CCL11 blocks IL-4 and GM-CSF signaling in hematopoietic cells and hinders dendritic cell differentiation via suppressor of cytokine signaling expression

Journal of Leukocyte Biology

Volumn 85, Issue 2, 2009, Pages 289-297

  Stevenson, Nigel J ^a   Addley, Mark R ^c   Ryan, Elizabeth J ^e   Boyd, Caroline R ^a   Carroll, Helen P ^a   Paunovic, Verica ^a   Bursill, Christina A ^c,d   Miller, Helen C ^c   Channon, Keith M ^d   McClurg, Angela E ^a   Armstrong, Marilyn A ^a   Coulter, Wilson A ^b   Greaves, David R ^c   Johnston, James A ^a,b  

^a Infection and Immunity   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Chemokines; Dendritic cells; Monocytes macrophages; Signal transduction

Indexed keywords

CYTOKINE; EOTAXIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 4; STAT5 PROTEIN; STAT6 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; C57BL 6 MOUSE; CELL DIFFERENTIATION; DENDRITIC CELL; ENDOCYTOSIS; HEMATOPOIETIC CELL; HUMAN; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INFLAMMATION; LEUKOCYTE MIGRATION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA ISOLATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CHEMOKINE CCL11; CYTOKINES; DENDRITIC CELLS; ENDOCYTOSIS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HEMATOPOIETIC SYSTEM; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-4; MACROPHAGES; MICE; MICE, INBRED C57BL; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

BOS; MURINAE;

EID: 59649114146     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0708394     Document Type: Article

References (43)

