Lung cancer stem cells: Molecular features and therapeutic targets

Molecular Aspects of Medicine

Volumn 39, Issue , 2014, Pages 50-60

  Singh, Sandeep ^b   Chellappan, Srikumar ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b National Institute of Biomedical Genomics (NIBMG) TB Hospital Building   (India)

Author keywords

Cancer stem cells; Heterogeneity; Molecular targets; NSCLC

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; H RAS PROTEIN; K RAS PROTEIN; NOTCH RECEPTOR; PROTEIN P53; RAS PROTEIN; RETINOBLASTOMA PROTEIN; SONIC HEDGEHOG PROTEIN; SURFACTANT PROTEIN C; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CANCER GROWTH; CANCER STEM CELL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL GROWTH; CELL HETEROGENEITY; CELL PROLIFERATION; CELL RENEWAL; CELLULAR DISTRIBUTION; CLARA CELL; DISEASE ASSOCIATION; GENE EXPRESSION PROFILING; HUMAN; LARGE CELL CARCINOMA; LUNG ADENOCARCINOMA; LUNG CANCER; NEUROSECRETORY CELL; NON SMALL CELL LUNG CANCER; NONHUMAN; NOTCH GENE; PROTEIN DEPLETION; PROTEIN EXPRESSION; SHH GENE; SIGNAL TRANSDUCTION; SMALL CELL LUNG CANCER; SQUAMOUS CELL CARCINOMA; STEM CELL NICHE; WNT GENE; DRUG EFFECTS; DRUG RESISTANCE; LUNG NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY;

DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84906966080     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2013.08.003     Document Type: Review

References (143)

1. M. Alamgeer, V. Ganju, A. Szczepny, P.A. Russell, Z. Prodanovic, B. Kumar, Z. Wainer, T. Brown, M. Schneider-Kolsky, M. Conron, G. Wright, and D.N. Watkins The prognostic significance of aldehyde dehydrogenase 1A1 (ALDH1A1) and CD133 expression in early stage non-small cell lung cancer Thorax 2013
2. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. USA 100 2003 3983 3988
3. M.R. Alison, N.J. Guppy, S.M. Lim, and L.J. Nicholson Finding cancer stem cells: are aldehyde dehydrogenases fit for purpose? J. Pathol. 222 2010 335 344
4. S. Artavanis-Tsakonas, M.D. Rand, and R.J. Lake Notch signaling: cell fate control and signal integration in development Science 284 1999 770 776
5. M.P. Barr, S.G. Gray, A.C. Hoffmann, R.A. Hilger, J. Thomale, J.D. O'Flaherty, D.A. Fennell, D. Richard, J.J. O'Leary, and K.J. O'Byrne Generation and characterisation of cisplatin-resistant non-small cell lung cancer cell lines displaying a stem-like signature PLoS One 8 2013 e54193
6. P.J. Barth, S. Koch, B. Muller, F. Unterstab, P. von Wichert, and R. Moll Proliferation and number of clara cell 10-kDa protein (CC10)-reactive epithelial cells and basal cells in normal, hyperplastic and metaplastic bronchial mucosa Virchows Arch. 437 2000 648 655
7. A.J. Bass, H. Watanabe, C.H. Mermel, S. Yu, S. Perner, R.G. Verhaak, S.Y. Kim, L. Wardwell, P. Tamayo, I. Gat-Viks, A.H. Ramos, M.S. Woo, B.A. Weir, G. Getz, R. Beroukhim, M. O'Kelly, A. Dutt, O. Rozenblatt-Rosen, P. Dziunycz, J. Komisarof, L.R. Chirieac, C.J. Lafargue, V. Scheble, T. Wilbertz, C. Ma, S. Rao, H. Nakagawa, D.B. Stairs, L. Lin, T.J. Giordano, P. Wagner, J.D. Minna, A.F. Gazdar, C.Q. Zhu, M.S. Brose, I. Cecconello Jr UR, S.K. Marie, O. Dahl, R.A. Shivdasani, M.S. Tsao, M.A. Rubin, K.K. Wong, A. Regev, W.C. Hahn, D.G. Beer, A.K. Rustgi, and M. Meyerson SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas Nat. Genet. 41 2009 1238 1242
8. S. Bellusci, Y. Furuta, M.G. Rush, R. Henderson, G. Winnier, and B.L. Hogan Involvement of sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis Development 124 1997 53 63
9. G. Bertolini, L. Roz, P. Perego, M. Tortoreto, E. Fontanella, L. Gatti, G. Pratesi, A. Fabbri, F. Andriani, S. Tinelli, E. Roz, R. Caserini, S. Lo Vullo, T. Camerini, L. Mariani, D. Delia, E. Calabro, U. Pastorino, and G. Sozzi Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment Proc. Natl. Acad. Sci. USA 106 2009 16281 16286
