Critical Reviews in Oncology / Hematology
Volume 75, Issue 2 , Pages 94-109 , August 2010

Histopathologic and genetic alterations as predictors of response to treatment and survival in lung cancer: A review of published data

  • Giannis Mountzios

      Affiliations

    • Department of Clinical Therapeutics, “Alexandra” Hospital, University of Athens School of Medicine, Athens, Greece
    • ,
  • Meletios-Athanassios Dimopoulos

      Affiliations

    • Department of Clinical Therapeutics, “Alexandra” Hospital, University of Athens School of Medicine, Athens, Greece
    • ,
  • Jean-Charles Soria

      Affiliations

    • Department of Medicine, Institut Gustave-Roussy, Villejuif, France
    • Université Paris XI, Kremlin-Bicêtre, France
    • ,
  • Despina Sanoudou

      Affiliations

    • Molecular Biology Division, Biomedical Research Foundation, Academy of Athens, Greece
    • Genomics and Genetics Division, Children's Hospital Boston, Harvard Medical School, Boston, USA
    • ,
  • Christos A. Papadimitriou

      Affiliations

    • Department of Clinical Therapeutics, “Alexandra” Hospital, University of Athens School of Medicine, Athens, Greece
    • Corresponding Author InformationCorresponding author at: Tatoiou 146, Nea Erythrea, PC 14671, Greece. Tel.: +30 6944628688; fax: +30 2103381511.

,Accepted 7 October 2009.

