Neuronal and non-neuronal functions of the AP-3 sorting machinery

Journal of Cell Science

Volumn 120, Issue 4, 2007, Pages 531-541

  Newell Liwa, Karen ^a,b   Seong, Eunju ^c,d   Burmeister, Margit ^c   Faundez, Victor ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d NONE   (United States)

Author keywords

AP 3; BLOC 1; Dysbindin; Hermansky Pudlak; Mental disorder; Schizophrenia; Synaptic vesicle; Zine transporter; ZnT3

Indexed keywords

ADAPTOR PROTEIN; LIPID TRANSFER PROTEIN; MEMBRANE PROTEIN; NEUROTRANSMITTER; SYNAPTOBREVIN;

ANIMAL CELL; ARTICLE; CELL SELECTION; ENZYME REGULATION; LYSOSOME; MELANOSOME; MEMBRANE VESICLE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; SCHIZOPHRENIA; SYNAPSE VESICLE;

ADAPTOR PROTEIN COMPLEX 3; ANIMALS; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; NEURONS; ORGANELLES; PROTEIN TRANSPORT;

MUS;

EID: 33947317259     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03365     Document Type: Article

References (138)

1. Alberts, P., Rudge, R., Hinners, I., Muzerelle, A., Martinez-Arca, S., Irinopoulou, T., Marthiens, V., Tooze, S., Rathjen, F., Gaspar, P. et al. (2003). Cross talk between tetanus neurotoxin-insensitive vesicle-associated membrane protein-mediated transport and L1-mediated adhesion. Mol. Biol. Cell 14, 4207-4220.
2. Austin, C., Boehm, M. and Tooze, S. A. (2002). Site-specific cross-linking reveals a differential direct interaction of class 1, 2, and 3 ADP-ribosylation factors with adaptor protein complexes 1 and 3. Biochemistry 41, 4669-4677.
3. Balla, A. and Balla, T. (2006). Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 16, 351-361.
4. Balla, A., Tuymetova, G., Barshishat, M., Geiszt, M. and Balla, T. (2002). Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 277, 20041-20050.
5. Balla, T. (2005). Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J. Cell Sci. 118, 2093-2104.
6. Benson, K. F., Li, F. Q., Person, R. E., Albani, D., Duan, Z., Wechsler, J., Meade-White, K., Williams, K., Acland, G. M., Niemeyer, G. et al. (2003). Mutations associated with neutropenia in dogs and humans disrupt intracellular transport of neutrophil elastase. Nat. Genet. 35, 90-96.
7. Benson, M. A., Sillitoe, R. V. and Blake, D. J. (2004). Schizophrenia genetics: dysbindin under the microscope. Trends Neurosci. 27, 516-519.
8. Blondeau, F., Ritter, B., Allaire, P. D., Wasiak, S., Girard, M., Hussain, N. K., Angers, A., Legendre-Guillemin, V., Roy, L., Boismenu, D. et al. (2004). Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. USA 101, 3833-3838.
9. Blumstein, J., Faundez, V., Nakatsu, F., Saito, T., Ohno, H. and Kelly, R. B. (2001). The neuronal form of adaptor protein-3 is required for synaptic vesicle formation from endosomes. J. Neurosci. 21, 8034-8042.
10. Boehm, M. and Bonifacino, J. S. (2001). Adaptins: the final recount. Mol. Biol. Cell 12, 2907-2920.
11. Boehm, M. and Bonifacino, J. S. (2002). Genetic analyses of adaptin function from yeast to mammals. Gene 286, 175-186.
12. Bogdanovic, A., Bennett, N., Kieffer, S., Louwagie, M., Mono, T., Garin, J., Satre, M. and Bruckert, F. (2002). Syntaxin 7, syntaxin 8, Vti1 and VAMP7 (vesicle-associated membrane protein 7) form an active SNARE complex for early macropinocytic compartment fusion in Dictyostelium discoideum. Biochem. J. 368, 29-39.
