Analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced proteome changes in 5L rat hepatoma cells reveals novel targets of dioxin action including the mitochondrial apoptosis regulator VDAC2

Molecular and Cellular Proteomics

Volumn 7, Issue 2, 2008, Pages 394-410

  Sarioglu, Hakan ^a   Brandner, Stefanie ^a   Haberger, Markus ^a   Jacobsen, Carola ^a   Lichtmannegger, Josef ^a   Wormke, Mark ^a   Andrae, Ulrich ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ADENOSYLHOMOCYSTEINASE; AROMATIC HYDROCARBON RECEPTOR; ASPARTATE TRANSFER RNA LIGASE; BETA ACTIN; CALPHOBINDIN II; CELL PROTEIN; COMPLEMENT COMPONENT C1; COPPER ZINC SUPEROXIDE DISMUTASE; DIHYDRORHODAMINE 123; GLUTATHIONE TRANSFERASE A2; GLUTATHIONE TRANSFERASE P1; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HYDROXYMETHYLGLUTARYL COENZYME A SYNTHASE; INITIATION FACTOR 4A; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LAMIN A; LEUKOTRIENE A4 HYDROLASE; LIPOCORTIN 1; MALATE DEHYDROGENASE; PROLYL ENDOPEPTIDASE; PROTEIN BAK; PROTEOME; PYRUVATE CARBOXYLASE; TRANSALDOLASE; TRANSCRIPTION FACTOR NRF2; VIMENTIN; VOLTAGE DEPENDENT ANION CHANNEL 2;

ANIMAL CELL; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; HEPATOMA CELL; HOMEOSTASIS; LIVER MITOCHONDRION; LIVER TOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEOMICS; RAT; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MITOCHONDRIAL PROTEINS; NEOPLASM PROTEINS; OXIDATIVE STRESS; PROTEOME; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; VOLTAGE-DEPENDENT ANION CHANNEL 2;

RATTUS;

EID: 39749127706     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700258-MCP200     Document Type: Article

References (100)

1. Gold, L. S., Slone, T. H., Manley, N. B., Garfinkel, G. B., Hudes, E. S., Rohrbach, L., and Ames, B. N. (1991) The Carcinogenic Potency Data-base, analyses of 4000 chronic animal cancer expedments published in the general literature and by the U.S. National Cancer Institute/ National Toxicology Program. Environ. Health Perspect. 96, 11-15
2. International Agency for Research an Cancer (IARC) (1997) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: Polychlorinated Dibenzo-para-dioxins and Polychlorinated Dibenzofurans, Vol. 69, International Agency for Research on Cancer, Lyon, France
3. Steenland, K., Bertazzi, P., Baccarelli, A., and Kogevinas, M. (2004) Dioxin revisited: developments since the 1997 IARC classification of dioxin as a human carcinogen. Environ. Health Perspect. 112, 1265-1268
4. Whitlock, J. P., Jr. (1999) Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol. 39, 103-125
5. Safe, S. (2001) Molecular biology of the Ah receptor and its role in carcinogenesis. Toxicol. Lett. 120, 11-7
6. Sogawa, K., Numayama-Tsuruta, K., Takahashi, T., Matsushita, N., Miura, C., Nikawa, J., Gotoh, O., Kikuchi, Y., and Fujii-Kuriyama, Y. (2004) A novel induction mechanism of the rat CYP1A2 gene mediated by Ah receptor-Amt heterodimer. Biochem. Biophys. Res. Commun. 318, 746-755
7. Boutros, P. C., Moffat, I. D., Franc, M. A., Tijet, N., Tuomisto, J., Pohjanvirta, R., and Okey, A. B. (2004) Dioxin-responsive AHRE-II gene battery, identification by phylogenetic footprinting. Biochem. Biophys. Res. Commun. 321, 707-715
8. Radjendirane, V., and Jaiswal, A. K. (1999) Antioxidant response element-mediated 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induction of human NAD(P)H:quinone oxidoreductase 1 gene expression. Biochem. Pharmacol. 58, 1649-1655
