Runx3 Inactivation Is a Crucial Early Event in the Development of Lung Adenocarcinoma

Cancer Cell

Volumn 24, Issue 5, 2013, Pages 603-616

  Lee, You Soub ^a   Lee, Jung Won ^a   Jang, Ju Won ^a   Chi, Xin Zi ^a   Kim, Jang Hyun ^a   Li, Ying Hui ^a   Kim, Min Kyu ^a   Kim, Da Mi ^a   Choi, Byeung Sub ^a   Kim, Eung Gook ^a   Chung, Jin Haeng ^b   Lee, Ok Jun ^a   Lee, You Mie ^c   Suh, Joo Won ^d   Chuang, LindaShyueHuey ^e   Ito, Yoshiaki ^e   Bae, Suk Chul ^a  

^a Chungbuk National University College of Medicine   (South Korea)

^b Seoul National University Bundang Hospital   (South Korea)

^c Kyungpook National University   (South Korea)

^d Myong Ji University   (South Korea)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; K RAS PROTEIN; PROTEIN P14; PROTEIN P21; TRANSCRIPTION FACTOR RUNX3;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL STIMULATION; CELL STRAIN HEK293; GENE EXPRESSION; GENE INACTIVATION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; LUNG ALVEOLUS EPITHELIUM; LUNG CARCINOGENESIS; MOUSE; NONHUMAN; ONCOGENE K RAS; PRIORITY JOURNAL;

EID: 84887533067     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.10.003     Document Type: Article

References (47)

