pH control mechanisms of tumor survival and growth

Journal of Cellular Physiology

Volumn 226, Issue 2, 2011, Pages 299-308

  Parks, Scott K ^a   Chiche, Johanna ^a   Pouyssegur, Jacques ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; BICARBONATE; CARBONATE DEHYDRATASE IX; CARBONATE DEHYDRATASE XII; MONOCARBOXYLATE TRANSPORTER; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM PROTON EXCHANGE PROTEIN;

ACIDIFICATION; ANION EXCHANGE; CELL PH; CELL SURVIVAL; HUMAN; MEMBRANE TRANSPORT; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL; TUMOR GROWTH;

CARBONIC ANHYDRASES; CELL HYPOXIA; CELL SURVIVAL; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE TRANSPORT PROTEINS; NEOPLASM METASTASIS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 78649659788     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22400     Document Type: Review

References (151)

1. Ahlskog JKJ, Dumelin CE, Trüssel S, Mårlind J, Neri D. 2009. In vivo targeting of tumor-associated carbonic anhydrases using acetazolamide derivatives. Bioorg Med Chem Lett 19: 4851-4856.
2. Ahmed S, Thomas G, Ghoussaini M, Healey CS, Humphreys MK, Platte R, Morrison J, Maranian M, Pooley KA, Luben R, Eccles D, Evans DG, Fletcher O, Johnson N, dos Santos Silva I, Peto J, Stratton MR, Rahman N, Jacobs K, Prentice R, Anderson GL, Rajkovic A, Curb JD, Ziegler RG, Berg CD, Buys SS, McCarty CA, Feigelson HS, Calle EE, Thun MJ, Diver WR, Bojesen S, Nordestgaard BG, Flyger H, Dörk T, Schürmann P, Hillemanns P, Karstens JH, Bogdanova NV, Antonenkova NN, Zalutsky IV, Bermisheva M, Fedorova S, Khusnutdinova E, SEARCH, Kang D, Yoo KY, Noh DY, Ahn SH, Devilee P, van Asperen CJ, Tollenaar RA, Seynaeve C, Garcia-Closas M, Lissowska J, Brinton L, Peplonska B, Nevanlinna H, Heikkinen T, Aittomäki K, Blomqvist C, Hopper JL, Southey MC, Smith L, Spurdle AB, Schmidt MK, Broeks A, van Hien RR, Cornelissen S, Milne RL, Ribas G, González-Neira A, Benitez J, Schmutzler RK, Burwinkel B, Bartram CR, Meindl A, Brauch H, Justenhoven C, Hamann U, GENICA Consortium, Chang-Claude J, Hein R, Wang-Gohrke S, Lindblom A, Margolin S, Mannermaa A, Kosma VM, Kataja V, Olson JE, Wang X, Fredericksen Z, Giles GG, Severi G, Baglietto L, English DR, Hankinson SE, Cox DG, Kraft P, Vatten LJ, Hveem K, Kumle M, Sigurdson A, Doody M, Bhatti P, Alexander BH, Hooning MJ, van den Ouweland AM, Oldenburg RA, Schutte M, Hall P, Czene K, Liu J, Li Y, Cox A, Elliott G, Brock I, Reed MW, Shen CY, Yu JC, Hsu GC, Chen ST, Anton-Culver H, Ziogas A, Andrulis IL, Knight JA, kConFab, Australian Ovarian Cancer Study Group, Beesley J, Goode EL, Couch F, Chenevix-Trench G, Hoover RN, Ponder BA, Hunter DJ, Pharoah PD, Dunning AM, Chanock SJ, Easton DF, 2009. Newly discovered breast cancer susceptibility loci on 3p24 and 17q23.2. Nat Genet 41: 585-590.
3. +-independent SLC4 anion exchangers. J Exp Biol 212: 1672-1683.
4. Alterio V, Hilvo M, Di Fiore A, Supuran CT, Pan P, Parkkila S, Scaloni A, Pastorek J, Pastorekova S, Pedone C, Scozzafava A, Monti SM, De Simone G. 2009. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci USA 106: 16233-16238.
5. Barnett DH, Sheng S, Charn TH, Waheed A, Sly WS, Lin CY, Liu ET, Katzenellenbogen BS. 2008. Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res 68: 3505-3515.
