SOCS3 is a modulator of human macrophage phagocytosis

Journal of Leukocyte Biology

Volumn 100, Issue 4, 2016, Pages 771-780

  Gordon, Peter ^a   Okai, Blessing ^a   Hoare, Joseph I ^a   Erwig, Lars P ^a   Wilson, Heather M ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Live cell imaging; PI3K; Rac1

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CARBOXYLIC ACID; F ACTIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 3; MICROSPHERE; RAC1 PROTEIN, HUMAN; SOCS3 PROTEIN, HUMAN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ADULT; APOPTOSIS; ARTICLE; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HUMAN EXPERIMENT; MACROPHAGE; MACROPHAGE MIGRATION; NORMAL HUMAN; PHAGOCYTOSIS; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; VIDEO MICROSCOPY; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CLASSIFICATION; DEFICIENCY; GENETICS; INFLAMMATION; PHYSIOLOGY; RNA INTERFERENCE; TIME LAPSE IMAGING; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; APOPTOSIS; CELLS, CULTURED; HUMANS; INFLAMMATION; MACROPHAGES; MICROSCOPY, VIDEO; MICROSPHERES; PHAGOCYTOSIS; PHAGOSOMES; PHOSPHATIDYLINOSITOL 3-KINASES; RAC1 GTP-BINDING PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING 3 PROTEIN; TIME-LAPSE IMAGING;

EID: 84988627028     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A1215-554RR     Document Type: Article

References (49)