13. Bonifacino, J. S. and Glick, B. S. (2004). The mechanisms of vesicle budding and fusion. Cell 116, 153-166.
14. Borner, G. H., Harbour, M., Hester, S., Lilley, K. S. and Robinson, M. S. (2006). Comparative proteomics of clathrin-coated vesicles. J. Cell Biol. 175, 571-578.
15. Bray, N. J., Preece, A., Williams, N. M., Moskvina, V., Buckland, P. R., Owen, M. J. and O'Donovan, M. C. (2005). Haplotypes at the dystrobrevin binding protein 1 (DTNBP1) gene locus mediate risk for schizophrenia through reduced DTNBP1 expression. Hum. Mol. Genet. 14, 1947-1954.
16. Breen, G., Prata, D., Osborne, S., Munro, J., Sinclair, M., Li, T., Staddon, S., Dempster, D., Sainz, R., Arroyo, B. et al. (2006). Association of the dysbindin gene with bipolar affective disorder. Am. J. Psychiatry 163, 1636-1638.
17. Camargo, L. M., Collura, V., Rain, J. C., Mizuguchi, K., Hermjakob, H., Kerrien, S., Bonnert, T. P., Whiting, P. J. and Brandon, N. J. (2007). Disrupted in Schizophrenia 1 Interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol. Psychiatry 12, 74-86.
18. Clark, R. H., Stinchcombe, J. C., Day, A., Blott, E., Booth, S., Bossi, G., Hamblin, T., Davies, E. G. and Griffiths, G. M. (2003). Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat. Immunol. 4, 1111-1120.
19. Cole, T. B., Wenzel, H. J., Kafer, K. E., Schwartzkroin, P. A. and Palmiter, R. D. (1999). Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc. Natl. Acad. Sci. USA 96, 1716-1721.
20. Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R. and Owen, D. J. (2002). Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523-535.
21. Conner, S. D. and Schmid, S. L. (2003). Regulated portals of entry into the cell. Nature 422, 37-44.
22. Crump, C. M., Xiang, Y., Thomas, L., Gu, F., Austin, C., Tooze, S. A. and Thomas, G. (2001). PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 20, 2191-2201.
23. Darnell, R. B., Furneaux, H. M. and Posner, J. B. (1991). Antiserum from a patient with cerebellar degeneration identifies a novel protein in Purkinje cells, cortical neurons, and neuroectodermal tumors. J. Neurosci. 11, 1224-1230.
24. Dell'Angelica, E. C. (2001). Clathrin-binding proteins: got a motif? Join the network! Trends Cell Biol. 11, 315-318.
25. Dell'Angelica, E. C., Ohno, H., Ooi, C. E., Rabinovich, E., Roche, K. W. and Bonifacino, J. S. (1997a). AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J. 16, 917-928.
26. Dell'Angelica, E. C., Ooi, C. E. and Bonifacino, J. S. (1997b). Beta3A-adaptin, a subunit of the adaptor-like complex AP-3. J. Biol. Chem. 272, 15078-15084.
27. Dell'Angelica, E. C., Klumperman, J., Stoorvogel, W. and Bonifacino, J. S. (1998). Association of the AP-3 adaptor complex with clathrin. Science 280, 431-434.
28. Dell'Angelica, E. C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A. and Bonifacino, J. S. (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21.
29. Di Paolo, G. and De Camilli, P. (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657.
30. Di Pietro, S. M. and Dell'Angelica, E. C. (2005). The cell biology of Hermansky-Pudlak syndrome: recent advances. Traffic 6, 525-533.
31. Di Pietro, S. M., Falcon-Perez, J. M., Tenza, D., Setty, S. R., Marks, M. S., Raposo, G. and Dell'angelica, E. C. (2006). BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes. Mol. Biol. Cell 17, 4027-4038.
32. Dong, X., Li, H., Derdowski, A., Ding, L., Burnett, A., Chen, X., Peters, T. R., Dermody, T. S., Woodruff, E., Wang, J. J. et al. (2005). AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 120, 663-674.
