The aryl hydrocarbon receptor interacts with ATP5α1, a subunit of the ATP synthase complex, and modulates mitochondrial function

Toxicology and Applied Pharmacology

Volumn 254, Issue 3, 2011, Pages 299-310

  Tappenden, Dorothy M ^a,b   Lynn, Scott G ^a,b   Crawford, Robert B ^c   Lee, KangAe ^a   Vengellur, Ajith ^a   Kaminski, Norbert E ^b,c   Thomas, Russell S ^d   LaPres, John J ^a,b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

Author keywords

Aryl hydrocarbon receptor; ATP synthase; ATP5a; Dioxin; Mitochondria

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE 5 ALPHA 1; AROMATIC HYDROCARBON RECEPTOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FRACTIONATION; COLLISIONALLY ACTIVATED DISSOCIATION; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; GEL ELECTROPHORESIS; GENE AMPLIFICATION; HEPATOMA CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ATP SYNTHETASE COMPLEXES; CELL LINE; CELL LINE, TUMOR; HOMEOSTASIS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MOLECULAR SEQUENCE DATA; OXIDATIVE PHOSPHORYLATION COUPLING FACTORS; PROTEIN BINDING; PROTEIN SUBUNITS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN;

MAMMALIA;

EID: 79960039241     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.05.004     Document Type: Article

References (51)