10. S. Bidlingmaier, X. Zhu, and B. Liu The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells J. Mol. Med. (Berl) 86 2008 1025 1032
11. D. Bonnet, and J.E. Dick Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat. Med. 3 1997 730 737
12. D.W. Borthwick, M. Shahbazian, Q.T. Krantz, J.R. Dorin, and S.H. Randell Evidence for stem-cell niches in the tracheal epithelium Am. J. Respir. Cell. Mol. Biol. 24 2001 662 670
13. E.P. Bottinger, J.L. Jakubczak, D.C. Haines, K. Bagnall, and L.M. Wakefield 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. 57 1997 5564 5570
14. J. Calbo, E. van Montfort, N. Proost, E. van Drunen, H.B. Beverloo, R. Meuwissen, and A. Berns A functional role for tumor cell heterogeneity in a mouse model of small cell lung cancer Cancer Cell 19 2011 244 256
15. D.N. Carney, A.F. Gazdar, and J.D. Minna Positive correlation between histological tumor involvement and generation of tumor cell colonies in agarose in specimens taken directly from patients with small-cell carcinoma of the lung Cancer Res. 40 1980 1820 1823
16. D.N. Carney, A.F. Gazdar, P.A. Bunn Jr., and J.G. Guccion Demonstration of the stem cell nature of clonogenic tumor cells from lung cancer patients Stem Cells 1 1982 149 164
17. C.L. Chaffer, I. Brueckmann, C. Scheel, A.J. Kaestli, P.A. Wiggins, L.O. Rodrigues, M. Brooks, F. Reinhardt, Y. Su, K. Polyak, L.M. Arendt, C. Kuperwasser, B. Bierie, and R.A. Weinberg Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state Proc. Natl. Acad. Sci. USA 108 2011 7950 7955
18. C.L. Chaffer, N.D. Marjanovic, T. Lee, G. Bell, C.G. Kleer, F. Reinhardt, A.C. D'Alessio, R.A. Young, and R.A. Weinberg Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity Cell 154 2013 61 74
19. Y.C. Chen, H.S. Hsu, Y.W. Chen, T.H. Tsai, C.K. How, C.Y. Wang, S.C. Hung, Y.L. Chang, M.L. Tsai, Y.Y. Lee, H.H. Ku, and S.H. Chiou Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells PLoS One 3 2008 e2637
20. J. Chen, Y. Li, T.S. Yu, R.M. McKay, D.K. Burns, S.G. Kernie, and L.F. Parada A restricted cell population propagates glioblastoma growth after chemotherapy Nature 488 2012 522 526
21. S.H. Chiou, M.L. Wang, Y.T. Chou, C.J. Chen, C.F. Hong, W.J. Hsieh, H.T. Chang, Y.S. Chen, T.W. Lin, H.S. Hsu, and C.W. Wu Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation Cancer Res. 70 2010 10433 10444
22. J.P. Chute, G.G. Muramoto, J. Whitesides, M. Colvin, R. Safi, N.J. Chao, and D.P. McDonnell Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells Proc. Natl. Acad. Sci. USA 103 2006 11707 11712
23. M.F. Clarke, J.E. Dick, P.B. Dirks, C.J. Eaves, C.H. Jamieson, D.L. Jones, J. Visvader, I.L. Weissman, and G.M. Wahl Cancer stem cells perspectives on current status and future directions: AACR workshop on cancer stem cells Cancer Res. 66 2006 9339 9344
24. H. Clevers Stem cells, asymmetric division and cancer Nat. Genet. 37 2005 1027 1028
25. B.J. Collins, W. Kleeberger, and D.W. Ball Notch in lung development and lung cancer Semin. Cancer Biol. 14 2004 357 364
26. L. Cortes-Dericks, D. Galetta, L. Spaggiari, R.A. Schmid, and G. Karoubi High expression of octamer-binding transcription factor 4A, prominin-1 and aldehyde dehydrogenase strongly indicates involvement in the initiation of lung adenocarcinoma resulting in shorter disease-free intervals Eur. J. Cardiothorac. Surg. 41 2012 e173 e181
27. S.J. Curtis, K.W. Sinkevicius, D. Li, A.N. Lau, R.R. Roach, R. Zamponi, A.E. Woolfenden, D.G. Kirsch, K.K. Wong, and C.F. Kim Primary tumor genotype is an important determinant in identification of lung cancer propagating cells Cell Stem Cell 7 2010 127 133
28. P. Dalerba, R.W. Cho, and M.F. Clarke Cancer stem cells: models and concepts Annu. Rev. Med. 58 2007 267 284
