Paulownia tomentosa flower polysaccharide as an effective immunopotentiator to enhance immune responses for Newcastle disease vaccine in mice
Main Article Content
Keywords
immune responses, immunopotentiator, Newcastle disease vaccine, Paulownia tomentosa flower polysaccharides
Abstract
To investigate the immunomodulatory activity and explore the mechanism of Paulownia tomentosa flower polysaccharides (PTFP). PTFP was orally administrated to mice for seven successive days before and after Newcastle disease vaccination. The results demonstrated that compared with the vaccine control (VC) group, PTFP enhanced the inhibition of hemagglutination assay antibody titers, promoted the antigen-specific immunoglobulin (Ig)G, IgG1, IgG2a, and IgG2b antibodies responses, enhanced proliferation of spleen T and B lymphocytes, increased the secretions of interferon-γ and interleukin-10 cytokines of spleen lymphocytes, and promoted the activation of natural killer cells. Therefore, PTFP, as an effective immunopotentiator, could induce a mixed T-helper (Th)1 and Th2 immune responses and an innate immune response.
References
Chen X., Han W., Wang G., Zhao X. 2020. Application prospect of polysaccharides in the development of anti-novel coronavirus drugs and vaccines. Int. J. Biol. Macromol. 164:331–343. 10.1016/j.ijbiomac.2020.07.106
Chen X., Yang H., Jia J., Chen Y., Wang J., Chen H., et al. 2021. Mulberry leaf polysaccharide supplementation contributes to enhancing the respiratory mucosal barrier immune response in Newcastle disease virus-vaccinated chicks. Poult Sci. 2021;100:592–602. 10.1016/j.psj.2020.11.039
Courant, T., Bayon, E., Reynaud-Dougier, H. L., Villiers, C., Menneteau M., Marche P.N., et al. 2017. Tailoring nanostructured lipid carriers for the delivery of protein antigens: physicochemical properties versus immunogenicity studies. Biomaterials. 136:29–42. 10.1016/j.biomaterials.2017.05.001
Dai B., Hu Z., Li H., Yan C., Zhang L. 2015. Simultaneous determination of six flavonoids from Paulownia tomentosa flower extract in rat plasma by LC-MS/MS and its application to a pharmacokinetic study. J. Chromatogr. B. 978-979:54–61. 10.1016/j.jchromb.2014.11.021
Feng H., Du X., Tang J., Cao X., Han X., Chen Z., et al. 2013. Enhancement of the immune responses to foot-and-mouth disease vaccination in mice by oral administration of a novel polysaccharide from the roots of Radix Cyathulae officinalis Kuan (RC). Cell. Immunol. 281(2):111–121. 10.1016/j.cellimm.2013.02.004
Gan T., Feng C., Lan H., Yang R., Zhang J., Li C., et al. 2021. Comparison of the structure and immunomodulatory activity of polysaccharides from fresh and dried longan. J. Funct. Foods. 2021;76:104323. 10.1016/j.jff.2020.104323
Huang R., Shen M., Yu Y., Liu X., Xie J. 2020. Physicochemical characterization and immunomodulatory activity of sulfated Chinese yam polysaccharide. Int. J. Biol. Macromol. 165:635–644. 10.1016/j.ijbiomac.2020.09.213
Huang Y., Jiang C., Hu Y., Zhao X., Shi C., Yu Y., et al. 2013. Immunoenhancement effect of Rehmannia glutinosa polysaccharide on lymphocyte proliferation and dendritic cell. Carbohydr. Polym. 2013;96(2):516–521. 10.1016/j.carbpol.2013.04.018
Kumar S., Kesharwani S.S., Kuppast B., Bakkari M.A., Tummala H. 2017. Pathogen-mimicking vaccine delivery system designed with a bioactive polymer (inulin acetate) for robust humoral and cellular immune responses. J Control Release. 261:263–274. 10.1016/j.jconrel.2017.06.026