References 

  1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58:71–96
  2. Subramanian J, Govindan R. Lung cancer in never smokers: a review. J Clin Oncol. 2007;25:561–570
  3. Mountzios G, Fouret P, Soria JC. Mechanisms of disease: signal transduction in lung carcinogenesis—a comparison of smokers and never-smokers. Nat Clin Pract Oncol. 2008;5:610–618
  4. Erman M, Grunenwald D, Penault-Llorca F, et al. Epidermal growth factor receptor, HER-2/neu and related pathways in lung adenocarcinomas with bronchioloalveolar features. Lung Cancer. 2005;47:315–323
  5. Toloza EM, Roth JA, Swisher SG. Molecular events in bronchogenic carcinoma and their implications for therapy. Semin Surg Oncol. 2000;18:91–99
  6. Hommura F, Dosaka-Akita H, Kinoshita I, et al. Predictive value of expression of p16INK4A, retinoblastoma and p53 proteins for the prognosis of non-small-cell lung cancers. Br J Cancer. 1999;81:696–701
  7. Mao L, Lee JS, Kurie JM, et al. Clonal genetic alterations in the lungs of current and former smokers. J Natl Cancer Inst. 1997;89:857–862
  8. Vincenzi B, Schiavon G, Silletta M, et al. Cell cycle alterations and lung cancer. Histol Histopathol. 2006;21:423–435
  9. Mohamed S, Yasufuku K, Hiroshima K, et al. Prognostic implications of cell cycle-related proteins in primary resectable pathologic N2 non-small cell lung cancer. Cancer. 2007;109:2506–2514
  10. Khayyata S, Yun S, Pasha T, et al. Value of P63 and CK5/6 in distinguishing squamous cell carcinoma from adenocarcinoma in lung fine-needle aspiration specimens. Diagn Cytopathol. 2009;37:178–183
  11. Poschmann G, Sitek B, Sipos B, et al. Identification of proteomic differences between squamous cell carcinoma of the lung and bronchial epithelium. Mol Cell Proteomics. 2009;[Epub ahead of print]
  12. Wu GP, Zhang SS, Fanq CQ, Liu SL, Wang EH. Immunocytochemical panel for distinguishing carcinoma cells from reactive mesothelial cells in pleural effusions. Cytopathology. 2008;19(August (4)):212–217
  13. Lopez-Malpartida AV, Ludena MD, Varela G, Pichel JG. Differential ErbB receptor expression and intracellular signaling activity in lung adenocarcinomas and squamous cell carcinomas. Lung Cancer. 2008;[Epub ahead of print]
  14. Skrzypski M, Jassem E, Taron M, et al. Three-gene expression signature predicts survival in early-stage squamous cell carcinoma of the lung. Clin Cancer Res. 2008;14:4794–4799
  15. Mitsudomi T, Hamajima N, Ogawa M, Takahashi T. Prognostic significance of p53 alterations in patients with non-small cell lung cancer: a meta-analysis. Clin Cancer Res. 2000;6:4055–4063
  16. Dutu T, Michiels S, Fouret P, et al. Differential expression of biomarkers in lung adenocarcinoma: a comparative study between smokers and never-smokers. Ann Oncol. 2005;16:1906–1914
  17. Al-Zahrani AM, Al-Raddadi RM. Nutritional knowledge of primary health care physicians in Jeddah, Saudi Arabia. Saudi Med J. 2009;30:284–287
  18. Ariel-Ronen S, Coe BP, Lau SK, et al. Genomic markers for malignant progression in pulmonary adenocarcinoma with bronchioloalveolar features. Proc Natl Acad Sci USA. 2008;105:10155–10160
  19. Moran CA, Suster S, Coppola D, Wick MR. Neuroendocrine carcinomas of the lung: a critical analysis. Am J Clin Pathol. 2009;131:206–221
  20. Stahel RA. Adenocarcinoma, a molecular perspective. Ann Oncol. 2007;18(Suppl. 9):ix147–ix149
  21. Beasley MB. Immunohistochemistry of pulmonary and pleural neoplasia. Arch Pathol Lab Med. 2008;132:1062–1072
  22. Raz DJ, Kim JY, Jablons DM. Diagnosis and treatment of bronchioloalveolar carcinoma. Curr Opin Pulm Med. 2007;13:290–296
  23. Le CF, Mukeria A, Hunt JD, et al. TP53 and KRAS mutation load and types in lung cancers in relation to tobacco smoke: distinct patterns in never, former, and current smokers. Cancer Res. 2005;65:5076–5083
