Next-generation sequencing survey of biliary tract cancer reveals the association between tumor somatic variants and chemotherapy resistance

Cancer

Volumn 122, Issue 23, 2016, Pages 3657-3666

  Ahn, Daniel H ^a,b   Javle, Milind ^c   Ahn, Chul W ^d   Jain, Apurva ^c   Mikhail, Sameh ^a   Noonan, Anne M ^a   Wu, Christina ^a   Shroff, Rachna T ^b   Chen, James L ^a,e   Bekaii Saab, Tanios ^b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

biliary tract cancer; gemcitabine and platinum based therapy response; next generation sequencing; tumor somatic variants

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; FORMALDEHYDE; GEMCITABINE; MUTANT PROTEIN; PARAFFIN; PLATINUM DERIVATIVE; PROTEIN ARID1A; PROTEIN P53; TUMOR MARKER; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE; DEOXYCYTIDINE; PLATINUM COMPLEX;

ADULT; AGED; ARTICLE; BILIARY TRACT CANCER; CANCER INCIDENCE; CANCER PROGNOSIS; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; NEXT GENERATION SEQUENCING; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN ANALYSIS; SOMATIC MUTATION; TREATMENT RESPONSE; VERY ELDERLY; ANALOGS AND DERIVATIVES; BILIARY TRACT NEOPLASMS; DISEASE FREE SURVIVAL; DRUG RESISTANCE; GENETICS; METABOLISM; MIDDLE AGED; MORTALITY; MUTATION; PROGNOSIS; QUESTIONNAIRE; TREATMENT OUTCOME; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BILIARY TRACT NEOPLASMS; CYCLIN-DEPENDENT KINASES; DEOXYCYTIDINE; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MALE; MIDDLE AGED; MUTATION; ORGANOPLATINUM COMPOUNDS; PROGNOSIS; SURVEYS AND QUESTIONNAIRES; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84994226420     PISSN: 0008543X     EISSN: 10970142     Source Type: Journal    
DOI: 10.1002/cncr.30247     Document Type: Article

References (57)

