Intracellular proton pumps as targets in chemotherapy: V-ATPases and cancer

Current Pharmaceutical Design

Volumn 18, Issue 10, 2012, Pages 1383-1394

  Hernández, Agustín ^a   Serrano Bueno, Gloria ^a   Pérez Castiñeira, José R ^a   Serrano, Aurelio ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Acidification; Apoptosis; Bafilomycin; Concanamycin; Proton gradients; Salicylihalamide; Traffic; V atpase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADOCIASULFATE 1; AMIDE; APICULAREN A; ARCHAZOLID A; BAFILOMYCIN A1; CHEMICAL COMPOUND; CONCANAMYCIN A; FUSIDIC ACID; INDOLE DERIVATIVE; LANSOPRAZOLE; LOBATAMIDE A; NIK 12192; OMEPRAZOLE; PROTON PUMP; SALICYLIHALIMIDE A; SB 242784; UNCLASSIFIED DRUG; VACUOLAR TYPE ADENOSINE TRIPHOSPHATASE;

ACIDIFICATION; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CHEMOTHERAPY; CARBOHYDRATE METABOLISM; CELL CYCLE ARREST; CELL DEATH; CHEMICAL STRUCTURE; CYTOLOGY; DRUG DISTRIBUTION; DRUG TARGETING; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME STRUCTURE; GENE EXPRESSION REGULATION; GLUCONEOGENESIS; HUMAN; NEOPLASM; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN HYDROLYSIS;

EID: 84857694659     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161212799504821     Document Type: Article

References (172)

1. Lagadic-Gossmann D, Huc L, Lecureur V. Alterations of intracel- lular pH homeostasis in apoptosis: origins and roles. Cell Death Differ 2004; 11(9): 953-61.
2. Ferreira LMR. Cancer metabolism: the Warburg effect today. Exp Mol Pathol 2010; 89(3): 372-80.
3. Joyce JA, Hanahan D. Multiple roles for cysteine cathepsins in cancer. Cell Cycle 2004; 3(12): 1516-9.
4. Mason SD, Joyce JA. Proteolytic networks in cancer. Trends Cell Biol 2011; 21 (4): 228-37.
5. Docampo R, Moreno SNJ. The acidocalcisome as a target for che-motherapeutic agents in protozoan parasites. Curr Pharm Des 2008; 14(9): 882-8.
6. McIntosh MT, Drozdowicz YM, Laroiya K, Rea PA, Vaidya AB. Two classes of plant-like vacuolar-type H(+)-pyrophosphatases in malaria parasites. Mol Biochem Parasitol 2001; 114(2): 183-95.
7. Brown D, Breton S. H(+)V-ATPase-dependent luminal acidifica-tion in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways. J Exp Biol 2000; 203(1): 137-45.
8. Kaunitz JD, Yamaguchi DT. TNAP, TrAP, ecto-purinergic signal-ing, and bone remodeling. J Cell Biochem 2008; 105(3): 655-62.
9. +-ATPase Promotes Distant Metastasis in the Mouse B16 Melanoma Cells. Mol Cancer Res 2011; 9(7): 845-55.
10. +-ATPase in cancer biology. Cell Biochem Biophys 2004; 40(2): 185-206.
11. +- ATPases in angiogenesis, diabetes and cancer. J Bioenerg Biomembr 2007; 39(5-6): 427-33.
12. Hinton A, Sennoune SR, Bond S, et al. Function of a subunit iso-forms of the V-ATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. J Biol Chem 2009; 284(24): 16400-8.
13. Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 2006; 6(10): 764-75.
14. Ungermann C, Wickner W, Xu Z. Vacuole acidification is required for trans-SNARE pairing, LMA1 release, and homotypic fusion. Proc Natl Acad Sci U S A 1999; 96(20): 11194-9.
15. Axelsson MA, Karlsson NG, Steel DM, Ouwendijk J, Nilsson T, Hansson GC. Neutralization of pH in the Golgi apparatus causes redistribution of glycosyltransferases and changes in the O-glycosylation of mucins. Glycobiology 2001; 11(8): 633-44.
16. Rivinoja A, Hassinen A, Kokkonen N, Kauppila A, Kellokumpu S. Elevated Golgi pH impairs terminal N-glycosylation by inducing mislocalization of Golgi glycosyltransferases. J Cell Physiol 2009; 220(1): 144-54.
