1887

Journal of Medical Microbiology logo

Volume 63, Issue 1

Role of carbonic anhydrases in pathogenic micro-organisms: a focus on Free

Abstract

is a ubiquitous saprophytic fungus responsible for organic material decomposition, and plays an important role in recycling environmental carbon and nitrogen. Besides its important role in the environment, this fungus has been reported as one of the most important fungal pathogens in immunocompromised patients. Due to changes in CO concentration that some pathogens face during the infection process, studies have been undertaken to understand the pathogenic roles of carbonic anhydrases (CAs), well-known CO hydration catalytic enzymes. As a basis for a discussion of the possible roles of CAs in pathogenicity, this review describes the main characteristics of the infection and the challenges for its treatment. In addition, it gathers findings from studies with CA inhibitor drugs as anti-infective agents in different pathogens.

  • Received:
  • Accepted:
  • Published Online:
© 2014 SGM
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.064444-0
2014-01-01
2024-04-30
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/1/15.html?itemId=/content/journal/jmm/10.1099/jmm.0.064444-0&mimeType=html&fmt=ahah

References

  1. Abad A., Fernández-Molina J. V., Bikandi J., Ramírez A., Margareto J., Sendino J., Hernando F. L., Pontón J., Garaizar J., Rementeria A. 2010; What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol 27:155–182 [View Article][PubMed]
     [Google Scholar]
  2. Akyol Erikci A., Ozyurt M., Terekeci H., Ozturk A., Karabudak O., Oncu K. 2009; Oesophageal aspergillosis in a case of acute lymphoblastic leukaemia successfully treated with caspofungin alone due to liposomal amphotericin B induced severe hepatotoxicity. Mycoses 52:84–86 [View Article][PubMed]
     [Google Scholar]
  3. Allen A. M., King R. D. 1978; Occlusion, carbon dioxide, and fungal skin infections. Lancet 311:360–362 [View Article][PubMed]
     [Google Scholar]
  4. Amoroso G., Morell-Avrahov L., Müller D., Klug K., Sültemeyer D. 2005; The gene NCE103 (YNL036w) from Saccharomyces cerevisiae encodes a functional carbonic anhydrase and its transcription is regulated by the concentration of inorganic carbon in the medium. Mol Microbiol 56:549–558 [View Article][PubMed]
     [Google Scholar]
  5. Arendrup M. C., Perkhofer S., Howard S. J., Garcia-Effron G., Vishukumar A., Perlin D., Lass-Flörl C. 2008; Establishing in vitro-in vivo correlations for Aspergillus fumigatus: the challenge of azoles versus echinocandins. Antimicrob Agents Chemother 52:3504–3511 [View Article][PubMed]
     [Google Scholar]
  6. Asano-Mori Y. 2010; Fungal infections after hematopoietic stem cell transplantation. Int J Hematol 91:576–587 [View Article][PubMed]
     [Google Scholar]
  7. Bahn Y. S., Mühlschlegel F. A. 2006; CO2 sensing in fungi and beyond. Curr Opin Microbiol 9:572–578 [View Article][PubMed]
     [Google Scholar]
  8. Bahn Y. S., Cox G. M., Perfect J. R., Heitman J. 2005; Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence. Curr Biol 15:2013–2020 [View Article][PubMed]
     [Google Scholar]
  9. Balloy V., Chignard M. 2009; The innate immune response to Aspergillus fumigatus . Microbes Infect 11:919–927 [View Article][PubMed]
     [Google Scholar]
  10. Barcia J. P. 1998; Hyperkalemia associated with rapid infusion of conventional and lipid complex formulations of amphotericin B. Pharmacotherapy 18:874–876[PubMed]
     [Google Scholar]
  11. Berg J. M., Tymoczko J. L., Stryer L. 2002; Catalytic strategies. In Biochemistry, 5th edn. pp. 227–258 New York: W. H. Freeman and Company; [View Article]
     [Google Scholar]
  12. Bowyer P., Moore C. B., Rautemaa R., Denning D. W., Richardson M. D. 2011; Azole antifungal resistance today: focus on Aspergillus. . Curr Infect Dis Rep 13:485–491 [View Article][PubMed]
     [Google Scholar]
  13. Buchieri M. V., Riafrecha L. E., Rodríguez O. M., Vullo D., Morbidoni H. R., Supuran C. T., Colinas P. A. 2013; Inhibition of the β-carbonic anhydrases from Mycobacterium tuberculosis with C-cinnamoyl glycosides: identification of the first inhibitor with anti-mycobacterial activity. Bioorg Med Chem Lett 23:740–743 [View Article][PubMed]
