TGF-β1 disrupts endotoxin signaling in microglial cells through Smad3 and MAPK pathways

Journal of Immunology

Volumn 173, Issue 2, 2004, Pages 962-968

  Le, Yingying ^a   Iribarren, Pablo ^a   Gong, Wanghua ^b   Cui, Yuhong ^a   Zhang, Xia ^a   Wang, Ji Ming ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ENDOTOXIN; FORMYLPEPTIDE; FORMYLPEPTIDE RECEPTOR 2; FORMYLPEPTIDE RECEPTOR LIKE 1; G PROTEIN COUPLED RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROTEIN P300; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN; EP300 PROTEIN, MOUSE; FORMYL PEPTIDE RECEPTOR 2, MOUSE; FORMYLPEPTIDE RECEPTOR; LIPOPOLYSACCHARIDE; NUCLEAR PROTEIN; SMAD3 PROTEIN, MOUSE; TGFB1 PROTEIN, HUMAN; TGFB1 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; DOSE RESPONSE; GENETIC TRANSFECTION; MICROGLIA; NEUROPROTECTION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; METABOLISM; MOUSE;

ANIMALS; DNA-BINDING PROTEINS; E1A-ASSOCIATED P300 PROTEIN; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; NUCLEAR PROTEINS; RECEPTORS, FORMYL PEPTIDE; SMAD3 PROTEIN; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 3142729969     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.2.962     Document Type: Article

References (44)

