Present Scenario of M-Cell Targeting Ligands for Oral Mucosal Immunization

Author(s): Surendra Saraf, Shailesh Jain, Rudra Narayan Sahoo, Subrata Mallick*

Journal Name: Current Drug Targets

Volume 21 , Issue 12 , 2020


  Journal Home
Translate in Chinese
Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

The immune system plays an important role in the prevention of infection and forms the first line of defense against pathogen attack. Delivering of antigen through mucosal route may elicit mucosal immune system as the mucosal surface is the most common site of pathogen entry. Mucosal immune system will be capable to counter pathogen at mucosal surface. Oral mucosal immunization opens the ways to deliver antigens at gut-associated lymphoid tissue. This can elicit both local and systemic immune response. Mucosal vaccines are economical, highly accessible, non parenteral delivery and capacity to produce mass immunization at the time of pandemics. To deliver antigens on the mucosal surface of the gastrointestinal tract, the immune system relies on specialized epithelial cell i.e. Microfold (M)-cell. An approach to exploit the targeting specific receptors on M-cell for entry of antigens has made a breakthrough in vaccine development. In this review, various strategies have been discussed for the possible entry of antigens through M-cells and an approach to increase the uptake and efficacy of vaccines for oral mucosal immunization.

Keywords: Oral mucosal immunization, M cell, gut-associated lymphoid tissues, Peyer’s patches, MALT, gastrointestinal.

[1]
Stern PL. The changing face of vaccines and vaccination. Vaccine 2016; 34(52): 6653-4.
[http://dx.doi.org/10.1016/j.vaccine.2016.11.014] [PMID: 27866771]
[2]
Baicus A. History of polio vaccination. World J Virol 2012; 1(4): 108-14.
[http://dx.doi.org/10.5501/wjv.v1.i4.108] [PMID: 24175215]
[3]
Owen JL, Sahay B, Mohamadzadeh M. New generation of oral mucosal vaccines targeting dendritic cells. Curr Opin Chem Biol 2013; 17(6): 918-24.
[http://dx.doi.org/10.1016/j.cbpa.2013.06.013] [PMID: 23835515]
[4]
Russell MW, Mestecky J. Mucosal Vaccines: An Overview In: Mucosal Immunology.4th 1039–46 Elsevier . 2015; pp. 1039-46.
[5]
Shukla A, Khatri K, Gupta PN, Goyal AK, Mehta A, Vyas SP. Oral immunization against hepatitis B using bile salt stabilized vesicles (bilosomes). J Pharm Pharm Sci 2008; 11(1): 59-66.
[http://dx.doi.org/10.18433/J3K01M] [PMID: 18445364]
[6]
Boyaka PN. Inducing Mucosal IgA: A Challenge for Vaccine Adjuvants and Delivery Systems. J Immunol 2017; 199(1): 9-16.
[http://dx.doi.org/10.4049/jimmunol.1601775] [PMID: 28630108]
[7]
Zhu Q, Berzofsky JA. Oral vaccines: directed safe passage to the front line of defense. Gut Microbes 2013; 4(3): 246-52.
[http://dx.doi.org/10.4161/gmic.24197]
[8]
Suzuki T, Ainai A, Hasegawa H. Functional and structural characteristics of secretory IgA antibodies elicited by mucosal vaccines against influenza virus. Vaccine 2017; 35(39): 5297-302.
[http://dx.doi.org/10.1016/j.vaccine.2017.07.093] [PMID: 28780981]
[9]
Li Y, Jin L, Chen T. The Effects of Secretory IgA in the Mucosal Immune System Pirozzi CJ 2020.
[10]
Corthésy B. Multi-faceted functions of secretory IgA at mucosal surfaces. Front Immunol 2013; 4: 185.
[http://dx.doi.org/10.3389/fimmu.2013.00185] [PMID: 23874333]
[11]
Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K. Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu Rev Immunol 2010; 28(1): 243-73.
[http://dx.doi.org/10.1146/annurev-immunol-030409-101314] [PMID: 20192805]
[12]
Lycke NY, Bemark M. The regulation of gut mucosal IgA B-cell responses: recent developments. Mucosal Immunol 2017; 10(6): 1361-74.
