Transepithelial antigen delivery in the small intestine: Different paths, different outcomes

Current Opinion in Gastroenterology

Volumn 29, Issue 2, 2013, Pages 112-118

  Knoop, Kathryn A ^a   Miller, Mark J ^a   Newberry, Rodney D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

antigen; dendritic cells; epithelium

Indexed keywords

ANTIGEN; IMMUNOGLOBULIN A; OSTEOCLAST DIFFERENTIATION FACTOR;

ANTIGEN FUNCTION; BINDING AFFINITY; CELLULAR IMMUNITY; DENDRITIC CELL; ENDOCYTOSIS; ENTEROBACTER CLOACAE; GOBLET CELL; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INTESTINE MUCOSA PERMEABILITY; LAMINA PROPRIA; LYMPH VESSEL; MESENTERY LYMPH NODE; NONHUMAN; PEYER PATCH; REVIEW; SMALL INTESTINE MUCOSA; STEADY STATE; TRANSCYTOSIS;

ANTIGEN PRESENTATION; ANTIGENS; DENDRITIC CELLS; GOBLET CELLS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; INTESTINAL MUCOSA; INTESTINE, SMALL;

EID: 84873333650     PISSN: 02671379     EISSN: 15317056     Source Type: Journal    
DOI: 10.1097/MOG.0b013e32835cf1cd     Document Type: Review

References (53)

