Advanced search
Publication Cover
Expert Opinion on Therapeutic Targets Volume 12, 2008 - Issue 10
Submit an article Journal homepage
303
Views
53
CrossRef citations to date
0
Altmetric
Review

Targeting topoisomerase I: molecular mechanisms and cellular determinants of response to topoisomerase I inhibitors

Giovanni Luca Beretta Fondazione IRCCS Istituto Nazionale dei Tumori, Via Venezian 1, 20133 Milan, Italy +39 02 23902267; +39 02 23902692; [email protected]
,
Paola Perego Fondazione IRCCS Istituto Nazionale dei Tumori, Via Venezian 1, 20133 Milan, Italy +39 02 23902267; +39 02 23902692; [email protected]
&
Franco Zunino Fondazione IRCCS Istituto Nazionale dei Tumori, Via Venezian 1, 20133 Milan, Italy +39 02 23902267; +39 02 23902692; [email protected]
Pages 1243-1256 | Published online: 09 Sep 2008

Bibliography

  • Wang J. Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 2002;3:430-40
  • Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006;6:789-802
  • Pommier Y, Cherfils J. Interfacial inhibition of macromolecular interactions: nature's paradigm for drug discovery. Trends Pharmacol Sci 2005;26:138-45
  • Staker BL, Feese MD, Cushman M, et al. Structures of three classes of anticancer agents bound to the human topoisomerase I-DNA covalent complex. J Med Chem 2005;48:2336-45
  • Staker BL, Hjerrild K, Feese MD, et al. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc Natl Acad Sci USA 2002;99:15387-92
  • Pratesi G, Beretta GL, Zunino F. Gimatecan, a novel camptothecin with a promising preclinical profile. Anticancer Drugs 2004;15:545-52
  • Dallavalle S, Rocchetta DG, Musso L, et al. Synthesis and cytotoxic activity of new 9-substituted camptothecins. Bioorg Med Chem Lett 2008;18:2781-7
  • Zunino F, Dallavalle S, Laccabue D, et al. Current status and perspectives in the development of camptothecins. Curr Pharm Des 2002;8:2505-20
  • Huang M, Gao H, Chen Y, et al. Chimmitecan, a novel 9-substituted camptothecin, with improved anticancer pharmacologic profiles in vitro and in vivo. Clin Cancer Res 2007;13:1298-307
  • Wadkins RM, Bears D, Manikumar G. Hydrophilic camptothecin analogs that form extremely stable cleavable complexes with DNA and topoisomerase I. Cancer Res 2004;64:6679-83
  • De Cesare M, Beretta GL, Tinelli S, et al. Preclinical efficacy of ST1976, a novel camptothecin analog of the 7-oxyiminomethyl series. Biochem Pharmacol 2007;73:656-64
  • Dallavalle S, Giannini G, Alloatti D, et al. Synthesis and cytotoxic activity of polyamine analogues of camptothecin. J Med Chem 2006;49:5177-86
  • Pisano C, Zuco V, De Cesare M, et al. Intracellular accumulation and DNA damage persistence as determinants of human squamous cell carcinoma hypersensitivity to the novel camptothecin ST1968. Eur J Cancer 2008;44:1332-40
  • Pisano C, De Cesare M, Beretta GL, et al. Preclinical profile of antitumor activity of a novel hydrophilic camptothecin, ST1968. Mol Cancer Ther 2008;7:2051-9
  • Beretta GL, Zunino F. Relevance of extracellular and intracellular interactions of camptothecins as determinants of antitumor activity. Biochem Pharmacol 2007;74:1437-44
  • Lansiaux A, Léonce S, Kraus-Berthier L, et al. Novel stable camptothecin derivatives replacing the E-ring lactone by a ketone function are potent inhibitors of topoisomerase I and promising antitumor drugs. Mol Pharmacol 2007;72:311-9