33. Drake, M. T., Zhu, Y. and Kornfeld, S. (2000). The assembly of AP-3 adaptor complex-containing clathrin-coated vesicles on synthetic liposomes. Mol. Biol. Cell 11, 3723-3736.
34. Faundez, V. and Kelly, R. B. (2000). The AP-3 complex required for endosomal synaptic vesicle biogenesis is associated with a casein kinase ialpha-like isoform. Mol. Biol. Cell 11, 2591-2604.
35. Faundez, V., Horng, J. T. and Kelly, R. B. (1997). ADP ribosylation factor 1 is required for synaptic vesicle budding in PC12 cells. J. Cell Biol. 138, 505-515.
36. Faundez, V., Horng, J. T. and Kelly, R. B. (1998). A function for the AP-3 coat complex in synaptic vesicle formation from endosomes. Cell 93, 423-432.
37. Feng, L., Seymour, A. B., Jiang, S., To, A., Peden, A. A., Novak, E. K., Zhen, L., Rusiniak, M. E., Eicher, E. M., Robinson, M. 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.
38. Folsch, H., Ohno, H., Bonifacino, J. S. and Mellman, I. (1999). A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99, 189-198.
39. Folsch, H., Pypaert, M., Schu, P. and Mellman, I. (2001). Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152, 595-606.
40. Folsch, H., Pypaert, M., Maday, S., Pelletier, L. and Mellman, I. (2003). The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J. Cell Biol. 163, 351-362.
41. Fontana, S., Parolini, S., Vermi, W., Booth, S., Gallo, F., Donini, M., Benassi, M., Gentili, F., Ferrari, D., Notarangelo, L. D. et al. (2006). Innate immunity defects in Hermansky-Pudlak type 2 syndrome. Blood 107, 4857-4864.
42. Funke, B., Finn, C. T., Plocik, A. M., Lake, S., DeRosse, P., Kane, J. M., Kucherlapati, R. and Malhotra, A. K. (2004). Association of the DTNBP1 locus with schizophrenia in a U.S. population. Am. J. Hum. Genet. 75, 891-898.
43. Gautam, R., Novak, E. K., Tan, J., Wakamatsu, K., Itoh, S. and Swank, R. T. (2006). Interaction of Hermansky-Pudlak syndrome genes in the regulation of lysosome-related organelles. Traffic 7, 779-792.
44. Gissen, P., Johnson, C. A., Morgan, N. V., Stapelbroek, J. M., Forshew, T., Cooper, W. N., McKiernan, P. J., Klomp, L. W., Morris, A. A., Wraith, J. E. et al. (2004). Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat. Genet. 36, 400-404.
45. Grabner, C. P., Price, S. D., Lysakowski, A., Cahill, A. L. and Fox, A. P. (2006). Regulation of large dense-core vesicle volume and neurotransmitter content mediated by adaptor protein 3. Proc. Natl. Acad. Sci. USA 103, 10035-10040.
46. Guo, J., Weak, M. R., Pellegrini, L., Onofri, F., Benfenati, F. and De Camilli, P. (2003). Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. USA 100, 3995-4000.
47. Gurkan, C., Lapp, H., Alory, C., So, A. I., Hogenesch, J. B. and Balch, W. E. (2005). Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol. Biol. Cell 16, 3847-3864.
48. Halim, N. D., Weickert, C. S., McClintock, B. W., Hyde, T. M., Weinberger, D. R., Kleinman, J. E. and Lipska, B. K. (2003). Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development. Mol. Psychiatry 8, 797-810.
49. Heldwein, E. E., Macia, E., Wang, J., Yin, H. L., Kirchhausen, T. and Harrison, S. C. (2004). Crystal structure of the clathrin adaptor protein 1 core. Proc. Natl. Acad. Sci. USA 101, 14108-14113.
