Programming dendritic cells to induce T H 2 and tolerogenic responses

Nature Immunology

Volumn 11, Issue 8, 2010, Pages 647-655

  Pulendran, Bali ^a   Tang, Hua ^a   Manicassamy, Santhakumar ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12;

CELL INTERACTION; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; INNATE IMMUNITY; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; TH2 CELL;

DENDRITIC CELLS; HOST-PATHOGEN INTERACTIONS; IMMUNE TOLERANCE; IMMUNITY, INNATE; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH2 CELLS;

EID: 77954932467     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1894     Document Type: Review

References (130)

1. Mosmann, T.R., Cherwinski, H., Bond, M.W., Giedlin, M.A. & Coffman, R.L. Two types of murine helper T cell clone. I. Defnition according to profles of lymphokine activities and secreted proteins. J. Immunol. 136, 2348-2357 (1986).
2. Zhu, J., Yamane, H. & Paul, W.E. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489 (2010).
3. Murphy, C.A. et al. Divergent pro-and antiinfammatory roles for IL-23 and IL-12 in joint autoimmune infammation. J. Exp. Med. 198, 1951-1957 (2003).
4. Chen, W. et al. Conversion of peripheral CD4+CD25-naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
5. Grainger, J.R., Hall, J.A., Bouladoux, N., Oldenhove, G. & Belkaid, Y. Microbe-dendritic cell dialog controls regulatory T-cell fate. Immunol. Rev. 234, 305-316 (2010).
6. Steinman, R.M. & Banchereau, J. Taking dendritic cells into medicine. Nature 449, 419-426 (2007).
7. Pulendran, B. et al. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 96, 1036-1041 (1999).
8. Maldonado-Lopez, R. et al. CD8α+ and CD8α-subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189, 587-592 (1999).
9. Soares, H. et al. A subset of dendritic cells induces CD4+ T cells to produce IFN-gamma by an IL-12-independent but CD70-dependent mechanism in vivo. J. Exp. Med. 204, 1095-1106 (2007).
10. Stumbles, P.A. et al. Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J. Exp. Med. 188, 2019-2031 (1998).
11. Lambrecht, B.N. et al. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway infammation. J. Clin. Invest. 106, 551-559 (2000).
12. Rissoan, M.C. et al. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283, 1183-1186 (1999).
13. Klechevsky, E. et al. Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity 29, 497-510 (2008).
14. Pulendran, B. et al. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J. Immunol. 167, 5067-5076 (2001).
15. d'Ostiani, C.F. et al. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191, 1661-1674 (2000).
16. Lamhamedi-Cherradi, S.E. et al. Fungal proteases induce Th2 polarization through limited dendritic cell maturation and reduced production of IL-12. J. Immunol. 180, 6000-6009 (2008).
17. MacDonald, A.S., Straw, A.D., Bauman, B. & Pearce, E.J. CD8-dendritic cell activation status plays an integral role in infuencing Th2 response development. J. Immunol. 167, 1982-1988 (2001).
18. Everts, B. et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 206, 1673-1680 (2009).
19. Steinfelder, S. et al. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 206, 1681-1690 (2009).
20. Whelan, M. et al. A flarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164, 6453-6460 (2000).
21. Braun, M.C., He, J., Wu, C.Y. & Kelsall, B.L. Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor beta1 and beta2 chain expression. J. Exp. Med. 189, 541-552 (1999).
22. Shreffer, W.G. et al. The major glycoprotein allergen from Arachis hypogaea, Ara h 1, is a ligand of dendritic cell-specifc ICAM-grabbing nonintegrin and acts as a Th2 adjuvant in vitro. J. Immunol. 177, 3677-3685 (2006).
23. Kobayashi, T. et al. Asthma-related environmental fungus, Alternaria, activates dendritic cells and produces potent Th2 adjuvant activity. J. Immunol. 182, 2502-2510 (2009).
24. Ghaemmaghami, A.M., Gough, L., Sewell, H.F. & Shakib, F. The proteolytic activity of the major dust mite allergen Der p 1 conditions dendritic cells to produce less interleukin-12: allergen-induced Th2 bias determined at the dendritic cell level. Clin. Exp. Allergy 32, 1468-1475 (2002).
25. Traidl-Hoffmann, C. et al. Pollen-associated phytoprostanes inhibit dendritic cell interleukin-12 production and augment T helper type 2 cell polarization. J. Exp. Med. 201, 627-636 (2005).
26. Bozza, S. et al. Immune sensing of Aspergillus fumigatus proteins, glycolipids, and polysaccharides and the impact on Th immunity and vaccination. J. Immunol. 183, 2407-2414 (2009).
