The effects of camptothecin on RNA polymerase II transcription: Roles of DNA topoisomerase I

Biochimie

Volumn 89, Issue 4, 2007, Pages 482-489

  Capranico, Giovanni ^a   Ferri, Francesca ^a   Fogli, Maria Vittoria ^a   Russo, Alessandra ^a   Lotito, Luca ^a   Baranello, Laura ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Alternative splicing; Chromatin; DNA topoisomerase I; RNA polymerase II; Transcription elongation

Indexed keywords

CAMPTOTHECIN; CELL DNA; DNA TOPOISOMERASE; RNA POLYMERASE II;

ARTICLE; CELL FUNCTION; CHROMATIN; DNA DAMAGE; DRUG EFFICACY; DRUG INHIBITION; DRUG MECHANISM; DRUG POTENCY; ENZYME MECHANISM; ENZYME STRUCTURE; HUMAN; NONHUMAN; RNA TRANSCRIPTION;

ANIMALS; CAMPTOTHECIN; CHROMATIN; DNA TOPOISOMERASES, TYPE I; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MODELS, GENETIC; RNA POLYMERASE II; RNA SPLICING; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 34247355825     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2007.01.001     Document Type: Article

References (73)

1. Wang J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol. 3 (2002) 430-440
2. Champoux J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70 (2001) 369-413
3. Zhang H., Barcelo J.M., Lee B., Kohlhagen G., Zimonjic D.B., Popescu N.C., and Pommier Y. Human mitochondrial topoisomerase I. Proc. Natl. Acad. Sci. USA 98 (2001) 10608-10613
4. Lee M.P., Brown S.D., Chen A., and Hsieh T.S. DNA topoisomerase I is essential in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 90 (1993) 6656-6660
5. Capranico G., Binaschi M., Borgnetto M.E., Zunino F., and Palumbo M. A protein-mediated mechanism for the DNA sequence-specific action of topoisomerase II poisons. Trends Pharmacol. Sci. 18 (1997) 323-329
6. Li T.K., and Liu L.F. Tumor cell death induced by topoisomerase-targeting drugs. Annu. Rev. Pharmacol. Toxicol. 41 (2001) 53-77
7. Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer. 6 (2006) 789-802
8. Staker B.L., Hjerrild K., Feese M.D., Behnke C.A., Burgin Jr. A.B., and Stewart L. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc. Natl. Acad. Sci. USA 99 (2002) 15387-15392
9. Staker B.L., Feese M.D., Cushman M., Pommier Y., Zembower D., Stewart L., and Burgin A.B. Structures of three classes of anticancer agents bound to the human topoisomerase I-DNA covalent complex. J. Med. Chem. 48 (2005) 2336-2345
10. Jaxel C., Capranico G., Kerrigan D., Kohn K.W., and Pommier Y. Effect of local DNA sequence on topoisomerase I cleavage in the presence or absence of camptothecin. J. Biol. Chem. 266 (1991) 20418-20423
11. Capranico G., Kohn K.W., and Pommier Y. Local sequence requirements for DNA cleavage by mammalian topoisomerase II in the presence of doxorubicin. Nucleic Acids Res. 18 (1990) 6611-6619
12. Pourquier P., and Pommier Y. Topoisomerase I-mediated DNA damage. Adv. Cancer Res. 80 (2001) 189-216
13. Lanza A., Tornaletti S., Rodolfo C., Scanavini M.C., and Pedrini A.M. Human DNA topoisomerase I-mediated cleavages stimulated by ultraviolet light-induced DNA damage. J. Biol. Chem. 271 (1996) 6978-6986
14. Levin N.A., Bjornsti M.A., and Fink G.R. A novel mutation in DNA topoisomerase I of yeast causes DNA damage and RAD9-dependent cell cycle arrest. Genetics 133 (1993) 799-814
15. Reid R.J., Benedetti P., and Bjornsti M.A. Yeast as a model organism for studying the actions of DNA topoisomerase-targeted drugs. Biochim. Biophys. Acta 1400 (1998) 289-300
