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Distinct endocytic recycling of myelin proteins promotes oligodendroglial membrane remodeling

Winterstein, Christine, Trotter, Jacqueline, Krämer-Albers, Eva-Maria·2008·Journal of Cell Science
DOI 10.1242/jcs.022731
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Abstract

The central nervous system myelin sheath is a multilayered specialized membrane with compacted and non-compacted domains of defined protein composition. How oligodendrocytes regulate myelin membrane trafficking and establish membrane domains during myelination is largely unknown. Oligodendroglial cells respond to neuronal signals by adjusting the relative levels of endocytosis and exocytosis of the major myelin protein, proteolipid protein (PLP). We investigated whether endocytic trafficking is common to myelin proteins and analyzed the endocytic fates of proteins with distinct myelin subdomain localization. Interestingly, we found that PLP, myelin-associated glycoprotein (MAG) and myelin-oligodendrocyte glycoprotein (MOG), which localize to compact myelin, periaxonal loops and abaxonal loops, respectively, exhibit distinct endocytic fates. PLP was internalized via clathrin-independent endocytosis, whereas MAG was endocytosed by a clathrin-dependent pathway, although both proteins were targeted to the late-endosomal/lysosomal compartment. MOG was also endocytosed by a clathrin-dependent pathway, but in contrast to MAG, trafficked to the recycling endosome. Endocytic recycling resulted in the association of PLP, MAG and MOG with oligodendroglial membrane domains mimicking the biochemical characteristics of myelin domains. Our results suggest that endocytic sorting and recycling of myelin proteins may assist plasma membrane remodeling, which is necessary for the morphogenesis of myelin subdomains.

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Research works printed but not linked: 52