[http://dx.doi.org/10.1038/mi.2017.62] [PMID: 28745325]
[13]
Gonzales AM, Wilde S, Roland KL. New Insights into the Roles of Long Polar Fimbriae and Stg Fimbriae in Salmonella Interactions with Enterocytes and M Cells. Infect Immun 2017; 85(9): e00172-17.
[http://dx.doi.org/10.1128/IAI.00172-17] [PMID: 28630073]
[14]
Kim SH, Lee KY, Jang YS. Mucosal immune system and M cell-targeting strategies for oral mucosal vaccination. Immune Netw 2012; 12(5): 165-75.
[http://dx.doi.org/10.4110/in.2012.12.5.165] [PMID: 23213309]
[15]
McGuckin MA, Lindén SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 2011; 9(4): 265-78.
[http://dx.doi.org/10.1038/nrmicro2538] [PMID: 21407243]
[16]
Pelaseyed T, Bergström JH, Gustafsson JK, et al. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 2014; 260(1): 8-20.
[http://dx.doi.org/10.1111/imr.12182] [PMID: 24942678]
[17]
Karlsson J, Pütsep K, Chu H, Kays RJ, Bevins CL, Andersson M. Regional variations in Paneth cell antimicrobial peptide expression along the mouse intestinal tract. BMC Immunol 2008; 9: 37.
[http://dx.doi.org/10.1186/1471-2172-9-37] [PMID: 18637162]
[18]
Dillon A, Lo DD. M Cells: Intelligent Engineering of Mucosal Immune Surveillance. Front Immunol 2019; 10: 1499.
[http://dx.doi.org/10.3389/fimmu.2019.01499] [PMID: 31312204]
[19]
Iliev ID, Mileti E, Matteoli G, Chieppa M, Rescigno M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol 2009; 2(4): 340-50.
[http://dx.doi.org/10.1038/mi.2009.13] [PMID: 19387433]
[20]
Brandtzaeg P, Kiyono H, Pabst R, Russell MW. Terminology: nomenclature of mucosa-associated lymphoid tissue. Mucosal Immunol 2008; 1(1): 31-7.
[http://dx.doi.org/10.1038/mi.2007.9] [PMID: 19079158]
[21]
Cesta MF. Normal structure, function, and histology of mucosa-associated lymphoid tissue. Toxicol Pathol 2006; 34(5): 599-608.
[http://dx.doi.org/10.1080/01926230600865531] [PMID: 17067945]
[22]
Williams IR, Owen RL. M Cells: Specialized Antigen Sampling Cells in the Follicle-Associated Epithelium. 4th ed. Amsterdam: Elsevier Inc 2015; Vol. 1: pp. 211-29.
[http://dx.doi.org/10.1016/B978-0-12-415847-4.00013-6]
[23]
Lo DD, Ling J, Eckelhoefer AH. M cell targeting by a Claudin 4 targeting peptide can enhance mucosal IgA responses. BMC Biotechnol 2012; 12(1): 7.
[http://dx.doi.org/10.1186/1472-6750-12-7] [PMID: 22413871]
[24]
Yamamoto M, Pascual DW, Kiyono H. M cell-targeted mucosal vaccine strategies. Curr Top Microbiol Immunol 2012; 354: 39-52.
[http://dx.doi.org/10.1007/82_2011_134] [PMID: 21688209]
[25]
Mach J, Hshieh T, Hsieh D, Grubbs N, Chervonsky A. Development of intestinal M cells. Immunol Rev 2005; 206(1): 177-89.
[http://dx.doi.org/10.1111/j.0105-2896.2005.00281.x] [PMID: 16048549]
[26]
Kucharzik T, Lügering N, Rautenberg K, et al. Role of M cells in intestinal barrier function. Ann N Y Acad Sci 2000; 915: 171-83.
[http://dx.doi.org/10.1111/j.1749-6632.2000.tb05240.x] [PMID: 11193574]
[27]
Corr SC, Gahan CC, Hill C. M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunol Med Microbiol 2008; 52(1): 2-12.
[http://dx.doi.org/10.1111/j.1574-695X.2007.00359.x] [PMID: 18081850]
[28]
Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449(7165): 1003-7.
[http://dx.doi.org/10.1038/nature06196] [PMID: 17934449]
[29]
Gregorieff A, Stange DE, Kujala P, et al. The ets-domain transcription factor Spdef promotes maturation of goblet and paneth cells in the intestinal epithelium. Gastroenterology 2009; 137(4): 1333- 45.e1, 3.
