Cloning, characterization, and inhibition of the novel β-carbonic anhydrase from parasitic blood fluke, Schistosoma mansoni

References

• Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368(9541):1106–1118.
   PubMed Web of Science ®Google Scholar
• McManus DP, Dunne DW, Sacko M, Utzinger J, Vennervald BJ, Zhou XN. Schistosomiasis. Nat Rev Dis Prim. 2018;4(1).
   PubMedGoogle Scholar
• Kamau E, Yates A, Maisiba R, Singoei V, Opot B, Adeny R, Arima CO, Otieno V, Sumbi CS, Okoth RO, et al. Epidemiological and clinical implications of asymptomatic malaria and schistosomiasis co-infections in a rural community in western Kenya. BMC Infect Dis. 2021;21(1).
   Web of Science ®Google Scholar
• Wilson S, Vennervald BJ, Dunne DW. Chronic hepatosplenomegaly in African school children: a common but neglected morbidity associated with schistosomiasis and malaria. PLOS Negl Trop Dis. 2011;5(8):e1149.
   PubMed Web of Science ®Google Scholar
• Gryseels B. Schistosomiasis. Infect Dis Clin North Am. 2012;26(2):383–397.
   PubMed Web of Science ®Google Scholar
• Elbaz T, Esmat G. Hepatic and intestinal schistosomiasis: review. J Adv Res. 2013;4(5):445–452.
   PubMedGoogle Scholar
• Nelwan ML. Schistosomiasis: life cycle, diagnosis, and control. Curr Ther Res Clin Exp. 2019;91:5–9.
   PubMed Web of Science ®Google Scholar
• Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383(9936):2253–2264.
   PubMed Web of Science ®Google Scholar
• Costain AH, MacDonald AS, Smits HH. Schistosome egg migration: mechanisms, pathogenesis and host immune responses. Front Immunol. 2018;9.
   PubMed Web of Science ®Google Scholar
• Siqueira L. d P, Fontes DAF, Aguilera CSB, Timóteo TRR, Ângelos MA, Silva LCPBB, de Melo CG, Rolim LA, da Silva RMF, Neto PJR, et al. Schistosomiasis: drugs used and treatment strategies. Acta Trop. 2017;176:179–187.
   PubMed Web of Science ®Google Scholar
• Gasim GI, Bella A, Adam I. Schistosomiasis, hepatitis B and hepatitis C co-infection. Virol J. 2015;12(1).
   PubMedGoogle Scholar
• Rahmani A, Baee M, Rostamtabar M, Karkhah A, Alizadeh S, Tourani M, Nouri HR. Development of a conserved chimeric vaccine based on helper T-cell and CTL epitopes for induction of strong immune response against Schistosoma mansoni using immunoinformatics approaches. Int J Biol Macromol. 2019;141:125–136.
   PubMed Web of Science ®Google Scholar
• Eyayu T, Zeleke AJ, Worku L. Current status and future prospects of protein vaccine candidates against Schistosoma mansoni infection. Parasite Epidemiol Control. 2020;11:e00176.
   PubMedGoogle Scholar
• LoVerde PT. Schistosomiasis. Adv Exp Med Biol. 2019;1154:45–70.
   PubMed Web of Science ®Google Scholar
• Cioli D, Pica-Mattoccia L, Basso A, Guidi A. Schistosomiasis control: praziquantel forever? Mol Biochem Parasitol. 2014;195(1):23–29.
   PubMed Web of Science ®Google Scholar
• Doenhoff MJ, Kusel JR, Coles GC, Cioli D. Resistance of Schistosoma mansoni to praziquantel: is there a problem? Trans R Soc Trop Med Hyg. 2002;96(5):465–469.
   PubMed Web of Science ®Google Scholar
• Botros SS, Bennett JL. Praziquantel resistance. Expert Opin Drug Discov. 2007;2(sup1):S35–S40.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Pat. 2013;23(6):693–704.
   PubMed Web of Science ®Google Scholar
• Bonardi A, Vermelho AB, da Silva Cardoso V, de Souza Pereira MC, da Silva Lara L, Selleri S, Gratteri P, Supuran CT, Nocentini A. N-nitrosulfonamides as carbonic anhydrase inhibitors: a promising chemotype for targeting Chagas disease and Leishmaniasis. ACS Med Chem Lett. 2019;10(4):413–418.
