Redox signalling in cardiovascular disease

Proteomics - Clinical Applications

Volumn 2, Issue 6, 2008, Pages 823-836

  Charles, Rebecca L ^a   Eaton, Philip ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cardiovascular disease; Redox signalling

Indexed keywords

ACONITATE HYDRATASE; ACTIN; ACYL COENZYME A DEHYDROGENASE; CALMODULIN; CREATINE KINASE; CYSTEINE; CYTOCHROME C OXIDASE; DESMIN; FIBRILLIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN; LACTATE DEHYDROGENASE; MALATE DEHYDROGENASE; MYOGLOBIN; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; OXYGEN; PEROXIREDOXIN; PHOSPHORYLASE KINASE; PROTEIN 14 3 3; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; TROPOMYOSIN; TROPONIN; TUBULIN;

CARDIOVASCULAR DISEASE; CELL FUNCTION; HUMAN; LIPID PEROXIDATION; MONITORING; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEIN PROCESSING; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 46749129745     PISSN: 18628346     EISSN: None     Source Type: Journal    
DOI: 10.1002/prca.200780104     Document Type: Review

References (110)

1. Griendling, K. K., FitzGerald, G. A., Oxidative stress and cardiovascular injury: Part I: basic mechanisms and in vivo monitoring of ROS. Circulation 2003, 108, 1912-1916.
2. Rhee, S. G., Redox signalling: hydrogen peroxide as intracellular messenger. Exp. Mol. Med. 1999, 31, 53-59.
3. MRC/BHF Heart Protection Study of antioxidant vitamin supplementation in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet 2002, 360, 23-33.
4. Yusuf, S., Dagenais, G., Pogue, J., Bosch, J., Sleight, P., Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 2000, 342, 154-160.
5. Blumberg, J. B., Frei, B., Why clinical trials of vitamin E and cardiovascular diseases may be fatally flawed. Commentary on "The relationship between dose of vitamin E and suppression of oxidative stress in humans". Free Radic. Biol. Med. 2007, 43, 1374-1376.
6. Smith, R. A., Porteous, C. M., Coulter, C. V., Murphy, M. P., Selective targeting of an antioxidant to mitochondria. Eur. J. Biochem. 1999, 263, 709-716.
7. +, free radicals, and vascular dysfunction in early diabetes mellitus. Diabetologia 1997, 40 Suppl 2, S115-117.
8. Kannurpatti, S. S., Joshi, N. B., Energy metabolism and NAD-NADH redox state in brain slices in response to glutamate exposure and ischemia. Metab. Brain Dis. 1999, 14, 33-43.
9. Lipinski, B., Evidence in support of a concept of reductive stress. Br. J. Nutr. 2002, 87, 93-94; discussion 94.
10. Ghyczy, M., Boros, M., Electrophilic methyl groups present in the diet ameliorate pathological states induced by reductive and oxidative stress: a hypothesis. Br. J. Nutr. 2001, 85, 409-414.
11. Rajasekaran, N. S., Connell, P., Christians, E. S., Yan, L. J. et al., Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 2007, 130, 427-439.
12. Valadi, H., Valadi, A., Ansell, R., Gustafsson, L. et al., NADH-reductive stress in Saccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1). Curr. Genet. 2004, 45, 90-95.
13. Tanaka, M., Fujiwara, H., Yamasaki, K., Sasayama, S., Superoxide dismutase and N-2-mercaptopropionyl glycine attenuate infarct size limitation effect of ischemic preconditioning in the rabbit. Cardiovasc. Res. 1994, 28, 980-986.
14. Sies, H., Dafre, A. L., Ji, Y., Akerboom, T. P., Protein S-thiolation and redox regulation of membrane-bound glutathione transferase. Chem. Biol. Interact. 1998, 111-112, 177-185.
15. Robin, E., Guzy, R. D., Loor, G., Iwase, H. et al., Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion. J. Biol. Chem. 2007, 282, 19133-19143.
16. Sauer, H., Wartenberg, M., Hescheler, J., Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell. Physiol. Biochem. 2001, 11, 173-186.
17. Akhter, S., Vignini, A., Wen, Z., English, A. et al., Evidence for S-nitrosothiol-dependent changes in fibrinogen that do not involve transnitrosation or thiolation. Proc. Natl. Acad. Sci. USA 2002, 99, 9172-9177.
18. Pagliaro, P., Mancardi, D., Rastaldo, R., Penna, C. et al., Nitroxyl affords thiol-sensitive myocardial protective effects akin to early preconditioning. Free Radic. Biol. Med. 2003, 34, 33-43.
