Lung-resident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance

Journal of Experimental Medicine

Volumn 210, Issue 4, 2013, Pages 775-788

  Soroosh, Pejman ^a   Doherty, Taylor A ^c   Duan, Wei ^a   Mehta, Amit Kumar ^a   Choi, Heonsik ^a   Adams, Yan Fei ^a   Mikulski, Zbigniew ^b   Khorram, Naseem ^c   Rosenthal, Peter ^c   Broide, David H ^c   Croft, Michael ^a  

^a Division of Immune Regulation   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD24 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RETINAL DEHYDROGENASE; RETINAL DEHYDROGENASE 1; RETINAL DEHYDROGENASE 2; RETINOIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ALLERGEN; ANTINEOPLASTIC AGENT; TOLL LIKE RECEPTOR;

AIRWAY HYPERREACTIVITY; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT DISEASE; UPREGULATION; ANIMAL; ASTHMA; DRUG EFFECT; GENETICS; IMMUNOLOGY; LUNG; MOUSE MUTANT; PATHOLOGY; SIGNAL TRANSDUCTION;

ALLERGENS; ANIMALS; ANTINEOPLASTIC AGENTS; ASTHMA; FEMALE; IMMUNE TOLERANCE; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTORS; TRANSFORMING GROWTH FACTOR BETA; TRETINOIN;

MLCS; MLOWN;

EID: 84878659255     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20121849     Document Type: Article

References (64)

