Multinucleated Giant Cells Are Specialized for Complement-Mediated Phagocytosis and Large Target Destruction

Cell Reports

Volumn 13, Issue 9, 2015, Pages 1937-1948

  Milde, Ronny ^a   Ritter, Julia ^a   Tennent, Glenys A ^b   Loesch, Andrzej ^b   Martinez, Fernando O ^c   Gordon, Siamon ^d   Pepys, Mark B ^b   Verschoor, Admar ^a,e   Helming, Laura ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; COMPLEMENT RECEPTOR 4; FC RECEPTOR; FC RECEPTOR IV; GLYCOPROTEIN P 15095; INTERLEUKIN 4; UNCLASSIFIED DRUG; AMYLOID; CD18 ANTIGEN; COLONY STIMULATING FACTOR 1; COMPLEMENT COMPONENT C3; PHORBOL 13 ACETATE 12 MYRISTATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL ADHESION; CELL FUNCTION; CELL SIZE; COMPARATIVE STUDY; COMPLEMENT ACTIVATION; COMPLEMENT MEDIATED PHAGOCYTOSIS; CONTROLLED STUDY; GIANT CELL; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MACROPHAGE ACTIVATION; MACROPHAGE FUSION; MEMBRANE BIOLOGY; MEMBRANE RUFFLE; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OPSONIZATION; PARTICLE SIZE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENETICS; HAMSTER; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; RAT; TRANSGENIC MOUSE;

AMYLOID; ANIMALS; ANTIGENS, CD11C; ANTIGENS, CD18; BONE MARROW CELLS; COMPLEMENT C3; CRICETINAE; GIANT CELLS; HUMANS; INTEGRIN ALPHAXBETA2; INTERLEUKIN-4; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHAGOCYTOSIS; RATS; RECEPTORS, IGG; TETRADECANOYLPHORBOL ACETATE; UP-REGULATION;

EID: 84949668185     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.10.065     Document Type: Article

References (46)

