Acknowledgement
This work was supported by Chungnam National University The authors thank Dr. Y.K. Choi (Chungbuk National University, South Korea) for providing H5N2/HA sequence-bearing plasmid and mouse-adapted A/Aquatic bird/Korea/W81/2005(H5N2) virus.
References
- Selleck P, Kirkland P. 2009. Avian influenza. Australian and New Zealand standard diagnostic procedures for animal diseases, Sub-Committee on Animal Health Laboratory Standards for Animal Health Committee, Australia [cited 2010 Feb 14]. http://www.scahls.org.au.
- Blagodatski A, Trutneva K, Glazova O, Mityaeva O, Shevkova L, Kegeles E, et al. 2021. Avian influenza in wild birds and poultry: Dissemination pathways, monitoring methods, and virus ecology. Pathogens 10: 630.
- Shirvani E, Varghese BP, Paldurai A, Samal SK. 2020. A recombinant avian paramyxovirus serotype 3 expressing the hemagglutinin protein protects chickens against H5N1 highly pathogenic avian influenza virus challenge. Sci. Rep. 10: 2221.
- Byrne AM, Reid SM, Seekings AH, Nunez A, Obeso Prieto AB, Ridout S, et al. 2021. H7N7 avian influenza virus mutation from low to high pathogenicity on a layer chicken farm in the UK. Viruses 13: 259.
- Seekings A, Slomka M, Russell C, Howard W, Choudhury B, Nunez A, et al. 2018. 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: 13-31. https://doi.org/10.1016/j.meegid.2018.06.005
- Laleye AT, Abolnik C. 2020. Emergence of highly pathogenic H5N2 and H7N1 influenza A viruses from low pathogenic precursors by serial passage in ovo. PLoS One 15: e0240290.
- Dhingra MS, Artois J, Dellicour S, Lemey P, Dauphin G, Von Dobschuetz S, et al. 2018. Geographical and historical patterns in the emergences of novel highly pathogenic avian influenza (HPAI) H5 and H7 viruses in poultry. Front. Vet. Sci. 5: 84.
- Lee YN, Lee DH, Cheon SH, Park YR, Baek YG, Si YJ, et al. 2020. Genetic characteristics and pathogenesis of H5 low pathogenic avian influenza viruses from wild birds and domestic ducks in South Korea. Sci. Rep. 10: 12151.
- Taubenberger J, Morens D. 2009. Pandemic influenza-including a risk assessment of H5N1. Rev. Sci. Tech. 28: 187-202. https://doi.org/10.20506/rst.28.1.1879
- Cui J, Qu N, Guo Y, Cao L, Wu S, Mei K, et al. 2017. Phylogeny, pathogenicity, and transmission of H5N1 avian influenza viruses in chickens. Front. Cell. Infect. Microbiol. 7: 328.
- Jang Y, Seo SH. 2022. H5 cleavage-site peptide vaccine protects chickens from lethal infection by highly pathogenic H5 avian influenza viruses. Arch. Virol. 167: 67-75. https://doi.org/10.1007/s00705-021-05284-8
- Liang WS, He YC, Wu HD, Li YT, Shih TH, Kao GS, et al. 2020. Ecological factors associated with persistent circulation of multiple highly pathogenic avian influenza viruses among poultry farms in Taiwan during 2015-17. PLoS One 15: e0236581.
- Spackman E, Prosser DJ, Pantin-Jackwood M, Stephens CB, Berlin AM. 2019. 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: 366-370. https://doi.org/10.1637/11950-081418-ResNote.1
- Marchenko V, Goncharova N, Susloparov I, Kolosova N, Gudymo A, Svyatchenko S, et al. 2018. Isolation and characterization of H5Nx highly pathogenic avian influenza viruses of clade 2.3. 4.4 in Russia. Virology 525: 216-223. https://doi.org/10.1016/j.virol.2018.09.024
- Zhao K, Gu M, Zhong L, Duan Z, Zhang Y, Zhu Y, et al. 2013. Characterization of three H5N5 and one H5N8 highly pathogenic avian influenza viruses in China. Vet. Microbiol. 163: 351-357. https://doi.org/10.1016/j.vetmic.2012.12.025
- Lee YJ, Kang HM, Lee EK, Song BM, Jeong J, Kwon YK, et al. 2014. Novel reassortant influenza A (H5N8) viruses, South Korea, 2014. Emerg. Infect. Dis. 20: 1087-1089.
