The fusion of early endosomes induces molecularmotor- driven tubule formation and fission

Journal of Cell Science

Volumn 125, Issue 8, 2012, Pages 1910-1919

  Skjeldal, Frode M ^a   Strunze, Sten ^a   Bergeland, Trygve ^a   Walseng, Even ^a   Gregers, Tone F ^a   Bakke, Oddmund ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

Early endosomal fusion and fission; Early endsomal tubule formation; Molecular motors

Indexed keywords

CHAPERONE; CYTOPLASMIC DYNEIN; KIF16B PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE PROTEIN; RAB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; MEMBRANE FUSION; MEMBRANE STABILIZATION; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL LINE; DOGS; DYNEINS; ENDOCYTOSIS; ENDOSOMES; HUMANS; KINESIN; MEMBRANE FUSION; MICROTUBULES; MOLECULAR MOTOR PROTEINS; RAB5 GTP-BINDING PROTEINS;

EID: 84863095295     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.092569     Document Type: Article

References (44)

1. Bakke, O. and Dobberstein, B. (1990). MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63, 707-716.
2. Bergeland, T., Widerberg, J., Bakke, O. and Nordeng, T. W. (2001). Mitotic partitioning of endosomes and lysosomes. Curr. Biol. 11, 644-651.
3. Bergeland, T., Haugen, L., Landsverk, O. J., Stenmark, H. and Bakke, O. (2008). Cell-cycle-dependent binding kinetics for the early endosomal tethering factor EEA1. EMBO Rep. 9, 171-178.
4. Bourekas, E. C., Christoforidis, G. A., Abduljalil, A. M., Kangarlu, A., Chakeres, D. W., Spigos, D. G. and Robitaille, P. M. (1999). High resolution MRI of the deep gray nuclei at 8 Tesla. J. Comput. Assisted Tomogr. 23, 867-874.
5. Burgess, R. E., Yu, Y., Christoforidis, G. A., Bourekas, E. C., Chakeres, D. W., Spigos, D., Kangarlu, A., Abduljalil, A. M. and Robitaille, P. M. (1999). Human leptomeningeal and cortical vascular anatomy of the cerebral cortex at 8 Tesla. J. Comput. Assisted Tomogr. 23, 850-856.
6. 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 clathrinmediated endocytosis. EMBO J. 20, 3676-3684.
7. Chavrier, P., Parton, R. G., Hauri, H. P., Simons, K. and Zerial, M. (1990). Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62, 317-329.
8. Christoforidis, S., McBride, H. M., Burgoyne, R. D. and Zerial, M. (1999a). The Rab5 effector EEA1 is a core component of endosome docking. Nature 397, 621-625.
9. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S. C., Waterfield, M. D., Backer, J. M. and Zerial, M. (1999b). Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1, 249-252.
10. Clague, M. J. (1998). Molecular aspects of the endocytic pathway. Biochem. J. 336, 271-282.
11. Coy, D. L., Wagenbach, M. and Howard, J. (1999). Kinesin takes one 8-nm step for each ATP that it hydrolyzes. J. Biol. Chem. 274, 3667-3671.
12. Driskell, O. J., Mironov, A., Allan, V. J. and Woodman, P. G. (2007). Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nat. Cell Biol. 9, 113-120.
13. Engering, A. J., Richters, C. D., Fluitsma, D. M., van Pelt, A. M., Kamperdijk, E. W., Hoefsmit, E. C. and Pieters, J. (1998). MHC class II and invariant chain biosynthesis and transport during maturation of human precursor dendritic cells. Int. Immunol. 10, 1713-1723.
14. Gorvel, J. P., Chavrier, P., Zerial, M. and Gruenberg, J. (1991). rab5 controls early endosome fusion in vitro. Cell 64, 915-925.
15. Gregers, T. F., Nordeng, T. W., Birkeland, H. C., Sandlie, I. and Bakke, O. (2003). The cytoplasmic tail of invariant chain modulates antigen processing and presentation. Eur. J. Immunol. 33, 277-286.
16. Gruenberg, J., Griffiths, G. and Howell, K. E. (1989). Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316.
17. Hirokawa, N., Noda, Y., Tanaka, Y. and Niwa, S. (2009). Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682-696.
18. Hoepfner, S., Severin, F., Cabezas, A., Habermann, B., Runge, A., Gillooly, D., Stenmark, H. and Zerial, M. (2005). Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121, 437-450.
19. Koster, G., Cacciuto, A., Derenyi, I., Frenkel, D. and Dogterom, M. (2005). Force barriers for membrane tube formation. Phys. Rev. Lett. 94, 068101.