6. +-lactate cotransport via monocarboxylate transporter 1. J Biol Chem 283: 21655-21667.
7. Becker HM, Fecher-Trost C, Hirnet D, Sültemeyer D, Deitmer JW. 2005. Transport activity of MCT1 expressed in Xenopus oocytes is increased by interaction with carbonic anhydrase. J Biol Chem 280: 39882-39889.
8. Becker HM, Klier M, Deitmer JW. 2010. Nonenzymatic augmentation of lactate transport via monocarboxylate transporter isoform 4 by carbonic anhydrase II. J Membr Biol 234: 125-135.
9. Bernstein L, Henderson BE, Hanisch R, Sullivan-Halley J, Ross RK. 1994. Physical exercise and reduced risk of breast cancer in young women. J Natl Cancer Inst 86: 1403-1408.
10. 2 availability on human cancer. Nat Rev Cancer 8: 967-975.
11. Boron WF, Chen L, Parker MD. 2009. Modular structure of sodium-coupled bicarbonate transporters. J Exp Biol 212: 1697-1706.
12. Boyer MJ, Tannock IF. 1992. Regulation of intracellular pH in tumor cell lines: Influence of microenvironmental conditions. Cancer Res 52: 4441-4447.
13. Brahimi-Horn MC, Pouyssegur J. 2009. HIF at a glance. J Cell Sci 122: 1055-1057.
14. Brahimi-Horn MC, Pouysségur J. 2007. Oxygen, a source of life and stress. FEBS Lett 581: 3582-3591.
15. Brahimi-Horn MC, Chiche J, Pouysségur J. 2007. Hypoxia and cancer. J Mol Med 85: 1301-1307.
16. Brooks C, Ketsawatsomkron P, Sui Y, Wang J, Wang CY, Yu FS, Dong Z. 2005. Acidic pH inhibits ATP depletion-induced tubular cell apoptosis by blocking caspase-9 activation in apoptosome. Am J Physiol Renal Physiol 289: F410-F419.
17. + exchanger in metastasis. Nat Rev Cancer 5: 786-795.
18. Casey JR, Grinstein S, Orlowski J. 2010. Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11: 50-61.
19. Chandrashekar J, Yarmolinsky D, Buchholtz LV, Oka Y, Sly W, Ryba NJP, Zuker CS. 2009. The taste of carbonation. Science 326: 443-445.
20. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J. 2000. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289: 625-628.
21. Chen Y, Choong LY, Lin Q, Philp R, Wong CH, Ang BK, Tan YL, Loh MC, Hew CL, Shah N, Druker BJ, Chong PK, Lim YP. 2007. Differential expression of novel tyrosine kinase substrates during breast cancer development. Mol Cell Proteomics 6: 2072-2087.
22. Chiche J, Ilc K, Laferrière J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, Pouyssegur J. 2009. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res 69: 358-368.
23. Chiche J, Brahimi-Horn MC, Pouyssegur J. 2010a. Tumour hypoxia induces a metabolic shift causing acidosis: A common feature in cancer. J Cell Mol Med 14: 771-794.
24. Chiche J, Ilc K, Brahimi-Horn MC, Pouyssegur J. 2010b. Membrane-bound carbonic anhydrases are key pH regulators controlling tumor growth and cell migration. Adv Enzyme Regul 50: 20-33.
25. Cianchi F, Vinci MC, Supuran CT, Peruzzi B, De Giuli P, Fasolis G, Perigli G, Pastorekova S, Papucci L, Pini A, Masini E, Puccetti L. 2010. Selective inhibition of carbonic anhydrase IX decreases cell proliferation and induces ceramide-mediated apoptosis in human cancer cells. J Pharmacol Exp Ther 334: 710-719.
26. Counillon L, Pouyssegur J. 2000. The expanding family of eucaryotic Na(+)/H(+) exchangers. J Biol Chem 275: 1-4.
27. De Milito A, Canese R, Marino ML, 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. 2010. pH-dependent antitumor activity of proton pump inhibitors against human melanoma is mediated by inhibition of tumor acidity. Int J Cancer 127: 207-219.
28. Denker SP, Barber DL. 2002. Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 159: 1087-1096.
29. Di Sario A, Bendia E, Omenetti A, De Minicis S, Marzioni M, Kleemann HW, Candelaresi C, Saccomanno S, Alpini G, Benedetti A. 2007. Selective inhibition of ion transport mechanisms regulating intracellular pH reduces proliferation and induces apoptosis in cholangiocarcinoma cells. Dig Liver Dis 39: 60-69.
