Vacuolar H+-ATPase Signaling Pathway in Cancer

Current Protein and Peptide Science

Volumn 13, Issue 2, 2012, Pages 152-163

  Sennoune, Souad R ^a   Martínez Zaguilán, Raul ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

(Pro)renin receptor ATP6ap2; Glycolysis; Hypoxia inducible factor; Metastasis; V ATPase; Wnt ( catenin

Indexed keywords

BETA CATENIN; GLUCOSE; HYPOXIA INDUCIBLE FACTOR; ISOENZYME; PRORENIN RECEPTOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; VACUOLAR PROTON ATPASE; WNT PROTEIN;

ACIDIFICATION; ALKALINITY; CELL FUNCTION; CELL PH; CELL SURFACE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; ENZYME STRUCTURE; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; INTRACELLULAR TRANSPORT; NEOPLASM; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84860788603     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920312800493197     Document Type: Review

References (142)

1. Warburg, O.; Wind, F.; Negelein, E. The Metabolism of Tumors in the Body. J. Gen. Physiol., 1927, 8, 519-530.
2. Warburg, O.; Wind, F.; Neglers, E. On the metabolism of tumors in the body. In: Metabolism of tumors. O. Warburg. Ed.; Constable & Co: London, 1930; pp. 254-270.
3. Warburg, O. On the origin of cancer cells. Science, 1956, 123, 309-314.
4. Vander Heiden, M.G.; Cantley, L.C.; Thompson, C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 2009, 324(5930), 1029-1033.
5. Gillies, R.J.; Robey, I.; Gatenby, R.A. Causes and consequences of increased glucose metabolism of cancers. J. Nucl. Med., 2008, 49, 24S-42S.
6. Gillies, R.J.; Martínez-Zaguilán, R.; Martinez, G.M.; Serrano, R.; Perona, R. Tumorigenic 3T3 cells maintain an alkaline intracellular pH under physiological conditions. Proc. Natl. Acad. Sci. USA, 1990, 87(19), 7414-7418.
7. Perona, R.; Serrano, R. Increased pH and tumorigenicity of fibroblasts expressing a yeast proton pump. Nature, 1988, 334(6181), 438-340.
8. Racker, E. Bioenergetics and the problem of tumor growth. Am. Sci., 1972, 60(1), 56-63.
9. +)-ATPases are functionally expressed in plasma membranes of human tumor cells. Am. J. Physiol., 1993, 265(4Pt1):C1015-C1029.
10. Chiche, J.; Lefur, Y.; Vilmen, C.; Frassineti, F.; Daniel, L.; Hal-estrap, A.P.; Cozzone, P.J.; Pouysségur, J.; Lutz, N.W. In vivo pH in metabolic-defective Ras-transformed fibroblast tumors. Key role of the monocarboxylate transporter, MCT4, for inducing an alkaline intracellular pH. Int. J. Cancer, 2011 Apr 11. doi: 10.1002/ijc.26125. [Epub ahead of print]
11. Newell, K.; Franchi, A.; Pouysségur, J.; Tannock, I. Studies with glycolysis-deficient cells suggest that production of lactic acid is not the only cause of tumor acidity. Proc. Natl. Acad. Sci. USA, 1993, 90, 1127-1131.
12. Parks, S.K.; Chiche, J.; Pouyssegur, J. pH control mechanisms of tumor survival and growth. J. Cell Physiol., 2011, 226, 299-308.
13. M. Vacuolar AT Pases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol., 2007, 8, 917-929.
14. Jefferies, K.C.; Cipriano, D.J.; Forgac, M. Function, structure and regulation of the vacuolar (H+) ATPases. Arch. Biochem. Biophys., 2008, 476, 33-42.
15. Cipriano, D.J.; Wang, Y.; Bond, S.; Hinton, A.; Jefferies, K.C.; Qi, J.; Forgac, M. Structure and regulation of the vacuolar ATPases. Biochim. Biophys. Acta, 2008, 1777, 599-604.