[http://dx.doi.org/10.1053/j.gastro.2009.06.044] [PMID: 19549527]
[30]
Fujkuyama Y, Tokuhara D, Kataoka K, et al. Novel vaccine development strategies for inducing mucosal immunity. Expert Rev Vaccines 2012; 11(3): 367-79.
[http://dx.doi.org/10.1586/erv.11.196] [PMID: 22380827]
[31]
Kim S, Jang Y. Antigen targeting to M cells for enhancing the efficacy of mucosal vaccines. Exp &amp. Mol Med 2014; 46(3): 85-8.
[32]
Hsieh E-H, Lo DD. Jagged1 and Notch1 help edit M cell patterning in Peyer’s patch follicle epithelium. Dev Comp Immunol 2012; 37(2): 306-12.
[http://dx.doi.org/10.1016/j.dci.2012.04.003] [PMID: 22504165]
[33]
Wood MB, Rios D, Williams IR. TNF-α augments RANKL-dependent intestinal M cell differentiation in enteroid cultures. Am J Physiol Cell Physiol 2016; 311(3): C498-507.
[http://dx.doi.org/10.1152/ajpcell.00108.2016] [PMID: 27413168]
[34]
Sehgal A, Kobayashi A, Donaldson DS, Mabbott NA. c-Rel is dispensable for the differentiation and functional maturation of M cells in the follicle-associated epithelium. Immunobiology 2017; 222(2): 316-26.
[http://dx.doi.org/10.1016/j.imbio.2016.09.008] [PMID: 27663963]
[35]
de Lau W, Kujala P, Schneeberger K, et al. Peyer’s patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured “miniguts”. Mol Cell Biol 2012; 32(18): 3639-47.
[http://dx.doi.org/10.1128/MCB.00434-12] [PMID: 22778137]
[36]
Fasciano AC, Blutt SE, Estes MK, Mecsas J. Induced differentiation of M cell-like cells in human stem cell-derived ileal enteroid monolayers. J Vis Exp 2019; 26(149)
[http://dx.doi.org/10.3791/59894] [PMID: 31403623]
[37]
Rouch JD, Scott A, Lei NY, et al. Development of functional microfold (M) cells from intestinal stem cells in primary human enteroids. PLoS One 2016; 11(1)e0148216
[http://dx.doi.org/10.1371/journal.pone.0148216] [PMID: 26820624]
[38]
Kimura S, Mutoh M, Hisamoto M, et al. Airway M cells arise in the lower airway due to RANKL signaling and reside in the bronchiolar epithelium associated with iBALT in murine models of respiratory disease. Front Immunol 2019; 10: 1323.
[http://dx.doi.org/10.3389/fimmu.2019.01323] [PMID: 31244859]
[39]
Mutoh M, Kimura S, Takahashi-Iwanaga H, Hisamoto M, Iwanaga T, Iida J. RANKL regulates differentiation of microfold cells in mouse nasopharynx-associated lymphoid tissue (NALT). Cell Tissue Res 2016; 364(1): 175-84.
[http://dx.doi.org/10.1007/s00441-015-2309-2] [PMID: 26553655]
[40]
Kimura S, Kobayashi N, Nakamura Y, et al. Sox8 is essential for M cell maturation to accelerate IgA response at the early stage after weaning in mice. J Exp Med 2019; 216(4): 831-46.
[http://dx.doi.org/10.1084/jem.20181604] [PMID: 30877171]
[41]
Özbek M, Bayraktaroğlu AG. Developmental study on the ileal Peyer’s patches of sheep, and cytokeratin-18 as a possible marker for M cells in follicle associated epithelium. Acta Histochem 2019; 121(3): 311-22.
[http://dx.doi.org/10.1016/j.acthis.2019.01.005] [PMID: 30745250]
[42]
Beloqui A, Brayden DJ, Artursson P, Préat V, des Rieux A. A human intestinal M-cell-like model for investigating particle, antigen and microorganism translocation. Nat Protoc 2017; 12(7): 1387-99.
[http://dx.doi.org/10.1038/nprot.2017.041] [PMID: 28617450]
[43]
Kanaya T, Ohno H. The mechanisms of M-cell differentiation. Biosci Microbiota Food Health 2014; 33(3): 91-7.
