Characterization of two nuclear proteins that interact with cytochrome P-450 1A2 mRNA. Regulation of RNA binding and possible role in the expression of the Cyp1a2 gene

European Journal of Biochemistry

Volumn 245, Issue 1, 1997, Pages 17-24

  Raffalli Mathieu, Françoise ^a   Geneste, Olivier ^a   Lang, Matti A ^a,b  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

3' untranslated region; Cytochrome P 450 1A2; Induction; RNA binding protein

Indexed keywords

3 METHYLCHOLANTHRENE; CYTOCHROME P450; MESSENGER RNA; NUCLEAR PROTEIN;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME INDUCTION; GENE EXPRESSION REGULATION; LIVER; MALE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA BINDING; TRANSLATION REGULATION;

ANIMALIA;

EID: 0030899712     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00017.x     Document Type: Article

References (56)

1. Nelson, D. R., Koymans, L., Kamataki, T., Stegeman, J. J., Feyereisen, R., Waxman, D. J., Waterman, M. R., Gotoh, O., Coon, M. J., Eastabrook, R. W., Gunsalus, I. C. & Nebert, D. W. (1996) P-450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature, Pharmacogenetics 6, 1-42.
2. Porter, T. D. & Coon, M. J. (1991) Cytochrome P-450. Multiplicity of isoforms, substrates, and catalytic and regulatory mechanisms, J. Biol. Chem. 266, 13469-13472.
3. Gonzalez, F. J. & Gelborn, H. V. (1994) Role of human cytochrome P-450 in the metabolic activation chemical carcinogens and toxins, Drug Metab. Rev. 26, 165-183.
4. Nebert, D. W. & Gonzalez, F. J. (1987) P450 genes: structure, evolution and regulation, Annu. Rev. Biochem. 56, 945-993.
5. Perdew, G. H. (1992) Chemical cross-linking of the cytosolic and nuclear forms of the Ah receptor in hepatoma cell line 1c1c7, Biochem. Biophys. Res. Commun. 182, 55-62.
6. Tukey, R. H., Hannah, R. R., Negishi, M., Nebert, D. W. & Eisen, H. J. (1982) The Ah locus: correlation of intranuclear appearance of inducer-receptor complex with induction of cytochrome P1-450 mRNA, Cell 31, 275-284.
7. Reyes, H., Reisz-Porszasz, S. & Hankinson, O. (1992) Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor, Science 256, 1193-1195.
8. Lusska, A., Shen, E. & Whitlock, J. P. Jr (1993) Protein-DNA interactions at a dioxin-responsive enhancer. Analysis of six bona fide DNA-binding sites for the liganded Ah receptor, J. Biol. Chem. 268, 6575-6580.
9. Quattrochi, L. C., Vu, T. & Tukey, R. H. (1994) The human CYP1A2 gene and induction by 3-methylcholanthrene. A region of DNA that supports AH-receptor binding and promoter-specific induction, J. Biol. Chem. 269, 6949-6954.
10. Gonzalez, F. J., Tukey, R. H. & Nebert, D. W. (1984) Structural gene products of the Ah locus. Transcriptional regulation of cytochrome P1-450 and P3-450 mRNA levels by 3-methylcholanthrene, Mol. Pharmacol. 26, 117-121.
11. Israel, D. I. & Whitlock, J. P. Jr (1984) Regulation of cytochrome P1-450 gene transcription by 2,3,7,8-tetrachlorodibenzo-p-dioxin in wild type and variant mouse hepatoma cells, J. Biol. Chem. 259, 5400-5402.
12. Fisher, J. M., Jones, K. W. & Whitlock, J. P. Jr (1989) Activation of transcription as a general mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin action, Mol. Carcinog. 1, 216-221.
13. Pasco, D. S., Boyum, K. W., Elbi, C., Siu, C. S. & Fagan, J. B. (1993) Inducer-dependent transcriptional activation of the P4501A2 gene in vivo and in isolated hepatocytes, J. Biol. Chem. 268, 1053-1057.
14. Adesnik, M. & Atchison, M. (1986) Genes for cytochrome P-450 and their regulation, CRC. Crit. Rev. Biochem. 19, 247-305.
15. Daujat, M., Clair, P., Astier, C., Fahre, I., Pineau, T. Yerle, M., Gellin, J. & Maurel, P. (1991) Induction, regulation and messenger half-life of cytochromes P450 IA1, IA2 and IIIA6 in primary cultures of rabbit hepatocytes. CYP IA1, 1A2 and 3A6 chromosome location in the rabbit and evidence that post-transcriptional control of gene IA2 does not involve mRNA stabilization, Eur. J. Biochem. 200, 501-510.
