靶向M细胞的抗原递送——增强黏膜免疫应答的关键策略
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摘要
黏膜是阻止病原入侵的第一道防线,黏膜免疫系统在抵抗感染方面起着至关重要的作用。通过黏膜途径接种疫苗可以同时诱导黏膜和全身免疫反应,因此,理论上针对黏膜的免疫策略是最合理和有效的。但黏膜免疫系统的复杂性和屏障作用造成抗原诱导的免疫应答水平低下,制约了黏膜疫苗的发展。M细胞(Microfoldcells)是黏膜免疫系统所独有的,其具有捕获腔内抗原和启动抗原特异性免疫应答的功能。M细胞摄取抗原的多少直接关系到黏膜疫苗的免疫效力,而利用M细胞配体可将抗原靶向递呈给M细胞,从而实现高效的黏膜免疫应答。靶向M细胞的抗原递送策略及其应用可以提高黏膜免疫应答水平,促进黏膜疫苗的研制。尽管如此,要成功研制安全高效的黏膜疫苗,今后依然有漫长的路要走,这可能有赖于进一步探究M细胞的特性和功能及黏膜免疫机制。
The mucosae represent the first line of defense against the invasion of most pathogens, and the mucosal immune system plays a crucial role in the control of infection. Mucosal vaccination can trigger both humoral and cell-mediated immune responses mucosally as well as systemically. Hence, protective immune responses can be elicited effectively by mucosal vaccination. Microfold(M) cells being unique to the mucosal immune system can take up luminal antigens and initiating antigen-specific immune responses. The number of antigen uptake by M cells is directly related to the immune efficacy of mucosal vaccines. Utilizing M cell ligands, M cells-targeting antigen delivery can achieve highly effective mucosal immune responses. The strategy of targeted delivery of antigens to M cells and its applications can be used for the improvement of mucosal immune responses and the development of mucosal vaccines. Despite these efforts, successful development of safe and effective mucosal vaccines remains a big challenge and needs a long way to go, and provably still resort to further researches on cellular properties and functions as well as mucosal immune mechanisms.
The mucosae represent the first line of defense against the invasion of most pathogens, and the mucosal immune system plays a crucial role in the control of infection. Mucosal vaccination can trigger both humoral and cell-mediated immune responses mucosally as well as systemically. Hence, protective immune responses can be elicited effectively by mucosal vaccination. Microfold(M) cells being unique to the mucosal immune system can take up luminal antigens and initiating antigen-specific immune responses. The number of antigen uptake by M cells is directly related to the immune efficacy of mucosal vaccines. Utilizing M cell ligands, M cells-targeting antigen delivery can achieve highly effective mucosal immune responses. The strategy of targeted delivery of antigens to M cells and its applications can be used for the improvement of mucosal immune responses and the development of mucosal vaccines. Despite these efforts, successful development of safe and effective mucosal vaccines remains a big challenge and needs a long way to go, and provably still resort to further researches on cellular properties and functions as well as mucosal immune mechanisms.
引文
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[3]Kim SH,Jang YS.The development of mucosal vaccines for both mucosal and systemic immune induction and the roles played by adjuvants.Clin Exp Vaccine Res,2017,6(1):15-21.
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[8]Pabst R,Russell MW,Brandtzaeg P.Tissue distribution of lymphocytes and plasma cells and the role of the gut.Trends Immunol,2008,29(5):206-208.
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[29]Kim SH,Jung DI,Yang IY,et al.M cells expressing the complement C5a receptor are efficient targets for mucosal vaccine delivery.Eur J Immunol,2011,41(11):3219-3229.
[30]Garinot M,Fiévez V,Pourcelle V,et al.PEGylated PLGA-based nanoparticles targeting M cells for oral vaccination.J Control Release,2007,120(3):195-204.
[31]Yoo MK,Kang SK,Choi JH,et al.Targeted delivery of chitosan nanoparticles to Peyer’s patch using Mcell-homing peptide selected by phage display technique.Biomaterials,2010,31(30):7738-7747.
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[34]Du LP,Yu ZY,Pang FJ,et al.Targeted delivery of GP5 antigen of PRRSV to M Cells enhances the antigen-specific systemic and mucosal immune responses.Front Cell Infect Microbiol,2018,8:7.