[http://dx.doi.org/10.12938/bmfh.33.91] [PMID: 25032083]
[44]
Yuasa H, Mantani Y, Masuda N, et al. Mechanism of M-cell differentiation accelerated by proliferation of indigenous bacteria in rat Peyer’s patches. J Vet Med Sci 2017; 79(11): 1826-35.
[http://dx.doi.org/10.1292/jvms.17-0470] [PMID: 28993550]
[45]
Khan IU, Huang J, Li X, Xie J, Zhu N. Nasal immunization with RSV F and G protein fragments conjugated to an M cell-targeting ligand induces an enhanced immune response and protection against RSV infection. Antiviral Res 2018; 159: 95-103.
[http://dx.doi.org/10.1016/j.antiviral.2018.10.001] [PMID: 30290196]
[46]
Cabellos J, Delpivo C, Fernández-Rosas E, et al. Contribution of M-cells and other experimental variables in the translocation of TiO2 nanoparticles across in vitro intestinal models. NanoImpact 2017; 5: 51-60.
[http://dx.doi.org/10.1016/j.impact.2016.12.005]
[47]
Blaschitz C, Raffatellu M. Th17 cytokines and the gut mucosal barrier. J Clin Immunol 2010; 30(2): 196-203.
[http://dx.doi.org/10.1007/s10875-010-9368-7] [PMID: 20127275]
[48]
Sheridan BS, Lefrançois L. Regional and mucosal memory T cells. Nat Immunol 2011; 12(6): 485-91.
[http://dx.doi.org/10.1038/ni.2029] [PMID: 21739671]
[49]
Borges O, Lebre F, Bento D, Borchard G, Junginger HE. Mucosal vaccines: recent progress in understanding the natural barriers. Pharm Res 2010; 27(2): 211-23.
[http://dx.doi.org/10.1007/s11095-009-0011-3] [PMID: 19953309]
[50]
Chionh YT, Wee JL, Every AL, Ng GZ, Sutton P. M-cell targeting of whole killed bacteria induces protective immunity against gastrointestinal pathogens. Infect Immun 2009; 77(7): 2962-70.
[http://dx.doi.org/10.1128/IAI.01522-08] [PMID: 19380476]
[51]
Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004; 21(4): 527-38.
[http://dx.doi.org/10.1016/j.immuni.2004.08.011] [PMID: 15485630]
[52]
Pavot V, Rochereau N, Genin C, Verrier B, Paul S. New insights in mucosal vaccine development. Vaccine 2012; 30(2): 142-54.
[http://dx.doi.org/10.1016/j.vaccine.2011.11.003] [PMID: 22085556]
[53]
Mestecky J, Nguyen H, Czerkinsky C, Kiyono H. Oral immunization: an update. Curr Opin Gastroenterol 2008; 24(6): 713-9.
[http://dx.doi.org/10.1097/MOG.0b013e32830d58be] [PMID: 19122521]
[54]
Kim SH, Jung DI, Yang IY, et al. Application of an M-cell-targeting ligand for oral vaccination induces efficient systemic and mucosal immune responses against a viral antigen. Int Immunol 2013; 25(11): 623-32.
[http://dx.doi.org/10.1093/intimm/dxt029] [PMID: 23900425]
[55]
Kim SH, Seo KW, Kim J, Lee KY, Jang YS. The M cell-targeting ligand promotes antigen delivery and induces antigen-specific immune responses in mucosal vaccination. J Immunol 2010; 185(10): 5787-95.
[http://dx.doi.org/10.4049/jimmunol.0903184] [PMID: 20952686]
[56]
Shim G, Kim M-G, Jin H, Kim J, Oh Y-K. Claudin 4-targeted nanographene phototherapy using a Clostridium perfringens enterotoxin peptide-photosensitizer conjugate. Acta Pharmacol Sin 2017; 38(6): 954-62.
[http://dx.doi.org/10.1038/aps.2017.46] [PMID: 28552914]
[57]
Beugeling M, De Zee J, Woerdenbag HJ, Frijlink HW, Wilschut JC, Hinrichs WLJ. Respiratory syncytial virus subunit vaccines based on the viral envelope glycoproteins intended for pregnant women and the elderly. Expert Rev Vaccines 2019; 18(9): 935-50.
[http://dx.doi.org/10.1080/14760584.2019.1657013] [PMID: 31446807]
[58]
Kobayashi N, Takahashi D, Takano S, Kimura S, Hase K. The Roles of Peyer’s Patches and Microfold Cells in the Gut Immune System: Relevance to Autoimmune Diseases. Front Immunol 2019; 10: 2345.
