Kinesin 5B is necessary for delivery of membrane and receptors during FcγR-mediated phagocytosis

Journal of Immunology

Volumn 186, Issue 2, 2011, Pages 816-825

  Silver, Kristen E ^a   Harrison, Rene E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; FC RECEPTOR; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN RECEPTOR; KINESIN 5; KINESIN 5B; MAC 1 RECEPTOR; RAB11 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; GENETIC TRANSFECTION; MACROPHAGE; MOLECULAR MECHANICS; MUTANT; OPSONIZATION; PHAGOCYTOSIS; PHAGOSOME; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PSEUDOPODIUM; SCANNING ELECTRON MICROSCOPY;

ANIMALS; CELL LINE; CELL POLARITY; DOWN-REGULATION; EXOCYTOSIS; INTRACELLULAR MEMBRANES; KINESIN; MICE; PHAGOCYTOSIS; PHAGOSOMES; PROTEIN BINDING; PROTEIN TRANSPORT; PSEUDOPODIA; RAB GTP-BINDING PROTEINS; RECEPTORS, IGG; SIGNAL TRANSDUCTION; SNARE PROTEINS; TRANSFECTION;

EID: 79251563457     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002161     Document Type: Article

References (46)

1. Greenberg, S., and S. Grinstein. 2002. Phagocytosis and innate immunity. Curr. Opin. Immunol. 14: 136-145.
2. Greenberg, S. 1999. Modular components of phagocytosis. J. Leukoc. Biol. 66: 712-717.
3. Greenberg, S. 1995. Signal transduction of phagocytosis. Trends Cell Biol. 5: 93-99.
4. May, R. C., and L. M. Machesky. 2001. Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114: 1061-1077.
5. Desjardins, M., J. E. Celis, G. van Meer, H. Dieplinger, A. Jahraus, G. Griffiths, and L. A. Huber. 1994. Molecular characterization of phagosomes. J. Biol. Chem. 269: 32194-32200.
6. Blocker, A., F. F. Severin, J. K. Burkhardt, J. B. Bingham, H. Yu, J. C. Olivo, T. A. Schroer, A. A. Hyman, and G. Griffiths. 1997. Molecular requirements for bidirectionalmovement of phagosomes alongmicrotubules. J. CellBiol. 137: 113-129.
7. Harrison, R. E., C. Bucci, O. V. Vieira, T. A. Schroer, and S. Grinstein. 2003. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell. Biol. 23: 6494-6506.
8. Bajno, L., X. R. Peng, A. D. Schreiber, H. P. Moore, W. S. Trimble, and S. Grinstein. 2000. Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation. J. Cell Biol. 149: 697-706.
9. Niedergang, F., and P. Chavrier. 2004. Signaling and membrane dynamics during phagocytosis: many roads lead to the phagos(R)ome. Curr. Opin. Cell Biol. 16: 422-428.
10. Braun, V., and F. Niedergang. 2006. Linking exocytosis and endocytosis during phagocytosis. Biol. Cell 98: 195-201.
11. Khandani, A., E. Eng, J. Jongstra-Bilen, A. D. Schreiber, D. Douda, P. Samavarchi-Tehrani, and R. E. Harrison. 2007. Microtubules regulate PI-3K activity and recruitment to the phagocytic cup during Fcgamma receptor-mediated phagocytosis in nonelicited macrophages. J. Leukoc. Biol. 82: 417-428.
12. Eng, E. W., A. Bettio, J. Ibrahim, and R. E. Harrison. 2007. MTOC reorientation occurs during FcgammaR-mediated phagocytosis in macrophages. Mol. Biol. Cell 18: 2389-2399.
13. Keller, H., and V. Niggli. 1995. Effects of cytochalasin D on shape and fluid pinocytosis in human neutrophils as related to cytoskeletal changes (actin, alpha-actinin and microtubules). Eur. J. Cell Biol. 66: 157-164.
14. Walczak, C. E. 2000. Microtubule dynamics and tubulin interacting proteins. Curr. Opin. Cell Biol. 12: 52-56.
15. Patel, P. C., K. H. Fisher, E. C. Yang, C. M. Deane, and R. E. Harrison. 2009. Proteomic analysis of microtubule-associated proteins during macrophage activation. Mol. Cell. Proteomics 8: 2500-2514.
16. Rivera, J., P. J. Chu, T. L. Lewis, Jr., and D. B. Arnold. 2007. The role of Kif5B in axonal localization of Kv1 K(+) channels. Eur. J. Neurosci. 25: 136-146.
17. Huynh, K. K., J. G. Kay, J. L. Stow, and S. Grinstein. 2007. Fusion, fission, and secretion during phagocytosis. Physiology (Bethesda) 22: 366-372.
18. Wiesner, C., J. Faix, M. Himmel, F. Bentzien, and S. Linder. 2010. KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 116: 1559-1569.
19. Rabinovitch, M., R. E. Manejias, and V. Nussenzweig. 1975. Selective phagocytic paralysis induced by immobilized immune complexes. J. Exp. Med. 142: 827-838.
20. Michl, J., M. M. Pieczonka, J. C. Unkeless, and S. C. Silverstein. 1979. Effects of immobilized immune complexes on Fc- and complement-receptor function in resident and thioglycollate-elicited mouse peritoneal macrophages. J. Exp. Med. 150: 607-621.
21. Cannon, G. J., and J. A. Swanson. 1992. The macrophage capacity for phagocytosis. J. Cell Sci. 101: 907-913.
