Proton pump inhibitors for the treatment of cancer in companion animals

Journal of Experimental and Clinical Cancer Research

Volumn 34, Issue 1, 2015, Pages

  Walsh, Megan ^a   Fais, Stefano ^b   Spugnini, Enrico Pierluigi ^c   Harguindey, Salvador ^d   Abu Izneid, Tareq ^e   Scacco, Licia ^d   Williams, Paula ^a   Allegrucci, Cinzia ^a   Rauch, Cyril ^a   Omran, Ziad ^e  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d Institute for Clinical Biology and Metabolism ^*  (Italy)

^e UMM AL QURA UNIVERSITY   (Saudi Arabia)

Author keywords

Cancer; Chemoresistance; Metastasis; pH; Proton pump inhibitors

Indexed keywords

AMILORIDE; BAFILOMYCIN; BICARBONATE; CISPLATIN; CYCLOPHOSPHAMIDE; DOXORUBICIN; ESOMEPRAZOLE; LANSOPRAZOLE; OMEPRAZOLE; PANTOPRAZOLE; PIROXICAM; PROTON PUMP INHIBITOR; RABEPRAZOLE; ANTINEOPLASTIC AGENT;

ACIDITY; ANIMAL DISEASE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER THERAPY; CELL KILLING; CLINICAL PROTOCOL; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; EXTRACELLULAR SPACE; GASTROESOPHAGEAL REFLUX; HEARTBURN; HUMAN; LUNG CARCINOMA; MELANOMA; METASTASIS; NEOPLASM; NONHUMAN; OSTEOSARCOMA; OUTCOME ASSESSMENT; PET ANIMAL; PH; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; SIDE EFFECT; TUMOR CELL; TUMOR MICROENVIRONMENT; VETERINARY MEDICINE; ANIMAL; DOG; DOG DISEASES; DRUG RESISTANCE; HORSE; HORSE DISEASES; NEOPLASMS; PATHOLOGY; VETERINARY;

ANIMALS; ANTINEOPLASTIC AGENTS; DOG DISEASES; DOGS; DRUG RESISTANCE, NEOPLASM; HORSE DISEASES; HORSES; HUMANS; HYDROGEN-ION CONCENTRATION; NEOPLASMS; PETS; PROTON PUMP INHIBITORS;

EID: 84940749834     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/s13046-015-0204-z     Document Type: Review

References (54)

