Progress and applications of mouse models for human lung cancer

European Respiratory Journal

Volumn 35, Issue 2, 2010, Pages 426-443

  De Seranno, S ^a   Meuwissen, R ^a  

^a INSERM   (France)

Author keywords

Lung cancer; Mouse models; Nonsmall cell lung cancer; Small cell lung cancer

Indexed keywords

1 (1 CYANO 1 METHYLETHYL) 3 METHYL 8 (3 QUINOLINYL)IMIDAZO[4,5 C]QUINOLIN 2(1H,3H) ONE; 4 [3 CHLORO 4 (2 PYRIDINYLMETHOXY)ANILINO] 3 CYANO 6 (4 DIMETHYLAMINOCROTONAMIDO) 7 ETHOXYQUINOLINE; 5 (4 BROMO 2 CHLOROANILINO) 4 FLUORO 1 METHYL 1H BENZIMIDAZOLE 6 CARBOHYDROXAMIC ACID 2 HYDROXYETHYL ESTER; B RAF KINASE; CETUXIMAB; CISPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; INDOMETACIN; K RAS PROTEIN; METOCLOPRAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; RETINOBLASTOMA PROTEIN;

ARTICLE; CANCER CLASSIFICATION; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER RESEARCH; CANCER STEM CELL; CARCINOGENESIS; DISEASE MODEL; DNA MODIFICATION; EXPERIMENTAL MOUSE; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; METASTASIS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; TRANSGENE; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE;

ALLELES; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; LUNG NEOPLASMS; MEDICAL ONCOLOGY; MICE; MICE, TRANSGENIC; MODELS, GENETIC; SMALL CELL LUNG CARCINOMA; STEM CELLS;

EID: 76149106864     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00124709     Document Type: Article

References (151)

