Identification and characterization of cytosolic malate dehydrogenase from the liver fluke Fasciola gigantica.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
07 08 2020
07 08 2020
Historique:
received:
03
03
2020
accepted:
29
06
2020
entrez:
10
8
2020
pubmed:
10
8
2020
medline:
15
12
2020
Statut:
epublish
Résumé
The liver fluke zoonoses, Fasciola spp. are parasitic helminths infecting humans and animals globally. Recent sequencing of the genome of Fasciola gigantica has provided a basis to understand the biochemistry of this parasite. Here, we identified the cytosolic malate dehydrogenase in F. gigantica (FgMDH) and characterized the enzyme biochemically and structurally. F. gigantica encodes a single cytosolic MDH, a key enzyme of the citric acid cycle. It catalyzes the reversible oxidation of malate to oxaloacetate using NAD
Identifiants
pubmed: 32770017
doi: 10.1038/s41598-020-70202-y
pii: 10.1038/s41598-020-70202-y
pmc: PMC7415141
doi:
Substances chimiques
Recombinant Proteins
0
Malate Dehydrogenase
EC 1.1.1.37
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13372Références
Mas-Coma, S., Bargues, M. D. & Valero, M. A. Fascioliasis and other plant-borne trematode zoonoses. Int. J. Parasitol.35, 1255–1278 (2005).
pubmed: 16150452
Robinson, M. W. & Dalton, J. P. Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philos. Trans. R. Soc. Lond. B Biol. Sci.364, 2763–2776 (2009).
pubmed: 19687044
pmcid: 2865092
Saba, R. et al. Human fascioliasis. Clin. Microbiol. Infect.10, 385–387 (2004).
pubmed: 15113313
Tripathi, T., Suttiprapa, S. & Sripa, B. Unusual thiol-based redox metabolism of parasitic flukes. Parasitol. Int.66, 390–395 (2017).
pubmed: 27238582
Ashrafi, K., Bargues, M. D., O’Neill, S. & Mas-Coma, S. Fascioliasis: a worldwide parasitic disease of importance in travel medicine. Travel Med. Infect. Dis.12, 636–649 (2014).
pubmed: 25287722
Cwiklinski, K., O’Neill, S. M., Donnelly, S. & Dalton, J. P. A prospective view of animal and human Fasciolosis. Parasite Immunol.38, 558–568 (2016).
pubmed: 27314903
pmcid: 5053257
WHO. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015. (World Health Organization, 2015).
Mas-Coma, S., Valero, M. A. & Bargues, M. D. Fascioliasis. Adv. Exp. Med. Biol.766, 77–114 (2014).
pubmed: 24903364
Mas-Coma, S. et al. The Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Trop. Med. Int. Health4, 454–467 (1999).
pubmed: 10444322
Parkinson, M., O’Neill, S. M. & Dalton, J. P. Endemic human fasciolosis in the Bolivian Altiplano. Epidemiol. Infect.135, 669–674 (2007).
pubmed: 17064455
Tolan, R. W. Fascioliasis due to Fasciola hepatica and Fasciola gigantica infection: an update on this “neglected” neglected tropical disease. Lab. Med.42, 107–116 (2011).
Coles, G. C. Anthelmintic activity of triclabendazole. J. Helminthol.60, 210–212 (1986).
pubmed: 3745874
Fairweather, I. Triclabendazole progress report, 2005–2009: an advancement of learning?. J. Helminthol.83, 139–150 (2009).
pubmed: 19366485
Brennan, G. P. et al. Understanding triclabendazole resistance. Exp. Mol. Pathol.82, 104–109 (2007).
pubmed: 17398281
Srinivasan, V. & Morowitz, H. J. Ancient genes in contemporary persistent microbial pathogens. Biol. Bull.210, 1–9 (2006).
pubmed: 16501059
Minarik, P., Tomaskova, N., Kollarova, M. & Antalik, M. Malate dehydrogenases–structure and function. Gen. Physiol. Biophys.21, 257–265 (2002).
pubmed: 12537350
Musrati, R. A., Kollarova, M., Mernik, N. & Mikulasova, D. Malate dehydrogenase: distribution, function and properties. Gen. Physiol. Biophys.17, 193–210 (1998).
pubmed: 9834842
Goward, C. R. & Nicholls, D. J. Malate dehydrogenase: a model for structure, evolution, and catalysis. Protein Sci.3, 1883–1888 (1994).
pubmed: 7849603
pmcid: 2142602
Gietl, C. Malate dehydrogenase isoenzymes: cellular locations and role in the flow of metabolites between the cytoplasm and cell organelles. Biochim. Biophys. Acta1100, 217–234 (1992).
