Proton pump inhibitors as anti vacuolar-ATPases drugs: A novel anticancer strategy

Journal of Experimental and Clinical Cancer Research

Volumn 29, Issue 1, 2010, Pages

  Spugnini, Enrico P ^a   Citro, Gennaro ^a   Fais, Stefano ^b  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CISPLATIN; DOXORUBICIN; FLUOROURACIL; OMEPRAZOLE; PROTON; PROTON PUMP INHIBITOR; ANTINEOPLASTIC AGENT; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACIDIFICATION; ACIDITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER CONTROL; CELL MEMBRANE; CELL PH; CHEMOSENSITIZATION; CUTANEOUS MELANOMA; DRUG EFFICACY; DRUG MECHANISM; DRUG RESISTANCE; GLUCOSE METABOLISM; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MALIGNANT NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL; TUMOR GROWTH; TUMOR INVASION; CANCER INVASION; CYTOPLASM; DISEASE COURSE; DRUG ANTAGONISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; METASTASIS; NEOPLASM;

ANTINEOPLASTIC AGENTS; CYTOPLASM; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; PROTON PUMP INHIBITORS; PROTON PUMPS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 77951951499     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-29-44     Document Type: Review

References (60)

1. Finbow ME, Harrison MA: The vacuolar H+-ATPase: A universal proton pump of eukaryotes. Biochem J 1997, 324:697-712.
2. Forgac M: Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2007, 8:917-929.
3. Cipriano DJ, Wang Y, Bond S, Hinton A, Jefferies KC, Qi J, Forgac M: Structure and regulation of the vacuolar ATPases. Biochim Biophys Acta 2008, 1777:599-604.
4. Jefferies KC, Cipriano DJ, Forgac M: Function, structure and regulation of the vacuolar (H+)-ATPases. Arch Biochem Biophys 2008, 476:33-42.
5. Arai H, Terres G, Pink S, Forgac M: Topography and subunit stoichiometry of the coated vesicle proton pump. J Biol Chem 1988, 263:8796-8802.
6. Xu T, Vasilyeva E, Forgac M: Subunit interactions in the clathrin-coated vesicle vacuolar (H(+))-ATPase complex. J Biol Chem 1999, 274:28909-28915.
7. Ohira M, Smardon AM, Charsky CM, Liu J, Tarsio M, Kane PM: The E and G subunits of the yeastV-ATPase interact tightly and are both present at more than one copy per V1 complex. J Biol Chem 2006, 281:22752-22760.
8. Sautin YY, Lu M, Gaugler A, Zhang L, Gluck SL: Phosphatidylinositol 3- kinase-mediated effects of glucose on vacuolar H+-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol Cell Biol 2005, 25:575-589.
9. Trombetta ES, Ebersold M, Garrett W, Pypaert M, Mellman I: Activation of lysosomal function during dendritic cell maturation. Science 2003, 299:1400-1403.
10. Feng Y, Forgac M: A novel mechanism for regulation of vacuolar acidification. J Biol Chem 1992, 267: 19769-19772.
11. Feng Y, Forgac M: Cysteine 254 of the 73-kDa A subunit is responsible for inhibition of the coated vesicle (H+)-ATPase upon modification by sulfhydryl reagents. J Biol Chem 1992, 267:5817-5822.
12. Feng Y, Forgac M: Inhibition of vacuolar H(+)-ATPase by disulfide bond formation between cysteine 254 and cysteine 532 in subunit A. J Biol Chem 1994, 269:13224-13230.
13. Forgac M: The vacuolar H+-ATPase of clathrin-coated vesicles is reversibly inhibited by Snitrosoglutathione. J Biol Chem 1999, 274:1301-1305.
14. Xu T, Forgac M: Subunit D (Vma8p) of the yeast vacuolar H+-ATPase plays a role in coupling of proton transport and ATP hydrolysis. J Biol Chem 2000, 275:22075-22081.
15. Kawasaki-Nishi S, Bowers K, Nishi T, Forgac M, Stevens TH: The aminoterminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxylterminal domain affects coupling of proton transport and ATP hydrolysis. J Biol 2001, 276: 47411-47420.
16. Saitoh O, Wang WC, Lotan R, Fukuda M: Differential glycosylation and cell surface expression of lysosomal membrane glycoproteins in sublines of a human colon cancer exhibiting distinct metastatic potentials. J Biol Chem 1992, 267:5700-5711.
17. Glunde K, Guggino SE, Solaiyappan M, Pathak AP, Ichikawa Y, Bhujwalla ZM: Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia 2003, 5:533-545.
18. Gatenby RA, Gillies RJ: Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004, 4:891-899.
