Nuclear receptor signalling in dendritic cells connects lipids, the genome and immune function

EMBO Journal

Volumn 27, Issue 18, 2008, Pages 2353-2362

  Szatmari, Istvan ^a   Nagy, Laszlo ^a,b  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Dendritic cells; Immunity; Lipid signalling; Nuclear receptors; PPAR

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOIC ACID RECEPTOR; RETINOID; VITAMIN D; VITAMIN D RECEPTOR;

ADAPTIVE IMMUNITY; CELL ACTIVATION; CELL DIFFERENTIATION; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL NUCLEUS; DENDRITIC CELLS; GENOME; HUMANS; IMMUNE SYSTEM; LIPIDS; MODELS, BIOLOGICAL; PPAR GAMMA; RECEPTORS, CALCITRIOL; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, GLUCOCORTICOID; RECEPTORS, RETINOIC ACID; SIGNAL TRANSDUCTION;

EID: 51949114424     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.160     Document Type: Review

References (84)

1. Abe M, Thomson AW (2003) Influence of immunosuppressive drugs on dendritic cells. Transpl Immunol 11: 357-365
2. Angeli V, Hammad H, Staels B, Capron M, Lambrecht BN, Trottein F (2003) Peroxisome proliferator-activated receptor gamma inhibits the migration of dendritic cells: consequences for the immune response. J Immunol 170: 5295-5301
3. Angeli V, Llodra J, Rong JX, Satoh K, Ishii S, Shimizu T, Fisher EA, Randolph GJ (2004) Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity 21: 561-574
4. Appel S, Mirakaj V, Bringmann A, Weck MM, Grunebach F, Brossart P (2005) PPAR-gamma agonists inhibit toll-like receptor mediated activation of dendritic cells via the MAP kinase and NF-kappaB pathways. Blood 106: 3888-3894
5. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392: 245-252
6. Barish GD, Narkar VA, Evans RM (2006) PPAR delta: a dagger in the heart of the metabolic syndrome. J Clin Invest 116: 590-597
7. Bedford PA, Knight SC (1989) The effect of retinoids on dendritic cell function. Clin Exp Immunol 75: 481-486
8. Benson MJ, Pino-Lagos K, Rosemblatt M, Noelle RJ (2007) All-trans retinoic acid mediates enhanced Treg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J Exp Med 204: 1765-1774
9. Bobryshev YV, Lord RS (1995) S-100 positive cells in human arterial intima and in atherosclerotic lesions. Cardiovasc Res 29: 689-696
10. Brigl M, Brenner MB (2004) CD1: antigen presentation and T cell function. Annu Rev Immunol 22: 817-890
11. Chen Q, Ross AC (2007) Retinoic acid regulates CD1d gene expression at the transcriptional level in human and rodent monocytic cells. Exp Biol Med (Maywood) 232: 488-494
12. Cools N, Ponsaerts P, Van Tendeloo VF, Berneman ZN (2007) Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J Leukoc Biol 82: 1365-1374
13. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, Powrie F (2007) A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory Tcells via a TGF-\{beta\} and reti. J Exp Med 204: 1757-1764
14. Coutant F, Perrin-Cocon L, Agaugue S, Delair T, Andre P, Lotteau V (2002) Mature dendritic cell generation promoted by lysophosphatidylcholine. J Immunol 169: 1688-1695
15. Darmanin S, Chen J, Zhao S, Cui H, Shirkoohi R, Kubo N, Kuge Y, Tamaki N, Nakagawa K, Hamada J, Moriuchi T, Kobayashi M (2007) All-trans retinoic acid enhances murine dendritic cell migration to draining lymph nodes via the balance of matrix metalloproteinases and their inhibitors. J Immunol 179: 4616-4625
16. Dong X, Craig T, Xing N, Bachman LA, Paya CV, Weih F, McKean DJ, Kumar R, Griffin MD (2003) Direct transcriptional regulation of RelB by 1alpha,25-dihydroxyvitamin D3 and its analogs: physiologic and therapeutic implications for dendritic cell function. J Biol Chem 278: 49378-49385
17. Dubrac S, Stoitzner P, Pirkebner D, Elentner A, Schoonjans K, Auwerx J, Saeland S, Hengster P, Fritsch P, Romani N, Schmuth M (2007) Peroxisome proliferator-activated receptor-alpha activation inhibits Langerhans cell function. J Immunol 178: 4362-4372
18. Duester G (2000) Families of retinoid dehydrogenases regulating vitamin A function: production of visual pigment and retinoic acid. Eur J Biochem 267: 4315-4324