1. Aly H.A., Domenech O. Cytotoxicity and mitochondrial dysfunction of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in isolated rat hepatocytes. Toxicol. Lett. 2009, 191:79-87.
2. Arnold L.W., LoCascio N.J., Lutz P.M., Pennell C.A., Klapper D., Haughton G. Antigen-induced lymphomagenesis: identification of a murine B cell lymphoma with known antigen specificity. J. Immunol. 1983, 131:2064-2068.
3. Baran A.A., Silverman K.A., Zeskand J., Koratkar R., Palmer A., McCullen K., Curran W.J., Edmonston T.B., Siracusa L.D., Buchberg A.M. The modifier of Min 2 (Mom2) locus: embryonic lethality of a mutation in the Atp5a1 gene suggests a novel mechanism of polyp suppression. Genome Res. 2007, 17:566-576.
4. Barhoover M.A., Hall J.M., Greenlee W.F., Thomas R.S. Aryl hydrocarbon receptor regulates cell cycle progression in human breast cancer cells via a functional interaction with cyclin-dependent kinase 4. Mol. Pharmacol. 2009, 77:195-201.
5. Bishop G.A., Haughton G. Induced differentiation of a transformed clone of Ly-1+ B cells by clonal T cells and antigen. P. Natl. Acad. Sci. USA 1986, 83:7410-7414.
6. Blankenship A., Matsumura F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced activation of a protein tyrosine kinase, pp 60src, in murine hepatic cytosol using a cell-free system. Mol. Pharmacol. 1997, 52:667-675.
7. Bradfield C.A., Poland A. A competitive binding assay for 2,3,7,8-tetrachlorodibenzo-p-dioxin and related ligands of the Ah receptor. Mol. Pharmacol. 1988, 34:682-688.
8. Budas, G. R., Churchill, E. N., Disatnik, M. H., Sun, L., and Mochly-Rosen, D., 2010. Mitochondrial import of PKCepsilon is mediated by HSP90: a role in cardioprotection from ischaemia and reperfusion injury. Cardiovasc Res 88, 83-92.
9. Bunger M.K., Moran S.M., Glover E., Thomae T.L., Lahvis G.P., Lin B.C., Bradfield C.A. Resistance to 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity and abnormal liver development in mice carrying a mutation in the nuclear localization sequence of the aryl hydrocarbon receptor 10.1074/jbc.M209594200. J. Biol. Chem. 2003, 278:17767-17774.
10. Bunger M.K., Glover E., Moran S.M., Walisser J.A., Lahvis G.P., Hsu E.L., Bradfield C.A. Abnormal liver development and resistance to 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in mice carrying a mutation in the DNA-binding domain of the aryl hydrocarbon receptor. Toxicol. Sci. 2008, 106:83-92.
11. Carver L.A., LaPres J.J., Jain S., Dunham E.E., Bradfield C.A. Characterization of the Ah receptor-associated protein, ARA9. J. Biol. Chem. 1998, 273:33580-33587.
12. Chan W.K., Yao G., Gu Y.Z., Bradfield C.A. Cross-talk between the aryl hydrocarbon receptor and hypoxia inducible factor signaling pathways. Demonstration of competition and compensation. J. Biol. Chem. 1999, 274:12115-12123.
13. Daum G., Gasser S.M., Schatz G. Import of proteins into mitochondria. Energy-dependent, two-step processing of the intermembrane space enzyme cytochrome b2 by isolated yeast mitochondria. J. Biol. Chem. 1982, 257:13075-13080.
14. Denison M.S., Fisher J.M., Whitlock J.P. The DNA recognition site for the dioxin-Ah receptor complex. Nucleotide sequence and functional analysis. J. Biol. Chem. 1988, 263:17221-17224.
15. Dragin N., Shi Z., Madan R., Karp C.L., Sartor M.A., Chen C., Gonzalez F.J., Nebert D.W. Phenotype of the Cyp1a1/1a2/1b1-/- triple-knockout mouse. Mol. Pharmacol. 2008, 73:1844-1856.
16. Forgacs A.L., Burgoon L.D., Lynn S.G., LaPres J.J., Zacharewski T. Effects of TCDD on the expression of nuclear encoded mitochondrial genes. Toxicol. Appl. Pharmacol. 2010, 246:58-65.
17. Fujisawa-Sehara A., Sogawa K., Yamane M., Fujii-Kuriyama Y. Characterization of xenobiotic responsive elements upstream from the drug-metabolizing cytochrome P-450c gene: a similarity to glucocorticoid regulatory elements. Nucleic Acids Res. 1987, 15:4179-4191.
18. Ge N.-L., Elferink C.J. A direct interaction between the aryl hydrocarbon receptor and retinoblastoma protein. Linking dioxin signaling to the cell cycle. J. Biol. Chem. 1998, 273:22708-22713.
19. Halestrap A.P. Mitochondria and preconditioning: a connexin connection?. Circ. Res. 2006, 99:10-12.
20. Kang B.H., Plescia J., Dohi T., Rosa J., Doxsey S.J., Altieri D.C. Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network. Cell 2007, 131:257-270.
21. Kearney P.C., Woolson E.A., Isensee A.R., Helling C.S. Tetrachlorodibenzodioxin in the environment: sources, fate, and decontamination. Environ Health Perspect. 1973, 5:273-277.
22. Lee K., Burgoon L.D., Gier L.E., Dere E., Zacharewski T.R., Hogenesch J.B., LaPres J.J. Identification and characterization of genes susceptible to transcriptional cross-talk between the hypoxia and dioxin signaling cascades. Chem. Res. Toxicol. 2006, 1284-1293.
23. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
