Intravenous immunoglobulin skews macrophages to an anti-inflammatory, IL-10-producing activation state

Journal of Leukocyte Biology

Volumn 98, Issue 6, 2015, Pages 983-994

  Kozicky, Lisa K ^a   Zhao, Zheng Yu ^a   Menzies, Susan C ^a   Fidanza, Mario ^a,b   Reid, Gregor S D ^a,b   Wilhelmsen, Kevin ^c   Hellman, Judith ^c   Hotte, Naomi ^d   Madsen, Karen L ^d   Sly, Laura M ^a  

^a BC CHILDREN S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Fc receptors; Macrophage activation; Map kinases; Regulatory macrophages; Sepsis

Indexed keywords

HUMAN IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR BETA; INTERLEUKIN 12; INTERLEUKIN 23P40; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; IL10 PROTEIN, MOUSE; IMMUNOGLOBULIN; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 12P40;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOINFLAMMATORY DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; KNOCKOUT MOUSE; PERITONEUM MACROPHAGE;

ANIMALS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNOGLOBULINS, INTRAVENOUS; INTERLEUKIN-10; INTERLEUKIN-12 SUBUNIT P40; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-10;

EID: 84949009592     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3VMA0315-078R     Document Type: Article

References (47)

1. Murray, P. J., Wynn, T. A. (2011) Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723–737.
2. Murray, P. J., Allen, J. E., Biswas, S. K., Fisher, E. A., Gilroy, D. W., Goerdt, S., Gordon, S., Hamilton, J. A., Ivashkiv, L. B., Lawrence, T., Locati, M., Mantovani, A., Martinez, F. O., Mege, J. L., Mosser, D.M., Natoli, G., Saeij, J. P., Schultze, J. L., Shirey, K. A., Sica, A., Suttles, J., Udalova, I., van Ginderachter, J. A., Vogel, S. N., Wynn, T. A. (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14–20.
3. Martinez, F. O., Gordon, S. (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6, 13.
4. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23–35.
5. Mosser, D. M., Edwards, J. P. (2008) Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958–969.
6. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890–898.
7. Fleming, B. D., Mosser, D. M. (2011) Regulatory macrophages: setting the threshold for therapy. Eur. J. Immunol. 41, 2498–2502.
8. Anderson, C. F., Gerber, J. S., Mosser, D. M. (2002) Modulating macrophage function with IgG immune complexes. J. Endotoxin Res. 8, 477–481.
9. Sutterwala, F. S., Noel, G. J., Salgame, P., Mosser, D. M. (1998) Reversal of proinflammatory responses by ligating the macrophage Fcgamma receptor type I. J. Exp. Med. 188, 217–222.
10. Edwards, J. P., Zhang, X., Frauwirth, K. A., Mosser, D. M. (2006) Biochemical and functional characterization of three activated macrophage populations. J. Leukoc. Biol. 80, 1298–1307.
11. Mosser, D. M., Zhang, X. (2008) Activation of murine macrophages. Curr. Protoc. Immunol. Chapter 14, Unit 14.2.
12. Mosser, D. M., Zhang, X. (2008) Interleukin-10: new perspectives on an old cytokine. Immunol. Rev. 226, 205–218.
13. Lucas, M., Zhang, X., Prasanna, V., Mosser, D. M. (2005) ERK activation following macrophage FcgammaR ligation leads to chromatin modifications at the IL-10 locus. J. Immunol. 175, 469–477.