   PubMed Web of Science ®Google Scholar
• D'Ambrosio K, Supuran CT, De Simone G. Are carbonic anhydrases suitable targets to fight protozoan parasitic diseases? Curr Med Chem. 2018;25(39):5266–5278.
   PubMed Web of Science ®Google Scholar
• Liljas A, Laurberg M. A wheel invented three times. The molecular structures of the three carbonic anhydrases. EMBO Rep. 2000;1(1):16–17.
   PubMed Web of Science ®Google Scholar
• De Simone G, Di Fiore A, Capasso C, Supuran CT. The zinc coordination pattern in the η-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett. 2015;25(7):1385–1389.
   PubMed Web of Science ®Google Scholar
• Jensen EL, Clement R, Kosta A, Maberly SC, Gontero B. A new widespread subclass of carbonic anhydrase in marine phytoplankton. ISME J. 2019;13(8):2094–2106.
   PubMed Web of Science ®Google Scholar
• Cox EH, McLendon GL, Morel FM, Lane TW, Prince RC, Pickering IJ, George GN. The active site structure of Thalassiosira weissflogii carbonic anhydrase 1. Biochemistry. 2000;39(40):12128–12130.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, Supuran CT, Capasso C. Biochemical characterization of the δ-carbonic anhydrase from the marine diatom Thalassiosira weissflogii, TweCA. J Enzyme Inhib Med Chem. 2014;29(6):906–911.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma- carbonic anhydrases from bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem. 2015;30(2):325–332.
   PubMed Web of Science ®Google Scholar
• Zolfaghari Emameh R, Kuuslahti M, Nosrati H, Lohi H, Parkkila S. Assessment of databases to determine the validity of β-A nd γ-carbonic anhydrase sequences from vertebrates. BMC Genomics. 2020;21(1):352.
   PubMed Web of Science ®Google Scholar
• Ferry JG. The γ class of carbonic anhydrases. Biochim Biophys Acta Proteins Proteomics. 2010;1804(2):374–381.
   PubMed Web of Science ®Google Scholar
• Alterio V, Langella E, Viparelli F, Vullo D, Ascione G, Dathan NA, Morel FMM, Supuran CT, De Simone G, Monti SM. Structural and inhibition insights into carbonic anhydrase CDCA1 from the marine diatom Thalassiosira weissflogii. Biochimie. 2012;94(5):1232–1241.
   PubMed Web of Science ®Google Scholar
• Park H, Song B, Morel FMM. Diversity of the cadmium-containing carbonic anhydrase in marine diatoms and natural waters. Environ Microbiol. 2007;9(2):403–413.
   PubMed Web of Science ®Google Scholar
• Chasen NM, Asady B, Lemgruber L, Vommaro RC, Kissinger JC, Coppens I, Moreno SNJ. A glycosylphosphatidylinositol-anchored carbonic anhydrase-related protein of Toxoplasma gondii is important for rhoptry biogenesis and virulence. mSphere. 2017;2(3).
   PubMed Web of Science ®Google Scholar
• Kikutani S, Nakajima K, Nagasato C, Tsuji Y, Miyatake A, Matsuda Y. Thylakoid luminal Θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA. 2016;113(35):9828–9833.
   PubMed Web of Science ®Google Scholar
• Angeli A, Berrino E, Carradori S, Supuran CT, Cirri M, Carta F, Costantino G. Amine- and amino acid-based compounds as carbonic anhydrase activators. Molecules. 2021;26(23):7331.
   PubMed Web of Science ®Google Scholar
• Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, et al. The genome of the blood fluke Schistosoma mansoni. Nature. 2009;460(7253):352–358.
   PubMed Web of Science ®Google Scholar
• Da’dara AA, Angeli A, Ferraroni M, Supuran CT, Skelly PJ. Crystal structure and chemical inhibition of essential schistosome host-interactive virulence factor carbonic anhydrase SmCA. Commun Biol. 2019;2(1).
   PubMedGoogle Scholar
• Ferraroni M, Angeli A, Carradori S, Supuran CT. Inhibition of Schistosoma mansoni carbonic anhydrase by the antiparasitic drug clorsulon: X-ray crystallographic and in vitro studies. Acta Crystallogr D Struct Biol. 2022;78(Pt 3):321–327.
   PubMedGoogle Scholar
• Supuran CT, Altamimi ASA, Carta F. Carbonic anhydrase inhibition and the management of glaucoma: a literature and patent review 2013–2019. Expert Opin Ther Pat. 2019;29(10):781–792.