[35]Kim SH,Seo KW,Kim J,et al.The M cell-targeting ligand promotes antigen delivery and induces antigen-specific immune responses in mucosal vaccination.J Immunol,2010,185(10):5787-5795.
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[38]Sato S,Kaneto S,Shibata N,et al.Transcription factor Spi-B-dependent and-independent pathways for the development of Peyer’s patch M cells.Mucosal Immunol,2013,6(4):838-846.
[39]Fukuda S,Hase K,Ohno H.Application of a mouse ligated Peyer’s patch intestinal loop assay to evaluate bacterial uptake by M cells.J Vis Exp,2011,(58):3225.
[40]Rynda A,Maddaloni M,Mierzejewska D,et al.Low-dose tolerance is mediated by the microfold cell ligand,reovirus proteinσ1.J Immunol,2008,180(8):5187-5200.
[41]Helander A,Silvey KJ,Mantis NJ,et al.The viralσ1 protein and glycoconjugates containingα2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces.J Virol,2003,77(14):7964-7977.
[42]Keely S,Glover LE,Weissmueller T,et al.Hypoxia-inducible factor-dependent regulation of platelet-activating factor receptor as a route for gram-positive bacterial translocation across epithelia.Mol Biol Cell,2010,21(4):538-546.
[43]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.
[44]Lo DD,Ling J,Eckelhoefer AH.M cell targeting by a Claudin 4 targeting peptide can enhance mucosal IgA responses.BMC Biotechnol,2012,12:7.
[45]Suzuki H,Nagatake T,Nasu A,et al.Impaired airway mucociliary function reduces antigen-specific IgA immune response to immunization with a claudin-4-targeting nasal vaccine in mice.Sci Rep,2018,8:2904.
[46]Suzuki H,Watari A,Hashimoto E,et al.C-terminal Clostridium perfringens enterotoxin-mediated antigen delivery for nasal pneumococcal vaccine.PLoS ONE,2015,10(5):e0126352.
[47]Shima H,Watanabe T,Fukuda S,et al.A novel mucosal vaccine targeting Peyer’s patch M cells induces protective antigen-specific IgA responses.Int Immunol,2014,26(11):619-625.
[48]Rochereau N,Pavot V,Verrier B,et al.Secretory IgAas a vaccine carrier for delivery of HIV antigen to Mcells.Eur J Immunol,2015,45(3):773-779.
[49]Mikulic J,Bioley G,Corthésy B.SIgA-Shigella immune complexes interact with dectin-1 and SIGNR3 to differentially regulate mouse Peyer’s patch and mesenteric lymph node dendritic cell’s responsiveness.J Mol Biol,2017,429(15):2387-2400.
[50]Rochereau N,Drocourt D,Perouzel E,et al.Dectin-1is essential for reverse transcytosis of glycosylated SIgA-antigen complexes by intestinal M cells.PLoSBiol,2013,11(9):e1001658.
[51]Kuolee R,Chen WX.M cell-targeted delivery of vaccines and therapeutics.Expert Opin Drug Deliv,2008,5(6):693-702.
[52]Schimpel C,Teubl B,Absenger M,et al.Development of an advanced intestinal in vitro triple culture permeability model to study transport of nanoparticles.Mol Pharmaceutics,2014,11(3):808-818.
[53]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):623-632.
[54]Liu L,Zhang W,Song Y,et al.Recombinant Lactococcus lactis co-expressing OmpH of an Mcell-targeting ligand and IBDV-VP2 protein provide immunological protection in chickens.Vaccine,2018,36(5):729-735.
[55]Gupta PN,Khatri K,Goyal AK,et al.M-cell targeted biodegradable PLGA nanoparticles for oral immunization against hepatitis B.J Drug Target,2007,15(10):701-713.
[56]Daifalla N,Cayabyab MJ,Xie E,et al.Commensal Streptococcus mitis is a unique vector for oral mucosal vaccination.Microbes Infect,2015,17(3):237-242.
[57]Lycke N.Recent progress in mucosal vaccine development:potential and limitations.Nat Rev Immunol,2012,12(8):592-605.
[58]Davitt CJH,Lavelle EC.Delivery strategies to enhance oral vaccination against enteric infections.Adv Drug Deliv Rev,2015,91:52-69.
