Characterization of DNA topoisomerase i in three SN-38 resistant human colon cancer cell lines reveals a new pair of resistanceassociated mutations

Journal of Experimental and Clinical Cancer Research

Volumn 35, Issue 1, 2016, Pages

  Jensen, Niels Frank ^a   Agama, Keli ^b   Roy, Amit ^c,d   Smith, David Hersi ^a,e   Pfister, Thomas D ^f   Rømer, Maria Unni ^a,g   Zhang, Hong Liang ^b   Doroshow, James H ^b,f   Knudsen, Birgitta R ^c   Stenvang, Jan ^a   Brünner, Nils ^a   Pommier, Yves ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NATIONAL CANCER INSTITUTE   (United States)

^c AARHUS UNIVERSITY   (Denmark)

^d National Institute of Pharmaceutical Education and Research (NIPER)   (India)

^e AGILENT TECHNOLOGIES   (United States)

^f FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^g FREDERIKSBERG HOSPITAL   (Denmark)

Author keywords

Colon cancer; DNA topoisomerase I; Irinotecan; Mutation; Resistance; SN 38; TOP1

Indexed keywords

ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE; EPIRUBICIN; ETOPOSIDE; FIRTECAN; ISOQUINOLINE DERIVATIVE; MESSENGER RNA; NSC 725776; NSC 743400; UNCLASSIFIED DRUG; 1,3 BENZODIOXOLE DERIVATIVE; 7-NITRO-1H-INDOLE-2-CARBOXYLIC ACID (4-(1-(GUANIDINOHYDRAZONE)ETHYL)PHENYL)AMIDE; CAMPTOTHECIN; GUANIDINE DERIVATIVE; HYDRAZONE DERIVATIVE; IRINOTECAN; TOP1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL LINE; CANCER RESISTANCE; CHROMOSOME 20; CHROMOSOME ABERRATION; COLON CANCER; CONTROLLED STUDY; CROSS RESISTANCE; DRUG BINDING SITE; ENZYME ACTIVITY; GENE DOSAGE; GENE EXPRESSION; GENE LOSS; GENE MUTATION; GENE SEQUENCE; GENETIC GAIN; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TOP1 GENE; ANALOGS AND DERIVATIVES; BINDING SITE; CHROMOSOME DELETION; COLON TUMOR; DRUG RESISTANCE; GENETICS; HCT 116 CELL LINE; HT-29 CELL LINE; METABOLISM; MUTATION; TUMOR CELL LINE;

BENZODIOXOLES; BINDING SITES; CAMPTOTHECIN; CELL LINE, TUMOR; CHROMOSOME DELETION; COLONIC NEOPLASMS; DNA TOPOISOMERASES, TYPE I; DRUG RESISTANCE, NEOPLASM; EPIRUBICIN; ETOPOSIDE; GENE DOSAGE; GUANIDINES; HCT116 CELLS; HT29 CELLS; HUMANS; HYDRAZONES; ISOQUINOLINES; MUTATION;

EID: 85008600545     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/s13046-016-0335-x     Document Type: Article

References (69)