  • Takagi K, Dexheimer TS, Redon C, et al. Novel E-ring camptothecin keto analogues (S38809 and S39625) are stable, potent, and selective topoisomerase I inhibitors without being substrates of drug efflux transporters. Mol Cancer Ther 2007;6:3229-38
  • Laco GS, Collins JR, Luke BT, et al. Human topoisomerase I inhibition: docking camptothecin and derivatives into a structure-based active site model. Biochemistry 2002;41:1428-35
  • Beretta GL, Petrangolini G, De Cesare M, et al. Biological properties of IDN5174, a new synthetic camptothecin with the open lactone ring, Cancer Res 2006;66:10976-82
  • Zhu S, Ruchelman AL, Zhou N, et al. 6-Substituted 6H-dibenzo[c,h][2,6]naphthyridin-5-ones: reversed lactam analogues of ARC-111 with potent topoisomerase I-targeting activity and cytotoxicity. Bioorg Med Chem 2006;14:3131-43
  • Dallavalle S, Gattinoni S, Mazzini S, et al. Synthesis and cytotoxic activity of a new series of topoisomerase I inhibitors. Bioorg Med Chem Lett 2008;18:1484-9
  • Zunino F, Pratesi G. Camptothecins in clinical development. Expert Opin Investig Drugs 2004;13:269-84
  • Yurkovetskiy AV, Hiller A, Syed S, et al. Synthesis of a macromolecular camptothecin conjugate with dual phase drug release. Mol Pharm 2004;1:375-82
  • Schluep T, Hwang J, Cheng J, et al. Preclinical efficacy of the camptothecin-polymer conjugate IT-101 in multiple cancer models. Clin Cancer Res 2006;12:1606-14
  • Furuta T, Takemura H, Liao ZY, et al. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA-double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 2003;278:20303-12
  • Sakasai R, Shinohe K, Ichijima Y, et al. Differential involvement of phosphatidylinositol 3-kinase-related protein kinases in hyperphosphorylation of replication protein A2 in response to replication-mediated DNA double-strand breaks. Genes Cells 2006;11:237-46
  • Tanaka T, Kurose A, Huang X, et al. ATM activation and histone H2AX phosphorylation as indicators of DNA damage by DNA topoisomerase I inhibitor topotecan and during apoptosis. Cell Prolif 2006;39:49-60
  • Pommier Y, Barcelo JM, Rao VA, et al. Repair of topoisomerase I-mediated DNA damage. Prog Nucleic Acid Res Mol Biol 2006;81:179-229
  • Rao VA, Fan AM, Meng L, et al. Phosphorylation of BLM, dissociation for topoisomerase III and colocalization with -H2AX after topoisomerase I-induced replication damage. Mol Cell Biol 2005;25:8925-37
  • Bartek J, Bartkova J, Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 2007;26:7773-9
  • Gupta M, Fan S, Zhan Q, et al. Inactivation of p53 increases the cytotoxicity of camptothecin in human colon HCT116 and breast MCF-7 cancer cells. Clin Cancer Res 1997;3:1653-60
  • Han Z, Wei W, Dunaway S, et al. Role of p21 in apoptosis and senescence of human colon cancer cells treated with camptothecin. J Biol Chem 2002;277:17154-60
  • Deptala A, Li X, Bedner E, et al. Differences in induction of p53, p21WAF1 and apoptosis in relation to cell cycle phase of MCF-7 cells treated with camptothecin. Int J Oncol 1999;15:861-71
  • Borgne A, Versteege I, Mahé M, et al. Analysis of cyclin B1 and CDK activity during apoptosis induced by camptothecin treatment. Oncogene 2006;25:7361-72
  • Hsiang YH, Lihou MG, Liu LF. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res 1989;15:5077-82
  • Desai SD, Zhang H, Rodriguez-Bauman A, et al. Transcription-dependent degradation of topoisomerase I-DNA covalent complexes. Mol Cell Biol 2003;23:2341-50
  • Wu J, Liu LF. Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res 1997;25:4181-6
