A synthetic lethality-based strategy to treat cancers harboring a genetic deficiency in the chromatin remodeling factor BRG1

Cancer Research

Volumn 73, Issue 17, 2013, Pages 5508-5518

  Oike, Takahiro ^a,d   Ogiwara, Hideaki ^a   Tominaga, Yuichi ^b   Ito, Kentaro ^b   Ando, Osamu ^b   Tsuta, Koji ^c   Mizukami, Tatsuji ^a,d   Shimada, Yoko ^a   Isomura, Hisanori ^a   Komachi, Mayumi ^d   Furuta, Koh ^c   Watanabe, Shun Ichi ^c   Nakano, Takashi ^d   Yokota, Jun ^a   Kohno, Takashi ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b DAIICHI SANKYO CO   (Japan)

^c NATIONAL CANCER CENTER HOSPITAL   (Japan)

^d GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE INHIBITOR; BRG1 PROTEIN; BRM PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; PROTEIN SWI; TRANSCRIPTION FACTOR SNF;

ADULT; AGED; ALK GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRM GENE; CANCER CELL; CANCER GENETICS; CANCER INHIBITION; CANCER THERAPY; CATALYSIS; CELL AGING; COHORT ANALYSIS; CONTROLLED STUDY; DDR2 GENE; EGFR GENE; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INHIBITION; FEMALE; FGFR1 GENE; FUSION GENE; GENE; GENE AMPLIFICATION; GENE MUTATION; GENE SILENCING; GENE TARGETING; GENETIC DISORDER; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SYNTHETIC LETHALITY THERAPY; TUMOR XENOGRAFT; UNDIFFERENTIATED CARCINOMA;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; CELL AGING; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; DNA HELICASES; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENES, LETHAL; HUMANS; IMMUNOENZYME TECHNIQUES; KINESIN; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; MUTATION; NEOPLASM STAGING; NUCLEAR PROTEINS; ONCOGENE PROTEINS, FUSION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 84883467670     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4593     Document Type: Article

References (46)