30. DiGiammarino EL, Lee AS, Cadwell C, Zhang W, Bothner B, Ribeiro RC, Zambetti G, Kriwacki RW. 2001. A novel mechanism of tumorigenesis involving pH-dependent destabilization of a mutant p53 tetramer. Nat Struct Biol 9: 12-16.
31. Ding JY, Kreipke CW, Speirs SL, Schafer P, Schafer S, Rafols JA. 2009. Hypoxia-inducible factor-1α signaling in aquaporin upregulation after traumatic brain injury. Neurosci Lett 453: 68-72.
32. Echevarría M, Muñoz-Cabello AM, Sánchez-Silva R, Toledo-Aral JJ, López-Barneo J. 2007. Development of cytosolic hypoxia and hypoxia-inducible factor stabilization are facilitated by aquaporin-1 expression. J Biol Chem 282: 30207-30215.
33. Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV, Supuran CT, King LS, Boron WF, Gros G. 2006. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J 20: 1974-1981.
34. Fais S, De Milito A, You H, Qin W. 2007. Targeting vacuolar H+-ATPases as a new strategy against cancer. Cancer Res 67: 10627-10630.
35. Fang JS, Gillies RJ, Gatenby RA. 2008. Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression. Sem Cancer Biol 18: 330-337.
36. Fraisl P, Baes M, Carmeliet P. 2008. Hungry for blood vessels: Linking metabolism and angiogenesis. Dev Cell 14: 313-314.
37. Friedenreich CM, Orenstein MR. 2002. Physical activity and cancer prevention: etiologic evidence and biological mechanisms. J Nutr 132: 3456S-3464S.
38. 1-integrin and its role in cell migration. Am J Physiol Cell Physiol 296: C414-C421.
39. Gatenby RA, Gillies RJ. 2004. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4: 891-899.
40. Gatenby RA, Gillies RJ. 2008. A microenvironmental model of carcinogenesis. Nat Rev Cancer 8: 56-61.
41. Gatenby RA, Vincent TL. 2003. An evolutionary model of carcinogenesis. Cancer Res 63: 6212-6220.
42. Gatenby RA, Gawlinski ET, Gmitro AF, Kaylor B, Gillies R. 2006. Acid-mediated tumor invasion: A multidisciplinary study. Cancer Res 66: 5216-5223.
43. Gatenby RA, Smallbone K, Maini PK, Rose F, Averill J, Nagle RB, Worrall L, Gillies RJ. 2007. Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer. Br J Cancer 97: 646-653.
44. Gillies RJ, Raghunand N, Karczmar GS, Bhujwalla ZM. 2002. MRI of the tumor microenvironment. J Magn Res Imag 16: 430-450.
45. Haapasalo J, Hilvo M, Nordfors K, Haapasalo H, Parkkila S, Hyrskyluoto A, Rantala I, Waheed A, Sly WS, Pastorekova S, Pastorek J, Parkkila A-K. 2008. Identification of an alternatively spliced isoform of carbonic anhydrase XII in diffusely infiltrating astrocytic gliomas. Neuro-Oncology 10: 131-138.
46. Halestrap A, Meredith D. 2004. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 477: 619-628.
47. Halestrap AP, Price NT. 1999. The proton-linked monocarboxylate transporter (MCT) family: Structure, function and regulation. Biochem J 343: 281-299.
48. Harguindey S, Arranz JL, Wahl ML, Orive G, Reshkin SJ. 2009. Proton transport inhibitors as potentially selective anticancer drugs. Anticancer Res 29: 2127-2136.
49. Helmlinger G, Sckell A, Dellian M, Forbes NS, Jain RK. 2002. Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism. Clin Cancer Res 8: 1284-1291.
50. Hsieh MJ, Chen KS, Chiou HL, Hsieh YS. 2010. Carbonic anhydrase XII promotes invasion and migration ability of MDA-MB-231 breast cancer cells through the p38 MAPK signaling pathway. Eur J Cell Biol 89: 598-606.
51. Huber V, De Milito A, Harguindey S, Reshkin SJ, Wahl ML, Rauch C, Chiesi A, Pouyssegur J, Gatenby RA, Rivoltini L, Fais S. 2010. Proton dynamics in cancer. J Transl Med 8: 57.
