Molecular Characteristics of the Malate Dehydrogenase (MDH) Gene Family in Spirometra mansoni (Cestoda: Diphyllobothriidea)
Abstract
:1. Introduction
2. Results
2.1. MDHs in Medical Platyhelminths
2.2. Manual Annotation of SmMDH Genes
2.3. Cloning, Expression and Identification of rSmMDH1
2.4. Enzyme Kinetics
3. Discussion
4. Materials and Methods
4.1. Ethical Approval
4.2. Samples and Experimental Animals
4.3. SmMDH Family Member Identification
4.4. Quantitative RT-PCR Analysis
4.5. Phylogenetic Analysis
4.6. Cloning, Expression and Identification of rSmMDH
4.7. Enzyme Activity Assays
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Chen, W.Q.; Liu, S.S.; Cheng, C.; Cui, J.; Wang, Z.Q.; Zhang, X. Molecular characteristics of glutathione transferase gene family in a neglect medical Spirometra tapeworm. Front. Vet. Sci. 2022, 9, 1035767. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Gao, F.; Wang, R.; Li, W.; Wang, S.; Zhang, X. Molecular Characteristics of the Fatty-Acid-Binding Protein (FABP) Family in Spirometra mansoni-A Neglected Medical Tapeworm. Animals 2023, 13, 2855. [Google Scholar] [CrossRef]
- Wang, R.J.; Li, W.; Liu, S.N.; Wang, S.Y.; Jiang, P.; Wang, Z.Q.; Zhang, X. Integrated transcriptomic and proteomic analyses of plerocercoid and adult Spirometra mansoni reveal potential important pathways in the development of the medical tapeworm. Parasit Vectors 2023, 16, 316. [Google Scholar] [CrossRef] [PubMed]
- Musrati, R.A.; Kollárová, M.; Mernik, N.; Mikulásová, D. Malate dehydrogenase: Distribution, function and properties. Gen. Physiol. Biophys. 1998, 17, 193–210. [Google Scholar] [PubMed]
- Madern, D. Molecular evolution within the L-malate and L-lactate dehydrogenase super-family. J. Mol. Evol. 2002, 54, 825–840. [Google Scholar] [CrossRef] [PubMed]
- Minárik, P.; Tomásková, N.; Kollárová, M.; Antalík, M. Malate dehydrogenases—structure and function. Gen. Physiol. Biophys. 2002, 21, 257–265. [Google Scholar] [PubMed]
- Goward, C.R.; Nicholls, D.J. Malate dehydrogenase: A model for structure, evolution, and catalysis. Protein Sci. 1994, 3, 1883–1888. [Google Scholar] [CrossRef]
- Gietl, C. Malate dehydrogenase isoenzymes: Cellular locations and role in the flow of metabolites between the cytoplasm and cell organelles. Biochim. Biophys. Acta 1992, 1100, 217–234. [Google Scholar] [CrossRef] [PubMed]
- 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. 2005, 40, 129–154. [Google Scholar] [CrossRef]
- Davis, W.L.; Goodman, D.B. Evidence for the glyoxylate cycle in human liver. Anat. Rec. 1992, 234, 461–468. [Google Scholar] [CrossRef]
- 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. 2008, 74, 1447–1452. [Google Scholar] [CrossRef]
- Amarneh, B.; Vik, S.B. Direct transfer of NADH from malate dehydrogenase to complex I in Escherichia coli. Cell Biochem. Biophys. 2005, 42, 251–261. [Google Scholar] [CrossRef]
- Singh, R.; Lemire, J.; Mailloux, R.J.; Appanna, V.D. A novel strategy involved in [corrected] anti-oxidative defense: The conversion of NADH into NADPH by a metabolic network. PLoS ONE 2008, 3, e2682. [Google Scholar] [CrossRef]
