Evolving concepts in lung carcinogenesis

Seminars in Respiratory and Critical Care Medicine

Volumn 32, Issue 1, 2011, Pages 32-43

  Gomperts, Brigitte N ^a,b   Spira, Avrum ^c   Massion, Pierre P ^d,e   Walser, Tonya C ^a   Wistuba, Ignacio I ^f   Minna, John D ^g   Dubinett, Steven M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MATTEL CHILDREN S HOSPITAL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VANDERBILT INGRAM CANCER CENTER   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^g UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

epigenomics; Field of cancerization; genomics; inflammation; proteomics; stem cells

Indexed keywords

ALDEHYDE DEHYDROGENASE; BIOLOGICAL MARKER; CD133 ANTIGEN; CYCLOOXYGENASE 2; CYTOKERATIN 14; DNA; HISTONE; MICRORNA; TRANSCRIPTION FACTOR SNAIL;

ARTICLE; CANCER STEM CELL; CHROMATIN; DNA METHYLATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENOMICS; HISTONE MODIFICATION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LUNG CARCINOGENESIS; PATHOGENESIS; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEOMICS; RISK FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; TUMOR IMMUNITY;

ANIMALS; ANTICARCINOGENIC AGENTS; EPIGENESIS, GENETIC; EPIGENOMICS; GENE EXPRESSION PROFILING; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFLAMMATION; LUNG NEOPLASMS; MUTATION; NEOPLASTIC STEM CELLS; PROTEOMICS;

EID: 79954591078     PISSN: 10693424     EISSN: 10989048     Source Type: Journal    
DOI: 10.1055/s-0031-1272867     Document Type: Article

References (133)