52. Hulikova A, Zatovicova M, Svastova E, Ditte P, Brasseur R, Kettmann R, Supuran CT, Kopacek J, Pastorek J, Pastorekova S. 2009. Intact intracellular tail is critical for proper functioning of the tumor-associated, hypoxia-regulated carbonic anhydrase IX. FEBS Lett 583: 3563-3568.
53. Hwang JM, Kao SH, Hsieh YH, Li KL, Wang PH, Hsu LS, Liu JY. 2009. Reduction of anion exchanger 2 expression induces apoptosis of human hepatocellular carcinoma cells. Mol Cell Biochem 327: 135-144.
54. Ilie MI, Hofman V, Ortholan C, Ammadi RE, Bonnetaud C, Havet K, Venissac N, Mouroux J, Mazure NM, Pouyssegur J, Hofman P. 2010a. Overexpression of carbonic anhydrase XII in tissues from resectable non-small cell lung cancers is a biomarker of good prognosis. Int J Cancer accepted article online, DOI: 10.1002/ijc.25491.
55. Ilie M, Mazure NM, Hofman V, Ammadi RE, Ortholan C, Bonnetaud C, Havet K, Venissac N, Mograbi B, Mouroux J, Pouyssegur J, Hofman P. 2010b. High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer. Br J Cancer 102: 1627-1635.
56. 2 hydration at acidic pH values characteristic of solid tumors. Bioorg Med Chem Lett 19: 5825-5828.
57. Ivanov SV, Kuzmin I, Wei MH, Pack S, Geil L, Johnson BE, Stanbridge EJ, Lerman MI. 1998. Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von Hippel-Lindau transgenes. Proc Natl Acad Sci USA 95: 12596-12601.
58. Ivanov S, Liao S-Y, Ivanova A, Danilkovitch-Miagkova A, Tarasova N, Weirich G, Merrill MJ, Proescholdt MA, Oldfield EH, Lee J, Zavada J, Waheed A, Sly W, Lerman MI, Stanbridge EJ. 2001. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol 158: 905-919.
59. Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB. 2007. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445: 86-90.
60. Kaluz S, Kaluzová M, Liao SY, Lerman M, Stanbridge EJ. 2009. Transcriptional control of the tumor- and hypoxia-marker carbonic anhydrase 9: A one transcription factor (HIF-1) show? Biochim Biophys Acta 1795: 162-172.
61. Kapoor N, Bartoszewski R, Qadri YJ, Bebok Z, Bubien JK, Fuller CM, Benos DJ. 2009. Knockdown of ASIC1 and epithelial sodium channel subunits inhibits glioblastoma whole cell current and cell migration. J Biol Chem 284: 24526-24541.
62. + exchange activities in renal carcinoma cells. Physiol Genomics 5: 119-128.
63. Kaur C, Sivakumar V, Zhang Y, Ling EA. 2006. Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia 54: 826-839.
64. Kruk J. 2007. Lifetime physical activity and the risk of breast cancer: A case control study. Cancer Detect Prev 31: 18-28.
65. Kumar AP, Quake AL, Chang MKX, Zhou T, Lim KSY, Singh R, Hewitt RE, Salto-Tellez M, Pervaiz S, Clément MV. 2009. Repression of NHE1 expression by PPAR activation is a potential new approach for specific inhibition of the growth of tumor cells in vitro and in vivo. Cancer Res 69: 8636.
66. + antiport activity on tumorigenic potential of hamster lung fibroblasts. J Cell Biochem 36: 249-260.
67. Lauritzen G, Jensen MB, Boedtkjer E, Dybboe R, Aalkjaer C, Nylandsted J, Pedersen SF. 2010. NBCn1 and NHE1 expression and activity in DeltaNErbB2 receptor-expressing MCF-7 breast cancer cells: Contributions to pH(i) regulation and chemotherapy resistance. Exp Cell Res 316: 2538-2553.
68. Li Y, Wang H, Oosterwijk E, Tu C, Shiverick KT, Silverman DN, Frost SC. 2009. Expression and activity of carbonic anhydrase IX Is associated with metabolic dysfunction in MDA-MB-231 breast cancer cells. Cancer Invest 27: 613-623.