[http://dx.doi.org/10.3389/fimmu.2019.02345] [PMID: 31649668]
[59]
Jass JR, Allison LJ, Stewart SM, Lane MR. Ulex europaeus agglutinin-1 binding in hereditary bowel cancer. Pathology 1993; 25(2): 114-9.
[http://dx.doi.org/10.3109/00313029309084782] [PMID: 8396230]
[60]
Nochi T, Yuki Y, Matsumura A, et al. A novel M cell-specific carbohydrate-targeted mucosal vaccine effectively induces antigen-specific immune responses. J Exp Med 2007; 204(12): 2789-96.
[http://dx.doi.org/10.1084/jem.20070607] [PMID: 17984304]
[61]
Wolf JL, Kauffman RS, Finberg R, Dambrauskas R, Fields BN, Trier JS. Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology 1983; 85(2): 291-300.
[http://dx.doi.org/10.1016/0016-5085(83)90313-X] [PMID: 6305756]
[62]
Wang M, Gao Z, Zhang Z, Pan L, Zhang Y. Roles of M cells in infection and mucosal vaccines. Hum Vaccin Immunother 2014; 10(12): 3544-51.
[http://dx.doi.org/10.4161/hv.36174] [PMID: 25483705]
[63]
Hase K, Kawano K, Nochi T, et al. Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 2009; 462(7270): 226-30.
[http://dx.doi.org/10.1038/nature08529] [PMID: 19907495]
[64]
Rand JH, Wu XX, Lin EY, Griffel A, Gialanella P, McKitrick JC. Annexin A5 binds to lipopolysaccharide and reduces its endotoxin activity. MBio 2012; 3(2): 292-311.
[http://dx.doi.org/10.1128/mBio.00292-11] [PMID: 22415004]
[65]
Molteni M, Gemma S, Rossetti C. The Role of Toll-Like Receptor 4 in Infectious and Noninfectious Inflammation. : Gómez , MI 2016.
[http://dx.doi.org/10.1155/2016/6978936]
[66]
Clark MA, Hirst BH, Jepson MA. M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer’s patch M cells. Infect Immun 1998; 66(3): 1237-43.
[http://dx.doi.org/10.1128/IAI.66.3.1237-1243.1998] [PMID: 9488419]
[67]
De Marzi MC, Todone M, Ganem MB, et al. Peptidoglycan recognition protein-peptidoglycan complexes increase monocyte/macrophage activation and enhance the inflammatory response. Immunology 2015; 145(3): 429-42.
[http://dx.doi.org/10.1111/imm.12460] [PMID: 25752767]
[68]
Nakato G, Hase K, Suzuki M, et al. Cutting Edge: Brucella abortus exploits a cellular prion protein on intestinal M cells as an invasive receptor. J Immunol 2012; 189(4): 1540-4.
[http://dx.doi.org/10.4049/jimmunol.1103332] [PMID: 22772447]
[69]
Giannasca PJ, Giannasca KT, Leichtner AM, Neutra MR. Human intestinal M cells display the sialyl Lewis A antigen. Infect Immun 1999; 67(2): 946-53.
[http://dx.doi.org/10.1128/IAI.67.2.946-953.1999] [PMID: 9916113]
[70]
Liu L, Zhang W, Song Y, et al. Recombinant Lactococcus lactis co-expressing OmpH of an M cell-targeting ligand and IBDV-VP2 protein provide immunological protection in chickens. Vaccine 2018; 36(5): 729-35.
[http://dx.doi.org/10.1016/j.vaccine.2017.12.027] [PMID: 29289381]
[71]
Fievez V, Plapied L, des Rieux A, et al. Targeting nanoparticles to M cells with non-peptidic ligands for oral vaccination. Eur J Pharm Biopharm 2009; 73(1): 16-24.
[http://dx.doi.org/10.1016/j.ejpb.2009.04.009] [PMID: 19409989]
[72]
Kim SH, Yang IY, Jang SH, et al. C5a receptor-targeting ligand-mediated delivery of dengue virus antigen to M cells evokes antigen-specific systemic and mucosal immune responses in oral immunization. Microbes Infect 2013; 15(13): 895-902.