- Pan M, Gao R, Lv Q, Huang S, Zhou Z, Yang L, et al. 2016. Human infection with a novel, highly pathogenic avian influenza A (H5N6) virus: virological and clinical findings. J. Infect. 72: 52-59. https://doi.org/10.1016/j.jinf.2015.06.009
- Lee JH, Pascua PNQ, Song MS, Baek YH, Kim CJ, Choi HW, et al. 2009. Isolation and genetic characterization of H5N2 influenza viruses from pigs in Korea. J. Virol. 83: 4205-4215. https://doi.org/10.1128/JVI.02403-08
- Choi WS, Baek YH, Kwon JJ, Jeong JH, Park SJ, Kim YI, et al. 2017. Rapid acquisition of polymorphic virulence markers during adaptation of highly pathogenic avian influenza H5N8 virus in the mouse. Sci. Rep. 7: 40667.
- Lee DH, Song CS. 2013. H9N2 avian influenza virus in Korea: evolution and vaccination. Clin. Exper. Vaccine Res. 2: 26-33. https://doi.org/10.7774/cevr.2013.2.1.26
- Bridges CB, Katz JM, Seto WH, Chan PK, Tsang D, Ho W, et al. 2000. Risk of influenza A (H5N1) infection among health care workers exposed to patients with influenza A (H5N1), Hong Kong. J. Infect. Dis. 181: 344-348. https://doi.org/10.1086/315213
- Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, Puthavathana P, et al. 2005. Probable person-to-person transmission of avian influenza A (H5N1). New England J. Med. 352: 333-340. https://doi.org/10.1056/NEJMoa044021
- Webster RG, Govorkova EA. 2006. H5N1 influenza-continuing evolution and spread. New Eng. J. Med. 355: 2174-2177. https://doi.org/10.1056/NEJMp068205
- Denney L, Ho L-P. 2018. The role of respiratory epithelium in host defence against influenza virus infection. Biomed. J. 41: 218-233. https://doi.org/10.1016/j.bj.2018.08.004
- Brokstad KA, Eriksson J-C, Cox RJ, Tynning T, Olofsson J, Jonsson R, et al. 2002. Parenteral vaccination against influenza does not induce a local antigen-specific immune response in the nasal mucosa. J. Infect. Dis. 185: 878-884. https://doi.org/10.1086/339710
- Liu H, Patil HP, de Vries-Idema J, Wilschut J, Huckriede A. 2013. Evaluation of mucosal and systemic immune responses elicited by GPI-0100-adjuvanted influenza vaccine delivered by different immunization strategies. PLoS One 8: e69649.
- Kim L, Martinez CJ, Hodgson KA, Trager GR, Brandl JR, Sandefer EP, et al. 2016. Systemic and mucosal immune responses following oral adenoviral delivery of influenza vaccine to the human intestine by radio controlled capsule. Sci. Rep. 6: 37295.
- Baker Jr JR, Farazuddin M, Wong PT, O'Konek JJ. 2022. The unfulfilled potential of mucosal immunization. J. Allergy Clin. Immunol. 150: 1-11. https://doi.org/10.1016/j.jaci.2022.05.002
- Calzas C, Chevalier C. 2019. Innovative mucosal vaccine formulations against influenza A virus infections. Front. Immunol. 10: 1605.
- Kikuchi Y, Kunitoh-Asari A, Hayakawa K, Imai S, Kasuya K, Abe K, et al. 2014. Oral administration of Lactobacillus plantarum strain AYA enhances IgA secretion and provides survival protection against influenza virus infection in mice. PLoS One 9: e86416.
