The natural inhibitor of DNA topoisomerase I, camptothecin, modulates HIF-1α activity by changing miR expression patterns in human cancer cells

Molecular Cancer Therapeutics

Volumn 13, Issue 1, 2014, Pages 239-248

  Bertozzi, Davide ^a   Marinello, Jessica ^a   Manzo, Stefano G ^a   Fornari, Francesca ^b   Gramantieri, Laura ^b   Capranico, Giovanni ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MICRORNA 155;

3' UNTRANSLATED REGION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL HYPOXIA; COMPETITIVE INHIBITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

CAMPTOTHECIN; CELL HYPOXIA; DNA TOPOISOMERASES, TYPE I; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICRORNAS; NEOPLASMS; RNA, MESSENGER; TOPOISOMERASE I INHIBITORS;

EID: 84892599954     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0729     Document Type: Article

References (44)

1. Jiang BH, Rue E, Wang GL, Roe R, Semenza GL. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 1996;271:17771-8.
2. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
3. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32.
4. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, et al. Overexpression of hypoxia-inducible factor 1 alpha in common human cancers and their metastases. Cancer Res 1999;59:5830-5.
5. Onnis B, Rapisarda A, Melillo G. Development of HIF-1 inhibitors for cancer therapy. J Cell Mol Med 2009;13:2780-6.
6. Rapisarda A, Uranchimeg B, Scudiero DA, Selby M, Sausville EA, Shoemaker RH, et al. Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res 2002;62:4316-24.
7. Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 2001;70:369-413.
8. Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006;6:789-802.
9. Capranico G, Marinello J, Baranello L. Dissecting the transcriptional functions of human DNA topoisomerase I by selective inhibitors: implications for physiological and therapeutic modulation of enzyme activity. Biochim Biophys Acta 2010;1806:240-50.
10. Pommier Y. Drugging topoisomerases: lessons and challenges. ACS Chem Biol 2012;8:82-95.
11. Pommier Y, Barcelo JM, Rao VA, Sordet O, Jobson AG, Thibaut L, et al. Repair of topoisomerase I-mediated DNA damage. Prog Nucleic Acid Res Mol Biol 2006;81:179-229.
12. Staker BL, Hjerrild K, Feese MD, Behnke CA, Burgin AB Jr., Stewart L. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc Natl Acad Sci U S A 2002;99:15387-92.
13. Ricci A, Marinello J, Bortolus M, Sanchez A, Grandas A, Pedroso E, et al. Electron paramagnetic resonance (EPR) study of spin-labeled camptothecin derivatives: a different look of the ternary complex. J Med Chem 2011;54:1003-9.
14. Khobta A, Ferri F, Lotito L, Montecucco A, Rossi R, Capranico G. Early effects of topoisomerase I inhibition on RNA polymerase II along transcribed genes in human cells. J Mol Biol 2006;357:127-38.
15. Lavelle C. Transcription elongation through a chromatin template. Biochimie 2007;89:516-27.
16. Kretzschmar M, Meisterernst M, Roeder RG. Identification of human DNA topoisomerase I as a cofactor for activator-dependent transcription by RNA polymerase II. Proc Natl Acad Sci U S A 1993; 90:11508-12.
17. Tuduri S, Crabbe L, Conti C, Tourriere H, Holtgreve-Grez H, Jauch A, et al. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat Cell Biol 2009;11:1315-24.
18. Wu HY, Shyy SH, Wang JC, Liu LF. Transcription generates positively and negatively supercoiled domains in the template. Cell 1988;53:433-40.
19. Wang JC. Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 2002;3:430-40.
20. Guerin E, Raffelsberger W, Pencreach E, Maier A, Neuville A, Schneider A, et al. In vivo topoisomerase I inhibition attenuates the expression of hypoxia-inducible factor 1 alpha target genes and decreases tumor angiogenesis. Mol Med 2011;18:83-94.
21. Rapisarda A, Uranchimeg B, Sordet O, Pommier Y, Shoemaker RH, Melillo G. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res 2004; 64:1475-82.
22. Rapisarda A, Zalek J, Hollingshead M, Braunschweig T, Uranchimeg B, Bonomi CA, et al. Schedule-dependent inhibition of hypoxia-inducible factor-1alpha protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts. Cancer Res 2004;64:6845-8.