Lee J.W., Seo K.H., Ryu H.W., Yuk H.J., Park H.A., Lim Y., et al. 2018. Anti-inflammatory effect of stem bark of Paulownia tomentosa Steud. in lipopolysaccharide (LPS)-stimulated RAW264.7 macrophages and LPS-induced murine model of acute lung injury. J. Ethnopharmacol. 210:23–30. 10.1016/j.jep.2017.08.028
Liu C., Ma J., Sun J., Cheng C., Feng Z., Jiang H., et al. 2017. Flavonoid-rich extract of paulownia fortunei flowers attenuates diet-induced hyperlipidemia, hepatic steatosis and insulin resistance in obesity mice by AMPK pathway. nutrients. 9(9):959. 10.3390/nu9090959
Liu Y., Jiao F., Qiu Y., Li W., Lao F., Zhou G., et al. 2009 .The effect of Gd@C82(OH)22 nanoparticles on the release of Th1/Th2 cytokines and induction of TNF-alpha mediated cellular immunity. Biomaterials. 30(23-24):3934–3945. http://ir.ihep.ac.cn/handle/311005/239953
Liu Y., Wang L., Zhang Y., Zhang W., Chen X., Yang T., et al. 2014. Uniform-sized water-in-oil vaccine formulations enhance immune response against Newcastle disease and avian influenza in chickens. Int. Immunopharmacol. 2014;23(2):603–608. 10.1016/j.intimp.2014.10.011
Lu T., Hu F., Yue H., Yang T., Ma G. 2020. The incorporation of cationic property and immunopotentiator in poly (lactic acid) microparticles promoted the immune response against chronic hepatitis B. J. Control. Release. 321:576–588. 10.1016/j.jconrel.2020.02.039
Ma X., Bi S., Wang Y., Chi X., Hu S. 2019.Combined adjuvant effect of ginseng stem-leaf saponins and selenium on immune responses to a live bivalent vaccine of Newcastle disease virus and infectious bronchitis virus in chickens. Poult Sci. 98(9):3548–3556. 10.3382/ps/pez207
Park H., Wang D., Hong H., Shin K. 2017. Antitumor and antimetastatic activities of pectic polysaccharides isolated from persimmon leaves mediated by enhanced natural killer cell activity. J. Funct. Foods. 37:460–466. 10.1016/j.jff.2017.08.027
Ren L., Zhang J., Zhang T. 2021. Immunomodulatory activities of polysaccharides from Ganoderma on immune effector cells. Food Chem. 340:127933. 10.1016/j.foodchem.2020.127933
Su C., Duan X., Liang L., Feng W., Zheng J., Fu X., et al. 2014. Lycium barbarum polysaccharides as an adjuvant for recombinant vaccine through enhancement of humoral immunity by activating Tfh cells. Vet. Immunol. Immunopathol. 158(1-2):98–104. 10.1016/j.vetimm.2013.05.006
Sun B., Yu S., Zhao D., Guo S., Wang X., Zhao K. 2018. Polysaccharides as vaccine adjuvants. Vaccine. 36(35):5226–5234. 10.1016/j.vaccine.2018.07.040
Sun H., Fei L., Zhu B., Shi M. 2020. Quick and improved immune responses to inactivated H9N2 avian influenza vaccine by purified active fraction of Albizia julibrissin saponins. BMC Vet Res. 16(1):427. 10.1186/s12917-020-02648-1
Tang C., Sun J., Liu J., Jin C., Wu X., Zhang X., et al. 2019. Immune-enhancing effects of polysaccharides from purple sweet potato. Int. J. Biol. Macromol. 123:923–930. 10.1016/j.ijbiomac.2018.11.187
Wang J., Ge B., Li Z., Guan F., Li F. 2016. Structural analysis and immunoregulation activity comparison of five polysaccharides from Angelica sinensis. Carbohydr. Polym. 140:6-12. 10.1016/j.carbpol.2015.12.050
