Inhibition of TWIST1 leads to activation of oncogene-induced senescence in oncogene-driven non-small cell lung cancer

Molecular Cancer Research

Volumn 11, Issue 4, 2013, Pages 329-338

  Burns, Timothy F ^a,c   Dobromilskaya, Irina ^a   Murphy, Sara C ^a   Gajula, Rajendra P ^a   Thiyagarajan, Saravanan ^a   Chatley, Sarah N H ^c   Aziz, Khaled ^a   Cho, Yoon Jae ^b   Tran, Phuoc T ^a   Rudin, Charles M ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN P16; PROTEIN P53; S PHASE KINASE ASSOCIATED PROTEIN 2; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER SURVIVAL; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; COLONY FORMATION; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GROWTH INHIBITION; HUMAN; HUMAN CELL; LUNG CARCINOGENESIS; LUNG NON SMALL CELL CANCER; METHYLATION; MOUSE; NONHUMAN; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL AGING; CELL LINE, TUMOR; GENE SILENCING; HEK293 CELLS; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED NOD; MICE, SCID; NUCLEAR PROTEINS; ONCOGENES; RNA, SMALL INTERFERING; TWIST TRANSCRIPTION FACTOR;

MUS MUSCULUS;

EID: 84876521231     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-12-0456     Document Type: Article