  1. Alberts, P. and Galli, T. (2003). The cell outgrowth secretory endosome (COSE): a specialized compartment involved in neuronal morphogenesis. Biol. Cell95, 419-424. · DOI · Paper page
  2. Anitei, M. and Pfeiffer, S. E. (2006). Myelin biogenesis: sorting out protein trafficking. Curr. Biol.16, R418-R421. · DOI
  3. Anitei, M., Ifrim, M., Ewart, M. A., Cowan, A. E., Carson, J. H., Bansal, R. and Pfeiffer, S. E. (2006). A role for Sec8 in oligodendrocyte morphological differentiation. J. Cell Sci.119, 807-818. · DOI
  4. Arantes, R. M. and Andrews, N. W. (2006). A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons. J. Neurosci.26, 4630-4637. · DOI
  5. Arroyo, E. J. and Scherer, S. S. (2000). On the molecular architecture of myelinated fibers. Histochem. Cell Biol.113, 1-18. · DOI · Paper page
  6. Bo, L., Quarles, R. H., Fujita, N., Bartoszewicz, Z., Sato, S. and Trapp, B. D. (1995). Endocytic depletion of L-MAG from CNS myelin in quaking mice. J. Cell Biol.131, 1811-1820. · DOI
  7. Boiko, T. and Winckler, B. (2006). Myelin under construction – teamwork required. J. Cell Biol.172, 799-801. · DOI
  8. Bouverat, B. P., Krueger, W. H., Coetzee, T., Bansal, R. and Pfeiffer, S. E. (2000). Expression of rab GTP-binding proteins during oligodendrocyte differentiation in culture. J. Neurosci. Res.59, 446-453. · DOI · Paper page
  9. Bretscher, M. S. and Aguado-Velasco, C. (1998). Membrane traffic during cell locomotion. Curr. Opin. Cell Biol.10, 537-541. · DOI
  10. de Vries, H. and Hoekstra, D. (2000). On the biogenesis of the myelin sheath: cognate polarized trafficking pathways in oligodendrocytes. Glycoconj. J.17, 181-190. · DOI
  11. de Vries, H., Schrage, C. and Hoekstra, D. (1998). An apical-type trafficking pathway is present in cultured oligodendrocytes but the sphingolipid-enriched myelin membrane is the target of a basolateral-type pathway. Mol. Biol. Cell9, 599-609. · DOI
  12. Dubois-Dalcq, M., Behar, T., Hudson, L. and Lazzarini, R. A. (1986). Emergence of three myelin proteins in oligodendrocytes cultured without neurons. J. Cell Biol.102, 384-392. · DOI
  13. Ford, M. G., Pearse, B. M., Higgins, M. K., Vallis, Y., Owen, D. J., Gibson, A., Hopkins, C. R., Evans, P. R. and McMahon, H. T. (2001). Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science291, 1051-1055. · DOI · Paper page
  14. Gow, A., Southwood, C. M., Li, J. S., Pariali, M., Riordan, G. P., Brodie, S. E., Danias, J., Bronstein, J. M., Kachar, B. and Lazzarini, R. A. (1999). CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell99, 649-659. · DOI
  15. Jung, M., Kramer, E., Grzenkowski, M., Tang, K., Blakemore, W., Aguzzi, A., Khazaie, K., Chlichlia, K., von Blankenfeld, G., Kettenmann, H. et al. (1995). Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. Eur. J. Neurosci.7, 1245-1265. · DOI
  16. Jung, M., Sommer, I., Schachner, M. and Nave, K. A. (1996). Monoclonal antibody O10 defines a conformationally sensitive cell-surface epitope of proteolipid protein (PLP): evidence that PLP misfolding underlies dysmyelination in mutant mice. J. Neurosci.16, 7920-7929. · DOI
  17. Karim, S. A., Barrie, J. A., McCulloch, M. C., Montague, P., Edgar, J. M., Kirkham, D., Anderson, T. J., Nave, K. A., Griffiths, I. R. and McLaughlin, M. (2007). PLP overexpression perturbs myelin protein composition and myelination in a mouse model of Pelizaeus-Merzbacher disease. Glia55, 341-351. · DOI
  18. Kippert, A., Trajkovic, K., Rajendran, L., Ries, J. and Simons, M. (2007). Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J. Neurosci.27, 3560-3570. · DOI
  19. Kirkham, M. and Parton, R. G. (2005). Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim. Biophys. Acta1746, 349-363. · DOI
  20. Kramer, E. M., Koch, T., Niehaus, A. and Trotter, J. (1997). Oligodendrocytes direct glycosyl phosphatidylinositol-anchored proteins to the myelin sheath in glycosphingolipid-rich complexes. J. Biol. Chem.272, 8937-8945. · DOI
  21. Kramer, E. M., Schardt, A. and Nave, K. A. (2001). Membrane traffic in myelinating oligodendrocytes. Microsc. Res. Tech.52, 656-671. · DOI
  22. Kramer-Albers, E. M., Gehrig-Burger, K., Thiele, C., Trotter, J. and Nave, K. A. (2006). Perturbed interactions of mutant proteolipid protein/DM20 with cholesterol and lipid rafts in oligodendroglia: implications for dysmyelination in spastic paraplegia. J. Neurosci.26, 11743-11752. · DOI
  23. Kroepfl, J. F. and Gardinier, M. V. (2001a). Identification of a basolateral membrane targeting signal within the cytoplasmic domain of myelin/oligodendrocyte glycoprotein. J. Neurochem.77, 1301-1309. · DOI
  24. Kroepfl, J. F. and Gardinier, M. V. (2001b). Mutually exclusive apicobasolateral sorting of two oligodendroglial membrane proteins, proteolipid protein and myelin/oligodendrocyte glycoprotein, in Madin-Darby canine kidney cells. J. Neurosci. Res.66, 1140-1148. · DOI · Paper page
  25. Larocca, J. N. and Rodriguez-Gabin, A. G. (2002). Myelin biogenesis: vesicle transport in oligodendrocytes. Neurochem. Res.27, 1313-1329. · DOI
  26. Lecuit, T. and Pilot, F. (2003). Developmental control of cell morphogenesis: a focus on membrane growth. Nat. Cell Biol.5, 103-108. · DOI
  27. Lu, H. and Bilder, D. (2005). Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol.7, 1232-1239. · DOI
  28. Marta, C. B., Taylor, C. M., Coetzee, T., Kim, T., Winkler, S., Bansal, R. and Pfeiffer, S. E. (2003). Antibody cross-linking of myelin oligodendrocyte glycoprotein leads to its rapid repartitioning into detergent-insoluble fractions, and altered protein phosphorylation and cell morphology. J. Neurosci.23, 5461-5471. · DOI