17. Contreres JO, Faure R, Baquiran G, Bergeron JJ, Posner BI. ATP-dependent desensitization of insulin binding and tyrosine kinase activity of the insulin receptor kinase. The role of endosomal acidification. J Biol Chem 1998; 273(34): 22007-13.
18. Authier F, Metioui M, Fabrega S, Kouach M, Briand G. Endosomal proteolysis of internalized insulin at the C-terminal region of the B chain by cathepsin D. J Biol Chem 2002; 277(11): 9437-46.
19. van Weert AW, Dunn KW, Gueze HJ, Maxfield FR, Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 1995; 130(4): 821-34.
20. Duvvuri M, Konkar S, Hong KH, Blagg BSJ, Krise JP. A new approach for enhancing differential selectivity of drugs to cancer cells. ACS Chem Biol 2006; 1(5): 309-15.
21. Paroutis P, Touret N, Grinstein S. The pH of the secretory pathway: measurement, determinants, and regulation. Physiology 2004; 19: 207-15.
22. Weisz OA. Acidification and protein traffic. Int Rev Cytol 2003; 226: 259-319.
23. +-translocating adenosine triphosphatase in vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 1981; 256(21): 10859-63.
24. + ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol 2006; 209(Pt 4): 577-89.
25. Grüber G, Marshansky V. New insights into structure-function relationships between archeal ATP synthase (A1A0) and vacuolar type ATPase (V1V0). BioEssays 2008; 30(11-12): 1096-109.
26. Smardon AM, Tarsio M, Kane PM. The RAVE complex is essential for stable assembly of the yeast V-ATPase. J Biol Chem 2002; 277(16): 13831-9.
27. Muench SP, Trinick J, Harrison MA. Structural divergence of the rotary ATPases. Q Rev Biophys 2011; 44(3): 311-56.
28. +-ATPases and microfilaments in osteoclasts. J Bioenerg Biomembr 2005; 37(6): 419-23.
29. +-ATPase contains a filamentous actin binding site. J Biol Chem 2000; 275(41): 32331-7.
30. Nakanishi-Matsui M, Sekiya M, Nakamoto RK, Futai M. The mechanism of rotating proton pumping ATPases. Biochim Biophys Acta 2010; 1797(8): 1343-52.
31. Perzov N, Padler-Karavani V, Nelson H, Nelson N. Characterization of yeast V-ATPase mutants lacking Vph1p or Stv1p and the effect on endocytosis. J Exp Biol 2002; 205(9): 1209-19.
32. +-ATPase. J Biol Chem 1999; 274(24): 17275-83.
33. Ochotny N, Van Vliet A, Chan N, et al. Effects of human a3 and a4 mutations that result in osteopetrosis and distal renal tubular acido-sis on yeast V-ATPase expression and activity. J Biol Chem 2006; 281(36): 26102-11.
34. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2007; 8(11): 917-29.
35. Puopolo K, Forgac M. Functional reassembly of the coated vesicle proton pump. J Biol Chem 1990; 265(25): 14836-41.
36. +)-ATPase. J Biol Chem 1992; 267(14): 9773-8.
37. +-ATPase. J Bioenerg Biomembr 2003; 35(4): 313-21.
38. [S. Glucose activates H(+)-ATPase in kidney epithelial cells. Am J Physiol Cell Physiol 2004; 287(1): C97-105-C97-105.
39. +-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol Cell Biol 2005; 25(2): 575-89.
40. Kuzinski J, Zitnan R, Warnke-Gurgel C, Schweigel M. The vacuo-lar-type H-ATPase in ovine rumen epithelium is regulated by metabolic signals. J Biomed Biotechnol 2010; 2010: 525034-4.
41. +-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J Biol Chem 2001; 276(32): 30407-13.
42. +-ATPase is essential for the assembly and activity of the proton pump. J Biol Chem 2007; 282(34): 24495-503.
43. Toei M, Saum R, Forgac M. Regulation and isoform function of the V-ATPases. Biochemistry 2010; 49(23): 4715-23.
44. +)-ATPase in yeast. J Biol Chem 2008; 283(52): 36513-21.