- 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. 2007, 73, 7837–7843. [Google Scholar] [CrossRef] [PubMed]
- 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. Acta 1972, 268, 271–284. [Google Scholar] [CrossRef] [PubMed]
- Landsperger, W.J.; Harris, B.G. NAD-malic enzyme. Regulatory properties of the enzyme from Ascaris suum. J. Biol. Chem. 1976, 251, 3599–3602. [Google Scholar] [PubMed]
- McNulty, S.N.; Tort, J.F.; Rinaldi, G.; Fischer, K.; Rosa, B.A.; Smircich, P.; Fontenla, S.; Choi, Y.J.; Tyagi, R.; Hallsworth-Pepin, K.; 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. 2017, 13, e1006537. [Google Scholar] [CrossRef]
- Yoon, S.J.; Koo, D.B.; Lee, K.A. Role of cytosolic malate dehydrogenase in oocyte maturation and embryo development. Fertil. Steril. 2006, 86, 1129–1136. [Google Scholar] [CrossRef] [PubMed]
- Lo, A.S.Y.; Liew, C.T.; Waye, M.M.Y. Developmental regulation and cellular distribution of human cytosolic malate dehydrogenase (MDH1). J. Cell. Biochem. 2005, 94, 763–773. [Google Scholar] [CrossRef]
- Tomaz, T.; Bagard, M.; Pracharoenwattana, I.; Lindén, P.; Lee, C.P.; Carroll, A.J.; Ströher, E.; Smith, S.M.; Gardeström, P.; Millar, A.H. Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis. Plant Physiol. 2010, 154, 1143–1157. [Google Scholar] [CrossRef]
- Chetri, P.B.; Shukla, R.; Tripathi, T. Identification and characterization of cytosolic malate dehydrogenase from the liver fluke Fasciola gigantica. Sci. Rep. 2020, 10, 13372. [Google Scholar] [CrossRef] [PubMed]
- Montes, C.L.; Zuñiga, E.I.; Vazquez, J.; Arce, C.; Gruppi, A. Trypanosoma cruzi mitochondrial malate dehydrogenase triggers polyclonal B-cell activation. Clin. Exp. Immunol. 2002, 127, 27–36. [Google Scholar] [CrossRef] [PubMed]
- Nava, G.; Laclette, J.P.; Bobes, R.; Carrero, J.C.; Reyes-Vivas, H.; Enriquez-Flores, S.; Mendoza-Hernández, G.; Plancarte, A. Cloning, sequencing and functional expression of cytosolic malate dehydrogenase from Taenia solium: Purification and characterization of the recombinant enzyme. Exp. Parasitol. 2011, 128, 217–224. [Google Scholar] [CrossRef] [PubMed]
- Grant, P.M.; Roderick, S.L.; Grant, G.A.; Banaszak, L.J.; Strauss, A.W. Comparison of the precursor and mature forms of rat heart mitochondrial malate dehydrogenase. Biochemistry 1987, 26, 128–134. [Google Scholar] [CrossRef] [PubMed]
- Dasika, S.K.; Vinnakota, K.C.; Beard, D.A. Characterization of the kinetics of cardiac cytosolic malate dehydrogenase and comparative analysis of cytosolic and mitochondrial isoforms. Biophys. J. 2015, 108, 420–430. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Ma, B.; Wang, C.; Chen, X.; Ruan, Y.L.; Yuan, Y.; Ma, F.; Li, M. MdWRKY126 modulates malate accumulation in apple fruit by regulating cytosolic malate dehydrogenase (MdMDH5). Plant Physiol. 2022, 188, 2059–2072. [Google Scholar] [CrossRef] [PubMed]
- Selinski, J.; König, N.; Wellmeyer, B.; Hanke, G.T.; Linke, V.; Neuhaus, H.E.; Scheibe, R. The plastid-localized NAD-dependent malate dehydrogenase is crucial for energy homeostasis in developing Arabidopsis thaliana seeds. Mol. Plant. 2014, 7, 170–186. [Google Scholar] [CrossRef] [PubMed]
