Achaete-scute homologue-1 tapers neuroendocrine cell differentiation in lungs after exposure to naphthalene

Toxicological Sciences

Volumn 117, Issue 1, 2010, Pages 238-248

  Jensen Taubman, Sandra ^a   Wang, Xiao Yang ^a   Linnoila, R Ilona ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Achaete scute homologue 1; Bronchiolization of the alveoli; Lung repair; Neuroendocrine; Transgenic mouse

Indexed keywords

CLARA CELL 10 PROTEIN; CYTOCHROME P450; CYTOCHROME P450 2F2; NAPHTHALENE; PROTEIN; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL DAMAGE; CELL DIFFERENTIATION; CELL HYPERPLASIA; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LUNG; LUNG ALVEOLUS; LUNG SMALL CELL CANCER; MOUSE; NEUROSECRETORY CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE, TUMOR; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUNG; MICE; MICE, TRANSGENIC; NAPHTHALENES; NEUROENDOCRINE CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MUS; MUS MUSCULUS;

EID: 77955861087     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq177     Document Type: Article

References (38)

1. Bernard, A., Marchandise, F. X., Depelchin, S., Lauwerys, R., and Sibille, Y. (1992). Clara cell protein in serum and bronchoalveolar lavage. Eur. Respir. J. 5, 1231-1238.
2. Borges, M., Linnoila, R. I., van de Velde, H. J., Chen, H., Nelkin, B. D., Mabry, M., Baylin, S. B., and Ball, D. W. (1997). An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 386, 852-855.
3. Bui, P. H., and Hankinson, O. (2009). Functional characterization of human cytochrome P450 2S1 using a synthetic gene-expressed protein in Escherichia coli. Mol. Pharmacol. 76, 1031-1043.
4. Castro, C. M., Yang, Y., Zhang, Z., and Linnoila, R. I. (2000). Attenuation of pulmonary neuroendocrine differentiation in mice lacking Clara cell secretory protein. Lab. Invest. J. Tech. Methods Pathol. 80, 1533-1540.
5. Evans, M. J., Cabral-Anderson, L. J., and Freeman, G. (1978). Role of the Clara cell in renewal of the bronchiolar epithelium. Lab. Invest. 38, 648-653.
6. Giangreco, A., Reynolds, S. D., and Stripp, B. R. (2002). Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am. J. Pathol. 161, 173-182.
7. Ito, T., Udaka, N., Yazawa, T., Okudela, K., Hayashi, H., Sudo, T., Guillemot, F., Kageyama, R., and Kitamura, H. (2000). Basic helixloop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127, 3913-3921.
8. Jensen, S. M., Jones, J. E., Pass, H., Steinberg, S. M., and Linnoila, R. I. (1994). Clara cell 10 kDa protein mRNA in normal and atypical regions of human respiratory epithelium. Int. J. Cancer 58, 629-637.
9. Jensen-Taubman, S. M., Steinberg, S. M., and Linnoila, R. I. (1998). Bronchiolization of the alveoli in lung cancer: pathology, patterns of differentiation and oncogene expression. Int. J. Cancer 75, 489-496.
10. Jiang, T., Collins, B. J., Jin, N., Watkins, D. N., Brock, M. V., Matsui, W., Nelkin, B. D., and Ball, D. W. (2009). Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. Cancer Res. 69, 845-854.
11. Khoor, A., Gray, M. E., Singh, G., and Stahlman, M. T. (1996). Ontogeny of Clara cell-specific protein and its mRNA: their association with neuroepithelial bodies in human fetal lung and in bronchopulmonary dysplasia. J. Histochem. Cytochem. 44, 1429-1438.
12. Kim, C. F., Jackson, E. L., Woolfenden, A. E., Lawrence, S., Babar, I., Vogel, S., Crowley, D., Bronson, R. T., and Jacks, T. (2005). Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835.
13. Linnoila, R. I. (2006). Functional facets of the pulmonary neuroendocrine system. Lab. Invest. 86, 425-444.
14. Linnoila, R. I., Jensen-Taubman, S., Kazanjian, A., and Grimes, H. L. (2007). Loss of GFI1 impairs pulmonary neuroendocrine cell proliferation, but the neuroendocrine phenotype has limited impact on post-naphthalene airway repair. Lab. Invest. 87, 336-344.
15. Linnoila, R. I., Mulshine, J. L., Steinberg, S. M., Funa, K., Matthews, M. J., Cotelingam, J. D., and Gazdar, A. F. (1988). Neuroendocrine differentiation in endocrine and nonendocrine lung carcinomas. Am. J. Clin. Pathol. 90, 641-652.
16. Linnoila, R. I., Sahu, A., Miki, M., Ball, D. W., and DeMayo, F. J. (2000a). Morphometric analysis of CC10-hASH1 transgenic mouse lung: a model for bronchiolization of alveoli and neuroendocrine carcinoma. Exp. Lung Res. 26, 595-615.
17. Linnoila, R. I., Zhao, B., DeMayo, J. L., Nelkin, B. D., Baylin, S. B., DeMayo, F. J., and Ball, D. W. (2000b). Constitutive achaete-scute homologue-1 promotes airway dysplasia and lung neuroendocrine tumors in transgenic mice. Cancer Res. 60, 4005-4009.
