Regulatory T Cell-Derived Interleukin-10 Limits Inflammation at Environmental Interfaces

Immunity

Volumn 28, Issue 4, 2008, Pages 546-558

  Rubtsov, Yuri P ^a   Rasmussen, Jeffrey P ^a   Chi, Emil Y ^a   Fontenot, Jason ^a   Castelli, Luca ^a   Ye, Xin ^a   Treuting, Piper ^a   Siewe, Lisa ^b   Roers, Axel ^b   Henderson Jr , William R ^a   Muller, Werner ^c   Rudensky, Alexander Y ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

CELLIMMUNO

Indexed keywords

CRE RECOMBINASE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNITY; BRONCHUS HYPERREACTIVITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COLITIS; COLON; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE LOCUS; IMMUNOMODULATION; INFLAMMATION; LUNG; MALE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SKIN ALLERGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; AUTOIMMUNE DISEASES; COLITIS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; INFLAMMATION MEDIATORS; INTEGRASES; INTERLEUKIN-10; LUMINESCENT PROTEINS; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; ORGAN SPECIFICITY; SKIN; T-LYMPHOCYTES, REGULATORY;

EID: 41549159660     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.02.017     Document Type: Article

References (55)

1. Anderson C.F., Oukka M., Kuchroo V.J., and Sacks D. CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204 (2007) 285-297
2. Annacker O., Asseman C., Read S., and Powrie F. Interleukin-10 in the regulation of T cell-induced colitis. J. Autoimmun. 20 (2003) 277-279
3. Asseman C., Mauze S., Leach M.W., Coffman R.L., and Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190 (1999) 995-1004
4. Asseman C., Read S., and Powrie F. Colitogenic Th1 cells are present in the antigen-experienced T cell pool in normal mice: control by CD4+ regulatory T cells and IL-10. J. Immunol. 171 (2003) 971-978
5. Berg D.J., Leach M.W., Kuhn R., Rajewsky K., Muller W., Davidson N.J., and Rennick D. Interleukin 10 but not interleukin 4 is a natural suppressant of cutaneous inflammatory responses. J. Exp. Med. 182 (1995) 99-108
6. Bopp T., Becker C., Klein M., Klein-Hessling S., Palmetshofer A., Serfling E., Heib V., Becker M., Kubach J., Schmitt S., et al. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J. Exp. Med. 204 (2007) 1303-1310
7. Brunkow M.E., Jeffery E.W., Hjerrild K.A., Paeper B., Clark L.B., Yasayko S.A., Wilkinson J.E., Galas D., Ziegler S.F., and Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27 (2001) 68-73
8. Burich A., Hershberg R., Waggie K., Zeng W., Brabb T., Westrich G., Viney J.L., and Maggio-Price L. Helicobacter-induced inflammatory bowel disease in IL-10- and T cell- deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281 (2001) G764-G778
9. Chen M.L., Pittet M.J., Gorelik L., Flavell R.A., Weissleder R., von Boehmer H., and Khazaie K. Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo. Proc. Natl. Acad. Sci. USA 102 (2005) 419-424
10. Deaglio S., Dwyer K.M., Gao W., Friedman D., Usheva A., Erat A., Chen J.F., Enjyoji K., Linden J., Oukka M., et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204 (2007) 1257-1265
11. Drakes M.L., Blanchard T.G., and Czinn S.J. Colon lamina propria dendritic cells induce a proinflammatory cytokine response in lamina propria T cells in the SCID mouse model of colitis. J. Leukoc. Biol. 78 (2005) 1291-1300
12. Fahlen L., Read S., Gorelik L., Hurst S.D., Coffman R.L., Flavell R.A., and Powrie F. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J. Exp. Med. 201 (2005) 737-746
13. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4 (2003) 330-336
