Differential requirement of lipid rafts for FcγRIIA mediated effector activities

Cellular Immunology

Volumn 265, Issue 2, 2010, Pages 111-119

  Vieth, Joshua A ^a   Kim, Moo kyung ^b   Pan, Xiao Qing ^b   Schreiber, Alan D ^b   Worth, Randall G ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Endocytosis; Fc receptors; Methyl cyclodextrin; Phagocytosis

Indexed keywords

FC RECEPTOR IIA; IMMUNOGLOBULIN G; METHYL BETA CYCLODEXTRIN;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; INTERNALIZATION; LIGAND BINDING; LIPID RAFT; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; WESTERN BLOTTING;

ANIMALS; BETA-CYCLODEXTRINS; CHO CELLS; CRICETINAE; CRICETULUS; ENDOCYTOSIS; HUMANS; IMMUNOGLOBULIN G; LIGANDS; MEMBRANE MICRODOMAINS; PHAGOCYTOSIS; PROTEIN BINDING; RECEPTORS, IGG;

EID: 77957016992     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2010.07.011     Document Type: Article

References (59)

1. Gavin A.L., Barnes N., Dijstelbloem H.M., Hogarth P.M. Identification of the mouse IgG3 receptor: implications for antibody effector function at the interface between innate and adaptive immunity. J. Immunol. 1998, 160:20-23.
2. Joshi T., Butchar J.P., Tridandapani S. Fc gamma receptor signaling in phagocytes. Int. J. Hematol. 2006, 84:210-216.
3. Hulett M.D., Hogarth P.M. Molecular basis of Fc receptor function. Adv. Immunol. 1994, 57:1-127.
4. Ravetch J.V., Kinet J.P. Fc receptors. Annu. Rev. Immunol. 1991, 9:457-492.
5. Ganesan L.P., Joshi T., Fang H., Kutala V.K., Roda J., Trotta R., Lehman A., Kuppusamy P., Byrd J.C., Carson W.E., Caligiuri M.A., Tridandapani S. Fc gammaR-induced production of superoxide and inflammatory cytokines is differentially regulated by SHIP through its influence on PI3K and/or Ras/Erk pathways. Blood 2006, 108:718-725.
6. Imamichi T., Koyama J. Two distinct types of Fc receptor for IgG on guinea pig macrophages activate the NADPH oxidase through different signal-transduction pathways. Biochem. Biophys. Res. Commun. 1990, 172:223-228.
7. Tamoto K., Koyama J. Superoxide anion production from guinea pig macrophages stimulated with immune complexes of different IgG subclasses. J. Biochem. 1980, 87:1649-1657.
8. Trivedi V., Zhang S.C., Castoreno A.B., Stockinger W., Shieh E.C., Vyas J.M., Frickel E.M., Nohturfft A. Immunoglobulin G signaling activates lysosome/phagosome docking. Proc. Natl. Acad. Sci. USA 2006, 103:18226-18231.
9. Gessner J.E., Heiken H., Tamm A., Schmidt R.E. The IgG Fc receptor family. Ann. Hematol. 1998, 76:231-248.
10. Cambier J.C. Antigen and Fc receptor signaling. The awesome power of the immunoreceptor tyrosine-based activation motif (ITAM). J. Immunol. 1995, 155:3281-3285.
11. Van den Herik-Oudijk I.E., Ter Bekke M.W., Tempelman M.J., Capel P.J., Van de Winkel J.G. Functional differences between two Fc receptor ITAM signaling motifs. Blood 1995, 86:3302-3307.
12. Worth R.G., Schreiber A.D. Fc Receptor Phagocytosis 2005, Springer.
13. Tse S.M., Furuya W., Gold E., Schreiber A.D., Sandvig K., Inman R.D., Grinstein S. Differential role of actin Clathrin, and dynamin in Fc gamma receptor-mediated endocytosis and phagocytosis. J. Biol. Chem. 2003, 278:3331-3338.
14. Huang Z.Y., Barreda D.R., Worth R.G., Indik Z.K., Kim M.K., Chien P., Schreiber A.D. Differential kinase requirements in human and mouse Fc-gamma receptor phagocytosis and endocytosis. J. Leukoc. Biol. 2006, 80:1553-1562.
15. Booth J.W., Kim M.K., Jankowski A., Schreiber A.D., Grinstein S. Contrasting requirements for ubiquitylation during Fc receptor-mediated endocytosis and phagocytosis. EMBO J. 2002, 21:251-258.
16. Worth R.G., Mayo-Bond L., Kim M.K., van de Winkel J.G., Todd R.F., Petty H.R., Schreiber A.D. The cytoplasmic domain of Fc gamma RIIA (CD32) participates in phagolysosome formation. Blood 2001, 98:3429-3434.
17. Indik Z.K., Park J.G., Hunter S., Mantaring M., Schreiber A.D. Molecular dissection of Fc gamma receptor-mediated phagocytosis. Immunol. Lett. 1995, 44:133-138.