- Schreier, T.B.; Cléry, A.; Schläfli, M.; Galbier, F.; Stadler, M.; Demarsy, E.; Albertini, D.; Maier, B.A.; Kessler, F.; Hörtensteiner, S.; et al. Plastidial NAD-Dependent Malate Dehydrogenase: A Moonlighting Protein Involved in Early Chloroplast Development through Its Interaction with an FtsH12-FtsHi Protease Complex. Plant Cell 2018, 30, 1745–1769. [Google Scholar] [CrossRef] [PubMed]
- Beeler, S.; Liu, H.C.; Stadler, M.; Schreier, T.; Eicke, S.; Lue, W.L.; Truernit, E.; Zeeman, S.C.; Chen, J.; Kötting, O. Plastidial NAD-dependent malate dehydrogenase is critical for embryo development and heterotrophic metabolism in Arabidopsis. Plant Physiol. 2014, 164, 1175–1190. [Google Scholar] [CrossRef]
- Teng, X.; Zhong, M.; Zhu, X.; Wang, C.; Ren, Y.; Wang, Y.; Zhang, H.; Jiang, L.; Wang, D.; Hao, Y.; et al. FLOURY ENDOSPERM16 encoding a NAD-dependent cytosolic malate dehydrogenase plays an important role in starch synthesis and seed development in rice. Plant Biotechnol. J. 2019, 17, 1914–1927. [Google Scholar] [CrossRef]
- Wang, Q.J.; Sun, H.; Dong, Q.L.; Sun, T.Y.; Jin, Z.X.; Hao, Y.J.; Yao, Y.X. The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant Biotechnol. J. 2016, 14, 1986–1997. [Google Scholar] [CrossRef]
- Nan, N.; Wang, J.; Shi, Y.; Qian, Y.; Jiang, L.; Huang, S.; Liu, Y.; Wu, Y.; Liu, B.; Xu, Z.Y. Rice plastidial NAD-dependent malate dehydrogenase 1 negatively regulates salt stress response by reducing the vitamin B6 content. Plant Biotechnol. J. 2020, 18, 172–184. [Google Scholar] [CrossRef] [PubMed]
- Hopp, T.P.; Woods, K.R. Prediction of protein antigenic determinants from amino acid sequences. Proc. Natl. Acad. Sci. USA 1981, 78, 3824–3828. [Google Scholar] [CrossRef]
- Chen, Q.; Li, C.; Zheng, G.; Yu, H.; Xu, J. Computational analysis of structure-activity relationship of industrial enzymes. Sheng Wu Gong Cheng Xue Bao 2019, 35, 1829–1842. (In Chinese) [Google Scholar] [PubMed]
- Nicholls, D.J.; Miller, J.; Scawen, M.D.; Clarke, A.R.; Holbrook, J.J.; Atkinson, T.; Goward, C.R. The importance of arginine 102 for the substrate specificity of Escherichia coli malate dehydrogenase. Biochem. Biophys. Res. Commun. 1992, 189, 1057–1062. [Google Scholar] [CrossRef]
- Liu, S.; Zhou, K.; Gao, F.; Li, W.; Wang, Z.; Zhang, X. Lactate Dehydrogenase Gene Family in Spirometra mansoni (Cestoda: Diphyllobothriidea)-Phylogenetic Patterns and Molecular Characteristics. Animals 2023, 13, 3642. [Google Scholar] [CrossRef] [PubMed]
- Medina-Puche, L.; Tan, H.; Dogra, V.; Wu, M.; Rosas-Diaz, T.; Wang, L.; Ding, X.; Zhang, D.; Fu, X.; Kim, C.; et al. A Defense Pathway Linking Plasma Membrane and Chloroplasts and Co-opted by Pathogens. Cell 2020, 182, 1109–1124.e25. [Google Scholar] [CrossRef]
- Yokochi, Y.; Yoshida, K.; Hahn, F.; Miyagi, A.; Wakabayashi, K.I.; Kawai-Yamada, M.; Weber, A.P.M.; Hisabori, T. Redox regulation of NADP-malate dehydrogenase is vital for land plants under fluctuating light environment. Proc. Natl. Acad. Sci. USA 2021, 118, e2016903118. [Google Scholar] [CrossRef]
