DNA cloning, characterization, and inhibition studies of an α-carbonic anhydrase from the pathogenic bacterium vibrio cholerae

Journal of Medicinal Chemistry

Volumn 55, Issue 23, 2012, Pages 10742-10748

  Del Prete, Sonia ^a   Isik, Semra ^b,c   Vullo, Daniela ^b   De Luca, Viviana ^a   Carginale, Vincenzo ^a   Scozzafava, Andrea ^b   Supuran, Claudiu T ^b   Capasso, Clemente ^a  

^a INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c BALIKESIR UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

[4 [4 [(2,3 DIHYDRO 1H INDEN 1 YL)AMINO] 7H PYRROLO[2,3 D]PYRIMIDIN 7 YL] 2 HYDROXYCYCLOPENTYLMETHYL] SULFAMATE; ACETAZOLAMIDE; ALPHA CARBONIC ANHYDRASE; BENZOLAMIDE; BICARBONATE; BRINZOLAMIDE; CARBONATE DEHYDRATASE; DICLOFENAMIDE; DORZOLAMIDE; ETHOXZOLAMIDE; INDISULAM; METHAZOLAMIDE; SULFANILAMIDE; SULFONAMIDE; SULPIRIDE; TOPIRAMATE; UNCLASSIFIED DRUG; ZONISAMIDE;

ARTICLE; BACTERIAL VIRULENCE; DNA PURIFICATION; DRUG STRUCTURE; ENZYME INHIBITION; ENZYME MECHANISM; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PHYLOGENY; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; BIOCATALYSIS; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASES; CLONING, MOLECULAR; DNA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; VIBRIO CHOLERAE;

EID: 84870988209     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm301611m     Document Type: Article

References (42)