24. MacKenzie J.A., Payne R.M. Mitochondrial protein import and human health and disease. Biochim. Biophys. Acta 2007, 1772:509-523.
25. Mandal P.K. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. B 2005, 175:221-230.
26. Paajarvi G., Viluksela M., Pohjanvirta R., Stenius U., Hogberg J. TCDD activates Mdm2 and attenuates the p53 response to DNA damaging agents. Carcinogenesis 2005, 26:201-208.
27. Pennington K., Peng J., Hung C.C., Banks R.E., Robinson P.A. Differential effects of wild-type and A53T mutant isoform of alpha-synuclein on the mitochondrial proteome of differentiated SH-SY5Y cells. J. Proteome Res. 2010, 9:2390-2401.
28. Perdew G.H. Association of the Ah receptor with the 90-kDa heat shock protein. J. Biol. Chem. 1988, 263:13802-13805.
29. Poland A., Glover E. Chlorinated biphenyl induction of aryl hydrocarbon hydroxylase activity: a study of the structure activity relationship. Mol. Pharmacol. 1977, 13:924.
30. Poland A., Glover E. 2,3,7,8-Tetrachlorodibenzo-p-dioxin: segregation of toxicity with the Ah locus. Mol. Pharm. 1980, 17:86-94.
31. Poland A., Kende A. The genetic expression of aryl hydrocarbon hydroxylase activity: evidence for a receptor mutation in nonresponsive mice. Cold Spring Harbor Lab. 1977, 847-867.
32. Poland A., Knutson J.C. 2,3,7,8-tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu. Rev. Pharmacol. 1982, 22:517-554.
33. Poland A., Glover E., Kende A.S. Stereospecific, high affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol. Evidence that the binding species is receptor for induction of aryl hydrocarbon hydroxylase. J. Biol. Chem. 1976, 251:4936-4946.
34. Poland A., Greenlee W.F., Kende A.S. Studies on the mechanism of action of the chlorinated dibenzo-p-dioxins and related compounds. Ann. N.Y. Acad. Sci. 1979, 320:214-230.
35. Prokipcak R.D., Denison M.S., Okey A.B. Nuclear Ah receptor from mouse hepatoma cells: effect of partial proteolysis on relative molecular mass and DNA-binding properties. Arch. Biochem. Biophys. 1990, 283:476-483.
36. Puga A., Barnes S.J., Dalton T.P., Chang C., Knudsen E.S., Maier M.A. Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J. Biol. Chem. 2000, 275:2943-2950.
37. Ray S., Swanson H.I. Activation of the aryl hydrocarbon receptor by TCDD inhibits senescence: a tumor promoting event?. Biochem. Pharmacol. 2009, 77:681-688.
38. Schmidt J.V., Bradfield C.A. AH receptor signaling pathways. Annu. Rev Cell. Dev. Bi. 1996, 12:55-89.
39. Senft A.P., Dalton T.P., Nebert D.W., Genter M.B., Puga A., Hutchinson R.J., Kerzee J.K., Uno S., Shertzer H.G. Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radic. Biol. Med. 2002, 33:1268-1278.
40. Seth R., Keeley J., Abu-Ali G., Crook S., Jackson D., Ilyas M. The putative tumour modifier gene ATP5A1 is not mutated in human colorectal cancer cell lines but expression levels correlate with TP53 mutations and chromosomal instability. J. Clin. Pathol. 2009, 62:598-603.
41. Shertzer H.G., Genter M.B., Shen D., Nebert D.W., Chen Y., Dalton T.P. TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F(0)F(1)-ATP synthase and ubiquinone. Toxicol. Appl. Pharmacol. 2006, 217:363-374.
42. Shertzer H.G., Schneider S.N., Kendig E.L., Clegg D.J., D'Alessio D.A., Johansson E., Genter M.B. Tetrahydroindenoindole inhibits the progression of diabetes in mice. Chem. Biol. Interact. 2009, 177:71-80.
43. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
44. Slavin S., Strober S. Spontaneous murine B-cell leukaemia. Nature 1978, 272:624-626.
45. Tian Y., Rabson A.B., Gallo M.A. Ah receptor and NF-[kappa]B interactions: mechanisms and physiological implications. Chem. Biol. Interact. 2002, 141:97-115.
46. Uemura H., Arisawa K., Hiyoshi M., Kitayama A., Takami H., Sawachika F., Dakeshita S., Nii K., Satoh H., Sumiyoshi Y., Morinaga K., Kodama K., Suzuki T., Nagai M. Prevalence of metabolic syndrome associated with body burden levels of dioxin and related compounds among Japan's general population. Environ Health Perspect. 2009, 117:568-573.
47. Van Gurp J.R., Hankinson O. Isolation and characterization of revertants from four different classes of aryl hydrocarbon hydroxylase-deficient hepa-1 mutants. Mol. Cell. Biol. 1984, 4:1597-1604.
48. Vengellur A., LaPres J.J. The role of hypoxia inducible factor 1{alpha} in cobalt chloride induced cell death in mouse embryonic fibroblasts. Toxicol. Sci. 2004, 82:638-646.
49. Yano M., Terada K., Mori M. AIP is a mitochondrial import mediator that binds to both import receptor Tom20 and preproteins. J. Cell Biol. 2003, 163:45-56.
50. Young J.C., Hoogenraad N.J., Hartl F.U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003, 112:41-50.
51. Yusenko M.V., Ruppert T., Kovacs G. Analysis of differentially expressed mitochondrial proteins in chromophobe renal cell carcinomas and renal oncocytomas by 2-D gel electrophoresis. Int. J. Biol. Sci. 2010, 6:213-224.