Wang Q., Meng X., Zhu L., Xu Y., Cui W., He X., et al. 2019. A polysaccharide found in Paulownia fortunei flowers can enhance cellular and humoral immunity in chickens. Int. J. Biol. Macromol. 130:213–219. 10.1016/j.ijbiomac.2019.01.168
Wang M., Meng X., Yang R., Qin T., Li Y., Zhang L., et al. 2013. Cordyceps militaris polysaccharides can improve the immune efficacy of Newcastle disease vaccine in chicken. Int. J. Biol. Macromol. 59:178–183. 10.1016/j.ijbiomac.2013.04.007
Wu Y., Wei W., Zhou M., Wang Y., Wu J., Ma G., et al. 2012. Thermal-sensitive hydrogel as adjuvant-free vaccine delivery system for H5N1 intranasal immunization. Biomaterials. 33(7):2351–2360. 10.1016/j.biomaterials.2011.11.068
Xie F., Li Y., Su F., Hu S. 2012. Adjuvant effect of Atractylodis macrocephalae Koidz polysaccharides on the immune response to foot-and-mouth disease vaccine. Carbohydr. Polym. 87(2):1713–1719. 10.1016/j.carbpol.2011.09.080
Xie X., Ma L., Zhou Y., Shen W., Xu D., Dou J., et al. 2019. Polysaccharide enhanced NK cell cytotoxicity against pancreatic cancer via TLR4/MAPKs/NF-kappaB pathway in vitro/vivo. Carbohydr. Polym. 225:115223. 10.1016/j.carbpol.2019.115223
Xu W., Fang S., Cui X., Guan R., Wang Y., Shi F., et al. 2019. Signaling pathway underlying splenocytes activation by polysaccharides from Atractylodis macrocephalae Koidz. Mol. Immunol. 111:19–26. 10.1016/j.molimm.2019.03.004
Yang H., Zhang P., Xu X., Chen X., Liu Q., Jiang C. 2019. The enhanced immunological activity of Paulownia tomentosa flower polysaccharide on Newcastle disease vaccine in chicken. Biosci. Rep. 39(5): BSR20190224. 10.1042/BSR20190224
Yang L., Hu Y., Xue J., Wang F., Wang D., Kong X., et al. 2018. Compound Chinese herbal medicinal ingredients can enhance immune response and efficacy of RHD vaccine in rabbit. Vaccine. 26(35):4451–4455. 10.1016/j.vaccine.2008.06.075
Yuan L., Wang Y., Li Z., Ma X., Cui X., Chi X., et al. 2020. Sunflower seed oil containing ginseng stem-leaf saponins (E515-D) is a safe adjuvant for Newcastle disease vaccine. Poult. Sci. 99(10):4795–4803. 10.1016/j.psj.2020.06.063
Yang Y., Xing R., Liu S., Qin Y., Li K., Yu H., et al. 2020. Chitosan, hydroxypropyltrimethyl ammonium chloride chitosan and sulfated chitosan nanoparticles as adjuvants for inactivated Newcastle disease vaccine. Carbohydr. Polym. 229:115423. 10.1016/j.carbpol.2019.115423
Yu Y., Song Q., Huang L., Shen M., Yu Q., Chen Y., et al. 2020. Immunomodulatory activities of sulfated Cyclocarya paliurus polysaccharides with different degrees of substitution on mouse spleen lymphocytes. J. Funct. Foods. 64:103706. 10.1016/j.jff.2019.103706
Zeng P., Li J., Chen Y., Zhang L. 2019. The structures and biological functions of polysaccharides from traditional Chinese herbs. Progress in molecular biology and translational science. 163:423–444. 10.1016/bs.pmbts.2019.03.003
Zhai L., Li Y., Wang W., Hu S. 2011a. Enhancement of humoral immune responses to inactivated Newcastle disease and avian influenza vaccines by oral administration of ginseng stem-and-leaf saponins in chickens. Poult. Sci. 90(9):1955–1959. 10.3382/ps.2011-01433
Zhai L., Li Y., Wang W., Wang Y., Hu S. 2011b. Effect of oral administration of ginseng stem-and-leaf saponins (GSLS) on the immune responses to Newcastle disease vaccine in chickens. Vaccine. 29(31):5007–5014. 10.1016/j.vaccine.2011.04.097