45. Perez-Sayans M, Garcia-Garcia A, Reboiras-Lopez MD, Gandara-Vila P. Role of V-ATPases in solid tumors: importance of the subunit C. Int J Oncol 2009; 34(6): 1513-20.
46. Voss M, Fechner L, Walz B, Baumann O. Calcineurin activity augments cAMP/PKA-dependent activation of V-ATPase in blowfly salivary glands. Am J Physiol Cell Physiol 2010; 298(5): C1047-56.
47. +)-ATPase by protein kinase A. J Biol Chem 2007; 282(46): 33735-42.
48. +-ATPase localization and activity via direct phosphorylation of the a subunit in kidney cells. J Biol Chem 2010; 285(32): 24676-85.
49. Dechant R, Binda M, Lee SS, Pelet S, Winderickx J, Peter M. Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J 2010; 29(15): 2515-26.
50. Brown D, Paunescu TG, Breton S, Marshansky V. Regulation of the V-ATPase in kidney epithelial cells: dual role in acid-base ho-meostasis and vesicle trafficking. J Exp Biol 2009; 212(11): 1762-72.
51. Dechant R, Peter M. The N-terminal domain of the V-ATPase subunit 'a' is regulated by pH in vitro and in vivo. Channels 2011; 5(1): 4-8.
52. Marshansky V. The V-ATPase a2-subunit as a putative endosomal pH-sensor. Biochem Soc Trans 2007; 35(5): 1092-9.
53. Diakov TT, Kane PM. Regulation of vacuolar proton-translocating ATPase activity and assembly by extracellular pH. J Biol Chem 2010; 285(31): 23771-8.
54. +-ATPase apical accumulation in kidney intercalated cells is regulated by PKA and AMP-activated protein kinase. Am J Physiol Renal Physiol 2010; 298(5): F1162-9.
55. +-ATPase accumulation in epididymal clear cells. Am J Physiol Cell Physiol 2009; 296(4): C672-81.
56. Marjuki H, Gornitzky A, Marathe BM, et al. Influenza A virus-induced early activation of ERK and PI3K mediates V-ATPase-dependent intracellular pH change required for fusion. Cell Micro-biol 2011; 13(4): 587-601.
57. +)-ATPase by angiotensin II in proximal tubule cells. Eur J Physiol 2009; 458(5): 969-79.
58. +-ATPase function and sorbic acid stress tolerance. Microbiology 2007; 153(12): 4016-26.
59. Merzendorfer H, Gräf R, Huss M, Harvey WR, Wieczorek H. Regulation of proton-translocating V-ATPases. J Exp Biol 1997; 200(Pt 2): 225-35.
60. Perez-Sayans M, Reboiras-Lopez MD, Somoza-Martin JM, et al. Measurement of ATP6V1C1 expression in brush cytology samples as a diagnostic and prognostic marker in oral squamous cell carcinoma. Cancer Biol Therap 2010; 9(12): 1057-64.
61. Otero-Rey EM, Somoza-Martin M, Barros-Angueira F, Garcia-Garcia A. Intracellular pH regulation in oral squamous cell carcinoma is mediated by increased V-ATPase activity via over-expression of the ATP6V1C1 gene. Oral Oncol 2008; 44(2): 193-9.
62. +-ATPase c subunit gene (ATP6L) in response to anticancer agents. J Biol Chem 2002; 277(39): 36534-43.
63. Peña-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, et al. Regulation of TFEB and V-ATPases by mTORC1. EMBO J 2011; 30(16): 3242-58.
64. Kawasaki-Nishi S, Bowers K, Nishi T, Forgac M, Stevens TH. The amino-terminal domain of the vacuolar proton-translocating AT-Pase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J Biol Chem 2001; 276(50): 47411-20.
65. Nyman JK, Vaananen HK. A rationale for osteoclast selectivity of inhibiting the lysosomal V-ATPase a3 isoform. Calcif Tissue Int 2010; 87(3): 273-83.
66. Kawasaki-Nishi S, Nishi T, Forgac M. Yeast V-ATPase complexes containing different isoforms of the 100-kDa a-subunit differ in coupling efficiency and in vivo dissociation. J Biol Chem 2001; 276(21): 17941-8.
67. Muller ML, Taiz L. Regulation of the lemon-fruit V-ATPase by variable stoichiometry and organic acids. J Membr Biol 2002; 185(3): 209-20.
