Serine phosphorylation-dependent coregulation of topoisomerase I by the p14ARF tumor suppressor

Biochemistry

Volumn 46, Issue 49, 2007, Pages 14325-14334

  Bandyopadhyay, Keya ^a   Lee, Casey ^a   Haghighi, Ali ^a   Banères, Jean Louis ^b   Parello, Joseph ^c   Gjerset, Ruth A ^a  

^a SIDNEY KIMMEL CANCER CENTER   (United States)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DNA; DRUG DELIVERY; ONCOLOGY; PHOSPHORYLATION; RNA;

CAMPTOTHECIN TREATMENT; CELLULAR RESISTANCE; DNA-BOUND TOPOISOMERASE I; TOPOISOMERASE;

TUMORS;

ARF PROTEIN; CAMPTOTHECIN; DNA TOPOISOMERASE; PROTEIN P14; PROTEIN SERINE KINASE; RECOMBINANT PROTEIN; SERINE; SMALL INTERFERING RNA;

AMINO ACID SEQUENCE; ARTICLE; CANCER CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VIVO STUDY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CAMPTOTHECIN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DNA DAMAGE; DNA TOPOISOMERASES, TYPE I, EUKARYOTIC; GENE EXPRESSION REGULATION; HUMANS; LUNG NEOPLASMS; PHOSPHORYLATION; PHOSPHOSERINE; SERINE; TUMOR SUPPRESSOR PROTEIN P14ARF;

EID: 37049037760     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7013618     Document Type: Article

References (66)