29. T.P. Dang, S. Eichenberger, A. Gonzalez, S. Olson, and D.P. Carbone Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice Oncogene 22 2003 1988 1997
30. V.C. Daniel, C.D. Peacock, and D.N. Watkins Developmental signalling pathways in lung cancer Respirology 11 2006 234 240
31. F.J. DeMayo, M.J. Finegold, T.N. Hansen, L.A. Stanley, B. Smith, and D.W. Bullock Expression of SV40 T antigen under control of rabbit uteroglobin promoter in transgenic mice Am. J. Physiol. 261 1991 L70 L76
32. G. Driessens, B. Beck, A. Caauwe, B.D. Simons, and C. Blanpain Defining the mode of tumour growth by clonal analysis Nature 488 2012 527 530
33. A. Dutt, and K.K. Wong Mouse models of lung cancer Clin. Cancer Res. 12 2006 4396s 4402s
34. A. Eramo, F. Lotti, G. Sette, E. Pilozzi, M. Biffoni, A. Di Virgilio, C. Conticello, L. Ruco, C. Peschle, and R. De Maria Identification and expansion of the tumorigenic lung cancer stem cell population Cell Death Differ. 15 2008 504 514
35. M.J. Evans, L.S. Van Winkle, M.V. Fanucchi, and C.G. Plopper Cellular and molecular characteristics of basal cells in airway epithelium Exp. Lung Res. 27 2001 401 415
36. G.H. Fisher, S.L. Wellen, D. Klimstra, J.M. Lenczowski, J.W. Tichelaar, M.J. Lizak, J.A. Whitsett, A. Koretsky, and H.E. Varmus 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. 15 2001 3249 3262
37. A.F. Gazdar, D.N. Carney, M.M. Nau, and J.D. Minna Characterization of variant subclasses of cell lines derived from small cell lung cancer having distinctive biochemical, morphological, and growth properties Cancer Res. 45 1985 2924 2930
38. A. Giangreco, K.R. Groot, and S.M. Janes Lung cancer and lung stem cells: strange bedfellows? Am. J. Respir. Crit. Care Med. 175 2007 547 553
39. A. Giangreco, E.N. Arwert, I.R. Rosewell, J. Snyder, F.M. Watt, and B.R. Stripp Stem cells are dispensable for lung homeostasis but restore airways after injury Proc. Natl. Acad. Sci. USA 106 2009 9286 9291
40. A. Golebiewska, N.H. Brons, R. Bjerkvig, and S.P. Niclou Critical appraisal of the side population assay in stem cell and cancer stem cell research Cell Stem Cell 8 2011 136 147
41. C. Gontan, A. de Munck, M. Vermeij, F. Grosveld, D. Tibboel, and R. Rottier Sox2 is important for two crucial processes in lung development: branching morphogenesis and epithelial cell differentiation Dev. Biol. 317 2008 296 309
42. M.A. Goodell, K. Brose, G. Paradis, A.S. Conner, and R.C. Mulligan Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo J. Exp. Med. 183 1996 1797 1806
43. L.V. Goodrich, and M.P. Scott Hedgehog and patched in neural development and disease Neuron 21 1998 1243 1257
44. M. Greaves, and C.C. Maley Clonal evolution in cancer Nature 481 2012 306 313
45. P.B. Gupta, C.M. Fillmore, G. Jiang, S.D. Shapira, K. Tao, C. Kuperwasser, and E.S. Lander Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells Cell 146 2011 633 644
46. J.S. Guseh, S.A. Bores, B.Z. Stanger, Q. Zhou, W.J. Anderson, D.A. Melton, and J. Rajagopal Notch signaling promotes airway mucous metaplasia and inhibits alveolar development Development 136 2009 1751 1759
47. M.T. Halpern, and K.E. Warner Motivations for smoking cessation: a comparison of successful quitters and failures J. Subst. Abuse. 5 1993 247 256
48. H. Han, D. Bourboulia, S. Jensen-Taubman, B. Isaac, B. Wei, and W.G. Stetler-Stevenson An endogenous inhibitor of angiogenesis inversely correlates with side population phenotype and function in human lung cancer cells Oncogene 2013
49. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
50. N. Haruki, K.S. Kawaguchi, S. Eichenberger, P.P. Massion, S. Olson, A. Gonzalez, D.P. Carbone, and T.P. Dang Dominant-negative Notch3 receptor inhibits mitogen-activated protein kinase pathway and the growth of human lung cancers Cancer Res. 65 2005 3555 3561