27. Kalinski, P., Schuitemaker, J.H., Hilkens, C.M. & Kapsenberg, M.L. Prostaglandin E2 induces the fnal maturation of IL-12-defcient CD1a+CD83+ dendritic cells: the levels of IL-12 are determined during the fnal dendritic cell maturation and are resistant to further modulation. J. Immunol. 161, 2804-2809 (1998).
28. Soumelis, V. et al. Human epithelial cells trigger dendritic cell mediated allergic infammation by producing TSLP. Nat. Immunol. 3, 673-680 (2002).
29. Ito, T. et al. TSLP-activated dendritic cells induce an infammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202, 1213-1223 (2005).
30. Zhou, B. et al. Thymic stromal lymphopoietin as a key initiator of allergic airway infammation in mice. Nat. Immunol. 6, 1047-1053 (2005).
31. Caron, G. et al. Histamine polarizes human dendritic cells into Th2 cell-promoting effector dendritic cells. J. Immunol. 167, 3682-3686 (2001).
32. van Rijt, L.S. et al. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201, 981-991 (2005).
33. Kool, M. et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating infammatory dendritic cells. J. Exp. Med. 205, 869-882 (2008).
34. Tang, H. et al. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11, 608-617 (2010).
35. Urban, J.F. Jr. et al. The importance of Th2 cytokines in protective immunity to nematodes. Immunol. Rev. 127, 205-220 (1992).
36. Khodoun, M.V., Orekhova, T., Potter, C., Morris, S. & Finkelman, F.D. Basophils initiate IL-4 production during a memory T-dependent response. J. Exp. Med. 200, 857-870 (2004).
37. Denzel, A. et al. Basophils enhance immunological memory responses. Nat. Immunol. 9, 733-742 (2008).
38. Min, B. & Paul, W.E. Basophils and type 2 immunity. Curr. Opin. Hematol. 15, 59-63 (2008).
39. Galli, S.J., Nakae, S. & Tsai, M. Mast cells in the development of adaptive immune responses. Nat. Immunol. 6, 135-142 (2005).
40. Kambayashi, T. et al. Indirect involvement of allergen-captured mast cells in antigen presentation. Blood 111, 1489-1496 (2008).
41. H2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat. Immunol. 10, 706-712 (2009).
42. Sokol, C.L. et al. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 10, 713-720 (2009).
43. H2 cytokine-dependent immunity. Nat. Immunol. 10, 697-705 (2009).
44. Yoshimoto, T., Bendelac, A., Watson, C., Hu-Li, J. & Paul, W.E. Role of NK1.1+ T cells in a TH2 response and in immunoglobulin E production. Science 270, 1845-1847 (1995).
45. Brown, D.R. et al. Beta 2-microglobulin-dependent NK1.1+ T cells are not essential for T helper cell 2 immune responses. J. Exp. Med. 184, 1295-1304 (1996).
46. Amsen, D. et al. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117, 515-526 (2004).
47. Brocker, T., Riedinger, M. & Karjalainen, K. Targeted expression of major histocompatibility complex (MHC) class II molecules demonstrates that dendritic cells can induce negative but not positive selection of thymocytes in vivo. J. Exp. Med. 185, 541-550 (1997).
48. Steinman, R.M. & Nussenzweig, M.C. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99, 351-358 (2002).
49. Jiang, A. et al. Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27, 610-624 (2007).
50. Morelli, A.E. & Thomson, A.W. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat. Rev. Immunol. 7, 610-621 (2007).
51. Mellor, A.L. & Munn, D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4, 762-774 (2004).
52. Steinman, R.M., Turley, S., Mellman, I. & Inaba, K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191, 411-416 (2000).
53. Belz, G.T. et al. The CD8α+ dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 196, 1099-1104 (2002).
54. Bonifaz, L. et al. Effcient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 196, 1627-1638 (2002).
55. Bonifazi, P. et al. Balancing infammation and tolerance in vivo through dendritic cells by the commensal Candida albicans. Mucosal Immunol. 2, 362-374 (2009).
56. van der Kleij, D. et al. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122-48129 (2002).
57. McGuirk, P., McCann, C. & Mills, K.H. Pathogen-specifc T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195, 221-231 (2002).
58. Depaolo, R.W. et al. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4, 350-361 (2008).
59. Garrett, W.S., Gordon, J.I. & Glimcher, L.H. Homeostasis and infammation in the intestine. Cell 140, 859-870 (2010).
60. Coombes, J.L. et al. 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 (2007).
61. Sun, C.M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
62. 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. 8, 1086-1094 (2007).
63. Murai, M. et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 10, 1178-1184 (2009).
64. + regulatory T cells. Blood 115, 1958-1968 (2010).