69. Lim JH, Park JW, Kim MS, Park SK, Johnson RS, Chun YS. 2006. Bafilomycin induces the p21-mediated growth inhibition of cancer cells under hypoxic conditions by expressing HIF-1α. Mol Pharmacol 70: 1856-1865.
70. Lim JH, Park JW, Kim SJ, Kim MS, Park SK, Johnson RS, Chun YS. 2007. ATP6V0C competes with Von Hippel-Lindau protein in hypoxia-inducible factor 1α (HIF-1α) binding and mediates HIF-1α expression by bafilomycin A1. Mol Pharmacol 71: 942-948.
71. Lingueglia E. 2007. Acid-sensing ion channels in sensory perception. J Biol Chem 282: 17325-17329.
72. Liu CJ, Hwang JM, Wu TT, Hsieh YH, Wu CC, Hsieh YS, Tsai CH, Wu HC, Huang CY, Liu JY. 2008. Anion exchanger inhibitor DIDS induces human poorly-differentiated malignant hepatocellular carcinoma HA22T cell apoptosis. Mol Cell Biochem 308: 117-125.
73. 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. 2005. 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 65: 6843-6849.
74. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM, Seuwen K. 2003. Proton-sensing G-protein-coupled receptors. Nature 425: 93-98.
75. Luo J, Tannock IF. 1994. Inhibition of the regulation of intracellular pH: potential of 5-(N, N-hexamethylene) amiloride in tumour-selective therapy. Br J Cancer 70: 617-624.
76. Mardones P, Medina JF, Elferink RP. 2008. Activation of cyclic AMP signaling in Ae2-deficient mouse fibroblasts. J Biol Chem 283: 12146-12153.
77. +)-ATPases are functionally expressed in plasma membranes of human tumor cells. Am J Physiol 265: C1015-C1029.
78. Mathers CD, Boerma T, Ma Fat D. 2009. Global and regional causes of death. Br Med Bull 92: 7-32.
79. Missner A, Kügler P, Saparov SM, Sommer K, Mathai JC, Zeidel ML, Pohl P. 2008. Carbon dioxide transport through membranes. J Biol Chem 283: 25340-25347.
80. Moellering RE, Black KC, Krishnamurty C, Baggett BK, Stafford P, Rain M, Gatenby RA, Gillies RJ. 2008. Acid treatment of melanoma cells selects for invasive phenotypes. Clin Exp Metastasis 25: 411-425.
81. Mullin JM, Gabello M, Murray LJ, Farrell CP, Bellows J, Wolov KR, Kearney KR, Rudolph D, Thornton JJ. 2009. Proton pump inhibitors: Actions and reactions. Drug Discov Today 14: 647-660.
82. 3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 106: 5406-5411.
83. 2 permeability of Xenopus oocytes. Am J Physiol Cell Physiol 274: C543-C548.
84. Newell KJ, Tannock IF. 1989. Reduction of intracellular pH as a possible mechanism for killing cells in acidic regions of solid tumors: Effects of carbonylcyanide-3-chlorophenylhydrazone. Cancer Res 49: 4477-4482.
85. Newell K, Wood P, Stratford I, Tannock I. 1992. Effects of agents which inhibit the regulation of intracellular pH on murine solid tumours. Br J Cancer 66: 311-317.
86. Newell K, Franchi A, Pouyssegur J, Tannock I. 1993. Studies with glycolysis-deficient cells suggest that production of lactic acid is not the only cause of tumor acidity. Proc Natl Acad Sci USA 90: 1127-1131.
87. Nordfors K, Haapasalo J, Korja M, Niemelä A, Laine J, Parkkila AK, Pastorekova S, Pastorek J, Waheed A, Sly WS, Parkkila S, Haapasalo H. 2010. The tumour-associated carbonic anhydrases CA II, CA IX and CA XII in a group of medulloblastomas and supratentorial primitive neuroectodermal tumours: An association of CA IX with poor prognosis. BMC Cancer 10: 148-158.
88. Ohana E, Yang D, Shcheynikov N, Muallem S. 2009. Diverse transport modes by the solute carrier 26 family of anion transporters. J Physiol 587: 2179-2185.
89. 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. 1998. Bafilomycin A1 induces apoptosis in the human pancreatic cancer cell line Capan-1. J Pathol 185: 324-330.
