Selective inhibition of carbonic anhydrase IX decreases cell proliferation and induces ceramide-mediated apoptosis in human cancer cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 334, Issue 3, 2010, Pages 710-719

  Cianchi, Fabio ^a   Vinci, Maria Cristina ^a   Supuran, Claudiu T ^a   Peruzzi, Benedetta ^b   De Giuli, Paolo ^c   Fasolis, Giuseppe ^c   Perigli, Giuliano ^a   Pastorekova, Silvia ^d   Papucci, Laura ^a,c   Pini, Alessandro ^a   Masini, Emanuela ^a   Puccetti, Luca ^a,c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b ISTITUTO TOSCANO TUMORI   (Italy)

^c San Lazzaro Hospital   (Italy)

^d INSTITUTE OF VIROLOGY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 SULFAMOYLPHENYLAMINO) 4,6 DICHLORO 1,3,5 TRIAZINE; 4 [3 (N,N DIMETHYLAMINOPROPYL)THIOREIDOPHENYLSULFONYLAMINOETHYL]BENZENESULFONAMIDE; ACETAZOLAMIDE; CARBONATE DEHYDRATASE IX; CASPASE 3; CERAMIDE; FUMONISIN B1; GA 15; MITOGEN ACTIVATED PROTEIN KINASE P38; SULFONAMIDE; TR 1; UNCLASSIFIED DRUG; 3-NITROTYROSINE; CA9 PROTEIN, HUMAN; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE INHIBITOR; CARBONATE DEHYDRATASE IV; TUMOR ANTIGEN; TYROSINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL PH; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL SURVIVAL; DRUG EFFECTS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; METABOLISM; NEOPLASM; PATHOLOGY; PH; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ACETAZOLAMIDE; ANTIGENS, NEOPLASM; APOPTOSIS; BLOTTING, WESTERN; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASE IV; CARBONIC ANHYDRASES; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CERAMIDES; FLOW CYTOMETRY; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; NEOPLASMS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TYROSINE;

EID: 77956253534     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.110.167270     Document Type: Article

References (32)

