Disruption of the endocytic protein HIP1 results in neurological deficits and decreased AMPA receptor trafficking

EMBO Journal

Volumn 22, Issue 13, 2003, Pages 3254-3266

  Metzler, Martina ^a   Li, Bo ^e   Gan, Lu ^a   Georgiou, John ^b   Gutekunst, Claire Anne ^d   Wang, Yushan ^e   Torre, Enrique ^d   Devon, Rebecca S ^a   Oh, Rosemary ^a   Legendre Guillemin, Valerie ^c   Rich, Mark ^d   Alvarez, Christine ^a   Gertsenstein, Marina ^b   McPhersons, Peter S ^c   Nagy, Andras ^b   Wang, Yu Tian ^e   Roder, John C ^b   Raymond, Lynn A ^e   Hayden, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NONE

Author keywords

Clathrin; Endocytosis; Glutamate receptors; Huntington's disease; Synapse

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; CLATHRIN; GLUTAMATE RECEPTOR; HUNTINGTIN INTERACTING PROTEIN 1; LIPOSOME; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CENTRAL NERVOUS SYSTEM; COATED VESICLE; CONTROLLED STUDY; DOSE RESPONSE; EMBRYO; ENDOCYTOSIS; FAILURE TO THRIVE; FEMALE; GENE; GENE MUTATION; HIP1 GENE; HIPPOCAMPUS; HUNTINGTON CHOREA; IN VIVO STUDY; INTERNALIZATION; KYPHOSIS; MALE; MOUSE; NERVE CELL STIMULATION; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; SYNAPSE; TREMOR;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; BRAIN; CARRIER PROTEINS; CLATHRIN; COLORIMETRY; DNA-BINDING PROTEINS; ENDOCYTOSIS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MICE; PHENOTYPE; PREGNANCY; PROTEIN TRANSPORT; RECEPTORS, AMPA; SPINAL CORD;

ANIMALIA;

EID: 0037926396     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg334     Document Type: Article

References (54)

