Mitochondrial targeting of mouse NQO1 and CYP1B1 proteins

Biochemical and Biophysical Research Communications

Volumn 435, Issue 4, 2013, Pages 727-732

  Dong, Hongbin ^a   Shertzer, Howard G ^a   Genter, Mary Beth ^a   Gonzalez, Frank J ^b   Vasiliou, Vasilis ^c   Jefcoate, Colin ^d   Nebert, Daniel W ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

CYP1A1; Cytochrome P450 1B1 (CYP1B1); Dioxin inducible enzymes; Endoplasmic reticulum targeting; Mitochondrial targeting; Mouse tissues (lung, spleen, uterus, small intestine, liver, kidney); NAD(P)H:quinone oxidoreductase 1 (NQO1); Subcellular localization

Indexed keywords

CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; DIHYDROPTERIDINE REDUCTASE; DIOXIN; OXIDOREDUCTASE; QUINONE OXIDOREDUCTASE 1; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSOL; DETOXIFICATION; ENDOPLASMIC RETICULUM; FEMALE; METABOLIC ACTIVATION; MICROSOME; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CELLS, CULTURED; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NAD(P)H DEHYDROGENASE (QUINONE);

MUS;

EID: 84878971174     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.05.051     Document Type: Article

References (43)

1. Anandatheerthavarada H.K., Addya S., Dwivedi R.S., Biswas G., Mullick J., Avadhani N.G. Localization of multiple forms of inducible cytochromes P450 in rat liver mitochondria: immunological characteristics and patterns of xenobiotic substrate metabolism. Arch. Biochem. Biophys. 1997, 339:136-150.
2. Anandatheerthavarada H.K., Addya S., Mullick J., Avadhani N.G. Interaction of adrenodoxin with P450 1A1 and its truncated form P450MT2 through different domains: differential modulation of enzyme activities. Biochemistry 1998, 37:1150-1160.
3. Anandatheerthavarada H.K., Biswas G., Mullick J., Sepuri N.B., Otvos L., Pain D., Avadhani N.G. Dual targeting of cytochrome P450 2B1 to endoplasmic reticulum and mitochondria involves a novel signal activation by cyclic AMP-dependent phosphorylation at Ser-128. EMBO J. 1999, 18:5494-5504.
4. Anandatheerthavarada H.K., Biswas G., Robin M.A., Avadhani N.G. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol. 2003, 161:41-54.
5. Bhagwat S.V., Biswas G., Anandatheerthavarada H.K., Addya S., Pandak W., Avadhani N.G. Dual targeting property of the N-terminal signal sequence of P450 1A1. Targeting of heterologous proteins to endoplasmic reticulum and mitochondria. J. Biol. Chem. 1999, 274:24014-24022.
6. Bianchet M.A., Faig M., Amzel L.M. Structure and mechanism of NAD(P)H: quinone acceptor oxidoreductases (NQOs). Methods Enzymol. 2004, 382:144-174.
7. Buters J.T., Sakai S., Richter T., Pineau T., Alexander D.L., Savas U., Doehmer J., Ward J.M., Jefcoate C.R., Gonzalez F.J. Cytochrome P450 CYP1B1 determines susceptibility to 7,12-dimethylbenzo[a]anthracene-induced lymphomas. Proc. Natl. Acad. Sci. USA 1999, 96:1977-1982.
8. Chen Y., Yang Y., Miller M.L., Shen D., Shertzer H.G., Stringer K.F., Wang B., Schneider S.N., Nebert D.W., Dalton T.P. Hepatocyte-specific Gclc deletion leads to rapid onset of steatosis with mitochondrial injury and liver failure. Hepatology 2007, 45:1118-1128.
9. Dalton T.P., Dieter M.Z., Matlib R.S., Childs N.L., Shertzer H.G., Genter M.B., Nebert D.W. Targeted knockout of Cyp1a1 gene does not alter hepatic constitutive expression of other genes in the mouse [Ah] battery. Biochem. Biophys. Res. Commun. 2000, 267:184-189.
