Anti-cancer effect and gene modulation of ET-743 in human biliary tract carcinoma preclinical models

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Peraldo Neia, Caterina ^a   Cavalloni, Giuliana ^b   Soster, Marco ^b   Gammaitoni, Loretta ^b   Marchiò, Serena ^b   Sassi, Francesco ^a   Trusolino, Livio ^a   Bertotti, Andrea ^a   Medico, Enzo ^b   Capussotti, Lorenzo ^c   Aglietta, Massimo ^a,b   Leone, Francesco ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b Laboratory of Tumor Microenvironment IRCCS Candiolo   (Italy)

^c MAURIZIANO HOSPITAL   (Italy)

Author keywords

Biliary tract carcinoma; Chemotherapy; ET 743; Patient derived xenograft; Preclinical model

Indexed keywords

ATM PROTEIN; HISTONE H2AX; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; PROTEIN P53; SONIC HEDGEHOG PROTEIN; TRABECTEDIN; WNT PROTEIN; 1,3 DIOXOLANE DERIVATIVE; ALKYLATING AGENT; ATM PROTEIN, HUMAN; H2AFX PROTEIN, HUMAN; HISTONE; TETRAHYDROISOQUINOLINE DERIVATIVE;

AEBP1 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; AOX1 GENE; APOPTOSIS; ARTICLE; BILE DUCT CARCINOMA; C FAM5C GENE; CADM1 GENE; CANCER INHIBITION; CDH11 GENE; CDH2 GENE; CLDN2 GENE; COL14A1 GENE; CONTROLLED STUDY; DNAJB4 GENE; DOWN REGULATION; DRUG EFFECT; DRUG RESPONSE; DRUG SENSITIVITY; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE MODULATION; HSPA6 GENE; HUMAN; HUMAN CELL; IC50; IL6R GENE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; KCMNA1 GENE; MALE; MODULATION; MOUSE; NCAM1 GENE; NONHUMAN; OBFC2A GENE; PCDHGA8 GENE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSTPIP1 GENE; TFF3 GENE; THBS2 GENE; THY1 GENE; TREATMENT DURATION; TUMOR VOLUME; UPREGULATION; WISP1 GENE; WNT SIGNALING PATHWAY; ANIMAL; BILIARY TRACT NEOPLASMS; CELL ADHESION; CELL PROLIFERATION; CELL TRANSFORMATION; DNA REPAIR; DRUG EFFECTS; DRUG SCREENING; GENETICS; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; NONOBESE DIABETIC MOUSE; PHOSPHORYLATION; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BILIARY TRACT NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DIOXOLES; DNA REPAIR; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HISTONES; HUMANS; INTERLEUKIN-6; MICE; MICE, INBRED NOD; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; TETRAHYDROISOQUINOLINES; TUMOR SUPPRESSOR PROTEIN P53; WNT SIGNALING PATHWAY;

EID: 84924357364     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-918     Document Type: Article

References (45)