68. Feng Y, Forgac M. A novel mechanism for regulation of vacuolar acidification. J Biol Chem 1992; 267(28): 19769-72.
69. +-ATPase by oxidation and reduction in vivo. J Biol Chem 1997; 272(44): 28149-57.
70. Breton S, Brown D. New insights into the regulation of V-ATPase-dependent proton secretion. Am J Physiol Renal Physiol 2007; 292(1): F1-10.
71. Pastor-Soler NM, Hallows KR, Smolak C, Gong F, Brown D, Breton S. Alkaline pH- and cAMP-induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. Am J Physiol Cell Physiol 2008; 294(2): C488-94.
72. Muller O, Neumann H, Bayer MJ, Mayer A. Role of the Vtc proteins in V-ATPase stability and membrane trafficking. J Cell Sci 2003; 116(6): 1107-15.
73. Vlotides G, Eigler T, Melmed S. Pituitary tumor-transforming gene: physiology and implications for tumorigenesis. Endocr Rev 2007; 28(2): 165-86.
74. Minematsu T, Egashira N, Kajiya H, et al. PTTG is a secretory protein in human pituitary adenomas and in mouse pituitary tumor cell lines. Endocr Pathol 2007; 18(1): 8-15.
75. Bacac M, Fusco C, Planche A, et al. Securin and separase modulate membrane traffic by affecting endosomal acidification. Traffic 2011; 12(5): 615-26.
76. +)-translocating ATPase. Effect of divalent cations, phospholipids, and subunit H (SFD). J Biol Chem 2003; 278(45): 44281-8.
77. Grasso EJ, Scalambro MB, Calderon RO. Differential Response of the Urothelial V-ATPase Activity to the Lipid Environment. Cell Biochem Biophys 2011; 61(1): 157-68.
78. van Meer G, Voelker DR, Feigenson GW. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 2008; 9(2): 112-24.
79. +)-ATPase of adrenal secretory granules. Rapid partial purification and reconstitution into proteoliposomes. Biochem J 1990; 271(1): 127-31.
80. Zhang YQ, Rao R. Beyond ergosterol: linking pH to antifungal mechanisms. Virulence 2010; 1(6): 551-4.
81. [Zhang YQ, Gamarra S, Garcia-Effron G, Park S, Perlin DS, Rao R. Requirement for ergosterol in V-ATPase function underlies anti-fungal activity of azole drugs. PLoS Pathog 2010; 6(6): e1000939.
82. Chung J-H, Lester RL, Dickson RC. Sphingolipid requirement for generation of a functional v1 component of the vacuolar ATPase. J Biol Chem 2003; 278(31): 28872-81.
83. Finnigan GC, Ryan M, Stevens TH. A genome-wide enhancer screen implicates sphingolipid composition in vacuolar ATPase function in Saccharomyces cerevisiae. Genetics 2011; 187(3): 771-83.
84. van der Poel S, Wolthoorn J, van den Heuvel D, et al. Hyper-acidification of trans Golgi network and endo/lysosomes in mela-nocytes by glucosylceramide-dependent V-ATPase activity. Traffic 2011; 12(11): 1634-47.
85. Lafourcade C, Sobo K, Kieffer-Jaquinod S, Garin J, van der Goot FG. Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS ONE 2008; 3(7): e2758.
86. van Poelje PD, Potter SC, Erion MD. In Diabetes-Perspectives in Drug Therapy. Handb Exp Pharmacol, Mathias Schwanstecher, ed.; Springer: Heidelberg, 2011, pp. 279-301.
87. Liu J, Brown CR, Chiang H-L. Degradation of the gluconeogenic enzyme fructose-1, 6-bisphosphatase is dependent on the vacuolar ATPase. Autophagy 2005; 1(3): 146-56.
88. Martinez-Muñoz GA, Kane P. Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J Biol Chem 2008; 283(29): 20309-19.
89. +-ATPase null mutants. J Biol Chem 2000; 275(51): 40088-95.
90. Tarsio M, Zheng H, Smardon AM, Martinez-Muñoz GA, Kane PM. Consequences of Loss of Vph1 Protein-containing Vacuolar ATPases (V-ATPases) for Overall Cellular pH Homeostasis. J Biol Chem 2011; 286(32): 28089-96.
