Proton pump inhibitors (PPIs) impact on tumour cell survival, metastatic potential and chemotherapy resistance, and affect expression of resistance-relevant miRNAs in esophageal cancer

Journal of Experimental and Clinical Cancer Research

Volumn 33, Issue 1, 2014, Pages

  Lindner, Kirsten ^a   Borchardt, Christiane ^a   Schöpp, Maren ^a   Bürgers, Anja ^a   Stock, Christian ^b   Hussey, Damian J ^c   Haier, Jörg ^b   Hummel, Richard ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c FLINDERS UNIVERSITY   (Australia)

Author keywords

Chemotherapy; Esophageal cancer; Metastasis; microRNA; PPI; Proton pump inhibitor; Resistance

Indexed keywords

CISPLATIN; ESOMEPRAZOLE; FLUOROURACIL; MICRORNA; MICRORNA 141; MICRORNA 155; MICRORNA 16; MICRORNA 200A; MICRORNA 200B; MICRORNA 200C; MICRORNA 221; MICRORNA 222; MICRORNA 24; MICRORNA 26A; PROTON PUMP INHIBITOR; ANTINEOPLASTIC AGENT; MIRN141 MICRORNA, HUMAN; MIRN200 MICRORNA, HUMAN; MIRN376 MICRORNA, HUMAN;

ACIDIFICATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL ADHESION; CELL MIGRATION; CELL PH; CELL SURVIVAL; CELL VIABILITY ASSAY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL CANCER CELL LINE; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS CANCER; HUMAN; HUMAN CELL; LD 50; METASTASIS POTENTIAL; PROTEIN EXPRESSION; SQUAMOUS CELL CARCINOMA CELL; TUMOR CELL; ADENOCARCINOMA; CARCINOMA, SQUAMOUS CELL; CELL MOTION; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PH; TUMOR CELL LINE; TUMOR INVASION;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; CISPLATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; ESOMEPRAZOLE; ESOPHAGEAL NEOPLASMS; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROGEN-ION CONCENTRATION; MICRORNAS; NEOPLASM INVASIVENESS; PROTON PUMP INHIBITORS;

EID: 84906966131     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/s13046-014-0073-x     Document Type: Article

References (45)

