CCAAT/enhancer binding protein-δ expression by dendritic cells regulates CNS autoimmune inflammatory disease

Journal of Neuroscience

Volumn 31, Issue 48, 2011, Pages 17612-17621

  Tsai, Vicky W W ^a   Mohammad, Mohammad G ^a   Tolhurst, Ornella ^a   Breit, Samuel N ^a   Sawchenko, Paul E ^b   Brown, David A ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN DELTA; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; RECEPTOR ANTIBODY; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOINFLAMMATORY DISEASE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE SEVERITY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MONONUCLEAR CELL; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH17 CELL; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INTERLEUKIN-10; MICE; MICE, KNOCKOUT; MYELIN-ASSOCIATED GLYCOPROTEIN; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; UP-REGULATION;

EID: 82555173846     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3449-11.2011     Document Type: Article

References (62)

1. Alam T, An MR, Papaconstantinou J (1992) Differential expression of three C/EBP isoforms in multiple tissues during the acute phase response. J Biol Chem 267:5021-5024.
2. Arora M, Poe SL, Oriss TB, Krishnamoorthy N, Yarlagadda M, Wenzel SE, Billiar TR, Ray A, Ray P (2010) TLR4/MyD88-induced CD11b(+)Gr-1(int)F4/80(+) non-migratory myeloid cells suppress Th2 effector function in the lung. Mucosal Immunol 3:578-593.
3. Bailey SL, Schreiner B, McMahon EJ, Miller SD (2007) CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4(+) T(H)-17 cells in relapsing EAE. Nat Immunol 8:172-180.
4. Bailey-Bucktrout SL, Caulkins SC, Goings G, Fischer JA, Dzionek A, Miller SD (2008) Cutting edge: central nervous system plasmacytoid dendritic cells regulate the severity of relapsing experimental autoimmune encephalomyelitis. J Immunol 180:6457-6461.
5. Ben-Sasson SZ, Hu-Li J, Quiel J, Cauchetaux S, Ratner M, Shapira I, Dinarello CA, Paul WE (2009) IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc Natl Acad Sci U S A 106:7119-7124.
6. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235-238.
7. Brasel K, De Smedt T, Smith JL, Maliszewski CR (2000) Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood 96:3029-3039.
8. Brown DA, Sawchenko PE (2007) Time course and distribution of inflammatory and neurodegenerative events suggest structural bases for the pathogenesis of experimental autoimmune encephalomyelitis. J Comp Neurol 502:236-260.
9. Brynedal B, Khademi M, Wallström E, Hillert J, Olsson T, Duvefelt K (2010) Gene expression profiling in multiple sclerosis: a disease of the central nervous system, but with relapses triggered in the periphery? Neurobiol Dis 37:613-621.
10. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM, Kaunzner UW, Liu K, Lindquist R, Nussenzweig MC, Steinman RM, McEwen BS (2008) CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol 508:687-710.
11. Cai G, Wang H, Qin Q, Zhang J, Zhu Z, Liu M, Shen Q (2009) Amelioration of myocarditis by HVEM-overexpressing dendritic cells through induction of IL-10-producing cells. Cardiovasc Res 84:425-433.
12. Cardinaux JR, Allaman I, Magistretti PJ (2000) Pro-inflammatory cytokines induce the transcription factors C/EBPbeta and C/EBPdelta in astrocytes. Glia 29:91-97.
13. Cortés-Canteli M, Wagner M, Ansorge W, Pérez-Castillo A (2004) Microarray analysis supports a role for ccaat/enhancer-binding protein-beta in brain injury. J Biol Chem 279:14409-14417.
14. Cua DJ, Groux H, Hinton DR, Stohlman SA, Coffman RL (1999) Transgenic interleukin 10 prevents induction of experimental autoimmune encephalomyelitis. J Exp Med 189:1005-1010.
15. De Biase A, Knoblach SM, Di Giovanni S, Fan C, Molon A, Hoffman EP, Faden AI (2005) Gene expression profiling of experimental traumatic spinal cord injury as a function of distance from impact site and injury severity. Physiol Genomics 22:368-381.
16. Domingues HS, Mues M, Lassmann H, Wekerle H, Krishnamoorthy G (2010) Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One 5:e15531.
17. Ejarque-Ortiz A, Medina MG, Tusell JM, Pérez-González AP, Serratosa J, Saura J (2007) Upregulation of CCAAT/enhancer binding protein beta in activated astrocytes and microglia. Glia 55:178-188.
18. Ejarque-Ortiz A, Gresa-Arribas N, Straccia M, Mancera P, Solá C, Tusell JM, Serratosa J, Saura J (2010) CCAAT/enhancer binding protein delta in microglial activation. J Neurosci Res 88:1113-1123.
