Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Proteomic and Immunological Identification of Diagnostic Antigens from Spirometra erinaceieuropaei Plerocercoid

  • Lu, Yan (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases) ;
  • Sun, Jia-Hui (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases) ;
  • Lu, Li-Li (The Third Hospital of Shijiazhuang City) ;
  • Chen, Jia-Xu (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases) ;
  • Song, Peng (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases) ;
  • Ai, Lin (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases) ;
  • Cai, Yu-Chun (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases) ;
  • Li, Lan-Hua (School of Public Health, Weifang Medical University) ;
  • Chen, Shao-Hong (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), WHO Collaborating Center for Tropical Diseases, NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), National Center for International Research on Tropical Diseases)
  • Received : 2021.07.22
  • Accepted : 2021.11.27
  • Published : 2021.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Human sparganosis is a food-borne parasitic disease caused by the plerocercoids of Spirometra species. Clinical diagnosis of sparganosis is crucial for effective treatment, thus it is important to identify sensitive and specific antigens of plerocercoids. The aim of the current study was to identify and characterize the immunogenic proteins of Spirometra erinaceieuropaei plerocercoids that were recognized by patient sera. Crude soluble extract of the plerocercoids were separated using 2-dimensional gel electrophoresis coupled with immunoblot and mass spectrometry analysis. Based on immunoblotting patterns and mass spectrometry results, 8 antigenic proteins were identified from the plerocercoid. Among the proteins, cysteine protease protein might be developed as an antigen for diagnosis of sparganosis.

Keywords

Acknowledgement

This work was supported by the General Program Shanghai Municipal Commission of Health and Family Planning of China (grant no. 201740076), the National Parasite Resource Bank (grant no. NPRC-2019-194-30), the Open Project of Key Laboratory of Parasite and Vector Biology, China Ministry of Health (grant no. WSBKFKT-201804, WSBKFKT-201806).

References

  1. Liu Q, Li MW, Wang ZD, Zhao GH, Zhu XQ. Human sparganosis, a neglected food borne zoonosis. Lancet Infect Dis 2015; 15: 1226-1235. https://doi.org/10.1016/S1473-3099(15)00133-4
  2. Li MW, Song HQ, Li C, Lin HY, Xie WT, Lin RQ, Zhu XQ. Sparganosis in mainland China. Int J Infect Dis 2011; 15: 154-156. https://doi.org/10.1016/j.ijid.2010.10.001
  3. Kim JG, Ahn CS, Sohn WM, Nawa Y, Kong Y. Human sparganosis in Korea. J Korean Med Sci 2018; 33: e273. https://doi.org/10.3346/jkms.2018.33.e273
  4. Magnino S, Colin P, Dei-Cas E, Madsen M, McLauchlin J, Nockler K, Maradona MP, Tsigarida E, Vanopdenbosch E, Peteghem CV. Biological risks associated with consumption of reptile products. Int J Food Microbiol 2009; 134: 163-175. http://doi.org/10.1016/j.ijfoodmicro.2009.07.001
  5. Jeon HK, Park H, Lee D, Choe S, Kim KH, Huh S, Sohn WM, Chai JY, Eom KS. Human infections with Spirometra decipiens plerocercoids identified by morphologic and genetic analyses in Korea. Korean J Parasitol 2015; 53: 299-305. http://doi.org/10.3347/kjp.2015.53.3.299
  6. Anantaphruti MT, Nawa Y, Vanvanitchai Y. Human sparganosis in Thailand: an overview. Acta Trop 2011; 118: 171-176. http://doi.org/10.1016/j.actatropica.2011.03.011
  7. Wiwanitkit V. A review of human sparganosis in Thailand. Int J Infect Dis 2005; 9: 312-316. http://doi.org/10.1016/j.ijid.2004.08.003
  8. Yamasaki H, Sanpool O, Rodpai R, Sadaow L, Laummaunwai P, Un M, Thanchomnang T, Laymanivong S, Aung WPP, Intapan PM, Maleewong W. Spirometra species from Asia: genetic diversity and taxonomic challenges. Parasitol Int 2021; 80: 102181. http://doi.org/10.1016/j.parint.2020.102181
  9. Kudo T, Fujioka A, Korenaga M, Yamasaki H, Morishima Y, Sugiyama H, Nakajima H, Sano S. Molecular identification of intramuscular and subcutaneous Spirometra erinaceiuropaei sparganosis in a Japanese patient. J Dermatol 2017; 44: 138-139. https://doi.org/10.1111/1346-8138.13739
  10. Cobbold TS. Description of Ligula mansoni, a new human cestode. Zool J Linn Soc Lond 1883; 17: 78-83. https://doi.org/10.1111/j.1096-3642.1883.tb00237.x
  11. Zhang X, Hong X, Liu SN, Jiang P, Zhao SC, Sun CX, Wang ZQ, 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. http://doi.org/10.1371/journal.pntd.0008019
  12. Cui J, Lin XM, Zhang HW, Xu BL, Wang ZQ. Sparganosis, Henan Province, central China. Emerg Infect Dis 2011; 17: 146-147. http://doi.org/10.3201/eid1701.101095
  13. Xia Q, Yan J. Diagnosis and surgical management of orbital sparganosis. Eye (Lond) 2019; 33: 1418-1422. http://doi.org/10.1038/s41433-019-0427-x