  • Shykind BM, Kim J, Stewart L, et al. Topoisomerase I enhances TFIID–TFIIA complex assembly during activation of transcription. Genes Dev 1997;11:397-407
  • Khobta A, Ferri F, Lotito L, et al. Early effects of topoisomerase I inhibition on RNA polymerase II along transcribed genes in human cells. J Mol Biol 2006;357:127-38
  • Morris EJ, Geller HM. Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. J Cell Biol 1996;134:757-70
  • Daoud SS, Munson PJ, Reinhold W, et al. Impact of p53 knockout and topotecan treatment on gene expression profiles in human colon carcinoma cells: a pharmacogenomic study. Cancer Res 2003;63:2782-93
  • Mialon A, Sankinen M, Söderström H, et al. 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 2005;25:5040-51
  • Rapisarda A, Uranchimeg B, Sordet O, et al. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res 2004;64:1475-82
  • Desai SD, Li Tk, Rodriguez-Bauman A, et al. Ubiquitin/26S proteasome-mediated degradation of topoisomerase I as a resistance mechanism to camptothecin in tumor cells. Cancer Res 2001;61:5926-32
  • Zhang HF, Tomida A, Koshimizu R, et al. Cullin 3 promotes proteasomal degradation of the topoisomerase I-DNA covalent complex. Cancer Res 2004;64:1114-21
  • Ulivi P, Zoli W, Fabbri F, et al. Cellular basis of antiproliferative and antitumor activity of the novel camptothecin derivative, gimatecan, in bladder carcinoma models. Neoplasia 2005;7:152-61
  • Hochster H, Liebes L, Speyer J, et al. A Effect of prolonged topotecan infusion on topoisomerase 1 levels: a phase I and pharmacodynamic study. Clin Cancer Res 1997;3:1245-52
  • Desai SD, Wood LM, Tsai YC, et al. ISG15 as a novel tumor biomarker for drug sensitivity. Mol Cancer Ther 2008;7:1430-9
  • Debéthune L, Kohlhagen G, Grandas A, et al. Processing of nucleopeptides mimicking the topoisomerase I-DNA covalent complex by tyrosyl-DNA phosphodiesterase. Nucleic Acids Res 2002;30:1198-204
  • Connelly JC, Leach DR. Repair of DNA covalently linked to protein. Mol Cell 2004;13:307-16
  • Barthelmes HU, Habermeyer M, Christensen MO, et al. TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerases I and II. J Biol Chem 2004;279:55618-25
  • Vance JR, Wilson TE. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc Natl Acad Sci USA 2002;99:13669-74
  • Katyal S, el-Khamisy SF, Russell HR, et al. TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J 2007;26:4720-31
  • Dexheimer TS, Antony S, Marchand C, et al. Tyrosyl-DNA phosphodiesterase as a target for anticancer therapy. Anticancer Agents Med Chem 2008;8:381-9
  • Jilani A, Ramotar D, Slack C, et al. Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3′-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J Biol Chem 1999;274:24176-86
  • Vidal AE, Boiteux SI, Hickson ID, et al. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J 2001;20:6530-9
  • Whitehouse CJ, Taylor RM, Thistlethwaite A, et al. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 2001;104:107-17
  • Park SY, Leung CH, Cheng YC. ATP Modulates Poly(ADP-ribose) Polymerase-1-Facilitated Topoisomerase I-linked DNA Religation in the Presence of Camptothecin. Mol Pharmacol 2008;73:1829-37
  • D'Amours D, Jackson SP. The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002;3:317-27
  • Bastin-Shanower SA, Fricke WM, Mullen JR, et al. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol Cell Biol 2003;23:3487-96