16. Brown, D.; Marshansky, V. Renal V-ATPase: Physiology and pathophysiology. In: Handbook of ATPases: Biochemistry, Cell Biology, Pathophysiology; M. Futai, Y. Wada, J. H. Kaplan. Ed.; Wiley-VCH: Weinheim, 2004; pp. 414-442.
17. Toyomura, T.; Murata, Y.; Yamamoto, A.; Oka, T.; Sun-Wada, G. H.; Wada, Y.; Futai, M. From lysosomes to the plasma membrane: Localization of vacuolar-type H+-ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem., 2003, 278, 22023-22030.
18. Hinton, A.; Sennoune, S.R.; Bond, S.; Fang, M.; Reuveni, M.; Sahagian, G.G.; Jay, D.; Martínez-Zaguilán, R.; Forgac, M. Function of a subunit isoforms of the V-ATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. J. Biol. Chem., 2009, 284(24), 16400-16408.
19. +-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am. J. Physiol. Cell Physiol., 2004, 286(6), C1443-1452.
20. +-ATPase in drug-resistant human breast carcinoma cell lines. Biochem. Pharmacol., 1999, 57(9):1037-46.
21. +)-ATPase may contribute to elevated intracellular pH (pHin) in some human tumor cells. Ann. N. Y. Acad. Sci., 1992, 671, 478-480.
22. Raghunand, N.; Martínez-Zaguilán, R.; Wright, S.H.; Gillies, R.J. pH and drug resistance. II. Turnover of acidic vesicles and resistance to weakly basic chemotherapeutic drugs. Biochem. Pharmacol., 1999, 57(9):1047-1058.
23. 2+]in in human melanoma cells with different metastatic potential. J. Cell Physiol., 1998, 176(1), 196-205.
24. Ohta, T.; Arakawa, H.; Futagami, F.; Fushida, S.; Kitagawa, H.; Kayahara, M.; Nagakawa, T.; Miwa, K.; Kurashima, K.; Numata, M.; Kitamura, Y.; Terada, T.; Ohkuma, S. Bafilomycin A1 induces apoptosis in the human pancreatic cancer cell line Capan-1. J. Pathol., 1998, 185(3), 324-330.
25. Cruciat, C.M.; Ohkawara, B.; Acebron, S.P.; Karaulanov, E.; Rein-hard, C.; Ingelfinger, D.; Boutros, M.; Niehrs, C. Requirement of prorenin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling. Science, 2010, 327(5964), 459-463.
26. Li, G.; Yang, Q.; Krishnan, S.; Alexander, E.A.; Borkan, S.C.; Schwartz, J.H. A novel cellular survival factor-the B2 subunit of vacuolar H+-ATPase inhibits apoptosis. Cell Death Differ., 2006, 13, 2109-2117.
27. Yan Y, Denef N, Schupbach T. The vacuolar proton pump, VAT-Pase, is required for notch signaling and endosomal trafficking in Drosophila. Dev. Cell, 2009, 17, 387-402.
28. Hermle, T.; Saltukoglu, D.; Grunewald, J.; Walz, G.; Simons, M. Regulation of Frizzled-dependent planar polarity signaling by a V-ATPase subunit. Curr Biol., 2010, 20, 1269-1276.
29. +)-ATPase causes conditional lethality. Proc. Natl. Acad. Sci. USA, 1990, 87(9), 3503-3507.
30. + ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol., 2006, 209(Pt4), 577-589.
31. Kirshner, N. Uptake of catecholamines by a particulate fraction of the adrenal medulla. J. Biol. Chem., 1962, 237, 2311-2317.
32. E. Immunity ininfective diseases, Cambridge University Press Warehouse, MacMillan & Co, Ldt: Cambridge, England, 1905.
33. +-ATPase in cancer biology. Cell Biochem Bio-phys., 2004, 40(2), 185-206.
34. +-ATPases in angiogenesis, diabetes and cancer. J. Bioenerg. Biomembr., 2007, 39(5-6):427-433.
