Thymidylate synthase protein and p53 mRNA form an in vivo ribonucleoprotein complex

Molecular and Cellular Biology

Volumn 19, Issue 2, 1999, Pages 1582-1594

  Chu, Edward ^a,d   Copur, Sitki M ^b   Ju, Jingfang ^a   Chen, Tian Men ^a   Khleif, Samir ^b   Voeller, Donna M ^b   Mizunuma, Nobuyuki ^b   Patel, Mahendra ^b   Maley, Gladys F ^c   Maley, Frank ^c   Allegra, Carmen J ^b  

^a YALE CANCER CENTER   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c WADSWORTH CENTER   (United States)

^d VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOXYCYCLINE; MESSENGER RNA; PROTEIN P53; RIBONUCLEOPROTEIN; TETRACYCLINE; THYMIDYLATE SYNTHASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; TUMOR SUPPRESSOR GENE;

ANIMALIA;

EID: 0032929245     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.2.1582     Document Type: Article

References (72)

1. Caelles, C., A. Heimberg, and M. Karin. 1994. p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370: 220-223.
2. Casey, J. L., M. W. Hentze, D. M. Koeller, S. W. Caughman, T. A. Rouault, R. D. Klausner, and J. B. Harford. 1988. Iron-responsive elements: regulatory RNA sequences that control mRNA levels and translation. Science 240:924-928.
3. Chiba, I., T. Takahashi, M. M. Nau, D. D'Amico, D. T. Curiel, T. Mitsudomi, D. L. Buchhagen, D. Carbone, S. Piantadosi, H. Koga, P. T. Reissman, D. J. Slamon, E. C. Holmes, and J. D. Minna. 1990. Mutations in the p53 gene are frequent in primary, resected non-small cell lung cancer. Oncogcne 5:1603-1610.
4. Chomicyznski, P., and N. Sacchi. 1987. Single-step method of RNA isolation hy acid guanidinium thiocyanate phenol-chloroform extraction. Anal. Biochem. 162:156-159.
5. Chu, E., D. M. Koeller, J. L. Casey, J. C. Drake, B. A. Chabner, P. C. Elwood, S. Zinn, and C. J. Allegra. 1991. Autoregulatlon of human thymidylate synthase messenger RNA translation by thymidylate synthase. Proc. Natl. Acad. Sci. USA 88:8977-8981.
6. Chu, E., D. M. Voeller, D. M. Koeller, J. C. Drake, C. H. Takimoto, F. Maley, G. F. Maley, and C. J. Allegra. 1993. Identification of an RNA binding site for human thymidylate synthase. Proc. Natl. Acad. Sci. USA 90:517-521.
7. Chu, E., D. M. Voeller, P. F. Morrison, K. L. Jones, T. Takechi, G. F. Maley, F. Maley, and C. J. Allegra. 1994. The effect of reducing reagents on binding of thymidylate synthase protein to thymidylate synthase messenger RNA. J. Biol. Chem. 269:20289-20293.
8. Chu, E., S. Zinn, D. Boarman, and C. J. Allegra. 1990. The interaction of gamma interferon and 5-fluorouracil in the H630 human colon carcinoma cell line. Cancer Res. 50:5834-5840.
9. Chu, E., D. M. Koeller, P. C. Johnston, S. Zinn, and C. J. Allegra. 1993. Regulation of thymidylate synthase in human colon cancer cells treated with 5-fluorouracil and interferon-gamma. Mol. Pharmacol. 43:527-533.
10. Chu, E., D. M. Voeller, K. L. Jones, T. Takechi, G. F. Maley, F. Maley, S. Segal, and C. J. Allegra. 1994. Identification of a thymidylate synthase ribonucleoprotein complex in human colon cancer cells. Mol. Cell. Biol. 14:207-213.
11. Chu, E., T. Takechi, K. L. Jones, D. M. Voeller, S. M. Copur, G. F. Maley, S. Segal, and C. J. Allegra. 1995. Thymidylate synthase protein hinds to c-myc RNA in human colon cancer cells and in vitro. Mol. Cell. Biol. 15:179-185.
