Role of DNA 5-methylcytosine transferase in cell transformation by fos

Science

Volumn 283, Issue 5400, 1999, Pages 387-390

  Bakin, A V ^a   Curran, T ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA 5 METHYLCYTOSINE TRANSFERASE; ONCOPROTEIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ARTICLE; CELL TRANSFORMATION; DEACETYLATION; DNA METHYLATION; ENZYME ANALYSIS; FIBROBLAST; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL;

5-METHYLCYTOSINE; ACETYLATION; ANIMALS; CELL SIZE; CELL TRANSFORMATION, NEOPLASTIC; CYTOSINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, FOS; HISTONE DEACETYLASES; HISTONES; HYDROXAMIC ACIDS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 0033555953     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.283.5400.387     Document Type: Article

References (55)

1. T. Curran, in The Oncogene Handbook, E. P. Reddy, A. M. Skalka, T. Curran, Eds. (Elsevier, Amsterdam, 1988), p. 307-325.
2. J. I. Morgan and T. Curran, Annu. Rev. Neurosci. 14, 421 (1991).
3. E. Saez et al., Cell 82, 721 (1995); J. Koistinaho and S. M. Sagar, Brain Res. Mol. Brain. Res. 29, 53 (1995); F. Hafezi et al., Nature Med. 3, 346 (1997).
4. E. Saez et al., Cell 82, 721 (1995); J. Koistinaho and S. M. Sagar, Brain Res. Mol. Brain. Res. 29, 53 (1995); F. Hafezi et al., Nature Med. 3, 346 (1997).
5. E. Saez et al., Cell 82, 721 (1995); J. Koistinaho and S. M. Sagar, Brain Res. Mol. Brain. Res. 29, 53 (1995); F. Hafezi et al., Nature Med. 3, 346 (1997).
6. M. P. Finkel, B. O. Biskis, P. B. Jinkins, Science 151, 698 (1966); A. E. Grigoriadis, Z. Q. Wang, E. F. Wagner, Trends Genet. 11, 436 (1995).
7. M. P. Finkel, B. O. Biskis, P. B. Jinkins, Science 151, 698 (1966); A. E. Grigoriadis, Z. Q. Wang, E. F. Wagner, Trends Genet. 11, 436 (1995).
8. A. D. Miller, T. Curran, I. M. Verma, Cell 36, 51 (1984); M. Neuberg, M. Schuermann, R. Muller, Oncogene 6, 1325 (1991); M. Schuermann et al., Cell 56, 507 (1989); R. Wisdon and I. M. Verma, Mol. Cell. Biol. 13, 7429 (1993).
9. A. D. Miller, T. Curran, I. M. Verma, Cell 36, 51 (1984); M. Neuberg, M. Schuermann, R. Muller, Oncogene 6, 1325 (1991); M. Schuermann et al., Cell 56, 507 (1989); R. Wisdon and I. M. Verma, Mol. Cell. Biol. 13, 7429 (1993).
10. A. D. Miller, T. Curran, I. M. Verma, Cell 36, 51 (1984); M. Neuberg, M. Schuermann, R. Muller, Oncogene 6, 1325 (1991); M. Schuermann et al., Cell 56, 507 (1989); R. Wisdon and I. M. Verma, Mol. Cell. Biol. 13, 7429 (1993).
11. A. D. Miller, T. Curran, I. M. Verma, Cell 36, 51 (1984); M. Neuberg, M. Schuermann, R. Muller, Oncogene 6, 1325 (1991); M. Schuermann et al., Cell 56, 507 (1989); R. Wisdon and I. M. Verma, Mol. Cell. Biol. 13, 7429 (1993).
12. T. Curran and N. M. Teich, Virology 116, 221 (1982); F. J. Rauscher III et al., Science 240, 1010 (1988).
13. T. Curran and N. M. Teich, Virology 116, 221 (1982); F. J. Rauscher III et al., Science 240, 1010 (1988).
14. G. G. Miao and T. Curran, Mol. Cell. Biol. 14, 4295 (1994).
15. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
16. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
17. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
18. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
19. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
20. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
21. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
22. S. Braselmann et al., J. Cell Sci. Suppl. 16, 97 (1992); R. F. Hennigan, K. L. Hawker, B. W. Ozanne, Oncogene 9, 3591 (1994); C. J. Kho and H. Zarbl, Proc. Natl. Acad. Sci. U.S.A. 89, 2200 (1992); C. J. Kho, Y. Wang, H. Zarbl, Cell Growth Differ. 7, 1157 (1996); R. F. Lamb et al., Mol. Cell. Biol. 17, 963 (1997); K. U. Jooss and R. Muller, Oncogene 10, 603 (1995); M. Orlandini, L. Marconcini, R. Ferruzzi, S. Oliviero, Proc. Natl. Acad. Sci. U.S.A. 93, 11675 (1996); Y. Yamada, J. Nezu, M. Shimane, Y. Hirata, Genomics 42, 483 (1997).
