The molecular basis of macrophage fusion

Immunobiology

Volumn 212, Issue 9-10, 2008, Pages 785-793

  Helming, Laura ^a   Gordon, Siamon ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cellular fusion; Granuloma; Macrophage; Multinucleated giant cell

Indexed keywords

A DISINTEGRIN AND METALLOPROTEASE; CD81 ANTIGEN; CD9 ANTIGEN; CD98 ANTIGEN; CELL SURFACE PROTEIN; CYTOKINE; GLYCOPROTEIN; GROWTH FACTOR; HYBRID PROTEIN; INTERLEUKIN 4; MELTRIN ALPHA; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PURINERGIC P2X7 RECEPTOR; TETRASPANIN; TM7 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL CULTURE; CELL FUNCTION; CELL FUSION; GIANT CELL; GRANULOMA; GRANULOMATOSIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SPACE; MACROPHAGE FUNCTION; MONOCYTE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION;

EID: 37049025380     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2007.09.012     Document Type: Article

References (73)

1. Abe E., Miyaura C., Tanaka H., Shiina Y., Kuribayashi T., Suda S., Nishii Y., DeLuca H.F., and Suda T. 1 alpha, 25-dihydroxyvitamin D3 promotes fusion of mouse alveolar macrophages both by a direct mechanism and by a spleen cell-mediated indirect mechanism. Proc. Natl. Acad. Sci. USA 80 (1983) 5583-5587
2. Abe E., Mocharla H., Yamate T., Taguchi Y., and Manolagas S.C. Meltrin-alpha, a fusion protein involved in multinucleated giant cell and osteoclast formation. Calcif. Tissue Int. 64 (1999) 508-515
3. Anderson J.M. Multinucleated giant cells. Curr. Opin. Hematol. 7 (2000) 40-47
4. Boros D.L. Immunopathology of Schistosoma mansoni infection. Clin. Microbiol. Rev. 2 (1989) 250-269
5. Chambers T.J. Fusion of hamster macrophages induced by lectins. J. Pathol. 123 (1977) 53-61
6. Chambers T.J. Studies on the phagocytic capacity of macrophage polykaryons. J. Pathol. 123 (1977) 65-77
7. Chambers T.J., and Spector W.G. Inflammatory giant cells. Immunobiology 161 (1982) 283-289
8. Chensue S.W., Terebuh P.D., Warmington K.S., Hershey S.D., Evanoff H.L., Kunkel S.L., and Higashi G.I. Role of IL-4 and IFN-gamma in Schistosoma mansoni egg-induced hypersensitivity granuloma formation. Orchestration, relative contribution, and relationship to macrophage function. J. Immunol. 148 (1992) 900-906
9. Chiozzi P., Sanz J.M., Ferrari D., Falzoni S., Aleotti A., Buell G.N., Collo G., and Di Virgilio F. Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2×7 receptor. J. Cell Biol. 138 (1997) 697-706
10. Cui W., Ke J.Z., Zhang Q., Ke H.Z., Chalouni C., and Vignery A. The intracellular domain of CD44 promotes the fusion of macrophages. Blood 107 (2006) 796-805
11. DeFife K.M., Jenney C.R., McNally A.K., Colton E., and Anderson J.M. Interleukin-13 induces human monocyte/macrophage fusion and macrophage mannose receptor expression. J. Immunol. 158 (1997) 3385-3390
12. Deves R., and Boyd C.A. Surface antigen CD98(4F2): not a single membrane protein, but a family of proteins with multiple functions. J. Membr. Biol. 173 (2000) 165-177
13. Di Virgilio F., Falzoni S., Chiozzi P., Sanz J.M., Ferrari D., and Buell G.N. ATP receptors and giant cell formation. J. Leukoc. Biol. 66 (1999) 723-726
14. Fais S., Burgio V.L., Silvestri M., Capobianchi M.R., Pacchiarotti A., and Pallone F. Multinucleated giant cells generation induced by interferon-gamma. Changes in the expression and distribution of the intercellular adhesion molecule-1 during macrophages fusion and multinucleated giant cell formation. Lab. Invest. 71 (1994) 737-744
15. Falzoni S., Chiozzi P., Ferrari D., Buell G., and Di Virgilio F. P2X(7) receptor and polykarion formation. Mol. Biol. Cell 11 (2000) 3169-3176
16. Fenouillet E., Clerget-Raslain B., Gluckman J.C., Guetard D., Montagnier L., and Bahraoui E. Role of N-linked glycans in the interaction between the envelope glycoprotein of human immunodeficiency virus and its CD4 cellular receptor. Structural enzymatic analysis. J. Exp. Med. 169 (1989) 807-822