     [Google Scholar]
  14. Burghout P., Cron L. E., Gradstedt H., Quintero B., Simonetti E., Bijlsma J. J., Bootsma H. J., Hermans P. W. 2010; Carbonic anhydrase is essential for Streptococcus pneumoniae growth in environmental ambient air. J Bacteriol 192:4054–4062 [View Article][PubMed]
     [Google Scholar]
  15. Cornely O. A., Maertens J., Bresnik M., Ebrahimi R., Ullmann A. J., Bouza E., Heussel C. P., Lortholary O., Rieger C. other authors 2007; Liposomal amphotericin B as initial therapy for invasive mold infection: a randomized trial comparing a high-loading dose regimen with standard dosing (AmBiLoad trial). Clin Infect Dis 44:1289–1297 [View Article][PubMed]
     [Google Scholar]
  16. Cottier F., Raymond M., Kurzai O., Bolstad M., Leewattanapasuk W., Jiménez-López C., Lorenz M. C., Sanglard D., Váchová L. other authors 2012; The bZIP transcription factor Rca1p is a central regulator of a novel CO2 sensing pathway in yeast. PLoS Pathog 8:e1002485 [View Article][PubMed]
     [Google Scholar]
  17. Cottier F., Leewattanapasuk W., Kemp L. R., Murphy M., Supuran C. T., Kurzai O., Mühlschlegel F. A. 2013; Carbonic anhydrase regulation and CO2 sensing in the fungal pathogen Candida glabrata involves a novel Rca1p ortholog. Bioorg Med Chem 21:1549–1554 [View Article][PubMed]
     [Google Scholar]
  18. Cox E. H., McLendon G. L., Morel F. M., Lane T. W., Prince R. C., Pickering I. J., George G. N. 2000; The active site structure of Thalassiosira weissflogii carbonic anhydrase 1. Biochemistry 39:12128–12130 [View Article][PubMed]
     [Google Scholar]
  19. Cronk J. D., Rowlett R. S., Zhang K. Y., Tu C., Endrizzi J. A., Lee J., Gareiss P. C., Preiss J. R. 2006; Identification of a novel noncatalytic bicarbonate binding site in eubacterial β-carbonic anhydrase. Biochemistry 45:4351–4361 [View Article][PubMed]
     [Google Scholar]
  20. Cuesta-Seijo J. A., Borchert M. S., Navarro-Poulsen J. C., Schnorr K. M., Mortensen S. B., Lo Leggio L. 2011; Structure of a dimeric fungal α-type carbonic anhydrase. FEBS Lett 585:1042–1048 [View Article][PubMed]
     [Google Scholar]
  21. da Silva Ferreira M. E., Capellaro J. L., dos Reis Marques E., Malavazi I., Perlin D., Park S., Anderson J. B., Colombo A. L., Arthington-Skaggs B. A. other authors 2004; In vitro evolution of itraconazole resistance in Aspergillus fumigatus involves multiple mechanisms of resistance. Antimicrob Agents Chemother 48:4405–4413 [View Article][PubMed]
     [Google Scholar]
  22. Del Prete S., Isik S., Vullo D., De Luca V., Carginale V., Scozzafava A., Supuran C. T., Capasso C. 2012; DNA cloning, characterization, and inhibition studies of an α-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae . J Med Chem 55:10742–10748 [View Article][PubMed]
     [Google Scholar]
  23. Denning D. W. 1998; Invasive aspergillosis. Clin Infect Dis 26:781–803, quiz 804–805 [View Article][PubMed]
     [Google Scholar]
  24. Denning D. W., Marr K. A., Lau W. M., Facklam D. P., Ratanatharathorn V., Becker C., Ullmann A. J., Seibel N. L., Flynn P. M. other authors 2006; Micafungin (FK463), alone or in combination with other systemic antifungal agents, for the treatment of acute invasive aspergillosis. J Infect 53:337–349 [View Article][PubMed]
     [Google Scholar]
  25. Deray G. 2002; Amphotericin B nephrotoxicity. J Antimicrob Chemother 49:Suppl 137–41 [View Article][PubMed]
     [Google Scholar]
  26. Du H., Guan G., Xie J., Cottier F., Sun Y., Jia W., Mühlschlegel F. A., Huang G. 2012; The transcription factor Flo8 mediates CO2 sensing in the human fungal pathogen Candida albicans . Mol Biol Cell 23:2692–2701 [View Article][PubMed]
     [Google Scholar]
  27. Eckmanns T., Rüden H., Gastmeier P. 2006; The influence of high-efficiency particulate air filtration on mortality and fungal infection among highly immunosuppressed patients: a systematic review. J Infect Dis 193:1408–1418 [View Article][PubMed]
     [Google Scholar]
