Comparative profiling of the mammalian mitochondrial proteome: Multiple aconitase-2 isoforms including N-formylkynurenine modifications as part of a protein biomarker signature for reactive oxidative species

Journal of Proteome Research

Volumn 5, Issue 3, 2006, Pages 625-633

  Hunzinger, Christian ^a   Wozny, Wojclech ^a   Schwall, Gerhard P ^a   Poznanović, Slobodan ^a   Stegmann, Werner ^a   Zengerling, Helmut ^a   Scaoepf, Rainer ^a   Groebe, Karlfried ^a   Cahill, Michael A ^a   Qsiewacz, Heinz D ^b   Jägemann, Nora ^c   Bloch, Monika ^c   Dencher, Norbert A ^c   Krause, Frank ^c   Schrattenholz, André ^a  

^a PROTEOSYS AG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

16 BAC SDS PAGE; Aconitase 2; Blue native SDS PAGE; IEF SDS PAGE; Membrane proteins; Mitochondria; Proteomics; Quantitative differential protein expression; Reactive oxygen species; Tricine urea SDS PAGE; Two dimensional polyacrylamide gel electrophoresis

Indexed keywords

ACONITATE HYDRATASE; ACONITATE HYDRATASE 2; BIOLOGICAL MARKER; FORMYLKYNURENINE; ISOENZYME; KYNURENINE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; TRYPTOPHAN; UNCLASSIFIED DRUG; UREA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL AGING; CELL DEATH; CELL SURVIVAL; COMPARATIVE STUDY; GENE EXPRESSION PROFILING; ISOELECTRIC FOCUSING; MAMMAL; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; OXIDATION; OXIDATIVE STRESS; PLASTICITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STRESS;

ACONITATE HYDRATASE; ANIMALS; BIOLOGICAL MARKERS; CATTLE; GENE EXPRESSION PROFILING; HUMANS; ISOENZYMES; KYNURENINE; MITOCHONDRIA, HEART; REACTIVE OXYGEN SPECIES;

ANIMALIA; BOVINAE; MAMMALIA;

EID: 33644845390     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr050377+     Document Type: Article

References (63)