1. Luster, A. D. (1998) Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338, 436-445.
2. Premack, B. A., Schall, T. J. (1996) Chemokine receptors: gateways to inflammation and infection. Nat. Med. 2, 1174-1178.
3. Gerard, C., Rollins, B. J. (2001) Chemokines and disease. Nat. Immunol. 2, 108-115.
4. Menzies-Gow, A., Ying, S., Sabroe, I., Stubbs, V. L., Soler, D., Williams, T. J., Kay, A. B. (2002) Eotaxin (CCL11) and eotaxin-2 (CCL24) induce recruitment of eosinophils, basophils, neutrophils, and macrophages as well as features of early- and late-phase allergic reactions following cutaneous injection in human atopic and nonatopic volunteers. J. Immunol. 169, 2712-2718.
5. Beaulieu, S., Robbiani, D. F., Du, X., Rodrigues, E., Ignatius, R., Wei, Y., Ponath, P., Young, J. W., Pope, M., Steinman, R. M., Mojsov, S. (2002) Expression of a functional eotaxin (CC chemokine ligand 11) receptor CCR3 by human dendritic cells. J. Immunol. 169, 2925-2936.
6. O'Shea, J. J., Gadina, M., Schreiber, R. D. (2002) Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109 (Suppl.), S121-S131.
7. Hamilton, J. A., Anderson, G. P. (2004) GM-CSF biology. Growth Factors 22, 225-231.
8. Takahashi, G. W., Andrews, D. F., Lilly, M. B., Singer, J. W., Alderson, M. R. (1993) Effect of granulocyte-macrophage colony-stimulating factor and interleukin-3 on interleukin-8 production by human neutrophils and monocytes. Blood 81, 357-364.
9. Sakurai, Y., Arai, K., Watanabe, S. (2000) In vitro analysis of STAT5 activation by granulocyte-macrophage colony-stimulating factor. Genes Cells 5, 937-947.
10. Al-Shami, A., Mahanna, W., Naccache, P. H. (1998) Granulocyte-macrophage colony-stimulating factor-activated signaling pathways in human neutrophils. Selective activation of Jak2, Stat3, and Stat5b. J. Biol. Chem. 273, 1058-1063.
11. Faderl, S., Harris, D., Van, Q., Kantarjian, H. M., Talpaz, M., Estrov, Z. (2003) Granulocyte-macrophage colony-stimulating factor (GM-CSF) induces antiapoptotic and proapoptotic signals in acute myeloid leukemia. Blood 102, 630-637.
12. Metcalf, D., Alexander, W. S., Elefanty, A. G., Nicola, N. A., Hilton, D. J., Starr, R., Mifsud, S., Di Rago, L. (1999) Aberrant hematopoiesis in mice with inactivation of the gene encoding SOCS-1. Leukemia 13, 926-934.
13. Noelle, R., Krammer, P. H., Ohara, J., Uhr, J. W., Vitetta, E. S. (1984) Increased expression of Ia antigens on resting B cells: an additional role for B-cell growth factor. Proc. Natl. Acad. Sci. USA 81, 6149-6153.
14. 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 α. J. Exp. Med. 179, 1109-1118.
15. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35.
16. Major, J., Fletcher, J. E., Hamilton, T. A. (2002) IL-4 pretreatment selectively enhances cytokine and chemokine production in lipopolysac-charide- stimulated mouse peritoneal macrophages. J. Immunol. 168, 2456-2463.
17. Hebenstreit, D., Luft, P., Schmiedlechner, A., Duschl, A., Horejs-Hoeck, J. (2005) SOCS-1 and SOCS-3 inhibit IL-4 and IL-13 induced activation of eotaxin-3/CCL26 gene expression in HEK293 cells. Mol. Immunol. 42, 295-303.
18. Losman, J. A., Chen, X. P., Hilton, D., Rothman, P. (1999) Cutting edge: SOCS-1 is a potent inhibitor of IL-4 signal transduction. J. Immunol. 162, 3770-3774.
19. Yoshimura, A., Ohkubo, T., Kiguchi, T., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., Hara, T., Miyajima, A. (1995) A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J. 14, 2816-2826.
20. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Gonda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A., Hilton, D. J. (1997) A family of cytokine-inducible inhibitors of signaling. Nature 387, 917-921.
21. Endo, T. A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H., Miyazaki, T., Leonor, N., Taniguchi, T., Fujita, T., Kanakura, Y., Komiya, S., Yoshimura, A. (1997) A new protein containing an SH2 domain that inhibits Jak kinases. Nature 387, 921-924.
22. Hilton, D. J., Richardson, R. T., Alexander, W. S., Viney, E. M., Willson, T. A., Sprigg, N. S., Starr, R., Nicholson, S. E., Metcalf, D., Nicola, N. A. (1998) Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. USA 95, 114-119.
23. Cohney, S. J., Sanden, D., Cacalano, N. A., Yoshimura, A., Mui, A., Migone, T. S., Johnston, J. A. (1999) SOCS-3 is tyrosine phosphorylated in response to interleukin-2 and suppresses STAT5 phosphorylation and lymphocyte proliferation. Mol. Cell. Biol. 19, 4980-4988.
