Achaete-scute homolog-1 linked to remodeling and preneoplasia of pulmonary epithelium

Laboratory Investigation

Volumn 87, Issue 6, 2007, Pages 527-539

  Wang, Xiao Yang ^a   Dakir, El Habib ^a   Naizhen, Xu ^a   Jensen Taubman, Sandra M ^a   DeMayo, Francesco J ^b   Linnoila, R Ilona ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Achaete scute homolog 1; Apoptosis; Bronchiolization of alveoli; Lung; Mouse model; Preneoplasia; Proliferation

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MATRILYSIN; PROTEIN BCL 2; PROTEIN C MYB; PROTEIN KINASE B; TRANSCRIPTION FACTOR MASH1;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRONCHIOLE; CANCER CELL; CELL DAMAGE; CELL IMMORTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; IN VITRO STUDY; KNOCKOUT GENE; LUNG ALVEOLUS EPITHELIUM; LUNG CARCINOGENESIS; LUNG CARCINOMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; TISSUE REGENERATION;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRONCHI; CARCINOMA, SMALL CELL; CARRIER PROTEINS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL TRANSFORMATION, VIRAL; DNA-BINDING PROTEINS; EPITHELIUM; GENES, MYB; HUMANS; HYPERPLASIA; LUNG; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 7; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; ONCOGENE PROTEIN V-AKT; PRECANCEROUS CONDITIONS; PULMONARY ALVEOLI; TRANSCRIPTION FACTORS; UTEROGLOBIN;

EID: 34249103543     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.3700552     Document Type: Article