91. +-ATPase-mediated acidification in sorting and release of the regulated secretory protein chromogranin A: evidence for a vesiculogenic function. J Biol Chem 2005; 280(5): 3885-97.
92. Eng CH, Abraham RT. The autophagy conundrum in cancer: influence of tumorigenic metabolic reprogramming. Oncogene 2011; 24(30): 4687-96.
93. [Pavlides S, Vera I, Gandara R, et al. Warburg Meets Autophagy: Cancer Associated Fibroblasts Accelerate Tumor Growth and Metastasis Via Oxidative Stress, Mitophagy and Aerobic Glycolysis. Antioxid Redox Signal 2011; In Press (doi:10.1089/ars.2011.4243).
94. Eskelinen E-L. The dual role of autophagy in cancer. Curr Opin Pharmacol 2011; 11(4): 294-300.
95. Nakamura N, Matsuura A, Wada Y, Ohsumi Y. Acidification of vacuoles is required for autophagic degradation in the yeast, Sac-charomyces cerevisiae. J Biochem 1997; 121(2): 338-44.
96. Mijaljica D, Prescott M, Devenish RJ. V-ATPase engagement in autophagic processes. Autophagy 2011; 7(6): 666-8.
97. Mehrpour M, Esclatine A, Beau I, Codogno P. Overview of mac-roautophagy regulation in mammalian cells. Cell Res 2010; 20(7): 748-62.
98. Platini F, Perez-Tomas R, Ambrosio S, Tessitore L. Understanding autophagy in cell death control. Curr Pharm Des 2010; 16(1): 101-13.
99. Mei S, Ni H-M, Manley S, et al. Differential Roles of Unsaturated and Saturated Fatty Acids on Autophagy and Apoptosis in Hepato-cytes. J Pharmacol Exp Ther 2011; 339(2): 487-97.
100. Mohan N, Banik NL, Ray SK. Combination of N-(4-hydroxyphenyl) retinamide and apigenin suppressed starvation-induced autophagy and promoted apoptosis in malignant neuroblas-toma cells. Neurosci Lett 2011; 502(1): 24-9.
101. Nakamura O, Hitora T, Akisue T, Kawamoto T, Yamagami Y, Yamamoto T. Inhibition of induced autophagy increases apoptosis of Nara-H cells. Intl J Oncol 2011; 39(6): 1545-52.
102. Ng S, Wu YT, Chen B, Zhou J, Shen HM. Impaired autophagy due to constitutive mTOR activation sensitizes TSC2-null cells to cell death under stress. Autophagy 2011; 7(10): 1173-86.
103. Noman MZ, Janji B, Kaminska B, et al. Blocking hypoxia-induced autophagy in tumors restores cytotoxic T cell activity and promotes regression. Cancer Res 2011; 71(18): 5976-86.
104. [Shimizu S, Takehara T, Hikita H, et al. Inhibition of autophagy potentiates the antitumor effect of the multikinase inhibitor soraf-enib in hepatocellular carcinoma. Intl J Cancer 2011; In Press (doi: 10.1002/ijc.26374).
105. Wu YC, Wu WKK, Li Y, et al. Inhibition of macroautophagy by bafilomycin A1 lowers proliferation and induces apoptosis in colon cancer cells. Biochem Biophys Res Commun 2009; 382(2): 451-6.
106. Shacka JJ, Klocke BJ, Roth KA. Autophagy, bafilomycin and cell death: the a-B-cs of plecomacrolide-induced neuroprotection. Autophagy 2006; 2(3): 228-30.
107. Chen VY, Rosania GR. The Great Multidrug-Resistance Paradox. ACS Chem Biol 2006; 1(5): 271-3.
108. Millot C, Millot JM, Morjani H, Desplaces A, Manfait M. Characterization of Acidic Vesicles in Multidrug-resistant and Sensitive Cancer Cells by Acridine Orange Staining and Confocal Mi-crospectrofluorometry. J Histochem Cytochem 1997; 45(9): 1255-64.
109. Altan N, Chen Y, Schindler M, Simon SM. Defective acidification in human breast tumor cells and implications for chemotherapy. J Exp Med 1998; 187(10): 1583-98.