50. Heuser, J. E. and Reese, T. S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344.
51. Hinrichsen, L., Meyerholz, A., Groos, S. and Ungewickell, E. J. (2006). Bending a membrane: how clathrin affects budding. Proc. Natl. Acad. Sci. USA 103, 8715-8720.
52. Honer, W. G. and Young, C. E. (2004). Presynaptic proteins and schizophrenia. Int. Rev. Neurobiol. 59, 175-199.
53. Honer, W. G., Falkai, P., Bayer, T. A., Xie, J., Hu, L., Li, H. Y., Arango, V., Mann, J. J., Dwork, A. J. and Trimble, W. S. (2002). Abnormalities of SNARE mechanism proteins in anterior frontal cortex in severe mental illness. Cereb. Cortex 12, 349-356.
54. Huang, L., Kuo, Y. M. and Gitschier, J. (1999). The pallid gene encodes a novel, syntaxin 13-interacting protein involved in platelet storage pool deficiency. Nat. Genet. 23, 329-332.
55. Ilardi, J. M., Mochida, S. and Sheng, Z. H. (1999). Snapin: a SNARE-associated protein implicated in synaptic transmission. Nat. Neurosci. 2, 119-124.
56. Jackson, C. L. and Casanova, J. E. (2000). Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 10, 60-67.
57. Janvier, K., Kato, Y., Boehm, M., Rose, J. R., Martina, J. A., Kim, B. Y., Venkatesan, S. and Bonifacino, J. S. (2003). Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 gamma-sigmal and AP-3 delta-sigma3 hemicomplexes. J. Cell Biol. 163, 1281-1290.
58. Jung, J., Bohn, G., Allroth, A., Boztug, K., Brandes, G., Sandrock, I., Schaffer, A. A., Rathinam, C., Kollner, I., Beger, C. et al. (2006). Identification of a homozygous deletion in the AP3B1 gene causing Hermansky-Pudlak syndrome, type 2. Blood 108, 362-369.
59. Kantheti, P., Qiao, X., Diaz, M. E., Peden, A. A., Meyer, G. E., Carskadon, S. L., Kapfhamer, D., Sufalko, D., Robinson, M. S., Noebels, J. L. et al. (1998). Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21, 111-122.
60. Kantheti, P., Diaz, M. E., Peden, A. E., Seong, E. E., Dolan, D. F., Robinson, M. S., Noebels, J. L. and Burmeister, M. L. (2003). Genetic and phenotypic analysis of the mouse mutant mh(2J), an Ap3d allele caused by IAP element insertion. Mamm. Genome 14, 157-167.
61. Kirchhausen, T. (2000). Clathrin. Annu. Rev. Biochem. 69, 699-727.
62. Knable, M. B., Barci, B. M., Webster, M. J., Meador-Woodruff, J. and Torrey, E. F. (2004). Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol. Psychiatry 9, 609-620, 544.
63. Lalli, G., Bohnert, S., Deinhardt, K., Verastegui, C. and Schiavo, G. (2003). The journey of tetanus and botulinum neurotoxins in neurons. Trends Microbiol. 11, 431-437.
64. Lane, P. W. and Deol, M. S. (1974). Mocha, a new coat color and behavior mutation on chromosome 10 of the mouse. J. Hered. 65, 362-364.
65. Lefrancois, S., Janvier, K., Boehm, M., Ooi, C. E. and Bonifacino, J. S. (2004). An ear-core interaction regulates the recruitment of the AP-3 complex to membranes. Dev. Cell 7, 619-625.
66. Li, W., Rusiniak, M. E., Chintala, S., Gautam, R., Novak, E. K. and Swank, R. T. (2004). Murine Hermansky-Pudlak syndrome genes: regulators of lysosome-related organelles. BioEssays 26, 616-628.
67. Li, W., Zhang, Q., Oiso, N., Novak, E. K., Gautam, R., O'Brien, E. P., Tinsley, C. L., Blake, D. J., Spritz, R. A., Copeland, N. G. et al. (2003). Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat. Genet. 35, 84-89.