1. Dakubo G D., Jakupciak J P., Birch-Machin M A., Parr R L. Clinical implications and utility of field cancerization. Cancer Cell Int 2007 7 2
2. Slaughter D P., Southwick H W., Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 1953 6 5 963-968
3. Auerbach O, Hammond E C., Kirman D, Garfinkel L. Effects of cigarette smoking on dogs, II: Pulmonary neoplasms. Arch Environ Health 1970 21 6 754-768
4. Guo M, House M G., Hooker C et al. Promoter hypermethylation of resected bronchial margins: a field defect of changes? Clin Cancer Res 2004 10 15 5131-5136 (Pubitemid 39099787)
5. Franklin W A., Gazdar A F., Haney J et al. Widely dispersed p53 mutation in respiratory epithelium: a novel mechanism for field carcinogenesis. J Clin Invest 1997 100 8 2133-2137 (Pubitemid 27459370)
6. Mao L, Lee J S., Kurie J M. et al. Clonal genetic alterations in the lungs of current and former smokers. J Natl Cancer Inst 1997 89 12 857-862 (Pubitemid 27268450)
7. Steiling K, Ryan J, Brody J S., Spira A. The field of tissue injury in the lung and airway. Cancer Prev Res (Phila) 2008 1 6 396-403
8. Tang X, Shigematsu H, Bekele B N. et al. EGFR tyrosine kinase domain mutations are detected in histologically normal respiratory epithelium in lung cancer patients. Cancer Res 2005 65 17 7568-7572 (Pubitemid 41297226)
9. Wistuba I I., Lam S, Behrens C et al. Molecular damage in the bronchial epithelium of current and former smokers. J Natl Cancer Inst 1997 89 18 1366-1373 (Pubitemid 27418028)
10. Nelson M A., Wymer J, Clements N Jr. Detection of K-ras gene mutations in non-neoplastic lung tissue and lung cancers. Cancer Lett 1996 103 1 115-121 (Pubitemid 26125172)
11. Powell C A., Klares S, O'Connor G, Brody J S. Loss of heterozygosity in epithelial cells obtained by bronchial brushing: clinical utility in lung cancer. Clin Cancer Res 1999 5 8 2025-2034 (Pubitemid 29399254)
12. Tang X, Varella-Garcia M, Xavier A C. et al. Epidermal growth factor receptor abnormalities in the pathogenesis and progression of lung adenocarcinomas. Cancer Prev Res (Phila) 2008 1 3 192-200
13. Hackett N R., Heguy A, Harvey B G. et al. Variability of antioxidant-related gene expression in the airway epithelium of cigarette smokers. Am J Respir Cell Mol Biol 2003 29 3 Pt 1 331-343 (Pubitemid 37093991)
14. Spira A, Beane J, Shah V et al. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc Natl Acad Sci U S A 2004 101 27 10143-10148 (Pubitemid 38891209)
15. Spira A, Beane J E., Shah V et al. Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat Med 2007 13 3 361-366 (Pubitemid 46376687)
16. Beane J, Sebastiani P, Whitfield T H. et al. A prediction model for lung cancer diagnosis that integrates genomic and clinical features. Cancer Prev Res (Phila) 2008 1 1 56-64
17. Bhutani M, Pathak A K., Fan Y H. et al. Oral epithelium as a surrogate tissue for assessing smoking-induced molecular alterations in the lungs. Cancer Prev Res (Phila) 2008 1 1 39-44
18. Sridhar S, Schembri F, Zeskind J et al. Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC Genomics 2008 9 259
19. Miyazu Y M., Miyazawa T, Hiyama K et al. Telomerase expression in noncancerous bronchial epithelia is a possible marker of early development of lung cancer. Cancer Res 2005 65 21 9623-9627 (Pubitemid 41541435)
20. Ocak S, Sos M L., Thomas R K., Massion P P. High-throughput molecular analysis in lung cancer: insights into biology and potential clinical applications. Eur Respir J 2009 34 2 489-506
21. Esteller M, Fraga M F., Paz M F. et al. Cancer epigenetics and methylation. Science 2002 297 1807-1808 discussion 1807-1808
22. Ahrendt S A., Chow J T., Xu L H. et al. Molecular detection of tumor cells in bronchoalveolar lavage fluid from patients with early stage lung cancer. J Natl Cancer Inst 1999 91 4 332-339 (Pubitemid 29102332)
23. Cheng X, Blumenthal R M. Mammalian DNA methyltransferases: a structural perspective. Structure 2008 16 3 341-350 (Pubitemid 351324115)
24. Métivier R, Gallais R, Tiffoche C et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008 452 7183 45-50 (Pubitemid 351355084)
25. Esteller M, Sanchez-Cespedes M, Rosell R, Sidransky D, Baylin S B., Herman J G. Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients. Cancer Res 1999 59 1 67-70 (Pubitemid 29062958)
26. Belinsky S A., Palmisano W A., Gilliland F D. et al. Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res 2002 62 8 2370-2377 (Pubitemid 34411720)