19. Fujii S, Nishimura MI, Lotze MT (2005) Regulatory balance between the immune response of tumor antigen-specific T-cell receptor genetransduced CD8 T cells and the suppressive effects of tolerogenic dendritic cells. Cancer Sci 96:897-902.
20. Fujimoto M, Nakano M, Terabe F, Kawahata H, Ohkawara T, Han Y, Ripley B, Serada S, Nishikawa T, Kimura A, Nomura S, Kishimoto T, Naka T (2011) The influence of excessive IL-6 production in vivo on the development and function of Foxp3_regulatory T cells. J Immunol 186:32-40.
21. Gregori S, Tomasoni D, Pacciani V, Scirpoli M, Battaglia M, Magnani CF, Hauben E, Roncarolo MG (2010) Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/ HLA-G pathway. Blood 116:935-944.
22. Greter M, Heppner FL, Lemos MP, Odermatt BM, Goebels N, Laufer T, Noelle RJ, Becher B (2005) Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 11:328-334.
23. Hofstetter HH, Ibrahim SM, Koczan D, Kruse N, Weishaupt A, Toyka KV, Gold R (2005) Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol 237:123-130.
24. Huseby ES, Liggitt D, Brabb T, Schnabel B, Ohlén C, Goverman J (2001) A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J Exp Med 194:669-676.
25. Isaksson M, Ardesjö B, Rönnblom L, Kämpe O, Lassmann H, Eloranta ML, Lobell A (2009) Plasmacytoid DC promote priming of autoimmune Th17 cells and EAE. Eur J Immunol 39:2925-2935.
26. Juan TS, Wilson DR, Wilde MD, Darlington GJ (1993) Participation of the transcription factor C/EBP delta in the acute-phase regulation of the human gene for complement component C3. Proc Natl Acad Sci U S A 90:2584-2588.
27. Kao JY, Zhang M, Miller MJ, Mills JC, Wang B, Liu M, Eaton KA, Zou W, Berndt BE, Cole TS, Takeuchi T, Owyang SY, Luther J (2010) Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138: 1046-1054.
28. Kimura A, Naka T, Kishimoto T (2007) IL-6-dependent and-independent pathways in the development of interleukin 17-producing T helper cells. Proc Natl Acad Sci U S A 104:12099-12104.
29. Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, Kakuta S, Sudo K, Iwakura Y (2006) IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol 177:566-573.
30. Korn T, Reddy J, Gao W, Bettelli E, Awasthi A, Petersen TR, Bäckström BT, Sobel RA, Wucherpfennig KW, Strom TB, Oukka M, Kuchroo VK (2007) Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 13:423-431.
31. Lacorte JM, Beigneux A, Parant M, Chambaz J (1997) Repression of apoCIII gene expression by TNFalpha involves C/EBPdelta/NF-IL6beta via an IL-1 independent pathway. FEBS Lett 415:217-220.
32. Lacorte JM, Ktistaki E, Beigneux A, Zannis VI, Chambaz J, Talianidis I (1997) Activation of CAAT enhancer-binding protein delta (C/EBPdelta) by interleukin-1 negatively influences apolipoprotein C-III expression. J Biol Chem 272:23578-23584.
33. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201:233-240.
34. Lavasani S, Dzhambazov B, Nouri M, Fåk F, Buske S, Molin G, Thorlacius H, Alenfall J, Jeppsson B, Weström B (2010) A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One 5:e9009.
35. Li R, Strohmeyer R, Liang Z, Lue LF, Rogers J (2004) CCAAT/enhancer binding protein delta (C/EBPdelta) expression and elevation in Alzheimer's disease. Neurobiol Aging 25:991-999.
36. Litvak V, Ramsey SA, Rust AG, Zak DE, Kennedy KA, Lampano AE, Nykter M, Shmulevich I, Aderem A (2009) Function of C/EBPdelta in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat Immunol 10:437-443.
37. Liu YW, Chen CC, Tseng HP, Chang WC (2006) Lipopolysaccharideinduced transcriptional activation of interleukin-10 is mediated by MAPK-and NF-kappaB-induced CCAAT/enhancer-binding protein delta in mouse macrophages. Cell Signal 18:1492-1500.
38. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H, Langer-Gould A, Strober S, Cannella B, Allard J, Klonowski P, Austin A, Lad N, Kaminski N, Galli SJ, Oksenberg JR, Raine CS, Heller R, Steinman L (2002) Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 8:500-508.
39. Lu YC, Kim I, Lye E, Shen F, Suzuki N, Suzuki S, Gerondakis S, Akira S, Gaffen SL, Yeh WC, Ohashi PS (2009) Differential role for c-Rel and C/EBPbeta/ delta in TLR-mediated induction of proinflammatory cytokines. J Immunol 182:7212-7221.
40. Matzinger P (2002) The danger model: a renewed sense of self. Science 296:301-305.
41. McCarter MD, Baumgartner J, Escobar GA, Richter D, Lewis K, Robinson W, Wilson C, Palmer BE, Gonzalez R (2007) Immunosuppressive dendritic and regulatory T cells are upregulated in melanoma patients. Ann Surg Oncol 14:2854-2860.
