Neuronal early endosomes require EHD1 for L1/NgCAM trafficking

Journal of Neuroscience

Volumn 30, Issue 49, 2010, Pages 16485-16497

  Lasiecka, Zofia M ^a   Yap, Chan Choo ^a   Caplan, Steven ^b   Winckler, Bettina ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY ENDOSOME ANTIGEN 1; EPS15 HOMOLOGY DOMAIN PROTEIN 1; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE L1; PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; DENDRITE; DOWN REGULATION; EMBRYO; ENDOSOME; IN VITRO STUDY; MOUSE; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER MEMBRANE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL ADHESION MOLECULES, NEURON-GLIA; CELLS, CULTURED; DENDRITES; DOWN-REGULATION; EMBRYO, MAMMALIAN; ENDOCYTOSIS; ENDOSOMES; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEINS; HIPPOCAMPUS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURONS; PROTEIN TRANSPORT; RATS; RNA, SMALL INTERFERING; TRANSFECTION; TRANSFERRIN; VESICULAR TRANSPORT PROTEINS;

EID: 78650065176     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3127-10.2010     Document Type: Article

References (41)

1. Aridor M, Hannan LA (2000) Traffic jam: a compendium of human diseases that affect intracellular transport processes. Traffic 1:836-851.
2. Blume JJ, Halbach A, Behrendt D, Paulsson M, Plomann M (2007) EHD proteins are associated with tubular and vesicular compartments and interact with specific phospholipids. Exp Cell Res 313:219-231.
3. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, Donaldson JG, Bonifacino JS (2002) A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J 21:2557-2567.
4. Christoforidis S, McBride HM, Burgoyne RD, Zerial M (1999) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621-625.
5. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT (2007) Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449:923-927.
6. Fourgeaud L, Bessis AS, Rossignol F, Pin JP, Olivo-Marin JC, Hémar A (2003) The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J Biol Chem 278:12222-12230.
7. Gaullier JM, Simonsen A, D'Arrigo A, Bremnes B, Stenmark H, Aasland R (1998) FYVE fingers bind PtdIns(3)P. Nature 394:432-433.
8. George M, Ying G, Rainey MA, Solomon A, Parikh PT, Gao Q, Band V, Band H (2007) Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans. BMC Cell Biol 8:3.
9. Grant BD, Caplan S (2008) Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9:2043-2052.
10. Gudmundsson H, Hund TJ, Wright PJ, Kline CF, Snyder JS, Qian L, Koval OM, Cunha SR, George M, Rainey MA, Kashef FE, Dun W, Boyden PA, Anderson ME, Band H, Mohler PJ (2010) EH domain proteins regulate cardiac membrane protein targeting. Circ Res 107:84-95.
11. Hoogenraad CC, Popa I, Futai K, Martinez-Sanchez E, Sanchez-Martinez E, Wulf PS, van Vlijmen T, Dortland BR, Oorschot V, Govers R, Monti M, Heck AJ, Sheng M, Klumperman J, Rehmann H, Jaarsma D, Kapitein LC, van der Sluijs P (2010) Neuron specific Rab4 effector GRASP-1 coordinates membrane specialization and maturation of recycling endosomes. PLoS Biol 8:e1000283.
12. Howe CL, Mobley WC (2004) Signaling endosome hypothesis: a cellular mechanism for long distance communication. J Neurobiol 58:207-216.
13. Jović M, Kieken F, Naslavsky N, Sorgen PL, Caplan S (2009) Eps15 homology domain 1-associated tubules contain phosphatidylinositol-4-phosphate and phosphatidylinositol-(4,5)-bisphosphate and are required for efficient recycling. Mol Biol Cell 20:2731-2743.
14. Jović M, Sharma M, Rahajeng J, Caplan S (2010) The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 25:99-112.
15. Kamiguchi H, Lemmon V (2000) Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 20:3676-3686. (Pubitemid 30266230)