110. Murakami T, Shibuya I, Ise T, et al. Elevated expression of vacuo-lar proton pump genes and cellular pH in cisplatin resistance. Int J Cancer 2001; 93(6): 869-74.
111. +-ATPase inhibitors overcome Bcl-xL-mediated chemoresistance through restoration of a caspase-independent apoptotic pathway. Cancer Sci 2009; 100(8): 1460-7.
112. Weylandt KH, Nebrig M, Jansen-Rosseck N, et al. ClC-3 expression enhances etoposide resistance by increasing acidification of the late endocytic compartment. Mol Cancer Ther 2007; 6(3): 979-86.
113. Straud S, Zubovych I, De Brabander JK, Roth MG. Inhibition of iron uptake is responsible for differential sensitivity to V-ATPase inhibitors in several cancer cell lines. PLoS ONE 2010; 5(7): e11629.
114. Myant K, Sansom OJ. Wnt/Myc interactions in intestinal cancer: Partners in crime. Exp Cell Res 2011; 15(317): 2725-31.
115. Barbolina MV, Burkhalter RJ, Stack MS. Diverse mechanisms for activation of Wnt signalling in the ovarian tumour microenviron-ment. Biochem J 2011; 437(1): 1-12.
116. +-ATPase-mediated acidification for Wnt signaling. Science 2010; 327(5964): 459-63.
117. +-ATPase (V-ATPase) activity and induce S-phase arrest and apoptosis in MCF-7 cells. J Cell Biochem 2010; 109(4): 634-42.
118. - symporter) inhibit the acidification of lysosomes and induce cell cycle blockage in colon cancer cells. Life Sci 2005; 78(2): 121-7.
119. Kawada M, Usami I, Ohba S, et al. Hygrolidin induces p21 expression and abrogates cell cycle progression at G1 and S phases. Bio-chem Biophys Res Commun 2002; 298(1): 178-83.
120. Lim J-H, Park J-W, Kim M-S, Park S-K, Johnson RS, Chun Y-S. Bafilomycin induces the p21-mediated growth inhibition of cancer cells under hypoxic conditions by expressing hypoxia-inducible factor-1alpha. Mol Pharmacol 2006; 70(6): 1856-65.
121. Koshiji M, Huang LE. Dynamic balancing of the dual nature of HIF-1alpha for cell survival. Cell Cycle 2004; 3(7): 853-4.
122. Zhan H, Yokoyama K, Otani H, et al. Different roles of proteolip-ids and 70-kDa subunits of V-ATPase in growth and death of cultured human cells. Genes Cells 2003; 8(6): 501-13.
123. Aiko K, Tsujisawa T, Koseki T, et al. Involvement of cytochrome c and caspases in apoptotic cell death of human submandibular gland ductal cells induced by concanamycin A. Cell Signal 2002; 14(8): 717-22.
124. Chevallier C, Laprévote O, Bignon J, Debitus C, Guénard D, Séve-net T. Isolation of cytotoxic chondropsins, macrolide lactams from the New-Caledonian marine sponge Psammoclemma sp. and elec-trospray ion trap multiple stage MS study of these macrolides. Nat Prod Res 2004; 18(5): 479-84.
125. Hong J, Yamaki K, Ishihara K, Ahn JW, Zee O, Ohuchi K. Induction of apoptosis of RAW 264.7 cells by the cytostatic macrolide apicularen A. J Pharm Pharmacol 2003; 55(9): 1299-306.
126. Morimura T, Fujita K, Akita M, Nagashima M, Satomi A. The proton pump inhibitor inhibits cell growth and induces apoptosis in human hepatoblastoma. Pediatr Surg Int 2008; 24(10): 1087-94.
127. +)-ATPases on endocytosis and apoptosis in RAW cells and RAW cell-derived osteoclasts. J Cell Biochem 2003; 88(6): 1256-64.
128. Yoshimoto Y, Imoto M. Induction of EGF-dependent apoptosis by vacuolar-type H(+)-ATPase inhibitors in A431 cells overexpressing the EGF receptor. Experimental Cell Research 2002; 279(1): 118-27.
129. Hinton A, Bond S, Forgac M. V-ATPase functions in normal and disease processes. Eur J Physiol 2009; 457(3): 589-98.
130. Williamson WR, Hiesinger PR. On the role of V-ATPase V0a1-dependent degradation in Alzheimer disease. Commun Integr Biol 2010; 3(6): 604-7.