35. De Milito, A.; Canese, R.; Marino, M. L.; Borghi, M.; Iero, M.; Villa, A.; Venturi, G.; Lozupone, F.; Iessi, E.; Logozzi, M.; Della Mina, P.; 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, 2010, 127, 207-219.
36. +-ATPases as a new strategy against cancer. Cancer Res., 2007, 67, 10627-10630.
37. Pérez-Sayáns, M.; Somoza-Martín, J.M.; Barros-Angueira, F.; Diz, P.G.; Rey, J.M.; García-García, A. Multidrug resistance in oral squamous cell carcinoma: The role of vacuolar ATPases. Cancer Lett., 2010, 295, 135-143.
38. +-ATPase: moving from low-resolution models to high resolution structures. J. Bioenerg. Biomembr., 2003, 35(4), 337-345.
39. +)-ATPases--nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol., 2002, 3, 94-103.
40. Wilkens, S.; Forgac, M. Three-dimensional structure of the vacuo-lar ATPase proton channel by electron microscopy. J. Biol. Chem., 2001, 276, 44064-44068.
41. Sun-Wada, G.H.; Wada, Y. Vacuolar-type proton pump ATPases: roles of subunit isoforms in physiology and pathology. Histol. Histopathol., 2010, 25(12), 1611-1620.
42. Toei, M.; Saum, R.; Forgac, M. Regulation and isoform function of the V-ATPases. Biochemistry, 2010, 49(23), 4715-4723.
43. +)-ATPase from chromaffin granules. J. Biol. Chem., 1994, 269, 24102-24106.
44. Getlawi, F.; Laslop, A.; Schägger, H.; Ludwig, J.; Haywood, J.; Apps, D. Chromaffin granule membrane glycoprotein IV is identical with Ac45, a membrane-integral subunit of the granule's H(+)-ATPase. Neurosci. Lett., 1996, 219,13-16.
45. +-ATPase accessory subunit Ac45 in Xenopus pituitary. Eur. J. Biochem., 1999, 262, 484-491.
46. Jansen, E.J.; van Bakel, N.H.; Coenen, A.J.; van Dooren, S.H.; van Lith, H.A.; Martens, G.J. An isoform of the vacuolar (H(+))-ATPase accessory subunit Ac45. Cell Mol. Life Sci., 2010, 67, 629-640.
47. Schoonderwoert, V.T.; Jansen, E.J.; Martens, G.J. The fate of newly synthesized V-ATPase accessory subunit Ac45 in the secretory pathway. Eur. J. Biochem., 2002, 269, 1844-1853.
48. Feng, H.; Cheng, T.; Pavlos, N.J.; Yip, K.H.; Carrello, A.; Seeber, R.; Eidne, K.; Zheng, M.H.; Xu, J. Cytoplasmic terminus of vacuolar type proton pump accessory subunit Ac45 is required for proper interaction with V(0) domain subunits and efficient osteoclastic bone resorption. J. Biol. Chem., 2008, 283, 13194-13204.
49. Nguyen, G. Renin, (pro)renin and receptor: an update. Clin. Sci. (Lond), 2011, 120(5), 169-178.
50. Nguyen, G.; Muller, D.N. The biology of the (pro)renin receptor. J. Am. Soc. Nephrol., 2010, 21, 18-23.
51. Louagie, E.; Taylor, N.A.; Flamez, D.; Roebroek, A.J.; Bright, N.A.; Meulemans, S.; Quintens, R.; Herrera, P.L.; Schuit, F.; Van de Ven, W.J.; Creemers, J.W. Role of furin in granular acidification in the endocrine pancreas: identification of the V-ATPase subunit Ac45 as a candidate substrate. Proc. Natl. Acad. Sci. USA, 2008, 105, 12319-12324.
52. Cousin, C.; Bracquart, D.; Contrepas, A.; Corvol, P.; Muller, L.; Nguyen, N. Soluble form of the (pro)renin receptor generated by intracellular cleavage by furin is secreted in plasma. Hypertension, 2009, 53(6), 1077-1082.
