Mitochondrial targeting of cytochrome P450 (CYP) 1B1 and its role in polycyclic aromatic hydrocarbon-induced mitochondrial dysfunction

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9936-9951

  Bansal, Seema ^a   Leu, Adrian N ^a   Gonzalez, Frank J ^b   Guengerich, F Peter ^c   Chowdhury, Anindya Roy ^a   Anandatheerthavarada, Hindupur K ^a   Avadhani, Narayan G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; MAMMALS; MOLECULAR BIOLOGY; PYRENE;

FERREDOXIN REDUCTASE; HYDROXYLASE ACTIVITY; LUNG EPITHELIAL CELLS; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL IMPORT; POLYCYCLIC AROMATIC HYDROCARBON (PAH); POLYCYCLIC AROMATICS; SITE DIRECTED MUTAGENESIS;

MITOCHONDRIA;

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ADRENODOXIN; BENZO[A]PYRENE; CYTOCHROME P450 1B1; CYTOCHROME P450 REDUCTASE; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; MITOCHONDRIAL DNA; POLYCYCLIC AROMATIC HYDROCARBON; SERINE PROTEINASE; UNSPECIFIC MONOOXYGENASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN;

CARCINOGENESIS; CYTOCHROME P450; DNA DAMAGE; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DNA;

ADRENODOXIN; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BENZO(A)PYRENE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MUTAGENESIS; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; TERATOGENS; TETRACHLORODIBENZODIOXIN;

EID: 84898059625     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.525659     Document Type: Article

References (66)

