Inducible CD4 +LAP +Foxp3 - regulatory T cells suppress allergic inflammation

Journal of Immunology

Volumn 187, Issue 12, 2011, Pages 6499-6507

  Duan, Wei ^a   So, Takanori ^a,b   Mehta, Amit K ^a   Choi, Heonsik ^a   Croft, Michael ^a  

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

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GRANZYME B; HERMES ANTIGEN; INTERLEUKIN 10; LATENCY ASSOCIATED PEPTIDE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; AIRWAY RESISTANCE; ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTHMA; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; INNATE IMMUNITY; LUNG LAVAGE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; OLIGOMERIZATION; PHENOTYPE; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH2 CELL;

ALLERGENS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EPITOPES, T-LYMPHOCYTE; FORKHEAD TRANSCRIPTION FACTORS; GENES, REPORTER; IMMUNE TOLERANCE; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 83755173097     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101398     Document Type: Article

References (51)

1. Lloyd, C. M., and C. M. Hawrylowicz. 2009. Regulatory T cells in asthma. Immunity 31: 438-449.
2. Kearley, J., J. E. Barker, D. S. Robinson, and C. M. Lloyd. 2005. Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+CD25+ regulatory T cells is interleukin 10 dependent. J. Exp. Med. 202: 1539-1547. (Pubitemid 41746600)
3. Joetham, A., K. Takeda, C. Taube, N. Miyahara, S.Matsubara, T. Koya, Y. H. Rha, A. Dakhama, and E. W. Gelfand. 2007. Naturally occurring lung CD4(+) CD25(+) T cell regulation of airway allergic responses depends on IL-10 induction of TGF-beta. [Published erratum appears in 2007 J. Immunol. 178: 5400.] J. Immunol. 178: 1433-1442. (Pubitemid 46154614)
4. 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. (Pubitemid 40516153)
5. Ostroukhova, M., Z. Qi, T. B. Oriss, B. Dixon-McCarthy, P. Ray, and A. Ray. 2006. Treg-mediated immunosuppression involves activation of the Notch-HES1 axis by membrane-bound TGF-beta. J. Clin. Invest. 116: 996-1004.
6. 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)
7. Duan, W., T. So, and M. Croft. 2008. Antagonism of airway tolerance by endotoxin/lipopolysaccharide through promoting OX40L and suppressing antigen-specific Foxp3+ T regulatory cells. J. Immunol. 181: 8650-8659.
8. Yang, Z., Z. Mu, B. Dabovic, V. Jurukovski, D. Yu, J. Sung, X. Xiong, and J. S. Munger. 2007. Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice. J. Cell Biol. 176: 787-793. (Pubitemid 46425539)
9. Saito, T., A. Kinoshita, Yoshiura Ki, Y. Makita, K. Wakui, K. Honke, N. Niikawa, and N. Taniguchi. 2001. Domain-specific mutations of a transforming growth factor (TGF)-beta 1 latency-associated peptide cause Camurati- Engelmann disease because of the formation of a constitutively active form of TGF-beta 1. J. Biol. Chem. 276: 11469-11472.
10. Ali, N. A., A. A. Gaughan, C. G. Orosz, C. P. Baran, S. McMaken, Y. Wang, T. D. Eubank, M. Hunter, F. J. Lichtenberger, N. A. Flavahan, et al. 2008. Latency associated peptide has in vitro and in vivo immune effects independent of TGF-beta1. PLoS ONE 3: e1914.
11. Ferreira, M. C., R. T. de Oliveira, R. M. da Silva, M. H. Blotta, and R. L. Mamoni. 2010. Involvement of regulatory T cells in the immunosuppression characteristic of patients with paracoccidioidomycosis. Infect. Immun. 78: 4392-4401.
12. Gasparoto, T. H., T. S. de Souza Malaspina, L. Benevides, E. J. de Melo, Jr., M. R. Costa, J. H. Damante, M. R. Ikoma, G. P. Garlet, K. A. Cavassani, J. S. da Silva, and A. P. Campanelli. 2010. Patients with oral squamous cell carcinoma are characterized by increased frequency of suppressive regulatory T cells in the blood and tumor microenvironment. Cancer Immunol. Immunother. 59: 819-828.
13. Hall, C. H., R. Kassel, R. S. Tacke, and Y. S. Hahn. 2010. HCV+ hepatocytes induce human regulatory CD4+ T cells through the production of TGF-beta. PLoS ONE 5: e12154.
