Special Issue:
动物医学合辑Veterninary Medicine
|
|
|
Lactate dehydrogenase: An important molecule involved in acetamizuril action against Eimeria tenella |
LIU Li-li1*, FEI Chen-zhong1*, DONG Hui1, ZHANG Ke-yu1, Fu Jian-jun2, LI Tao1, XUE Fei-qun1 |
1 Key Laboratory of Animal Parasitology, Ministry of Agriculture/Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, P.R.China
2 East China University of Science and Technology, Shanghai 200237, P.R.China |
|
|
Abstract Lactate dehydrogenase (LDH), a vital enzyme in anaerobic glycolysis, is closely associated with the survival of parasites. Previous studies of some parasites have shown that LDH exhibits unique physicochemical properties and molecular structures and may be an ideal potential target for diagnosis and drug screening. In this study, we aimed to investigate the effects of acetamizuril, a novel anticoccidial compound, on LDH in the second-generation merozoites of Eimeria tenella (mz-LDH). Quantitative real-time PCR, Western blot, immunofluorescence and enzyme activity assays were each applied to detect the changes of mz-LDH. Our results indicated that the mRNA and protein levels of mz-LDH were reduced upon acetamizuril treatment. Immunolocalization of mz-LDH demonstrated that considerable amount of mz-LDH was distributed around or in the nuclei of second-generation merozoites within the untreated group; in contrast, the acetamizuril-treated group had very low level of mz-LDH. Meanwhile, LDH enzyme activity assay suggested that a decreased LDH enzyme activity in both cytoplasm and nucleus of merozoites in the acetamizuril-treated group. Moreover, the induced apoptosis in second-generation merozoites by the acetamizuril was evaluated by detecting caspase 3 activity, and acetamizuril was found to significantly increase caspase 3 activity. The above findings show that LDH may play an important role in the mediating the activity of acetamizuril against coccidiosis, and further investigation into this aspect might contribute to new light on the pathogenesis of E. tenella during its interaction with acetamizuril.
|
Received: 12 July 2019
Accepted:
|
Fund: This work was supported by the National Natural Science Foundation of China (31101857, 31272607 and 31472235). |
Corresponding Authors:
Correspondence LI Tao, E-mail: litao@shvrI.ac.cn, XUE Fei-qun, E-mail: fqxue@shvri.ac.cn
|
About author:
LIU Li-li, E-mail: Liull0728@163.com; * These authors contributed equally to this study.
|
Cite this article:
LIU Li-li, FEI Chen-zhong, DONG Hui, ZHANG Ke-yu, Fu Jian-jun, LI Tao, XUE Fei-qun.
2020.
Lactate dehydrogenase: An important molecule involved in acetamizuril action against Eimeria tenella . Journal of Integrative Agriculture, 19(5): 1332-1339.
|
Abboud J, Storey K B. 2013. Novel control of lactate dehydrogenase from the freeze tolerant wood frog: Role of posttranslational modifications. PeerJ, 1, e12.
Abdelbaset A E, Fox B A, Karram M H, Abd Ellah M R, Bzik D J, Igarashi M. 2017. Lactate dehydrogenase in Toxoplasma gondii controls virulence, bradyzoite differentiation, and chronic infection. PLoS ONE, 12, e0173745.
Atchade P S, Doderer-Lang C, Chabi N, Perrotey S, Abdelrahman T, Akpovi C D, Anani L, Bigot A, Sanni A, Candolfi E. 2013. Is a Plasmodium lactate dehydrogenase (pLDH) enzyme-linked immunosorbent (ELISA)-based assay a valid tool for detecting risky malaria blood donations in Africa? Malaria Journal, 12, 279.
Basco L K, Marquet F, Makler M M, Le Bras J. 1995. Plasmodium falciparum and Plasmodium vivax: lactate dehydrogenase activity and its application for in vitro drug susceptibility assay. Experimental Parasitology, 80, 260–271.