19. Faveeuw C, Fougeray S, Angeli V, Fontaine J, Chinetti G, Gosset P, Delerive P, Maliszewski C, Capron M, Staels B, Moser M, Trottein F (2000) Peroxisome proliferator-activated receptor gamma activators inhibit interleukin-12 production in murine dendritic cells. FEBS Lett 486: 261-266
20. Freeman L, Hewison M, Hughes SV, Evans KN, Hardie D, Means TK, Chakraverty R (2005) Expression of 11beta-hydroxysteroid dehydrogenase type 1 permits regulation of glucocorticoid bioavailability by human dendritic cells. Blood 106: 2042-2049
21. Fritsche J, Mondal K, Ehrnsperger A, Andreesen R, Kreutz M (2003) Regulation of 25-hydroxyvitamin D3-1 alpha-hydroxylase and production of 1 alpha,25-dihydroxyvitamin D3 by human dendritic cells. Blood 102: 3314-3316
22. Fu X, Menke JG, Chen Y, Zhou G, MacNaul KL, Wright SD, Sparrow CP, Lund EG (2001) 27-Hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J Biol Chem 276: 38378-38387
23. Geissmann F, Revy P, Brousse N, Lepelletier Y, Folli C, Durandy A, Chambon P, Dy M (2003) Retinoids regulate survival and antigen presentation by immature dendritic cells. J Exp Med 198: 623-634
24. Geyeregger R, Zeyda M, Bauer W, Kriehuber E, Saemann MD, Zlabinger GJ, Maurer D, Stulnig TM (2007) Liver X receptors regulate dendritic cell phenotype and function through blocked induction of the actin-bundling protein fascin. Blood 109: 4288-4295
25. Gogolak P, Rethi B, Szatmari I, Lanyi A, Dezso B, Nagy L, Rajnavolgyi E (2007) Differentiation of CD1a- and CD1a+ monocyte-derived dendritic cells is biased by lipid environment and PPARgamma. Blood 109: 643-652
26. Gosset P, Charbonnier AS, Delerive P, Fontaine J, Staels B, Pestel J, Tonnel AB, Trottein F (2001) Peroxisome proliferator-activated receptor gamma activators affect the maturation of human monocyte-derived dendritic cells. Eur J Immunol 31: 2857-2865
27. Griffin MD, Kumar R (2003) Effects of 1alpha,25(OH)2D3 and its analogs on dendritic cell function. J Cell Biochem 88: 323-326
28. Griffin MD, Lutz W, Phan VA, Bachman LA, McKean DJ, Kumar R (2001) Dendritic cell modulation by 1alpha,25 dihydroxyvitamin D3 and its analogs: a vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo. Proc Natl Acad Sci USA 98: 6800-6805
29. Grohmann U, Volpi C, Fallarino F, Bozza S, Bianchi R, Vacca C, Orabona C, Belladonna ML, Ayroldi E, Nocentini G, Boon L, Bistoni F, Fioretti MC, Romani L, Riccardi C, Puccetti P (2007) Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat Med 13: 579-586
30. Hackstein H, Thomson AW (2004) Dendritic cells: emerging pharmacological targets of immunosuppressive drugs. Nat Rev Immunol 4: 24-34
31. Hammad H, de Heer HJ, Soullie T, Angeli V, Trottein F, Hoogsteden HC, Lambrecht BN (2004) Activation of peroxisome proliferator-activated receptor-gamma in dendritic cells inhibits the development of eosinophilic airway inflammation in a mouse model of asthma. Am J Pathol 164: 263-271
32. Hammond KJ, Kronenberg M (2003) Natural killer T cells: natural or unnatural regulators of autoimmunity? Curr Opin Immunol 15: 683-689
33. Harizi H, Gualde N (2005) The impact of eicosanoids on the crosstalk between innate and adaptive immunity: the key roles of dendritic cells. Tissue Antigens 65: 507-514
34. Hewison M, Freeman L, Hughes SV, Evans KN, Bland R, Eliopoulos AG, Kilby MD, Moss PA, Chakraverty R (2003) Differential regulation of vitamin D receptor and its ligand in human monocyte-derived dendritic cells. J Immunol 170: 5382-5390
35. Huang JT, Welch JS, Ricote M, Binder CJ, Willson TM, Kelly C, Witztum JL, Funk CD, Conrad D, Glass CK (1999) Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 400: 378-382
36. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY (2004) Retinoic acid imprints gut-homing specificity on T cells. Immunity 21: 527-538
37. Klotz L, Dani I, Edenhofer F, Nolden L, Evert B, Paul B, Kolanus W, Klockgether T, Knolle P, Diehl L (2007) Peroxisome proliferator-activated receptor gamma control of dendritic cell function contributes to development of CD4+ T cell anergy. J Immunol 178: 2122-2131
