Lung cancer cell lines as tools for biomedical discovery and research.

Lung cancer cell lines have made a substantial contribution to lung cancer translational research and biomedical discovery. A systematic approach to initiating and characterizing cell lines from small cell and non-small cell lung carcinomas has led to the current collection of more than 200 lung cancer cell lines, a number that exceeds those for other common epithelial cancers combined. The ready availability and widespread dissemination of the lines to investigators worldwide have resulted in more than 9000 citations, including multiple examples of important biomedical discoveries. The high (but not perfect) genomic similarities between lung cancer cell lines and the lung tumor type from which they were derived provide evidence of the relevance of their use. However, major problems including misidentification or cell line contamination remain. Ongoing studies and new approaches are expected to reveal the full potential of the lung cancer cell line panel.

[1]  Amanda Capes-Davis,et al.  Check your cultures! A list of cross‐contaminated or misidentified cell lines , 2010, International journal of cancer.

[2]  J. Minna,et al.  Lung cancer cell lines: Useless artifacts or invaluable tools for medical science? , 2010, Lung cancer.

[3]  A. Sparks,et al.  The mutation spectrum revealed by paired genome sequences from a lung cancer patient , 2010, Nature.

[4]  W. Ansorge.  Next generation DNA sequencing techniques and applications , 2010 .

[5]  Paula Chaves,et al.  Verification and unmasking of widely used human esophageal adenocarcinoma cell lines. , 2010, Journal of the National Cancer Institute.

[6]  Tom Royce,et al.  A comprehensive catalogue of somatic mutations from a human cancer genome , 2010, Nature.

[7]  G. Hutchins,et al.  Henrietta Lacks, HeLa cells, and cell culture contamination. , 2009, Archives of pathology & laboratory medicine.

[8]  Calum MacAulay,et al.  Oncogene Mutations, Copy Number Gains and Mutant Allele Specific Imbalance (MASI) Frequently Occur Together in Tumor Cells , 2009, PloS one.

[9]  U. Schumacher,et al.  Increased numbers of spontaneous SCLC metastasis in absence of NK cells after subcutaneous inoculation of different SCLC cell lines into pfp/rag2 double knock out mice. , 2009, Cancer letters.

[10]  A. Gazdar,et al.  Activating and resistance mutations of EGFR in non-small-cell lung cancer: role in clinical response to EGFR tyrosine kinase inhibitors , 2009, Oncogene.

[11]  Patricia Greninger,et al.  A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. , 2009, Cancer cell.

[12]  Laura Tolosi,et al.  Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. , 2009, The Journal of clinical investigation.

[13]  H. Pass,et al.  Tumorigenic properties of alternative osteopontin isoforms in mesothelioma. , 2009, Biochemical and biophysical research communications.

[14]  Fang Liu,et al.  Tobacco smoke induces polycomb-mediated repression of Dickkopf-1 in lung cancer cells. , 2009, Cancer research.

[15]  M. Stratton,et al.  The cancer genome , 2009, Nature.

[16]  Sudhir Varma,et al.  DNA fingerprinting of the NCI-60 cell line panel , 2009, Molecular Cancer Therapeutics.

[17]  V. Detours,et al.  Human cancer cell lines: Experimental models for cancer cells in situ? For cancer stem cells? , 2009, Biochimica et biophysica acta.

[18]  Michael Peyton,et al.  Alterations in Genes of the EGFR Signaling Pathway and Their Relationship to EGFR Tyrosine Kinase Inhibitor Sensitivity in Lung Cancer Cell Lines , 2009, PloS one.

[19]  M. Brock,et al.  Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. , 2009, Cancer research.

[20]  E. Richer,et al.  High-throughput quantitative bioluminescence imaging for assessing tumor burden. , 2009, Methods in molecular biology.

[21]  William Pao,et al.  Genetic predictors of MEK dependence in non-small cell lung cancer. , 2008, Cancer research.

[22]  M. Ringel.  "Thyroid cancer" cell line misidentification: a time for proactive change. , 2008, The Journal of clinical endocrinology and metabolism.

[23]  Christopher Korch,et al.  Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. , 2008, The Journal of clinical endocrinology and metabolism.

[24]  W. Lam,et al.  PIK3CA mutations and copy number gains in human lung cancers. , 2008, Cancer research.

[25]  Bradley P. Coe,et al.  DNA amplification is a ubiquitous mechanism of oncogene activation in lung and other cancers , 2008, Oncogene.

[26]  A. Rojas,et al.  Cell line cross-contamination in biomedical research: a call to prevent unawareness , 2008, Acta Pharmacologica Sinica.

[27]  I Petersen,et al.  Genomic profiling identifies TITF1 as a lineage-specific oncogene amplified in lung cancer , 2008, Oncogene.

[28]  F. Hirsch,et al.  EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines. , 2008, Annals of oncology : official journal of the European Society for Medical Oncology.

