The clinical relevance of cancer cell lines

Journal of the National Cancer Institute

Volumn 105, Issue 7, 2013, Pages 452-458

  Gillet, Jean Pierre ^a   Varma, Sudhir ^b   Gottesman, Michael M ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b HiThru Analytics LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT;

CANCER CELL CULTURE; EX VIVO STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC HETEROGENEITY; GLIOBLASTOMA; HELA CELL; HUMAN; IN VITRO STUDY; LIVER CELL CARCINOMA; LUNG SMALL CELL CANCER; OVARY CANCER; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SENSITIVITY AND SPECIFICITY; SHORT TANDEM REPEAT; STOMACH CANCER;

ANTINEOPLASTIC AGENTS; BORONIC ACIDS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; HUMANS; MOLECULAR TARGETED THERAPY; MULTIPLE MYELOMA; NEOPLASMS; PYRAZINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; TRANSCRIPTOME; TRANSLATIONAL MEDICAL RESEARCH; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84875992357     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djt007     Document Type: Review

References (108)

1. Sharma SV, Haber DA, Settleman J. Cell line-based platforms to evaluate the therapeutic efficacy of candidate anticancer agents. Nat Rev Cancer. 2010;10(4):241-253.
2. Scherer WF, Syverton JT, Gey GO. Studies on the propagation in vitro of poliomyelitis viruses. IV. Viral multiplication in a stable strain of human malignant epithelial cells (strain HeLa) derived from an epidermoid carcinoma of the cervix. J Exp Med. 1953;97(5):695-710.
3. Mattern J, Bak M, Hahn EW, et al. Human tumor xenografts as model for drug testing. Cancer Metastasis Rev. 1988;7(3):263-284.
4. Borrell B. How accurate are cancer cell lines? Nature. 2010;463(7283):858.
5. Weinstein JN. Drug discovery: cell lines battle cancer. Nature. 2012;483(7391):544-545.
6. Nelson-Rees WA. The identification and monitoring of cell line specificity. Prog Clin Biol Res. 1978;26:25-79.
7. Nelson-Rees WA, Flandermeyer RR. Inter-and intraspecies contamination of human breast tumor cell lines HBC and BrCa5 and other cell cultures. Science. 1977;195(4284):1343-1344. (Pubitemid 8097906)
8. Nelson-Rees WA, Flandermeyer RR, Hawthorne PK. Banded marker chromosomes as indicators of intraspecies cellular contamination. Science. 1974;184(4141):1093-1096.
9. Nelson-Rees WA, Owens RB, Arnstein P, et al. Source, alterations, characteristics and use of a new dog cell line (Cf2Th). In Vitro. 1976;12(10):665-669. (Pubitemid 8084966)
10. Akiyama S, Fojo A, Hanover JA, et al. Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somat Cell Mol Genet. 1985;11(2):117-126. (Pubitemid 15149285)
11. Shoemaker RH, Abbott BJ, Macdonald MM, et al. Use of the KB cell line for in vitro cytotoxicity assays. Cancer Treat Rep. 1983;67(1):97.
12. Shoemaker RH, Curt GA, Carney DN. Evidence for multidrugresistant cells in human tumor cell populations. Cancer Treat Rep. 1983;67(10):883-888. (Pubitemid 14231379)
13. Perdue RE Jr. KB cell culture I. Role in discovery of antitumor agents from higher plants. J Nat Prod. 1982;45(4):418-426. (Pubitemid 13252730)
14. Boyd M. The NCI in vitro anticancer drug discovery screen: concept, implementation, and operation, 1985-1995. In: Teicher B, ed. Anticancer Drug Development Guide: Preclinical Screening, Clinical Trials, and Approval. Totowa, NJ: Humana Press; 1997:23-42.
15. Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer. 2006;6(10):813-823. (Pubitemid 44450469)
16. Yamori T, Matsunaga A, Sato S, et al. Potent antitumor activity of MS-247, a novel DNA minor groove binder, evaluated by an in vitro and in vivo human cancer cell line panel. Cancer Res. 1999;59(16):4042-4049. (Pubitemid 29393575)
17. Yamori T. Panel of human cancer cell lines provides valuable database for drug discovery and bioinformatics. Cancer Chemother Pharmacol. 2003;52(suppl 1):S74-S79. (Pubitemid 37047027)
18. Cell line misidentification: the beginning of the end. Nat Rev Cancer. 2010;10(6):441-448.
19. Barallon R, Bauer SR, Butler J, et al. Recommendation of short tandem repeat profiling for authenticating human cell lines, stem cells, and tissues. In Vitro Cell Dev Biol Anim. 2010;46(9):727-732.
20. Nims RW, Sykes G, Cottrill K, et al. Short tandem repeat profiling: part of an overall strategy for reducing the frequency of cell misidentification. In Vitro Cell Dev Biol Anim. 2010;46(10):811-819.
21. Casado-Vela J, Cebrian A, Gomez del Pulgar MT, et al. Approaches for the study of cancer: towards the integration of genomics, proteomics and metabolomics. Clin Transl Oncol. 2011;13(9):617-628.
22. McDermott U, Sharma SV, Settleman J. High-throughput lung cancer cell line screening for genotype-correlated sensitivity to an EGFR kinase inhibitor. Methods Enzymol. 2008;438:331-341.
23. Barretina J, Caponigro G, Stransky N, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483(7391):603-607.
24. Lamb J. The Connectivity Map: a new tool for biomedical research. Nat Rev Cancer. 2007;7(1):54-60. (Pubitemid 46020847)
25. Lamb J, Crawford ED, Peck D, et al. The Connectivity Map: using geneexpression signatures to connect small molecules, genes, and disease. Science. 2006;313(5795):1929-1935. (Pubitemid 44497995)
26. Borst P, Wessels L. Do predictive signatures really predict response to cancer chemotherapy? Cell Cycle. 2010;9(24):4836-4840.
27. Oldenhuis CN, Oosting SF, Gietema JA, et al. Prognostic versus predictive value of biomarkers in oncology. Eur J Cancer. 2008;44(7):946-953.
28. Gillet JP, Gottesman MM. Mechanisms of multidrug resistance in cancer. In: Zhou J, ed. MultiDrug Resistance in Cancer. Totowa, NJ: Humana Press; 2010:47-76.
29. Gillet JP, Gottesman MM. Advances in the molecular detection of ABC transporters involved in multidrug resistance in cancer. Curr Pharm Biotechnol. 2011;12(4):686-692.
30. Orina JN, Calcagno AM, Wu CP, et al. Evaluation of current methods used to analyze the expression profiles of ATP-binding cassette transporters yields an improved drug-discovery database. Mol Cancer Ther. 2009;8(7):2057-2066.
31. Langmann T, Mauerer R, Schmitz G. Human ATP-binding cassette transporter TaqMan low-density array: analysis of macrophage differentiation and foam cell formation. Clin Chem. 2006;52(2):310-313. (Pubitemid 43185496)
32. Desai A, Jere A. Next-generation sequencing: ready for the clinics? Clin Genet. 2012;81(6):503-510.
33. Gazdar AF, Gao B, Minna JD. Lung cancer cell lines: useless artifacts or invaluable tools for medical science? Lung Cancer. 2010;68(3):309-318.
34. Gazdar AF, Girard L, Lockwood WW, et al. Lung cancer cell lines as tools for biomedical discovery and research. J Natl Cancer Inst. 2010;102(17):1310- 1321.
35. Gandhi J, Zhang J, Xie Y, et al. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS One. 2009;4(2):e4576.
36. Gillet JP, Calcagno AM, Varma S, et al. Multidrug resistance-linked gene signature predicts overall survival of patients with primary ovarian serous carcinoma. Clin Cancer Res. 2012;18(11):3197-3206.
37. Gillet JP, Wang J, Calcagno AM, et al. Clinical relevance of multidrug resistance gene expression in ovarian serous carcinoma effusions. Mol Pharm. 2011;8(6):2080-2088.
38. Gillet JP, Calcagno AM, Varma S, et al. Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci USA. 2011;108(46):18708-18713.
