Cloning, expression, and purification of an α-carbonic anhydrase from Toxoplasma gondii to unveil its kinetic parameters and anion inhibition profile.

References

• Acosta Davila JA, Hernandez De Los Rios A. An overview of peripheral blood mononuclear cells as a model for immunological research of Toxoplasma gondii and other apicomplexan parasites. Front Cell Infect Microbiol. 2019;9:1.
   PubMed Web of Science ®Google Scholar
• Kim K, Weiss LM. Toxoplasma gondii: the model apicomplexan. Int J Parasitol. 2004;34(3):423–11.
   PubMed Web of Science ®Google Scholar
• Delgado ILS, Tavares A, Francisco S, Santos D, Coelho J, Basto AP, Zúquete S, Müller J, Hemphill A, Meissner M, et al. Characterization of a MOB1 homolog in the apicomplexan parasite Toxoplasma gondii. Biology (Basel). 2021;10(12):1233–1258.
   PubMedGoogle Scholar
• Herneisen AL, Lourido S. Thermal proteome profiling to identify protein-ligand interactions in the apicomplexan parasite Toxoplasma gondii. Bio Protoc. 2021;11:e4207.
   PubMed Web of Science ®Google Scholar
• Dini FM, Morselli S, Marangoni A, Taddei R, Maioli G, Roncarati G, Balboni A, Dondi F, Lunetta F, Galuppi R. Spread of among animals and humans in Northern Italy: a retrospective analysis in a one-health framework. Food Waterb Parasit. 2023;32:e00197.
   PubMedGoogle Scholar
• de Barros RAM, Torrecilhas AC, Marciano MAM, Mazuz ML, Pereira-Chioccola VL, Fux B. Toxoplasmosis in human and animals around the world. Diagnosis and perspectives in the one health approach. Acta Trop. 2022;231:106432.
   PubMed Web of Science ®Google Scholar
• E SA-M. Toxoplasmosis: stages of the protozoan life cycle and risk assessment in humans and animals for an enhanced awareness and an improved socio-economic status. Saudi J Biol Sci. 2021;28:962–969.
   PubMed Web of Science ®Google Scholar
• Robert-Gangneux F, Dardé M-L. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012;25(2):264–296.
   PubMed Web of Science ®Google Scholar
• Dubey JP, Lindsay DS, Speer CA. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev. 1998;11(2):267–299.
   PubMed Web of Science ®Google Scholar
• Delgado ILS, S Z, Santos D, Basto AP, Leitão A, Nolasco S. The apicomplexan parasite Toxoplasma gondii. Encyclopedia. 2022;2(1):189–211.
   Google Scholar
• Cerutti A, Blanchard N, Besteiro S. The bradyzoite: A key developmental stage for the persistence and pathogenesis of toxoplasmosis. Pathogens. 2020;9(3):234.
   PubMed Web of Science ®Google Scholar
• Sanchez SG, Bassot E, Cerutti A, Mai Nguyen H, Aida A, Blanchard N, Besteiro S. The apicoplast is important for the viability and persistence of Toxoplasma gondii bradyzoites. Proc Natl Acad Sci USA. 2023;120:e2309043120.
   PubMed Web of Science ®Google Scholar
• Zhu W, Li J, Pappoe F, Shen J, Yu L. Strategies developed by Toxoplasma gondii to survive in the host. Front Microbiol. 2019;10:899.
   PubMed Web of Science ®Google Scholar
• Lima TS, Lodoen MB. Mechanisms of human innate immune evasion by Toxoplasma gondii. Front Cell Infect Microbiol. 2019;9:103.
   PubMed Web of Science ®Google Scholar
• Chulanetra M, Chaicumpa W. Revisiting the mechanisms of immune evasion employed by human parasites. Front Cell Infect Microbiol. 2021;11:702125.
   PubMed Web of Science ®Google Scholar
• Fox BA, Guevara RB, Rommereim LM, Falla A, Bellini V, Pètre G, Rak C, Cantillana V, Dubremetz J-F, Cesbron-Delauw M-F, et al. Toxoplasma gondii parasitophorous vacuole membrane-associated dense granule proteins orchestrate chronic infection and GRA12 underpins resistance to host gamma interferon. mBio. 2019;10(4):e00589-19. https://doi.org/10.1128/mBio.00589-19.
