The trans-Golgi network accessory protein p56 promotes long-range movement of GGA/clathrin-containing transport carriers and lysosomal enzyme sorting

Molecular Biology of the Cell

Volumn 18, Issue 9, 2007, Pages 3486-3501

  Mardones, Gonzalo A ^a   Burgos, Patricia V ^a   Brooks, Doug A ^b,c   Parkinson Lawrence, Emma ^b,c   Mattera, Rafael ^a   Bonifacino, Juan S ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c Lysosomal Diseases Research Unit   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACID HYDROLASE; CARRIER PROTEIN; CATHEPSIN D; CLATHRIN; LYSOSOME ENZYME; MONOMER; PROTEIN P56; SOMATOMEDIN B RECEPTOR;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; COATED VESICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RAT; RNA INTERFERENCE; TRANS GOLGI NETWORK;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADP-RIBOSYLATION FACTORS; ANIMALS; CATHEPSIN D; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CLATHRIN; COS CELLS; FIBROBLASTS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; LYSOSOMES; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TRANS-GOLGI NETWORK; TRANSPORT VESICLES;

EID: 34548482956     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-02-0190     Document Type: Article

References (71)

1. Ahle, S., and Ungewickell, E. (1990). Auxilin, a newly identified clathrin-associated protein in coated vesicles from bovine brain. J. Cell Biol. 111, 19-29.
2. Boehm, M., and Bonifacino, J. S. (2001). Adaprins: the final recount. Mol. Biol. Cell 12, 2907-2920.
3. Bolte, S., and Cordelières, F. P. (2006). A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232.
4. Boman, A. L., Zhang, C. J., Zhu, X., and Kahn, R. A. (2000). A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol. Biol. Cell 11, 1241-1255.
5. Bonifacino, J. S. (2004). The GGA proteins: adaptors on the move. Nat. Rev. Mol. Cell Biol. 5, 23-32.
6. Bowers, K., and Stevens, T. H. (2005). Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1744, 438-454.
7. Burgos, P. V., Klattenhoff, C., de la Fuente, E., Rigotti, A., and González, A. (2004). Cholesterol depletion induces PKA-mediated basolateral-to-apical transcytosis of the scavenger receptor class B type I in MDCK cells. Proc. Natl. Acad. Sci. USA 101, 3845-3850.
8. Collins, B. M., Praefcke, G. J., Robinson, M. S., and Owen, D. J. (2003). Structural basis for binding of accessory proteins by the appendage domain of GGAs. Nat. Struct. Biol. 10, 607-613.
9. Dell'Angelica, E. C., Puertollano, R., Mullins, C., Aguilar, R. C., Vargas, J. D., Hartnell, L. M., and Bonifacino, J. S. (2000). GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J. Cell Biol. 149, 81-94.
10. Doray, B., Ghosh, P., Griffith, J., Geuze, H. J., and Kornfeld, S. (2002). Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297, 1700-1703.
11. Doray, B., and Kornfeld, S. (2001). Gamma subunit of the AP-1 adaptor complex binds clathrin: implications for cooperative binding in coated vesicle assembly. Mol. Biol. Cell 12, 1925-1935.
12. Duncan, M. C., Costaguta, G., and Payne, G. S. (2003). Yeast epsin-related proteins required for Golgi-endosome traffic define a gamma-adaptin ear-binding motif. Nat. Cell Biol. 5, 77-81.
13. Galperin, E., and Sorkin, A. (2003). Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted Rab5 on clathrin-dependent endocytosis. J. Cell Sci. 116, 4799-4810.
14. Ghosh, P., Dahms, N. M., and Kornfeld, S. (2003a). Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4, 202-212.
15. Ghosh, P., Griffith, J., Geuze, H. J., and Kornfeld, S. (2003b). Mammalian GGAs act together to sort mannose 6-phosphate receptors. J. Cell Biol. 163, 755-766.
16. Ghosh, P., and Kornfeld, S. (2004). The GGA proteins: key players in protein sorting at the trans-Golgi network. Eur. J. Cell Biol. 83, 257-262.
17. Gordon, G. W., Berry, G., Liang, X. H., Levine, B., and Herman, B. (1998). Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74, 2702-2713.
18. He, X., Li, F., Chang, W. P., and Tang, J. (2005). GGA proteins mediate the recycling pathway of memapsin 2 (BACE). J. Biol. Chem. 280, 11696-11703.
19. Hirst, J., Borner, G. H., Harbour, M., and Robinson, M. S. (2005). The aftiphiHn/p200/gamma-synergin complex. Mol. Biol. Cell 16, 2554-2565.