1. Time trends of gastroesophageal reflux disease: a systematic review. HB El-Serag, Clinical Gastroent Hepatol 2007 5 17 26 10.1016/j.cgh.2006.09.016
2. Increasing incidence of Barrett's oesophagus in the general population. EM van Soest, JP Dieleman, PD Siersema, MC Sturkenboom, EJ Kuipers, Gut 2005 54 1062 1066 10.1136/gut.2004.063685 15857935
3. Histomorphologic tumor regression and lymph node metastases determine prognosis following neoadjuvant radiochemotherapy for esophageal cancer: implications for response classification. PM Schneider, SE Baldus, R Metzger, M Kocher, R Bongartz, E Bollschweiler, H Schaefer, J Thiele, HP Dienes, RP Mueller, AH Hoelscher, Ann Surg 2005 242 684 692 10.1097/01.sla.0000186170.38348.7b 16244542
4. A meta-analysis of randomized controlled trials that compared neoadjuvant chemoradiation and surgery to surgery alone for resectable esophageal cancer. JD Urschel, H Vasan, Am J Surg 2003 185 538 543 10.1016/S0002-9610(03)00066-7 12781882
5. Preoperative chemoradiotherapy for oesophageal cancer: a systematic review and meta-analysis. F Fiorica, D Di Bona, F Schepis, A Licata, L Shahied, A Venturi, AM Falchi, A Craxì C Cammà Gut 2004 53 925 930 10.1136/gut.2003.025080 15194636
6. Neoadjuvant chemoradiotherapy for esophageal carcinoma. X Zhang, DI Watson, GG Jamieson, JR Bessell, PG Devitt, Dis Esophagus 2005 18 104 108 10.1111/j.1442-2050.2005.00461.x 16053485
7. Survival benefits from neoadjuvant chemoradiotherapy or chemotherapy in oesophageal carcinoma: a meta-analysis. V Gebski, B Burmeister, BM Smithers, K Foo, J Zalcberg, J Simes, Lancet Oncol 2007 8 226 234 10.1016/S1470-2045(07)70039-6 17329193
8. Long-term outcomes following neoadjuvant chemoradiotherapy. JV Reynolds, C Muldoon, D Hollywood, N Ravi, S Rowley, K O'Byrne, J Kennedy, TJ Murphy, Ann Surg 2007 245 707 716 10.1097/01.sla.0000254367.15810.38 17457163
9. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. KM Sjoquist, BH Burmeister, BM Smithers, JR Zalcberg, RJ Simes, A Barbour, V Gebski, Lancet Oncol 2011 12 681 692 10.1016/S1470-2045(11)70142-5 21684205
10. Mir-148a improves response to chemotherapy in sensitive and resistant oesophageal adenocarcinoma and squamous cell carcinoma cells. R Hummel, DI Watson, C Smith, J Kist, MZ Michael, J Haier, DJ Hussey, J Gastrointest Surg 2011 15 429 438 10.1007/s11605-011-1418-9 21246413
11. Chemoradiotherapy in gastrointestinal malignancies. CG Willett, BG Czito, Clin Oncol 2009 21 543 556 10.1016/j.clon.2009.05.004
12. Outcomes from chemoradiotherapy for patients with esophageal cancer. AZ Pantling, JA Gossage, R Mamidanna, G Newman, A Robinson, DK Manifold, PC Hale, Dis Esophagus 2011 24 172 176 10.1111/j.1442-2050.2010.01121.x 21073614
13. Proton pump inhibitors as anti vacuolar-ATPases drugs: a novel anticancer strategy. EP Spugnini, G Citro, S Fais, J Exp Clin Cancer Res 2010 8 44 10.1186/1756-9966-29-44
14. Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspase-independent mechanism involving reactive oxygen species. A De Milito, E Iessi, M Logozzi, F Lozupone, M Spada, ML Marino, C Federici, M Perdicchio, P Matarrese, L Lugini, A Nilsson, S Fais, Cancer Res 2007 67 5408 5417 10.1158/0008-5472.CAN-06-4095 17545622
15. Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. N Raghunand, BP Mahoney, RJ Gillies, Biochem Pharmacol 2003 66 1219 1229 10.1016/S0006-2952(03)00468-4 14505801
16. Small interfering RNA targeting the subunit ATP6L of proton pump V-ATPase overcomes chemoresistance of breast cancer cells. H You, J Jin, H Shu, B Yu, A De Milito, F Lozupone, Y Deng, N Tang, G Yao, S Fais, J Gu, W Qin, Cancer Lett 2009 280 110 119 10.1016/j.canlet.2009.02.023 19299075