1. Akbari, O., R.H. DeKruyff, and D.T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2:725-731. http://dx.doi.org/10.1038/90667
2. Akdis, M. 2006. Healthy immune response to allergens: T regulatory cells and more. Curr. Opin. Immunol. 18:738-744. http://dx.doi.org/10.1016/j.coi.2006.06.003
3. Bakocevic, N., T. Worbs, A. Davalos-Misslitz, and R. Förster. 2010. T cell-dendritic cell interaction dynamics during the induction of respiratory tolerance and immunity. J. Immunol. 184:1317-1327. http://dx.doi.org/10.4049/jimmunol.0902277
4. Bang, B.R., E. Chun, E.J. Shim, H.S. Lee, S.Y. Lee, S.H. Cho, K.U. Min, Y.Y. Kim, and H.W. Park. 2011. Alveolar macrophages modulate allergic inflammation in a murine model of asthma. Exp. Mol. Med. 43:275-280. http://dx.doi.org/10.3858/emm.2011.43.5.028
5. Beaty, S.R., C.E. Rose Jr., and S.S. Sung. 2007. Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 178:1882-1895.
6. Benson, M.J., K. Pino-Lagos, M. Rosemblatt, and R.J. Noelle. 2007. Alltrans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204:1765-1774. http://dx.doi.org/10.1084/jem.20070719
7. Bilyk, N., and P.G. Holt. 1993. Inhibition of the immunosuppressive activity of resident pulmonary alveolar macrophages by granulocyte/ macrophage colony-stimulating factor. J. Exp. Med. 177:1773-1777. http://dx.doi.org/10.1084/jem.177.6.1773
8. Blumenthal, R.L., D.E. Campbell, P. Hwang, R.H. DeKruyff, L.R. Frankel, and D.T. Umetsu. 2001. Human alveolar macrophages induce functional inactivation in antigen-specific CD4 T cells. J. Allergy Clin. Immunol. 107:258-264. http://dx.doi.org/10.1067/mai.2001.112845
9. Braedel, S., M. Radsak, H. Einsele, J.P. Latgé, A. Michan, J. Loeffler, Z. Haddad, U. Grigoleit, H. Schild, and H. Hebart. 2004. Aspergillus fumigatus antigens activate innate immune cells via toll-like receptors 2 and 4. Br. J. Haematol. 125:392-399. http://dx.doi.org/10.1111/j.1365-2141.2004.04922.x
10. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198:1875-1886. http://dx.doi.org/10.1084/jem.20030152
11. + regulatory T cells via a TGF-β-and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757-1764. http://dx.doi.org/10.1084/jem.20070590
12. Cose, S., C. Brammer, K.M. Khanna, D. Masopust, and L. Lefrançois. 2006. Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur. J. Immunol. 36:1423-1433. http://dx.doi.org/10.1002/eji.200535539
13. + regulatory T cell-dependent and -independent control of allergic inflammation. Immunity. 29:114-126. http://dx.doi.org/10.1016/j.immuni.2008.05.010
14. de Heer, H.J., H. Hammad, T. Soullié, D. Hijdra, N. Vos, M.A. Willart, H.C. Hoogsteden, and B.N. Lambrecht. 2004. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200:89-98. http://dx.doi.org/10.1084/jem.20040035
15. Denning, T.L., Y.C. Wang, S.R. Patel, I.R. Williams, and B. Pulendran. 2007. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8:1086-1094. http://dx.doi.org/10.1038/ni1511
16. Denning, T.L., B.A. Norris, O. Medina-Contreras, S. Manicassamy, D. Geem, R. Madan, C.L. Karp, and B. Pulendran. 2011. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J. Immunol. 187:733-747. http://dx.doi.org/10.4049/jimmunol.1002701
17. reg development and function during allergic airway inflammation in vivo. J. Clin. Invest. 115:313-325. (published erratum appears in J. Clin. Invest. 2005. 115:1388)
18. Doherty, T., and D. Broide. 2007. Cytokines and growth factors in airway remodeling in asthma. Curr. Opin. Immunol. 19:676-680. http://dx.doi.org/10.1016/j.coi.2007.07.017
19. + T regulatory cells. J. Immunol. 181: 8650-8659.
20. Duan, W., A.K. Mehta, J.G. Magalhaes, S.F. Ziegler, C. Dong, D.J. Philpott, and M. Croft. 2010. Innate signals from Nod2 block respiratory tolerance and program T(H)2-driven allergic inflammation. J. Allergy Clin. Immunol. 126:1284-1293: e10. http://dx.doi.org/10.1016/j.jaci.2010.09.021
21. Duan, W., T. So, A.K. Mehta, H. Choi, and M. Croft. 2011. Inducible CD4+LAP+Foxp3-regulatory T cells suppress allergic inflammation. J. Immunol. 187:6499-6507. http://dx.doi.org/10.4049/jimmunol.1101398
22. Furuhashi, K., T. Suda, H. Hasegawa, Y. Suzuki, D. Hashimoto, N. Enomoto, T. Fujisawa, Y. Nakamura, N. Inui, K. Shibata, et al. 2012. Mouse lung CD103+ and CD11bhigh dendritic cells preferentially induce distinct CD4+ T-cell responses. Am. J. Respir. Cell Mol. Biol. 46: 165-172. http://dx.doi.org/10.1165/rcmb.2011-0070OC
23. Fütterer, A., K. Mink, A. Luz, M.H. Kosco-Vilbois, and K. Pfeffer. 1998. The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity. 9:59-70. http://dx.doi.org/10.1016/S1074-7613(00)80588-9