1. Kamb, A., Gruis, N. A., Weaver-Feldhaus, J., Liu, Q., Harshman, K., Tavtigian, S. V., Stockert, E., Day, R. S., 3rd, Johnson, B. E., and Skolnick, M. H. (1994) A cell cycle regulator potentially involved in genesis of many tumor types [see comments], Science 264, 436-440.
2. Bates, S., Phillips, A. C., Clark, P. A., Stott, F., Peters, G., Ludwig, R. L., and Vousden, K. H. (1998) p14ARF links the tumour suppressors RB and p53, Nature 395, 124-125.
3. Palmero, I., Pantoja, C., and Serrano, M. (1998) p19ARF links the tumour suppressor p53 to Ras, Nature 395, 125-126.
4. Sherr, C. J. (2004) An Arf(GFP/GFP) reporter mouse reveals that the Arf tumor suppressor monitors latent oncogenic signals in vivo, Cell Cycle 3, 239-240.
5. Gjerset, R. A. (2006) DNA damage, p14ARF, nucleophosmin (NPM/B23), and cancer, J. Mol. Histol. 37, 239-251.
6. Saadatmandi, N., Tyler, T., Huang, Y., Haghighi, A., Frost, G., Borgstrom, P., and Gjerset, R. A. (2002) Growth suppression by a p14(ARF) exon 1beta adenovirus in human tumor cell lines of varying p53 and Rb status, Cancer Gene Ther. 9, 830-839.
7. Weber, J. D., Jeffers, J. R., Rehg, J. E., Randle, D. H., Lozano, G., Roussel, M. F., Sherr, C. J., and Zambetti, G. P. (2000) p53-independent functions of the p19(ARF) tumor suppressor, Genes Dev. 14, 2358-2365.
8. Ayrault, O., Karayan, L., Riou, J. F., Larsen, C. J., and Seite, P. (2003) Delineation of the domains required for physical and functional interaction of p14ARF with human topoisomerase I, Oncogene 22, 1945-1954.
9. Karayan, L., Riou, J. F., Seite, P., Migeon, J., Cantereau, A., and Larsen, C. J. (2001) Human ARF protein interacts with topoisomerase I and stimulates its activity, Oncogene 20, 836-848.
10. Culotta, V., and Sollner-Webb, B. (1988) Sites of topoisomerase I action on X. laevis ribosomal chromatin: Transcriptionally active rDNA has an approximately 200 bp repeating structure, Cell 52, 585-597.
11. Pommier, Y., Pourquier, P., Fan, Y., and Strumberg, D. (1998) Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme, Biochim. Biophys. Acta 1400, 83-105.
12. Wang, J. C. (1996) DNA topoisomerases, Annu. Rev. Biochem. 65, 635-692.
13. Champoux, J. J. (2001) DNA topoisomerases: Structure, function, and mechanism, Annu. Rev. Biochem. 70, 369-413.
14. Garcia-Carbonero, R., and Supko, J. G. (2002) Current perspectives on the clinical experience, pharmacology, and continued development of the camptothecins, Clin. Cancer Res. 8, 641-661.
15. Rasheed, Z. A., and Rubin, E. H. (2003) Mechanisms of resistance to topoisomerase I-targeting drugs, Oncogene 22, 7296-7304.
16. Xu, Y., and Villalona-Calero, M. A. (2002) Irinotecan: Mechanisms of tumor resistance and novel strategies for modulating its activity, Ann. Oncol. 13, 1841-1851.
17. Pommier, Y., Gupta, M., Valenti, M., and Nieves-Neira, W. (1996) Cellular resistance to camptothecins, Ann. N.Y. Acad. Sci. 803, 60-73.
18. Takahashi, T., Carbone, D., Takahashi, T., Nau, M. M., Hida, T., Linnoila, I., Ueda, R., and Minna, J. D. (1992) Wild-type but not mutant p53 suppresses the growth of human lung cancer cells bearing multiple genetic lesions, Cancer Res. 52, 2340-2343.
19. Huang, Y., Tyler, T., Saadatmandi, N., Lee, C., Borgstrom, P., and Gjerset, R. A. (2003) Enhanced tumor suppression by a p14ARF/p53 bicistronic adenovirus through increased p53 protein translation and stability, Cancer Res. 63, 3646-3653.
20. Ayrault, O., Andrique, L., Larsen, C. J., and Seite, P. (2004) Human Arf tumor suppressor specifically interacts with chromatin containing the promoter of rRNA genes, Oncogene 23, 8097-8104.
21. Lee, C., Smith, B. A., Bandyopadhyay, K., and Gjerset, R. A. (2005) DNA damage disrupts the p14ARF-B23(nucleophosmin) interaction and triggers a transient subnuclear redistribution of p14ARF, Cancer Res. 65, 9834-9842.
22. Olnes, M. I., and Kurl, R. N. (1994) Isolation of nuclear extracts from fragile cells: A simplified procedure applied to thymocytes, Biotechniques 17, 828-829.
23. Kaiserman, H. B., Ingebritsen, T. S., and Benbow, R. M. (1988) Regulation of Xenopus laevis DNA topoisomerase I activity by phosphorylation in vitro, Biochemistry 27, 3216-3222.
24. Vivo, M., Calogero, R. A., Sansone, F., Calabro, V., Parisi, T., Borrelli, L., Saviozzi, S., and La, Mantia, G. (2001) The human tumor suppressor arf interacts with spinophilin/neurabin II, a type 1 protein-phosphatase- binding protein, J. Biol. Chem. 276, 14161-14169.
