Membrane-bound carbonic anhydrases are key pH regulators controlling tumor growth and cell migration

Advances in Enzyme Regulation

Volumn 50, Issue 1, 2010, Pages 20-33

  Chiche, Johanna ^a   Ilc, Karine ^a   Brahimi Horn, M Christiane ^a   Pouysségur, Jacques ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE INHIBITOR; ISOENZYME;

ANIMAL; ANOXIA; CANCER TRANSPLANTATION; CELL MEMBRANE; CELL MOTION; GENETICS; HUMAN; METABOLISM; MOUSE; NEOPLASM; NUDE MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PH; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; REVIEW; TUMOR CELL LINE;

ANIMALS; ANOXIA; BICARBONATES; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASES; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; HUMANS; HYDROGEN-ION CONCENTRATION; ISOENZYMES; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY;

EID: 77955296520     PISSN: 00652571     EISSN: None     Source Type: Book Series    
DOI: 10.1016/j.advenzreg.2009.10.005     Document Type: Article

References (83)

1. 3- cotransporter. J Biol Chem 2007, 282:13508-13521.
2. Becker H.M., Deitmer J.W. Non-enzymatic proton handling by carbonic anhydrase II during H+-lactate cotransport via monocarboxylate transporter 1. J Biol Chem 2008, 283:21655-21667.
3. Brahimi-Horn M.C., Chiche J., Pouyssegur J. Hypoxia and cancer. J Mol Med 2007, 85:1301-1307.
4. Brahimi-Horn M.C., Chiche J., Pouyssegur J. Hypoxia signalling controls metabolic demand. Curr Opin Cell Biol 2007, 19:223-229.
5. Brahimi-Horn M.C., Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett 2007, 581:3582-3591.
6. Brennan D.J., Jirstrom K., Kronblad A., Millikan R.C., Landberg G., Duffy M.J., et al. CA IX is an independent prognostic marker in premenopausal breast cancer patients with one to three positive lymph nodes and a putative marker of radiation resistance. Clin Cancer Res 2006, 12:6421-6431.
7. Bui M.H., Seligson D., Han K.R., Pantuck A.J., Dorey F.J., Huang Y., et al. Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: implications for prognosis and therapy. Clin Cancer Res 2003, 9:802-811.
8. Chia S.K., Wykoff C.C., Watson P.H., Han C., Leek R.D., Pastorek J., et al. Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J Clin Oncol 2001, 19:3660-3668.
9. Cardone R.A., Casavola V., Reshkin S.J. The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat Rev Cancer 2005, 5:786-795.
10. Chambard J.C., 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, 164:282-294.
11. Chiche J., Ilc K., Laferriere J., Trottier E., Dayan F., Mazure N.M., et al. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res 2009, 69:358-368.
12. Choi S.W., Kim J.Y., Park J.Y., Cha I.H., Kim JLee S. Expression of carbonic anhydrase IX is associated with postoperative recurrence and poor prognosis in surgically treated oral squamous cell carcinoma. Hum Pathol 2008, 39:1317-1322.
13. Couvelard A., O'Toole D., Leek R., Turley H., Sauvanet A., Degott C., et al. Expression of hypoxia-inducible factors is correlated with the presence of a fibrotic focus and angiogenesis in pancreatic ductal adenocarcinomas. Histopathology 2005, 46:668-676.
14. Crabb S.J., Bajdik C.D., Leung S., Speers C.H., Kennecke H., Huntsman D.G., et al. Can clinically relevant prognostic subsets of breast cancer patients with four or more involved axillary lymph nodes be identified through immunohistochemical biomarkers? A tissue microarray feasibility study. Breast Cancer Res 2008, 10:R6.
15. Counillon L., Pouyssegur J. The expanding family of eucaryotic Na(+)/H(+) exchangers. J Biol Chem 2000, 275:1-4.
16. Dayan F., Bilton R.L., Laferriere J., Trottier E., Roux D., Pouyssegur J., et al. Activation of HIF-1alpha in exponentially growing cells via hypoxic stimulation is independent of the Akt/mTOR pathway. J Cell Physiol 2009, 218:167-174.
17. Dorai T., Sawczuk I.S., Pastorek J., Wiernik P.H., Dutcher J.P. The role of carbonic anhydrase IX overexpression in kidney cancer. Eur J Cancer 2005, 41:2935-2947.
