GATA2 is epigenetically repressed in human and mouse lung tumors and is not requisite for survival of KRAS mutant lung cancer

Journal of Thoracic Oncology

Volumn 9, Issue 6, 2014, Pages 784-793

  Tessema, Mathewos ^a   Yingling, Christin M ^a   Snider, Amanda M ^a   Do, Kieu ^a   Juri, Daniel E ^a   Picchi, Maria A ^a   Zhang, Xiequn ^a   Liu, Yushi ^a   Leng, Shuguang ^a   Tellez, Carmen S ^a   Belinsky, Steven A ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

Author keywords

Carcinogenesis; Epigenetics; GATA2; K RAS; Mutation

Indexed keywords

CYTOSINE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR GATA 2; GATA2 PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; KRAS2 PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN P21; RAS PROTEIN;

ANIMAL CELL; ARTICLE; CANCER CELL LINE; CANCER SURVIVAL; CELL SURVIVAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GATA2 GENE; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG CARCINOGENESIS; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE K RAS; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; CELL DEATH; CELL TRANSFORMATION; CHEMICALLY INDUCED; EPIGENETIC REPRESSION; GENE EXPRESSION; GENE SILENCING; GENETICS; LUNG TUMOR; METABOLISM; NON SMALL CELL LUNG CANCER; TUMOR CELL LINE;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLANDS; CYTOSINE; DNA METHYLATION; EPIGENETIC REPRESSION; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MICE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS P21(RAS); RAS PROTEINS;

EID: 84901632668     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1097/JTO.0000000000000165     Document Type: Article