1. Ahlskog JK, Dumelin CE, Trüssel S, Mårlind J, and Neri D (2009) In vivo targeting of tumor-associated carbonic anhydrases using acetazolamide derivatives. Bioorg Med Chem Lett 19:4851-4856.
2. Barrier L, Ingrand S, Piriou A, Touzalin A, and Fauconneau B (2005) Lactic acidosis stimulates ganglioside and ceramide generation without sphingomyelin hydrolysis in rat cortical astrocytes. Neurosci Lett 385:224-229. (Pubitemid 40980405)
3. Bond J and Varley J (2005) Use of flow cytometry and SNARF to calibrate and measure intracellular pH in NS0 cells. Cytometry A 64:43-50. (Pubitemid 40315707)
4. Chen CL, Lin CF, Chang WT, Huang WC, Teng CF, and Lin YS (2008) Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin- interacting protein-mediated pathway. Blood 111:4365-4374.
5. Chia SK, Wykoff CC, Watson PH, Han C, Leek RD, Pastorek J, Gatter KC, Ratcliffe P, and Harris AL (2001) Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J Clin Oncol 19:3660-3668. (Pubitemid 32786278)
6. Chiche J, Ilc K, Brahimi-Horn MC, and Pouysségur J (2010) Membrane-bound carbonic anhydrases are key pH regulators controlling tumor growth and cell migration. Adv Enzyme Regul 50:20-33.
7. Chiche J, Ilc K, Laferrière J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, and Pouysségur 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.
8. Chrastina A (2003) High cell density-mediated pericellular hypoxia is a crucial factor inducing expression of the intrinsic hypoxia marker CA IX in vitro in HeLa cells. Neoplasma 50:251-256.
9. Cianchi F, Cortesini C, Fantappiè O, Messerini L, Sardi I, Lasagna N, Perna F, Fabbroni V, Di Felice A, Perigli G, et al. (2004) Cyclooxygenase-2 activation mediates the proangiogenic effect of nitric oxide in colorectal cancer. Clin Cancer Res 10:2694-2704.
10. Cianchi F, Cortesini C, Magnelli L, Fanti E, Papucci L, Schiavone N, Messerini L, Vannacci A, Capaccioli S, Perna F, et al. (2006) Inhibition of 5-lipoxygenase by MK886 augments the antitumor activity of celecoxib in human colon cancer cells. Mol Cancer Ther 5:2716-2726.
11. Cianchi F, Papucci L, Schiavone N, Lulli M, Magnelli L, Vinci MC, Messerini L, Manera C, Ronconi E, Romagnani P, et al. (2009) Cannabinoid receptor activation induces apoptosis through tumor necrosis factor α-mediated ceramide de novo synthesis in colon cancer cells. Clin Cancer Res 14:7691-7700.
12. Cuzzocrea S, Di Paola R, Genovese T, Mazzon E, Esposito E, Crisafulli C, Bramanti P, and Salvemini D (2008) Anti-inflammatory and antiapoptotic effects of fumonisin B1, an inhibitor of ceramide synthase, in a rodent model of splanchnic ischemia and reperfusion injury. J Pharmacol Exp Ther 327:45-57.
13. Dorai T, Sawczuk I, Pastorek J, Wiernik PH, and Dutcher JP (2006) Role of carbonic anhydrases in the progression of renal cell carcinoma subtypes: proposal of a unified hypothesis. Cancer Invest 24:754-779. (Pubitemid 44949880)
14. Garaj V, Puccetti L, Fasolis G, Winum JY, Montero JL, Scozzafava A, Vullo D, Innocenti A, and Supuran CT (2004) Carbonic anhydrase inhibitors: synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, and IX with sulfonamides incorporating 1,2,4-triazine moieties. Bioorg Med Chem Lett 14:5427-5433. (Pubitemid 39348939)
15. Gatenby RA and Gillies RJ (2004) Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4:891-899.
16. Giatromanolaki A, Koukourakis MI, Sivridis E, Pastorek J, Wykoff CC, Gatter KC, and Harris AL (2001) Expression of hypoxia-inducible carbonic anhydrase-9 relates to angiogenic pathways and independently to poor outcome in non-small cell lung cancer. Cancer Res 61:7992-7998. (Pubitemid 33049392)
17. Gnarra JR, Tory K, Weng Y, Schmidt L, Wei MH, Li H, Latif F, Liu S, Chen F, Duh FM, et al. (1994) Mutations of the VHL tumor suppressor gene in renal carcinoma. Nat Genet 7:85-90.
18. Morsy SM, Badawi AM, Cecchi A, Scozzafava A, and Supuran CT (2009) Carbonic anhydrase inhibitors. Biphenylsulfonamides with inhibitory action towards the transmembrane, tumor-associated isozymes IX possess cytotoxic activity against human colon, lung and breast cancer cell lines. J Enzyme Inhib Med Chem 24:499-505.
19. Ogretmen B and Hannun YA (2004) Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 4:604-616. (Pubitemid 39025055)
20. Parkkila S, Rajaniemi H, Parkkila AK, Kivela J, Waheed A, Pastorekova S, Pastorek J, and Sly WS (2000) Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci USA 97:2220-2224. (Pubitemid 30134049)
21. Pastorekova S, Kopacek J, and Pastorek J (2007) Carbonic anhydrase inhibitors and the management of cancer. Curr Top Med Chem 7:865-878. (Pubitemid 46830331)
22. Pastorekova S, Parkkila S, Pastorek J, and Supuran CT (2004) Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J Enzyme Inhib Med Chem 19:199-229. (Pubitemid 39004275)
23. Puccetti L, Fasolis G, Cecchi A, Winum JY, Gamberi A, Montero JL, Scozzafava A, and Supuran CT (2005) Carbonic anhydrase inhibitors: synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, and IX with sulfonamides incorporating thioureido-sulfanilyl scaffolds. Bioorg Med Chem Lett 15:2359-2364.
24. Robertson N, Potter C, and Harris AL (2004) Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res 64:6160-6165.
25. Supuran CT (2004) Carbonic anhydrases: catalytic mechanisms, distribution and physiological roles, in Carbonic Anhydrase: Its Inhibitors and Activators (Supuran CT, Scozzafava A, and Conway J eds) pp 1-24, CRC Press, Boca Raton, FL.
26. Supuran CT (2008) Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7:168-181.
27. Supuran CT and Scozzafava A (2002) Applications of carbonic anhydrase inhibitors and activators in therapy. Expert Opin Ther Patents 12:217-242.
28. Swietach P, Patiar S, Supuran CT, Harris AL, and 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.
29. Swietach P, Vaughan-Jones RD, and Harris AL (2007) Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev 26:299-310.
30. Thiry A, Dogné JM, Masereel B, and Supuran CT (2006) Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 27:566-573.
31. Vaupel P, Kallinowski F, and Okunieff P (1990) Blood flow, oxygen consumption and tissue oxygenation of human tumors. Adv Exp Med Biol 277:895-905.
32. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, et al. (2000) Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60:7075-7083.