1. Ahle, S., Mann, A., Eichelsbacher, U. and Ungewickell, E. (1988) Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J., 7, 919-929.
2. Brodsky, F.M., Chen, C.Y., Knuehl, C., Towler, M.C. and Wakeham, D.E. (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell. Dev. Biol., 17, 517-568.
3. Buckley, K.M., Melikian, H.E., Provoda, C.J. and Waring, M.T. (2000) Regulation of neuronal function by protein trafficking: a role for the endosomal pathway. J. Physiol., 525, 11-19.
4. Burbea, M., Dreier, L., Dittman, J.S., Grunwald, M.E. and Kaplan, J.M. (2002) Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron, 35, 107-120.
5. Carroll, R.C., Beattie, E.C., Xia, H., Luscher, C., Altschuler, Y., Nicoll, R.A., Malenka, R.C. and Von Zastrow, M. (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc. Natl Acad. Sci. USA, 96, 14112-14117.
6. Chopra, V.S. et al. (2000) HIP12 is a non-proapoptotic member of a gene family including HIP1, an interacting protein with huntingtin. Mamm. Genome, 11, 1006-1015.
7. Cremona, O. et al. (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell, 99, 179-188.
8. De Camilli, P., Slepnev, V.I., Shupliakov, O. and Brodin, L. (2001) Synaptic vesicle endocytosis. In Cowan, W.M., Sudhof, T.C., Stevens, C.F. and Davies, K. (eds), Synapse. The Johns Hopkins University Press, Baltimore, MD, pp. 217-274.
9. DiFiglia, M. et al. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron, 14, 1075-1081.
10. Di Paolo, G. et al. (2002). Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron, 33, 789-804.
11. Ehlers, M.D. (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron, 28, 511-525.
12. Faber, P.W., Barnes, G.T., Srinidhi, J., Chen, J., Gusella, J.F. and MacDonald, M.E. (1998) Huntingtin interacts with a family of WW domain proteins. Hum. Mol. Genet., 7, 1463-1474.
13. 4,5P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science, 291, 1051-1055.
14. Ford, M.G., Mills, I.G., Peter, B.J., Vallis, Y., Praefcke, G.J., Evans, P.R. and McMahon, H.T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature, 419, 361-366.
15. Gervais, F.G. et al. (2002) Recruitment and activation of caspase-8 by the Huntingtin-interacting protein Hip-1 and a novel partner Hippi. Nat. Cell Biol., 4, 95-105.
16. Gonzalez-Gaitan, M. and Jackle, H. (1997) Role of Drosophila α-adaptin in presynaptic vesicle recycling. Cell, 88, 767-776.
17. Hao, W., Luo, Z., Zheng, L., Prasad, K. and Lafer, E.M. (1999) AP180 and AP-2 interact directly in a complex that cooperatively assembles clathrin. J. Biol. Chem., 274, 22785-22794.
18. Hardingham, G.E., Fukunaga, Y. and Bading, H. (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci., 5, 405-414.
19. Hussain, N.K., Yamabhai, M., Bhakar, A.L., Metzler, M., Ferguson, S.S.G., Hayden, M.R., McPherson, P.S. and Kay, B.K. (2003) A role for ENTH/ANTH domains in tubulin binding. J. Biol. Chem., submitted.
20. Inglis, F.M., Crockett, R., Korada, S., Abraham, W.C., Hollmann, M. and Kalb, R.G. (2002) The AMPA receptor subunit GluR1 regulates dendritic architecture of motor neurons. J. Neurosci., 22, 8042-8051.
21. Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S. and Takenawa, T. (2001) Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science, 291, 1047-1051.
22. Johnston, M.V. (1997) Hypoxic and ischemic disorders of infants and children. Lecture for 38th meeting of Japanese Society of Child Neurology, Tokyo, Japan, July 1996. Brain Dev., 19, 235-239.
23. Kalchman, M.A. et al. (1997) HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain. Nat. Genet., 16, 44-53.
24. Lee, S.H., Liu, L., Wang, Y.T. and Sheng, M. (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron, 36, 661-674.
25. Legendre-Guillemin, V., Metzler, M., Charbonneau, M., Gan, L., Chopra, V., Philie, J., Hayden, M.R. and McPherson, P.S. (2002) HIP1 and HIP12 display differential binding to F-actin, AP2, and clathrin. Identification of a novel interaction with clathrin light chain. J. Biol. Chem., 277, 19897-19904.
26. Glued. J. Neurosci., 18, 1261-1269.
27. Li, X.J., Li, S.H., Sharp, A.H., Nucifora, F.C., Jr., Schilling, G., Lanahan, A., Worley, P., Snyder, S.H. and Ross, C.A. (1995) A huntingtin-associated protein enriched in brain with implications for pathology. Nature, 378, 398-402.
28. Li, Y., Chin, L.S., Levey, A.I. and Li, L. (2002) Huntingtin-associated protein 1 interacts with hepatocyte growth factor-regulated tyrosine kinase substrate and functions in endosomal trafficking. J. Biol. Chem., 277, 28212-28221.
