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Enhancing immune responses to inactivated foot-and-mouth virus vaccine by a polysaccharide adjuvant of aqueous extracts from Artemisia rupestris L.

  • Wang, Danyang (Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University) ;
  • Yang, Yu (Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University) ;
  • Li, Jinyu (Laboratory of Plant Stress Biology in Arid Land, College of Life Sciences, Xinjiang Normal University) ;
  • Wang, Bin (Key Lab of Medical Molecular Virology, School of Basic Medical Science, Shanghai Medical College, Fudan University) ;
  • Zhang, Ailian (Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University)
  • Received : 2020.07.21
  • Accepted : 2021.02.15
  • Published : 2021.05.31

Abstract

Background: New-generation adjuvants for foot-and-mouth disease virus (FMDV) vaccines can improve the efficacy of existing vaccines. Chinese medicinal herb polysaccharide possesses better promoting effects. Objectives: In this study, the aqueous extract from Artemisia rupestris L. (AEAR), an immunoregulatory crude polysaccharide, was utilized as the adjuvant of inactivated FMDV vaccine to explore their immune regulation roles. Methods: The mice in each group were subcutaneously injected with different vaccine formulations containing inactivated FMDV antigen adjuvanted with three doses (low, medium, and high) of AEAR or AEAR with ISA-206 adjuvant for 2 times respectively in 1 and 14 days. The variations of antibody level, lymphocyte count, and cytokine secretion in 14 to 42 days after first vaccination were monitored. Then cytotoxic T lymphocyte (CTL) response and antibody duration were measured after the second vaccination. Results: AEAR significantly induced FMDV-specific antibody titers and lymphocyte activation. AEAR at a medium dose stimulated Th1/Th2-type response through interleukin-4 and interferon-γ secreted by CD4+ T cells. Effective T lymphocyte counts were significantly elevated by AEAR. Importantly, the efficient CTL response was remarkably provoked by AEAR. Furthermore, AEAR at a low dose and ISA-206 adjuvant also synergistically promoted immune responses more significantly in immunized mice than those injected with only ISA-206 adjuvant and the stable antibody duration without body weight loss was 6 months. Conclusions: These findings suggested that AEAR had potential utility as a polysaccharide adjuvant for FMDV vaccines.

Keywords

Acknowledgement

We thank Dr. Jiong Huang and Hui Cao from Tecon Biology Co., Ltd for experiment's help. We wish to thank Prof. J He (Urumqi, China) for kindly providing materials.

