Circulatory Antigen Processing by Mucosal Dendritic Cells Controls CD8+ T Cell Activation

Immunity

Volumn 38, Issue 1, 2013, Pages 153-165

  Chang, Sun Young ^a,e   Song, Joo Hye ^a   Guleng, Bayasi ^a   Cotoner, Carmen Alonso ^a   Arihiro, Seiji ^a   Zhao, Yun ^a   Chiang, Hao Sen ^a   O'Keeffe, Michael ^b   Liao, Gongxian ^b   Karp, Christopher L ^c   Kweon, Mi Na ^d   Sharpe, Arlene H ^b   Bhan, Atul ^a   Terhorst, Cox ^c   Reinecker, Hans Christian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d International Vaccine Institute   (South Korea)

^e Ajou University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR3; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 9;

ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; DENDRITIC CELL; ENTERITIS; IMMUNE RESPONSE; INTESTINE MUCOSA; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CROSS-PRIMING; DENDRITIC CELLS; ENTERITIS; EPITOPES, T-LYMPHOCYTE; INTESTINAL MUCOSA; INTESTINE, SMALL; LYMPHOCYTE ACTIVATION; MICE; RECEPTORS, CHEMOKINE;

EID: 84872788181     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.09.018     Document Type: Article

References (48)

1. Brimnes J., Allez M., Dotan I., Shao L., Nakazawa A., Mayer L. Defects in CD8+ regulatory T cells in the lamina propria of patients with inflammatory bowel disease. J. Immunol. 2005, 174:5814-5822.
2. Clementi F., Palade G.E. Intestinal capillaries. I. Permeability to peroxidase and ferritin. J. Cell Biol. 1969, 41:33-58.
3. Colony P.C., Neutra M.R. Macromolecular transport in the fetal rat intestine. Gastroenterology 1985, 89:294-306.
4. Coombes J.L., Maloy K.J. Control of intestinal homeostasis by regulatory T cells and dendritic cells. Semin. Immunol. 2007, 19:116-126.
5. Danese S. IBD: of mice and men-shedding new light on IL-13 activity in IBD. Nat. Rev. Gastroenterol. Hepatol. 2011, 8:128-129.
6. De Jong Y.P., Comiskey M., Kalled S.L., Mizoguchi E., Flavell R.A., Bhan A.K., Terhorst C. Chronic murine colitis is dependent on the CD154/CD40 pathway and can be attenuated by anti-CD154 administration. Gastroenterology 2000, 119:715-723.
7. Delamarre L., Pack M., Chang H., Mellman I., Trombetta E.S. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005, 307:1630-1634.
8. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 2007, 8:1086-1094.
9. DePaolo R.W., Abadie V., Tang F., Fehlner-Peach H., Hall J.A., Wang W., Marietta E.V., Kasarda D.D., Waldmann T.A., Murray J.A., et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature 2011, 471:220-224.
10. Dobbins W.O., Rollins E.L. Intestinal mucosal lymphatic permeability: an electron microscopic study of endothelial vesicles and cell junctions. J. Ultrastruct. Res. 1970, 33:29-59.
11. Faria A.M., Weiner H.L. Oral tolerance. Immunol. Rev. 2005, 206:232-259.
12. Grainger J.R., Hall J.A., Bouladoux N., Oldenhove G., Belkaid Y. Microbe-dendritic cell dialog controls regulatory T-cell fate. Immunol. Rev. 2010, 234:305-316.
13. Granger D.N., Taylor A.E. Permeability of intestinal capillaries to endogenous macromolecules. Am. J. Physiol. 1980, 238:H457-H464.
14. Granger D.N., Taylor A.E. Permselectivity of intestinal capillaries. Physiologist 1980, 23:47-52.
15. Hadis U., Wahl B., Schulz O., Hardtke-Wolenski M., Schippers A., Wagner N., Müller W., Sparwasser T., Förster R., Pabst O. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity 2011, 34:237-246.
16. Hashimoto D., Miller J., Merad M. Dendritic cell and macrophage heterogeneity in vivo. Immunity 2011, 35:323-335.
17. Heyman M., Ducroc R., Desjeux J.F., Morgat J.L. Horseradish peroxidase transport across adult rabbit jejunum in vitro. Am. J. Physiol. 1982, 242:G558-G564.
18. Hooper L.V., Macpherson A.J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 2010, 10:159-169.
19. Iwata M., Hirakiyama A., Eshima Y., Kagechika H., Kato C., Song S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004, 21:527-538.
20. Jung S., Aliberti J., Graemmel P., Sunshine M.J., Kreutzberg G.W., Sher A., Littman D.R. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 2000, 20:4106-4114.
21. Kamanaka M., Kim S.T., Wan Y.Y., Sutterwala F.S., Lara-Tejero M., Galán J.E., Harhaj E., Flavell R.A. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 2006, 25:941-952.
22. Kimm M.H., Hardin J.A., Gall D.G. Transport of albumin into the intestinal lumen of the rat. Can. J. Physiol. Pharmacol. 1997, 75:193-198.
23. Kunisawa J., Kurashima Y., Higuchi M., Gohda M., Ishikawa I., Ogahara I., Kim N., Shimizu M., Kiyono H. Sphingosine 1-phosphate dependence in the regulation of lymphocyte trafficking to the gut epithelium. J. Exp. Med. 2007, 204:2335-2348.