17. Garcia-Palacios V., Yeon Chung H., Jin Choi S., Sarmasik A., Kurihara N., Won Lee J., Galson D.L., Collins R., and Roodman G.D. Eosinophil chemotactic factor-L (ECF-L) enhances osteoclast formation by increasing in osteoclast precursors expression of LFA-1 and ICAM-1. Bone 40 (2007) 316-322
18. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 3 (2003) 23-35
19. Han X., Sterling H., Chen Y., Saginario C., Brown E.J., Frazier W.A., Lindberg F.P., and Vignery A. CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J. Biol. Chem. 275 (2000) 37984-37992
20. Helming L., and Gordon S. Macrophage fusion induced by IL-4 alternative activation is a multistage process involving multiple target molecules. Eur. J. Immunol. 37 (2007) 33-42
21. Herbert D.R., Holscher C., Mohrs M., Arendse B., Schwegmann A., Radwanska M., Leeto M., Kirsch R., Hall P., Mossmann H., Claussen B., Forster I., and Brombacher F. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20 (2004) 623-635
22. Hernandez-Pando R., Orozcoe H., Sampieri A., Pavon L., Velasquillo C., Larriva-Sahd J., Alcocer J.M., and Madrid M.V. Correlation between the kinetics of Th1, Th2 cells and pathology in a murine model of experimental pulmonary tuberculosis. Immunology 89 (1996) 26-33
23. Higuchi S., Tabata N., Tajima M., Ito M., Tsurudome M., Sudo A., Uchida A., and Ito Y. Induction of human osteoclast-like cells by treatment of blood monocytes with anti-fusion regulatory protein-1/CD98 monoclonal antibodies. J. Bone Miner. Res. 13 (1998) 44-49
24. Humphrey M.B., Ogasawara K., Yao W., Spusta S.C., Daws M.R., Lane N.E., Lanier L.L., and Nakamura M.C. The signaling adapter protein DAP12 regulates multinucleation during osteoclast development. J. Bone Miner. Res. 19 (2004) 224-234
25. Ishii M., Iwai K., Koike M., Ohshima S., Kudo-Tanaka E., Ishii T., Mima T., Katada Y., Miyatake K., Uchiyama Y., and Saeki Y. RANKL-induced expression of tetraspanin CD9 in lipid raft membrane microdomain is essential for cell fusion during osteoclastogenesis. J. Bone Miner. Res. 21 (2006) 965-976
26. Ito Y., Komada H., Kusagawa S., Tsurudome M., Matsumura H., Kawano M., Ohta H., and Nishio M. Fusion regulation proteins on the cell surface: isolation and characterization of monoclonal antibodies which enhance giant polykaryocyte formation in Newcastle disease virus-infected cell lines of human origin. J. Virol. 66 (1992) 5999-6007
27. Kahnert A., Seiler P., Stein M., Bandermann S., Hahnke K., Mollenkopf H., and Kaufmann S.H. Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur. J. Immunol. 36 (2006) 631-647
28. Kaji K., Oda S., Shikano T., Ohnuki T., Uematsu Y., Sakagami J., Tada N., Miyazaki S., and Kudo A. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat. Genet. 24 (2000) 279-282
29. Kao W.J., McNally A.K., Hiltner A., and Anderson J.M. Role for interleukin-4 in foreign-body giant cell formation on a poly(etherurethane urea) in vivo. J. Biomed. Mater. Res. 29 (1995) 1267-1275
30. Kazazi F., Chang J., Lopez A., Vadas M., and Cunningham A.L. Interleukin 4 and human immunodeficiency virus stimulate LFA-1-ICAM-1-mediated aggregation of monocytes and subsequent giant cell formation. J. Gen. Virol. 75 Pt 10 (1994) 2795-2802
31. Ke H.Z., Qi H., Weidema A.F., Zhang Q., Panupinthu N., Crawford D.T., Grasser W.A., Paralkar V.M., Li M., Audoly L.P., Gabel C.A., Jee W.S., Dixon S.J., Sims S.M., and Thompson D.D. Deletion of the P2×7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol. Endocrinol. 17 (2003) 1356-1367
32. Kim M.S., Day C.J., Selinger C.I., Magno C.L., Stephens S.R., and Morrison N.A. MCP-1-induced human osteoclast-like cells are tartrate-resistant acid phosphatase, NFATc1, and calcitonin receptor-positive but require receptor activator of NFkappaB ligand for bone resorption. J. Biol. Chem. 281 (2006) 1274-1285