12. Chu, E., C. H. Takimoto, D. Voeller, J. L. Grem, and C. J. Allegra. 1993. Specific binding of human dihydrofolate reductase protein to dihydrofolate reductase messenger RNA in vitro. Biochemistry 32:4756-4760.
13. Chu, E., T. Cogliati, S. M. Copur, A. Borre, D. M. Voeller, C. J. Allegra, and S. Segal. 1996. Identification of in vivo target RNA sequences bound by thymidylate synthase. Nucleic Acids Res. 24:3222-3228.
14. Ciesla, J., K. X. B. Weiner, R. S. Weiner, J. T. Reston, G. F. Maley, and F. Maley. 1995. Isolation and expression of rat thymidylate synthase cDNA. Phylogenetic comparison with human and mouse thymidylate synthases. Biochim. Biophys. Acta 1261:233-242.
15. Dandekar, T., R. Stripecke, N. K. Gray, B. Goossen, A. Constable, H. E. Johansson, and M. W. Hentze. 1991. Identification of a novel iron-responsive element in murine and human erythroid 8-aminolevulinic acid synthase mRNA. EMBO J. 10:1903-1909.
16. Davisson, V. J., W. Sirawaraporn, and D. V. Santi. 1989. Expression of human thymidyiate synthase in Escherichia coli. J. Biol. Chem. 264:9145-9148.
17. Deffie, A., H. Wu, V. Reinke, and G. Lozano. 1993. The tumor suppressor p53 regulates its own transcription. Mol. Cell. Biol. 13:3415-3423.
18. Ewen, M. E., and S. J. Miller. 1996. p53 and translational control. Biochim. Biophys. Acta 1242:181-184.
19. Feinberg, A. P., and B. Vogelstein. 1984. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 137:266-267.
20. Fried, J., A. G. Perez, and V. D. Clarkson. 1978. Rapid hypotonic method for flow cytofluorometry of monolayer cell culture. J. Histochem. Cytochem. 26:921-926.
21. Fu, L., M. D. Minden, and S. Benchimol. 1996. Translational regulation of human p53 gene expression. EMBO J. 15:4392-4401.
22. Gallie, D. R. 1991. The cap and poly (A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5:2108-2116.
23. Gossen, M., S. Freundlieb, G. Bender, G. Muller, W. Hillen, and H. Bujard. 1995. Transcriptional activation by tetracyclines in mammalian cells. Science 268:1766-1769.
24. Greenblatt, M. S., W. P. Bennett, M. Hallstein, and C. C. Harris. 1994. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 54:4855-4878.
25. Hardy, L. W., J. S. Finer-Moore, W. R. Montfort, M. O. Jones, D. V. Santi, and R. M. Stroud. 1987. Atomic structure of thymidylate synthase: target for rational drug design. Science 235:448-455.
26. Harris, C. C., and M. Hollstein. 1993. Clinical implications of the p53 tumor-suppressor gene. N. Engl. J. Med. 329:1318-1327.
27. Helman, L. J., T. G. Ahn, M. A. Levine, A. Allison, P. S. Cohen, M. J. Cooper, D. V. Conn, and M. A. Israel. 1988. Molecular cloning and primary structure of human chromogranin A (secretory protein 1) cDNA. J. Biol. Chem. 263:11559-11563.
28. Henderson, B. R., E. Menotti, C. Bonnard, and L. C. Kuhn. 1994. Optimal sequence and structure of iron-responsive elements. J. Biol. Chem. 269: 17481-17489.
29. Hentze, M. W., S. W. Caughman, T. A. Rouault, J. G. Barriocanal, A. Dancis, J. B. Harford, and R. D. Klausner. 1987. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science 238:1570-1573.
30. Hollstein, M., D. Sidransky, B. Vogelstein, and C. C. Harris. 1991. p53 mutations in human cancers. Science 253:49-53.
31. Hudson, J. M., R. Frade, and M. Bar-Eli. 1995. Wild-type p53 regulates its own transcription in a cell-type specific manner. DNA Cell Biol. 14:759-766.