19. Fais S, De Milito A, You H, Qin W: Targeting vacuolar H+-ATPases as a new strategy against cancer. Cancer Res 2007, 67:10627-10630.
20. Nishi T, Forgac M: The vacuolar (H+)-ATPases nature's most versatile proton pumps. Nat Rev Mol Cell Biol 2002, 3:94-103.
21. Martinez-Zaguilan R, Lynch RM, Martinez GM, Gillies RJ: Vacuolar-type H(+)-ATPases are functionally expressed in plasma membranes of human tumor cells. Am J Physiol 1993, 265:1015-29.
22. Martínez-Zaguilán R, Seftor EA, Seftor RE, Chu YW, Gillies RJ, Hendrix MJ: Acidic pH enhances the invasive behavior of human melanoma cells. Clin Exp Metastasis 1996, 14:176-186.
23. Razaq S, Wilkins RJ, Urban JP: The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus. Eur Spine J 2003, 12:341-319.
24. Webb SD, Sherratt JA, Fish RG: Modelling tumour acidity and invasion. Novartis Found Symp 2001, 240:169-181. discussion 181-185.
25. Koukourakis MI, Giatromanolaki A, Sivridis E, Bougioukas G, Didilis V, Gatter KC, Harris AL, Tumour and Angiogenesis Research Group: Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis. Br J Cancer 2003, 89:877-885.
26. Rofstad EK, Mathiesen B, Kindem K, Galappathi K: Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res 2006, 66:6699-6707.
27. Coussens LM, Fingleton B, Matrisian LM: Matrix metalloproteinase inhibitor and cancer: Trials and tribulations. Science 2002, 295:2387-2392.
28. Lu X, Qin W, Li J, Tan N, Pan D, Zhang H, Xie L, Yao G, Shu H, Yao M, Wan D, Gu J, Yang S: The growth and metastasis of human hepatocellular carcinoma xenografts are inhibited by small interfering RNA targeting to the subunit ATP6L of proton pump. Cancer Res 2005, 65:6843-6849.
29. Sennoune SR, Bakunts K, Martínez GM, Chua-Tuan JL, Kebir Y, Attaya MN, Martínez-Zaguilán R: Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am J PhysiolCell Physiol 2004, 286:1443-1452.
30. Rojas JD, Sennoune SR, Maiti D, Bakunts K, Reuveni M, Sanka SC, Martinez GM, Seftor EA, Meininger CJ, Wu G, Wesson DE, Hendrix MJ, Martínez- Zaguilán R: Vacuolar-type H+-ATPases at the plasma membrane regulate pH and cell migration in microvascular endothelial cells. Am J Physiol Heart Circ Physiol 2006, 291:1147-1157.
31. Hinton A, Sennoune SR, Bond S, Fang M, Reuveni M, Sahagian GG, Jay D, Martinez-Zaguilan R, Forgac M: Function of a subunit isoforms of the VATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. J Biol Chem 2009, 284:16400-16408.
32. Mahoney BP, Raghunand N, Bagget B, Gillies RJ: Tumor acidity, ione trapping and chemotherapeutics I. Acid pH effects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol 2003, 66:1207-1218.
33. Simon S, Roy D, Schindler M: Intracellular pH and the control of multidrug resistance. Proc Nat Acad Sci USA 1993, 91:1128-1132.
34. Raghunand N, Mahoney BP, Gillies RJ: Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol 2003, 66:1219-1229.
35. Martínez-Zaguilán R, Raghunand N, Lynch RM, Bellamy W, Martinez GM, Rojas B, Smith D, Dalton WS, Gillies RJ: pH and drug resistance. I. Functional expression of plasmalemmal V-type H+-ATPase in drugresistant human breast carcinoma cell lines. Biochem Pharmacol 1999, 57:1037-1046.
36. Raghunand N, Martínez-Zaguilán R, Wright SH, Gillies RJ: pH and drug resistance. II. Turnover of acidic vesicles and resistance to weakly basic chemotherapeutic drugs. Biochem Pharmacol 1999, 57: 1047-1058.
37. Bobichon H, Colin M, Depierreux C, Liautaud-Roger F, Jardillier JC: Ultrastructural changes related to multidrug resistance in CEM cells: role of cytoplasmic vesicles in drug exclusion. J Exp Ther Oncol 1996, 1: 49-61.
38. Raghunand N, Altbach MI, van Sluis R, Baggett B, Taylor CW, Bhujwalla ZM, Gillies RJ: Plasmalemmal pH-gradients in drug-sensitive and drugresistant MCF-7 human breast carcinoma xenografts measured by 31P magnetic resonance spectroscopy. Biochem Pharmacol 1999, 57:309-312.
39. Raghunand N: Tissue pH measurement by magnetic resonance spectroscopy and imaging. Methods Mol Med 2006, 124:347-364.
40. Raghunand N, He X, van Sluis R, Mahoney B, Baggett B, Taylor CW, Paine-Murrieta G, Roe D, Bhujwalla ZM, Gillies RJ: Enhancement of chemotherapy by manipulation of tumour pH. Br J Cancer 1999, 80: 1005-1011.
