Mucosal Administration of Lactobacillus casei Surface-Displayed HA1 Induces Protective Immune Responses against Avian Influenza A Virus in Mice
2
조회
0
다운로드
1
인용
0
참고문헌
키워드
초록
Avian influenza is a serious threat to both public health and the poultry industry worldwide. This respiratory virus can be combated by eliciting robust immune responses at the site of infection through mucosal immunization. Recombinant probiotics, specifically lactic acid bacteria, are safe and effective carriers for mucosal vaccines. In this study, we engineered recombinant fusion protein by fusing the hemagglutinin 1 (HA1) subunit of the A/Aquatic bird/Korea/W81/2005 (H5N2) with the Bacillus subtilis poly γ-glutamic acid synthetase A (pgsA) at the surface of Lactobacillus casei (pgsAHA1/L. casei). Using subcellular fractionation and flow cytometry we confirmed the surface localization of this fusion protein. Mucosal administration of pgsA-HA1/L. casei in mice resulted in significant levels of HA1-specific serum IgG, mucosal IgA and neutralizing antibodies against the H5N2 virus. Additionally, pgsA-HA1/L. casei-induced systemic and local cell-mediated immune responses specific to HA1, as evidenced by an increased number of IFN-γ and IL-4 secreting cells in the spleens and higher levels of IL-4 in the local lymphocyte supernatants. Finally, mice inoculated with pgsAHA1/L. casei were protected against a 10LD50 dose of the homologous mouse-adapted H5N2 virus. These results suggest that mucosal immunization with L. casei displaying HA1 on its surface could be a potential strategy for developing a mucosal vaccine against other H5 subtype viruses.
Abstract
Avian influenza is a serious threat to both public health and the poultry industry worldwide. This respiratory virus can be combated by eliciting robust immune responses at the site of infection through mucosal immunization. Recombinant probiotics, specifically lactic acid bacteria, are safe and effective carriers for mucosal vaccines. In this study, we engineered recombinant fusion protein by fusing the hemagglutinin 1 (HA1) subunit of the A/Aquatic bird/Korea/W81/2005 (H5N2) with the Bacillus subtilis poly γ-glutamic acid synthetase A (pgsA) at the surface of Lactobacillus casei (pgsAHA1/L. casei). Using subcellular fractionation and flow cytometry we confirmed the surface localization of this fusion protein. Mucosal administration of pgsA-HA1/L. casei in mice resulted in significant levels of HA1-specific serum IgG, mucosal IgA and neutralizing antibodies against the H5N2 virus. Additionally, pgsA-HA1/L. casei-induced systemic and local cell-mediated immune responses specific to HA1, as evidenced by an increased number of IFN-γ and IL-4 secreting cells in the spleens and higher levels of IL-4 in the local lymphocyte supernatants. Finally, mice inoculated with pgsAHA1/L. casei were protected against a 10LD50 dose of the homologous mouse-adapted H5N2 virus. These results suggest that mucosal immunization with L. casei displaying HA1 on its surface could be a potential strategy for developing a mucosal vaccine against other H5 subtype viruses.
참고문헌 (68)
- "Avian influenza" (2009)[URL]
- Blagodatski A, "Avian influenza in wild birds and poultry : Dissemination pathways, monitoring methods, and virus ecology", Pathogens, 10, pp.630~ (2021)
- Shirvani E, "A recombinant avian paramyxovirus serotype 3 expressing the hemagglutinin protein protects chickens against H5N1 highly pathogenic avian influenza virus challenge", Sci. Rep, 10, pp.2221~ (2020)
- Byrne AM, "H7N7 avian influenza virus mutation from low to high pathogenicity on a layer chicken farm in the UK", Viruses, 13, pp.259~ (2021)
- Seekings A, "Direct evidence of H7N7 avian influenza virus mutation from low to high virulence on a single poultry premises during an outbreak in free range chickens in the UK, 2008", Infect. Genet. Evol, 64, pp.13~31 (2018)
- Laleye AT, "Emergence of highly pathogenic H5N2 and H7N1 influenza A viruses from low pathogenic precursors by serial passage in ovo", PLoS One, 15, pp.e0240290~ (2020)
- Dhingra MS, "Geographical and historical patterns in the emergences of novel highly pathogenic avian influenza(HPAI)H5 and H7 viruses in poultry", Front. Vet. Sci, 5, pp.84~ (2018)
- Lee YN, "Genetic characteristics and pathogenesis of H5 low pathogenic avian influenza viruses from wild birds and domestic ducks in South Korea", Sci. Rep, 10, pp.12151~ (2020)
- Taubenberger J, "Pandemic influenza–including a risk assessment of H5N1", Rev. Sci. Tech, 28, pp.187~202 (2009)
- Cui J, "Phylogeny, pathogenicity, and transmission of H5N1 avian influenza viruses in chickens", Front. Cell. Infect. Microbiol, 7, pp.328~ (2017)