9. Enan, E., and Matsumura, F. (11996) Identification of c-Src as the integral component of the cytosolic Ah receptor complex, transducing the signal of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) through the protein phosphorylation pathway. Biochem. Pharmacol. 52, 1599-1612
10. Puga, A., Barnes, S. J., Dalton, T. P., Chang, C., Knudsen, E. S., and Maier, M. A. (2000) Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transccription and cell cycle arrest. J. Biol. Chem. 275, 2943-2950
11. Weiss, C., Faust, D., Durk, H., Kolluri, S. K., Pelzer, A., Schneider, S., Dietrich, C., Oesch, F., and Göttlicher, M. (2005) TCDD induces c-jun expression via a novel Ah (dioxin) receptor-mediated p38-MAPK-dependent pathway. Oncogene 24, 4975-4983
12. Puga, A., Maier, A., and Medvedovic, M. (2000) The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem. Pharmacol. 60, 1129-1142
13. Frueh, F. W., Hayashibara, K. C., Brown, P. O., and Whitlock, J. P., Jr. (2001) Use of cDNA microarrays to analyze dioxin-induced changes in human liver gene expression. Toxicol. Lett. 122, 189-203
14. Kolluri, S. K., Balduf, C., Hofmann, M., and Göttlicher, M. (2001) Novel target genes of the Ah (dioxin) receptor, transccriptional induction of N-myristoyltransferase 2. Cancer Res. 61, 8534-8539
15. Kurachi, M., Hashimoto, S., Obata, A., Nagai, S., Nagahata, T., Inadera, H., Sone, H., Tohyama, C., Kaneko, S., Kobayashi, K., and Matsushima, K. (2002) Identification of 2,3,7,8-tetrachlorodibenzo-p-dioxin-responsive genes in mouse liver by serial analysis of gene expression. Biochem. Biophys. Res. Commun. 292, 368-377
16. Zeytun, A., McKallip, R. J., Fisher, M., Camacho, I., Nagarkatti, M., and Nagarkatti, P. S. (2002) Analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced gene expression profile in vivo using pathway-specific cDNA arrays. Toxicology 178, 241-260
17. Boverhof, D. R., Burgoon, L. D., Tashiro, C., Chittim, B., Harkema, J. R., Jump, D. B., and Zacharewski, T. R. (2005) Temporal and dose-dependent hepatic gene expression patterns in mice provide new insights into TCDD-mediated hepatotoxicity. Toxicol. Sci. 85, 1048-1063
18. Boverhof, D. R., Burgoon, L. D., Tashiro, C., Sharratt, B., Chittim, B., Harkema, J. R., Mendrick, D. L., and Zacharewski, T. R. (2006) Comparative toxicogenomic analysis of the hepatotoxic effects of TCDD in Sprague Dawley rats and C57BL/6 mice. Toxicol. Sci. 94, 398-416
19. Fletcher, N., Wahistrom, D., Lundberg, R., Nilsson, C. B., Nilsson, K. C., Stockling, K., Hellmold, H., and Hakansson, H. (2005) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters the mRNA expression of critical genes associated with cholesterol metabolism, bile acid biosynthesis, and bile transport in rat liver, a microarray study. Toxicol. Appl. Pharmacol. 207, 1-24
20. Tijet, N., Boutros, P. C., Moffat, I. D., Okey, A. B., Tuomisto, J., and Pohjanvirta, R. (2006) Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Mol. Pharmacol. 69, 140-153
21. Lee, S. H., Lee, D. Y., Son, W. K., Joo, W. A., and Kim, C. W. (2005) Proteomic characterization of rat liver exposed to 2,3,7,8-tetrachlorobenzo-p-dioxin. J. Proteome Res. 4, 335-343