18. Mitchell M.A., Huang M.M., Chien P., Indik Z.K., Pan X.Q., Schreiber A.D. Substitutions and deletions in the cytoplasmic domain of the phagocytic receptor Fc gamma RIIA: effect on receptor tyrosine phosphorylation and phagocytosis. Blood 1994, 84:1753-1759.
19. Indik Z.K., Mitchell M.A., Chien P., Schreiber A.D. Structural requirements for phagocytosis by the human Fc receptor Fc gamma RIIA. Trans. Assoc. Am. Physicians 1993, 106:77-85.
20. R.G. Worth, M.K. Kim, A.L. Kindzelskii, H.R. Petty, and A.D. Schreiber, Signal sequence within Fc{gamma}RIIA controls calcium wave propagation patterns: Apparent role in phagolysosome fusion, Proc. Natl. Acad. Sci. USA (2003).
21. Alijani A., Hanna G.B., Cuschieri A. Abdominal wall lift versus positive-pressure capnoperitoneum for laparoscopic cholecystectomy: randomized controlled trial. Ann. Surg. 2004, 239:388-394.
22. Hoessli D.C., Ilangumaran S., Soltermann A., Robinson P.J., Borisch B., Nasir Ud D. Signaling through sphingolipid microdomains of the plasma membrane: the concept of signaling platform. Glycoconj. J. 2000, 17:191-197.
23. Kono H., Suzuki T., Yamamoto K., Okada M., Yamamoto T., Honda Z. Spatial raft coalescence represents an initial step in Fc gamma R signaling. J. Immunol. 2002, 169:193-203.
24. Flaswinkel H., Barner M., Reth M. The tyrosine activation motif as a target of protein tyrosine kinases and SH2 domains. Semin. Immunol. 1995, 7:21-27.
25. Ghazizadeh S., Bolen J.B., Fleit H.B. Tyrosine phosphorylation and association of Syk with Fc gamma RII in monocytic THP-1 cells. Biochem. J. 1995, 305(2):669-674.
26. Greenberg S. Modular components of phagocytosis. J. Leukoc. Biol. 1999, 66:712-717.
27. Hunter S., Kamoun M., Schreiber A.D. Transfection of an Fc gamma receptor cDNA induces T cells to become phagocytic. Proc. Natl. Acad. Sci. USA 1994, 91:10232-10236.
28. Engelhardt W., Gorczytza H., Butterweck A., Monkemann H., Frey J. Structural requirements of the cytoplasmic domains of the human macrophage Fc gamma receptor IIa and B cell Fc gamma receptor IIb2 for the endocytosis of immune complexes. Eur. J. Immunol. 1991, 21:2227-2238.
29. Ukkonen P., Lewis V., Marsh M., Helenius A., Mellman I. Transport of macrophage Fc receptors and Fc receptor-bound ligands to lysosomes. J. Exp. Med. 1986, 163:952-971.
30. Garcia-Garcia E., Brown E.J., Rosales C. Transmembrane mutations to FcgammaRIIA alter its association with lipid rafts: implications for receptor signaling. J. Immunol. 2007, 178:3048-3058.
31. Barnes N.C., Powell M.S., Trist H.M., Gavin A.L., Wines B.D., Hogarth P.M. Raft localisation of Fc gamma RIIa and efficient signaling are dependent on palmitoylation of cysteine 208. Immunol. Lett. 2006, 104:118-123.
32. Mousavi S.A., Sporstol M., Fladeby C., Kjeken R., Barois N., Berg T. Receptor-mediated endocytosis of immune complexes in rat liver sinusoidal endothelial cells is mediated by Fc gamma RIIb2. Hepatology 2007, 46:871-884.
33. Bournazos S., Hart S.P., Chamberlain L.H., Glennie M.J., Dransfield I. Association of Fc gamma RIIa (CD32a) with lipid rafts regulates ligand binding activity. J. Immunol. 2009, 182:8026-8036.
34. Wessel D., Flugge U.I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 1984, 138:141-143.
35. Worth R.G., Chien C.D., Chien P., Reilly M.P., McKenzie S.E., Schreiber A.D. Platelet Fc gamma RIIA binds and internalizes IgG-containing complexes. Exp. Hematol. 2006, 34:1490-1495.
36. Barenholz Y. Sphingomyelin and cholesterol: from membrane biophysics and rafts to potential medical applications. Subcell Biochem. 2004, 37:167-215.
37. Ostrom R.S., Liu X. Detergent and detergent-free methods to define lipid rafts and caveolae. Meth. Mol. Biol. 2007, 400:459-468.
38. Zidovetzki R., Levitan I. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta 2007, 1768:1311-1324.