  • Ciccia A, Constantinou A, West SC. Identification and characterization of the human mus81-eme1 endonuclease. J Biol Chem 2003;278:25172-8
  • Fasullo M, Zeng L, Giallanza P. Enhanced stimulation of chromosomal translocations by radiomimetic DNA damaging agents and camptothecin in Saccharomyces cerevisiae rad9 checkpoint mutants. Mutat Res 2004;547:123-32
  • Otsuki M, Seki M, Kawabe Y, et al. WRN counteracts the NHEJ pathway upon camptothecin exposure. Biochem Biophys Res Commun 2007;355:477-82
  • Hickson ID. RecQ helicases: caretakers of the genome. Nat Rev Cancer 2003;3:169-78
  • Wu L, Hickson ID. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 2003;426:870-4
  • Bjergbaek L, Cobb JA, Tsai-Pflugfelder M, Gasser SM. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J 2005;24:405-17
  • Perego P, Ciusani E, Gatti L, et al. Sensitization to gimatecan-induced apoptosis by tumor necrosis factor-related apoptosis inducing ligand in prostate carcinoma cells. Biochem Pharmacol 2006;71:791-8
  • Hayward RL, Macpherson JS, Cummings J, et al. Bcl-xl down-regulation switches the response to topoisomerase I inhibition from senescence to apoptosis in colorectal cancer cells, enhancing global cytotoxicity. Clin Cancer Res 2003;9:2856-65
  • Rodríguez-Hernández A, Brea-Calvo G, Fernández-Ayala DJ, et al. Nuclear caspase-3 and caspase-7 activation, and poly(ADP-ribose) polymerase cleavage are early events in camptothecin-induced apoptosis. Apoptosis 2006;11:131-9
  • Medema JP, Scaffidi C, Kischkel FC, et al. FLICE is activated by association with the CD95 death-inducing signaling complex DISC. EMBO J 1997;16:2794-804
  • Muzio M, Stockwell BR, Stennicke HR, et al. An induced proximity model for caspase-8 activation. J Biol Chem 1998;273:2926-30
  • Chatterjee D, Schmitz I, Krueger A, et al. Induction of apoptosis in 9-nitrocamptothecin-treated DU145 human prostate carcinoma cells correlates with de novo synthesis of CD95 and CD95 ligand and down-regulation of c-FLIP(short). Cancer Res 2001;61:7148-54
  • Meza-Lamas E, Bollain-y-Goytia JJ, Ramírez-Sandoval R, et al. Camptothecin induces the transit of FasL trimers to the cell surface in apoptotic HEp-2 cells. Cell Mol Biol Lett 2006;11:299-311
  • Chauvier D, Morjani H, Manfait M. Ceramide involvement in homocamptothecin- and camptothecin-induced cytotoxicity and apoptosis in colon HT29 cells. Int J Oncol 2002;20:855-63
  • Akao Y, Kusakabe S, Banno Y, et al. Ceramide accumulation is independent of camptothecin-induced apoptosis in prostate cancer LNCaP cells. Biochem Biophys Res Commun 2002;294:363-70
  • Verheij M, Bose R, Lin XH, et al. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 1996;380:75-9
  • Kaufmann SH. Cell death induced by topoisomerase-targeted drugs: more questions than answers. Biochim Biophys Acta 1998;1400:195-211
  • Shao RG, Cao CX, Shimizu T, et al. Abrogation of an S-phase checkpoint and potentiation of camptothecin cytotoxicity by 7-hydroxystaurosporine (UCN-01) in human cancer cell lines, possibly influenced by p53. Cancer Res 1997;57:4029-35
  • Pommier Y, Weinstein JN, Aladjem MI, et al. Chk2 molecular interaction map and rationale for Chk2 inhibitors. Clin Cancer Res 2006;12:2657-61
  • Flatten K, Dai NT, Vroman BT, et al. The role of checkpoint kinase 1 in sensitivity to topoisomerase I poisons. J Biol Chem 2005;280:14349-55
  • Hickson I, Zhao Y, Richardson CJ, et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004;64:9152-9
