EphA4 is localized in clathrin-coated and synaptic vesicles in adult mouse brain

Journal of Neurochemistry

Volumn 113, Issue 1, 2010, Pages 153-165

  Bouvier, David ^a   Tremblay, Marie Ève ^a   Riad, Mustapha ^a   Corera, Amadou T ^b   Gingras, Diane ^a   Horn, Katherine E ^b   Fotouhi, Maryam ^b   Girard, Martine ^b   Murai, Keith K ^c   Kennedy, Timothy E ^b   McPherson, Peter S ^b   Pasquale, Elena B ^d   Fon, Edward A ^b   Doucet, Guy ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MONTREAL GENERAL HOSPITAL   (Canada)

^d BURNHAM INSTITUTE   (United States)

Author keywords

Cell fractionation; Electron microscopy; EphA4; Hippocampus; Immunocytochemistry; Immunoisolation; Vesicles

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; CLATHRIN; GLUTAMATE TRANSPORTER; POTASSIUM CHLORIDE; PROTEIN; PROTEIN ANTIBODY; PROTEIN EPHA4; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN NERVE CELL; CELL CULTURE; CELL FRACTIONATION; CELL MEMBRANE; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IN VIVO STUDY; MALE; MEMBRANE DEPOLARIZATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; SYNAPSE VESICLE;

ANIMALS; BRAIN; CELLS, CULTURED; CLATHRIN; CLATHRIN-COATED VESICLES; EMBRYO, MAMMALIAN; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; NEOSTIGMINE; NEURONS; POTASSIUM CHLORIDE; RECEPTOR, EPHA4; SUBCELLULAR FRACTIONS; SYNAPTIC VESICLES; SYNAPTOTAGMINS; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 77749271079     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06582.x     Document Type: Article

References (66)

