Identification of bronchioalveolar stem cells in normal lung and lung cancer

Cell

Volumn 121, Issue 6, 2005, Pages 823-835

  Bender Kim, Carla F ^a   Jackson, Erica L ^a,b   Woolfenden, Amber E ^a   Lawrence, Sharon ^a   Babar, Imran ^a   Vogel, Sinae ^a   Crowley, Denise ^a   Bronson, Roderick T ^c   Jacks, Tyler ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRONCHUS; BRONCHUS INJURY; CELL CULTURE; CELL ISOLATION; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; EPITHELIUM CELL; LUNG ADENOCARCINOMA; LUNG ALVEOLUS CELL; LUNG CANCER; MOUSE; NONHUMAN; ONCOGENE K RAS; PRIORITY JOURNAL; STEM CELL;

EID: 20444397431     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.03.032     Document Type: Article

References (58)

1. 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
2. Y. Aso, K. Yoneda, and Y. Kikkawa Morphologic and biochemical study of pulmonary changes induced by bleomycin in mice Lab. Invest. 35 1976 558 568
3. L.H. Bannister Respiratory system P.L. Williams R. Warwick M. Dyson L.H. Bannister Gray's Anatomy Thirty-Eighth Edition 1999 Churchill Livingstone New York 1666 1672
4. C. Blanpain, W.E. Lowry, A. Geoghegan, L. Polak, and E. Fuchs Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche Cell 118 2004 635 648
5. 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
6. 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
7. A.E. Bortnick, E. Favari, J.Q. Tao, O.L. Francone, M. Reilly, Y. Zhang, G.H. Rothblat, and S.R. Bates Identification and characterization of rodent ABCA1 in isolated type II pneumocytes Am. J. Physiol. Lung Cell. Mol. Physiol. 285 2003 L869 L878
8. B.J. Chiasson, V. Tropepe, C.M. Morshead, and D. van der Kooy Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics J. Neurosci. 19 1999 4462 4471
9. A. Cozzio, E. Passegue, P.M. Ayton, H. Karsunky, M.L. Cleary, and I.L. Weissman Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors Genes Dev. 17 2003 3029 3035
10. H.E. Daly, C.M. Baecher-Allan, R.K. Barth, C.T. D'Angio, and J.N. Finkelstein Bleomycin induces strain-dependent alterations in the pattern of epithelial cell-specific marker expression in mouse lung Toxicol. Appl. Pharmacol. 142 1997 303 310
11. H.E. Daly, C.M. Baecher-Allan, A.T. Paxhia, R.M. Ryan, R.K. Barth, and J.N. Finkelstein Cell-specific gene expression reveals changes in epithelial cell populations after bleomycin treatment Lab. Invest. 78 1998 393 400
12. A. Delplanque, C. Coraux, R. Tirouvanziam, I. Khazaal, E. Puchelle, P. Ambros, D. Gaillard, and B. Peault Epithelial stem cell-mediated development of the human respiratory mucosa in SCID mice J. Cell Sci. 113 2000 767 778
13. K.B. Deome, L.J. Faulkin Jr., H.A. Bern, and P.B. Blair Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice Cancer Res. 19 1959 515 520
14. G.B. Dermer Origin of bronchioloalveolar carcinoma and peripheral bronchial adenocarcinoma Cancer 49 1982 881 887
15. F. Doetsch, I. Caille, D.A. Lim, J.M. Garcia-Verdugo, and A. Alvarez-Buylla Subventricular zone astrocytes are neural stem cells in the adult mammalian brain Cell 97 1999 703 716
16. F.H. Gage, P.W. Coates, T.D. Palmer, H.G. Kuhn, L.J. Fisher, J.O. Suhonen, D.A. Peterson, S.T. Suhr, and J. Ray Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain Proc. Natl. Acad. Sci. USA 92 1995 11879 11883