[59]Gullberg E,Keita ?V,Salim SY,et al.Identification of cell adhesion molecules in the human follicle-associated epithelium that improve nanoparticle uptake into the Peyer’s patches.JPharmacol Exp Ther,2006,319(2):632-639.
[60]Tyrer PC,Ruth Foxwell A,Kyd JM,et al.Receptor mediated targeting of M-cells.Vaccine,2007,25(16):3204-3209.
[61]Ashour HM.Immune tolerance elicited via unique ocular and oral routes.Curr Mol Med,2015,15(1):78-81.
[62]Liu XH,Wu HZ,Chang XY,et al.Notable mucosal immune responses induced in the intestine of zebrafish(Danio rerio)bath-vaccinated with a live attenuated Vibrio anguillarum vaccine.Fish Shellfish Immunol,2014,40(1):99-108.
[63]Canadian Paediatric Society,Infectious Diseases and Immunization Committee.FluMist vaccine:questions and answers-summary.Paediatr Child Health,2011,16(1):31.
[64]Li QH,Jin G,Wang JY,et al.Live attenuated Salmonella displaying HIV-1 10E8 epitope on fimbriae:systemic and mucosal immune responses in BALB/c mice by mucosal administration.Sci Rep,2016,6:29556.
[65]Ma ST,Wang L,Huang XW,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,2018,17:20.
[66]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):368-378.
[2]Payne AM.Oral immunization against poliomyelitis.Bull World Health Organ,1960,23(6):695-703.
[3]Kim SH,Jang YS.The development of mucosal vaccines for both mucosal and systemic immune induction and the roles played by adjuvants.Clin Exp Vaccine Res,2017,6(1):15-21.
[4]Longet S,Lundahl MLE,Lavelle EC.Targeted strategies for mucosal vaccination.Bioconjugate Chem,2018,29(3):613-623.
[5]Martens EC,Neumann M,Desai MS.Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier.Nat Rev Microbiol,2018,16:457-470.
[6]Azizi A,Kumar A,Diaz-Mitoma F,et al.Enhancing oral vaccine potency by targeting intestinal M cells.PLoS Pathog,2010,6(11):e1001147.
[7]Macpherson AJ,McCoy KD,Johansen FE,et al.The immune geography of IgA induction and function.Mucosal Immunol,2008,1(1):11-22.
[8]Pabst R,Russell MW,Brandtzaeg P.Tissue distribution of lymphocytes and plasma cells and the role of the gut.Trends Immunol,2008,29(5):206-208.
[9]Brandtzaeg P.Induction of secretory immunity and memory at mucosal surfaces.Vaccine,2007,25(30):5467-5484.
[10]Owen RL,Jones AL.Epithelial cell specialization within human Peyer’s patches:an ultrastructural study of intestinal lymphoid follicles.Gastroenterology,1974,66(2):189-203.
[11]Corr SC,Gahan CCGM,Hill C.M-cells:origin,morphology and role in mucosal immunity and microbial pathogenesis.FEMS Immunol Med Microbiol,2008,52(1):2-12.
[12]Mabbott NA,Donaldson DS,Ohno H,et al.Microfold(M)cells:important immunosurveillance posts in the intestinal epithelium.Mucosal Immunol,2013,6(4):666-677.
[13]Miller H,Zhang J,Kuolee R,et al.Intestinal M cells:the fallible sentinels?World J Gastroenterol,2007,13(10):1477-1486.
[14]Clark MA,Hirst BH.Expression of junction-associated proteins differentiates mouse intestinal M cells from enterocytes.Histochem Cell Biol,2002,118(2):137-147.
[15]Neutra MR,Mantis NJ,Kraehenbuhl JP.Collaboration of epithelial cells with organized mucosal lymphoid tissues.Nat Immunol,2001,2(11):1004-1009.
[16]Roy U,Ding H,Pilakka-Kanthikeel S,et al.Preparation and characterization of anti-HIVnanodrug targeted to microfold cell of gut-associated lymphoid tissue.Int J Nanomedicine,2015,10:5819-5835.
[17]Schulz O,Pabst O.Antigen sampling in the small intestine.Trends Immunol,2013,34(4):155-161.
[18]Kishikawa S,Sato S,Kaneto S,et al.Allograft inflammatory factor 1 is a regulator of transcytosis in M cells.Nat Commun,2017,8:14509.
