Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T16:05:06.211Z Has data issue: false hasContentIssue false

Evaluation of immune response to Bacillus subtilis spores expressing Clonorchis sinensis serpin3

Published online by Cambridge University Press:  14 May 2020

Zhipeng Lin
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Hengchang Sun
Affiliation:
Department of laboratory medicine, The Third Affiliated Hospital, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Yan Ma
Affiliation:
Department of respiratory medicine, Fifth Affiliated Hospital, Sun Yat-sen University, Zhuhai519099, People's Republic of China
Xinyi Zhou
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Hongye Jiang
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Xi Wang
Affiliation:
Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Jiaman Song
Affiliation:
Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Zeli Tang
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Department of Cell Biology and Genetics, School of Pre-clinical Medicine, Guangxi Medical University, Nanning530021, People's Republic of China
Qing Bian
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Zhen Zhang
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Yan Huang*
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
Xinbing Yu*
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou510080, People's Republic of China Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-Sen University, Guangzhou510080, People's Republic of China
*
Author for correspondence: Xinbing Yu, E-mail: [email protected], Yan Huang, E-mail: [email protected]
Author for correspondence: Xinbing Yu, E-mail: [email protected], Yan Huang, E-mail: [email protected]

Abstract

Clonorchis sinensis (C. sinensis) is one of the most serious food-borne parasites, which can lead to liver fibrosis or cholangiocarcinoma. Effective measures for clonorchiasis prevention are still urgently needed. Bacillus subtilis (B. subtilis) is an effective antigen delivery platform for oral vaccines. Chonorchis sinensis serpin (CsSerpin) was proved to be potential vaccine candidates. In this study, CsSerpin3 was displayed on the surface of B. subtilis spore and recombinant spores were orally administrated to BALB/C mice. CsSerpin3-specific IgA levels in faecal, bile and intestinal mucous increased at 4–8 weeks after the first administration compared with those in control groups. The mucus production and the number of goblet cells in intestinal mucosa elevated in B.s-CotC-CsSerpin3 (CotC, coat protein of B. subtilis spore) spores treated group compared to those in blank control. No significant difference in the activities of glutamic-pyruvic transaminase/ alanine aminotransferase and glutamic oxalacetic transaminase/aspartate aminotransferase were observed between groups. There was no side effect inflammation and observable pathological damage in the liver tissue of mice after administration. Moreover, collagen deposition and Ishak score were statistically reduced in B.s-CotC-CsSerpin3 spores treated mice. In conclusion, B. subtilis spores displaying CsSerpin3 could be investigated further as an oral vaccine against clonorchiasis.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Choi, BI, Han, JK, Hong, ST and Lee, KH (2004) Clonorchiasis and cholangiocarcinoma: etiologic relationship and imaging diagnosis. Clinical Microbiology Reviews 17, 540552.CrossRefGoogle ScholarPubMed
Daifalla, N, Cayabyab, MJ, Xie, E, Kim, HB, Tzipori, S, Stashenko, P, Duncan, M and Campos-Neto, A (2015) Commensal Streptococcus mitis is a unique vector for oral mucosal vaccination. Microbes and Infection 17, 237242.CrossRefGoogle ScholarPubMed
Deplancke, B and Gaskins, HR (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. American Journal of Clinical Nutrition 73, 1131S1141S.CrossRefGoogle ScholarPubMed
Epstein, JE and Richie, TL (2013) The whole parasite, pre-erythrocytic stage approach to malaria vaccine development: a review. Current Opinion in Infectious Diseases 26, 420428.Google ScholarPubMed