53. Schoonderwoert, V.T.; Martens G.J. Targeted disruption of the mouse gene encoding the V-ATPase accessory subunit Ac45. Mol. Membr. Biol., 2002, 19, 67-71.
54. Amsterdam, A.; Nissen, R.M.; Sun, Z.; Swindell, E.C.; Farrington, S.; Hopkins, N.; Identification of 315 genes essential for early ze-brafish development. Proc. Natl. Acad. Sci. USA, 2004, 101, 12792-12797.
55. Sihn, G.; Rousselle, A.; Vilianovitch, L.; Burckle, C.; Bader, M. Physiology of the (pro)renin receptor: Wnt of change? Kidney Int., 2010, 78, 246-256.
56. Nishi, T.; Forgac, M. Molecular cloning and expression of three isoforms of the 100-kDa a subunit of the mouse vacuolar proton-translocating ATPase. J. Biol. Chem., 2000, 275(10), 6824-6830.
57. Scott, B.B.; Chapman, C.G. The putative 116 kDa osteoclast specific vacuolar proton pump subunit has ubiquitous tissue distribution. Eur. J. Pharmacol., 1998, 346(1), R3-4.
58. Toyomura, T.; Oka, T.; Yamaguchi, C.; Wada, Y.; Futai, M. Three subunits a isoforms of mouse vacuolar V-type H+-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem., 2000, 275, 8760-8765.
59. Pietrement, C.; Sun-Wada, G. H.; Silva, N. D.; McKee, M.; Mar-shansky, V.; Brown, D.; Futai, M.; Breton, S. Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol. Reprod., 2006, 74, 185-194.
60. Gu, F.; Gruenberg, J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J. Biol. Chem., 2000, 275(11), 8154-8160.
61. Merkulova, M.; Hurtado-Lorenzo, A.; Hosokawa, H.; Zhuang, Z.; Brown, D.; Ausiello, D.A.; Marshansky, V. Aldolase directly interacts with ARNO and modulates cell morphology and acidic vesicle distribution. Am. J. Physiol. Cell Physiol., 2011 Feb 9. [Epub ahead of print].
62. +)-ATPase in vesicular trafficking: targeting, regulation and function. Curr. Opin. Cell Biol., 2008, 20, 415-426.
63. Hurtado-Lorenzo, A.; Skinner, M.; El Annan, J.; Futai, M.; Sun-Wada, G.H.; Bourgoin, S.; Casanova, J.; Wildeman, A.; Bechoua, S.; Ausiello, D.A.; Brown, D.; Marshansky, V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol., 2006, 8, 124-136.
64. D'Souza-Schorey, C.; Chavrier, P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol., 2006, 7, 347-358.
65. Perez, L.; Carrasco, L. Involvement of the vacuolar H+-ATPase in animal virus entry. J. Gen. Virol., 1994, 75, 2595-2606.
66. Peters, C.; Bayer, M.J.; Buhler, S.; Andersen, J.S.; Mann, M.; Mayer, A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature, 2001, 409, 581-588.
67. Guinea, R.; Carrasco, L. Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J. Virol., 1995; 69, 2306-2312.
68. Nanda, A.; Brumell, J.H.; Nordstrom, T.; Kjeldsen, L.; Sengelov, H.; Borregaard, N.; Rotstein, O.D.; Grinstein, S. Activation of proton pumping in human neutrophils occurs by exocytosis of vesicles bearing vacuolar-type H+-ATPases. J. Biol. Chem., 1996, 271, 15963-15970.
69. Bonifacino, J.S.; Glick, B.S. The mechanisms of vesicle budding and fusion. Cell, 2004, 116, 153-166.
70. Liegeois, S.; Benedetto, A.; Garnier, J.M.; Schwab, Y.; Labouesse, M. The V0- ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol., 2006, 173, 949-961.