[19]Anosova NG,Chabot S,Shreedhar V,et al.Cholera toxin,E.coli heat-labile toxin,and non-toxic derivatives induce dendritic cell migration into the follicle-associated epithelium of Peyer’s patches.Mucosal Immunol,2008,1(1):59-67.
[20]Chabot S,Wagner JS,Farrant S,et al.TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium.J Immunol,2006,176(7):4275-4283.
[21]Man AL,Lodi F,Bertelli E,et al.Macrophage migration inhibitory factor plays a role in the regulation of microfold(M)cell-mediated transport in the gut.J Immunol,2008,181(8):5673-5680.
[22]Mantis NJ,Rol N,Corthésy B.Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut.Mucosal Immunol,2011,4(6):603-611.
[23]Kadaoui KA,Corthésy B.Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer’s patches with restriction to mucosal compartment.J Immunol,2007,179(11):7751-7757.
[24]Gicheva N,Macauley MS,Arlian BM,et al.Siglec-Fis a novel intestinal M cell marker.Biochem Biophys Res Commun,2016,479(1):1-4.
[25]Zhao JY,Li XY,Luo QF,et al.Screening of surface markers on rat intestinal mucosa microfold cells by using laser capture microdissection combined with protein chip technology.Int J Clin Exp Med,2014,7(4):932-939.
[26]Bies C,Lehr CM,Woodley JF.Lectin-mediated drug targeting:history and applications.Adv Drug Deliv Rev,2004,56(4):425-435.
[27]Ramirez JEV,Sharpe LA,Peppas NA.Current state and challenges in developing oral vaccines.Adv Drug Deliv Rev,2017,114:116-131.
[28]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):226-230.
[29]Kim SH,Jung DI,Yang IY,et al.M cells expressing the complement C5a receptor are efficient targets for mucosal vaccine delivery.Eur J Immunol,2011,41(11):3219-3229.
[30]Garinot M,Fiévez V,Pourcelle V,et al.PEGylated PLGA-based nanoparticles targeting M cells for oral vaccination.J Control Release,2007,120(3):195-204.
[31]Yoo MK,Kang SK,Choi JH,et al.Targeted delivery of chitosan nanoparticles to Peyer’s patch using Mcell-homing peptide selected by phage display technique.Biomaterials,2010,31(30):7738-7747.
[32]Singh B,Maharjan S,Jiang T,et al.Combinatorial approach of antigen delivery using M cell-homing peptide and mucoadhesive vehicle to enhance the efficacy of oral vaccine.Mol Pharm,2015,12(11):3816-3828.
[33]Misstear K,McNeela EA,Murphy AG,et al.Targeted nasal vaccination provides antibody-independent protection against Staphylococcus aureus.J Infect Dis,2014,209(9):1479-1484.
[34]Du LP,Yu ZY,Pang FJ,et al.Targeted delivery of GP5 antigen of PRRSV to M Cells enhances the antigen-specific systemic and mucosal immune responses.Front Cell Infect Microbiol,2018,8:7.
[35]Kim SH,Seo KW,Kim J,et al.The M cell-targeting ligand promotes antigen delivery and induces antigen-specific immune responses in mucosal vaccination.J Immunol,2010,185(10):5787-5795.
[36]Kim SH,Kim YN,Kim J,et al.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,2018,325:41-47.
[37]Nochi T,Yuki Y,Matsumura A,et al.A novel Mcell-specific carbohydrate-targeted mucosal vaccine effectively induces antigen-specific immune responses.J Exp Med,2007,204(12):2789-2796.
[38]Sato S,Kaneto S,Shibata N,et al.Transcription factor Spi-B-dependent and-independent pathways for the development of Peyer’s patch M cells.Mucosal Immunol,2013,6(4):838-846.
[39]Fukuda S,Hase K,Ohno H.Application of a mouse ligated Peyer’s patch intestinal loop assay to evaluate bacterial uptake by M cells.J Vis Exp,2011,(58):3225.
[40]Rynda A,Maddaloni M,Mierzejewska D,et al.Low-dose tolerance is mediated by the microfold cell ligand,reovirus proteinσ1.J Immunol,2008,180(8):5187-5200.
[41]Helander A,Silvey KJ,Mantis NJ,et al.The viralσ1 protein and glycoconjugates containingα2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces.J Virol,2003,77(14):7964-7977.
