1,528
Views
72
CrossRef citations to date
0
Altmetric
Research Article

Inhibition of carbonic anhydrase activity modifies the toxicity of doxorubicin and melphalan in tumour cells in vitro

, , , , , & show all
Pages 360-369 | Received 29 Aug 2012, Accepted 02 Oct 2012, Published online: 19 Nov 2012

References

  • Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011;473:298–307.
  • Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989;49:6449–6465.
  • Brown JM, Giaccia AJ. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res 1998;58:1408–1416.
  • Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996;379:88–91.
  • Semenza GL. HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 2001;107:1–3.
  • Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 2002;64:993–998.
  • Erler JT, Bennewith KL, Nicolau M, Dornhöfer N, Kong C, Le QT et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006;440:1222–1226.
  • Brown JM. The hypoxic cell: a target for selective cancer therapy–eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res 1999;59:5863–5870.
  • Goonewardene TI, Sowter HM, Harris AL. Hypoxia-induced pathways in breast cancer. Microsc Res Tech 2002;59:41–48.
  • Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996;56:4509–4515.
  • Höckel M, Schlenger K, Höckel S, Vaupel P. Hypoxic cervical cancers with low apoptotic index are highly aggressive. Cancer Res 1999;59:4525–4528.
  • Kim CY, Tsai MH, Osmanian C, Graeber TG, Lee JE, Giffard RG et al. Selection of human cervical epithelial cells that possess reduced apoptotic potential to low-oxygen conditions. Cancer Res 1997;57:4200–4204.
  • Brizel DM, Scully SP, Harrelson JM, Layfield LJ, Bean JM, Prosnitz LR et al. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res 1996;56:941–943.
  • Chegwidden WR, Dodgson SJ, Spencer IM. The roles of carbonic anhydrase in metabolism, cell growth and cancer in animals. EXS 2000:343–363.
  • Ivanov S, Liao SY, 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.
  • Potter CP, Harris AL. Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer. Br J Cancer 2003;89:2–7.
  • Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000;60:7075–7083.
  • Svastová E, Hulíková A, Rafajová M, Zat’ovicová M, Gibadulinová 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.
  • Beasley NJ, Wykoff CC, Watson PH, Leek R, Turley H, Gatter K et al. Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density. Cancer Res 2001;61:5262–5267.
  • Loncaster JA, Harris AL, Davidson SE, Logue JP, Hunter RD, Wycoff CC 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.
  • Olive PL, Aquino-Parsons C, MacPhail SH, Liao SY, Raleigh JA, Lerman MI et al. Carbonic anhydrase 9 as an endogenous marker for hypoxic cells in cervical cancer. Cancer Res 2001;61:8924–8929.
  • Airley RE, Loncaster J, Raleigh JA, Harris AL, Davidson SE, Hunter RD et al. GLUT-1 and CAIX as intrinsic markers of hypoxia in carcinoma of the cervix: relationship to pimonidazole binding. Int J Cancer 2003;104:85–91.
  • Hoskin PJ, Sibtain A, Daley FM, Wilson GD. 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.
  • Wike-Hooley JL, van den Berg AP, van der Zee J, Reinhold HS. Human tumour pH and its variation. Eur J Cancer Clin Oncol 1985;21:785–791.
  • Stubbs M, Rodrigues L, Howe FA, Wang J, Jeong KS, Veech RL et al. Metabolic consequences of a reversed pH gradient in rat tumors. Cancer Res 1994;54:4011–4016.
  • Li Y, Tu C, Wang H, Silverman DN, Frost SC. Catalysis and pH control by membrane-associated carbonic anhydrase IX in MDA-MB-231 breast cancer cells. J Biol Chem 2011;286:15789–15796.
  • Chiche J, Ilc K, Laferrière J, Trottier E, Dayan F, Mazure NM 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.
  • Parks SK, Chiche J, Pouyssegur J. pH control mechanisms of tumor survival and growth. J Cell Physiol 2011;226:299–308.
  • Ojugo AS, McSheehy PM, Stubbs M, Alder G, Bashford CL, Maxwell RJ et al. Influence of pH on the uptake of 5-fluorouracil into isolated tumour cells. Br J Cancer 1998;77:873–879.
  • Mahoney BP, Raghunand N, Baggett B, Gillies RJ. Tumour acidity, ion trapping and chemotherapeutics I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol 2003;66:1207–1218.
  • Supuran CT. Inhibition of carbonic anhydrase IX as a novel anticancer mechanism. World J Clin Oncol 2012;3:98–103.
  • McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012;3:84–97.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–181.
  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–777.
  • Stillebroer AB, Mulders PF, Boerman OC, Oyen WJ, Oosterwijk E. Carbonic anhydrase IX in renal cell carcinoma: implications for prognosis, diagnosis, and therapy. Eur Urol 2010;58:75–83.