22. Pastorelli, R., Carpi, D., Campagna, R., Airoldi, L., Pohjanvirta, R., Viluksela, M., Hakansson, H., Boutros, P. C., Moffat, I. D., Okay, A. B., and Fanelli, R. (2006) Differential expression profiling of the hepatic proteome in a rat model of dioxin resistance, correlation with genomic and transcriptomic analyses. Mol. Cell. Proteomics 5, 882-894
23. Oberemm, A., Meckert, C., Brandenburger, L., Herzig, A., Lindner, Y., Kalenberg, K., Krause, E., Ittrich, C., Kopp-Schneider, A., Stahlmann, R., Richter-Reichhelm, H. B., and Gundert-Remy, U. (2005) Differential signatures of protein expression in marmoset liver and thymus induced by single-dose TCDD treatment. Toxicology 206, 33-48
24. Wildgruber, R., Harder, A., Obermaier, C., Boguth, G., Weiss, W., Fey, S. J., Larsen, P. M., and Görg, A. (2000) Towards higher resolution, two-dimensional electrophoresis of Saccharomyces cerevisiae proteins using overlapping narrow immobilized pH gradients. Electrophoresis 21, 2610-2616
25. Görg, A., Weiss, W., and Dunn, M. J. (2004) Current two-dimensional electrophoresis technology for proteomics. Proteomics, 4, 3665-3685
26. Göttlicher, M., Cikryt, P., and Wiebel, F. J. (1990) Inhibition of growth by 2,3,7,8-tetrachlorodibenzo-p-dioxin in 5L rat hepatoma cells is associated with the presence of Ah receptor. Carcinogenesis 11, 2205-2210
27. Göttlicher, M., and Wiebel, F. J. (1991) 2,3,7,8-Tetrachlorodibenzo-p-dioxin causes unbalanced growth in 5L rat hepatoma cells. Toxicol. Appl. Pharmacol. 111, 496-503
28. Wiebel, F. J., Klose, U., and Kiefer, F. (1991) Toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in vitro, H411EC3-derived 5L hepatoma cells as a model system. Toxicol. Lett. 55, 161-169
29. Weiss, C., Kolluri, S. K., Kiefer, F., and Göttlicher, M. (1996) Complementation of Ah receptor deficiency in hepatoma cells, negative feedback regulation and cell cycle control by the Ah receptor. Exp. Cell Res. 226, 154-163
30. Ge, N. L., and Elferink, C. J. (1998) A direct interaction between the aryl hydrocarbon receptor and retinoblastoma protein. J. Biol. Chem. 273, 22708-22713
31. Reiners, J. J., Jr., Clift, R., and Mathieu, P. (1999) Suppression of cell cycle progression by flavonoids: dependence on the aryl hydrocarbon receptor. Carcinogenesis 20, 1561-1566
32. Elferink, C. J., Ge, N. L., and Levine, A. (2001) Maximal aryl hydrocarbon receptor activity depends on an interaction with the retinoblastoma protein. Mol. Pharmacol. 59, 664-673
33. Levine-Fridman, A., Chen, L., and Elferink, C. J. (2004) Cytochrome P4501A1 promotes G1 phase cell cycle progression by controlling aryl hydrocarbon receptor activity. Mol. Pharmacol. 65, 461-469
34. Munzel, P. A., Schmohl, S., Buckler, F., Jaehrling, J., Raschko, F. T., Köhle, C., and Bock, K. W. (2003) Contribution of the Ah receptor to the phenolic antioxidant-mediated expression of human and rat UDP-glucuronosyltransferase UGT1A6 in Caco-2 and rat hepatoma 5L cells. Biochem. Pharmacol. 66, 841-847
35. Kolluri, S. K., Weiss, C., Koff, A., and Göttlicher, M. (1999) p27 (Kip1) induction and inhibition of proliferation by the intracellular Ah receptor in developing thymus and hepatoma cells. Genes Dev. 13, 1742-17453
36. Schmidt, A., Kellermann, J., and Lottspeich, F. (2005) A novel strategy for quantitative proteomics using isotope-coded protein labels. Proteomics 5 ,4-15