1. McKay, J. A., Murray, G. I., Ah-See, A. K., Greenlee, W. F., Marcus, C. B., Burke, M. D., andMelvin, W. T. (1996) Differential expression of CYP1A1 and CYP1B1 in human breast cancer. Biochem. Soc. Trans. 24, 327S
2. Conney, A. H. (1982) Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G. H. A. Clowes Memorial Lecture. Cancer Res. 42, 4875-4917
3. Kim, D., and Guengerich, F. P. (2005) Cytochrome P450 activation of arylamines and heterocyclic amines. Annu. Rev. Pharmacol. Toxicol. 45, 27-49
4. Gelboin, H. V. (1980) Benzo[a]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol. Rev. 60, 1107-1166
5. Jerina, D. M. (1983) The 1982 Bernard B. Brodie Award Lecture. Metabolism of aromatic hydrocarbons by the cytochrome P-450 system and epoxide hydrolase. DrugMetab. Dispos. 11, 1-4
6. Miller, K. P., and Ramos, K. S. (2001) Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab. Rev. 33, 1-35
7. Gonzalez, F. J., Jaiswal, A. K., and Nebert, D. W. (1986) P450 genes: evolution, regulation, and relationship to human cancer and pharmacogenetics. Cold Spring Harbor Symp. Quant. Biol. 51, 879-890
8. Nebert, D. W., Jaiswal, A. K., Meyer, U. A., and Gonzalez, F. J. (1987) Human P-450 genes: evolution, regulation and possible role in carcinogenesis. Biochem. Soc. Trans. 15, 586-589
9. Nebert, D.W., Dalton, T. P., Okey, A. B., and Gonzalez, F. J. (2004) Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 279, 23847-23850
10. Schweikl, H., Taylor, J. A., Kitareewan, S., Linko, P., Nagorney, D., and Goldstein, J. A. (1993) Expression of CYP1A1 and CYP1A2 genes in human liver. Pharmacogenetics 3, 239-249
11. Hankinson, O. (1995) The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35, 307-340
12. Nebert, D. W., Roe, A. L., Dieter, M. Z., Solis, W. A., Yang, Y., and Dalton, T. P. (2000) Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59, 65-85
13. Shimada, T., Hayes, C. L., Yamazaki, H., Amin, S., Hecht, S. S., Guengerich, F.P., and Sutter, T. R. (1996) Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56, 2979-2984
14. Sutter, T. R., Tang, Y. M., Hayes, C. L., Wo, Y. Y., Jabs, E. W., Li, X., Yin, H., Cody, C. W., and Greenlee, W. F. (1994) Complete cDNA sequence of a human dioxin-inducible mRNA identifies a new gene subfamily of cytochrome P450 that maps to chromosome 2. J. Biol. Chem. 269, 13092-13099
15. Hakkola, J., Pasanen, M., Pelkonen, O., Hukkanen, J., Evisalmi, S., Anttila, S., Rane, A., Mäntylä, M., Purkunen, R., Saarikoski, S., Tooming, M., and Raunio, H. (1997) Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor li-gands in human placenta and cultured cells. Carcinogenesis 18, 391-397
16. Tang, Y. M., Chen, G. F., Thompson, P. A., Lin, D. X., Lang, N. P., and Kadlubar, F. F. (1999) Development of an antipeptide antibody that binds to the C-terminal region of human CYP1B1. Drug Metab. Dispos. 27, 274-280
17. Edwards, R. J., Adams, D. A., Watts, P. S., Davies, D. S., and Boobis, A. R. (1998) Development of a comprehensive panel of antibodies against the major xenobiotic metabolising forms of cytochrome P450 in humans. Biochem. Pharmacol. 56, 377-387
18. Dutheil, F., Beaune, P., and Loriot, M. A. (2008) Xenobiotic metabolizing enzymes in the central nervous system: Contribution of cytochrome P450 enzymes in normal and pathological human brain. Biochimie 90, 426-436
19. Murray, G. I., Taylor, V. E., McKay, J. A., Weaver, R. J., Ewen, S. W., Melvin, W. T., and Burke, M. D. (1995) The immunohistochemical localization of drug-metabolizing enzymes in prostate cancer. J. Pathol. 177, 147-152
20. Murray, G. I., Taylor, M. C, McFadyen, M. C, McKay, J. A., Greenlee, W. F., Burke, M. D., and Melvin, W. T. (1997) Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res. 57, 3026-3031
21. Buters, J. T., Sakai, S., Richter, T., Pineau, T., Alexander, D. L., Savas, U., Doehmer, J., Ward, J. M., Jefcoate, C. R., and Gonzalez, F. J. (1999) Cytochrome P450 CYP1B1 determines susceptibility to 7, 12-dimethylben-z[a] anthracene-induced lymphomas. Proc. Natl. Acad. Sci. U.S.A. 96, 1977-1982
22. Hayes, C. L., Spink, D. C, Spink, B. C, Cao, J. Q., Walker, N. J., and Sutter, T. R. (1996) 17/3-Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93, 9776-9781
23. McKay, J. A., Melvin, W. T., Ah-See, A. K., Ewen, S. W., Greenlee, W. F., Marcus, C. B., Burke, M. D., and Murray, G. I. (1995) Expression of cytochrome P450 CYP1B1 in breast cancer. FEBS Lett. 374, 270-272
24. Badawi, A. F., Cavalieri, E. L., and Rogan, E. G. (2001) Role of human cytochrome P450 1A1, 1A2, 1B1, and 3A4 in the 2-, 4-, and 16-a-hydroxy-lation of 17/3-estradiol. Metabolism 50, 1001-1003
25. Lee, A. J., Cai, M. X., Thomas, P. E., Conney, A. H., and Zhu, B. T. (2003) Characterization of the oxidative metabolites of 17/3-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144, 3382-3398