1. De Milito A, Fais S. Tumor acidity, chemoresistance and proton pump inhibitors. Future Oncol. 2005;1(6):779-86.
2. Howlader N NA, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z,Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (2013) http://seer.cancer.gov/csr/1975-2012/.
3. Martinez-Zaguilan R, Raghunand N, Lynch RM, Bellamy W, Martinez GM, Rojas B, et al. pH and drug resistance. I. Functional expression of plasmalemmal V-type H + -ATPase in drug-resistant human breast carcinoma cell lines. Biochem Pharmacol. 1999;57(9):1037-46.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74.
5. De Milito A, Marino ML, Fais S. A rationale for the use of proton pump inhibitors as antineoplastic agents. Curr Pharm Des. 2012;18(10):1395-406.
6. Merida I, Avila-Flores A. Tumor metabolism: new opportunities for cancer therapy. Clin Transl Oncol. 2006;8(10):711-6.
7. Xu RH, Pelicano H, Zhou Y, Carew JS, Feng L, Bhalla KN, et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res. 2005;65(2):613-21.
8. Warburg O. On the origin of cancer cells. Science. 1956;123(3191):309-14.
9. Mahon BP, Pinard MA, McKenna R. Targeting carbonic anhydrase IX activity and expression. Molecules. 2015;20(2):2323-48.
10. Kennedy KM, Dewhirst MW. Tumor metabolism of lactate: the influence and therapeutic potential for MCT and CD147 regulation. Future Oncol. 2010;6(1):127-35.
11. Demaurex N. pH Homeostasis of Cellular Organelles. 2002.
12. Alexander SP, Mathie A, Peters JA. Guide to Receptors and Channels (GRAC), 5th edition. Br J Pharmacol. 2011;164 Suppl 1:S1-324.
13. Nakamura S. Handbook of H + -ATPases. 2014. Pan Stanford. CRC Press, Taylor & Francis Group, UK
14. Slepkov ER, Rainey JK, Sykes BD, Fliegel L. Structural and functional analysis of the Na+/H+ exchanger. Biochem J. 2007;401(3):623-33.
15. Ferrari S, Perut F, Fagioli F, Brach Del Prever A, Meazza C, Parafioriti A, et al. Proton pump inhibitor chemosensitization in human osteosarcoma: from the bench to the patients' bed. J Transl Med. 2013;11:268.
16. Iessi EMM, Lozupone F, Fais S. De Milito A Tumor acidity and malignancy: novel aspects in the design of anti-tumor therapy. Cancer Therapy. 2008;6:55-66.
17. Rauch C. Toward a mechanical control of drug delivery. On the relationship between Lipinski's 2nd rule and cytosolic pH changes in doxorubicin resistance levels in cancer cells: a comparison to published data. Eur Biophys J. 2009;38(7):829-46.
18. Panagiotopoulou V, Richardson G, Jensen OE, Rauch C. On a biophysical and mathematical model of Pgp-mediated multidrug resistance: understanding the "space-time" dimension of MDR. Eur Biophys J. 2010;39(2):201-11.
19. Daniel C, Bell C, Burton C, Harguindey S, Reshkin SJ, Rauch C. The role of proton dynamics in the development and maintenance of multidrug resistance in cancer. Biochim Biophys Acta. 2013;1832(5):606-17.
20. Calcinotto A, Filipazzi P, Grioni M, Iero M, De Milito A, Ricupito A, et al. Modulation of microenvironment acidity reverses anergy in human and murine tumor-infiltrating T lymphocytes. Cancer Res. 2012;72(11):2746-56.
21. Harguindey S, Orive G, Luis Pedraz J, Paradiso A, Reshkin SJ. The role of pH dynamics and the Na+/H+ antiporter in the etiopathogenesis and treatment of cancer. Two faces of the same coin - one single nature. Biochim Biophys Acta. 2005;1756(1):1-24.
22. Sennoune SR, Bakunts K, Martinez GM, Chua-Tuan JL, Kebir Y, Attaya MN, et al. Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am J Physiol Cell Physiol. 2004;286(6):C1443-52.
23. Fais S. Proton pump inhibitor-induced tumour cell death by inhibition of a detoxification mechanism. J Intern Med. 2010;267(5):515-25.
24. Luciani F, Spada M, De Milito A, Molinari A, Rivoltini L, Montinaro A, et al. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst. 2004;96(22):1702-13.
25. Harguindey S, Arranz JL, Polo Orozco JD, Rauch C, Fais S, Cardone RA, et al. Cariporide and other new and powerful NHE1 inhibitors as potentially selective anticancer drugs - an integral molecular/biochemical/metabolic/clinical approach after one hundred years of cancer research. J Transl Med. 2013;11:282.
26. Harguindey S, Arranz JL, Wahl ML, Orive G, Reshkin SJ. Proton transport inhibitors as potentially selective anticancer drugs. Anticancer Res. 2009;29(6):2127-36.
27. Nakashima S, Hiraku Y, Tada-Oikawa S, Hishita T, Gabazza EC, Tamaki S, et al. Vacuolar H+-ATPase inhibitor induces apoptosis via lysosomal dysfunction in the human gastric cancer cell line MKN-1. J Biochem. 2003;134(3):359-64.
28. McCarty MF, Whitaker J. Manipulating tumor acidification as a cancer treatment strategy. Altern Med Rev. 2010;15(3):264-72.
29. Matthews H, Ranson M, Kelso MJ. Anti-tumour/metastasis effects of the potassium-sparing diuretic amiloride: an orally active anti-cancer drug waiting for its call-of-duty? Int J Cancer. 2011;129(9):2051-61.