  24. Nikliński J, Niklińska W, Laudanski J, Chyczewska E, Chyczewski L. Prognostic molecular markers in non-small cell lung cancer. Lung Cancer. 2001;34(December (Suppl. 2)):S53–S58
  25. Riely GJ, Kris MG, Rosenbaum D, et al. Frequency and distinctive spectrum of KRAS mutations in never smokers with lung adenocarcinoma. Clin Cancer Res. 2008;14:5731–5734
  26. Subramanian J, Govindan R. Molecular genetics of lung cancer in people who have never smoked. Lancet Oncol. 2008;9:676–682
  27. Kim SJ, Rabbani ZN, Dong F, et al. Phosphorylated epidermal growth factor receptor and cyclooxygenase-2 expression in localized non-small cell lung cancer. Med Oncol. 2009;
  28. Lim EH, Zhang SL, Li JL, et al. Using whole genome amplification (WGA) of low-volume biopsies to assess the prognostic role of EGFR, KRAS, p53, and CMET mutations in advanced-stage non-small cell lung cancer (NSCLC). J Thorac Oncol. 2009;4(January (1)):12–21
  29. Guo NL, Wan YW, Tosun K, et al. Confirmation of gene expression-based prediction of survival in non-small cell lung cancer. Clin Cancer Res. 2008;14:8213–8220
  30. Raz DJ, Ray MR, Kim JY, et al. A multigene assay is prognostic of survival in patients with early-stage lung adenocarcinoma. Clin Cancer Res. 2008;14:5565–5570
  31. Hauso O, Gustafsson BI, Kidd M, et al. Neuroendocrine tumor epidemiology: contrasting Norway and North America. Cancer. 2008;113:2655–2664
  32. Garcia-Yuste M, Matilla JM, Gonzalez-Aragoneses F. Neuroendocrine tumors of the lung. Curr Opin Oncol. 2008;20:148–154
  33. Moran CA, Suster S, Coppola D, Wick MR. Neuroendocrine carcinomas of the lung: a critical analysis. Am J Clin Pathol. 2009;131(February (2)):206–221
  34. Roncalli M, Doglioni C, Springall DR, et al. Abnormal p53 expression in lung neuroendocrine tumors. Diagnostic and prognostic implications. Diagn Mol Pathol. 1992;1:129–135
  35. Carter D, Yesner R. Carcinomas of the lung with neuroendocrine differentiation. Semin Diagn Pathol. 1985;2:235–254
  36. Olaussen KA, Mountzios G, Soria JC. ERCC1 as a risk stratifier in platinum-based chemotherapy for non-small-cell lung cancer. Curr Opin Pulm Med. 2007;13:284–289
  37. Olaussen KA, Dunant A, Fouret P, et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med. 2006;355:983–991
  38. Zhou W, Gurubhagavatula S, Liu G, et al. Excision repair cross-complementation group 1 polymorphism predicts overall survival in advanced non-small cell lung cancer patients treated with platinum-based chemotherapy. Clin Cancer Res. 2004;10:4939–4943
  39. Isla D, Sarries C, Rosell R, et al. Single nucleotide polymorphisms and outcome in docetaxel-cisplatin-treated advanced non-small-cell lung cancer. Ann Oncol. 2004;15:1194–1203
  40. Scagliotti GV, Selvaggi G. New data integrating multitargeted antifolates into treatment of first-line and relapsed non-small-cell lung cancer. Clin Lung Cancer. 2008;9(Suppl. 3):S122–S128
  41. Rosell R, Taron M, Barnadas A, et al. Nucleotide excision repair pathways involved in Cisplatin resistance in non-small-cell lung cancer. Cancer Control. 2003;10:297–305
  42. Lord RV, Brabender J, Gandara D, et al. Low ERCC1 expression correlates with prolonged survival after cisplatin plus gemcitabine chemotherapy in non-small cell lung cancer. Clin Cancer Res. 2002;8:2286–2291
  43. Rosell R, Cobo M, Isla D, Camps C, Massuti B. Pharmacogenomics and gemcitabine. Ann Oncol. 2006;17(Suppl. 5):v13–v16
  44. Bepler G, Kusmartseva I, Sharma S, et al. RRM1 modulated in vitro and in vivo efficacy of gemcitabine and platinum in non-small-cell lung cancer. J Clin Oncol. 2006;24:4731–4737
  45. Ceppi P, Volante M, Novello S, et al. ERCC1 and RRM1 gene expressions but not EGFR are predictive of shorter survival in advanced non-small-cell lung cancer treated with cisplatin and gemcitabine. Ann Oncol. 2006;17:1818–1825
  46. Zheng Z, Chen T, Li X, Haura E, Sharma A, Bepler G. DNA synthesis and repair genes RRM1 and ERCC1 in lung cancer. N Engl J Med. 2007;356(February 22 (8)):800–808