41. You H, Jin J, Shu H, Yu B, De Milito A, Lozupone F, Deng Y, Tang N, Yao G, Fais S, Gu J, Qin W: Small interfering RNA targeting the subunit ATP6L of proton pump V-ATPase overcomes chemoresistance of breast cancer cells. Cancer Lett 2009, 280:110-119.
42. Robey IF, Baggett BK, Kirkpatrick ND, Roe DJ, Dosescu J, Sloane BF, Hashim AI, Morse DL, Raghunand N, Gatenby RA, Gillies RJ: Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res 2009, 69:2260-2268.
43. Raghunand N, Mahoney B, van Sluis R, Baggett B, Gillies RJ: Acute metabolic alkalosis enhances response of C3H mouse mammary tumors to the weak base mitoxantrone. Neoplasia 2001, 3:227-235.
44. Luciani F, Spada M, De Milito A, Molinari A, Rivoltini L, Montinaro A, Marra M, Lugini L, Logozzi M, Lozupone F, Federici C, Iessi E, Parmiani G, Arancia G, Belardelli F, Fais S: Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst 2004, 96: 1702-1713.
45. De Milito A, Canese R, Marino ML, Borghi M, Iero M, Villa A, Venturi G, Lozupone F, Iessi E, Logozzi M, Mina PD, Santinami M, Rodolfo M, Podo F, Rivoltini L, Fais S: pH-dependent antitumor activity of proton pump inhibitors against human melanoma is mediated by inhibition of tumor acidity. Int J Cancer 2009 in press.
46. Murakami T, Shibuya I, Ise T, Chen ZS, Akiyama S, Nakagawa M, Izumi H, Nakamura T, Matsuo K, Yamada Y, Kohno K: Elevated expression of vacuolar proton pump genes and cellular pH in cisplatin resistance. Int J Cancer 2001, 93:869-874.
47. Torigoe T, Izumi H, Ishiguchi H, Uramoto H, Murakami T, Ise T, Yoshida Y, Tanabe M, Nomoto M, Itoh H, Kohno K: Enhanced expression of the human vacuolar H+-ATPase c subunit gene (ATP6L) in response to anticancer agents. J Biol Chem 2002, 277:36534-36543.
48. Torigoe T, Izumi H, Yoshida Y, Ishiguchi H, Okamoto T, Itoh H, Kohno K: Low pH enhances Sp1 DNA binding activity and interaction with TBP. Nucleic Acids Res 2003, 31:4523-4530.
49. Thamm DH, Vail DM: Mast cell tumors. In Small Animal Clinical Oncology 4th edition. Edited by: Withrow SJ, MacEwen EG. Philadelphia, PA: WB Saunders Co; 2007:402-424.
50. De Milito A, Iessi E, Logozzi M, Lozupone F, Spada M, Marino ML, Federici C, Perdicchio M, Matarrese P, Lugini L, Nilsson A, Fais S: Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspaseindependent mechanism involving reactive oxygen species. ncer Res 2007, 67: 5408-5417.
51. Cardone RA, Casavola V, Reshkin SJ: The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat Rev Cancer 2005, 5:786-795.
52. Semenza GL: Tumor metabolism: cancer cells give and take lactate. J Clin Invest 2008, 118:3835-3837.
53. Robertson N, Potter C, Harris AL: Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res 2004, 64:6160-6165.
54. Shimokawa O, Matsui H, Nagano Y, Kaneko T, Shibahara T, Nakahara A, Hyodo I, Yanaka A, Majima HJ, Nakamura Y, Matsuzaki Y: Neoplastic transformation and induction of H+, K+ -adenosine triphosphatase by N-methyl-N'-nitro-N-nitrosoguanidine in the gastric epithelial RGM-1 cell line. In Vitro Cell Dev Biol Anim 2008, 44: 26-30.
55. Gervasoni JE Jr, Fields SZ, Krishna S, Baker MA, Rosado M, Thuraisamy K, Hindenburg AA, Taub RN: Subcellular distribution of daunorubicin in Pglycoprotein- positive and -negative drug-resistant cell lines using laser-assisted confocal microscopy. Cancer Res 1991, 51:4955-4963.
56. Klohs WD, Steinkampf RW: The effect of lysosomotropic agents and secretory inhibitors on anthracycline retention and activity in multiple drug-resistant cells. Mol Pharmacol 1988, 34:180-185.
57. Simon SM, Schindler M: Cell biological mechanisms of multidrug resistance in tumors. Proc Natl Acad Sci USA 1994, 91:3497-3504.
58. Fletcher JI, Haber M, Henderson MJ, Norris MD: ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 2010, 10:147-156.
59. Mullin JM, Gabello M, Murray LJ, Farrell CP, Bellows J, Wolov KR, Kearney KR, Rudolph D, Thornton JJ: Proton pump inhibitors: Actions and reactions. Drug Discov Today 2009, 14:647-60.
60. Lugini L, Matarrese P, Tinari A, Lozupone F, Federici C, Iessi E, Gentile M, Luciani F, Parmiani G, Rivoltini L, Malorni W, Fais S: Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res 2006, 66:3629-38.