Carboxylesterase 2 as a Determinant of Response to Irinotecan and Neoadjuvant FOLFIRINOX Therapy in Pancreatic Ductal Adenocarcinoma

Journal of the National Cancer Institute

Volumn 107, Issue 8, 2015, Pages

  Capello, Michela ^a   Lee, Minhee ^b   Wang, Hong ^a   Babel, Ingrid ^b   Katz, Matthew H ^a   Fleming, Jason B ^a   Maitra, Anirban ^a   Wang, Huamin ^a   Tian, Weihua ^a   Taguchi, Ayumu ^a   Hanash, Samir M ^a  

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

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLESTERASE; CARBOXYLESTERASE 2; FIRTECAN; FLUOROURACIL; FOLINIC ACID; IRINOTECAN; MESSENGER RNA; OXALIPLATIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CAMPTOTHECIN; CES2 PROTEIN, HUMAN; PLATINUM COMPLEX;

ADJUVANT THERAPY; ADULT; AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CANCER ADJUVANT THERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CANCER SURVIVAL; CANCER TISSUE; CELL LYSATE; CELL SURFACE; CELL VIABILITY; CELLULAR DISTRIBUTION; CLINICAL FEATURE; ENZYME ACTIVITY; ENZYME SUBSTRATE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; IC50; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SPACE; MALE; MASS SPECTROMETRY; MIDDLE AGED; MULTIPLE CYCLE TREATMENT; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEOMICS; RNA SEQUENCE; TISSUE MICROARRAY; TISSUE SECTION; TREATMENT RESPONSE; WESTERN BLOTTING; ADJUVANT CHEMOTHERAPY; AGED; ANALOGS AND DERIVATIVES; CARCINOMA, PANCREATIC DUCTAL; DRUG SCREENING; ENZYMOLOGY; GENETICS; KAPLAN MEIER METHOD; METABOLISM; PANCREATIC NEOPLASMS; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TREATMENT OUTCOME; TUMOR CELL LINE;

ADULT; AGED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CAMPTOTHECIN; CARBOXYLESTERASE; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CHEMOTHERAPY, ADJUVANT; FEMALE; FLUOROURACIL; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MASS SPECTROMETRY; MIDDLE AGED; NEOADJUVANT THERAPY; ORGANOPLATINUM COMPOUNDS; PANCREATIC NEOPLASMS; RADIOTHERAPY, ADJUVANT; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TISSUE ARRAY ANALYSIS; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84939456074     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djv132     Document Type: Article

References (47)