19. O'Donnell, V. B., Eiserich, J. P., Bloodsworth, A., Chumley, P. H. et al., Nitration of unsaturated fatty acids by nitric oxide-derived reactive species. Methods Enzymol. 1999, 301, 454-470.
20. Gallogly, M. M., Mieyal, J. J., Mechanisms of reversible protein glutathionylation in redox signalling and oxidative stress. Curr. Opin. Pharmacol. 2007, 7, 381-391.
21. Mallis, R. J., Buss, J. E., Thomas, J. A., Oxidative modification of H-ras: S-thiolation and S-nitrosylation of reactive cysteines. Biochem. J. 2001, 355, 145-153.
22. Barrett, W. C., DeGnore, J. P., Keng, Y. F., Zhang, Z. Y. et al., Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J. Biol. Chem. 1999, 274, 34543-34546.
23. Barrett, W. C., DeGnore, J. P., Konig, S., Fales, H. M. et al., Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry1999, 38, 6699-6705.
24. Humphries, K. M., Juliano, C., Taylor, S. S., Regulation of cAMP-dependent protein kinase activity by glutathionylation. J. Biol. Chem. 2002, 277, 43505-43511.
25. Sadidi, M., Geddes, T. J., Kuhn, D. M., S-thiolation of tyrosine hydroxylase by reactive nitrogen species in the presence of cysteine or glutathione. Antioxid. Redox Signal. 2005, 7, 863-869.
26. Chu, F., Ward, N. E., O'Brian, C. A., Potent inactivation of representative members of each PKC isozyme subfamily and PKD via S-thiolation by the tumor-promotion/progression antagonist glutathione but not by its precursor cysteine. Carcinogenesis2001, 22, 1221-1229.
27. Davis, D. A., Dorsey, K., Wingfield, P. T., Stahl, S. J. et al., Regulation of HIV-1 protease activity through cysteine modification. Biochemistry 1996, 35, 2482-2488.
28. Chu, F., O'Brian, C. A., PKC sulfhydryl targeting by disulfiram produces divergent isozymic regulatory responses that accord with the cancer preventive activity of the thiuram disulfide. Antioxid. Redox Signal. 2005, 7, 855-862.
29. Biteau, B., Labarre, J., Toledano, M. B., ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature2003, 425, 980-984.
30. Budanov, A. V., Sablina, A. A., Feinstein, E., Koonin, E. V., Chumakov, P. M., Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 2004, 304, 596-600.
31. Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C. et al., Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 2003, 423, 769-773.
32. Stamler, J. S., Lamas, S., Fang, F. C., Nitrosylation. the prototypic redox-based signalling mechanism. Cell 2001, 106, 675-683.
33. Mitchell, D. A., Morton, S. U., Fernhoff, N. B., Marletta, M. A., Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc. Natl. Acad. Sci. USA 2007, 104, 11609-11614.
34. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E., Stamler, J. S., Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 2005, 6, 150-166.
35. Greco, T. M., Hodara, R., Parastatidis, I., Heijnen, H. F. et al., Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA 2006, 103, 7420-7425.
36. Sun, J., Xin, C., Eu, J. P., Stamler, J. S., Meissner, G., Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc. Natl. Acad. Sci. USA 2001, 98, 11158-11162.
37. Linke, K., Jakob, U., Not every disulfide lasts forever: disulfide bond formation as a redox switch. Antioxid. Redox Signal. 2003, 5, 425-434.
38. Brennan, J. P., Wait, R., Begum, S., Bell, J. R. et al., Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J. Biol. Chem. 2004, 279, 41352-41360.
39. Gitler, C., Zarmi, B., Kalef, E., General method to identify and enrich vicinal thiol proteins present in intact cells in the oxidized, disulfide state. Anal. Biochem. 1997, 252, 48-55.
40. Vogt, W., Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic. Biol. Med. 1995, 18, 93-105.
41. Hoshi, T., Heinemann, S., Regulation of cell function by methionine oxidation and reduction. J. Physiol. 2001, 531, 1-11.
42. + channels. J. Physiol. 2006, 571, 329-348.
43. Levine, R. L., Mosoni, L., Berlett, B. S., Stadtman, E. R., Methionine residues as endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. USA 1996, 93, 15036-15040.
44. Shacter, E., Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev. 2000, 32, 307-326.
45. Berlett, B. S., Stadtman, E. R., Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 1997, 272, 20313-20316.
46. Kamisaki, Y., Wada, K., Bian, K., Balabanli, B. et al., An activity in rat tissues that modifies nitrotyrosine-containing proteins. Proc. Natl. Acad. Sci. USA 1998, 95, 11584-11589.