  14. Kazemi A, Awosika O, Burgess C. Subcutaneous Sparganosis of the Breast. J Clin Aesthet Dermatol 2018; 11: 26-27.
  15. Hwang JM, Hwang DS, Kang C, Lee JW. Subcutaneous sparganosis mimicking soft tissue tumor: a case report. Int Med Case Rep J 2019; 12: 47-50. http://doi.org/10.2147/IMCRJ.S192764
  16. Otranto D, Eberhard ML. Zoonotic helminths affecting the human eye. Parasit Vectors 2011; 4: 41. http://doi.org/10.1186/1756-3305-4-41
  17. Hong D, Xie H, Zhu M, Wan H, Xu R, Wu Y. Cerebral sparganosis in mainland Chinese patients. J Clin Neurosci 2013; 20: 1514-1519. http://doi.org/10.1016/j.jocn.2012.12.018
  18. Zhang P, Zou Y, Yu FX, Wang Z, Lv H, Liu XH, Ding HY, Zhang TT, Zhao PF, Yin HX, Yang ZH, Wang ZC. Follow-up study of high-dose praziquantel therapy for cerebral sparganosis. PLoS Negl Trop Dis 2019; 13: e0007018. http://doi.org/10.1371/journal.pntd.0007018
  19. Cui J, Wang Y, Zhang X, Lin XM, Zhang HW, Wang ZQ, Chen JX. A neglected risk for sparganosis: eating live tadpoles in central China. Infect Dis Poverty 2017; 6: 58. http://doi.org/10.1186/s40249-017-0265-7
  20. Murata K, Abe T, Gohda M, Inoue R, Ishii K, Wakabayashi Y, Kamida T, Fujiki M, Kobayashi H, Takaoka H. Difficulty in diagnosing a case with apparent sequel cerebral sparganosis. Surg Neurol 2007; 67: 409-411. http://doi.org/10.1016/j.surneu.2006.06.056
  21. Song T, Wang WS, Zhou BR, Mai WW, Li ZZ, Guo HC, Zhou F. CT and MR characteristics of cerebral sparganosis. Am J Neuroradiol 2007; 28: 1700-1705. http://doi.org/10.3174/ajnr.A0659
  22. Liao HY, Li DT, Zhou B, Liu J, Li YJ, Liu H, Wu YZ, Zhu XZ, Tan CL. Imaging characteristics of cerebral sparganosis with live worms. J Neuroradiol 2016; 43: 378-383. http://doi.org/10.1016/j.neurad.2016.08.001
  23. Lee JH, Yu JS, Park MS, Lee SI, Yang SW. Abdominal sparganosis presenting as an abscess with fistulous communication to the bowel. Am J Roentgenol 2005; 185: 1084-1085. http://doi.org/10.2214/AJR.04.1680
  24. Koo JH, Cho WH, Kim HT, Lee SM, Chung BS, Joo CY. A case of sparganosis mimicking a varicose vein. Korean J Parasitol 2006; 44: 91-94. http://doi.org/10.3347/kjp.2006.44.1.91
  25. Rengarajan S, Nanjegowda N, Bhat D, Mahadevan A, Sampath S, Krishna S. Cerebral sparganosis: a diagnostic challenge. Br J Neurosurg 2008; 22: 784-786. http://doi.org/10.1080/02688690802088073
  26. Kong Y, Kang SY, Cho SY. Single step purification of potent antigenic protein from sparganum by gelatin-affinity chromatography. Kisaengchunghak Chapchi 1991; 29: 1-7. http://doi.org/10.3347/kjp.1991.29.1.1
  27. Nishiyama T, Ide T, Himes SR Jr., Ishizaka S, Araki T. Immunodiagnosis of human sparganosis mansoni by micro-chemiluminescence enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 1994; 88: 663-665. http://doi.org/10.1016/0035-9203(94)90218-6