1. Glimelius B, Cavalli-Bjorkman N. Metastatic colorectal cancer: current treatment and future options for improved survival. Medical approach-present status. Scand J Gastroenterol. 2012;47(3):296-314.
2. Van Cutsem E, Nordlinger B, Cervantes A. Advanced colorectal cancer: ESMO Clinical Practice Guidelines for treatment. Ann Oncol. 2010;21 Suppl 5:v93-7.
3. Tournigand C, Andre T, Achille E, Lledo G, Flesh M, Mery-Mignard D, Quinaux E, Couteau C, Buyse M, Ganem G, Landi B, Colin P, et al. FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study. J Clin Oncol. 2004;22(2):229-37.
4. Colucci G, Gebbia V, Paoletti G, Giuliani F, Caruso M, Gebbia N, Carteni G, Agostara B, Pezzella G, Manzione L, Borsellino N, Misino A, et al. Phase III randomized trial of FOLFIRI versus FOLFOX4 in the treatment of advanced colorectal cancer: a multicenter study of the Gruppo Oncologico Dell'Italia Meridionale. J Clin Oncol. 2005;23(22):4866-75.
5. O'Connell JB, Maggard MA, Ko CY. Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. J Natl Cancer Inst. 2004;96(19):1420-5.
6. Jensen NF, Smith DH, Nygard SB, Romer MU, Nielsen KV, Brunner N. Predictive biomarkers with potential of converting conventional chemotherapy to targeted therapy in patients with metastatic colorectal cancer. Scand J Gastroenterol. 2012;47(3):340-55.
7. Koopman M, Venderbosch S, Nagtegaal ID, Van Krieken JH, Punt CJ. A review on the use of molecular markers of cytotoxic therapy for colorectal cancer, what have we learned? Eur J Cancer. 2009;45(11):1935-49.
8. Pommier Y. Drugging topoisomerases: lessons and challenges. ACS Chem Biol. 2013;8(1):82-95.
9. Pizzolato JF, Saltz LB. The camptothecins. Lancet. 2003;361(9376):2235-42.
10. Hsiang YH, Liu LF. Identification of mammalian DNA topoisomerase I as an intracellular target of the anticancer drug camptothecin. Cancer Res. 1988;48(7):1722-6.
11. Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem. 2001;70:369-413.
12. Nitiss JL. Targeting DNA, topoisomerase II in cancer chemotherapy. Nat Rev Cancer. 2009;9(5):338-50.
13. Pommier Y. DNA Topoisomerases and Cancer. New York, Dordrecht, Heidelberg, London: Springer & Humana Press; 2012.
14. Pfister TD, Reinhold WC, Agama K, Gupta S, Khin SA, Kinders RJ, Parchment RE, Tomaszewski JE, Doroshow JH, Pommier Y. Topoisomerase I levels in the NCI-60 cancer cell line panel determined by validated ELISA and microarray analysis and correlation with indenoisoquinoline sensitivity. Mol Cancer Ther. 2009;8(7):1878-84.
15. Jansen WJ, Zwart B, Hulscher ST, Giaccone G, Pinedo HM, Boven E. CPT-11 in human colon-cancer cell lines and xenografts: characterization of cellular sensitivity determinants. Int J Cancer. 1997;70(3):335-40.
16. Burgess DJ, Doles J, Zender L, Xue W, Ma B, McCombie WR, Hannon GJ, Lowe SW, Hemann MT. Topoisomerase levels determine chemotherapy response in vitro and in vivo. Proc Natl Acad Sci U S A. 2008;105(26):9053-8.
17. Romer MU, Jensen NF, Nielsen SL, Muller S, Nielsen KV, Nielsen HJ, Brunner N. TOP1 gene copy numbers in colorectal cancer samples and cell lines and their association to in vitro drug sensitivity. Scand J Gastroenterol. 2012;47(1):68-79.
18. Braun MS, Richman SD, Quirke P, Daly C, Adlard JW, Elliott F, Barrett JH, Selby P, Meade AM, Stephens RJ, Parmar MK, Seymour MT. Predictive biomarkers of chemotherapy efficacy in colorectal cancer: results from the UK MRC FOCUS trial. J Clin Oncol. 2008;26(16):2690-8.
19. Paradiso A, Xu J, Mangia A, Chiriatti A, Simone G, Zito A, Montemurro S, Giuliani F, Maiello E, Colucci G. Topoisomerase-I, thymidylate synthase primary tumour expression and clinical efficacy of 5-FU/CPT-11 chemotherapy in advanced colorectal cancer patients. Int J Cancer. 2004;111(2):252-8.