27. Ng C S., Zhang J, Wan S et al. Tumor p16M is a possible marker of advanced stage in non-small cell lung cancer. J Surg Oncol 2002 79 2 101-106 (Pubitemid 34111935)
28. Palmisano W A., Divine K K., Saccomanno G et al. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res 2000 60 21 5954-5958
29. Brock M V., Hooker C M., Ota-Machida E et al. DNA methylation markers and early recurrence in stage I lung cancer. N Engl J Med 2008 358 11 1118-1128 (Pubitemid 351398486)
30. Zhong S, Fields C R., Su N, Pan Y X., Robertson K D. Pharmacologic inhibition of epigenetic modifications, coupled with gene expression profiling, reveals novel targets of aberrant DNA methylation and histone deacetylation in lung cancer. Oncogene 2007 26 18 2621-2634 (Pubitemid 46632003)
31. Rauch T A., Zhong X, Wu X et al. High-resolution mapping of DNA hypermethylation and hypomethylation in lung cancer. Proc Natl Acad Sci U S A 2008 105 1 252-257
32. Brena R M., Morrison C, Liyanarachchi S et al. Aberrant DNA methylation of OLIG1, a novel prognostic factor in non-small cell lung cancer. PLoS Med 2007 4 3 e108
33. Brehm A, Miska E A., McCance D J., Reid J L., Bannister A J., Kouzarides T. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 1998 391 6667 597-601 (Pubitemid 28157603)
34. Mukhopadhyay N K., Weisberg E, Gilchrist D, Bueno R, Sugarbaker D J., Jaklitsch M T. Effectiveness of trichostatin A as a potential candidate for anticancer therapy in non-small-cell lung cancer. Ann Thorac Surg 2006 81 3 1034-1042 (Pubitemid 43247683)
35. Kim S M., Kee H J., Eom G H. et al. Characterization of a novel WHSC1-associated SET domain protein with H3K4 and H3K27 methyltransferase activity. Biochem Biophys Res Commun 2006 345 1 318-323
36. Loprevite M, Tiseo M, Grossi F et al. In vitro study of CI-994, a histone deacetylase inhibitor, in non-small cell lung cancer cell lines. Oncol Res 2005 15 1 39-48 (Pubitemid 40470531)
37. Kouzarides T. Chromatin modifications and their function. Cell 2007 128 4 693-705 (Pubitemid 46273577)
38. Ambros V. MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 2003 113 6 673-676 (Pubitemid 36724931)
39. Yanaihara N, Caplen N, Bowman E et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006 9 3 189-198 (Pubitemid 43357945)
40. Takamizawa J, Konishi H, Yanagisawa K et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004 64 11 3753-3756 (Pubitemid 38697282)
41. Johnson S M., Grosshans H, Shingara J et al. RAS is regulated by the let-7 microRNA family. Cell 2005 120 5 635-647 (Pubitemid 40343076)
42. Kumar M S., Erkeland S J., Pester R E. et al. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci U S A 2008 105 10 3903-3908 (Pubitemid 351723497)
43. Trang P, Medina P P., Wiggins J F. et al. Regression of murine lung tumors by the let-7 microRNA. Oncogene 2010 29 11 1580-1587
44. Ender C, Krek A, Friedländer M R. et al. A human snoRNA with microRNA-like functions. Mol Cell 2008 32 4 519-528
45. Eiring A M., Harb J G., Neviani P et al. miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 2010 140 5 652-665
46. Agulló-Ortuño M T., López-Ríos F, Paz-Ares L. Lung cancer genomic signatures. J Thorac Oncol 2010 5 10 1673-1691
47. Boland C R., Thibodeau S N., Hamilton S R. et al. A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 1998 58 22 5248-5257 (Pubitemid 28521189)
48. Pinkel D, Segraves R, Sudar D et al. High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 1998 20 2 207-211 (Pubitemid 28455458)
49. Pollack J R., Perou C M., Alizadeh A A. et al. Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nat Genet 1999 23 1 41-46 (Pubitemid 29418785)
50. Ishkanian A S., Malloff C A., Watson S K. et al. A tiling resolution DNA microarray with complete coverage of the human genome. Nat Genet 2004 36 3 299-303 (Pubitemid 38282757)
51. Imoto I, Yuki Y, Sonoda I et al. Identification of ZASC1 encoding a Krüppel-like zinc finger protein as a novel target for 3q26 amplification in esophageal squamous cell carcinomas. Cancer Res 2003 63 18 5691-5696 (Pubitemid 37187462)
52. Singh B, Gogineni S K., Sacks P G. et al. Molecular cytogenetic characterization of head and neck squamous cell carcinoma and refinement of 3q amplification. Cancer Res 2001 61 11 4506-4513 (Pubitemid 32685781)
53. Levin N A., Brzoska P M., Warnock M L., Gray J W., Christman M F. Identification of novel regions of altered DNA copy number in small cell lung tumors. Genes Chromosomes Cancer 1995 13 3 175-185