1. Guha, M., and N. Mackman. 2001. LPS induction of gene expression in human monocytes. Cell. Signal. 13:85.
2. Barron, K. D. 2003. Microglia: history, cytology, and reactions. J. Neurol. Sci. 207:98.
3. Nelson, P. T., L. A. Soma, and E. Lavi. 2002. Microglia in diseases of the central nervous system. Ann. Med. 34:491.
4. Lacroix, S., D. Feinstein, and S. Rivest. 1998. The bacterial endotoxin lipopolysaccharide has the ability to target the brain in upregulating its membrane CD14 receptor within specific cellular populations. Brain Pathol. 8:625.
5. Hausler, K. G., M. Prinz, C. Nolte, J. R. Weber, R. R. Schumann, H. Kettenmann, and U. K. Hanisch. 2002. Interferon-γ differentially modulates the release of cytokines and chemokines in lipopolysaccharide- and pneumococcal cell wall-stimulated mouse microglia and macrophages. Eur. J. Neurosci. 16:2113.
6. Cui, Y. H., Y. Le, W. Gong, P. Proost, J. Van Damme, W. J. Murphy, and J. M. Wang. 2002. Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells. J. Immunol. 168:434.
7. Liang, T. S., J. M. Wang, P. M. Murphy, and J. L. Gao. 2000. Serum amyloid A is a chemotactic agonist at FPR2, a low-affinity N-formylpeptide receptor on mouse neutrophils. Biochem. Biophys. Res. Commun. 270:331.
8. Tiffany, H. L., M. C. Lavigne, Y. H. Cui, J. M. Wang, T. L. Leto, J. L. Gao, and P. M. Murphy. 2001. Amyloid-β induces chemotaxis and oxidant stress by acting at formylpeptide receptor 2, a G protein-coupled receptor expressed in phagocytes and brain. J. Biol. Chem. 276:23645.
9. Hu, J. Y., Y. Le, W. Gong, N. M. Dunlop, J. L. Gao, P. M. Murphy, and J. M. Wang. 2001. Synthetic peptide MMK-1 is a highly specific chemotactic agonist for leukocyte FPRL1. J. Leukocyte Biol. 70:155.
10. Letterio, J. J., and A. B. Roberts. 1998. Regulation of immune responses by TGF-β. Annu. Rev. Immunol. 16:137.
11. Shull, M. M., I. Ormsby, A. B. Kier, S. Pawlowski, R. J. Diebold, M. Yin, R. Allen, C. Sidman, G. Proetzel, D. Calvin, et al. 1992. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359:693.
12. Kulkarni, A. B., C. G. Huh, D. Becker, A. Geiser, M. Lyght, K. C. Flanders, A. B. Roberts, M. B. Sporn, J. M. Ward, and S. Karlsson. 1993. Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA 90:770.
13. Ulich, T. R., S. Yin, K. Guo, E. S. Yi, D. Remick, and J. del Castillo. 1991. Intratracheal injection of endotoxin and cytokines. II. Interleukin-6 and transforming growth factor β inhibit acute inflammation. Am. J. Pathol. 138:1097.
14. Perrella, M. A., C. M. Hsieh, W. S. Lee, S. Shieh, J. C. Tsai, C. Patterson, C. J. Lowenstein, N. C. Long, E. Haber, S. Shore, and M. E. Lee. 1996. Arrest of endotoxin-induced hypotension by transforming growth factor β1. Proc. Natl. Acad. Sci. USA 93:2054.
15. Imai, K., A. Takeshita, and S. Hanazawa. 2000. Transforming growth factor-β inhibits lipopolysaccharide-stimulated expression of inflammatory cytokines in mouse macrophages through downregulation of activation protein 1 and CD14 receptor expression. Infect. Immun. 68:2418.
16. Shen, W., P. Proost, B. Li, W. Gong, Y. Le, R. Sargeant, P. M. Murphy, J. Van Damme, and J. M. Wang. 2000. Activation of the chemotactic peptide receptor FPRL1 in monocytes phosphorylates the chemokine receptor CCR5 and attenuates cell responses to selected chemokines. Biochem. Biophys. Res. Commun. 272:276.
17. Zhang, Y., X. Feng, R. We, and R. Derynck. 1996. Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature 383:168.
18. Suzukawa, K., and N. H. Colburn. 2002. AP-1 transrepressing retinoic acid does not deplete coactivators or AP-1 monomers but may target specific Jun or Fos containing dimers. Oncogene 21:2181.
19. Ferrari, D., P. Chiozzi, S. Falzoni, S. Hanau, and F. Di Virgilio. 1997. Purinergic modulation of interleukin-1β release from microglial cells stimulated with bacterial endotoxin. J. Exp. Med. 185:579.
20. Iribarren, P., Y.-H. Cui, Y. Le, G. Ying, X. Zhang, W. Gong, and J. M. Wang. 2003. IL-4 down-regulates lipopolysaccharide-induced formyl peptide receptor 2 in murine microglial cells by inhibiting the activation of mitogen-activated protein kinases. J. Immunol. 171:5482.
21. Xiao, Y. Q., K. Malcolm, G. S. Worthen, S. Gardai, W. P. Schiemann, V. A. Fadok, D. L. Bratton, and P. M. Henson. 2002. Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-β. J. Biol. Chem. 277:14884.
22. Kaisho, T., and S. Akira. 2002. Toll-like receptors as adjuvant receptors. Biochim. Biophys. Acta 1589:1.
23. Vaughn, M. W., R. J. Proske, and D. L. Haviland. 2002. Identification, cloning, and functional characterization of a murine lipoxin A4 receptor homologue gene. J. Immunol. 169:3363.
24. Shi, Y., and J. Massague. 2003. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113:685.
25. Feng, X. H., Y. Zhang, R. Y. Wu, and R. Derynck. 1998. The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for smad3 in TGF-β-induced transcriptional activation. Genes Dev. 12:2153.
26. Janknecht, R., N. J. Wells, and T. Hunter. 1998. TGF-β-stimulated cooperation of smad proteins with the coactivators CBP/p300. Genes Dev. 12:2114.
27. Hirsch, E. C., T. Breidert, E. Rousselet, S. Hunot, A. Hartmann, and P. P. Michel. 2003. The role of glial reaction and inflammation in Parkinson's disease. Ann. NY Acad. Sci. 991:214.
28. Minagar, A., P. Shapshak, R. Fujimura, R. Ownby, M. Heyes, and C. Eisdorfer. 2002. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J. Neurol. Sci. 202:13.
29. Pocock, J. M., A. C. Liddle, C. Hooper, D. L. Taylor, C. M. Davenport, and S. C. Morgan. 2002. Activated microglia in Alzheimer's disease and stroke. Ernst Schering Res. Found. Workshop 39:105.
30. 42), in murine microglial cells by TNFα. Neurobiol. Dis. 10:366.
31. Kalaria, R. N. 1999. Microglia and Alzheimer's disease. Curr. Opin. Hematol. 6:15.
32. Akiyama, H., S. Barger, S. Barnum, B. Bradt, J. Bauer, G. M. Cole, N. R. Cooper, P. Eikelenboom, M. Emmerling, B. L. Fiebich, et al. 2000. Inflammation and Alzheimer's disease. Neurobiol. Aging 21:383.
33. Hull, M., K. Lieb, and B. L. Fiebich. 2002. Pathways of inflammatory activation in Alzheimer's disease: potential targets for disease modifying drugs. Curr. Med. Chem. 9:83.
34. Hardy, J., and D. J. Selkoe. 2002. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353.
35. McCartney-Francis, N. L., M. Frazier-Jessen, and S. M. Wahl. 1998. TGF-β: a balancing act. Int. Rev. Immunol. 16:553.
36. Yue, J., and K. M. Mulder. 2000. Activation of the mitogen-activated protein kinase pathway by transforming growth factor-β. Methods Mol. Biol. 142:125.
37. Mulder, K. M. 2000. Role of Ras and Mapks in TGFβ signaling. Cytokine Growth Factor Rev. 11:23.
38. Zhang, G., and S. Ghosh. 2000. Molecular mechanisms of NF-κB activation induced by bacterial lipopolysaccharide through Toll-like receptors. J. Endotoxin Res. 6:453.
39. Haller, D., L. Holt, S. C. Kim, R. F. Schwabe, R. B. Sartor, and C. Jobin. 2003. Transforming growth factor-β1 inhibits non-pathogenic Gram negative bacteria-induced NF-κB recruitment to the interleukin-6 gene promoter in intestinal epithelial cells through modulation of histone acetylation. J. Biol. Chem. 278:23851.
40. Topper, J. N., M. R. DiChiara, J. D. Brown, A. J. Williams, D. Falb, T. Collins, and M. A. Gimbrone, Jr. 1998. CREB binding protein is a required coactivator for Smad-dependent, transforming growth factor β transcriptional responses in endothelial cells. Proc. Natl. Acad. Sci. USA 95:9506.
41. DiChiara, M. R., J. M. Kiely, M. A. Jr. Gimbrone, M. E. Lee, M. A. Perrella, and J. N. Topper. 2000. Inhibition of E-selectin gene expression by transforming growth factor β in endothelial cells involves coactivator integration of Smad and nuclear factor κB-mediated signals. J. Exp. Med. 192:695.
42. Wyss-Coray, T., C. Lin, F. Yan, G. Q. Yu, M. Rohde, L. McConlogue, E. Masliah, and L. Mucke. 2001. TGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice. Nat. Med. 7:612.
43. Frautschy, S. A., F. Yang, L. Calderon, and G. M. Cole. 1996. Rodent models of Alzheimer's disease: rat Aβ infusion approaches to amyloid deposits. Neurobiol. Aging 17:311.
44. 42) is internalized via the G-protein-coupled receptor FPRL1 and forms fibrillar aggregates in macrophages. FASEB J. 15:2454.