51. K.A. Hassan, L. Wang, H. Korkaya, G. Chen, I. Maillard, D.G. Beer, G.P. Kalemkerian, and M.S. Wicha Notch pathway activity identifies cells with cancer stem cell-like properties and correlates with worse survival in lung adenocarcinoma Clin. Cancer Res. 19 2013 1972 1980
52. C.J. Henry, L.H. Billups, M.D. Avery, T.H. Rude, D.R. Dansie, A. Lopez, B. Sass, C.E. Whitmire, and R.E. Kouri Lung cancer model system using 3-methylcholanthrene in inbred strains of mice Cancer Res. 41 1981 5027 5032
53. E. Herpel, K. Jensen, T. Muley, A. Warth, P.A. Schnabel, M. Meister, F.J. Herth, H. Dienemann, M. Thomas, and S. Gottschling The cancer stem cell antigens CD133, BCRP1/ABCG2 and CD117/c-KIT are not associated with prognosis in resected early-stage non-small cell lung cancer Anticancer Res. 31 2011 4491 4500
54. M.M. Ho, A.V. Ng, S. Lam, and J.Y. Hung Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells Cancer Res. 67 2007 4827 4833
55. K. Hochedlinger, Y. Yamada, C. Beard, and R. Jaenisch Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues Cell 121 2005 465 477
56. H. Iida, M. Suzuki, R. Goitsuka, and H. Ueno Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2 Int. J. Oncol. 40 2012 71 79
57. T. Ito, N. Udaka, T. Yazawa, K. Okudela, H. Hayashi, T. Sudo, F. Guillemot, R. Kageyama, and H. Kitamura Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium Development 127 2000 3913 3921
58. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, T. Murray, and M.J. Thun Cancer statistics, 2008 CA Cancer J. Clin. 58 2008 71 96
59. A. Jemal, M.J. Thun, L.A. Ries, H.L. Howe, H.K. Weir, M.M. Center, E. Ward, X.C. Wu, C. Eheman, R. Anderson, U.A. Ajani, B. Kohler, and B.K. Edwards Annual report to the nation on the status of cancer, 1975-2005, featuring trends in lung cancer, tobacco use, and tobacco control J. Natl. Cancer Inst. 100 2008 1672 1694
60. P. Jeremy George, A.K. Banerjee, C.A. Read, C. O'Sullivan, M. Falzon, F. Pezzella, A.G. Nicholson, P. Shaw, G. Laurent, and P.H. Rabbitts Surveillance for the detection of early lung cancer in patients with bronchial dysplasia Thorax 62 2007 43 50
61. H. Ji, D. Li, L. Chen, T. Shimamura, S. Kobayashi, K. McNamara, U. Mahmood, A. Mitchell, Y. Sun, R. Al-Hashem, L.R. Chirieac, R. Padera, R.T. Bronson, W. Kim, P.A. Janne, G.I. Shapiro, D. Tenen, B.E. Johnson, R. Weissleder, N.E. Sharpless, and K.K. Wong The impact of human EGFR kinase domain mutations on lung tumorigenesis and in vivo sensitivity to EGFR-targeted therapies Cancer Cell 9 2006 485 495
62. F. Jiang, Q. Qiu, A. Khanna, N.W. Todd, J. Deepak, L. Xing, H. Wang, Z. Liu, Y. Su, S.A. Stass, and R.L. Katz Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer Mol. Cancer Res. 7 2009 330 338
63. T. Jiang, B.J. Collins, N. Jin, D.N. Watkins, M.V. Brock, W. Matsui, B.D. Nelkin, and D.W. Ball Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer Cancer Res. 69 2009 845 854
64. S.B. Keysar, and A. Jimeno More than markers: biological significance of cancer stem cell-defining molecules Mol. Cancer Ther. 9 2010 2450 2457
65. C.F. Kim, E.L. Jackson, A.E. Woolfenden, S. Lawrence, I. Babar, S. Vogel, D. Crowley, R.T. Bronson, and T. Jacks Identification of bronchioalveolar stem cells in normal lung and lung cancer Cell 121 2005 823 835
66. J. Kim, J. Chu, X. Shen, J. Wang, and S.H. Orkin An extended transcriptional network for pluripotency of embryonic stem cells Cell 132 2008 1049 1061
67. P. Kirstetter, K. Anderson, B.T. Porse, S.E. Jacobsen, and C. Nerlov Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block Nat. Immunol. 7 2006 1048 1056
68. J. Konishi, K.S. Kawaguchi, H. Vo, N. Haruki, A. Gonzalez, D.P. Carbone, and T.P. Dang Gamma-secretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers Cancer Res. 67 2007 8051 8057