38. Le Naour F, Hohenkirk L, Grolleau A, Misek DE, Lescure P, Geiger JD, Hanash S, Beretta L (2001) Profiling changes in gene expression during differentiation and maturation of monocyte-derived dendritic cells using both oligonucleotide microarrays and proteomics. J Biol Chem 276: 17920-17931
39. Lefebvre P, Chinetti G, Fruchart JC, Staels B (2006) Sorting out the roles of PPAR alpha in energy metabolism and vascular homeostasis. J Clin Invest 116: 571-580
40. Leslie DS, Dascher CC, Cembrola K, Townes MA, Hava DL, Hugendubler LC, Mueller E, Fox L, Roura-Mir C, Moody DB, Vincent MS, Gumperz JE, Illarionov PA, Besra GS, Reynolds CG, Brenner MB (2008) Serum lipids regulate dendritic cell CD1 expression and function. Immunology (doi:10.1111/j.1365-2567.2008. 02842.x)
41. Mangelsdorf DJ, Evans RM (1995) The RXR heterodimers and orphan receptors. Cell 83: 841-850
42. Meunier L, Bohjanen K, Voorhees JJ, Cooper KD (1994) Retinoic acid upregulates human Langerhans cell antigen presentation and surface expression of HLA-DR and CD11c, a beta 2 integrin critically involved in T-cell activation. J Invest Dermatol 103: 775-779
43. Mohty M, Morbelli S, Isnardon D, Sainty D, Arnoulet C, Gaugler B, Olive D (2003) All-trans retinoic acid skews monocyte differentiation into interleukin-12-secreting dendritic-like cells. Br J Haematol 122: 829-836
44. Mora JR, Iwata M, Eksteen B, Song SY, Junt T, Senman B, Otipoby KL, Yokota A, Takeuchi H, Ricciardi-Castagnoli P, Rajewsky K, Adams DH, von Andrian UH (2006) Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314: 1157-1160
45. Moser M, De Smedt T, Sornasse T, Tielemans F, Chentoufi AA, Muraille E, Van Mechelen M, Urbain J, Leo O (1995) Glucocorticoids down-regulate dendritic cell function in vitro and in vivo. Eur J Immunol 25: 2818-2824
46. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, Cheroutre H (2007) Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317: 256-260
47. Nagler-Anderson C, Shi HN (2001) Peripheral nonresponsiveness to orally administered soluble protein antigens. Crit Rev Immunol 21: 121-131
48. Nagy L, Tontonoz P, Alvarez JG, Chen H, Evans RM (1998) Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 93: 229-240
49. Nencioni A, Grunebach F, Schmidt SM, Muller MR, Boy D, Patrone F, Ballestrero A, Brossart P (2008) The use of dendritic cells in cancer immunotherapy. Crit Rev Oncol Hematol 65: 191-199
50. Nencioni A, Grunebach F, Zobywlaski A, Denzlinger C, Brugger W, Brossart P (2002) Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor gamma. J Immunol 169: 1228-1235
51. Ni K, O'Neill HC (1997) The role of dendritic cells in T cell activation. Immunol Cell Biol 75: 223-230
52. Niederreither K, Subbarayan V, Dolle P, Chambon P (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21: 444-448
53. Norbury CC (2006) Drinking a lot is good for dendritic cells. Immunology 117: 443-451
54. Okuda K, Usui E, Ohyama Y (1995) Recent progress in enzymology and molecular biology of enzymes involved in vitamin D metabolism. J Lipid Res 36: 1641-1652
55. Pascual G, Fong AL, Ogawa S, Gamliel A, Li AC, Perissi V, Rose DW, Willson TM, Rosenfeld MG, Glass CK (2005) A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 437: 759-763
56. Penna G, Adorini L (2000) 1 Alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol 164: 2405-2411
57. Piemonti L, Monti P, Allavena P, Sironi M, Soldini L, Leone BE, Socci C, Di Carlo V (1999) Glucocorticoids affect human dendritic cell differentiation and maturation. J Immunol 162: 6473-6481
58. Piemonti L, Monti P, Sironi M, Fraticelli P, Leone BE, Dal Cin E, Allavena P, Di Carlo V (2000) Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol 164: 4443-4451
59. Rea D, van Kooten C, van Meijgaarden KE, Ottenhoff TH, Melief CJ, Offringa R (2000) Glucocorticoids transform CD40-triggering of dendritic cells into an alternative activation pathway resulting in antigen-presenting cells that secrete IL-10. Blood 95: 3162-3167