  28. Elleuche S., Pöggeler S. 2009a; Evolution of carbonic anhydrases in fungi. Curr Genet 55:211–222 [View Article][PubMed]
     [Google Scholar]
  29. Elleuche S., Pöggeler S. 2009b; β-Carbonic anhydrases play a role in fruiting body development and ascospore germination in the filamentous fungus Sordaria macrospora . PLoS ONE 4:e5177 [View Article][PubMed]
     [Google Scholar]
  30. Elleuche S., Pöggeler S. 2010; Carbonic anhydrases in fungi. Microbiology 156:23–29 [View Article][PubMed]
     [Google Scholar]
  31. Ferry J. G. 2013; Carbonic anhydrases of anaerobic microbes. Bioorg Med Chem 21:1392–1395 [View Article][PubMed]
     [Google Scholar]
  32. Ferry J. G., House C. H. 2006; The stepwise evolution of early life driven by energy conservation. Mol Biol Evol 23:1286–1292 [View Article][PubMed]
     [Google Scholar]
  33. Filler S. G., Sheppard D. C. 2006; Fungal invasion of normally non-phagocytic host cells. PLoS Pathog 2:e129 [View Article][PubMed]
     [Google Scholar]
  34. Fortún J., Meije Y., Fresco G., Moreno S. 2012; Aspergilosis. Formas clínicas y tratamiento. Enferm Infecc Microbiol Clin 30:201–208 [View Article][PubMed]
     [Google Scholar]
  35. Friedberg C. K., Taymor R., Minor J. B., Halpern M. 1953; The use of diamox, a carbonic anhydrase inhibitor, as an oral diuretic in patients with congestive heart failure. N Engl J Med 248:883–889 [View Article][PubMed]
     [Google Scholar]
  36. Garnaud C., Brenier-Pinchart M. P., Thiebaut-Bertrand A., Hamidfar R., Quesada J. L., Bosseray A., Lebeau B., Mallaret M. R., Maubon D. other authors 2012; Seven-year surveillance of nosocomial invasive aspergillosis in a French University Hospital. J Infect 65:559–567 [View Article][PubMed]
     [Google Scholar]
  37. Gloster J., Perkins E. S. 1955; Effect of a carbonic anhydrase inhibitor (Diamox) on intra-ocular pressure of rabbits and cats. Br J Ophthalmol 39:647–658 [View Article][PubMed]
     [Google Scholar]
  38. Götz R., Gnann A., Zimmermann F. K. 1999; Deletion of the carbonic anhydrase-like gene NCE103 of the yeast Saccharomyces cerevisiae causes an oxygen-sensitive growth defect. Yeast 15:855–864 [View Article][PubMed]
     [Google Scholar]
  39. Gray W. D., Maren T. H., Sisson G. M., Smith F. H. 1957; Carbonic anhydrase inhibition. VII. Carbonic anhydrase inhibition and anticonvulsant effect. J Pharmacol Exp Ther 121:160–170[PubMed]
     [Google Scholar]
  40. Haiduven D. 2009; Nosocomial aspergillosis and building construction. Med Mycol 47:Suppl 1S210–S216 [View Article][PubMed]
     [Google Scholar]
  41. Han K.-H., Chun Y.-H., De Castro Pimentel Figueiredo B., Soriani F. M., Savoldi M., Almeida A., Rodrigues F., Cairns C. T., Bignell E. other authors 2010; The conserved and divergent roles of carbonic anhydrases in the filamentous fungi Aspergillus fumigatus and Aspergillus nidulans . Mol Microbiol 75:1372–1388 [View Article][PubMed]
     [Google Scholar]
  42. Henry R. P. 1996; Multiple roles of carbonic anhydrase in cellular transport and metabolism. Annu Rev Physiol 58:523–538 [View Article][PubMed]
     [Google Scholar]
  43. Herbrecht R., Denning D. W., Patterson T. F., Bennett J. E., Greene R. E., Oestmann J. W., Kern W. V., Marr K. A., Ribaud P. other authors 2002; Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med 347:408–415 [View Article][PubMed]
     [Google Scholar]
  44. Hewitson K. S., Vullo D., Scozzafava A., Mastrolorenzo A., Supuran C. T. 2012; Molecular cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Malassezia globosa, a potential antidandruff target. J Med Chem 55:3513–3520 [View Article][PubMed]
     [Google Scholar]
  45. Hogan L. H., Klein B. S., Levitz S. M. 1996; Virulence factors of medically important fungi. Clin Microbiol Rev 9:469–488[PubMed]
     [Google Scholar]
  46. Hope W. W., Walsh T. J., Denning D. W. 2005; The invasive and saprophytic syndromes due to Aspergillus spp. Med Mycol 43:Suppl 1207–238 [View Article][PubMed]
     [Google Scholar]
  47. Howard S. J., Arendrup M. C. 2011; Acquired antifungal drug resistance in Aspergillus fumigatus: epidemiology and detection. Med Mycol 49:S1S90–S95 [View Article][PubMed]