  47. Lee HW, Choi YW, Han JH, et al. Expression of excision repair cross-complementation group 1 protein predicts poor outcome in advanced non-small cell lung cancer patients treated with platinum-based doublet chemotherapy. Lung Cancer. 2009;(January 15):[Epub ahead of print]
  48. Boukovinas I, Papadaki C, Mendez P, et al. Tumor BRCA1, RRM1 and RRM2 mRNA expression levels and clinical response to first-line gemcitabine plus docetaxel in non-small-cell lung cancer patients. PLoS One. 2008;3(11):e3695
  49. Kikuchi T, Daigo Y, Katagiri T, et al. Expression profiles of non-small cell lung cancers on cDNA microarrays: identification of genes for prediction of lymph-node metastasis and sensitivity to anti-cancer drugs. Oncogene. 2003;22(April 10 (14)):2192–2205
  50. Rosell R, Taron M, Camps C, et al. Influence of genetic markers on survival in non-small cell lung cancer. Drugs Today (Barc). 2003;39(October (10)):775–786
  51. Toh CK, Gao F, Lim WT, et al. Differences between small-cell lung cancer and non-small-cell lung cancer among tobacco smokers. Lung Cancer. 2007;56:161–166
  52. Tsao MS, Sakurada A, Cutz JC, et al. Erlotinib in lung cancer—molecular and clinical predictors of outcome. N Engl J Med. 2005;353:133–144
  53. Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350:2129–2139
  54. Paez JG, Janne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004;304:1497–1500
  55. Shigematsu H, Lin L, Takahashi T, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst. 2005;97:339–346
  56. Zhu CQ, da Cunha SG, Ding K, et al. Role of KRAS and EGFR as biomarkers of response to erlotinib in National Cancer Institute of Canada Clinical Trials Group Study BR.21. J Clin Oncol. 2008;26:4268–4275
  57. Cortes-Funes H, Gomez C, Rosell R, et al. Epidermal growth factor receptor activating mutations in Spanish gefitinib-treated non-small-cell lung cancer patients. Ann Oncol. 2005;16:1081–1086
  58. Han SW, Kim TY, Hwang PG, et al. Predictive and prognostic impact of epidermal growth factor receptor mutation in non-small-cell lung cancer patients treated with gefitinib. J Clin Oncol. 2005;23:2493–2501
  59. Mitsudomi T, Kosaka T, Endoh H, et al. Mutations of the epidermal growth factor receptor gene predict prolonged survival after gefitinib treatment in patients with non-small-cell lung cancer with postoperative recurrence. J Clin Oncol. 2005;23:2513–2520
  60. Takano T, Ohe Y, Sakamoto H, et al. Epidermal growth factor receptor gene mutations and increased copy numbers predict gefitinib sensitivity in patients with recurrent non-small-cell lung cancer. J Clin Oncol. 2005;23:6829–6837
  61. Cappuzzo F, Hirsch FR, Rossi E, et al. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst. 2005;97:643–655
  62. Pao W, Miller VA, Politi KA, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2005;2:e73
  63. Kwak EL, Sordella R, Bell DW, et al. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc Natl Acad Sci USA. 2005;102:7665–7670
  64. Hirsch FR, Varella-Garcia M, McCoy J, et al. Increased epidermal growth factor receptor gene copy number detected by fluorescence in situ hybridization associates with increased sensitivity to gefitinib in patients with bronchioloalveolar carcinoma subtypes: a Southwest Oncology Group Study. J Clin Oncol. 2005;23:6838–6845
  65. Dziadziuszko R, Holm B, Skov BG, et al. Epidermal growth factor receptor gene copy number and protein level are not associated with outcome of non-small-cell lung cancer patients treated with chemotherapy. Ann Oncol. 2007;18:447–452
  66. Hirsch FR, Varella-Garcia M, Bunn PA, et al. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small-cell lung cancer. J Clin Oncol. 2006;24(31):5034–5042
  67. Chi DD, Hing AV, Helms C, et al. Two chromosome 7 dinucleotide repeat polymorphisms at gene loci epidermal growth factor receptor (EGFR) and pro alpha 2 (I) collagen (COL1A2). Hum Mol Genet. 1992;1(2):135
