Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells

Journal of Neuroscience

Volumn 27, Issue 13, 2007, Pages 3560-3570

  Kippert, Angelika ^a,b   Trajkovic, Katarina ^a,b   Rajendran, Lawrence ^d   Ries, Jonas ^c   Simons, Mikael ^a,b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Endocytosis; Late endosomes lysosomes; Myelin; Neurons; Oligodendrocytes; Rho GTPases

Indexed keywords

PROTEIN TYROSINE KINASE; PROTEOLIPID PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; CELL POLARITY; CELL SPECIFICITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; ENZYME INACTIVATION; LYSOSOME; MEMBRANE VESICLE; MOUSE; NONHUMAN; OLIGODENDROGLIA; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; CELL DIFFERENTIATION; CELL MEMBRANE; CELLS, CULTURED; ENDOCYTOSIS; ENDOSOMES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MICE; MYELIN SHEATH; NEURONS; OLIGODENDROGLIA; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RHO GTP-BINDING PROTEINS; SRC-FAMILY KINASES;

EID: 34047126867     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4926-06.2007     Document Type: Article

References (62)

1. Arantes RM, Andrews NW (2006) A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons. J Neurosci 26:4630-4637.
2. Bagatolli LA, Sanchez SA, Hazlett T, Gratton E (2003) Giant vesicles, Laurdan, and two-photon fluorescence microscopy: evidence of lipid lateral separation in bilayers. Methods Enzymol 360:481-500.
3. Barres BA, Raff MC (1999) Axonal control of oligodendrocyte development. J Cell Biol 147:1123-1128.
4. Bomsel M, Prydz K, Parton RG, Gruenberg J, Simons K (1989) Endocytosis in filter-grown Madin-Darby canine kidney cells. J Cell Biol 109:3243-3258.
5. Buttery PC, ffrench-Constant C (1999) Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol Cell Neurosci 14:199-212.
6. Cheng ZJ, Singh RD, Sharma DK, Holicky EL, Hanada K, Marks DL, Pagano RE (2006) Distinct mechanisms of clathrin-independent endocytosis have unique sphingolipid requirements. Mol Biol Cell 17:3197-3210.
7. Chun SJ, Rasband MN, Sidman RL, Habib AA, Vartanian T (2003) Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J Cell Biol 163:397-408.
8. Colognato H, Ramachandrappa S, Olsen IM, ffrench-Constant C (2004) Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 167:365-375.
9. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168:477-488.
10. Debruin LS, Harauz G (2007) White matter rafting-membrane microdomains in myelin. Neurochem Res 32:213-228.
11. del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande-Garcia A, Anderson RG, Schwartz MA (2005) Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 7:901-908.
12. Dubois-Dalcq M, Behar T, Hudson L, Lazzarini RA (1986) Emergence of three myelin proteins in oligodendrocytes cultured without neurons. J Cell Biol 102:384-392.
13. Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA (2006) Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26:10967-10983.
14. Edgar JM, McLaughlin M, Yool D, Zhang SC, Fowler JH, Montague P, Barrie JA, McCulloch MC, Duncan ID, Garbern J, Nave KA, Griffiths IR (2004) Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J Cell Biol 166:121-131.
15. Fernandez-Borja M, Janssen L, Verwoerd D, Hordijk P, Neefjes J (2005) RhoB regulates endosome transport by promoting actin assembly on endosomal membranes through Dia1. J Cell Sci 118:2661-2670.
16. Fitzner D, Schneider A, Kippert A, Mobius W, Willig KI, Hell SW, Bunt G, Gaus K, Simons M (2006) Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin. EMBO J 25:5037-5048.
17. Fivaz M, Vilbois F, Thurnheer S, Pasquali C, Abrami L, Bickel PE, Parton RG, van der Goot FG (2002) Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J 21:3989-4000.
18. Gasman S, Kalaidzidis Y, Zerial M (2003) RhoD regulates endosome dynamics through Diaphanous-related Formin and Src tyrosine kinase. Nat Cell Biol 5:195-204.
19. Gatto CL, Walker BJ, Lambert S (2003) Local ERM activation and dynamic growth cones at Schwann cell tips implicated in efficient formation of nodes of Ranvier. J Cell Biol 162:489-498.
20. Gaus K, Gratton E, Kable EP, Jones AS, Gelissen I, Kritharides L, Jessup W (2003) Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc Natl Acad Sci USA 100:15554-15559.
21. Gaus K, Le Lay S, Balasubramanian N, Schwartz MA (2006) Integrin-mediated adhesion regulates membrane order. J Cell Biol 174:725-734.
22. Gielen E, Baron W, Vandeven M, Steels P, Hoekstra D, Ameloot M (2006) Rafts in oligodendrocytes: evidence and structure-function relationship. Glia 54:499-512.
23. Gudz TI, Schneider TE, Haas TA, Macklin WB (2002) Myelin proteolipid protein forms a complex with integrins and may participate in integrin receptor signaling in oligodendrocytes. J Neurosci 22:7398-7407.
24. Gudz TI, Komuro H, Macklin WB (2006) Glutamate stimulates oligodendrocyte progenitor migration mediated via an α-v integrin/myelin proteolipid protein complex. J Neurosci 26:2458-2466.
25. 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.
26. Jung M, Sommer I, Schachner M, Nave KA (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.
27. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168:465-476.
28. Kramer-Albers EM, Gehrig-Burger K, Thiele C, Trotter J, Nave KA (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.
29. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A (2001) Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 7:661-671.
30. Liang X, Draghi NA, Resh MD (2004) Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 24:7140-7149.
31. McLaughlin M, Barrie JA, Karim S, Montague P, Edgar JM, Kirkham D, Thomson CE, Griffiths IR (2006) Processing of PLP in a model of Pelizaeus-Merzbacher disease/SPG2 due to the rumpshaker mutation. Glia 53:715-722.
32. Melendez-Vasquez CV, Rios JC, Zanazzi G, Lambert S, Bretscher A, Salzer JL (2001) Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci USA 98:1235-1240.
33. Melendez-Vasquez CV, Einheber S, Salzer JL (2004) Rho kinase regulates Schwann cell myelination and formation of associated axonal domains. J Neurosci 24:3953-3963.
34. Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, Chang J, Thill G, Levesque M, Zhang M, Hession C, Sah D, Trapp B, He Z, Jung V, McCoy JM, Pepinsky RB (2005) LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 8:745-751.
35. Milner RJ, Lai C, Nave KA, Lenoir D, Ogata J, Sutcliffe JG (1985) Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell 42:931-939.
36. Mirsky R, Winter J, Abney ER, Pruss RM, Gavrilovic J, Raff MC (1980) Myelin-specific proteins and glycolipids in rat Schwann cells and oligodendrocytes in culture. J Cell Biol 84:483-494.
37. Orlandi PA, Fishman PH (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141:905-915.
38. Osterhout DJ, Wolven A, Wolf RM, Resh MD, Chao MV (1999) Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145:1209-1218.
39. Pfeiffer SE, Warrington AE, Bansal R (1993) The oligodendrocyte and its many cellular processes. Trends Cell Biol 3:191-197.
40. Qualmann B, Mellor H (2003) Regulation of endocytic traffic by Rho GTPases. Biochem J 371:233-241.
41. Ren XD, Kiosses WB, Schwartz MA (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18:578-585.
42. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522-529.
43. Robertson D, Paterson HF, Adamson P, Hall A, Monaghan P (1995) Ultra-structural localization of ras-related proteins using epitope-tagged plasmids. J Histochem Cytochem 43:471-480.
44. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2:411-423.
45. Salzer JL (2003) Polarized domains of myelinated axons. Neuron 40:297-318.
46. Sandilands E, Cans C, Fincham VJ, Brunton VG, Mellor H, Prendergast GC, Norman JC, Superti-Furga G, Frame MC (2004) RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev Cell 7:855-869.
47. Schafer DP, Rasband MN (2006) Glial regulation of the axonal membrane at nodes of Ranvier. Curr Opin Neurobiol 16:508-514.
48. Schmalzing G, Richter HP, Hansen A, Schwarz W, Just I, Aktories K (1995) Involvement of the GTP binding protein Rho in constitutive endocytosis in Xenopus laevis oocytes. J Cell Biol 130:1319-1332.
49. Schneider A, Lander H, Schulz G, Wolburg H, Nave KA, Schulz JB, Simons M (2005) Palmitoylation is a sorting determinant for transport to the myelin membrane. J Cell Sci 118:2415-2423.
50. Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683-690.
51. Simons M, Trajkovic K (2006) Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. J Cell Sci 119:4381-4389.
52. Simons M, Kramer EM, Thiele C, Stoffel W, Trotter J (2000) Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains. J Cell Biol 151:143-154.
53. Simons M, Kramer EM, Macchi P, Rathke-Hartlieb S, Trotter J, Nave KA, Schulz JB (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.
54. Siskova Z, Baron W, de Vries H, 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.
55. Taylor CM, Marta CB, Claycomb RJ, Han DK, Rasband MN, Coetzee T, Pfeiffer SE (2004) Proteomic mapping provides powerful insights into functional myelin biology. Proc Natl Acad Sci USA 101:4643-4648.
56. Thurnherr T, Benninger Y, Wu X, Chrostek A, Krause SM, Nave KA, Franklin RJ, Brakebusch C, Suter U, Relvas JB (2006) Cdc42 and Rac1 signaling are both required for and act synergistically in the correct formation of myelin sheaths in the CNS. J Neurosci 26:10110-10119.
57. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, Bunt G, Nave KA, Simons M (2006) Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172:937-948.
58. Wherlock M, Gampel A, Futter C, Mellor H (2004) Farnesyltransferase inhibitors disrupt EGF receptor traffic through modulation of the RhoB GTPase. J Cell Sci 117:3221-3231.
59. Wolf RM, Wilkes JJ, Chao MV, Resh MD (2001) Tyrosine phosphorylation of p190 RhoGAP by Fyn regulates oligodendrocyte differentiation. J Neurobiol 49:62-78.
60. Wubbolts R, Fernandez-Borja M, Oomen L, Verwoerd D, Janssen H, Calafat J, Tulp A, Dusseljee S, Neefjes J (1996) Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J Cell Biol 135:611-622.
61. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7:617-627.
62. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, Mochizuki N, Nagashima K, Matsuda M (2003) Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J Cell Biol 162:223-232.