37. Sarioglu, H., Brandner, S., Jacobsen, C., Meindl, T., Schmidt, A., Kellermann, J., Lottspeich, F., and Andrae, U. (2006) Quantitative analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced proteome alterations in 5L rat hepatoma cells using isotope-coded protein labels. Proteomics 6, 2407-2421
38. DeSouza, L., Diehl, G., Rodrigues, M. J., Guo, J., Romaschin, A. D., Colgan, T. J., and Siu, K. W. (2005) Search for cancer markers from endometrial tissues using differentially labeled tags iTRAQ and cICAT with multidimensional liquid chromatography and tandem mass spectrometry. J. Proteome Res. 4, 377-386
39. Wu, W., Wang, G., Baek, S. J., and Shen, R. F. (2006) Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J. Proteome Res. 5, 651-658
40. Moore, E. E., and Weiss, M. C. (1982) Selective isolation of stable and unstable dedifferentiated variants from a rat hepatoma cell line. J. Cell. Physiol. 111, 1-8
41. Pitot, H., Peraino, C., Morse, P. A., and Potter, V. E. (1964) Hepatomas in tissue culture compared with adapting liver in vivo. Natl. Cancer Inst. Monogr. 13, 229-246
42. Reuber, M. D., (1961) A transplantable bile-secreting hepatocellular carcinoma in the rat. J. Natl. Cancer Inst. 26, 891-900
43. Lamanda, A., Zahn, A., Roder, D., and Langan, H. (2004) Improved ruthenium II tris (bathophenantroline disulfonate) staining and destaining protocol for a better signal-to-background ratio and improved baseline resolution. Proteomics 4, 599-608
44. Shevchenko, A., Wilm, W., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
45. 2+/calmodulin kinase II in rod outer segments. Mol. Cell. Proteomics 5, 324 -336
46. Miao, W., Hu, L., Kandouz, M., and Batist, G. (2003) Oltipraz is a bifunctional inducer activating both phase I and phase II drug-metabolizing enzymes via the xenobiotic responsive element. Mol. Pharmacol. 64, 346-354
47. Kwak, M. K., Wakabayashi, N., Itoh, K, Motohashi, H., Yamamoto, M., and Kensler, T. W. (2003) Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1 -Nrf2 pathway. Identification of novel gene clusters for cell survival. J. Biol. Chem. 278, 8135-8145
48. Thimmulappa, R. K., Mai, K. H., Srisuma, S., Kensler, T. W., Yamamoto, M., and Biswal, S. (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62, 5196-5203
49. Ellis, E. M., Slattery, C. M., and Hayes, J. D. (2003) Characterization of the rat aflatoxin B1 aldehyde reductase gene, AKR7A1. Structure and chromosomal localization of AKR7A1 as well as identification of antioxidant response elements in the gene promoter. Carcinogenesis 24, 727-737
50. Dos Remedios, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A., and Nosworthy, N. J. (2003) Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83, 433-473
51. Valpuesta, J. M., Martin-Benito, J., Gomez-Puertas, P., Carrascosa, J. L., and Willison, K. R. (2002) Structure and function of a protein folding machine, the eukaryotic cytosolic chaperonin CCT. FEBS Lett. 529, 11-16
52. Yu, J. H., Yun, S. Y., Lim, J. W., Kim, H., and Kim, K. H. (2003) Mass spectrometry and tandem mass spectrometry analysis of rat mitochondrial ATP synthase, up-regulation in pancreatic acinar cells treated with cerulein. Proteomics 3, 2437-2445
53. Miller, I., Gemeiner, M., Gessibauer, B., Kungl, A., Piskemik, C., Haindl, S., Numberger, S., Bahrami, S., Redl, H., and Kozlov, A. V. (2006) Proteome analysis of rat liver mitochondria reveals a possible compensatory response to enclotoxic shock. FEBS Lett. 580, 1257-1262