1. Cash, R. A.; Music, S. I.; Libonati, J. P.; Snyder, M. J.; Wenzel, R. P.; Hornick, R. B. Response of man to infection with Vibrio cholerae. I. Clinical, serologic, and bacteriologic responses to a known inoculum J. Infect. Dis. 1974, 129, 45-52
2. Harris, J. B.; LaRocque, R. C.; Qadri, F.; Ryan, E. T.; Calderwood, S. B. Cholera Lancet 2012, 379, 2466-2476
3. Abuaita, B. H.; Withey, J. H. Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity Infect. Immun. 2009, 77, 4111-4120
4. Kovacikova, G.; Lin, W.; Skorupski, K. The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis J. Bacteriol. 2010, 192, 4181-4191
5. Ushijima, B.; Smith, A.; Aeby, G. S.; Callahan, S. M. Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata PLoS One 2012, 7, e46717
6. Mandal, S.; Mandal, M. D.; Pal, N. K. Cholera: a great global concern Asian Pac. J. Trop. Med. 2011, 4, 573-580
7. Ivarsson, M. E.; Leroux, J. C.; Castagner, B. Targeting bacterial toxins Angew. Chem., Int. Ed. 2012, 51, 4024-4045
8. Supuran, C. T. Bacterial carbonic anhydrases as drug targets: toward novel antibiotics? Front. Pharmacol. 2011, 2, 34
9. Supuran, C. T. Carbonic anhydrase inhibitors and activators for novel therapeutic applications Future Med. Chem. 2011, 3, 1165-1180
10. Supuran, C. T. Carbonic anhydrase inhibitors Bioorg. Med. Chem. Lett. 2010, 20, 3467-3474
11. Supuran, C. T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators Nat. Rev. Drug Discovery 2008, 7, 168-181
12. Smith, K. S.; Ferry, J. G. Prokaryotic carbonic anhydrases FEMS Microbiol. Rev. 2000, 24, 335-366
13. Cronk, J. D.; Rowlett, R. S.; Zhang, K. Y.; Tu, C.; Endrizzi, J. A.; Lee, J.; Gareiss, P. C.; Preiss, J. R. Identification of a novel noncatalytic bicarbonate binding site in eubacterial β-carbonic anhydrase Biochemistry 2006, 45, 4351-4361
14. Maeda, S.; Price, G. D.; Badger, M. R.; Enomoto, C.; Omata, T. Bicarbonate binding activity of the CmpA protein of the cyanobacterium Synechococcus sp. strain PCC 7942 involved in active transport of bicarbonate J. Biol. Chem. 2000, 275, 20551-20555
15. Joseph, P.; Ouahrani-Bettache, S.; Montero, J. L.; Nishimori, I.; Vullo, D.; Scozzafava, A.; Winum, J. Y.; Köhler, S.; Supuran, C. T. A new Brucella suis β-carbonic anhydrase, bsCA II: inhibition of bsCA I and II with sulfonamides and sulfamates inhibits the pathogen growth Bioorg. Med. Chem. 2011, 19, 1172-1178
16. Joseph, P.; Turtaut, F.; Ouahrani-Bettache, S.; Montero, J. L.; Nishimori, I.; Minakuchi, T.; Vullo, D.; Scozzafava, A.; Köhler, S.; Winum, J. Y.; Supuran, C. T. Cloning, characterization and inhibition studies of a β-carbonic anhydrase from Brucella suis J. Med. Chem. 2010, 53, 2277-2285
17. Suarez Covarrubias, A.; Larsson, A. M.; Hogbom, M.; Lindberg, J.; Bergfors, T.; Bjorkelid, C.; Mowbray, S. L.; Unge, T.; Jones, T. A. Structure and function of carbonic anhydrases from Mycobacterium tuberculosis J. Biol. Chem. 2005, 280, 18782-18789
18. Nishimori, I.; Minakuchi, T.; Vullo, D.; Scozzafava, A.; Innocenti, A.; Supuran, C. T. Carbonic anhydrase inhibitors. Cloning, characterization, and inhibition studies of a new β-carbonic anhydrase from Mycobacterium tuberculosis J. Med. Chem. 2009, 52, 3116-3120
19. Güzel, Ö.; Maresca, A.; Scozzafava, A.; Salman, A.; Balaban, A. T.; Supuran, C. T. Discovery of low nanomolar and subnanomolar inhibitors of the mycobacterial β-carbonic anhydrases Rv1284 and Rv3273 J. Med. Chem. 2009, 52, 4063-4067
20. Carta, F.; Maresca, A.; Suarez Covarrubias, A.; Mowbray, S. L.; Jones, T. A.; Supuran, C. T. Carbonic anhydrase inhibitors. Characterization and inhibition studies of the most active β-carbonic anhydrase from Mycobacterium tuberculosis, Rv3588c Bioorg. Med. Chem. Lett. 2009, 19, 6649-6654
21. 2 sensing with cAMP signaling and virulence Curr. Biol. 2005, 15, 2021-2026
22. 2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1 Eukaryotic Cell 2006, 5, 103-111
23. Burghout, P.; Vullo, D.; Scozzafava, A.; Hermans, P. W. M.; Supuran, C. T. Inhibition of the β-carbonic anhydrase from Streptococcus pneumoniae by inorganic anions and small molecules: towards innovative drug design of antiinfectives? Bioorg. Med. Chem. 2011, 19, 243-248
