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ORIGINAL ARTICLES Cellular and Molecular Biology

Expression and Activity of Carbonic Anhydrase IX Is Associated With Metabolic Dysfunction in MDA-MB-231 Breast Cancer Cells

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Pages 613-623 | Published online: 20 Jul 2009

REFERENCES

  • Dang C. V., Semenza G. L. Oncogenic alterations of metabolism. Trends Biochem. Sci. 1999; 24: 68–69
  • Cairns R., Papandreou I., Denko N. Overcoming physiologic barriers to cancer treatment by molecularly targeting the tumor microenvironment. Mol Cancer Res. 2006; 4: 61–70
  • Warburg O. On the origin of cancer cells. Science 1956; 123: 309–314
  • Younes M., Brown R. W., Mody D. R., Fernandez L., Laucirica R. GLUT1 expression in human breast carcinoma: correlation with known prognostic markers. Anticancer Res. 1995; 15: 2895–2898
  • Younes M., Lechago L. V., Somoano J. R., Mosharaf M., Lechago J. Wide expression of the human erythrocyte glucose transporter GLUT1 in human cancers. Cancer Res. 1996; 56: 1164–1167
  • Brown R., Wahl R. L. Overexpression of Glut-1 glucose transporter in human breast cancer: an immunohistolochemical study. Cancer 1993; 72: 2979–2985
  • Koukourakis M. I., Giatromanolaki A., Harris A. L., Sivridis E. Comparison of metabolic pathways in cancer cells and stromal cells in colorectal cancer: a metabolic survival role for tumor-associated stroma. Cancer Res. 2006; 66: 623–627
  • Sennoune S. R., Bakunts K., Martinez G. M., Chua-Tuan J. L., Kebir Y., Attaya M. N., Martinez-Zaguilan R. Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am J Physiol. 2004; 286: C1443–C1452
  • Stockwin L. H., Blonder J., Bumke M. A., Lucas D. A., Chan K. C., Conrads T. P., Issaq H. J., Veenstra T. D., Newton D. L., Rybak S. M. Proteomic analysis of plasma membrane from hypoxia-adapted malignant melanoma. J Proteome Res. 2006; 5: 2996–3007
  • McLean L. A., Roscoe J., Jorgensen N. K., Gorin F. A., Cala P. M. Malignant gliomas display altered pH regulation by NHE1 compared to nontransformed astrocytes. Am J Physiol. 2000; 278: C676–C688
  • Stubbs M., McSheehy P. M.J., Griffiths J. R., Bashford C. L. Causes and consequences of tumour acidity and implications for treatment. Mol Med Today 2000; 6: 15–19
  • Yamagata M., Hasuda K., Stamato T., Tannock I. F. The contribution of lactic acid to acidification of tumours: studies of variant cells lacking lactate dehydrogenase. Br J Cancer 1998; 77: 1726–1731
  • Helmlinger G., Sckell A., Dellian M., Forbes N. S., Jain R. K. Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism. Clin Cancer Res. 2002; 8: 1284–1291
  • Pastorek J., Pastoreková S., Callebaut I., Mornon J. P., Zelník V., Opavsky R., Zat'ovicová M., Liao S., Portetelle D., Stanbridge E. J., Závada J., Burny A., Kettmann R. Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix–loop–helix DNA binding segment. Oncogene 1994; 9: 2877–2888
  • Pastorekova S., Parkkila S., Parkkila A., Opavsky R., Zelnik V., Saarnio J., Pastorek J. Carbonic anhydrase IX, MN/CAIX: analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts. Gastroenterology 1997; 112: 398–408
  • Saarnio J., Parkkila S., Parkkila A.-K., Waheed A., Casey M. C., Zhou X. Y., Pastoreková S., Pastorek J., Karttunen T., Haukipuro K., Kairaluoma M. I., Sly W. S. Immunohistochemistry of carbonic anhydrase isozyme IX (MN/CA IX) in human gut reveals polarized expression in epithelial cells with the highest proliferative capacity. J Histochem Cytochem. 1998; 46: 497–504
  • Loncaster J. A., Harris A. L., Davidson S. E., Logue J. P., Hunter R. D., Wykoff C. C., Pastorek J., Ratcliffe P. J., Stratford I. J., West C. M.L. Carbonic anhydrase (CAIX) 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
  • Wykoff C. C., Beasley N. J.P., Watson P. H., Turner K. J., Pastorek J., Sibtain A., Wilson G. D., Turley H., Talks K. L., Maxwell P. H., Pugh C. W., Ratcliffe P. J., Harris A. L. Hypoxia-inducible expression of tumor-associated carbonic anhydrase. Cancer Res. 2000; 60: 7075–7083