18. Mahvi, D., Bank, H., and Harley, R. (1977). Morphology of a naphthaleneinduced bronchiolar lesion. Am. J. Pathol. 86, 558-572.
19. Nettesheim, P., and Szakal, A. K. (1972). Morphogenesis of alveolar bronchiolization. Lab. Invest. 26, 210-219.
20. Osada, H., Tatematsu, Y., Yatabe, Y., Horio, Y., and Takahashi, T. (2005). ASH1 gene is a specific therapeutic target for lung cancers with neuroendocrine features. Cancer Res. 65, 10680-10685.
21. Osada, H., Tomida, S., Yatabe, Y., Tatematsu, Y., Takeuchi, T., Murakami, H., Kondo, Y., Sekido, Y., and Takahashi, T. (2008). Roles of achaete-scute homologue 1 in DKK1 and E-cadherin repression and neuroendocrine differentiation in lung cancer. Cancer Res. 68, 1647-1655.
22. Peake, J. L., Reynolds, S. D., Stripp, B. R., Stephens, K. E., and Pinkerton, K. E. (2000). Alteration of pulmonary neuroendocrine cells during epithelial repair of naphthalene-induced airway injury. Am. J. Pathol. 156, 279-286.
23. Phimister, A. J., Nagasawa, H. T., Buckpitt, A. R., and Plopper, C. G. (2005). Prevention of naphthalene-induced pulmonary toxicity by glutathione prodrugs: roles for glutathione depletion in adduct formation and cell injury. J. Biochem. Mol. Toxicol. 19, 42-51.
24. Plopper, C. G., Macklin, J., Nishio, S. J., Hyde, D. M., and Buckpitt, A. R. (1992). Relationship of cytochrome P-450 activity to Clara cell cytotoxicity. III. Morphometric comparison of changes in the epithelial populations of terminal bronchioles and lobar bronchi in mice, hamsters, and rats after parenteral administration of naphthalene. Lab. Invest. 67, 553-565.
25. Poulsen, T. T., Naizhen, X., Poulsen, H. S., and Linnoila, R. I. (2008). Acute damage by naphthalene triggers expression of the neuroendocrine marker PGP9.5 in airway epithelial cells. Toxicol. Lett. 181, 67-74.
26. Preuss, R., Angerer, J., and Drexler, H. (2003). Naphthalene-an environmental and occupational toxicant. Int. Arch. Occup. Environ. Health 76, 556-576.
27. Ray, M. K., Wang, G., Barrish, J., Finegold, M. J., and DeMayo, F. J. (1996). Immunohistochemical localization of mouse Clara cell 10-KD protein using antibodies raised against the recombinant protein. J. Histochem. Cytochem. 44, 919-927.
28. Reynolds, S. D., Giangreco, A., Power, J. H., and Stripp, B. R. (2000a). Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am. J. Pathol. 156, 269-278.
29. Reynolds, S. D., Hong, K. U., Giangreco, A., Mango, G. W., Guron, C., Morimoto, Y., and Stripp, B. R. (2000b). Conditional clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells. Am. J. Physiol. Lung Cell Mol. Physiol. 278, L1256-L1263.
30. Schuurmans, C., and Guillemot, F. (2002). Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26-34.
31. Shultz, M. A., Choudary, P. V., and Buckpitt, A. R. (1999). Role of murine cytochrome P-450 2F2 in metabolic activation of naphthalene and metabolism of other xenobiotics. J. Pharmacol. Exp. Ther. 290, 281-288.
32. Singh, G., Singh, J., Katyal, S. L., Brown, W. E., Kramps, J. A., Paradis, I. L., Dauber, J. H., Macpherson, T. A., and Squeglia, N. (1988). Identification, cellular localization, isolation, and characterization of human Clara cellspecific 10 KD protein. J. Histochem. Cytochem. 36, 73-80.
33. Sommer, L., Shah, N., Rao, M., and Anderson, D. J. (1995). The cellular function of MASH1 in autonomic neurogenesis. Neuron 15, 1245-1258.
34. Stevens, T. P., McBride, J. T., Peake, J. L., Pinkerton, K. E., and Stripp, B. R. (1997). Cell proliferation contributes to PNEC hyperplasia after acute airway injury. Am. J. Physiol. 272, L486-L493.
35. Stripp, B. R., Maxson, K., Mera, R., and Singh, G. (1995). Plasticity of airway cell proliferation and gene expression after acute naphthalene injury. Am. J. Physiol. 269, L791-L799.
36. Van Winkle, L. S., Buckpitt, A. R., Nishio, S. J., Isaac, J. M., and Plopper, C. G. (1995). Cellular response in naphthalene-induced Clara cell injury and bronchiolar epithelial repair in mice. Am. J. Physiol. 269, L800-L818.
37. Wang, X. Y., Dakir el, H., Naizhen, X., Jensen-Taubman, S. M., DeMayo, F. J., and Linnoila, R. I. (2007). Achaete-scute homolog-1 linked to remodeling and preneoplasia of pulmonary epithelium. Lab. Invest. 87, 527-539.
38. West, J. A., Williams, K. J., Toskala, E., Nishio, S. J., Fleschner, C. A., Forman, H. J., Buckpitt, A. R., and Plopper, C. G. (2002). Induction of tolerance to naphthalene in Clara cells is dependent on a stable phenotypic adaptation favoring maintenance of the glutathione pool. Am. J. Pathol. 160, 1115-1127.