18. Gatenby R.A., Gillies R.J. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer 2004, 4:891-899.
19. Giatromanolaki A., Koukourakis M.I., Sivridis E., Pastorek J., Wykoff C.C., Gatter K.C., et al. Expression of hypoxia-inducible carbonic anhydrase-9 relates to angiogenic pathways and independently to poor outcome in non-small cell lung cancer. Cancer Res 2001, 61:7992-7998.
20. Haapasalo J.A., Nordfors K.M., Hilvo M., Rantala I.J., Soini Y., Parkkila A.K., et al. Expression of carbonic anhydrase IX in astrocytic tumors predicts poor prognosis. Clin Cancer Res 2006, 12:473-477.
21. Hedley D., Pintilie M., Woo J., Morrison A., Birle D., Fyles A., et al. Carbonic anhydrase IX expression, hypoxia, and prognosis in patients with uterine cervical carcinomas. Clin Cancer Res 2003, 9:5666-5674.
22. Hilvo M., Baranauskiene L., Salzano A.M., Scaloni A., Matulis D., Innocenti A., et al. Biochemical characterization of CA IX, one of the most active carbonic anhydrase isozymes. J Biol Chem 2008, 283:27799-27809.
23. Hoskin P.J., Sibtain A., Daley FMWilson G.D. GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br J Cancer 2003, 89:1290-1297.
24. Hui E.P., Chan A.T., Pezzella F., Turley H., To K.F., Poon T.C., et al. Coexpression of hypoxia-inducible factors 1alpha and 2alpha, carbonic anhydrase IX, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival. Clin Cancer Res 2002, 8:2595-2604.
25. Hussain S.A., Ganesan R., Reynolds G., Gross L., Stevens A., Pastorek J., et al. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 2007, 96:104-109.
26. Ivanov S., Liao S.Y., Ivanova A., Danilkovitch-Miagkova A., Tarasova N., Weirich G., et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol 2001, 158:905-919.
27. Ivanov S.V., Kuzmin I., Wei M.H., Pack S., Geil L., Johnson B.E., 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, 95:12596-12601.
28. Izumi H., Torigoe T., Ishiguchi H., Uramoto H., Yoshida Y., Tanabe M., et al. Cellular pH regulators: potentially promising molecular targets for cancer chemotherapy. Cancer Treat Rev 2003, 29:541-549.
29. Jonathan R.A., Wijffels K.I., Peeters W., de Wilde P.C., Marres H.A., Merkx M.A., et al. The prognostic value of endogenous hypoxia-related markers for head and neck squamous cell carcinomas treated with ARCON. Radiother Oncol 2006, 79:288-297.
30. Järvelä S., Parkkila S., Bragge H., Kähkönen M., Parkkila A.K., Soini Y., Pastorekova S., Pastorek J., Haapasalo H. Carbonic anhydrase IX in oligodendroglial brain tumors. BMC Cancer 2008, 8:1.
31. Kaluz S., Kaluzova M., Liao S.Y., Lerman M., Stanbridge E.J. Transcriptional control of the tumor- and hypoxia-marker carbonic anhydrase 9: a one transcription factor (HIF-1) show?. Biochim Biophys Acta 2009, 1795:162-172.
32. Kappler M., Taubert H., Holzhausen H.J., Reddemann R., Rot S., Becker A., et al. Immunohistochemical detection of HIF-1alpha and CAIX in advanced head-and-neck cancer. Prognostic role and correlation with tumor markers and tumor oxygenation parameters. Strahlenther Onkol 2008, 184:393-399.
33. 3- exchange and Na+/H+ exchange activities in renal carcinoma cells. Physiol Genom 2001, 5:119-128.
34. Kim S.J., Rabbani Z.N., Vollmer R.T., Schreiber E.G., Oosterwijk E., Dewhirst M.W., et al. Carbonic anhydrase IX in early-stage non-small cell lung cancer. Clin Cancer Res 2004, 10:7925-7933.
35. Klatte T., Seligson D.B., Rao J.Y., Yu H., de Martino M., Kawaoka K., et al. Carbonic anhydrase IX in bladder cancer: a diagnostic, prognostic, and therapeutic molecular marker. Cancer 2009, 115:1448-1458.
36. Korhonen K., Parkkila A.K., Helen P., Valimaki R., Pastorekova S., Pastorek J., et al. Carbonic anhydrases in meningiomas: association of endothelial carbonic anhydrase II with aggressive tumor features. J Neurosurg 2009.
37. Korkeila E., Talvinen K., Jaakkola P.M., Minn H., Syrjanen K., Sundstrom J., et al. Expression of carbonic anhydrase IX suggests poor outcome in rectal cancer. Br J Cancer 2009, 100:874-880.