69. T. Lapidot, C. Sirard, J. Vormoor, B. Murdoch, T. Hoang, J. Caceres-Cortes, M. Minden, B. Paterson, M.A. Caligiuri, and J.E. Dick A cell initiating human acute myeloid leukaemia after transplantation into SCID mice Nature 367 1994 645 648
70. H. Lemjabbar-Alaoui, V. Dasari, S.S. Sidhu, A. Mengistab, W. Finkbeiner, M. Gallup, and C. Basbaum Wnt and Hedgehog are critical mediators of cigarette smoke-induced lung cancer PLoS One 1 2006 e93
71. V. Levina, A.M. Marrangoni, R. DeMarco, E. Gorelik, and A.E. Lokshin Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties PLoS One 3 2008 e3077
72. C. Lin, H. Song, C. Huang, E. Yao, R. Gacayan, S.M. Xu, and P.T. Chuang Alveolar type II cells possess the capability of initiating lung tumor development PLoS One 7 2012 e53817
73. Y. Litingtung, L. Lei, H. Westphal, and C. Chiang Sonic hedgehog is essential to foregut development Nat. Genet. 20 1998 58 61
74. Y.P. Liu, C.J. Yang, M.S. Huang, C.T. Yeh, A.T. Wu, Y.C. Lee, T.C. Lai, C.H. Lee, Y.W. Hsiao, J. Lu, C.N. Shen, P.J. Lu, and M. Hsiao Cisplatin selects for multidrug-resistant CD133+ cells in lung adenocarcinoma by activating Notch signaling Cancer Res. 73 2013 406 416
75. C. Lo Celso, D.M. Prowse, and F.M. Watt Transient activation of beta-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours Development 131 2004 1787 1799
76. Y. Lu, C. Futtner, J.R. Rock, X. Xu, W. Whitworth, B.L. Hogan, and M.W. Onaitis Evidence that SOX2 overexpression is oncogenic in the lung PLoS One 5 2010 e11022
77. L. Lundholm, P. Haag, D. Zong, T. Juntti, B. Mork, R. Lewensohn, and K. Viktorsson Resistance to DNA-damaging treatment in non-small cell lung cancer tumor-initiating cells involves reduced DNA-PK/ATM activation and diminished cell cycle arrest Cell Death Dis. 4 2013 e478
78. J.P. Medema Cancer stem cells: the challenges ahead Nat. Cell Biol. 15 2013 338 344
79. R. Meuwissen, and A. Berns Mouse models for human lung cancer Genes Dev. 19 2005 643 664
80. R. Meuwissen, S.C. Linn, R.I. Linnoila, J. Zevenhoven, W.J. Mooi, and A. Berns Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model Cancer Cell 4 2003 181 189
81. J.D. Minna, J.M. Kurie, and T. Jacks A big step in the study of small cell lung cancer Cancer Cell 4 2003 163 166
82. D. Mizrak, M. Brittan, and M.R. Alison CD133: molecule of the moment J. Pathol. 214 2008 3 9
83. H. Mizugaki, J. Sakakibara-Konishi, J. Kikuchi, J. Moriya, K.C. Hatanaka, E. Kikuchi, I. Kinoshita, S. Oizumi, H. Dosaka-Akita, Y. Matsuno, and M. Nishimura CD133 expression: a potential prognostic marker for non-small cell lung cancers Int. J. Clin. Oncol. 2013
84. J.S. Moreb Aldehyde dehydrogenase as a marker for stem cells Curr. Stem Cell Res. Ther. 3 2008 237 246
85. J. Moreb, M. Schweder, A. Suresh, and J.R. Zucali Overexpression of the human aldehyde dehydrogenase class I results in increased resistance to 4-hydroperoxycyclophosphamide Cancer Gene Ther. 3 1996 24 30
86. S.J. Morrison, and J. Kimble Asymmetric and symmetric stem-cell divisions in development and cancer Nature 441 2006 1068 1074
87. M. Nilsson, A.B. Unden, D. Krause, U. Malmqwist, K. Raza, P.G. Zaphiropoulos, and R. Toftgard Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1 Proc. Natl. Acad. Sci. USA 97 2000 3438 3443
88. P.C. Nowell The clonal evolution of tumor cell populations Science 194 1976 23 28
89. K. Okudela, T. Woo, H. Mitsui, M. Tajiri, M. Masuda, and K. Ohashi Expression of the potential cancer stem cell markers, CD133, CD44, ALDH1, and beta-catenin, in primary lung adenocarcinoma-their prognostic significance Pathol. Int. 62 2012 792 801