16. Kennedy MJ, Ehlers MD (2006) Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 29:325-362.
17. Lakadamyali M, Rust MJ, Zhuang X (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124:997-1009.
18. Lasiecka ZM, Yap CC, Vakulenko M, Winckler B (2009) Compartmentalizing the neuronal plasma membrane from axon initial segments to synapses. Int Rev Cell Mol Biol 272:303-389.
19. Lin SX, Grant B, Hirsh D, Maxfield FR (2001) Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol 3:567-572.
20. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
21. Miaczynska M, Zerial M (2002) Mosaic organization of the endocytic pathway. Exp Cell Res 272:8-14.
22. Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S (2006) Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol Biol Cell 17:163-177.
23. Naslavsky N, Rahajeng J, Chenavas S, Sorgen PL, Caplan S (2007) EHD1 and Eps15 interact with phosphatidylinositols via their Eps15 homology domains. J Biol Chem 282:16612-16622.
24. Naslavsky N, McKenzie J, Altan-Bonnet N, Sheff D, Caplan S (2009) EHD3 regulates early-endosome-to-Golgi transport and preserves Golgi morphology. J Cell Sci 122:389-400.
25. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975. (Pubitemid 39287999)
26. Prekeris R, Foletti DL, Scheller RH (1999) Dynamics of tubulovesicular recycling endosomes in hippocampal neurons. J Neurosci 19:10324-10337.
27. Rainey MA, George M, Ying G, Akakura R, Burgess DJ, Siefker E, Bargar T, Doglio L, Crawford SE, Todd GL, Govindarajan V, Hess RA, Band V, Naramura M, Band H (2010) The endocytic recycling regulator EHD1 is essential for spermatogenesis and male fertility in mice. BMC Dev Biol 10:37.
28. Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, Fein A, Caplan S, Joyner AL, Horowitz M (2006) Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7:52-60.
29. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735-749.
30. Schweizer FE, Ryan TA (2006) The synaptic vesicle: cycle of exocytosis and endocytosis. Curr Opin Neurobiol 16:298-304.
31. Sharma M, Naslavsky N, Caplan S (2008) A role for EHD4 in the regulation of early endosomal transport. Traffic 9:995-1018.
32. Sharma M, Giridharan SS, Rahajeng J, Naslavsky N, Caplan S (2009) MICAL-L1 links EHD1 to tubular recycling endosomes and regulates receptor recycling. Mol Biol Cell 20:5181-5194.
33. Simonsen A, Lippé R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394:494-498.
34. Steiner P, Sarria JC, Glauser L, Magnin S, Catsicas S, Hirling H (2002) Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD. J Cell Biol 157:1197-1209.
35. Steiner P, Alberi S, Kulangara K, Yersin A, Sarria JC, Regulier E, Kasas S, Dietler G, Muller D, Catsicas S, Hirling H (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J 24:2873-2884.
36. Wisco D, Anderson ED, Chang MC, Norden C, Boiko T, Fölsch H, Winckler B (2003) Uncovering multiple axonal targeting pathways in hippocampal neurons. J Cell Biol 162:1317-1328. (Pubitemid 37210887)
37. Yap CC, Nokes RL, Wisco D, Anderson E, Fölsch H, Winckler B (2008a) Pathway selection to the axon depends on multiple targeting signals in NgCAM. J Cell Sci 121:1514-1525.
38. Yap CC, Wisco D, Kujala P, Lasiecka ZM, Cannon JT, Chang MC, Hirling H, Klumperman J, Winckler B (2008b) The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J Cell Biol 180:827-842.
39. Yap CC, Lasiecka ZM, Caplan S, Winckler B (2010) Alterations of EHD1/EHD4 protein levels interfere with L1/NgCAM endocytosis in neurons and disrupt axonal targeting. J Neurosci 30:6646-6657.
40. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107-117.
41. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P (2009) A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136:1110-1121.