47. Irie, Y., Saeki, M., Kamisaki, Y., Martin, E., Murad, F., Histone H1.2 is a substrate for denitrase, an activity that reduces nitrotyrosine immunoreactivity in proteins. Proc. Natl. Acad. Sci. USA 2003, 100, 5634-5639.
48. Schaur, R. J., Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Mol. Aspects Med. 2003, 24, 149-159.
49. Ceaser, E. K., Moellering, D. R., Shiva, S., Ramachandran, A. et al., Mechanisms of signal transduction mediated by oxidized lipids: the role of the electrophile-responsive proteome. Biochem. Soc. Trans. 2004, 32, 151-155.
50. Levonen, A. L., Landar, A., Ramachandran, A., Ceaser, E. K. et al., Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem. J. 2004, 378, 373-382.
51. Sanchez-Gomez, F. J., Cernuda-Morollon, E., Stamatakis, K., Perez-Sala, D., Protein thiol modification by 15-deoxy-Delta12, 14-prostaglandin J2 addition in mesangial cells: role in the inhibition of pro-inflammatory genes. Mol. Pharmacol. 2004, 66, 1349-1358.
52. Charles, R. L., Schroder, E., May, G., Free, P. et al., Protein sulfenation as a redox sensor: Proteomics studies using a novel biotinylated dimedone analogue. Mol. Cell. Proteomics 2007, 6, 1473-1484.
53. Ellis, H. R., Poole, L. B., Novel application of 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. Biochemistry 1997, 36, 15013-15018.
54. Poole, L. B., Karplus, P. A., Claiborne, A., Protein sulfenic acids in redox signaling. Annu. Rev. Pharmacol. Toxicol. 2004, 44, 325-347.
55. Poole, L. B., Zeng, B. B., Knaggs, S. A., Yakubu, M., King, S. B., Synthesis of chemical probes to map sulfenic acid modifications on proteins. Bioconjug. Chem. 2005, 16, 1624-1628.
56. Saurin, A. T., Neubert, H., Brennan, J. P., Eaton, P., Widespread sulfenic acid formation in tissues in response to hydrogen peroxide. Proc. Natl. Acad. Sci. USA 2004, 101, 17982-17987.
57. Jaffrey, S. R., Snyder, S. H., The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE. 2001, 2001, L1.
58. Sullivan, D. M., Wehr, N. B., Fergusson, M. M., Levine, R. L., Finkel, T., Identification of oxidant-sensitive proteins: TNF-alpha induces protein glutathiolation. Biochemistry 2000, 39, 11121-11128.
59. Brennan, J. P., Miller, J. I., Fuller, W., Wait, R. et al., The utility of N,N-biotinyl glutathione disulfide in the study of protein S-glutathiolation. Mol. Cell. Proteomics 2006, 5, 215-225.
60. Sommer, A., Traut, R. R., Diagonal polyacrylamide-dodecyl sulfate gel electrophoresis for the identification of ribosomal proteins crosslinked with methyl-4-mercaptobutyrimidate. Proc. Natl. Acad. Sci. USA 1974, 71, 3946-3950.
61. Wasinger, V. C., Cordwell, S. J., Cerpa-Poljak, A., Yan, J. X. et al., Progress with gene-product mapping of the Mollicutes: Mycoplasma genitalium. Electrophoresis 1995, 16, 1090-1094.
62. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F. et al., Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17, 994-999.
63. Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B. et al., Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 2004, 3, 1154-1169.
64. Wolters, D. A., Washburn, M. P., Yates, J. R., III, An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 2001, 73, 5683-5690.
65. Eaton, P., Protein thiol oxidation in health and disease: Techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic. Biol. Med. 2006, 40, 1889-1899.
66. Gorg, A., Obermaier, C., Boguth, G., Harder, A. et al., The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 2000, 21, 1037-1053.
67. Gorg, A., Weiss, W., Dunn, M. J., Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4, 3665-3685.
68. Rabilloud, T., Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics 2002, 2, 3-10.
69. Garlick, P. B., Davies, M. J., Hearse, D. J., Slater, T. F., Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ. Res. 1987, 61, 757-760.
70. Eaton, P., Byers. H. L., Leeds, N., Ward, M. A., Shattock, M. J., Detection, quantitation, purification, and identification of cardiac proteins S-thiolated during ischemia and reperfusion. J. Biol. Chem. 2002, 277, 9806-9811.