  • Potter C., Harris A. L. Hypoxia inducible carbonic anhydrase IX, marker of tumor hypoxia, survival pathway and therapy target. Cell Cycle 2004; 3: 164–167
  • Wingo T., Tu C., Laipis P. J., Silverman D. N. The catalytic properties of human carbonic anhydrase IX. Biochem Biophys Res Comm. 2001; 288: 666–669
  • Supuran C. T., Briganti F., Tilli S., Chegwidden W. R., Scozzafava A. Carbonic anhydrase inhibitors: sulfonamides as antitumor agents?. Bioorg Med Chem. 2001; 9: 703–714
  • 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
  • Lacroix M., Leclercq G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat. 2004; 83: 249–289
  • Engel L. W., Young N. A. Human breast carcinoma cells in continuous culture: a review. Cancer Res. 1978; 38: 4327–4339
  • Neve R. M., Chin K., Fridlyand J., Yeh J., Baehner F. L., Fevr T., Clark L., Bayani N., Coppe J., Tong F., Speed T., Spellman P. T., DeVries S., Lapuk A., Wang N. J., Kuo W., Stilwell J. L., Pinkel D., Albertson D. G., Waldman F. M., McCormick F., Dickson R. B., Johnson M. D., Lippman M., Ethier S., Gazdar A., Gray J. W. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10: 515–527
  • Hussain S. A., Ganesan R., Reynolds G., Gross L., Stevens A., Pastorek J., Murray P. G., Perunovic B., Anwar M. S., Billingham L., James N. D., Spooner D., Poole C. J., Rea D. W., Palmer D. H. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 2007; 96: 104–109
  • Markwell M. A.K., Haas S. M., Lieber L. L., Tolbert N. E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem. 1978; 87: 206–210
  • Fisher M. D., Frost S. C. Translocation of GLUT1 does not account for elevated glucose transport in glucose-deprived 3T3-L1 adipocytes. J Biol Chem. 1996; 271: 11806–11809
  • Balch W. E., Rothman J. E. Characterization of protein transport between successive compartments of the Golgi apparatus: asymmetric properties of donor and acceptor activities in a cell-free system. Arch Biochem Biophys. 1985; 240: 413–425
  • Weber T. M., Joost H. G., Simpson I. A., Cushman S. W. Methods for assessment of glucose transport activity and the number of glucose transporters in isolated rat adipose cells and membrane fractions, in Receptor Biochemistry and Methodology (The Insulin Receptor). R.C. Kahn, L.C. Harrison. Alan R. Liss, New York 1988; 171–187
  • Wingo T., Tu C., Laipis P. J., Silverman D. N. The catalytic properties of human carbonic anhydrase IX. Biochem Biophys Res Comm. 2001; 288: 666–669
  • Kitzman H. H., Jr., McMahon R. J., Williams M. G., Frost S. C. Effect of glucose deprivation on GLUT1 expression in 3T3-L1 adipocytes. J Biol Chem. 1993; 268: 1320–1325
  • Kitzman H. H., Jr., McMahon R. J., Aslanian A. M., Fadia P. M., Frost S. C. Differential regulation of GRP78 and GLUT1 expression in 3T3-L1 adipocytes. Mol Cell Biochem. 1996; 162: 51–58
  • 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
  • Vince J. W., Reithmeier R. A.F. Carbonic anhydrase II binds to the carboxyl-terminus of human band 3, the erythrocyte Cl−/HCO−3 exchanger. J Biol Chem. 1998; 273: 28430–28437
  • Conroy C. W., Wynns G. C., Maren T. H. Synthesis and properties of two new membrane-impermeant high-molecular-weight carbonic anhydrase inhibitors. Bioorg Chem. 1996; 24: 262–272
  • Helmlinger G., Yuan F., Dellian M., Jain R. K. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal lack of correlation. Nat Med. 1997; 3: 177–182
  • Brizel D. M., Scully S. P., Harrelson J. M., Layfield L. J., Bean J. M., Prosnitz L. R., Dewhirst M. W. Tumour oxygenation predicts for likelihood of distant metastases in human soft tissue sarcoma. Cancer Res. 1996; 56: 941–943
  • Graeber T. G., Osmanian C., Jacks T., Housman D. E., Koch C. J., Lowe S. W., Giaccia A. J. Hypoxia-mediated selection of cells with diminshed apoptotic potential in solid tumours. Nature 1996; 379: 88–91