Zhang W., Gong L., Liu Y., Zhou Z., Wan C., Xu J., et al. 2020. Immunoenhancement effect of crude polysaccharides of Helvella leucopus on cyclophosphamide-induced immunosuppressive mice. J. Funct. Foods. 69:103942. 10.1016/j.jff.2020.103942
Zhang W., Wang L., Liu Y., Chen X., Li J., Yang T., et al. 2014. Comparison of PLA microparticles and alum as adjuvants for H5N1 influenza split vaccine: adjuvanticity evaluation and preliminary action mode analysis. Pharm. Res. 31(4):1015–1031. 10.1007/s11095-013-1224-z
Zhao Y., Yan B., Wang Z., Li M., Zhao W. 2020. Natural polysaccharides with immunomodulatory activities. Mini. Rev. Med. Chem. 20(2):96–106. 10.2174/1389557519666190913151632
Chen X., Yang H., Jia J., Chen Y., Wang J., Chen H., et al. 2021. Mulberry leaf polysaccharide supplementation contributes to enhancing the respiratory mucosal barrier immune response in Newcastle disease virus-vaccinated chicks. Poult Sci. 2021;100:592–602. 10.1016/j.psj.2020.11.039
Courant, T., Bayon, E., Reynaud-Dougier, H. L., Villiers, C., Menneteau M., Marche P.N., et al. 2017. Tailoring nanostructured lipid carriers for the delivery of protein antigens: physicochemical properties versus immunogenicity studies. Biomaterials. 136:29–42. 10.1016/j.biomaterials.2017.05.001
Dai B., Hu Z., Li H., Yan C., Zhang L. 2015. Simultaneous determination of six flavonoids from Paulownia tomentosa flower extract in rat plasma by LC-MS/MS and its application to a pharmacokinetic study. J. Chromatogr. B. 978-979:54–61. 10.1016/j.jchromb.2014.11.021
Feng H., Du X., Tang J., Cao X., Han X., Chen Z., et al. 2013. Enhancement of the immune responses to foot-and-mouth disease vaccination in mice by oral administration of a novel polysaccharide from the roots of Radix Cyathulae officinalis Kuan (RC). Cell. Immunol. 281(2):111–121. 10.1016/j.cellimm.2013.02.004
Gan T., Feng C., Lan H., Yang R., Zhang J., Li C., et al. 2021. Comparison of the structure and immunomodulatory activity of polysaccharides from fresh and dried longan. J. Funct. Foods. 2021;76:104323. 10.1016/j.jff.2020.104323
Huang R., Shen M., Yu Y., Liu X., Xie J. 2020. Physicochemical characterization and immunomodulatory activity of sulfated Chinese yam polysaccharide. Int. J. Biol. Macromol. 165:635–644. 10.1016/j.ijbiomac.2020.09.213
Huang Y., Jiang C., Hu Y., Zhao X., Shi C., Yu Y., et al. 2013. Immunoenhancement effect of Rehmannia glutinosa polysaccharide on lymphocyte proliferation and dendritic cell. Carbohydr. Polym. 2013;96(2):516–521. 10.1016/j.carbpol.2013.04.018
Kumar S., Kesharwani S.S., Kuppast B., Bakkari M.A., Tummala H. 2017. Pathogen-mimicking vaccine delivery system designed with a bioactive polymer (inulin acetate) for robust humoral and cellular immune responses. J Control Release. 261:263–274. 10.1016/j.jconrel.2017.06.026
Lee J.W., Seo K.H., Ryu H.W., Yuk H.J., Park H.A., Lim Y., et al. 2018. Anti-inflammatory effect of stem bark of Paulownia tomentosa Steud. in lipopolysaccharide (LPS)-stimulated RAW264.7 macrophages and LPS-induced murine model of acute lung injury. J. Ethnopharmacol. 210:23–30. 10.1016/j.jep.2017.08.028
Liu C., Ma J., Sun J., Cheng C., Feng Z., Jiang H., et al. 2017. Flavonoid-rich extract of paulownia fortunei flowers attenuates diet-induced hyperlipidemia, hepatic steatosis and insulin resistance in obesity mice by AMPK pathway. nutrients. 9(9):959. 10.3390/nu9090959