131. Beutler JA, McKee TC. Novel marine and microbial natural product inhibitors of vacuolar ATPase. Curr Med Chem 2003; 10(9): 787-96.
132. +-ATPases as a new strategy against cancer. Cancer Res 2007; 67(22): 10627-30.
133. Huss M, Wieczorek H. Inhibitors of V-ATPases: old and new players. J Exp Biol 2009; 212(3): 341-6.
134. Perez-Sayans M, Somoza-Martin JM, Barros-Angueira F, Rey JMG, Garcia-Garcia A. V-ATPase inhibitors and implication in cancer treatment. Cancer Treat Rev 2009; 35(8): 707-13.
135. Yet L. Chemistry and biology of salicylihalamide a and related compounds. Chem Rev 2003; 103(11): 4283-306.
136. Werner G, Hagenmaier H, Drautz H, Baumgartner A, Zahner H. Metabolic products of microorganisms. 224. Bafilomycins, a new group of macrolide antibiotics. Production, isolation, chemical structure and biological activity. J Antibiot (Tokyo) 1984; 37(2): 110-7.
137. Kinashi H, Someno K, Sakaguchi K. Isolation and characterization of concanamycins A, B and C. J Antibiot (Tokyo) 1984; 37(11): 1333-43.
138. Toshima K, Jyojima T, Yamaguchi H, et al. Total Synthesis of Bafilomycin A(1). J Org Chem 1997; 62(10): 3271-84.
139. Toshima K, Jyojima T, Miyamoto N, Katohno M, Nakata M, Matsumura S. The first total synthesis of concanamycin f (con-canolide a). J Org Chem 2001; 66(5): 1708-15.
140. Huss M, Ingenhorst G, Konig S, et al. Concanamycin A, the Specific Inhibitor of V-ATPases, Binds to the Vo Subunit c. J Biol Chem 2002; 277(43): 40544-8.
141. Zhang J, Feng Y, Forgac M. Proton conduction and bafilomycin binding by the V0 domain of the coated vesicle V-ATPase. J Biol Chem 1994; 269(38): 23518-23.
142. Wang Y, Inoue T, Forgac M. Subunit a of the yeast V-ATPase participates in binding of bafilomycin. J Biol Chem 2005; 280(49): 40481-8.
143. Teplova VV, Tonshin AA, Grigoriev PA, Saris N-EL, Salkinoja-Salonen MS. Bafilomycin A1 is a potassium ionophore that impairs mitochondrial functions. J Bioenerg Biomembr 2007; 39(4): 321-9.
144. +)-ATPase inhibitors bafilomycin A1 and concanamycin A and its possible role in apoptosis in RAW 264.7 cells. J Pharmacol Exp Ther 2006; 319(2): 672-81.
145. +-ATPase of osteoclasts with bone antire-sorptive activity. J Med Chem 1998; 41(10): 1568-73.
146. Nadler G, Morvan M, Delimoge I, et al. (2Z,4E)-5-(5,6-dichloro-2-indolyl)-2-methoxy-N-(1,2,2,6,6- pentamethylpiperidin-4-yl)-2,4-pentadienamide, a novel, potent and selective inhibitor of the os-teoclast V-ATPase. Bioorg Med Chem Lett 1998; 8(24): 3621-6.
147. +)-ATPase with the transmembrane V0-sector. Biochemistry 2004; 43(38): 12297-305.
148. +-ATPase bind with high affinity to the purified proteolipid subunit of the membrane domain. Biochemistry 2005; 44(45): 15024-31.
149. +)-ATPase. Curr Pharm Des 2002; 8(23): 2033-48.
150. Hesselink RW, Fedorov A, Hemminga MA, Prieto M. Membrane-bound peptides from V-ATPase subunit a do not interact with an indole-type inhibitor. J Pept Sci 2008; 14(4): 383-8.
151. +)-ATPases. J Pharmacol Exp Ther 2001; 297(1): 114-20.
152. Erickson K, Beutler J, Cardellina Ii J, Boyd M. Salicylihalamides A and B, Novel Cytotoxic Macrolides from the Marine Sponge Hali-clona sp. J Org Chem 1997; 62(23): 8188-92.
