Isocitrate dehydrogenase mutations confer dasatinib hypersensitivity and SRC dependence in intrahepatic cholangiocarcinoma

Cancer Discovery

Volumn 6, Issue 7, 2016, Pages 727-739

  Saha, Supriya K ^a   Gordan, John D ^b   Kleinstiver, Benjamin P ^a,c   Vu, Phuong ^a   Najem, Mortada S ^a   Yeo, Jia Chi ^a   Shi, Lei ^a   Kato, Yasutaka ^a   Levin, Rebecca S ^d   Webber, James T ^b   Damon, Leah J ^a   Egan, Regina K ^a   Greninger, Patricia ^a   McDermott, Ultan ^e   Garnett, Mathew J ^e   Jenkins, Roger L ^f   Rieger Chris, Kimberly M ^f   Sullivan, Travis B ^f   Hezel, Aram F ^g   Liss, Andrew S ^c   Mizukami, Yusuke ^a,h   Goyal, Lipika ^a   Ferrone, Cristina R ^a   Zhu, Andrew X ^a   Joung, J Keith ^a,c   Shokat, Kevan M ^d,i   Benes, Cyril H ^a   Bardeesy, Nabeel ^a   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f LAHEY HOSPITAL AND MEDICAL CENTER   (United States)

^g UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^h Sapporo Higashi Tokushukai Hospital   (Japan)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOSUTINIB; CASPASE 3; DAPORINAD; DASATINIB; PONATINIB; PROTEIN KINASE P60; SARACATINIB; VENETOCLAX; ISOCITRATE DEHYDROGENASE; PROTEIN TYROSINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BILE DUCT CARCINOMA; CELL DEATH; CELL PROLIFERATION ASSAY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; FEMALE; GENE; GENE MUTATION; HALF LIFE TIME; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERSENSITIVITY; IC50; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; ISOCITRATE DEHYDROGENASE GENE; MASS SPECTROMETRY; MOUSE; NONHUMAN; SEQUENCE ANALYSIS; TUMOR REGRESSION; TUMOR XENOGRAFT; ANIMAL; BILE DUCT TUMOR; CELL PROLIFERATION; CLUSTER ANALYSIS; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MUTATION; TUMOR CELL LINE;

ANIMALS; BILE DUCT NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CHOLANGIOCARCINOMA; CLUSTER ANALYSIS; DASATINIB; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; HUMANS; ISOCITRATE DEHYDROGENASE; MICE; MUTATION; SRC-FAMILY KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84977512278     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-15-1442     Document Type: Article

References (48)

