Methotrexate resistance in vitro is achieved by a dynamic selection process of tumor cell variants emerging during treatment

International Journal of Cancer

Volumn 119, Issue 7, 2006, Pages 1607-1615

  De Anta, Josep M ^a,d   Mayo, Clara ^a   Solé, Francesc ^b   Salido, Marta ^b   Espinet, Blanca ^b   Corzo, Cristina ^b   Petzold, Myriam ^a   Villa, Olaya ^b   Serrano, Sergi ^b   Real, Francisco X ^a,c   Mayol, Xavier ^a  

^a INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^b HOSPITAL DEL MAR   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cell survival; Cultured tumor cells; Neoplasm drug resistance; Nucleosides; Residual neoplasm

Indexed keywords

DIPYRIDAMOLE; METHOTREXATE;

ADAPTATION; ARTICLE; CANCER CHEMOTHERAPY; CELL DEATH; CELL DENSITY; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; CELL STRAIN HT29; CELL SURVIVAL; CENTROSOME; CHROMOSOME 5Q; COLON CANCER; CONTROLLED STUDY; DRUG RESISTANCE; DRUG SENSITIVITY; GENE AMPLIFICATION; GENETIC HETEROGENEITY; GENETIC RECOMBINATION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; TURNOVER TIME;

CELL LINE, TUMOR; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; DIPYRIDAMOLE; DRUG RESISTANCE, NEOPLASM; HUMANS; METHOTREXATE; NEOPLASMS; NUCLEOSIDES; SELECTION (GENETICS); VARIATION (GENETICS);

EID: 33747466753     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22028     Document Type: Article

References (33)

1. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998;396:643-9.
2. Cahill DP, Kinzler KW, Vogelstein B, Lengauer C. Genetic instability and darwinian selection in tumours. Trends Cell Biol 1999;9:M57-60.
3. Rosenberg SM. Evolving responsively: adaptive mutation. Nat Rev Genet 2001;2:504-15.
4. Taylor ST, Hickman JA, Dive C. Survival signals within the tumour microenvironment suppress drug-induced apoptosis: lessons learned from B lymphomas. Endocr Relat Cancer 1999;6:21-3.
5. Hazlehurst LA, Landowski TH, Dalton WS. Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death. Oncogene 2003;22:7396-402.
6. Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris VL, Chambers AF, Groom AC. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol 1998;153:865-73.
7. Braun S, Pantel K. Micrometastatic bone marrow involvement: detection and prognostic significance. Med Oncol 1999;16:154-65.
8. Tomida A, Tsuruo T. Drug resistance mediated by cellular stress response to the microenvironment of solid tumors. Anticancer Drug Des 1999;14:169-77.
9. Naumov GN, MacDonald IC, Chambers AF, Groom AC. Solitary cancer cells as a possible source of tumour dormancy? Semin Cancer Biol 2001;11:271-6.
10. Yu JL, Coomber BL, Kerbel RS. A paradigm for therapy-induced microenvironmental changes in solid tumors leading to drug resistance. Differentiation 2002;70:599-609.
11. de Anta JM, Real FX, Mayol X. Low tumor cell density environment yields survival advantage of tumor cells exposed to MTX in vitro. Biochim Biophys Acta 2005;1721:98-106.
12. Kinsella AR, Smith D, Pickard M. Resistance to chemotherapeutic antimetabolites: a function of salvage pathway involvement and cellular response to DNA damage. Br J Cancer 1997;75:935-45.
13. Zhen YS, Taniki T, Weber G. Azidothymidine and dipyridamole as biochemical response modifiers: synergism with methotrexate and 5-fluorouracil in human colon and pancreatic carcinoma cells. Oncol Res 1992;4:73-8.
14. Lesuffleur T, Barbat A, Dussaulx E, Zweibaum A. Growth adaptation to methotrexate of HT-29 human colon carcinoma cells is associated with their ability to differentiate into columnar absorptive and mucussecreting cells. Cancer Res 1990;50:6334-43.
15. Lesuffleur T, Barbat A, Luccioni C, Beaumatin J, Clair M, Kornowski A, Dussaulx E, Dutrillaux B, Zweibaum A. Dihydrofolate reductase gene amplification-associated shift of differentiation in methotrexate-adapted HT-29 cells. J Cell Biol 1991;115:1409-18.
16. Singer MJ, Mesner LD, Friedman CL, Trask BJ, Hamlin JL. Amplification of the human dihydrofolate reductase gene via double minutes is initiated by chromosome breaks. Proc Natl Acad Sci USA 2000;97:7921-6.
17. Almasan A, Linke SP, Paulson TG, Huang LC, Wahl GM. Genetic instability as a consequence of inappropriate entry into and progression through S-phase. Cancer Metastasis Rev 1995;14:59-73.
18. Corzo C, Petzold M, Mayol X, Espinet B, Salido M, Serrano S, Real FX, Sole F. RxFISH karyotype and MYC amplification in the HT-29 colon adenocarcinoma cell line. Genes Chromosomes Cancer 2003;36:425-6.
19. de Nonancourt-Didion M, Gueant JL, Adjalla C, Chery C, Hatier R, Namour F. Overexpression of folate binding protein α is one of the mechanism explaining the adaptation of HT29 cells to high concentration of methotrexate. Cancer Lett 2001;171:139-45.
20. Banerjee D, Mayer-Kuckuk P, Capiaux G, Budak-Alpdogan T, Gorlick R, Bertino JR. Novel aspects of resistance to drugs targeted to dihydrofolate reductase and thymidylate synthase. Biochim Biophys Acta 2002;1587:164-73.
21. Lingle WL, Salisbury JL. The role of the centrosome in the development of malignant tumors. Curr Top Dev Biol 2000;49:313-29.
22. Lorico A, Toffoli G, Boiocchi M, Erba E, Broggini M, Rappa G, D'Incalci M. Accumulation of DNA strand breaks in cells exposed to methotrexate or N10-propargyl-5,8-dideazafolic acid. Cancer Res 1988;48:2036-41.
23. Ma C, Martin S, Trask B, Hamlin JL. Sister chromatid fusion initiates amplification of the dihydrofolate reductase gene in Chinese hamster cells. Genes Dev 1993;7:605-20.
24. Poupon MF, Smith KA, Chernova OB, Gilbert C, Stark GR. Inefficient growth arrest in response to dNTP starvation stimulates gene amplification through bridge-breakage-fusion cycles. Mol Biol Cell 1996;7:345-54.
25. Lundin C, Erixon K, Arnaudeau C, Schultz N, Jenssen D, Meuth M, Helleday T. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol Cell Biol 2002;22:5869-78.
26. Noe V, Alemany C, Nicolas M, Ciudad CJ. Sp1 involvement in the 4-β-phorbol 12-myristate 13-acetate (TPA)-mediated increase in resistance to methotrexate in Chinese hamster ovary cells. Eur J Biochem 2001;268:3163-73.
27. Roschke AV, Stover K, Tonon G, Schaffer AA, Kirsch IR. Stable karyo-types in epithelial cancer cell lines despite high rates of ongoing structural and numerical chromosomal instability. Neoplasia 2002;4:19-31.
28. Ribas M, Masramon L, Aiza G, Capella G, Miro R, Peinado MA. The structural nature of chromosomal instability in colon cancer cells. FASEB J 2003;17:289-91.
29. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997;386:623-7.
30. Tomlinson I, Bodmer W. Selection, the mutation rate and cancer: ensuring that the tail does not wag the dog. Nat Med 1999;5:11-12.
31. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995;1:149-53.
32. Hahnfeldt P, Panigrahy D, Folkman J, Hlatky L. Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy. Cancer Res 1999;59:4770-5.
33. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002;196:254-65.