[29]  P. Jänne,et al.  Mechanisms of Acquired Resistance to Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors in Non–Small Cell Lung Cancer , 2008, Clinical Cancer Research.

[30]  A. Jauch,et al.  Characterization of Human Mesothelioma Cell Lines as Tumor Models for Suicide Gene Therapy , 2008, Oncology Research and Treatment.

[31]  T. Gajewski,et al.  Diagnosis and Treatment of Mycoplasma‐Contaminated Cell Cultures , 2000, Current protocols in cytometry.

[32]  田中 寿明.  Lineage-specific dependency of lung adenocarcinomas on the lung development regulator TTF-1 , 2008 .

[33]  N. Hanna,et al.  MET Amplification Leads to Gefitinib Resistance in Lung Cancer by Activating ERBB3 Signaling , 2008 .

[34]  M. Sanchez-Cespedes.  A role for LKB1 gene in human cancer beyond the Peutz–Jeghers syndrome , 2007, Oncogene.

[35]  G. Sato.  Tissue culture: the unrealized potential , 2007, Cytotechnology.

[36]  Derek Y. Chiang,et al.  Characterizing the cancer genome in lung adenocarcinoma , 2007, Nature.

[37]  R. Kerbel,et al.  On the development of models in mice of advanced visceral metastatic disease for anti-cancer drug testing , 2007, Cancer and Metastasis Reviews.

[38]  B. Gunawan,et al.  Establishment and characterization of two distinct malignant mesothelioma cell lines with common clonal origin. , 2007, Cancer genetics and cytogenetics.

[39]  G. Lucignani,et al.  Cancer modeling: modern imaging applications in the generation of novel animal model systems to study cancer progression and therapy. , 2007, The international journal of biochemistry & cell biology.

[40]  Roland M. Nardone,et al.  Eradication of cross-contaminated cell lines: A call for action , 2007, Cell Biology and Toxicology.

[41]  Michael Peyton,et al.  Synthetic lethal screen identification of chemosensitizer loci in cancer cells , 2007, Nature.

[42]  I. Fidler,et al.  Murine models to evaluate novel and conventional therapeutic strategies for cancer. , 2007, The American journal of pathology.

[43]  Daniel A. Haber,et al.  Epidermal growth factor receptor mutations in lung cancer , 2007, Nature Reviews Cancer.

[44]  S. Gabriel,et al.  High-throughput oncogene mutation profiling in human cancer , 2007, Nature Genetics.

[45]  Simion I. Chiosea,et al.  Overexpression of Dicer in precursor lesions of lung adenocarcinoma. , 2007, Cancer research.

[46]  Adeeba Kamarulzaman,et al.  AIDS Res Hum Retroviruses , 2006 .

[47]  W. Gerald,et al.  A Genome-Wide Screen for Promoter Methylation in Lung Cancer Identifies Novel Methylation Markers for Multiple Malignancies , 2006, PLoS medicine.

[48]  R. Hotchkiss,et al.  Apoptosis and caspases regulate death and inflammation in sepsis , 2006, Nature Reviews Immunology.

[49]  R. Shoemaker.  The NCI60 human tumour cell line anticancer drug screen , 2006, Nature Reviews Cancer.

[50]  David A. Tuveson,et al.  The Use of Targeted Mouse Models for Preclinical Testing of Novel Cancer Therapeutics , 2006, Clinical Cancer Research.

[51]  Shuguang Huang,et al.  Comparative analysis and integrative classification of NCI60 cell lines and primary tumors using gene expression profiling data , 2006, BMC Genomics.

[52]  P. Mires.  Lines , 2006 .

[53]  Bradley P. Coe,et al.  Differential disruption of cell cycle pathways in small cell and non-small cell lung cancer , 2006, British Journal of Cancer.

[54]  R. Mangues,et al.  Mouse models in oncogenesis and cancer therapy , 2006, Clinical & translational oncology : official publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico.

[55]  S. Lam,et al.  High resolution analysis of non‐small cell lung cancer cell lines by whole genome tiling path array CGH , 2006, International journal of cancer.

[56]  Calum MacAulay,et al.  Gain of a region on 7p22.3, containing MAD1L1, is the most frequent event in small‐cell lung cancer cell lines , 2006, Genes, chromosomes & cancer.

[57]  M. Giovannini,et al.  Membrane organization and tumorigenesis--the NF2 tumor suppressor, Merlin. , 2005, Genes & development.

[58]  Patricia L. Harris,et al.  Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  S. Jhanwar,et al.  The NF2 Tumor Suppressor Gene Product, Merlin, Inhibits Cell Proliferation and Cell Cycle Progression by Repressing Cyclin D1 Expression , 2005, Molecular and Cellular Biology.