1. Razumilava N, Gores GJ. Cholangiocarcinoma. Lancet 2014; 383: 2168-79
2. Khan SA, Thomas HC, Davidson BR, Taylor-Robinson SD. Cholangiocarcinoma. Lancet 2005; 366: 1303-14
3. Saha SK, Zhu AX, Fuchs CS, Brooks GA. Forty-year trends in cholangiocarcinoma incidence in the U.S.: intrahepatic disease on the rise. Oncologist 2016;21:594-9
4. Hainsworth JD, Rubin MS, Spigel DR, Boccia RV, Raby S, Quinn R, et al. Molecular gene expression profiling to predict the tissue of origin and direct site-specific therapy in patients with carcinoma of unknown primary site: a prospective trial of the Sarah Cannon research institute. J Clin Oncol 2013; 31: 217-23
5. Varadhachary GR, Raber MN. Cancer of unknown primary site. N Engl J Med 2014; 371: 757-65
6. Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med 2010; 362: 1273-81
7. Borger DR, Tanabe KK, Fan KC, Lopez HU, Fantin VR, Straley KS, et al. Frequent mutation of isocitrate dehydrogenase (IDH)1 and IDH2 in cholangiocarcinoma identified through broad-based tumor genotyping. Oncologist 2012; 17: 72-9
8. Chan-On W, Nairismagi ML, Ong CK, Lim WK, Dima S, Pairojkul C, et al. Exome sequencing identifies distinct mutational patterns in liver fl uke-related and non-infection-related bile duct cancers. Nat Genet 2013; 45: 1474-8
9. Jiao Y, Pawlik TM, Anders RA, Selaru FM, Streppel MM, Lucas DJ, et al. Exome sequencing identifies frequent inactivating mutations in BAP1, ARID1A and PBRM1 in intrahepatic cholangiocarcinomas. Nat Genet 2013; 45: 1470-3
10. Kipp BR, Voss JS, Kerr SE, Barr Fritcher EG, Graham RP, Zhang L, et al. Isocitrate dehydrogenase 1 and 2 mutations in cholangiocarcinoma. Human Pathol 2012; 43: 1552-8
11. Ross JS, Wang K, Gay L, Al-Rohil R, Rand JV, Jones DM, et al. New routes to targeted therapy of intrahepatic cholangiocarcinomas revealed by next-generation sequencing. Oncologist 2014; 19: 235-42
12. Sia D, Losic B, Moeini A, Cabellos L, Hao K, Revill K, et al. Massive parallel sequencing uncovers actionable FGFR2-PPHLN1 fusion and ARAF mutations in intrahepatic cholangiocarcinoma. Nat Commun 2015; 6: 6087
13. Voss JS, Holtegaard LM, Kerr SE, Fritcher EG, Roberts LR, Gores GJ, et al. Molecular profiling of cholangiocarcinoma shows potential for targeted therapy treatment decisions. Hum Pathol 2013; 44: 1216-22
14. Wang P, Dong Q, Zhang C, Kuan PF, Liu Y, Jeck WR, et al. Mutations in isocitrate dehydrogenase 1 and 2 occur frequently in intrahepatic cholangiocarcinomas and share hypermethylation targets with glioblastomas. Oncogene 2012;32:3091-100
15. Cairns RA, Mak TW. Oncogenic isocitrate dehydrogenase mutations: mechanisms, models, and clinical opportunities. Cancer Discov 2013; 3: 730-41
16. Lu C, Ward PS, Kapoor GS, Rohle D, Turcan S, Abdel-Wahab O, et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 2012; 483: 474-8
17. Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 2012; 483: 479-83
18. Wang P, Dong Q, Zhang C, Kuan PF, Liu Y, Jeck WR, et al. Mutations in isocitrate dehydrogenase 1 and 2 occur frequently in intrahepatic cholangiocarcinomas and share hypermethylation targets with glioblastomas. Oncogene 2013; 32: 3091-100
19. Saha SK, Parachoniak CA, Bardeesy N. IDH mutations in liver cell plasticity and biliary cancer. Cell Cycle 2014; 13: 3176-82
20. Saha SK, Parachoniak CA, Ghanta KS, Fitamant J, Ross KN, Najem MS, et al. Mutant IDH inhibits HNF-4alpha to block hepatocyte differentiation and promote biliary cancer. Nature 2014; 513: 110-4
21. Stein E, Tallman M, Pollyea DA, Flinn IW, Fathi AT, Stone R M, et al. Abstract CT103: Clinical safety and activity in a phase I trial of AG-221, a first in class, potent inhibitor of the IDH2-mutant protein, in patients with IDH2 mutant positive advanced hematologic malignancies. Cancer Res 2014; 74: CT103-CT103
22. Burris H, Mellinghoff I, Maher E, Wen P, Beeram M, Touat M, et al. Abstract PL04-05: The first reported results of AG-120, a first-inclass, potent inhibitor of the IDH1 mutant protein, in a Phase I study of patients with advanced IDH1-mutant solid tumors, including gliomas. Molecular Cancer Thera 2015; 14: PL04-05
23. Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009; 136: 823-37
24. Shah NP, Kasap C, Weier C, Balbas M, Nicoll JM, Bleickardt E, et al. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis. Cancer Cell 2008; 14: 485-93
25. Shah NP, Kim DW, Kantarjian H, Rousselot P, Llacer PE, Enrico A, et al. Potent, transient inhibition of BCR-ABL with dasatinib 100 mg daily achieves rapid and durable cytogenetic responses and high transformation-free survival rates in chronic phase chronic myeloid leukemia patients with resistance, suboptimal response or intolerance to imatinib. Haematologica 2010; 95: 232-40
26. Davis MI, Hunt JP, Herrgard S, Ciceri P, Wodicka LM, Pallares G, et al. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol 2011; 29: 1046-51
27. Green TP, Fennell M, Whittaker R, Curwen J, Jacobs V, Allen J, et al. Preclinical anticancer activity of the potent, oral Src inhibitor AZD0530. Mol Oncol 2009; 3: 248-61
28. Chan SM, Thomas D, Corces-Zimmerman MR, Xavy S, Rastogi S, Hong WJ, et al. Isocitrate dehydrogenase 1 and 2 mutations induce BCL-2 dependence in acute myeloid leukemia. Nat Med 2015; 21: 178-84
29. Tateishi K, Wakimoto H, Iafrate AJ, Tanaka S, Loebel F, Lelic N, et al. Extreme vulnerability of IDH1 mutant cancers to NAD+ depletion. Cancer Cell 2015; 28: 773-84
30. O’Dell MR, Huang JL, Whitney-Miller CL, Deshpande V, Rothberg P, Grose V, et al. Kras(G12D) and p53 mutation cause primary intrahepatic cholangiocarcinoma. Cancer Res 2012; 72: 1557-67
31. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008; 26: 127-32
32. Duncan JS, Whittle MC, Nakamura K, Abell AN, Midland AA, Zawistowski JS, et al. Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell 2012; 149: 307-21
33. Sos ML, Levin RS, Gordan JD, Oses-Prieto JA, Webber JT, Salt M, et al. Oncogene mimicry as a mechanism of primary resistance to BRAF inhibitors. Cell Rep 2014; 8: 1037-48
34. Liu Y, Shah K, Yang F, Witucki L, Shokat KM. A molecular gate which controls unnatural ATP analogue recognition by the tyrosine kinase v-Src. Bioorg Med Chem 1998; 6: 1219-26
35. Daub H, Specht K, Ullrich A. Strategies to overcome resistance to targeted protein kinase inhibitors. Nat Rev Drug Discov 2004; 3: 1001-10
36. Hsu PD, Lander ES, Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 2014; 157: 1262-78
37. Sander JD, Joung JK. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 2014; 32: 347-55
38. Chen C, Liu Y, Lu C, Cross JR, Morris JPT, Shroff AS, et al. Cancerassociated IDH2 mutants drive an acute myeloid leukemia that is susceptible to Brd4 inhibition. Gen Develop 2013; 27: 1974-85
39. Brunton VG, Frame MC. Src and focal adhesion kinase as therapeutic targets in cancer. Curr Opin Pharmacol 2008; 8: 427-32
40. Garnett MJ, Edelman EJ, Heidorn SJ, Greenman CD, Dastur A, Lau KW, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012; 483: 570-5
41. http://www.cancerRxgene.org
42. http://www.broadinstitute.org/cancer/software/GENE-E/
43. Davis MI, Gross S, Shen M, Straley KS, Pragani R, Lea WA, et al. Biochemical, cellular, and biophysical characterization of a potent inhibitor of mutant isocitrate dehydrogenase IDH1. J Biol Chem 2014; 289: 13717-25
44. Schilling B, Rardin MJ, MacLean BX, Zawadzka AM, Frewen BE, Cusack MP, et al. Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline: application to protein acetylation and phosphorylation. Mol Cell Proteom 2012; 11: 202-14
45. Choi M, Chang CY, Clough T, Broudy D, Killeen T, MacLean B, et al. MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments. Bioinformatics 2014; 30: 2524-6
46. Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, et al. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 2015; 523: 481-5
47. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 2013; 31: 822-6
48. Nicolay B N, Danielian P S, Kottakis F, Lapek J D Jr., Sanidas I, Miles W O, et al. Proteomic analysis of pRb loss highlights a signature of decreased mitochondrial oxidative phosphorylation. Gen Devel 2015; 29: 1875-89.