1. Rawlings ND, Barrett AJ, Bateman A. MEROPS: the peptidase database. Nucleic Acids Res. 2010;38(Database issue):D227-D233.
2. Simon GM, Cravatt BF. Activity-based proteomics of enzyme superfamilies: serine hydrolases as a case study. J Biol Chem. 2010;285(15):11051-11055.
3. Nomura DK, Long JZ, Niessen S, et al. Monoacylglycerol lipase regulates a fatty acid network that promotes cancer pathogenesis. Cell. 2010;140(1):49-61.
4. Shields DJ, Niessen S, Murphy EA, et al. RBBP9: a tumor-associated serine hydrolase activity required for pancreatic neoplasia. Proc Natl Acad Sci U S A. 2010;107(5):2189-2194.
5. Borgono CA, Diamandis EP. The emerging roles of human tissue kallikreins in cancer. Nat Rev Cancer. 2004;4(11):876-890.
6. Del Rosso M, Fibbi G, Pucci M, et al. Multiple pathways of cell invasion are regulated by multiple families of serine proteases. Clin Exp Metastasis. 2002;19(3):193-207.
7. Jessani N, Humphrey M, McDonald WH, et al. Carcinoma and stromal enzyme activity profiles associated with breast tumor growth in vivo. Proc Natl Acad Sci U S A. 2004;101(38):13756-13761.
8. Bachovchin DA, Cravatt BF. The pharmacological landscape and therapeutic potential of serine hydrolases. Nat Rev Drug Discov. 2012;11(1):52-68.
9. Siegel R, Ma J, Zou Z, et al. Cancer statistics, 2014. CA Cancer J Clin. 2014;64(1):9-29.
10. Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med. 2014;371(11):1039-1049.
11. Conroy T, Desseigne F, Ychou M, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364(19):1817-1825.
12. Von Hoff DD, Goldstein D, Renschler MF. Albumin-bound paclitaxel plus gemcitabine in pancreatic cancer. N Engl J Med. 2014;370(5):479-480.
13. Khanna R, Morton CL, Danks MK, et al. Proficient metabolism of irinotecan by a human intestinal carboxylesterase. Cancer Res. 2000;60(17):4725-4728.
14. Xu G, Zhang W, Ma MK, et al. Human carboxylesterase 2 is commonly expressed in tumor tissue and is correlated with activation of irinotecan. Clin Cancer Res. 2002;8(8):2605-2611.
15. Jones RP, Sutton P, Greensmith RM, et al. Hepatic activation of irinotecan predicts tumour response in patients with colorectal liver metastases treated with DEBIRI: exploratory findings from a phase II study. Cancer Chemother Pharmacol. 2013;72(2):359-368.
16. Hwang RF, Wang H, Lara A, et al. Development of an integrated biospecimen bank and multidisciplinary clinical database for pancreatic cancer. Ann Surg Oncol. 2008;15(5):1356-1366.
17. Tzeng CW, Fleming JB, Lee JE, et al. Defined clinical classifications are associated with outcome of patients with anatomically resectable pancreatic adenocarcinoma treated with neoadjuvant therapy. Ann Surg Oncol. 2012;19(6):2045-2053.
18. Katz MH, Marsh R, Herman JM, et al. Borderline resectable pancreatic cancer: need for standardization and methods for optimal clinical trial design. Ann Surg Oncol. 2013;20(8):2787-2795.
19. Katz MH, Fleming JB, Bhosale P, et al. Response of borderline resectable pancreatic cancer to neoadjuvant therapy is not reflected by radiographic indicators. Cancer. 2012;118(23):5749-5756.
20. Beaufay H, Amar-Costesec A, Feytmans E, et al. Analytical study of microsomes and isolated subcellular membranes from rat liver. I. Biochemical methods. J Cell Biol. 1974;61(1):188-200.
21. Simplicio AL, Coroadinha AS, Gilmer JF, et al. A methodology for detection and quantification of esterase activity. Methods Mol Biol. 2013;984:309-319.
22. Wang H, Zhang W, Fuller GN. Tissue microarrays: applications in neuropathology research, diagnosis, and education. Brain Pathol. 2002;12(1):95-107.
23. Kim MP, Evans DB, Wang H, et al. Generation of orthotopic and heterotopic human pancreatic cancer xenografts in immunodeficient mice. Nat Protoc. 2009;4(11):1670-1680.
24. Kim MP, Truty MJ, Choi W, et al. Molecular profiling of direct xenograft tumors established from human pancreatic adenocarcinoma after neoadjuvant therapy. Ann Surg Oncol. 2012;19(Suppl 3):S395-S403.
25. Satoh T, Hosokawa M. The mammalian carboxylesterases: from molecules to functions. Annu Rev Pharmacol Toxicol. 1998;38:257-288.