23. Baranello L, Bertozzi D, Fogli MV, Pommier Y, Capranico G. DNA topoisomerase I inhibition by camptothecin induces escape of RNA polymerase II from promoter-proximal pause site, antisense transcription and histone acetylation at the human HIF-1alpha gene locus. Nucleic Acids Res 2009;38:159-71.
24. Bertozzi D, Iurlaro R, Sordet O, Marinello J, Zaffaroni N, Capranico G. Characterization of novel antisense HIF-1alpha transcripts in human cancers. Cell Cycle 2011;10:3189-97.
25. Thrash-Bingham CA, Tartof KD. aHIF: a natural antisense transcript overexpressed in human renal cancer and during hypoxia. J Natl Cancer Inst 1999;91:143-51.
26. Sordet O, Larochelle S, Nicolas E, Stevens EV, Zhang C, Shokat KM, et al. Hyperphosphorylation of RNA polymerase II in response to topoisomerase I cleavage complexes and its association with transcription- and BRCA1-dependent degradation of topoisomerase I. J Mol Biol 2008;381:540-9.
27. Amente S, Gargano B, Napolitano G, Lania L, Majello B. Camptothecin releases P-TEFb from the inactive 7SK snRNP complex. Cell Cycle 2009;8:1249-55.
28. Sordet O, Nakamura AJ, Redon CE, Pommier Y. DNA double-strand breaks and ATMactivation by transcription-blocking DNA lesions. Cell Cycle 2009;9:274-8.
29. Sordet O, Redon CE, Guirouilh-Barbat J, Smith S, Solier S, Douarre C, et al. Ataxia telangiectasia mutated activation by transcription- and topoisomerase I-induced DNA double-strand breaks. EMBO Rep 2009;10:887-93.
30. Marinello J, Chillemi G, Bueno S, Manzo SG, Capranico G. Antisense transcripts enhanced by camptothecin at divergent CpG-island promoters associated with bursts of topoisomerase I-DNA cleavage complex and R-loop formation. Nucleic Acids Res. Epub 2013 Sep 2.
31. Ferracin M, Zagatti B, Rizzotto L, Cavazzini F, Veronese A, Ciccone M, et al. MicroRNAs involvement in fludarabine refractory chronic lymphocytic leukemia. Mol Cancer 2010;9:123.
32. Solier S, Barb J, Zeeberg BR, Varma S, Ryan MC, Kohn KW, et al. Genome-wide analysis of novel splice variants induced by topoisomerase I poisoning shows preferential occurrence in genes encoding splicing factors. Cancer Res 2010;70:8055-65.
33. Aguilera A, Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 2008;9:204-17.
34. Huang HS, Allen JA, Mabb AM, King IF, Miriyala J, Taylor-Blake B, et al. Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature 2011;481:185-9.
35. Powell WT, Coulson RL, Gonzales ML, Crary FK, Wong SS, Adams S, et al. R-loop formation at Snord116 mediates topotecan inhibition of Ube3a-antisense and allele-specific chromatin decondensation. Proc Natl Acad Sci U S A 2013;110:13938-43.
36. Yates LA, Norbury CJ, Gilbert RJ. The long and short of microRNA. Cell 2013;153:516-9.
37. Lotito L, Russo A, Bueno S, Chillemi G, Fogli MV, Capranico G. A specific transcriptional response of yeast cells to camptothecin dependent on the Swi4 and Mbp1 factors. Eur J Pharmacol 2009; 603:29-36.
38. Lotito L, Russo A, Chillemi G, Bueno S, Cavalieri D, Capranico G. Global transcription regulation by DNA topoisomerase I in exponentially growing saccharomyces cerevisiae cells: activation of telomere-proximal genes by TOP1 deletion. J Mol Biol 2008;377: 311-22.
39. Galban S, Kuwano Y, Pullmann R Jr., Martindale JL, Kim HH, Lal A, et al. RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol Cell Biol 2008;28:93-107.
40. Solier S, Ryan MC, Martin SE, Varma S, Kohn KW, Liu H, et al. Transcription poisoning by topoisomerase I is controlled by gene length, splice sites, and miR-142-3p. Cancer Res 2013;73:4830-9.
41. Bitarte N, Bandres E, Boni V, Zarate R, Rodriguez J, Gonzalez-Huarriz M, et al. MicroRNA-451 is involved in the self-renewal, tumorigenicity, and chemoresistance of colorectal cancer stem cells. Stem Cells 2011;29:1661-71.
42. Gmeiner WH, Reinhold WC, Pommier Y. Genome-wide mRNA and microRNA profiling of the NCI 60 cell-line screen and comparison of FdUMP[10] with fluorouracil, floxuridine, and topoisomerase 1 poisons. Mol Cancer Ther 2010;9:3105-14.
43. Tong JL, Zhang CP, Nie F, Xu XT, Zhu MM, Xiao SD, et al. MicroRNA 506 regulates expression of PPAR alpha in hydroxycamptothecin-resistant human colon cancer cells. FEBS Lett 2011;585:3560-8.
44. Zeng CW, Zhang XJ, Lin KY, Ye H, Feng SY, Zhang H, et al. Camptothecin induces apoptosis in cancer cells via microRNA- 125b-mediated mitochondrial pathways. Mol Pharmacol 2012;81: 578-86.