- Lee YN, Youn HN, Kwon JH, Lee DH, Park JK, Yuk SS, et al. 2013. Sublingual administration of Lactobacillus rhamnosus affects respiratory immune responses and facilitates protection against influenza virus infection in mice. Antiviral Res. 98: 284-290. https://doi.org/10.1016/j.antiviral.2013.03.013
- Wang Z, Yu Q, Fu J, Liang J, Yang Q. 2013. Immune responses of chickens inoculated with recombinant L actobacillus expressing the haemagglutinin of the avian influenza virus. J. Appl. Microbiol. 115: 1269-1277. https://doi.org/10.1111/jam.12325
- Poo H, Pyo HM, Lee TY, Yoon SW, Lee JS, Kim CJ, et al. 2006. Oral administration of human papillomavirus type 16 E7 displayed on Lactobacillus casei induces E7-specific antitumor effects in C57/BL6 mice. Int. J. Cancer 119: 1702-1709. https://doi.org/10.1002/ijc.22035
- Lee JS, Poo H, Han DP, Hong SP, Kim K, Cho MW, et al. 2006. Mucosal immunization with surface-displayed severe acute respiratory syndrome coronavirus spike protein on Lactobacillus casei induces neutralizing antibodies in mice. J. Virol. 80: 4079-4087. https://doi.org/10.1128/JVI.80.8.4079-4087.2006
- Li R, Chowdhury MY, Kim JH, Kim TH, Pathinayake P, Koo WS, et al. 2015. 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: 250-263. https://doi.org/10.1016/j.vetmic.2015.07.020
- Chowdhury MY, Li R, Kim JH, Park ME, Kim TH, Pathinayake P, et al. 2014. 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. PLoS One 9: e94051.
- Zhang N, Zheng BJ, Lu L, Zhou Y, Jiang S, Du L. 2015. Advancements in the development of subunit influenza vaccines. Microb. Infect. 17: 123-134. https://doi.org/10.1016/j.micinf.2014.12.006
- Khurana S, Verma S, Verma N, Crevar CJ, Carter DM, Manischewitz J, et al. 2011. Bacterial HA1 vaccine against pandemic H5N1 influenza virus: evidence of oligomerization, hemagglutination, and cross-protective immunity in ferrets. J. Virol. 85: 1246-1256. https://doi.org/10.1128/JVI.02107-10
- Du L, Zhao G, Sun S, Zhang X, Zhou X, Guo Y, et al. 2013. A critical HA1 neutralizing domain of H5N1 influenza in an optimal conformation induces strong cross-protection. PLoS One 8: e53568.
- Palomino MM, Allievi MC, Prado-Acosta M, Sanchez-Rivas C, Ruzal SM. 2010. New method for electroporation of Lactobacillus species grown in high salt. J. Microbiol. Methods 83: 164-167. https://doi.org/10.1016/j.mimet.2010.08.017
- Velumani S, Ho HT, He F, Musthaq S, Prabakaran M, Kwang J. 2011. A novel peptide ELISA for universal detection of antibodies to human H5N1 influenza viruses. PLoS One 6: e20737.
- Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 27: 493-497. https://doi.org/10.1093/oxfordjournals.aje.a118408
- Gross FL, Bai Y, Jefferson S, Holiday C, Levine MZ. 2017. Measuring influenza neutralizing antibody responses to A (H3N2) viruses in human sera by microneutralization assays using MDCK-SIAT1 cells. J. Vis. Exp. 129: 56448.
- van Riet E, Ainai A, Suzuki T, Hasegawa H. 2012. Mucosal IgA responses in influenza virus infections; thoughts for vaccine design. Vaccine 30: 5893-5900. https://doi.org/10.1016/j.vaccine.2012.04.109
- Putcharoen O, Wacharapluesadee S, Chia WN, Paitoonpong L, Tan CW, Suwanpimolkul G, et al. 2021. Early detection of neutralizing antibodies against SARS-CoV-2 in COVID-19 patients in Thailand. PLoS One 16: e0246864.
- Lopez CE, Legge KL. 2020. Influenza A virus vaccination: immunity, protection, and recent advances toward a universal vaccine. Vaccines 8: 434.