[60]  H. Varmus,et al.  Acquired Resistance of Lung Adenocarcinomas to Gefitinib or Erlotinib Is Associated with a Second Mutation in the EGFR Kinase Domain , 2005, PLoS medicine.

[61]  Elena Marchiori,et al.  Breakpoint identification and smoothing of array comparative genomic hybridization data , 2004, Bioinform..

[62]  K. Kondo,et al.  Orthotopically implanted SCID mouse model of human lung cancer suitable for investigating metastatic potential and anticancer drug effects. , 2004, Oncology reports.

[63]  S. Gabriel,et al.  EGFR Mutations in Lung Cancer: Correlation with Clinical Response to Gefitinib Therapy , 2004, Science.

[64]  Y. Yatabe,et al.  Reduced Expression of the let-7 MicroRNAs in Human Lung Cancers in Association with Shortened Postoperative Survival , 2004, Cancer Research.

[65]  Bradley P. Coe,et al.  A tiling resolution DNA microarray with complete coverage of the human genome , 2004, Nature Genetics.

[66]  John N Weinstein,et al.  Integromic analysis of the NCI-60 cancer cell lines. , 2004, Breast disease.

[67]  S. Dairkee,et al.  Genome-wide allelotyping of a new in vitro model system reveals early events in breast cancer progression. , 2002, Cancer research.

[68]  F. Kaye,et al.  RB and cyclin dependent kinase pathways: defining a distinction between RB and p16 loss in lung cancer , 2002, Oncogene.

[69]  J. Minna,et al.  Tumor suppressor genes on chromosome 3p involved in the pathogenesis of lung and other cancers , 2002, Oncogene.

[70]  A. Nicholson,et al.  Mutations of the BRAF gene in human cancer , 2002, Nature.

[71]  J. Masters.  HeLa cells 50 years on: the good, the bad and the ugly , 2002, Nature Reviews Cancer.

[72]  Masters,et al.  TIMELINEHeLa cells 50 years on: the good, the bad and the ugly , 2002 .

[73]  W. Travis,et al.  The new World Health Organization classification of lung tumours , 2001, European Respiratory Journal.

[74]  J A Thomson,et al.  Short tandem repeat profiling provides an international reference standard for human cell lines , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[75]  J. Minna,et al.  Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression. , 2001, Journal of the National Cancer Institute.

[76]  S. Baylin,et al.  Notch signaling induces cell cycle arrest in small cell lung cancer cells. , 2001, Cancer research.

[77]  Chun Xing Li,et al.  Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3 , 2000, Nature Genetics.

[78]  Gregory Sykes,et al.  Utility of gender determination in cell line identity , 2000, In Vitro Cellular & Developmental Biology - Animal.

[79]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[80]  J. Minna,et al.  The 630-kb Lung Cancer Homozygous Deletion Region on Human Chromosome 3 p 21 . 3 : Identification and Evaluation of the Resident Candidate Tumor Suppressor Genes 1 , 2000 .

[81]  J. Minna,et al.  Comparison of features of human lung cancer cell lines and their corresponding tumors. , 1999, Clinical cancer research : an official journal of the American Association for Cancer Research.

[82]  J. Minna,et al.  Comparison of features of human breast cancer cell lines and their corresponding tumors. , 1999, Clinical cancer research : an official journal of the American Association for Cancer Research.

[83]  M. Westerfield,et al.  Characterization of paired tumor and non‐tumor cell lines established from patients with breast cancer , 1998, International journal of cancer.

[84]  J. Minna,et al.  Allelotyping demonstrates common and distinct patterns of chromosomal loss in human lung cancer types , 1998, Genes, chromosomes & cancer.

[85]  Douglas L. Weed,et al.  Methodologic Guidelines for Review Papers , 1997 .

[86]  Harvey I. Pass,et al.  Lung cancer : principles and practice , 1996 .

[87]  J. Minna,et al.  NCI series of cell lines: An historical perspective , 1996, Journal of cellular biochemistry. Supplement.

[88]  S. Steinberg,et al.  MYC family DNA amplification in 126 tumor cell lines from patients with small cell lung cancer , 1996, Journal of cellular biochemistry. Supplement.

[89]  A. Gazdar,et al.  Cell culture methods for the establishment of the NCI series of lung cancer cell lines , 1996, Journal of cellular biochemistry. Supplement.

[90]  H. Pass,et al.  In vitro and in vivo studies of mesothelioma , 1996, Journal of cellular biochemistry. Supplement.

[91]  J. Minna,et al.  Neurofibromatosis type 2 (NF2) gene is somatically mutated in mesothelioma but not in lung cancer. , 1995, Cancer research.

[92]  A. Gazdar.  5 – Cell Culture of Lung Cancers , 1994 .

[93]  A. Gazdar,et al.  Atlas of human tumor cell lines , 1994 .