   PubMed Web of Science ®Google Scholar
• Lomelino C, McKenna R. Carbonic anhydrase inhibitors: a review on the progress of patent literature (2011–2016). Expert Opin Ther Pat. 2016;26(8):947–956.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhang Y, Zhang Y. Research advances in pathogenesis and prophylactic measures of acute high altitude illness. Respir Med. 2018;145:145–152.
   PubMed Web of Science ®Google Scholar
• Imray C, Wright A, Subudhi A, Roach R. Acute mountain sickness: pathophysiology, prevention, and treatment. Prog Cardiovasc Dis. 2010;52(6):467–484.
   PubMed Web of Science ®Google Scholar
• Davis C, Hackett P. Advances in the prevention and treatment of high altitude illness. Emerg Med Clin North Am. 2017;35(2):241–260.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov. 2017;12(1):61–88.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat. 2018;28(10):709–712.
   PubMed Web of Science ®Google Scholar
• McKenna R, Supuran CT. Carbonic anhydrase inhibitors drug design. Subcell Biochem. 2014;75:291–323.
   PubMedGoogle Scholar
• Supuran CT. Novel carbonic anhydrase inhibitors. Future Med Chem. 2021;13(22):1935–1937.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008;7(2):168–181.
   PubMed Web of Science ®Google Scholar
• Emameh RZ, Syrjänen L, Barker H, Supuran CT, Parkkila S. Drosophila melanogaster: a model organism for controlling Dipteran vectors and pests. J Enzyme Inhib Med Chem. 2015;30(3):505–513.
   PubMed Web of Science ®Google Scholar
• Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol. 2011;7(1):539.
   PubMed Web of Science ®Google Scholar
• Madeira F, Pearce M, Tivey ARN, Basutkar P, Lee J, Edbali O, Madhusoodanan N, Kolesnikov A, Lopez R. Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res. 2022;50(W1):W276–W279.
   PubMed Web of Science ®Google Scholar
• Gouy M, Guindon S, Gascuel O. Sea view version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27(2):221–224.
   PubMed Web of Science ®Google Scholar
• Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188–1190.
   PubMed Web of Science ®Google Scholar
• Robert X, Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014;42(W1):W320–W324.
   PubMed Web of Science ®Google Scholar
• Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A, et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50(D1):D439–D444.
   PubMed Web of Science ®Google Scholar
• Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583–589.
   PubMed Web of Science ®Google Scholar
• Evans R, O’Neill M, Pritzel A, et al. Protein complex prediction with AlphaFold-Multimer. bioRxiv. 2021:2021.10.04.463034.
   Google Scholar
• Naville M, Ghuillot-Gaudeffroy A, Marchais A, Gautheret D. ARNold: a web tool for the prediction of rho-independent transcription terminators. RNA Biol. 2011;8(1):11–13.
   PubMed Web of Science ®Google Scholar
• Urbański LJ, Di Fiore A, Azizi L, Hytönen VP, Kuuslahti M, Buonanno M, Monti SM, Angeli A, Zolfaghari Emameh R, Supuran CT, et al. Biochemical and structural characterisation of a protozoan beta-carbonic anhydrase from Trichomonas vaginalis. J Enzyme Inhib Med Chem. 2020;35(1):1292–1299.
   PubMed Web of Science ®Google Scholar
• Haapanen S, Bua S, Kuuslahti M, Parkkila S, Supuran CT. Cloning, characterization and anion inhibition studies of a β-carbonic anhydrase from the pathogenic protozoan Entamoeba histolytica. Molecules. 2018;23(12):3112.
   PubMed Web of Science ®Google Scholar
• Kopp J, Slouka C, Ulonska S, Kager J, Fricke J, Spadiut O, Herwig C. Impact of glycerol as carbon source onto specific sugar and inducer uptake rates and inclusion body productivity in E. coli BL21(DE3). Bioengineering. 2017;5(1):1.
   PubMedGoogle Scholar
• Khalifah RG. 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(8):2561–2573.
   PubMed Web of Science ®Google Scholar
• Berrino E, Bua S, Mori M, Botta M, Murthy VS, Vijayakumar V, Tamboli Y, Bartolucci G, Mugelli A, Cerbai E, et al. Novel sulfamide-containing compounds as selective carbonic anhydrase I inhibitors. Molecules. 2017;22(7):1049.
