Foxm1 transcription factor is required for the initiation of lung tumorigenesis by oncogenic KrasG12D

Oncogene

Volumn 33, Issue 46, 2014, Pages 5391-5396

  Wang, I C ^a,b   Ustiyan, V ^a   Zhang, Y ^a   Cai, Y ^a   Kalin, T V ^a   Kalinichenko, V V ^a  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

FOXM1; K Ras; Non small cell lung cancer; Transgenic mice

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; FORKHEAD BOX PROTEIN M1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SECURIN; STRESS ACTIVATED PROTEIN KINASE; ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, MOUSE; KRAS2 PROTEIN, MOUSE; PROTEIN BINDING; PROTEIN P21;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA BINDING; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE OVEREXPRESSION; HISTOPATHOLOGY; HUMAN; IKBKB GENE; JNK1 GENE; LUNG CANCER; LUNG CARCINOGENESIS; MOUSE; NFKB1 GENE; NFKB2 GENE; NONHUMAN; ONCOGENE; ONCOGENE C MYB; ONCOGENE K RAS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN TARGETING; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CARCINOGENESIS; DRUG EFFECTS; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; LUNG; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLOTTING, WESTERN; CARCINOGENESIS; DOXORUBICIN; EPITHELIUM; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUNG; LUNG NEOPLASMS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS P21(RAS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 85028143024     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.475     Document Type: Article