14. Zhang, L., A. M. Bertucci, R. Ramsey-Goldman, R. K. Burt, and S. K. Datta. 2009. Regulatory T cell (Treg) subsets return in patients with refractory lupus following stem cell transplantation, and TGF-beta-producing CD8+ Treg cells are associated with immunological remission of lupus. J. Immunol. 183: 6346-6358.
15. Tran, D. Q., J. Andersson, D. Hardwick, L. Bebris, G. G. Illei, and E. M. Shevach. 2009. Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/CD121b) on activated human FOXP3+ regulatory T cells allows for their purification from expansion cultures. Blood 113: 5125-5133.
16. Chen, M. L., B. S. Yan, Y. Bando, V. K. Kuchroo, and H. L. Weiner. 2008. Latency-associated peptide identifies a novel CD4+CD25+ regulatory T cell subset with TGFbeta-mediated function and enhanced suppression of experimental autoimmune encephalomyelitis. J. Immunol. 180: 7327-7337.
17. Gandhi, R., M. F. Farez, Y. Wang, D. Kozoriz, F. J. Quintana, and H. L. Weiner. 2010. Cutting edge: human latency-associated peptide+ T cells: a novel regulatory T cell subset. J. Immunol. 184: 4620-4624.
18. Oida, T., and H. L. Weiner. 2010. Overexpression of TGF-β 1 gene induces cell surface localized glucose-regulated protein 78-associated latency-associated peptide/TGF-β. J. Immunol. 185: 3529-3535.
19. Oida, T., and H. L. Weiner. 2010. TGF-β induces surface LAP expression on murine CD4 T cells independent of Foxp3 induction. PLoS ONE 5: e15523.
20. 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. (Pubitemid 29399182)
21. 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. (Pubitemid 32747162)
22. Akbari, O., G. J. Freeman, E. H. Meyer, E. A. Greenfield, T. T. Chang, A. H. Sharpe, G. Berry, R. H. DeKruyff, and D. T. Umetsu. 2002. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 8: 1024-1032. (Pubitemid 35033708)
23. Stock, P., O. Akbari, G. Berry, G. J. Freeman, R. H. Dekruyff, and D. T. Umetsu. 2004. Induction of T helper type 1-like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat. Immunol. 5: 1149-1156. (Pubitemid 39549629)
24. Di Giacinto, C., M. Marinaro, M. Sanchez, W. Strober, and M. Boirivant. 2005. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J. Immunol. 174: 3237-3246. (Pubitemid 40354026)
25. Banz, A., A. Peixoto, C. Pontoux, C. Cordier, B. Rocha, and M. Papiernik. 2003. A unique subpopulation of CD4+ regulatory T cells controls wasting disease, IL-10 secretion and T cell homeostasis. Eur. J. Immunol. 33: 2419-2428. (Pubitemid 37138974)
26. Zelenika, D., E. Adams, S. Humm, L. Graca, S. Thompson, S. P. Cobbold, and H. Waldmann. 2002. Regulatory T cells overexpress a subset of Th2 gene transcripts. J. Immunol. 168: 1069-1079. (Pubitemid 34094470)
27. Cao, X., S. F. Cai, T. A. Fehniger, J. Song, L. I. Collins, D. R. Piwnica-Worms, and T. J. Ley. 2007. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27: 635-646. (Pubitemid 47628832)
28. Gondek, D. C., L. F. Lu, S. A. Quezada, S. Sakaguchi, and R. J. Noelle. 2005. Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J. Immunol. 174: 1783-1786. (Pubitemid 40223916)
29. Sherman, L., J. Sleeman, P. Herrlich, and H. Ponta. 1994. Hyaluronate receptors: key players in growth, differentiation, migration and tumor progression. Curr. Opin. Cell Biol. 6: 726-733. (Pubitemid 24295307)
30. Ayroldi, E., L. Cannarile, G. Migliorati, A. Bartoli, I. Nicoletti, and C. Riccardi. 1995. CD44 (Pgp-1) inhibits CD3 and dexamethasone-induced apoptosis. Blood 86: 2672-2678.
31. Firan, M., S. Dhillon, P. Estess, and M. H. Siegelman. 2006. Suppressor activity and potency among regulatory T cells is discriminated by functionally active CD44. Blood 107: 619-627. (Pubitemid 43076386)
32. Bollyky, P. L., J. D. Lord, S. A. Masewicz, S. P. Evanko, J. H. Buckner, T. N. Wight, and G. T. Nepom. 2007. Cutting edge: high molecular weight hyaluronan promotes the suppressive effects of CD4+CD25+ regulatory T cells. J. Immunol. 179: 744-747.
33. Bollyky, P. L., B. A. Falk, S. A. Long, A. Preisinger, K. R. Braun, R. P. Wu, S. P. Evanko, J. H. Buckner, T. N. Wight, and G. T. Nepom. 2009. CD44 costimulation promotes FoxP3+ regulatory T cell persistence and function via production of IL-2, IL-10, and TGF-beta. J. Immunol. 183: 2232-2241.