1. Wakamatsu N, Devereux TR, Hong HH, et al. Overview of the molecular carcinogenesis of mouse lung tumor models of human lung cancer. Toxicol Pathol 2007; 35: 75-80.
2. Shimkin MB, Stoner GD. Lung tumors in mice: application to carcinogenesis bioassay. Adv Cancer Res 1975; 21: 1-58.
3. Pfeifer GP, Denissenko MF, Olivier M, et al. Tobacco smoke carcinogens, DNA damage and p53 mutations in smokingassociated cancers. Oncogene 2002; 21: 7435-7451.
4. Witschi H. A/J mouse as a model for lung tumorigenesis caused by tobacco smoke: strengths and weaknesses. Exp Lung Res 2005; 31: 3-18.
5. Hutt JA, Vuillemenot BR, Barr EB, et al. Life-span inhalation exposure to mainstream cigarette smoke induces lung cancer in B6C3F1 mice through genetic and epigenetic pathways. Carcinogenesis 2005; 26: 1999-2009.
6. Sato M, Shames DS, Gazdar AF, et al. A translational view of the molecular pathogenesis of lung cancer. J Thorac Oncol 2007; 2: 327-343.
7. Malkinson AM. Primary lung tumors in mice as an aid for understanding, preventing, and treating human adenocarcinoma of the lung. Lung Cancer 2001; 32: 265-279.
8. You M, Wang Y, Nash B, et al. K-rasmutations in benzotrichlorideinduced lung tumors of A/J mice. Carcinogenesis 1993; 14: 1247-1249.
9. Chen B, Johanson L, Wiest JS, et al. The second intron of the K-ras gene contains regulatory elements associated with mouse lung tumor susceptibility. Proc Natl Acad Sci USA 1994; 91: 1589-1593.
10. DeMayo FJ, Finegold MJ, Hansen TN, et al. Expression of SV40 T antigen under control of rabbit uteroglobin promoter in transgenic mice. Am J Physiol 1991; 261: L70-L76.
11. Sandmoller A, Halter R, Gomez-La-Hoz E, et al. The uteroglobin promoter targets expression of the SV40 T antigen to a variety of secretory epithelial cells in transgenic mice. Oncogene 1994; 9: 2805-2815.
12. Wikenheiser KA, Clark JC, Linnoila RI, et al. Simian virus 40 large T antigen directed by transcriptional elements of the human surfactant protein C gene produces pulmonary adenocarcinomas in transgenic mice. Cancer Res 1992; 52: 5342-5352.
13. Wikenheiser KA, Whitsett JA. Tumor progression and cellular differentiation of pulmonary adenocarcinomas in SV40 large T antigen transgenic mice. Am J Respir Cell Mol Biol 1997; 16: 713-723.
14. Geick A, Redecker P, Ehrhardt A, et al. Uteroglobin promotertargeted c-MYC expression in transgenic mice cause hyperplasia of Clara cells and malignant transformation of T-lymphoblasts and tubular epithelial cells. Transgenic Res 2001; 10: 501-511.
15. Sekido Y, Fong KM, Minna JD. Molecular genetics of lung cancer. Annu Rev Med 2003; 54: 73-87.
16. Jacks T, Fazeli A, Schmitt EM, et al. Effects of an Rb mutation in the mouse. Nature 1992; 359: 295-300.
17. Meuwissen R, Berns A. Mouse models for human lung cancer. Genes Dev 2005; 19: 643-664.
18. Olive KP, Tuveson DA, Ruhe ZC, et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004; 119: 847-860.
19. Lang GA, Iwakuma T, Suh YA, et al. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 2004; 119: 861-872.
20. Smith AJ, Xian J, Richardson M, et al. Cre-loxP chromosome engineering of a targeted deletion in the mouse corresponding to the 3p21.3 region of homozygous loss in human tumours. Oncogene 2002; 21: 4521-4529.
21. Tommasi S, Dammann R, Zhang Z, et al. Tumor susceptibility of Rassf1a knockout mice. Cancer Res 2005; 65: 92-98.
22. Zanesi N, Mancini R, Sevignani C, et al. Lung cancer susceptibility in Fhit-deficient mice is increased by Vhl haploinsufficiency. Cancer Res 2005; 65: 6576-6582.
23. Johnson L, Mercer K, Greenbaum D, et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001; 410: 1111-1116.
24. Jonkers J, Berns A. Conditional mouse models of sporadic cancer. Nat Rev Cancer 2002; 2: 251-265.