1. Bailey, S. M.; Landar, A.; Darley-Usmar, V. Mitochondrial proteomics in free radical research. Free Radic Biol. Med. 2005, 30, 175-188.
2. Fukada, K.; Zhang, F.; Vien, A.; Cashman, N. R.; Zhu, H. Mitochondrial proteomic analysis of a cell line model of familial amyotrophic lateral sclerosis. Mol. Cell Proteomics 2004, 3, 1211-1223.
3. Gabaldon, T.; Huynen, M. A. Shaping the mitochondrial proteome. Biochim Biophys. Acta 2004, 1659, 212-220.
4. Jin, J.; Meredith, G. E.; Chen, L.; Zhou, Y.; Xu, J.; Shie, F. S.; Lockhart, P.; Zhang, J. Quantitative proteomic analysis of mitochondrial proteins: relevance to Lewy body formation and Parkinson's disease. Brain Res. Mol. Brain Res. 2005, 134, 119-138.
5. Lopez, M. F.; Melov, S.; Johnson, F.; Nagulko, N.; Golenko, E.; Kuzdzal, S.; Ackloo, S.; Mikulskis, A. Proteomic analysis of mitochondrial proteins. Int. Rev. Neurobiol. 2004, 61, 31-48.
6. Sickmann, A.; Reinders, J.; Wagner, Y.; Joppich, C.; Zahedi, R.; Meyer, H. E.; Schonfisch, B.; Perschil, I.; Chacinska, A.; Guiard, B.; Rehling, P.; Pfanner, N.; Meisinger, C. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13207-13212.
7. Taylor, S. W.; Fahy, E.; Zhang, B.; Glenn, G. M.; Warnock, D. E.; Wiley, S.; Murphy, A. N.; Gaucher, S. P.; Capaldi, R. A.; Gibson, B. W.; Ghosh, S. S. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 2003, 21, 281-286.
8. Gaucher, S. P.; Taylor, S. W.; Fahy, E.; Zhang, B.; Warnock, D. E.; Ghosh, S. S.; Gibson, B. W. Expanded coverage of the human heart mitochondrial proteome using multidimensional liquid chromatography coupled with tandem mass spectrometry. J. Proteome Res. 2004, 3, 495-505.
9. Alonso, J.; Rodriguez, J. M.; Baena-Lopez, L. A.; Santaren, J. F. Characterization of the Drosophila melanogaster Mitochondrial Proteome. J. Proteome Res. 2005, 4, 1636-1645.
10. Poznanovic, S.; Schwall, G.; Zengerling, H.; Cahill, M. A. Isoelectric focusing in serial immobilized pH gradient gels to improve protein separation in proteomic analysis. Electrophoresis 2005, 26, 3185-3190.
11. Schägger, H.; von lagow, G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem 1991, 199, 223-231.
12. Brookes, P. S.; Pinner, A.; Ramachandran, A.; Coward, L.; Barnes, S.; Kim, H.; Darley-Usmar, V. M. High throughput two-dimensional blue-native electrophoresis: a tool for functional proteomics of mitochondria and signaling complexes. Proteomics 2002, 2, 969-977.
13. Krause, F.; Reifschneider, N. H.; Goto, S.; Dencher, N. A. Active oligomeric ATP synthases in mammalian mitochondria. Biochem. Biophys. Res. Commun. 2005, 329, 583-590.
14. Schägger, H. Blue-native gels to isolate protein complexes from mitochondria. Methods Cell Biol. 2001, 65, 231-244.
15. Rais, I.; Karas, M.; Schägger, H. Two-dimensional electrophoresis for the isolation of integral membrane proteins and mass spectrometric identification. Proteomics 2004, 4, 2567-2571.
16. Hartinger, J.; Stenius, K.; Hogemann, D.; Jahn, R. 16-BAC/SDS-PAGE: a two-dimensional gel electrophoresis system suitable for the separation of integral membrane proteins. Anal Biochem. 1996, 240, 126-133.
17. Shadel, G. S. Mitochondrial DNA, aconitase 'wraps' it up. Trends Biochem. Sci. 2005, 30, 294-296.
18. Yarian, C. S.; Rebrin, I.; Sohal, R. S. Aconitase and ATP synthase are targets of malondialdehyde modification and undergo an age-related decrease in activity in mouse heart mitochondria. Biochem. Biophys. Res. Commun. 2005, 330, 151-156.
19. Chen, X. J.; Wang, X.; Kaufman, B. A.; Butow, R. A. Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 2005, 307, 714-717.
20. Yan, L. J.; Levine, R. L.; Sohal, R. S. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 11168-11172.
21. Yang, E. S.; Yang, J. H.; Park, J. E.; Park, J. W. Oxalomalate, a competitive inhibitor of NADP+ -dependent isocitrate dehydrogenase, regulates lipid peroxidation-mediated apoptosis in U937 cells. Free Radic Res. 2005, 39, 89-94.