1. Allaire P. D., Ritter B., Thomas S. et al. (2006) Connecdenn, a novel DENN domain-containing protein of neuronal clathrin-coated vesicles functioning in synaptic vesicle endocytosis. J. Neurosci. 26, 13202 13212.
2. Armstrong J. N., Saganich M. J., Xu N. J., Henkemeyer M., Heinemann S. F. Contractor A. (2006) B-ephrin reverse signaling is required for NMDA-independent long-term potentiation of mossy fibers in the hippocampus. J. Neurosci. 26, 3474 3481.
3. Banker G. A. Cowan W. M. (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res. 126, 397 425.
4. Bendayan M. (1984) Protein A-gold electron microscopic immunocytochemistry: methods, applications, and limitations. J. Electron Microsc. Tech. 1, 243 270.
5. Bouvier D., Corera A. T., Tremblay M. E., Riad M., Chagnon M., Murai K. K., Pasquale E. B., Fon E. A. Doucet G. (2008) Pre-synaptic and post-synaptic localization of EphA4 and EphB2 in adult mouse forebrain. J. Neurochem. 106, 682 695.
6. Bouzioukh F., Wilkinson G. A., Adelmann G., Frotscher M., Stein V. Klein R. (2007) Tyrosine phosphorylation sites in ephrinB2 are required for hippocampal long-term potentiation but not long-term depression. J. Neurosci. 27, 11279 11288.
7. Bronfman F. C., Tcherpakov M., Jovin T. M. Fainzilber M. (2003) Ligand-induced internalization of the p75 neurotrophin receptor: a slow route to the signaling endosome. J. Neurosci. 23, 3209 3220.
8. Carmona M. A., Murai K. K., Wang L., Roberts A. J. Pasquale E. B. (2009) Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proc. Natl Acad. Sci. U S A 106, 12524 12529.
9. Carter R. E. Sorkin A. (1998) Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J. Biol. Chem. 273, 35000 35007.
10. Contractor A., Rogers C., Maron C., Henkemeyer M., Swanson G. T. Heinemann S. F. (2002) Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296, 1864 1869.
11. Dalva M. B. (2007) There's more than one way to skin a chimaerin. Neuron 55, 681 684.
12. Deininger K., Eder M., Kramer E. R., Zieglgansberger W., Dodt H. U., Dornmair K., Colicelli J. Klein R. (2008) The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc. Natl Acad. Sci. U S A 105, 12539 12544.
13. Dresbach T., Torres V., Wittenmayer N. et al. (2006) Assembly of active zone precursor vesicles: obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. J. Biol. Chem. 281, 6038 6047.
14. Fattorini G., Verderio C., Melone M., Giovedi S., Benfenati F., Matteoli M. Conti F. (2009) VGLUT1 and VGAT are sorted to the same population of synaptic vesicles in subsets of cortical axon terminals. J. Neurochem. 110, 1538 1546.
15. Filosa A., Paixao S., Honsek S. D. et al. (2009) Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat. Neurosci. 12, 1285 1292.
16. Fischer von Mollard G., Stahl B., Walch-Solimena C., Takei K., Daniels L., Khoklatchev A., De Camilli P., Sudhof T. C. Jahn R. (1994) Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur. J. Cell Biol. 65, 319 326.
17. Frank C. A., Pielage J. Davis G. W. (2009) A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 61, 556 569.
18. Fu W. Y., Chen Y., Sahin M. et al. (2007) Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 10, 67 76.
19. Girard M., Allaire P. D., Blondeau F. McPherson P. S. (2005a) Isolation of clathrin-coated vesicles by differential and density gradient centrifugation. Curr. Protoc. Cell. Biol. Chapter 3, Unit 3.13. doi :.
20. Girard M., Allaire P. D., McPherson P. S. Blondeau F. (2005b) Non-stoichiometric relationship between clathrin heavy and light chains revealed by quantitative comparative proteomics of clathrin-coated vesicles from brain and liver. Mol. Cell Proteomics 4, 1145 1154.
21. Goldshmit Y., McLenachan S. Turnley A. (2006) Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res. Rev. 52, 327 345.
22. Gomes R. A., Hampton C., El-Sabeawy F., Sabo S. L. McAllister A. K. (2006) The dynamic distribution of TrkB receptors before, during, and after synapse formation between cortical neurons. J. Neurosci. 26, 11487 11500.
23. Grimes M. L., Zhou J., Beattie E. C. et al. (1996) Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 16, 7950 7964.
24. Grimes M. L., Beattie E. Mobley W. C. (1997) A signaling organelle containing the nerve growth factor-activated receptor tyrosine kinase, TrkA. Proc. Natl Acad. Sci. U S A 94, 9909 9914.
25. Grunwald I. C., Korte M., Adelmann G., Plueck A., Kullander K., Adams R. H., Frotscher M., Bonhoeffer T. Klein R. (2004) Hippocampal plasticity requires postsynaptic ephrinBs. Nat. Neurosci. 7, 33 40.
26. Henderson J. T., Georgiou J., Jia Z., Robertson J., Elowe S., Roder J. C. Pawson T. (2001) The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32, 1041 1056.
27. Himanen J. P. Nikolov D. B. (2003) Eph receptors and ephrins. Int. J. Biochem. Cell Biol. 35, 130 134.
28. Hopper N. A. O'Connor V. (2005) Ephrin tempers two-faced synaptojanin 1. Nat. Cell Biol. 7, 454 456.
29. Huttner W. B., Schiebler W., Greengard P. De Camilli P. (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374 1388.
30. Irie F., Okuno M., Pasquale E. B. Yamaguchi Y. (2005) EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nat. Cell Biol. 7, 501 509.
31. Jiang X., Huang F., Marusyk A. Sorkin A. (2003) Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 14, 858 870.
32. Jin Y. Garner C. C. (2008) Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 24, 237 262.
33. Jung N. Haucke V. (2007) Clathrin-mediated endocytosis at synapses. Traffic 8, 1129 1136.