Berwal R, Gopalan N, Chandel K, Prasad G B, Prakash S. 2008. Plasmodium falciparum: Enhanced soluble expression, purification and biochemical characterization of lactate dehydrogenase. Experimental Parasitology, 120, 135–141.
del Cacho E, Gallego M, Francesch M, Quilez J, Sanchez-Acedo C. 2010. Effect of artemisinin on oocyst wall formation and sporulation during Eimeria tenella infection. Parasitology International, 59, 506–511.
Chuan K H, Lim S F, Martin L, Yun C Y, Loh S O H, Lasne F, Song Z W. 2006. Caspase activation, sialidase release and changes in sialylation pattern of recombinant human erythropoietin produced by CHO cells in batch and fed-batch cultures. Cytotechnology, 51, 67–79.
Cook W J, Senkovich O, Hernandez A, Speed H, Chattopadhyay D. 2015. Biochemical and structural characterization of Cryptosporidium parvum lactate dehydrogenase. International Journal of Biological Macromolecules, 74, 608–619.
D’Alessandro S, Silvestrini F, Dechering K, Corbett Y, Parapini S, Timmerman M, Galastri L, Basilico N, Sauerwein R, Alano P, Taramelli D. 2013. A Plasmodium falciparum screening assay for anti-gametocyte drugs based on parasite lactate dehydrogenase detection. The Journal of Antimicrobial Chemotherapy, 68, 2048–2058.
Dalloul R A, Lillehoj H S. 2006. Poultry coccidiosis: Recent advancements in control measures and vaccine development. Expert Review of Vaccines, 5, 143–163.
Denton H, Brown S M, Roberts C W, Alexander J, McDonald V, Thong K W, Coombs G H. 1996. Comparison of the phosphofructokinase and pyruvate kinase activities of Cryptosporidium parvum, Eimeria tenella and Toxoplasma gondii. Molecular of Biochemical Parasitology, 76, 23–29.
Dong H, Wang Y E, Zhao Q P, Han H Y, Zhu S H, Li LJ, Wu Y L, Huang B. 2014. Molecular cloning and characterization of lactate dehydrogenase gene from Eimeria tenella. Parasitology Research, 113, 2915–2923.
Dunn C R, Banfield M J, Barker J J, Higham C W, Moreton K M, Turgut-Balik D, Brady R L, Holbrook J J. 1996. The structure of lactate dehydrogenase from Plasmodium falciparum reveals a new target for anti-malarial design. Nature Structural Biology, 3, 912–915.
Gomez M S, Piper R C, Hunsaker L A, Royer R E, Deck L M, Makler M T, Vander Jagt D L. 1997. Substrate and cofactor specificity and selective inhibition of lactate dehydrogenase from the malarial parasite P. falciparum. Molecular of Biochemical Parasitology, 90, 235–246.
Harmych S E, Sidawy E, Komuniecki R. 1996. Lactate dehydrogenase from the protozoan parasite, Trichomonas vaginalis. Comparative Biochemistry & Physiology (Part B: Biochemistry & Molecular Biology), 115, 405–409.
Jafari R A, Kiani R, Shahriyari A, Asadi F, Hamidinejat H. 2012. Effect of dietary vitamin E on plasma oxidative stress in broiler chicks infected with Eimeria tenella. Comparative Clinical Pathology, 21, 895–899.
Jelinek T, Kilian A H, Henk M, Mughusu E B, Nothdurft H D, Loscher T, Knobloch J, Van Sonnenburg F. 1996. Parasite-specific lactate dehydrogenase for the diagnosis of Plasmodium falciparum infection in an endemic area in west Uganda. Tropical Medicine & International Health, 1, 227–230.
Jenkins M C, O’Brien C N, Fuller L, Mathis G F, Fetterer R. 2014. A rapid method for determining salinomycin and monensin sensitivity in Eimeria tenella. Veterinary Parasitology, 206, 153–158.
Koiri R K, Trigun S K, Mishra L, Pandey K, Dixit D, Dubey S K. 2009. Regression of Dalton’s lymphoma in vivo via decline in lactate dehydrogenase and induction of apoptosis by a ruthenium(II)-complex containing 4-carboxy N-ethylbenzamide as ligand. Investigational New Drugs, 27, 503–516.