  28. Cui J, Li N, Wang ZQ, Jiang P, Lin XM. Serodiagnosis of experimental sparganum infections of mice and human sparganosis by ELISA using ES antigens of Spirometra mansoni spargana. Parasitol Res 2011; 108: 1551-1556. http://doi.org/10.1007/s00436-010-2206-2
  29. Yeo IS, Yong TS, Im K. Serodiagnosis of human sparganosis by a monoclonal antibody-based competition ELISA. Yonsei Med J 1994; 35: 43-48. http://doi.org/10.3349/ymj.1994.35.1.43
  30. Ju C, Xu B, Lu Y, Mo XJ, Zhang T, Chen SB, Liu F, Cui SJ, Liu W, Chen JH, Feng Z, Peng JX, Hu W. Comparative immunomic analysis of Schistosoma japonicum soluble egg antigens reacting with patient sera before and after praziquantel treatment. J Anim Vet Adv 2012; 11: 2828-2838. http://doi.org/10.3923/javaa.2012.2828.2838
  31. Acevedo N, Mohr J, Zakzuk J, Samonig M, Briza P, Erler A, Pomes A, Huber CG, Ferreira F, Caraballo L. Proteomic and immunochemical characterization of glutathione transferase as a new allergen of the nematode Ascaris lumbricoides. PLoS One 2013; 8: e78353. http://doi.org/10.1371/journal.pone.0078353
  32. Grzelak S, Stachyra A, Bien-Kalinowska J. The first analysis of Trichinella spiralis and Trichinella britovi adult worm excretory-secretory proteins by two-dimensional electrophoresis coupled with LC-MS/MS. Vet Parasitol 2021: 109096. http://doi.org/10.1016/j.vetpar.2020.109096
  33. Sun XM, Ji YS, Elashram SA, Lu ZM, Liu XY, Suo X, Chen QJ, Wang H. Identification of antigenic proteins of Toxoplasma gondii RH strain recognized by human immunoglobulin G using immunoproteomics. J Proteomics 2012; 77: 423-432. http://doi.org/10.1016/j.jprot.2012.09.018
  34. Xu B, Liu XF, Cai YC, Huang JL, Zhang RX, Chen JH, Chen XJ, Zhou X, Xu XN, Zhou Y, Zhang T, Chen SB, Li J, Wu QF, Sun CS, Fu YF, Chen JX, Zhou XN, Hu W. Screening for biomarkers reflecting the progression of Babesia microti infection. Parasit Vectors, 2018; 11: 379. http://doi.org/10.1186/s13071-018-2951-0
  35. Hu DD, Cui J, Xiao D, Wang L, Liu LN, Liu RD, Zhang JZ, Wang ZQ. Identification of early diagnostic antigens from Spirometra erinaceieuropaei sparganum soluble proteins using immunoproteomics. Southeast Asian J Trop Med Public Health 2014; 45: 576-583.
  36. Hu DD, Cui J, Wang L, Liu LN, Wei T, Wang ZQ. Immunoproteomic Analysis of the Excretory-Secretory Proteins from Spirometra mansoni Sparganum. Iran J Parasitol 2013; 8: 408-416.
  37. Lu Y , Chen JX , Li H, Cai YC, Ai L, Chu YH, Song P, Chen SH. Infection of Spirometra mansoni plerocercoid in snakes from Shanghai Zoo. Chin J Parasitol Parasit Dis 2018; 36: 593-596 (in Chinese).
