C5a-regulated CCAAT/enhancer-binding proteins β and δ are essential in Fcγ receptor-mediated inflammatory cytokine and chemokine production in macrophages

Journal of Biological Chemistry

Volumn 287, Issue 5, 2012, Pages 3217-3230

  Yan, Chunguang ^a   Zhu, Mei ^b   Staiger, Jennifer ^c   Johnson, Peter F ^d   Gao, Hongwei ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MOUNT ST MARY S UNIVERSITY   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT/ENHANCER-BINDING PROTEINS; CHEMOKINES; CYTOKINES; IMMUNE COMPLEX; INFLAMMATORY RESPONSE; KEY REGULATORS; P38 MAPK; PROTEIN LEVEL;

CHEMICAL ACTIVATION; GENES; PROTEINS;

MACROPHAGES;

CCAAT ENHANCER BINDING PROTEIN BETA; CCAAT ENHANCER BINDING PROTEIN DELTA; CHEMOKINE; COMPLEMENT COMPONENT C5A; CYTOKINE; FC RECEPTOR; IMMUNOGLOBULIN G; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; INFLAMMATION; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL LINE; CHEMOKINES; COMPLEMENT C5A; INFLAMMATION; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 3; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, IGG;

EID: 84856295957     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.280834     Document Type: Article

References (53)