54. Setoguchi, K., Otera, H., and Mihara, K. (2006) Cytosolic factor and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J. 25, 5635-5647
55. Cheng, E. H., Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301, 513-517
56. Ishii, T., Itoh, K., Takahashi, S., Sato, H., Yanagawa, T., Katoh, Y., Bannai, S., and Yamamoto, M. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275, 16023-16029
57. Wakabayashi, N., Dinkova-Kostova, A. T., Holtzclaw, W. D., Kang, M. I., Kobayashi, A., Yamamoto, M., Kensler, T. W., and Talalay, P. (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. U. S. A. 101, 2040-2045
58. Kang, K. W., Lee, S. J., and Kim, S. G. (2005) Molecular mechanism of nrf2 activation by oxidative stress. Antioxid. Redox Signal. 7, 1664-1673
59. Hanlon, P. R., Zheng, W., Ko, A. Y., and Jefcoate, C. R. (2005) Idehtification of novel TCDD-regulated genes by microarray analysis. Toxicol. Appl. Pharmacol. 202, 215-228
60. Boesch, J. S., Miskimins, R., Miskimins, W. K., and Lindahl, R. (1990) The same xenobiotic response element is required for constitutive and inducible expression of the mammalian aldehyde dehydrogenase-3 gene. Arch. Biochem. Biophys. 361, 223-230
61. Favreau, L. V., and Pickett, C. B. (1991) Transcriptional regulation of the rat NAD(P)H:quinone reductase gene. Identification of regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J. Biol. Chem. 266, 4556-4561
62. Rushmore, T. H., King, R. G., Paulson, K. E., and Pickett, C. B. (1990) Regulation of glutathione S-transferase Ya subunit gene expression, identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc. Natl. Acad. Sci. U. S. A. 87, 3826-3830
63. Schrenk, D. (1998) Impact of dioxin-type induction of drug-metabolizing enzymes on the metabolism of endo- and xenobiotics. Biochem. Pharmacol. 55, 1155-1162
64. Santostefano, M. J., Ross, D. G., Savas, U., Jefcoate, C. R., and Birnbaum, L. S. (1997) Differential time-course and dose-response relationships of TCDD-induced CYP1B1, CYP1A1, and CYP1A2 proteins in rats. Biochem. Biophys. Res. Commun. 233, 20-24
65. Fountoulakis, M., Juranville, J. F., Berndt, P., Langan, H., and Suter, L. (2001) Two-dimensional database of mouse liver proteins. An update. Electrophoresis 22, 1747-1763
66. Fountoulakis, M., and Suter, L. (2002) Proteomic analysis of the rat liver. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 782, 197-218
67. Eliasson, E., Mkrtchian, S., Halper, J. R., and Ingelman-Sundberg, M. (1994) Substrate-regulated, cAMP-dependent phosphorylation, denaturation, and degradation of glucocorticoid-inclucible rat liver cytochrome P450 3A1. J. Biol. Chem. 269, 18378-18383
68. Wang, X., Medzihradszky, K. F., Maltby, D., and Correia, M. A. (2001) Phosphorylation of native and heme-modified CYP3A4 by protein kinase C, a mass spectrometric characterization of the phosphorylated peptides. Biochemistry 40, 11318-11326
69. Favreau, L. V., and Pickett, C. B. (1993) Transcriptional regulation of the rat NAD(P)H:quinone reductase gene. Characterization of a DNA-protein interaction at the antioxidant responsive element and induction by 12-O-tetradecanoylphorbol 13-acetate. J. Biol. Chem. 268, 19875-19881
70. Rushmore, T. H., Morton, M. R., and Pickett, C. B. (11991) The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266, 11632-11639