1. Patel T: Cholangiocarcinoma. Nat Clin Pract 2006,3(1):33-42.
2. Anderson CD, Pinson CW, Berlin J, Chari RS: Diagnosis and treatment of cholangiocarcinoma. Oncologist 2004,9(1):43-57. 10.1634/theoncologist.9-1-43
3. Marino D, Leone F, Cavalloni G, Cagnazzo C, Aglietta M: Biliary tract carcinomas: from chemotherapy to targeted therapy. Crit Rev Oncol/Hematol 2013,85(2):136-148. 10.1016/j.critrevonc.2012.06.006
4. Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, Madhusudan S, Iveson T, Hughes S, Pereira SP, Roughton M, Bridgewater J: Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med 2010,362(14):1273-1281. 10.1056/NEJMoa0908721
5. Valle JW, Furuse J, Jitlal M, Beare S, Mizuno N, Wasan H, Bridgewater J, Okusaka T: Cisplatin and gemcitabine for advanced biliary tract cancer: a meta-analysis of two randomised trials. Ann Oncol 2014,25(2):391-398. 10.1093/annonc/mdt540
6. Okusaka T, Nakachi K, Fukutomi A, Mizuno N, Ohkawa S, Funakoshi A, Nagino M, Kondo S, Nagaoka S, Funai J, Koshiji M, Nambu Y, Furuse J, Miyazaki M, Nimura Y: Gemcitabine alone or in combination with cisplatin in patients with biliary tract cancer: a comparative multicentre study in Japan. Br J Cancer 2010,103(4):469-474. 10.1038/sj.bjc.6605779
7. Erba E, Bergamaschi D, Bassano L, Damia G, Ronzoni S, Faircloth GT, D'Incalci M: Ecteinascidin-743 (ET-743), a natural marine compound, with a unique mechanism of action. Eur J Cancer 2001,37(1):97-105. 10.1016/S0959-8049(00)00357-9
8. Pommier Y, Kohlhagen G, Bailly C, Waring M, Mazumder A, Kohn KW: DNA sequence- and structure-selective alkylation of guanine N2 in the DNA minor groove by ecteinascidin 743, a potent antitumor compound from the Caribbean tunicate Ecteinascidia turbinata. Biochemistry 1996,35(41):13303-13309. 10.1021/bi960306b
9. Valoti G, Nicoletti MI, Pellegrino A, Jimeno J, Hendriks H, D'Incalci M, Faircloth G, Giavazzi R: Ecteinascidin-743, a new marine natural product with potent antitumor activity on human ovarian carcinoma xenografts. Clin Cancer Res 1998,4(8):1977-1983.
10. Hendriks HR, Fiebig HH, Giavazzi R, Langdon SP, Jimeno JM, Faircloth GT: High antitumour activity of ET743 against human tumour xenografts from melanoma, non-small-cell lung and ovarian cancer. Ann Oncol 1999,10(10):1233-1240. 10.1023/A:1008364727071
11. Krasner CN, Poveda A, Herzog TJ, Vermorken JB, Kaye SB, Nieto A, Claret PL, Park YC, Parekh T, Monk BJ: Patient-reported outcomes in relapsed ovarian cancer: results from a randomized phase III study of Trabectedin with Pegylated Liposomal Doxorubicin (PLD) versus PLD Alone. Gynecol Oncol 2012,127(1):161-167. 10.1016/j.ygyno.2012.06.034
12. Baruchel S, Pappo A, Krailo M, Baker KS, Wu B, Villaluna D, Lee-Scott M, Adamson PC, Blaney SM: A phase 2 trial of trabectedin in children with recurrent rhabdomyosarcoma, Ewing sarcoma and non-rhabdomyosarcoma soft tissue sarcomas: a report from the Children's Oncology Group. Eur J Canc 2002,48(4):579-585.
13. Germano G, Frapolli R, Simone M, Tavecchio M, Erba E, Pesce S, Pasqualini F, Grosso F, Sanfilippo R, Casali PG, Gronchi A, Virdis E, Tarantino E, Pilotti S, Greco A, Nebuloni M, Galmarini CM, Tercero JC, Mantovani A, D'Incalci M, Allavena P: Antitumor and anti-inflammatory effects of trabectedin on human myxoid liposarcoma cells. Cancer Res 2010,70(6):2235-2244. 10.1158/0008-5472.CAN-09-2335
14. Schottenfeld D, Beebe-Dimmer J: Chronic inflammation: a common and important factor in the pathogenesis of neoplasia. CA Cancer J Clin 2006,56(2):69-83. 10.3322/canjclin.56.2.69
15. Kulbe H, Chakravarty P, Leinster DA, Charles KA, Kwong J, Thompson RG, Coward JI, Schioppa T, Robinson SC, Gallagher WM, Galletta L, Salako MA, Smyth JF, Hagemann T, Brennan DJ, Bowtell DD, Balkwill FR, Australian Ovarian Cancer Study Group: A dynamic inflammatory cytokine network in the human ovarian cancer microenvironment. Cancer Res 2012,72(1):66-75. 10.1158/0008-5472.CAN-11-2178