90. + exchanger 1 by neurotensin signaling in pancreatic cancer cell lines. Biochem Biophys Res Commun 393: 414-419.
91. Pan P, Leppilampi M, Pastorekova S, Pastorek J, Waheed A, Sly WS, Parkkila S. 2006. Carbonic anhydrase gene expression in CA II-deficient (Car2-/-) and CA IX-deficient (Car9-/-) mice.
92. Parkkila AK, Herva R, Parkkila S, Rajaniemi H. 1995. Immunohistochemical demonstration of human carbonic anhydrase isoenzyme II in brain tumours. Histochem J 27: 974-982.
93. Parkkila S, Lasota J, Fletcher JA, Ou W-b, Kivelä AJ, Nuorva K, Parkkila A-K, Ollikainen J, Sly WS, Waheed A, Pastorekova S, Pastorek J, Isola J, Miettinen M. 2010. Carbonic anhydrase II. A novel biomarker for gastrointestinal stromal tumors. Mod Path 23: 743-750.
94. Pérez-Sayáns M, Somoza-Martín JM, Barros-Angueira F, Rey JMG, García-García A. 2009. V-ATPase inhibitors and implication in cancer treatment. Cancer Treat Rev 35: 707-713.
95. + antiport activity in hamster fibroblasts precludes growth at neutral and acidic pH. Proc Natl Acad Sci USA 81: 4833-4837.
96. Pouyssegur J, Franchi A, L'Allemain G, Paris S. 1985. Cytoplasmic pH, a key determinant of growth factor-induced DNA synthesis in quiescent fibroblasts. FEBS Lett 190: 115-119.
97. Pouyssegur J, Franchi A, Pagès G. 2001. pHi, aerobic glycolysis and vascular endothelial growth factor in tumour growth. Novartis Found Symp 240: 186-196; discussion 196-8.
98. Pouyssegur J, Dayan F, Mazure NM. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443.
99. + exchange, motility, and invasion induced by serum deprivation. J Biol Chem 275: 5361-5369.
100. + Exchanger (NHE) NHE Isoform 1 in human breast cancer cells. Clin Cancer Res 9: 2366-2373.
101. Ribeiro RC, Sandrini F, Figueiredo B, Zambetti GP, Michalkiewicz E, Lafferty AR, DeLacerda L, Rabin M, Cadwell C, Sampaio G, Cat I, Stratakis CA, Sandrini R. 2001. An inherited p53 mutation that contributes in a tissue-specific manner to pediatric adrenal cortical carcinoma. Proc Natl Acad Sci USA 98: 9330-9335.
102. + exchanger. Blood 95: 1427-1434.
103. Rios EJ, Fallon M, Wang J, Shimoda LA. 2005. Chronic hypoxia elevates intracellular pH and activates Na+/H+ exchange in pulmonary arterial smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 289: L867-L874.
104. Rite I, Machado A, Cano J, Venero JL. 2008. Intracerebral VEGF injection highly upregulates AQP4 mRNA and protein in the perivascular space and glia limitans externa. Neurochem Int 52: 897-903.
105. Robey IF, Baggett BK, Kirkpatrick ND, Roe DJ, Dosescu J, Sloane BF, Hashim AI, Morse DL, Raghunand N, Gatenby RA, Gillies RJ. 2009. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res 69: 2260-2268.
106. Rofstad EK, Mathiesen B, Kindem K, Galappathi K. 2006. Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res 66: 6699-6707.
107. Roos A, Boron WF. 1981. Intracelluar pH. Physiol Rev 61: 296-434.
108. Rotin D, Wan P, Grinstein S, Tannock I. 1987. Cytotoxicity of compounds that interfere with the regulation of intracellular pH: A potential new class of anticancer drugs. Cancer Res 47: 1497-1504.
109. + exchanger for tumor growth. Cancer Res 49: 205-211.
110. Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS. 2005. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434: 786-792.
111. Schneiderhan W, Scheler M, Holzmann KH, Marx M, Gschwend JE, Bucholz M, Gress TM, Seufferlein T, Adler G, Oswald F. 2009. CD147 silencing inhibits lactate transport and reduces malignant potential of pancreatic cancer cells in in vivo and in vitro models. Gut 58: 1391-1398.
112. +-ATPase in human breast cancer cells with distinct metastatic potential: Distribution and functional activity. Am J Physiol Cell Physiol 286: C1443-C1452.