Lee S, Song K M, Jeon W, Jo H, Shim Y B, Ban C. 2012. A highly sensitive aptasensor towards Plasmodium lactate dehydrogenase for the diagnosis of malaria. Biosensors & Bioelectronics, 35, 291–296.
Liu L H, Xu L X, Yan F B, Yan R F, Song X K, Li X R. 2009. Immunoproteomic analysis of the second-generation merozoite proteins of Eimeria tenella. Veterinary Parasitology, 164, 173–182.
Liu L L, Chen H, Fei C, Wang X, Zheng W, Wang M, Zhang K, Zhang L, Li T, Xue F. 2016a. Ultrastructural effects of acetamizuril on endogenous phases of Eimeria tenella. Parasitology Research, 115, 1245–1252.
Liu L L, Chen Z G, Mi R S, Zhang K Y, Liu Y C, Jiang W, Fei C Z, Xue F Q, Li T. 2016b. Effect of acetamizuril on enolase in second-generation merozoites of Eimeria tenella. Veterinary Parasitology, 215, 88–91.
Livak K J, SchmittgenT D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.
Lu G, Hu X C, Huang C, Lu Y J, Wu L X, Li L H, Xu J, Yu X B. 2010a. Effect of artmether, hemin and Fe3+ on recombinant lactate dehydrogenase from Schistosoma japonicum. Asian Pacific Journal of Tropical Medicine, 3, 930–933.
Lu G, Lu Y J, Li L H, Wu L X, Fan Z G, Shi D Z, Wang H, Han X M. 2010b. Identification and bioinformatics analysis of lactate dehydrogenase genes from Echinococcus granulosus. Asian Pacific Journal of Tropical Medicine, 3, 757–761.
Makler M T, Piper R C, Milhous W K. 1998. Lactate dehydrogenase and the diagnosis of malaria. Parasitology Today, 14, 376–377.
Matsubayashi M, Hatta T, Miyoshi T, Anisuzzaman Sasai K, Shimura K, Isobe T, Kita K, Tsuji N. 2013. High-throughput RNA sequencing profiles and transcriptional evidence of aerobic respiratory enzymes in sporulating oocysts and sporozoites of Eimeria tenella. Infection, Genetics and Evolution, 18, 269–276.
Menting J G, Tilley L, Deady L W, Ng K, Simpson R J, Cowman A F, Foley M. 1997. The antimalarial drug, chloroquine, interacts with lactate dehydrogenase from Plasmodium falciparum. Molecular and Biochemistry Parasitology, 88, 215–224.
Miao P, Sheng S, Sun X, Liu J, Huang G. 2013. Lactate dehydrogenase A in cancer: A promising target for diagnosis and therapy. IUBMB Life, 65, 904–910.
Ojimelukwe A E, Emedhem D E, Agu G O, Nduka F O, Abah A E. 2018. Populations of Eimeria tenella express resistance to commonly used anticoccidial drugs in southern Nigeria. International Journal of Veterinary Science and Medicine, 6, 192–200.
Peek H W, Landman W J M. 2011. Coccidiosis in poultry: Anticoccidial products, vaccines and other prevention strategies. Veterinary Quarterly, 31, 143–161.
Read J A, Wilkinson K W, Tranter R, Sessions R B, Brady R L. 1999. Chloroquine binds in the cofactor binding site of Plasmodium falciparum lactate dehydrogenase. Journal of Biological Chemistry, 274, 10213–10218.
Schaap D, Arts G, Kroeze J, Niessen R, Roosmalen-Vos S V, Spreeuwenberg K, Kuiper C M, Beek-Verhoeven N V D, Kok J J, Knegtel R M A, Vermeulen A N. 2004. An Eimeria vaccine candidate appears to be lactate dehydrogenase; characterization and comparative analysis. Parasitology, 128, 603–616.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.
Shen X, Wang C, Zhu Q, Li T, Yu L, Zheng W, Fei C, Qiu M, Xue F. 2012. Effect of the diclazuril on Hsp90 in the second-generation merozoites of Eimeria tenella. Veterinary Parasitology, 185, 290–295.