   Web of Science ®Google Scholar
• Fisch D, Clough B, Frickel EM. Human immunity to Toxoplasma gondii. PLoS Pathog. 2019;15(12):e1008097.
   PubMed Web of Science ®Google Scholar
• Uddin A, Hossain D, Ahsan MI, Atikuzzaman M, Karim MR. Review on diagnosis and molecular characterization of Toxoplasma gondii in humans and animals. Trop Biomed. 2021;38:511–539.
   PubMed Web of Science ®Google Scholar
• Konstantinovic N, Guegan H, Stäjner T, Belaz S, Robert-Gangneux F. Treatment of toxoplasmosis: current options and future perspectives. Food Waterborne Parasitol. 2019;15:e00036.
   PubMedGoogle Scholar
• Hajj RE, Tawk L, Itani S, Hamie M, Ezzeddine J, El Sabban M, El Hajj H. Toxoplasmosis: current and emerging parasite druggable targets. Microorganisms. 2021;9(12):2531.
   PubMed Web of Science ®Google Scholar
• Spalenka J, Escotte-Binet S, Bakiri A, Hubert J, Renault JH, Velard F, Duchateau S, Aubert D, Huguenin A, Villena I. Discovery of new inhibitors of toxoplasma gondii via the pathogen box. Antimicrob Agents Ch. 2018;62.
   PubMed Web of Science ®Google Scholar
• He TY, Li YT, Liu ZD, Cheng H, Bao YF, Zhang JL. Lipid metabolism: the potential targets for toxoplasmosis treatment. Parasit Vectors. 2024;17(1):111. https://doi.org/10.1186/s13071-024-06213-9. https://doi.org/10.1016/j.fawpar.2019.e00036.
   Google Scholar
• Konstantinovic N, Guegan H, Stajner T, Belaz S, Robert-Gangneux F. Treatment of toxoplasmosis: current options and future perspectives. Food Waterb Parasit. 2019;15:e00036. https://doi.org/10.1016/j.fawpar.2019.e00036.
   PubMedGoogle Scholar
• Robert-Gangneux F. It is not only the cat that did it: how to prevent and treat congenital toxoplasmosis. J Infect. 2014;68 Suppl 1:S125–S133.
   PubMed Web of Science ®Google Scholar
• Torre D, Casari S, Speranza F, Donisi A, Gregis G, Poggio A, Ranieri S, Orani A, Angarano G, Chiodo F, et al. Randomized ­trial of trimethoprim-sulfamethoxazole versus pyrimethamine-sulfadiazine for therapy of toxoplasmic encephalitis in patients with AIDS. Italian Collaborative Study Group. Antimicrob Agents Chemother. 1998;42(6):1346–1349.
   PubMed Web of Science ®Google Scholar
• Valentini P, Annunziata ML, Angelone DF, Masini L, Santis M, Testa A, Grillo RL, Speziale D, Ranno O. Role of spiramycin/cotrimoxazole association in the mother-to-child transmission of toxoplasmosis infection in pregnancy (vol 28, pg 298, 2009). Eur J Clin Microbiol Infect Dis. 2009;28(7):879–879.
   Web of Science ®Google Scholar
• Djurković-Djaković O, Nikolić T, Robert-Gangneux F, Bobić B, Nikolić A. Synergistic effect of clindamycin and atovaquone in acute murine toxoplasmosis. Antimicrob Agents Chemother. 1999;43(9):2240–2244.
   PubMed Web of Science ®Google Scholar
• Heath RJ, Rock CO. Enoyl-acyl carrier protein reductase (Fabi) plays a determinant role in completing cycles of fatty-acid elongation in Escherichia-coli. J Biol Chem. 1995;270(44):26538–26542.
   PubMed Web of Science ®Google Scholar
• Ling Y, Li ZH, Miranda K, Oldfield E, Moreno SNJ. The Farnesyl-diphosphate/geranylgeranyl-diphosphate synthase of Toxoplasma gondii is a bifunctional enzyme and a molecular target of bisphosphonates. J Biol Chem. 2007;282(42):30804–30816.