25. Lewandoski M. Conditional control of gene expression in the mouse. Nat Rev Genet 2001; 2: 743-755.
26. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 1992; 89: 5547-5551.
27. Perl AK, Tichelaar JW, Whitsett JA. Conditional gene expression in the respiratory epithelium of the mouse. Transgenic Res 2002; 11: 21-29.
28. Tichelaar JW, Lu W, Whitsett JA. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 2000; 275: 11858-11864.
29. Fisher GH, Wellen SL, Klimstra D, et al. Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev 2001; 15: 3249-3262.
30. Gu H, Zou YR, Rajewsky K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 1993; 73: 1155-1164.
31. Meuwissen R, Linn SC, van der Vaulk M, et al. Mouse model for lung tumorigenesis through Cre/lox controlled sporadic activation of the K-Ras oncogene. Oncogene 2001; 20: 6551-6558.
32. Frese KK, Tuveson DA. Maximizing mouse cancer models. Nat Rev Cancer 2007; 7: 654-658.
33. Jackson EL, Willis N, Mercer K, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001; 15: 3243-3248.
34. Guerra C, Mijimolle N, Dhawahir A, et al. Tumor induction by an endogenous K-ras oncogene is highly dependent on cellular context. Cancer Cell 2003; 4: 111-120.
35. Sweet-Cordero A, Mukherjee S, Subramanian A, et al. An oncogenic KRAS2 expression signature identified by crossspecies gene-expression analysis. Nat Genet 2005; 37: 48-55.
36. Stearman RS, Dwyer-Nield L, Zerbe L, et al. Analysis of orthologous gene expression between human pulmonary adenocarcinoma and a carcinogen-induced murine model. Am J Pathol 2005; 167: 1763-1775.
37. Ji H, Houghton AM, Mariani TJ, et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 2006; 25: 2105-2112.
38. Floyd HS, Farnsworth CL, Kock ND, et al. Conditional expression of the mutant Ki-rasG12C allele results in formation of benign lung adenomas: development of a novel mouse lung tumor model. Carcinogenesis 2005; 26: 2196-2206.
39. You M, Candrian U, Maronpot RR, et al. Activation of the Ki-ras protooncogene in spontaneously occurring and chemically induced lung tumors of the strain A mouse. Proc Natl Acad Sci USA 1989; 86: 3070-3074.
40. Omer CA, Kohl NE. CA1A2X-competitive inhibitors of farnesyltransferase as anti-cancer agents. Trends Pharmacol Sci 1997; 18: 437-444.
41. Hancock JF. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 2003; 4: 373-384.
42. To MD, Wong CE, Karnezis AN, et al. Kras regulatory elements and exon 4A determine mutation specificity in lung cancer. Nat Genet 2008; 40: 1240-1244.
43. Berns A. Kras and Hras - what is the difference? Nat Genet 2008; 40: 1149-1150.
44. Zhang Z, Wang Y, Vikis HG, et al. Wildtype Kras2 can inhibit lung carcinogenesis in mice. Nat Genet 2001; 29: 25-33.
45. Wang Y, Zhang Z, Lubet RA, et al. A mouse model for tumor progression of lung cancer in ras and p53 transgenic mice. Oncogene 2006; 25: 1277-1280.
46. Ji H, Wang Z, Perera SA, et al. Mutations in BRAF and KRAS converge on activation of the mitogen-activated protein kinase pathway in lung cancer mouse models. Cancer Res 2007; 67: 4933-4939.
47. Davies H, Bignell GR, Cox C, et al. Mutations of the BRAF gene in human cancer. Nature 2002; 417: 949-954.
48. Shigematsu H, Gazdar AF. Somatic mutations of epidermal growth factor receptor signaling pathway in lung cancers. Int J Cancer 2006; 118: 257-262.
49. Dankort D, Filenova E, Collado M, et al. A new mouse model to explore the initiation, progression, and therapy of BRAFV600Einduced lung tumors. Genes Dev 2007; 21: 379-384.
50. Shaw AT, Meissner A, Dowdle JA, et al. Sprouty-2 regulates oncogenic K-ras in lung development and tumorigenesis. Genes Dev 2007; 21: 694-707.
