Calcyon, a mammalian specific NEEP21 family member, interacts with adaptor protein complex 3 (AP-3) and regulates targeting of AP-3 cargoes

Journal of Neurochemistry

Volumn 123, Issue 1, 2012, Pages 60-72

  Muthusamy, Nagendran ^a,c   Faundez, Victor ^b   Bergson, Clare ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

clathrin mediated endocytosis; PI4KII ; synaptic vesicle; tyrosine motif; YXX ; ZnT3

Indexed keywords

ADAPTOR PROTEIN; CALCYON; CLATHRIN LIGHT CHAIN; MEMBRANE PROTEIN; NEURONAL ENRICHED ENDOSOMAL PROTEIN OF 21; PHOSPHATIDYLINOSITOL 4 KINASE TYPE II ALPHA; PHOSPHATIDYLINOSITOL KINASE; TYROSINE; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER 3;

ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CALCYON GENE; CELLULAR DISTRIBUTION; COATED VESICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE; GENE DELETION; GENE FUNCTION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC REGULATION; HIPPOCAMPAL MOSSY FIBER; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SITE DIRECTED MUTAGENESIS;

ADAPTOR PROTEIN COMPLEX 3; ANALYSIS OF VARIANCE; ANIMALS; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; CLATHRIN; CLATHRIN LIGHT CHAINS; COS CELLS; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MOSSY FIBERS, HIPPOCAMPAL; MUTAGENESIS; MUTATION; NERVE TISSUE PROTEINS; NEURONS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; TRANSFECTION; TYROSINE;

MAMMALIA; MUS;

EID: 84866249528     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07814.x     Document Type: Article

References (41)