References (44)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Dominioni L, Imperatori A, Rovera F, Ochetti A, Torrigiotti G, Paolucci M. Stage I nonsmall cell lung carcinoma: analysis of survival and implications for screening. Cancer 2000;89(11 Suppl):2334-2344.
3. Pao W, Girard N. New driver mutations in non-small-cell lung cancer. Lancet Oncol 2011;12:175-180.
4. Inoue A, Kobayashi K, Usui K, et al.; North East Japan Gefitinib Study Group. First-line gefitinib for patients with advanced non-small-cell lung cancer harboring epidermal growth factor receptor mutations without indication for chemotherapy. J Clin Oncol 2009;27:1394-1400.
5. Inoue A, Suzuki T, Fukuhara T, et al. Prospective phase II study of gefitinib for chemotherapy-naive patients with advanced non-small-cell lung cancer with epidermal growth factor receptor gene mutations. J Clin Oncol 2006;24:3340-3346. (Pubitemid 46638887)
6. Sequist LV, Martins RG, Spigel D, et al. First-line gefitinib in patients with advanced non-small-cell lung cancer harboring somatic EGFR mutations. J Clin Oncol 2008;26:2442-2449.
7. Bang YJ. Treatment of ALK-positive non-small cell lung cancer. Arch Pathol Lab Med 2012;136:1201-1204.
8. Eder JP, Vande Woude GF, Boerner SA, LoRusso PM. Novel therapeutic inhibitors of the c-Met signaling pathway in cancer. Clin Cancer Res 2009;15:2207-2214.
9. Hainsworth JD, Cebotaru CL, Kanarev V, et al. A phase II, open- label, randomized study to assess the efficacy and safety of AZD6244 (ARRY-142886) versus pemetrexed in patients with non-small cell lung cancer who have failed one or two prior chemotherapeutic regimens. J Thorac Oncol 2010;5:1630-1636.
10. Markman B, Tabernero J, Krop I, et al. Phase I safety, pharmacokinetic, and pharmacodynamic study of the oral phosphatidylinositol-3-kinase and mTOR inhibitor BGT226 in patients with advanced solid tumors. Ann Oncol 2012;23:2399-2408.
11. Tsai J, Lee JT, Wang W, et al. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci U S A 2008;105:3041-3046. (Pubitemid 351723664)
12. Yap TA, Yan L, Patnaik A, et al. First-in-man clinical trial of the oral pan- AKT inhibitor MK-2206 in patients with advanced solid tumors. J Clin Oncol 2011;29:4688-4695.
13. Kumar MS, Hancock DC, Molina-Arcas M, et al. The GATA2 transcriptional network is requisite for RAS oncogene-driven non-small cell lung cancer. Cell 2012;149:642-655.
14. Molkentin JD. The zinc finger-containing transcription factors GATA- 4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression. J Biol Chem 2000;275:38949-38952. (Pubitemid 32058903)
15. Bresnick EH, Martowicz ML, Pal S, Johnson KD. Developmental control via GATA factor interplay at chromatin domains. J Cell Physiol 2005;205:1-9. (Pubitemid 41262845)
16. Vicente C, Conchillo A, García-Sánchez MA, Odero MD. The role of the GATA2 transcription factor in normal and malignant hematopoiesis. Crit Rev Oncol Hematol 2012;82:1-17.
17. Ling KW, Ottersbach K, van Hamburg JP, et al. GATA-2 plays two functionally distinct roles during the ontogeny of hematopoietic stem cells. J Exp Med 2004;200:871-882. (Pubitemid 39362923)
18. Tsai FY, Keller G, Kuo FC, et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 1994;371:221-226. (Pubitemid 24293019)
19. Tsai FY, Orkin SH. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 1997;89:3636-3643. (Pubitemid 27227086)
20. Persons DA, Allay JA, Allay ER, et al. Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood 1999;93:488-499. (Pubitemid 29035730)
21. Fadilah SA, Cheong SK, Roslan H, Rozie-Hanisa M, Yen GK. GATA-1 and GATA-2 gene expression is related to the severity of dysplasia in myelodysplastic syndrome. Leukemia 2002;16:1563-1565.
22. Hahn CN, Chong CE, Carmichael CL, et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat Genet 2011;43:1012-1017.
23. Ostergaard P, Simpson MA, Connell FC, et al. Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nat Genet 2011;43:929-931.
24. Akiyama Y, Watkins N, Suzuki H, et al. GATA-4 and GATA-5 transcription factor genes and potential downstream antitumor target genes are epigenetically silenced in colorectal and gastric cancer. Mol Cell Biol 2003;23:8429-8439. (Pubitemid 37433351)
25. Guo M, Akiyama Y, House MG, et al. Hypermethylation of the GATA genes in lung cancer. Clin Cancer Res 2004;10:7917-7924. (Pubitemid 39587531)
26. Tessema M, Klinge DM, Yingling CM, Do K, Van Neste L, Belinsky SA. Re-expression of CXCL14, a common target for epigenetic silencing in lung cancer, induces tumor necrosis. Oncogene 2010;29:5159-5170.
27. Wakamatsu N, Collins JB, Parker JS, et al. Gene expression studies demonstrate that the K-ras/Erk MAP kinase signal transduction pathway and other novel pathways contribute to the pathogenesis of cumene-induced lung tumors. Toxicol Pathol 2008;36:743-752.
28. Damiani LA, Yingling CM, Leng S, Romo PE, Nakamura J, Belinsky SA. Carcinogen-induced gene promoter hypermethylation is mediated by DNMT1 and causal for transformation of immortalized bronchial epithelial cells. Cancer Res 2008;68:9005-9014.
29. Tellez CS, Juri DE, Do K, et al. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 2011;71:3087-3097.
30. Belinsky SA, Palmisano WA, Gilliland FD, et al. Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res 2002;62:2370-2377. (Pubitemid 34411720)
31. Ramirez RD, Sheridan S, Girard L, et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 2004;64:9027-9034. (Pubitemid 39665513)
32. Belinsky SA, Devereux TR, Foley JF, Maronpot RR, Anderson MW. Role of the alveolar type II cell in the development and progression of pulmonary tumors induced by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in the A/J mouse. Cancer Res 1992;52:3164-3173.
33. Vuillemenot BR, Pulling LC, Palmisano WA, Hutt JA, Belinsky SA. Carcinogen exposure differentially modulates RAR-beta promoter hypermethylation, an early and frequent event in mouse lung carcinogenesis. Carcinogenesis 2004;25:623-629. (Pubitemid 38499951)
34. Tessema M, Yu YY, Stidley CA, et al. Concomitant promoter methylation of multiple genes in lung adenocarcinomas from current, former and never smokers. Carcinogenesis 2009;30:1132-1138.
35. Tessema M, Willink R, Do K, et al. Promoter methylation of genes in and around the candidate lung cancer susceptibility locus 6q23-25. Cancer Res 2008;68:1707-1714. (Pubitemid 351416555)
36. Bibikova M, Barnes B, Tsan C, et al. High density DNA methylation array with single CpG site resolution. Genomics 2011;98: 288-295.
37. Tessema M, Yingling CM, Thomas CL, et al. SULF2 methylation is prognostic for lung cancer survival and increases sensitivity to topoisomerase- I inhibitors via induction of ISG15. Oncogene 2012;31:4107-4116.
38. Leng S, Bernauer AM, Hong C, et al. The A/G allele of rs16906252 predicts for MGMT methylation and is selectively silenced in premalignant lesions from smokers and in lung adenocarcinomas. Clin Cancer Res 2011;17:2014-2023.
39. Tessema M, Yingling CM, Grimes MJ, et al. Differential epigenetic regulation of TOX subfamily high mobility group box genes in lung and breast cancers. PLoS One 2012;7:e34850.
40. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408. (Pubitemid 34164012)
41. Barbacid M. Opening a new GATAway for treating KRAS-driven lung tumors. Cancer Cell 2012;21:598-600.
42. Minegishi N, Ohta J, Suwabe N, et al. Alternative promoters regulate transcription of the mouse GATA-2 gene. J Biol Chem 1998;273: 3625-3634. (Pubitemid 28109788)
43. Pan X, Minegishi N, Harigae H, et al. Identification of human GATA-2 gene distal IS exon and its expression in hematopoietic stem cell fractions. J Biochem 2000;127:105-112. (Pubitemid 30094099)
44. Eickhoff B, Rüller S, Laue T, et al. Trichostatin A modulates expression of p21waf1/cip1, Bcl-xL, ID1, ID2, ID3, CRAB2, GATA-2, hsp86 and TFIID/TAFII31 mRNA in human lung adenocarcinoma cells. Biol Chem 2000;381:107-112. (Pubitemid 30130733)