90. K. Okudela, T. Woo, H. Mitsui, T. Suzuki, M. Tajiri, Y. Sakuma, Y. Miyagi, Y. Tateishi, S. Umeda, M. Masuda, and K. Ohashi Downregulation of ALDH1A1 expression in non-small cell lung carcinomas-its clinicopathologic and biological significance Int. J. Clin. Exp. Pathol. 6 2013 1 12
91. R. Pardal, M.F. Clarke, and S.J. Morrison Applying the principles of stem-cell biology to cancer Nat. Rev. Cancer 3 2003 895 902
92. D.M. Parkin, F. Bray, J. Ferlay, and P. Pisani Global cancer statistics, 2002 CA Cancer J. Clin. 55 2005 74 108
93. E. Passegue, C.H. Jamieson, L.E. Ailles, and I.L. Weissman Normal and leukemic hematopoiesis: are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc. Natl. Acad. Sci. USA 100 Suppl 1 2003 11842 11849
94. M. Patel, L. Lu, D.S. Zander, L. Sreerama, D. Coco, and J.S. Moreb ALDH1A1 and ALDH3A1 expression in lung cancers: correlation with histologic type and potential precursors Lung Cancer 59 2008 340 349
95. C.V. Pepicelli, P.M. Lewis, and A.P. McMahon Sonic hedgehog regulates branching morphogenesis in the mammalian lung Curr. Biol. 8 1998 1083 1086
96. D. Perumal, S. Singh, S.J. Yoder, G.C. Bloom, and S.P. Chellappan A novel five gene signature derived from stem-like side population cells predicts overall and recurrence-free survival in NSCLC PLoS One 7 2012 e43589
97. K. Politi, M.F. Zakowski, P.D. Fan, E.A. Schonfeld, W. Pao, and H.E. Varmus Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to down-regulation of the receptors Genes Dev. 20 2006 1496 1510
98. R.N. Proctor Tobacco and the global lung cancer epidemic Nat. Rev. Cancer 1 2001 82 86
99. J. Que, X. Luo, R.J. Schwartz, and B.L. Hogan Multiple roles for Sox2 in the developing and adult mouse trachea Development 136 2009 1899 1907
100. E.L. Rawlins, and B.L. Hogan Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133 2006 2455 2465
101. E.L. Rawlins, C.P. Clark, Y. Xue, and B.L. Hogan The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells Development 136 2009 3741 3745
102. G. Raz, K.E. Allen, C. Kingsley, I. Cherni, S. Arora, A. Watanabe, C.D. Lorenzo, V.D. Edwards, S. Sridhar, G. Hostetter, and G.J. Weiss Hedgehog signaling pathway molecules and ALDH1A1 expression in early-stage non-small cell lung cancer Lung Cancer 76 2012 191 196
103. T. Reya, and H. Clevers Wnt signalling in stem cells and cancer Nature 434 2005 843 850
104. T. Reya, A.W. Duncan, L. Ailles, J. Domen, D.C. Scherer, K. Willert, L. Hintz, R. Nusse, and I.L. Weissman A role for Wnt signalling in self-renewal of haematopoietic stem cells Nature 423 2003 409 414
105. S.D. Reynolds, A.C. Zemke, A. Giangreco, B.L. Brockway, R.M. Teisanu, J.A. Drake, T. Mariani, P.Y. Di, M.M. Taketo, and B.R. Stripp Conditional stabilization of beta-catenin expands the pool of lung stem cells Stem Cells 26 2008 1337 1346
106. A. Roesch, M. Fukunaga-Kalabis, E.C. Schmidt, S.E. Zabierowski, P.A. Brafford, A. Vultur, D. Basu, P. Gimotty, T. Vogt, and M. Herlyn A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth Cell 141 2010 583 594
107. C.D. Salcido, A. Larochelle, B.J. Taylor, C.E. Dunbar, and L. Varticovski Molecular characterisation of side population cells with cancer stem cell-like characteristics in small-cell lung cancer Br. J. Cancer 102 2010 1636 1644
108. A.V. Salnikov, J. Gladkich, G. Moldenhauer, M. Volm, J. Mattern, and I. Herr 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 126 2010 950 958
109. A.G. Schepers, H.J. Snippert, D.E. Stange, M. van den Born, J.H. van Es, M. van de Wetering, and H. Clevers Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas Science 337 2012 730 735
110. M.M. Shi, Y.L. Xiong, X.S. Jia, X. Li, L. Zhang, X.L. Li, and E.H. Wang Fluorouracil selectively enriches stem-like cells in the lung adenocarcinoma cell line SPC Tumour Biol. 34 2013 1503 1510