Liu Y., Jiao F., Qiu Y., Li W., Lao F., Zhou G., et al. 2009 .The effect of Gd@C82(OH)22 nanoparticles on the release of Th1/Th2 cytokines and induction of TNF-alpha mediated cellular immunity. Biomaterials. 30(23-24):3934–3945. http://ir.ihep.ac.cn/handle/311005/239953
Liu Y., Wang L., Zhang Y., Zhang W., Chen X., Yang T., et al. 2014. Uniform-sized water-in-oil vaccine formulations enhance immune response against Newcastle disease and avian influenza in chickens. Int. Immunopharmacol. 2014;23(2):603–608. 10.1016/j.intimp.2014.10.011
Lu T., Hu F., Yue H., Yang T., Ma G. 2020. The incorporation of cationic property and immunopotentiator in poly (lactic acid) microparticles promoted the immune response against chronic hepatitis B. J. Control. Release. 321:576–588. 10.1016/j.jconrel.2020.02.039
Ma X., Bi S., Wang Y., Chi X., Hu S. 2019.Combined adjuvant effect of ginseng stem-leaf saponins and selenium on immune responses to a live bivalent vaccine of Newcastle disease virus and infectious bronchitis virus in chickens. Poult Sci. 98(9):3548–3556. 10.3382/ps/pez207
Park H., Wang D., Hong H., Shin K. 2017. Antitumor and antimetastatic activities of pectic polysaccharides isolated from persimmon leaves mediated by enhanced natural killer cell activity. J. Funct. Foods. 37:460–466. 10.1016/j.jff.2017.08.027
Ren L., Zhang J., Zhang T. 2021. Immunomodulatory activities of polysaccharides from Ganoderma on immune effector cells. Food Chem. 340:127933. 10.1016/j.foodchem.2020.127933
Su C., Duan X., Liang L., Feng W., Zheng J., Fu X., et al. 2014. Lycium barbarum polysaccharides as an adjuvant for recombinant vaccine through enhancement of humoral immunity by activating Tfh cells. Vet. Immunol. Immunopathol. 158(1-2):98–104. 10.1016/j.vetimm.2013.05.006
Sun B., Yu S., Zhao D., Guo S., Wang X., Zhao K. 2018. Polysaccharides as vaccine adjuvants. Vaccine. 36(35):5226–5234. 10.1016/j.vaccine.2018.07.040
Sun H., Fei L., Zhu B., Shi M. 2020. Quick and improved immune responses to inactivated H9N2 avian influenza vaccine by purified active fraction of Albizia julibrissin saponins. BMC Vet Res. 16(1):427. 10.1186/s12917-020-02648-1
Tang C., Sun J., Liu J., Jin C., Wu X., Zhang X., et al. 2019. Immune-enhancing effects of polysaccharides from purple sweet potato. Int. J. Biol. Macromol. 123:923–930. 10.1016/j.ijbiomac.2018.11.187
Wang J., Ge B., Li Z., Guan F., Li F. 2016. Structural analysis and immunoregulation activity comparison of five polysaccharides from Angelica sinensis. Carbohydr. Polym. 140:6-12. 10.1016/j.carbpol.2015.12.050
Wang Q., Meng X., Zhu L., Xu Y., Cui W., He X., et al. 2019. A polysaccharide found in Paulownia fortunei flowers can enhance cellular and humoral immunity in chickens. Int. J. Biol. Macromol. 130:213–219. 10.1016/j.ijbiomac.2019.01.168
Wang M., Meng X., Yang R., Qin T., Li Y., Zhang L., et al. 2013. Cordyceps militaris polysaccharides can improve the immune efficacy of Newcastle disease vaccine in chicken. Int. J. Biol. Macromol. 59:178–183. 10.1016/j.ijbiomac.2013.04.007
Wu Y., Wei W., Zhou M., Wang Y., Wu J., Ma G., et al. 2012. Thermal-sensitive hydrogel as adjuvant-free vaccine delivery system for H5N1 intranasal immunization. Biomaterials. 33(7):2351–2360. 10.1016/j.biomaterials.2011.11.068