[42]Keely S,Glover LE,Weissmueller T,et al.Hypoxia-inducible factor-dependent regulation of platelet-activating factor receptor as a route for gram-positive bacterial translocation across epithelia.Mol Biol Cell,2010,21(4):538-546.
[43]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.
[44]Lo DD,Ling J,Eckelhoefer AH.M cell targeting by a Claudin 4 targeting peptide can enhance mucosal IgA responses.BMC Biotechnol,2012,12:7.
[45]Suzuki H,Nagatake T,Nasu A,et al.Impaired airway mucociliary function reduces antigen-specific IgA immune response to immunization with a claudin-4-targeting nasal vaccine in mice.Sci Rep,2018,8:2904.
[46]Suzuki H,Watari A,Hashimoto E,et al.C-terminal Clostridium perfringens enterotoxin-mediated antigen delivery for nasal pneumococcal vaccine.PLoS ONE,2015,10(5):e0126352.
[47]Shima H,Watanabe T,Fukuda S,et al.A novel mucosal vaccine targeting Peyer’s patch M cells induces protective antigen-specific IgA responses.Int Immunol,2014,26(11):619-625.
[48]Rochereau N,Pavot V,Verrier B,et al.Secretory IgAas a vaccine carrier for delivery of HIV antigen to Mcells.Eur J Immunol,2015,45(3):773-779.
[49]Mikulic J,Bioley G,Corthésy B.SIgA-Shigella immune complexes interact with dectin-1 and SIGNR3 to differentially regulate mouse Peyer’s patch and mesenteric lymph node dendritic cell’s responsiveness.J Mol Biol,2017,429(15):2387-2400.
[50]Rochereau N,Drocourt D,Perouzel E,et al.Dectin-1is essential for reverse transcytosis of glycosylated SIgA-antigen complexes by intestinal M cells.PLoSBiol,2013,11(9):e1001658.
[51]Kuolee R,Chen WX.M cell-targeted delivery of vaccines and therapeutics.Expert Opin Drug Deliv,2008,5(6):693-702.
[52]Schimpel C,Teubl B,Absenger M,et al.Development of an advanced intestinal in vitro triple culture permeability model to study transport of nanoparticles.Mol Pharmaceutics,2014,11(3):808-818.
[53]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):623-632.
[54]Liu L,Zhang W,Song Y,et al.Recombinant Lactococcus lactis co-expressing OmpH of an Mcell-targeting ligand and IBDV-VP2 protein provide immunological protection in chickens.Vaccine,2018,36(5):729-735.
[55]Gupta PN,Khatri K,Goyal AK,et al.M-cell targeted biodegradable PLGA nanoparticles for oral immunization against hepatitis B.J Drug Target,2007,15(10):701-713.
[56]Daifalla N,Cayabyab MJ,Xie E,et al.Commensal Streptococcus mitis is a unique vector for oral mucosal vaccination.Microbes Infect,2015,17(3):237-242.
[57]Lycke N.Recent progress in mucosal vaccine development:potential and limitations.Nat Rev Immunol,2012,12(8):592-605.
[58]Davitt CJH,Lavelle EC.Delivery strategies to enhance oral vaccination against enteric infections.Adv Drug Deliv Rev,2015,91:52-69.
[59]Gullberg E,Keita ?V,Salim SY,et al.Identification of cell adhesion molecules in the human follicle-associated epithelium that improve nanoparticle uptake into the Peyer’s patches.JPharmacol Exp Ther,2006,319(2):632-639.
[60]Tyrer PC,Ruth Foxwell A,Kyd JM,et al.Receptor mediated targeting of M-cells.Vaccine,2007,25(16):3204-3209.
[61]Ashour HM.Immune tolerance elicited via unique ocular and oral routes.Curr Mol Med,2015,15(1):78-81.
[62]Liu XH,Wu HZ,Chang XY,et al.Notable mucosal immune responses induced in the intestine of zebrafish(Danio rerio)bath-vaccinated with a live attenuated Vibrio anguillarum vaccine.Fish Shellfish Immunol,2014,40(1):99-108.
[63]Canadian Paediatric Society,Infectious Diseases and Immunization Committee.FluMist vaccine:questions and answers-summary.Paediatr Child Health,2011,16(1):31.
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