14. Fontenot J.D., Rasmussen J.P., Williams L.M., Dooley J.L., Farr A.G., and Rudensky A.Y. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22 (2005) 329-341
15. Fontenot J.D., and Rudensky A.Y. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6 (2005) 331-337
16. Gavin M.A., Clarke S.R., Negrou E., Gallegos A., and Rudensky A. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat. Immunol. 3 (2002) 33-41
17. Gavin M.A., Rasmussen J.P., Fontenot J.D., Vasta V., Manganiello V.C., Beavo J.A., and Rudensky A.Y. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445 (2007) 771-775
18. Gondek D.C., Lu L.F., Quezada S.A., Sakaguchi S., and Noelle R.J. Cutting edge: Contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J. Immunol. 174 (2005) 1783-1786
19. Grimbaldeston M.A., Nakae S., Kalesnikoff J., Tsai M., and Galli S.J. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat. Immunol. 8 (2007) 1095-1104
20. Guenther M.G., Levine S.S., Boyer L.A., Jaenisch R., and Young R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130 (2007) 77-88
21. Henderson Jr. W.R., Banerjee E.R., and Chi E.Y. Differential effects of (S)- and (R)-enantiomers of albuterol in a mouse asthma model. J. Allergy Clin. Immunol. 116 (2005) 332-340
22. Henderson Jr. W.R., Chi E.Y., Bollinger J.G., Tien Y.T., Ye X., Castelli L., Rubtsov Y.P., Singer A.G., Chiang G.K., Nevalainen T., et al. Importance of group X-secreted phospholipase A2 in allergen-induced airway inflammation and remodeling in a mouse asthma model. J. Exp. Med. 204 (2007) 865-877
23. Henderson Jr. W.R., Lewis D.B., Albert R.K., Zhang Y., Lamm W.J., Chiang G.K., Jones F., Eriksen P., Tien Y.T., Jonas M., and Chi E.Y. The importance of leukotrienes in airway inflammation in a mouse model of asthma. J. Exp. Med. 184 (1996) 1483-1494
24. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science (N. Y) 299 (2003) 1057-1061
25. Jankovic D., Kullberg M.C., Feng C.G., Goldszmid R.S., Collazo C.M., Wilson M., Wynn T.A., Kamanaka M., Flavell R.A., and Sher A. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204 (2007) 273-283
26. Kamanaka M., Kim S.T., Wan Y.Y., Sutterwala F.S., Lara-Tejero M., Galan J.E., Harhaj E., and Flavell R.A. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 25 (2006) 941-952
27. Khattri R., Cox T., Yasayko S.A., and Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4 (2003) 337-342
28. Kim J.M., Rasmussen J.P., and Rudensky A.Y. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8 (2007) 191-197
29. Komatsu N., and Hori S. Full restoration of peripheral Foxp3+ regulatory T cell pool by radioresistant host cells in scurfy bone marrow chimeras. Proc. Natl. Acad. Sci. USA 104 (2007) 8959-8964
30. Kuhn R., Lohler J., Rennick D., Rajewsky K., and Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75 (1993) 263-274
31. Kullberg M.C., Hay V., Cheever A.W., Mamura M., Sher A., Letterio J.J., Shevach E.M., and Piccirillo C.A. TGF-beta1 production by CD4+ CD25+ regulatory T cells is not essential for suppression of intestinal inflammation. Eur. J. Immunol. 35 (2005) 2886-2895
32. Li M.O., Wan Y.Y., and Flavell R.A. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 26 (2007) 579-591
33. Lin W., Haribhai D., Relland L.M., Truong N., Carlson M.R., Williams C.B., and Chatila T.A. Regulatory T cell development in the absence of functional Foxp3. Nat. Immunol. 8 (2007) 359-368
34. Mahic M., Yaqub S., Johansson C.C., Tasken K., and Aandahl E.M. FOXP3+CD4+CD25+ adaptive regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E2-dependent mechanism. J. Immunol. 177 (2006) 246-254