1. Nimmerjahn, F., and Ravetch, J. V. (2008) Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47
2. Halstead, S. B., Mahalingam, S., Marovich, M. A., Ubol, S., and Mosser, D. M. (2010) Intrinsic antibody-dependent enhancement of microbial infection in macrophages. Disease regulation by immune complexes. Lancet Infect. Dis. 10, 712-722
3. Fernández, N., Renedo, M., García-Rodríguez, C., and Sánchez Crespo, M. (2002) Activation of monocytic cells through Fc γreceptors induces the expression of macrophage-inflammatory protein (MIP)-1α, MIP-1β, and RANTES. J. Immunol. 169, 3321-3328
4. Gao, H., Neff, T., and Ward, P. A. (2006) Regulation of lung inflammation in the model of IgG immune-complex injury. Annu. Rev. Pathol. 1, 215-242
5. Bayón, Y., Alonso, A., and Sánchez Crespo, M. (1997) Stimulation of Fc γreceptors in rat peritoneal macrophages induces the expression of nitric oxide synthase and chemokines by mechanisms showing different sensitivities to antioxidants and nitric oxide donors. J. Immunol. 159, 887-894
6. Schmal, H., Czermak, B. J., Lentsch, A. B., Bless, N. M., Beck-Schimmer, B., Friedl, H. P., and Ward, P. A. (1998) Soluble ICAM-1 activates lung macrophages and enhances lung injury. J. Immunol. 161, 3685-3693
7. Descombes, P., and Schibler, U. (1991) A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67, 569-579 (Pubitemid 121001471)
8. Tanaka, T., Akira, S., Yoshida, K., Umemoto, M., Yoneda, Y., Shirafuji, N., Fujiwara, H., Suematsu, S., Yoshida, N., and Kishimoto, T. (1995) Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80, 353-361
9. Uematsu, S., Kaisho, T., Tanaka, T., Matsumoto, M., Yamakami, M., Omori, H., Yamamoto, M., Yoshimori, T., and Akira, S. (2007) The C/EBP β isoform 34-kDa LAP is responsible for NF-IL-6-mediated gene induction in activated macrophages but is not essential for intracellular bacteria killing. J. Immunol. 179, 5378-5386
10. Matsumoto, M., Tanaka, T., Kaisho, T., Sanjo, H., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., and Akira, S. (1999) A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J. Immunol. 163, 5039-5048 (Pubitemid 29501272)
11. 2 synthase gene induced by the Toll-like receptor 4/MyD88/NF-IL6 pathway. J. Immunol. 168, 5811-5816
12. Cloutier, A., Guindi, C., Larivée, P., Dubois, C. M., Amrani, A., and Mc- Donald, P. P. (2009) Inflammatory cytokine production by human neutrophils involves C/EBP transcription factors. J. Immunol. 182, 563-571
13. Gorgoni, B., Maritano, D., Marthyn, P., Righi, M., and Poli, V. (2002) C/EBP β gene inactivation causes both impaired and enhanced gene expression and inverse regulation of IL-12 p40 and p35 mRNAs in macrophages. J. Immunol. 168, 4055-4062 (Pubitemid 34298412)
14. Cox, G. W., Mathieson, B. J., Gandino, L., Blasi, E., Radzioch, D., and Varesio, L. (1989) Heterogeneity of hematopoietic cells immortalized by v-myc/v-raf recombinant retrovirus infection of bone marrow or fetal liver. J. Natl. Cancer Inst. 81, 1492-1496 (Pubitemid 19252402)
15. Sterneck, E., Paylor, R., Jackson-Lewis, V., Libbey, M., Przedborski, S., Tessarollo, L., Crawley, J. N., and Johnson, P. F. (1998) Selectively enhanced contextual fear conditioning in mice lacking the transcriptional regulator CCAAT/enhancer binding protein δ. Proc. Natl. Acad. Sci. U.S.A. 95, 10908-10913 (Pubitemid 28413167)
16. Sterneck, E., Tessarollo, L., and Johnson, P. F. (1997) An essential role for C/EBPβ in female reproduction. Genes Dev. 11, 2153-2162 (Pubitemid 27387967)
17. Rittirsch, D., Flierl, M. A., Day, D. E., Nadeau, B. A., Zetoune, F. S., Sarma, J. V., Werner, C. M., Wanner, G. A., Simmen, H. P., Huber-Lang, M. S., and Ward, P. A. (2009) Cross-talk between TLR4 and FcγReceptor III (CD16) pathways. PLoS Pathog. 5, e1000464
18. Poli, V. (1998) The role of C/EBP isoforms in the control of inflammatory and native immunity functions. J. Biol. Chem. 273, 29279-29282
19. Anastasov, N., Bonzheim, I., Rudelius, M., Klier, M., Dau, T., Angermeier, D., Duyster, J., Pittaluga, S., Fend, F., Raffeld, M., and Quintanilla-Martinez, L. (2010) C/EBPβ expression in ALK-positive anaplastic large cell lymphomas is required for cell proliferation and is induced by the STAT3 signaling pathway. Haematologica 95, 760-767