29. Lin, J.W., Ju, W., Foster, K., Lee, S.H., Ahmadian, G., Wyszynski, M., Wang, Y.T. and Sheng, M. (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat. Neurosci., 3, 1282-1290.
30. Lissin, D.V., Carroll, R.C., Nicoll, R.A., Malenka, R.C. and Von Zastrow, M. (1999) Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J. Neurosci., 19, 1263-1272.
31. Lobe, C.G., Koop, K.E., Kreppner, W., Lomeli, H., Gertsenstein, M. and Nagy, A. (1999) Z/AP, a double reporter for cre-mediated recombination. Dev. Biol., 208, 281-292.
32. Malinow, R. and Malenka, R.C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci., 25, 103-126.
33. Man, H.Y., Lin, J.W., Ju, W.H., Ahmadian, G., Liu, L., Becker, L.E., Sheng, M. and Wang, Y.T. (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron, 25, 649-662.
34. Martin, L.J., Furuta, A. and Blackstone, C.D. (1998) AMPA receptor protein in developing rat brain: glutamate receptor-1 expression and localization change at regional, cellular, and subcellular levels with maturation. Neuroscience, 83, 917-928.
35. McPherson, P.S., Kay, B.K. and Hussain, N.K. (2001) Signaling on the endocytic pathway. Traffic, 2, 375-384.
36. Metzler, M., Gertz, A., Sarkar, M., Schachter, H., Schrader, J.W. and Marth, J.D. (1994) Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J., 13, 2056-2065.
37. Metzler, M., Legendre-Guillemin, V., Gan, L., Chopra, V., Kwok, A., McPherson, P.S. and Hayden, M.R. (2001) HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J. Biol. Chem., 276, 39271-39276.
38. Miller, W.E. and Lefkowitz, R.J. (2001) Arrestins as signaling molecules involved in apoptotic pathways: a real eye opener. Sci. STKE., 2001, E1.
39. Mishra, S.K., Agostinelli, N.R., Brett, T.J., Mizukami, I., Ross, T.S. and Traub, L.M. (2001) Clathrin- and AP-2-binding sites in HIP1 uncover a general assembly role for endocytic accessory proteins. J. Biol. Chem., 276, 46230-46236.
40. Mishra, S.K., Keyel, P.A., Hawryluk, M.J., Agostinelli, N.R., Watkins, S.C. and Traub, L.M. (2002) Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J., 21, 4915-4926.
41. Ohno, H. et al. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science, 269, 1872-1875.
42. Prange, O. and Murphy, T.H. (2001) Modular transport of postsynaptic density-95 clusters and association with stable spine precursors during early development of cortical neurons. J. Neurosci., 21, 9325-9333.
43. Roche, K.W., Standley, S., McCallum, J., Dune, L.C., Ehlers, M.D. and Wenthold, R.J. (2001) Molecular determinants of NMDA receptor internalization. Nat. Neurosci., 4, 794-802.
44. Rosenthal, J.A., Chen, H., Slepnev, V.I., Pellegrini, L., Salcini, A.E., Di Fiore, P.P. and De Camilli, P. (1999) The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module. J. Biol. Chem., 274, 33959-33965.
45. Sheng, M. and Kim, M.J. (2002) Postsynaptic signaling and plasticity mechanisms. Science, 298, 776-780.
46. Sittler, A., Walter, S., Wedemeyer, N., Hasenbank, R., Scherzinger, E., Eickhoff, H., Bates, G.P., Lehrach, H. and Wanker, E.E. (1998) SH3GL3 associates with the Huntingtin exon 1 protein and promotes the formation of polygin-containing protein aggregates. Mol. Cell, 2, 427-436.
47. Snyder, E.M., Philpot, B.D., Huber, K.M., Dong, X., Fallon, J.R. and Bear, M.F. (2001) Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat. Neurosci., 4, 1079-1085.
48. Sun, J.Y., Wu, X.S. and Wu, L.G. (2002) Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature, 417, 555-559.
49. Takei, K., Mundigl, O., Daniell, L. and De Camilli, P. (1996) The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol., 133, 1237-1250.
50. Tanaka, H., Grooms, S.Y., Bennett, M.V. and Zukin, R.S. (2000) The AMPAR subunit GluR2: still front and center-stage. Brain Res., 886, 190-207.
51. Verstreken, P., Kjaerulff, O., Lloyd, T.E., Atkinson, R., Zhou, Y., Meinertzhagen, I.A. and Bellen, H.J. (2002) Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell, 109, 101-112.
52. Waelter, S. et al. (2001) The huntingtin interacting protein HIP1 is a clathrin and α-adaptin-binding protein involved in receptor-mediated endocytosis. Hum. Mol. Genet., 10, 1807-1817.
53. Wanker, E.E., Rovira, C., Scherzinger, E., Hasenbank, R., Walter, S., Tait, D., Colicelli, J. and Lehrach, H. (1997) HIP-1: a huntingtin interacting protein isolated by the yeast two-hybrid system. Hum. Mol. Genet., 6, 487-495.
54. Zhang, B., Koh, Y.H., Beckstead, R.B., Budnik, V., Ganetzky, B. and Bellen, H.J. (1998) Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron, 21, 1465-1475.