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New roles for endosomes: from vesicular carriers to multi-purpose platforms

Abstract

The careful sorting and recycling of membranes and cargo and the intracellular delivery of proteins, toxins and viruses by endocytosis are well-established roles for the endocytic apparatus, which is present in all eukaryotic cells. Recently, it has become clear that endosomes have key roles in such diverse processes as cytokinesis, polarization and migration, in which their functions might be distinct from those classically associated with endosomes. We speculate that endosomes function as multifunctional platforms on which unique sets of molecular machines are assembled to suit different cellular roles.

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Figure 1: Endosome platforms in cytokinesis.
Figure 2: Endosome platforms in cell migration.

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References

  1. Seaman, M. N. Endosome protein sorting: motifs and machinery. Cell. Mol. Life Sci. 65, 2842–2858 (2008).

    Article  CAS  Google Scholar 

  2. Lemmon, S. K. & Traub, L. M. Sorting in the endosomal system in yeast and animal cells. Curr. Opin. Cell Biol. 12, 457–466 (2000).

    Article  CAS  Google Scholar 

  3. Sönnichsen, B., De Renzis, S., Neilsen, E., Rietdorf, J. & Zerial, M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901–914 (2000).

    Article  Google Scholar 

  4. Christoforidis, S. et al. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nature Cell Biol. 1, 249–252 (1999).

    Article  CAS  Google Scholar 

  5. Gaullier, J.-M. et al. FYVE fingers bind PtdIns(3)P. Nature 394, 432–433 (1998).

    Article  CAS  Google Scholar 

  6. Miaczynska, M. & Zerial, M. Mosaic organization of the endocytic pathway. Exp. Cell Res. 272, 8–14 (2002).

    Article  CAS  Google Scholar 

  7. Emery, G. & Knoblich, J. A. Endosome dynamics during development. Curr. Opin. Cell Biol. 18, 407–415 (2006).

    Article  CAS  Google Scholar 

  8. Miaczynska, M., Pelkmans, L. & Zerial, M. Not just a sink: endosomes in control of signal transduction. Curr. Opin. Cell Biol. 16, 400–406 (2004).

    Article  CAS  Google Scholar 

  9. Sorkin, A. & von Zastrow, M. Signal transduction and endocytosis: close encounters of many kinds. Nature Rev. Mol. Cell Biol. 3, 600–614 (2002).

    Article  CAS  Google Scholar 

  10. Barr, F. A. & Gruneberg, U. Cytokinesis: placing and making the final cut. Cell 131, 847–860 (2007).

    Article  CAS  Google Scholar 

  11. Glotzer, M. The molecular requirements for cytokinesis. Science 307, 1735–1739 (2005).

    Article  CAS  Google Scholar 

  12. Albertson, R., Riggs, B. & Sullivan, W. Membrane traffic: a driving force in cytokinesis. Trends Cell Biol. 15, 92–101 (2005).

    Article  CAS  Google Scholar 

  13. Gromley, A. et al. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75–87 (2005).

    Article  CAS  Google Scholar 

  14. Goss, J. W. & Toomre, D. K. Both daughter cells traffic and exocytose membrane at the cleavage furrow during mammalian cytokinesis. J. Cell Biol. 181, 1047–1054 (2008).

    Article  CAS  Google Scholar 

  15. Fielding, A. B. et al. Rab11–FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 24, 3389–3399 (2005).

    Article  CAS  Google Scholar 

  16. Kouranti, I., Sachse, M., Arouche, N., Goud, B. & Echard, A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol. 16, 1719–1725 (2006).

    Article  CAS  Google Scholar 

  17. Desautels, M., Den Haese, J. P., Slupsky, C. M., McIntosh, L. P. & Hemmingsen, S. M. Cdc4p, a contractile ring protein essential for cytokinesis in Schizosaccharomyces pombe, interacts with a phosphatidylinositol 4-kinase. J. Biol. Chem. 276, 5932–5942 (2001).

    Article  CAS  Google Scholar 

  18. Emoto, K., Inadome, H., Kanaho, Y., Narumiya, S. & Umeda, M. Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J. Biol. Chem. 280, 37901–37907 (2005).

    Article  CAS  Google Scholar 

  19. Field, S. J. et al. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr. Biol. 15, 1407–1412 (2005).

    Article  CAS  Google Scholar 

  20. Janetpopoulos, C., Borleis, J., Vazquez, F., Iijima, M. & Devreotes, P. Temporal and spatial regulation of phosphoinositide signaling mediates cytokinesis. Dev. Cell 8, 467–477 (2005).

    Article  Google Scholar 

  21. Pohl, C. & Jentsch, S. Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132, 832–845 (2008).

    Article  CAS  Google Scholar 

  22. Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908–1912 (2007).

    Article  CAS  Google Scholar 

  23. Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215–4227 (2007).

    Article  CAS  Google Scholar 

  24. Hanson, P. I., Roth, R., Lin, Y. & Heuser, J. E. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389–402 (2008).

    Article  CAS  Google Scholar 

  25. Dukes, J. D., Richardson, J. D., Simmons, R. & Whitley, P. A dominant-negative ESCRT-III protein perturbs cytokinesis and trafficking to lysosomes. Biochem. J. 411, 233–239 (2008).