20. Lu, Y. C., Kim, I., Lye, E., Shen, F., Suzuki, N., Suzuki, S., Gerondakis, S., Akira, S., Gaffen, S. L., Yeh, W. C., and Ohashi, P. S. (2009) Differential role for c-Rel and C/EBPβ/δ in TLR-mediated induction of proinflammatory cytokines. J. Immunol. 182, 7212-7221
21. Maitra, U., Gan, L., Chang, S., and Li, L. (2011) Low-dose endotoxin induces inflammation by selectively removing nuclear receptors and activating CCAAT/enhancer-binding protein δ. J. Immunol. 186, 4467-4473
22. Widmer, U., Manogue, K. R., Cerami, A., and Sherry, B. (1993) Genomic cloning and promoter analysis of macrophage inflammatory protein (MIP)-2, MIP-1 α, and MIP-1 β, members of the chemokine superfamily of proinflammatory cytokines. J. Immunol. 150, 4996-5012 (Pubitemid 23150367)
23. Wolpe, S. D., Sherry, B., Juers, D., Davatelis, G., Yurt, R. W., and Cerami, A. (1989) Identification and characterization of macrophage inflammatory protein 2. Proc. Natl. Acad. Sci. U.S.A. 86, 612-616 (Pubitemid 19037791)
24. Wolpe, S. D., Davatelis, G., Sherry, B., Beutler, B., Hesse, D. G., Nguyen, H. T., Moldawer, L. L., Nathan, C. F., Lowry, S. F., and Cerami, A. (1988) Macrophages secrete a novel heparin-binding protein with inflammatory and neutrophil chemokinetic properties. J. Exp. Med. 167, 570-581 (Pubitemid 18073655)
25. Davatelis, G., Tekamp-Olson, P., Wolpe, S. D., Hermsen, K., Luedke, C., Gallegos, C., Coit, D., Merryweather, J., and Cerami, A. (1988) Cloning and characterization of a cDNA for murine macrophage inflammatory protein (MIP), a novel monokine with inflammatory and chemokinetic properties. J. Exp. Med. 167, 1939-1944
26. Wolpe, S. D., and Cerami, A. (1989) Macrophage inflammatory proteins 1 and 2. Members of a novel superfamily of cytokines. FASEB J. 3, 2565-2573 (Pubitemid 20013270)
27. Oppenheim, J. J., Zachariae, C. O., Mukaida, N., and Matsushima, K. (1991) Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu. Rev. Immunol. 9, 617-648
28. Nimmerjahn, F., and Ravetch, J. V. (2007) Fc receptors as regulators of immunity. Adv. Immunol. 96, 179-204
29. Akagi, T., Luong, Q. T., Gui, D., Said, J., Selektar, J., Yung, A., Bunce, C. M., Braunstein, G. D., and Koeffler, H. P. (2008) Induction of sodium iodide symporter gene and molecular characterization of HNF3 β/FoxA2, TTF-1, and C/EBP β in thyroid carcinoma cells. Br. J. Cancer 99, 781-788
30. Bianchi, G., Montecucco, F., Bertolotto, M., Dallegri, F., and Ottonello, L. (2007) Immune complexes induce monocyte survival through defined intracellular pathways. Ann. N.Y. Acad. Sci. 1095, 209-219 (Pubitemid 47092453)
31. Shushakova, N., Skokowa, J., Schulman, J., Baumann, U., Zwirner, J., Schmidt, R. E., and Gessner, J. E. (2002) C5a anaphylatoxin is a major regulator of activating versus inhibitory FcγRs in immune complex-induced lung disease. J. Clin. Invest. 110, 1823-1830 (Pubitemid 36076489)
32. Bless, N. M., Warner, R. L., Padgaonkar, V. A., Lentsch, A. B., Czermak, B. J., Schmal, H., Friedl, H. P., and Ward, P. A. (1999) Roles for C-X-C chemokines and C5a in lung injury after hindlimb ischemia-reperfusion. Am. J. Physiol. 276, L57-L63 (Pubitemid 29061665)
33. Kumar, V., Ali, S. R., Konrad, S., Zwirner, J., Verbeek, J. S., Schmidt, R. E., and Gessner, J. E. (2006) Cell-derived anaphylatoxins as key mediators of antibody-dependent type II autoimmunity in mice. J. Clin. Invest. 116, 512-520 (Pubitemid 43228369)
34. Litvak, V., Ramsey, S. A., Rust, A. G., Zak, D. E., Kennedy, K. A., Lampano, A. E., Nykter, M., Shmulevich, I., and Aderem, A. (2009) Function of C/EBPδ in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat. Immunol. 10, 437-443
35. Adelmant, G., Gilbert, J. D., and Freytag, S. O. (1998) Human translocation liposarcoma-CCAAT/enhancer-binding protein (C/EBP) homologous protein (TLS-CHOP) oncoprotein prevents adipocyte differentiation by directly interfering with C/EBPβ function. J. Biol. Chem. 273, 15574-15581 (Pubitemid 28298170)
36. Akira, S., Isshiki, H., Sugita, T., Tanabe, O., Kinoshita, S., Nishio, Y., Nakajima, T., Hirano, T., and Kishimoto, T. (1990) A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9, 1897-1906