25. Danks, M. K., Garrett, K. E., Marion, R. C., and Whipple, D. O. (1996) Subcellular redistribution of DNA topoisomerase I in anaplastic astrocytoma cells treated with topotecan, Cancer Res. 56, 1664-1673.
26. Gobert, C., Skladanowski, A., and Larsen, A. K. (1999) The interaction between p53 and DNA topoisomerase I is regulated differently in cells with wild-type and mutant p53, Proc. Natl. Acad. Sci. U.S.A. 96, 10355-10360.
27. D'Arpa, P., Machlin, P. S., Ratrie, H., 3rd, Rothfield, N. F., Cleveland, D. W., and Earnshaw, W. C. (1988) cDNA cloning of human DNA topoisomerase I: Catalytic activity of a 67.7-kDa carboxyl-terminal fragment, Proc. Natl. Acad. Sci. U.S.A. 85, 2543-2547.
28. Liu, L. F., and Miller, K. G. (1981) Eukaryotic DNA topoisomerases: Two forms of type I DNA topoisomerases from HeLa cell nuclei, Proc. Natl. Acad. Sci. U.S.A. 78, 3487-3491.
29. Rubin, E., Pantazis, P., Bharti, A., Toppmeyer, D., Giovanella, B., and Kufe, D. (1994) Identification of a mutant human topoisomerase I with intact catalytic activity and resistance to 9-nitro-camptothecin, J. Biol. Chem. 269, 2433-2439.
30. Mao, Y., Mehl, I. R., and Muller, M. T. (2002) Subnuclear distribution of topoisomerase I is linked to ongoing transcription and p53 status, Proc. Natl. Acad. Sci. U.S.A. 99, 1235-1240.
31. Durban, E., Mills, J. S., Roll, D., and Busch, H. (1983) Phosphorylation of purified Novikoff hepatoma topoisomerase I, Biochem. Biophys. Res. Commun. 111, 897-905.
32. Pommier, Y., Kerrigan, D., Hartman, K. D., and Glazer, R. I. (1990) Phosphorylation of mammalian DNA topoisomerase I and activation by protein kinase C, J. Biol. Chem. 265, 9418-9422.
33. Chi, S. G., deVere, White, R. W., Muenzer, J. T., and Gumerlock, P. H. (1997) Frequent alteration of CDKN2 (p16(INK4A)/MTS1) expression in human primary prostate carcinomas, Clin. Cancer Res. 3, 1889-1897.
34. Sirikantaramas, S., Asano, T., Sudo, H., Yamazaki, M., and Saito, K. (2007) Camptothecin: Therapeutic potential and biotechnology, Curr. Pharm. Biotechnol. 8, 196-202.
35. Turman, M. A., and Douvas, A. (1993) A casein kinase type II (CKII)-like nuclear protein kinase associates with, phosphorylates, and activates topoisomerase I, Biochem. Med. Metab. Biol. 50, 210-225.
36. Coderoni, S., Paparelli, M., and Gianfranceschi, G. L. (1990) Phosphorylation sites for type N II protein kinase in DNA-topoisomerase I from calf thymus, Int. J. Biochem. 22, 737-746.
37. Samuels, D. S., and Shimizu, N. (1992) DNA topoisomerase I phosphorylation in murine fibroblasts treated with 12-O-tetradecanoylphorbol-13-acetate and in vitro by protein kinase, J. Biol. Chem. 267, 11156-11162.
38. Ackerman, P., Glover, C. V., and Osheroff, N. (1985) Phosphorylation of DNA topoisomerase II by casein kinase II: Modulation of eukaryotic topoisomerase II activity in vitro, Proc. Natl. Acad. Sci. U.S.A. 82, 3164-3168.
39. Durban, E., Goodenough, M., Mills, J., and Busch, H. (1985) Topoisomerase I phosphorylation in vitro and in rapidly growing Novikoff hepatoma cells, EMBO J. 4, 2921-2926.
40. Yu, D., Khan, E., Khaleque, M. A., Lee, J., Laco, G., Kohlhagen, G., Kharbanda, S., Cheng, Y. C., Pommier, Y., and Bharti, A. (2004) Phosphorylation of DNA topoisomerase I by the c-Abl tyrosine kinase confers camptothecin sensitivity, J. Biol. Chem. 279, 51851-51861.
41. Javaherian, K., and Liu, L. F. (1983) Association of eukaryotic DNA topoisomerase I with nucleosomes and chromosomal proteins, Nucleic Acids Res. 11, 461-472.
42. Bauer, P. I., Chen, H. J., Kenesi, E., Kenessey, I., Buki, K. G., Kirsten, E., Hakam, A., Hwang, J. I., and Kun, E. (2001) Molecular interactions between poly(ADP-ribose) polymerase (PARP I) and topoisomerase I (Topo I): Identification of topology of binding, FEBS Lett. 506, 239-242.
43. Straub, T., Grue, P., Uhse, A., Lisby, M., Knudsen, B. R., Tange, T. O., Westergaard, O., and Boege, F. (1998) The RNA-splicing factor PSF/p54 controls DNA-topoisomerase I activity by a direct interaction, J. Biol. Chem. 273, 26261-26264.
44. Lebel, M., Spillare, E. A., Harris, C. C., and Leder, P. (1999) The Werner syndrome gene product co-purifies with the DNA replication complex and interacts with PCNA and topoisomerase I, J. Biol. Chem. 274, 37795-37799.
45. Bharti, A. K., Olson, M. O., Kufe, D. W., and Rubin, E. H. (1996) Identification of a nucleolin binding site in human topoisomerase I, J. Biol. Chem. 271, 1993-1997.