References

  1. Grubman MJ, Baxt B. Foot-and-mouth disease. Clin Microbiol Rev. 2004;17(2):465-493. https://doi.org/10.1128/CMR.17.2.465-493.2004
  2. Diaz-San Segundo F, Medina GN, Stenfeldt C, Arzt J, de Los Santos T. Foot-and-mouth disease vaccines. Vet Microbiol. 2017;206:102-112. https://doi.org/10.1016/j.vetmic.2016.12.018
  3. Park JH. Requirements for improved vaccines against foot-and-mouth disease epidemics. Clin Exp Vaccine Res. 2013;2(1):8-18. https://doi.org/10.7774/cevr.2013.2.1.8
  4. Dar P, Kalaivanan R, Sied N, Mamo B, Kishore S, Suryanarayana VV, et al. Montanide ISATM 201 adjuvanted FMD vaccine induces improved immune responses and protection in cattle. Vaccine. 2013;31(33):3327-3332. https://doi.org/10.1016/j.vaccine.2013.05.078
  5. Saravanan P, Sreenivasa BP, Selvan RP, Basagoudanavar SH, Hosamani M, Reddy ND, et al. Protective immune response to liposome adjuvanted high potency foot-and-mouth disease vaccine in Indian cattle. Vaccine. 2015;33(5):670-677. https://doi.org/10.1016/j.vaccine.2014.12.008
  6. Cao Y. Adjuvants for foot-and-mouth disease virus vaccines: recent progress. Expert Rev Vaccines. 2014;13(11):1377-1385. https://doi.org/10.1586/14760584.2014.963562
  7. Jiang MH, Zhu L, Jiang JG. Immunoregulatory actions of polysaccharides from Chinese herbal medicine. Expert Opin Ther Targets. 2010;14(12):1367-1402. https://doi.org/10.1517/14728222.2010.531010
  8. Li P, Wang F. Polysaccharides: candidates of promising vaccine adjuvants. Drug Discov Ther. 2015;9(2):88-93. https://doi.org/10.5582/ddt.2015.01025
  9. Xie F, Li Y, Su F, Hu S. Adjuvant effect of Atractylodis macrocephalae Koidz. polysaccharides on the immune response to foot-and-mouth disease vaccine. Carbohydr Polym. 2012;87(2):1713-1719. https://doi.org/10.1016/j.carbpol.2011.09.080
  10. Gordon D, Kelley P, Heinzel S, Cooper P, Petrovsky N. Immunogenicity and safety of AdvaxTM, a novel polysaccharide adjuvant based on delta inulin, when formulated with hepatitis B surface antigen: a randomized controlled phase 1 study. Vaccine. 2014;32(48):6469-6477. https://doi.org/10.1016/j.vaccine.2014.09.034
  11. Saade F, Honda-Okubo Y, Trec S, Petrovsky N. A novel hepatitis B vaccine containing AdvaxTM, a polysaccharide adjuvant derived from delta inulin, induces robust humoral and cellular immunity with minimal reactogenicity in preclinical testing. Vaccine. 2013;31(15):1999-2007. https://doi.org/10.1016/j.vaccine.2012.12.077
  12. Zhang N, Li J, Hu Y, Cheng G, Zhu X, Liu F, et al. Effects of astragalus polysaccharide on the immune response to foot-and-mouth disease vaccine in mice. Carbohydr Polym. 2010;82(3):680-686. https://doi.org/10.1016/j.carbpol.2010.05.030
  13. Juteau F, Masotti V, Bessiere JM, Dherbomez M, Viano J. Antibacterial and antioxidant activities of Artemisia annua essential oil. Fitoterapia. 2002;73(6):532-535. https://doi.org/10.1016/S0367-326X(02)00175-2
  14. Li J, Li J, Zhang F. The immunoregulatory effects of Chinese herbal medicine on the maturation and function of dendritic cells. J Ethnopharmacol. 2015;171:184-195. https://doi.org/10.1016/j.jep.2015.05.050
  15. Zhang A, Yang Y, Wang Y, Zhao G, Yang X, Wang D, et al. Adjuvant-active aqueous extracts from Artemisia rupestris L. improve immune responses through TLR4 signaling pathway. Vaccine. 2017;35(7):1037-1045. https://doi.org/10.1016/j.vaccine.2017.01.002
  16. Zhang A, Wang D, Li J, Gao F, Fan X. The effect of aqueous extract of Xinjiang Artemisia rupestris L. (an influenza virus vaccine adjuvant) on enhancing immune responses and reducing antigen dose required for immunity. PLoS One. 2017;12(8):e0183720. https://doi.org/10.1371/journal.pone.0183720