References (33)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74–108.
2. Alberg AJ, Samet JM. Epidemiology of lung cancer. Chest 2003; 123: 21S–49S.
3. Kim IM, Ackerson T, Ramakrishna S, Tretiakova M, Wang IC, Kalin TV et al. The forkhead box m1 transcription factor stimulates the proliferation of tumor cells during development of lung cancer. Cancer Res 2006; 66: 2153–2161.
4. Costa RH, Kalinichenko VV, Major ML, Raychaudhuri P. New and unexpected: forkhead meets ARF. Curr Opin Genet Dev 2005; 15: 42–48.
5. Kalin TV, Ustiyan V, Kalinichenko VV. Multiple faces of FoxM1 transcription factor: lessons from transgenic mouse models. Cell cycle (Georgetown, Tex) 2011; 10: 396–405.
6. Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet 2006; 38: 1043–1048.
7. 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: 4137–4149.
8. Wang IC, Meliton L, Ren X, Zhang Y, Balli D, Snyder J et al. Deletion of Forkhead Box M1 transcription factor from respiratory epithelial cells inhibits pulmonary tumorigenesis. PLoS One 2009; 4: e6609.
9. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ 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: 3249–3262.
10. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001; 15: 3243–3248.
11. Johnson L, Mercer K, Greenbaum D, Bronson RT, Crowley D, Tuveson DA et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001; 410: 1111–1116.
12. Major ML, Lepe R, Costa RH. Forkhead Box M1B (FoxM1B) transcriptional activity requires binding of Cdk/Cyclin complexes for phosphorylation-dependent recruitment of p300/cbp co-activators. Mol Cell Biol 2004; 24: 2649–2661.
13. Ma RY, Tong TH, Cheung AM, Tsang AC, Leung WY, Yao KM. Raf/MEK/MAPK signaling stimulates the nuclear translocation and transactivating activity of FOXM1c. J Cell Sci 2005; 118: 795–806.
14. Wang IC, Snyder J, Zhang Y, Lander J, Nakafuku Y, Lin J et al. Foxm1 mediates cross talk between Kras/mitogen-activated protein kinase and canonical Wnt pathways during development of respiratory epithelium. Mol Cell Biol 2012; 32: 3838–3850.
15. Behren A, Muhlen S, Acuna Sanhueza GA, Schwager C, Plinkert PK, Huber PE et al. Phenotype-assisted transcriptome analysis identifies FOXM1 downstream from Ras-MKK3-p38 to regulate in vitro cellular invasion. Oncogene 2010; 29: 1519–1530.
16. Kalin TV, Wang IC, Meliton L, Zhang Y, Wert SE, Ren X et al. Forkhead Box m1 transcription factor is required for perinatal lung function. Proc Natl Acad Sci USA 2008; 105: 19330–19335.
17. Sweet-Cordero A, Mukherjee S, Subramanian A, You H, Roix JJ, Ladd-Acosta C et al. An oncogenic KRAS2 expression signature identified by cross-species gene-expression analysis. Nat Genet 2005; 37: 48–55.
18. Watters JW, Roberts CJ. Developing gene expression signatures of pathway deregulation in tumors. Mol Cancer Ther 2006; 5: 2444–2449.
19. Acosta JC, O’Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008; 133: 1006–1018.
20. Ahn YH, Yang Y, Gibbons DL, Creighton CJ, Yang F, Wistuba II et al. Map2k4 functions as a tumor suppressor in lung adenocarcinoma and inhibits tumor cell invasion by decreasing peroxisome proliferator-activated receptor gamma2 expression. Mol Cell Biol 2011; 31: 4270–4285.
21. Magudia K, Lahoz A, Hall A. K-Ras and B-Raf oncogenes inhibit colon epithelial polarity establishment through up-regulation of c-myc. J Cell Biol 2012; 198: 185–194.
22. Shin S, Dimitri CA, Yoon SO, Dowdle W, Blenis J. ERK2 but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signaling events. Mol Cell 2010; 38: 114–127.
23. Whitsett JA, Glasser SW. Regulation of surfactant protein gene transcription. Biochim Biophys Acta 1998; 19: 2–3.
24. Iwao K, Watanabe T, Fujiwara Y, Takami K, Kodama K, Higashiyama M et al. Isolation of a novel human lung-specific gene, LUNX, a potential molecular marker for detection of micrometastasis in non-small-cell lung cancer. Int J Cancer 2001; 91: 433–437.
25. Koishi R, Ando Y, Ono M, Shimamura M, Yasumo H, Fujiwara T et al. Angptl3 regulates lipid metabolism in mice. Nat Genet 2002; 30: 151–157.
26. Kwei KA, Kim YH, Girard L, Kao J, Pacyna-Gengelbach M, Salari K et al. Genomic profiling identifies TITF1 as a lineage-specific oncogene amplified in lung cancer. Oncogene 2008; 27: 3635–3640.
27. Whitsett JA, Wert SE, Weaver TE. Alveolar surfactant homeostasis and the pathogenesis of pulmonary disease. Ann Rev Med 2010; 61: 105–119.
28. Ihara Y, Kihara Y, Hamano F, Yanagida K, Morishita Y, Kunita A et al. The G protein-coupled receptor T-cell death-associated gene 8 (TDAG8) facilitates tumor development by serving as an extracellular pH sensor. Proc Natl Acad Sci USA 2010; 107: 17309–17314.
29. Zhou Y, Rideout III WM, Zi T, Bressel A, Reddypalli S, Rancourt R et al. Chimeric mouse tumor models reveal differences in pathway activation between ERBB family-and KRAS-dependent lung adenocarcinomas. Nat Biotechnol 2010; 28: 71–78.
30. Cellurale C, Sabio G, Kennedy NJ, Das M, Barlow M, Sandy P et al. Requirement of c-Jun NH(2)-terminal kinase for Ras-initiated tumor formation. Mol Cell Biol 2011; 31: 1565–1576.
31. Wang IC, Chen YJ, Hughes DE, Ackerson T, Major ML, Kalinichenko VV et al. FOXM1 regulates transcription of JNK1 to promote the G1/S transition and tumor cell invasiveness. J Biol Chem 2008; 283: 20770–20778.
32. Meylan E, Dooley AL, Feldser DM, Shen L, Turk E, Ouyang C et al. Requirement for NF-kappaB signalling in a mouse model of lung adenocarcinoma. Nature 2009; 462: 104–107.
33. Wang IC, Zhang Y, Snyder J, Sutherland MJ, Burhans MS, Shannon JM et al. Increased expression of FoxM1 transcription factor in respiratory epithelium inhibits lung sacculation and causes Clara cell hyperplasia. Dev Biol 2010; 347: 301–314.