46. Carty, S. M., and Greenleaf, A. L. (2002) Hyperphosphorylated C-terminal repeat domain-associating proteins in the nuclear proteome link transcription to DNA/chromatin modification and RNA processing, Mol. Cell. Proteom. 1, 598-610.
47. Merino, A., Madden, K. R., Lane, W. S., Champoux, J. J., and Reinberg, D. (1993) DNA topoisomerase I is involved in both repression and activation of transcription, Nature 365, 227-232.
48. Haluska, P., Jr., Saleem, A., Rasheed, Z., Ahmed, F., Su, E. W., Liu, L. F., and Rubin, E. H. (1999) Interaction between human topoisomerase I and a novel RING finger/arginine-serine protein, Nucleic Acids Res. 27, 2538-2544.
49. Czubaty, A., Girstun, A., Kowalska-Loth, B., Trzcinska, A. M., Purta, E., Winczura, A., Grajkowski, W., and Staron, K. (2005) Proteomic analysis of complexes formed by human topoisomerase I, Biochim. Biophys. Acta 1749, 133-141.
50. Haluska, P., Jr., and Rubin, E. H. (1998) A role for the amino terminus of human topoisomerase I, Adv. Enzyme Regul. 38, 253-262.
51. Liu, L. F. (1989) DNA topoisomerase poisons as antitumor drugs, Annu. Rev. Biochem. 58, 351-375.
52. Madelaine, I., Prost, S., Naudin, A., Riou, G., Lavelle, F., and Riou, J. F. (1993) Sequential modifications of topoisomerase I activity in a camptothecin-resistant cell line established by progressive adaptation, Biochem. Pharmacol. 45, 339-348.
53. Urasaki, Y., Laco, G. S., Pourquier, P., Takebayashi, Y., Kohlhagen, G., Gioffre, C., Zhang, H., Chatterjee, D., Pantazis, P., and Pommier, Y. (2001) Characterization of a novel topoisomerase I mutation from a camptothecin- resistant human prostate cancer cell line, Cancer Res. 61, 1964-1969.
54. Kubota, N., Kanzawa, F., Nishio, K., Takeda, Y., Ohmori, T., Fujiwara, Y., Terashima, Y., and Saijo, N. (1992) Detection of topoisomerase I gene point mutation in CPT-11 resistant lung cancer cell line, Biochem. Biophys. Res. Commun. 188, 571-577.
55. Tamura, H., Kohchi, C., Yamada, R., Ikeda, T., Koiwai, O., Patterson, E., Keene, J. D., Okada, K., Kjeldsen, E., Nishikawa, K., and et al. (1991) Molecular cloning of a cDNA of a camptothecin-resistant human DNA topoisomerase I and identification of mutation sites, Nucleic Acids Res. 19, 69-75.
56. Tanizawa, A., Beitrand, R., Kohlhagen, G., Tabuchi, A., Jenkins, J., and Pommier, Y. (1993) Cloning of Chinese hamster DNA topoisomerase I cDNA and identification of a single point mutation responsible for camptothecin resistance, J. Biol. Chem. 268, 25463-25468.
57. Staron, K., Kowalska-Loth, B., and Szumiel, I. (1996) Lowered phosphorylation of topoisomerase I is a direct reason for reduced sensitivity of L5178Y-S cells to camptothecin, Ann. N.Y. Acad. Sci. 803, 321-323.
58. Andrews, P. A., Jones, J. A., Varki, N. M., and Howell, S. B. (1990) Rapid emergence of acquired cis-diamminedichloroplatinum(II) resistance in an in vivo model of human ovarian carcinoma, Cancer Commun. 2, 93-100.
59. Isonishi, S., Jekunen, A. P., Hom, D. K., Eastman, A., Edelstein, P. S., Thiebaut, F. B., Christen, R. D., and Howell, S. B. (1992) Modulation of cisplatin sensitivity and growth rate of an ovarian carcinoma cell line by bombesin and tumor necrosis factor-alpha, J. Clin. Invest. 90, 1436-1442.
60. Bertwistle, D., Sugimoto, M., and Sherr, C. J. (2004) Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23, Mol. Cell. Biol. 24, 985-996.
61. Savkur, R. S., and Olson, M. O. (1998) Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease, Nucleic Acids Res. 26, 4508-4515.
62. Itahana, K., Bhat, K. P., Jin, A., Itahana, Y., Hawke, D., Kobayashi, R., and Zhang, Y. (2003) Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation, Mol. Cell 12, 1151-1164.
63. Sugimoto, M., Kuo, M. L., Roussel, M. F., and Sherr, C. J. (2003) Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing, Mol. Cell 11, 415-424.
64. Ayrault, O., Andrique, L., Fauvin, D., Eymin, B., Gazzeri, S., and Seite, P. (2006) Human tumor suppressor p14ARF negatively regulates rRNA transcription and inhibits UBF1 transcription factor phosphorylation, Oncogene 25, 7577-7586.
65. Korgaonkar, C., Hagen, J., Tompkins, V., Frazier, A. A., Allamargot, C., Quelle, F. W., and Quelle, D. E. (2005) Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function, Mol. Cell. Biol. 25, 1258-1271.
66. Rizos, H., McKenzie, H. A., Ayub, A. L., Woodruff, S., Becker, T. M., Scurr, L. L., Stahl, J., and Kefford, R. F. (2006) Physical and functional interaction of the p14ARF tumor suppressor with ribosomes, J. Biol. Chem. 281, 38080-38088.