Nfkb1 inhibits LPS-induced IFN-β and IL-12 p40 production in macrophages by distinct mechanisms

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Zhao, Xixing ^a   Ross, Erik J ^a   Wang, Yanyan ^a   Horwitz, Bruce H ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CARBOXY TERMINAL TELOPEPTIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN 1; INTERLEUKIN 12P40; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEAR FACTOR KAPPA B SUBUNIT P105; NUCLEAR FACTOR KAPPA B SUBUNIT P50; PROTEIN P105; PROTEIN P50; TRANSCRIPTION FACTOR REL; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; INTERLEUKIN 10; NFKB1 PROTEIN, MOUSE; RAG2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE; IFNB GENE; IL12B GENE; MACROPHAGE; MOUSE; NFKB1 GENE; NONHUMAN; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETROVIRUS; ANALYSIS OF VARIANCE; ANIMAL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MURINAE;

ANALYSIS OF VARIANCE; ANIMALS; DNA-BINDING PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; INTERFERON-BETA; INTERLEUKIN-10; INTERLEUKIN-12 SUBUNIT P40; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, KNOCKOUT; NF-KAPPA B P50 SUBUNIT;

EID: 84863231956     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032811     Document Type: Article

References (36)

1. Grilli M, Chiu JJ, Lenardo MJ, (1993) NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int Rev Cytol 143: 1-62.
2. Cao S, Zhang X, Edwards JP, Mosser DM, (2006) NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J Biol Chem 281: 26041-26050.
3. Cheng CS, Feldman KE, Lee J, Verma S, Huang DB, et al. (2011) The specificity of innate immune responses is enforced by repression of interferon response elements by NF-kappaB p50. Sci Signal 4: ra11.
4. Hagemann T, Lawrence T, McNeish I, Charles KA, Kulbe H, et al. (2008) "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J Exp Med 205: 1261-1268.
5. Porta C, Rimoldi M, Raes G, Brys L, Ghezzi P, et al. (2009) Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci U S A 106: 14978-14983.
6. Tomczak MF, Erdman SE, Davidson A, Wang YY, Nambiar PR, et al. (2006) Inhibition of Helicobacter hepaticus-Induced Colitis by IL-10 Requires the p50/p105 Subunit of NF-kappaB. J Immunol 177: 7332-7339.
7. Tomczak MF, Erdman SE, Poutahidis T, Rogers AB, Holcombe H, et al. (2003) NF-kappa B is required within the innate immune system to inhibit microflora-induced colitis and expression of IL-12 p40. J Immunol 171: 1484-1492.
8. Yang HT, Wang Y, Zhao X, Demissie E, Papoutsopoulou S, et al. (2011) NF-kappaB1 inhibits TLR-induced IFN-beta production in macrophages through TPL-2-dependent ERK activation. J Immunol 186: 1989-1996.
9. Erdman S, Fox JG, Dangler CA, Feldman D, Horwitz BH, (2001) Typhlocolitis in NF-kappa B-deficient mice. J Immunol 166: 1443-1447.
10. Ghosh S, Gifford AM, Riviere LR, Tempst P, Nolan GP, et al. (1990) Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell 62: 1019-1029.
11. Hatada EN, Nieters A, Wulczyn FG, Naumann M, Meyer R, et al. (1992) The ankyrin repeat domains of the NF-kappa B precursor p105 and the protooncogene bcl-3 act as specific inhibitors of NF-kappa B DNA binding. Proc Natl Acad Sci U S A 89: 2489-2493.
12. Inoue J, Kerr LD, Kakizuka A, Verma IM, (1992) I kappa B gamma, a 70 kd protein identical to the C-terminal half of p110 NF-kappa B: a new member of the I kappa B family. Cell 68: 1109-1120.
13. Kieran M, Blank V, Logeat F, Vandekerckhove J, Lottspeich F, et al. (1990) The DNA binding subunit of NF-kappa B is identical to factor KBF1 and homologous to the rel oncogene product. Cell 62: 1007-1018.
14. Liou HC, Nolan GP, Ghosh S, Fujita T, Baltimore D, (1992) The NF-kappa B p50 precursor, p105, contains an internal I kappa B-like inhibitor that preferentially inhibits p50. Embo J 11: 3003-3009.
15. Rice NR, MacKichan ML, Israel A, (1992) The precursor of NF-kappa B p50 has I kappa B-like functions. Cell 71: 243-253.