113. Shen WW, Wu J, Cai L, Liu BY, Gao Y, Chen GQ, Fu GH. 2007. Expression of anion exchanger 1 sequestrates p16 in the cytoplasm in gastric and colonic adenocarcinoma. Neoplasia 9: 812-819.
114. Shimoda LA, Fallon M, Pisarcik S, Wang J, Semenza GL. 2006. HIF-1 regulates hypoxic induction of NHE1 expression and alkalinization of intracellular pH in pulmonary arterial myocytes. Am J Physiol Lung Cell Mol Physiol 291: L941-L949.
115. Silva AS, Yunes JA, Gillies RJ, Gatenby RA. 2009. The potential role of systemic buffers in reducing intratumoral extracellular pH and acid-mediated invasion. Cancer Res 69: 2677-2684.
116. Smallbone K, Maini PK, Gatenby RA. 2010. Episodic, transient systemic acidosis delays evolution of the malignant phenotype: Possible mechanism for cancer prevention by increased physical activity. Biol Direct 5: 22-30.
117. Spugnini EP, Citro G, Fais S. 2010. Proton pump inhibitors as anti vacuolar-ATPases drugs: A novel anticancer strategy. J Exp Clin Cancer Res 29: 44-48.
118. Srivastava J, Barber DL, Jacobson MP. 2007. Intracellular pH sensors: Design principles and functional significance. Physiology 22: 30-39.
119. + exchangers and RhoA regulate acidic extracellular pH-induced lysosome trafficking in prostate cancer cells. Traffic 10: 737-753.
120. Stock C, Schwab A. 2009. Protons make tumor cells move like clockwork. Pflugers Arch 458: 981-992.
121. + exchange. J Physiol 567: 225-238.
122. Stürzbecher HW, Brain R, Addison C, Rudge K, Remm M, Grimaldi M, Keenan E, Jenkins JR. 1992. A C-terminal alpha-helix plus basic region motif is the major structural determinant of p53 tetramerization. Oncogene 7: 1513-1523.
123. Su J, Chen X, Kanekura T. 2009. A CD147-targeting siRNA inhibits the proliferation, invasiveness, and VEGF production of human malignant melanoma cells by down-regulating glycolysis. Cancer Lett 273: 140-147.
124. Supuran CT. 2008. Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators. Nat Rev Drug Disc 7: 168-181.
125. Supuran CT. 2010. Carbonic anhydrase inhibitors. Bioorg Med Chem Lett 20: 3467-3474.
126. Suzuki S, Kojima M, Tokudome S, Mori M, Sakauchi F, Fujino Y, Wakai K, Lin Y, Kikuchi S, Tamakoshi K, Yatsuya H, Tamakoshi A. 2008. Effect of physical activity on breast cancer risk: Findings of the Japan collaborative cohort study. Cancer Epidemiol Biomarkers Prev 17: 3396-3401.
127. Svastova E, Hulikova A, Rafajová M, Zat'ovicová M, Gibadulinová A, Casini A, Cecchi A, Scozzafava A, Supuran CT, Pastorek J, Pastoreková S. 2004. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 577: 439-445.
128. Svastová E, Zilka N, Zat'ovicová M, Gibadulinová A, Ciampor F, Pastorek J, Pastoreková S. 2003. Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with beta-catenin. Exp Cell Res 290: 332-345.
129. Swietach P, Vaughan-Jones RD, Harris AL. 2007. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev 26: 299-310.
130. Swietach P, Wigfield S, Cobden P, Supuran CT, Harris AL, Vaughan-Jones RD. 2008. Tumor-associated carbonic anhydrase 9 spatially co-ordinates intracellular pH in three-dimensional multicellular growths. J Biol Chem 200: 20473-20483.
131. Swietach P, Patiar S, Supuran CT, Harris AL, Vaughan-Jones RD. 2009. The role of carbonic anhydrase 9 in regulating extracellular and intracellular pH in three-dimensional tumor cell growths. J Biol Chem 284: 20299-20310.
132. Townsend PD, Holliday PM, Fenyk S, Hess KC, Gray MA, Hodgson DR, Cann MJ. 2009. Stimulation of mammalian G-protein-responsive adenylyl cyclases by carbon dioxide. J Biol Chem 284: 784-791.
