Fusion between Phagosomes, Early and Late Endosomes: A Role for Actin in Fusion between Late, but Not Early Endocytic Organelles

Kjeken, Rune, Egeberg, Morten, Habermann, Anja, Kuehnel, Mark, Peyron, Pascale, Floetenmeyer, Matthias, Walther, Paul, Jahraus, Andrea, Defacque, Hélène, Kuznetsov, Sergei A. and Griffiths, Gareth (2004) Fusion between Phagosomes, Early and Late Endosomes: A Role for Actin in Fusion between Late, but Not Early Endocytic Organelles. Molecular Biology of The Cell, 15 1: 345-358. doi:10.1091/mbc.E03-05-0334

Attached Files (Some files may be inaccessible until you login with your UQ eSpace credentials)
Name Description MIMEType Size Downloads
UQ160087_OA.pdf Full text (open access) application/pdf 1.84MB 0

Author Kjeken, Rune
Egeberg, Morten
Habermann, Anja
Kuehnel, Mark
Peyron, Pascale
Floetenmeyer, Matthias
Walther, Paul
Jahraus, Andrea
Defacque, Hélène
Kuznetsov, Sergei A.
Griffiths, Gareth
Title Fusion between Phagosomes, Early and Late Endosomes: A Role for Actin in Fusion between Late, but Not Early Endocytic Organelles
Journal name Molecular Biology of The Cell   Check publisher's open access policy
ISSN 1059-1524
Publication date 2004-01-01
Year available 2004
Sub-type Article (original research)
DOI 10.1091/mbc.E03-05-0334
Open Access Status File (Publisher version)
Volume 15
Issue 1
Start page 345
End page 358
Total pages 14
Place of publication Bethesda MD
Publisher American Society for Cell Biology
Language eng
Subject 0601 Biochemistry and Cell Biology
06 Biological Sciences
Abstract Actin is implicated in membrane fusion, but the precise mechanisms remain unclear. We showed earlier that membrane organelles catalyze the de novo assembly of F-actin that then facilitates the fusion between latex bead phagosomes and a mixture of early and late endocytic organelles. Here, we correlated the polymerization and organization of F-actin with phagosome and endocytic organelle fusion processes in vitro by using biochemistry and light and electron microscopy. When membrane organelles and cytosol were incubated at 37°C with ATP, cytosolic actin polymerized rapidly and became organized into bundles and networks adjacent to membrane organelles. By 30-min incubation, a gel-like state was formed with little further polymerization of actin thereafter. Also during this time, the bulk of in vitro fusion events occurred between phagosomes/endocytic organelles. The fusion between latex bead phagosomes and late endocytic organelles, or between late endocytic organelles themselves was facilitated by actin, but we failed to detect any effect of perturbing F-actin polymerization on early endosome fusion. Consistent with this, late endosomes, like phagosomes, could nucleate F-actin, whereas early endosomes could not. We propose that actin assembled by phagosomes or late endocytic organelles can provide tracks for fusion-partner organelles to move vectorially toward them, via membrane-bound myosins, to facilitate fusion.