71. Sun-Wada, G.H.; Toyomura, T.; Murata, Y.; Yamamoto, A.; Futai, M.; Wada, Y. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta cells. J. Cell Sci., 2006, 119, 4531-4540.
72. Li, Y.P.; Chen, W.; Liang, Y.; Li, E.; Stashenko, P. Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast mediated extracellular acidification. Nat. Genet., 1999, 23, 447-451.
73. Frattini, A.; Orchard, P.J.; Sobacchi, C.; Giliani, S.; Abinun, M.; Mattsson, J.P.; Keeling, D.J.; Andersson, A.K.; Wallbrandt, P.; Zecca, L.; Notarangelo, L.D.; Vezzoni, P.; Villa, A. Defects in TCIRG1subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat. Genet., 2000, 25, 343-346.
74. Kartner, N.; Yao, Y.; Li, K.; Crasto, G.J.; Datti, A.; Manolson, M.F. Inhibition of osteoclast bone resorption by disrupting vacuolar H+-ATPase a3-B2 subunit interaction. J. Biol. Chem., 2010, 285(48), 37476-37490.
75. Pastor-Soler, N.; Beaulieu, V.; Litvin, T.N.; Da Silva, N.; Chen, Y.; Brown, D.; Buck, J.; Levin, L.R.; Breton, S. Bicarbonateregulated adenylyl cyclase (sAC) is a sensor that regulates pH dependent V-ATPase recycling. J. Biol. Chem., 2003, 278, 49523-49529.
76. Karet, F.E.; Finberg, K.E.; Nelson, R.D.; Nayir, A.; Mocan, H.; Sanjad, S.A., Rodriguez-Soriano, J.; Santos, F.; Cremers, C.W.; Di Pietro, A.; Hoffbrand, B.I.; Winiarski, J.; Bakkaloglu, A.; Ozen, S.; Dusunsel, R.; Goodyer, P.; Hulton, S.A.; Wu, D.K.; Skvorak, A.B.; Morton, C.C.; Cunningham, M.J.; Jha, V.; Lifton, R.P. Mutations in the gene encoding B1 subunit of H+-ATPase cause renal tubular acidosis with sensorineural deafness. Nat. Genet., 1999, 21, 84-90.
77. Oka, T.; Murata, Y.; Namba, M.; Yoshimizu, T.; Toyomura, T.; Yamamoto, A.; Sun-Wada, G. H.; Hamasaki, N.; Wada, Y.; Fu-tai, M. a4, a unique kidney-specific isoform of mouse vacuolar H+-ATPase subunit a. J. Biol. Chem., 2001, 276, 40050-40054.
78. Rojas, J.D.; Sennoune, S.R.; Maiti, D.; Bakunts, K.; Reuveni, M.; Sanka, S.C.; Martinez, G.M.; Seftor, E.A.; Meininger, C.J.; Wu, G.; Wesson, D.E.; Hendrix, M.J.; 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(3), H1147-1157.
79. Rojas, J.D.; Sennoune, S.R.; Maiti, D.; Martinez, G.M.; Bakunts, K.; Wesson, D.E.; Martínez-Zaguilán, R. Plasmalemmal V-H(+)-ATPases regulate intracellular pH in human lung microvascular endothelial cells. Biochem. Biophys. Res. Commun., 2004, 320(4), 1123-1132.
80. Steinberg, B.E.; Touret, N.; Vargas-Caballero, M.; Grinstein, S. In situ measurement of the electrical potential across the phagosomal membrane using FRET and its contribution to the proton-motive force. Proc. Natl. Acad. Sci. USA, 2007, 104(22), 9523-9528.
81. Hinton, A.; Bond, S.; Forgac, M. V-ATPase functions in normal and disease processes. Pflugers Arch., 2009, 457(3), 589-598.
82. +)-ATPase. J. Cell Physiol., 1994, 161(1):129-141.
83. 2+]in in human melanoma cells with different metastatic potential. J. Cell Physiol., 1998, 176(1), 196-205.