  38. Schloer S, Pajonczyk D, Rescher U. Annexins in translational research: hidden treasures to be found. Int J Mol Sci 2018; 19: 1781. http://doi.org/10.3390/ijms19061781
  39. Cantacessi C, Seddon JM, Miller TL, Leow CY, Thomas L, Mason L, Willis C, Walker G, Loukas A, Gasser RB, Jones MK, Hofmann A. A genome-wide analysis of annexins from parasitic organisms and their vectors. Sci Rep 2013; 3: 2893. http://doi.org/10.1038/srep02893
  40. Moss SE, Morgan RO. The annexins. Genome Biol 2004; 5, 219. https://doi.org/10.1186/gb-2004-5-4-219
  41. Hofmann A, Osman A, Leow CY, Driguez P, McManus DP, Jones MK. Parasite annexins--new molecules with potential for drug and vaccine development. Bioessays, 2010; 32: 967-776. http://doi.org/10.1002/bies.200900195
  42. Gerke V, Moss SE. Annexins: from structure to function. Physiol Rev 2002; 82: 331-371. http://doi.org/10.1152/physrev.00030.2001
  43. Zhang Y, Wang KH, Guo YJ, Lu YM, Yan HL, Song YL, Wang F, Ding FX, Sun SH. Annexin B1 from Taenia solium metacestodes is a newly characterized member of the annexin family. Biol Chem 2007; 388: 601-610. http://doi.org/10.1515/BC.2007.071
  44. Yan HL, Xue G, Mei Q, Ding FX, Wang YZ, Sun SH. Calcium-dependent proapoptotic effect of Taenia solium metacestodes annexin B1 on human eosinophils: a novel strategy to prevent host immune response. Int J Biochem Cell Biol 2008; 40: 2151-2163. http://doi.org/10.1016/j.biocel.2008.02.018
  45. Leow CY, Willis C, Leow CH, Hofmann A, Jones M. Molecular characterization of Schistosoma mansoni tegument annexins and comparative analysis of antibody responses following parasite infection. Mol Biochem Parasitol 2019; 234: 111231. https://doi.org/10.1016/j.molbiopara.2019.111231
  46. Wu Q, Li DD, Ma PP, Lv G. Application of bioinformatic analysis in Annexin E1 of Spirometra erinaceieuropaei. J Hainan Med Coll 2010; 16: 1106-1110 (in Chinese).
  47. Siles-Lucas Mdel M, Gottstein B. The 14-3-3 protein: a key molecule in parasites as in other organisms. Trends Parasitol 2003; 19: 575-581. http://doi.org/10.1016/j.pt.2003.10.003
  48. Liu J, Giri BR, Chen Y, Cheng G. 14-3-3 protein and ubiquitin C acting as SjIAP interaction partners facilitate tegumental integrity in Schistosoma japonicum. Int J Parasitol 2019; 49: 355-364. http://doi.org/10.1016/j.ijpara.2018.11.011
  49. Gardino AK, Yaffe MB. 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol 2011; 22: 688-695. http://doi.org/10.1016/j.semcdb.2011.09.008
  50. Obsilova V, Kopecka M, Kosek D, Kacirova M, Kylarova S, Rezabkova L, Obsil T. Mechanisms of the 14-3-3 protein function: regulation of protein function through conformational modulation. Physiol Res 2014; 63 (suppl): 155-164. http://doi.org/10.33549/physiolres.932659
  51. Stevers LM, Sijbesma E, Botta M, MacKintosh C, Obsil T, Landrieu I, Cau Y, Wilson AJ, Karawajczyk A, Eickhoff J, Davis J, Hann M, O'Mahony G, Doveston RG, Brunsveld L, Ottmann C. Modulators of 14-3-3 Protein-Protein Interactions. J Med Chem 2018; 61: 3755-3778. http://doi.org/10.1021/acs.jmedchem.7b00574
  52. Li FC, Liu Q, Elsheikha HM, Yang WB, Hou JL, Zhu XQ. Identification of two novel host proteins interacting with Toxoplasma gondii 14-3-3 protein by yeast two-hybrid system. Parasitol Res 2018; 117: 1291-1296. http://doi.org/10.1007/s00436-018-5812-z
  53. Qian CY, Huang B, Yu CX, Zhang J, Yin XR, Wang J, Song LJ, Zhang W, Ke XD. Detection of the circulating antigen 14-3-3 protein of Schistosoma japonicum by time-resolved fluoroimmunoassay in rabbits. Parasit Vectors 2011; 4: 95. http://doi.org/10.1186/1756-3305-4-95