39. Romanenko V.G., Fang Y., Byfield F., Travis A.J., Vandenberg C.A., Rothblat G.H., Levitan I. Cholesterol sensitivity and lipid raft targeting of Kir2.1 channels. Biophys. J. 2004, 87:3850-3861.
40. Astarie-Dequeker C., Le Guyader L., Malaga W., Seaphanh F.K., Chalut C., Lopez A., Guilhot C. Phthiocerol dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog. 2009, 5:e1000289.
41. Le Cabec V., Carreno S., Moisand A., Bordier C., Maridonneau-Parini I. Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during non-opsonic and opsonic phagocytosis respectively. J. Immunol. 2002, 169:2003-2009.
42. Peyron P., Bordier C., N'Diaye E.N., Maridonneau-Parini I. Nonopsonic phagocytosis of Mycobacterium kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol-anchored proteins. J. Immunol. 2000, 165:5186-5191.
43. Cuschieri J. Implications of lipid raft disintegration: enhanced anti-inflammatory macrophage phenotype. Surgery 2004, 136:169-175.
44. Cuschieri J., Bulmus V., Gourlay D., Garcia I., Hoffman A., Stayton P., Maier R.V. Modulation of macrophage responsiveness to lipopolysaccharide by IRAK-1 manipulation. Shock 2004, 21:182-188.
45. Cuschieri J., Umanskiy K., Solomkin J. PKC-zeta is essential for endotoxin-induced macrophage activation. J. Surg. Res. 2004, 121:76-83.
46. Worth R.G., Mayo-Bond L., van de Winkel J.G., Todd R.F., Petty H.R. CR3 (alphaM beta2; CD11b/CD18) restores IgG-dependent phagocytosis in transfectants expressing a phagocytosis-defective Fc gammaRIIA (CD32) tail-minus mutant. J. Immunol. 1996, 157:5660-5665.
47. Mukherjee S., Ghosh R.N., Maxfield F.R. Endocytosis. Physiol. Rev. 1997, 77:759-803.
48. Allen L.A., Aderem A. Mechanisms of phagocytosis. Curr. Opin. Immunol. 1996, 8:36-40.
49. Walters M.N., Papadimitriou J.M. Phagocytosis: a review. CRC Crit. Rev. Toxicol. 1978, 5:377-421.
50. Hinkovska-Galcheva V., Boxer L.A., Kindzelskii A., Hiraoka M., Abe A., Goparju S., Spiegel S., Petty H.R., Shayman J.A. Ceramide 1-phosphate, a mediator of phagocytosis. J. Biol. Chem. 2005, 280:26612-26621.
51. Mansfield P.J., Hinkovska-Galcheva V., Borofsky M.S., Shayman J.A., Boxer L.A. Phagocytic signaling molecules in lipid rafts of COS-1 cells transfected with Fc gamma RIIA. Biochem. Biophys. Res. Commun. 2005, 331:132-138.
52. Kwiatkowska K., Frey J., Sobota A. Phosphorylation of Fc gamma RIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J. Cell Sci. 2003, 116:537-550.
53. Korzeniowski M., Kwiatkowska K., Sobota A. Insights into the association of Fc gamma RII and TCR with detergent-resistant membrane domains: isolation of the domains in detergent-free density gradients facilitates membrane fragment reconstitution. Biochemistry 2003, 42:5358-5367.
54. Abdel Shakor A.B., Kwiatkowska K., Sobota A. Cell surface ceramide generation precedes and controls Fc gamma RII clustering and phosphorylation in rafts. J. Biol. Chem. 2004, 279:36778-36787.
55. Strzelecka-Kiliszek A., Korzeniowski M., Kwiatkowska K., Mrozinska K., Sobota A. Activated Fc gamma RII and signalling molecules revealed in rafts by ultra-structural observations of plasma-membrane sheets. Mol. Membr. Biol. 2004, 21:101-108.
56. Mero P., Zhang C.Y., Huang Z.Y., Kim M.K., Schreiber A.D., Grinstein S., Booth J.W. Phosphorylation-independent ubiquitylation and endocytosis of Fc gamma RIIA. J. Biol. Chem. 2006, 281:33242-33249.
57. Yeung T., Gilbert G.E., Shi J., Silvius J., Kapus A., Grinstein S. Membrane phosphatidylserine regulates surface charge and protein localization. Science 2008, 319:210-213.
58. Yeung T., Terebiznik M., Yu L., Silvius J., Abidi W.M., Philips M., Levine T., Kapus A., Grinstein S. Receptor activation alters inner surface potential during phagocytosis. Science 2006, 313:347-351.
59. Bakht O., Pathak P., London E. Effect of the structure of lipids favoring disordered domain formation on the stability of cholesterol-containing ordered domains (lipid rafts): identification of multiple raft-stabilization mechanisms. Biophys. J. 2007, 93:4307-4318.