   PubMed Web of Science ®Google Scholar
• Urbanski LJ, Bua S, Angeli A, Kuuslahti M, Hytönen VP, Supuran CT, Parkkila S. Sulphonamide inhibition profile of Staphylococcus aureus β-carbonic anhydrase. J Enzyme Inhib Med Chem. 2020;35(1):1834–1839.
   PubMed Web of Science ®Google Scholar
• Bua S, Haapanen S, Kuuslahti M, Parkkila S, Supuran CT. Sulfonamide inhibition studies of a new β-carbonic anhydrase from the pathogenic protozoan entamoeba histolytica. Int J Mol Sci. 2018;19(12):3946.
   PubMed Web of Science ®Google Scholar
• Kimber MS, Pai EF. The active site architecture of Pisum sativum beta-carbonic anhydrase is a mirror image of that of alpha-carbonic anhydrases. EMBO J. 2000;19(7):1407–1418.
   PubMed Web of Science ®Google Scholar
• Vale N, Gouveia MJ, Rinaldi G, Brindley PJ, Gärtner F, Da Costa JMC. Praziquantel for schistosomiasis: single-drug metabolism revisited, mode of action, and resistance. Antimicrob Agents Chemother. 2017;61(5).
   PubMed Web of Science ®Google Scholar
• Li EY, Gurarie D, Lo NC, Zhu X, King CH. Improving public health control of schistosomiasis with a modified WHO strategy: a model-based comparison study. Lancet Glob Health. 2019;7(10):e1414–e1422.
   PubMed Web of Science ®Google Scholar
• Wang W, Wang L, Liang YS. Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitol Res. 2012;111(5):1871–1877.
   PubMed Web of Science ®Google Scholar
• Syrjänen L, Vermelho AB, Rodrigues I. d A, Corte-Real S, Salonen T, Pan P, Vullo D, Parkkila S, Capasso C, Supuran CT. Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Leishmania donovani chagasi, the protozoan parasite responsible for leishmaniasis. J Med Chem. 2013;56(18):7372–7381.
   PubMed Web of Science ®Google Scholar
• Zolfaghari Emameh R, Kuuslahti M, Vullo D, Barker HR, Supuran CT, Parkkila S. Ascaris lumbricoides β carbonic anhydrase: a potential target enzyme for treatment of ascariasis. Parasites Vectors. 2015;8(1).
   PubMedGoogle Scholar
• Khubchandani IT, Bub DS. Parasitic infections. Clin Colon Rectal Surg. 2019;32(5):364–371.
   PubMed Web of Science ®Google Scholar
• Mansour NS, Youssef FG, Mikhail EM, Mohareb EW. Amebiasis in schistosomiasis endemic and non-endemic areas in Egypt. J Egypt Soc Parasitol. 1997;27(3):617–628.
   PubMedGoogle Scholar
• Dolabella SS, Coelho PMZ, Borçari IT, Mello NAST, Andrade ZDA, Silva EF. Morbidity due to Schistosoma mansoni – Entamoeba histolytica coinfection in hamsters (Mesocricetus auratus). Rev Soc Bras Med Trop. 2007;40(2):170–174.
   PubMed Web of Science ®Google Scholar
• Gulati S, Aref AA. Oral acetazolamide for intraocular pressure lowering: balancing efficacy and safety in ophthalmic practice. Expert Rev Clin Pharmacol. 2021;14(8):955–961.
   PubMed Web of Science ®Google Scholar
• Leaf DE, Goldfarb DS. Mechanisms of action of acetazolamide in the prophylaxis and treatment of acute mountain sickness. J Appl Physiol. 2007;102(4):1313–1322.
   PubMed Web of Science ®Google Scholar
• Adamson R, Swenson ER. Acetazolamide use in severe chronic obstructive pulmonary disease pros and cons. Ann Am Thorac Soc. 2017;14(7):1086–1093.
   PubMed Web of Science ®Google Scholar
• Van Berkel MA, Elefritz JL. Evaluating off-label uses of acetazolamide. Am J Health Syst Pharm. 2018;75(8):524–531.
   PubMed Web of Science ®Google Scholar
• Cong-Hui Z, Huai-Min Z. Cloning and characterization of β-carbonic anhydrase, a potential drug target of Schistosoma japonicum. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi. 2016;28(2):161–166.
   PubMedGoogle Scholar
• Llanwarne F, Helmby H. Granuloma formation and tissue pathology in Schistosoma japonicum versus Schistosoma mansoni infections. Parasite Immunol. 2021;43(2):e12778.
   PubMed Web of Science ®Google Scholar