  • Zhao Y, Thomas HD, Batey MA, et al. Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer Res 2006;66:5354-62
  • Bowman KJ, Newell DR, Calvert AH, et al. Differential effects of the poly (ADP-ribose) polymerase (PARP) inhibitor NU1025 on topoisomerase I and II inhibitor cytotoxicity in L1210 cells in vitro. Br J Cancer 2001;84:106-12
  • Cimmino G, Pepe S, Laus G, et al. Poly(ADPR)polymerase-1 signalling of the DNA damage induced by DNA topoisomerase I poison in D54(p53wt) and U251(p53mut) glioblastoma cell lines. Pharmacol Res 2007;55:49-56
  • Thomas HD, Calabrese CR, Batey MA, et al. Preclinical selection of a novel poly(ADP-ribose) polymerase inhibitor for clinical trial. Mol Cancer Ther 2007;6:945-56
  • Smith LM, Willmore E, Austin CA, et al. The novel poly(ADP-Ribose) polymerase inhibitor, AG14361, sensitizes cells to topoisomerase I poisons by increasing the persistence of DNA strand breaks. Clin Cancer Res 2005;11:8449-57
  • Jagtap P, Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nature Rev Drug Discov 2005;4:421-40
  • Liao Z, Thibaut L, Jobson A, et al. Inhibition of human tyrosyl-DNA phosphodiesterase by aminoglycoside antibiotics and ribosome inhibitors. Mol Pharmacol 2006;70(1):366-72
  • Beretta GL, Gatti L, Benedetti V, et al. Small molecules targeting p53 to improve antitumor therapy. Mini Rev Med Chem 2008;8:856-68
  • Wang H, Wang S, Nan L, et al. Antisense anti-MDM2 mixed-backbone oligonucleotides enhance therapeutic efficacy of topoisomerase I inhibitor irinotecan in nude mice bearing human cancer xenografts: in vivo activity and mechanisms. Int J Oncol 2002;20:745-52
  • Becker K, Marchenko ND, Maurice M, et al. Hyperubiquitylation of wild-type p53 contributes to cytoplasmic sequestration in neuroblastoma. Cell Death Differ 2007;14:1350
  • Huang TT, Wuerzberger-Davis SM, Seufzer BJ, et al. NFκB activation by camptothecin. A linkage between nuclear DNA damage and cytoplasmic signaling events. J Biol Chem 2000;275:9501-9
  • Catley L, Tai YT, Shringarpure R, et al. Proteasomal degradation of topoisomerase I is preceded by c-Jun NH2-terminal kinase activation, Fas up-regulation, and poly(ADP-ribose) polymerase cleavage in SN38-mediated cytotoxicity against multiple myeloma. Cancer Res 2004;64:8746-53
  • De Cesare M, Perego P, Righetti SC, et al. Enhanced antitumour efficacy of gimatecan in combination with Bcl-2 antisense oligonucleotide in human melanoma xenografts. Eur J Cancer 2005;41:1213-22
  • Braun AH, Stark K, Dirsch O, et al. The epidermal growth factor receptor tyrosine kinase inhibitor gefitinib sensitizes colon cancer cells to irinotecan. Anticancer Drugs 2005;16:1099-108
  • Yang CH, Huang CJ, Yang CS, et al. Gefitinib reverses chemotherapy resistance in gefitinib-insensitive multidrug resistant cancer cells expressing ATP-binding cassette family protein. Cancer Res 2005;65:6943-9
  • Petrangolini G, Supino R, Pratesi G, et al. Effect of a novel vacuolar-H+-ATPase inhibitor on cell and tumor response to camptothecins. J Pharmacol Exp Ther 2006;318:939-46
  • Teicher BA. Next generation topoisomerase I inhibitors: rationale and biomarker strategies. Biochem Pharmacol 2008;75:1262-71
  • Petrangolini G, Pratesi G, De Cesare M, et al. Antiangiogenic effects of the novel camptothecin ST1481 (Gimatecan) in human tumor xenografts. Mol Cancer Res 2003;1:863-70
  • Samorì C, Guerrini A, Varchi G, et al. Thiocamptothecin. J Med Chem 2008;51:3040-4

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.