16. Scaldaferro S., Tinelli S., Borgnetto M.E., Azzini A., and Capranico G. Directed evolution to increase camptothecin sensitivity of human DNA topoisomerase I. Chem. Biol. 8 (2001) 871-881
17. Capranico G., Zagotto G., and Palumbo M. Development of DNA topoisomerase-related therapeutics: a short perspective of new challenges. Curr. Med. Chem. Anticancer Agents 4 (2004) 335-345
18. Sordet O., Khan Q.A., Kohn K.W., and Pommier Y. Apoptosis induced by topoisomerase inhibitors. Curr. Med. Chem. Anticancer Agents 3 (2003) 271-290
19. Liu L.F., and Wang J.C. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84 (1987) 7024-7027
20. Drolet M. Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol. Microbiol. 59 (2006) 723-730
21. Wang Z., and Droge P. Differential control of transcription-induced and overall DNA supercoiling by eukaryotic topoisomerases in vitro. EMBO J. 15 (1996) 581-589
22. Choder M. A general topoisomerase I-dependent transcriptional repression in the stationary phase in yeast. Genes Dev. 5 (1991) 2315-2326
23. Brill S.J., DiNardo S., Voelkel-Meiman K., and Sternglanz R. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 326 (1987) 414-416
24. Brill S.J., and Sternglanz R. Transcription-dependent DNA supercoiling in yeast DNA topoisomerase mutants. Cell 54 (1988) 403-411
25. Osborne B.I., and Guarente L. Transcription by RNA polymerase II induces changes of DNA topology in yeast. Genes Dev. 2 (1988) 766-772
26. Gartenberg M.R., and Wang J.C. Positive supercoiling of DNA greatly diminishes mRNA synthesis in yeast. Proc. Natl. Acad. Sci. USA 89 (1992) 11461-11465
27. Shaiu W.L., and Hsieh T.S. Targeting to transcriptionally active loci by the hydrophilic N-terminal domain of Drosophila DNA topoisomerase I. Mol. Cell. Biol. 18 (1998) 4358-4367
28. Christensen M.O., Barthelmes H.U., Feineis S., Knudsen B.R., Andersen A.H., Boege F., and Mielke C. Changes in mobility account for camptothecin-induced subnuclear relocation of topoisomerase I. J. Biol. Chem. 277 (2002) 15661-15665
29. Kretzschmar M., Meisterernst M., and Roeder R.G. Identification of human DNA topoisomerase I as a cofactor for activator-dependent transcription by RNA polymerase II. Proc. Natl. Acad. Sci. USA 90 (1993) 11508-11512
30. Merino A., Madden K.R., Lane W.S., Champoux J.J., and Reinberg D. DNA topoisomerase I is involved in both repression and activation of transcription. Nature 365 (1993) 227-232
31. Shykind B.M., Kim J., Stewart L., Champoux J.J., and Sharp P.A. Topoisomerase I enhances TFIID-TFIIA complex assembly during activation of transcription. Genes Dev. 11 (1997) 397-407
32. Mizutani M., Ura K., and Hirose S. DNA superhelicity affects the formation of transcription preinitiation complex on eukaryotic genes differently. Nucleic Acids Res. 19 (1991) 2907-2911
33. Mizutani M., Ohta T., Watanabe H., Handa H., and Hirose S. Negative supercoiling of DNA facilitates an interaction between transcription factor IID and the fibroin gene promoter. Proc. Natl. Acad. Sci. USA 88 (1991) 718-722
34. Liu J., He L., Collins I., Ge H., Libutti D., Li J., Egly J.M., and Levens D. The FBP interacting repressor targets TFIIH to inhibit activated transcription. Mol. Cell 5 (2000) 331-341
35. Collins I., Weber A., and Levens D. Transcriptional consequences of topoisomerase inhibition. Mol. Cell. Biol. 21 (2001) 8437-8451
36. Liu J., Akoulitchev S., Weber A., Ge H., Chuikov S., Libutti D., Wang X.W., Conaway J.W., Harris C.C., Conaway R.C., Reinberg D., and Levens D. Defective interplay of activators and repressors with TFIH in xeroderma pigmentosum. Cell 104 (2001) 353-363