20. Lawe, D. C., Chawla, A., Merithew, E., Dumas, J., Carrington, W., Fogarty, K., Lifshitz, L., Tuft, R., Lambright, D. and Corvera, S. (2002). Sequential roles for phosphatidylinositol 3-phosphate and Rab5 in tethering and fusion of early endosomes via their interaction with EEA1. J. Biol. Chem. 277, 8611-8617.
21. Li, G., D'Souza-Schorey, C., Barbieri, M. A., Roberts, R. L., Klippel, A., Williams, L. T. and Stahl, P. D. (1995). Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc. Natl. Acad. Sci. USA 92, 10207-10211.
22. Lippincott-Schwartz, J., Roberts, T. H. and Hirschberg, K. (2000). Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16, 557-589.
23. Loubery, S., Wilhelm, C., Hurbain, I., Neveu, S., Louvard, D. and Coudrier, E. (2008). Different microtubule motors move early and late endocytic compartments. Traffic 9, 492-509.
24. McBride, H. M., Rybin, V., Murphy, C., Giner, A., Teasdale, R. and Zerial, M. (1999). Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98, 377-386.
25. Morris, S. M., Arden, S. D., Roberts, R. C., Kendrick-Jones, J., Cooper, J. A., Luzio, J. P. and Buss, F. (2002). Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3, 331-341.
26. Mukherjee, S. and Maxfield, F. R. (2000). Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic 1, 203-211.
27. Murray, J. W. and Wolkoff, A. W. (2003). Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv. Drug Deliv. Rev. 55, 1385-1403.
28. Nakata, T. and Hirokawa, N. (1995). Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J. Cell Biol. 131, 1039-1053.
29. Nath, S., Bananis, E., Sarkar, S., Stockert, R. J., Sperry, A. O., Murray, J. W. and Wolkoff, A. W. (2007). Kif5B and Kifc1 interact and are required for motility and fission of early endocytic vesicles in mouse liver. Mol. Biol. Cell 18, 1839-1849.
30. Nielsen, E., Severin, F., Backer, J. M., Hyman, A. A. and Zerial, M. (1999). Rab5 regulates motility of early endosomes on microtubules. Nat. Cell Biol. 1, 376-382.
31. Nordeng, T. W., Gregers, T. F., Kongsvik, T. L., Meresse, S., Gorvel, J. P., Jourdan, F., Motta, A. and Bakke, O. (2002). The cytoplasmic tail of invariant chain regulates endosome fusion and morphology. Mol. Biol. Cell 13, 1846-1856.
32. Pantazatos, D. P. and MacDonald, R. C. (1999). Directly observed membrane fusion between oppositely charged phospholipid bilayers. J. Membr. Biol. 170, 27-38.
33. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R. and McMahon, H. T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499.
34. Roberts, R. L., Barbieri, M. A., Pryse, K. M., Chua, M., Morisaki, J. H. and Stahl, P. D. (1999). Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112, 3667-3675.
35. Roepstorff, K., Grandal, M. V., Henriksen, L., Knudsen, S. L., Lerdrup, M., Grovdal, L., Willumsen, B. M. and van Deurs, B. (2009). Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 10, 1115-1127.
36. Romagnoli, P., Layet, C., Yewdell, J., Bakke, O. and Germain, R. N. (1993). Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments. J. Exp. Med. 177, 583-596.
37. Roux, A., Cappello, G., Cartaud, J., Prost, J., Goud, B. and Bassereau, P. (2002). A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc. Natl. Acad. Sci. USA 99, 5394-5539.
38. Schepis, A., Stauber, T. and Krijnse Locker, J. (2007). Kinesin-1 plays multiple roles during the vaccinia virus life cycle. Cell Microbiol. 9, 1960-1973.
39. Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J. M., Brech, A., Callaghan, J., Toh, B. H., Murphy, C., Zerial, M. and Stenmark, H. (1998). EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494-498.
40. Stang, E. and Bakke, O. (1997). MHC class II-associated invariant chain-induced enlarged endosomal structures: a morphological study. Exp. Cell Res. 235, 79-92.
41. Stenmark, H., Parton, R. G., Steele-Mortimer, O., Lutcke, A., Gruenberg, J. and Zerial, M. (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296.
42. Tanaka, Y., Kanai, Y., Okada, Y., Nonaka, S., Takeda, S., Harada, A. and Hirokawa, N. (1998). Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93, 1147-1158.
43. Vale, R. D. and Hotani, H. (1988). Formation of membrane networks in vitro by kinesin-driven microtubule movement. J. Cell Biol. 107, 2233-2241.
44. Verhey, K. J. and Hammond, J. W. (2009). Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 10, 765-777.