Shen X J, Li T, Fu J J, Zhang K Y, Wang X Y, Liu Y C, Zhang H J, Fan C, Fei C Z, Xue F Q. 2014. Proteomic analysis of the effect of diclazuril on second-generation merozoites of Eimeria tenella. Parasitology Research, 113, 903–909.
Shirley M W. 1995. Eimeria species and strains of chickens. In: Eckert J, Braun R, Shirley M W, Coudert P, eds., Biotechnology-guidelines on Techniques in Coccidiosis Research. European Commission DGXII, Luxembourg, pp. 1–24.
Singh V, Kaushal D C, Rathaur S, Kumar N, Kaushal N A. 2012. Cloning, overexpression, purification and characterization of Plasmodium knowlesi lactate dehydrogenase. Protein Expression and Purification, 84, 195–203.
Song H, Yan R, Xu L, Song X, Shah M A, Zhu H, Li X. 2010. Efficacy of DNA vaccines carrying Eimeria acervulina lactate dehydrogenase antigen gene against coccidiosis. Experimental Parasitology, 126, 224–231.
Song T, Gan W, Chen J, Huang L, Yin H, He T, Huang H, Hu X. 2016. Antibodies against Clonorchis sinensis LDH could cross-react with LDHB localizing on the plasma membrane of human hepatocarcinoma cell SMMC-7721 and induce apoptosis. Parasitology Research, 115, 1595–1603.
Sun H, Wang L J, Wang T T, Zhang J, Liu Q, Chen P P, Chen Z T, Wang F K, Li H M, Xiao Y H, Zhao X M. 2014. Display of Eimeria tenella EtMic2 protein on the surface of Saccharomyces cerevisiae as a potential oral vaccine against chicken coccidiosis. Vaccine, 32, 1869–1876.
Thielmann H W, Popanda O, Fox G. 1995. The nuclear form of lactate dehydrogenase modulates uvinduced DNA repair synthesis in human fibroblasts. Journal of Cancer Research and Clinical Oncology, 121, A16-A16.
Turgut-Balik D, Shoemark D K, Sessions R B, Moreton K M, Holbrook J J. 2001. Mutagenic exploration of the active site of lactate dehydrogenase from Plasmodium falciparum. Biotechnology Letters, 23, 923–927.
Venkatas J, Adeleke M A. 2019. Emerging threat of Eimeria operational taxonomic units (OTUs) on poultry production. Parasitology, 146, 1615–1619.
Vivas L, Easton A, Kendrick H, Cameron A, Lavandera J, Barros D, de las Heras F G, Brady R L, Croft S L. 2005. Plasmodium falciparum: Stage specific effects of a selective inhibitor of lactate dehydrogenase. Experimental Parasitology, 111, 105–114.
Wang C, Han C, Li T, Yang D, Shen X, Fan Y, Xu Y, Zheng W, Fei C, Zhang L, Xue F. 2013. Nuclear translocation and accumulation of glyceraldehyde-3-phosphate dehydrogenase involved in diclazuril-induced apoptosis in Eimeria tenella (E. tenella). Veterinary Research, 44, 29.
Williams R B. 2002. Anticoccidial vaccines for broiler chickens: Pathways to success. Avian Pathology, 31, 317–353.
Winter V J, Cameron A, Tranter R, Sessions R B, Brady R L. 2003. Crystal structure of Plasmodium berghei lactate dehydrogenase indicates the unique structural differences of these enzymes are shared across the Plasmodium genus. Molecular and Biochemistry Parasitology, 131, 1–10.
Zheng J, Gong P T, Jia H L, Li M Y, Zhang G C, Zhang X C, Li J H. 2014. Eimeria tenella rhomboid 3 has a potential role in microneme protein cleavage. Veterinary Parasitology, 201, 146–149.
Zhou B H, Wang H, Xue F, Wang X, Fei C, Wang M, Zhang T, Yao X, He P. 2010. Effects of diclazuril on apoptosis and mitochondrial transmembrane potential in second-generation merozoites of Eimeria tenella. Veterinary Parasitology, 168, 217–222.
|
No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|