20. Vallbohmer D, Iqbal S, Yang DY, Rhodes KE, Zhang W, Gordon M, Fazzone W, Schultheis AM, Sherrod AE, Danenberg KD, Lenz HJ. Molecular determinants of irinotecan efficacy. Int J Cancer. 2006;119(10):2435-42.
21. McLeod HL, Keith WN. Variation in topoisomerase I gene copy number as a mechanism for intrinsic drug sensitivity. Br J Cancer. 1996;74(4):508-12.
22. Yu J, Miller R, Zhang W, Sharma M, Holtschlag V, Watson MA, McLeod HL. Copy-number analysis of topoisomerase and thymidylate synthase genes in frozen and FFPE DNAs of colorectal cancers. Pharmacogenomics. 2008;9(10):1459-66.
23. Bandyopadhyay K, Gjerset RA. Protein kinase CK2 is a central regulator of topoisomerase I hyperphosphorylation and camptothecin sensitivity in cancer cell lines. Biochemistry. 2011;50(5):704-14.
24. Sorensen M, Sehested M, Jensen PB. Characterisation of a human small-cell lung cancer cell line resistant to the DNA topoisomerase I-directed drug topotecan. Br J Cancer. 1995;72(2):399-404.
25. Madelaine I, Prost S, Naudin A, Riou G, Lavelle F, Riou JF. Sequential modifications of topoisomerase I activity in a camptothecin-resistant cell line established by progressive adaptation. Biochem Pharmacol. 1993;45(2):339-48.
26. Sugimoto Y, Tsukahara S, Oh-hara T, Isoe T, Tsuruo T. Decreased expression of DNA topoisomerase I in camptothecin-resistant tumor cell lines as determined by a monoclonal antibody. Cancer Res. 1990;50(21):6925-30.
27. Beretta GL, Perego P, Zunino F. Mechanisms of cellular resistance to camptothecins. Curr Med Chem. 2006;13(27):3291-305.
28. Fujimori A, Hoki Y, Popescu NC, Pommier Y. Silencing and selective methylation of the normal topoisomerase I gene in camptothecin-resistant CEM/C2 human leukemia cells. Oncol Res. 1996;8(7-8):295-301.
29. Tsurutani J, Nitta T, Hirashima T, Komiya T, Uejima H, Tada H, Syunichi N, Tohda A, Fukuoka M, Nakagawa K. Point mutations in the topoisomerase I gene in patients with non-small cell lung cancer treated with irinotecan. Lung Cancer. 2002;35(3):299-304.
30. Seymour MT, Maughan TS, Ledermann JA, Topham C, James R, Gwyther SJ, Smith DB, Shepherd S, Maraveyas A, Ferry DR, Meade AM, Thompson L, et al. Different strategies of sequential and combination chemotherapy for patients with poor prognosis advanced colorectal cancer (MRC FOCUS): a randomised controlled trial. Lancet. 2007;370(9582):143-52.
31. Koopman M, Antonini NF, Douma J, Wals J, Honkoop AH, Erdkamp FL, De Jong RS, Rodenburg CJ, Vreugdenhil G, Loosveld OJ, Van BA, Sinnige HA, et al. Sequential versus combination chemotherapy with capecitabine, irinotecan, and oxaliplatin in advanced colorectal cancer (CAIRO): a phase III randomised controlled trial. Lancet. 2007;370(9582):135-42.
32. Koopman M, Knijn N, Richman S, Seymour M, Quirke P, Van Tinteren H, et al. The correlation between Topoisomerase-I (Topo1) expression and outcome of treatment with capecitabine and irinotecan in advanced colorectal cancer (ACC) patients (pts) treated in the CAIRO study of the Dutch Colorectal Cancer Group (DCCG)., 7 ed 2009. p. 321.
33. Teicher BA. Next generation topoisomerase I inhibitors: Rationale and biomarker strategies. Biochem Pharmacol. 2008;75(6):1262-71.
34. Pommier Y, Cushman M. The indenoisoquinoline noncamptothecin topoisomerase I inhibitors: update and perspectives. Mol Cancer Ther. 2009;8(5):1008-14.
35. Antony S, Agama KK, Miao ZH, Takagi K, Wright MH, Robles AI, Varticovski L, Nagarajan M, Morrell A, Cushman M, Pommier Y. Novel indenoisoquinolines NSC 725776 and NSC 724998 produce persistent topoisomerase I cleavage complexes and overcome multidrug resistance. Cancer Res. 2007;67(21):10397-405.