24. Supuran, C. T. Carbonic anhydrase inhibition/activation: trip of a scientist around the world in the search of novel chemotypes and drug targets Curr. Pharm. Des. 2010, 16, 3233-3245
25. Vullo, D.; Nishimori, I.; Minakuchi, T.; Scozzafava, A.; Supuran, C. T. Inhibition studies with anions and small molecules of two novel β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium Bioorg. Med. Chem. Lett. 2011, 21, 3591-3595
26. Heidelberg, J. F.; Eisen, J. A.; Nelson, W. C.; Clayton, R. A.; Gwinn, M. L.; Dodson, R. J.; Haft, D. H.; Hickey, E. K.; Peterson, J. D.; Umayam, L.; Gill, S. R.; Nelson, K. E.; Read, T. D.; Tettelin, H.; Richardson, D.; Ermolaeva, M. D.; Vamathevan, J.; Bass, S.; Qin, H.; Dragoi, I.; Sellers, P.; McDonald, L.; Utterback, T.; Fleishmann, R. D.; Nierman, W. C.; White, O.; Salzberg, S. L.; Smith, H. O.; Colwell, R. R.; Mekalanos, J. J.; Venter, J. C.; Fraser, C. M. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae Nature 2000, 406, 477-483
27. Nishimori, I.; Minakuchi, T.; Morimoto, K.; Sano, S.; Onishi, S.; Takeuchi, H.; Vullo, D.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: DNA cloning and inhibition studies of the alpha-carbonic anhydrase from Helicobacter pylori, a new target for developing sulfonamide and sulfamate gastric drugs J. Med. Chem. 2006, 49, 2117-2126
28. Nishimori, I.; Onishi, S.; Takeuchi, H.; Supuran, C. T. The α and β classes carbonic anhydrases from Helicobacter pylori as novel drug targets Curr. Pharm. Des. 2008, 14, 622-630
29. Nishimori, I.; Minakuchi, T.; Kohsaki, T.; Onishi, S.; Takeuchi, H.; Vullo, D.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors. The β-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors Bioorg. Med. Chem. Lett. 2007, 17, 3585-3594
30. Khalifah, R. G. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C J. Biol. Chem. 1971, 246, 2561-2573
31. Vullo, D.; De Luca, V.; Scozzafava, A.; Carginale, V.; Rossi, M.; Supuran, C. T.; Capasso, C. The alpha-carbonic anhydrase from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1 is highly susceptible to inhibition by sulfonamides. Bioorg. Med. Chem. [Online early access]. DOI: 10.1016/j.bmc.2012.07.024. Published Online: July 20, 2012.
32. De Luca, V.; Vullo, D.; Scozzafava, A.; Carginale, V.; Rossi, M.; Supuran, C. T.; Capasso, C. Anion inhibition studies of an alpha-carbonic anhydrase from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1 Bioorg. Med. Chem. Lett. 2012, 22, 5630-5634
33. Capasso, C.; De Luca, V.; Carginale, V.; Cannio, R.; Rossi, M. Biochemical properties of a novel and highly thermostable bacterial alpha-carbonic anhydrase from Sulfurihydrogenibium yellowstonense YO3AOP1 J. Enzyme Inhib. Med. Chem. 2012, 27, 892-897
34. 2 hydration reaction. Bioorg. Med. Chem. [Online early access]. DOI: 10.1016/j.bmc.2012.09.047. Published Online: September 20, 2012.
35. Vullo, D.; De Luca, V.; Scozzafava, A.; Carginale, V.; Rossi, M.; Supuran, C. T.; Capasso, C. Anion inhibition studies of the fastest carbonic anhydrase (CA) known, the extremo-CA from the bacterium Sulfurihydrogenibium azorense Bioorg. Med. Chem. Lett. 2012, 22, 7142-7145
36. Chirica, L. C.; Elleby, B.; Jonsson, B. H.; Lindskog, S. The complete sequence, expression in Escherichia coli, purification and some properties of carbonic anhydrase from Neisseria gonorrhoeae Eur. J. Biochem. 1997, 244, 755-760
37. Pastorekova, S.; Parkkila, S.; Pastorek, J.; Supuran, C. T. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects J. Enzyme Inhib. Med. Chem. 2004, 19, 199-229
38. Supuran, C. T.; Scozzafava, A.; Casini, A. Carbonic anhydrase inhibitors Med. Res. Rev. 2003, 23, 146-189
39. Scozzafava, A.; Mastrolorenzo, A.; Supuran, C. T. Modulation of carbonic anhydrase activity and its applications in therapy Expert Opin. Ther. Pat. 2004, 14, 667-702
40. Supuran, C. T.; Scozzafava, A.; Casini, A. Development of Sulfonamide Carbonic Anhydrase Inhibitors. In Carbonic Anhydrase: Its Inhibitors and Activators; Supuran, C. T.; Scozzafava, A.; Conway, J., Eds.; CRC Press: Boca Raton, FL, 2004; pp 67-147.
41. Thompson, J. D.; Higgins, D. G.; Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 1994, 22, 4673-4680
42. Guindon, S.; Dufayard, J. F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Syst. Biol. 2010, 59, 307-321