22. Jo, S. H.; Son, M. K.; Koh, H. J.; Lee, S. M.; Song, I. H.; Kim, Y. O.; Lee, Y. S.; Jeong, K. S.; Kim, W. B.; Park, J. W.; Song, B. J.; Huh, T. L. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 2001, 276, 16168-16176.
23. KU, I. S.; Lee, J. H.; Shin, A. H.; Park, J. W. Glycation-induced inactivation of NADP(+)-dependent isocitrate dehydrogenase: implications for diabetes and aging. Free Radic Biol. Med. 2004, 37, 1765-1778.
24. KU, I. S.; Park, J. W. Regulation of mitochondrial NADP+-dependent isocitrate dehydrogenase activity by glutathionylation. J. Biol. Chem. 2005, 200, 10846-10854.
25. Kil, I. S.; Lee, Y. S.; Bae, Y. S.; Huh, T. L.; Park, J. W. Modulation of NADP(+)-dependent isocitrate dehydrogenase in aging. Redox Rep. 2004, 9, 271-277.
26. Taylor, S. W.; Fahy, E.; Murray, J.; Capaldi, R. A.; Ghosh, S. S. Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J. Biol. Chem. 2003, 278, 19587-19590.
27. Smith, A. L. Preparations, properties and conditions for assay of mitochondria: slaughterhouse material, small scale. Methods Enzymol. 1967, 10, 81-86.
28. Schägger, H.; Pfeiffer, K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. Embo J. 2000, 19, 1777-1783.
29. Krause, F.; Scheckhuber, C. Q.; Werner, A.; Rexroth, S.; Reif-schneider, N. H.; Dencher, N. A.; Osiewacz, H. D. Supramolecular organization of cytochrome c oxidase- and alternative oxidase-dependent respiratory chains in the filamentous fungus Podospora anserina. J. Biol. Chem. 2004, 279, 26453-26461.
30. Krause, F.; Reifschneider, N. H.; Vocke, D.; Seelen, H.; Rexroth, S.; Dencher, N. A. "Respirasome"-like supercomplexes in green leaf mitochondria of spinach. J. Biol. Chem. 2004, 279, 48369-48375.
31. Schägger, H.; von Jagow, G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 1987, 166, 368-379.
32. Blum, H.; Beier, H.; Gross, H. J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8, 93-99.
33. Rabilloud, T.; Carpentier, G.; Tarroux, P. Improvement and simplification of low-background silver staining of proteins by using sodium dithionite. Electrophoresis 1988, 9, 288-291.
34. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 60, 850-858.
35. Cahill, M. A.; Wozny, W.; Schwall, G.; Schroer, K.; Holzer, K.; Poznanovic, S.; Hunzinger, C.; Vogt, J. A.; Stegmann, W.; Matthies, H.; Schrattenholz, A. Analysis of relative isotopologue abundances for quantitative profiling of complex protein mixtures labeled with the acrylamide/D3-acrylamide alkylation tag system. Rapid Commun. Mass Spectrom. 2003, 17, 1283-1290.
36. Sommer, S.; Hunzinger, C.; Schillo, S.; Klemm, M.; Biefang-Arndt, K.; Schwall, G.; Pütter, S.; Hoelzer, K.; Schroer, K.; Stegmann, W.; Schrattenholz, A. Molecular analysis of homocysteic acid-induced neuronal stress. J. Proteome Res. 2004, 3, 572-581.
37. Kyte, J.; Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157, 105-132.
38. Zahedi, R. P.; Meisinger, C.; Sickmann, A. Two-dimensional benzyldimethyl-n-hexadecylammonium chloride/SDS-PAGE for membrane proteomics. Proteomics 2005, 1, 1.
39. Devreese, B.; Vanrobaeys, F.; Smet, J.; Van Beeumen, J.; Van Coster, R. Mass spectrometric identification of mitochondrial oxidative phosphorylation subunits separated by two-dimensional blue-native polyacrylamide gel electrophoresis. Electrophoresis 2002, 23, 2525-2533.
40. Bulteau, A. L.; Lundberg, K. C.; Ikeda-Saito, M.; Isaya, G.; Szweda, L. I. Reversible redox-dependent modulation of mitochondrial aconitase and proteolytic activity during in vivo cardiac ischemia/reperfusion. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 5987-5991.
41. Yarian, C. S.; Sohal, R. S. In the aging housefly aconitase is the only citric acid cycle enzyme to decline significantly. J. Bioenerg. Biomembr. 2005, 37, 91-96.
42. Schrattenholz, A. Proteomics: how to control highly dynamic patterns of millions of molecules and interpret changes correctly? Drug Discov. Today Technol. 2004, 1, 1-8.