26. Shimada, T., Watanabe, J., Inoue, K., Guengerich, F. P., and Gillam, E. M. (2001) Specificity of 17/3-oestradiol and benzo[a]pyrene oxidation by polymorphic human cytochrome P4501B1 variants substituted at residues 48, 119 and 432. Xenobiotica 31, 163-176
27. Shimada, T., Watanabe, J., Kawajiri, K., Sutter, T. R., Guengerich, F. P., Gillam, E. M., and Inoue, K. (1999) Catalytic properties of polymorphic human cytochrome P450 1B1 variants. Carcinogenesis 20, 1607-1613
28. Tsuchiya, Y., Nakajima, M., Kyo, S., Kanaya, T., Inoue, M., and Yokoi, T. (2004) Human CYP1B1 is regulated by estradiol via estrogen receptor. Cancer Res. 64, 3119-3125
29. Vasiliou, V., and Gonzalez, F. J. (2008) Role of CYP1B1 in glaucoma. Annu. Rev. Pharmacol. Toxicol. 48, 333-358
30. Bagiyeva, S., Marfany, G., Gonzalez-Angulo, O., and Gonzalez-Duarte, R. (2007) Mutational screening of CYP1B1 in Turkish PCG families and functional analyses of newly detected mutations. Mol. Vis. 13, 1458-1468
31. Sangar, M. C, Bansal, S., and Avadhani, N. G. (2010) Bimodal targeting of microsomal cytochrome P450s to mitochondria: implications in drug metabolism and toxicity. Expert Opin. DrugMetab. Toxicol. 6, 1231-1251
32. Boopathi, E., Srinivasan, S., Fang, J. K., and Avadhani, N. G. (2008) Bimodal protein targeting through activation of cryptic mitochondrial targeting signals by an inducible cytosolic endoprotease.Mol. Cell32, 32-42
33. 2-terminal chimeric signals involves an unusual TOM20/TOM22 bypass mechanism. J. Biol. Chem. 284, 17352-17363
34. Sepuri, N. B., Yadav, S., Anandatheerthavarada, H. K., and Avadhani, N. G. (2007) Mitochondrial targeting of intact CYP2B1 and CYP2E1 and N-ter-minal truncated CYP1A1 proteins in Saccharomyces cerevisiae-role of protein kinase A in the mitochondrial targeting of CYP2E1. FEBS J. 274, 4615-4630
35. Dasari, V. R., Anandatheerthavarada, H. K., Robin, M. A., Boopathi, E., Biswas, G., Fang, J. K., Nebert, D. W., and Avadhani, N. G. (2006) Role of protein kinase C-mediated protein phosphorylation in mitochondrial translocation of mouse CYP1A1, which contains a non-canonical targeting signal. J. Biol. Chem. 281, 30834-30847
36. Bhagwat, S. V., Biswas, G., Anandatheerthavarada, H. K., Addya, S., Pandak, W., and Avadhani, N. G. (1999) Dual targeting property of the N-terminal signal sequence of P4501A1. Targeting of heterologous proteins to endoplasmic reticulum and mitochondria. J. Biol. Chem. 274, 24014-24022
37. 2-terminal- processed microsomal protein to mitochondria: a novel pathway for the biogenesis of hepatic mitochondrial P450MT2. J. Cell Biol. 139, 589-599
38. Anandatheerthavarada, H. K., Addya, S., Dwivedi, R. S., Biswas, G., Mul-lick, J., and Avadhani, N. G. (1997) Localization of multiple forms of inducible cytochromes P450 in rat liver mitochondria: immunological characteristics and patterns of xenobiotic substrate metabolism. Arch. Biochem. Biophys. 339, 136-150
39. Anandatheerthavarada, H. K., Biswas, G., Mullick, J., Sepuri, N. B., Otvos, L., Pain, D., and Avadhani, N. G. (1999) Dual targeting of cytochrome P4502B1 to endoplasmic reticulum and mitochondria involves a novel signal activation by cyclic AMP-dependent phosphorylation at ser128. EMBOJ. 18, 5494-5504
40. Robin, M. A., Anandatheerthavarada, H. K., Biswas, G., Sepuri, N. B., Gordon, D. M., Pain, D., and Avadhani, N. G. (2002) Bimodal targeting of microsomal CYP2E1 to mitochondria through activation of an N-terminal chimeric signal by cAMP-mediated phosphorylation. J. Biol. Chem. 277, 40583-40593
41. Sangar, M. C, Anandatheerthavarada, H. K., Tang, W., Prabu, S. K., Martin, M. V., Dostalek, M., Guengerich, F. P., and Avadhani, N. G. (2009) Human liver mitochondrial cytochrome P450 2D6-individual variations and implications in drug metabolism. FEBS J. 276, 3440-3453
42. Sangar, M. C, Anandatheerthavarada, H. K., Martin, M. V., Guengerich, F. P., and Avadhani, N. G. (2010) Identification of genetic variants of human cytochrome P450 2D6 with impaired mitochondrial targeting. Mol. Genet. Metab. 99, 90-97
43. Robin, M. A., Prabu, S. K., Raza, H, Anandatheerthavarada, H. K., and Avadhani, N. G. (2003) Phosphorylation enhances mitochondrial targeting of GSTA4-4 through increased affinity for binding to cytoplasmic Hsp70. J. Biol. Chem. 278, 18960-18970
44. 2-terminal truncated cytochrome P4501A1 in rat brain during chronic treatment with/3-naphthoflavone. A role in the metabolism of neuroactive drugs. J. Biol. Chem. 275, 34415-34423
45. Robin, M. A., Anandatheerthavarada, H. K., Fang, J. K., Cudic, M., Otvos, L., and Avadhani, N. G. (2001) Mitochondrial targeted cytochrome P450 2E1 (P450 MT5) contains an intact N terminus and requires mitochondrial specific electron transfer proteins for activity. J. Biol. Chem. 276, 24680-24689