1. Abbas T., Dutta A. p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer 2009, 9:400-414.
2. Adnane J., Jackson R.J., Nicosia S.V., Cantor A.B., Pledger W.J., Sebti S.M. Loss of p21WAF1/CIP1 accelerates Ras oncogenesis in a transgenic/knockout mammary cancer model. Oncogene 2000, 19:5338-5347.
3. Aslanian A., Iaquinta P.J., Verona R., Lees J.A. Repression of the Arf tumor suppressor by E2F3 is required for normal cell cycle kinetics. Genes Dev. 2004, 18:1413-1422.
4. Bakshi R., Hassan M.Q., Pratap J., Lian J.B., Montecino M.A., van Wijnen A.J., Stein J.L., Imbalzano A.N., Stein G.S. The human SWI/SNF complex associates with RUNX1 to control transcription of hematopoietic target genes. J.Cell. Physiol. 2010, 225:569-576.
5. Beck C.A., Weigel N.L., Edwards D.P. Effects of hormone and cellular modulators of protein phosphorylation on transcriptional activity, DNA binding, and phosphorylation of human progesterone receptors. Mol. Endocrinol. 1992, 6:607-620.
6. Borgdorff V., Lleonart M.E., Bishop C.L., Fessart D., Bergin A.H., Overhoff M.G., Beach D.H. Multiple microRNAs rescue from Ras-induced senescence by inhibiting p21(Waf1/Cip1). Oncogene 2010, 29:2262-2271.
7. Chi X.Z., Yang J.O., Lee K.Y., Ito K., Sakakura C., Li Q.L., Kim H.R., Cha E.J., Lee Y.H., Kaneda A., et al. RUNX3 suppresses gastric epithelial cell growth by inducing p21(WAF1/Cip1) expression in cooperation with transforming growth factor beta-activated SMAD. Mol. Cell. Biol. 2005, 25:8097-8107.
8. Chi X.Z., Kim J., Lee Y.H., Lee J.W., Lee K.S., Wee H., Kim W.J., Park W.Y., Oh B.C., Stein G.S., et al. Runt-related transcription factor RUNX3 is a target of MDM2-mediated ubiquitination. Cancer Res. 2009, 69:8111-8119.
9. Denis G.V., McComb M.E., Faller D.V., Sinha A., Romesser P.B., Costello C.E. Identification of transcription complexes that contain the double bromodomain protein Brd2 and chromatin remodeling machines. J.Proteome Res. 2006, 5:502-511.
10. DuPage M., Dooley A.L., Jacks T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat. Protoc. 2009, 4:1064-1072.
11. Efeyan A., Serrano M. p53: guardian of the genome and policeman of the oncogenes. Cell Cycle 2007, 6:1006-1010.
12. Feldser D.M., Kostova K.K., Winslow M.M., Taylor S.E., Cashman C., Whittaker C.A., Sanchez-Rivera F.J., Resnick R., Bronson R., Hemann M.T., Jacks T. Stage-specific sensitivity to p53 restoration during lung cancer progression. Nature 2010, 468:572-575.
13. Gontan C., de Munck A., Vermeij M., Grosveld F., Tibboel D., Rottier R. Sox2 is important for two crucial processes in lung development: branching morphogenesis and epithelial cell differentiation. Dev. Biol. 2008, 317:296-309.
14. Guo N., Faller D.V., Denis G.V. Activation-induced nuclear translocation of RING3. J.Cell Sci. 2000, 113:3085-3091.
15. Ito K., Lim A.C., Salto-Tellez M., Motoda L., Osato M., Chuang L.S., Lee C.W., Voon D.C., Koo J.K., Wang H., et al. RUNX3 attenuates beta-catenin/T cell factors in intestinal tumorigenesis. Cancer Cell 2008, 14:226-237.
16. Jackson E.L., Willis N., Mercer K., Bronson R.T., Crowley D., Montoya R., Jacks T., Tuveson D.A. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 2001, 15:3243-3248.
17. Jin Y.H., Jeon E.J., Li Q.L., Lee Y.H., Choi J.K., Kim W.J., Lee K.Y., Bae S.C. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J.Biol. Chem. 2004, 279:29409-29417.
18. Junttila M.R., Karnezis A.N., Garcia D., Madriles F., Kortlever R.M., Rostker F., Brown Swigart L., Pham D.M., Seo Y., Evan G.I., Martins C.P. Selective activation of p53-mediated tumour suppression in high-grade tumours. Nature 2010, 468:567-571.
19. Kilbey A., Terry A., Cameron E.R., Neil J.C. Oncogene-induced senescence: an essential role for Runx. Cell Cycle 2008, 7:2333-2340.
20. Kim C.F., Jackson E.L., Woolfenden A.E., Lawrence S., Babar I., Vogel S., Crowley D., Bronson R.T., Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005, 121:823-835.
21. Kim W.J., Kim E.J., Jeong P., Quan C., Kim J., Li Q.L., Yang J.O., Ito Y., Bae S.C. RUNX3 inactivation by point mutations and aberrant DNA methylation in bladder tumors. Cancer Res. 2005, 65:9347-9354.
22. Komori H., Enomoto M., Nakamura M., Iwanaga R., Ohtani K. Distinct E2F-mediated transcriptional program regulates p14ARF gene expression. EMBO J. 2005, 24:3724-3736.
23. Kruse J.P., Gu W. Modes of p53 regulation. Cell 2009, 137:609-622.