16. Silver, G. & Krauter, K. S. (1990) Aryl hydrocarbon induction of rat cytochrome P-450d results from increased precursor RNA processing, Mol. Cell. Biol. 10, 6765-6768.
17. Jackson, R. J. (1993) Cytoplasmic regulation of mRNA function: the importance of the 3′ untranslated region, Cell 74, 9-14.
18. Chen, C. Y. & Shyu, A. B. (1995) AU-rich elements: characterization and importance in mRNA degradation, Trends Riochem. Sci. 20, 465-470.
19. Zubiaga, A. M., Belasco, J. G. & Greenberg, M. E. (1995) The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation, Mol. Cell. Biol. 15, 2219-2230.
20. Morris, D. R., Kakegawa, T., Kaspar, R. L. & White, M. W. (1993) Polypyrimidine tracts and their binding proteins: regulatory sites for posttranscriptional modulation of gene expression, Biochemistry 32, 2931-2937.
21. Pandey, N. B. & Marzluff, W. F. (1987) The stem-loop structure at the 3′ end of historic mRNA is necessary and sufficient for regulation of historic mRNA stability, Mol. Cell. Biol. 7, 4557-4559.
22. Mullner, E. W. & Kuhn, L. C. (1988) A stem-loop in the 3′ untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm, Cell 53, 815-825.
23. Gillis, P. & Malter, J. S. (1991) The adenosine-uridine binding factor recognizes the AU-rich elements of cytokine, lymphokine, and oncogene mRNAs, J. Biol. Chem. 266, 3172-3177.
24. Pandey, N. B., Sun, J. H. & Marzluff, W. F. (1991) Different complexes are formed on the 3′ end of historic mRNA with nuclear and polyribosomal proteins, Nucleic Acids Res. 19, 5653-5659.
25. Zhang, W., Wagner, B. J., Ehrenman, K., Schaefer, A. W., DeMaria, C. T., Crater, D., DeHaven, K., Long, L. & Brewer, G. (1993) Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1, Mol. Cell. Biol. 13, 7652-7665.
26. Kimura, S., Gonzalez, F. J. & Nebert, D. W. (1984) Mouse cytochrome P3-450: complete cDNA and amino acid sequence, Nucleic Acids Res. 12, 2917-2928.
27. Geneste, O., Raffalli, F. & Lang, M. A. (1996) Identification and characterization of a 44 kDa protein that binds specifically to the 3′-untranslated region of Cyp2a5 mRNA: inducibility, subcellular distribution and role in mRNA stabilization, Biochem. J. 313, 1029-1037.
28. Gorski, K., Carneiro, M. & Schibler, U. (1986) Tissue-specific in vitro transcription from the mouse albumin promoter, Cell. 47, 767-776.
29. Dignam, J. D., Lebovitz, R. M. & Roeder, R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei, Nucleic Acids Res. 11, 1475-1489.
30. Brewer, G. & Ross, J. (1990) Messenger RNA turnover in cell-free extracts, Methods Enzymol. 181, 202-209.
31. Lowry, O. H., Rosehrough, N. J., Farr, A. L. & Randall, R. J. (1951) Protein measurements with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
32. Malter, J. S. & Hong, Y. (1991) A redox switch and phosphorylation are involved in the post-translational up-regulation of the adenosine-uridine binding factor by phorbol ester and ionophore, J. Biol. Chem. 266, 3167-3171.
33. Leibold, H. A. & Munro, H. N. (1988) Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy- and light-subunit mRNAs, Proc. Natl Acad. Sci. USA 85, 2171-2175.
34. Hamilton, B. J., Nagy, E., Malter, J. S., Arrick, B. A. & Rigby, W. F. (1993) Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences, J. Biol. Chem. 268, 8881-8887.
35. Dreyfuss, G., Matunis, M. J., Pinol-Roma, S. & Burd, C. G. (1993) hnRNP proteins and the biogenesis of mRNA, Annu. Rev. Biochem. 62, 289-321.
36. Williams, A. S., Ingledue, T. C., Kay, B. K. & Marzluff, W. F. (1994) Changes in the stem-loop at the 3′ terminus of histone mRNA affects its nucleocytoplasmic transport and cytoplasmic regulation, Nucleic Acids Res. 22, 4660-4666.
37. Williams, A. S. & Marzluff, W. F. (1995) The sequence of the stem and flanking sequences at the 3′ end of histone mRNA are critical determinants for the binding of the stem-loop binding protein, Nucleic Acids Res. 23, 654-662.