71. Pulford, D. J., and Hayes, J. D. (1996) Characterization of the rat glutathione S-transferase Yc2 subunit gene, GSTA5, identification of a putative antioxidant-responsive element in the 5′-flanking region of rat GSTA5 that may mediate chemoprotection against aflatoxin B1. Biochem. J. 318, 75-84
72. Okuda, A., Imagawa, M., Maeda, Y., Sakai, M., and Muramatsu, M. (1989) Structural and functional analysis of an enhancer GPEI having a phorbol 12-O-tetradecanoate 13-acetate responsive element-like sequence found in the rat glutathione transferase P gene. J. Biol. Chem. 264, 16919-16926
73. Yates, M. S., Kwak, M. K., Egner, P. A., Groopman, J. D., Bodreddigari, S., Sutter, T. R., Baurngartner, K. J., Roebuck, B. D., Liby, K. T., Yore, M. M., Honda, T., Gribble, G. W., Sporn, M. B., and Kensler, T. W. (2006) Potent protection against aflatoxin-induced tumorigenesis through induction of Nrf2-regulated pathways by the triterpenoid 1-[2-cyano-3-,12-dioxooleana-1,9(11)-dien-28-oyl] imidazole. Cancer Res. 66, 2488-2494
74. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M., and Nabeshima, Y. (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322
75. Arthur, J. R., Morrice, P. C., Nicol, F., Beddows, S. E., Boyd, R., Hayes, J. D., and Beckett, G. J. (1987) The effects of selenium and copper deficiencies on glutathione S-transferase and glutathione peroxidase in rat liver. Biochem. J. 248, 539-544
76. Khan, M. F., Srivastava, S. K., Singhal, S. S., Chaubey, M., Awasthi, S., Petersen, D. R., Ansari, G. A., and Awasthi, Y. C. (1995) Iron-induced lipid peroxidation in rat liver is accompanied by preferential induction of glutathione S-transferase 8-8 isozyme. Toxicol. Appl. Pharmacol. 13l, 63-72
77. Xia, C., Hu, J., Ketterer, B., and Taylor, J. B. (1996) The organization of the human GSTP1-1 gene promoter and its response to retinoic acid and cellular redox status. Biochem. J. 313, 155-161
78. Adler, V., Yin, Z., Fuchs, S. Y., Benezra, M., Rosario, L., Tew, K. D., Pincus, M. R., Sardana, M., Henderson, C. J., Wolf, C. R., Davis, R. J., and Ronai, Z. (1999) Regulation of JNK signaling by GSTp. EMBO J. 18, 132113-132134
79. Wang, T., Arifoglu, P., Ronai, Z., and Tew, K. D. (2001) Glutathione S-transferase P1-1 (GSTP1-1) inhibits c-Jun N-terminal kinase (JNK1) signaling through interaction with the C terminus. J. Biol. Chem. 276, 20999-21003
80. Devary, Y., Gottlieb, R. A., Smeal, T., and Karin, M. (1992) The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71, 1081-1091
81. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., and Greenberg, M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331
82. Kirsch, M., and De Groot, H. (2001) NAD(P)H, a directly operating antioxidant? FASEB J. 15, 1569-1574
83. Srivastava, S., Harter, T. M., Chandra, A., Bhatnagar, A., Srivastava, S. K., and Petrash, J. M. (1998) Kinetic studies of FR-1, a growth factor-inducible aldo-keto reductase. Biochemistry 37, 12909-12917
84. Donohue, P. J., Alberts, G. F., Hampton, B. S., and Winkles, J. A. (1994) A delayed-early gene activated by fibroblast growth factor-1 encodes a protein related to aldose reductase. J. Biol. Chem. 269, 8604-8609
85. Butkevich, E., Hütsmann, S., Wenzel, D., Shirao, T., Duden, R., and Majoul, I. (2004) Drebrin is a novel connexin-43 binding partner that links gap junctions to the submembrane cytoskeleton. Curr. Biol. 14, 650-658
