Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH

Cancer Research

Volumn 69, Issue 1, 2009, Pages 358-368

  Chiche, Johanna ^a   Ilc, Karine ^a   Laferrière, Julie ^a   Trottier, Eric ^a   Dayan, Frédéric ^a   Mazure, Nathalie M ^a   Brahimi Horn, M Christiane ^a   Pouysségur, Jacques ^a,b  

^a CENTRE DE BIOCHIMIE   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE IX; CARBONATE DEHYDRATASE XII; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTON;

ACIDOSIS; ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER SURVIVAL; CELL HYPOXIA; CELL PH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VOLUME; TUMOR XENOGRAFT;

ACIDOSIS; ANIMALS; ANTIGENS, NEOPLASM; CARBONIC ANHYDRASES; CELL GROWTH PROCESSES; CELL HYPOXIA; CELL LINE, TUMOR; COLONIC NEOPLASMS; CRICETINAE; CRICETULUS; CYTOPLASM; ENZYME INDUCTION; FIBROBLASTS; HUMANS; HYDROGEN-ION CONCENTRATION; MALE; MICE; MICE, NUDE; SPHEROIDS, CELLULAR;

EID: 58249094845     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2470     Document Type: Article

References (50)

1. Pouyssegur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006;441:437-43.
2. Brahimi-Horn MC, Chiche J, Pouyssegur J. Hypoxia signalling controls metabolic demand. Curr Opin Cell Biol 2007;19:223-9.
3. Gullino PM, Clark SH, Grantham FH. The interstitial fluid of solid tumors. Cancer Res 1964;24:780-96.
4. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004;4:891-9.
5. Roos A, Boron WF. Intracelluar pH. Physiol Rev 1981;61:296-434.
6. Pouyssegur J, Sardet C, Franchi A, L'Allemain G, Paris S. A specific mutation abolishing Na+/H+ antiport activity in hamster fibroblasts precludes growth at neutral and acidic pH. Proc Natl Acad Sci U S A 1984;81:4833-7.
7. Chambard JC, Pouyssegur J. Intracellular pH controls growth factor-induced ribosomal protein S6 phosphorylation and protein synthesis in the G0-G1 transition of fibroblasts. Exp Cell Res 1986;164:282-94.
8. Brahimi-Horn MC, Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett 2007;581:3582-91.
9. Sardet C, Franchi A, Pouyssegur J. Molecular cloning, primary structure, and expression of the human growth factor-activatable Na+/H+ antiporter. Cell 1989;56:271-80.
10. Wakabayashi S, Shigekawa M, Pouyssegur J. Molecular physiology of vertebrate Na+/H+ exchangers. Physiol Rev 1997;77:51-74.
11. Cardone RA, Casavola V, Reshkin SJ. The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat Rev Cancer 2005;5:786-95.
12. Shimoda LA, Fallon M, Pisarcik S, Wang J, Semenza GL. HIF-1 regulates hypoxic induction of NHE1 expression and alkalinization of intracellular pH in pulmonary arterial myocytes. Am J Physiol Lung Cell Mol Physiol 2006;291:L941-9.
13. Ullah MS, Davies AJ, Halestrap AP. The plasma membrane lactate transporter MCT4, but not MCT1, is up-regulated by hypoxia through a HIF-1α dependent mechansm. J Biol Chem 2006;281:9030-7.
14. Pouyssegur J, Franchi A, Pages G. pHi, aerobic glycolysis and vascular endothelial growth factor in tumour growth. In: Novartis Found Symp; 2001:John Wiley & Sons, Ltd; 2001. p. 186-96.
15. Alper SL. Molecular physiology of SLC4 anion exchangers. Exp Physiol 2006;91:153-61.
16. - transporters. Pflugers Arch 2004;447:495-509.
17. Izumi H, Torigoe T, Ishiguchi H, et al. Cellular pH regulators: potentially promising molecular targets for cancer chemotherapy. Cancer Treat Rev 2003;29:541-459.
18. Ivanov S, Liao SY, Ivanova A, et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases inhuman cancer.AmJ Pathol 2001;158:905-19.
19. Swietach P, Vaughan-Jones RD, Harris AL. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev 2007;26:299-310.
20. Thiry A, Dogne JM, Masereel B, Supuran CT. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 2006;27:566-73.
21. Ivanov SV, Kuzmin I, Wei MH, et al. Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von Hippel-Lindau transgenes. Proc Natl Acad Sci U S A 1998;95:12596-601.
22. Wykoff CC, Beasley NJ, Watson PH, et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000;60:7075-83.
23. Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168-81.
24. Pastorekova S, Zatovicova M, Pastorek J. Cancer-associated carbonic anhydrases and their inhibition. Curr Pharm Des 2008;14:685-98.
25. Whittington DA, Waheed A, Ulmasov B, et al. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proc Natl Acad Sci U S A 2001;98:9545-50.
26. Dayan F, Roux D, Brahimi-Horn MC, Pouyssegur J, Mazure NM. The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1α. Cancer Res 2006;66:3688-98.
27. Hussain SA, Ganesan R, Reynolds G, et al. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 2007;96:104-9.
28. Zavada J, Zavadova Z, Pastorek J, Biesova Z, Jezek J, Velek J. Human tumour-associated cell adhesion protein MN/CA IX: identification of M75epitope and of the region mediating cell adhesion. Br J Cancer 2000;82:1808-13.
29. Svastova E, Zilka N, Zat'ovicova M, et al. Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with β-catenin. Exp Cell Res 2003;290:332-45.
30. Dorai T, Sawczuk IS, Pastorek J, Wiernik PH, Dutcher JP. The role of carbonic anhydrase IX overexpression in kidney cancer. Eur J Cancer 2005;41:2935-47.
31. Svastova E, Hulikova A, Rafajova M, et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 2004;577:439-45.
32. Swietach P, Wigfield S, Cobden P, Supuran CT, Harris AL, Vaughan-Jones RD. Tumor-associated carbonic anhydrase 9 spatially co-ordinates intracellular pH in three-dimensional multicellular growths. J Biol Chem 2008;283:20473-83.
33. van de Wetering M, Oving I, Muncan V, et al. Specific inhibition of gene expression using a stably integrated, inducible small-interfering-RNA vector. EMBO Rep 2003;4:609-15.
34. Trastour C, Benizri E, Ettore F, et al. HIF-1α and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. Int J Cancer 2007;120:1451-8.
35. L'Allemain G, Paris S, Pouyssegur J. Growth factor action and intracellular pH regulation in fibroblasts. Evidence for a major role of the Na+/H+ antiport. J Biol Chem 1984;259:5809-15.
36. Cardone RA, Bellizzi A, Busco G, et al. The NHERF1 PDZ2 Domain Regulates PKA-RhoA-p38-mediated NHE1 Activation and Invasion in Breast Tumor Cells. Mol Biol Cell 2007;18:1768-80.
37. Counillon L, Pouyssegur J. The expanding family of eucaryotic Na(+)/H(+) exchangers. J Biol Chem 2000;275:1-4.
38. - exchange and Na+/H+ exchange activities in renal carcinoma cells. Physiol Genomics 2001;5:119-28.
39. Pouyssegur J, Franchi A, L'Allemain G, Paris S. Cytoplasmic pH, a key determinant of growth factor-induced DNA synthesis in quiescent fibroblasts. FEBS Lett 1985;190:115-9.
40. Sterling D, Reithmeier RAF, Casey JR. A transport metabolon. Functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers. J Biol Chem 2001;276:47886-94.
41. - cotransporter. J Biol Chem 2007;282:13508-21.
42. Becker HM, Deitmer JW. Non-enzymatic proton handling by carbonic anhydrase II during H+-lactate cotransport via monocarboxylate transporter 1. J Biol Chem 2008;283:21655-67.
43. Lu J, Daly CM, Parker MD, et al. Effect of human carbonic anhydrase II on the activity of the human electogenic Na/HCO3 cotransporter NBCe1-A in Xenopus Oocytes. J Biol Chem 2006;281:19241-50.
44. Morgan PE, Pastorekova S, Stuart-Tilley AK, Alper SL, Casey JR. Interactions of transmembrane carbonic anhydrase, CAIX, with bicarbonate transporters. Am J Physiol Cell Physiol 2007;293:C738-48.
45. Walenta S, Mueller-Klieser WF. Lactate: mirror and motor of tumor malignancy. Semin Radiat Oncol 2004;14:267-74.
46. 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;66:6699-707.
47. Parkkila S, Rajaniemi H, Parkkila A-K, et al. Carboninc anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci U S A 2000;97:2220-4.
48. Robertson N, Potter C, Harris AL. Role of carbonic anhydrase IX in human tumor cell growth, survival and invasion. Cancer Res 2004;64:6160-5.
49. Melillo G. Targeting hypoxia cell signaling for cancer therapy. Cancer Metastasis Rev 2007;26:341-52.
50. Semenza GL. Evaluation of HIF-1 inhibitors as anticancer agents. Drug Discov Today 2007;12:854-7.