  68. Gebhardt F, Zänker KS, Brandt B. Modulation of epidermal growth factor receptor gene transcription by a polymorphic dinucleotide repeat in intron 1. J Biol Chem. 1999;274(May 7 (19)):13176–13180
  69. Etienne-Grimaldi MC, Pereira S, Magne N, et al. Analysis of the dinucleotide repeat polymorphism in the epidermal growth factor receptor (EGFR) gene in head and neck cancer patients. Ann Oncol. 2005;16(6):934–941
  70. Liu W, Innocenti F, Chen P, et al. Interethnic difference in the allelic distribution of human epidermal growth factor receptor intron 1 polymorphism. Clin Cancer Res. 2003;9(March (3)):1009–1012
  71. Susman E. Rash correlates with tumour response after cetuximab. Lancet Oncol. 2004;5(November (11)):64
  72. Dubey S, Stephenson P, Levy DE, et al. EGFR dinucleotide repeat polymorphism as a prognostic indicator in non-small cell lung cancer. J Thorac Oncol. 2006;1(June (5)):406–412
  73. Han SW, Jeon YK, Lee KH, et al. Intron 1 CA dinucleotide repeat polymorphism and mutations of epidermal growth factor receptor and gefitinib responsiveness in non-small-cell lung cancer. Pharmacogenet Genomics. 2007;17(May (5)):313–319
  74. Liu G, Gurubhagavatula S, Zhou W, et al. Epidermal growth factor receptor polymorphisms and clinical outcomes in non-small-cell lung cancer patients treated with gefitinib. Pharmacogenomics J. 2008;8(April (2)):129–138
  75. Rudin CM, Liu W, Desai A, et al. Pharmacogenomic and pharmacokinetic determinants of erlotinib toxicity. J Clin Oncol. 2008;26(March 1 (7)):1119–1127
  76. Tamura K, Fukuoka M. Gefitinib in non-small cell lung cancer. Expert Opin Pharmacother. 2005;6(June (6)):985–993
  77. Hirsch FR, Varella-Garcia M, Cappuzzo F, et al. Combination of EGFR gene copy number and protein expression predicts outcome for advanced non-small-cell lung cancer patients treated with gefitinib. Ann Oncol. 2007;18(April (4)):752–760
  78. Cappuzzo F, Magrini E, Ceresoli GL, et al. Akt phosphorylation and gefitinib efficacy in patients with advanced non-small-cell lung cancer. J Natl Cancer Inst. 2004;96:1133–1141
  79. Singhal S, Vachani A, Antin-Ozerkis D, et al. Prognostic implications of cell cycle, apoptosis, and angiogenesis biomarkers in non-small cell lung cancer: a review. Clin Cancer Res. 2005;11(June 1 (11)):3974–3986
  80. Petty RD, Nicolson MC, Kerr KM, et al. Gene expression profiling in non-small cell lung cancer: from molecular mechanisms to clinical application. Clin Cancer Res. 2004;10(May 15 (10)):3237–3248
  81. Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med. 2006;355(December 14 (24)):2542–2550
  82. Yang JC, Haworth L, Sherry RM, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349(July 31 (5)):427–434
  83. Watson CJ, Webb NJ, Bottomley MJ, Brenchley PE. Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine. 2000;12(August (8)):1232–1235
  84. Krippl P, Langsenlehner U, Renner W, et al. A common 936C/T gene polymorphism of vascular endothelial growth factor is associated with decreased breast cancer risk. Int J Cancer. 2003;106(September 10 (4)):468–471
  85. Heist RS, Zhai R, Liu G, et al. VEGF polymorphisms and survival in early-stage non-small-cell lung cancer. J Clin Oncol. 2008;26(February 20 (6)):856–862
  86. Siegfried JM, Weissfeld LA, Luketich JD, et al. The clinical significance of hepatocyte growth factor for non-small cell lung cancer. Ann Thorac Surg. 1998;66(December (6)):1915–1918
  87. Tokunou M, Niki T, Eguchi K, et al. c-MET expression in myofibroblasts: role in autocrine activation and prognostic significance in lung adenocarcinoma. Am J Pathol. 2001;158(April (4)):1451–1463
  88. Takanami I, Tanana F, Hashizume T, et al. Hepatocyte growth factor and c-Met/hepatocyte growth factor receptor in pulmonary adenocarcinomas: an evaluation of their expression as prognostic markers. Oncology. 1996;53(September–October (5)):392–397