1. Bockman DE, Cooper MD. Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer's patches. An electron microscopic study. Am J Anat 1973; 136:455-477.
2. Jang MH, Kweon MN, Iwatani K, et al. Intestinal villousMcells: An antigen entry site in the mucosal epithelium. Proc Natl Acad Sci USA 2004; 101:6110-6115.
3. Tyrer PC, Ruth Foxwell A, Kyd JM, et al. Receptor mediated targeting of M-cells. Vaccine 2007; 25:3204-3209.
4. Hase K, Kawano K, Nochi T, et al. Uptake through glycoprotein 2 of FimH bacteria by M cells initiates mucosal immune response. Nature 2009; 462:226-230.
5. Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M cells: Gateways for mucosal infection and immunization. Cell 1996; 86:345-348.
6. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol 2008; 1:11-22.
7. Lorenz RG, Newberry RD. Isolated lymphoid follicles can function as sites for induction of mucosal immune responses. Ann N Y Acad Sci 2004; 1029: 44-57.
8. Mora JR, Iwata M, Eksteen B, et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006; 314:1157-1160.
9. Tsuji M, Suzuki K, Kitamura H, et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 2008; 29:261-271.
10. Lorenz RG, Chaplin DD, McDonald KG, et al. Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin-sufficient B lymphocytes, lymphotoxin beta receptor, and TNF receptor I function. J Immunol 2003; 170:5475-5482.
11. Newberry RD, McDonough JS, McDonald KG, Lorenz RG. Postgestational lymphotoxin/lymphotoxin beta receptor interactions are essential for the presence of intestinal B lymphocytes. J Immunol 2002; 168:4988-4997.
12. Sansonetti PJ, Phalipon A. M cells as ports of entry for enteroinvasive pathogens: mechanisms of interaction, consequences for the disease process. Semin Immunol 1999; 11:193-203.
13. Hutchings AB, Helander A, Silvey KJ, et al. Secretory immunoglobulin A antibodies against the s1 outer capsid protein of reovirus type 1 Lang prevent infection of mouse Peyer's patches. J Virol 2004; 78:947-957.
14. Martinoli C, Chiavelli A, Rescigno M. Entry route of Salmonella typhimurium directs the type of induced immune response. Immunity 2007; 27:975-984.
15. Kraehenbuhl JP, Neutra MR. Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 2000; 16:301-332.
16. Mach J, Hshieh T, Hsieh D, et al. Development of intestinal M cells. Immunol Rev 2005; 206:177-189.
17. Kanaya T, Hase K, Takahashi D, et al. The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells. Nat Immunol 2012; 13:729-736.
18. de Lau W, Kujala P, Schneeberger K, et al. Peyer's Patch M cells derive from Lgr5 stem cells require SpiB and are induced by RankL in cultured 'organoids'. Mol Cell Biol 2012; 32:3639-3647.
19. Knoop KA, Kumar N, Butler BR, et al. RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J Immunol 2009; 183:5738-5747.
20. Taylor RT, Patel SR, Lin E, et al. Lymphotoxin-independent expression of TNFrelated activation-induced cytokine by stromal cells in cryptopatches, isolated lymphoid follicles, and Peyer's patches. J Immunol 2007; 178:5659-5667.
21. Jepson MA, Clark MA, Foster N, et al. Targeting to intestinal M cells. J Anat 1996; 189:507-516.
22. Brayden DJ, Baird AW. Apical membrane receptors on intestinal M cells: potential targets for vaccine delivery. Adv Drug Deliv Rev 2004; 56:721-726.
23. Azizi A, Kumar A, Diaz-Mitoma F, Mestecky J. Enhancing oral vaccine potency by targeting intestinal M Cells. PLoS Pathog 2010; 6:e1001147.
24. Nochi T, Yuki Y, Matsumura A, et al. A novel M cell-specific carbohydratetargeted mucosal vaccine effectively induces antigen-specific immune responses. J Exp Med 2007; 204:2789-2796.
25. Chionh Y-T, Wee JLK, Every AL, et al. M-cell targeting of whole killed bacteria induces protective immunity against gastrointestinal pathogens. Infect Immun 2009; 77:2962-2970.
26. Rey J, Garin N, Spertini F, Corthé sy B. Targeting of secretory IgA to Peyer's patch dendritic and T cells after transport by intestinal M cells. J Immunol 2004; 172:3026-3033.
27. Rol N, Favre L, Benyacoub J, Corthé sy B. The role of secretory immunoglobulin A in the natural sensing of commensal bacteria by mouse Peyer's patch dendritic cells. J Biol Chem 2012; 287:40074-40082.
28. Man AL, Prieto-Garcia ME, Nicoletti C. Improving M cell mediated transport across mucosal barriers: do certain bacteria hold the keys? Immunology 2004; 113:15-22.
29. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004; 303:1662-1665.
30. McDole JR, Wheeler LW, McDonald KG, et al. Goblet cells deliver luminal antigen to CD103dendritic cells in the small intestine. Nature 2012; 483: 345-349.
31. Strobel S, Mowat AM. Immune responses to dietary antigens: Oral tolerance. Immunol Today 1998; 19:173-181.
32. Schulz O, Jaensson E, Persson EK, et al. Intestinal CD103 but not CX3CR1, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 2009; 206:3101-3114.
33. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, et al. A functionally specialized population of mucosal CD103 DCs induces Foxp3 regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007; 204:1757-1764.
34. Sun C-M, Hall JA, Blank RB, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 2007; 204:1775-1785.
35. Iwata M, Hirakiyama A, Eshima Y, et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004; 21:527-538.
36. Annacker O, Coombes JL, Malmstrom V, et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med 2005; 202:1051-1061.
37. Jaensson E, Uronen-Hansson H, Pabst O, et al. Small intestinal CD103 dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med 2008; 205:2139-2149.
38. Harshyne LA, Watkins SC, Gambotto A, Barratt-Boyes SM. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J Immunol 2001; 166:3717-3723.
39. Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001; 2:361-367.
40. Chieppa M, Rescigno M, Huang AY, Germain RN. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med 2006; 203:2841-2852.
41. Niess JH, Brand S, Gu X, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005; 307:254-258.
42. Lelouard H, Fallet M, de Bovis B, et al. Peyer's patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology 2012; 142:592-601.; e593.
43. Vallon-Eberhard A, Landsman L, Yogev N, et al. Transepithelial pathogen uptake into the small intestinal lamina propria. J Immunol 2006; 176:2465-2469.
44. Denning TL, Wang YC, Patel SR, et al. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 2007; 8:1086-1094.
45. Niess JH, Adler G. Enteric flora expands gut lamina propria CX3CR1 dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J Immuno 2010; 184:2026-2037.
46. Nicoletti C, Arques JL, Bertelli E. CX3CR1 is critical for Salmonella-induced migration of dendritic cells into the intestinal lumen. Gut Microbes 2010; 1:131-134.
47. Machen TE, Erlij D, Wooding FBP. Permeable junctional complexes. J Cell Biol 1972; 54:302-312.
48. Shen L, Weber CR, Raleigh DR, et al. Tight junction pore and leak pathways: A dynamic duo. Annu Rev Physiol 2011; 73:283-309.
49. Diamond JM. The epithelial junction: Bridge, gate, and fence. Physiologist 1977; 20:10-18.
50. Turner Jr. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9:799-809.
51. Su L, Shen L, Clayburgh DR, et al. Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 2009; 136:551-563.
52. Arrieta MC, Madsen K, Doyle J, Meddings J. Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse. Gut 2009; 58:41-48.
53. Miller MJ, McDole JR, Newberry RD. Microanatomy of the intestinal lymphatic system. Ann N Y Acad Sci 2010; 1207:E21-E28.