17. Function of a subunit isoforms of the V-ATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. A Hinton, SR Sennoune, S Bond, M Fang, M Reuveni, GG Sahagian, D Jay, R Martinez-Zaguilan, M Forgac, J Biol Chem 2009 284 16400 16408 10.1074/jbc.M901201200 19366680
18. Intracellular pH regulation in oral squamous cell carcinoma is mediated by increased V-ATPase activity via over-expression of the ATP6V1C1 gene. EM Otero-Rey, M Somoza-Martín, F Barros-Angueira, A García-García, Oral Oncol 2008 44 193 199 10.1016/j.oraloncology.2007.02.011 17467328
19. V-ATPase inhibitors and implication in cancer treatment. M Pérez-Sayáns, JM Somoza-Martín, F Barros-Angueira, JM Rey, A García-García, Cancer Treat Rev 2009 35 707 713 10.1016/j.ctrv.2009.08.003 19758758
20. The growth and metastasis of human hepatocellular carcinoma xenografts are inhibited by small interfering RNA targeting to the subunit ATP6L of proton pump. X Lu, W Qin, J Li, N Tan, D Pan, H Zhang, L Xie, G Yao, H Shu, M Yao, D Wan, J Gu, S Yang, Cancer Res 2005 65 6843 6849 10.1158/0008-5472.CAN-04-3822 16061667
21. The vacuolar-ATPase modulates matrix metalloproteinase isoforms in human pancreatic cancer. C Chung, CC Mader, JC Schmitz, J Atladottir, P Fitchev, ML Cornwell, AJ Koleske, SE Crawford, F Gorelick, Lab Invest 2011 91 732 743 10.1038/labinvest.2011.8 21339745
22. Silencing of a novel tumor metastasis suppressor gene LASS2/TMSG1 promotes invasion of prostate cancer cell in vitro through increase of vacuolar ATPase activity. X Xu, J You, F Pei, J Cell Biochem 2012 113 2356 2363 10.1002/jcb.24106 22573553
23. Inhibitors of vacuolar ATPase proton pumps inhibit human prostate cancer cell invasion and prostate-specific antigen expression and secretion. V Michel, Y Licon-Munoz, K Trujillo, M Bisoffi, KJ Parra, Int J Cancer 2012 132 1 10 10.1002/ijc.27811
24. PH and drug resistance. I. Functional expression of plasmalemmal V-type H + -ATPase in drug-resistant human breast carcinoma cell lines. R Martínez-Zaguilán, N Raghunand, RM Lynch, W Bellamy, GM Martinez, B Rojas, D Smith, WS Dalton, RJ Gillies, Biochem Pharmacol 1999 57 1037 1046 10.1016/S0006-2952(99)00022-2 10796074
25. Intracellular proton pumps as targets in chemotherapy: V-ATPases and cancer. A Hernandez, G Serrano-Bueno, JR Perez-Castineira, A Serrano, Curr Pharm 2012 18 1383 1394 10.2174/138161212799504821
26. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. F Luciani, M Spada, A De Milito, A Molinari, L Rivoltini, A Montinaro, M Marra, L Lugini, M Logozzi, F Lozupone, C Federici, E Iessi, G Parmiani, G Arancia, F Belardelli, S Fais, J Natl Cancer Inst 2004 96 1702 1713 10.1093/jnci/djh305 15547183
27. Selective induction of apoptosis with proton pump inhibitor in gastric cancer cells. M Yeo, DK Kim, YB Kim, TY Oh, JE Lee, SW Cho, HC Kim, KB Hahm, Clin Cancer Res 2004 10 8687 8696 10.1158/1078-0432.CCR-04-1065 15623654
28. The proton pump inhibitor inhibits cell growth and induces apoptosis in human hepatoblastoma. T Morimura, K Fujita, M Akita, M Nagashima, A Satomi, Pediatr Surg Int 2008 24 1087 1094 10.1007/s00383-008-2229-2 18712525
29. Chemotherapy-induced modification of microRNA expression in esophageal cancer. R Hummel, T Wang, DI Watson, MZ Michael, M Van der Hoek, J Haier, DJ Hussey, Oncol Rep 2011 26 1011 1017 21743970
30. The multiple facets of drug resistance: one history, different approaches. EL Niero, B Rocha-Sales, C Lauand, BA Cortez, MM de Souza, P Rezende-Teixeira, MS Urabayashi, AA Martens, JH Neves, GM Machado-Santelli, J Exp Clin Cancer Res 2014 33 37 10.1186/1756-9966-33-37 24775603