pubmed: 1610875
Chakravarty, K., Cassuto, H., Reshef, L. & Hanson, R. W. Factors that control the tissue-specific transcription of the gene for phosphoenolpyruvate carboxykinase-C. Crit. Rev. Biochem. Mol. Biol.40, 129–154 (2005).
pubmed: 15917397
Davis, W. L. & Goodman, D. B. Evidence for the glyoxylate cycle in human liver. Anat. Rec.234, 461–468 (1992).
pubmed: 1456449
Sakai, S., Inokuma, K., Nakashimada, Y. & Nishio, N. Degradation of glyoxylate and glycolate with ATP synthesis by a thermophilic anaerobic bacterium, Moorella sp. strain HUC22–1. Appl. Environ. Microbiol.74, 1447–1452 (2008).
pubmed: 18083850
Amarneh, B. & Vik, S. B. Direct transfer of NADH from malate dehydrogenase to complex I in Escherichia coli. Cell Biochem. Biophys.42, 251–261 (2005).
pubmed: 15976458
Hall, M. D., Levitt, D. G. & Banaszak, L. J. Crystal structure of Escherichia coli malate dehydrogenase. A complex of the apoenzyme and citrate at 1.87 A resolution. J. Mol. Biol.226, 867–882 (1992).
pubmed: 1507230
Madern, D. Molecular evolution within the L-malate and L-lactate dehydrogenase super-family. J. Mol. Evol.54, 825–840 (2002).
pubmed: 12029364
Nicholls, D. J. et al. The importance of arginine 102 for the substrate specificity of Escherichia coli malate dehydrogenase. Biochem. Biophys. Res. Commun.189, 1057–1062 (1992).
pubmed: 1472016
Singh, R., Lemire, J., Mailloux, R. J. & Appanna, V. D. A novel strategy involved in anti-oxidative defense: the conversion of NADH into NADPH by a metabolic network. PLoS ONE3, e2682 (2008).
Wu, H., Li, Z. M., Zhou, L. & Ye, Q. Improved succinic acid production in the anaerobic culture of an Escherichia coli pflB ldhA double mutant as a result of enhanced anaplerotic activities in the preceding aerobic culture. Appl. Environ. Microbiol.73, 7837–7843 (2007).
pubmed: 17951436
pmcid: 2168152
Fodge, D. W., Gracy, R. W. & Harris, B. G. Studies on enzymes from parasitic helminths. I. Purification and physical properties of malic enzyme from the muscle tissue of Ascaris suum. Biochim. Biophys. Acta268, 271–284 (1972).
pubmed: 4402077
Landsperger, W. J. & Harris, B. G. NAD-malic enzyme. Regulatory properties of the enzyme from Ascaris suum. J. Biol. Chem.251, 3599–3602 (1976).
pubmed: 180002
McNulty, S. N. et al. Genomes of Fasciola hepatica from the Americas reveal colonization with Neorickettsia Endobacteria related to the agents of potomac horse and human Sennetsu Fevers. PLoS Genet.13, e1006537 (2017).
pubmed: 28060841
pmcid: 5257007
Muller, M. et al. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev.76, 444–495 (2012).
pubmed: 22688819
pmcid: 3372258
Hong, S. J., Seong, K. Y., Sohn, W. M. & Song, K. Y. Molecular cloning and immunological characterization of phosphoglycerate kinase from Clonorchis sinensis. Mol. Biochem. Parasitol.108, 207–216 (2000).
pubmed: 10838223
Chan, M. & Sim, T. S. Functional characterization of an alternative [lactate dehydrogenase-like] malate dehydrogenase in Plasmodium falciparum. Parasitol. Res.92, 43–47 (2004).
pubmed: 14598170
Chapman, A. D., Cortes, A., Dafforn, T. R., Clarke, A. R. & Brady, R. L. Structural basis of substrate specificity in malate dehydrogenases: crystal structure of a ternary complex of porcine cytoplasmic malate dehydrogenase, alpha-ketomalonate and tetrahydoNAD. J. Mol. Biol.285, 703–712 (1999).
pubmed: 10075524
Pandey, T. et al. Draft genome of the liver fluke Fasciola gigantica. ACS Omega5, 11084–11091 (2020).
pubmed: 32455229
pmcid: 7241025
Moriyama, S., Nishio, K. & Mizushima, T. Structure of glyoxysomal malate dehydrogenase (MDH3) from Saccharomyces cerevisiae. Acta Crystallogr. F Struct. Biol. Commun.74, 617–624 (2018).
pubmed: 30279312
Zheng, N. et al. Clonorchis sinensis: molecular cloning and functional expression of novel cytosolic malate dehydrogenase. Exp. Parasitol.109, 220–227 (2005).
pubmed: 15755419
Nava, G. et al. Cloning, sequencing and functional expression of cytosolic malate dehydrogenase from Taenia solium: purification and characterization of the recombinant enzyme. Exp. Parasitol.128, 217–224 (2011).
pubmed: 21439955
Lopez-Calcagno, P. E. et al. Cloning, expression and biochemical characterization of mitochondrial and cytosolic malate dehydrogenase from Phytophthora infestans. Mycol. Res.113, 771–781 (2009).
pubmed: 19249364
Lobanov, M., Bogatyreva, N. S. & Galzitskaia, O. V. Radius of gyration is indicator of compactness of protein structure. Mol. Biol. (Mosk)42, 701–706 (2008).