     [Google Scholar]
  48. Howard S. J., Webster I., Moore C. B., Gardiner R. E., Park S., Perlin D. S., Denning D. W. 2006; Multi-azole resistance in Aspergillus fumigatus . Int J Antimicrob Agents 28:450–453 [View Article][PubMed]
     [Google Scholar]
  49. Husain A., Madhesia D. 2012; Heterocyclic compounds as carbonic anhydrase inhibitor. J Enzyme Inhib Med Chem 27:773–783 [View Article][PubMed]
     [Google Scholar]
  50. Imtaiyaz Hassan M., Shajee B., Waheed A., Ahmad F., Sly W. S. 2013; Structure, function and applications of carbonic anhydrase isozymes. Bioorg Med Chem 21:1570–1582 [View Article][PubMed]
     [Google Scholar]
  51. Innocenti A., Mühlschlegel F. A., Hall R. A., Steegborn C., Scozzafava A., Supuran C. T. 2008; Carbonic anhydrase inhibitors: inhibition of the β-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with simple anions. Bioorg Med Chem Lett 18:5066–5070 [View Article][PubMed]
     [Google Scholar]
  52. Innocenti A., Hall R. A., Schlicker C., Scozzafava A., Steegborn C., Mühlschlegel F. A., Supuran C. T. 2009a; Carbonic anhydrase inhibitors. Inhibition and homology modeling studies of the fungal β-carbonic anhydrase from Candida albicans with sulfonamides. Bioorg Med Chem 17:4503–4509 [View Article][PubMed]
     [Google Scholar]
  53. Innocenti A., Winum J. Y., Hall R. A., Mühlschlegel F. A., Scozzafava A., Supuran C. T. 2009b; Carbonic anhydrase inhibitors. Inhibition of the fungal β-carbonic anhydrases from Candida albicans and Cryptococcus neoformans with boronic acids. Bioorg Med Chem Lett 19:2642–2645 [View Article][PubMed]
     [Google Scholar]
  54. Innocenti A., Leewattanapasuk W., Manole G., Scozzafava A., Mühlschlegel F. A., Supuran C. T. 2010; Carbonic anhydrase activators: activation of the β-carbonic anhydrase from the pathogenic yeast Candida glabrata with amines and amino acids. Bioorg Med Chem Lett 20:1701–1704 [View Article][PubMed]
     [Google Scholar]
  55. Isik S., Kockar F., Arslan O., Guler O. O., Innocenti A., Supuran C. T. 2008; Carbonic anhydrase inhibitors. Inhibition of the β-class enzyme from the yeast Saccharomyces cerevisiae with anions. Bioorg Med Chem Lett 18:6327–6331 [View Article][PubMed]
     [Google Scholar]
  56. Jeurissen A., Cooreman S., Van Kerckhoven W., Van Leemput J., Vanhove P., Lagrou K., Heytens L. 2012; Invasive pulmonary aspergillosis due to a multi-azole resistant Aspergillus fumigatus . Acta Clin Belg 67:46–48[PubMed]
     [Google Scholar]
  57. Joseph P., Turtaut F., Ouahrani-Bettache S., Montero J. L., Nishimori I., Minakuchi T., Vullo D., Scozzafava A., Köhler S. other authors 2010; Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Brucella suis . J Med Chem 53:2277–2285 [View Article][PubMed]
     [Google Scholar]
  58. Joseph P., Ouahrani-Bettache S., Montero J. L., Nishimori I., Minakuchi T., Vullo D., Scozzafava A., Winum J. Y., Köhler S., Supuran C. T. 2011; A new β-carbonic anhydrase from Brucella suis, its cloning, characterization, and inhibition with sulfonamides and sulfamates, leading to impaired pathogen growth. Bioorg Med Chem 19:1172–1178 [View Article][PubMed]
     [Google Scholar]
  59. Jung S. I., Kang T. W., Kim S. O., Kwon D. D., Park K., Ryu S. B. 2007; Surgical treatment of invasive renal aspergillosis after chemotherapy. J Pediatr Urol 3:250–252 [View Article][PubMed]
     [Google Scholar]
  60. Jungbluth M., Mösch H. U., Taxis C. 2012; Acetate regulation of spore formation is under the control of the Ras/cyclic AMP/protein kinase A pathway and carbon dioxide in Saccharomyces cerevisiae . Eukaryot Cell 11:1021–1032 [View Article][PubMed]
     [Google Scholar]
  61. Kalokhe A. S., Rouphael N., El Chami M. F., Workowski K. A., Ganesh G., Jacob J. T. 2010; Aspergillus endocarditis: a review of the literature. Int J Infect Dis 14:e1040–e1047 [View Article][PubMed]
     [Google Scholar]
  62. Karthaus M. 2011; Prophylaxis and treatment of invasive aspergillosis with voriconazole, posaconazole and caspofungin: review of the literature. Eur J Med Res 16:145–152 [View Article][PubMed]
     [Google Scholar]