51. Kissil JL, Walmsley MJ, Hanlon L, et al. Requirement for Rac1 in a K-ras induced lung cancer in the mouse. Cancer Res 2007; 67: 8089-8094.
52. Samuels Y, Velculescu VE. Oncogenic mutations of PIK3CA in human cancers. Cell Cycle 2004; 3: 1221-1224.
53. Angulo B, Suarez-Gauthier A, Lopez-Rios F, et al. Expression signatures in lung cancer reveal a profile for EGFR-mutant tumours and identify selective PIK3CA overexpression by gene amplification. J Pathol 2008; 214: 347-356.
54. Engelman JA, Chen L, Tan X, et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat Med 2008; 30: 30.
55. Gupta S, Ramjaun AR, Haiko P, et al. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 2007; 129: 957-968.
56. Jakowlew SB. Transforming growth factor-beta in cancer and metastasis. Cancer Metastasis Rev 2006; 25: 435-457.
57. Sun L. Tumor-suppressive and promoting function of transforming growth factor beta. Front Biosci 2004; 9: 1925-1935.
58. Pandey J, Umphress SM, Kang Y, et al. Modulation of tumor induction and progression of oncogenic K-ras-positive tumors in the presence of TGF-b1 haploinsufficiency. Carcinogenesis 2007; 28: 2589-2596.
59. 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.
60. Ji H, Li D, Chen L, et al. The impact of human EGFR kinase domain mutations on lung tumorigenesis and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 2006; 9: 485-495.
61. Politi K, Zakowski MF, Fan PD, et al. Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to downregulation of the receptors. Genes Dev 2006; 20: 1496-1510.
62. Ji H, Zhao X, Yuza Y, et al. Epidermal growth factor receptor variant III mutations in lung tumorigenesis and sensitivity to tyrosine kinase inhibitors. Proc Natl Acad Sci USA 2006; 103: 7817-7822.
63. Yanagi S, Kishimoto H, Kawahara K, et al. Pten controls lung morphogenesis, bronchioalveolar stem cells, and onset of lung adenocarcinomas in mice. J Clin Invest 2007; 117: 2929-2940.
64. Iwanaga K, Yang Y, Raso MG, et al. Pten inactivation accelerates oncogenic K-ras-initiated tumorigenesis in a mouse model of lung cancer. Cancer Res 2008; 68: 1119-1127.
65. Sanchez-Cespedes M. A role for LKB1 gene in human cancer beyond the Peutz-Jeghers syndrome. Oncogene 2007; 26: 7825-7832.
66. Giardiello FM, Brensinger JD, Tersmette AC, et al. Very high risk of cancer in familial Peutz-Jeghers syndrome. Gastroenterology 2000; 119: 1447-1453.
67. Hearle N, Schumacher V, Menko FH, et al. Frequency and spectrum of cancers in the Peutz-Jeghers syndrome. Clin Cancer Res 2006; 12: 3209-3215.
68. Sanchez-Cespedes M, Parrella P, Esteller M, et al. Inactivation of LKB1/STK11 is a common event in adenocarcinomas of the lung. Cancer Res 2002; 62: 3659-3662.
69. Matsumoto S, Iwakawa R, Takahashi K, et al. Prevalence and specificity of LKB1 genetic alterations in lung cancers. Oncogene 2007; 26: 5911-5918.
70. Ji H, Ramsey MR, Hayes DN, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature 2007; 448: 807-810.
71. Shah U, Sharpless NE, Hayes DN. LKB1 and lung cancer: more than the usual suspects. Cancer Res 2008; 68: 3562-3565.
72. Ghaffar H, Sahin F, Sanchez-Cepedes M, et al. LKB1 protein expression in the evolution of glandular neoplasia of the lung. Clin Cancer Res 2003; 9: 2998-3003.
73. Hayashita Y, Osada H, Tatematsu Y, et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628-9632.
74. Kumar MS, Lu J, Mercer KL, et al. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007; 39: 673-677.
75. Johnson SM, Grosshans H, Shingara J, et al. RAS is regulated by the let-7 microRNA family. Cell 2005; 120: 635-647.
76. Esquela-Kerscher A, Trang P, Wiggins JF, et al. The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle 2008; 7: 759-764.