68. Lim, D. S., Kirsch, D. G., Canman, C. E., Ahn, J. H., Ziv, Y., Newman, L. S., Darnell, R. B., Shiloh, Y. and Kastan, M. B. (1998). ATM binds to beta-adaptin in cytoplasmic vesicles. Proc. Natl. Acad. Sci. USA 95, 10146-10151.
69. Lloyd, V., Ramaswami, M. and Kramer, H. (1998). Not just pretty eyes: Drosophila eye-colour mutations and lysosomal delivery. Trends Cell Biol. 8, 257-259.
70. Martinez-Arca, S., Rudge, R., Vacca, M., Raposo, G., Camonis, J., Proux-Gillardeaux, V., Daviet, L., Formstecher, E., Hamburger, A., Filippini, F. et al. (2003). A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. USA 100, 9011-9016.
71. Miller, C. L., Burmeister, M. and Stevens, K. E. (1999). Hippocampal auditory gating in the hyperactive mocha mouse. Neurosci. Lett. 276, 57-60.
72. Minogue, S., Waugh, M. G., De Matteis, M. A., Stephens, D. J., Berditchevski, F. and Hsuan, J. J. (2006). Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J. Cell Sci. 119, 571-581.
73. Mirnics, K., Middleton, F. A., Marquez, A., Lewis, D. A. and Levitt, P. (2000). Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 28, 53-67.
74. Miwako, I., Schroter, T. and Schmid, S. L. (2003). Clathrin- and dynamin-dependent coated vesicle formation from isolated plasma membranes. Traffic 4, 376-389.
75. Moriyama, K. and Bonifacino, J. S. (2002). Pallidin is a component of a multi-protein complex involved in the biogenesis of lysosome-related organelles. Traffic 3, 666-677.
76. Mukaetova-Ladinska, E. B., Hurt, J., Honer, W. G., Harrington, C. R. and Wischik, C. M. (2002). Loss of synaptic but not cytoskeletal proteins in the cerebellum of chronic schizophrenics. Neurosci. Lett. 317, 161-165.
77. Mullock, B. M., Smith, C. W., Ihrke, G., Bright, N. A., Lindsay, M., Parkinson, E. J., Brooks, D. A., Parton, R. G., James, D. E., Luzio, J. P. et al. (2000). Syntaxin 7 is localized to late endosome compartments, associates with Vamp 8, and is required for late endosome-lysosome fusion. Mol. Biol. Cell 11, 3137-3153.
78. Murthy, V. N. and De Camilli, P. (2003). Cell biology of the presynaptic terminal. Annu. Rev. Neurosci. 26, 701-728.
79. Nakatsu, F., Okada, M., Mori, F., Kumazawa, N., Iwasa, H., Zhu, G., Kasagi, Y., Kamiya, H., Harada, A., Nishimura, K. et al. (2004). Defective function of GABA-containing synaptic vesicles in mice lacking the AP-3B clathrin adaptor. J. Cell Biol. 167, 293-302.
80. Newman, L. S., McKeever, M. O., Okano, H. J. and Darnell, R. B. (1995). Beta-NAP, a cerebellar degeneration antigen, is a neuron-specific vesicle coat protein. Cell 82, 773-783.
81. Nie, Z. and Randazzo, P. A. (2006). Arf GAPS and membrane traffic. J. Cell Sci. 119, 1203-1211.
82. Nie, Z., Stanley, K. T., Stauffer, S., Jacques, K. M., Hirsch, D. S., Takei, J. and Randazzo, P. A. (2002). AGAP1, an endosome-associated, phosphoinositide-dependent ADP-ribosylation factor GTPase-activating protein that affects actin cytoskeleton. J. Biol. Chem. 277, 48965-48975.
83. Nie, Z., Boehm, M., Boja, E. S., Vass, W. C., Bonifacino, J. S., Fales, H. M. and Randazzo, P. A. (2003). Specific regulation of the adaptor protein complex AP-3 by the Arf GAP AGAP1. Dev. Cell 5, 513-521.