34. Klein R. (2004) Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr. Opin. Cell Biol. 16, 580 589.
35. Klein R. (2009) Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat. Neurosci. 12, 15 20.
36. Konstantinova I., Nikolova G., Ohara-Imaizumi M., Meda P., Kucera T., Zarbalis K., Wurst W., Nagamatsu S. Lammert E. (2007) EphA-Ephrin-A-mediated beta cell communication regulates insulin secretion from pancreatic islets. Cell 129, 359 370.
37. Lim Y. S., McLaughlin T., Sung T. C., Santiago A., Lee K. F. O'Leary D. D. (2008) p75(NTR) mediates ephrin-A reverse signaling required for axon repulsion and mapping. Neuron 59, 746 758.
38. Marler K. J., Becker-Barroso E., Martinez A. et al. (2008) A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis. J. Neurosci. 28, 12700 12712.
39. Marston D. J., Dickinson S. Nobes C. D. (2003) Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat. Cell Biol. 5, 879 888.
40. Martone M. E., Holash J. A., Bayardo A., Pasquale E. B. Ellisman M. H. (1997) Immunolocalization of the receptor tyrosine kinase EphA4 in the adult rat central nervous system. Brain Res. 771, 238 250.
41. McPherson P. S., Kay B. K. Hussain N. K. (2001) Signaling on the endocytic pathway. Traffic 2, 375 384.
42. Monami G., Emiliozzi V. Morrione A. (2008) Grb10/Nedd4-mediated multiubiquitination of the insulin-like growth factor receptor regulates receptor internalization. J. Cell. Physiol. 216, 426 437.
43. Murai K. K. Pasquale E. B. (2004) Eph receptors, ephrins, and synaptic function. Neuroscientist 10, 304 314.
44. Murai K. K., Nguyen L. N., Irie F., Yamaguchi Y. Pasquale E. B. (2003) Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6, 153 160.
45. Nakata T., Terada S. Hirokawa N. (1998) Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J. Cell Biol. 140, 659 674.
46. Parker M., Roberts R., Enriquez M., Zhao X., Takahashi T., Pat Cerretti D., Daniel T. Chen J. (2004) Reverse endocytosis of transmembrane ephrin-B ligands via a clathrin-mediated pathway. Biochem. Biophys. Res. Commun. 323, 17 23.
47. Pasquale E. B. (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6, 462 475.
48. Poupon V., Girard M., Legendre-Guillemin V., Thomas S., Bourbonniere L., Philie J., Bright N. A. McPherson P. S. (2008) Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc. Natl Acad. Sci. U S A 105, 168 173.
49. Richardson D. S., Lai A. Z. Mulligan L. M. (2006) RET ligand-induced internalization and its consequences for downstream signaling. Oncogene 25, 3206 3211.
50. Rodenas-Ruano A., Perez-Pinzon M. A., Green E. J., Henkemeyer M. Liebl D. J. (2006) Distinct roles for ephrinB3 in the formation and function of hippocampal synapses. Dev. Biol. 292, 34 45.
51. Rosenmund C., Rettig J. Brose N. (2003) Molecular mechanisms of active zone function. Curr. Opin. Neurobiol. 13, 509 519.
52. Shapira M., Zhai R. G., Dresbach T., Bresler T., Torres V. I., Gundelfinger E. D., Ziv N. E. Garner C. C. (2003) Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38, 237 252.
53. Shimizu H., Kawamura S. Ozaki K. (2003) An essential role of Rab5 in uniformity of synaptic vesicle size. J. Cell Sci. 116, 3583 3590.
54. Soans C., Holash J. A. Pasquale E. B. (1994) Characterization of the expression of the Cek8 receptor-type tyrosine kinase during development and in tumor cell lines. Oncogene 9, 3353 3361.
55. Sorkina T., Huang F., Beguinot L. Sorkin A. (2002) Effect of tyrosine kinase inhibitors on clathrin-coated pit recruitment and internalization of epidermal growth factor receptor. J. Biol. Chem. 277, 27433 27441.
56. Star E. N., Newton A. J. Murthy V. N. (2005) Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function. J. Physiol. 569, 103 117.
57. Takamori S., Riedel D. Jahn R. (2000) Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J. Neurosci. 20, 4904 4911.
58. Tao-Cheng J. H. (2007) Ultrastructural localization of active zone and synaptic vesicle proteins in a preassembled multi-vesicle transport aggregate. Neuroscience 150, 575 584.
59. Tremblay M. E., Riad M., Bouvier D., Murai K. K., Pasquale E. B., Descarries L. Doucet G. (2007) Localization of EphA4 in axon terminals and dendritic spines of adult rat hippocampus. J. Comp. Neurol. 501, 691 702.
60. Tremblay M. E., Riad M., Chierzi S., Murai K. K., Pasquale E. B. Doucet G. (2009) Developmental course of EphA4 cellular and subcellular localization in the postnatal rat hippocampus. J. Comp. Neurol. 512, 798 813.
61. Watson F. L., Heerssen H. M., Moheban D. B., Lin M. Z., Sauvageot C. M., Bhattacharyya A., Pomeroy S. L. Segal R. A. (1999) Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J. Neurosci. 19, 7889 7900.
62. Yamaguchi Y. Pasquale E. B. (2004) Eph receptors in the adult brain. Curr. Opin. Neurobiol. 14, 288 296.
63. Zaremba S. Keen J. H. (1983) Assembly polypeptides from coated vesicles mediate reassembly of unique clathrin coats. J. Cell Biol. 97, 1339 1347.
64. Zheng J., Shen W. H., Lu T. J. et al. (2008) Clathrin-dependent endocytosis is required for TrkB-dependent Akt-mediated neuronal protection and dendritic growth. J. Biol. Chem. 283, 13280 13288.
65. Zhou L., Martinez S. J., Haber M. et al. (2007) EphA4 signaling regulates phospholipase Cgamma1 activation, cofilin membrane association, and dendritic spine morphology. J. Neurosci. 27, 5127 5138.
66. Zimmer M., Palmer A., Kohler J. Klein R. (2003) EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat. Cell Biol. 5, 869 878.