1. Acsády L., Kamondi A., Sík A., Freund T., and, Buzsáki G., (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386-3403. (Pubitemid 28186030)
2. Ali M. K., and, Bergson C., (2003) Elevated intracellular calcium triggers recruitment of the receptor cross-talk accessory protein calcyon to the plasma membrane. J.Biol.Chem. 278, 51654-51663. (Pubitemid 38020411)
3. Baust T., Anitei M., Czupalla C., Parshyna I., Bourel L., Thiele C., Krause E., and, Hoflack B., (2008) Protein networks supporting AP-3 function in targeting lysosomal membrane proteins. Mol. Biol. Cell 19, 1942-1951.
4. Bonifacino J. S., and, Traub L.M., (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447. (Pubitemid 36930451)
5. Chicurel M. E., and, Harris K. M., (1992) Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J. Comp. Neurol. 325, 169-182.
6. Craige B., Salazar G., and, Faundez V., (2008) Phosphatidylinositol-4- kinase type II alpha contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic. Mol. Biol. Cell 19, 1415-1426. (Pubitemid 351805096)
7. Creutz C. E., and, Snyder S. L., (2005) Interactions of annexins with the mu subunits of the clathrin assembly proteins. Biochemistry 44, 13795-13806. (Pubitemid 41507460)
8. Davidson H. T., Xiao J., Dai R., and, Bergson C., (2009) Calcyon is necessary for activity-dependent AMPA receptor internalization and LTD in CA1 neurons of hippocampus. Eur.J.Neurosci. 29, 42-54.
9. Debaigt C., Hirling H., Steiner P., Vincent J. P., and, Mazella J., (2004) Crucial role of neuron-enriched endosomal protein of 21 kDa in sorting between degradation and recycling of internalized G-protein-coupled receptors. J.Biol.Chem. 279, 35687-35691. (Pubitemid 39100572)
10. Deborde S., Perret E., Gravotta D., Deora A., Salvarezza Schreiner S. R., and, Rodriguez-Boulan E., (2008) Clathrin is a key regulator of basolateral polarity. Nature 452, 719-723. (Pubitemid 351521081)
11. Dell' Angelica E. C., (2009) AP-3-dependent trafficking and disease: the first decade. Curr. Opin. Cell Biol. 21, 552-559.
12. Feng L., Seymour A. B., Jiang S., et al. (1999) The beta3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky-Pudlak syndrome and night blindness. Hum. Mol. Genet. 8, 323-330. (Pubitemid 29054274)
13. Gan Y., McGraw T. E., and, Rodriguez-Boulan E., (2002) The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat. Cell Biol. 4, 605-609.
14. Kirchhausen T., (1999) Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 15, 705-732. (Pubitemid 32250390)
15. Larimore J., Tornieri K., Ryder P. V., et al. (2011) The schizophrenia susceptibility factor dysbindin and its associated complex sort cargoes from cell bodies to the synapse. Mol. Biol. Cell 22, 4854-4867.
16. Luscher C., Xia H., Beattie E. C., Carroll R. C., von Zastrow M., Malenka R. C., and, Nicoll R. A., (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24, 649-658.
17. Muthusamy N., Ahmed S. A., Rana B. K., Navarre S., Kozlowski D. J., Liberles D. A., and, Bergson C., (2009) Phylogenetic analysis of the NEEP21/calcyon/P19 family of endocytic proteins: evidence for functional evolution in the vertebrate CNS. J. Mol. Evol. 69, 319-332.
18. Nakatsu F., Okada M., Mori F., et al. (2004) Defective function of GABA-containing synaptic vesicles in mice lacking the AP-3B clathrin adaptor. J. Cell Biol. 167, 293-302. (Pubitemid 39435072)
19. Newell-Litwa K., Seong E., Burmeister M., and, Faundez V., (2007) Neuronal and non-neuronal functions of the AP-3 sorting machinery. J. Cell Sci. 120, 531-541. (Pubitemid 46437888)
20. Newell-Litwa K., Salazar G., Smith Y., and, Faundez V., (2009) Roles of BLOC-1 and adaptor protein-3 complexes in cargo sorting to synaptic vesicles. Mol. Biol. Cell 20, 1441-1453.
21. Newell-Litwa K., Chintala S., Jenkins S., Pare J.-F., McGaha L., Smith Y., and, Faundez V., (2010) Hermansky-Pudlak protein complexes, AP-3 and BLOC-1, differentially regulate presynaptic composition in the striatum and hippocampus. J. Neurosci. 30, 820-831.
22. Oakman S. A., and, Meador-Woodruff J. H., (2004) Calcyon transcript expression in macaque brain. J.Comp Neurol. 468, 264-276. (Pubitemid 37490357)
23. Ohno H., Aguilar R. C., Yeh D., Taura D., Saito T., and, Bonifacino J. S., (1998) The medium subunits of adaptor complexes recognize distinct but overlapping sets of tyrosine-based sorting signals. J. Biol. Chem. 273, 25915-25921. (Pubitemid 28475822)
24. Ooi C. E., Dell'Angelica E. C., and, Bonifacino J. S., (1998) ADP-Ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol. 142, 391-402. (Pubitemid 28361547)
25. Owen D. J., and, Evans P.R., (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1327-1332. (Pubitemid 28524497)
26. Poupon V., Girard M., Legendre-Guillemin V., Thomas S., Bourbonniere L., Philie J., Bright N. A., and, McPherson P. S., (2008) Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc. Natl Acad. Sci. USA 105, 168-173.
27. Saberan-Djoneidi D., Marey-Semper I., Picart R., Studler J. M., Tougard C., Glowinski J., and, Levi-Strauss M., (1995) A 19-kDa protein belonging to a new family is expressed in the Golgi apparatus of neural cells. J.Biol.Chem. 270, 1888-1893.
28. Saberan-Djoneidi D., Picart R., Escalier D., Gelman M., Barret A., Tougard C., Glowinski J., and, Levi-Strauss M., (1998) A 21-kDa polypeptide belonging to a new family of proteins is expressed in the Golgi apparatus of neural and germ cells. J.Biol.Chem. 273, 3909-3914. (Pubitemid 28103249)
29. Salazar G., Love R., Styers M. L., Werner E., Peden A., Rodriguez S., Gearing M., Wainer B.H., and, Faundez V., (2004a) AP-3-dependent mechanisms control the targeting of a chloride channel (ClC-3) in neuronal and non-neuronal cells. J. Biol. Chem. 279, 25430-25439. (Pubitemid 38756800)
30. Salazar G., Love R., Werner E., Doucette M. M., Cheng S., Levey A., and, Faundez V., (2004b) The zinc transporter ZnT3 interacts with AP-3 and it is preferentially targeted to a distinct synaptic vesicle subpopulation. Mol. Biol. Cell 15, 575-587. (Pubitemid 38146475)
31. Salazar G., Craige B., Wainer B. H., Guo J., De Camilli P., and, Faundez V., (2005) Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 16, 3692-3704. (Pubitemid 41077079)
32. Scheuber A., Rudge R., Danglot L., Raposo G., Binz T., Poncer J.-C., and, Galli T., (2006) Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc. Natl Acad. Sci. USA 103, 16562-16567. (Pubitemid 44715235)
33. Seong E., Wainer B. H., Hughes E. D., Saunders T. L., Burmeister M., and, Faundez V., (2005) Genetic analysis of the neuronal and ubiquitous AP-3 adaptor complexes reveals divergent functions in brain. Mol. Biol. Cell 16, 128-140. (Pubitemid 40024297)
34. Steiner P., Sarria J. C., Glauser L., Magnin S., Catsicas S., and, Hirling H., (2002) Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD. J.Cell Biol. 157, 1197-1209. (Pubitemid 34847790)
35. Steiner P., Alberi S., Kulangara K., et al. (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J. 24, 2873-2884. (Pubitemid 43079891)
36. Suyama S., Hikima T., Sakagami H., Ishizuka T., and, Yawo H., (2007) Synaptic vesicle dynamics in the mossy fiber-CA3 presynaptic terminals of mouse hippocampus. Neurosci. Res. 59, 481-490. (Pubitemid 350007818)
37. Trantham-Davidson H., Vazdarjanova A., Dai R., Terry A., and, Bergson C., (2008) Up-regulation of calcyon results in locomotor hyperactivity and reduced anxiety in mice. Behav.Brain Res. 189, 244-249.
38. Voglmaier S. M., Kam K., Yang H., Fortin D. L., Hua Z., Nicoll R. A., and, Edwards R. H., (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51, 71-84. (Pubitemid 43963342)
39. Xiao J., Dai R., Negyessy L., and, Bergson C., (2006) Calcyon, a novel partner of clathrin light chain, stimulates clathrin-mediated endocytosis. J.Biol.Chem. 281, 15182-15193. (Pubitemid 43855108)
40. Yap C. C., Wisco D., Kujala P., Lasiecka Z. M., Cannon J. T., Chang M. C., Hirling H., Klumperman J., and, Winckler B., (2008) The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J.Cell Biol. 180, 827-842. (Pubitemid 351397781)
41. Zelenin S., Aperia A., and, Diaz H. R., (2002) Calcyon in the rat brain: cloning of cDNA and expression of mRNA. J.Comp Neurol. 446, 37-45. (Pubitemid 34252848)