65. Grohmann, U. et al. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat. Med. 13, 579-586 (2007).
66. Iwasaki, A. & Medzhitov, R. Regulation of adaptive immunity by the innate immune system. Science 327, 291-295 (2010).
67. Maizels, R.M., Pearce, E.J., Artis, D., Yazdanbakhsh, M. & Wynn, T.A. Regulation of pathogenesis and immunity in helminth infections. J. Exp. Med. 206, 2059-2066 (2009).
68. Kiura, K., Kataoka, H., Yasuda, M., Inoue, N. & Shibata, K. The diacylated lipopeptide FSL-1 induces TLR2-mediated Th2 responses. FEMS Immunol. Med. Microbiol. 48, 44-55 (2006).
69. Dillon, S. et al. A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells. J. Immunol. 172, 4733-4743 (2004).
70. Agrawal, S. et al. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171, 4984-4989 (2003).
71. Redecke, V. et al. Cutting edge: activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J. Immunol. 172, 2739-2743 (2004).
72. van Riet, E. et al. Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization. BMC Immunol. 10, 9 (2009).
73. Liu, T. et al. Staphylococcal enterotoxin B increases TIM4 expression in human dendritic cells that drives naive CD4 T cells to differentiate into Th2 cells. Mol. Immunol. 44, 3580-3587 (2007).
74. Yang, D. et al. Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. J. Exp. Med. 205, 79-90 (2008).
75. Dillon, S. et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116, 916-928 (2006).
76. Manicassamy, S. et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat. Med. 15, 401-409 (2009).
77. Karumuthil-Melethil, S., Perez, N., Li, R. & Vasu, C. Induction of innate immune response through TLR2 and dectin 1 prevents type 1 diabetes. J. Immunol. 181, 8323-8334 (2008).
78. McKimmie, C.S. et al. A TLR2 ligand suppresses infammation by modulation of chemokine receptors and redirection of leukocyte migration. Blood 113, 4224-4231 (2009).
79. Abdollahi-Roodsaz, S. et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J. Clin. Invest. 118, 205-216 (2008).
80. Loures, F.V., Pina, A., Felonato, M. & Calich, V.L. TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J. Immunol. 183, 1279-1290 (2009).
81. Nichols, J.R. et al. TLR2 defciency leads to increased Th17 infltrates in experimental brain abscesses. J. Immunol. 182, 7119-7130 (2009).
82. Chau, T.A. et al. Toll-like receptor 2 ligands on the staphylococcal cell wall downregulate superantigen-induced T cell activation and prevent toxic shock syndrome. Nat. Med. 15, 641-648 (2009).
83. Eisenbarth, S.C. et al. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J. Exp. Med. 196, 1645-1651 (2002).
84. Hammad, H. et al. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 15, 410-416 (2009).
85. Trompette, A. et al. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 457, 585-588 (2009).
86. Ting, J.P., Duncan, J.A. & Lei, Y. How the noninfammasome NLRs function in the innate immune system. Science 327, 286-290 (2010).
87. Fritz, J.H. et al. Nod1-mediated innate immune recognition of peptidoglycan contributes to the onset of adaptive immunity. Immunity 26, 445-459 (2007).
88. Magalhaes, J.G. et al. Nod2-dependent Th2 polarization of antigen-specifc immunity. J. Immunol. 181, 7925-7935 (2008).
89. Eisenbarth, S.C., Colegio, O.R., O'Connor, W., Sutterwala, F.S. & Flavell, R.A. Crucial role for the Nalp3 infammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453, 1122-1126 (2008).
90. Kool, M. et al. Cutting edge: alum adjuvant stimulates infammatory dendritic cells through activation of the NALP3 infammasome. J. Immunol. 181, 3755-3759 (2008).
91. Li, H., Willingham, S.B., Ting, J.P. & Re, F. Cutting edge: infammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J. Immunol. 181, 17-21 (2008).
92. Geijtenbeek, T.B. & Gringhuis, S.I. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9, 465-479 (2009).
93. Rogers, N.C. et al. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22, 507-517 (2005).
94. LeibundGut-Landmann, S. et al. Syk-and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8, 630-638 (2007).
95. Bergman, M.P. et al. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J. Exp. Med. 200, 979-990 (2004).
96. Nimmerjahn, F. & Ravetch, J.V. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47 (2008).
97. Anderson, C.F., Lucas, M., Gutierrez-Kobeh, L., Field, A.E. & Mosser, D.M. T cell biasing by activated dendritic cells. J. Immunol. 173, 955-961 (2004).
98. Sutterwala, F.S., Noel, G.J., Salgame, P. & Mosser, D.M. Reversal of proinfammatory responses by ligating the macrophage Fcγ receptor type I. J. Exp. Med. 188, 217-222 (1998).