  63. Kartsonis N. A., Nielsen J., Douglas C. M. 2003; Caspofungin: the first in a new class of antifungal agents. Drug Resist Updat 6:197–218 [View Article][PubMed]
     [Google Scholar]
  64. Kim C. W., Seo J. S., Kim M. K., Jun E. J., Choi J. C., Choi B. W. 2010a; Secondary cutaneous aspergillosis disseminated from the lungs of a patient with asthma on 1 month steroid treatment. Diagn Microbiol Infect Dis 66:104–107 [View Article][PubMed]
     [Google Scholar]
  65. Kim M. S., Ko Y. J., Maeng S., Floyd A., Heitman J., Bahn Y. S. 2010b; Comparative transcriptome analysis of the CO2 sensing pathway via differential expression of carbonic anhydrase in Cryptococcus neoformans . Genetics 185:1207–1219 [View Article][PubMed]
     [Google Scholar]
  66. Klengel T., Liang W. J., Chaloupka J., Ruoff C., Schröppel K., Naglik J. R., Eckert S. E., Mogensen E. G., Haynes K. other authors 2005; Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15:2021–2026 [View Article][PubMed]
     [Google Scholar]
  67. Klepser M. 2011; The value of amphotericin B in the treatment of invasive fungal infections. J Crit Care 26:225.e1–225.e10 [View Article][PubMed]
     [Google Scholar]
  68. Krungkrai J., Supuran C. T. 2008; The alpha-carbonic anhydrase from the malaria parasite and its inhibition. Curr Pharm Des 14:631–640 [View Article][PubMed]
     [Google Scholar]
  69. Krungkrai S. R., Wutipraditkul N., Krungkrai J. 2008; Dihydroorotase of human malarial parasite Plasmodium falciparum differs from host enzyme. Biochem Biophys Res Commun 366:821–826 [View Article][PubMed]
     [Google Scholar]
  70. Lane T. W., Morel F. M. 2000; Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii . Plant Physiol 123:345–352 [View Article][PubMed]
     [Google Scholar]
  71. Latgé J. P. 1999; Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12:310–350[PubMed]
     [Google Scholar]
  72. Lavoie H., Hogues H., Mallick J., Sellam A., Nantel A., Whiteway M. 2010; Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol 8:e1000329 [View Article][PubMed]
     [Google Scholar]
  73. Liljas A., Laurberg M. 2000; A wheel invented three times.. EMBO Rep 1:16–17 [View Article][PubMed]
     [Google Scholar]
  74. Lin S. J., Schranz J., Teutsch S. M. 2001; Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 32:358–366 [View Article][PubMed]
     [Google Scholar]
  75. Lindskog S. 1997; Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74:1–20 [View Article][PubMed]
     [Google Scholar]
  76. Madureira A., Bergeron A., Lacroix C., Robin M., Rocha V., de Latour R. P., Ferry C., Devergie A., Lapalu J. other authors 2007; Breakthrough invasive aspergillosis in allogeneic haematopoietic stem cell transplant recipients treated with caspofungin. Int J Antimicrob Agents 30:551–554 [View Article][PubMed]
     [Google Scholar]
  77. Maertens J., Raad I., Petrikkos G., Boogaerts M., Selleslag D., Petersen F. B., Sable C. A., Kartsonis N. A., Ngai A. other authors 2004; Efficacy and safety of caspofungin for treatment of invasive aspergillosis in patients refractory to or intolerant of conventional antifungal therapy. Clin Infect Dis 39:1563–1571 [View Article][PubMed]
     [Google Scholar]
  78. Manavathu E. K., Abraham O. C., Chandrasekar P. H. 2001; Isolation and in vitro susceptibility to amphotericin B, itraconazole and posaconazole of voriconazole-resistant laboratory isolates of Aspergillus fumigatus . Clin Microbiol Infect 7:130–137 [View Article][PubMed]
     [Google Scholar]
  79. Marcus E. A., Moshfegh A. P., Sachs G., Scott D. R. 2005; The periplasmic α-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J Bacteriol 187:729–738 [View Article][PubMed]
     [Google Scholar]
  80. Maresca A., Vullo D., Scozzafava A., Supuran C. T. 2013; Inhibition of the alpha- and beta-carbonic anhydrases from the gastric pathogen Helycobacter pylori with anions. J Enzyme Inhib Med Chem 28:388–391 [View Article][PubMed]
     [Google Scholar]
  81. Mayr A., Lass-Flörl C. 2011; Epidemiology and antifungal resistance in invasive aspergillosis according to primary disease: review of the literature. Eur J Med Res 16:153–157 [View Article][PubMed]
     [Google Scholar]