- Jang Y, "H5 cleavage-site peptide vaccine protects chickens from lethal infection by highly pathogenic H5 avian influenza viruses", Arch. Virol, 167, pp.67~75 (2022)
- Liang WS, "Ecological factors associated with persistent circulation of multiple highly pathogenic avian influenza viruses among poultry farms in Taiwan during 2015-17", PLoS One, 15, pp.e0236581~ (2020)
- Spackman E, "Clade 2.3. 4.4 H5 north american highly pathogenic avian influenza viruses infect, but do not cause clinical signs in, American Black Ducks (Anas rubripes)", Avian Dis, 63, pp.366~370 (2019)
- Marchenko V, "Isolation and characterization of H5Nx highly pathogenic avian influenza viruses of clade 2.3. 4.4 in Russia", Virology, 525, pp.216~223 (2018)
- Zhao K, "Characterization of three H5N5 and one H5N8 highly pathogenic avian influenza viruses in China", Vet. Microbiol, 163, pp.351~357 (2013)
- Lee YJ, "Novel reassortant influenza A(H5N8)viruses, South Korea, 2014", Emerg. Infect. Dis, 20, pp.1087~1089 (2014)
- Pan M, "Human infection with a novel, highly pathogenic avian influenza A(H5N6)virus : virological and clinical findings", J. Infect, 72, pp.52~59 (2016)
- Lee JH, "Isolation and genetic characterization of H5N2 influenza viruses from pigs in Korea", J. Virol, 83, pp.4205~4215 (2009)
- Choi WS, "Rapid acquisition of polymorphic virulence markers during adaptation of highly pathogenic avian influenza H5N8 virus in the mouse", Sci. Rep, 7, pp.40667~ (2017)
- Lee DH, "H9N2 avian influenza virus in Korea : evolution and vaccination", Clin. Exper. Vaccine Res, 2, pp.26~33 (2013)
- Bridges CB, "Risk of influenza A(H5N1)infection among health care workers exposed to patients with influenza A(H5N1), Hong Kong", J. Infect. Dis, 181, pp.344~348 (2000)
- Ungchusak K, "Probable person-to-person transmission of avian influenza A(H5N1)", New England J. Med, 352, pp.333~340 (2005)
- Webster RG, "H5N1 influenza—continuing evolution and spread", New Eng. J. Med, 355, pp.2174~2177 (2006)
- Denney L, "The role of respiratory epithelium in host defence against influenza virus infection", Biomed. J, 41, pp.218~233 (2018)
- Brokstad KA, "Parenteral vaccination against influenza does not induce a local antigen-specific immune response in the nasal mucosa", J. Infect. Dis, 185, pp.878~884 (2002)
- Liu H, "Evaluation of mucosal and systemic immune responses elicited by GPI-0100-adjuvanted influenza vaccine delivered by different immunization strategies", PLoS One, 8, pp.e69649~ (2013)
- Kim L, "Systemic and mucosal immune responses following oral adenoviral delivery of influenza vaccine to the human intestine by radio controlled capsule", Sci. Rep, 6, pp.37295~ (2016)
- Baker Jr JR, "The unfulfilled potential of mucosal immunization", J. Allergy Clin. Immunol, 150, pp.1~11 (2022)
- Calzas C, "Innovative mucosal vaccine formulations against influenza A virus infections", Front. Immunol, 10, pp.1605~ (2019)
- Kikuchi Y, "Oral administration of Lactobacillus plantarum strain AYA enhances IgA secretion and provides survival protection against influenza virus infection in mice", PLoS One, 9, pp.e86416~ (2014)
- Lee YN, "Sublingual administration of Lactobacillus rhamnosus affects respiratory immune responses and facilitates protection against influenza virus infection in mice", Antiviral Res, 98, pp.284~290 (2013)
- Wang Z, "Immune responses of chickens inoculated with recombinant L actobacillus expressing the haemagglutinin of the avian influenza virus", J. Appl. Microbiol, 115, pp.1269~1277 (2013)
- Poo H, "Oral administration of human papillomavirus type 16 E7 displayed on Lactobacillus casei induces E7-specific antitumor effects in C57", BL6 mice, 2006, pp.119, 1702~1709
- Lee JS, "Mucosal immunization with surface-displayed severe acute respiratory syndrome coronavirus spike protein on Lactobacillus casei induces neutralizing antibodies in mice", J. Virol, 80, pp.4079~4087 (2006)
- Li R, "Mucosally administered Lactobacillus surface-displayed influenza antigens(sM2 and HA2)with cholera toxin subunit A1(CTA1)Induce broadly protective immune responses against divergent influenza subtypes", Vet. Microbiol, 179, pp.250~263 (2015)
- Chowdhury MY, "Mucosal vaccination with recombinant Lactobacillus casei-displayed CTA1-conjugated consensus matrix protein-2(sM2)induces broad protection against divergent influenza subtypes in BALB", c mice, 2014, pp.9, e94051~
- Zhang N, "Advancements in the development of subunit influenza vaccines", Microb. Infect, 17, pp.123~134 (2015)