38. Koukourakis M.I., Giatromanolaki A., Sivridis E., Simopoulos K., Pastorek J., Wykoff C.C., et al. Hypoxia-regulated carbonic anhydrase-9 (CA9) relates to poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy. Clin Cancer Res 2001, 7:3399-3403.
39. 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, 259:5809-5815.
40. Lancashire L.J., Powe D.G., Reis-Filho J.S., Rakha E., Lemetre C., Weigelt B., et al. A validated gene expression profile for detecting clinical outcome in breast cancer using artificial neural networks. Breast Cancer Res Treat 2009.
41. Leibovich B.C., Sheinin Y., Lohse C.M., Thompson R.H., Cheville J.C., Zavada J., et al. Carbonic anhydrase IX is not an independent predictor of outcome for patients with clear cell renal cell carcinoma. J Clin Oncol 2007, 25:4757-4764.
42. Loncaster J.A., Harris A.L., Davidson S.E., Logue J.P., Hunter R.D., Wycoff C.C., et al. Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res 2001, 61:6394-6399.
43. 3 cotransporter NBCe1-A in Xenopus oocytes. J Biol Chem 2006, 281:19241-19250.
44. Mâseide K., Kandel R.A., Bell R.S., Catton C.N., O'Sullivan B., Wunder J.S., et al. Carbonic anhydrase IX as a marker for poor prognosis in soft tissue sarcoma. Clin Cancer Res 2004, 10:4464-4471.
45. Melillo G. Targeting hypoxia cell signaling for cancer therapy. Cancer Metastasis Rev 2007, 26:341-352.
46. Morgan P.E., Pastorekova S., Stuart-Tilley A.K., Alper S.L., Casey J.R. Interactions of transmembrane carbonic anhydrase, CAIX, with bicarbonate transporters. Am J Physiol Cell Physiol 2007, 293:C738-C748.
47. Parkkila S., Rajaniemi H., Parkkila A.-K., Kivelä J., Waheed A., Pastorekova S., et al. Carboninc anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci U S A 2000, 97:2220-2224.
48. Pastorekova S., Zatovicova M., Pastorek J. Cancer-associated carbonic anhydrases and their inhibition. Curr Pharmaceut Des 2008, 14:685-698.
49. Patard J.J., Fergelot P., Karakiewicz P.I., Klatte T., Trinh Q.D., Rioux-Leclercq N., et al. Low CAIX expression and absence of VHL gene mutation are associated with tumor aggressiveness and poor survival of clear cell renal cell carcinoma. Int J Cancer 2008, 123:395-400.
50. Pouyssegur J., Dayan F., Mazure N.M. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006, 441:437-443.
51. Pouyssegur J., Franchi A., Pages G. pHi, aerobic glycolysis and vascular endothelial growth factor in tumour growth. Novartis Foundation Symposium 2001, vol. 240:186-196. John Wiley & Sons, Ltd.
52. 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, 81:4833-4837.
53. Rajaganeshan R., Prasad R., Guillou P.J., Poston G., Scott NJayne D.G. The role of hypoxia in recurrence following resection of Dukes' B colorectal cancer. Int J Colorectal Dis 2008, 23:1049-1055.
54. Rasheed S., Harris A.L., Tekkis P.P., Turley H., Silver A., McDonald P.J., et al. Assessment of microvessel density and carbonic anhydrase-9 (CA-9) expression in rectal cancer. Pathol Res Pract 2009, 205:1-9.
55. Robertson N., Potter C., Harris A.L. Role of carbonic anhydrase IX in human tumor cell growth, survival and invasion. Cancer Res 2004, 64:6160-6165.
56. Rofstad E.K., Mathiesen B., Kindem K., Galappathi K. Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res 2006, 66:6699-6707.
57. Roos A., Boron W.F. Intracellular pH. Physiol Rev 1981, 61:296-434.
58. Sardet C., Franchi A., Pouyssegur J. Molecular cloning, primary structure, and expression of the human growth factor-activatable Na+/H+ antiporter. Cell 1989, 56:271-280.
59. Semenza G.L. Evaluation of HIF-1 inhibitors as anticancer agents. Drug Discov Today 2007, 12:854-857.
60. Sherwood B.T., Colquhoun A.J., Richardson D., Bowman K.J., O'Byrne K.J., Kockelbergh R.C., et al. Carbonic anhydrase IX expression and outcome after radiotherapy for muscle-invasive bladder cancer. Clin Oncol (R Coll Radiol) 2007, 19:777-783.
