KrasG12D and Nkx2-1 haploinsufficiency induce mucinous adenocarcinoma of the lung

Journal of Clinical Investigation

Volumn 122, Issue 12, 2012, Pages 4388-4400

  Maeda, Yutaka ^a   Tsuchiya, Tomoshi ^b   Hao, Haiping ^c   Tompkins, David H ^a   Xu, Yan ^a   Mucenski, Michael L ^a   Du, Lingling ^a   Keiser, Angela R ^a   Fukazawa, Takuya ^d   Naomoto, Yoshio ^d   Nagayasu, Takeshi ^b   Whitsett, Jeffrey A ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b Graduate School of Biomedical Sciences   (Japan)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d KAWASAKI MEDICAL SCHOOL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AP 1 PROTEIN; KRAS PROTEIN; NK2 HOMEOBOX 1 PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CHRONIC LUNG DISEASE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ASSOCIATION; GOBLET CELL; HAPLOINSUFFICIENCY; HUMAN; IN VIVO STUDY; LUNG ADENOCARCINOMA; LUNG TUMOR; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOCARCINOMA, MUCINOUS; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION, NEOPLASTIC; GOBLET CELLS; HAPLOINSUFFICIENCY; HEPATOCYTE NUCLEAR FACTOR 3-GAMMA; HUMANS; LUNG NEOPLASMS; MICE; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-ETS; PROTO-ONCOGENE PROTEINS P21(RAS); PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TUMOR BURDEN; URETHANE;

EID: 84870547933     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64048     Document Type: Article

References (57)