10. Dong H., Dalton T.P., Miller M.L., Chen Y., Uno S., Shi Z., Shertzer H.G., Bansal S., Avadhani N.G., Nebert D.W. Knock-in mouse lines expressing either mitochondrial or microsomal CYP1A1: differing responses to dietary benzo[a]pyrene as proof of principle. Mol. Pharmacol. 2009, 75:555-567.
11. Ernster L., Danielson L., Ljunggren M. DT diaphorase. I. Purification from the soluble fraction of rat-liver cytoplasm, and properties. Biochim. Biophys. Acta 1962, 58:171-188.
12. Franke W.W., Kartenbeck J. Outer mitochondrial membrane continuous with endoplasmic reticulum. Protoplasma 1971, 73:35-41.
13. Gálvez-Peralta M., Shi Z., Chen J., Miller M.L., Nebert D.W. Oral benzo[a]pyrene in Cyp1a1/1b1(-/-) double-knockout mice. Microarray analysis during squamous cell carcinoma formation in preputial gland duct. Int. J. Cancer 2013, 132:2065-2075.
14. Genter M.B., Clay C.D., Dalton T.P., Dong H., Nebert D.W., Shertzer H.G. Comparison of mouse hepatic mitochondrial versus microsomal cytochromes P450 following TCDD treatment. Biochem. Biophys. Res. Commun. 2006, 342:1375-1381.
15. Hartl F.U., Pfanner N., Nicholson D.W., Neupert W. Mitochondrial protein import. Biochim. Biophys. Acta 1989, 988:1-45.
16. Jones D.P. Disruption of mitochondrial redox circuitry in oxidative stress. Chem. Biol. Interact. 2006, 163:38-53.
17. Kimura S., Kawabe M., Ward J.M., Morishima H., Kadlubar F.F., Hammons G.J., Fernandez-Salguero P., Gonzalez F.J. CYP1A2 is not the primary enzyme responsible for 4-aminobiphenyl-induced hepatocarcinogenesis in mice. Carcinogenesis 1999, 20:1825-1830.
18. Ma X., Idle J.R., Malfatti M.A., Krausz K.W., Nebert D.W., Chen C.S., Felton J.S., Waxman D.J., Gonzalez F.J. Mouse lung CYP1A1 catalyzes the metabolic activation of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 2007, 28:732-737.
19. Murray G.I., Melvin W.T., Greenlee W.F., Burke M.D. Regulation, function, and tissue-specific expression of cytochrome P450 CYP1B1. Annu. Rev. Pharmacol. Toxicol. 2001, 41:297-316.
20. Nebert D.W., Dalton T.P. The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat. Rev. Cancer 2006, 6:947-960.
21. Nebert D.W., Dalton T.P., Okey A.B., Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279:23847-23850.
22. Nebert D.W., Karp C.L. Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J. Biol. Chem. 2008, 283:36061-36065.
23. Nebert D.W., Wikvall K., Miller W.L. Human cytochromes P450 in health and disease. Philos. Trans. R. Soc. London B Biol. Sci. 2013, 368:20120431.
24. Nelson D.R., Zeldin D.C., Hoffman S.M., Maltais L.J., Wain H.M., Nebert D.W. Comparison of cytochrome P450 (CYP) genes from the mouse and human genomes, including nomenclature recommendations for genes, pseudogenes and alternative-splice variants. Pharmacogenetics 2004, 14:1-18.
25. Pottenger L.H., Christou M., Jefcoate C.R. Purification and immunological characterization of a novel cytochrome P450 from C3H/10T1/2 cells. Arch. Biochem. Biophys. 1991, 286:488-497.
26. Radjendirane V., Joseph P., Lee Y.H., Kimura S., Klein-Szanto A.J., Gonzalez F.J., Jaiswal A.K. Disruption of the DT diaphorase gene (Nqo1) in mice leads to increased menadione toxicity. J. Biol. Chem. 1998, 273:7382-7389.
27. Rapoport T.A. Protein translocation across and integration into membranes. CRC Crit. Rev. Biochem. 1986, 20:73-137.