61. Shimoda L.A., Fallon M., Pisarcik S., Wang J., Semenza G.L. 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-L949.
62. Span P.N., Bussink J., Manders P., Beex LVSweep C.G. Carbonic anhydrase-9 expression levels and prognosis in human breast cancer: association with treatment outcome. Br J Cancer 2003, 89:271-276.
63. Sterling D., Reithmeier R.A.F., Casey J.R. A transport metabolon. Functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers. J Biol Chem 2001, 276:47886-47894.
64. Stock C., Schwab A. Protons make tumor cells move like clockwork. Pflugers Arch 2009.
65. Supuran C.T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008, 7:168-181.
66. Svastova E., Hulikova A., Rafajova M., Zat'ovicova M., Gibadulinova A., Casini A., et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 2004, 577:439-445.
67. Svastova E., Zilka N., Zat'ovicova M., Gibadulinova A., Ciampor F., Pastorek J., et al. Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with beta-catenin. Exp Cell Res 2003, 290:332-345.
68. Swietach P., Patiar S., Supuran C.T., Harris A.L., Vaughan-Jones R.D. The role of carbonic anhydrase 9 in regulating extracellular and intracellular pH in 3-D tumor-cell growths. J Biol Chem 2009.
69. Swietach P., Vaughan-Jones R.D., Harris A.L. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev 2007, 26:299-310.
70. Swietach P., Wigfield S., Cobden P., Supuran C.T., Harris A.L., Vaughan-Jones R.D. Tumor-associated carbonic anhydrase 9 spatially co-ordinates intracellular pH in three-dimensional multicellular growths. J Biol Chem 2008, 283:20473-20483.
71. Swinson D.E., Jones J.L., Richardson D., Wykoff C., Turley H., Pastorek J., et al. Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer. J Clin Oncol 2003, 21:473-482.
72. Tan E.Y., Yan M., Campo L., Han C., Takano E., Turley H., et al. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br J Cancer 2009, 100:405-411.
73. Tanaka N., Kato H., Inose T., Kimura H., Faried A., Sohda M., et al. Expression of carbonic anhydrase 9, a potential intrinsic marker of hypoxia, is associated with poor prognosis in oesophageal squamous cell carcinoma. Br J Cancer 2008, 99:1468-1475.
74. Thiry A., Dogne J.M., Masereel B., Supuran C.T. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 2006, 27:566-573.
75. Trastour C., Benizri E., Ettore F., Ramaioli A., Chamorey E., Pouyssegur J., et al. HIF-1alpha and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. Int J Cancer 2007, 120:1451-1458.
76. Turner J.R., Odze R.D., Crum CPResnick M.B. MN antigen expression in normal, preneoplastic, and neoplastic esophagus: a clinicopathological study of a new cancer-associated biomarker. Hum Pathol 1997, 28:740-744.
77. Ullah M.S., Davies A.J., Halestrap A.P. The plasma membrane lactate transporter MCT4, but not MCT1, is up-regulated by hypoxia through a HIF-1alpha dependent mechanism. J Biol Chem 2006, 281:9030-9037.
78. Walenta S., Mueller-Klieser W.F. Lactate: mirror and motor of tumor malignancy. Semin Radiat Oncol 2004, 14:267-274.
79. Watson P.H., Chia S.K., Wykoff C.C., Han C., Leek R.D., Sly W.S., et al. Carbonic anhydrase XII is a marker of good prognosis in invasive breast carcinoma. Br J Cancer 2003, 88:1065-1070.
80. Wykoff C.C., Beasley N.J., Watson P.H., Turner K.J., Pastorek J., Sibtain A., et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000, 60:7075-7083.
81. Xu Y., Feng L., Jeffrey P.D., Shi Y., Morel F.M. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 2008, 452:56-61.
82. Zavada J., Zavadova Z., Pastorek J., Biesova Z., Jezek J., Velek J. Human tumour-associated cell adhesion protein MN/CA IX: identification of M75 epitope and of the region mediating cell adhesion. Br J Cancer 2000, 82:1808-1813.
83. Zatovicova M., Sedlakova O., Svastova E., Ohradanova A., Ciampor F., Arribas J., et al. Ectodomain shedding of the hypoxia-induced carbonic anhydrase IX is a metalloprotease-dependent process regulated by TACE/ADAM17. Br J Cancer 2005, 93:1267-1276.