133. Tresguerres M, Buck J, Levin LR. 2010. Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch DOI: 10.1007/s00424-010-0865-6.
134. Türeci O, Sahin U, Vollmar E, Siemer S, Göttert E, Seitz G, Parkkila AK, Shah GN, Grubb JH, Pfreundschuh M, Sly WS. 1998. Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers. Proc Natl Acad Sci USA 95: 7608-7613.
135. Ullah MS, Davies AJ, Halestrap AP. 2006. The plasma membrane lactate transporter MCT4, but not MCT1, is up-regulated by hypoxia through a HIF-1alpha-dependent mechanism. J Biol Chem 281: 9030-9037.
136. + exchangers. Physiol Rev 77: 51-74.
137. Warburg O. 1956. On respiratory impairment in cancer cells. Science 124: 269-270.
138. Watson PH, Chia SK, Wykoff CC, Han C, Leek RD, Sly WS, Gatter KC, Ratcliffe P, Harris AL. 2003. Carbonic anhydrase XII is a marker of good prognosis in invasive breast carcinoma. Br J Cancer 88: 1065-1070.
139. Wong P, Kleemann HW, Tannock IF. 2002. Cytostatic potential of novel agents that inhibit the regulation of intracellular pH. Br J Cancer 87: 238-245.
140. Wong P, Lee C, Tannock IF. 2005. Reduction of intracellular pH as a strategy to enhance the pH-dependent cytotoxic effects of melphalan for human breast cancer cells. Clin Cancer Res 11: 3553-3557.
141. Wu J, Zhang YC, Suo WH, Liu XB, Shen WW, Tian H, Fu GH. 2010. Induction of anion exchanger-1 translation and its opposite roles in the carcinogenesis of gastric cancer cells and differentiation of K562 cells. Oncogene 29: 1987-1996.
142. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL. 2000. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60: 7075-7083.
143. Xu WQ, Song LJ, Liu Q, Zhao L, Zheng L, Yan ZW, Fu GH. 2009. Expression of anion exchanger 1 is associated with tumor progress in human gastric cancer. J Cancer Res Clin Oncol 135: 1323-1330.
144. Yamada H, Yamazaki S, Moriyama N, Hara C, Horita S, Enomoto Y, Kudo A, Kawakami H, Tanaka Y, Fujita T, Sekia G. 2003. Biochem Biophys Res Commun 310: 1213-1218.
145. Yamagata M, Tannock IF. 1996. The chronic administration of drugs that inhibit the regulation of intracellular pH: In vitro and anti-tumour effects. Br J Cancer 73: 1328-1334.
146. Yamagata M, Hasuda K, Stamato T, Tannock IF. 1998. The contribution of lactic acid to acidification of tumours: Studies of variant cells lacking lactate dehydrogenase. Br J Cancer 77: 1726-1731.
147. Yang Y, Wu PP, Wu J, Shen WW, Wu YL, Fu AF, Zheng L, Jin XL, Fu GH. 2008. Expression of anion exchanger 2 in human gastric cancer. Exp Oncol 30: 81-87.
148. Yang X, Wang D, Dong W, Song Z, Dou K. 2010a. Inhibition of Na(+)/H(+) exchanger 1 by 5-(N-ethyl-N-isopropyl) amiloride reduces hypoxia-induced hepatocellular carcinoma invasion and motility. Cancer Lett 295: 198-204.
149. Yang X, Wang D, Dong W, Song Z, Dou K. 2010b. Suppression of Na(+)/H (+) exchanger 1 by RNA interference or amiloride inhibits human hepatoma cell line SMMC-7721 cell invasion. Med Oncol DOI: 10.1007/s12032-010-9447-x.
150. Ye JH, Gao J, Wu YN, Hu YJ, Zhang CP, Xu TL. 2007. Identification of acid-sensing ion channels in adenoid cystic carcinomas. Biochem Biophys Res Commun 355: 986-992.
151. Yoshiura K, Nakaoka T, Nishishita T, Sato K, Yamamoto A, Shimada S, Saida T, Kawakami Y, Takahashi TA, Fukuda H, Imajoh-Ohmi S, Oyaizu N, Yamashita N. 2005. Carbonic anhydrase II is a tumor vessel endothelium-associated antigen targeted by dendritic cell therapy. Clin Cancer Res 11: 8201-8207.