34. Sancho, D., M. Gómez, and F. Sánchez-Madrid. 2005. CD69 is an immuno-regulatory molecule induced following activation. Trends Immunol. 26: 136-140. (Pubitemid 40312520)
35. Han, Y., Q. Guo, M. Zhang, Z. Chen, and X. Cao. 2009. CD69+ CD4+ CD25-T cells, a new subset of regulatory T cells, suppress T cell proliferation through membrane-bound TGF-beta 1. J. Immunol. 182: 111-120.
36. Li, M. O., S. Sanjabi, and R. A. Flavell. 2006. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25: 455-471. (Pubitemid 44354214)
37. Marie, J. C., D. Liggitt, and A. Y. Rudensky. 2006. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 25: 441-454. (Pubitemid 44354215)
38. Ochi, H., M. Abraham, H. Ishikawa, D. Frenkel, K. Yang, A. S. Basso, H. Wu, M. L. Chen, R. Gandhi, A. Miller, et al. 2006. Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+ CD252 LAP+ T cells. Nat. Med. 12: 627-635. (Pubitemid 43865230)
39. Cates, E. C., R. Fattouh, J. Wattie, M. D. Inman, S. Goncharova, A. J. Coyle, J. C. Gutierrez-Ramos, and M. Jordana. 2004. Intranasal exposure of mice to house dust mite elicits allergic airway inflammation via a GM-CSF-mediated mechanism. J. Immunol. 173: 6384-6392. (Pubitemid 39487798)
40. 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.
41. O'Hehir, R. E., L. M. Gardner, M. P. de Leon, B. J. Hales, M. Biondo, J. A. Douglass, J. M. Rolland, and A. Sandrini. 2009. House dust mite sublingual immunotherapy: the role for transforming growth factor-beta and functional regulatory T cells. Am. J. Respir. Crit. Care Med. 180: 936-947.
42. Radulovic, S., M. R. Jacobson, S. R. Durham, and K. T. Nouri-Aria. 2008. Grass pollen immunotherapy induces Foxp3-expressing CD4+ CD25+ cells in the nasal mucosa. J. Allergy Clin. Immunol. 121: 1467-1472, 1472.e1.
43. Pereira-Santos, M. C., A. P. Baptista, A. Melo, R. R. Alves, R. S. Soares, E. Pedro, M. Pereira-Barbosa, R. M. Victorino, and A. E. Sousa. 2008. Expansion of circulating Foxp3+)D25bright CD4+ T cells during specific venom immunotherapy. Clin. Exp. Allergy 38: 291-297.
44. Karagiannidis, C., M. Akdis, P. Holopainen, N. J. Woolley, G. Hense, B. Rückert, P. Y. Mantel, G. Menz, C. A. Akdis, K. Blaser, and C. B. Schmidt-Weber. 2004. Glucocorticoids upregulate FOXP3 expression and regulatory T cells in asthma. J. Allergy Clin. Immunol. 114: 1425-1433. (Pubitemid 39575901)
45. Morgan, R. K., B. McAllister, L. Cross, D. S. Green, H. Kornfeld, D. M. Center, and W. W. Cruikshank. 2007. Histamine 4 receptor activation induces recruitment of FoxP3+ T cells and inhibits allergic asthma in a murine model. J. Immunol. 178: 8081-8089. (Pubitemid 46898080)
46. Andersson, J., D. Q. Tran, M. Pesu, T. S. Davidson, H. Ramsey, J. J. O'Shea, and E. M. Shevach. 2008. CD4+ FoxP3+ regulatory T cells confer infectious tolerance in a TGF-beta-dependent manner. J. Exp. Med. 205: 1975-1981.
47. Ochi, H., M. Abraham, H. Ishikawa, D. Frenkel, K. Yang, A. Basso, H. Wu, M. L. Chen, R. Gandhi, A. Miller, et al. 2008. New immunosuppressive approaches: oral administration of CD3-specific antibody to treat autoimmunity. J. Neurol. Sci. 274: 9-12.
48. Ishikawa, H., H. Ochi, M. L. Chen, D. Frenkel, R. Maron, and H. L. Weiner. 2007. Inhibition of autoimmune diabetes by oral administration of anti-CD3 monoclonal antibody. Diabetes 56: 2103-2109. (Pubitemid 47195835)
49. Ilan, Y., R. Maron, A. M. Tukpah, T. U. Maioli, G. Murugaiyan, K. Yang, H. Y. Wu, and H. L. Weiner. 2010. Induction of regulatory T cells decreases adipose inflammation and alleviates insulin resistance in ob/ob mice. Proc. Natl. Acad. Sci. USA 107: 9765-9770.
50. Nakamura, K., A. Kitani, I. Fuss, A. Pedersen, N. Harada, H. Nawata, and W. Strober. 2004. TGF-beta 1 plays an important role in the mechanism of CD4+ CD25+ regulatory T cell activity in both humans and mice. J. Immunol. 172: 834-842. (Pubitemid 38113739)
51. Wu, H. Y., R. Maron, A. M. Tukpah, and H. L. Weiner. 2010. Mucosal anti-CD3 monoclonal antibody attenuates collagen-induced arthritis that is associated with induction of LAP+ regulatory T cells and is enhanced by administration of an emulsome-based Th2-skewing adjuvant. J. Immunol. 185: 3401-3407.