[http://dx.doi.org/10.1016/j.micinf.2013.07.006] [PMID: 23892099]
[73]
Park J, Seo KW, Kim SH, et al. Nasal immunization with M cell-targeting ligand-conjugated ApxIIA toxin fragment induces protective immunity against Actinobacillus pleuropneumoniae infection in a murine model. Vet Microbiol 2015; 177(1-2): 142-53.
[http://dx.doi.org/10.1016/j.vetmic.2015.03.005] [PMID: 25818577]
[74]
Fievez V, Plapied L, Plaideau C, et al. In vitro identification of targeting ligands of human M cells by phage display. Int J Pharm 2010; 394(1-2): 35-42.
[http://dx.doi.org/10.1016/j.ijpharm.2010.04.023] [PMID: 20417702]
[75]
Yoshimoto J, Okada S, Kishi M, Misaka T. Ulex Europaeus Agglutinin-1 is a reliable taste bud marker for in situ hybridization analyses. J Histochem Cytochem 2016; 64(3): 205-15.
[http://dx.doi.org/10.1369/0022155415626987] [PMID: 26718243]
[76]
Foster N, Clark MA, Jepson MA, Hirst BH. Ulex europaeus 1 lectin targets microspheres to mouse Peyer’s patch M-cells in vivo. Vaccine 1998; 16(5): 536-41.
[http://dx.doi.org/10.1016/S0264-410X(97)00222-3] [PMID: 9491509]
[77]
Wang XN, Wang L, Zheng DZ, et al. Oral immunization with a Lactobacillus casei-based anti-porcine epidemic diarrhoea virus (PEDV) vaccine expressing microfold cell-targeting peptide Co1 fused with the COE antigen of PEDV. J Appl Microbiol 2018; 124(2): 368-78.
[http://dx.doi.org/10.1111/jam.13652] [PMID: 29178509]
[78]
Kim SH, Kim YN, Kim J, Jang YS. C5a receptor targeting of partial non-structural protein 3 of dengue virus promotes antigen-specific IFN-γ-producing T-cell responses in a mucosal dengue vaccine model. Cell Immunol 2018; 325: 41-7.
[http://dx.doi.org/10.1016/j.cellimm.2018.01.016] [PMID: 29397905]
[79]
Huy NX, Kim SH, Yang MS, Kim TG. Immunogenicity of a neutralizing epitope from porcine epidemic diarrhea virus: M cell targeting ligand fusion protein expressed in transgenic rice calli. Plant Cell Rep 2012; 31(10): 1933-42.
[http://dx.doi.org/10.1007/s00299-012-1306-0] [PMID: 22736145]
[80]
Ma S, Wang L, Huang X, et al. Oral recombinant Lactobacillus vaccine targeting the intestinal microfold cells and dendritic cells for delivering the core neutralizing epitope of porcine epidemic diarrhea virus. Microb Cell Fact 2018; 17(1): 20.
[http://dx.doi.org/10.1186/s12934-018-0861-7] [PMID: 29426335]
[81]
Bal J, Jung HY, Nguyen LN, Park J, Jang YS, Kim DH. Evaluation of cell-surface displayed synthetic consensus dengue EDIII cells as a potent oral vaccine candidate. Microb Cell Fact 2018; 17(1): 146.
[http://dx.doi.org/10.1186/s12934-018-0994-8] [PMID: 30217208]
[82]
Nguyen NL, So KK, Kim JM, et al. Expression and characterization of an M cell-specific ligand-fused dengue virus tetravalent epitope using Saccharomyces cerevisiae. J Biosci Bioeng 2015; 119(1): 19-27.
[http://dx.doi.org/10.1016/j.jbiosc.2014.06.005] [PMID: 25027708]
[83]
Davitt CJ, Lavelle EC. Delivery strategies to enhance oral vaccination against enteric infections. Adv Drug Deliv Rev 2015; 91: 52-69.
[http://dx.doi.org/10.1016/j.addr.2015.03.007] [PMID: 25817337]
[84]
Holmgren J. Mucosal immunity and vaccination. FEMS Microbiol Immunol 1991; 4(1): 1-9.
[PMID: 1815705]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 12
Year: 2020
Published on: 09 June, 2020
Page: [1276 - 1284]
Pages: 9
DOI: 10.2174/1389450121666200609113252
Price: $65

Article Metrics

PDF: 28
HTML: 4