IFN-γ and STAT1 arrest monocyte migration and modulate RAC/CDC42 pathways

Journal of Immunology

Volumn 180, Issue 12, 2008, Pages 8057-8065

  Hu, Yang ^a,d   Hu, Xiaoyu ^a   Boumsell, Laurence ^b   Ivashkiv, Lionel B ^a,c  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b INSERM   (France)

^c Weill Cornell Medical Center   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE 2; GAMMA INTERFERON; MONOCYTE CHEMOTACTIC PROTEIN 1; P21 ACTIVATED KINASE; PROTEIN CDC42; RAC PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; ACTIN; CCL2 PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN; STAT1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ACTIN FILAMENT; ARTICLE; CELL MIGRATION; CELL POLARITY; CYTOSKELETON; ENZYME ACTIVITY; IMMUNOMODULATION; MOLECULAR DYNAMICS; MONOCYTE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; LEUKOCYTE MIGRATION INHIBITION TEST; METABOLISM; MOUSE; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL MIGRATION INHIBITION; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOTAXIS, LEUKOCYTE; GENE EXPRESSION REGULATION; HUMANS; INTERFERON TYPE II; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MONOCYTES; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 50949121438     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.12.8057     Document Type: Article

References (54)

1. Tacke, R, and G. J. Randolph. 2006. Migratory fate and differentiation of blood monocyte subsets. Immunobiology 211: 609-618.
2. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82.
3. Rot, A., and U. H. von Andrian. 2004. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22: 891-928.
4. Ludewig, B., and J. D. Laman. 2004. The in and out of monocytes in atherosclerotic plaques: balancing inflammation through migration. Proc. Nail. Acad. Sci. USA 101: 11529-11530.
5. Rotta, G., E. W. Edwards, S. Sangaletti, C. Bennett, S. Ronzoni, M. P. Colombo, R. M. Steinman, G. J. Randolph, and M. Rescigno. 2003. Lipopolysaccharide or whole bacteria block the conversion of inflammatory monocytes into dendritic cells in vivo. J. Exp. Med. 198: 1253-1263.
6. Schneider, H., J. Downey, A. Smith, B. H. Zinselmeyer, C. Rush, J. M. Brewer, B. Wei, N. Hogg, P. Garside, and C. E. Rudd. 2006. Reversal of the TCR stop signal by CTLA-4. Science 313: 1972-1975.
7. Llodra, J., V. Angeli, J. Liu, E. Trogan, E. A. Fisher, and G. J. Randolph. 2004. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc. Natl. Acad. Sci. USA 101: 11779-11784.
8. Sica, A., A. Saccani, A. Borsatti, C. A. Power, T. N. Wells, W. Luini, N. Polentarutti, S. Sozzani, and A. Mantovani. 1997. Bacterial lipopolysaccharide rapidly inhibits expression of C-C chemokine receptors in human monocytes. J. Exp. Med. 185: 969-974.
9. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferon-γ. an overview of signals, mechanisms and functions. J. Leukocyte Biol. 75: 163-189.
10. Bettelli, E., M. Oukka, and V. K. Kuchroo. 2007. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8: 345-350.
11. Hu, X., H. H. Ho, O. Lou, C. Hidaka, and L. B. Ivashkiv. 2005. Homeostatic role of interferons conferred by inhibition of IL-1-mediated inflammation and tissue destruction. J. Immunol. 175: 131-138.
12. Manoury-Schwartz, B., G. Chiocchia, N. Bessis, O. Abehsira-Amar, F. Batteux, S. Muller, S. Huang, M. C. Boissier, and C. Fournier. 1997. High susceptibility to collagen-induced arthritis in mice lacking IFN-γ receptors. J. Immunol. 158: 5501-5506.
13. Vermeire, K., H. Heremans, M. Vandeputte, S. Huang, A. Billiau, and P. Matthys. 1997. Accelerated collagen-induced arthritis in IFN-γ receptor-deficient mice. J. Immunol. 158: 5507-5513.
14. Guedez, Y. B., K. B. Whittington, J. L. Clayton, L. A. Joosten, F. A. van de Loo. W. B. van den Berg, and E. F. Rosloniec. 2001. Genetic ablation of interferon-γ up-regulates interleukin-1β expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum. 44: 2413-2424.
15. Krakowski, M., and T. Owens. 1996. Interferon-γ confers resistance to experimental allergic encephalomyelitis. Eur. J. Immunol. 26: 1641-1646.