  82. Mayr A., Aigner M., Lass-Flörl C. 2012; Caspofungin: when and how? The microbiologist’s view. Mycoses 55:27–35 [View Article][PubMed]
     [Google Scholar]
  83. Meldrum N. U., Roughton F. J. W. 1933; Carbonic anhydrase. Its preparation and properties. J Physiol 80:113–142[PubMed] [CrossRef]
     [Google Scholar]
  84. Messer S. A., Jones R. N., Fritsche T. R. 2006; International surveillance of Candida spp. and Aspergillus spp.: report from the SENTRY Antimicrobial Surveillance Program (2003). J Clin Microbiol 44:1782–1787 [View Article][PubMed]
     [Google Scholar]
  85. Millichap J. G., Woodbury D. M., Goodman L. S. 1955; Mechanism of the anticonvulsant action of acetazoleamide, a carbonic anhydrase inhibitor. J Pharmacol Exp Ther 115:251–258[PubMed]
     [Google Scholar]
  86. Mogensen E. G., Janbon G., Chaloupka J., Steegborn C., Fu M. S., Moyrand F., Klengel T., Pearson D. S., Geeves M. A. other authors 2006; Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 5:103–111 [View Article][PubMed]
     [Google Scholar]
  87. Mohite U., Kell J., Haj M. A., O’Brien C., Kundu S., Rees J., Burnett A. K. 2007; Invasive aspergillosis localised to the colon presenting as toxic megacolon. Eur J Haematol 78:270–273 [View Article][PubMed]
     [Google Scholar]
  88. Monti S. M., Maresca A., Viparelli F., Carta F., De Simone G., Mühlschlegel F. A., Scozzafava A., Supuran C. T. 2012; Dithiocarbamates are strong inhibitors of the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata. . Bioorg Med Chem Lett 22:859–862 [View Article][PubMed]
     [Google Scholar]
  89. Morishita S., Nishimori I., Minakuchi T., Onishi S., Takeuchi H., Sugiura T., Vullo D., Scozzafava A., Supuran C. T. 2008; Cloning, polymorphism, and inhibition of β-carbonic anhydrase of Helicobacter pylori. . J Gastroenterol 43:849–857 [View Article][PubMed]
     [Google Scholar]
  90. Mullins J., Harvey R., Seaton A. 1976; Sources and incidence of airborne Aspergillus fumigatus (Fres). Clin Allergy 6:209–217 [View Article][PubMed]
     [Google Scholar]
  91. Neofytos D., Horn D., Anaissie E., Steinbach W., Olyaei A., Fishman J., Pfaller M., Chang C., Webster K., Marr K. 2009; Epidemiology and outcome of invasive fungal infection in adult hematopoietic stem cell transplant recipients: analysis of Multicenter Prospective Antifungal Therapy (PATH) Alliance registry. Clin Infect Dis 48:265–273 [View Article][PubMed]
     [Google Scholar]
  92. Neofytos D., Fishman J. A., Horn D., Anaissie E., Chang C. H., Olyaei A., Pfaller M., Steinbach W. J., Webster K. M., Marr K. A. 2010; Epidemiology and outcome of invasive fungal infections in solid organ transplant recipients. Transpl Infect Dis 12:220–229 [View Article][PubMed]
     [Google Scholar]
  93. Nishimori I., Minakuchi T., Kohsaki T., Onishi S., Takeuchi H., Vullo D., Scozzafava A., Supuran C. T. 2007; Carbonic anhydrase inhibitors: the β-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors. Bioorg Med Chem Lett 17:3585–3594 [View Article][PubMed]
     [Google Scholar]
  94. Nishimori I., Minakuchi T., Vullo D., Scozzafava A., Innocenti A., Supuran C. T. 2009; Carbonic anhydrase inhibitors. Cloning, characterization, and inhibition studies of a new β-carbonic anhydrase from Mycobacterium tuberculosis . J Med Chem 52:3116–3120 [View Article][PubMed]
     [Google Scholar]
  95. Nishimori I., Minakuchi T., Maresca A., Carta F., Scozzafava A., Supuran C. T. 2010; The β-carbonic anhydrases from Mycobacterium tuberculosis as drug targets. Curr Pharm Des 16:3300–3309 [View Article][PubMed]
     [Google Scholar]
  96. Nishimori I., Minakuchi T., Vullo D., Scozzafava A., Supuran C. T. 2011; Inhibition studies of the β-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium with sulfonamides and sulfamates. Bioorg Med Chem 19:5023–5030 [View Article][PubMed]
     [Google Scholar]
  97. Ostrosky-Zeichner L., Marr K. A., Rex J. H., Cohen S. H. 2003; Amphotericin B: time for a new “gold standard”. Clin Infect Dis 37:415–425 [View Article][PubMed]
     [Google Scholar]
  98. Patel R., Paya C. V. 1997; Infections in solid-organ transplant recipients. Clin Microbiol Rev 10:86–124[PubMed]