26. Li B, Sedlacek M, Manoharan I, et al. Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma. Biochem Pharmacol. 2005;70(11):1673-1684.
27. Lamego J, Coroadinha AS, Simplicio AL. Detection and quantification of carboxylesterase 2 activity by capillary electrophoresis. Anal Chem. 2011;83(3):881-887.
28. Crow JA, Borazjani A, Potter PM, et al. Hydrolysis of pyrethroids by human and rat tissues: examination of intestinal, liver and serum carboxylesterases. Toxicol Appl Pharmacol. 2007;221(1):1-12.
29. Quinney SK, Sanghani SP, Davis WI, et al. Hydrolysis of capecitabine to 5′-deoxy-5-fluorocytidine by human carboxylesterases and inhibition by loperamide. J Pharmacol Exp Ther. 2005;313(3):1011-1016.
30. Papadatos-Pastos D, Thillai K, Rabbie R, et al. FOLFIRINOX - a new paradigm in the treatment of pancreatic cancer. Expert Rev Anticancer Ther. 2014;14(10):1115-1125.
31. Choi W, Cogdell D, Feng Y, et al. Transcriptional activation of the carboxylesterase 2 gene by the p53 pathway. Cancer Biol Ther. 2006;5(11):1450-1456.
32. Ellinger-Ziegelbauer H, Stuart B, Wahle B, et al. Characteristic expression profiles induced by genotoxic carcinogens in rat liver. Toxicol Sci. 2004;77(1):19-34.
33. Hatfield MJ, Tsurkan L, Garrett M, et al. Organ-specific carboxylesterase profiling identifies the small intestine and kidney as major contributors of activation of the anticancer prodrug CPT-11. Biochem Pharmacol. 2011;81(1):24-31.
34. Kawato Y, Aonuma M, Hirota Y, et al. Intracellular roles of SN-38, a metabolite of the camptothecin derivative CPT-11, in the antitumor effect of CPT-11. Cancer Res. 1991;51(16):4187-4191.
35. Cunningham D, Pyrhonen S, James RD, et al. Randomised trial of irinotecan plus supportive care versus supportive care alone after fluorouracil failure for patients with metastatic colorectal cancer. Lancet. 1998;352(9138):1413-1418.
36. Rougier P, Van Cutsem E, Bajetta E, et al. Randomised trial of irinotecan versus fluorouracil by continuous infusion after fluorouracil failure in patients with metastatic colorectal cancer. Lancet. 1998;352(9138):1407-1412.
37. Vanhoefer U, Harstrick A, Achterrath W, et al. Irinotecan in the treatment of colorectal cancer: clinical overview. J Clin Oncol. 2001;19(5):1501-1518.
38. Fukuoka M, Niitani H, Suzuki A, et al. A phase II study of CPT-11, a new derivative of camptothecin, for previously untreated non-small-cell lung cancer. J Clin Oncol. 1992;10(1):16-20.
39. Uchida K, Otake K, Tanaka K, et al. Clinical implications of CES2 RNA expression in neuroblastoma. J Pediatr Surg. 2013;48(3):502-509.
40. Yano H, Kayukawa S, Iida S, et al. Overexpression of carboxylesterase-2 results in enhanced efficacy of topoisomerase I inhibitor, irinotecan (CPT- 11), for multiple myeloma. Cancer Sci. 2008;99(11):2309-2314.
41. Schiel MA, Green SL, Davis WI, et al. Expression and characterization of a human carboxylesterase 2 splice variant. J Pharmacol Exp Ther. 2007;323(1):94-101.
42. Xu Y, Villalona-Calero MA. Irinotecan: mechanisms of tumor resistance and novel strategies for modulating its activity. Ann Oncol. 2002;13(12): 1841-1851.
43. Sakata Y, Shimada Y, Yoshino M, et al. [A late phase II study of CPT-11, irinotecan hydrochloride, in patients with advanced pancreatic cancer. CPT-11 Study Group on Gastrointestinal Cancer]. Gan To Kagaku Ryoho. 1994;21(7):1039-1046.
44. Wagener DJ, Verdonk HE, Dirix LY, et al. Phase II trial of CPT-11 in patients with advanced pancreatic cancer, an EORTC early clinical trials group study. Ann Oncol. 1995;6(2):129-132.
45. Ueno H, Okusaka T, Funakoshi A, et al. A phase II study of weekly irinotecan as first-line therapy for patients with metastatic pancreatic cancer. Cancer Chemother Pharmacol. 2007;59(4):447-454.
46. Ko AH, Tempero MA, Shan YS, et al. A multinational phase 2 study of nanoliposomal irinotecan sucrosofate (PEP02, MM-398) for patients with gemcitabine-refractory metastatic pancreatic cancer. Br J Cancer. 2013;109(4):920-925.
47. Pratt SE, Durland-Busbice S, Shepard RL, et al. Human carboxylesterase-2 hydrolyzes the prodrug of gemcitabine (LY2334737) and confers prodrug sensitivity to cancer cells. Clin Cancer Res. 2013;19(5):1159-1168.