1. Khan SA, Thomas HC, Davidson BR, Taylor-Robinson SD. Cholangiocarcinoma. Lancet. 2005;366:1303–1314.
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65:5–29.
3. Goydos JS, Brumfield AM, Frezza E, Booth A, Lotze MT, Carty SE. Marked elevation of serum interleukin-6 in patients with cholangiocarcinoma: validation of utility as a clinical marker. Ann Surg. 1998;227:398–404.
4. Park J, Tadlock L, Gores GJ, Patel T. Inhibition of interleukin 6–mediated mitogen-activated protein kinase activation attenuates growth of a cholangiocarcinoma cell line. Hepatology. 1999;30:1128–1133.
5. Valle J, Wasan H, Palmer DH, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–1281.
6. Hezel AF, Zhu AX. Systemic therapy for biliary tract cancers. Oncologist. 2008;13:415–423.
7. Eckel F, Schmid RM. Chemotherapy in advanced biliary tract carcinoma: a pooled analysis of clinical trials. Br J Cancer. 2007;96:896–902.
8. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 1993;74:957–967.
9. Vasey PA, Jones NA, Jenkins S, Dive C, Brown R. Cisplatin, camptothecin, and taxol sensitivities of cells with p53-associated multidrug resistance. Mol Pharmacol. 1996;50:1536–1540.
10. Vikhanskaya F, Clerico L, Valenti M, et al. Mechanism of resistance to cisplatin in a human ovarian-carcinoma cell line selected for resistance to doxorubicin: possible role of p53. Int J Cancer. 1997;72:155–159.
11. Choi YJ, Anders L. Signaling through cyclin D-dependent kinases. Oncogene. 2014;33:1890–1903.
12. Wu JN, Roberts CW. ARID1A mutations in cancer: another epigenetic tumor suppressor? Cancer Discov. 2013;3:35–43.
13. Sia D, Losic B, Moeini A, et al. Massive parallel sequencing uncovers actionable FGFR2-PPHLN1 fusion and ARAF mutations in intrahepatic cholangiocarcinoma. Nat Commun. 2015;6:6087.
14. Lee H, Wang K, Johnson A, et al. Comprehensive genomic profiling of extrahepatic cholangiocarcinoma reveals a long tail of therapeutic targets. J Clin Pathol. 2016;69:403–408.
15. Zhu AX, Borger DR, Kim Y, et al. Genomic profiling of intrahepatic cholangiocarcinoma: refining prognosis and identifying therapeutic targets. Ann Surg Oncol. 2014;21:3827–3834.
16. Ross JS, Wang K, Gay L, et al. New routes to targeted therapy of intrahepatic cholangiocarcinomas revealed by next-generation sequencing. Oncologist. 2014;19:235–242.
17. Gnirke A, Melnikov A, Maguire J, et al. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol. 2009;27:182–189.
18. Dahl F, Stenberg J, Fredriksson S, et al. Multigene amplification and massively parallel sequencing for cancer mutation discovery. Proc Natl Acad Sci U S A. 2007;104:9387–9392.
19. Porreca GJ, Zhang K, Li JB, et al. Multiplex amplification of large sets of human exons. Nat Methods. 2007;4:931–936.
20. Foundation One. Technical information and test overview. http://foundationone.com/ONE-I-001-20140804_(nobleed)TechnicalSpecs.pdf?__hstc=197910000.ca54bd200688390fb3cfffed497960ad.1401198872498.1424965584578.1424969165476.20&__hssc=197910000.1.1424969165476&__hsfp=3761051387. Accessed February 26, 2015.
21. Li M, Zhang Z, Li X, et al. Whole-exome and targeted gene sequencing of gallbladder carcinoma identifies recurrent mutations in the ErbB pathway. Nat Genet. 2014;46:872–876.
22. Jiao Y, Pawlik TM, Anders RA, et al. Exome sequencing identifies frequent inactivating mutations in BAP1, ARID1A and PBRM1 in intrahepatic cholangiocarcinomas. Nat Genet. 2013;45:1470–1473.
23. Ong CK, Subimerb C, Pairojkul C, et al. Exome sequencing of liver fluke-associated cholangiocarcinoma. Nat Genet. 2012;44:690–693.
24. Chan-On W, Nairismagi ML, Ong CK, et al. Exome sequencing identifies distinct mutational patterns in liver fluke–related and non–infection-related bile duct cancers. Nat Genet. 2013;45:1474–1478.
25. Robl B, Pauli C, Botter SM, Bode-Lesniewska B, Fuchs B. Prognostic value of tumor suppressors in osteosarcoma before and after neoadjuvant chemotherapy. BMC Cancer. 2015;15:379.
26. Wu RC, Wang TL, Shih IM. The emerging roles of ARID1A in tumor suppression. Cancer Biol Ther. 2014;15:655–664.
27. Reles A, Wen WH, Schmider A, et al. Correlation of p53 mutations with resistance to platinum-based chemotherapy and shortened survival in ovarian cancer. Clin Cancer Res. 2001;7:2984–2997.
28. Fiorini C, Cordani M, Padroni C, Blandino G, Di Agostino S, Donadelli M. Mutant p53 stimulates chemoresistance of pancreatic adenocarcinoma cells to gemcitabine. Biochim Biophys Acta. 2015;1853:89–100.
29. Dhayat SA, Mardin WA, Seggewiss J, et al. MicroRNA profiling implies new markers of gemcitabine chemoresistance in mutant p53 pancreatic ductal adenocarcinoma. PLoS One. 2015;10:e0143755.
30. Katagiri A, Nakayama K, Rahman MT, et al. Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod Pathol. 2012;25:282–288.