111. K. Shien, S. Toyooka, K. Ichimura, J. Soh, M. Furukawa, Y. Maki, T. Muraoka, N. Tanaka, T. Ueno, H. Asano, K. Tsukuda, M. Yamane, T. Oto, K. Kiura, and S. Miyoshi Prognostic impact of cancer stem cell-related markers in non-small cell lung cancer patients treated with induction chemoradiotherapy Lung Cancer 77 2012 162 167
112. K. Shien, S. Toyooka, H. Yamamoto, J. Soh, M. Jida, K.L. Thu, S. Hashida, Y. Maki, E. Ichihara, H. Asano, K. Tsukuda, N. Takigawa, K. Kiura, A.F. Gazdar, W.L. Lam, and S. Miyoshi Acquired resistance to EGFR inhibitors is associated with a manifestation of stem cell-like properties in cancer cells Cancer Res. 73 2013 3051 3061
113. L.M. Sholl, J.A. Barletta, B.Y. Yeap, L.R. Chirieac, and J.L. Hornick Sox2 protein expression is an independent poor prognostic indicator in stage I lung adenocarcinoma Am. J. Surg. Pathol. 34 2010 1193 1198
114. R. Siegel, D. Naishadham, and A. Jemal Cancer statistics, 2012 CA Cancer J. Clin. 62 2012 10 29
115. S. Singh, J. Trevino, N. Bora-Singhal, D. Coppola, E. Haura, S. Altiok, and S.P. Chellappan EGFR/Src/Akt signaling modulates Sox2 expression and self-renewal of stem-like side-population cells in non-small cell lung cancer Mol. Cancer 11 2012 73
116. S. Singh, N. Bora-Singhal, J. Kroeger, H. Laklai, and S.P. Chellappan BetaArrestin-1 and Mcl-1 modulate self-renewal growth of cancer stem-like side-population cells in non-small cell lung cancer PLoS One 8 2013 e55982
117. M. Smalley, and A. Ashworth Stem cells and breast cancer: a field in transit Nat. Rev. Cancer 3 2003 832 844
118. B.R. Stripp, and S.D. Reynolds Maintenance and repair of the bronchiolar epithelium Proc. Am. Thorac. Soc. 5 2008 328 333
119. J.P. Sullivan, M. Spinola, M. Dodge, M.G. Raso, C. Behrens, B. Gao, K. Schuster, C. Shao, J.E. Larsen, L.A. Sullivan, S. Honorio, Y. Xie, P.P. Scaglioni, J.M. DiMaio, A.F. Gazdar, J.W. Shay, I.I. Wistuba, and J.D. Minna Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling Cancer Res. 70 2010 9937 9948
120. M.E. Sunday, K.J. Haley, K. Sikorski, S.A. Graham, R.L. Emanuel, F. Zhang, Q. Mu, A. Shahsafaei, and D. Hatzis Calcitonin driven v-Ha-ras induces multilineage pulmonary epithelial hyperplasias and neoplasms Oncogene 18 1999 4336 4347
121. K.D. Sutherland, N. Proost, I. Brouns, D. Adriaensen, J.Y. Song, and A. Berns Cell of origin of small cell lung cancer: inactivation of Trp53 and rb1 in distinct cell types of adult mouse lung Cancer Cell 19 2011 754 764
122. J. Taipale, and P.A. Beachy The Hedgehog and Wnt signalling pathways in cancer Nature 411 2001 349 354
123. D.H. Tompkins, V. Besnard, A.W. Lange, S.E. Wert, A.R. Keiser, A.N. Smith, R. Lang, and J.A. Whitsett Sox2 is required for maintenance and differentiation of bronchiolar clara, ciliated, and goblet cells PLoS One 4 2009 e8248
124. L. Tong, M.R. Spitz, J.J. Fueger, and C.A. Amos Lung carcinoma in former smokers Cancer 78 1996 1004 1010
125. P.N. Tsao, F. Chen, K.I. Izvolsky, J. Walker, M.A. Kukuruzinska, J. Lu, and W.V. Cardoso Gamma-secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung J. Biol. Chem. 283 2008 29532 29544
126. K. Uematsu, B. He, L. You, Z. Xu, F. McCormick, and D.M. Jablons Activation of the Wnt pathway in non small cell lung cancer: evidence of dishevelled overexpression Oncogene 22 2003 7218 7221
127. K. Uematsu, S. Kanazawa, L. You, B. He, Z. Xu, K. Li, B.M. Peterlin, F. McCormick, and D.M. Jablons Wnt pathway activation in mesothelioma: evidence of dishevelled overexpression and transcriptional activity of beta-catenin Cancer Res. 63 2003 4547 4551
128. J. Vestergaard, M.W. Pedersen, N. Pedersen, C. Ensinger, Z. Tumer, N. Tommerup, H.S. Poulsen, and L.A. Larsen Hedgehog signaling in small-cell lung cancer: frequent in vivo but a rare event in vitro Lung Cancer 52 2006 281 290