60. Sallusto F, Lanzavecchia A (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/ macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179: 1109-1118
61. Sandell LL, Sanderson BW, Moiseyev G, Johnson T, Mushegian A, Young K, Rey JP, Ma JX, Staehling-Hampton K, Trainor PA (2007) RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development. Genes Dev 21: 1113-1124
62. Saurer L, McCullough KC, Summerfield A (2007) In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J Immunol 179: 3504-3514
63. Savina A, Amigorena S (2007) Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 219: 143-156
64. Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, Hagens K, Modlin RL, Brinkmann V, Kaufmann SH (2003) Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 9: 1039-1046
65. Seckl JR, Walker BR (2001) Minireview: 11beta-hydroxysteroid dehydrogenase type 1 - a tissue-specific amplifier of glucocorticoid action. Endocrinology 142: 1371-1376
66. Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7: 19-30
67. Sigmundsdottir H, Pan J, Debes GF, Alt C, Habtezion A, Soler D, Butcher EC (2007) DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat Immunol 8: 285-293
68. Steinman R, Cohn Z (1973) Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med 137: 1142-1162
69. Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M, Mora JR, Belkaid Y (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
70. Szatmari I, Gogolak P, Im JS, Dezso B, Rajnavolgyi E, Nagy L (2004) Activation of PPARgamma specifies a dendritic cell subtype capable of enhanced induction of iNKT cell expansion. Immunity 21: 95-106
71. Szatmari I, Pap A, Ruhl R, Ma JX, Illarionov PA, Besra GS, Rajnavolgyi E, Dezso B, Nagy L (2006a) PPARgamma controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J Exp Med 203: 2351-2362
72. Szatmari I, Torocsik D, Agostini M, Nagy T, Gurnell M, Barta E, Chatterjee K, Nagy L (2007) PPARgamma regulates the function of human dendritic cells primarily by altering lipid metabolism. Blood 110: 3271-3280
73. Szatmari I, Vamosi G, Brazda P, Balint BL, Benko S, Szeles L, Jeney V, Ozvegy-Laczka C, Szanto A, Barta E, Balla J, Sarkadi B, Nagy L (2006b) Peroxisome proliferator-activated receptor gamma-regulated ABCG2 expression confers cytoprotection to human dendritic cells. J Biol Chem 281: 23812-23823
74. Tsuji M (2006) Glycolipids and phospholipids as natural CD1d-binding NKT cell ligands. Cell Mol Life Sci 63: 1889-1898
75. Underwood BA, Arthur P (1996) The contribution of vitamin A to public health. FASEB J 10: 1040-1048
76. van den Elzen P, Garg S, Leon L, Brigl M, Leadbetter EA, Gumperz JE, Dascher CC, Cheng TY, Sacks FM, Illarionov PA, Besra GS, Kent SC, Moody DB, Brenner MB (2005) Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 437: 906-910
77. van Etten E, Mathieu C (2005) Immunoregulation by 1,25-dihydroxyvitamin D3: basic concepts. J Steroid Biochem Mol Biol 97: 93-101
78. Villadangos JA, Schnorrer P (2007) Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 7: 543-555
79. Willcox BE, Willcox CR, Dover LG, Besra G (2007) Structures and functions of microbial lipid antigens presented by CD1. Curr Top Microbiol Immunol 314: 73-110
80. Willson TM, Lambert MH, Kliewer SA (2001) Peroxisome proliferator- activated receptor gamma and metabolic disease. Annu Rev Biochem 70: 341-367
81. Wu L, Liu YJ (2007) Development of dendritic-cell lineages. Immunity 26: 741-750
82. Zapata-Gonzalez F, Rueda F, Petriz J, Domingo P, Villarroya F, de Madariaga A, Domingo JC (2007) 9-cis-Retinoic acid (9cRA), a retinoid X receptor (RXR) ligand, exerts immunosuppressive effects on dendritic cells by RXR-dependent activation: inhibition of peroxisome proliferator-activated receptor gamma blocks some of the 9cRA activities, and precludes them to mature phenotype development. J Immunol 178: 6130-6139
83. Zelcer N, Tontonoz P (2006) Liver X receptors as integrators of metabolic and inflammatory signaling. J Clin Invest 116: 607-614
84. Zenke M, Hieronymus T (2006) Towards an understanding of the transcription factor network of dendritic cell development. Trends Immunol 27: 140-145