  29. Marta, C. B., Montano, M. B., Taylor, C. M., Taylor, A. L., Bansal, R. and Pfeiffer, S. E. (2005). Signaling cascades activated upon antibody cross-linking of myelin oligodendrocyte glycoprotein: potential implications for multiple sclerosis. J. Biol. Chem.280, 8985-8993. · DOI
  30. Matthieu, J. M., Quarles, R. H., Brady, R. O. and Webster, H. d. F. (1973). Variation of proteins, enzyme markers and gangliosides in myelin subfractions. Biochim. Biophys. Acta329, 305-317. · DOI
  31. Minuk, J. and Braun, P. E. (1996). Differential intracellular sorting of the myelin-associated glycoprotein isoforms. J. Neurosci. Res.44, 411-420. · DOI · Paper page
  32. Morita, K., Sasaki, H., Fujimoto, K., Furuse, M. and Tsukita, S. (1999). Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J. Cell Biol.145, 579-588. · DOI
  33. Niehaus, A., Stegmuller, J., Diers-Fenger, M. and Trotter, J. (1999). Cell-surface glycoprotein of oligodendrocyte progenitors involved in migration. J. Neurosci.19, 4948-4961. · DOI
  34. Park, M., Salgado, J. M., Ostroff, L., Helton, T. D., Robinson, C. G., Harris, K. M. and Ehlers, M. D. (2006). Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron52, 817-830. · DOI · Paper page
  35. Perret, E., Lakkaraju, A., Deborde, S., Schreiner, R. and Rodriguez-Boulan, E. (2005). Evolving endosomes: how many varieties and why? Curr. Opin. Cell Biol.17, 423-434. · DOI
  36. Pfeiffer, S. E., Warrington, A. E. and Bansal, R. (1993). The oligodendrocyte and its many cellular processes. Trends Cell Biol.3, 191-197. · DOI · Paper page
  37. Popko, B. (2000). Myelin galactolipids: mediators of axon-glial interactions? Glia29, 149-153. · DOI
  38. Rios, J. C., Melendez-Vasquez, C. V., Einheber, S., Lustig, M., Grumet, M., Hemperly, J., Peles, E. and Salzer, J. L. (2000). Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J. Neurosci.20, 8354-8364. · DOI
  39. Rodriguez-Boulan, E., Kreitzer, G. and Musch, A. (2005). Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol.6, 233-247. · DOI · Paper page
  40. Rodriguez-Gabin, A. G., Cammer, M., Almazan, G., Charron, M. and Larocca, J. N. (2001). Role of rRAB22b, an oligodendrocyte protein, in regulation of transport of vesicles from trans Golgi to endocytic compartments. J. Neurosci. Res.66, 1149-1160. · DOI
  41. Rodriguez-Gabin, A. G., Almazan, G. and Larocca, J. N. (2004). Vesicle transport in oligodendrocytes: probable role of Rab40c protein. J. Neurosci. Res.76, 758-770. · DOI
  42. Salzer, J. L. (2003). Polarized domains of myelinated axons. Neuron40, 297-318. · DOI
  43. Schaeren-Wiemers, N., Bonnet, A., Erb, M., Erne, B., Bartsch, U., Kern, F., Mantei, N., Sherman, D. and Suter, U. (2004). The raft-associated protein MAL is required for maintenance of proper axon-glia interactions in the central nervous system. J. Cell Biol.166, 731-742. · DOI
  44. Schneider, A., Lander, H., Schulz, G., Wolburg, H., Nave, K. A., Schulz, J. B. and Simons, M. (2005). Palmitoylation is a sorting determinant for transport to the myelin membrane. J. Cell Sci.118, 2415-2423. · DOI
  45. Sherman, D. L. and Brophy, P. J. (2005). Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci.6, 683-690. · DOI · Paper page
  46. Sherman, D. L., Tait, S., Melrose, S., Johnson, R., Zonta, B., Court, F. A., Macklin, W. B., Meek, S., Smith, A. J., Cottrell, D. F. et al. (2005). Neurofascins are required to establish axonal domains for saltatory conduction. Neuron48, 737-742. · DOI
  47. Simons, M. and Trajkovic, K. (2006). Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. J. Cell Sci.119, 4381-4389. · DOI
  48. Simons, M., Kramer, E. M., Macchi, P., Rathke-Hartlieb, S., Trotter, J., Nave, K. A. and Schulz, J. B. (2002). Overexpression of the myelin proteolipid protein leads to accumulation of cholesterol and proteolipid protein in endosomes/lysosomes: implications for Pelizaeus-Merzbacher disease. J. Cell Biol.157, 327-336. · DOI · Paper page
  49. Siskova, Z., Baron, W., de Vries, H. and Hoekstra, D. (2006). Fibronectin impedes “myelin” sheet-directed flow in oligodendrocytes: a role for a beta 1 integrin-mediated PKC signaling pathway in vesicular trafficking. Mol. Cell. Neurosci.33, 150-159. · DOI
  50. Trajkovic, K., Dhaunchak, A. S., Goncalves, J. T., Wenzel, D., Schneider, A., Bunt, G., Nave, K. A. and Simons, M. (2006). Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J. Cell Biol.172, 937-948. · DOI · Paper page
  51. Trapp, B. D., Andrews, S. B., Cootauco, C. and Quarles, R. (1989). The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J. Cell Biol.109, 2417-2426. · DOI
  52. Wisco, D., Anderson, E. D., Chang, M. C., Norden, C., Boiko, T., Folsch, H. and Winckler, B. (2003). Uncovering multiple axonal targeting pathways in hippocampal neurons. J. Cell Biol.162, 1317-1328. · DOI · Paper page

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Metadata

Authors
Winterstein, C., Trotter, J., & Krämer-Albers, E.-M.
Affiliations
Department of Biology, Unit of Molecular Cell Biology, University of Mainz, Bentzelweg 3, 55128 Mainz, Germany
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2008-03-15
Volume
121
Issue
6
Pages
834-842
ISSN
  • 1477-9137
  • 0021-9533
DOI
10.1242/jcs.022731
Cited by
92
References
1
Language
en

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