Abstract
Enolase is a crucial enzyme involved in the glycolytic pathway and gluconeogenesis in parasites. It also has been reported to function as a plasminogen receptor and may be involved in tissue invasion. In this study, the biochemical properties of the enolase of Spirometra mansoni (Smenolase) were investigated. The Smenolase gene was found to cluster closely with the enolase genes of Clonorchis sinensis and Echinococcus granulosus, and some functional motifs were identified as conserved. Smenolase was confirmed to be a component of the secretory/excretory products (ESPs) and a circulating antigen of spargana. Recombinant Smenolase expressed in vitro was able to bind to human plasminogen. Smenolase was detected in the eggs, testicles, and vitellaria of adult worms and the tegument of spargana. The transcription level of Smenolase was highest at the gravid proglottid stage. When spargana were cultured with glucose of different concentration in vitro, it was observed that the expression levels of Smenolase in the low-glucose groups were consistent with that of Smenolase in vivo. These results indicate that Smenolase is a critical enzyme involved in supplying energy to support the development and reproduction of the parasite, and it may also play a role in sparganum invasion.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn SK, Choi HJ, Kim JH (2019) Subcutaneous sparganosis on abdomen mimicking multiple lipomas. Korean J Parasitol 57(5):513–516. https://doi.org/10.3347/kjp.2019.57.5.513
Anantaphruti MT, Nawa Y, Vanvanitchai Y (2011) Human sparganosis in Thailand: an overview. Acta Trop 118(3):171–176. https://doi.org/10.1016/j.actatropica.2011.03.011
Beltran Fabian M, Somocursio Peralta J, Coras Alvarez N et al (2015) Ocular infestation by plerocercoid of Spirometra mansonoides: first case report in Peru. Rev Peru Med Exp Salud Publica 32(2):391–394
Bhowmick IP, Kumar N, Sharma S et al (2009) Plasmodium falciparum enolase: stage-specific expression and sub-cellular localization. Malar J 8:179. https://doi.org/10.1186/1475-2875-8-179
Cayir E, Erdemir A, Ozkan E, Topuzogullari M, Bolat ZB, Akat A, Turgut-Balik D (2014) Cloning of intron-removed enolase gene and expression, purification, kinetic characterization of the enzyme from Theileria annulata. Mol Biotechnol 56(8):689–696. https://doi.org/10.1007/s12033-014-9747-z
Chai JY (2013) Praziquantel treatment in trematode and cestode infections: an update. Infect Chemother 45(1):32–43. https://doi.org/10.3947/ic.2013.45.1.32
da Fonseca Pires S, Fialho LC Jr, Silva SO et al (2014) Identification of virulence factors in Leishmania infantum strains by a proteomic approach. J Proteome Res 13(4):1860–1872. https://doi.org/10.1021/pr400923g
Figueiredo BC, Da'dara AA, Oliveira SC et al (2015) Schistosomes enhance plasminogen activation: the role of tegumental enolase. PLoS Pathog 11(12):e1005335. https://doi.org/10.1371/journal.ppat.1005335
Gupta R, Kumar V, Kushawaha PK, Tripathi CP, Joshi S, Sahasrabuddhe AA, Mitra K, Sundar S, Siddiqi MI, Dube A (2014) Characterization of glycolytic enzymes--rAldolase and rEnolase of Leishmania donovani, identified as Th1 stimulatory proteins, for their immunogenicity and immunoprophylactic efficacies against experimental visceral leishmaniasis. PLoS One 9(1):e86073. https://doi.org/10.1371/journal.pone.0086073
Huang JM, Zhong SF, Lu G et al (2014) Establishment cultive systerm and experimental observation of Spargana mansoni in vitro. Hainan Med J 25(12):1723–1724. [In Chinese]. https://doi.org/10.3969/j.issn.1003-6350.2014.12.0671
Hong D, Xie H, Wan H, An N, Xu C, Zhang J (2018) Efficacy comparison between long-term high-dose praziquantel and surgical therapy for cerebral sparganosis: A multicenter retrospective cohort study. PLoS Negl Trop Dis 12(10):e0006918. https://doi.org/10.1371/journal.pntd.0006918
Jiang P, Zao YJ, Yan SW, Song YY, Yang DM, Dai LY, Liu RD, Zhang X, Wang ZQ, Cui J (2019) Molecular characterization of a Trichinella spiralis enolase and its interaction with the host's plasminogen. Vet Res 50(1):106. https://doi.org/10.1186/s13567-019-0727-y
Jiang W, Han X, Wang Q, Li X, Yi L, Liu Y, Ding C (2014) Vibrio parahaemolyticus enolase is an adhesion-related factor that binds plasminogen and functions as a protective antigen. Appl Microbiol Biotechnol 98(11):4937–4948. https://doi.org/10.1007/s00253-013-5471-z