14. Vos, A. C., Wildenberg, M. E., Duijvestein, M., Verhaar, A. P., van den Brink, G. R., Hommes, D. W. (2011) Anti-tumor necrosis factor-a antibodies induce regulatory macrophages in an Fc region-dependent manner. Gastroenterology 140, 221–230.
15. Riquelme, P., Tomiuk, S., Kammler, A., Fändrich, F., Schlitt, H. J., Geissler, E. K., Hutchinson, J. A. (2013) IFN-g-induced iNOS expression in mouse regulatory macrophages prolongs allograft survival in fully immunocompetent recipients. Mol. Ther. 21, 409–422.
16. Hutchinson, J. A., Riquelme, P., Geissler, E. K. (2012) Human regulatory macrophages as a cell-based medicinal product. Curr. Opin. Organ Transplant. 17, 48–54.
17. Hutchinson, J. A., Riquelme, P., Sawitzki, B., Tomiuk, S., Miqueu, P., Zuhayra, M., Oberg, H. H., Pascher, A., Lützen, U., Janssen, U., Broichhausen, C., Renders, L., Thaiss, F., Scheuermann, E., Henze, E., Volk, H. D., Chatenoud, L., Lechler, R. I., Wood, K. J., Kabelitz, D., Schlitt, H. J., Geissler, E. K., Fändrich, F. (2011) Cutting edge: immunological consequences and trafficking of human regulatory macrophages administered to renal transplant recipients. J. Immunol. 187, 2072–2078.
18. Gelfand, E. W. (2013) Intravenous immune globulin in autoimmune and inflammatory diseases. N. Engl. J. Med. 368, 777.
19. Nimmerjahn, F., Ravetch, J. V. (2010) Antibody-mediated modulation of immune responses. Immunol. Rev. 236, 265–275.
20. Anthony, R. M., Kobayashi, T., Wermeling, F., Ravetch, J. V. (2011) Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature 475, 110–113.
21. Schwab, I., Nimmerjahn, F. (2013) Intravenous immunoglobulin therapy: how does IgG modulate the immune system? Nat. Rev. Immunol. 13, 176–189.
22. Negi, V. S., Elluru, S., Sibéril, S., Graff-Dubois, S., Mouthon, L., Kazatchkine, M. D., Lacroix-Desmazes, S., Bayry, J., Kaveri, S. V. (2007) Intravenous immunoglobulin: an update on the clinical use and mechanisms of action. J. Clin. Immunol. 27, 233–245.
23. Sly, L. M., Hamilton, M. J., Kuroda, E., Ho, V. W., Antignano, F. L., Omeis, S. L., van Netten-Thomas, C. J., Wong, D., Brugger, H. K., Williams, O., Feldman, M. E., Houseman, B. T., Fiedler, D., Shokat, K. M., Krystal, G. (2009) SHIP prevents lipopolysaccharide from triggering an antiviral response in mice. Blood 113, 2945–2954.
24. Weisser, S. B., McLarren, K. W., Voglmaier, N., van Netten-Thomas, C. J., Antov, A., Flavell, R. A., Sly, L. M. (2011) Alternative activation of macrophages by IL-4 requires SHIP degradation. Eur. J. Immunol. 41, 1742–1753.
25. Polumuri, S. K., Toshchakov, V. Y., Vogel, S. N. (2007) Role of phosphatidylinositol-3 kinase in transcriptional regulation of TLRinduced IL-12 and IL-10 by Fc gamma receptor ligation in murine macrophages. J. Immunol. 179, 236–246.
26. Anthony, R. M., Ravetch, J. V. (2010) A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs. J. Clin. Immunol. 30 (Suppl 1), S9–S14.
27. Chaikuad, A., Tacconi, E. M., Zimmer, J., Liang, Y., Gray, N. S., Tarsounas, M., Knapp, S. (2014) A unique inhibitor binding site in ERK1/2 is associated with slow binding kinetics. Nat. Chem. Biol. 10, 853–860.
28. Nishimoto, S., Nishida, E. (2006) MAPK signalling: ERK5 versus ERK1/2. EMBO Rep. 7, 782–786.
29. Gallo, P., Gonçalves, R., Mosser, D. M. (2010) The influence of IgG density and macrophage Fc (gamma) receptor cross-linking on phagocytosis and IL-10 production. Immunol. Lett. 133, 70–77.
