Cutting edge: Inhaled antigen upregulates retinaldehyde dehydrogenase in lung CD103+ but not plasmacytoid dendritic cells to induce Foxp3 de novo in CD4+ T cells and promote airway tolerance

Journal of Immunology

Volumn 191, Issue 1, 2013, Pages 25-29

  Khare, Anupriya ^a   Krishnamoorthy, Nandini ^a   Oriss, Timothy B ^a   Fei, Mingjian ^a,b   Ray, Prabir ^a   Ray, Anuradha ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD103 ANTIGEN; RETINAL DEHYDROGENASE; RETINAL DEHYDROGENASE 2; RETINOIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BATF3 GENE; CD4+ T LYMPHOCYTE; CELL INTERACTION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME REGULATION; GENE; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; INHALATION; LUNG; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE; UPREGULATION;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIGENS, CD; ANTIGENS, CD11C; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNE TOLERANCE; INTEGRIN ALPHA CHAINS; LUNG; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; UP-REGULATION;

EID: 84879627201     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300193     Document Type: Article

References (30)

1. Ray, A., A. Khare, N. Krishnamoorthy, Z. Qi, and P. Ray. 2010. Regulatory T cells in many flavors control asthma. Mucosal Immunol. 3: 216-229.
2. Mold, J. E., J. Michaëlsson,T.D. Burt, M. O. Muench,K. P. Beckerman, M. P. Busch, T. H. Lee, D. F. Nixon, and J. M. McCune. 2008. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322: 1562-1565.
3. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell 133: 775-787. (Pubitemid 351707693)
4. Bluestone, J. A., and A. K. Abbas. 2003. Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3: 253-257. (Pubitemid 37323210)
5. Curotto de Lafaille, M. A., N. Kutchukhidze, S. Shen, Y. Ding, H. Yee, and J. J. Lafaille. 2008. Adaptive Foxp3+ regulatory T cell-dependent and -independent control of allergic inflammation. Immunity 29: 114-126.
6. Haribhai, D., J. B. Williams, S. Jia, D. Nickerson, E. G. Schmitt, B. Edwards, J. Ziegelbauer, M. Yassai, S. H. Li, L. M. Relland, et al. 2011. A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity 35: 109-122.
7. 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.
8. Coombes, J. L., K. R. Siddiqui, C. V. Arancibia-Cárcamo, J. Hall, C. M. Sun, Y. Belkaid, and F. Powrie. 2007. 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. 204: 1757-1764. (Pubitemid 47236314)
9. 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. (Pubitemid 47236316)
10. McMenamin, C., C. Pimm, M. McKersey, and P. G. Holt. 1994. Regulation of IgE responses to inhaled antigen in mice by antigen-specific gamma delta T cells. Science 265: 1869-1871. (Pubitemid 24324243)
11. 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. (Pubitemid 39071641)
12. van Rijt, L. S., S. Jung, A. Kleinjan, N. Vos, M. Willart, C. Duez, H. C. Hoogsteden, and B. N. Lambrecht. 2005. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201: 981-991. (Pubitemid 40524467)
13. Oriss, T. B., M. Ostroukhova, C. Seguin-Devaux, B. Dixon-McCarthy, D. B. Stolz, S. C. Watkins, B. Pillemer, P. Ray, and A. Ray. 2005. Dynamics of dendritic cell phenotype and interactions with CD4+ T cells in airway inflammation and tolerance. J. Immunol. 174: 854-863. (Pubitemid 40094280)
14. Krishnamoorthy, N., T. B. Oriss, M. Paglia, B. Vahaesebroek, A. Ray, and P. Ray. 2008. Activation of c-Kit in dendritic cells regulates T helper cell differentiation and allergic asthma. Nat. Med. 14: 565-573. (Pubitemid 351655220)
15. Lambrecht, B. N., and H. Hammad. 2009. Biology of lung dendritic cells at the origin of asthma. Immunity 31: 412-424.
16. Kim, T. S., and T. J. Braciale. 2009. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PLoS ONE 4: e4204.
17. Chen, C. H., C. Seguin-Devaux, N. A. Burke, T. B. Oriss, S. C. Watkins, N. Clipstone, and A. Ray. 2003. Transforming growth factor beta blocks Tec kinase phosphorylation, Ca2+ influx, and NFATc translocation causing inhibition of T cell differentiation. J. Exp. Med. 197: 1689-1699. (Pubitemid 36745344)
18. Liu, Y., P. Zhang, J. Li, A. B. Kulkarni, S. Perruche, and W. Chen. 2008. A critical function for TGF-beta signaling in the development of natural CD4+CD25+Foxp3 + regulatory T cells. Nat. Immunol. 9: 632-640. (Pubitemid 351712634)
19. Benson, M. J., K. Pino-Lagos, M. Rosemblatt, and R. J. Noelle. 2007. All-trans 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. (Pubitemid 47236315)
20. 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. (Pubitemid 47423756)
21. 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. (Pubitemid 47076203)
22. Kang, S. G., H. W. Lim, O. M. Andrisani, H. E. Broxmeyer, and C. H. Kim. 2007. Vitamin A metabolites induce gut-homing FoxP3+ regulatory T cells. J. Immunol. 179: 3724-3733.
23. Schambach, F., M. Schupp, M. A. Lazar, and S. L. Reiner. 2007. Activation of retinoic acid receptor-alpha favours regulatory T cell induction at the expense of IL-17-secreting T helper cell differentiation. Eur. J. Immunol. 37: 2396-2399. (Pubitemid 47423609)
24. Elias, K. M., A. Laurence, T. S. Davidson, G. Stephens, Y. Kanno, E. M. Shevach, and J. J. O'Shea. 2008. Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway. Blood 111: 1013-1020. (Pubitemid 351213378)
25. Nolting, J., C. Daniel, S. Reuter, C. Stuelten, P. Li, H. Sucov, B. G. Kim, J. J. Letterio, K. Kretschmer, H. J. Kim, and H. von Boehmer. 2009. Retinoic acid can enhance conversion of naive into regulatory T cells independently of secreted cytokines. J. Exp. Med. 206: 2131-2139.
26. Szatmari, I., A. Pap, R. Rühl, J. X. Ma, P. A. Illarionov, G. S. Besra, E. Rajnavolgyi, B. Dezso, and L. Nagy. 2006. PPARgamma controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J. Exp. Med. 203:2351-2362. (Pubitemid 44498369)
27. 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.
28. Klatt, N. R., J. D. Estes, X. Sun, A. M. Ortiz, J. S. Barber, L. D. Harris, B. Cervasi, L. K. Yokomizo, L. Pan, C. L. Vinton, et al. 2012. Loss of mucosal CD103+ DCs and IL-17+ and IL-22+ lymphocytes is associated with mucosal damage in SIV infection. Mucosal Immunol. 5: 646-657.
29. Edelson, B. T., W. Kc, R. Juang, M. Kohyama, L. A. Benoit, P. A. Klekotka, C. Moon, J. C. Albring, W. Ise, D. G. Michael, et al. 2010. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 207: 823-836.
30. Soroosh, P., T. A. Doherty, W. Duan, A. K. Mehta, H. Choi, Y. F. Adams, Z. Mikulski, N. Khorram, P. Rosenthal, D. H. Broide, and M. Croft. 2013. Lung-resident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J. Exp. Med. 210: 775-788.