33. Kudo Y., and Boyd C.A. RNA interference-induced reduction in CD98 expression suppresses cell fusion during syncytialization of human placental BeWo cells. FEBS Lett. 577 (2004) 473-477
34. Kyriakides T.R., Foster M.J., Keeney G.E., Tsai A., Giachelli C.M., Clark-Lewis I., Rollins B.J., and Bornstein P. The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am. J. Pathol. 165 (2004) 2157-2166
35. Langhans T. Ueber Riesenzellen mit wandständigen Kernen in Tuberkeln und die fibröse Form des Tuberkels. Virchows Arch. Pathol. Anat. 42 (1868) 382-404
36. Lay G., Poquet Y., Salek-Peyron P., Puissegur M.P., Botanch C., Bon H., Levillain F., Duteyrat J.L., Emile J.F., and Altare F. Langhans giant cells from M. tuberculosis-induced human granulomas cannot mediate mycobacterial uptake. J. Pathol. 211 (2007) 76-85
37. Le Naour F., Rubinstein E., Jasmin C., Prenant M., and Boucheix C. Severely reduced female fertility in CD9-deficient mice. Science 287 (2000) 319-321
38. Lundberg P., Koskinen C., Baldock P.A., Lothgren H., Stenberg A., Lerner U.H., and Oldenborg P.A. Osteoclast formation is strongly reduced both in vivo and in vitro in the absence of CD47/SIRPalpha-interaction. Biochem. Biophys. Res. Commun. 352 (2007) 444-448
39. Marsh M., and Helenius A. Virus entry: open sesame. Cell 124 (2006) 729-740
40. Mbalaviele G., Chen H., Boyce B.F., Mundy G.R., and Yoneda T. The role of cadherin in the generation of multinucleated osteoclasts from mononuclear precursors in murine marrow. J. Clin. Invest. 95 (1995) 2757-2765
41. McInnes A., and Rennick D.M. Interleukin 4 induces cultured monocytes/macrophages to form giant multinucleated cells. J. Exp. Med. 167 (1988) 598-611
42. McNally A.K., and 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. 147 (1995) 1487-1499
43. McNally A.K., and Anderson J.M. Beta1 and beta2 integrins mediate adhesion during macrophage fusion and multinucleated foreign body giant cell formation. Am. J. Pathol. 160 (2002) 621-630
44. McNally A.K., DeFife K.M., and Anderson J.M. Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am. J. Pathol. 149 (1996) 975-985
45. Miyado K., Yamada G., Yamada S., Hasuwa H., Nakamura Y., Ryu F., Suzuki K., Kosai K., Inoue K., Ogura A., Okabe M., and Mekada E. Requirement of CD9 on the egg plasma membrane for fertilization. Science 287 (2000) 321-324
46. Mizuno K., Okamoto H., and Horio T. Muramyl dipeptide and mononuclear cell supernatant induce Langhans-type cells from human monocytes. J. Leukoc. Biol. 70 (2001) 386-394
47. Moore J.P., Trkola A., and Dragic T. Co-receptors for HIV-1 entry. Curr. Opin. Immunol. 9 (1997) 551-562
48. Mori K., Miyamoto N., Higuchi Y., Nanba K., Ito M., Tsurudome M., Nishio M., Kawano M., Uchida A., and Ito Y. Cross-talk between RANKL and FRP-1/CD98 systems: RANKL-mediated osteoclastogenesis is suppressed by an inhibitory anti-CD98 heavy chain mAb and CD98-mediated osteoclastogenesis is suppressed by osteoclastogenesis inhibitory factor. Cell. Immunol. 207 (2001) 118-126
49. Most J., Neumayer H.P., and Dierich M.P. Cytokine-induced generation of multinucleated giant cells in vitro requires interferon-gamma and expression of LFA-1. Eur. J. Immunol. 20 (1990) 1661-1667
50. Namba K., Nishio M., Mori K., Miyamoto N., Tsurudome M., Ito M., Kawano M., Uchida A., and Ito Y. Involvement of ADAM9 in multinucleated giant cell formation of blood monocytes. Cell. Immunol. 213 (2001) 104-113
51. Ohuchi M., Ohuchi R., Feldmann A., and Klenk H.D. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J. Virol. 71 (1997) 8377-8384
52. Okada Y., Morimoto I., Ura K., Watanabe K., Eto S., Kumegawa M., Raisz L., Pilbeam C., and Tanaka Y. Cell-to-cell adhesion via intercellular adhesion molecule-1 and leukocyte function-associated antigen-1 pathway is involved in 1alpha,25(OH)2D3, PTH and IL-1alpha-induced osteoclast differentiation and bone resorption. Endocr. J. 49 (2002) 483-495
53. Okamoto H., Mizuno K., and Horio T. Monocyte-derived multinucleated giant cells and sarcoidosis. J. Dermatol. Sci. 31 (2003) 119-128