36. Jensen NF, Stenvang J, Beck MK, Hanakova B, Belling KC, Do KN, Viuff B, Nygard SB, Gupta R, Rasmussen MH, Tarpgaard LS, Hansen TP, et al. Establishment and characterization of models of chemotherapy resistance in colorectal cancer: Towards a predictive signature of chemoresistance. Mol Oncol. 2015;9(6):1169-85.
37. Smith DH, Christensen IJ, Jensen NF, Markussen B, Romer MU, Nygard SB, Muller S, Nielsen HJ, Brunner N, Nielsen KV. Mechanisms of topoisomerase I (TOP1) gene copy number increase in a stage III colorectal cancer patient cohort. PLoS One. 2013;8(4):e60613.
38. Gongora C, Vezzio-Vie N, Tuduri S, Denis V, Causse A, Auzanneau C, Collod-Beroud G, Coquelle A, Pasero P, Pourquier P, Martineau P, Del RM. New Topoisomerase I mutations are associated with resistance to camptothecin. Mol Cancer. 2011;10:64.
39. Pfister TD, Hollingshead M, Kinders RJ, Zhang Y, Evrard YA, Ji J, Khin SA, Borgel S, Stotler H, Carter J, Divelbiss R, Kummar S, et al. Development and validation of an immunoassay for quantification of topoisomerase I in solid tumor tissues. PLoS One. 2012;7(12):e50494.
40. Andersen FF, Stougaard M, Jorgensen HL, Bendsen S, Juul S, Hald K, Andersen AH, Koch J, Knudsen BR. Multiplexed detection of site specific recombinase and DNA topoisomerase activities at the single molecule level. ACS Nano. 2009;3(12):4043-54.
41. Stougaard M, Lohmann JS, Mancino A, Celik S, Andersen FF, Koch J, Knudsen BR. Single-molecule detection of human topoisomerase I cleavage-ligation activity. ACS Nano. 2009;3(1):223-33.
42. Covey JM, Jaxel C, Kohn KW, Pommier Y. Protein-linked DNA strand breaks induced in mammalian cells by camptothecin, an inhibitor of topoisomerase I. Cancer Res. 1989;49(18):5016-22.
43. Nitiss J, Wang JC. DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc Natl Acad Sci U S A. 1988;85(20):7501-5.
44. Kotoh S, Naito S, Yokomizo A, Kumazawa J, Asakuno K, Kohno K, Kuwano M. Increased expression of DNA topoisomerase I gene and collateral sensitivity to camptothecin in human cisplatin-resistant bladder cancer cells. Cancer Res. 1994;54(12):3248-52.
45. Perego P, Capranico G, Supino R, Zunino F. Topoisomerase I gene expression and cell sensitivity to camptothecin in human cell lines of different tumor types. Anticancer Drugs. 1994;5(6):645-9.
46. Pommier Y, Leo E, Zhang H, Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol. 2010;17(5):421-33.
47. Pommier Y, Pourquier P, Urasaki Y, Wu J, Laco GS. Topoisomerase I inhibitors: selectivity and cellular resistance. Drug Resist Updat. 1999;2(5):307-18.
48. Losasso C, Cretaio E, Palle K, Pattarello L, Bjornsti MA, Benedetti P. Alterations in linker flexibility suppress DNA topoisomerase I mutantinduced cell lethality. J Biol Chem. 2007;282(13):9855-64.
49. Li XG, Haluska Jr P, Hsiang YH, Bharti AK, Kufe DW, Liu LF, Rubin EH. Involvement of amino acids 361 to 364 of human topoisomerase I in camptothecin resistance and enzyme catalysis. Biochem Pharmacol. 1997;53(7):1019-27.
50. Urasaki Y, Laco GS, Pourquier P, Takebayashi Y, Kohlhagen G, Gioffre C, Zhang H, Chatterjee D, Pantazis P, Pommier Y. Characterization of a novel topoisomerase I mutation from a camptothecin-resistant human prostate cancer cell line. Cancer Res. 2001;61(5):1964-9.
51. Rubin E, Pantazis P, Bharti A, Toppmeyer D, Giovanella B, Kufe D. Identification of a mutant human topoisomerase I with intact catalytic activity and resistance to 9-nitro-camptothecin. J Biol Chem. 1994;269(4):2433-9.
52. Chrencik JE, Staker BL, Burgin AB, Pourquier P, Pommier Y, Stewart L, Redinbo MR. Mechanisms of camptothecin resistance by human topoisomerase I mutations. J Mol Biol. 2004;339(4):773-84.