Kalyanasundaram A, Jawahar S, Ilangopathy M, Palavesam A, Raman M (2015) Comparative immunoprophylactic efficacy of Haemonchus contortus recombinant enolase (rHcENO) and Con A purified native glycoproteins in sheep. Exp Parasitol 154:98–107. https://doi.org/10.1016/j.exppara.2015.04.016
Kwon OC, Kwak BS (2018) Breast sparganosis: a case report. J Parasit Dis 43(3):442–443. https://doi.org/10.1007/s12639-018-1003-1
Li MW, Song HQ, Li C, Lin HY, Xie WT, Lin RQ, Zhu XQ (2011) Sparganosis in mainland China. Int J Infect Dis 15(3):e154–e156. https://doi.org/10.1016/j.ijid.2010.10.001
Li S, Chen XQ, Zhou JJ, Xie Z, Shang M, He L, Liang P, Chen T, Mao Q, Liang C, Li X, Huang Y, Yu X (2020) Amino acids serve as an important energy source for adult flukes of Clonorchis sinensis. PLoS Negl Trop Dis 14(4):e0008287. https://doi.org/10.1371/journal.pntd.0008287
Li WH, Qu ZG, Zhang NZ, Yue L, Jia WZ, Luo JX, Yin H, Fu BQ (2015) Molecular characterization of enolase gene from Taenia multiceps. Res Vet Sci 102:53–58. https://doi.org/10.1016/j.rvsc.2015.06.013
Liu Q, Li MW, Wang ZD, Zhao GH, Zhu XQ (2015) Human sparganosis, a neglected food borne zoonosis. Lancet Infect Dis 15(10):1226–1235. https://doi.org/10.1016/S1473-3099(15)00133-4
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lo Presti A, Aguirre DT, De Andrés P, Daoud L, Fortes J, Muñiz J (2015) Cerebral sparganosis: case report and review of the European cases. Acta Neurochirurgica 157 (8):1339–1343
Lunghi M, Galizi R, Magini A, Carruthers VB, Di Cristina M (2015) Expression of the glycolytic enzymes enolase and lactate dehydrogenase during the early phase of Toxoplasma differentiation is regulated by an intron retention mechanism. Mol Microbiol 96(6):1159–1175. https://doi.org/10.1111/mmi.12999
Jiang W, Xue JX, Liu YC, Li T, Han XG, Wang SH, Chen YJ, Qi J, Yu SQ, Wang Q (2016) Identification and characterization of an immunogenic antigen, enolase 2, among excretory/secretory antigens (ESA) of Toxoplasma gondii. Protein Expr Purif 127:88–97. https://doi.org/10.1016/j.pep.2016.07.011
Pancholi V (2001) Multifunctional α-enolase: its role in diseases. Cell Mol Life Sci 58(7):902–920. https://doi.org/10.1007/pl00000910
Seweryn E, Pietkiewicz J, Szamborska A, Gamian A (2007) Enolase on the surface of prockaryotic and eukaryotic cells is a receptor for human plasminogen. Postepy Hig Med Dosw (Online) 61:672–682
Wang Y, Zhang J, Yuan ZY et al (2012) Cloning, expression and immunodiagnostic evaluation of enolase from Echinococcus granulosus. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 24(5):549–552, 556
Wang X, Chen W, Hu F, Deng C, Zhou C, Lv X, Fan Y, Men J, Huang Y, Sun J, Hu D, Chen J, Yang Y, Liang C, Zheng H, Hu X, Xu J, Wu Z, Yu X (2011) Clonorchis sinensis enolase: identification and biochemical characterization of a glycolytic enzyme from excretory/secretory products. Mol Biochem Parasitol 177(2):135–142. https://doi.org/10.1016/j.molbiopara.2011.02.011
Yang HJ (2010) Production of polyclonal antibodies against the tegument of sparganum (plerocercoid of Spirometra mansoni) and its immunolocalization. Korean J Parasitol 48(2):183–185. https://doi.org/10.3347/kjp.2010.48.2.183
Xie X, Hu J, Sun G, Ding B, Feng L (2018) Orbital sparganosis in an 8-year boy: a case report. BMC Ophthalmol 18(1):13. https://doi.org/10.1186/s12886-018-0675-8
Funding
The study was supported by the Program of Hainan Association for Science and Technology Plan to Youth R&D Innovation (No. QCXM201918), grants from the National Natural Science Foundation of China (No. 81560332 to L. P. and No. 31760246 to D. W.), a project supported by the Education Department of Hainan Province (Hnky2018-43), and the Natural Science Foundation of Hainan Province (No. 814298).
Author information
Authors and Affiliations
Contributions
Conceived of or designed study: Pei Liang and Dayong Wang
Performed the research: Pei Liang and Ruijia Fu
Analyzed the data: Pei Liang and Ruijia Fu
Contributed new methods or models: Pei Liang and Gang Lu
Wrote the paper: Pei Liang and Xiuji Cui
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no competing interests.
Additional information
Section Editor: Xing-Quan ZHU
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liang, P., Cui, X., Fu, R. et al. Identification of an enolase gene and its physiological role in Spirometra mansoni. Parasitol Res 120, 2095–2102 (2021). https://doi.org/10.1007/s00436-021-07175-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07175-y