31. Lowery WJ, Schildkraut JM, Akushevich L, et al. Loss of ARID1A-associated protein expression is a frequent event in clear cell and endometrioid ovarian cancers. Int J Gynecol Cancer. 2012;22:9–14.
32. Guan B, Wang TL, Shih IM. ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res. 2011;71:6718–6727.
33. Bosse T, ter Haar NT, Seeber LM, et al. Loss of ARID1A expression and its relationship with PI3K-Akt pathway alterations, TP53 and microsatellite instability in endometrial cancer. Mod Pathol. 2013;26:1525–1535.
34. Huang HN, Lin MC, Huang WC, Chiang YC, Kuo KT. Loss of ARID1A expression and its relationship with PI3K-Akt pathway alterations and ZNF217 amplification in ovarian clear cell carcinoma. Mod Pathol. 2014;27:983–990.
35. Bitler BG, Fatkhutdinov N, Zhang R. Potential therapeutic targets in ARID1A-mutated cancers. Expert Opin Ther Targets. 2015;19:1419–1422.
36. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434:917–921.
37. Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434:913–917.
38. Ledermann J, Harter P, Gourley C, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med. 2012;366:1382–1392.
39. Shen J, Peng Y, Wei L, et al. ARID1A deficiency impairs the DNA damage checkpoint and sensitizes cells to PARP inhibitors. Cancer Discov. 2015;5:752–767.
40. Ma X, Ezzeldin HH, Diasio RB. Histone deacetylase inhibitors: current status and overview of recent clinical trials. Drugs. 2009;69:1911–1934.
41. Ruscetti M, Dadashian EL, Guo W, et al. HDAC inhibition impedes epithelial-mesenchymal plasticity and suppresses metastatic, castration-resistant prostate cancer. Oncogene. 2016;35:3781–3795.
42. Vleeshouwer-Neumann T, Phelps M, Bammler TK, MacDonald JW, Jenkins I, Chen EY. Histone deacetylase inhibitors antagonize distinct pathways to suppress tumorigenesis of embryonal rhabdomyosarcoma. PLoS One. 2015;10:e0144320.
43. Bluethner T, Niederhagen M, Caca K, et al. Inhibition of histone deacetylase for the treatment of biliary tract cancer: a new effective pharmacological approach. World J Gastroenterol. 2007;13:4761–4770.
44. Xu LN, Wang X, Zou SQ. Effect of histone deacetylase inhibitor on proliferation of biliary tract cancer cell lines. World J Gastroenterol. 2008;14:2578–2581.
45. Iwahashi S, Ishibashi H, Utsunomiya T, et al. Effect of histone deacetylase inhibitor in combination with 5-fluorouracil on pancreas cancer and cholangiocarcinoma cell lines. J Med Invest. 2011;58:106–109.
46. Wiegand KC, Hennessy BT, Leung S, et al. A functional proteogenomic analysis of endometrioid and clear cell carcinomas using reverse phase protein array and mutation analysis: protein expression is histotype-specific and loss of ARID1A/BAF250a is associated with AKT phosphorylation. BMC Cancer. 2014;14:120.
47. Tanno S, Yanagawa N, Habiro A, et al. Serine/threonine kinase AKT is frequently activated in human bile duct cancer and is associated with increased radioresistance. Cancer Res. 2004;64:3486–3490.
48. Yoon H, Min JK, Lee JW, Kim DG, Hong HJ. Acquisition of chemoresistance in intrahepatic cholangiocarcinoma cells by activation of AKT and extracellular signal-regulated kinase (ERK)1/2. Biochem Biophys Res Commun. 2011;405:333–337.
49. Bitler BG, Aird KM, Garipov A, et al. Synthetic lethality by targeting EZH2 methyltransferase activity in ARID1A-mutated cancers. Nat Med. 2015;21:231–238.
50. Samartzis EP, Gutsche K, Dedes KJ, Fink D, Stucki M, Imesch P. Loss of ARID1A expression sensitizes cancer cells to PI3K- and AKT-inhibition. Oncotarget. 2014;5:5295–5303.
51. Kelley RK, Bardeesy N. Biliary tract cancers: finding better ways to lump and split. J Clin Oncol. 2015;33:2588–2590.
52. Sherr CJ, Beach D, Shapiro GI. Targeting CDK4 and CDK6: from discovery to therapy. Cancer Discov. 2016;6:353–367.
53. Turner NC, Ro J, Andre F, et al. Palbociclib in hormone-receptor–positive advanced breast cancer. N Engl J Med. 2015;373:209–219.
54. Finn RS, Crown JP, Lang I, et al. The cyclin-dependent kinase 4/6 inhibitor palbociclib in combination with letrozole versus letrozole alone as first-line treatment of oestrogen receptor-positive, HER2-negative, advanced breast cancer (PALOMA-1/TRIO-18): a randomised phase 2 study. Lancet Oncol. 2015;16:25–35.
55. Stone A, Sutherland RL, Musgrove EA. Inhibitors of cell cycle kinases: recent advances and future prospects as cancer therapeutics. Crit Rev Oncog. 2012;17:175–198.
56. Fry DW, Harvey PJ, Keller PR, et al. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther. 2004;3:1427–1438.
57. Rashid A, Ueki T, Gao YT, et al. K-ras mutation, p53 overexpression, and microsatellite instability in biliary tract cancers: a population-based study in China. Clin Cancer Res. 2002;8:3156–3163.