84. Nie, Z., Fei, J., Premont, R. T. and Randazzo, P. A. (2005). The Arf GAPs AGAP1 and AGAP2 distinguish between the adaptor protein complexes AP-1 and AP-3. J. Cell Sci. 118, 3555-3566.
85. Nishimura, N., Plutner H., Hahn, K. and Balch, W. E. (2002). The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface. Proc. Natl. Acad. Sci. USA 99, 6755-6760.
86. Noebels, J. L. and Sidman, R. L. (1989). Persistent hypersynchronization of neocortical neurons in the mocha mutant of mouse. J. Neurogenet. 6, 53-56.
87. Norton, N., Williams, H. J. and Owen, M. J. (2006). An update on the genetics of schizophrenia. Curr. Opin. Psychiatry 19, 158-164.
88. Numakawa, T., Yagasaki, Y., Ishimoto, T., Okada, T., Suzuki, T., Iwata, N., Ozaki, N., Taguchi, T., Tatsumi, M., Kamijima, K. et al. (2004). Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia. Hum. Mol. Genet. 13, 2699-2708.
89. Odorizzi, G., Cowles, C. R. and Emr, S. D. (1998). The AP-3 complex: a coat of many colours. Trends Cell Biol. 8, 282-288.
90. Ohno, H. (2006). Clathrin-associated adaptor protein complexes. J. Cell Sci. 119, 3719-3721.
91. Ohno, H., Stewart, J., Fournier, M. C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser A., Kirchhausen, T. and Bonifacino, J. S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
92. 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.
93. Ohno, H., Tomemori, T., Nakatsu, F., Okazaki, Y., Aguilar, R. C., Foelsch, H., Mellman, I., Saito, T., Shirasawa, T. and Bonifacino, J. S. (1999). MulB, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449, 215-220.
94. 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.
95. Owen, M. J., Craddock, N. and O'Donovan, M. C. (2005). Schizophrenia: genes at last? Trends Genet. 21, 518-525.
96. Pagano, A., Crottet, P., Prescianotto-Baschong, C. and Spiess, M. (2004). In vitro formation of recycling vesicles from endosomes requires adaptor protein-1/clathrin and is regulated by rab4 and the connector rabaptin-5. Mol. Biol. Cell 15, 4990-5000.
97. Palmiter, R. D., Cole, T. B., Quaife, C. J. and Findley, S. D. (1996). ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc. Natl. Acad. Sci. USA 93, 14934-14939.
98. Peden, A. A., Rudge, R. E., Lui, W. W. and Robinson, M. S. (2002). Assembly and function of AP-3 complexes in cells expressing mutant subunits. J. Cell Biol. 156, 327-336.
99. Peden, A. A., Oorschot, V., Hesser, B. A., Austin, C. D., Scheller, R. H. and Klumperman, J. (2004). Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 164, 1065-1076.
100. Pevsner, J., Volknandt, W., Wong, B. R. and Scheller, R. H. (1994). Two rat homologs of clathrin-associated adaptor proteins. Gene 146, 279-283.
101. Pryor, P. R., Mullock, B. M., Bright, N. A., Lindsay, M. R., Gray, S. R., Richardson, S. C., Stewart, A., James, D. E., Piper, R. C. and Luzio, J. P. (2004). Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 5, 590-595.
102. Robinson, M. S. (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167-174.
103. Rolfsen, R. M. and Erway, L. C. (1984). Trace metals and otolith defects in mocha mice. J. Hered. 75, 159-162.
104. Ruder, C., Reimer, T., Delgado-Martinez, I., Hermosilla, R., Engelsberg, A., Nehring, R., Dorken, B. and Rehm, A. (2005). EBAG9 adds a new layer of control on large dense-core vesicle exocytosis via interaction with Snapin. Mol. Biol. Cell 16, 1245-1257.