References * Anes, E., Kuhnel, M.P., Bos, E., Pereira, J.M., Habermann, A., and Griffiths, G. (2003). Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat. Cell Biol. 5:, 793-802. [PubMed]. * Al-Haddad, A., et al. (2001). Myosin Va bound to phagosomes binds to F-actin and delays microtubule-dependent motility. Mol. Biol. Cell 12:, 2742-2755. [PubMed]. * Allen, L.H., and Aderem, A. (1995). A role for MARCKS, the alpha isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J. Exp. Med. 182:, 829-840. [PubMed]. * Amann, K.J., and Pollard, T.D. (2000). Cellular regulation of actin network assembly. Curr. Biol. 10:, R728-730. [PubMed]. * Bader, M.F., Holz, R.W., Kumakura, K., and Vitale, N. (2002). Exocytosis: the chromaffin cell as a model system. Ann. N.Y. Acad. Sci. 971:, 178-183. [PubMed]. * Bernstein, B.W., DeWit, M., and Bamburg, J.R. (1998). Actin disassembles reversibly during electrically induced recycling of synaptic vesicles in cultured neurons. Brain Res. Mol. Brain Res. 53:, 236-251. [PubMed]. * Blocker, A., Severin, F.F., Habermann, A., Hyman, A.A., Griffiths, G., and Burkhardt, J.K. (1996). Microtubule-associated protein-dependent binding of phagosomes to microtubules. J. Biol. Chem. 271:, 3803-3811. [PubMed]. * Burgoyne, R.D., and Cheek, T.R. (1987). Reorganisation of peripheral actin filaments as a prelude to exocytosis. Biosci. Rep. 7:, 281-288. [PubMed]. * Buss, F., Arden, S.D., Lindsay, M., Luzio, J.P., and Kendrick-Jones, J. (2001). Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J. 20:, 3676-3684. [PubMed]. * Cano, M.L., Cassimeris, L., Joyce, M., and Zigmond, S.H. (1992). Characterization of tetramethylrhodaminyl-phalloidin binding to cellular F-actin. Cell Motil. Cytoskeleton 21:, 147-158. * Carlier, M.F. (1998). Control of actin dynamics. Curr. Opin. Cell Biol. 10:, 45-51. [PubMed]. * Carlier, M.F., and Pantaloni, D. (1994). Actin assembly in response to extracellular signals: role of capping proteins, thymosin beta 4 and profilin. Semin. Cell Biol. 5:, 183-191. * Carraway, K.L., and Carraway, C.A. (1989). Membrane-cytoskeleton interactions in animal cells. Biochim. Biophys. Acta 988:, 147-171. [PubMed]. * Cordonnier, M.N., Dauzonne, D., Louvard, D., and Coudrier, E. (2001). Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell 12:, 4013-4029. [PubMed]. * Cox, D., Berg, J.S., Cammer, M., Chinegwundoh, J.O., Dale, B.M., Cheney, R.E., and Greenberg, S. (2002). Myosin X is a downstream effector of PI(3)K during phagocytosis. Nat. Cell Biol. 4:, 469-477. [PubMed]. * Defacque, H., Bos, E., Garvalov, B., Barret, C., Roy, C., Mangeat, P., Shin, H.W., Rybin, V., and Griffiths, G. (2002). Phosphoinositides regulate membrane-dependent actin assembly by latex bead phagosomes. Mol. Biol. Cell 13:, 1190-1202. [PubMed]. * Defacque, H., Egeberg, M., Antzberger, A., Ansorge, W., Way, M., and Griffiths, G. (2000b). Actin assembly induced by polylysine beads or purified phagosomes: Quantitation by a new flow cytometry assay. Cytometry 41:, 46-54. [PubMed]. * Defacque, H., et al. (2000a). Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO J. 19:, 199-212. [PubMed]. * DePina, A.S., and Langford, G.M. (1999). Vesicle transport: the role of actin filaments and myosin motors. Microsc. Res. Tech. 47:, 93-106. [PubMed]. * Desjardins, M., and Griffiths, G. (2003). Phagocytosis: latex leads the way. Curr. Opin. Cell Biol. 15:, 498-503. [PubMed]. * Diakonova, M., Bokoch, G., and Swanson, J.A. (2002). Dynamics of cytoskeletal proteins during Fcgamma receptor-mediated phagocytosis in macrophages. Mol. Biol. Cell 13:, 402-411. [PubMed]. * Diaz, R., Mayorga, L., and Stahl, P. (1988). In vitro fusion of endosomes following receptor-mediated endocytosis. J. Biol. Chem. 263:, 6093-6100. [PubMed]. * Dickinson, R.B., and Purich, D.L. (2002). Clamped