23. N. Lisitsyn, N. Lisitsyn, M. Wigler, Science 259, 946 (1993); M. Hubank and D. G. Schatz, Nucleic Acids Res. 22, 5640 (1994).
24. N. Lisitsyn, N. Lisitsyn, M. Wigler, Science 259, 946 (1993); M. Hubank and D. G. Schatz, Nucleic Acids Res. 22, 5640 (1994).
25. For RDA analysis (9), mRNA isolated from Lacl-fos cells that were maintained for 72 hours in the presence or absence of IPTG was used to prepare double-stranded cDNA. cDNA from transformed cells was used as a tester, and cDNA from normal cells was used as a driver. A 100-fold excess of driver over tester was used in the first subtraction step, and a 400-fold excess was used in each subsequent step. After the third round of RDA, amplicons were subcloned into pBluescript (SK+), and inserts were amplified with T7 and T3 primers. Amplified sequences were hybridized with cDNA probes that were prepared from normal and fos-transformed cells, and differentially regulated clones were sequenced. Cell lines from clonal rat 208F fibroblasts were isolated by transfection with lipofectamin (GIBCO BRL), and multiple G418-resistant lines were selected. For dnmt1 antisense cell lines, we selected clones with a flat cell morphology that expressed both antisense dnmt1 and fos. The dnmt1 construct that was used to create the stable cell lines does not contain sequences from the first exon so the product is smaller than the endogenous rat Dnmt1 protein (Fig. 2A).
26. L. Joseph, S. Lapid, V. Sukhatme, Nucleic Acids Res. 15, 3186 (1987); B. R. Troen, D. Ascherman, D. Atlas, M. M. Gottesman, J. Biol. Chem. 263, 254 (1988); F. Umenishi and A. S. Verkman, Genomics 47, 341 (1998).
27. L. Joseph, S. Lapid, V. Sukhatme, Nucleic Acids Res. 15, 3186 (1987); B. R. Troen, D. Ascherman, D. Atlas, M. M. Gottesman, J. Biol. Chem. 263, 254 (1988); F. Umenishi and A. S. Verkman, Genomics 47, 341 (1998).
28. L. Joseph, S. Lapid, V. Sukhatme, Nucleic Acids Res. 15, 3186 (1987); B. R. Troen, D. Ascherman, D. Atlas, M. M. Gottesman, J. Biol. Chem. 263, 254 (1988); F. Umenishi and A. S. Verkman, Genomics 47, 341 (1998).
29. Previously, cathepsin L mRNA was reported to be upregulated in v-fos-transformed rat fibroblasts and in ras-transformed mouse fibroblasts. Cathepsin L is a cysteine protease that has been associated with the remodeling of the extracellular matrix and the activation of proenzymes. Application of E-64, a specific inhibitor of cathepsin L, did not affect the morphology of fos-transformed fibroblasts, which suggests that this protein is not required for fos-induced transformation.
30. A. D. Miller, I. M. Verma, T. Curran, J. Virol. 55, 521 (1985).
31. J. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 90, 8891 (1993); P. M. Vertino, R. W. Yen, J. Gao, S. B. Baylin, Mol. Cell. Biol. 16, 4555 (1996).
32. J. Wu et al., Proc. Natl. Acad. Sci. U.S.A. 90, 8891 (1993); P. M. Vertino, R. W. Yen, J. Gao, S. B. Baylin, Mol. Cell. Biol. 16, 4555 (1996).
33. T. L. Kautiainen and P. A. Jones, J. Biol. Chem. 261, 1594 (1986); S. B. Baylin, J. G. Herman, J. R. Graff, P. M. Vertino, J. P. Issa, Adv. Cancer Res. 72, 141 (1998).
34. T. L. Kautiainen and P. A. Jones, J. Biol. Chem. 261, 1594 (1986); S. B. Baylin, J. G. Herman, J. R. Graff, P. M. Vertino, J. P. Issa, Adv. Cancer Res. 72, 141 (1998).
35. A. R. MacLeod, J. Rouleau, M. Szyf, J. Biol. Chem. 270, 11327 (1995); J. Rouleau, A. R. MacLeod, M. Szyf, ibid., p. 1595.
36. A. R. MacLeod, J. Rouleau, M. Szyf, J. Biol. Chem. 270, 11327 (1995); J. Rouleau, A. R. MacLeod, M. Szyf, ibid., p. 1595.