71. Martinez-Ruiz, A., Lames, S., Detection and proteomic identification of S-nitrosylated proteins in endothelial cells. Arch. Biochem. Biophys. 2004, 423, 192-199.
72. Sethuraman, M., McComb, M. E., Huang, H., Huang, S. et al., Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J. Proteome Res. 2004, 3, 1228-1233.
73. Canton, M., Neverova, I., Menabo, R., Van Eyk, J., Di Lisa, F., Evidence of myofibrillar protein oxidation induced by post-ischemic reperfusion in isolated rat hearts. Am. J. Physiol. Heart Circ. Physiol. 2004, 286, H870-877.
74. Brennan, J. P., Bardswell, S. C., Burgoyne, J. R., Fuller, W. et al., Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. J. Biol. Chem. 2006, 281, 21827-21836.
75. Burgoyne, J. R., Madhani, M., Cuello, F., Charles, R. L. et al., Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 2007, 317, 1393-1397.
76. Gopalakrishna, R., Jaken, S., Protein kinase C signaling and oxidative stress. Free Radic. Biol. Med. 2000, 28, 1349-1361.
77. Chu, F., Chen, L. H., O'Brian, C. A., Cellular protein kinase C isozyme regulation by exogenously delivered physiological disulfides-implications of oxidative protein kinase C regulation to cancer prevention. Carcinogenesis 2004, 25, 585-596.
78. Chu, F., Ward, N. E., O'Brian, C. A., PKC isozyme S-cysteinylation by cystine stimulates the pro-apoptotic isozyme PKC delta and inactivates the oncogenic isozyme PKC epsilon. Carcinogenesis 2003, 24, 317-325.
79. Ward, N. E., Chu, F., O'Brian, C. A., Regulation of protein kinase C isozyme activity by S-glutathiolation. Methods Enzymol. 2002, 353, 89-100.
80. Ward, N. E., Pierce, D. S., Chung, S. E., Gravitt, K. R., O'Brian, C. A., Irreversible inactivation of protein kinase C by glutathione. J. Biol. Chem. 1998, 273, 12558-12566.
81. Ward, N. E., Stewart, J. R., Ioannides, C. G., O'Brian, C. A., Oxidant-induced S-glutathiolation inactivates protein kinase C-alpha (PKC-alpha): a potential mechanism of PKC isozyme regulation. Biochemistry 2000, 39, 10319-10329.
82. Adachi, T., Weisbrod, R. M., Pimentel, D. R., Ying, J. et al., S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat. Med. 2004, 10, 1200-1207.
83. Santacruz-Toloza, L., Ottolia, M., Nicoll, D. A., Philipson, K. D., Functional analysis of a disulfide bond in the cardiac Na(+)-Ca(2+) exchanger. J. Biol. Chem. 2000, 275, 182-188.
84. 2+ release channel from oxidation induced activation. J. Biol. Chem. 1997, 272, 25462-25467.
85. Boraso, A., Williams, A. J., Modification of the gating of the cardiac sarcoplasmic reticulum Ca(2+)-release channel by H2O2 and dithiothreitol. Am. J. Physiol. 1994, 267, H1010-1016.
86. Xie, H., Zhu, P. H., Biphasic modulation of ryanodine receptors by sulfhydryl oxidation in rat ventricular myocytes. Biophys. J. 2006, 91, 2882-2891.
87. Eaton, P., Fuller, W., Shattock, M. J., S-thiolation of HSP27 regulates its multimeric aggregate size independently of phosphorylation. J. Biol. Chem. 2002, 277, 21189-21196.
88. Canton, M., Skyschally, A., Menabo, R., Boengler, K. et al., Oxidative modification of tropomyosin and myocardial dysfunction following coronary microembolization. Eur. Heart J. 2006, 27, 875-881.
89. Han, B., Stevens, J. F., Maier, C. S., Design, synthesis, and application of a hydrazide-functionalized isotope-coded affinity tag for the quantification of oxylipid-protein conjugates. Anal. Chem. 2007, 79, 3342-3354.
90. Chen, J., Schenker, S., Frosto, T. A., Henderson, G. I., Inhibition of cytochrome c oxidase activity by 4-hydroxynonenal (HNE). Role of HNE adduct formation with the enzyme subunits. Biochim. Biophys. Acta 1998, 1380, 336-344.
91. Eaton, P., Li, J. M., Hearse, D. J., Shattock, M. J., Formation of 4-hydroxy-2-nonenal-modified proteins in ischemic rat heart. Am. J. Physiol 1999, 276, H935-H943.