  • Wood PJ, Sansom JM, Newell K, Tannock IF, Stratford IJ. Reduction of tumour intracellular pH and enhancement of melphalan cytotoxicity by the ionophore Nigericin. Int J Cancer 1995;60:264–268.
  • Robertson N, Potter C, Harris AL. Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res 2004;64:6160–6165.
  • Wilbur KM, Anderson NG. Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 1948;176:147–154.
  • Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 1968;25:192–205.
  • Truppo E, Supuran CT, Sandomenico A, Vullo D, Innocenti A, Di Fiore A et al. Carbonic anhydrase VII is S-glutathionylated without loss of catalytic activity and affinity for sulfonamide inhibitors. Bioorg Med Chem Lett 2012;22:1560–1564.
  • Giatromanolaki A, Koukourakis MI, Sivridis E, Pastorek J, Wykoff CC, Gatter KC 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.
  • Kivela AJ, Saarnio J, Karttunen TJ, Kivelä J, Parkkila AK, Pastorekova S et al. Differential expression of cytoplasmic carbonic anhydrases, CA I and II, and membrane-associated isozymes, CA IX and XII, in normal mucosa of large intestine and in colorectal tumors. Dig Dis Sci 2001;46:2179–2186.
  • Bartosová M, Parkkila S, Pohlodek K, Karttunen TJ, Galbavý S, Mucha V et al. Expression of carbonic anhydrase IX in breast is associated with malignant tissues and is related to overexpression of c-erbB2. J Pathol 2002;197:314–321.
  • Kaluz S, Kaluzová M, Stanbridge EJ. Expression of the hypoxia marker carbonic anhydrase IX is critically dependent on SP1 activity. Identification of a novel type of hypoxia-responsive enhancer. Cancer Res 2003;63:917–922.
  • Wingo T, Tu C, Laipis PJ, Silverman DN. The catalytic properties of human carbonic anhydrase IX. Biochem Biophys Res Commun 2001;288:666–669.
  • Supuran CT, Scozzafava A. Carbonic anhydrase inhibitors–Part 94. 1,3,4-thiadiazole-2-sulfonamidederivatives as antitumor agents? Eur J Med Chem 2000;35:867–874.
  • Turkmen H, Durgun M, Yilmaztekin S, Emul M, Innocenti A, Vullo D et al. Carbonic anhydrase inhibitors. Novel sulfanilamide/acetazolamide derivatives obtained by the tail approach and their interaction with the cytosolic isozymes I and II, and the tumor-associated isozyme IX. Bioorg Med Chem Lett 2005;15:367–372.
  • Parkkila S, Rajaniemi H, Parkkila AK, Kivela J, Waheed A, Pastorekova S et al. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci USA 2000;97:2220–2224.
  • Whittington DA, Waheed A, Ulmasov B, Shah GN, Grubb JH, Sly WS 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 USA 2001;98:9545–9550.
  • Pacchiano F, Carta F, McDonald PC, Lou Y, Vullo D, Scozzafava A et al. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem 2011;54:1896–1902.
  • Lou Y, McDonald PC, Oloumi A, Chia S, Ostlund C, Ahmadi A et al. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res 2011;71:3364–3376.
  • Jähde E, Glüsenkamp KH, Rajewsky MF. Increased drug cytotoxicity at reduced pH counteracts cyclophosphamide resistance in cultured rat mammary carcinoma cells. Int J Cancer 1989;44:1082–1087.
  • Matthews NE, Adams MA, Maxwell LR, Gofton TE, Graham CH. Nitric oxide-mediated regulation of chemosensitivity in cancer cells. J Natl Cancer Inst 2001;93:1879–1885.
  • Kennedy KA, Siegfried JM, Sartorelli AC, Tritton TR. Effects of anthracyclines on oxygenated and hypoxic tumor cells. Cancer Res 1983;43:54–59.
  • Potmesil M, Kirschenbaum S, Israel M, Levin M, Khetarpal VK, Silber R. Relationship of adriamycin concentrations to the DNA lesions induced in hypoxic and euoxic L1210 cells. Cancer Res 1983;43:3528–3533.
  • Atema A, Buurman KJ, Noteboom E, Smets LA. Potentiation of DNA-adduct formation and cytotoxicity of platinum-containing drugs by low pH. Int J Cancer 1993;54:166–172.
  • Swietach P, Hulikova A, Patiar S, Vaughan-Jones RD, Harris AL. Importance of intracellular pH in determining the uptake and efficacy of the weakly basic chemotherapeutic drug, doxorubicin. PLoS ONE 2012;7:e35949.
  • Chen G, Waxman DJ. Role of cellular glutathione and glutathione S-transferase in the expression of alkylating agent cytotoxicity in human breast cancer cells. Biochem Pharmacol 1994;47:1079–1087.
  • Teicher BA, Liu SD, Liu JT, Holden SA, Herman TS. A carbonic anhydrase inhibitor as a potential modulator of cancer therapies. Anticancer Res 1993;13:1549–1556.
  • Goossens JF, Hénichart JP, Dassonneville L, Facompré M, Bailly C. Relation between intracellular acidification and camptothecin-induced apoptosis in leukemia cells. Eur J Pharm Sci 2000;10:125–131.
  • Tannock IF, Rotin D. Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res 1989;49:4373–4384.
  • Gieling RG, Babur M, Mamnani L, Burrows N, Telfer BA, Carta F et al. Antimetastatic effect of sulfamate carbonic anhydrase IX inhibitors in breast carcinoma xenografts. J Med Chem 2012;55:5591–5600.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.