References (61)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-130.
2. Borges M, Linnoila RI, van de Velde HJ, et al. An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 1997;386:852-855.
3. Ledent V, Paquet O, Vervoort M. Phylogenetic analysis of the human basic helix-loop-helix proteins. Genome Biol 2002;3:research0030.1-research0030.18.
4. Huber K, Bruhl B, Guillemot F, et al. Development of chromaffin cells depends on MASH1 function. Development 2002;129:4729-4738.
5. Lanigan TM, DeRaad SK, Russo AF. Requirement of the MASH-1 transcription factor for neuroendocrine differentiation of thyroid C cells. J Neurobiol 1998;34:126-134.
6. Kameda Y. Mash1 is required for glomus cell formation in the mouse carotid body. Dev Biol 2005;283:128-139.
7. Linnoila RI. Functional facets of the pulmonary neuroendocrine system. Lab Invest 2006;86:425-444.
8. Ito T, Udaka N, Yazawa T, et al. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 2000;127:3913-3921.
9. Schuurmans C, Guillemot F. Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr Opin Neurobiol 2002;12:26-34.
10. Sommer L, Shah N, Rao M, et al. The cellular function of MASH1 in autonomic neurogenesis. Neuron 1995;15:1245-1258.
11. Osada H, Tatematsu Y, Yatabe Y, et al. ASH1 gene is a specific therapeutic target for lung cancers with neuroendocrine features. Cancer Res 2005;65:10680-10685.
12. Ray MK, Magdaleno SW, Finegold MJ, et al. cis-acting elements involved in the regulation of mouse Clara cell-specific 10-kDa protein gene. In vitro and in vivo analysis. J Biol Chem 1995;270:2689-2694.
13. Margraf LR, Finegold MJ, Stanley LA, et al. Cloning and tissue-specific expression of the cDNA for the mouse Clara cell 10 kD protein: comparison of endogenous expression to rabbit uteroglobin promoter-driven transgene expression. Am J Respir Cell Mol Biol 1993;9:231-238.
14. Brody AR, Hook GE, Cameron GS, et al. The differentiation capacity of Clara cells isolated from the lungs of rabbits. Lab Invest 1987;57:219-229.
15. Evans MJ, Cabral-Anderson LJ, Freeman G. Role of the Clara cell in renewal of the bronchiolar epithelium. Lab Invest 1978;38:648-653.
16. 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.
17. 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.
18. 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.
19. Kim CF, Jackson EL, Woolfenden AE, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823-835.
20. Nettesheim P, Szakal AK. Morphogenesis of alveolar bronchiolization. Lab Invest 1972;26:210-219.
21. Jensen-Taubman SM, Steinberg SM, Linnoila RI. Bronchiolization of the alveoli in lung cancer: pathology, patterns of differentiation and oncogene expression. Int J Cancer 1998;75:489-496.
22. Linnoila RI, Jensen SM, Steinberg SM, et al. Peripheral airway cell marker expression in non-small cell lung carcinoma. Association with distinct clinicopathologic features. Am J Clin Pathol 1992;97:233-243.
23. Yang Y, Zhang Z, Mukherjee AB, Linnoila RI. Increased susceptibility of mice lacking Clara cell 10-kDa protein to lung tumorigenesis by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone, a potent carcinogen in cigarette smoke. J Biol Chem 2004;279:29336-29340.
24. Tamaoki J, Tagaya E, Kawatani K, et al. Airway mucosal thickening and bronchial hyperresponsiveness induced by inhaled beta 2-agonist in mice. Chest 2004;126:205-212.
25. Betsuyaku T, Griffin GL, Watson MA, et al. Laser capture microdissection and real-time reverse transcriptase/polymerase chain reaction of bronchiolar epithelium after bleomycin. Am J Respir Cell Mol Biol 2001;25:278-284.
26. Jones MB, Krutzsch H, Shu H, et al. Proteomic analysis and identification of new biomarkers and therapeutic targets for invasive ovarian cancer. Proteomics 2002;2:76-84.
27. Sriuranpong V, Borges MW, Ravi RK, et al. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res 2001;61:3200-3205.
28. Tsurutani J, Castillo SS, Brognard J, et al. Tobacco components stimulate Akt-dependent proliferation and NF{kappa}B-dependent survival in lung cancer cells. Carcinogenesis 2005;26:1182-1195.
29. Westerman BA, Neijenhuis S, Poutsma A, et al. Quantitative reverse transcription-polymerase chain reaction measurement of HASH1 (ASCL1), a marker for small cell lung carcinomas with neuroendocrine features. Clin Cancer Res 2002;8:1082-1086.
30. Gibson UE, Heid CA, Williams PM. A novel method for real time quantitative RT-PCR. Genome Res 1996;6:995-1001.
31. Neuringer IP, Randell SH. Stem cells and repair of lung injuries. Respir Res 2004;5:6.
32. Hu Y, Wang T, Stormo GD, et al. RNA interference of achaete-scute homolog 1 in mouse prostate neuroendocrine cells reveals its gene targets and DNA binding sites. Proc Natl Acad Sci USA 2004;101:5559-5564.