filament elongation model for actin-based motors. Biophys. J. 82:, 605-617. [PubMed]. * Durrbach, A., Louvard, D., and Coudrier, E. (1996). Actin filaments facilitate two steps of endocytosis. J. Cell Sci. 109:, 457-465. [PubMed]. * Durrbach, A., Raposo, G., Tenza, D., Louvard, D., and Coudrier, E. (2000). Truncated brush border myosin I affects membrane traffic in polarized epithelial cells. Traffic 1:, 411-424. [PubMed]. * Eitzen, G., Wang, L., Thorngren, N., and Wickner, W. (2002). Remodeling of organelle-bound actin is required for yeast vacuole fusion. J. Cell Biol. 158:, 669-679. [PubMed]. * Emans, N., and Verkman, A.S. (1996). Real-time fluorescence measurement of cell-free endosome fusion: regulation by second messengers. Biophys. J. 71:, 487-494. [PubMed]. * Foissner, I., Lichtscheidl, I.K., and Wasteneys, G.O. (1996). Actin-based vesicle dynamics and exocytosis during wound wall formation in characean internodal cells. Cell Motil. Cytoskeleton 35:, 35-48. [PubMed]. * Griffiths, G. (1993). Fine Structure Immunocytochemistry. Springer, Berlin. * Harder, T., Kellner, R., Parton, R.G., and Gruenberg, J. (1997). Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8:, 533-545. [PubMed]. * Hasson, T., and Cheney, R.E. (2001). Mechanisms of motor protein reversal. Curr. Opin. Cell Biol. 13:, 29-35. [PubMed]. * Hermann, R., Walther, P., and Muller, M. (1996). Immunogold labeling in scanning electron microscopy. Histochem. Cell Biol. 106:, 31-39. [PubMed]. * Horiuchi, H., et al. (1997). A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90:, 1149-1159. [PubMed]. * Hoglund, A.S., Karlsson, R., Arro, E., Fredriksson, B.A., and Lindberg, U. (1980). Visualization of the peripheral weave of microfilaments in glia cells. J. Muscle Res. Cell Motil. 1:, 127-146. [PubMed]. * Jahraus, A., Egeberg, M., Hinner, B., Habermann, A., Sackmann, E., Pralle, A., Faulstich, H., Rybin, V., Defacque, H., and Griffiths, G. (2001). ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol. Biol. Cell 12:, 155-170. [PubMed]. * Jahraus, A., Tjelle, T.E., Berg, T., Habermann, A., Storrie, B., Ullrich, O., and Griffiths, G. (1998). In vitro fusion of phagosomes with different endocytic organelles from J774 macrophages. J. Biol. Chem. 273:, 30379-30390. [PubMed]. * Kellogg, D.R., Mitchison, T.J., and Alberts, B.M. (1988). Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103:, 675-686. [PubMed]. * Lang, T., Wacker, I., Wunderlich, I., Rohrbach, A., Giese, G., Soldati, T., and Almers, W. (2000). Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys. J. 78:, 2863-2877. [PubMed]. * Lee, E., and Knecht, D.A. (2002). Visualization of actin dynamics during macropinocytosis and exocytosis. Traffic 3:, 186-192. [PubMed]. * Lindberg, U., Hoglund, A.S., and Karlsson, R. (1981). On the ultrastructural organization of the microfilament system and the possible role of profilactin. Biochimie 63:, 307-323. [PubMed]. * Machesky, L.M., and Insall, R.H. (1999). Signaling to actin dynamics. J. Cell Biol. 146:, 267-272. [PubMed]. * Merrifield, C.J., Moss, S.E., Ballestrem, C., Imhof, B.A., Giese, G., Wunderlich, I., and Almers, W. (1999). Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat. Cell Biol. 1:, 72-74. [PubMed]. * Mitchison, T.J., and Cramer, L.P. (1996). Actin-based cell motility and cell locomotion. Cell 84:, 371-379. [PubMed]. * Neuhaus, E.M., and Soldati, T. (2000). A myosin I is involved in membrane recycling from early endosomes. J. Cell Biol. 150:, 1013-1026. [PubMed]. * Olazabal, I.M., Caron, E., May, R.C., Schilling, K., Knecht, D.A., and Machesky, L.M. (2002). Rho-kinase and myosin-II control phagocytic cup formation during CR, but not FcgammaR, phagocytosis. Curr. Biol. 12:, 1413-1418. [PubMed]. * Orci, L., Gabbay, K.H., and Malaisse, W.J. (1972). Pancreatic beta-cell