46. Shi, Z., Dragin, N, Miller, M. L., Stringer, K. F., Johansson, E., Chen, J., Uno, S., Gonzalez, F. J., Rubio, C. A., and Nebert, D. W. (2010) Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs depend on the mouse Cyp1 genotype. Int. J. Cancer 127, 2334-2350
47. Bhagwat, S. V., Mullick, J., Raza, H, and Avadhani, N. G. (1999) Constitutive and inducible cytochromes P450 in rat lung mitochondria: xenobiotic induction, relative abundance, and catalytic properties. Toxicol. Appl. Pharmacol. 156, 231-240
48. Anandatheerthavarada, H. K., Vijayasarathy, C, Bhagwat, S. V., Biswas, G., Mullick, J., and Avadhani, N G. (1999) Physiological role of the N-terminal processed P4501A1 targeted to mitochondria in erythromycin metabolism and reversal of erythromycin-mediated inhibition of mitochondrial protein synthesis. J. Biol. Chem. 274, 6617-6625
49. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
50. Wu, M., Neilson, A., Swift, A. L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J., Chomicz, S., and Ferrick, D. A. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136
51. Clark, B. J., and Waterman, M. R. (1991) The hydrophobic amino-terminal sequence of bovine 17a-hydroxylase is required for the expression of a functional hemoprotein in COS 1 cells. J. Biol. Chem. 266, 5898-5904
52. Nebert, D. W., and Gelboin, H. V. (1968) Substrate-inducible microsomal aryl hydroxylase in mammalian cell culture. I. Assay and properties of induced enzyme. J. Biol. Chem. 243, 6242-6249
53. Omura, T., and Sato, R. (1964) The carbon monoxide-binding pigment of liver microsomes. II. solubilization, purification, and properties. J. Biol. Chem. 239, 2379-2385
54. Guengerich, F. P., Dannan, G. A., Wright, S.T., Martin, M.V., andKamin-sky, L. S. (1982) Purification and characterization of liver microsomal cytochromes p-450: electrophoretic, spectral, catalytic, and immunochemical properties and inducibility of eight isozymes isolated from rats treated with Phenobarbital or/3-naphthoflavone. Biochemistry 21, 6019-6030
55. Prabu, S. K., Anandatheerthavarada, H. K., Raza, H., Srinivasan, S., Spear, J. F., and Avadhani, N. G. (2006) Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J. Biol. Chem. 281, 2061-2070
56. Birch-Machine, M. A., and Turnbull, D. M. (2001) Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol. 65, 97-117
57. Bansal, S., Liu, C. P., Sepuri, N. B., Anandatheerthavarada, H. K., Several, V., Hook, J., Milne, G. L., Guengerich, F. P., and Avadhani, N. G. (2010) Mitochondria-targeted cytochrome P450 2E1 induces oxidative damage and augments alcohol-mediated oxidative stress. J. Biol. Chem. 285, 24609-24619
58. Yaks, F. M., and Van Houston, B. (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 94, 514-519
59. Dong, H, Dalton, T. P., Miller, M. L., Chen, Y., Uno, S., Shi, Z., Shorter, H. G., Bansal, S., Avadhani, N. G., and Nebert, D. W. (2009) Knock-in mouse lines expressing either mitochondrial or microsomal CYP1A1: differing responses to dietary benzo[a]pyrene as proof of principle. Mol. Pharmacol. 75, 555-567
60. Raza, H, and Avadhani, N. G. (1988) Hepatic mitochondrial cytochrome P-450 system. Purification and characterization of two distinct forms of mitochondrial cytochrome P-450 from/3-naphthoflavone-induced rat liver. J. Biol. Chem. 263, 9533-9541
61. Avadhani, N. G., Sangar, M. C., Bansal, S., and Baja, P. (2011) Bimodal targeting of cytochrome P450s to endoplasmic reticulum and mitochondria: the concept of chimeric signals. FEBS J. 278, 4218-4229
62. Dragin, N, Uno, S., Wang, B., Dalton, T. P., and Nebert, D. W. (2007) Generation of 'humanized' hCYP1A1-1A2-Cyp1a1/1a2(-/-) mouse line. Biochem. Biophys. Res. Commun. 359, 635-642
63. Liang, H. C., Li, H., McKinnon, R. A., Duffy, J. J., Potter, S. S., Pug, A., and Nebert, D. W. (1996) Cyp1a2(-/-) null mutant mice develop normally but show deficient drug metabolism. Proc. Natl. Acad. Sci. U.S.A. 93, 1671-1676
64. Nebert, D. W., Shi, Z., Gales-Peralta, M., Uno, S., and Dragin, N. (2013) Oral benzo[a]pyrene: understanding pharmacokinetics, defoliation, and consequences-Cyp1 knockout mouse lines as a paradigm. Mol. Pharmacol. 84, 304-313
65. Uno, S., Dalton, T. P., Dragin, N, Curran, C. P., Darkener, S., Miller, M. L., Shorter, H. G., Gonzalez, F. J., and Nebert, D. W. (2006) Oral benzo[a]pyr-ene in Cyp1 knockout mouse lines: CYP1A1 important in defoliation, CYP1B1 metabolism required for immune damage independent of total-body burden and clearance rate. Mol. Pharmacol. 69, 1103-1114
66. Bauer, E., Guo, Z., Jeng, Y. F., Bell, L. C., Seldin, D., and Guengerich, F. P. (1995) Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem. Res. Toxicol. 8, 136-142