Chen, J., Wang, J. & Zhu, W. Zinc ion-induced conformational changes in new Delphi metallo-beta-lactamase 1 probed by molecular dynamics simulations and umbrella sampling. Phys. Chem. Chem. Phys.19, 3067–3075 (2017).
pubmed: 28079218
Rajendran, V. & Sethumadhavan, R. Drug resistance mechanism of PncA in Mycobacterium tuberculosis. J. Biomol. Struct. Dyn.32, 209–221 (2014).
pubmed: 23383724
Chenna, R. et al. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res.31, 3497–3500 (2003).
pubmed: 12824352
pmcid: 168907
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol.35, 1547–1549 (2018).
pubmed: 29722887
pmcid: 5967553
Wise, D. J., Anderson, C. D. & Anderson, B. M. Purification and kinetic characterization of Haemophilus parasuis malate dehydrogenase. Arch. Biochem. Biophys.344, 176–183 (1997).
pubmed: 9244395
Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res.42, W320-324 (2014).
pubmed: 24753421
pmcid: 4086106
Webb, B. & Sali, A. Comparative protein structure modeling using MODELLER. Curr. Protoc. Bioinformatics54, 5–6 (2016).
pubmed: 27322406
pmcid: 5031415
Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem.25, 1605–1612 (2004).
Wiederstein, M. & Sippl, M. J. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res.35, W407-410 (2007).
pubmed: 17517781
pmcid: 1933241
Laskowski, R. A. et al. PDBsum: a Web-based database of summaries and analyses of all PDB structures. Trends Biochem. Sci.22, 488–490 (1997).
pubmed: 9433130
Bowie, J. U., Luthy, R. & Eisenberg, D. A method to identify protein sequences that fold into a known three-dimensional structure. Science253, 164–170 (1991).
pubmed: 1853201
Frayne, J., Taylor, A., Cameron, G. & Hadfield, A. T. Structure of insoluble rat sperm glyceraldehyde-3-phosphate dehydrogenase (GAPDH) via heterotetramer formation with Escherichia coli GAPDH reveals target for contraceptive design. J. Biol. Chem.284, 22703–22712 (2009).
pubmed: 19542219
pmcid: 2755679
Goodsell, D. S., Morris, G. M. & Olson, A. J. Automated docking of flexible ligands: applications of AutoDock. J. Mol. Recognit.9, 1–5 (1996).
pubmed: 8723313
Shukla, H., Shukla, R., Sonkar, A. & Tripathi, T. Alterations in conformational topology and interaction dynamics caused by L418A mutation leads to activity loss of Mycobacterium tuberculosis isocitrate lyase. Biochem. Biophys. Res. Commun.490, 276–282 (2017).
pubmed: 28610921
Pandey, T. et al. A combined biochemical and computational studies of the rho-class glutathione s-transferase sll1545 of Synechocystis PCC 6803. Int. J. Biol. Macromol.94, 378–385 (2017).
pubmed: 27760379
Sonkar, A. et al. UDP-N-Acetylglucosamine enolpyruvyl transferase (MurA) of Acinetobacter baumannii (AbMurA): structural and functional properties. Int. J. Biol. Macromol.97, 106–114 (2017).
pubmed: 28064057
Shukla, H., Shukla, R., Sonkar, A., Pandey, T. & Tripathi, T. Distant Phe345 mutation compromises the stability and activity of Mycobacterium tuberculosis isocitrate lyase by modulating its structural flexibility. Sci. Rep.7, 1058 (2017).
pubmed: 28432345
pmcid: 5430663
Oostenbrink, C., Villa, A., Mark, A. E. & van Gunsteren, W. F. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem.25, 1656–1676 (2004).
pubmed: 15264259
Schuttelkopf, A. W. & van Aalten, D. M. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr.60, 1355–1363 (2004).
pubmed: 15272157
Hess, B., Bekker, H., Berendsen, H. J. & Fraaije, J. G. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem.18, 1463–1472 (1997).
Ryckaert, J. P., Ciccotti, G. & Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys.23, 327–341 (1977).
Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph.14(33–38), 27–38 (1996).