     [Google Scholar]
  99. Patterson T. F., Boucher H. W., Herbrecht R., Denning D. W., Lortholary O., Ribaud P., Rubin R. H., Wingard J. R., DePauw B. other authors 2005; Strategy of following voriconazole versus amphotericin B therapy with other licensed antifungal therapy for primary treatment of invasive aspergillosis: impact of other therapies on outcome. Clin Infect Dis 41:1448–1452 [View Article][PubMed]
     [Google Scholar]
  100. Pfaller M. A., Diekema D. J. 2010; Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36:1–53 [View Article][PubMed]
     [Google Scholar]
  101. Phai Pang K.-A., Godet C., Fekkar A., Scholler J., Nivoix Y., Letscher-Bru V., Massias L., Kauffmann-Lacroix C., Elsendoorn A. other authors 2012; Breakthrough invasive mould infections in patients treated with caspofungin. J Infect 64:424–429 [View Article][PubMed]
     [Google Scholar]
  102. Potter C. P., Harris A. L. 2003; Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer. Br J Cancer 89:2–7 [View Article][PubMed]
     [Google Scholar]
  103. Pushker N., Meel R., Kashyap S., Bajaj M. S., Sen S. 2011; Invasive aspergillosis of orbit in immunocompetent patients: treatment and outcome. Ophthalmology 118:1886–1891 [View Article][PubMed]
     [Google Scholar]
  104. Rowlett R. S. 2010; Structure and catalytic mechanism of the β-carbonic anhydrases. Biochim Biophys Acta 1804:362–373 [View Article][PubMed]
     [Google Scholar]
  105. Schlicker C., Hall R. A., Vullo D., Middelhaufe S., Gertz M., Supuran C. T., Mühlschlegel F. A., Steegborn C. 2009; Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans . J Mol Biol 385:1207–1220 [View Article][PubMed]
     [Google Scholar]
  106. Scott C. J., Lambert J. S., Taylor C. B., Poulton M. B. 2007; Invasive Aspergillus fumigatus associated with liver and bone involvement in a patient with AIDS. Int J Infect Dis 11:550–553 [View Article][PubMed]
     [Google Scholar]
  107. Shapiro R. S., Robbins N., Cowen L. E. 2011; Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 75:213–267 [View Article][PubMed]
     [Google Scholar]
  108. Snelders E., Camps S. M., Karawajczyk A., Schaftenaar G., Kema G. H., van der Lee H. A., Klaassen C. H., Melchers W. J., Verweij P. E. 2012; Triazole fungicides can induce cross-resistance to medical triazoles in Aspergillus fumigatus . PLoS ONE 7:e31801 [View Article][PubMed]
     [Google Scholar]
  109. So A. K., Espie G. S., Williams E. B., Shively J. M., Heinhorst S., Cannon G. C. 2004; A novel evolutionary lineage of carbonic anhydrase (ϵ class) is a component of the carboxysome shell. J Bacteriol 186:623–630 [View Article][PubMed]
     [Google Scholar]
  110. Stadie W. C., O'Brien H. 1933; The catalysis of the hydration of carbon dioxide and dehydration of carbonic acid by an enzyme isolated from red blood cells. J Biol Chem 103:521–529
     [Google Scholar]
  111. Stähler F. N., Ganter L., Lederer K., Kist M., Bereswill S. 2005; Mutational analysis of the Helicobacter pylori carbonic anhydrases. FEMS Immunol Med Microbiol 44:183–189 [View Article][PubMed]
     [Google Scholar]
  112. Steinbach W. J., Marr K. A., Anaissie E. J., Azie N., Quan S. P., Meier-Kriesche H. U., Apewokin S., Horn D. L. 2012; Clinical epidemiology of 960 patients with invasive aspergillosis from the PATH Alliance registry. J Infect 65:453–464 [View Article][PubMed]
     [Google Scholar]
  113. Supuran C. T. 2008a; Carbonic anhydrases – an overview. Curr Pharm Des 14:603–614 [View Article][PubMed]
     [Google Scholar]
  114. Supuran C. T. 2008b; Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7:168–181 [View Article][PubMed]
     [Google Scholar]
  115. Supuran C. T. 2010; Carbonic anhydrase inhibition/activation: trip of a scientist around the world in the search of novel chemotypes and drug targets. Curr Pharm Des 16:3233–3245 [View Article][PubMed]
     [Google Scholar]
  116. Supuran C. T. 2011; Carbonic anhydrase inhibitors and activators for novel therapeutic applications. Future Med Chem 3:1165–1180 [View Article][PubMed]
     [Google Scholar]