35. Makela M.J., Kanehiro A., Borish L., Dakhama A., Loader J., Joetham A., Xing Z., Jordana M., Larsen G.L., and Gelfand E.W. IL-10 is necessary for the expression of airway hyperresponsiveness but not pulmonary inflammation after allergic sensitization. Proc. Natl. Acad. Sci. USA 97 (2000) 6007-6012
36. Marson A., Kretschmer K., Frampton G.M., Jacobsen E.S., Polansky J.K., MacIsaac K.D., Levine S.S., Fraenkel E., von Boehmer H., and Young R.A. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445 (2007) 931-935
37. Maynard C.L., Harrington L.E., Janowski K.M., Oliver J.R., Zindl C.L., Rudensky A.Y., and Weaver C.T. Regulatory T cells expressing interleukin 10 develop from Foxp3(+) and Foxp3(-) precursor cells in the absence of interleukin 10. Nat. Immunol. 8 (2007) 931-941
38. Miyara M., and Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol. Med. 13 (2007) 108-116
39. Moore K.W., de Waal Malefyt R., Coffman R.L., and O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19 (2001) 683-765
40. Nylen S., Maurya R., Eidsmo L., Manandhar K.D., Sundar S., and Sacks D. Splenic accumulation of IL-10 mRNA in T cells distinct from CD4+CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J. Exp. Med. 204 (2007) 805-817
41. Oderup C., Cederbom L., Makowska A., Cilio C.M., and Ivars F. Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4+ CD25+ regulatory T-cell-mediated suppression. Immunology 118 (2006) 240-249
42. Ohl L., Mohaupt M., Czeloth N., Hintzen G., Kiafard Z., Zwirner J., Blankenstein T., Henning G., and Forster R. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21 (2004) 279-288
43. Paust S., Lu L., McCarty N., and Cantor H. Engagement of B7 on effector T cells by regulatory T cells prevents autoimmune disease. Proc. Natl. Acad. Sci. USA 101 (2004) 10398-10403
44. Powrie F., Carlino J., Leach M.W., Mauze S., and Coffman R.L. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183 (1996) 2669-2674
45. Roers A., Siewe L., Strittmatter E., Deckert M., Schluter D., Stenzel W., Gruber A.D., Krieg T., Rajewsky K., and Muller W. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200 (2004) 1289-1297
46. Shevach E.M., McHugh R.S., Piccirillo C.A., and Thornton A.M. Control of T-cell activation by CD4+ CD25+ suppressor T cells. Immunol. Rev. 182 (2001) 58-67
47. Singh B., Read S., Asseman C., Malmstrom V., Mottet C., Stephens L.A., Stepankova R., Tlaskalova H., and Powrie F. Control of intestinal inflammation by regulatory T cells. Immunol. Rev. 182 (2001) 190-200
48. Tang Q., Boden E.K., Henriksen K.J., Bour-Jordan H., Bi M., and Bluestone J.A. Distinct roles of CTLA-4 and TGF-beta in CD4+CD25+ regulatory T cell function. Eur. J. Immunol. 34 (2004) 2996-3005
49. Uhlig H.H., Coombes J., Mottet C., Izcue A., Thompson C., Fanger A., Tannapfel A., Fontenot J.D., Ramsdell F., and Powrie F. Characterization of Foxp3+CD4+CD25+ and IL-10-secreting CD4+CD25+ T cells during cure of colitis. J. Immunol. 177 (2006) 5852-5860
50. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat. Immunol. 6 (2005) 338-344
51. Wan Y.Y., and Flavell R.A. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 445 (2007) 766-770
52. Wildin R.S., and Freitas A. IPEX and FOXP3: Clinical and research perspectives. J. Autoimmun. 25 Suppl (2005) 56-62
53. Williams L.M., and Rudensky A.Y. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat. Immunol. 8 (2007) 277-284
54. Zhang Y., Lamm W.J., Albert R.K., Chi E.Y., Henderson Jr. W.R., and Lewis D.B. Influence of the route of allergen administration and genetic background on the murine allergic pulmonary response. Am. J. Respir. Crit. Care Med. 155 (1997) 661-669
55. Zheng Y., Josefowicz S.Z., Kas A., Chu T.T., Gavin M.A., and Rudensky A.Y. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445 (2007) 936-940