105. 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.
106. 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 targeted to a distinct synaptic vesicle subpopulation. Mol. Biol. Cell 15, 575-587.
107. Salazar, G., Craige, B., Love, R., Kalman, D. and Faundez, V. (2005a). Vglut1 and ZnT3 co-targeting mechanisms regulate vesicular zinc stores in PC12 cells. J. Cell Sci. 118, 1911-1921.
108. Salazar, G., Craige, B., Wainer, B. H., Guo, J., De Camilli, P. and Faundez, V. (2005b). Phosphatidylinositol-4-kinase type II {alpha} is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 16, 3692-3704.
109. Salazar, G., Craige, B., Styers, M. L., Newell-Litwa, K. A., Doucette, M. M., Wainer, B. H., Falcon-Perez, J. M., Dell'angelica, E. C., Peden, A. A., Werner, E. et al. (2006). BLOC-1 complex deficiency alters the targeting of adaptor protein complex-3 cargoes. Mol. Biol. Cell 17, 4014-4026.
110. Salem, N., Faundez, V., Horng, J. T. and Kelly, R. B. (1998). A v-SNARE participates in synaptic vesicle formation mediated by the AP3 adaptor complex. Nat. Neurosci. 1, 551-556.
111. 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.
112. 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.
113. Setty, S. R., Tenza, D., Truschel, S. T., Chou, E., Sviderskaya, E. V., Theos, A. C., Lamoreux, M. L., Di Pietro, S. M., Starcevic, M., Bennett, D. C., et al. (2007). BLOC-1 Is Required for Cargo-specific Sorting from Vacuolar Early Endosomes toward Lysosome-related Organelles. Mol. Biol. Cell. PMID: 17182842
114. Shi, G., Faundez, V., Roos, J., Dell'Angelica, E. C. and Kelly, R. B. (1998). Neuroendocrine synaptic vesicles are formed in vitro by both clathrin-dependent and clathrin-independent pathways. J. Cell Biol. 143, 947-955.
115. Simpson, F., Bright, N. A., West, M. A., Newman, L. S., Darnell, R. B. and Robinson, M. S. (1996). A novel adaptor-related protein complex. J. Cell Biol. 133, 749-760.
116. Sorkin, A. (2004). Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr. Opin. Cell Biol. 16, 392-399.
117. Stoltenberg, M., Nejsum, L. N., Larsen, A. and Danscher G. (2004). Abundance of zinc ions in synaptic terminals of mocha mutant mice: zinc transporter 3 immunohistochemistry and zinc sulphide autometallography. J. Mol. Histol. 35, 141-145.
118. Straub, R. E., Mayhew, M., Vakkalanka, R., Kolachana, B., Goldberg, T., Egan, M. and Weinberger, D. R. (2005). MUTED (6p24.3), a protein that binds to dysbindin (DTNBP1, 6p22.3), is strongly associated with schizophrenia and exhibits statistical epistasis with COMT. Neuropsychopharmacology 30, S1-S270.
119. Styers, M. L., Salazar, G., Love, R., Peden, A. A., Kowalczyk, A. P. and Faundez, V. (2004). The endo-lysosomal sorting machinery interacts with the intermediate filament cytoskeleton. Mol. Biol. Cell 15, 5369-5382.
120. Styers, M. L., Kowalczyk, A. P. and Faundez, V. (2006). Architecture of the vimentin cytoskeleton is modified by perturbation of the GTPase ARF1. J. Cell Sci. 119, 3643-3654.
121. Sugimoto, H., Sugahara, M., Folsch, H., Koide, Y., Nakatsu, F., Tanaka, N., Nishimura, T., Furukawa, M., Mullins, C., Nakamura, N. et al. (2002). Differential recognition of tyrosine-based basolateral signals by AP-1B subunit mu1B in polarized epithelial cells. Mol. Biol. Cell 13, 2374-2382.