24. Stoiber, D., Kovarik, P., Cohney, S., Johnston, J. A., Steinlein, P., Decker, T. (1999) Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-γ. J. Immunol. 163, 2640-2647.
25. Soriano, S. F., Hernanz-Falcon, P., Rodriguez-Frade, J. M., De Ana, A. M., Garzón, R., Carvalho-Pinto, C., Vila-Coro, A. J., Zaballos, A., Balomenos, D., Martínez-A, C., Mellado, M. (2002) Functional inactivation of CXC chemokine receptor 4-mediated responses through SOCS3 up-regulation. J. Exp. Med. 196, 311-321.
26. Garzon, R., Soriano, S. F., Rodriguez-Frade, J. M., Gomez, L., Martin De Ana, A., Sanchez-Gomez, M., Martinez, A. C., Mellado, M. (2004) CXCR4-mediated SOCS upregulation inactivates growth hormone function. J. Biol. Chem. 279, 44460-44466.
27. Stevenson, N. J., Haan, S., McClurg, A. E., McGrattan, M. J., Armstrong, M. A., Heinrich, P. C., Johnston, J. A. (2004) The chemoattractants, IL-8 and formyl-methionyl-leucyl-phenylalanine, regulate granulocyte colony-stimulating factor signaling by inducing suppressor of cytokine signaling-1 expression. J. lmmunol. 173, 3243-3249.
28. Campbell, J. J., Foxman, E. F., Butcher, E. C. (1997) Chemoattractant receptor cross talk as a regulatory mechanism in leukocyte adhesion and migration. Eur. J. lmmunol. 27, 2571-2578.
29. Duddy, M. E., Dickson, G., Hawkins, S. A., Armstrong, M. A. (2001) Monocyte-derived dendritic cells: a potential target for therapy in multiple sclerosis (MS). Clin. Exp. lmmunol. 123, 280-287.
30. Paine III, R., Morris, S. B., Jin, H., Wilcoxen, S. E., Phare, S. M., Moore, B. B., Coffey, M. J., Toews, G. B. (2001) Impaired functional activity of alveolar macrophages from GM-CSF-deficient mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L1210-L1218.
31. Leonard, W. J., O'Shea, J. J. (1998) Jaks and STATs: biological implications. Annu. Rev. lmmunol. 16, 293-322.
32. Marriott, I., Bost, K. L. (2000) IL-4 and IFN-γ up-regulate substance P receptor expression in murine peritoneal macrophages. J. lmmunol. 165, 182-191.
33. Thivierge, M., Stankova, J., Rola-Pleszczynski, M. (2001) IL-13 and IL-4 up-regulate cysteinyl leukotriene 1 receptor expression in human monocytes and macrophages. J. Immunol. 167, 2855-2860.
34. Matsuguchi, T., Zhao, Y., Lilly, M. B., Kraft, A. S. (1997)The cytoplasmic domain of granulocyte-macrophage colony-stimulating factor (GM-CSF) receptor a subunit is essential for both GM-CSF-mediated growth and differentiation. J. Biol. Chem. 272, 17450-17459.
35. Kitayama, J., Carr, M. W., Roth, S. J., Buccola, J., Springer, T. A. (1997) Contrasting responses to multiple chemotactic stimuli in transendothelial migration: heterologous desensitization in neutrophils and augmentation of migration in eosinophils. J. Immunol. 158, 2340-2349.
36. Bromley, S. K., Peterson, D. A., Gunn, M. D., Dustin, M. L. (2000) Cutting edge: hierarchy of chemokine receptor and TCR signals regulating T cell migration and proliferation. J. Immunol. 165, 15-19.
37. Hoogsteden, H. C., Verhoeven, G. T., Lambrecht, B. N., Prins, J. B. (1999) Airway inflammation in asthma and chronic obstructive pulmonary disease with special emphasis on the antigen-presenting dendritic cell: influence of treatment with fluticasone propionate. Clin. Exp. Allergy 29 (Suppl. 2), 116-124.
38. Saint-Mezard, P., Berard, F., Dubois, B., Kaiserlian, D., Nicolas, J. F. (2004) The role of CD4+ and CD8+ T cells in contact hypersensitivity and allergic contact dermatitis. Eur. J. Dermatol. 14, 131-138.
39. Wan, H., Dupasquier, M. (2005) Dendritic cells in vivo and in vitro. Cell. Mol. Immunol. 2, 28-35.
40. Li, L., Gronning, L. M., Anderson, P. O., Li, S., Edvardsen, K., Johnston, J., Kioussis, D., Shepherd, P. R., Wang, P. (2004) Insulin induces SOCS-6 expression and its binding to the p85 monomer of phosphoinositide 3-kinase, resulting in improvement in glucose metabolism. J. Biol. Chem. 279, 34107-34114.
41. Badewa, A. P., Heiman, A. S. (2003) Inhibition of CCL11, CCL24, and CCL26-induced degranulation in HL-60 eosinophilic cells by specific inhibitors of MEK1/MEK2, p38 MAP kinase, and PI 3-kinase. Immuno-pharmacol. Immunotoxicol. 25, 145-157.
42. Pease, J. E., Williams, T. J. (2001) Eotaxin and asthma. Curr. Opin. Pharmacol. 1, 248-253.
43. Menzies-Gow, A., Ying, S., Phipps, S., Kay, A. B. (2004) Interactions between eotaxin, histamine and mast cells in early microvascular events associated with eosinophil recruitment to the site of allergic skin reactions in humans. Clin. Exp. Allergy 34, 1276-1282.