- Cassman, M.; Englard, S. Beef heart malic dehydrogenases. V. A kinetic study of the reaction catalyzed by the supernatant enzyme. J. Biol. Chem. 1966, 241, 793–799. [Google Scholar] [CrossRef]
- Silverstein, E.; Sulebele, G. Equilibrium kinetic study of the mechanism of mitochondrial and supernatant malate dehydrogenases of bovine heart. Biochim. Biophys. Acta 1969, 185, 297–304. [Google Scholar] [CrossRef]
- Mueggler, P.A.; Wolfe, R.G. Malate dehydrogenase. Kinetic studies of substrate activation of supernatant enzyme by L-malate. Biochemistry 1978, 17, 4615–4620. [Google Scholar] [CrossRef]
- Sorribas, A.; Puig, J.; Cortés, A.; Bozal, J. Thermal stability of the molecular forms of guinea-pig skeletal muscle cytoplasmic malate dehydrogenase and kinetic mechanism of the thermostable form. Int. J. Biochem. 1981, 13, 355–364. [Google Scholar] [CrossRef] [PubMed]
- Baró, J.; Cortés, A.; Bozal Fés, J. Influence of pH on the kinetic mechanism of chicken liver cytoplasmic malate dehydrogenase (B form). Int. J. Biochem. 1981, 13, 463–469. [Google Scholar] [CrossRef] [PubMed]
- Frieden, C.; Fernandez-Sousa, J. Kinetic studies on pig heart cytoplasmic malate dehydrogenase. J. Biol. Chem. 1975, 250, 2106–2113. [Google Scholar] [CrossRef] [PubMed]
- Lodola, A.; Shore, J.D.; Parker, D.M.; Holbrook, J. Malate dehydrogenase of the cytosol. A kinetic investigation of the reaction mechanism and a comparison with lactate dehydrogenase. Biochem. J. 1978, 175, 987–998. [Google Scholar] [CrossRef]
- Crow, K.E.; Braggins, T.J.; Hardman, M.J. Human liver cytosolic malate dehydrogenase: Purification, kinetic properties, and role in ethanol metabolism. Arch. Biochem. Biophys. 1983, 225, 621–629. [Google Scholar] [CrossRef]
- Chapman, A.D.; Cortés, 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. 1999, 285, 703–712. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Hong, X.; Duan, J.Y.; Han, L.L.; Hong, Z.Y.; Jiang, P.; Wang, Z.Q.; Cui, J. Development of EST-derived microsatellite markers to investigate the population structure of sparganum—the causative agent of zoonotic sparganosis. Parasitology 2019, 146, 947–955. [Google Scholar] [CrossRef]
- Kuchta, R.; Kołodziej-Sobocińska, M.; Brabec, J.; Młocicki, D.; Sałamatin, R.; Scholz, T. Sparganosis (Spirometra) in Europe in the Molecular Era. Clin. Infect. Dis. 2021, 72, 882–890. [Google Scholar] [CrossRef]
- Zhang, X.; Hong, X.; Liu, S.N.; Jiang, P.; Zhao, S.C.; Sun, C.X.; Wang, Z.Q.; Cui, J. Large-scale survey of a neglected agent of sparganosis Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidae) in wild frogs in China. PLoS Negl. Trop. Dis. 2020, 14, e0008019. [Google Scholar] [CrossRef]
- Iwata, S. Experimental and morphological studies of Manson’s tapeworm, Diphyllobothrium erinacei, Rudolphi. Special reference with its scientific name and relationship with Sparganum proliferum, Ijima. Progr. Med. Parasitol. Jpn. 1972, 4, 536–590. [Google Scholar]