54. Amos C I., Wu X, Broderick P et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet 2008 40 5 616-622 (Pubitemid 351601203)
55. Hung R J., McKay J D., Gaborieau V et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 2008 452 7187 633-637 (Pubitemid 351483367)
56. Thorgeirsson T E., Geller F, Sulem P et al. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 2008 452 7187 638-642 (Pubitemid 351483366)
57. Gustafson A M., Soldi R, Anderlind C et al. Airway PI3K pathway activation is an early and reversible event in lung cancer development. Sci Transl Med 2010 2 26 26ra25
58. Yanagisawa K, Shyr Y, Xu B J. et al. Proteomic patterns of tumour subsets in non-small-cell lung cancer. Lancet 2003 362 9382 433-439 (Pubitemid 36999706)
59. Rahman S M., Shyr Y, Yildiz P B. et al. Proteomic patterns of preinvasive bronchial lesions. Am J Respir Crit Care Med 2005 172 12 1556-1562 (Pubitemid 43076545)
60. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009 30 7 1073-1081
61. Brody J S., Spira A. State of the art: chronic obstructive pulmonary disease, inflammation, and lung cancer. Proc Am Thorac Soc 2006 3 6 535-537 (Pubitemid 44285546)
62. Smith C J., Perfetti T A., King J A. Perspectives on pulmonary inflammation and lung cancer risk in cigarette smokers. Inhal Toxicol 2006 18 9 667-677
63. Dubinett S M., Sharma S, Huang M, Dohadwala M, Pold M, Mao J T. Cyclooxygenase-2 in lung cancer. Prog Exp Tumor Res 2003 37 138-162 (Pubitemid 36767984)
64. Dohadwala M, Batra R K., Luo J et al. Autocrine/paracrine prostaglandin E2 production by non-small cell lung cancer cells regulates matrix metalloproteinase-2 and CD44 in cyclooxygenase-2-dependent invasion. J Biol Chem 2002 277 52 50828-50833 (Pubitemid 36042248)
65. Lee J M., Mao J T., Krysan K, Dubinett S M. Significance of cyclooxygenase-2 in prognosis, targeted therapy and chemoprevention of NSCLC. Future Oncol 2007 3 2 149-153 (Pubitemid 46592722)
66. Khuri F R., Wu H, Lee J J. et al. Cyclooxygenase-2 overexpression is a marker of poor prognosis in stage I non-small cell lung cancer. Clin Cancer Res 2001 7 4 861-867 (Pubitemid 32708722)
67. Tsubochi H, Sato N, Hiyama M et al. Combined analysis of cyclooxygenase-2 expression with p53 and Ki-67 in nonsmall cell lung cancer. Ann Thorac Surg 2006 82 4 1198-1204 (Pubitemid 44402329)
68. Kim H S., Youm H R., Lee J S., Min K W., Chung J H., Park C S. Correlation between cyclooxygenase-2 and tumor angiogenesis in non-small cell lung cancer. Lung Cancer 2003 42 2 163-170
69. Huang M, Stolina M, Sharma S et al. Non-small cell lung cancer cyclooxygenase-2-dependent regulation of cytokine balance in lymphocytes and macrophages: up-regulation of interleukin 10 and down-regulation of interleukin 12 production. Cancer Res 1998 58 6 1208-1216 (Pubitemid 28183210)
70. Mao J T., Cui X, Reckamp K et al. Chemoprevention strategies with cyclooxygenase-2 inhibitors for lung cancer. Clin Lung Cancer 2005 7 1 30-39 (Pubitemid 41150471)
71. Subbaramaiah K, Altorki N, Chung W J., Mestre J R., Sampat A, Dannenberg A J. Inhibition of cyclooxygenase-2 gene expression by p53. J Biol Chem 1999 274 16 10911-10915
72. Csiki I, Yanagisawa K, Haruki N et al. Thioredoxin-1 modulates transcription of cyclooxygenase-2 via hypoxia-inducible factor-1alpha in non-small cell lung cancer. Cancer Res 2006 66 1 143-150 (Pubitemid 43166019)
73. Cui X, Zhang L, Luo J et al. Unphosphorylated STAT6 contributes to constitutive cyclooxygenase-2 expression in human non-small cell lung cancer. Oncogene 2007 26 29 4253-4260 (Pubitemid 46975804)
74. Heuze-Vourc'h N, Zhu L, Krysan K, Batra R K., Sharma S, Dubinett S M. Abnormal interleukin 10Ralpha expression contributes to the maintenance of elevated cyclooxygenase-2 in non-small cell lung cancer cells. Cancer Res 2003 63 4 766-770 (Pubitemid 36231973)
75. Krysan K, Merchant F H., Zhu L et al. COX-2-dependent stabilization of survivin in non-small cell lung cancer. FASEB J 2004 18 1 206-208
76. Põld M, Krysan K, Põld A et al. Cyclooxygenase-2 modulates the insulin-like growth factor axis in non-small-cell lung cancer. Cancer Res 2004 64 18 6549-6555 (Pubitemid 39297913)
77. Sharma S, Stolina M, Yang S C. et al. Tumor cyclooxygenase 2-dependent suppression of dendritic cell function. Clin Cancer Res 2003 9 3 961-968 (Pubitemid 36323698)