28. Rendic S., Guengerich F.P. Summary of information on the effects of diseases and environmental factors on human cytochrome P450 (CYP) enzymes and transporters. Curr. Drug Metab. 2010, 11:4-84.
29. Robertson J.A., Chen H.C., Nebert D.W. NAD(P)H:menadione oxidoreductase. Novel purification of enzyme, cDNA and complete amino acid sequence, and gene regulation. J. Biol. Chem. 1986, 261:15794-15799.
30. Robin M.A., Anandatheerthavarada H.K., Biswas G., Sepuri N.B., Gordon D.M., Pain D., Avadhani N.G. Bimodal targeting of microsomal CYP2E1 to mitochondria through activation of an N-terminal chimeric signal by cAMP-mediated phosphorylation. J. Biol. Chem. 2002, 277:40583-40593.
31. Robin M.A., Prabu S.K., Raza H., Anandatheerthavarada H.K., Avadhani N.G. Phosphorylation enhances mitochondrial targeting of GSTA4-4 through increased affinity for binding to cytoplasmic Hsp70. J. Biol. Chem. 2003, 278:18960-18970.
32. Ruby J.R., Dyer R.F., Skalko R.G. Continuities between mitochondria and endoplasmic reticulum in the mammalian ovary. Z. Zellforsch. Mikrosk. Anat. 1969, 97:30-37.
33. 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 Radical Biol. Med. 2002, 33:1268-1278.
34. Shaw P.M., Reiss A., Adesnik M., Nebert D.W., Schembri J., Jaiswal A.K. The human dioxin-inducible NAD(P)H: quinone oxidoreductase cDNA-encoded protein expressed in COS-1 cells is identical to diaphorase-4. Eur. J. Biochem. 1991, 195:171-176.
35. Shi Z., Dragin N., Galvez-Peralta M., Jorge-Nebert L.F., Miller M.L., Wang B., Nebert D.W. Organ-specific roles of CYP1A1 during detoxication of dietary benzo[a]pyrene. Mol. Pharmacol. 2010, 78:46-57.
36. Shi Z., Dragin N., Miller M.L., Stringer K.F., Johansson E., Chen J., Uno S., Gonzalez F.J., Rubio C.A., Nebert D.W. Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs depend on the mouse Cyp1 genotype. Int. J. Cancer 2010, 127:2334-2350.
37. Silver P., Goodson H. Nuclear protein transport. Crit. Rev. Biochem. Mol. Biol. 1989, 24:419-435.
38. Tsuneoka Y., Dalton T.P., Miller M.L., Clay C.D., Shertzer H.G., Talaska G., Medvedovic M., Nebert D.W. 4-Aminobiphenyl-induced liver and urinary bladder DNA adduct formation in Cyp1a2(-/-) and Cyp1a2(+/+) mice. J. Natl. Cancer Inst. 2003, 95:1227-1237.
39. Uno S., Dalton T.P., Derkenne S., Curran C.P., Miller M.L., Shertzer H.G., Nebert D.W. Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol. Pharmacol. 2004, 65:1225-1237.
40. Uno S., Dalton T.P., Dragin N., Curran C.P., Derkenne S., Miller M.L., Shertzer H.G., Gonzalez F.J., Nebert D.W. Oral benzo[a]pyrene in Cyp1 knockout mouse lines: CYP1A1 important in detoxication, CYP1B1 metabolism required for immune damage independent of total-body burden and clearance rate. Mol. Pharmacol. 2006, 69:1103-1114.
41. Uno S., Dragin N., Miller M.L., Dalton T.P., Gonzalez F.J., Nebert D.W. Basal and inducible CYP1 mRNA quantitation and protein localization throughout the mouse gastrointestinal tract. Free Radical Biol. Med. 2008, 44:570-583.
42. Vasiliou V., Ross D., Nebert D.W. Update of the NAD(P)H: quinone oxidoreductase (NQO) gene family. Hum. Genomics 2006, 2:329-335.
43. Winski S.L., Koutalos Y., Bentley D.L., Ross D. Subcellular localization of NAD(P)H: quinone oxidoreductase-1 in human cancer cells. Cancer Res. 2002, 62:1420-1424.