37. Weber A., Liu J., Collins I., and Levens D. TFIIH operates through an expanded proximal promoter to fine-tune c-myc expression. Mol. Cell. Biol. 25 (2005) 147-161
38. Carty S.M., and Greenleaf A.L. Hyperphosphorylated C-terminal repeat domain-associating proteins in the nuclear proteome link transcription to DNA/chromatin modification and RNA processing. Mol. Cell. Proteomics 1 (2002) 598-610
39. Wu R.S., Kumar A., and Warner J.R. Ribosome formation is blocked by camptothecin, a reversible inhibitor of RNA synthesis. Proc. Natl. Acad. Sci. USA 68 (1971) 3009-3014
40. Bendixen C., Thomsen B., Alsner J., and Westergaard O. Camptothecin-stabilized topoisomerase I-DNA adducts cause premature termination of transcription. Biochemistry 29 (1990) 5613-5619
41. Wu J., and Liu L.F. Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res. 25 (1997) 4181-4186
42. Khobta A., Ferri F., Lotito L., Montecucco A., Rossi R., and Capranico G. Early effects of topoisomerase I inhibition on RNA polymerase II along transcribed genes in human cells. J. Mol. Biol. 357 (2006) 127-138
43. Ljungman M., and Hanawalt P.C. The anti-cancer drug camptothecin inhibits elongation but stimulates initiation of RNA polymerase II transcription. Carcinogenesis 17 (1996) 31-35
44. Casse C., Giannoni F., Nguyen V.T., Dubois M.F., and Bensaude O. The transcriptional inhibitors, actinomycin D and alpha-amanitin, activate the HIV-1 promoter and favor phosphorylation of the RNA polymerase II C-terminal domain. J. Biol. Chem. 274 (1999) 16097-16106
45. Pommier Y. Diversity of DNA topoisomerases I and inhibitors. Biochimie. 80 (1998) 255-270
46. Zhang H., Wang J.C., and Liu L.F. Involvement of DNA topoisomerase I in transcription of human ribosomal RNA genes. Proc. Natl. Acad. Sci. USA 85 (1988) 1060-1064
47. Sims III R.J., Belotserkovskaya R., and Reinberg D. Elongation by RNA polymerase II: the short and long of it. Genes Dev. 18 (2004) 2437-2468
48. Lee M.S., and Garrard W.T. Positive DNA supercoiling generates a chromatin conformation characteristic of highly active genes. Proc. Natl. Acad. Sci. USA 88 (1991) 9675-9679
49. Felsenfeld G., Clark D., and Studitsky V. Transcription through nucleosomes. Biophys. Chem. 86 (2000) 231-237
50. Mondal N., and Parvin J.D. DNA topoisomerase IIalpha is required for RNA polymerase II transcription on chromatin templates. Nature 413 (2001) 435-438
51. Mondal N., Zhang Y., Jonsson Z., Dhar S.K., Kannapiran M., and Parvin J.D. Elongation by RNA polymerase II on chromatin templates requires topoisomerase activity. Nucleic Acids Res. 31 (2003) 5016-5024
52. Salceda J., Fernandez X., and Roca J. Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J. 25 (2006) 2575-2583
53. Duann P., Sun M., Lin C.T., Zhang H., and Liu L.F. Plasmid linking number change induced by topoisomerase I-mediated DNA damage. Nucleic Acids Res. 27 (1999) 2905-2911
54. Uemura T., and Yanagida M. Isolation of type I and II DNA topoisomerase mutants from fission yeast: single and double mutants show different phenotypes in cell growth and chromatin organization. EMBO J. 3 (1984) 1737-1744
55. Soret J., Gabut M., Dupon C., Kohlhagen G., Stevenin J., Pommier Y., and Tazi J. Altered serine/arginine-rich protein phosphorylation and exonic enhancer-dependent splicing in mammalian cells lacking topoisomerase I. Cancer Res. 63 (2003) 8203-8211
56. Tazi J., Rossi F., Labourier E., Gallouzi I., Brunel C., and Antoine E. DNA topoisomerase I: customs officer at the border between DNA and RNA worlds?. J. Mol. Med. 75 (1997) 786-800