1. Travis WD, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6(2):244-285.
2. Subramanian J, Govindan R. Molecular genetics of lung cancer in people who have never smoked. Lancet Oncol. 2008;9(7):676-682. (Pubitemid 351878053)
3. Maeda Y, Davé V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev. 2007;87(1):219-244. (Pubitemid 46207714)
4. Maeda Y, et al. Airway epithelial transcription factor NK2 homeobox 1 inhibits mucous cell metaplasia and Th2 inflammation. Am J Respir Crit Care Med. 2011;184(4):421-429.
5. Kendall J, et al. Oncogenic cooperation and coamplification of developmental transcription factor genes in lung cancer. Proc Natl Acad Sci U S A. 2007;104(42):16663-16668. (Pubitemid 350211073)
6. Weir BA, et al. Characterizing the cancer genome in lung adenocarcinoma. Nature. 2007;450(7171):893-898. (Pubitemid 350231325)
7. Kwei KA, et al. Genomic profiling identifies TITF1 as a lineage-specific oncogene amplified in lung cancer. Oncogene. 2008;27(25):3635-3640. (Pubitemid 351793793)
8. Tanaka H, et al. Lineage-specific dependency of lung adenocarcinomas on the lung development regulator TTF-1. Cancer Res. 2007;67(13):6007-6011. (Pubitemid 47037477)
9. Yamaguchi T, et al. NKX2-1/TITF1/TTF-1-induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer Cell. 2012;21(3):348-361.
10. Winslow MM, et al. Suppression of lung adenocarcinoma progression by Nkx2-1. Nature. 2011;473(7345):101-104.
11. Hosono Y, et al. MYBPH, a transcriptional target of TTF-1, inhibits ROCK1, and reduces cell motility and metastasis. EMBO J. 2011;31(2):481-493.
12. Fisher GH, 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(24):3249-3262. (Pubitemid 34008191)
13. Kimura S, et al. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev. 1996;10(1):60-69. (Pubitemid 26025299)
14. Zhang Y, et al. GATA and Nkx factors synergistically regulate tissue-specific gene expression and development in vivo. Development. 2007;134(1):189-198. (Pubitemid 46152719)
15. Chen G, et al. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J Clin Invest. 2009;119(10):2914-2924.
16. Chen G, et al. Foxa2 programs Th2 cell-mediated innate immunity in the developing lung. J Immunol. 2010;184(11):6133-6141.
17. Park KS, et al. SPDEF regulates goblet cell hyperplasia in the airway epithelium. J Clin Invest. 2007;117(4):978-988.
18. Politi K, Zakowski MF, Fan PD, Schonfeld EA, Pao W, Varmus HE. 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. 2006;20(11):1496-1510. (Pubitemid 43830656)
19. Engelman JA, et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat Med. 2008;14(12):1351-1356.
20. Stathopoulos GT, et al. Epithelial NF-kappaB activation promotes urethane-induced lung carcinogenesis. Proc Natl Acad Sci U S A. 2007;104(47):18514-18519. (Pubitemid 350210728)
21. Malkinson AM. Primary lung tumors in mice as an aid for understanding, preventing, and treating human adenocarcinoma of the lung. Lung Cancer. 2001;32(3):265-279. (Pubitemid 32487687)
22. Ramirez RD, et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 2004;64(24):9027-9034. (Pubitemid 39665513)
23. Lewis CC, et al. Unique and overlapping gene expression patterns driven by IL-4 and IL-13 in the mouse lung. J Allergy Clin Immunol. 2009;123(4):795-804.
24. Kolla V, et al. Thyroid transcription factor in differentiating type II cells: regulation, isoforms, and target genes. Am J Respir Cell Mol Biol. 2007;36(2):213-225. (Pubitemid 46233475)
25. Saito RA, et al. Thyroid transcription factor-1 inhibits transforming growth factor-beta-mediated epithelial-to-mesenchymal transition in lung adenocarcinoma cells. Cancer Res. 2009;69(7):2783-2791.
26. Behrens C, et al. Immunohistochemical expression of basic fibroblast growth factor and fibroblast growth factor receptors 1 and 2 in the pathogenesis of lung cancer. Clin Cancer Res. 2008;14(19):6014-6022.
27. Spinola M, et al. Functional FGFR4 Gly388Arg polymorphism predicts prognosis in lung adenocarcinoma patients. J Clin Oncol. 2005;23(29):7307-7311. (Pubitemid 46202344)
28. Fürstenberger G, Senn HJ. Insulin-like growth factors and cancer. Lancet Oncol. 2002;3(5):298-302. (Pubitemid 34546447)
29. Chen BB, Glasser JR, Coon TA, Mallampalli RK. F-box protein FBXL2 exerts human lung tumor suppressor-like activity by ubiquitin-mediated degradation of cyclin D3 resulting in cell cycle arrest. Oncogene. 2012;31(20):2566-2579.
30. Wang IC, Meliton L, Tretiakova M, Costa RH, Kalinichenko VV, Kalin TV. Transgenic expression of the forkhead box M1 transcription factor induces formation of lung tumors. Oncogene. 2008;27(30):4137-4149. (Pubitemid 351969912)
31. Laman H, et al. Transforming activity of Fbxo7 is mediated specifically through regulation of cyclin D/cdk6. EMBO J. 2005;24(17):3104-3116. (Pubitemid 41486346)
32. Owen-Schaub LB. Fas function and tumor progression: use it and lose it. Cancer Cell. 2002;2(2):95-96. (Pubitemid 41039108)
33. Finan KM, et al. In vitro susceptibility to the proapoptotic effects of TIMP-3 gene delivery translates to greater in vivo efficacy versus gene delivery for TIMPs-1 or -2. Lung Cancer. 2006;53(3):273-284. (Pubitemid 44189570)
34. Anagnostou VK, Syrigos KN, Bepler G, Homer RJ, Rimm DL. Thyroid transcription factor 1 is an independent prognostic factor for patients with stage I lung adenocarcinoma. J Clin Oncol. 2009;27(2):271-278.
35. O'Byrne KJ, et al. Molecular biomarkers in non-small-cell lung cancer: a retrospective analysis of data from the phase 3 FLEX study. Lancet Oncol. 2011;12(8):795-805.
36. Bruno MD, Bohinski RJ, Huelsman KM, Whitsett JA, Korfhagen TR. Lung cell-specific expression of the murine surfactant protein A (SP-A) gene is mediated by interactions between the SP-A promoter and thyroid transcription factor-1. J Biol Chem. 1995;270(12):6531-6536.
37. Islam KN, Mendelson CR. Permissive effects of oxygen on cyclic AMP and interleukin-1 stimulation of surfactant protein A gene expression are mediated by epigenetic mechanisms. Mol Cell Biol. 2006;26(8):2901-2912.
38. MacQuarrie KL, Fong AP, Morse RH, Tapscott SJ. Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet. 2011;27(4):141-148.
39. Majewski J, Ott J. Distribution and characterization of regulatory elements in the human genome. Genome Res. 2002;12(12):1827-1836. (Pubitemid 35469931)
40. Bohinski RJ, Di Lauro R, Whitsett JA. The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol Cell Biol. 1994;14(9):5671-5681.
41. Heintz NH, Janssen-Heininger YM, Mossman BT. Asbestos, lung cancers, and mesotheliomas: from molecular approaches to targeting tumor survival pathways. Am J Respir Cell Mol Biol. 2010;42(2):133-139.
42. Gensch E, et al. Tobacco smoke control of mucin production in lung cells requires oxygen radicals AP-1 and JNK. J Biol Chem. 2004;279(37):39085-39093. (Pubitemid 39296071)
43. Kato S, et al. MUC5AC mucin gene regulation in pancreatic cancer cells. Int J Oncol. 2006;29(1):33-40.
44. Adiseshaiah P, Lindner DJ, Kalvakolanu DV, Reddy SP. FRA-1 proto-oncogene induces lung epithelial cell invasion and anchorage-independent growth in vitro, but is insufficient to promote tumor growth in vivo. Cancer Res. 2007;67(13):6204-6211. (Pubitemid 47037501)
45. Wan H, et al. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development. 2004;131(4):953-964. (Pubitemid 38263209)
46. Plantier L, et al. Ectopic respiratory epithelial cell differentiation in bronchiolised distal airspaces in idiopathic pulmonary fibrosis. Thorax. 2011;66(8):651-657.
47. Hoshi S, et al. Role of NKX2-1 in N-bis(2-hydroxypropyl)-nitrosamine- induced thyroid adenoma in mice. Carcinogenesis. 2009;30(9):1614-1619.
48. Ji H, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature. 2007;448(7155):807-810. (Pubitemid 47266337)
49. Tang X, et al. Abnormalities of the TITF-1 lineage-specific oncogene in NSCLC: implications in lung cancer pathogenesis and prognosis. Clin Cancer Res. 2011;17(8):2434-2443.
50. Tian J, Mahmood R, Hnasko R, Locker J. Loss of Nkx2.8 deregulates progenitor cells in the large airways and leads to dysplasia. Cancer Res. 2006;66(21):10399-10407. (Pubitemid 44799760)
51. Harris T, et al. Both gene amplification and allelic loss occur at 14q13.3 in lung cancer. Clin Cancer Res. 2011;17(4):690-699.
52. Whitsett JA, Haitchi HM, Maeda Y. Intersections between pulmonary development and disease. Am J Respir Crit Care Med. 2011;184(4):401-406.
53. Bass AJ, et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet. 2009;41(11):1238-1242.
54. Wright GW, Simon RM. A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics. 2003;19(18):2448-2455. (Pubitemid 38016644)
55. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
56. Robinson JT, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29(1):24-26.
57. Ji H, Jiang H, Ma W, Johnson DS, Myers RM, Wong WH. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat Biotechnol. 2008;26(11):1293-1300.