   PubMed Web of Science ®Google Scholar
• Scheele S, Geiger JA, DeRocher AE, Choi R, Smith TR, Hulverson MA, Vidadala RSR, Barrett LK, Maly DJ, Merritt EA, et al. Toxoplasma calcium-dependent protein kinase 1 inhibitors: probing activity and resistance using cellular thermal shift assays. Antimicrob Agents Ch. 2018;62:e00051-18. https://doi.org/10.1128/AAC.00051-18.
   PubMed Web of Science ®Google Scholar
• Montazeri M, Mehrzadi S, Sharif M, Sarvi S, Shahdin S, Daryani A. Activities of anti-toxoplasma drugs and compounds against tissue cysts in the last three decades (1987 to 2017), a systematic review. Parasitol Res. 2018;117(10):3045–3057.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. The management of Babesia, amoeba and other zoonotic diseases provoked by protozoa. Expert Opin Ther Pat. 2023;33(3):179–192.
   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
• Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites. 2017;7(4):56.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets. 2015;19(12):1689–1704.
   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
• Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci (Lond). 2021;135(10):1233–1249.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Supuran CT, Waheed A, Sly WS, Parkkila S. Mitochondrial carbonic anhydrase VA and VB: properties and roles in health and disease. J Physiol. 2023;601(2):257–274.
   PubMed Web of Science ®Google Scholar
• Aggarwal M, Boone CD, Kondeti B, McKenna R. Structural annotation of human carbonic anhydrases. J Enzyme Inhib Med Chem. 2013;28(2):267–277.
   PubMed Web of Science ®Google Scholar
• Maret W. New perspectives of zinc coordination environments in proteins. J Inorg Biochem. 2012;111:110–116.
   PubMed Web of Science ®Google Scholar
• Emameh RZ, Barker H, Tolvanen MEE, Ortutay C, Parkkila S. Bioinformatic analysis of beta carbonic anhydrase sequences from protozoans and metazoans. Parasite Vector. 2014;7:38–49.
   PubMed Web of Science ®Google Scholar
• Xu F, Lu X, Cheng R, Zhu Y, Miao S, Huang Q, Xu Y, Qiu L, Zhou Y. The influence of exposure to Toxoplasma gondii on host lipid metabolism. BMC Infect Dis. 2020;20(1):415.
   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):e00027-17. https://doi.org/10.1128/mSphere.00027-17.
   PubMed Web of Science ®Google Scholar
• Pan P, Vermelho AB, Scozzafava A, Parkkila S, Capasso C, Supuran CT. Anion inhibition studies of the alpha-carbonic anhydrase from the protozoan pathogen Trypanosoma cruzi, the causative agent of Chagas disease. Bioorg Med Chem. 2013;21(15):4472–4476.
   PubMed Web of Science ®Google Scholar
• Güzel-Akdemir Ö, Akdemir A, Pan PW, Vermelho AB, Parkkila S, Scozzafava A, Capasso C, Supuran CT. A class of sulfonamides with strong inhibitory action against the α-carbonic anhydrase from Trypanosoma cruzi. J Med Chem. 2013;56(14):5773–5781.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Inhibition of carbonic anhydrase from Trypanosoma cruzi for the management of Chagas disease: an underexplored therapeutic opportunity. Future Med Chem. 2016;8(3):311–324.
   PubMed Web of Science ®Google Scholar
• De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem. 2012;111:117–129.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Angeli A, Carta F, Winum JY, Zalubovskis R, Carradori S, Capasso C, Donald WA, Supuran CT. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. J Enzyme Inhib Med Chem. 2021;36(1):561–580.
   PubMed Web of Science ®Google Scholar
• Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–410.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Ghobril C, Hitce J, Clavaud C, Marat X, Capasso C, Supuran CT. Cloning, purification, and characterization of a beta-carbonic anhydrase from malassezia restricta, an opportunistic pathogen involved in dandruff and seborrheic dermatitis. Int J Mol Sci. 2019;20:2447–2458.