24. Gajewska, B.U., D. Alvarez, M. Vidric, S. Goncharova, M.R. Stämpfli, A.J. Coyle, J.C. Gutierrez-Ramos, and M. Jordana. 2001a. Generation of experimental allergic airways inflammation in the absence of draining lymph nodes. J. Clin. Invest. 108:577-583.
25. Gajewska, B.U., F.K. Swirski, D. Alvarez, S.A. Ritz, S. Goncharova, M. Cundall, D.P. Snider, A.J. Coyle, J.C. Gutierrez-Ramos, M.R. Stämpfli, and M. Jordana. 2001b. Temporal-spatial analysis of the immune response in a murine model of ovalbumin-induced airways inflammation. Am. J. Respir. Cell Mol. Biol. 25:326-334.
26. + regulatory T cells in the lamina propria. Immunity. 34:237-246. http://dx.doi.org/10.1016/j.immuni.2011.01.016
27. Halwani, R., S. Al-Muhsen, H. Al-Jahdali, and Q. Hamid. 2011. Role of transforming growth factor-β in airway remodeling in asthma. Am. J. Respir. Cell Mol. Biol. 44:127-133. http://dx.doi.org/10.1165/rcmb.2010-0027TR
28. Hamann, A., K. Klugewitz, F. Austrup, and D. Jablonski-Westrich. 2000. Activation induces rapid and profound alterations in the trafficking of T cells. Eur. J. Immunol. 30:3207-3218. http://dx.doi.org/10.1002/1521-4141(200011)30:11<3207::AID-IMMU3207>3.0.CO;2-L
29. Hammad, H., M. Chieppa, F. Perros, M.A. Willart, R.N. Germain, and B.N. Lambrecht. 2009. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 15:410-416. http://dx.doi.org/10.1038/nm.1946
30. Harp, J.R., and T.M. Onami. 2010. Naïve T cells re-distribute to the lungs of selectin ligand deficient mice. PLoS ONE. 5:e10973. http://dx.doi.org/10.1371/journal.pone.0010973
31. Hawrylowicz, C.M., and A. O'Garra. 2005. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 5:271-283. http://dx.doi.org/10.1038/nri1589
32. Hintzen, G., L. Ohl, M.L. del Rio, J.I. Rodriguez-Barbosa, O. Pabst, J.R. Kocks, J. Krege, S. Hardtke, and R. Förster. 2006. Induction of tolerance to innocuous inhaled antigen relies on a CCR7-dependent dendritic cell-mediated antigen transport to the bronchial lymph node. J. Immunol. 177:7346-7354.
33. Holt, P.G., J. Oliver, N. Bilyk, C. McMenamin, P.G. McMenamin, G. Kraal, and T. Thepen. 1993. Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J. Exp. Med. 177:397-407. http://dx.doi.org/10.1084/jem.177.2.397
34. Josefowicz, S.Z., R.E. Niec, H.Y. Kim, P. Treuting, T. Chinen, Y. Zheng, D.T. Umetsu, and A.Y. Rudensky. 2012. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature. 482:395-399. http://dx.doi.org/10.1038/nature10772
35. Kamada, N., T. Hisamatsu, S. Okamoto, T. Sato, K. Matsuoka, K. Arai, T. Nakai, A. Hasegawa, N. Inoue, N. Watanabe, et al. 2005. Abnormally differentiated subsets of intestinal macrophage play a key role in Th1-dominant chronic colitis through excess production of IL-12 and IL-23 in response to bacteria. J. Immunol. 175:6900-6908.
36. Kauffman, H.F., M. Tamm, J.A. Timmerman, and P. Borger. 2006. House dust mite major allergens Der p 1 and Der p 5 activate human airway-derived epithelial cells by protease-dependent and protease-independent mechanisms. Clin. Mol. Allergy. 4:5. http://dx.doi.org/10.1186/1476-7961-4-5
37. Kheradmand, F., A. Kiss, J. Xu, S.H. Lee, P.E. Kolattukudy, and D.B. Corry. 2002. A protease-activated pathway underlying Th cell type 2 activation and allergic lung disease. J. Immunol. 169:5904-5911.
38. Kirby, A.C., M.C. Coles, and P.M. Kaye. 2009. Alveolar macrophages transport pathogens to lung draining lymph nodes. J. Immunol. 183:1983-1989. http://dx.doi.org/10.4049/jimmunol.0901089
39. Larché, M. 2007. Regulatory T cells in allergy and asthma. Chest. 132:1007-1014. http://dx.doi.org/10.1378/chest.06-2434
40. Lekkerkerker, A.N., J. Aarbiou, T. van Es, and R.A. Janssen. 2012. Cellular players in lung fibrosis. Curr. Pharm. Des. 18:4093-4102. http://dx.doi.org/10.2174/138161212802430396
41. Lipscomb, M.F., A.M. Pollard, and J.L. Yates. 1993. A role for TGF-beta in the suppression by murine bronchoalveolar cells of lung dendritic cell initiated immune responses. Reg. Immunol. 5:151-157.
42. Lloyd, C.M., and C.M. Hawrylowicz. 2009. Regulatory T cells in asthma. Immunity. 31:438-449. http://dx.doi.org/10.1016/j.immuni.2009.08.007
43. Mambula, S.S., K. Sau, P. Henneke, D.T. Golenbock, and S.M. Levitz. 2002. Toll-like receptor (TLR) signaling in response to Aspergillus fumigatus. J. Biol. Chem. 277:39320-39326. http://dx.doi.org/10.1074/jbc.M201683200
44. Mucida, D., N. Kutchukhidze, A. Erazo, M. Russo, J.J. Lafaille, and M.A. Curotto de Lafaille. 2005. Oral tolerance in the absence of naturally occurring Tregs. J. Clin. Invest. 115:1923-1933. http://dx.doi.org/10.1172/JCI24487
45. Mucida, D., Y. Park, G. Kim, O. Turovskaya, I. Scott, M. Kronenberg, and H. Cheroutre. 2007. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 317:256-260. http://dx.doi.org/10.1126/science.1145697