37. J. A. Yoder et al., ibid. 271, 31092 (1996); K. L. Tucker et al., Proc. Natl. Acad. Sci. U.S.A. 93, 12920 (1996).
38. J. A. Yoder et al., ibid. 271, 31092 (1996); K. L. Tucker et al., Proc. Natl. Acad. Sci. U.S.A. 93, 12920 (1996).
39. S. Xanthoudakis and T. Curran, EMBO J. 11, 653 (1992).
40. X. Nan et al., Nature 393, 386 (1998); P. L. Jones et al., Nature Genet. 19, 187 (1998).
41. X. Nan et al., Nature 393, 386 (1998); P. L. Jones et al., Nature Genet. 19, 187 (1998).
42. M. Yoshida, M. Kijima, M. Akita, T. Beppu, Exp. Cell Res. 192, 122 (1991).
43. K. Sugita, H. Yoshida, M. Matsumoto, S. Matsutani, Biochem. Biophys. Res. Commun. 182, 379 (1992); M. Futamura et al., Oncogene 10, 1119 (1995).
44. K. Sugita, H. Yoshida, M. Matsumoto, S. Matsutani, Biochem. Biophys. Res. Commun. 182, 379 (1992); M. Futamura et al., Oncogene 10, 1119 (1995).
45. C. Lengauer, K. W. Kinzler, B. Vogelstein, Proc. Natl. Acad. Sci. U.S.A. 94, 2545 (1997).
46. P. W. Laird et al., Cell 81, 197 (1995); P. W. Laird and R. Jaenisch, Annu. Rev. Genet. 30, 441 (1996).
47. P. W. Laird et al., Cell 81, 197 (1995); P. W. Laird and R. Jaenisch, Annu. Rev. Genet. 30, 441 (1996).
48. W. L. Hsiao, S. Gattoni-Celli, I. B. Weinstein, J. Virol. 57, 1119 (1986); J. A. Mietz and E. L. Kuff, Proc. Natl. Acad. Sci. U.S.A. 87, 2269 (1990); A. Dupressoir and T. Heidmann, Mol. Cell. Biol. 16, 4495 (1996); R. J. W. O'Neill, M. J. O'Neill, J. A. M. Graves, Nature 393, 68 (1998); R. Z. Chen, U. Pettersson, C. Beard, L. Jackson- Grusby, R. Jaenisch, ibid. 395, 89 (1998).
49. W. L. Hsiao, S. Gattoni-Celli, I. B. Weinstein, J. Virol. 57, 1119 (1986); J. A. Mietz and E. L. Kuff, Proc. Natl. Acad. Sci. U.S.A. 87, 2269 (1990); A. Dupressoir and T. Heidmann, Mol. Cell. Biol. 16, 4495 (1996); R. J. W. O'Neill, M. J. O'Neill, J. A. M. Graves, Nature 393, 68 (1998); R. Z. Chen, U. Pettersson, C. Beard, L. Jackson- Grusby, R. Jaenisch, ibid. 395, 89 (1998).
50. W. L. Hsiao, S. Gattoni-Celli, I. B. Weinstein, J. Virol. 57, 1119 (1986); J. A. Mietz and E. L. Kuff, Proc. Natl. Acad. Sci. U.S.A. 87, 2269 (1990); A. Dupressoir and T. Heidmann, Mol. Cell. Biol. 16, 4495 (1996); R. J. W. O'Neill, M. J. O'Neill, J. A. M. Graves, Nature 393, 68 (1998); R. Z. Chen, U. Pettersson, C. Beard, L. Jackson- Grusby, R. Jaenisch, ibid. 395, 89 (1998).
51. W. L. Hsiao, S. Gattoni-Celli, I. B. Weinstein, J. Virol. 57, 1119 (1986); J. A. Mietz and E. L. Kuff, Proc. Natl. Acad. Sci. U.S.A. 87, 2269 (1990); A. Dupressoir and T. Heidmann, Mol. Cell. Biol. 16, 4495 (1996); R. J. W. O'Neill, M. J. O'Neill, J. A. M. Graves, Nature 393, 68 (1998); R. Z. Chen, U. Pettersson, C. Beard, L. Jackson- Grusby, R. Jaenisch, ibid. 395, 89 (1998).
52. W. L. Hsiao, S. Gattoni-Celli, I. B. Weinstein, J. Virol. 57, 1119 (1986); J. A. Mietz and E. L. Kuff, Proc. Natl. Acad. Sci. U.S.A. 87, 2269 (1990); A. Dupressoir and T. Heidmann, Mol. Cell. Biol. 16, 4495 (1996); R. J. W. O'Neill, M. J. O'Neill, J. A. M. Graves, Nature 393, 68 (1998); R. Z. Chen, U. Pettersson, C. Beard, L. Jackson-Grusby, R. Jaenisch, ibid. 395, 89 (1998).
53. M.-H. Kuo and C. D. Allis, Bioessays 20, 615 (1998).
54. M. A. Gama-Sosa et al., Nucleic Acids Res. 11, 6883 (1983).
55. We thank S. Baylin for the CMVdnmt1 expression vector; M. Szyf for antibodies to Dnmt1 and for plasmids containing the 5′-end region of the dnmt1 gene; T. Bestor for antibodies to mouse Dnmt1; and C. Sherr, S. Baker, and colleagues in the Curran lab for helpful discussions and critical comments on this manuscript. Supported in part by NIH Cancer Center Support CORE grant P30 CA21765 and by the American Lebanese Syrian Associated Charities (ALSAC).