30. Kalesnikoff, J., Huber, M., Lam, V., Damen, J. E., Zhang, J., Siraganian, R. P., Krystal, G. (2001) Monomeric IgE stimulates signaling pathways in mast cells that lead to cytokine production and cell survival. Immunity 14, 801–811.
31. Bayry, J., Lacroix-Desmazes, S., Delignat, S., Mouthon, L., Weill, B., Kazatchkine, M. D., Kaveri, S. V. (2003) Intravenous immunoglobulin abrogates dendritic cell differentiation induced by interferon-alpha present in serum from patients with systemic lupus erythematosus. Arthritis Rheum. 48, 3497–3502.
32. Durandy, A., Kaveri, S. V., Kuijpers, T. W., Basta, M., Miescher, S., Ravetch, J. V., Rieben, R. (2009) Intravenous immunoglobulins—understanding properties and mechanisms. Clin. Exp. Immunol. 158 (Suppl 1), 2–13.
33. Okamura, H., Kashiwamura, S., Tsutsui, H., Yoshimoto, T., Nakanishi, K. (1998) Regulation of interferon-gamma production by IL-12 and IL-18. Curr. Opin. Immunol. 10, 259–264.
34. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T., Kastelein, R. A., Cua, D. J. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201, 233–240.
35. Tang, C., Chen, S., Qian, H., Huang, W. (2012) Interleukin-23: as a drug target for autoimmune inflammatory diseases. Immunology 135, 112–124.
36. Palladino, M. A., Bahjat, F. R., Theodorakis, E. A., Moldawer, L. L. (2003) Anti-TNF-alpha therapies: the next generation. Nat. Rev. Drug Discov. 2, 736–746.
37. Dienz, O., Rincon, M. (2009) The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 130, 27–33.
38. Alejandria, M. M., Lansang, M. A., Dans, L. F., Mantaring, J. B. (2002) Intravenous immunoglobulin for treating sepsis and septic shock. Cochrane Database Syst. Rev. (1:):CD001090.
39. Bruhns, P., Samuelsson, A., Pollard, J. W., Ravetch, J. V. (2003) Colonystimulating factor-1-dependent macrophages are responsible for IVIG protection in antibody-induced autoimmune disease. Immunity 18, 573–581.
40. Park-Min, K. H., Serbina, N. V., Yang, W., Ma, X., Krystal, G., Neel, B. G., Nutt, S. L., Hu, X., Ivashkiv, L. B. (2007) FcgammaRIII-dependent inhibition of interferon-gamma responses mediates suppressive effects of intravenous immune globulin. Immunity 26, 67–78.
41. Bruhns, P. (2012) Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119, 5640–5649.
42. Saraiva, M., O’Garra, A. (2010) The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170–181.
43. Tatake, R. J., O’Neill, M. M., Kennedy, C. A., Wayne, A. L., Jakes, S., Wu, D., Kugler, Jr., S. Z., Kashem, M. A., Kaplita, P., Snow, R. J. (2008) Identification of pharmacological inhibitors of the MEK5/ERK5 pathway. Biochem. Biophys. Res. Commun. 377, 120–125.
44. Zhu, W., Downey, J. S., Gu, J., Di Padova, F., Gram, H., Han, J. (2000) Regulation of TNF expression by multiple mitogen-activated protein kinase pathways. J. Immunol. 164, 6349–6358.
45. Fiorentino, D. F., Zlotnik, A., Mosmann, T. R., Howard, M., O’Garra, A. (1991) IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147, 3815–3822.
46. Alejandria, M. M., Lansang, M. A., Dans, L. F., Mantaring, J. B. III (2013) Intravenous immunoglobulin for treating sepsis, severe sepsis and septic shock. Cochrane Database Syst. Rev. 9, CD001090.
47. Li, M. C., He, S. H. (2004) IL-10 and its related cytokines for treatment of inflammatory bowel disease. World J. Gastroenterol. 10, 620–625.