92. Chen, J., Henderson, G. I., Freeman, G. L., Role of 4-hydroxynonenal in modification of cytochrome c oxidase in ischemia/reperfused rat heart. J. Mol. Cell. Cardiol. 2001, 33, 1919-1927.
93. Adachi, T., Pimentel, D. R., Heibeck, T., Hou, X. et al., S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 2004, 279, 29857-29862.
94. Galeva, N. A., Esch, S. W., Williams, T. D., Markille, L. M., Squier, T. C., Rapid method for quantifying the extent of methionine oxidation in intact calmodulin. J. Am. Soc. Mass Spectrom. 2005, 16, 1470-1480.
95. Musatov, A., Carroll, C. A., Liu, Y. C., Henderson, G. I. et al., Identification of bovine heart cytochrome c oxidase subunits modified by the lipid peroxidation product 4-hydroxy-2-nonenal. Biochemistry 2002, 41, 8212-8220.
96. Gallego-Delgado, J., Lazaro, A., Osende, J. I., Barderas, M. G. et al., Comparison of the protein profile of established and regressed hypertension-induced left ventricular hypertrophy. J. Proteome Res. 2006, 5, 404-413.
97. Lindsey, M. L., Goshorn, D. K., Comte-Walters, S., Hendrick, J. W. et al., A multidimensional proteomic approach to identify hypertrophy-associated proteins. Proteomics 2006, 6, 2225-2235.
98. Kim, N., Lee, Y., Kim, H., Joo, H. et al., Potential biomarkers for ischemic heart damage identified in mitochondrial proteins by comparative proteomics. Proteomics 2006, 6, 1237-1249.
99. Bagnato, C., Thumar, J., Mayya, V., Hwang, S. I. et al., Proteomics analysis of human coronary atherosclerotic plaque: a feasibility study of direct tissue proteomics by liquid chromatography and tandem mass spectrometry. Mol. Cell. Proteomics 2007, 6, 1088-1102.
100. Banfi, C., Brioschi, M., Wait, R., Begum, S. et al., Proteomic analysis of membrane microdomains derived from both failing and non-failing human hearts. Proteomics 2006, 6, 1976-1988.
101. Weekes, J., Wheeler, C. H., Yan, J. X., Weil, J. et al., Bovine dilated cardiomyopathy: proteomic analysis of an animal model of human dilated cardiomyopathy. Electrophoresis 1999, 20, 898-906.
102. Heinke, M. Y., Wheeler, C. H., Yan, J. X., Amin, V. et al., Changes in myocardial protein expression in pacing-induced canine heart failure. Electrophoresis 1999, 20, 2086-2093.
103. Macri, J., Rapundalo, S. T., Application of proteomics to the study of cardiovascular biology. Trends Cardiovasc. Med. 2001, 11, 66-75.
104. Arnott, D., O'Connell, K. L., King, K. L., Stults, J. T., An integrated approach to proteome analysis: identification of proteins associated with cardiac hypertrophy. Anal. Biochem. 1998, 258, 1-18.
105. White, M. Y., Cordwell, S. J., McCarron, H. C., Prasan, A. M. et al., Proteomics of ischemia/reperfusion injury in rabbit myocardium reveals alterations to proteins of essential functional systems. Proteomics 2005, 5, 1395-1410.
106. Heinke, M. Y., Wheeler, C. H., Chang, D., Einstein, R. et al., Protein changes observed in pacing-induced heart failure using two-dimensional electrophoresis. Electrophoresis 1998, 19, 2021-2030.
107. Jin, X., Xia, L., Wang, L. S., Shi, J. Z. et al., Differential protein expression in hypertrophic heart with and without hypertension in spontaneously hypertensive rats. Proteomics 2006, 6, 1948-1956.
108. Tompkins, A. J., Burwell, L. S., Digerness, S. B., Zaragoza, C. et al., Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim. Biophys. Acta 2006, 1762, 223-231.
109. White, M. Y., Tchen, A. S., McCarron, H. C., Hambly, B. D. et al., Proteomics of ischemia and reperfusion injuries in rabbit myocardium with and without intervention by an oxygen-free radical scavenger. Proteomics 2006, 6, 6221-6233.
110. Mayr, M., Chung, Y. L., Mayr, U., Yin, X. et al., Proteomic and metabolomic analyses of atherosclerotic vessels from apolipoprotein E-deficient mice reveal alterations in inflammation, oxidative stress, and energy metabolism. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 2135-2142.