four serine residues within the non-alpha-helical head domain. J Biol Chem 264 (1989) 5674-5678
76. Capetanaki Y. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med 12 (2002) 339-348
77. Faber M.J., Dalinghaus M., Lankhuizen I.M., Bezstarosti K., Dekkers D.H., Duncker D.J., et al. Proteomic changes in the pressure overloaded right ventricle after 6 weeks in young rats: correlations with the degree of hypertrophy. Proteomics 5 (2005) 2519-2530
78. Buscemi N., Murray C., Doherty-Kirby A., Lajoie G., Sussman M.A., and Van Eyk J.E. Myocardial subproteomic analysis of a constitutively active Rac1-expressing transgenic mouse with lethal myocardial hypertrophy. Am J Physiol Heart Circ Physiol 289 (2005) H2325-H2333
79. Baines C.P., Zhang J., Wang G.W., Zheng Y.T., Xiu J.X., Cardwell E.M., et al. Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res 90 (2002) 390-397
80. Uecker M., Da Silva R., Grampp T., Pasch T., Schaub M.C., and Zaugg M. Translocation of protein kinase C isoforms to subcellular targets in ischemic and anesthetic preconditioning. Anesthesiology 99 (2003) 138-147
81. Weiss J.N., Korge P., Honda H.M., and Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93 (2003) 292-301
82. Jaburek M., Costa A.D., Burton J.R., Costa C.L., and Garlid K.D. Mitochondrial PKC epsilon and mitochondrial ATP-sensitive K+ channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes. Circ Res 99 (2006) 878-883
83. Churchill E.N., Murriel C.L., Chen C.H., Mochly-Rosen D., and Szweda L.I. Reperfusion-induced translocation of deltaPKC to cardiac mitochondria prevents pyruvate dehydrogenase reactivation. Circ Res 97 (2005) 78-85
84. Churchill E.N., and Szweda L.I. Translocation of deltaPKC to mitochondria during cardiac reperfusion enhances superoxide anion production and induces loss in mitochondrial function. Arch Biochem Biophys 439 (2005) 194-199
85. Varma T., Liu S.Q., West M., Thongboonkerd V., Ruvolo P.P., May W.S., et al. Protein kinase C-dependent phosphorylation and mitochondrial translocation of aldose reductase. FEBS Lett 534 (2003) 175-179
86. Pagliarini D.J., and Dixon J.E. Mitochondrial modulation: reversible phosphorylation takes center stage?. Trends Biochem Sci 31 (2006) 26-34
87. Bijur G.N., and Jope R.S. Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria. Neuroreport 14 (2003) 2415-2419
88. Bijur G.N., and Jope R.S. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J Neurochem 87 (2003) 1427-1435
89. Zhang J., Ping P., Vondriska T.M., Tang X.L., Wang G.W., Cardwell E.M., et al. Cardioprotection involves activation of NF-kappa B via PKC-dependent tyrosine and serine phosphorylation of I kappa B-alpha. Am J Physiol Heart Circ Physiol 285 (2003) H1753-H1758
90. Cross H.R., Murphy E., Bolli R., Ping P., and Steenbergen C. Expression of activated PKC epsilon (PKC epsilon) protects the ischemic heart, without attenuating ischemic H(+) production. J Mol Cell Cardiol 34 (2002) 361-367
91. Bowling N., Huang X., Sandusky G.E., Fouts R.L., Mintze K., Esterman M., et al. Protein kinase C-alpha and -epsilon modulate connexin-43 phosphorylation in human heart. J Mol Cell Cardiol 33 (2001) 789-798
92. Hunter J.J., and Chien K.R. Signaling pathways for cardiac hypertrophy and failure. N Engl J Med 341 (1999) 1276-1283
93. White M.Y., Cordwell S.J., McCarron H.C., Prasan A.M., Craft G., Hambly B.D., et al. Proteomics of ischemia/reperfusion injury in rabbit myocardium reveals alterations to proteins of essential functional systems. Proteomics 5 (2005) 1395-1410
94. Schilling B., Aggeler R., Schulenberg B., Murray J., Row R.H., Capaldi R.A., et al. Mass spectrometric identification of a novel phosphorylation site in subunit NDUFA10 of bovine mitochondrial complex I. FEBS Lett 579 (2005) 2485-2490
95. Schulenberg B., Aggeler R., Beechem J.M., Capaldi R.A., and Patton W.F. Analysis of steady-state protein phosphorylation in mitochondria using a novel fluorescent phosphosensor dye. J Biol Chem 278 (2003) 27251-27255
96. Augereau O., Claverol S., Boudes N., Basurko M.J., Bonneu M., Rossignol R., et al. Identification of tyrosine-phosphorylated proteins of the mitochondrial oxidative phosphorylation machinery. Cell Mol Life Sci 62 (2005) 1478-1488
97. Ko Y.H., Pan W., Inoue C., and Pedersen P.L. Signal transduction to mitochondrial ATP synthase: evidence that PDGF-dependent phosphorylation of the delta-subunit occurs in several cell lines, involves tyrosine, and is modulated by lysophosphatidic acid. Mitochondrion 1 (2002) 339-348
98. Lee I., Salomon A.R., Yu K., Doan J.W., Grossman L.I., and Huttemann M. New prospects for an old enzyme: mammalian cytochrome c is tyrosine-phosphorylated in vivo. Biochemistry 45 (2006) 9121-9128