Guoyan, Z, Yingfeng, A, Zabed, H, Qi, G, Yang, M, Jiao, Y, Li, W, Wenjing, S and Xianghui, Q (2019) Bacillus subtilis spore surface display technology: a review of Its development and applications. Journal of Microbiology and Biotechnology 29, 179190.CrossRefGoogle ScholarPubMed
Ishak, K, Baptista, A, Bianchi, L, Callea, F, De Groote, J, Gudat, F, Denk, H, Desmet, V, Korb, G and MacSween, RN (1995) Histological grading and staging of chronic hepatitis. Journal of Hepatology 22, 696699.CrossRefGoogle ScholarPubMed
Jiang, H, Chen, T, Sun, H, Tang, Z, Yu, J, Lin, Z, Ren, P, Zhou, X, Huang, Y, Li, X and Yu, X (2017) Immune response induced by oral delivery of Bacillus subtilis spores expressing enolase of Clonorchis sinensis in grass carps (Ctenopharyngodon Idellus). Fish & Shellfish Immunology 60, 318325.CrossRefGoogle Scholar
Karauzum, H, Updegrove, TB, Kong, M, Wu, IL, Datta, SK and Ramamurthi, KS (2018) Vaccine display on artificial bacterial spores enhances protective efficacy against Staphylococcus aureus infection. FEMS Microbiology Letters 365, fny190. doi: 10.1093/femsle/fny190.CrossRefGoogle ScholarPubMed
Keiser, J and Utzinger, J (2009) Food-borne trematodiases. Clinical Microbiology Reviews 22, 466483.CrossRefGoogle ScholarPubMed
Law, RH, Zhang, Q, McGowan, S, Buckle, AM, Silverman, GA, Wong, W, Rosado, CJ, Langendorf, CG, Pike, RN, Bird, PI and Whisstock, JC (2006) An overview of the serpin superfamily. Genome Biology 7, 216.CrossRefGoogle ScholarPubMed
Lei, H, Tian, Y, Chen, W, Wang, X, Li, X, Mao, Q, Sun, J, Li, R, Xu, Y, Liang, C, Huang, Y and Yu, X (2013) The biochemical and immunological characterization of two serpins from Clonorchis sinensis. Molecular Biology Reports 40, 39773985.CrossRefGoogle ScholarPubMed
Levenhagen, MA, Conte, H and Costa-Cruz, JM (2016) Current progress toward vaccine and passive immunization approaches for Strongyloides spp. Immunology Letters 180, 1723.CrossRefGoogle ScholarPubMed
Li, R, Xue, W, Huang, L, Xiong, Q and Wang, B (2011) Competent preparation and plasmid transformation of Bacillus subtilis. Biotechnology Bulletin 05, 227230.Google Scholar
Lun, Z-R, Gasser, RB, Lai, D-H, Li, A-X, Zhu, X-Q, Yu, X-B and Fang, Y-Y (2005) Clonorchiasis: a key foodborne zoonosis in China. The Lancet Infectious Diseases 5, 3141.CrossRefGoogle ScholarPubMed
Mangan, MS, Kaiserman, D and Bird, PI (2008) The role of serpins in vertebrate immunity. Tissue Antigens 72, 110.CrossRefGoogle ScholarPubMed
Mantis, NJ, Rol, N and Corthésy, B (2011) Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunology 4, 603611.CrossRefGoogle Scholar
Mingmongkolchai, S and Panbangred, W (2018) Bacillus probiotics: an alternative to antibiotics for livestock production. Journal of Applied Microbiology 124, 13341346.CrossRefGoogle ScholarPubMed
Oeser, K, Schwartz, C and Voehringer, D (2015) Conditional IL-4/IL-13-deficient mice reveal a critical role of innate immune cells for protective immunity against gastrointestinal helminths. Mucosal Immunology 8, 672682.CrossRefGoogle ScholarPubMed
Permpoonpattana, P, Hong, HA, Phetcharaburanin, J, Huang, JM, Cook, J, Fairweather, NF and Cutting, SM (2011) Immunization with Bacillus Spores expressing toxin A peptide repeats protects against infection with Clostridium difficile strains producing toxins A and B. Infection and Immunity 79, 22952302.CrossRefGoogle ScholarPubMed
Qian, M-B, Utzinger, J, Keiser, J and Zhou, X-N (2016) Clonorchiasis. The Lancet 387, 800810.CrossRefGoogle ScholarPubMed
Ramirez, V, Sharpe, JE, Peppas, LA and AN (2017) Current state and challenges in developing oral vaccines. Advanced Drug Delivery Reviews 114, 116131.CrossRefGoogle Scholar
Rau, JC, Beaulieu, LM, Huntington, JA and Church, FC (2007) Serpins in thrombosis, hemostasis and fibrinolysis. Journal of Thrombosis and Haemostasis: JTH 5, 102115.CrossRefGoogle ScholarPubMed