- Liu, S.N.; Su, X.Y.; Chen, W.Q.; Yu, J.W.; Li, J.R.; Jiang, P.; Cui, J.; Wang, Z.Q.; Zhang, X. Transcriptome profiling of plerocercoid and adult developmental stages of the neglected medical tapeworm Spirometra erinaceieuropaei. Acta Trop. 2022, 232, 106483. [Google Scholar] [CrossRef] [PubMed]
- Potter, S.C.; Luciani, A.; Eddy, S.R.; Park, Y.; Lopez, R.; Finn, R.D. HMMER web server: 2018 update. Nucleic Acids Res. 2018, 46, W200–W204. [Google Scholar] [CrossRef]
- Johansson, M.U.; Zoete, V.; Michielin, O.; Guex, N. Defining and searching for structural motifs using DeepView/Swiss-PdbViewer. BMC Bioinform. 2012, 13, 173. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.N.; Wang, Z.Q.; Zhang, X.; Jiang, P.; Qi, X.; Liu, R.D.; Zhang, Z.F.; Cui, J. Characterization of Spirometra erinaceieuropaei Plerocercoid Cysteine Protease and Potential Application for Serodiagnosis of Sparganosis. PLoS Negl. Trop. Dis. 2015, 9, e0003807. [Google Scholar] [CrossRef]
- Lal, A.; Roudebush, W.E.; Mainigi, M.; Chosed, R.J. Fluorescent-dependent comparative Ct method for qPCR gene expression analysis in IVF clinical pre-implantation embryonic testing. Biol. Methods Protoc. 2021, 6, bpab001. [Google Scholar] [CrossRef]
- Bailey, T.L.; Johnson, J.; Grant, C.E.; Noble, W.S. The MEME Suite. Nucleic Acids Res. 2015, 43, W39–W49. [Google Scholar] [CrossRef] [PubMed]
- Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef]
- Ronquist, F.; Teslenko, M.; van der Mark, P.; Ayres, D.L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M.A.; Huelsenbeck, J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012, 61, 539–542. [Google Scholar] [CrossRef]
Gene Name | Gene ID | MDH Domain Coordinates | Protein Length (aa) | Domain Length (aa) |
---|---|---|---|---|
SmMDH1 | SERJ2_LOCUS4602 | 157–324 | 331 | 168 |
SmMDH2 | SPER_0002854401 | 6–153, 157–198 | 198 | 148, 42 |
SmMDH3 | SPER_0003366401 | 1–61, 63–157 | 157 | 61, 95 |
SmMDH4 | SERJ2_LOCUS18211 | 29–172, 32–116, 174–337 | 343 | 144, 85, 263 |
SmMDH5 | TRINITY_DN32812_c0_g1_i1 | 11–114 | 123 | 104 |
SmMDH6 | TRINITY_DN32812_c0_g1_i9 | 11–114 | 123 | 104 |
SmMDH7 | TRINITY_DN32812_c0_g1_i10 | 11–114 | 123 | 104 |
SmMDH8 | TRINITY_DN32812_c0_g1_i11 | 11–114 | 123 | 104 |
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Wang, R.; Hao, J.; Cao, C.; Li, J.; Zhang, X. Molecular Characteristics of the Malate Dehydrogenase (MDH) Gene Family in Spirometra mansoni (Cestoda: Diphyllobothriidea). Int. J. Mol. Sci. 2024, 25, 8802. https://doi.org/10.3390/ijms25168802
Wang R, Hao J, Cao C, Li J, Zhang X. Molecular Characteristics of the Malate Dehydrogenase (MDH) Gene Family in Spirometra mansoni (Cestoda: Diphyllobothriidea). International Journal of Molecular Sciences. 2024; 25(16):8802. https://doi.org/10.3390/ijms25168802
Chicago/Turabian StyleWang, Ruijie, Jie Hao, Chengyue Cao, Jing Li, and Xi Zhang. 2024. "Molecular Characteristics of the Malate Dehydrogenase (MDH) Gene Family in Spirometra mansoni (Cestoda: Diphyllobothriidea)" International Journal of Molecular Sciences 25, no. 16: 8802. https://doi.org/10.3390/ijms25168802