77. Kumar MS, Erkeland SJ, Pester RE, et al. Suppression of nonsmall cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci USA 2008; 105: 3903-3908.
78. Meuwissen R, Linn SC, Linnoila RI, et al. Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 2003; 4: 181-189.
79. Brambilla E, Lantuejoul S, Sturm N. Divergent differentiation in neuroendocrine lung tumors. Semin Diagn Pathol 2000; 17: 138-148.
80. Wistuba II, Gazdar AF. Characteristic genetic alterations in lung cancer. Methods Mol Med 2003; 74: 3-28.
81. Ho VM, Schaffer BE, Karnezis AN, et al. The retinoblastoma gene Rb and its family member p130 suppress lung adenocarcinoma induced by oncogenic K-Ras. Oncogene 2009; 28: 1393-1399.
82. Linnoila RI, Zhao B, DeMayo JL, et al. Constitutive achaete-scute homologue-1 promotes airway dysplasia and lung neuroendocrine tumors in transgenic mice. Cancer Res 2000; 60: 4005-4009.
83. Linnoila RI, Piantadosi S, Ruckdeschel JC. Impact of neuroendocrine differentiation in non-small cell lung cancer. The LCSG experience. Chest 1994; 106: Suppl. 6, 367S-371S.
84. Pei XH, Bai F, Smith MD, et al. p18Ink4c collaborates with Men1 to constrain lung stem cell expansion and suppress non-smallcell lung cancers. Cancer Res 2007; 67: 3162-3170.
85. Wistuba II, Mao L, Gazdar AF. Smoking molecular damage in bronchial epithelium. Oncogene 2002; 21: 7298-7306.
86. Jetten AM, Nervi C, Vollberg TM. Control of squamous differentiation in tracheobronchial and epidermal epithelial cells: role of retinoids. J Natl Cancer Inst Monogr 1992; 93-100.
87. Nettesheim P, Hammons AS. Induction of squamous cell carcinoma in the respiratory tract of mice. J Natl Cancer Inst 1971; 47: 697-701.
88. Rehm S, Lijinsky W, Singh G, et al. Mouse bronchiolar cell carcinogenesis. Histologic characterization and expression of Clara cell antigen in lesions induced by N-nitrosobis-(2-chloroethyl) ureas. Am J Pathol 1991; 139: 413-422.
89. Wang Y, Zhang Z, Yan Y, et al. A chemically induced model for squamous cell carcinoma of the lung in mice: histopathology and strain susceptibility. Cancer Res 2004; 64: 1647-1654.
90. Dakir EL, Feigenbaum L, Linnoila RI. Constitutive expression of human keratin 14 gene in mouse lung induces premalignant lesions and squamous differentiation. Carcinogenesis 2008; 29: 2377-2384.
91. Calbo J, Meuwissen R, van Montfort E, et al. Genotypephenotype relationships in a mouse model for human smallcell lung cancer. Cold Spring Harb Symp Quant Biol 2005; 70: 225-232.
92. Witschi H. The complexities of an apparently simple lung tumor model: The A/J mouse. Exp Toxicol Pathol 2005; 57: Suppl. 1, 171-181.
93. Belinsky SA, Stefanski SA, Anderson MW. The A/J mouse lung as a model for developing new chemointervention strategies. Cancer Res 1993; 53: 410-416.
94. Chung EL. Chemoprevention of lung cancer by isothiocyanates and their conjugates in A/J mouse. Exp Lung Res 2001; 27: 319-330.
95. You M, Bergman G. Preclinical and clinical models of lung cancer chemoprevention. Hematol Oncol Clin North Am 1998; 12: 1037-1053.
96. Wang Y, Zhang Z, Kastens E, et al. Mice with alterations in both p53 and Ink4a/Arf display a striking increase in lung tumor multiplicity and progression: differential chemopreventive effect of budesonide in wild-type and mutant A/J mice. Cancer Res 2003; 63: 4389-4395.
97. Lu Y, Yao R, Yan Y, et al. A gene expression signature that can predict green tea exposure and chemopreventive efficacy of lung cancer in mice. Cancer Res 2006; 66: 1956-1963.
98. Yan Y, Lu Y, Wang M, et al. Effect of an epidermal growth factor receptor inhibitor in mouse models of lung cancer. Mol Cancer Res 2006; 4: 971-981.