39. Lukk M, Kapushesky M, Nikkila J, et al. A global map of human gene expression. Nat Biotechnol. 2010;28(4):322-324.
40. Neve RM, Chin K, Fridlyand J, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 2006;10(6):515-527. (Pubitemid 44854747)
41. Wang H, Huang S, Shou J, et al. Comparative analysis and integrative classification of NCI60 cell lines and primary tumors using gene expression profiling data. BMC Genomics. 2006;7:166.
42. Woodbury MA. Will the real cancer cell please stand up? Biotechniques. 2012. http://www.biotechniques.com/news/Will-the-Real-Cancer-Cell-Please-Stand- Up/biotechniques-329467.html. Accessed January 16, 2013.
43. Garnett MJ, Edelman EJ, Heidorn SJ, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature. 2012;483(7391):570-575.
44. Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9(5):391-403. (Pubitemid 43668737)
45. Gillet JP, Okabe M, Gottesman MM. The hepatocyte and the cancer cell: Dr. Jekyll and Mr. Hyde. In: Arias IM, Fausto N, Boyer JL, et al., eds. The Liver: Biology and Pathobiology. 5th ed. Oxford: Wiley-Blackwell; 2009:1075-1090.
46. Toussaint O, Weemaels G, Debacq-Chainiaux F, et al. Artefactual effects of oxygen on cell culture models of cellular senescence and stem cell biology. J Cell Physiol. 2011;226(2):315-321.
47. Okita K, Yamanaka S. Induced pluripotent stem cells: opportunities and challenges. Philos Trans R Soc Lond B Biol Sci. 2011;366(1575):2198-2207.
48. Holmberg J, Perlmann T. Maintaining differentiated cellular identity. Nat Rev Genet. 2012;13(6):429-439.
49. Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883-892.
50. McCarthy N. Mouse models: of mice and men. Nat Rev Cancer. 2012;12(5):318-319.
51. Rottenberg S, Borst P. Drug resistance in the mouse cancer clinic. Drug Resist Updat. 2012;15(1-2):81-89.
52. Garber K. From human to mouse and back: "tumorgraft" models surge in popularity. J Natl Cancer Inst. 2009;101(1):6-8.
53. Heyer J, Kwong LN, Lowe SW, et al. Non-germline genetically engineered mouse models for translational cancer research. Nat Rev Cancer. 2010;10(7):470-480.
54. Zhang YA, Maitra A, Hsieh JT, et al. Frequent detection of infectious xenotropic murine leukemia virus (XMLV) in human cultures established from mouse xenografts. Cancer Biol Ther. 2011;12(7):617-628.
55. Sharma SV, Haber DA, Settleman J. Cell line-based platforms to evaluate the therapeutic efficacy of candidate anticancer agents. Nat Rev Cancer. 2010;10(4):241-253.
56. Scherer WF, Syverton JT, Gey GO. Studies on the propagation in vitro of poliomyelitis viruses. IV. Viral multiplication in a stable strain of human malignant epithelial cells (strain HeLa) derived from an epidermoid carcinoma of the cervix. J Exp Med. 1953;97(5):695-710.
57. Mattern J, Bak M, Hahn EW, et al. Human tumor xenografts as model for drug testing. Cancer Metastasis Rev. 1988;7(3):263-284.
58. Borrell B. How accurate are cancer cell lines? Nature. 2010;463(7283):858.
59. Weinstein JN. Drug discovery: cell lines battle cancer. Nature. 2012;483(7391):544-545.
60. Nelson-Rees WA. The identification and monitoring of cell line specificity. Prog Clin Biol Res. 1978;26:25-79.
61. Nelson-Rees WA, Flandermeyer RR. Inter-and intraspecies contamination of human breast tumor cell lines HBC and BrCa5 and other cell cultures. Science. 1977;195(4284):1343-1344. (Pubitemid 8097906)
62. Nelson-Rees WA, Flandermeyer RR, Hawthorne PK. Banded marker chromosomes as indicators of intraspecies cellular contamination. Science. 1974;184(4141):1093-1096.