84. Kane, P.M. The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol. Mol. Biol. Rev., 2006, 70, 177-191.
85. Kane, P.M.; Parra, K.J. Assembly and regulation of the yeast vacuolar H(+)-ATPase. J. Exp. Biol., 2000, 203, 81-87.
86. Parra, K.J.; Kane, P.M. Reversible association between the V1 and V0 domains of yeast vacuolar H -ATPase is an unconventional glucose-induced effect. Mol. Cell. Biol., 1998, 18, 7064-7074.
87. Kane, P. M. Disassembly and reassembly of the yeast vacuolar H -ATPase in vivo. J. Biol. Chem., 1995, 270, 17025-17032.
88. +-ATPase assembly, translocation, and acidification of intracellu-lar compartments in renal epithelial cells. Mol. Cell Biol., 2005, 25, 575-589.
89. Qi, J.; Forgac, M. Cellular environment is important in controlling V-ATPase dissociation and its dependence on activity. J. Biol. Chem., 2007, 282, 24743-24751.
90. Bond, S.; Forgac, M. The Ras/cAMP/protein kinase A pathway regulates glucose-dependent assembly of the vacuolar (H+)-ATPase in yeast. J. Biol. Chem., 2008, 283, 36513-36521, 2008.
91. +]lux. EMBO J., 2010, 29, 2473-2474.
92. Dechant, R.; Binda, M.; Lee, S.S.; 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, 2515-2526.
93. +-ATPase in vivo. J. Biol. Chem., 2001, 276, 24855-24861.
94. Seol, J.H.; Shevchenko, A.; Deshaies, R.J. Skp1 forms multiple protein complexes, including RAVE, a regulator of V-ATPase assembly. Nat. Cell Biol., 2001, 3, 384-391.
95. Smardon, A. M.; Kane, P.M. RAVE is essential for the efficient assembly of the C subunit with the vacuolar H-ATPase. J. Biol. Chem., 2007, 282, 26185-26194.
96. Smardon, A. M.; Tarsio, M.; Kane, P.M. The RAVE complex is essential for stable assembly of the yeast V-ATPase. J. Biol. Chem., 2002, 277, 13831-13839.
97. +-ATPase is essential for the assembly and activity of the proton pump. J. Biol. Chem., 2007, 282, 24495-24503.
98. +-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J. Biol. Chem., 2001, 276, 30407-30413.
99. +-ATPase. J. Biol. Chem., 2004, 279, 8732-8739.
100. Martinez-Munoz, G.A.; Kane, P. Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J. Biol. Chem., 2008, 283, 20309-20319.
101. Kinouchi, K.; Ichihara, A.; Sano, M.; Sun-Wada, G.H.; Wada, Y.; Kurauchi-Mito, A.; Bokuda, K.; Narita, T.; Oshima, Y.; Sakoda, M.; Tamai, Y.; Sato, H.; Fukuda, K.; Itoh, H. The (Pro)renin recep-tor/ ATP6AP2 is essential for vacuolar H+ ATPase assembly in murine cardiomyocytes. Circ. Res., 2010, 107, 30-34.
102. Ludwig, J.; Kerscher, S.; Brandt, U.; Pfeiffer, K.; Getlawi, F.; Apps, D.K.; Schägger, H. Identification and characterization of a novel 9.2-kDa membrane sector-associated protein of vacuolar pro-ton-ATPase from chromaffin granules. J. Biol. Chem., 1998, 273,10939-10947.
103. Nguyen, G.; Delarue, F.; Burckle, C.; Bouzhir, L.; Giller, L.; Sraer, J.D. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J. Clin. Invest., 2002, 109, 1417-1427.
104. Burckle, C.; Bader, M. Prorenin and its ancient receptor. Hypertension, 2006, 48(4), 549-551.
105. Bader M. The second life of the (pro)renin receptor. J. Renin. An-giotensin. Aldosterone. Syst., 2007, 8, 205-208.
106. Contrepas, A.; Walker, J.; Koulakoff, A.; Franek, K.J.; Qadri, F.; Giaume, C.; Corvol, P.; Schwartz, C.E.; Nguyen, G. A role of the (pro)renin receptor in neuronal cell differentiation. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2009, 297(2), R250-R257.