37. Zhang, Y., and Rom, W. N. (1993) Regulation of the interleukin-1 β (IL-1 β) gene by mycobacterial components and lipopolysaccharide is mediated by two nuclear factor-IL6 motifs. Mol. Cell. Biol. 13, 3831-3837 (Pubitemid 23157320)
38. Kinoshita, S., Akira, S., and Kishimoto, T. (1992) A member of the C/EBP family, NF-IL6 β, forms a heterodimer and transcriptionally synergizes with NF-IL6. Proc. Natl. Acad. Sci. U.S.A. 89, 1473-1476
39. Alam, T., An, M. R., and Papaconstantinou, J. (1992) Differential expression of three C/EBP isoforms in multiple tissues during the acute phase response. J. Biol. Chem. 267, 5021-5024
40. Pope, R. M., Leutz, A., and Ness, S. A. (1994) C/EBP β regulation of the tumor necrosis factor α gene. J. Clin. Invest. 94, 1449-1455
41. Walpen, S., Beck, K. F., Schaefer, L., Raslik, I., Eberhardt, W., Schaefer, R. M., and Pfeilschifter, J. (2001) Nitric oxide induces MIP-2 transcription in rat renal mesangial cells and in a rat model of glomerulonephritis. FASEB J 15, 571-573
42. Arnett, B., Soisson, P., Ducatman, B. S., and Zhang, P. (2003) Expression of CAAT enhancer-binding protein β (C/EBP β) in cervix and endometrium. Mol. Cancer 2, 21
43. Ramji, D. P., Vitelli, A., Tronche, F., Cortese, R., and Ciliberto, G. (1993) The two C/EBP isoforms, IL-6DBP/NF-IL6 and C/EBP δ/NF-IL6 β, are induced by IL-6 to promote acute phase gene transcription via different mechanisms. Nucleic Acids Res. 21, 289-294 (Pubitemid 23151900)
44. Trotta, R., Kanakaraj, P., and Perussia, B. (1996) Fc γ R-dependent mitogen- activated protein kinase activation in leukocytes. A common signal transduction event necessary for expression of TNF-α and early activation genes. J. Exp. Med. 184, 1027-1035
45. Hillyard, D. Z., Jardine, A. G., McDonald, K. J., and Cameron, A. J. (2004) Fluvastatin inhibits raft-dependent Fcγ receptor signaling in human monocytes. Atherosclerosis 172, 219-228 (Pubitemid 38167532)
46. Lucas, M., Zhang, X., Prasanna, V., and Mosser, D. M. (2005) ERK activation following macrophage FcγR ligation leads to chromatin modifications at the IL-10 locus. J. Immunol. 175, 469-477 (Pubitemid 40884351)
47. Song, X., Tanaka, S., Cox, D., and Lee, S. C. (2004) Fcγ receptor signaling in primary human microglia. Differential roles of PI-3K and Ras/ERK MAPK pathways in phagocytosis and chemokine induction. J. Leukoc. Biol. 75, 1147-1155 (Pubitemid 38720659)
48. Sánchez-Mejorada, G., and Rosales, C. (1998) Fcγ receptor-mediated mitogen- activated protein kinase activation in monocytes is independent of Ras. J. Biol. Chem. 273, 27610-27619 (Pubitemid 28500484)
49. García-García, E., Sánchez-Mejorada, G., and Rosales, C. (2001) Phosphatidylinositol 3-kinase and ERK are required for NF-κB activation but not for phagocytosis. J. Leukoc. Biol. 70, 649-658 (Pubitemid 32954777)
50. Nakano, H., Shindo, M., Sakon, S., Nishinaka, S., Mihara, M., Yagita, H., and Okumura, K. (1998) Differential regulation of IκB kinase α and β by two upstream kinases, NF-κB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1. Proc. Natl. Acad. Sci. U.S.A. 95, 3537-3542
51. Gerbitz, A., Ewing, P., Olkiewicz, K., Willmarth, N. E., Williams, D., Hildebrandt, G., Wilke, A., Liu, C., Eissner, G., Andreesen, R., Holler, E., Guo, R., Ward, P. A., and Cooke, K. R. (2005) A role for CD54 (intercellular adhesion molecule-1) in leukocyte recruitment to the lung during the development of experimental idiopathic pneumonia syndrome. Transplantation 79, 536-542 (Pubitemid 40365881)
52. Konrad, S., Engling, L., Schmidt, R. E., and Gessner, J. E. (2007) Characterization of the murine IgG Fc receptor III and IIB gene promoters. A single two-nucleotide difference determines their inverse responsiveness to C5a. J. Biol. Chem. 282, 37906-37912
53. Konrad, S., Ali, S. R., Wiege, K., Syed, S. N., Engling, L., Piekorz, R. P., Hirsch, E., Nürnberg, B., Schmidt, R. E., and Gessner, J. E. (2008) Phosphoinositide 3-kinases γ and δ, linkers of coordinate C5a receptor-Fcγ receptor activation and immune complex-induced inflammation. J. Biol. Chem. 283, 33296-33303