The cell cycle-coupled expression of topoisomerase IIα during S phase is regulated by mRNA stability and is disrupted by heat shock or ionizing radiation

Molecular and Cellular Biology

Volumn 16, Issue 4, 1996, Pages 1500-1508

  Goswami, Prabhat C ^a   Roti Roti, Joseph L ^a   Hunt, Clayton R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); MESSENGER RNA;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; GENE EXPRESSION REGULATION; HEAT SHOCK; HUMAN; HUMAN CELL; IONIZING RADIATION; MESSENGER RNA SYNTHESIS; PRIORITY JOURNAL; PROTEIN STABILITY;

EID: 0029928174     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.4.1500     Document Type: Article

References (50)

1. Andrews, G. K., M. A. Harding, J. P. Calvet, and E. D. Adamson. 1987. The heat shock response in HeLa cells is accompanied by elevated expression of the c-fos proto-oncogene Mol Cell. Biol. 7:3452-3458.
2. Austin, C. A., and L. M. Fisher. 1990. Isolation and characterization of a human cDNA clone encoding a novel DNA topoisomerase II homologue from HeLa cells. FEBS Lett. 266:115-117.
3. Bjorklund, S., E. Skoguran, and L. Thelander. 1992. An S-phase specific release from a transcriptional block regulates the expression of mouse ribonucleotide reductase R2 subunit. EMBO J. 11:4953-4959.
4. Coppock, D. T., and A. B. Pardee. 1987. Control of thymidine kinase mRNA during the cell cycle Mol. Cell. Biol. 7:2925-2932.
5. Dalton, S. 1992. Cell cycle regulation of the human cdc2 gene. EMBO J. 11:1797-1804
6. Datta, R., R. Hass, H. Gunji, R. Weichselbaum, and D. Kufe. 1992. Down-regulation of cell cycle control genes by ionizing radiation. Cell Growth Differ. 3:637-644
7. 1/S-regulated E2F-containing protein complexes bind to the mouse thymidine kinase gene promoter. J. Biol. Chem. 269:1306-1313.
8. Downes, C. S., D. J. Clarke, A. M. Mullinger, J. F. Gimenez-Abian, A. M. Creighton, and R. T. Johnson. 1994 A topoisomerase II-dependent G2 checkpoint in mammalian cells. Nature (London) 372:467-470.
9. Drummond, I. A. S., S. A. McClure, M. Poenie, R. Y. Tsien, and R. A. Steinhardt. 1986 Large changes in intracellular pH and calcium observed during heat shock are not responsible for the induction of heat shock proteins in Drosophila melanogaster Mol. Cell. Biol. 6:1767-1775.
10. Earnshaw, W. C., and M. M. S. Heck. 1985 Localization of topoisomerase II in mitotic chromosomes J. Cell Biol. 100:1716-1715.
11. 1, p. 176-183. In D. Beach, C. Basilico, and J. Newport (ed.), Cell cycle control in eukaryotes. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
12. Farnham, P. J., and R. T. Schimke. 1985. Transcriptional regulation of mouse dihydiofolate reductase in the cell cycle. J. Biol. Chem. 260:7675-7680.
13. Glotzer, M., A. W. Murray, and M. W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature (London) 349:132-138.
14. 1-transit following transient inhibition of DNA replication. Exp. Cell Res 214:198-208
15. Goswami, P. C., M. Hill, R. Higashikubo, W. D. Wright, and J. L. Roti Roti. 1992 The suppression of the synthesis of a nuclear protein in cells blocked in G2 phase. identification of NP-170 as topoisomerase II. Radiat. Res 132:162-167.
16. Greenberg, M. E., and T. P. Bender. 1992. Identification of newly transcribed RNA. p. 4.10.1-4.10.9. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol 1. John Wiley & Sons, New York.
17. Harris, M. E., R. Bohni, M. H. Schneiderman, L. Ramamurthy, D. Schumerli, and W. F. Marzluff. 1991. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two post-transcriptional steps. Mol. Cell. Biol. 11:2416-2424.
18. Heck, M. M. S., W. N. Hittelman, and W. C. Earnshaw. 1988. Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc. Natl. Acad. Sci. USA 85:1086-1090.
19. Hochhauser, D., C. A. Stanway, A. L. Harris, and I. D. Hickson. 1992. Cloning and characterization of the 5′-flanking region of the human topoisomerase IIα gene J. Biol. Chem 267:18961-18965.
20. Holm, C. 1994 Coming undone: how to untangle a chromosome. Cell 77: 955-957.
21. Hunt, C., and R. Morimoto. 1985. Conserved features of eukaryotic HSP70 genes revealed by comparison with the nucleotide sequence of human HSP70. Proc. Natl. Acad. Sci. USA 82:6455-6459
22. Ishida, R., M. Sato, T. Narita, K. R. Utsumi, T. Nishimoto, T. Marita, H. Nagata, and T. Andoh. 1994. Inhibition of DNA topoisomerase II by ICRF-193 induces polyploidization by uncoupling chromosome dynamics from other cell cycle events. J. Cell Biol. 126:1341-1351