31. Antimetastatic effect of a small-molecule vacuolar H + -ATPase inhibitor in in vitro and in vivo preclinical studies. R Supino, G Petrangolini, G Pratesi, M Tortoreto, E Favini, LD Bo, P Casalini, E Radaelli, AC Croce, G Bottiroli, P Misiano, C Farina, F Zunino, J Pharmacol Exp Ther 2008 324 15 22 10.1124/jpet.107.128587 17909082
32. Effects and mechanisms of proton pump inhibitors as a novel chemosensitizer on human gastric adenocarcinoma (SGC7901) cells. M Chen, X Zou, H Luo, J Cao, X Zhang, B Zhang, W Liu, Cell Biol Int 2009 33 1008 1019 10.1016/j.cellbi.2009.05.004 19501661
33. Inhibitors of vacuolar H + -ATPase impair the preferential accumulation of daunomycin in lysosomes and reverse the resistance to anthracyclines in drug-resistant renal epithelial cells. Z Ouar, M Bens, C Vignes, M Paulais, C Pringel, J Fleury, F Cluzeaud, R Lacave, A Vandewalle, Biochem J 2003 370 185 193 10.1042/BJ20021411 12435274
34. Vacuolar H + -ATPase inhibitors overcome Bcl-xL-mediated chemoresistance through restoration of a caspase-independent apoptotic pathway. Y Sasazawa, Y Futamura, E Tashiro, M Imoto, Cancer Sci 2009 100 1460 1467 10.1111/j.1349-7006.2009.01194.x 19459857
35. Extracellular acidity as favouring factor of tumor progression and metastatic dissemination. L Calorini, S Peppicelli, F Bianchini, Exp Oncol 2012 34 79 84 23013757
36. The vacuolar (H+)-ATPases-nature's most versatile proton pumps. T Nishi, M Forgac, Nat Rev Mol Cell Biol 2002 3 94 103 10.1038/nrm729 11836511
37. High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers. S Walenta, M Wetterling, M Lehrke, G Schwickert, K Sundfør, EK Rofstad, W Mueller-Klieser, Cancer Res 2000 60 916 921 10706105
38. Clastogenicity of low pH to various cultured mammalian cells. T Morita, T Nagaki, I Fukuda, K Okumura, Mutat Res 1992 268 297 305 10.1016/0027-5107(92)90235-T 1379335
39. MicroRNA-141 confers resistance to cisplatin-induced apoptosis by targeting YAP1 in human esophageal squamous cell carcinoma. Y Imanaka, S Tsuchiya, F Sato, Y Shimada, K Shimizu, G Tsujimoto, J Hum Genet 2011 56 270 276 10.1038/jhg.2011.1 21289630
40. miR-141 regulates KEAP1 and modulates cisplatin sensitivity in ovarian cancer cells. MT van Jaarsveld, J Helleman, AW Boersma, PF van Kuijk, WF van Ijcken, E Despierre, I Vergote, RH Mathijssen, EM Berns, J Verweij, J Pothof, EA Wiemer, Oncogene 2013 32 4284 4293 10.1038/onc.2012.433 23045278
41. MicroRNA-200b regulates cell proliferation, invasion, and migration by directly targeting ZEB2 in gastric carcinoma. J Kurashige, H Kamohara, M Watanabe, Y Hiyoshi, M Iwatsuki, Y Tanaka, K Kinoshita, S Saito, Y Baba, H Baba, Ann Surg Oncol 2012 19 656 S664 10.1245/s10434-012-2217-6 22311119
42. MicroRNA expression profiles associated with development of drug resistance in Ehrlich ascites tumor cells. S Husted, R Søkilde, L Rask, S Cirera, PK Busk, J Eriksen, T Litman, Mol Pharm 2011 8 2055 2062 10.1021/mp200255d 21899346
43. Formosa A, Markert EK, Lena AM, Italiano D, Finazzi-Agro E, Levine AJ, Bernardini S, Garabadgiu AV, Melino G, Candi E: MicroRNAs, miR-154, miR-299-5p, miR-376a, miR-376c, miR-377, miR-381, miR-487b, miR-485-3p, miR-495 and miR-654-3p, mapped to the 14q32.31 locus, regulate proliferation, apoptosis, migration and invasion in metastatic prostate cancer cells. Oncogene 2013. doi: 10.1038/onc.2013.451. [Epub ahead of print].
44. MicroRNA-376a sensitizes cells following DNA damage by downregulating MEPE expression. J Sheng, W Luo, F Yu, N Gao, B Hu, Cancer Biother Radiopharm 2013 28 523 529 10.1089/cbr.2012.1446 23570370
45. Prescribing proton pump inhibitors: is it time to pause and rethink? N Vakil, Drugs 2012 72 437 445 10.2165/11599320-000000000-00000 22356286