122. Sugita, M., Cao, X., Watts, G. F., Rogers, R. A., Bonifacino, J. S. and Brenner, M. B. (2002). Failure of trafficking and antigen presentation by CD1 in AP-3-deficient cells. Immunity 16, 697-706.
123. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Gronborg, M., Riedel, D., Urlaub, H., Schenck, S., Brugger, B., Ringler, P. et al. (2006). Molecular anatomy of a trafficking organelle. Cell 127, 831-846.
124. Talbot, K., Eidem, W. L., Tinsley, C. L., Benson, M. A., Thompson, E. W., Smith, R. J., Hahn, C. G., Siegel, S. J., Trojanowski, J. Q., Gur, R. E. et al. (2004). Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J. Clin. Invest. 113, 1353-1363.
125. Talbot, K., Cho, D. S., Ong, W. Y., Benson, M. A., Han, L. Y., Kazi, H. A., Kamins, J., Hahn, C. G., Blake, D. J. and Arnold, S. E. (2006). Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. Hum. Mol. Genet. 15, 3041-3054.
126. ter Haar, E., Harrison, S. C. and Kirchhausen, T. (2000). Peptide-in-groove interactions link target proteins to the beta- propeller of clathrin. Proc. Natl. Acad. Sci. USA 97, 1096-1100.
127. Theos, A. C., Tenza, D., Martina, J. A., Hurbain, I., Peden, A. A., Sviderskaya, E. V., Stewart, A., Robinson, M. S., Bennett, D. C., Cutler, D. F. et al. (2005). Functions of adaptor protein (AP)-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes. Mol. Biol. Cell 16, 5356-5372.
128. Tian, J. H., Wu, Z. X., Unzicker, M., Lu, L., Cai, Q., Li, C., Schirra, C., Matti, U., Stevens, D., Deng, C. et al. (2005). The role of Snapin in neurosecretion: snapin knock-out mice exhibit impaired calcium-dependent exocytosis of large dense-core vesicles in chromaffin cells. J. Neurosci. 25, 10546-10555.
129. Traub, L. M. (2005). Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta 1744, 415-437.
130. VanRenterghem, B., Morin, M., Czech, M. P. and Heller-Harrison, R. A. (1998). Interaction of insulin receptor substrate-1 with the sigma3A subunit of the adaptor protein complex-3 in cultured adipocytes. J. Biol. Chem. 273, 29942-29949.
131. 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.
132. Vogt, K., Mellor, J., Tong, G. and Nicoll, R. (2000). The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26, 187-196.
133. Ward, D. M., Pevsner, J., Scullion, M. A., Vaughn, M. and Kaplan, J. (2000). Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol. Biol. Cell 11, 2327-2333.
134. Wei, M. L. (2006). Hermansky-Pudlak syndrome: a disease of protein trafficking and organelle function. Pigment Cell Res. 19, 19-42.
135. Yang, W., Li, C., Ward, D. M., Kaplan, J. and Mansour, S. L. (2000). Defective organellar membrane protein trafficking in Ap3b1-deficient cells. J. Cell Sci. 113, 4077-4086.
136. Zakharenko, S., Chang, S., O'Donoghue, M. and Popov, S. V. (1999). Neurotransmitter secretion along growing nerve processes: comparison with synaptic vesicle exocytosis. J. Cell Biol. 144, 507-518.
137. Zeghouf, M., Guibert, B., Zeeh, J. C. and Cherfils, J. (2005). Arf, Sec7 and Brefeldin A: a model towards the therapeutic inhibition of guanine nucleotide-exchange factors. Biochem. Soc. Trans. 33, 1265-1268.
138. Zhen, L., Jiang, S., Feng, L., Bright, N. A., Peden, A. A., Seymour, A. B., Novak, E. K., Elliott, R., Gorin, M. B., Robinson, M. S. et al. (1999). Abnormal expression and subcellular distribution of subunit proteins of the AP-3 adaptor complex lead to platelet storage pool deficiency in the pearl mouse. Blood 94, 146-155.