16. Mantovani A, Allavena P, Sica A: Tumour-associated macrophages as a prototypic type II polarised phagocyte population: role in tumour progression. Eur J Cancer 2004,40(11):1660-1667. 10.1016/j.ejca.2004.03.016
17. Lewis CE, Pollard JW: Distinct role of macrophages in different tumor microenvironments. Cancer Res 2006,66(2):605-612. 10.1158/0008-5472.CAN-05-4005
18. Allavena P, Mantovani A: Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 2012,167(2):195-205. 10.1111/j.1365-2249.2011.04515.x
19. Orre M, Rogers PA: Macrophages and microvessel density in tumors of the ovary. Gynecol Oncol 1999,73(1):47-50. 10.1006/gyno.1998.5292
20. Germano G, Frapolli R, Belgiovine C, Anselmo A, Pesce S, Liguori M, Erba E, Uboldi S, Zucchetti M, Pasqualini F, Nebuloni M, van Rooijen N, Mortarini R, Beltrame L, Marchini S, Fuso Nerini I, Sanfilippo R, Casali PG, Pilotti S, Galmarini CM, Anichini A, Mantovani A, D'Incalci M, Allavena P: Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell 2013,23(2):249-262. 10.1016/j.ccr.2013.01.008
21. Subimerb C, Pinlaor S, Lulitanond V, Khuntikeo N, Okada S, McGrath MS, Wongkham S: Circulating CD14(+) CD16(+) monocyte levels predict tissue invasive character of cholangiocarcinoma. Clin Exp Immunol 2010,161(3):471-479. 10.1111/j.1365-2249.2010.04200.x
22. Gore L, Rivera E, Basche M, Moulder-Thompson SL, Li J, Eppers S, Grolnic S, O'Bryant C, Cleere D, Elsayed YA, Eckhardt SG: Phase I combination study of trabectedin and capecitabine in patients with advanced malignancies. Invest New Drugs 2012,30(5):1942-1949. 10.1007/s10637-011-9747-9
23. Peraldo Neia C, Cavalloni G, Chiorino G, Ostano P, Aglietta M, Leone F: Antitumor activity, gene and miRNA modulation upon ET-743 treatment in an intrahepatic cholangiocarcinoma patient derived xenograft model. In Annual Meeting of American Association for Cancer Research. San Diego, CA: Philadelphia, PA Abstract Number 5551; 2014.
24. Takahashi N, Li W, Banerjee D, Guan Y, Wada-Takahashi Y, Brennan MF, Chou TC, Scotto KW, Bertino JR: Sequence-dependent synergistic cytotoxicity of ecteinascidin-743 and paclitaxel in human breast cancer cell lines in vitro and in vivo. Cancer Res 2002,62(23):6909-6915.
25. D'Incalci M, Colombo T, Ubezio P, Nicoletti I, Giavazzi R, Erba E, Ferrarese L, Meco D, Riccardi R, Sessa C, Cavallini E, Jimeno J, Faircloth GT: The combination of yondelis and cisplatin is synergistic against human tumor xenografts. Eur J Cancer 2003,39(13):1920-1926. 10.1016/S0959-8049(03)00490-8
26. Romano M, Frapolli R, Zangarini M, Bello E, Porcu L, Galmarini CM, García-Fernández LF, Cuevas C, Allavena P, Erba E, D'Incalci M: Comparison of in vitro and in vivo biological effects of trabectedin, lurbinectedin (PM01183) and Zalypsis® (PM00104). Int J Cancer 2013,133(9):2024-2033. 10.1002/ijc.28213
27. Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
28. Pignochino Y, Sarotto I, Peraldo-Neia C, Penachioni JY, Cavalloni G, Migliardi G, Casorzo L, Chiorino G, Risio M, Bardelli A, Aglietta M, Leone F: Targeting EGFR/HER2 pathways enhances the antiproliferative effect of gemcitabine in biliary tract and gallbladder carcinomas. BMC Cancer 2010, 10:631. 10.1186/1471-2407-10-631
29. Mosnier JF, Kandel C, Cazals-Hatem D, Bou-Hanna C, Gournay J, Jarry A, Laboisse CL: N-cadherin serves as diagnostic biomarker in intrahepatic and perihilar cholangiocarcinomas. Mod Pathol 2009,22(2):182-190. 10.1038/modpathol.2008.123
30. Rivat C, Christine R, Rodrigues S, Sylvie R, Bruyneel E, Erik B, Piétu G, Geneviève P, Robert A, Amélie R, Rivat C, Rodrigues S, Bruyneel E, Piétu G, Robert A, Redeuilh G, Bracke M, Gespach C, Attoub S: Implication of STAT3 signaling in human colonic cancer cells during intestinal trefoil factor 3 (TFF3) - and vascular endothelial growth factor-mediated cellular invasion and tumor growth. Cancer Res 2005,65(1):195-202.