129. J.E. Visvader, and G.J. Lindeman Cancer stem cells in solid tumours: accumulating evidence and unresolved questions Nat. Rev. Cancer 8 2008 755 768
130. Y. Wang, Z. Zhang, Y. Yan, W.J. Lemon, M. LaRegina, C. Morrison, R. Lubet, and M. You A chemically induced model for squamous cell carcinoma of the lung in mice: histopathology and strain susceptibility Cancer Res. 64 2004 1647 1654
131. D.N. Watkins, D.M. Berman, S.G. Burkholder, B. Wang, P.A. Beachy, and S.B. Baylin Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer Nature 422 2003 313 317
132. K.A. Wikenheiser, J.C. Clark, R.I. Linnoila, M.T. Stahlman, and J.A. Whitsett 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. 52 1992 5342 5352
133. R.A. Winn, L. Marek, S.Y. Han, K. Rodriguez, N. Rodriguez, M. Hammond, M. Van Scoyk, H. Acosta, J. Mirus, N. Barry, Y. Bren-Mattison, T.J. Van Raay, R.A. Nemenoff, and L.E. Heasley Restoration of Wnt-7a expression reverses non-small cell lung cancer cellular transformation through frizzled-9-mediated growth inhibition and promotion of cell differentiation J. Biol. Chem. 280 2005 19625 19634
134. R.A. Winn, M. Van Scoyk, M. Hammond, K. Rodriguez, J.T. Crossno Jr., L.E. Heasley, and R.A. Nemenoff Antitumorigenic effect of Wnt 7a and Fzd 9 in non-small cell lung cancer cells is mediated through ERK-5-dependent activation of peroxisome proliferator-activated receptor gamma J. Biol. Chem. 281 2006 26943 26950
135. C. Wu, and B.A. Alman Side population cells in human cancers Cancer Lett. 268 2008 1 9
136. X. Xu, J.R. Rock, Y. Lu, C. Futtner, B. Schwab, J. Guinney, B.L. Hogan, and M.W. Onaitis Evidence for type II cells as cells of origin of K-Ras-induced distal lung adenocarcinoma Proc. Natl. Acad. Sci. USA 109 2012 4910 4915
137. C. Xu, D. Xie, S.C. Yu, X.J. Yang, L.R. He, J. Yang, Y.F. Ping, B. Wang, L. Yang, S.L. Xu, W. Cui, Q.L. Wang, W.J. Fu, Q. Liu, C. Qian, Y.H. Cui, J.N. Rich, H.F. Kung, X. Zhang, and X.W. Bian Beta-catenin/POU5F1/SOX2 transcription factor complex mediates IGF-I receptor signaling and predicts poor prognosis in lung adenocarcinoma Cancer Res. 73 2013 3181 3189
138. T. Yoshimoto, F. Hirao, M. Sakatani, H. Nishikawa, and T. Ogura Induction of squamous cell carcinoma in the lung of C57BL/6 mice by intratracheal instillation of benzo[a]pyrene with charcoal powder Gann 68 1977 343 352
139. T. Yoshimoto, T. Inoue, H. Iizuka, H. Nishikawa, M. Sakatani, T. Ogura, F. Hirao, and Y. Yamamura Differential induction of squamous cell carcinomas and adenocarcinomas in mouse lung by intratracheal instillation of benzo(a)pyrene and charcoal powder Cancer Res. 40 1980 4301 4307
140. L. You, B. He, Z. Xu, K. Uematsu, J. Mazieres, I. Mikami, N. Reguart, T.W. Moody, J. Kitajewski, F. McCormick, and D.M. Jablons Inhibition of Wnt-2-mediated signaling induces programmed cell death in non-small-cell lung cancer cells Oncogene 23 2004 6170 6174
141. A.C. Zemke, R.M. Teisanu, A. Giangreco, J.A. Drake, B.L. Brockway, S.D. Reynolds, and B.R. Stripp Beta-catenin is not necessary for maintenance or repair of the bronchiolar epithelium Am. J. Respir. Cell Mol. Biol. 41 2009 535 543
142. W.C. Zhang, N. Shyh-Chang, H. Yang, A. Rai, S. Umashankar, S. Ma, B.S. Soh, L.L. Sun, B.C. Tai, M.E. Nga, K.K. Bhakoo, S.R. Jayapal, M. Nichane, Q. Yu, D.A. Ahmed, C. Tan, W.P. Sing, J. Tam, A. Thirugananam, M.S. Noghabi, Y.H. Pang, H.S. Ang, W. Mitchell, P. Robson, P. Kaldis, R.A. Soo, S. Swarup, E.H. Lim, and B. Lim Glycine decarboxylase activity drives non-small cell lung cancer tumor-initiating cells and tumorigenesis Cell 148 2012 259 272
143. S. Zhou, J.D. Schuetz, K.D. Bunting, A.M. Colapietro, J. Sampath, J.J. Morris, I. Lagutina, G.C. Grosveld, M. Osawa, H. Nakauchi, and B.P. Sorrentino The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype Nat. Med. 7 2001 1028 1034