57. Andersen F.F., Tange T.O., Sinnathamby T., Olesen J.R., Andersen K.E., Westergaard O., Kjems J., and Knudsen B.R. The RNA splicing factor ASF/SF2 inhibits human topoisomerase I mediated DNA relaxation. J. Mol. Biol. 322 (2002) 677-686
58. Straub T., Grue P., Uhse A., Lisby M., Knudsen B.R., Tange T.O., Westergaard O., and Boege F. The RNA-splicing factor PSF/p54 controls DNA-topoisomerase I activity by a direct interaction. J. Biol. Chem. 273 (1998) 26261-26264
59. Czubaty A., Girstun A., Kowalska-Loth B., Trzcinska A.M., Purta E., Winczura A., Grajkowski W., and Staron K. Proteomic analysis of complexes formed by human topoisomerase I. Biochim. Biophys. Acta 1749 (2005) 133-141
60. Solier S., Lansiaux A., Logette E., Wu J., Soret J., Tazi J., Bailly C., Desoche L., Solary E., and Corcos L. Topoisomerase I and II inhibitors control caspase-2 pre-messenger RNA splicing in human cells. Mol. Cancer Res. 2 (2004) 53-61
61. Soret J., Bakkour N., Maire S., Durand S., Zekri L., Gabut M., Fic W., Divita G., Rivalle C., Dauzonne D., Nguyen C.H., Jeanteur P., and Tazi J. Selective modification of alternative splicing by indole derivatives that target serine-arginine-rich protein splicing factors. Proc. Natl. Acad. Sci. USA 102 (2005) 8764-8769
62. Gatto B., Capranico G., and Palumbo M. Drugs acting on DNA topoisomerases: recent advances and future perspectives. Curr. Pharm. Des. 5 (1999) 195-215
63. Mialon A., Sankinen M., Soderstrom H., Junttila T.T., Holmstrom T., Koivusalo R., Papageorgiou A.C., Johnson R.S., Hietanen S., Elenius K., and Westermarck J. DNA topoisomerase I is a cofactor for c-Jun in the regulation of epidermal growth factor receptor expression and cancer cell proliferation. Mol. Cell. Biol. 25 (2005) 5040-5051
64. Rapisarda A., Uranchimeg B., Sordet O., Pommier Y., Shoemaker R.H., and Melillo G. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res. 64 (2004) 1475-1482
65. Marshall J. Clinical implications of the mechanism of epidermal growth factor receptor inhibitors. Cancer 107 (2006) 1207-1218
66. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3 (2003) 721-732
67. Melillo G. Inhibiting hypoxia-inducible factor 1 for cancer therapy. Mol. Cancer Res. 4 (2006) 601-605
68. Ponzielli R., Katz S., Barsyte-Lovejoy D., and Penn L.Z. Cancer therapeutics: targeting the dark side of Myc, Eur. J. Cancer 41 (2005) 2485-2501
69. Tazi J., Durand S., and Jeanteur P. The spliceosome: a novel multi-faceted target for therapy. Trends Biochem. Sci. 30 (2005) 469-478
70. Pilch B., Allemand E., Facompre M., Bailly C., Riou J.F., Soret J., and Tazi J. Specific inhibition of serine- and arginine-rich splicing factors phosphorylation, spliceosome assembly, and splicing by the antitumor drug NB-506. Cancer Res. 61 (2001) 6876-6884
71. Katzenberger R.J., Marengo M.S., and Wassarman D.A. ATM and ATR pathways signal alternative splicing of Drosophila TAF1 pre-mRNA in response to DNA damage. Mol. Cell. Biol. 26 (2006) 9256-9267
72. Labourier E., Rossi F., Gallouzi I.E., Allemand E., Divita G., and Tazi J. Interaction between the N-terminal domain of human DNA topoisomerase I and the arginine-serine domain of its substrate determines phosphorylation of SF2/ASF splicing factor. Nucleic Acids Res. 26 (1998) 2955-2962
73. Kowalska-Loth B., Girstun A., Trzcinska A.M., Piekielko-Witkowska A., and Staron K. SF2/ASF protein binds to the cap region of human topoisomerase I through two RRM domains. Biochem. Biophys. Res. Commun. 331 (2005) 398-403