31. Shimizu T, Yokomuro S, Mizuguchi Y, Kawahigashi Y, Arima Y, Taniai N, Mamada Y, Yoshida H, Akimaru K, Tajiri T: Effect of transforming growth factor-beta1 on human intrahepatic cholangiocarcinoma cell growth. World J Gastroenterol 2006,12(39):6316-6324.
32. Benckert C, Jonas S, Cramer T, Von Marschall Z, Schäfer G, Peters M, Wagner K, Radke C, Wiedenmann B, Neuhaus P, Höcker M, Rosewicz S: Transforming growth factor beta 1 stimulates vascular endothelial growth factor gene transcription in human cholangiocellular carcinoma cells. Cancer Res 2003,63(5):1083-1092.
33. André T, Tournigand C, Rosmorduc O, Provent S, Maindrault-Goebel F, Avenin D, Selle F, Paye F, Hannoun L, Houry S, Gayet B, Lotz JP, de Gramont A, Louvet C: Gemcitabine combined with oxaliplatin (GEMOX) in advanced biliary tract adenocarcinoma: a GERCOR study. Ann Oncol 2004,15(9):1339-1343. 10.1093/annonc/mdh351
34. Gütgemann I, Haas S, Berg JP, Zhou H, Büttner R, Fischer HP: CD56 expression aids in the differential diagnosis of cholangiocarcinomas and benign cholangiocellular lesions. Virchows Arch 2006,448(4):407-411. 10.1007/s00428-005-0145-6
35. Isomoto H: Epigenetic alterations in cholangiocarcinoma-sustained IL-6/STAT3 signaling in cholangio- carcinoma due to SOCS3 epigenetic silencing. Digestion 2009,79(Suppl 1):2-8.
36. El Khatib M, Kalnytska A, Palagani V, Kossatz U, Manns MP, Malek NP, Wilkens L, Plentz RR: Inhibition of hedgehog signaling attenuates carcinogenesis in vitro and increases necrosis of cholangiocellular carcinoma. Hepatology 2013,57(3):1035-1045. 10.1002/hep.26147
37. Riedlinger D, Bahra M, Boas-Knoop S, Lippert S, Bradtmöller M, Guse K, Seehofer D, Bova R, Sauer IM, Neuhaus P, Koch A, Kamphues C: Hedgehog pathway as a potential treatment target in human cholangiocarcinoma. J Hepatobiliary Pancreat Sci 2014,21(8):607-615. 10.1002/jhbp.107
38. Zhang KS, Zhou Q, Wang YF, Liang LJ: Inhibition of Wnt signaling induces cell apoptosis and suppresses cell proliferation in cholangiocarcinoma cells. Oncol Rep 2013,30(3):1430-1438.
39. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W: Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 2002,12(2):162-169. 10.1016/S0959-437X(02)00282-4
40. Guirouilh-Barbat J, Redon C, Pommier Y: Transcription-coupled DNA double-strand breaks are mediated via the nucleotide excision repair and the Mre11-Rad50-Nbs1 complex. Mol Biol Cell 2008,19(9):3969-3981. 10.1091/mbc. E08-02-0215
41. Bertotti A, Migliardi G, Galimi F, Sassi F, Torti D, Isella C, Corà D, Di Nicolantonio F, Buscarino M, Petti C, Ribero D, Russolillo N, Muratore A, Massucco P, Pisacane A, Molinaro L, Valtorta E, Sartore-Bianchi A, Risio M, Capussotti L, Gambacorta M, Siena S, Medico E, Sapino A, Marsoni S, Comoglio PM, Bardelli A, Trusolino L: A molecularly annotated platform of patient-derived xenografts (xenopatients) identifies HER2 as an effective therapeutic target in cetuximab-resistant colorectal cancer. Canc Discov 2011,1(6):508-523. 10.1158/2159-8290.CD-11-0109
42. Bertotti A, Trusolino L: From bench to bedside: does preclinical practice in translational oncology need some rebuilding? J Natl Cancer Inst 2013,105(19):1426-1427. 10.1093/jnci/djt253
43. Tanaka S, Sugimachi K, Kameyama T, Maehara S, Shirabe K, Shimada M, Wands JR, Maehara Y: Human WISP1v, a member of the CCN family, is associated with invasive cholangiocarcinoma. Hepatology 2003,37(5):1122-1129. 10.1053/jhep.2003.50187
44. Ailawadhi S, Nagase H, Khoury T, Yu J, Tan D, Black J, Brattain M, Javle M: Intestinal trefoil factor (TFF-3) and extracellular signal-regulated kinase (ERK) in cholangiocarcinoma. Hepatogastroenterology 2007,54(77):1339-1344.
45. The pre-publication history for this paper can be accessed here: http://www.biomedcentral.com/1471-2407/14/918/prepub