32. Jackson, R. J., and N. Standard. 1990. Do the poly(A) tail and 3′ untranslated region control mRNA translation? Cell 62:15-24.
33. Jackson, R. J. 1993. Cytoplasmic regulation of mRNA function: the importance of the 3′ untranslated region. Cell 74:9-14.
34. Johnston, P. G., C. M. Liang, S. Henry, B. A. Chabner, and C. J. Allegra. 1991. Production and characterization of monoclonal antibodies that localize human thymidylate synthase in the cytoplasm of human cells and tissue. Cancer Res. 51:6668-6676.
35. Kastan, M. B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
36. Keyomarsi, K., J. Samet, S. Gyongyi, G. Molnar, and A. B. Pardee. 1993. The thymidylate synthase inhibitor, ICI D1694, overcomes translational detainment of the enzyme. J. Biol. Chem. 268:15142-15149.
37. Klausner, R. D., T. A. Rouault, and J. B. Harford. 1993. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72:19-28.
38. Ko, L. J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10:1054-1072.
39. Konarska, M. M., and P. A. Sharp. 1986. Electrophoretic separation of complexes involved in the splicing of precursors to mRNAs. Cell 476:845-855.
40. Kozak, M. 1991. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266:19867-19870.
41. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
42. Lamb, P., and L. Crawford. 1986. Characterization of the human p53 gene. Mol. Cell. Biol. 6:1379-1385.
43. Leathers, V., R. Tanguay, M. Kobayashi, and D. R. Gallie. 1993. A phylogenetically conserved sequence within viral 3′ untranslated RNA pseudoknots regulates translation. Mol. Cell. Biol. 13:5331-5347.
44. Leibold, E. A., and H. N. Munro. 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.
45. Lerner, M. R., and J. A. Steitz. 1979. Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 76:5495-5499.
46. Levine, A. J., J. Momand, and C. A. Finlay. 1991. The p53 tumour suppressor gene. Nature 351:453-456.
47. Levine, A. J. 1997. p53. the cellular gatekeeper for growth and division. Cell 88:323-331.
48. Linke, S. P., K. C. Clarkin, A. DiLeonardo, A. Tsou, and G. M. Wahl. 1996. A reversible, p53-dependent G0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10:934-947.
49. Lowe, S. W., H. E. Ruley, T. Jacks, and D. E. Houseman. 1993. p53-dependenl apoptosis modulates the cytotoxicity of anticancer agents. Cell 74:957-968.
50. Maltzman, W., and L. Czyzyk. 1984. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol. Cell. Biol. 4: 1689-1694.
51. Matlashewski, G., P. Lamb, J. Pim, J. Peacock, L. Crawford, and S. Benchimol. 1984. Isolation and characterisation of a human p53 cDNA clone: expression of the human p53 gene. EMBO J. 3:3257-3262.
52. Matlashewski, G. J., S. Tuck, D. Pim, P. Lamb, J. Schneider, and L. V. Crawford. 1987. Primary structure polymorphism at amino acid residue 72 of human p53. Mol. Cell. Biol. 7:961-963.
53. Melefors, O., and M. W. Hentze. 1993. Translational regulation by mRNA/dprotein interactions in eukaryotic cells: ferritin and beyond. Bioessays 15: 85-90.
54. Mosner, J., T. Mummenbrauer, C. Bauer, G. Sczakiel, F. Grosse, and W. Deppert. 1995. Negative feedback regulation of wild-type p53 biosynthesis. EMBO J. 14:4442-4449.
