Enhancer-targeted genome editing selectively blocks innate resistance to oncokinase inhibition

Genome Research

Volumn 24, Issue 5, 2014, Pages 751-760

  Webster, Dan E ^a   Barajas, Brook ^b   Bussat, Rose T ^b   Yan, Karen J ^a   Neela, Poornima H ^a   Flockhart, Ross J ^a   Kovalski, Joanna ^a   Zehnder, Ashley ^a   Khavari, Paul A ^a  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; ONCOKINASE; PHOSPHOTRANSFERASE; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; VEMURAFENIB; B RAF KINASE; BRAF PROTEIN, HUMAN; CHROMATIN; INDOLE DERIVATIVE; MET PROTEIN, HUMAN; MITF PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; SULFONAMIDE; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN; CONTROLLED STUDY; ENHANCER REGION; ENZYME INHIBITION; EPIGENETICS; GENE DELETION; HUMAN; HUMAN CELL; INNATE IMMUNITY; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY DNA SEQUENCE; ANTAGONISTS AND INHIBITORS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HUMAN GENOME; METABOLISM; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMATIN; DRUG RESISTANCE, NEOPLASM; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HUMANS; INDOLES; MELANOMA; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; PROMOTER REGIONS, GENETIC; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-MET; SULFONAMIDES; TRANSCRIPTOME;

EID: 84899818056     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.166231.113     Document Type: Article

References (54)