    Article  CAS  Google Scholar 

  26. Lee, H. H., Elia, N., Ghirlando, R., Lippincott-Schwartz, J. & Hurley, J. H. Midbody targeting of the ESCRT machinery by a noncanonical coiled coil in CEP55. Science 322, 576–580 (2008).

    Article  CAS  Google Scholar 

  27. Yang, D. et al. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nature Struct. Mol. Biol. 15, 1278–1286 (2008).

    Article  CAS  Google Scholar 

  28. Boucrot, E. & Kirchhausen, T. Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl Acad. Sci. USA 104, 7939–7944 (2007).

    Article  CAS  Google Scholar 

  29. Giansanti, M. G., Belloni, G. & Gatti, M. Rab11 is required for membrane trafficking and actomyosin ring constriction in meiotic cytokinesis of Drosophila males. Mol. Biol. Cell 18, 5034–5047 (2007).

    Article  CAS  Google Scholar 

  30. Sommer, B., Oprins, A., Rabouille, C. & Munro, S. The exocyst component Sec5 is present on endocytic vesicles in the oocyte of Drosophila melanogaster. J. Cell Biol. 169, 953–963 (2005).

    Article  CAS  Google Scholar 

  31. Langevin, J. et al. Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell 9, 365–376 (2005).

    Article  CAS  Google Scholar 

  32. Deborde, S. et al. Clathrin is a key regulator of basolateral polarity. Nature 452, 719–725 (2008).

    Article  CAS  Google Scholar 

  33. Nance, J. PAR proteins and the establishment of cell polarity during C. elegans development. Bioessays 27, 126–135 (2005).

    Article  CAS  Google Scholar 

  34. Balklava, Z., Pant, S., Fares, H. & Grant, B. D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nature Cell Biol. 9, 1066–1073 (2007).

    Article  CAS  Google Scholar 

  35. Moberg, K. H., Schelble, S., Burdick, S. K. & Hariharan, I. K. Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9, 699–710 (2005).

    Article  CAS  Google Scholar 

  36. Thompson, B. J. et al. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711–720 (2005).

    Article  CAS  Google Scholar 

  37. Vaccari, T. & Bilder, D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687–698 (2005).

    Article  CAS  Google Scholar 

  38. Gillette, J. M., Larochelle, A., Dunbar, C. E. & Lippincott-Schwartz, J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nature Cell Biol. 8 Feb 2009 (doi: 10.1038/ncb1838).

    Article  CAS  Google Scholar 

  39. Webb, D. J., Parsons, J. T. & Horwitz, A. F. Adhesion assembly, disassembly and turnover in migrating cells — over and over and over again. Nature Cell Biol. 4, E97–E100 (2002).

    Article  CAS  Google Scholar 

  40. Sturge, J., Wienke, D. & Isacke, C. M. Endosomes generate localized Rho–ROCK–MLC2-based contractile signals via Endo180 to promote adhesion disassembly. J. Cell Biol. 175, 337–347 (2006).

    Article  CAS  Google Scholar 

  41. Witze, E. S., Litman, E. S., Argast, G. M., Moon, R. T. & Ahn, N. G. Wnt5a control of cell polarity and directional movement by polarized redistribution of adhesion receptors. Science 320, 365–369 (2008).

    Article  CAS  Google Scholar 

  42. Machesky, L. M. Lamellipodia and filopodia in metastasis and invasion. FEBS Lett. 582, 2102–2011 (2008).

    Article  CAS  Google Scholar 

  43. Palamidessi, A. et al. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134, 135–147 (2008).

    Article  CAS  Google Scholar 

  44. Olivotto, M., Arcangeli, A., Carlà, M. & Wanke, E. Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. Bioessays 18, 495–504 (1996).

    Article  CAS  Google Scholar 

  45. Yeung, T. et al. Receptor activation alters inner surface potential during phagocytosis. Science 313, 347–351 (2006).

    Article  CAS  Google Scholar 

  46. Yeung, T. et al. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210–213 (2008).

    Article  CAS  Google Scholar 

  47. Bonifacino, J. S. & Glick, B. S. The mechanisms of vesicle budding and fusion. Cell 116, 153–166 (2004).

    Article  CAS  Google Scholar 

  48. Mayor, S. & Pagano, R. E. Pathways of clathrin-independent endocytosis. Nature Rev. Mol. Cell Biol. 8, 603–612 (2007).

    Article  CAS  Google Scholar 

  49. Hurley, J. H. & Emr, S. D. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35, 277–298 (2006).

    Article  CAS  Google Scholar 

  50. Schütze, S., Tchikov, V. & Schneider-Brachret, W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nature Rev. Mol. Cell Biol. 9, 655–662 (2008).

    Article  Google Scholar 

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Acknowledgements

Work in the G.W.G. laboratory is supported by grants from the Wellcome Trust and the Biotechnology and Biological Sciences Research Council, Cancer Research UK and the Association for International Cancer Research. G.W.G. thanks C. Isacke and N. Bryant for helpful comments on the manuscript.

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Gould, G., Lippincott-Schwartz, J. New roles for endosomes: from vesicular carriers to multi-purpose platforms. Nat Rev Mol Cell Biol 10, 287–292 (2009). https://doi.org/10.1038/nrm2652

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