63. Nelson-Rees WA, Owens RB, Arnstein P, et al. Source, alterations, characteristics and use of a new dog cell line (Cf2Th). In Vitro. 1976;12(10):665-669. (Pubitemid 8084966)
64. Akiyama S, Fojo A, Hanover JA, et al. Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somat Cell Mol Genet. 1985;11(2):117-126. (Pubitemid 15149285)
65. Shoemaker RH, Abbott BJ, Macdonald MM, et al. Use of the KB cell line for in vitro cytotoxicity assays. Cancer Treat Rep. 1983;67(1):97.
66. Shoemaker RH, Curt GA, Carney DN. Evidence for multidrugresistant cells in human tumor cell populations. Cancer Treat Rep. 1983;67(10):883-888. (Pubitemid 14231379)
67. Perdue RE Jr. KB cell culture I. Role in discovery of antitumor agents from higher plants. J Nat Prod. 1982;45(4):418-426. (Pubitemid 13252730)
68. Boyd M. The NCI in vitro anticancer drug discovery screen: concept, implementation, and operation, 1985-1995. In: Teicher B, ed. Anticancer Drug Development Guide: Preclinical Screening, Clinical Trials, and Approval. Totowa, NJ: Humana Press; 1997:23-42.
69. Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer. 2006;6(10):813-823. (Pubitemid 44450469)
70. Yamori T, Matsunaga A, Sato S, et al. Potent antitumor activity of MS-247, a novel DNA minor groove binder, evaluated by an in vitro and in vivo human cancer cell line panel. Cancer Res. 1999;59(16):4042-4049. (Pubitemid 29393575)
71. Yamori T. Panel of human cancer cell lines provides valuable database for drug discovery and bioinformatics. Cancer Chemother Pharmacol. 2003;52(suppl 1):S74-S79. (Pubitemid 37047027)
72. Cell line misidentification: the beginning of the end. Nat Rev Cancer. 2010;10(6):441-448.
73. Barallon R, Bauer SR, Butler J, et al. Recommendation of short tandem repeat profiling for authenticating human cell lines, stem cells, and tissues. In Vitro Cell Dev Biol Anim. 2010;46(9):727-732.
74. Nims RW, Sykes G, Cottrill K, et al. Short tandem repeat profiling: part of an overall strategy for reducing the frequency of cell misidentification. In Vitro Cell Dev Biol Anim. 2010;46(10):811-819.
75. Casado-Vela J, Cebrian A, Gomez del Pulgar MT, et al. Approaches for the study of cancer: towards the integration of genomics, proteomics and metabolomics. Clin Transl Oncol. 2011;13(9):617-628.
76. McDermott U, Sharma SV, Settleman J. High-throughput lung cancer cell line screening for genotype-correlated sensitivity to an EGFR kinase inhibitor. Methods Enzymol. 2008;438:331-341.
77. Barretina J, Caponigro G, Stransky N, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483(7391):603-607.
78. Lamb J. The Connectivity Map: a new tool for biomedical research. Nat Rev Cancer. 2007;7(1):54-60. (Pubitemid 46020847)
79. Lamb J, Crawford ED, Peck D, et al. The Connectivity Map: using geneexpression signatures to connect small molecules, genes, and disease. Science. 2006;313(5795):1929-1935. (Pubitemid 44497995)
80. Borst P, Wessels L. Do predictive signatures really predict response to cancer chemotherapy? Cell Cycle. 2010;9(24):4836-4840.
81. Oldenhuis CN, Oosting SF, Gietema JA, et al. Prognostic versus predictive value of biomarkers in oncology. Eur J Cancer. 2008;44(7):946-953.
82. Gillet JP, Gottesman MM. Mechanisms of multidrug resistance in cancer. In: Zhou J, ed. MultiDrug Resistance in Cancer. Totowa, NJ: Humana Press; 2010:47-76.
83. Gillet JP, Gottesman MM. Advances in the molecular detection of ABC transporters involved in multidrug resistance in cancer. Curr Pharm Biotechnol. 2011;12(4):686-692.
84. Orina JN, Calcagno AM, Wu CP, et al. Evaluation of current methods used to analyze the expression profiles of ATP-binding cassette transporters yields an improved drug-discovery database. Mol Cancer Ther. 2009;8(7):2057-2066.