1. Lovly CM, Carbone DP. Lung cancer in 2010: one size does not fit all. Nat Rev Clin Oncol 2011;8:68-70.
2. Kohno T, Ichikawa H, Totoki Y, Yasuda K, Hiramoto M, Nammo T, et al. KIF5B-RET fusions in lung adenocarcinoma. Nat Med 2012;18:375-7.
3. Lipson D, Capelletti M, Yelensky R, Otto G, Parker A, Jarosz M, et al. Identification of new ALK and RET gene fusions from colorectal and lung cancer biopsies. Nat Med 2012;18:382-4.
4. Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, et al. RET, ROS1 and ALK fusions in lung cancer. Nat Med 2012;18:378-81.
5. Hammerman PS, Sos ML, Ramos AH, Xu C, Dutt A, Zhou W, et al. Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discov 2011;1:78-89.
6. Weiss J, Sos ML, Seidel D, Peifer M, Zander T, Heuckmann JM, et al. Frequent and focal FGFR1 amplification associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med 2010;2:62ra93.
7. Wilson BG, Roberts CW. SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 2011;11:481-92.
8. Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, et al. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of nonhomologous end joining factors. Oncogene 2011;30:2135-46.
9. Chan DA, Giaccia AJ. Harnessing synthetic lethal interactions in anticancer drug discovery. Nat Rev Drug Discov 2011;10:351-64.
10. Muller FL, Colla S, Aquilanti E, Manzo VE, Genovese G, Lee J, et al. Passenger deletions generate therapeutic vulnerabilities in cancer. Nature 2012;488:337-42.
11. Chan DA, Sutphin PD, Nguyen P, Turcotte S, Lai EW, Banh A, et al. Targeting GLUT1 and the Warburg effect in renal cell carcinoma by chemical synthetic lethality. Sci Transl Med 2011;3:94ra70.
12. Martin SA, McCabe N, Mullarkey M, Cummins R, Burgess DJ, Nakabeppu Y, et al. DNA polymerases as potential therapeutic targets for cancers deficient in the DNA mismatch repair proteins MSH2 or MLH1. Cancer Cell 2010;17:235-48.
13. Medina PP, Romero OA, Kohno T, Montuenga LM, Pio R, Yokota J, et al. Frequent BRG1/SMARCA4-inactivating mutations in human lung cancer cell lines. Hum Mutat 2008;29:617-22. (Pubitemid 351614585)
14. Reisman DN, Sciarrotta J, Wang W, Funkhouser WK, Weissman BE. Loss of BRG1/BRM in human lung cancer cell lines and primary lung cancers: correlation with poor prognosis. Cancer Res 2003;63:560-6. (Pubitemid 36158131)
15. Wong AK, Shanahan F, Chen Y, Lian L, Ha P, Hendricks K, et al. BRG1, a component of the SWI-SNF complex, is mutated in multiple human tumor cell lines. Cancer Res 2000;60:6171-7.
16. Medina PP, Carretero J, Fraga MF, Esteller M, Sidransky D, Sanchez-Cespedes M. Genetic and epigenetic screening for gene alterations of the chromatin-remodeling factor, SMARCA4/BRG1, in lung tumors. Genes Chromosomes Cancer 2004;41:170-7. (Pubitemid 39096743)
17. Blanco R, Iwakawa R, Tang M, Kohno T, Angulo B, Pio R, et al. A genealteration profile of human lung cancer cell lines. Hum Mutat 2009;30:1199-206.
18. Rodriguez-Nieto S, Canada A, Pros E, Pinto AI, Torres-Lanzas J, Lopez-Rios F, et al. Massive parallel DNA pyrosequencing analysis of the tumor suppressor BRG1/SMARCA4 in lung primary tumors. Hum Mutat 2011;32:E1999-2017.
19. Pugh TJ, Weeraratne SD, Archer TC, Krummel Pomeranz DA, Auclair D, Bochicchio J, et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012;488:106-10.
20. Jones DT, Jager N, Kool M, Zichner T, Hutter B, Sultan M, et al. Dissecting the genomic complexity underlying medulloblastoma. Nature 2012;488:100-5.
21. Love C, Sun Z, Jima D, Li G, Zhang J, Miles R, et al. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet 2012;44:1321-5.
22. Reisman D, Glaros S, Thompson EA. The SWI/SNF complex and cancer. Oncogene 2009;28:1653-68.
23. Reyes JC, Barra J, Muchardt C, Camus A, Babinet C, Yaniv M. Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha). EMBO J 1998;17:6979-91. (Pubitemid 28550292)
24. Schneppenheim R, Fruhwald MC, Gesk S, Hasselblatt M, Jeibmann A, Kordes U, et al. Germline nonsense mutation and somatic inactivation of SMARCA4/BRG1 in a family with rhabdoid tumor predisposition syndrome. Am J Hum Genet 2010;86:279-84.
25. Bultman SJ, Herschkowitz JI, Godfrey V, Gebuhr TC, Yaniv M, Perou CM, et al. Characterization of mammary tumors from Brg1 heterozygous mice. Oncogene 2008;27:460-8.
26. Takano T, Ohe Y, Sakamoto H, Tsuta K, Matsuno Y, Tateishi U, et al. Epidermal growth factor receptor gene mutations and increased copy numbers predict gefitinib sensitivity in patients with recurrent non-small-cell lung cancer. J Clin Oncol 2005;23:6829-37.
27. Yoshida A, Tsuta K, Nakamura H, Kohno T, Takahashi F, Asamura H, et al. Comprehensive histologic analysis of ALK-rearranged lung carcinomas. Am J Surg Pathol 2011;35:1226-34.
28. Schildhaus HU, Heukamp LC, Merkelbach-Bruse S, Riesner K, Schmitz K, Binot E, et al. Definition of a fluorescence in-situ hybridization score identifies high- and low-level FGFR1 amplification types in squamous cell lung cancer. Mod Pathol 2012;25:1473-80.
29. Wiznerowicz M, Trono D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 2003;77:8957-61. (Pubitemid 36936105)
30. Zhang J, Ohta T, Maruyama A, Hosoya T, Nishikawa K, Maher JM, et al. BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress. Mol Cell Biol 2006;26:7942-52. (Pubitemid 44630994)
31. Romero OA, Setien F, John S, Gimenez-Xavier P, Gomez-Lopez G, Pisano D, et al. The tumour suppressor and chromatin-remodelling factor BRG1 antagonizes Myc activity and promotes cell differentiation in human cancer. EMBO Mol Med 2012;4:603-16.
32. Seo JS, Ju YS, Lee WC, Shin JY, Lee JK, Bleazard T, et al. The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res 2012;22:2109-19.
33. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, et al. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 2012;150:1107-20.
34. Bruno T, Desantis A, Bossi G, Di Agostino S, Sorino C, De Nicola F, et al. Che-1 promotes tumor cell survival by sustaining mutant p53 transcription and inhibiting DNA damage response activation. Cancer Cell 2010;18:122-34.
35. Roninson IB. Tumor cell senescence in cancer treatment. Cancer Res 2003;63:2705-15. (Pubitemid 36667137)
36. Zhang R, Adams PD. Heterochromatin and its relationship to cell senescence and cancer therapy. Cell Cycle 2007;6:784-9. (Pubitemid 46572614)
37. Al-Ejeh F, Kumar R, Wiegmans A, Lakhani SR, Brown MP, Khanna KK. Harnessing the complexity of DNA-damage response pathways to improve cancer treatment outcomes. Oncogene 2010;29:6085-98.
38. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, et al. Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 2001;409:1067-70. (Pubitemid 32204062)
39. Amann J, Kalyankrishna S, Massion PP, Ohm JE, Girard L, Shigematsu H, et al. Aberrant epidermal growth factor receptor signaling and enhanced sensitivity to EGFR inhibitors in lung cancer. Cancer Res 2005;65:226-35. (Pubitemid 40070814)
40. Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, Holmes AJ, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin Cancer Res 2008;14:4275-83.
41. Chene P. The ATPases: a new family for a family-based drug design approach. Expert Opin Ther Targets 2003;7:453-61. (Pubitemid 36722229)
42. Decristofaro MF, Betz BL, Rorie CJ, Reisman DN, Wang W, Weissman BE. Characterization of SWI/SNF protein expression in human breast cancer cell lines and other malignancies. J Cell Physiol 2001;186:136-45.
43. Yamamichi N, Inada K, Ichinose M, Yamamichi-Nishina M, Mizutani T, Watanabe H, et al. Frequent loss of Brm expression in gastric cancer correlateswith histologic features and differentiation state. Cancer Res 2007;67:10727-35. (Pubitemid 350145899)
44. Shain AH, Pollack JR. The spectrum of SWI/SNF mutations, ubiquitous in human cancers. PLoS ONE 2013;8:e55119.
45. Northcott PA, Korshunov A, Pfister SM, Taylor MD. The clinical implications of medulloblastoma subgroups. Nat Rev Neurol 2012;8:340-51.
46. Fukuoka J, Fujii T, Shih JH, Dracheva T, Meerzaman D, Player A, et al. Chromatin remodeling factors and BRM/BRG1 expression as prognostic indicators in non-small cell lung cancer. Clin Cancer Res 2004;10:4314-24. (Pubitemid 38878869)