web: its possible role in insulin secretion. Science 175:, 1128-1130. [PubMed]. * Pruyne, D., and Bretscher, A. (2000). Polarization of cell growth in yeast. J. Cell Sci. 113:, 571-585. [PubMed]. * Reck-Peterson, S.L., Provance, D.W., Jr., Mooseker, M.S., and Mercer, J.A. (2000). Class V myosins. Biochim. Biophys. Acta 1496:, 36-51. [PubMed]. * Riezman, H., Munn, A., Geli, M.I., and Hicke, L. (1996). Actin-, myosin- and ubiquitin-dependent endocytosis. Experientia 52:, 1033-1041. [PubMed]. * Rozelle, A.L., Machesky, L.M., Yamamoto, M., Driessens, M.H., Insall, R.H., Roth, M.G., Luby-Phelps, K., Marriott, G., Hall, A., and Yin, H.L. (2000). Phosphatidylinositol 4, 5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10:, 311-320. [PubMed]. * Safer, D., and Nachmias, V.T. (1994). Beta thymosins as actin binding peptides. Bioessays 16:, 590 [PubMed]. * Small, J.V., Rottner, K., and Kaverina, I. (1999). Functional design in the actin cytoskeleton. Curr. Opin. Cell Biol. 11:, 54-60. [PubMed]. * Southwick, F.S., Li, W., Zhang, F., Zeile, W.L., and Purich, D.L. (2003). Actin-based endosome and phagosome rocketing in macrophages: activation by the secretagogue antagonists lanthanum and zinc. Cell Motil. Cytoskeleton 54:, 41-55. [PubMed]. * Swanson, J.A., Johnson, M.T., Beningo, K., Post, P., Mooseker, M., and Araki, N. (1999). A contractile activity that closes phagosomes in macrophages. J. Cell Sci. 112:, 307-316. [PubMed]. * Taunton, J., Rowning, B.A., Coughlin, M.L., Wu, M., Moon, R.T., Mitchison, T.J., and Larabell, C.A. (2000). Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148:, 519-530. [PubMed]. * Tilney, L.G. (1975). The role of actin in nonmuscle cell motility. Soc. Gen. Physiol. Ser. 30:, 339-388. [PubMed]. * Tilney, L.G. (1976). Actin: its association with membranes and the regulation of its polymerization. In: International Cell Biology 1976–1977, eds. B.R. Brinkley and K.R. Porter, New York: Rockefeller University Press, 388-402. * Tilney, L.G., and Cardell, Jr., R.R. (1970). Factors controlling the reassembly of the microvillous border of the small intestine of the salamander. J. Cell Biol. 47:, 408-422. * Tilney, L.G., and Mooseker, M.S. (1976). Actin filament-membrane attachment: are membrane particles involved? J. Cell Biol. 71:, 402-416. [PubMed]. * Tokuyasu, K.T. (1978). A study of positive staining of ultrathin frozen sections. J. Ultrastruct. Res. 63:, 287-307. [PubMed]. * Trifaro, J.M., Rodriguez del Castillo, A., and Vitale, M.L. (1992). Dynamic changes in chromaffin cell cytoskeleton as prelude to exocytosis. Mol. Neurobiol. 6:, 339-358. [PubMed]. * Wang, L., Merz, A.J., Collins, K.M., and Wickner, W. (2003). Hierarchy of protein assembly at the vertex ring domain for yeast vacuole docking and fusion. J. Cell Biol. 160:, 365-374. [PubMed]. * Wang, L., Seeley, E.S., Wickner, W., and Merz, A.J. (2002). Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle. Cell 108:, 357-369. [PubMed]. * Wu, X., Jung, G., and Hammer, J. A., 3rd. (2000). Functions of unconventional myosins. Curr. Opin. Cell Biol. 12:, 42-51. [PubMed]. * Yin, H., Pruyne, D., Huffaker, T.C., and Bretscher, A. (2000). Myosin V orientates the mitotic spindle in yeast. Nature 406:, 1013-1015. [PubMed]. * Zhang, F., Southwick, F.S., and Purich, D.L. (2002). Actin-based phagosome motility. Cell Motil. Cytoskeleton 53:, 81-88. [PubMed].
Q-Index Code C1
Q-Index Status Provisional Code
Institutional Status Unknown

Version Filter Type
Citation counts: TR Web of Science Citation Count  Cited 74 times in Thomson Reuters Web of Science Article | Citations
Scopus Citation Count Cited 79 times in Scopus Article | Citations
Google Scholar Search Google Scholar
Created: Wed, 07 Jan 2009, 16:01:30 EST by Ms Lynette Adams on behalf of School of Chemistry & Molecular Biosciences