38. Pandey, N. B., Williams, A. S., Sun, J. H., Brown, V. D., Bond, U. & Marzluff, W. F. (1994) Point mutations in the stem-loop at the 3′ end of mouse histone mRNA reduce expression by reducing the efficiency of 3′ end formation, Mol. Cell. Biol. 14, 1709-1720.
39. Kimura, S., Gonzalez, F. J. & Nebert, D. W. (1984) The murine Ah locus. Comparison of the complete cytochrome P1-450 and P3-450 cDNA nucleotide and amino acid sequences, J. Biol. Chem. 259, 10705-10713.
40. Katz, D. A., Theodorakis, N. G., Cleveland, D. W., Lindsten, T. & Thompson, C. B. (1994) AU-A, an RNA-binding activity distinct from hnRNP A1, is selective for AUUUA repeats and shuttles between the nucleus and the cytoplasm, Nucleic Acids Res. 22, 238-246.
41. Swanson, M. S. & Dreyfuss, G. (1988) Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities, Mol. Cell. Biol. 8, 2237-2241.
42. Wilusz, J. & Shenk, T. (1990) A uridylate tract mediates efficient heterogeneous nuclear ribonucleoprotein C protein-RNA cross-linking and functionally substitutes for the downstream element of the polyadenylation signal, Mol. Cell. Biol. 10, 6397-6407.
43. Gorlach, M., Burd, C. G. & Dreyfuss, G. (1994) The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins, J. Biol. Chem. 269, 23074-23078.
44. Huang, M., Reeh, J. E., Northington, S. J., Flicker, P. K. Mayeda, A., Krainer, A. R. & LeStourgeon, W. M. (1994) The C-protein tetramer binds 230 to 240 nucleotides of pre-mRNA and nucleates the assembly of 40S heterogeneous nuclear ribonucleoprotein particles, Mol. Cell. Biol. 14, 518-533.
45. Choi, Y. D., Grabowski, P. J., Sharp, P. A. & Dreyfuss, G. (1986) Heterogeneous nuclear ribonucleoproteins: role in RNA splicing, Science 231, 1534-1549.
46. Santoro, B., De-Gregorio, F., Caffarelli, E. & Bozzoni, I. (1994) RNA-protein interactions in the nuclei of Xenopus oocytes: complex formation and processing activity on the regulatory intron of ribosomal protein gene L1, Mol. Cell. Biol. 14, 6975-6982.
47. Zaidi, S. H., Denman, R. & Malter, J. S. (1994) Multiple proteins interact at a unique cis-element in the 3′-untranslated region of amyloid precursor protein mRNA, J. Biol. Chem. 269, 24000-24006.
48. Swanson, M. S., & Dreyfuss, G. (1988) RNA binding specificity of hnRNP proteins: a subset bind to the 3′ end of introns, EMBO. J. 7, 3519-3529.
49. Wilusz, J., Feig, D. I. & Shenk, T. (1988) The C proteins of heterogeneous nuclear ribonucleoprotein complexes interact with RNA sequences downstream of polyadenylation cleavage sites, Mol. Cell. Biol. 8, 4477-4483.
50. An, G. & Wu, R. (1993) cDNA cloning of a hnRNP A1 isoform and its regulation by retinol in monkey tracheohronchial epithelial cells, Biochim. Biophys. Acta 1172, 292-300.
51. Mayrand, S. H., Dwen, P. & Pederson, T. (1993) Serine/threonine phosphorylation regulates binding of C hnRNP proteins to pre-mRNA, Proc. Natl Acad. Sci. USA 90, 7764-7768.
52. Pinol-Roma, S. & Dreyfuss, G. (1993) Cell cycle-regulated phosphorylation of the pre-mRNA-binding (heterogeneous nuclear ribonucleoprotein) C proteins, Mol. Cell. Biol. 13, 5762-5770.
53. Holcomb, E. R. & Friedman, D. L. (1984) Phosphorylation of the C-proteins of HeLa cell hnRNP particles. Involvement of a casein kinase II-type enzyme, J. Biol. Chem. 259, 31-40.
54. Riddick, D. S., Huang, Y., Harper, P. A. & Okey, A. B. (1994) 2,3,7,8-Tetrachlorodibenzo-p-dioxin versus 3-methylcholanthrene: comparative studies of Ah receptor binding, transformation, and induction of CYP1A1, J. Biol. Chem. 269, 12118-12128.
55. Enan, E. & Matsumura, F. (1995) Evidence for a second pathway in the action mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Significance of Ah-receptor mediated activation of protein kinase under cell-free conditions, Biochem. Pharmacol. 49, 249-261.
56. Enan, E. & Matsumura, F. (1995) Regulation by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) of the DNA binding activity of transcriptional factors via nuclear protein phosphorylation in guinea pig adipose tissue, Biochem. Pharmacol. 50, 1199-1206.