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 217:680-685.
24. Lam, E. W. F., and R. J. Watson. 1993 An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J. 2:2705-2713.
25. Lindquist, S. 1981. Regulation of protein synthesis during heat shock. Nature (London) 293:311-314.
26. Liu, R. Y., X. Li, L. Li, and G. C. Li. 1992. Expression of human hsp70 in rat fibroblast enhances cell survival and facilitates recovery from translational and transcriptional inhibition following heat shock. Cancer Res. 52:3667-3673.
27. Lüscher, B., and R. N. Eisenman. 1988. c-myc and c-myb protein degradation: effect of metabolic inhibitors and heat shock. Mol. Cell. Biol. 8:2504-2512.
28. Means, A. L., J. E. Slansky, S. L. McMahon, M. W. Knuth, and P. J. Farnham. 1992. The HIP1 binding site is required for growth regulation of the dihydrofolate reductase gene promoter. Mol. Cell. Biol. 12:1054-1063.
29. Milarski, K. L., and R. I. Morimoto. 1986. Expression of human HSP70 during the synthetic phase of the cell cycle. Proc. Natl. Acad Sci USA 83:9517-9521.
30. Muschel, R. J., H. B. Zhang, G. Iliakis, and W. G. McKenna. 1991. Cyclin B expression in HeLa cells during the G2 block induced by ionizing radiation Cancer Res. 51:5113-5117.
31. Paraq, H. A., B. Raboy, and R. G. Kulka. 1987. Effect of heat shock on protein degradation in mammalian cells: involvement of the ubiquitin system. EMBO J. 6:55-61.
32. cdc2. Cell 58:833-846.
33. Pines, J., and T. Hunter. 1990 Human cyclin A is adenovirus EIA-associated protein P60 and behaves differently from cyclin B. Nature (London) 346: 760-763.
34. Plumb, M., J. Stein, and G. Stein. 1983. Influence of DNA synthesis inhibition on the coordinate expression of core human histone genes during S phase. Nucleic Acids Res. 11:7927-7945.
35. Poenie, M., J. Alderton, R. Steinhardt, and R. Tsien. 1986. Calcium rises abruptly and briefly throughout the cell at the onset of anaphase. Science 233:886-889.
36. Puck, T. T., and P. I. Marcus. 1956 Action of x-rays on mammalian cells J Exp Med. 103:653-666.
37. Sadis, S., E. Hickey, and L. A. Weber. 1988. Effect of heat shock on RNA metabolism in HeLa cells. J. Cell. Physiol. 135:377-386.
38. Sapareto, S. A., L. E. Hopwood, W. C. Dewey, M. R. Raju, and J. W. Gray. 1978. Effects of hyperthermia on survival and progression of Chinese hamster ovary cells. Cancer Res. 38:393-400.
39. Snapka, R. M., M. A. Powelson, and J. M. Strayer. 1988. Swiveling and decatenation of replicating simian virus 40 genomes in vivo. Mol. Cell. Biol 8:515-521.
40. Sundin, O., and V. Varshavsky. 1981. Arrest of segregation leads to accumulation in highly itwined catenated dimers: dissection of the final stages of SV40 replication. Cell 47:659-669.
41. Tanabe, K., Y. Ikegami, R. Ishida, and T. Andoh. 1991 Inhibition of topoisomerase II by arititumor agents bis (2,6-dioxopiperazine) derivatives. Cancer Res. 51:4903-4908
42. Terasima, T., and L. J. Tolmach. 1963. Growth and nucleic acid synthesis in synchronously dividing populations of HeLa cells. Exp. Cell Res. 30:344-362
43. Thomas, D. Y., F. H. Drake, K. B. Tan, S. R. Per, S. T. Crooke, and C. K. Miranelli. 1989. Characterization and immunological identification of cDNA clones encoding two human DNA topoisomerase II isozymes. Proc. Natl. Acad Sci. USA 86:9431-9435.
44. Tsai-Pflugfelder, M., L. F. Liu, A. A. Liu, K. M. Tewey, J. Whang-Peng, T. Knutsen, K. Huebner, C. M. Croce, and J. C. Wang. 1988. Cloning and sequencing of cDNA encoding human DNA topoisomerase II and localization of the gene to chromosome region 17q21-22. Proc. Natl. Acad. Sci USA 85:7177-7181.
45. Uemura, T., H. Ohkura, Y. Adachi, K. Morino, K. Shiozaki, and M. Yanagida. 1987. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S pombe Cell 50:917-925
46. Wang, J. C. 1985. DNA topoisomerases. Annu. Rev. Biochem. 54:665-697.
47. Wang, J. C. 1991. DNA topoisomerase: why so many. J. Biol. Chem. 266: 6659-6662.
48. Woessner, R. D., M. R. Mattern, C. K. Mirabelli, R. K. Johnson, and F. H. Drake. 1991. Proliferation- and cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells Cell Growth Differ. 209:209-214.
49. Wood, E. R., and W. C. Earnshaw. 1990. Mitotic chromatin condensation in vitro using somatic cell extracts and nuclei with variable levels of endogenous topoisomerase II. J. Cell Biol. 111:2839-2850.
50. Wu, B. J., R. E. Kingston, and R. I. Morimoto. 1986. Human HSP70 promoter contains at least two distinct regulatory domains. Proc. Natl. Acad. Sci. USA 83:629-633.