  117. Supuran C. T., Scozzafava A. 2007; Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem 15:4336–4350 [View Article][PubMed]
     [Google Scholar]
  118. Supuran C. T., Scozzafava A., Casini A. 2003; Carbonic anhydrase inhibitors. Med Res Rev 23:146–189 [View Article][PubMed]
     [Google Scholar]
  119. Tahir C., Garbati M., Nggada H. A., Terna Yawe E. H., Abubakar A. M. 2011; Primary cutaneous aspergillosis in an immunocompetent patient. J Surg Tech Case Rep 3:94–96 [View Article][PubMed]
     [Google Scholar]
  120. Tekaia F., Latgé J. P. 2005; Aspergillus fumigatus: saprophyte or pathogen?. Curr Opin Microbiol 8:385–392 [View Article][PubMed]
     [Google Scholar]
  121. Thakar S., Chickabasaviah Y. T., Hegde A. S. 2012; Spontaneous resolution of invasive cerebral aspergillosis following partial resection in a medically untreated infant. J Neurosurg Pediatr 10:71–74 [View Article][PubMed]
     [Google Scholar]
  122. Tripp B. C., Smith K., Ferry J. G. 2001; Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276:48615–48618 [View Article][PubMed]
     [Google Scholar]
  123. van Burik J. A., Colven R., Spach D. H. 1998; Cutaneous aspergillosis. J Clin Microbiol 36:3115–3121[PubMed]
     [Google Scholar]
  124. VandenBussche H. L., Van Loo D. A. 2010; A clinical review of echinocandins in pediatric patients. Ann Pharmacother 44:166–177 [View Article][PubMed]
     [Google Scholar]
  125. Verweij P. E., Snelders E., Kema G. H., Mellado E., Melchers W. J. 2009; Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use?. Lancet Infect Dis 9:789–795 [View Article][PubMed]
     [Google Scholar]
  126. Vonberg R.-P., Gastmeier P. 2006; Nosocomial aspergillosis in outbreak settings. J Hosp Infect 63:246–254 [View Article][PubMed]
     [Google Scholar]
  127. Walsh T. J. 1998; Editorial response: primary cutaneous aspergillosis – an emerging infection among immunocompromised patients. Clin Infect Dis 27:453–457 [View Article][PubMed]
     [Google Scholar]
  128. Walsh T. J., Anaissie E. J., Denning D. W., Herbrecht R., Kontoyiannis D. P., Marr K. A., Morrison V. A., Segal B. H., Steinbach W. J. other authors 2008; Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 46:327–360 [View Article][PubMed]
     [Google Scholar]
  129. White M. H., Bowden R. A., Sandler E. S., Graham M. L., Noskin G. A., Wingard J. R., Goldman M., van Burik J. A., McCabe A. other authors 1998; Randomized, double-blind clinical trial of amphotericin B colloidal dispersion vs. amphotericin B in the empirical treatment of fever and neutropenia. Clin Infect Dis 27:296–302 [View Article][PubMed]
     [Google Scholar]
  130. Wilson A. C., Soyer M., Hoch J. A., Perego M. 2008; The bicarbonate transporter is essential for Bacillus anthracis lethality. PLoS Pathog 4:e1000210 [View Article][PubMed]
     [Google Scholar]
  131. Winterstein A. R., Bohndorf K., Vollert K., Wagner T., Gnekow A., Roemer F. W. 2010; Invasive aspergillosis osteomyelitis in children – a case report and review of the literature. Skeletal Radiol 39:827–831 [View Article][PubMed]
     [Google Scholar]
  132. Winum J. Y., Carta F., Ward C., Mullen P., Harrison D., Langdon S. P., Cecchi A., Scozzafava A., Kunkler I., Supuran C. T. 2012; Ureido-substituted sulfamates show potent carbonic anhydrase IX inhibitory and antiproliferative activities against breast cancer cell lines. Bioorg Med Chem Lett 22:4681–4685 [View Article][PubMed]
     [Google Scholar]
  133. Xu Y., Feng L., Jeffrey P. D., Shi Y., Morel F. M. 2008; Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61 [View Article][PubMed]
     [Google Scholar]
  134. Yu O. H., Keet A. W., Sheppard D. C., Brewer T. 2010; Articular aspergillosis: case report and review of the literature. Int J Infect Dis 14:e433–e435 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.064444-0
Loading
Role of carbonic anhydrases in pathogenic micro-organisms: a focus on Aspergillus fumigatus
J. Med. Microbiol. 63, 15 (2014); https://doi.org/10.1099/jmm.0.064444-0
/content/journal/jmm/10.1099/jmm.0.064444-0
/content/journal/jmm/10.1099/jmm.0.064444-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error