153. Galinis DL, McKee TC, Pannell LK, Cardellina JH, Boyd MR. Lobatamides A and B, Novel Cytotoxic Macrolides from the Tunicate Aplidium lobatum. J Org Chem 1997; 62(26): 8968-9.
154. Kunze B, Jansen R, Sasse F, Höfle G, Reichenbach H. Apicularens A and B, new cytostatic macrolides from Chondromyces species (myxobacteria): production, physico-chemical and biological properties. J Antibiot (Tokyo) 1998; 51(12): 1075-80.
155. Lewis A, Stefanuti I, Swain SA, Smith SA, Taylor RJ. A formal total synthesis of (+)-apicularen A: base-induced conversion of api-cularen-derived intermediates into salicylihalamide-like products. Org Biomol Chem 2003; 1(1): 104-16.
156. Shen R, Lin CT, Porco JA. Total synthesis and stereochemical assignment of the salicylate antitumor macrolide lobatamide C(1). J Am Chem Soc 2002; 124(20): 5650-1.
157. Wu Y, Liao X, Wang R, Xie X-S, De Brabander JK. Total synthesis and initial structure-function analysis of the potent V-ATPase inhibitors salicylihalamide A and related compounds. J Am Chem Soc 2002; 124(13): 3245-53.
158. Xie X-S, Padron D, Liao X, Wang J, Roth MG, De Brabander JK. Salicylihalamide A inhibits the V0 sector of the V-ATPase through a mechanism distinct from bafilomycin A1. J Biol Chem 2004; 279(19): 19755-63.
159. Huss M, Sasse F, Kunze B, et al. Archazolid and apicularen: novel specific V-ATPase inhibitors. BMC Biochem 2005; 6: 13-13.
160. Oh, YK, Park, TG. siRNA delivery systems for cancer treatment. Adv Drug Deliv Rev 2009; 61(10): 850-62.
161. You H, Jin J, Shu H, et al. Small interfering RNA targeting the subunit ATP6L of proton pump V-ATPase overcomes chemoresis-tance of breast cancer cells. Cancer Lett 2009; 280(1): 110-19.
162. Young CD, Anderson SM. Sugar and fat - that's where it's at: metabolic changes in tumors. Breast Cancer Res 2008; 10(1): 202.
163. Tosi MR, Tugnoli V. Cholesteryl esters in malignancy. Clin Chim Acta 2005; 359(1-2): 27-45.
164. Ryland LK, Fox TE, Liu X, Loughran TP, Kester M. Dysregulation of sphingolipid metabolism in cancer. Cancer Biol Ther 2011; 11(2): 138-49.
165. Buchwald H. Cholesterol inhibition, cancer, and chemotherapy. Lancet 1992; 339(8802): 1154-6.
166. Canals D, Perry DM, Jenkins RW, Hannun YA. Drug targeting of sphingolipid metabolism: sphingomyelinases and ceramidases. Br J Pharmacol 2011; 163(4): 694-712.
167. Schroeder A, Levins CG, Cortez C, Langer R, Anderson DG. Lipid-based nanotherapeutics for siRNA delivery. J Intern Med 2010; 267(1): 9-21.
168. Ho YK, Smith RG, Brown MS, Goldstein JL. Low-density lipopro-tein (LDL) receptor activity in human acute myelogenous leukemia cells. Blood 1978; 52(6): 1099-14.
169. +-ATPases by fusidic acid and suramin. FEBS Lett 1988; 234(2): 383-6.
170. Kalaitzis JA, de Almeida Leone P, Harris L, et al. Adociasulfates 1, 7, and 8: New Bioactive Hexaprenoid Hydroquinones from the Marine Sponge Adocia sp. J Org Chem 1999; 64(15): 5571-5574.
171. Hernandez A, Serrano G, Herrera-Palau R, Perez-Castiñeira JR, Serrano A. Intraorganellar acidification by V-ATPases: a target in cell proliferation and cancer therapy. Recent Pat Anticancer Drug Discov 2010; 5(2): 88-98.
172. Hettiarachchi KD, Zimmet PZ, Myers MA. The effects of repeated exposure to sub-toxic doses of plecomacrolide antibiotics on the endocrine pancreas. Food Chem Tox 2006; 44(12): 1966-77.