[94]  F. Kaye,et al.  Absence of p16INK4 protein is restricted to the subset of lung cancer lines that retains wildtype RB. , 1994, Oncogene.

[95]  R. Metcalf,et al.  p53 and Kirsten-ras mutations in human mesothelioma cell lines. , 1992, Cancer research.

[96]  E. Rubinstein.  The untold story of HUT78. , 1990, Science.

[97]  R. Gallo,et al.  Expanded HIV-1 cellular tropism by phenotypic mixing with murine endogenous retroviruses. , 1990, Science.

[98]  J. Minna,et al.  p53: a frequent target for genetic abnormalities in lung cancer. , 1989, Science.

[99]  A. Gazdar.  Innovative chemotherapy. Xenografts and in vitro drug sensitivity testing. , 1989, Chest.

[100]  S. O’Brien,et al.  Origin of the HIV-susceptible human CD4+ cell line H9. , 1989, AIDS research and human retroviruses.

[101]  R. Makuch,et al.  myc family DNA amplification in small cell lung cancer patients' tumors and corresponding cell lines. , 1988, Cancer research.

[102]  J. Minna,et al.  Abnormalities in structure and expression of the human retinoblastoma gene in SCLC. , 1988, Science.

[103]  M. Boyd,et al.  Metastasis models for human tumors in athymic mice: useful models for drug development. , 1987, Cancer detection and prevention. Supplement : official publication of the International Society for Preventive Oncology, Inc.

[104]  A. Gazdar,et al.  Establishment and Characterization of a Human Plasma Cell Myeloma Culture Having a Rearranged Cellular myc Proto-oncogene , 1986 .

[105]  J. Battey,et al.  L-myc, a new myc-related gene amplified and expressed in human small cell lung cancer , 1985, Nature.

[106]  J. Minna,et al.  Characterization of variant subclasses of cell lines derived from small cell lung cancer having distinctive biochemical, morphological, and growth properties. , 1985, Cancer research.

[107]  G. Bepler,et al.  Establishment and identification of small cell lung cancer cell lines having classic and variant features. , 1985, Cancer research.

[108]  J. Whang‐Peng,et al.  Cytogenetics of human small cell lung cancer. , 1985, Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer.

[109]  J. Minna,et al.  Amplification and expression of the c-myc oncogene in human lung cancer cell lines , 1983, Nature.

[110]  J. Minna,et al.  A nonrandom chromosomal abnormality, del 3p(14-23), in human small cell lung cancer (SCLC). , 1982, Cancer genetics and cytogenetics.

[111]  J. Minna,et al.  Specific chromosome defect associated with human small-cell lung cancer; deletion 3p(14-23). , 1982, Science.

[112]  A. Gazdar,et al.  Heterotransplantation of small‐cell carcinoma of the lung into nude mice: Comparison of intracranial and subcutaneous routes , 1981, International journal of cancer.

[113]  K. Miyazaki,et al.  The culture of human tumor cells in serum-free medium. , 1981, Methods in enzymology.

[114]  John D. Minna,et al.  Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma , 1980, Proceedings of the National Academy of Sciences.

[115]  J. Minna,et al.  Growth of human small cell (oat cell) carcinoma of the lung in serum-free growth factor-supplemented medium. , 1980, Cancer research.

[116]  J. Minna,et al.  Establishment of continuous, clonable cultures of small-cell carcinoma of lung which have amine precursor uptake and decarboxylation cell properties. , 1980, Cancer research.

[117]  A. Gazdar,et al.  Activities of L-dopa decarboxylase and diamine oxidase (histaminase) in human lung cancers and decarboxylase as a marker for small (oat) cell cancer in cell culture. , 1980, Cancer research.

[118]  N. Kaplan,et al.  Highly efficient induction of type C retroviruses by a human tumor in athymic mice. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[119]  A. Rizzino,et al.  The growth of cells in serum-free hormone-supplemented media. , 1979, Methods in enzymology.

[120]  E. Zimmerman,et al.  Isolation and characterization of a hormone-producing cell line from human small cell anaplastic carcinoma of the lung. , 1977, Journal of the National Cancer Institute.

[121]  Barry H. Smith,et al.  A continuous tumor‐cell line from a human lung carcinoma with properties of type II alveolar epithelial cells , 1976, International journal of cancer.

[122]  J. M. Whitcutt,et al.  Adaptation of cells derived from human malignant tumours to growth in vitro. , 1976, The South African journal of medical sciences.

[123]  W. Nelson-Rees,et al.  HeLa-like marker chromosomes and type-A variant glucose-6-phosphate dehydrogenase isoenzyme in human cell cultures producing Mason-Pfizer monkey virus-like particles. , 1974, Journal of the National Cancer Institute.

[124]  Y. Shimosato,et al.  A new floating cell line derived from human pulmonary carcinoma of oat cell type. , 1971, Gan.