30. Mattsson JP, Vaananen K, Wallmark B, Lorentzon P. Omeprazole and bafilomycin, two proton pump inhibitors: differentiation of their effects on gastric, kidney and bone H(+)-translocating ATPases. Biochim Biophys Acta. 1991;1065(2):261-8.
31. Moriyama Y, Patel V, Ueda I, Futai M. Evidence for a common binding site for omeprazole and N-ethylmaleimide in subunit A of chromaffin granule vacuolar-type H(+)-ATPase. Biochem Biophys Res Commun. 1993;196(2):699-706.
32. Parks SK, Chiche J, Pouyssegur J. Disrupting proton dynamics and energy metabolism for cancer therapy. Nat Rev Cancer. 2013;13(9):611-23.
33. De Milito A, Iessi E, Logozzi M, Lozupone F, Spada M, Marino ML, et al. Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspase-independent mechanism involving reactive oxygen species. Cancer Res. 2007;67(11):5408-17.
34. Thomson AB, Sauve MD, Kassam N, Kamitakahara H. Safety of the long-term use of proton pump inhibitors. World J Gastroenterol. 2010;16(19):2323-30.
35. Shin JM, Sachs G. Pharmacology of proton pump inhibitors. Curr Gastroenterol Rep. 2008;10(6):528-34.
36. Wallmark B, Brandstrom A, Larsson H. Evidence for acid-induced transformation of omeprazole into an active inhibitor of (H+ + K+)-ATPase within the parietal cell. Biochim Biophys Acta. 1984;778(3):549-58.
37. Shin JM, Cho YM, Sachs G. Chemistry of covalent inhibition of the gastric (H+, K+)-ATPase by proton pump inhibitors. J Am Chem Soc. 2004;126(25):7800-11.
38. Shin JM, Kim N. Pharmacokinetics and pharmacodynamics of the proton pump inhibitors. J Neurogastroenterol Motil. 2013;19(1):25-35.
39. Marino ML, Fais S, Djavaheri-Mergny M, Villa A, Meschini S, Lozupone F, et al. Proton pump inhibition induces autophagy as a survival mechanism following oxidative stress in human melanoma cells. Cell Death Dis. 2010;1:e87.
40. Udelnow A, Kreyes A, Ellinger S, Landfester K, Walther P, Klapperstueck T, et al. Omeprazole inhibits proliferation and modulates autophagy in pancreatic cancer cells. PLoS One. 2011;6(5):e20143.
41. Wojtkowiak JW, Rothberg JM, Kumar V, Schramm KJ, Haller E, Proemsey JB, et al. Chronic autophagy is a cellular adaptation to tumor acidic pH microenvironments. Cancer Res. 2012;72(16):3938-47.
42. Roepe PD. pH and multidrug resistance. Novartis Found Symp. 2001;240:232-47. discussion 47-50, 65-8.
43. Robey IF, Baggett BK, Kirkpatrick ND, Roe DJ, Dosescu J, Sloane BF, et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res. 2009;69(6):2260-8.
44. Spugnini EP, Baldi A, Buglioni S, Carocci F, de Bazzichini GM, Betti G, et al. Lansoprazole as a rescue agent in chemoresistant tumors: a phase I/II study in companion animals with spontaneously occurring tumors. J Transl Med. 2011;9:221.
45. Spugnini EP, Buglioni S, Carocci F, Francesco M, Vincenzi B, Fanciulli M, et al. High dose lansoprazole combined with metronomic chemotherapy: a phase I/II study in companion animals with spontaneously occurring tumors. J Transl Med. 2014;12:225.
46. Veterinary cooperative oncology group - common terminology criteria for adverse events (VCOG-CTCAE) following chemotherapy or biological antineoplastic therapy in dogs and cats v1.1. Vet Comp Oncol. 2011. doi: 10.1111/j.1476-5829.2011.00283.x
47. Spugnini EP, Citro G, Fais S. Proton pump inhibitors as anti vacuolar-ATPases drugs: a novel anticancer strategy. J Exp Clin Cancer Res. 2010;29:44.
48. Wen-L Z, Jian W, Yan-Fang T, Xing F, Yan-Hong L, Xue-Ming Z, et al. Inhibition of the ecto-beta subunit of F1F0-ATPase inhibits proliferation and induces apoptosis in acute myeloid leukemia cell lines. J Exp Clin Cancer Res. 2012;31:92.
49. Linder K, Borchard C, Schopp M, Burger A, Stock C, Hussey DJ, et al. Proton pump inhibitors (PPIs) impact on tumour cell survival, metastatic potential and chemotherapy resistance, and affect expression of resistance-relevant miRNAs in esophageal cancer. J Exp Clin Cancer Res. 2014;33:73.
50. Hornick JR JR, Suwanna Vangveravong S, Spitzer D, Abate C, Berardi F, Goedegebuure P, et al. Lysosomal Membrane Permeabilization is an Early Event in Sigma-2 Receptor Ligand Mediated Cell Death in Pancreatic Cancer. J Exp Clin Cancer Res. 2012;31:41.
51. Malm SW, Hanke NT, Alexander G, Liliana C, Baker AF. The anti-tumor efficacy of 2-deoxyglucose and D-allose are enhanced with p38 inhibition in pancreatic and ovarian cell lines. J Exp Clin Cancer Res. 2015;34:31.
52. Tu H, Nengbin H, Yunsong Y, Chengqian Y, Nianli S, Qingcheng Y. DEC2 expression is positively correlated with HIF-1 activation and the invasiveness of human osteosarcomas. J Exp Clin Cancer Res. 2015;34:22.
53. Han S, Stephanie D, Dilda PJ, Eric H, Chung SA, Luk PP, et al. Dual-targeting of aberrant glucose metabolism in glioblastoma. J Exp Clin Cancer Res. 2015;34:14.
54. Qin Q, Wei F, Li B. Multiple functions of hypoxia-regulated miR-210 in cancer. J Exp Clin Cancer Res. 2014;33:50.