54. Oldenborg P.A., Gresham H.D., and Lindberg F.P. CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J. Exp. Med. 193 (2001) 855-862
55. Rubinstein E., Ziyyat A., Prenant M., Wrobel E., Wolf J.P., Levy S., Le Naour F., and Boucheix C. Reduced fertility of female mice lacking CD81. Dev. Biol. 290 (2006) 351-358
56. Rubinstein E., Ziyyat A., Wolf J.P., Le Naour F., and Boucheix C. The molecular players of sperm-egg fusion in mammals. Semin. Cell. Dev. Biol. 17 (2006) 254-263
57. Saginario C., Sterling H., Beckers C., Kobayashi R., Solimena M., Ullu E., and Vignery A. MFR, a putative receptor mediating the fusion of macrophages. Mol. Cell Biol. 18 (1998) 6213-6223
58. Sollner T.H. Intracellular and viral membrane fusion: a uniting mechanism. Curr. Opin. Cell Biol. 16 (2004) 429-435
59. Staege H., Brauchlin A., Schoedon G., and Schaffner A. Two novel genes FIND and LIND differentially expressed in deactivated and Listeria-infected human macrophages. Immunogenetics 53 (2001) 105-113
60. Stein M., Keshav S., Harris N., and Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176 (1992) 287-292
61. Sterling H., Saginario C., and Vignery A. CD44 occupancy prevents macrophage multinucleation. J. Cell Biol. 143 (1998) 837-847
62. Tabata N., Ito M., Shimokata K., Suga S., Ohgimoto S., Tsurudome M., Kawano M., Matsumura H., Komada H., Nishio M., and Ito Y. Expression of fusion regulatory proteins (FRPs) on human peripheral blood monocytes. Induction of homotypic cell aggregation and formation of multinucleated giant cells by anti-FRP-1 monoclonal antibodies. J. Immunol. 153 (1994) 3256-3266
63. Tachibana I., and Hemler M.E. Role of transmembrane 4 superfamily (TM4SF) proteins CD9 and CD81 in muscle cell fusion and myotube maintenance. J. Cell Biol. 146 (1999) 893-904
64. Takashima T., Ohnishi K., Tsuyuguchi I., and Kishimoto S. Differential regulation of formation of multinucleated giant cells from concanavalin A-stimulated human blood monocytes by IFN-gamma and IL-4. J. Immunol. 150 (1993) 3002-3010
65. Takeda Y., Tachibana I., Miyado K., Kobayashi M., Miyazaki T., Funakoshi T., Kimura H., Yamane H., Saito Y., Goto H., Yoneda T., Yoshida M., Kumagai T., Osaki T., Hayashi S., Kawase I., and Mekada E. Tetraspanins CD9 and CD81 function to prevent the fusion of mononuclear phagocytes. J. Cell Biol. 161 (2003) 945-956
66. Vaananen H.K., Zhao H., Mulari M., and Halleen J.M. The cell biology of osteoclast function. J. Cell Sci. 113 Pt 3 (2000) 377-381
67. Vignery A. Macrophage fusion: the making of osteoclasts and giant cells. J. Exp. Med. 202 (2005) 337-340
68. Weinberg J.B., Hobbs M.M., and Misukonis M.A. Recombinant human gamma-interferon induces human monocyte polykaryon formation. Proc. Natl. Acad. Sci. USA 81 (1984) 4554-4557
69. Yagami-Hiromasa T., Sato T., Kurisaki T., Kamijo K., Nabeshima Y., and Fujisawa-Sehara A. A metalloprotease-disintegrin participating in myoblast fusion. Nature 377 (1995) 652-656
70. Yagi M., Miyamoto T., Sawatani Y., Iwamoto K., Hosogane N., Fujita N., Morita K., Ninomiya K., Suzuki T., Miyamoto K., Oike Y., Takeya M., Toyama Y., and Suda T. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J. Exp. Med. 202 (2005) 345-351
71. Yasuda H., Shima N., Nakagawa N., Yamaguchi K., Kinosaki M., Mochizuki S., Tomoyasu A., Yano K., Goto M., Murakami A., Tsuda E., Morinaga T., Higashio K., Udagawa N., Takahashi N., and Suda T. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA 95 (1998) 3597-3602
72. Yi T., Kim H.J., Cho J.Y., Woo K.M., Ryoo H.M., Kim G.S., and Baek J.H. Tetraspanin CD9 regulates osteoclastogenesis via regulation of p44/42 MAPK activity. Biochem. Biophys. Res. Commun. 347 (2006) 178-184
73. Zhao Q., Topham N., Anderson J.M., Hiltner A., Lodoen G., and Payet C.R. Foreign-body giant cells and polyurethane biostability: in vivo correlation of cell adhesion and surface cracking. J. Biomed. Mater. Res. 25 (1991) 177-183