  17. Wang D, Cao H, Li J, Zhao B, Wang Y, Zhang A, et al. Adjuvanticity of aqueous extracts of Artemisia rupestris L. for inactivated foot-and-mouth disease vaccine in mice. Res Vet Sci. 2019;124:191-199. https://doi.org/10.1016/j.rvsc.2019.03.016
  18. Yang Y, Yang XM, Zhao G, Yu Y, Zhang HZ, Zhang AL. Immunoregulative action of polysaccharides in wild and cultivated Artemisia rupestris L. in Xinjiang on bone marrow dendritic cells. Shengwu Jishu Tongbao. 2016;32(7):217-226.
  19. Guo XP, Tian CR, Gao CY, Meng YW. Study on removal process of proteins from crude Sphallerocarpus gracilis polysaccharides and its scavenging capability to nitrite. Sci Technol Food Ind. 2011;32:274-276.
  20. Park ME, Lee SY, Kim RH, Ko MK, Lee KN, Kim SM, et al. Enhanced immune responses of foot-and-mouth disease vaccine using new oil/gel adjuvant mixtures in pigs and goats. Vaccine. 2014;32(40):5221-5227. https://doi.org/10.1016/j.vaccine.2014.07.040
  21. Rodriguez LL, Gay CG. Development of vaccines toward the global control and eradication of foot-and-mouth disease. Expert Rev Vaccines. 2011;10(3):377-387. https://doi.org/10.1586/erv.11.4
  22. Park ME, You SH, Lee SY, Lee KN, Ko MK, Choi JH, et al. Immune responses in pigs and cattle vaccinated with half-volume foot-and-mouth disease vaccine. J Vet Sci. 2017;18(S1):323-331. https://doi.org/10.4142/jvs.2017.18.S1.323
  23. de Los Santos T, Diaz-San Segundo F, Rodriguez LL. The need for improved vaccines against foot-and-mouth disease. Curr Opin Virol. 2018;29:16-25. https://doi.org/10.1016/j.coviro.2018.02.005
  24. Licciardi PV, Underwood JR. Plant-derived medicines: a novel class of immunological adjuvants. Int Immunopharmacol. 2011;11(3):390-398. https://doi.org/10.1016/j.intimp.2010.10.014
  25. Rey-Ladino J, Ross AG, Cripps AW, McManus DP, Quinn R. Natural products and the search for novel vaccine adjuvants. Vaccine. 2011;29(38):6464-6471. https://doi.org/10.1016/j.vaccine.2011.07.041
  26. Zhang L, Zhang J, Chen HT, Zhou JH, Ma LN, Ding YZ, et al. Research in advance for FMD novel vaccines. Virol J. 2011;8(1):268. https://doi.org/10.1186/1743-422X-8-268
  27. Capozzo AV, Periolo OH, Robiolo B, Seki C, La Torre JL, Grigera PR. Total and isotype humoral responses in cattle vaccinated with foot and mouth disease virus (FMDV) immunogen produced either in bovine tongue tissue or in BHK-21 cell suspension cultures. Vaccine. 1997;15(6-7):624-630. https://doi.org/10.1016/S0264-410X(96)00284-8
  28. Carr BV, Lefevre EA, Windsor MA, Inghese C, Gubbins S, Prentice H, et al. CD4+ T-cell responses to foot-and-mouth disease virus in vaccinated cattle. J Gen Virol. 2013;94(Pt 1):97-107. https://doi.org/10.1099/vir.0.045732-0
  29. Shi XJ, Wang B, Zhang C, Wang M. Expressions of bovine IFN-gamma and foot-and-mouth disease VP1 antigen in P. pastoris and their effects on mouse immune response to FMD antigens. Vaccine. 2006;24(1):82-89. https://doi.org/10.1016/j.vaccine.2005.07.051
  30. Oh Y, Fleming L, Statham B, Hamblin P, Barnett P, Paton DJ, et al. Interferon-γ induced by in vitro re-stimulation of CD4+ T-cells correlates with in vivo FMD vaccine induced protection of cattle against disease and persistent infection. PLoS One. 2012;7(9):e44365. https://doi.org/10.1371/journal.pone.0044365
  31. Guzman E, Taylor G, Charleston B, Skinner MA, Ellis SA. An MHC-restricted CD8+ T-cell response is induced in cattle by foot-and-mouth disease virus (FMDV) infection and also following vaccination with inactivated FMDV. J Gen Virol. 2008;89(Pt 3):667-675. https://doi.org/10.1099/vir.0.83417-0
  32. Cox SJ, Aggarwal N, Statham RJ, Barnett PV. Longevity of antibody and cytokine responses following vaccination with high potency emergency FMD vaccines. Vaccine. 2003;21(13-14):1336-1347. https://doi.org/10.1016/S0264-410X(02)00691-6