24. Lee Y.H., Ishida Y., Rifa'i M., Shi Z., Isobe K., Suzuki H. Essential role of CD8+CD122+ regulatory T cells in the recovery from experimental autoimmune encephalomyelitis. J. Immunol. 2008, 180:825-832.
25. Lin T., Matsuzaki G., Yoshida H., Kobayashi N., Kenai H., Omoto K., Nomoto K. CD3-CD8+ intestinal intraepithelial lymphocytes (IEL) and the extrathymic development of IEL. Eur. J. Immunol. 1994, 24:1080-1087.
26. Madan R., Demircik F., Surianarayanan S., Allen J.L., Divanovic S., Trompette A., Yogev N., Gu Y., Khodoun M., Hildeman D., et al. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J. Immunol. 2009, 183:2312-2320.
27. Masopust D., Vezys V., Usherwood E.J., Cauley L.S., Olson S., Marzo A.L., Ward R.L., Woodland D.L., Lefrançois L. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J. Immunol. 2004, 172:4875-4882.
28. Matteoli G., Mazzini E., Iliev I.D., Mileti E., Fallarino F., Puccetti P., Chieppa M., Rescigno M. Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction. Gut 2010, 59:595-604.
29. Mayer L., Shao L. Therapeutic potential of oral tolerance. Nat. Rev. Immunol. 2004, 4:407-419.
30. Mayer C.T., Floess S., Baru A.M., Lahl K., Huehn J., Sparwasser T. CD8+ Foxp3+ T cells share developmental and phenotypic features with classical CD4+ Foxp3+ regulatory T cells but lack potent suppressive activity. Eur. J. Immunol. 2011, 41:716-725.
31. McSorley S.J., Asch S., Costalonga M., Reinhardt R.L., Jenkins M.K. Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 2002, 16:365-377.
32. Ménager-Marcq I., Pomié C., Romagnoli P., van Meerwijk J.P. CD8+CD28- regulatory T lymphocytes prevent experimental inflammatory bowel disease in mice. Gastroenterology 2006, 131:1775-1785.
33. Milici A.J., Bankston P.W. Fetal and neonatal rat intestinal capillaries: permeability to carbon, ferritin, hemoglobin, and myoglobin. Am. J. Anat. 1982, 165:165-186.
34. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., Vyas J.M., Boes M., Ploegh H.L., Fox J.G., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005, 307:254-258.
35. Reynoso E.D., Elpek K.G., Francisco L., Bronson R., Bellemare-Pelletier A., Sharpe A.H., Freeman G.J., Turley S.J. Intestinal tolerance is converted to autoimmune enteritis upon PD-1 ligand blockade. J. Immunol. 2009, 182:2102-2112.
36. Rifa'i M., Kawamoto Y., Nakashima I., Suzuki H. Essential roles of CD8+CD122+ regulatory T cells in the maintenance of T cell homeostasis. J. Exp. Med. 2004, 200:1123-1134.
37. Satpathy A.T., Wu X., Albring J.C., Murphy K.M. Re(de)fining the dendritic cell lineage. Nat. Immunol. 2012, 13:1145-1154.
38. Schulz O., Jaensson E., Persson E.K., Liu X., Worbs T., Agace W.W., Pabst O. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 2009, 206:3101-3114.
39. Simionescu N., Simionescu M., Palade G.E. Permeability of intestinal capillaries. Pathway followed by dextrans and glycogens. J. Cell Biol. 1972, 53:365-392.
40. Snell L.M., McPherson A.J., Lin G.H., Sakaguchi S., Pandolfi P.P., Riccardi C., Watts T.H. CD8 T cell-intrinsic GITR is required for T cell clonal expansion and mouse survival following severe influenza infection. J. Immunol. 2010, 185:7223-7234.
41. Staton T.L., Habtezion A., Winslow M.M., Sato T., Love P.E., Butcher E.C. CD8+ recent thymic emigrants home to and efficiently repopulate the small intestine epithelium. Nat. Immunol. 2006, 7:482-488.
42. Strobel S., Mowat A.M. Oral tolerance and allergic responses to food proteins. Curr. Opin. Allergy Clin. Immunol. 2006, 6:207-213.
43. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., Belkaid Y. 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.
44. Suzuki M., Konya C., Goronzy J.J., Weyand C.M. Inhibitory CD8+ T cells in autoimmune disease. Hum. Immunol. 2008, 69:781-789.
45. Varol C., Vallon-Eberhard A., Elinav E., Aychek T., Shapira Y., Luche H., Fehling H.J., Hardt W.D., Shakhar G., Jung S. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 2009, 31:502-512.
46. Weber B., Saurer L., Schenk M., Dickgreber N., Mueller C. CX3CR1 defines functionally distinct intestinal mononuclear phagocyte subsets which maintain their respective functions during homeostatic and inflammatory conditions. Eur. J. Immunol. 2011, 41:773-779.
47. Weissleder R., Tung C.H., Mahmood U., Bogdanov A. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat. Biotechnol. 1999, 17:375-378.
48. Zhang N., Bevan M.J. CD8(+) T cells: foot soldiers of the immune system. Immunity 2011, 35:161-168.