22. Marshall, J. G., J. W. Booth, V. Stambolic, T. Mak, T. Balla, A. D. Schreiber, T. Meyer, and S. Grinstein. 2001. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis. J. Cell Biol. 153: 1369-1380.
23. Jongstra-Bilen, J., R. Harrison, and S. Grinstein. 2003. Fcgamma-receptors induce Mac-1 (CD11b/CD18) mobilization and accumulation in the phagocytic cup for optimal phagocytosis. J. Biol. Chem. 278: 45720-45729.
24. Touret, N., P. Paroutis, M. Terebiznik, R. E. Harrison, S. Trombetta, M. Pypaert, A. Chow, A. Jiang, J. Shaw, C. Yip, et al. 2005. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123: 157-170.
25. Tapper, H., W. Furuya, and S. Grinstein. 2002. Localized exocytosis of primary (lysosomal) granules during phagocytosis: role of Ca2+-dependent tyrosine phosphorylation and microtubules. J. Immunol. 168: 5287-5296. (Pubitemid 34495997)
26. Nishida, K., S. Yamasaki, Y. Ito, K. Kabu, K. Hattori, T. Tezuka, H. Nishizumi, D. Kitamura, R. Goitsuka, R. S. Geha, et al. 2005. FcepsilonRI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell Biol. 170: 115-126.
27. Rothwell, S. W., C. C. Deal, J. Pinto, and D. G. Wright. 1993. Affinity purifi- cation and subcellular localization of kinesin in human neutrophils. J. Leukoc. Biol. 53: 372-380.
28. Damiani, M. T., and M. I. Colombo. 2003. Microfilaments and microtubules regulate recycling from phagosomes. Exp. Cell Res. 289: 152-161.
29. Harrison, P. T., W. Davis, J. C. Norman, A. R. Hockaday, and J. M. Allen. 1994. Binding of monomeric immunoglobulin G triggers Fc gamma RI-mediated endocytosis. J. Biol. Chem. 269: 24396-24402.
30. Patel, P. C., and R. E. Harrison. 2008. Membrane ruffles capture C3bi-opsonized particles in activated macrophages. Mol. Biol. Cell 19: 4628-4639.
31. Aderem, A., and D. M. Underhill. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17: 593-623.
32. Rodionov, V. I., F. K. Gyoeva, E. Tanaka, A. D. Bershadsky, J. M. Vasiliev, and V. I. Gelfand. 1993. Microtubule-dependent control of cell shape and pseudopodial activity is inhibited by the antibody to kinesin motor domain. J. Cell Biol. 123: 1811-1820.
33. Lin, S. X., G. G. Gundersen, and F. R. Maxfield. 2002. Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol. Biol. Cell 13: 96-109.
34. Binker, M. G., D. Y. Zhao, S. J. Pang, and R. E. Harrison. 2007. Cytoplasmic linker protein-170 enhances spreading and phagocytosis in activated macrophages by stabilizing microtubules. J. Immunol. 179: 3780-3791.
35. Desjardins, M. 1995. Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 5: 183-186.
36. Lee, W. L., M. K. Kim, A. D. Schreiber, and S. Grinstein. 2005. Role of ubiquitin and proteasomes in phagosome maturation. Mol. Biol. Cell 16: 2077-2090.
37. Botelho, R. J., D. J. Hackam, A. D. Schreiber, and S. Grinstein. 2000. Role of COPI in phagosome maturation. J. Biol. Chem. 275: 15717-15727.
38. Vale, R. D., and H. Hotani. 1988. Formation of membrane networks in vitro by kinesin-driven microtubule movement. J. Cell Biol. 107: 2233-2241.
39. Ward, E. S., C. Martinez, C. Vaccaro, J. Zhou, Q. Tang, and R. J. Ober. 2005. From sorting endosomes to exocytosis: association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol. Biol. Cell 16: 2028-2038.
40. Toyoshima, I., H. Yu, E. R. Steuer, and M. P. Sheetz. 1992. Kinectin, a major kinesin-binding protein on ER. J. Cell Biol. 118: 1121-1131.
41. Hotta, K., K. Tanaka, A. Mino, H. Kohno, and Y. Takai. 1996. Interaction of the Rho family small G proteins with kinectin, an anchoring protein of kinesin motor. Biochem. Biophys. Res. Commun. 225: 69-74.
42. Hollenbeck, P. J., and J. A. Swanson. 1990. Radial extension of macrophage tubular lysosomes supported by kinesin. Nature 346: 864-866.
43. Swanson, J. A., A. Locke, P. Ansel, and P. J. Hollenbeck. 1992. Radial movement of lysosomes along microtubules in permeabilized macrophages. J. Cell Sci. 103: 201-209.
44. Raghavan, M., and P. J. Bjorkman. 1996. Fc receptors and their interactions with immunoglobulins. Annu. Rev. Cell Dev. Biol. 12: 181-220.
45. Nagarajan, S., S. Chesla, L. Cobern, P. Anderson, C. Zhu, and P. Selvaraj. 1995. Ligand binding and phagocytosis by CD16 (Fc gamma receptor III) isoforms. Phagocytic signaling by associated zeta and gamma subunits in Chinese hamster ovary cells. J. Biol. Chem. 270: 25762-25770.
46. Guyre, C. A., T. Keler, S. L. Swink, L. A. Vitale, R. F. Graziano, and M. W. Fanger. 2001. Receptor modulation by Fc gamma RI-specific fusion proteins is dependent on receptor number and modified by IgG. J. Immunol. 167: 6303-6311.