Reed, SG, Coler, RN, Mondal, D, Kamhawi, S and Valenzuela, JG (2016) Leishmania vaccine development: exploiting the host-vector-parasite interface. Expert Review of Vaccines 15, 8190.CrossRefGoogle ScholarPubMed
Sun, H, Lin, Z, Zhao, L, Chen, T, Shang, M, Jiang, H, Tang, Z, Zhou, X, Shi, M, Zhou, L, Ren, P, Qu, H, Lin, J, Li, X, Xu, J, Huang, Y and Yu, X (2018) Bacillus subtilis spore with surface display of paramyosin from Clonorchis sinensis potentializes a promising oral vaccine candidate. Parasites & Vectors 11, 156.CrossRefGoogle ScholarPubMed
Takahashi, A, Sekiya, C, Yazaki, Y, Ono, M, Sato, H, Hasebe, C, Ishikawa, Y, Okuno, K, Yamada, M and Namiki, M (1986) [Hepatic GOT and GPT activities in patients with various liver diseases--especially alcoholic liver disease]. Hokkaido Igaku Zasshi 61, 431436.Google Scholar
Tang, Z, Shang, M, Chen, T, Ren, P, Sun, H, Qu, H, Lin, Z, Zhou, L, Yu, J, Jiang, H, Zhou, X, Li, X, Huang, Y, Xu, J and Yu, X (2016a) The immunological characteristics and probiotic function of recombinant Bacillus subtilis spore expressing Clonorchis sinensis cysteine protease. Parasites & Vectors 9, 648.CrossRefGoogle Scholar
Tang, ZL, Huang, Y and Yu, XB (2016b) Current status and perspectives of Clonorchis sinensis and clonorchiasis: epidemiology, pathogenesis, omics, prevention and control. Infectious Diseases of Poverty 5, 71.CrossRefGoogle Scholar
Turner, JE, Stockinger, B and Helmby, H (2013) IL-22 mediates goblet cell hyperplasia and worm expulsion in intestinal helminth infection. PLoS Pathogens 9, e1003698.CrossRefGoogle ScholarPubMed
Vogt, CM, Armua-Fernandez, MT, Tobler, K, Hilbe, M, Aguilar, C, Ackermann, M, Deplazes, P and Eichwald, C (2018) Oral application of recombinant Bacillus subtilis spores to dogs results in a humoral response against specific Echinococcus granulosus paramyosin and tropomyosin antigens. Infection and Immunity 86, e0049517. doi: 10.1128/IAI.00495-17.Google Scholar
Wang, X, Chen, W, Tian, Y, Mao, Q, Lv, X, Shang, M, Li, X, Yu, X and Huang, Y (2014) Surface display of Clonorchis sinensis enolase on Bacillus subtilis spores potentializes an oral vaccine candidate. Vaccine 32, 13381345.CrossRefGoogle ScholarPubMed
Wu, W, Qian, X, Huang, Y and Hong, Q (2012) A review of the control of clonorchiasis sinensis and Taenia Solium taeniasis/cysticercosis in China. Parasitology Research 111, 18791884.CrossRefGoogle ScholarPubMed
Yang, Y, Hu, D, Wang, L, Liang, C, Hu, X, Wang, X, Chen, J, Xu, J and Yu, X (2009) Molecular cloning and characterization of a novel serpin gene of Clonorchis sinensis, highly expressed in the stage of metacercaria. Parasitology Research 106, 221225.CrossRefGoogle ScholarPubMed
Yang, Y, Hu, D, Wang, L, Liang, C, Hu, X, Xu, J, Huang, Y and Yu, X (2014) Comparison of two serpins of Clonorchis sinensis by bioinformatics, expression, and localization in metacercaria. Pathogens and Global Health 108, 179185.CrossRefGoogle ScholarPubMed
Yao, YY, Chen, DD, Cui, ZW, Zhang, XY, Zhou, YY, Guo, X, Li, AH and Zhang, YA (2019) Oral vaccination of tilapia against Streptococcus agalactiae using Bacillus subtilis spores expressing Sip. Fish & Shellfish Immunology 86, 9991008.CrossRefGoogle ScholarPubMed
Yu, J, Chen, T, Xie, Z, Liang, P, Qu, H, Shang, M, Mao, Q, Ning, D, Tang, Z, Shi, M, Zhou, L, Huang, Y and Yu, X (2015) Oral delivery of Bacillus subtilis spore expressing enolase of Clonorchis sinensis in rat model: induce systemic and local mucosal immune responses and has no side effect on liver function. Parasitology Research 114, 24992505.CrossRefGoogle ScholarPubMed
Zhou, Z, Xia, H, Hu, X, Huang, Y, Li, Y, Li, L, Ma, C, Chen, X, Hu, F, Xu, J, Lu, F, Wu, Z and Yu, X (2008) Oral administration of a Bacillus subtilis spore-based vaccine expressing Clonorchis sinensis tegumental protein 22.3 kDa confers protection against Clonorchis sinensis. Vaccine 26, 18171825.CrossRefGoogle ScholarPubMed
Supplementary material: File

Lin et al. supplementary material

Lin et al. supplementary material

Download Lin et al. supplementary material(File)
File 93.4 KB