   PubMed Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1–2):248–254.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–685.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Iandolo E, Supuran CT, Capasso C. Protonography, a powerful tool for analyzing the activity and the oligomeric state of the gamma-carbonic anhydrase identified in the genome of Porphyromonas gingivalis. Bioorg Med Chem. 2015;23(13):3747–3750.
   PubMed Web of Science ®Google Scholar
• Capasso C, De Luca V, Carginale V, Cannio R, Rossi M. Biochemical properties of a novel and highly thermostable bacterial α-carbonic anhydrase from. J Enzyme Inhib Med Chem. 2012;27(6):892–897.
   PubMed Web of Science ®Google Scholar
• Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797.
   PubMed Web of Science ®Google Scholar
• Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–321.
   PubMed Web of Science ®Google Scholar
• Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296–W303.
   PubMed Web of Science ®Google 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
• Lineweaver H, Dean B. The determination of enzyme dissociation constants. J Am Chem Soc. 1934;56:658–666.
   Google Scholar
• Craig DA. The Cheng-Prusoff relationship – something lost in the translation. Trends Pharmacol Sci. 1993;14(3):89–91.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, Carginale V, di Fonzo P, Osman SM, AlOthman Z, Supuran CT, Capasso C. Anion inhibition profiles of α-, β- and γ-carbonic anhydrases from the pathogenic bacterium. Bioorg Med Chem. 2016;24(16):3413–3417.
   PubMed Web of Science ®Google Scholar
• Sigrist CJA, de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L. Xenarios, I. New and continuing developments at PROSITE. Nucleic Acids Res. 2013;41:E344–E347.
   PubMed Web of Science ®Google Scholar
• Akbary Moghaddam V, Kasmaeifar V, Mahmoodi Z, Ghafouri H, Saberi O, Mohammadi A. A novel sulfamethoxazole derivative as an inhibitory agent against HSP70: a combination of computational with in vitro studies. Int J Biol Macromol. 2021;189:194–205.
   PubMed Web of Science ®Google Scholar
• Somalinga V, Buhrman G, Arun A, Rose RB, Grunden AM. A high-resolution crystal structure of a psychrohalophilic alpha-carbonic anhydrase from Photobacterium profundum reveals a unique dimer interface. PLoS One. 2016;11(12):e0168022.
   PubMed Web of Science ®Google Scholar
• Coppens I. Contribution of host lipids to Toxoplasma pathogenesis. Cell Microbiol. 2006;8(1):1–9.
   PubMed Web of Science ®Google Scholar
• Blume M, Seeber F. Metabolic interactions between Toxoplasma gondii and its host. F1000Res. 2018;7:1719.
   Google Scholar
• Seeber F. Past and present seroprevalence and disease burden estimates of Toxoplasma gondii infections in Germany: an appreciation of the role of serodiagnostics. Int J Med Microbiol. 2023;313(6):151592.
   PubMed Web of Science ®Google Scholar
• Warschkau D, Seeber F. Advances towards the complete in vitro life cycle of Toxoplasma gondii. Fac Rev. 2023;12(1):1.
   PubMedGoogle Scholar
• Hagemann CL, Macedo AJ, Tasca T. Therapeutic potential of antimicrobial peptides against pathogenic protozoa. Parasitol Res. 2024;123(2):122.
   PubMed Web of Science ®Google Scholar
• Chorlton SD. Toxoplasma gondii and schizophrenia: a review of published RCTs. Parasitol Res. 2017;116(7):1793–1799.
   PubMed Web of Science ®Google Scholar
• Han RX, Jiang PC, Han B, Zhou HY, Wang YL, Guan JY, Liu ZR, He SY, Zhou CX. Anti-Toxoplasma gondii effect of tylosin in vitro and in vivo. Parasit Vectors. 2024;17:59.
   PubMed Web of Science ®Google Scholar
• Kuzminac IZ, Savić MP, Ajduković JJ, Nikolić AR. Steroid and triterpenoid compounds with antiparasitic properties. Curr Top Med Chem. 2023;23(9):791–815.
   PubMed Web of Science ®Google Scholar