78. Põld M, Zhu L X., Sharma S et al. Cyclooxygenase-2-dependent expression of angiogenic CXC chemokines ENA-78/CXC Ligand (CXCL) 5 and interleukin-8/CXCL8 in human non-small cell lung cancer. Cancer Res 2004 64 5 1853-1860 (Pubitemid 38428711)
79. Dohadwala M, Batra R K., Luo J et al. Autocrine/paracrine prostaglandin E2 production by non-small cell lung cancer cells regulates matrix metalloproteinase-2 and CD44 in cyclooxygenase-2-dependent invasion. J Biol Chem 2002 277 52 50828-50833 (Pubitemid 36042248)
80. Dohadwala M, Yang S-C, Luo J et al. Cyclooxygenase-2-dependent regulation of E-cadherin: prostaglandin E(2) induces transcriptional repressors ZEB1 and snail in non-small cell lung cancer. Cancer Res 2006 66 10 5338-5345 (Pubitemid 43844959)
81. Yang L, Huang Y, Porta R et al. Host and direct antitumor effects and profound reduction in tumor metastasis with selective EP4 receptor antagonism. Cancer Res 2006 66 19 9665-9672 (Pubitemid 44623666)
82. Lee J M., Dedhar S, Kalluri R, Thompson E W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006 172 7 973-981
83. Mani S A., Guo W, Liao M J. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008 133 4 704-715 (Pubitemid 351636299)
84. Krysan K, Lee J M., Dohadwala M et al. Inflammation, epithelial to mesenchymal transition, and epidermal growth factor receptor tyrosine kinase inhibitor resistance. J Thorac Oncol 2008 3 2 107-110 (Pubitemid 351323182)
85. Gotzmann J, Mikula M, Eger A et al. Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. Mutat Res 2004 566 1 9-20 (Pubitemid 38045586)
86. Huber M A., Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005 17 5 548-558 (Pubitemid 41267170)
87. Radisky D C., LaBarge M A. Epithelial-mesenchymal transition and the stem cell phenotype. Cell Stem Cell 2008 2 6 511-512 (Pubitemid 351729219)
88. St John M A., Dohadwala M, Luo J et al. Proinflammatory mediators upregulate snail in head and neck squamous cell carcinoma. Clin Cancer Res 2009 15 19 6018-6027
89. Baratelli F, Lin Y, Zhu L et al. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4 + T cells. J Immunol 2005 175 3 1483-1490 (Pubitemid 41023048)
90. Gavin M A., Rasmussen J P., Fontenot J D. et al. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007 445 7129 771-775 (Pubitemid 46279714)
91. Krysan K, Reckamp K L., Dalwadi H et al. Prostaglandin E2 activates mitogen-activated protein kinase/Erk pathway signaling and cell proliferation in non-small cell lung cancer cells in an epidermal growth factor receptor-independent manner. Cancer Res 2005 65 14 6275-6281 (Pubitemid 40994413)
92. Ailles L E., Weissman I L. Cancer stem cells in solid tumors. Curr Opin Biotechnol 2007 18 5 460-466 (Pubitemid 350116595)
93. Boman B M., Wicha M S. Cancer stem cells: a step toward the cure. J Clin Oncol 2008 26 17 2795-2799
94. Clarke M F., Fuller M. Stem cells and cancer: two faces of eve. Cell 2006 124 6 1111-1115
95. Huntly B J., Gilliland D G. Cancer biology: summing up cancer stem cells. Nature 2005 435 7046 1169-1170 (Pubitemid 40943069)
96. McDonald S A., Graham T A., Schier S, Wright N A., Alison M R. Stem cells and solid cancers. Virchows Arch 2009 455 1 1-13
97. Rosen J M., Jordan C T. The increasing complexity of the cancer stem cell paradigm. Science 2009 324 5935 1670-1673
98. Visvader J E., Lindeman G J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008 8 10 755-768
99. Ward R J., Dirks P B. Cancer stem cells: at the headwaters of tumor development. Annu Rev Pathol 2007 2 175-189 (Pubitemid 46448063)
100. Kim C F., Jackson E L., Woolfenden A E. et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005 121 6 823-835 (Pubitemid 40806415)
101. Curtis S J., Sinkevicius K W., Li D et al. Primary tumor genotype is an important determinant in identification of lung cancer propagating cells. Cell Stem Cell 2010 7 1 127-133
102. Moreb J S. Aldehyde dehydrogenase as a marker for stem cells. Curr Stem Cell Res Ther 2008 3 4 237-246
103. Storms R W., Trujillo A P., Springer J B. et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci U S A 1999 96 16 9118-9123 (Pubitemid 29374717)
104. Carpentino J E., Hynes M J., Appelman H D. et al. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 2009 69 20 8208-8215
105. Chen Y C., Chen Y W., Hsu H S. et al. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 2009 385 3 307-313