  • Hockel M., Schlenger K., Mitze M., Schaffer U., Vaupel P. Hypoxia and radiation response in human tumors. Semin Radiat Oncol. 1996; 6: 3–9
  • Kim C. Y., Tsai M. H., Osmanian C., Graeber T. G., Lee J. E., Giffard R. G., DiPaolo J. A., Peehl D. M., Giaccia A. J. Selection of human cervical epithelial cells that possess reduced apoptotic potenial to low-oxygen conditions. Cancer Res. 1997; 57: 4200–4204
  • Hussain S. A., Ganesan R., Reynolds G., Gross L., Stevens A., Pastorek J., Murray P. G., Perunovic B., Anwar M. S., Billingham L., James N. D., Spooner D., Poole C. J., Rea D. W., Palmer D. H. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 2007; 96: 104–109
  • Cecchi A., Hulikova A., Pastorek J., Pastorekova S., Scozzafava A., Winum J.-Y., Montero J.-L., Supuran C. T. Carbonic anhydrase inhibitors: design of fluorescent sulfonamides as probes of tumor-associated carbonic anhydrase IX that inhibit isozyme IX-mediated acidification of hypoxic tumors. J Med Chem. 2005; 48: 4841
  • Svastova E., HulÍková A., Rafajová M., Zat'ovicová M., Gibadulinová A., Casini A., Cecchi A., Scozzafava A., Supuran C. T., Pastorek J., Pastoreková S. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett. 2004; 577: 439–445
  • Parkkila S., Rajaniemi H., Parkkila A., Kivela J., Waheed A., Pastorekova S., Pastorek J., Sly W. S. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Nat Acad Sci USA 2000; 97: 2220–2224
  • Gatenby R. A., Gillies R. J. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer 2004; 4: 891–899
  • Gatenby R. A., Gawlinski E. T., Gmitro A. F., Kaylor B., Gillies R. J. Acid-mediated tumor invasion: a multidisplinary study. Cancer Res. 2006; 66: 5216–5223
  • Sterling D., Brown N. J.D., Supuran C. T., Casey J. R. The functional and physical relationship between the DRA bicarbonate transporter and carbonic anhydrase II. Am J Physiol. 2002; 283: C1522–C1529
  • Sterling D., Alvarez B. V., Casey J. R. The extracellular component of a transport metabolon: extracellular loop 4 of the human AE1 Cl−/HCO−3 exchanger binds carbonic anhydrase IV. J Biol Chem. 2002; 277: 25239–25246
  • Potter C., Harris A. L. Hypoxia inducible carbonic anhydrase IX, marker of tumor hypoxia, survival pathway and therapy target. Cell Cycle 2004; 3: 164–167
  • Ivanov S., Liao S.-Y., Ivanova A., Danilkovitch-Miagkova A., Tarasova N., Weirich G., Merrill M. J., Proescholdt M. A., Oldfield E. H., Lee J., Zavada J., Waheed A., Sly W., Lerman M. I., Stanbridge E. J. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol. 2001; 158: 905–919
  • Rafajova M., Zatovicova M., Kettmann R., Pastorek J., Pastorekova S. Induction by hypoxia combined with low glucose or low bicarbonate and high posttranslational stability upon reoxygenation contribute to carbonic anhydrase IX expression in cancer cells. Int J Oncol. 2004; 24: 995–1004
  • Kaluzová M., Kaluz S., Lerman M. I., Stanbridge E. J. DNA damage is a prerequisite for p53-mediated proteasomal degradation of HIF-1α in hypoxic cells and downregulation of the hypoxia marker carbonic anhydrase IX. Mol Cell Biol. 2004; 24: 5757–5766
  • Ideker T., Thorsson V., Ranish J. A., Christmas R., Buhler J., Eng J. K., Bumgarner R., Goodlett D. R., Aebersold R., Hood L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 2001; 292: 929–934
  • Barnett D. H., Sheng S., Charn T. H., Waheed A., Sly W. S., Lin C.-Y., Liu E. T., Katzenellenbogen B. S. Estrogen receptor regulation of carboinc anhydrase XII through a distal enhancer in breast cancer. Cancer Res. 2008; 68: 3505–3515
  • Ivanov S., Liao S.-Y., Ivanova A., Danilkovitch-Miagkova A., Tarasova N., Weirich G., Merrill M. J., Proescholdt M. A., Oldfield E. H., Lee J., Zavada J., Waheed A., Sly W., Lerman M. I., Stanbridge E. J. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol. 2001; 158: 905–919

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