107. Karlas, A.; Machuy, N.; Shin, Y.; Pleissner, K.P.; Artarini, A.; Heuer, D.; Becker, D.; Khalil, H.; Ogilvie, L.A.; Hess, S.; Mäurer, A.P.; Müller, E.; Wolff, T.; Rudel, T.; Meyer, T.F. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature, 2010, 463(7282), 818-822.
108. König, R.; Stertz, S.; Zhou, Y.; Inoue, A.; Hoffmann, H.H.; Bhat-tacharyya, S.; Alamares, J.G.; Tscherne, D.M.; Ortigoza, M.B.; Liang, Y.; Gao, Q.; Andrews, S.E.; Bandyopadhyay, S.; De Jesus, P.; Tu, B.P.; Pache, L.; Shih, C.; Orth, A.; Bonamy, G.; Miraglia, L.; Ideker, T.; García-Sastre, A.; Young, J.A.; Palese, P.; Shaw, M.L.; Chanda, S.K. Human host factors required for influenza virus replication. Nature, 2010, 463(7282), 813-817.
109. Advani, A.; Kelly, D.J.; Cox, A.J.; White, K.E.; Advani, S.L.; Thai, K.; Connelly, K.A.; Yuen, D.; Trogadis, J.; Herzenberg, A.M.; Kuliszewski, M.A.; Leong-Poi, H.; Gilbert, R.E. The (Pro)renin receptor: site-specific and functional linkage to the vacuolar H-ATPase in the kidney. Hypertension, 2009, 54(2), 261-269.
110. Marshansky, V. The V-ATPase a2-subunit as a putative endosomal pH-sensor. Biochem. Soc. Trans., 2007, 35, 1092-1099.
111. Buechling, T.; Bartscherer, K.; Ohkawara, B.; Chaudhary, V.; Spirohn, K.; Niehrs, C.; Boutros, M. Wnt/Frizzled signaling requires dPRR, the Drosophila homolog of the prorenin receptor. Curr. Biol., 2010, 20, 1263-1268.
112. Nusse, R.; Varmus, H.E. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell, 1982, 31(1), 99-109.
113. Cadigan, K.M.; Nusse, R. Wnt signaling: a common theme in animal development. Genes Dev., 1997, 11, 3286-3305.
114. Clevers, H. Wnt/beta-catenin signaling in development and disease. Cell, 2006, 127(3), 469-480.
115. Katoh, M. WNT signaling in stem cell biology and regenerative medicine. Curr. Drug Targets, 2008, 9, 565-570.
116. Katoh, M. WNT/PCP signaling pathway and human cancer. Oncol. Rep., 2005, 14, 1583-1588.
117. Kohn, A.D.; Moon, R.T. Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium, 2005, 38, 439-446.
118. Moon, R.T.; Bowerman, B.; Boutros, M.; Perrimon, N. The promise and perils of Wnt signaling through beta-catenin. Science, 2002, 296, 1644-1646.
119. Lustig, B.; Behrens, J. The Wnt signaling pathway and its role in tumor development. J Cancer Res. Clin. Oncol., 2003, 129, 199-221.
120. He, X.; Semenov, M.; Tamai, K.; Zeng, X. LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: Arrows point the way. Development, 2004, 131(8), 1663-1677.
121. Kikuchi, A.; Yamamoto, H. Regulation of Wnt signalling by receptor-mediated endocytosis. J. Biochem., 2007, 141(4), 443-451.
122. Nelson, W.J.; Nusse, R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science, 2004, 303, 1483-1487.
123. Hermle, T.; Petzoldt, A.G.; Simons, M. The role of proton transporters in epithelial Wnt signaling pathways. Pediatr. Nephrol., 2011, Mar 5. [Epub ahead of print]
124. Taelman, V.F.; Dobrowolski, R.; Plouhinec, J.L.; Fuentealba, L.C.; Vorwald, P.P.; Gumper, I.; Sabatini, D.D.; De Robertis, E.M. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell, 2010, 143(7), 1136-1148.