24. Lee K.S., Lee Y.S., Lee J.M., Ito K., Cinghu S., Kim J.H., Jang J.W., Li Y.H., Goh Y.M., Chi X.Z., et al. Runx3 is required for the differentiation of lung epithelial cells and suppression of lung cancer. Oncogene 2010, 29:3349-3361.
25. LeRoy G., Rickards B., Flint S.J. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Mol. Cell 2008, 30:51-60.
26. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell 1997, 88:323-331.
27. Li Q.L., Ito K., Sakakura C., Fukamachi H., Inoue Ki., Chi X.Z., Lee K.Y., Nomura S., Lee C.W., Han S.B., et al. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 2002, 109:113-124.
28. Li Q.L., Kim H.R., Kim W.J., Choi J.K., Lee Y.H., Kim H.M., Li L.S., Kim H., Chang J., Ito Y., et al. Transcriptional silencing of the RUNX3 gene by CpG hypermethylation is associated with lung cancer. Biochem. Biophys. Res. Commun. 2004, 314:223-228.
29. Licchesi J.D., Westra W.H., Hooker C.M., Machida E.O., Baylin S.B., Herman J.G. Epigenetic alteration of Wnt pathway antagonists in progressive glandular neoplasia of the lung. Carcinogenesis 2008, 29:895-904.
30. Linggi B., Müller-Tidow C., van de Locht L., Hu M., Nip J., Serve H., Berdel W.E., van der Reijden B., Quelle D.E., Rowley J.D., et al. The t(8;21) fusion protein, AML1 ETO, specifically represses the transcription of the p14(ARF) tumor suppressor in acute myeloid leukemia. Nat. Med. 2002, 8:743-750.
31. Lowe S.W., Sherr C.J. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr. Opin. Genet. Dev. 2003, 13:77-83.
32. Lund A.H., van Lohuizen M. RUNX: a trilogy of cancer genes. Cancer Cell 2002, 1:213-215.
33. Maeda Y., Tsuchiya T., Hao H., Tompkins D.H., Xu Y., Mucenski M.L., Du L., Keiser A.R., Fukazawa T., Naomoto Y., et al. Kras(G12D) and Nkx2-1 haploinsufficiency induce mucinous adenocarcinoma of the lung. J.Clin. Invest. 2012, 122:4388-4400.
34. Mallakin A., Sugiyama T., Taneja P., Matise L.A., Frazier D.P., Choudhary M., Hawkins G.A., D'Agostino R.B., Willingham M.C., Inoue K. Mutually exclusive inactivation of DMP1 and ARF/p53 in lung cancer. Cancer Cell 2007, 12:381-394.
35. Michieli P., Chedid M., Lin D., Pierce J.H., Mercer W.E., Givol D. Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res. 1994, 54:3391-3395.
36. Minoo P., Hu L., Xing Y., Zhu N.L., Chen H., Li M., Borok Z., Li C. Physical and functional interactions between homeodomain NKX2.1 and winged helix/forkhead FOXA1 in lung epithelial cells. Mol. Cell. Biol. 2007, 27:2155-2165.
37. Naoe Y., Setoguchi R., Akiyama K., Muroi S., Kuroda M., Hatam F., Littman D.R., Taniuchi I. Repression of interleukin-4 in T helper type 1 cells by Runx/Cbf beta binding to the Il4 silencer. J.Exp. Med. 2007, 204:1749-1755.
38. Palmero I., Pantoja C., Serrano M. p19ARF links the tumour suppressor p53 to Ras. Nature 1998, 395:125-126.
39. Sherr C.J. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 2006, 6:663-673.
40. Snyder E.L., Watanabe H., Magendantz M., Hoersch S., Chen T.A., Wang D.G., Crowley D., Whittaker C.A., Meyerson M., Kimura S., Jacks T. Nkx2-1 represses a latent gastric differentiation program in lung adenocarcinoma. Mol. Cell 2013, 50:185-199.
41. Somasundaram K., El-Deiry W.S. Inhibition of p53-mediated transactivation and cell cycle arrest by E1A through its p300/CBP-interacting region. Oncogene 1997, 14:1047-1057.
42. Subramanian J., Govindan R. Molecular genetics of lung cancer in people who have never smoked. Lancet Oncol. 2008, 9:676-682.
43. Travis W.D. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart 2004, World Health Organization, International Agency for Research on CancerInternational Agency for Research on Cancer, International Association for the Study of Lung CancerInternational Association for the Study of Lung Cancer, International Academy of PathologyInternational Academy of Pathology, IARC Press, Lyon.
44. Weisenberger D.J., Siegmund K.D., Campan M., Young J., Long T.I., Faasse M.A., Kang G.H., Widschwendter M., Weener D., Buchanan D., et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat. Genet. 2006, 38:787-793.
45. Winslow M.M., Dayton T.L., Verhaak R.G., Kim-Kiselak C., Snyder E.L., Feldser D.M., Hubbard D.D., DuPage M.J., Whittaker C.A., Hoersch S., et al. Suppression of lung adenocarcinoma progression by Nkx2-1. Nature 2011, 473:101-104.
46. Wistuba I.I., Gazdar A.F. Lung cancer preneoplasia. Annu. Rev. Pathol. 2006, 1:331-348.
47. Xu X., Rock J.R., Lu Y., Futtner C., Schwab B., Guinney J., Hogan B.L., Onaitis M.W. Evidence for type II cells as cells of origin of K-Ras-induced distal lung adenocarcinoma. Proc. Natl. Acad. Sci. USA 2012, 109:4910-4915.