17. A. Giangreco, S.D. Reynolds, and B.R. Stripp Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction Am. J. Pathol. 161 2002 173 182
18. A. Giangreco, H. Shen, S.D. Reynolds, and B.R. Stripp Molecular phenotype of airway side population cells Am. J. Physiol. Lung Cell. Mol. Physiol. 286 2003 L624 L630 10.1152/ajplung.00149.2003
19. 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
20. W.T. Gunning, G.D. Stoner, and P.J. Goldblatt Glyceraldehyde-3-phosphate dehydrogenase and other enzymatic activity in normal mouse lung and in lung tumors Exp. Lung Res. 17 1991 255 261
21. A.K. Hadjantonakis, M. Gertsenstein, M. Ikawa, M. Okabe, and A. Nagy Non-invasive sexing of preimplantation stage mammalian embryos Nat. Genet. 19 1998 220 222
22. R.G. Harris, E.L. Herzog, E.M. Bruscia, J.E. Grove, J.S. Van Arnam, and D.S. Krause Lack of a fusion requirement for development of bone marrow-derived epithelia Science 305 2004 90 93
23. K.U. Hong, S.D. Reynolds, A. Giangreco, C.M. Hurley, and B.R. Stripp 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. 24 2001 671 681
24. K. Hoshino, and W.U. Gardner Transplantability and life span of mammary gland during serial transplantation in mice Nature 213 1967 193 194
25. B.E. Isakson, R.L. Lubman, G.J. Seedorf, and S. Boitano Modulation of pulmonary alveolar type II cell phenotype and communication by extracellular matrix and KGF Am. J. Physiol. Cell Physiol. 281 2001 C1291 C1299
26. N.B. Ivanova, J.T. Dimos, C. Schaniel, J.A. Hackney, K.A. Moore, and I.R. Lemischka A stem cell molecular signature Science 298 2002 601 604
27. E.L. Jackson, N. Willis, K. Mercer, R.T. Bronson, D. Crowley, R. Montoya, T. Jacks, and D.A. Tuveson Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras Genes Dev. 15 2001 3243 3248
28. C.B. Johansson, S. Momma, D.L. Clarke, M. Risling, U. Lendahl, and J. Frisen Identification of a neural stem cell in the adult mammalian central nervous system Cell 96 1999 25 34
29. D.N. Kotton, B.Y. Ma, W.V. Cardoso, E.A. Sanderson, R.S. Summer, M.C. Williams, and A. Fine Bone marrow-derived cells as progenitors of lung alveolar epithelium Development 128 2001 5181 5188
30. D.S. Krause, N.D. Theise, M.I. Collector, O. Henegariu, S. Hwang, R. Gardner, S. Neutzel, and S.J. Sharkis Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell Cell 105 2001 369 377
31. G.M. Kruger, J.T. Mosher, S. Bixby, N. Joseph, T. Iwashita, and S.J. Morrison Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness Neuron 35 2002 657 669
32. R.J. Mason, M. Kalina, L.D. Nielsen, A.M. Malkinson, and J.M. Shannon Surfactant protein C expression in urethane-induced murine pulmonary tumors Am. J. Pathol. 156 2000 175 182
33. J.D. Minna, J.A. Roth, and A.F. Gazdar Focus on lung cancer Cancer Cell 1 2002 49 52
34. M. Mori, R. Chiba, and T. Takahashi Atypical adenomatous hyperplasia of the lung and its differentiation from adenocarcinoma. Characterization of atypical cells by morphometry and multivariate cluster analysis Cancer 72 1993 2331 2340
35. M. Mori, S.K. Rao, H.H. Popper, P.T. Cagle, and A.E. Fraire Atypical adenomatous hyperplasia of the lung: a probable forerunner in the development of adenocarcinoma of the lung Mod. Pathol. 14 2001 72 84
36. R.J. Morris, Y. Liu, L. Marles, Z. Yang, C. Trempus, S. Li, J.S. Lin, J.A. Sawicki, and G. Cotsarelis Capturing and profiling adult hair follicle stem cells Nat. Biotechnol. 22 2004 411 417