125. Bilic, J.; Huang, Y.L.; Davidson, G.; Zimmermann, T.; Cruciat, C.M.; Bienz, M.; Niehrs, C. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science, 2007, 316(5831), 1619-1622.
126. Niehrs, C.; Acebron, S.P. Wnt signaling: multivesicular bodies hold GSK3 captive. Cell, 2010, 143(7), 1044-1046.
127. Aragonés, J.; Fraisl, P.; Baes, M.; Carmeliet, P. Oxygen sensors at the crossroad of metabolism. Cell Metab., 2009, 9(1), 11-22.
128. Bertout, J.A.; Patel, S.A.; Simon, M.C. The impact of O2 availability on human cancer. Nat. Rev. Cancer, 2008, 8(12), 967-975.
129. Kaelin, W.G. Jr.; Thompson, C.B. Q&A: Cancer: clues from cell metabolism. Nature, 2010; 465, 562-564.
130. Semenza, G.L.; Wang, G.L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell Biol., 1992, 12, 5447-5454.
131. Robey, I.F.; Lien, A.D.; Welsh, S.J.; Baggett, B.K.; Gillies, R.J. Hypoxia-inducible factor-1alpha and the glycolytic phenotype in tumors. Neoplasia, 2005, 7(4), 324-330.
132. Robey, I.F.; Stephen, R.M.; Brown, K.S.; Baggett, B.K.; Gatenby, R.A., Gillies, R.J. Regulation of the Warburg effect in early-passage breast cancer cells. Neoplasia, 2008, 10(8), 745-756.
133. Kaelin, W.G.; Ratcliffe, P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell., 2008, 30(4), 393-402.
134. Maxwell, P.H. The HIF pathway in cancer. Semin. Cell Dev. Biol., 2005, 16, 523-530.
135. Semenza, G.L. HIF-1: upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev., 2010, 20, 51-56.
136. Mekhail, K.; Gunaratnam, L.; Bonicalzi, M.E.; Lee, S. HIF activation by pH-dependent nucleolar sequestration of VHL. Nat. Cell Biol., 2004, 6, 642-647.
137. Kim, J.W.; Tchernyshyov, I.; Semenza, G.L.; Dang, C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Me-tab., 2006, 3, 177-185.
138. Kim, J.W.; Gao, P.; Liu, Y.C.; Semenza, G.L.; Dang, C.V. Hy-poxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol. Cell Biol., 2007, 27, 7381-7393.
139. Quintero, M.; Brennan, P.A.; Thomas, G.J.; Moncada, S. Nitric oxide is a factor in the stabilization of hypoxia-inducible factor-1 in cancer: role of free radical formation. Cancer Res., 2006, 66, 770-774.
140. Sonveaux, P.; Végran, F.; Schroeder, T.; Wergin, M.C.; Verrax, J.; Rabbani, Z.N.; De Saedeleer, C.J.; Kennedy, K.M.; Diepart, C.; Jordan, B.F.; Kelley, M.J.; Gallez, B.; Wahl, M.L.; Feron, O.; De-whirst, M.W. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J. Clin. Invest., 2008, 118, 3930-3942.
141. Lim, J.H.; Park, J.W.; Kim, M.S.; Park, S.K.; Johnson, R.S.; 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), 1856-1865.
142. Lim, J.H.; Park, J.W.; Kim, S.J.; Kim, M.S.; Park, S.K.; Johnson, R.S.; Chun, Y.S. ATP6V0C competes with von Hippel-Lindau protein in hypoxia-inducible factor 1 alpha (HIF-1alpha) binding and mediates HIF-1alpha expression by bafilomycin A1. Mol. Pharmacol., 2007, 71(3), 942-948.