99. Bandukwala, H.S. et al. Signaling through Fc gamma RIII is required for optimal T helper type (Th)2 responses and Th2-mediated airway infammation. J. Exp. Med. 204, 1875-1889 (2007).
100. Marth, T. & Kelsall, B.L. Regulation of interleukin-12 by complement receptor 3 signaling. J. Exp. Med. 185, 1987-1995 (1997).
101. Karp, C.L. et al. Mechanism of suppression of cell-mediated immunity by measles virus. Science 273, 228-231 (1996).
102. Hawlisch, H. et al. C5a negatively regulates toll-like receptor 4-induced immune responses. Immunity 22, 415-426 (2005).
103. Chapman, M.D., Wunschmann, S. & Pomes, A. Proteases as Th2 adjuvants. Curr. Allergy Asthma Rep. 7, 363-367 (2007).
104. Kouzaki, H., O'Grady, S.M., Lawrence, C.B. & Kita, H. Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J. Immunol. 183, 1427-1434 (2009).
105. Briot, A. et al. Kallikrein 5 induces atopic dermatitis-like lesions through PAR2-mediated thymic stromal lymphopoietin expression in Netherton syndrome. J. Exp. Med. 206, 1135-1147 (2009).
106. Yi, A.K. et al. Role of mitogen-activated protein kinases in CpG DNA-mediated IL-10 and IL-12 production: central role of extracellular signal-regulated kinase in the negative feedback loop of the CpG DNA-mediated Th1 response. J. Immunol. 168, 4711-4720 (2002).
107. Kaji, R., Kiyoshima-Shibata, J., Nagaoka, M., Nanno, M. & Shida, K. Bacterial teichoic acids reverse predominant IL-12 production induced by certain lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J. Immunol. 184, 3505-3513 (2010).
108. Koga, K. et al. Cyclic adenosine monophosphate suppresses the transcription of proinfammatory cytokines via the phosphorylated c-Fos protein. Immunity 30, 372-383 (2009).
109. Luo, X. et al. Inhibition of monocyte-derived dendritic cell differentiation and interleukin-12 production by complement iC3b via a mitogen-activated protein kinase signalling pathway. Exp. Dermatol. 14, 303-310 (2005).
110. Kroening, P.R. et al. Cigarette smoke-induced oxidative stress suppresses generation of dendritic cell IL-12 and IL-23 through ERK-dependent pathways. J. Immunol. 181, 1536-1547 (2008).
111. Caparros, E. et al. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 107, 3950-3958 (2006).
112. Lucas, M., Zhang, X., Prasanna, V. & Mosser, D.M. ERK activation following macrophage FcγR ligation leads to chromatin modifcations at the IL-10 locus. J. Immunol. 175, 469-477 (2005).
113. Merck, E. et al. Fc receptor gamma-chain activation via hOSCAR induces survival and maturation of dendritic cells and modulates Toll-like receptor responses. Blood 105, 3623-3632 (2005).
114. Correa, F., Mestre, L., Docagne, F. & Guaza, C. Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling. Br. J. Pharmacol. 145, 441-448 (2005).
115. Banerjee, A., Gugasyan, R., McMahon, M. & Gerondakis, S. Diverse Toll-like receptors utilize Tpl2 to activate extracellular signal-regulated kinase (ERK) in hemopoietic cells. Proc. Natl. Acad. Sci. USA 103, 3274-3279 (2006).
116. Kaiser, F. et al. TPL-2 negatively regulates interferon-beta production in macrophages and myeloid dendritic cells. J. Exp. Med. 206, 1863-1871 (2009).
117. Arima, K. et al. Distinct signal codes generate dendritic cell functional plasticity. Sci. Signal. 3, ra4 (2010).
118. Bedard, K. & Krause, K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313 (2007).
119. Binder, C.J. et al. Innate and acquired immunity in atherogenesis. Nat. Med. 8, 1218-1226 (2002).
120. Imai, Y. et al. Identifcation of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133, 235-249 (2008).
121. Riedl, M.A. & Nel, A.E. Importance of oxidative stress in the pathogenesis and treatment of asthma. Curr. Opin. Allergy Clin. Immunol. 8, 49-56 (2008).
122. Gelderman, K.A. et al. Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J. Clin. Invest. 117, 3020-3028 (2007).
123. Manicassamy, S. et al. Activation of β-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science (in the press).
124. Moro, K. et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463, 540-544 (2010).
125. H2 cytokine responses. Nature 464, 1362-1366 (2010).
126. Neill, D.R. et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370 (2010).
127. Gabrilovich, D.I. & Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174 (2009).
128. Swamy, M., Jamora, C., Havran, W. & Hayday, A. A. Epithelial decision-makers: in search of the 'epimmunome'. Nat. Immunol. (20 July 2010) doi:10.1038/ni.1905.
129. Hawiger, D. et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194, 769-779 (2001).
130. Geijtenbeek, T.B. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003).