46. Nakano, H., M.E. Free, G.S. Whitehead, S. Maruoka, R.H. Wilson, K. Nakano, and D.N. Cook. 2012. Pulmonary CD103(+) dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol. 5:53-65. http://dx.doi.org/10.1038/mi.2011.47
47. Neveu, W.A., J.B. Allard, O. Dienz, M.J. Wargo, G. Ciliberto, L.A. Whittaker, and M. Rincon. 2009. IL-6 is required for airway mucus production induced by inhaled fungal allergens. J. Immunol. 183:1732-1738. http://dx.doi.org/10.4049/jimmunol.0802923
48. Ostroukhova, M., C. Seguin-Devaux, T.B. Oriss, B. Dixon-McCarthy, L. Yang, B.T. Ameredes, T.E. Corcoran, and A. Ray. 2004. Tolerance induced by inhaled antigen involves CD4(+) T cells expressing membrane-bound TGF-beta and FOXP3. J. Clin. Invest. 114:28-38.
49. Roth, M.D., and S.H. Golub. 1993. Human pulmonary macrophages utilize prostaglandins and transforming growth factor beta 1 to suppress lymphocyte activation. J. Leukoc. Biol. 53:366-371.
50. Stevens, W.W., T.S. Kim, L.M. Pujanauski, X. Hao, and T.J. Braciale. 2007. Detection and quantitation of eosinophils in the murine respiratory tract by flow cytometry. J. Immunol. Methods. 327:63-74. http://dx.doi.org/10.1016/j.jim.2007.07.011
51. Strickland, D., U.R. Kees, and P.G. Holt. 1996. Regulation of T-cell activation in the lung: alveolar macrophages induce reversible T-cell anergy in vitro associated with inhibition of interleukin-2 receptor signal transduction. Immunology. 87:250-258. http://dx.doi.org/10.1046/j.1365-2567.1996.459542.x
52. Sun, C.M., J.A. Hall, R.B. Blank, N. Bouladoux, M. Oukka, J.R. Mora, and Y. Belkaid. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204:1775-1785. http://dx.doi.org/10.1084/jem.20070602
53. Thepen, T., C. McMenamin, B. Girn, G. Kraal, and P.G. Holt. 1992. Regulation of IgE production in pre-sensitized animals: in vivo elimination of alveolar macrophages preferentially increases IgE responses to inhaled allergen. Clin. Exp. Allergy. 22:1107-1114. http://dx.doi.org/ 10.1111/j.1365-2222.1992.tb00137.x
54. Thepen, T., E. Claassen, K. Hoeben, J. Brevé, and G. Kraal. 1993. Migration of alveolar macrophages from alveolar space to paracortical T cell area of the draining lymph node. Adv. Exp. Med. Biol. 329:305-310. http://dx.doi.org/10.1007/978-1-4615-2930-9_51
55. Tone, Y., K. Furuuchi, Y. Kojima, M.L. Tykocinski, M.I. Greene, and M. Tone. 2008. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9:194-202. http://dx.doi.org/10.1038/ni1549
56. Trompette, A., S. Divanovic, A. Visintin, C. Blanchard, R.S. Hegde, R. Madan, P.S. Thorne, M. Wills-Karp, T.L. Gioannini, J.P. Weiss, and C.L. Karp. 2009. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature. 457:585-588. http://dx.doi.org/10.1038/nature07548
57. Tsitoura, D.C., R.H. DeKruyff, J.R. Lamb, and D.T. Umetsu. 1999. Intranasal exposure to protein antigen induces immunological tolerance mediated by functionally disabled CD4+ T cells. J. Immunol. 163:2592-2600.
58. Umetsu, D.T., and R.H. Dekruyff. 2006. Immune dysregulation in asthma. Curr. Opin. Immunol. 18:727-732. http://dx.doi.org/10.1016/j.coi.2006.09.007
59. Upham, J.W., D.H. Strickland, N. Bilyk, B.W. Robinson, and P.G. Holt. 1995. Alveolar macrophages from humans and rodents selectively inhibit T-cell proliferation but permit T-cell activation and cytokine secretion. Immunology. 84:142-147.
60. Vermaelen, K., and R. Pauwels. 2004. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by flow cytometry: methodology and new insights. Cytometry A. 61A:170-177. http://dx.doi.org/10.1002/cyto.a.20064
61. Wikstrom, M.E., E. Batanero, S.R. Judd, K. Wiqvist, P.G. Holt, and P.A. Stumbles. 2010. Lung homing T-cell generation is dependent on strength and timing of antigen delivery to lymph nodes. Immunol. Cell Biol. 88:658-666. http://dx.doi.org/10.1038/icb.2010.18
62. Willart, M.A., K. Deswarte, P. Pouliot, H. Braun, R. Beyaert, B.N. Lambrecht, and H. Hammad. 2012. Interleukin-1α controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. J. Exp. Med. 209:1505-1517. http://dx.doi.org/10.1084/jem.20112691
63. Zaslona, Z., J. Wilhelm, L. Cakarova, L.M. Marsh, W. Seeger, J. Lohmeyer, and W. von Wulffen. 2009. Transcriptome profiling of primary murine monocytes, lung macrophages and lung dendritic cells reveals a distinct expression of genes involved in cell trafficking. Respir. Res. 10:2. http://dx.doi.org/10.1186/1465-9921-10-2
64. Zheng, Y., S. Josefowicz, A. Chaudhry, X.P. Peng, K. Forbush, and A.Y. Rudensky. 2010. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature. 463:808-812. http://dx.doi.org/10.1038/nature08750