37. S.J. Morrison, and I.L. Weissman The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype Immunity 1 1994 661 673
38. S. Nielsen, L.S. King, B.M. Christensen, and P. Agre Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat Am. J. Physiol. 273 1997 C1549 C1561
39. K.P. Olive, D.A. Tuveson, Z.C. Ruhe, B. Yin, N.A. Willis, R.T. Bronson, D. Crowley, and T. Jacks Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome Cell 119 2004 847 860
40. M. Osawa, K. Hanada, H. Hamada, and H. Nakauchi Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell Science 273 1996 242 245
41. W.R. Otto Lung epithelial stem cells J. Pathol. 197 2002 527 535
42. E. Passegue, E.F. Wagner, and I.L. Weissman JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells Cell 119 2004 431 443
43. M. Ramalho-Santos, S. Yoon, Y. Matsuzaki, R.C. Mulligan, and D.A. Melton "Stemness": transcriptional profiling of embryonic and adult stem cells Science 298 2002 597 600
44. T. Reya, S.J. Morrison, M.F. Clarke, and I.L. Weissman Stem cells, cancer, and cancer stem cells Nature 414 2001 105 111
45. S.D. Reynolds, A. Giangreco, J.H. Power, and B.R. Stripp Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration Am. J. Pathol. 156 2000 269 278
46. S.D. Reynolds, K.U. Hong, A. Giangreco, G.W. Mango, C. Guron, Y. Morimoto, and B.R. Stripp Conditional clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells Am. J. Physiol. Lung Cell. Mol. Physiol. 278 2000 L1256 L1263
47. J. Rosai, and L.H. Sobin Atlas of Tumor Pathology Third Series Edition 1995 Armed Forces Institute of Pathology Washington, DC
48. R.M. Seaberg, and D. van der Kooy Stem and progenitor cells: the premature desertion of rigorous definitions Trends Neurosci. 26 2003 125 131
49. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, J. Squire, and P.B. Dirks Identification of a cancer stem cell in human brain tumors Cancer Res. 63 2003 5821 5828
50. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, T. Hide, R.M. Henkelman, M.D. Cusimano, and P.B. Dirks Identification of human brain tumour initiating cells Nature 432 2004 396 401
51. G.J. Spangrude, D.M. Brooks, and D.B. Tumas Long-term repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function Blood 85 1995 1006 1016
52. R. Summer, D.N. Kotton, X. Sun, B. Ma, K. Fitzsimmons, and A. Fine Side population cells and Bcrp1 expression in lung Am. J. Physiol. Lung Cell. Mol. Physiol. 285 2003 L97 104
53. L.G. Thaete, and A.M. Malkinson Cells of origin of primary pulmonary neoplasms in mice: morphologic and histochemical studies Exp. Lung Res. 17 1991 219 228
54. V. Tropepe, B.L. Coles, B.J. Chiasson, D.J. Horsford, A.J. Elia, R.R. McInnes, and D. van der Kooy Retinal stem cells in the adult mammalian eye Science 287 2000 2032 2036
55. T. Tumbar, G. Guasch, V. Greco, C. Blanpain, W.E. Lowry, M. Rendl, and E. Fuchs Defining the epithelial stem cell niche in skin Science 303 2004 359 363
56. B.E. Welm, S.B. Tepera, T. Venezia, T.A. Graubert, J.M. Rosen, and M.A. Goodell Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population Dev. Biol. 245 2002 42 56
57. 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
58. C.W. Wuenschell, M.E. Sunday, G. Singh, P. Minoo, H.C. Slavkin, and D. Warburton Embryonic mouse lung epithelial progenitor cells co-express immunohistochemical markers of diverse mature cell lineages J. Histochem. Cytochem. 44 1996 113 123