86. Baker, T. K., Kwiatkowski, A. P., Madhukar, B. V., and Klaunig, J. E. (1995) Inhibition of gap junctional intercellular communication by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in rat hepatocytes. Carcinogenesis 16, 2321-2326
87. Diry, M., Tomkiewicz, C., Koehle, C., Coumoul, X., Bock, K. W., Barouki, R., and Transy, C. (2006) Activation of the dioxin/aryl hydrocarbon receptor (AhR) modulates cell plasticity through a JNK-dependent mechanism. Oncogene 25, 5570-5574
88. Stohs, S. J., Alsharif, N. Z., Shara, M. A., al-Bayati, Z. A., and Wahba, Z. Z. (1991) Evidence for the induction of an oxidative stress in rat hepatic mitochondria by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Adv. Exp. Med. Biol. 283, 827-831
89. Senft, A. P., Dalton, T. P., Nebert, D. W., Genter, M. B., Hutchinson, R. J., and Shertzer, H. G. (2002) Dioxin increases reactive oxygen production in mouse liver mitochondria. Toxicol. Appl. Pharmacol. 178, 15-21
90. Shen, D., Dalton, T. P., Nebert, D. W., and Shertzer, H. G. (2005) Glutsthione redox state regulates mitochondrial reactive oxygen production. J. Biol. Chem. 280, 25305-25312
91. 1-ATP synthase and ubiquinone. Toxicol. Appl. Pharmacol. 217, 363-374
92. Baines, C. P., Song, C. X., Zheng, Y. T., Wang, G. W., Zhang, J., Wang, O. L., Guo, Y., Bolli, R., Cardwell, E. M., and Ping, P. (2003) Protein kinase Cε interacts with and inhibits the permeability transition pore in cardiac mitochondria. Orc. Res. 92, 873-880
93. Majewski, N., Nogueira, V., Bhaskar, P., Coy, P. E., Skeen, J. E., Gottlob, K., Chandel, N. S., Thompson, C. B., Robey, R. B., and Hay, N. (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830
94. Robey, R. B., and Hay, N. (2006) Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene 25, 4683-4696
95. Lemasters, J. J., and Holmuhamedov, E. (2006) Voltage-dependent anion channel (VDAC) as mitochondrial governator - thinking outside the box. Biochim. Biophys. Acta 1762, 181-190
96. Yamamoto, T., Yamada, A., Watanabe, M., Yoshimura, Y., Yamazaki, N., Yoshimura, Y., Yamauchi, T., Kataoka, M., Nagata, T., Terada, H., and Shinohara, Y. (20065) VDAC1, having a shorter N-terminus than VDAC2 but showing the same migration in an SDS-polyacrylamide gel, is the predominant form expressed in mitochondria of various tissues. J. Proteome Res. 5, 3336-3344
97. Liberatori, S., Canas, B., Tani, C., Bini, L., Buonocore, G., Godovac-Zimmermann, J., Mishra, O. P., Delivoria-Papadopoulos, M., Bracci, R., and Pallini, V. (20134) Proteomic approach to the identification of voltage-dependent anion channel protein isoforms in guinea pig brain synaptosomes. Proteomics 4, 1335-1340
98. Kim, S. C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Chang, T., Kho, Y., Xiao, H., Xiao, L., Grishin, N. V., White, M., Yang, X. J., and Zhao, Y. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 23, 607-618
99. Jin, K., Mao, X. O., Eshoo, M. W., del Rio, G., Rao, R., Chen, D., Simon, R. P., and Greenberg, D. A. (2002) cDNA microarray analysis of changes in gene expression induced by neuronal hypoxia in vitro. Neurochem. Res. 27, 1105-1112
100. Wolff, S., Otto, A., Albrecht, D., Zeng, J. S., Buttner, K., Gluckmann, M., Hecker, M., and Becher, D. (2006) Gel-free and gel-based proteomics in Bacillus subtilis, a comparative study. Mol. Cell. Proteomics. 5, 1183-1192