99. Omer CA, Chen Z, Diehl RE, et al. Mouse mammary tumor virus-Ki-rasB transgenic mice develop mammary carcinomas that can be growth-inhibited by a farnesyl:protein transferase inhibitor. Cancer Res 2000; 60: 2680-2688.
100. Mahgoub N, Taylor BR, Gratiot M, et al. In vitro and in vivo effects of a farnesyltransferase inhibitor on Nf1-deficient hematopoietic cells. Blood 1999; 94: 2469-2476.
101. Hadjantonakis AK, Dickinson ME, Fraser SE, et al. Technicolour transgenics: imaging tools for functional genomics in the mouse. Nature Rev Genet 2003; 4: 613-625.
102. Contag CH, Jenkins D, Contag PR, et al. Use of reporter genes for optical measurements of neoplastic disease in vivo. Neoplasia 2000; 2: 41-52.
103. Lyons SK, Meuwissen R, Krimpenfort P, et al. The generation of a conditional reporter that enables bioluminescence imaging of Cre/loxP-dependent tumorigenesis in mice. Cancer Res 2003; 63: 7042-7046.
104. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
105. Carney DN, Gazdar AF, Bunn PA Jr, et al. Demonstration of the stem cell nature of clonogenic tumor cells from lung cancer patients. Stem cells 1982; 1: 149-164.
106. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
107. Weissman IL, Anderson DJ, Gage F. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol 2001; 17: 387-403.
108. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 2003; 3: 895-902.
109. Schiller JH. Current standards of care in small-cell and nonsmall-cell lung cancer. Oncology 2001; 61: Suppl. 1, 3-13.
110. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
111. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
112. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988.
113. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
114. Shipitsin M, Polyak K. The cancer stem cell hypothesis: in search of definitions, markers, and relevance. Lab Invest 2008; 88: 459-463.
115. Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene 2004; 23: 7274-7282.
116. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8: 755-768.
117. Adams JM, Strasser A. Is tumor growth sustained by rare cancer stem cells or dominant clones? Cancer Res 2008; 68: 4018-4021.
118. Quintana E, Shackleton M, Sabel MS, et al. Efficient tumour formation by single human melanoma cells. Nature 2008; 456: 593-598.
119. Stripp BR, Reynolds SD. Maintenance and repair of the bronchiolar epithelium. Proc Am Thorac Soc 2008; 5: 328-333.
120. Stripp BR. Hierarchical organization of lung progenitor cells: is there an adult lung tissue stem cell? Proc Am Thorac Soc 2008; 5: 695-698.
121. Evans MJ, Johnson LV, Stephens RJ, et al. Cell renewal in the lungs of rats exposed to low levels of ozone. Exp Mol Pathol 1976; 24: 70-83.
122. Reynolds SD, Giangreco A, Power JH, et al. Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am J Pathol 2000; 156: 269-278.
123. Giangreco A, Reynolds SD, Stripp BR. Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am J Pathol 2002; 161: 173-182.
124. Hong KU, Reynolds SD, Giangreco A, et al. Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 2001; 24: 671-681.
125. Hong KU, Reynolds SD, Watkins S, et al. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 2004; 164: 577-588.
126. Giangreco A, Shen H, Reynolds SD, et al. Molecular phenotype of airway side population cells. Am J Physiol Lung Cell Mol Physiol 2004; 286: L624-L630.
127. Reynolds SD, Hong KU, Giangreco A, et al. Conditional clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells. Am J Physiol Lung Cell Mol Physiol 2000; 278: L1256-L1263.
128. Engelhardt JF. Stem cell niches in the mouse airway. Am J Respir Cell Mol Biol 2001; 24: 649-652.
129. Kim CF, Jackson EL, Woolfenden AE, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005; 121: 823-835.