85. Langmann T, Mauerer R, Schmitz G. Human ATP-binding cassette transporter TaqMan low-density array: analysis of macrophage differentiation and foam cell formation. Clin Chem. 2006;52(2):310-313. (Pubitemid 43185496)
86. Desai A, Jere A. Next-generation sequencing: ready for the clinics? Clin Genet. 2012;81(6):503-510.
87. Gazdar AF, Gao B, Minna JD. Lung cancer cell lines: useless artifacts or invaluable tools for medical science? Lung Cancer. 2010;68(3):309-318.
88. Gazdar AF, Girard L, Lockwood WW, et al. Lung cancer cell lines as tools for biomedical discovery and research. J Natl Cancer Inst. 2010;102(17):1310- 1321.
89. Gandhi J, Zhang J, Xie Y, et al. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS One. 2009;4(2):e4576.
90. Gillet JP, Calcagno AM, Varma S, et al. Multidrug resistance-linked gene signature predicts overall survival of patients with primary ovarian serous carcinoma. Clin Cancer Res. 2012;18(11):3197-3206.
91. Gillet JP, Wang J, Calcagno AM, et al. Clinical relevance of multidrug resistance gene expression in ovarian serous carcinoma effusions. Mol Pharm. 2011;8(6):2080-2088.
92. Gillet JP, Calcagno AM, Varma S, et al. Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci USA. 2011;108(46):18708-18713.
93. Lukk M, Kapushesky M, Nikkila J, et al. A global map of human gene expression. Nat Biotechnol. 2010;28(4):322-324.
94. Neve RM, Chin K, Fridlyand J, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 2006;10(6):515-527. (Pubitemid 44854747)
95. Wang H, Huang S, Shou J, et al. Comparative analysis and integrative classification of NCI60 cell lines and primary tumors using gene expression profiling data. BMC Genomics. 2006;7:166.
96. Woodbury MA. Will the real cancer cell please stand up? Biotechniques. 2012. http://www.biotechniques.com/news/Will-the-Real-Cancer-Cell-Please-Stand- Up/biotechniques-329467.html. Accessed January 16, 2013.
97. Garnett MJ, Edelman EJ, Heidorn SJ, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature. 2012;483(7391):570-575.
98. Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9(5):391-403. (Pubitemid 43668737)
99. Gillet JP, Okabe M, Gottesman MM. The hepatocyte and the cancer cell: Dr. Jekyll and Mr. Hyde. In: Arias IM, Fausto N, Boyer JL, et al., eds. The Liver: Biology and Pathobiology. 5th ed. Oxford: Wiley-Blackwell; 2009:1075-1090.
100. Toussaint O, Weemaels G, Debacq-Chainiaux F, et al. Artefactual effects of oxygen on cell culture models of cellular senescence and stem cell biology. J Cell Physiol. 2011;226(2):315-321.
101. Okita K, Yamanaka S. Induced pluripotent stem cells: opportunities and challenges. Philos Trans R Soc Lond B Biol Sci. 2011;366(1575):2198-2207.
102. Holmberg J, Perlmann T. Maintaining differentiated cellular identity. Nat Rev Genet. 2012;13(6):429-439.
103. Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883-892.
104. McCarthy N. Mouse models: of mice and men. Nat Rev Cancer. 2012;12(5):318-319.
105. Rottenberg S, Borst P. Drug resistance in the mouse cancer clinic. Drug Resist Updat. 2012;15(1-2):81-89.
106. Garber K. From human to mouse and back: "tumorgraft" models surge in popularity. J Natl Cancer Inst. 2009;101(1):6-8.
107. Heyer J, Kwong LN, Lowe SW, et al. Non-germline genetically engineered mouse models for translational cancer research. Nat Rev Cancer. 2010;10(7):470-480.
108. Zhang YA, Maitra A, Hsieh JT, et al. Frequent detection of infectious xenotropic murine leukemia virus (XMLV) in human cultures established from mouse xenografts. Cancer Biol Ther. 2011;12(7):617-628.