1. Murray, P. J., Wynn, T. A. (2011) Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737.
2. Martinez, F. O., Sica, A., Mantovani, A., Locati, M. (2008) Macrophage activation and polarization. Front. Biosci. 13, 453-461.
3. 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.
4. Poon, I. K., Lucas, C. D., Rossi, A. G., Ravichandran, K. S. (2014) Apoptotic cell clearance: basic biology and therapeutic potential. Nat. Rev. Immunol. 14, 166-180.
5. Erwig, L. P., Henson, P. M. (2007) Immunological consequences of apoptotic cell phagocytosis. Am. J. Pathol. 171, 2-8.
6. Erwig, L. P., Henson, P. M. (2008) Clearance of apoptotic cells by phagocytes. Cell Death Differ. 15, 243-250.
7. Erwig, L. P., McPhilips, K. A., Wynes, M. W., Ivetic, A., Ridley, A. J., Henson, P. M. (2006) Differential regulation of phagosome maturation in macrophages and dendritic cells mediated by Rho GTPases and ezrinradixin-moesin (ERM) proteins. Proc. Natl. Acad. Sci. USA 103, 12825-12830.
8. 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.
9. Thorp, E., Tabas, I. (2009) Mechanisms and consequences of efferocytosis in advanced atherosclerosis. J. Leukoc. Biol. 86, 1089-1095.
10. Gumienny, T. L., Brugnera, E., Tosello-Trampont, A. C., Kinchen, J. M., Haney, L. B., Nishiwaki, K., Walk, S. F., Nemergut, M. E., Macara, I. G., Francis, R., Schedl, T., Qin, Y., Van Aelst, L., Hengartner, M. O., Ravichandran, K. S. (2001) CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107, 27-41.
11. Leverrier, Y., Ridley, A. J. (2001) Requirement for Rho GTPases and PI 3-kinases during apoptotic cell phagocytosis by macrophages. Curr. Biol. 11, 195-199.
12. Wilson, H. M. (2014) SOCS proteins in macrophage polarization and function. Front. Immunol. 5, 357-361.
13. Strebovsky, J., Walker, P., Dalpke, A. H. (2012) Suppressor of cytokine signaling proteins as regulators of innate immune signaling. Front. Biosci. (Landmark Ed.) 17, 1627-1639.
14. Dalpke, A., Heeg, K., Bartz, H., Baetz, A. (2008) Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213, 225-235.
15. Chong, M. M., Metcalf, D., Jamieson, E., Alexander, W. S., Kay, T. W. (2005) Suppressor of cytokine signaling-1 in T cells and macrophages is critical for preventing lethal inflammation. Blood 106, 1668-1675.
16. Whyte, C. S., Bishop, E. T., Rückerl, D., Gaspar-Pereira, S., Barker, R. N., Allen, J. E., Rees, A. J., Wilson, H. M. (2011) Suppressor of cytokine signaling (SOCS)1 is a key determinant of differential macrophage activation and function. J. Leukoc. Biol. 90, 845-854.
17. Liu, Y., Stewart, K. N., Bishop, E., Marek, C. J., Kluth, D. C., Rees, A. J., Wilson, H. M. (2008) Unique expression of suppressor of cytokine signaling 3 is essential for classical macrophage activation in rodents in vitro and in vivo. J. Immunol. 180, 6270-6278.
18. Arnold, C. E., Whyte, C. S., Gordon, P., Barker, R. N., Rees, A. J., Wilson, H. M. (2014) A critical role for suppressor of cytokine signalling 3 in promoting M1 macrophage activation and function in vitro and in vivo. Immunology 141, 96-110.
19. Qin, H., Holdbrooks, A. T., Liu, Y., Reynolds, S. L., Yanagisawa, L. L., Benveniste, E. N. (2012) SOCS3 deficiency promotes M1 macrophage polarization and inflammation. J. Immunol. 189, 3439-3448.
20. Wang, Y. C., He, F., Feng, F., Liu, X. W., Dong, G. Y., Qin, H. Y., Hu, X. B., Zheng, M. H., Liang, L., Feng, L., Liang, Y. M., Han, H. (2010) Notch signaling determines the M1 versus M2 polarization of macrophages in antitumor immune responses. Cancer Res. 70, 4840-4849.
21. Labuzek, K., Suchy, D., Gabryel, B., Pierzchała, O., Okopień, B. (2012) Role of the SOCS in monocytes/macrophages-related pathologies. Are we getting closer to a new pharmacological target? Pharmacol. Rep. 64, 1038-1054.
22. Marine, J. C., Topham, D. J., McKay, C., Wang, D., Parganas, E., Stravopodis, D., Yoshimura, A., Ihle, J. N. (1999) SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 98, 609-616.
23. Starr, R., Metcalf, D., Elefanty, A. G., Brysha, M., Willson, T. A., Nicola, N. A., Hilton, D. J., Alexander, W. S. (1998) Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. USA 95, 14395-14399.
24. Brysha, M., Zhang, J.-G., Bertolino, P., Corbin, J. E., Alexander, W. S., Nicola, N. A., Hilton, D. J., Starr, R. (2001) Suppressor of cytokine signaling-1 attenuates the duration of interferon g signal transduction in vitro and in vivo. J. Biol. Chem. 276, 22086-22089.
25. Lang, R., Pauleau, A. L., Parganas, E., Takahashi, Y., Mages, J., Ihle, J. N., Rutschman, R., Murray, P. J. (2003) SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 4, 546-550.
26. Croker, B. A., Krebs, D. L., Zhang, J. G., Wormald, S., Willson, T. A., Stanley, E. G., Robb, L., Greenhalgh, C. J., Förster, I., Clausen, B. E., Nicola, N. A., Metcalf, D., Hilton, D. J., Roberts, A. W., Alexander, W. S. (2003) SOCS3 negatively regulates IL-6 signaling in vivo. Nat. Immunol. 4, 540-545.