130. Khoor A, Stahlman MT, Gray ME, et al. Temporal-spatial distribution of SP-B and SP-C proteins and mRNAs in developing respiratory epithelium of human lung. J Histochem Cytochem 1994; 42: 1187-1199.
131. Kim CF. Paving the road for lung stem cell biology: bronchioalveolar stem cells and other putative distal lung stem cells. Am J Physiol Lung Cell Mol Physiol 2007; 293: L1092-L1098.
132. Ivanova NB, Dimos JT, Schaniel C, et al. A stem cell molecular signature. Science 2002; 298: 601-604.
133. McQualter JL, Brouard N, Williams B, et al. Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the Sca-1 positive cell fraction. Stem cells 2008; 11: 11.
134. Teisanu RM, Lagasse E, Whitesides JF, et al. Prospective isolation of bronchiolar stem cells based upon immunophenotypic and autofluorescence characteristics. Stem cells 2008; 4: 4.
135. Ling TY, Kuo MD, Li CL, et al. Identification of pulmonary Oct-4+ stem/progenitor cells and demonstration of their susceptibility to SARS coronavirus (SARS-CoV) infection in vitro. Proc Natl Acad Sci USA 2006; 103: 9530-9535.
136. Peacock CD, Watkins DN. Cancer stem cells and the ontogeny of lung cancer. J Clin Oncol 2008; 26: 2883-2889.
137. Eramo A, Lotti F, Sette G, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008; 15: 504-514.
138. Mizrak D, Brittan M, Alison M. CD133: molecule of the moment. J Pathol 2008; 214: 3-9.
139. Ventura JJ, Tenbaum S, Perdiguero E, et al. p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat Genet 2007; 39: 750-758.
140. Yang Y, Iwanaga K, Raso MG, et al. Phosphatidylinositol 3-kinase mediates bronchioalveolar stem cell expansion in mouse models of oncogenic K-ras-induced lung cancer. PLoS ONE 2008; 3: e2220.
141. Besson A, Hwang HC, Cicero S, et al. Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype. Genes Dev 2007; 21: 1731-1746.
142. Dovey JS, Zacharek SJ, Kim CF, et al. Bmi1 is critical for lung tumorigenesis and bronchioalveolar stem cell expansion. Proc Natl Acad Sci USA 2008; 105: 11857-11862.
143. Carraresi L, Tripodi SA, Mulder LC, et al. Thymic hyperplasia and lung carcinomas in a line of mice transgenic for keratin 5-driven HPV16 E6/E7 oncogenes. Oncogene 2001; 20: 8148-8153.
144. Bottinger EP, Jakubczak JL, Haines DC, et al. Transgenic mice overexpressing a dominant-negative mutant type II transforming growth factor beta receptor show enhanced tumorigenesis in the mammary gland and lung in response to the carcinogen 7,12-dimethylbenz-[a]-anthracene. Cancer Res 1997; 57: 5564-5570.
145. Berard J, Gaboury L, Landers M, et al. Hyperplasia and tumours in lung, breast and other tissues in mice carrying a RAR beta 4-like transgene. EMBO J 1994; 13: 5570-5580.
146. Linnoila RI, Sahu A, Miki M, et al. Morphometric analysis of CC10-hASH1 transgenic mouse lung: a model for bronchiolization of alveoli and neuroendocrine carcinoma. Exp Lung Res 2000; 26: 595-615.
147. Ehrhardt A, Bartels T, Geick A, et al. Development of pulmonary bronchiolo-alveolar adenocarcinomas in transgenic mice overexpressing murine c-myc and epidermal growth factor in alveolar type II pneumocytes. Br J Cancer 2001; 84: 813-818.
148. Kerkhoff E, Fedorov LM, Siefken R, et al. Lung-targeted expression of the c-Raf-1 kinase in transgenic mice exposes a novel oncogenic character of the wild-type protein. Cell Growth Differ 2000; 11: 185-190.
149. Berard J, Laboune F, Mukuna M, et al. Lung tumors in mice expressing an antisense RARbeta2 transgene. FASEB J 1996; 10: 1091-1097.
150. Sunday ME, Haley KJ, Sikorski K, et al. Calcitonin driven v-Haras induces multilineage pulmonary epithelial hyperplasias and neoplasms. Oncogene 1999; 18: 4336-4347.
151. Jackson EL, Olive KP, Tuveson DA, et al. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res 2005; 65: 10280-10288.