16. Ghosh S, May MJ, Kopp EB, (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225-260.
17. Beinke S, Robinson MJ, Hugunin M, Ley SC, (2004) Lipopolysaccharide activation of the TPL-2/MEK/extracellular signal-regulated kinase mitogen-activated protein kinase cascade is regulated by IkappaB kinase-induced proteolysis of NF-kappaB1 p105. Mol Cell Biol 24: 9658-9667.
18. Lang V, Janzen J, Fischer GZ, Soneji Y, Beinke S, et al. (2003) betaTrCP-mediated proteolysis of NF-kappaB1 p105 requires phosphorylation of p105 serines 927 and 932. Mol Cell Biol 23: 402-413.
19. Waterfield MR, Zhang M, Norman LP, Sun SC, (2003) NF-kappaB1/p105 regulates lipopolysaccharide-stimulated MAP kinase signaling by governing the stability and function of the Tpl2 kinase. Mol Cell 11: 685-694.
20. Salmeron A, Janzen J, Soneji Y, Bump N, Kamens J, et al. (2001) Direct phosphorylation of NF-kappaB1 p105 by the IkappaB kinase complex on serine 927 is essential for signal-induced p105 proteolysis. J Biol Chem 276: 22215-22222.
21. Heissmeyer V, Krappmann D, Hatada EN, Scheidereit C, (2001) Shared pathways of IkappaB kinase-induced SCF(betaTrCP)-mediated ubiquitination and degradation for the NF-kappaB precursor p105 and IkappaBalpha. Mol Cell Biol 21: 1024-1035.
22. Kang SM, Tran AC, Grilli M, Lenardo MJ, (1992) NF-kappa B subunit regulation in nontransformed CD4+ T lymphocytes. Science 256: 1452-1456.
23. Zhong H, May MJ, Jimi E, Ghosh S, (2002) The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 9: 625-636.
24. Goriely S, Molle C, Nguyen M, Albarani V, Haddou NO, et al. (2006) Interferon regulatory factor 3 is involved in Toll-like receptor 4 (TLR4)- and TLR3-induced IL-12p35 gene activation. Blood 107: 1078-1084.
25. Maruyama S, Sumita K, Shen H, Kanoh M, Xu X, et al. (2003) Identification of IFN regulatory factor-1 binding site in IL-12 p40 gene promoter. J Immunol 170: 997-1001.
26. Masumi A, Tamaoki S, Wang IM, Ozato K, Komuro K, (2002) IRF-8/ICSBP and IRF-1 cooperatively stimulate mouse IL-12 promoter activity in macrophages. FEBS Lett 531: 348-353.
27. Agrawal S, Agrawal A, Doughty B, Gerwitz A, Blenis J, et al. (2003) 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.
28. Dillon S, Agrawal A, Van Dyke T, Landreth G, McCauley L, et al. (2004) 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.
29. Kaiser F, Cook D, Papoutsopoulou S, Rajsbaum R, Wu X, et al. (2009) TPL-2 negatively regulates interferon-beta production in macrophages and myeloid dendritic cells. J Exp Med 206: 1863-1871.
30. Dumitru CD, Ceci JD, Tsatsanis C, Kontoyiannis D, Stamatakis K, et al. (2000) TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103: 1071-1083.
31. Gerondakis S, Morrice N, Richardson IB, Wettenhall R, Fecondo J, et al. (1993) The activity of a 70 kilodalton I kappa B molecule identical to the carboxyl terminus of the p105 NF-kappa B precursor is modulated by protein kinase A. Cell Growth Differ 4: 617-627.
32. Grumont RJ, Gerondakis S, (1994) Alternative splicing of RNA transcripts encoded by the murine p105 NF-kappa B gene generates I kappa B gamma isoforms with different inhibitory activities. Proc Natl Acad Sci U S A 91: 4367-4371.
33. Sanjabi S, Hoffmann A, Liou HC, Baltimore D, Smale ST, (2000) Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc Natl Acad Sci U S A 97: 12705-12710.
34. Wang Y, Rickman BH, Poutahidis T, Schlieper K, Jackson EA, et al. (2008) c-Rel is essential for the development of innate and T cell-induced colitis. J Immunol 180: 8118-8125.
35. Murphy TL, Cleveland MG, Kulesza P, Magram J, Murphy KM, (1995) Regulation of interleukin 12 p40 expression through an NF-kappa B half-site. Mol Cell Biol 15: 5258-5267.
36. Tomczak MF, Gadjeva M, Wang YY, Brown K, Maroulakou I, et al. (2006) Defective activation of ERK in macrophages lacking the p50/p105 subunit of NF-kappaB is responsible for elevated expression of IL-12 p40 observed after challenge with Helicobacter hepaticus. J Immunol 176: 1244-1251.