16. Willenborg, D. Q., S. Fordham, C. C. Bernard, W. B. Cowden, and 1. A. Ramshaw. 1996. IFN-γ plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157: 3223-3227.
17. Kelchtermans, H., S. Struyf, B. De Klerck, T. Mitera, M. Alen, L. Geboes, M. Van Balen, C. Dillen, W. Put, C. Gysemans, et al. 2007. Protective role of IFN-γ in collagen-induced arthritis conferred by inhibition of mycobacteria-in-duced granulocyte chemotactic protein-2 production. J. Leukocyte Biol. 81: 1044-1053.
18. Bettelli, E., B. Sullivan, S. J. Szabo, R. A. Sobel, L. H. Glimcher, and V. K. Kuchroo. 2004. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 200: 79-87.
19. Wu, X., W. Hou, S. Sun, E. Bi, Y. Wang, M. Shi, J. Zang, C. Dong, and B. Sun. 2006. Novel function of IFN-γ: negative regulation of dendritic cell migration and T cell priming. J. Immunol. 177: 934-943.
20. Robson, R. L., R. M. McLoughlin, J. Wilowski, P. Loetscher, T. S. Wilkinson, S. A. Jones, and N. Topley. 2001. Differential regulation of chemokine production in human peritoneal mesothelial cells: IFN-γ controls neutrophil migration across the mesothelium in vitro and in vivo. J. Immunol. 167: 1028-1038.
21. Melrose, J., N. Tsurushita, G. Liu, and E. L. Berg. 1998. IFN-γ inhibits activation-induced expression of E- and P-selectin on endothelial cells. J. Immunol. 161: 2457-2464.
22. Granstein, R. D., M. R. Deak, S. L. Jacques, R. J. Margolis, T. J. Flotte, D. Whitaker, F. H. Long, and E. P. Amento. 1989. The systemic administration of γ interferon inhibits collagen synthesis and acute inflammation in a murine skin wounding model. J. Invest. Dermatol. 93: 18-27.
23. Oliveira, I. C, P. J. Sciavolino, T. H. Lee, and J. Vilcek. 1992. Downregulation of interleukin 8 gene expression in human fibroblasts: unique mechanism of transcriptional inhibition by interferon. Proc. Nail. Acad. Sci. USA 89: 9049-9053.
24. Kopydlowski, K. M., C. A. Salkowski, M. J. Cody, N. van Rooijen, J. Major, T. A. Hamilton, and S. N. Vogel. 1999. Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J. Immunol. 163: 1537-1544.
25. van der Pouw Kraan, T. C, F. A. van Gaalen, P. V. Kasperkovitz, N. L. Verbeet, T. J. Smeets, M. C. Kraan, M. Fero, P. P. Tak, T. W. Huizinga, E. Pieterman, et al. 2003. Rheumatoid arthritis is a heterogeneous disease: evidence for differences in the activation of the STAT-1 pathway between rheumatoid tissues. Arthritis Rheum. 48: 2132-2145.
26. Jones, L. S., L. V. Rizzo, R. K. Agarwal, T. K. Tarrant, C. C. Chan, B. Wiggert, and R. R. Caspi. 1997. IFN-γ-deficient mice develop experimental autoimmune uveitis in the context of a deviant effector response. J. Immunol. 158: 5997-6005.
27. Wu, H. J., H. Sawaya, B. Binstadt, M. Brickelmaier, A. Blasius, L. Gorelik, U. Mahmood, R. Weissleder, J. Carulli, C. Benoist, and D. Mathis. 2007. Inflammatory arthritis can be reined in by CpG-induced DC NK cell cross talk. J. Exp. Med. 204: 1911-1922.
28. Mueller, S. N., K. A. Hosiawa-Meagher, B. T. Konieczny, B. M. Sullivan, M. F. Bachmann, R. M. Locksley R. Ahmed, and M. Matloubian. 2007. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 317: 670-674.
29. Williams, A. S., P. J. Richards, E. Thomas, S. Cany, M. A. Nowell. R. M. Goodfellow, C. M. Dent, B. D. Williams, S. A. Jones, and N. Topley. 2007. Interferon-γ protects against the development of structural damage in experimental arthritis by regulating polymorphonuclear neutrophil influx into diseased joints. Arthritis Rheum. 56: 2244-2254.
30. Delaire, S., C. Billard, R. Tordjman, A. Chedotal, A. Elhabazi, A. Bensussan, and L. Boumsell. 2001. Biological activity of soluble CD100: II. Soluble CD100, similarly to H-SemaIII, inhibits immune cell migration. J. Immunol. 166: 4348-4354.
31. Ho, H. H., and L. B. Ivashkiv. 2006. Role of STAT3 in type I interferon responses: negative regulation of STAT1-dependent inflammatory gene activation. J. Biol. Chem. 281: 14111-14118.
32. Hu, Y., and L. B. Ivashkiv. 2006. Costimulation of chemokine receptor signaling by matrix metalloproteinase-9 mediates enhanced migration of IFN-α dendritic cells. J. Immunol. 176: 6022-6033.