1. Aguilar P.S., Baylies M.K., Fleissner A., Helming L., Inoue N., Podbilewicz B., Wang H., Wong M. Genetic basis of cell-cell fusion mechanisms. Trends Genet. 2013, 29:427-437.
2. Anderson J.M., Rodriguez A., Chang D.T. Foreign body reaction to biomaterials. Semin. Immunol. 2008, 20:86-100.
3. Bianco C., Griffin F.M., Silverstein S.C. Studies of the macrophage complement receptor. Alteration of receptor function upon macrophage activation. J. Exp. Med. 1975, 141:1278-1290.
4. Bodin K., Ellmerich S., Kahan M.C., Tennent G.A., Loesch A., Gilbertson J.A., Hutchinson W.L., Mangione P.P., Gallimore J.R., Millar D.J., et al. Antibodies to human serum amyloid P component eliminate visceral amyloid deposits. Nature 2010, 468:93-97.
5. Cannon G.J., Swanson J.A. The macrophage capacity for phagocytosis. J. Cell Sci. 1992, 101:907-913.
6. Caron E., Self A.J., Hall A. The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr. Biol. 2000, 10:974-978.
7. Chambers T.J. Studies on the phagocytic capacity of macrophage polykaryons. J. Pathol. 1977, 123:65-77.
8. Champion J.A., Mitragotri S. Role of target geometry in phagocytosis. Proc. Natl. Acad. Sci. USA 2006, 103:4930-4934.
9. Criss A.K., Seifert H.S. Gonococci exit apically and basally from polarized epithelial cells and exhibit dynamic changes in type IV pili. Cell. Microbiol. 2006, 8:1430-1443.
10. Croke M., Ross F.P., Korhonen M., Williams D.A., Zou W., Teitelbaum S.L. Rac deletion in osteoclasts causes severe osteopetrosis. J. Cell Sci. 2011, 124:3811-3821.
11. Feldmann M., Pepys M.B. Role of C3 in in vitro lymphocyte cooperation. Nature 1974, 249:159-161.
12. Gadjeva M., Verschoor A., Brockman M.A., Jezak H., Shen L.M., Knipe D.M., Carroll M.C. Macrophage-derived complement component C4 can restore humoral immunity in C4-deficient mice. J. Immunol. 2002, 169:5489-5495.
13. Gonzalo P., Guadamillas M.C., Hernández-Riquer M.V., Pollán A., Grande-García A., Bartolomé R.A., Vasanji A., Ambrogio C., Chiarle R., Teixidó J., et al. MT1-MMP is required for myeloid cell fusion via regulation of Rac1 signaling. Dev. Cell 2010, 18:77-89.
14. Helming L., Gordon S. Macrophage fusion induced by IL-4 alternative activation is a multistage process involving multiple target molecules. Eur. J. Immunol. 2007, 37:33-42.
15. Helming L., Gordon S. Molecular mediators of macrophage fusion. Trends Cell Biol. 2009, 19:514-522.
16. Iwanaga T., Wakasugi S., Inomoto T., Uehira M., Ohnishi S., Nishiguchi S., Araki K., Uno M., Miyazaki J., Maeda S., et al. Liver-specific and high-level expression of human serum amyloid P component gene in transgenic mice. Dev. Genet. 1989, 10:365-371.
17. Jay S.M., Skokos E., Laiwalla F., Krady M.M., Kyriakides T.R. Foreign body giant cell formation is preceded by lamellipodia formation and can be attenuated by inhibition of Rac1 activation. Am. J. Pathol. 2007, 171:632-640.
18. Kao W.J., McNally A.K., Hiltner A., Anderson J.M. Role for interleukin-4 in foreign-body giant cell formation on a poly(etherurethane urea) in vivo. J. Biomed. Mater. Res. 1995, 29:1267-1275.
19. Kopf M., Herren S., Wiles M.V., Pepys M.B., Kosco-Vilbois M.H. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 1998, 188:1895-1906.
20. Kourtzelis I., Rafail S., DeAngelis R.A., Foukas P.G., Ricklin D., Lambris J.D. Inhibition of biomaterial-induced complement activation attenuates the inflammatory host response to implantation. FASEB J. 2013, 27:2768-2776.
21. Lai S., Zhou X. Inflammatory cells in tissues of gout patients and their correlations with comorbidities. Open Rheumatol. J. 2013, 7:26-31.
22. Langhans T. Über riesenzellen mit wandständigen kernen in tuberkeln und die fibröse form des tuberkels. Virchows Arch. 1868, 42:382-404.
23. Lay G., Poquet Y., Salek-Peyron P., Puissegur M.P., Botanch C., Bon H., Levillain F., Duteyrat J.L., Emile J.F., Altare F. Langhans giant cells from M. tuberculosis-induced human granulomas cannot mediate mycobacterial uptake. J. Pathol. 2007, 211:76-85.
24. McNally A.K., Anderson J.M. Interleukin-4 induces foreign body giant cells from human monocytes/macrophages. Differential lymphokine regulation of macrophage fusion leads to morphological variants of multinucleated giant cells. Am. J. Pathol. 1995, 147:1487-1499.
25. McNally A.K., Anderson J.M. Beta1 and beta2 integrins mediate adhesion during macrophage fusion and multinucleated foreign body giant cell formation. Am. J. Pathol. 2002, 160:621-630.