27. Yasukawa, H., Ohishi, M., Mori, H., Murakami, M., Chinen, T., Aki, D., Hanada, T., Takeda, K., Akira, S., Hoshijima, M., Hirano, T., Chien, K. R., Yoshimura, A. (2003) IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 4, 551-556.
28. Dimitriou, I. D., Clemenza, L., Scotter, A. J., Chen, G., Guerra, F. M., Rottapel, R. (2008) Putting out the fire: coordinated suppression of the innate and adaptive immune systems by SOCS1 and SOCS3 proteins. Immunol. Rev. 224, 265-283.
29. White, G. E., Cotterill, A., Addley, M. R., Soilleux, E. J., Greaves, D. R. (2011) Suppressor of cytokine signalling protein SOCS3 expression is increased at sites of acute and chronic inflammation. J. Mol. Histol. 42, 137-151.
30. Okai, B., Lyall, N., Gow, N. A., Bain, J. M., Erwig, L. P. (2015) Rab14 regulates maturation of macrophage phagosomes containing the fungal pathogen Candida albicans and outcome of the host-pathogen interaction. Infect. Immun. 83, 1523-1535.
31. Lukinavičius, G., Reymond, L., D’Este, E., Masharina, A., Göttfert, F., Ta, H., Güther, A., Fournier, M., Rizzo, S., Waldmann, H., Blaukopf, C., Sommer, C., Gerlich, D. W., Arndt, H.-D., Hell, S. W., Johnsson,K. (2014) Fluorogenic probes for live-cell imaging of the cytoskeleton. Nat. Methods 11, 731-733.
32. Korns, D., Frasch, S. C., Fernandez-Boyanapalli, R., Henson, P. M., Bratton, D. L. (2011) Modulation of macrophage efferocytosis in inflammation. Front. Immunol. 2, 57.
33. Underhill, D. M., Goodridge, H. S. (2012) Information processing during phagocytosis. Nat. Rev. Immunol. 12, 492-502.
34. Canton, J. (2014) Phagosome maturation in polarized macrophages. J. Leukoc. Biol. 96, 729-738.
35. O’Connor, J. C., Sherry, C. L., Guest, C. B., Freund, G. G. (2007) Type 2 diabetes impairs insulin receptor substrate-2-mediated phosphatidylinositol 3-kinase activity in primary macrophages to induce a state of cytokine resistance to IL-4 in association with overexpression of suppressor of cytokine signaling-3. J. Immunol. 178, 6886-6893.
36. Metlakunta, A. S., Sahu, M., Yasukawa, H., Dhillon, S. S., Belsham, D. D., Yoshimura, A., Sahu, A. (2011) Neuronal suppressor of cytokine signaling-3 deficiency enhances hypothalamic leptin-dependent phosphatidylinositol 3-kinase signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1185-R1193.
37. Ueki, K., Kondo, T., Kahn, C. R. (2004) Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol. Cell. Biol. 12, 5434-5446.
38. Castellano, F., Montcourrier, P., Chavrier, P. (2000) Membrane recruitment of Rac1 triggers phagocytosis. J. Cell Sci. 113, 2955-2961.
39. Frasch, S. C., Fernandez-Boyanapalli, R. F., Berry, K. Z., Leslie, C. C., Bonventre, J. V., Murphy, R. C., Henson, P. M., Bratton, D. L. (2011) Signaling via macrophage G2A enhances efferocytosis of dying neutrophils by augmentation of Rac activity. J. Biol. Chem. 286, 12108-12122.
40. Savill, J., Dransfield, I., Gregory, C., Haslett, C. (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975.
41. McPhillips, K., Janssen, W. J., Ghosh, M., Byrne, A., Gardai, S., Remigio, L., Bratton, D. L., Kang, J. L., Henson, P. (2007) TNF-alpha inhibits macrophage clearance of apoptotic cells via cytosolic phospholipase A2 and oxidant-dependent mechanisms. J. Immunol. 178, 8117-8126.
42. Soki, F. N., Koh, A. J., Jones, J. D., Kim, Y. W., Dai, J., Keller, E. T., Pienta, K. J., Atabai, K., Roca, H., McCauley, L. K. (2014) Polarization of prostate cancer-associated macrophages is induced by milk fat globule-EGF factor 8 (MFG-E8)-mediated efferocytosis. J. Biol. Chem. 289, 24560-24572.
43. Juncadella, I. J., Kadl, A., Sharma, A. K., Shim, Y. M., Hochreiter-Hufford, A., Borish, L., Ravichandran, K. S. (2013) Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 493, 547-551.
44. Neukomm, L. J., Frei, A. P., Cabello, J., Kinchen, J. M., Zaidel-Bar, R., Ma, Z., Haney, L. B., Hardin, J., Ravichandran, K. S., Moreno, S., Hengartner, M. O. (2011) Loss of the RhoGAP SRGP-1 promotes the clearance of dead and injured cells in Caenorhabditis elegans. Nat. Cell Biol. 13, 79-86.
45. Finnemann, S. C. (2003) Focal adhesion kinase signaling promotes phagocytosis of integrin-bound photoreceptors. EMBO J. 22, 4143-4154.
46. Liu, E., Ĉoté, J. F., Vuori, K. (2003) Negative regulation of FAK signaling by SOCS proteins. EMBO J. 22, 5036-5046.
47. Aziz, M., Jacob, A., Matsuda, A., Wu, R., Zhou, M., Dong, W., Yang, W. L., Wang, P. (2011) Pre-treatment of recombinant mouse MFG-E8 downregulates LPS-induced TNF-a production in macrophages via STAT3-mediated SOCS3 activation. PLoS One 6, e27685.
48. Bain, J. M., Louw, J., Lewis, L. E., Okai, B.,Walls, C. A., Ballou, E. R.,Walker, L. A., Reid, D., Munro, C. A., Brown, A. J., Brown, G. D., Gow, N. A., Erwig, L. P. (2014) Candida albicans hypha formation and mannan masking of b-glucan inhibit macrophage phagosome maturation. MBio 5, e01874.
49. Kratochvill, F., Neale, G., Haverkamp, J. M., Van de Velde, L. A., Smith, A. M., Kawauchi, D., McEvoy, J., Roussel, M. F., Dyer, M. A., Qualls, J. E., Murray, P. J. (2015) TNF counterbalances the emergence of M2 tumor macrophages. Cell Reports 12, 1902-1914.