53. Fiorani P, Amatruda JF, Silvestri A, Butler RH, Bjornsti MA, Benedetti P. Domain interactions affecting human DNA topoisomerase I catalysis and camptothecin sensitivity. Mol Pharmacol. 1999;56(6):1105-15.
54. Benedetti P, Fiorani P, Capuani L, Wang JC. Camptothecin resistance from a single mutation changing glycine 363 of human DNA topoisomerase I to cysteine. Cancer Res. 1993;53(18):4343-8.
55. Arakawa Y, Suzuki H, Saito S, Yamada H. Novel missense mutation of the DNA topoisomerase I gene in SN-38-resistant DLD-1 cells. Mol Cancer Ther. 2006;5(3):502-8.
56. Wang LF, Ting CY, Lo CK, Su JS, Mickley LA, Fojo AT, Whang-Peng J, Hwang J. Identification of mutations at DNA topoisomerase I responsible for camptothecin resistance. Cancer Res. 1997;57(8):1516-22.
57. Van Der Merwe M, Bjornsti MA. Mutation of Gly721 alters DNA topoisomerase I active site architecture and sensitivity to camptothecin. J Biol Chem. 2008;283(6):3305-15.
58. Knab AM, Fertala J, Bjornsti MA. A camptothecin-resistant DNA topoisomerase I mutant exhibits altered sensitivities to other DNA topoisomerase poisons. J Biol Chem. 1995;270(11):6141-8.
59. Fertala J, Vance JR, Pourquier P, Pommier Y, Bjornsti MA. Substitutions of Asn-726 in the active site of yeast DNA topoisomerase I define novel mechanisms of stabilizing the covalent enzyme-DNA intermediate. J Biol Chem. 2000;275(20):15246-53.
60. Woo MH, Vance JR, Marcos AR, Bailly C, Bjornsti MA. Active site mutations in DNA topoisomerase I distinguish the cytotoxic activities of camptothecin and the indolocarbazole, rebeccamycin. J Biol Chem. 2002;277(6):3813-22.
61. Kubota N, Kanzawa F, Nishio K, Takeda Y, Ohmori T, Fujiwara Y, Terashima Y, Saijo N. Detection of topoisomerase I gene point mutation in CPT-11 resistant lung cancer cell line. Biochem Biophys Res Commun. 1992;188(2):571-7.
62. Losasso C, Cretaio E, Fiorani P, D'Annessa I, Chillemi G, Benedetti P. A single mutation in the 729 residue modulates human DNA topoisomerase IB DNA binding and drug resistance. Nucleic Acids Res. 2008;36(17):5635-44.
63. Tesauro C, RB Md, Ottaviani A, Coletta A, Zuccaro L, Arno B, D'Annessa I, Fiorani P, Desideri A. Molecular mechanism of the camptothecin resistance of Glu710Gly topoisomerase IB mutant analyzed in vitro and in silico. Mol Cancer. 2013;12(1):100.
64. Bonadonna G, Gianni L, Santoro A, Bonfante V, Bidoli P, Casali P, Demicheli R, Valagussa P. Drugs ten years later: epirubicin. Ann Oncol. 1993;4(5):359-69.
65. Miao ZH, Player A, Shankavaram U, Wang YH, Zimonjic DB, Lorenzi PL, Liao ZY, Liu H, Shimura T, Zhang HL, Meng LH, Zhang YW, et al. Nonclassic functions of human topoisomerase I: genome-wide and pharmacologic analyses. Cancer Res. 2007;67(18):8752-61.
66. Sugimoto Y, Tsukahara S, Oh-hara T, Liu LF, Tsuruo T. Elevated expression of DNA topoisomerase II in camptothecin-resistant human tumor cell lines. Cancer Res. 1990;50(24):7962-5.
67. Cinelli MA, Reddy PV, Lv PC, Liang JH, Chen L, Agama K, Pommier Y, Van Breemen RB, Cushman M. Identification, synthesis, and biological evaluation of metabolites of the experimental cancer treatment drugs indotecan (LMP400) and indimitecan (LMP776) and investigation of isomerically hydroxylated indenoisoquinoline analogues as topoisomerase I poisons. J Med Chem. 2012;55(24):10844-62.
68. Wu CP, Hsieh CH, Wu YS. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm. 2011;8(6):1996-2011.
69. Kerr ID, Haider AJ, Gelissen IC. The ABCG family of membrane-associated transporters: you don't have to be big to be mighty. Br J Pharmacol. 2011;164(7):1767-79.