Xie F., Li Y., Su F., Hu S. 2012. Adjuvant effect of Atractylodis macrocephalae Koidz polysaccharides on the immune response to foot-and-mouth disease vaccine. Carbohydr. Polym. 87(2):1713–1719. 10.1016/j.carbpol.2011.09.080
Xie X., Ma L., Zhou Y., Shen W., Xu D., Dou J., et al. 2019. Polysaccharide enhanced NK cell cytotoxicity against pancreatic cancer via TLR4/MAPKs/NF-kappaB pathway in vitro/vivo. Carbohydr. Polym. 225:115223. 10.1016/j.carbpol.2019.115223
Xu W., Fang S., Cui X., Guan R., Wang Y., Shi F., et al. 2019. Signaling pathway underlying splenocytes activation by polysaccharides from Atractylodis macrocephalae Koidz. Mol. Immunol. 111:19–26. 10.1016/j.molimm.2019.03.004
Yang H., Zhang P., Xu X., Chen X., Liu Q., Jiang C. 2019. The enhanced immunological activity of Paulownia tomentosa flower polysaccharide on Newcastle disease vaccine in chicken. Biosci. Rep. 39(5): BSR20190224. 10.1042/BSR20190224
Yang L., Hu Y., Xue J., Wang F., Wang D., Kong X., et al. 2018. Compound Chinese herbal medicinal ingredients can enhance immune response and efficacy of RHD vaccine in rabbit. Vaccine. 26(35):4451–4455. 10.1016/j.vaccine.2008.06.075
Yuan L., Wang Y., Li Z., Ma X., Cui X., Chi X., et al. 2020. Sunflower seed oil containing ginseng stem-leaf saponins (E515-D) is a safe adjuvant for Newcastle disease vaccine. Poult. Sci. 99(10):4795–4803. 10.1016/j.psj.2020.06.063
Yang Y., Xing R., Liu S., Qin Y., Li K., Yu H., et al. 2020. Chitosan, hydroxypropyltrimethyl ammonium chloride chitosan and sulfated chitosan nanoparticles as adjuvants for inactivated Newcastle disease vaccine. Carbohydr. Polym. 229:115423. 10.1016/j.carbpol.2019.115423
Yu Y., Song Q., Huang L., Shen M., Yu Q., Chen Y., et al. 2020. Immunomodulatory activities of sulfated Cyclocarya paliurus polysaccharides with different degrees of substitution on mouse spleen lymphocytes. J. Funct. Foods. 64:103706. 10.1016/j.jff.2019.103706
Zeng P., Li J., Chen Y., Zhang L. 2019. The structures and biological functions of polysaccharides from traditional Chinese herbs. Progress in molecular biology and translational science. 163:423–444. 10.1016/bs.pmbts.2019.03.003
Zhai L., Li Y., Wang W., Hu S. 2011a. Enhancement of humoral immune responses to inactivated Newcastle disease and avian influenza vaccines by oral administration of ginseng stem-and-leaf saponins in chickens. Poult. Sci. 90(9):1955–1959. 10.3382/ps.2011-01433
Zhai L., Li Y., Wang W., Wang Y., Hu S. 2011b. Effect of oral administration of ginseng stem-and-leaf saponins (GSLS) on the immune responses to Newcastle disease vaccine in chickens. Vaccine. 29(31):5007–5014. 10.1016/j.vaccine.2011.04.097
Zhang W., Gong L., Liu Y., Zhou Z., Wan C., Xu J., et al. 2020. Immunoenhancement effect of crude polysaccharides of Helvella leucopus on cyclophosphamide-induced immunosuppressive mice. J. Funct. Foods. 69:103942. 10.1016/j.jff.2020.103942
Zhang W., Wang L., Liu Y., Chen X., Li J., Yang T., et al. 2014. Comparison of PLA microparticles and alum as adjuvants for H5N1 influenza split vaccine: adjuvanticity evaluation and preliminary action mode analysis. Pharm. Res. 31(4):1015–1031. 10.1007/s11095-013-1224-z
Zhao Y., Yan B., Wang Z., Li M., Zhao W. 2020. Natural polysaccharides with immunomodulatory activities. Mini. Rev. Med. Chem. 20(2):96–106. 10.2174/1389557519666190913151632
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