References (47)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 2011;61:212-36.
2. Mok TS. Personalized medicine in lung cancer: what we need to know. Nat Rev Clin Oncol 2011;8:661-8.
3. Sequist LV, Waltman BA, Dias-Santagata D, Digumarthy S, Turke AB, Fidias P, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011;3: 75ra26.
4. Katayama R, Shaw AT, Khan TM, Mino-Kenudson M, Solomon BJ, Halmos B, et al. Mechanisms of acquired crizotinib resistance in ALK-rearranged lung cancers. Sci Transl Med 2012;4:120ra17.
5. Riely GJ, Marks J, Pao W. KRAS mutations in non-small cell lung cancer. Proc Am Thorac Soc 2009;6:201-5.
6. Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009;136:823-37.
7. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 2009;462:108-12.
8. Luo J, Emanuele MJ, Li D, Creighton CJ, Schlabach MR, West-brook TF, et al. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009; 137:835-48.
9. Puyol M. A synthetic lethal interaction between K-Ras oncogenes and Cdk4 unveils a therapeutic strategy for non-small cell lung carcinoma. Cancer Cell 2010;18:63-73.
10. Scholl C, Fröhling S, Dunn IF, Schinzel AC, Barbie DA, Kim SY, et al. Synthetic Lethal interaction between oncogenic KRAS dependency and STK33 suppression in human cancer cells. Cell 2009;137:821-34.
11. Singh A, Greninger P, Rhodes D, Koopman L, Violette S, Bardeesy N, et al. A Gene expression signature associated with "K-Ras Addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 2009;15:489-500.
12. Babij C, Zhang Y, Kurzeja RJ, Munzli A, Shehabeldin A, Fernando M, et al. STK33 kinase activity is non-essential in KRAS-dependent cancer cells. Cancer Res 2011;71:5818-26.
13. Collado M, Serrano M. Senescence in tumours: evidence from mice and humans. Nat Rev Cancer 2010;10:51-7.
14. Acosta JC, Gil J. Senescence: a new weapon for cancer therapy. Trends Cell Biol 2012;22:211-9.
15. Nardella C, Clohessy JG, Alimonti A, Pandolfi PP. Pro-senescence therapy for cancer treatment. Nat Rev Cancer 2011;11:503-11.
16. Collado M. Tumour biology: senescence in premalignant tumours. Nature 2005;436:642. (Pubitemid 41117258)
17. Prieur A, Peeper DS. Cellular senescence in vivo: a barrier to tumor-igenesis. Curr Opin Cell Biol 2008;20:150-5.
18. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997;88:593-602. (Pubitemid 27152402)
19. Lin HK. Skp2 targeting suppresses tumorigenesis by Arf-p53-inde-pendent cellular senescence. Nature 2010;464:374-9.
20. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008; 14:79-89. (Pubitemid 351890463)
21. Lee KE, Bar-Sagi D. Oncogenic KRas suppresses inflammation-associated senescence of pancreatic ductal cells. Cancer Cell 2010;18: 448-58.
22. Barnes RM, Firulli AB. A twist of insight-the role of Twist-family bHLH factors in development. Int J Dev Biol 2009;53:909-24.
23. Chen ZF, Behringer RR. twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev 1995;9:686-99.
24. el Ghouzzi V, Le Merrer M, Perrin-Schmitt F, Lajeunie E, Benit P, Renier D, et al. Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat Genet 1997; 15: 42-6. (Pubitemid 27014948)
25. Ansieau S, Morel AP, Hinkal G, Bastid J, Puisieux A. TWISTing an embryonic transcription factor into an oncoprotein. Oncogene 2010; 29:3173-84.
26. Tran PT, Shroff EH, Burns TF, Thiyagarajan S, Das ST, Zabuawala T, et al. Twist1 suppresses senescence programs and thereby accelerates and maintains mutant Kras-induced lung tumorigenesis. PLoS Genet 2012;8:e1002650.
27. Ozoren N, Fisher MJ, Kim K, Liu CX, Genin A, Shifman Y, et al. Homozygous deletion of the death receptor DR4 gene in a nasopha-ryngeal cancer cell line is associated with TRAIL resistance. Int J Oncol 2000;16:917-25.
28. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 2006;124:1283-98.
29. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-101. (Pubitemid 40262113)
30. Wiederschain D, Wee S, Chen L, Loo A, Yang G, Huang A, et al. Singlevector inducible lentiviral RNAi system for oncology target validation. Cell Cycle 2009;8:498-504.
31. Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L, et al. Twist is a potential oncogene that inhibits apoptosis. Genes Dev 1999;13:2207-17. (Pubitemid 29426726)
32. Serres MP, Zlotek-Zlotkiewicz E, Concha C, Gurian-West M, Daburon V, Roberts JM, et al. Cytoplasmic p27 is oncogenic and cooperates with Ras both in vivo and in vitro. Oncogene 2011;30:2846-58.
33. Wander SA, Zhao D, Slingerland JM. p27: a barometer of signaling deregulation and potential predictor of response to targeted therapies. Clin Cancer Res 2011;17:12-8.
34. Frescas D, Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer 2008;8:438-49. (Pubitemid 351744963)
35. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-50. (Pubitemid 41528093)
36. Shiota M, Izumi H, Onitsuka T, Miyamoto N, Kashiwagi E, Kidani A, et al. Twist promotes tumor cell growth through YB-1 expression. Cancer Res 2008;68:98-105. (Pubitemid 351380110)
37. Piccinin S, Tonin E, Sessa S, Demontis S, Rossi S, Pecciarini L, et al. A "twist box" code of p53 inactivation: twist box: p53 interaction promotes p53 degradation. Cancer Cell 2012;22:404-15.
38. Shiota M, Izumi H, Onitsuka T, Miyamoto N, Kashiwagi E, Kidani A, et al. Twist and p53 reciprocally regulate target genes via direct interaction. Oncogene 2008;27:5543-53.
39. Vichalkovski A, Gresko E, Hess D, Restuccia DF, Hemmings BA. PKB/AKT phosphorylation of the transcription factor Twist-1 at Ser42 inhibits p53 activity in response to DNA damage. Oncogene 2010; 29:3554-65.
40. Xu M. Beta-catenin expression results in p53-independent DNA damage and oncogene-induced senescence in prely-mphomagenic thymocytes in vivo. Mol Cell Biol 2008;28: 1713-23.
41. Blons H, Pallier K, Le Corre D, Danel C, Tremblay-Gravel M, Houdayer C, et al. Genome wide SNP comparative analysis between EGFR and KRAS mutated NSCLC and characterization of two models of onco-genic cooperation in non-small cell lung carcinoma. BMC Med Geno-mics 2008;1:25.
42. Pallier K, Cessot A, Cote JF, Just PA, Cazes A, Fabre E, et al. TWIST1 a new determinant of epithelial to mesenchymal transition in EGFR mutated lung adenocarcinoma. PloS One 2012; 7:e29954.
43. Cooke Vesselina G, LeBleu Valerie S, Keskin D, Khan Z, O'Connell Joyce T, Teng Y, et al. Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated byMet signaling pathway. Cancer Cell 2012;21:66-81.
44. Feng Y, Thiagarajan PS, Ma PC. MET signaling: novel targeted inhibition and its clinical development in lung cancer. J Thorac Oncol 2012;7:459-67.
45. Oxnard GR, Arcila ME, Chmielecki J, Ladanyi M, Miller VA, Pao W. New strategies in overcoming acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in lung cancer. Clin Cancer Res 2011;17:5530-7.
46. Chen YT, Akinwunmi PO, Deng JM, Tam OH, Behringer RR. Generation of a Twist1 conditional null allele in the mouse. Genesis 2007; 45:588-92. (Pubitemid 350013056)
47. Pan D, Fujimoto M, Lopes A, Wang YX. Twist-1 is a PPARdelta-inducible, negative-feedback regulator of PGC-1alpha in brown fat metabolism. Cell 2009;137:73-86.