26. Melo M.D., Catchpole I.R., Haggar G., Stokes R.W. Utilization of CD11b knockout mice to characterize the role of complement receptor 3 (CR3, CD11b/CD18) in the growth of Mycobacterium tuberculosis in macrophages. Cell. Immunol. 2000, 205:13-23.
27. Michl J., Unkeless J.C., Pieczonka M.M., Silverstein S.C. Modulation of Fc receptors of mononuclear phagocytes by immobilized antigen-antibody complexes. Quantitative analysis of the relationship between ligand number and Fc receptor response. J. Exp. Med. 1983, 157:1746-1757.
28. Moreno J.L., Mikhailenko I., Tondravi M.M., Keegan A.D. IL-4 promotes the formation of multinucleated giant cells from macrophage precursors by a STAT6-dependent, homotypic mechanism: contribution of E-cadherin. J. Leukoc. Biol. 2007, 82:1542-1553.
29. Nakanishi-Matsui M., Yano S., Matsumoto N., Futai M. Lipopolysaccharide induces multinuclear cell from RAW264.7 line with increased phagocytosis activity. Biochem. Biophys. Res. Commun. 2012, 425:144-149.
30. Noursadeghi M., Bickerstaff M.C., Gallimore J.R., Herbert J., Cohen J., Pepys M.B. Role of serum amyloid P component in bacterial infection: protection of the host or protection of the pathogen. Proc. Natl. Acad. Sci. USA 2000, 97:14584-14589.
31. Patel P.C., Harrison R.E. Membrane ruffles capture C3bi-opsonized particles in activated macrophages. Mol. Biol. Cell 2008, 19:4628-4639.
32. Prokop S., Heppner F.L., Goebel H.H., Stenzel W. M2 polarized macrophages and giant cells contribute to myofibrosis in neuromuscular sarcoidosis. Am. J. Pathol. 2011, 178:1279-1286.
33. Richards D.B., Cookson L.M., Berges A.C., Barton S.V., Lane T., Ritter J.M., Fontana M., Moon J.C., Pinzani M., Gillmore J.D., et al. Therapeutic clearance of amyloid by antibodies to serum amyloid P component. N. Engl. J. Med. 2015, 373:1106-1114.
34. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
35. Rosen H., Gordon S. Monoclonal antibody to the murine type 3 complement receptor inhibits adhesion of myelomonocytic cells in vitro and inflammatory cell recruitment in vivo. J. Exp. Med. 1987, 166:1685-1701.
36. Samokhin A.O., Wilson S., Nho B., Lizame M.L., Musenden O.E., Brömme D. Cholate-containing high-fat diet induces the formation of multinucleated giant cells in atherosclerotic plaques of apolipoprotein E-/- mice. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1166-1173.
37. Schlesinger L., Musson R.A., Johnston R.B. Functional and biochemical studies of multinucleated giant cells derived from the culture of human monocytes. J. Exp. Med. 1984, 159:1289-1294.
38. Shilagardi K., Li S., Luo F., Marikar F., Duan R., Jin P., Kim J.H., Murnen K., Chen E.H. Actin-propelled invasive membrane protrusions promote fusogenic protein engagement during cell-cell fusion. Science 2013, 340:359-363.
39. Sterling H., Saginario C., Vignery A. CD44 occupancy prevents macrophage multinucleation. J. Cell Biol. 1998, 143:837-847.
40. Tang L., Liu L., Elwing H.B. Complement activation and inflammation triggered by model biomaterial surfaces. J. Biomed. Mater. Res. 1998, 41:333-340.
41. Vachon E., Martin R., Kwok V., Cherepanov V., Chow C.W., Doerschuk C.M., Plumb J., Grinstein S., Downey G.P. CD44-mediated phagocytosis induces inside-out activation of complement receptor-3 in murine macrophages. Blood 2007, 110:4492-4502.
42. Verschoor A., Brockman M.A., Knipe D.M., Carroll M.C. Cutting edge: myeloid complement C3 enhances the humoral response to peripheral viral infection. J. Immunol. 2001, 167:2446-2451.
43. Verschoor A., Brockman M.A., Gadjeva M., Knipe D.M., Carroll M.C. Myeloid C3 determines induction of humoral responses to peripheral herpes simplex virus infection. J. Immunol. 2003, 171:5363-5371.
44. Wessels M.R., Butko P., Ma M., Warren H.B., Lage A.L., Carroll M.C. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. USA 1995, 92:11490-11494.
45. Wright S.D., Craigmyle L.S., Silverstein S.C. Fibronectin and serum amyloid P component stimulate C3b- and C3bi-mediated phagocytosis in cultured human monocytes. J. Exp. Med. 1983, 158:1338-1343.
46. Wu H., Gower R.M., Wang H., Perrard X.Y., Ma R., Bullard D.C., Burns A.R., Paul A., Smith C.W., Simon S.I., Ballantyne C.M. Functional role of CD11c+ monocytes in atherogenesis associated with hypercholesterolemia. Circulation 2009, 119:2708-2717.