  89. Thomson S, Buck E, Petti F, et al. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res. 2005;65:9455–9462
  90. Witta SE, Gemmill RM, Hirsch FR, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 2006;66:944–950
  91. Yauch RL, Januario T, Eberhard DA, et al. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin Cancer Res. 2005;11:8686–8698
  92. Cappuzzo F, Varella-Garcia M, Shigematsu H, et al. Increased HER2 gene copy number is associated with response to gefitinib therapy in epidermal growth factor receptor-positive non-small-cell lung cancer patients. J Clin Oncol. 2005;23:5007–5018
  93. Cappuzzo F, Toschi L, Domenichini I, et al. HER3 genomic gain and sensitivity to gefitinib in advanced non-small-cell lung cancer patients. Br J Cancer. 2005;93:1334–1340
  94. Engelman JA, Janne PA, Mermel C, et al. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proc Natl Acad Sci USA. 2005;102:3788–3793
  95. Eberhard DA, Johnson BE, Amler LC, et al. Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with non-small-cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol. 2005;23:5900–5909
  96. Hirsch FR, Varella-Garcia M, Dziadziuszko R, et al. Fluorescence in situ hybridization subgroup analysis of TRIBUTE, a phase III trial of erlotinib plus carboplatin and paclitaxel in non-small cell lung cancer. Clin Cancer Res. 2008;14:6317–6323
  97. Huang RS, Ratain MJ. Pharmacogenetics and pharmacogenomics of anticancer agents. CA Cancer J Clin. 2009;59(January–February (1)):42–45
  98. Bhattacharjee A, Richards WG, Staunton J, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci USA. 2001;98(November 20 (24)):13790–13795
  99. Garber ME, Troyanskaya OG, Schluens K, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA. 2001;98(November 20 (24)):13784–13789
  100. Beer DG, Kardia SL, Huang CC, et al. Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med. 2002;8(August (8)):816–824
  101. Wigle DA, Jurisica I, Radulovich N, et al. Molecular profiling of non-small cell lung cancer and correlation with disease-free survival. Cancer Res. 2002;62(June 1 (11)):3005–3008
  102. Chen HY, Yu SL, Chen CH, et al. A five-gene signature and clinical outcome in non-small-cell lung cancer. N Engl J Med. 2007;356(January 4 (1)):11–20
  103. Natsume T, Nakamura T, Koh Y, et al. Gene expression profiling of exposure to TZT-1027, a novel microtubule-interfering agent, in non-small cell lung cancer PC-14 cells and astrocytes. Invest New Drugs. 2001;19(4):293–302
  104. Ohira T, Akutagawa S, Usuda J, et al. Up-regulated gene expression of angiogenesis factors in post-chemotherapeutic lung cancer tissues determined by cDNA macroarray. Oncol Rep. 2002;9(July–August (4)):723–728
  105. Staunton JE, Slonim DK, Coller HA, et al. Chemosensitivity prediction by transcriptional profiling. Proc Natl Acad Sci USA. 2001;98(September 11 (19)):10787–10792
  106. Zembutsu H, Ohnishi Y, Tsunoda T, et al. Genome-wide cDNA microarray screening to correlate gene expression profiles with sensitivity of 85 human cancer xenografts to anticancer drugs. Cancer Res. 2002;62(January 15 (2)):518–527
  107. Dan S, Tsunoda T, Kitahara O, et al. An integrated database of chemosensitivity to 55 anticancer drugs and gene expression profiles of 39 human cancer cell lines. Cancer Res. 2002;62(February 15 (4)):1139–1147
  108. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med. 2008;359(September 25 (13)):1367–1380
  109. Chang BD, Swift ME, Shen M, et al. Molecular determinants of terminal growth arrest induced in tumor cells by a chemotherapeutic agent. Proc Natl Acad Sci USA. 2002;99(January 8 (1)):389–394

PII: S1040-8428(09)00200-5

doi: 10.1016/j.critrevonc.2009.10.002

Critical Reviews in Oncology / Hematology
Volume 75, Issue 2 , Pages 94-109 , August 2010

Article Tools

* Image Usage & Resolution