- Fukuyama Y, Tokuhara D, Kataoka K, Gilbert RS, McGhee JR, Yuki Y, et al. 2012. Novel vaccine development strategies for inducing mucosal immunity. Expe. Rev. Vaccines 11: 367-379. https://doi.org/10.1586/erv.11.196
- Munoz-Provencio D, Llopis M, Antolin M, De Torres I, Guarner F, Perez-Martinez G, et al. 2009. Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix. Arch. Microbiol. 191: 153-161. https://doi.org/10.1007/s00203-008-0436-9
- Christensen HR, Frokiaer H, Pestka JJ. 2002. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 168: 171-178. https://doi.org/10.4049/jimmunol.168.1.171
- D'Arienzo R, Maurano F, Luongo D, Mazzarella G, Stefanile R, Troncone R, et al. 2008. Adjuvant effect of Lactobacillus casei in a mouse model of gluten sensitivity. Immunol. Lett. 119: 78-83. https://doi.org/10.1016/j.imlet.2008.04.006
- Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, et al. 2005. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc. Natl. Acad. Sci. 102: 2880-2885. https://doi.org/10.1073/pnas.0500098102
- Pouwels PH, Leer RJ, Shaw M, den Bak-Glashouwer M-JH, Tielen FD, Smit E, et al. 1998. Lactic acid bacteria as antigen delivery vehicles for oral immunization purposes. Int. J. Food Microbiol. 41: 155-167. https://doi.org/10.1016/S0168-1605(98)00048-8
- Lee SY, Choi JH, Xu Z. 2003. Microbial cell-surface display. Trends Biotechnol. 21: 45-52. https://doi.org/10.1016/S0167-7799(02)00006-9
- Russell CJ, Hu M, Okda FA. 2018. Influenza hemagglutinin protein stability, activation, and pandemic risk. Trends Microbiol. 26: 841-853. https://doi.org/10.1016/j.tim.2018.03.005
- Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Ann. Rev. Biochemy. 69: 531-569. https://doi.org/10.1146/annurev.biochem.69.1.531
- Wiley DC, Skehel JJ. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochemy. 56: 365-394. https://doi.org/10.1146/annurev.bi.56.070187.002053
- Gerhard W, Yewdell J, Frankel ME, Webster R. 1981. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290: 713-717. https://doi.org/10.1038/290713a0
- Zhang Y, Yang L, Zhang J, Huang K, Sun X, Yang Y, et al. 2022. 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: 185.
- Lei H, Sheng Z, Ding Q, Chen J, Wei X, Lam DM-K, et al. 2011. 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: 1046-1051. https://doi.org/10.1128/CVI.00050-11
- Rosenbaum P, Tchitchek N, Joly C, Rodriguez Pozo A, Stimmer L, Langlois S, et al. 2021. Vaccine inoculation route modulates early immunity and consequently antigen-specific immune response. Front. Immunol. 12: 645210.
- Wang Z, Yu Q, Gao J, Yang Q. 2012. Mucosal and systemic immune responses induced by recombinant Lactobacillus spp. expressing the hemagglutinin of the avian influenza virus H5N1. Clin. Vaccine Immunol. 19: 174-179. https://doi.org/10.1128/CVI.05618-11
- Vissers YM, Snel J, Zuurendonk PF, Smit BA, Wichers HJ, Savelkoul HF. 2010. Differential effects of Lactobacillus acidophilus and Lactobacillus plantarum strains on cytokine induction in human peripheral blood mononuclear cells. FEMS Immunol. Med. Microbiol. 59: 60-70. https://doi.org/10.1111/j.1574-695X.2010.00662.x
- Wiley JA, Tighe MP, Harmsen AG. 2005. 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: 3186-3196. https://doi.org/10.4049/jimmunol.175.5.3186
- de Pinho Favaro MT, Atienza-Garriga J, Martinez-Torro C, Parlade E, Vazquez E, Corchero JL, et al. 2022. Recombinant vaccines in 2022: a perspective from the cell factory. Microb. Cell Fact. 21: 1-17. https://doi.org/10.1186/s12934-021-01718-9
- Singh SK, Roeffen W, Mistarz UH, Chourasia BK, Yang F, Rand KD, et al. 2017. Construct design, production, and characterization of Plasmodium falciparum 48/45 R0. 6C subunit protein produced in Lactococcus lactis as candidate vaccine. Microb. Cell Fact. 16: 1-11. https://doi.org/10.1186/s12934-016-0616-2
- LeCureux JS, Dean GA. 2018. Lactobacillus mucosal vaccine vectors: immune responses against bacterial and viral antigens. Msphere. 3: 10.1128/msphere. 00061-00018.
- Shirdast H, Ebrahimzadeh F, Taromchi AH, Mortazavi Y, Esmaeilzadeh A, Sekhavati MH, et al. 2021. Recombinant Lactococcus lactis dsplaying Omp31 antigen of Brucella melitensis can induce an immunogenic response in BALB/c Mice. Probiotics Antimicrob. Proteins 13: 80-89. https://doi.org/10.1007/s12602-020-09684-1
- Detmer A, Glenting J. 2006. Live bacterial vaccines-a review and identification of potential hazards. Microb. Cell Fact. 5: 1-12. https://doi.org/10.1186/1475-2859-5-1