42. Monti P, Leone BE, Zerbi A, Balzano G, Cainarca S, Sordi V, Pontillo M, Mercalli A, Di Carlo V, Allavena P, Piemonti L (2004) Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10highIL-12low regulatory dendritic cell. J Immunol 172:7341-7349.
43. Naik SH, O'Keeffe M, Proietto A, Shortman HH, Wu L (2010) CD8+, CD8-, and plasmacytoid dendritic cell generation in vitro using flt3 ligand. Methods Mol Biol 595:167-176.
44. O'Farrell AM, Liu Y, Moore KW, Mui AL (1998) IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and-independent pathways.EMBOJ 17:1006-1018.
45. Okazaki K, Li J, Yu H, Fukui N, Sandell LJ (2002) CCAAT/enhancerbinding proteins beta and delta mediate the repression of gene transcription of cartilage-derived retinoic acid-sensitive protein induced by interleukin-1 beta. J Biol Chem 277:31526-31533.
46. Poncini CV, Giménez G, Pontillo CA, Alba-Soto CD, de Isola EL, Piazzòn I, Cappa SM (2010) Central role of extracellular signal-regulated kinase and Toll-like receptor 4 in IL-10 production in regulatory dendritic cells induced by Trypanosoma cruzi. Mol Immunol 47:1981-1988.
47. Reyes TM, Walker JR, DeCino C, Hogenesch JB, Sawchenko PE (2003) Categorically distinct acute stressors elicit dissimilar transcriptional profiles in the paraventricular nucleus of the hypothalamus. J Neurosci 23:5607-5616.
48. Riveros C, Mellor D, Gandhi KS, McKay FC, Cox MB, Berretta R, Vaezpour SY, Inostroza-Ponta M, Broadley SA, Heard RN, Vucic S, Stewart GJ, Williams DW, Scott RJ, Lechner-Scott J, Booth DR, Moscato P (2010) A transcription factor map as revealed by a genome-wide gene expression analysis of whole-blood mRNA transcriptome in multiple sclerosis. PLoS One 5:e14176.
49. Ruddy MJ, Wong GC, Liu XK, Yamamoto H, Kasayama S, Kirkwood KL, Gaffen SL (2004) Functional cooperation between interleukin-17 and tumor necrosis factor-alpha is mediated by CCAAT/enhancer-binding protein family members. J Biol Chem 279:2559-2567.
50. Rutella S, Danese S, Leone G (2006) Tolerogenic dendritic cells: cytokine modulation comes of age. Blood 108:1435-1440.
51. Sandhir R, Berman NE (2010) Age-dependent Response of CCAAT/Enhancer Binding Proteins following Traumatic Brain Injury in Mice. Neurochem Int 56:188-193.
52. Schwartz M, Shechter R (2010) Systemic inflammatory cells fight off neurodegenerative disease. Nat Rev Neurol 6:405-410.
53. Shen F, Hu Z, Goswami J, Gaffen SL (2006) Identification of common transcriptional regulatory elements in interleukin-17 target genes. J Biol Chem 281:24138-24148.
54. Steiner GE, Newman ME, Paikl D, Stix U, Memaran-Dagda N, Lee C, Marberger MJ (2003) Expression and function of pro-inflammatory interleukin IL-17 and IL-17 receptor in normal, benign hyperplastic, and malignant prostate. Prostate 56:171-182.
55. Sterneck E, Paylor R, Jackson-Lewis V, Libbey M, Przedborski S, Tessarollo L, Crawley JN, Johnson PF (1998) Selectively enhanced contextual fear conditioning in mice lacking the transcriptional regulator CCAAT/enhancer binding protein delta. Proc Natl Acad Sci U S A 95:10908-10913.
56. Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, Esiri MM, Fugger L (2008) Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 172:146-155.
57. Valliéres L, Sawchenko PE (2003) Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity. J Neurosci 23:5197-5207.
58. Vaughan JM, Rivier J, Corrigan AZ, McClintock R, Campen CA, Jolley D, Voglmayr JK, Bardin CW, Rivier C, Vale W (1989) Detection and purification of inhibin using antisera generated against synthetic peptide fragments. Methods Enzymol 168:588-617.
59. Waldner H, Collins M, Kuchroo VK (2004) Activation of antigenpresenting cells by microbial products breaks self tolerance and induces autoimmune disease. J Clin Invest 113:990-997.
60. Wedel A, Ziegler-Heitbrock HW (1995) The C/EBP family of transcription factors. Immunobiology 193:171-185.
61. Yoshiki R, Kabashima K, Sakabe J, Sugita K, Bito T, Nakamura M, Malissen B, Tokura Y (2010) The mandatory role of IL-10-producing and OX40 ligand-expressing mature Langerhans cells in local UVB-induced immunosuppression. J Immunol 184:5670-5677.
62. Zozulya AL, Ortler S, Lee J, Weidenfeller C, Sandor M, Wiendl H, Fabry Z (2009) Intracerebral dendritic cells critically modulate encephalitogenic versus regulatory immune responses in the CNS. J Neurosci 29:140-152.