1. Ahmadiyeh N, Pomerantz MM, Grisanzio C, Herman P, Jia L, Almendro V, He HH, Brown M, Liu XS, Davis M, et al. 2010. 8q24 prostate, breast, and colon cancer risk loci show tissue-specific long-range interaction with MYC. Proc Natl Acad Sci 107: 9742-9746.
2. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
3. Beuret L, Flori E, Denoyelle C, Bille K, Busca R, Picardo M, Bertolotto C, Ballotti R. 2007. Up-regulation of MET expression by a-melanocytestimulating hormone and MITF allows hepatocyte growth factor to protect melanocytes and melanoma cells from apoptosis. J Biol Chem 282: 14140-14147.
4. Bogdanove AJ, Voytas DF. 2011. TAL effectors: customizable proteins for DNA targeting. Science 333: 1843-1846.
5. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, Spevak W, Zhang C, Zhang Y, Habets G, et al. 2010. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 467: 596-599.
6. Boni A, Cogdill AP, Dang P, Udayakumar D, Njauw CNJ, Sloss CM, Ferrone CR, Flaherty KT, Lawrence DP, Fisher DE, et al. 2010. Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function. Cancer Res 70: 5213-5219.
7. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF. 2011. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39: e82.
8. Cheli Y, Ohanna M, Ballotti R, Bertolotto C. 2010. Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res 23: 27-40.
9. Corso S, Giordano S. 2013. Cell-autonomous and non-cell-autonomous mechanisms of HGF/MET-driven resistance to targeted therapies: from basic research to a clinical perspective. Cancer Discov 3: 978-992.
10. Court F, Miro J, Braem C, Lelay-Taha M-N, Brisebarre A, Atger F, Gostan T, Weber M, Cathala G, Forné T. 2011. Modulated contact frequencies at gene-rich loci support a statistical helix model for mammalian chromatin organization. Genome Biol 12: R42.
11. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
12. Dekker J, Rippe K, Dekker M, Kleckner N. 2002. Capturing chromosome conformation. Science 295: 1306-1311.
13. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95: 14863-14868.
14. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
15. Feng J, Liu T, Qin B, Zhang Y, Liu XS. 2012. Identifying ChIP-seq enrichment using MACS. Nat Protoc 7: 1728-1740.
16. Flockhart RJ,Webster DE,Qu K, Mascarenhas N, Kovalski J, Kretz M, Khavari PA. 2012. BRAFV600E remodels the melanocyte transcriptome and induces BANCR to regulate melanoma cell migration. Genome Res 22: 1006-1014.
17. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, Ramaswamy S, Beroukhim R, Milner DA, Granter SR, Du J, et al. 2005. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436: 117-122.
18. Ghoussaini M, Song H, Koessler T, Olama Al AA, Kote-Jarai Z, Driver KE, Pooley KA, Ramus SJ, Kjaer SK, Hogdall E, et al. 2008. Multiple loci with different cancer specificities within the 8q24 gene desert. J Natl Cancer Inst 100: 962-966.
19. Gorkin DU, Lee D, Reed X, Fletez-Brant C, Bessling SL, Loftus SK, Beer MA, Pavan WJ, McCallion AS. 2012. Integration of ChIP-seq and machine learning reveals enhancers and a predictive regulatory sequence vocabulary in melanocytes. Genome Res 22: 2290-2301.
20. Grisanzio C, Freedman ML. 2010. Chromosome 8q24-associated cancers and MYC. Genes Cancer 1: 555-559.
21. Gross DS, Garrard WT. 1988. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem 57: 159-197.
22. Hagège H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, de Laat W, Forné T.2007.Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc2:1722-1733.
23. Haq R, Yokoyama S, Hawryluk EB, Jönsson GB, Frederick DT, McHenry K, Porter D, Tran T-N, Love KT, Langer R, et al. 2013. BCL2A1 is a lineagespecific antiapoptotic melanoma oncogene that confers resistance to BRAF inhibition. Proc Natl Acad Sci 110: 4321-4326.
24. Kentsis A, Reed C, Rice KL, Sanda T, Rodig SJ, Tholouli E, Christie A, Valk PJM, Delwel R, Ngo V, et al. 2012. Autocrine activation of the MET receptor tyrosine kinase in acute myeloid leukemia. Nat Med 18: 1118-1122.
25. Kono M, Dunn IS, Durda PJ, Butera D, Rose LB, Haggerty TJ, Benson EM, Kurnick JT. 2006. Role of the mitogen-activated protein kinase signaling pathway in the regulation of human melanocytic antigen expression. Mol Cancer Res 4: 779-792.
26. Kretz M,Webster DE, Flockhart RJ, Lee CS, Zehnder A, Lopez-Pajares V,Qu K, Zheng GXY, Chow J, Kim GE, et al. 2012. Suppression of progenitor differentiation requires the long noncoding RNA ANCR. Genes Dev 26: 338-343.
27. Kretz M, Siprashvili Z, Chu C, Webster DE, Zehnder A, Qu K, Lee CS, Flockhart RJ, Groff AF, Chow J, et al. 2013. Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature 493: 231-235.
28. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
29. Levy C, Khaled M, Fisher DE. 2006. MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol Med 12: 406-414.
30. Liu C, PengW, Xu C, Lou Y, ZhangM,Wargo JA, Chen JQ, Li HS,Watowich SS, Yang Y, et al. 2013. BRAF inhibition increases tumor infiltration by T cells and enhances the antitumor activity of adoptive immunotherapy in mice. Clin Cancer Res 19: 393-403.
31. McGill G, Haq R, Nishimura E, Fisher D. 2006. c-Met expression is regulated by Mitf in the melanocyte lineage. J Biol Chem 281: 10365-10373.
32. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB,Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cisregulatory regions. Nat Biotechnol 28: 495-501.
33. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, et al. 2011. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148.
34. Pennacchio LA, Bickmore W, Dean A, Nobrega MA, Bejerano G. 2013. Enhancers: five essential questions. Nat Rev Genet 14: 288-295.
35. Pleasance ED, Cheetham RK, Stephens PJ, McBride DJ, Humphray SJ, Greenman CD, Varela I, LinM-L, Ordóñez GR, Bignell GR, et al. 2010. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463: 191-196.
36. Pomerantz MM, Ahmadiyeh N, Jia L, Herman P, Verzi MP, Doddapaneni H, Beckwith CA, Chan JA, Hills A, Davis M, et al. 2009. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat Genet 41: 882-884.
37. Price ER, Ding HF, Badalian T, Bhattacharya S, Takemoto C, Yao TP, Hemesath TJ, Fisher DE. 1998. Lineage-specific signaling in melanocytes. C-kit stimulation recruits p300/CBP to microphthalmia. J Biol Chem 273: 17983-17986.
38. Quinlan AR, Hall IM. 2010. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
39. Rosenbloom KR, Sloan CA, Malladi VS, Dreszer TR, Learned K, Kirkup VM, Wong MC, Maddren M, Fang R, Heitner SG, et al. 2013. ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res 41: D56-D63.
40. Sanyal A, Lajoie BR, Jain G, Dekker J. 2012. The long-range interaction landscape of gene promoters. Nature 489: 109-113.
41. Sen GL, Webster DE, Barragan DI, Chang HY, Khavari PA. 2008. Control of differentiation in a self-renewing mammalian tissue by the histone demethylase JMJD3. Genes Dev 22: 1865-1870.
42. Sen GL, Boxer LD, Webster DE, Bussat RT, Qu K, Zarnegar BJ, Johnston D, Siprashvili Z, Khavari PA. 2012. ZNF750 is a p63 target gene that induces KLF4 to drive terminal epidermal differentiation. Dev Cell 22: 669-677.
43. Steingrímsson E, Copeland NG, Jenkins NA. 2004. Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 38: 365-411.
44. Straussman R, Morikawa T, Shee K, Barzily-RokniM, Qian ZR, Du J, Davis A, Mongare MM, Gould J, Frederick DT, et al. 2012. Tumour microenvironment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487: 500-504.
45. Taslim C, Wu J, Yan P, Singer G, Parvin J, Huang T, Lin S, Huang K. 2009. ChIP-Seq of ERa and RNA polymerase II defines genes differentially responding to ligands. EMBO J 28: 1418-1428.
46. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. 2012. The accessible chromatin landscape of the human genome. Nature 489: 75-82.
47. Tsao H, Chin L, Garraway LA, Fisher DE. 2012. Melanoma: from mutations to medicine. Genes Dev 26: 1131-1155.
48. Tuupanen S, Turunen M, Lehtonen R, Hallikas O, Vanharanta S, Kivioja T, Björklund M, Wei G, Yan J, Niittymäki I, et al. 2009. The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling. Nat Genet 41: 885-890.
49. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: W71-W74.
50. Wasserman NF, Aneas I, Nobrega MA. 2010. An 8q24 gene desert variant associated with prostate cancer risk confers differential in vivo activity to a MYC enhancer. Genome Res 20: 1191-1197.
51. Wellbrock C, Rana S, Paterson H, Pickersgill H, Brummelkamp T, Marais R. 2008. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS ONE 3: e2734.
52. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, Peng J, Lin E, Wang Y, Sosman J, et al. 2012. Widespread potential for growth-factordriven resistance to anticancer kinase inhibitors. Nature 487: 505-509.
53. Wright JB, Brown SJ, Cole MD. 2010. Upregulation of c-MYC in cis through a large chromatin loop linked to a cancer risk-associated singlenucleotide polymorphism in colorectal cancer cells. Mol Cell Biol 30: 1411-1420.
54. Wu M, Hemesath TJ, Takemoto CM, Horstmann MA, Wells AG, Price ER, Fisher DZ, Fisher DE. 2000. c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev 14: 301-312.