  54. Teichmann A, Vargas DM, Monteiro KM, Meneghetti BV, Dutra CS, Paredes R, Galanti N, Zaha A, Ferreira HB. Characterization of 14-3-3 isoforms expressed in the Echinococcus granulosus pathogenic larval stage. J Proteome Res 2015; 14: 1700-1715. http://doi.org/10.1021/pr5010136
  55. Tian AL, Lu M, Calderon-Mantilla G, Petsalaki E, Dottorini T, Tian XW, Wang YJ, Huang SY, Hou JL, Li XR, Elisheikha HM, Zhu XQ. A recombinant Fasciola gigantica 14-3-3 epsilon protein (rFg14-3-3e) modulates various functions of goat peripheral blood mononuclear cells. Parasit Vectors 2018; 11: 152. http://doi.org/10.1186/s13071-018-2745-4
  56. Lee MR, Kim YJ, Kim DW, Yoo WG, Cho SH, Hwang KY, Ju JW, Lee WJ. The identification of antigenic proteins: 14-3-3 protein and propionyl-CoA carboxylase in Clonorchis sinensis. Mol Biochem Parasitol 2012; 182: 1-6. http://doi.org/10.1016/j.molbiopara.2011.11.006
  57. Kafle A, Puchadapirom P, Plumworasawat S, Dontumprai R, Chan-On W, Buates S, Laha T, Sripa B, Suttiprapa S. Identification and characterization of protein 14-3-3 in carcinogenic liver fluke Opisthorchis viverrini. Parasitol Int 2017; 66: 426-431. http://doi.org/10.1016/j.parint.2016.10.021
  58. Stachyra A, Grzelak S, Basalaj K, Zawistowska-Deniziak A, BienKalinowska J. immunization with a recombinant protein of Trichinella britovi 14-3-3 triggers an immune response but no protection in mice. Vaccines (Basel) 2020; 8: 515. http://doi.org/10.3390/vaccines8030515
  59. Masoori L, Falak R, Mokhtarian K, Bandehpour M, Razmjou E, Jalallou N, Jafarian F, Akhlaghi L, Meamar AR. Production of recombinant 14-3-3 protein and determination of its immunogenicity for application in serodiagnosis of strongyloidiasis. Trans R Soc Trop Med Hyg 2019; 113: 326-331. http://doi.org/10.1093/trstmh/trz006
  60. Li ZJ, Wang YN, Wang Q, Zhao W. Echinococcus granulosus 14-3-3 protein: a potential vaccine candidate against challenge with Echinococcus granulosus in mice. Biomed Environ Sci 2012; 25: 352-358. http://doi.org/10.3967/0895-3988.2012.03.014
  61. Siqueira-Neto JL, Debnath A, McCall LI, Bernatchez JA, Ndao M, Reed SL, Rosenthal PJ. Cysteine proteases in protozoan parasites. PLoS Negl Trop Dis 2018; 12: e0006512. http://doi.org/10.1371/journal.pntd.0006512
  62. Song CY, Chappell CL. Purification and partial characterization of cysteine proteinase from Spirometra mansoni plerocercoids. J Parasitol 1993; 79: 517-524. http://doi.org/10.2307/3283376
  63. Fukase T, Matsuda Y, Akihama S, Itagaki H. Purification and some properties of cysteine protease of Spirometra erinacei plerocercoid (Cestoda: Diphyllobothriidae). Jpn J Parasitol 1985; 34, 351-360.
  64. Kong Y, Kang SY, Kim SH, Chung YB, Cho SY. A neutral cysteine protease of Spirometra mansoni plerocercoid invoking an IgE response. Parasitology 1997; 114: 263-271. http://doi.org/10.1017/s0031182096008529
  65. Cho SY, Chung YB, Kong Y. Component proteins and protease activities in excretory-secretory product of sparganum. Korean J Parasitol 1992; 30: 227-230. http://doi.org/10.3347/kjp.1992.30.3.227
  66. Liu LN, Wang ZQ, Zhang X, Jiang P, Qi X, Liu RD, Zhang ZF, Cui J. Characterization of Spirometra erinaceieuropaei Plerocercoid Cysteine Protease and Potential Application for Serodiagnosis of Sparganosis. PLoS Negl Trop Dis 2015; 9: e0003807. http://doi.org/10.1371/journal.pntd.0003807
  67. Cui J, Wei T, Liu LN, Zhang X, Qi X, Zhang ZF, Wang ZQ. Molecular characterization of a Spirometra mansoni antigenic polypeptide gene encoding a 28.7 kDa protein. Parasitol Res 2014; 113: 3511-3516. http://doi.org/10.1007/s00436-014-4065-8
  68. Lu YJ, Lu G, Shi DZ, Li LH, Zhong SF. Bioinformatic analysis for structure and function of TCTP from Spirometra mansoni. Asian Pac J Trop Med 2013; 6: 709-712. http://doi.org/10.1016/s1995-7645(13)60123-6