43. Rexroth, S.; Meyer zu Tittingdorf, J. M.; Krause, F.; Dencher, N. A.; Seelert, H. Thylakoid membrane at altered metabolic state: challenging the forgotten realms of the proteome. Electrophoresis 2003, 24, 2814-2823.
44. Sanchez, J. C.; Chiappe, D.; Converset, V.; Hoogland, C.; Binz, P. A.; Paesano, S.; Appel, R. D.; Wang, S.; Sennitt, M.; Nolan, A.; Cawthorne, M. A.; Hochstrasser, D. F. The mouse SWISS-2D PAGE database: a tool for proteomics study of diabetes and obesity. Proteomics 2001, 1, 136-163.
45. Richly, E.; Chinnery, P. F.; Leister, D. Evolutionary diversification of mitochondrial proteomes: implications for human disease. Trends Genet. 2003, 19, 356-362.
46. Heazlewood, J. L.; Millar, A. H.; Day, D. A.; Whelan, J. What makes a mitochondrion? Genome Biol. 2003, 4, 218.
47. Zolg, J. W.; Langen, H. How industry is approaching the search for new diagnostic markers and biomarkers. Mol. Cell Proteomics 2004, 3, 345-354.
48. Eldadah, B. A.; Faden, A. I. Caspase pathways, neuronal apoptosis, and CNS injury. J. Neurotrauma 2000, 17, 811-829.
49. Saraste, A.; Pulkki, K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc. Res. 2000, 45, 528-537.
50. Blonder, J.; Goshe, M. B.; Xiao, W.; Camp, D. G., 2nd; Wingerd, M.; Davis, R. W.; Smith, R. D. Global analysis of the membrane subproteome of Pseudomonas aeruginosa using liquid chromatography-tandem mass spectrometry. J. Proteome Res. 2004, 3, 434-444.
51. Goshe, M. B.; Blonder, J.; Smith, R. D. Affinity labeling of highly hydrophobic integral membrane proteins for proteome-wide analysis. J. Proteome Res. 2003, 2, 153-161.
52. Jiang, X. S.; Zhou, H.; Zhang, L.; Sheng, Q. H.; Li, S. J.; Li, L.; Hao, P.; Li, Y. X.; Xia, Q. C.; Wu, J. R.; Zeng, R. A high-throughput approach for subcellular proteome: identification of rat liver proteins using subcellular fractionation coupled with two-dimensional liquid chromatography tandem mass spectrometry and bioinformatic analysis. Mol. Cell Proteomics 2004, 3, 441-555.
53. Faustin, B.; Rossignol, R.; Rocher, C.; Benard, G.; Malgat, M.; Letellier, T. Mobilization of adenine nucleotide translocators as molecular bases of the biochemical threshold effect observed in mitochondrial diseases. J. Biol. Chem. 2004, 279, 20411-20421.
54. Vahsen, N.; Cande, C.; Briere, J. J.; Benit, P.; Joza, N.; Larochette, N.; Mastroberardino, P. G.; Pequignot, M. O.; Casares, N.; Lazar, V.; Feraud, O.; Debili, N.; Wissing, S.; Engelhardt, S.; Madeo, F.; Piacentini, M.; Penninger, J. M.; Schagger, H.; Rustin, P.; Kroemer, G. AIF deficiency compromises oxidative phosphorylation. Embo J. 2004, 23, 4679-4689. Epub 2004 Nov 4.
55. Delaval, E.; Perichon, M.; Friguet, B. Age-related impairment of mitochondrial matrix aconitase and ATP-stimulated protease in rat liver and heart. Eur. J. Biochem. 2004, 271, 4559-4564.
56. Das, N.; Levine, R. L.; Orr, W. C.; Sohal, R. S. Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 2001, 360, 209-216.
57. Liang, L. P.; Patel, M. Iron-sulfur enzyme mediated mitochondrial superoxide toxicity in experimental Parkinson's disease. J. Neurochem. 2004, 90, 1076-1084.
58. Cooper, C. E. Nitric oxide and iron proteins. Biochim. Biophys. Acta 1999, 1411, 290-309.
59. Gardner, P. R.; Costantino, G.; Szabo, C.; Salzman, A. L. Nitric oxide sensitivity of the aconitases. J. Biol. Chem. 1997, 272, 25071-25076.
60. Castro, L.; Rodriguez, M.; Radi, R. Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J. Biol. Chem. 1994, 269, 29409-29415.
61. Sastre, J.; Pallardo, F. V.; Vina, J. The role of mitochondrial oxidative stress in aging. Free Radic Biol. Med. 2003, 35, 1-8.
62. Patel, M.; Li, Q. Y. Age dependence of seizure-induced oxidative stress. Neuroscience 2003, 118, 431-437.
63. Bota, D. A.; Davies, K. J. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol 2002, 4, 674-680.