33. Wu, Y., P. Stabach, M. Michaud, and J. A. Madri. 2005. Neutrophils lacking platelet-endothelial cell adhesion molecule-1 exhibit loss of directionality and motility in CXCR2-mediated chemotaxis. J. Immunol. 175: 3484-3491.
34. Ahmed, S. T., A. Mayer, J. D. Ji, and L. B. Ivashkiv. 2002. Inhibition of IL-6 signaling by a p38-dependent pathway occurs in the absence of new protein synthesis. J. Leukocyte Biol. 72: 154-162.
35. Levy, D. E., and J. E. Darnell, Jr. 2002. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3: 651-662.
36. Mellado, M., J. M. Rodriguez-Frade, S. Manes, and A. C. Martinez. 2001. Chemokine signaling and functional responses: the role of receptor dimerization and TK pathway activation. Annu. Rev. Immunol. 19: 397-421.
37. Lefkowitz, R. J., and S. K. Shenoy. 2005. Transduction of receptor signals by β-arrestins. Science 308: 512-517.
38. Foger, N., L. Rangell, D. M. Danilenko, and A. C. Chan. 2006. Requirement for eoronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 313: 839-842.
39. Pollard, T. D., and G. G. Borisy. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
40. Tsuboi, S. 2006. A complex of Wiskott-AIdrich syndrome protein with mammalian verprolins plays an important role in monocyte chemotaxis. J. Immunol. 176: 6576-6585.
41. Meili, R., and R. A. Firtel. 2003. Two poles and a compass. Cell 114: 153-156.
42. Jaffe, A. B., and A. Hall. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21: 247-269.
43. Suzuki, K., M. C. Wilkes, N. Garamszegi, M. Edens, and E. B. Leof. 2007. Transforming growth factor β signaling via Ras in mesenchymal cells requires p21-activated kinase 2 for extracellular signal-regulated kinase-dependent transcriptional responses. Cancer Res. 67: 3673-3682.
44. Wang, S. E., I. Shin, F. Y. Wu, D. B. Friedman, and C. L. Arteaga. 2006. HER2/Neu (ErbB2) signaling to Racl-Pakl is temporally and spatially modulated by transforming growth factor β. Cancer Res. 66: 9591-9600.
45. Ulloa, L., J. Doody, and J. Massague. 1999. Inhibition of transforming growth factor-β/SMAD signalling by the interferon-γ/STAT pathway. Nature 397: 710-713.
46. Letterio, J. J., and A. B. Roberts. 1998. Regulation of immune responses by TGF-β. Annu. Rev. Immunol. 16: 137-161.
47. Klesney-Tait, J., I. R. Turnbull, and M. Colonna. 2006. The TREM receptor family and signal integration. Nat. Immunol. 7: 1266-1273.
48. Raptis, S. Z., S. D. Shapiro, P. M. Simmons, A. M. Cheng, and C. T. Pham. 2005. Serine protease cathepsin G regulates adhesion-dependent neutrophil effector functions by modulating integrin clustering. Immunity 22: 679-691.
49. Zhang, H., F. Meng, C. L. Chu, T. Takai, and C. A. Lowell. 2005. The Src family kinases Hck and Fgr negatively regulate neutrophil and dendritic cell chemokine signaling via PIR-B. Immunity 22: 235-246.
50. McLoughlin, R. M., J. Witowski, R. L. Robson, T. S. Wilkinson, S. M. Hunt, A. S. Williams, J. D. Williams, S. Rose-John, S. A. Jones, and N. Topley. 2003. Interplay between IFN-γ and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J. Clin. Invest. 112: 598-607.
51. Hurst, S. M., T. S. Wilkinson, R. M. McLoughlin, S. Jones, S. Horiuchi, N. Yamamoto, S. Rose-John, G. M. Fuller, N. Topley, and S. A. Jones. 2001.11-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 14: 705-714.
52. Yamashita, S., C. Miyagi, T. Fukada, N. Kagara, Y. S. Che, and T. Hirano. 2004. Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gas-trula organizer. Nature 429: 298-302.
53. Dechow, T. N., L. Pedranzini, A. Leitch, K. Leslie, W. L. Gerald, I. Linkov, and J. F. Bromberg. 2004. Requirement of matrix metalloproteinase-9 for the transformation of human mammary epithelial cells by Stat3-C. Proc. Natl. Acad. Sci. USA 101: 10602-10607.
54. Harada, T., V. Kyttaris, Y. Li, Y. T. Juang, Y. Wang, and G. C. Tsokos. 2007. Increased expression of STAT3 in SLE T cells contributes to enhanced chemo-kine-mediated cell migration. Autoimmunity 40: 1-8.