33. Ramsay RG, Barton AL, Gonda TJ. Targeting c-Myb expression in human disease. Expert Opin Ther Targets 2003;7:235-248.
34. Wilson CL, Matrisian LM. Matrilysin: an epithelial matrix metalloproteinase with potentially novel functions. Int J Biochem Cell Biol 1996;28:123-136.
35. Parks WC, Shapiro SD. Matrix metalloproteinases in lung biology. Respir Res 2001;2:10-19.
36. West KA, Linnoila IR, Belinsky SA, et al. Tobacco carcinogen-induced cellular transformation increases activation of the phosphatidylinositol 3'-kinase/Akt pathway in vitro and in vivo. Cancer Res 2004;64:446-451.
37. Have-Opbroek AA, De Vries EC. Clara cell differentiation in the mouse: ultrastructural morphology and cytochemistry for surfactant protein A and Clara cell 10 kD protein. Microsc Res Tech 1993;26:400-411.
38. Perl AK, Wert SE, Nagy A, et al. Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc Natl Acad Sci USA 2002;99:10482-10487.
39. Amy RW, Bowes D, Burri PH, et al. Postnatal growth of the mouse lung. J Anat 1977;124:131-151.
40. Ferron PE, Bagni I, Guidoboni M, et al. Combined and sequential expression of p53, Rb, Ras and Bcl-2 in bronchial preneoplastic lesions. Tumori 1997;83:587-593.
41. Tsao AS, McDonnell T, Lam S, et al. Increased phospho-AKT (Ser(473)) expression in bronchial dysplasia: implications for lung cancer prevention studies. Cancer Epidemiol Biomarkers Prev 2003;12:660-664.
42. Massion PP, Taflan PM, Shyr Y, et al. Early involvement of the phosphatidylinositol 3-kinase/Akt pathway in lung cancer progression. Am J Respir Crit Care Med 2004;170:1088-1094.
43. Balsara BR, Pei J, Mitsuuchi Y, et al. Frequent activation of AKT in non-small cell lung carcinomas and preneoplastic bronchial lesions. Carcinogenesis 2004;25:2053-2059.
44. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002;2:647-656.
45. Tsujimoto Y. Cell death regulation by the Bcl-2 protein family in the mitochondria. J Cell Physiol 2003;195:158-167.
46. Testa JR, Bellacosa A. AKT plays a central role in tumorigenesis. Proc Natl Acad Sci USA 2001;98:10983-10985.
47. Okudela K, Hayashi H, Ito T, et al. K-ras gene mutation enhances motility of immortalized airway cells and lung adenocarcinoma cells via Akt activation: possible contribution to non-invasive expansion of lung adenocarcinoma. Am J Pathol 2004;164:91-100.
48. Kumar BS, Huang J, Persaud S, et al. Down-regulation of Bcl-2 is associated with cisplatin resistance in human small cell lung cancer H69 cells. Mol Cancer Ther 2004;3:327-334.
49. Tsurutani J, West KA, Sayyah J, et al. Inhibition of the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway but not the MEK/ERK pathway attenuates laminin-mediated small cell lung cancer cellular survival and resistance to imatinib mesylate or chemotherapy. Cancer Res 2005;65:8423-8432.
50. Polette M, Nawrocki-Raby B, Gilles C, et al. Tumour invasion and matrix metalloproteinases. Crit Rev Oncol Hematol 2004;49:179-186.
51. Newell KJ, Witty JP, Rodgers WH, et al. Expression and localization of matrix-degrading metalloproteinases during colorectal tumorigenesis. Mol Carcinog 1994;10:199-206.
52. Takeuchi N, Ichikawa Y, Ishikawa T, et al. Matrilysin gene expression in sporadic and familial colorectal adenomas. Mol Carcinog 1997;19:225-229.
53. McDonnell S, Navre M, Coffey Jr RJ, et al. Expression and localization of the matrix metalloproteinase pump-Date: 1 (MMP-7) in human gastric and colon carcinomas. Mol Carcinog 1991;4:527-533.
54. Knox JD, Wolf C, McDaniel K, et al. Matrilysin expression in human prostate carcinoma. Mol Carcinog 1996;15:57-63.
55. Heppner KJ, Matrisian LM, Jensen RA, et al. Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Am J Pathol 1996;149:273-282.
56. Shigemasa K, Tanimoto H, Sakata K, et al. Induction of matrix metalloprotease-7 is common in mucinous ovarian tumors including early stage disease. Med Oncol 2000;17:52-58.
57. Wilson CL, Heppner KJ, Labosky PA, et al. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA 1997;94:1402-1407.
58. Rudolph-Owen LA, Chan R, Muller WJ, et al. The matrix metalloproteinase matrilysin influences early-stage mammary tumorigenesis. Cancer Res 1998;58:5500-5506.
59. Cogswell JP, Cogswell PC, Kuehl WM, et al. Mechanism of c-myc regulation by c-Myb in different cell lineages. Mol Cell Biol 1993;13:2858-2869.
60. Kaspar P, Pajer P, Sedlak D, et al. c-Myb inhibits myogenic differentiation through repression of MyoD. Exp Cell Res 2005;309:419-428.
61. Thompson MA, Rosenthal MA, Ellis SL, et al. c-Myb down-regulation is associated with human colon cell differentiation, apoptosis, and decreased Bcl-2 expression. Cancer Res 1998;58:5168-5175.