55. Ostareck-Lederer, A. D., D. H. Ostareck, N. Standard, and B. J. Thiele. 1994. Translation of 15-lipooxygenase mRNA is inhibited by a protein that binds to a repeated sequence in the 3′ untranslated region. EMBO J. 13: 1476-1481.
56. Park, J. G., H. K. Oie, P. H. Sugarbaker, J. G. Henslee, T. R. Chen, B. E. Johnson, and A. Gazdar. 1987. Characteristics of cell lines established from human colorectal carcinoma. Cancer Res. 47:6710-6718.
57. Ramirez, M., R. C. Wek, and A. G. Hinnebusch. 1991. Ribosome association of GCN2 protein kinase, a translational activator of the GCN4 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 11:3027-3036.
58. Rhee, M. S., M. Balinska, M. Bunni, D. G. Priest, G. F. Maley, and F. Maley. 1990. Role of substrate depletion in the inhibition of thymidylate biosynthesis by the dihydrofolate reductase inhibitor trimetrexate in cultured hepatoma cells. Cancer Res. 50:3979-3984.
59. Rode, W., B. L. Dolnick, and J. R. Bertino. 1980. Isolation of a homogeneous preparation of human thymidylate synthetase from HeLa cells. Biochem. Pharmacol. 29:723-726.
60. Samsonoff, W. A., J. Reston, M. McKee, B. O'Connor, J. Galivan, G. Maley, and F. Maley. 1997. Intracellular location of thymidylate synthase and its state of phosphorylation. J. Biol. Chem. 272:13281-13285.
61. Santi, D. V., and P. V. Danenberg. 1984. Folates in pyrimidine nucleotide biosynthesis, p. 345-398. In R. L. Blakely and S. J. Benkovic (ed.), Folates and pteridines, vol. 1. John Wiley & Sons, Inc., New York, N.Y.
62. Scatchard, G. 1949. The attraction of proteins for small molecules and ions. Ann. N. Y. Acad. Sci. 51:660-692.
63. Steitz, J. A. 1989. Immunoprecipitation of ribonucleoproteins using autoantibodies. Methods Enzymol. 180:468-481.
64. Takahashi, T., M. M. Nau, I. Chiba, M. J. Birrer, R. K. Rosenberg, M. Vinocour, M. Levitt, H. Pass, A. F. Gazdar, and J. D. Minna. 1989. p53: a frequent target for genetic abnormalities in lung cancer. Science 246:491-494.
65. Theodorakis, N. G., and R I. Morimoto. 1987. Posttranscriptional regulation of hsp70 expression in human cells: effects of heat shock, inhibition of protein synthesis, and adenovirus infection on translation and mRNA stability. Mol. Cell. Biol. 7:4357-4368.
66. Uhlenbeck, O. C., H.-N. Wu, and J. R. Sampson. 1987. Recognition of RNA by proteins, p. 285-294. In M. Inouye and B. S. Dudock (ed.), Molecular biology of RNA. Academic Press, Inc., New York, N.Y.
67. Ullrich, S. J., C. W. Anderson, W. E. Mercer, and E. J. Appela. 1992. The p53 tumor suppressor protein, a modulator of cell proliferation. J. Biol. Chem. 267:15259-15262.
68. Vogelstein, B., and K. W. Kinzler. 1992. p53 function and dysfunction. Cell 70:523-526.
69. Weiner, K. X. B., R. S. Weiner, F. Maley, and G. F. Maley. 1993. Primary structure of human deoxycytidylate deaminase and overexpression of its functional protein in Escherichia coli. J. Biol. Chem. 168:12983-12989.
70. Wolf, D., and V. Rotter. 1985. Major deletions in the gene encoding the p53 tumor antigen cause lack of p53 expression in HL-60 cells. Proc Natl. Acad. Sci. USA 82:790-794.
71. Wolf, D. I., Z. Laver-Rudich, and V. Rotter. 1985. In vitro expression of human p53 cDNA clones and characterization of the cloned human p53 gene. Mol. Cell. Biol. 5:1887-1893.
72. Zhan, Q., F. Carrier, and A. J. Fornace, Jr. 1993. Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol. Cell. Biol. 13: 4242-4250.