106. Huang E H., Hynes M J., Zhang T et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009 69 8 3382-3389
107. Jiang F, Qiu Q, Khanna A et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009 7 3 330-338
108. Eramo A, Lotti F, Sette G et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008 15 3 504-514 (Pubitemid 351267301)
109. Salnikov A V., Gladkich J, Moldenhauer G, Volm M, Mattern J, Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer 2010 126 4 950-958
110. Bertolini G, Roz L, Perego P et al. Highly tumorigenic lung cancer CD133 + cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci U S A 2009 106 38 16281-16286
111. Li F, Zeng H, Ying K. The combination of stem cell markers CD133 and ABCG2 predicts relapse in stage I non-small cell lung carcinomas. Med Oncol 2010 Aug 18. [Epub ahead of print]
112. Engelhardt J F., Schlossberg H, Yankaskas J R., Dudus L. Progenitor cells of the adult human airway involved in submucosal gland development. Development 1995 121 7 2031-2046
113. Hong K U., Reynolds S D., Watkins S, Fuchs E, Stripp B R. In vivo differentiation potential of tracheal basal cells: evidence for multipotent and unipotent subpopulations. Am J Physiol Lung Cell Mol Physiol 2004 286 4 L643-L649 (Pubitemid 38365046)
114. Rock J R., Onaitis M W., Rawlins E L. et al. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci U S A 2009 106 31 12771-12775
115. Schoch K G., Lori A, Burns K A., Eldred T, Olsen J C., Randell S H. A subset of mouse tracheal epithelial basal cells generates large colonies in vitro. Am J Physiol Lung Cell Mol Physiol 2004 286 4 L631-L642 (Pubitemid 38365045)
116. Ooi A T., Mah V, Nickerson D W. et al. Presence of a putative tumor-initiating progenitor cell population predicts poor prognosis in smokers with non-small cell lung cancer. Cancer Res 2010 70 16 6639-6648
117. Sánchez-García I. The crossroads of oncogenesis and metastasis. N Engl J Med 2009 360 3 297-299
118. Mani S A., Guo W, Liao M-J et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008 133 4 704-715 (Pubitemid 351636299)
119. Yu M, Smolen G A., Zhang J et al. A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression. Genes Dev 2009 23 15 1737-1742
120. Wellner U, Schubert J, Burk U C. et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009 11 12 1487-1495
121. Yanagawa J, Walser T C., Zhu L X. et al. Snail promotes CXCR2 ligand-dependent tumor progression in non-small cell lung carcinoma. Clin Cancer Res 2009 15 22 6820-6829
122. Walser T C., Yanagawa J, Luo J et al. Snail-induced and EMT-mediated early lung cancer development: promotion of invasion and expansion of stem cell populations. [abstract] Paper presented at: Proceedings of the Seventh Annual AACR International Conference on Frontiers in Cancer Prevention Research; November 16-19, 2008; Washington, DC
123. Wicha M S., Liu S L., Dontu G. Cancer stem cells: an old ideaa paradigm shift. Cancer Res 2006 66 4 1883-1890 discussion 1895-1896
124. Sun S, Schiller J H., Gazdar A F. Lung cancer in never smokersa different disease. Nat Rev Cancer 2007 7 10 778-790 (Pubitemid 47463669)
125. Fan X, Matsui W, Khaki L et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006 66 15 7445-7452 (Pubitemid 44289197)
126. Farnie G, Clarke R B. Mammary stem cells and breast cancerrole of Notch signalling. Stem Cell Rev 2007 3 2 169-175 (Pubitemid 350129719)
127. Konishi J, Kawaguchi K S., Vo H et al. Gamma-secretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers. Cancer Res 2007 67 17 8051-8057 (Pubitemid 47395139)
128. Westhoff B, Colaluca I N., D'Ario G et al. Alterations of the Notch pathway in lung cancer. Proc Natl Acad Sci U S A 2009 106 52 22293-22298
129. Meuwissen R, Berns A. Mouse models for human lung cancer. Genes Dev 2005 19 6 643-664 (Pubitemid 40395076)
130. Olive K P., Tuveson D A., Ruhe Z C. et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004 119 6 847-860 (Pubitemid 40017690)
131. Hoffman J A., Giraudo E, Singh M et al. Progressive vascular changes in a transgenic mouse model of squamous cell carcinoma. Cancer Cell 2003 4 5 383-391 (Pubitemid 37491099)
132. Sato M, Vaughan M B., Girard L et al. Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res 2006 66 4 2116-2128
133. Vaughan M B., Ramirez R D., Wright W E., Minna J D., Shay J W. A three-dimensional model of differentiation of immortalized human bronchial epithelial cells. Differentiation 2006 74 4 141-148