- Khurana S, "Bacterial HA1 vaccine against pandemic H5N1influenza virus : evidence of oligomerization, hemagglutination, and cross-protective immunity in ferrets", J. Virol, 85, pp.1246~1256 (2011)
- Du L, "A critical HA1 neutralizing domain of H5N1 influenza in an optimal conformation induces strong cross-protection", PLoS One, 8, pp.e53568~ (2013)
- Palomino MM, "New method for electroporation of Lactobacillus species grown in high salt", J. Microbiol. Methods, 83, pp.164~167 (2010)
- Velumani S, "A novel peptide ELISA for universal detection of antibodies to human H5N1 influenza viruses", PLoS One, 6, pp.e20737~ (2011)
- Reed LJ, "A simple method of estimating fifty per cent endpoints", Am. J. Epidemiol, 27, pp.493~497 (1938)
- Gross FL, "Measuring influenza neutralizing antibody responses to A(H3N2)viruses in human sera by microneutralization assays using MDCK-SIAT1 cells", J. Vis. Exp, 129, pp.56448~ (2017)
- van Riet E, "Mucosal IgA responses in influenza virus infections; thoughts for vaccine design", Vaccine, 30, pp.5893~5900 (2012)
- Putcharoen O, "Early detection of neutralizing antibodies against SARS-CoV-2 in COVID-19 patients in Thailand", PLoS One, 16, pp.e0246864~ (2021)
- Lopez CE, "Influenza A virus vaccination : immunity, protection, and recent advances toward a universal vaccine", Vaccines, 8, pp.434~ (2020)
- Fukuyama Y, "Novel vaccine development strategies for inducing mucosal immunity", Expe. Rev. Vaccines, 11, pp.367~379 (2012)
- Muñoz-Provencio D, "Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix", Arch. Microbiol, 191, pp.153~161 (2009)
- Christensen HR, "Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells", J. Immunol, 168, pp.171~178 (2002)
- D’Arienzo R, "Adjuvant effect of Lactobacillus casei in a mouse model of gluten sensitivity", Immunol. Lett, 119, pp.78~83 (2008)
- Mohamadzadeh M, "Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization", Proc. Natl. Acad. Sci, 102, pp.2880~2885 (2005)
- Pouwels PH, "Lactic acid bacteria as antigen delivery vehicles for oral immunization purposes", Int. J. Food Microbiol, 41, pp.155~167 (1998)
- Lee SY, "Microbial cell-surface display", Trends Biotechnol, 21, pp.45~52 (2003)
- Russell CJ, "Influenza hemagglutinin protein stability, activation, and pandemic risk", Trends Microbiol, 26, pp.841~853 (2018)
- Skehel JJ, "Receptor binding and membrane fusion in virus entry : the influenza hemagglutinin", Ann. Rev. Biochemy, 69, pp.531~569 (2000)
- Wiley DC, "The structure and function of the hemagglutinin membrane glycoprotein of influenza virus", Annu. Rev. Biochemy, 56, pp.365~394 (1987)
- Gerhard W, "Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies", Nature, 290, pp.713~717 (1981)
- Zhang Y, "Oral or intranasal immunization with recombinant Lactobacillus plantarum displaying head domain of Swine Influenza A virus hemagglutinin protects mice from H1N1 virus", Microb. Cell. Fact, 21, pp.185~ (2022)
- Lei H, "Evaluation of oral immunization with recombinant avian influenza virus HA1 displayed on the Lactococcus lactis surface and combined with the mucosal adjuvant cholera toxin subunit B", Clin. Vaccine Immunol, 18, pp.1046~1051 (2011)
- Rosenbaum P, "Vaccine inoculation route modulates early immunity and consequently antigen-specific immune response", Front. Immunol, 12, pp.645210~ (2021)
- Wang Z, "Mucosal and systemic immune responses induced by recombinant Lactobacillus spp. expressing the hemagglutinin of the avian influenza virus H5N1", Clin. Vaccine Immunol, 19, pp.174~179 (2012)
- Vissers YM, "Differential effects of Lactobacillus acidophilus and Lactobacillus plantarum strains on cytokine induction in human peripheral blood mononuclear cells", FEMS Immunol. Med. Microbiol, 59, pp.60~70 (2010)
- Wiley JA, "Upper respiratory tract resistance to influenza infection is not prevented by the absence of either nasal-associated lymphoid tissue or cervical lymph nodes", J. Immunol, 175, pp.3186~3196 (2005)
- de Pinho Favaro MT, "Recombinant vaccines in 2022 : a perspective from the cell factory", Microb. Cell Fact, 21, pp.1~17 (2022)
- Singh SK, "Construct design, production, and characterization of Plasmodium falciparum 48", 45 R0. 6C subunit protein produced in Lactococcus lactis as candidate vaccine, 2017, pp.16, 1~11
- LeCureux JS, "Lactobacillus mucosal vaccine vectors : immune responses against bacterial and viral antigens", Msphere, 3 (2018)[DOI]
- Shirdast H, "Recombinant Lactococcus lactis dsplaying Omp31 antigen of Brucella melitensis can induce an immunogenic response in BALB", c Mice, 2021, pp.13, 80~89
- Detmer A, "Live bacterial vaccines–a review and identification of potential hazards", Microb. Cell Fact, 5, pp.1~12 (2006)