20. Hirst, J., Lui, W. W., Bright, N. A., Totty, N., Seaman, M. N., and Robinson, M. S. (2000). A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J. Cell Biol. 149, 67-80.
21. Hirst, J., Motley, A., Harasaki, K., Peak Chew, S. Y., and Robinson, M. S. (2003). EpsinR: an ENTH domain-containing Protein that Interacts with AP-1. Mol. Biol. Cell 14, 625-641.
22. Honing, S., Sosa, M., Hille-Rehfeld, A., and von Figura, K. (1997). The 46-kDa mannose 6-phosphate receptor contains multiple binding sites for clathrin adaptors. J. Biol. Chem. 272, 19884-19890.
23. Huang, F., Nesterov, A., Carter, R. E., and Sorkin, A. (2001). Trafficking of yellow-fluorescent-protein-tagged mul subunit of clathrin adaptor AP-1 complex in living cells. Traffic 2, 345-357.
24. Iversen, T. G., Skretting, G., van Deurs, B., and Sandvig, K. (2003). Clathrin-coated pits with long, dynamin-wrapped necks upon expression of a clathrin antisense RNA. Proc. Natl. Acad. Sci. USA 100, 5175-5180.
25. Janvier, K., and Bonifacino, J. S. (2005). Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins. Mol. Biol. Cell 16, 4231-4242.
26. Kametaka, S., Moriyama, K., Burgos, P. V., Eisenberg, E., Greene, L. E., Mattera, R., and Bonifacino, J. S. (2007). Canonical interaction of cyclin G-associated kinase with adaptor protein 1 regulates lysosomal enzyme sorting. Mol. Biol. Cell 18, 2991-3001.
27. Kalthoff, C., Groos, S., Kohl, R., Mahrhold, S., and Ungewickell, E. J. (2002). Clint: a novel clathrin-binding ENTH-domain protein at the Golgi. Mol. Biol. Cell 13, 4060-4073.
28. Kent, H. M., McMahon, H. T., Evans, P. R., Benmerah, A., and Owen, D. J. (2002). Gamma-adaptin appendage domain: structure and binding site for Eps15 and gamma-synergin. Structure (Camb.) 10, 1139-1148.
29. Kornfeld, S. (1992). Structure and function of the mannose 6-phosphate/ insulinlike growth factor II receptors. Annu. Rev. Biochem. 61, 307-330.
30. Koster, A., Saftig, P., Matzner, U., von Figura, K., Peters, C., and Pohlmann, R. (1993). Targeted disruption of the M(r) 46,000 mannose 6-phosphate receptor gene in mice results in misrouting of lysosomal proteins. EMBO J. 12, 5219-5223.
31. Kimura, S. H., Tsuruga, H., Yabuta, N., Endo, Y., and Nojima, H. (1997). Structure, expression, and chromosomal localization of human GAK. Genomics 44, 179-187.
32. Klumperman, J., Hille, A., Veenendaal, T., Oorschot, V., Stoorvogel, W., von Figura, K., and Geuze, H. J. (1993). Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J. Cell Biol. 121, 997-1010.
33. Le Borgne, R., and Hoflack, B. (1997). Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN. J. Cell Biol. 137, 335-345.
34. Ludwig, T., Ovitt, C. E., Bauer, U., Hollinshead, M., Remmler, J., Lobel, P., Ruther, U., and Hoflack, B. (1993). Targeted disruption of the mouse cation-dependent mannose 6-phosphate receptor results in partial missorting of multiple lysosomal enzymes. EMBO J. 12, 5225-5235.
35. Ludwig, T., Eggenschwiler, J., Fisher, P., D'Ercole, A. J., Davenport, M. L., and Efstratiadis, A. (1996). Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev. Biol. 177, 517-535.
36. Lui, W. W., Collins, B. M., Hirst, J., Motley, A., Millar, C., Schu, P., Owen, D. J., and Robinson, M. S. (2003). Binding partners for the COOH-terminal appendage domains of the GGAs and γ-adaprin. Mol. Biol. Cell 14, 2385-2398.
37. Manders, E., Stap, J., Brakenhoff, G., van Driel, R., and Aten, J. (1992). Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 103, 857-862.
38. Mardones, G. A., Snyder, C. M., and Howell, K. E. (2006). cis-Golgi matrix proteins move directly to endoplasmic reticulum exit sites by association with tubules. Mol. Biol. Cell 17, 525-538.
39. Martina, J. A., Moriyama, K., and Bonifacino, J. S. (2003). BLOC-3, a protein complex containing the Hermansky-Pudlak syndrome gene products HPS1 and HPS4. J. Biol. Chem. 278, 29376-29384.
40. Mattera, R., Arighi, C. N., Lodge, R., Zerial, M., and Bonifacino, J. S. (2003). Divalent interaction of the GGAs with the Rabaptin-5-Rabex-5 complex. EMBO J. 22, 78-88.
41. Mattera, R., Ritter, B., Sidhu, S. S., McPherson, P. S., and Bonifacino, J. S. (2004). Definition of the consensus motif recognized by gamma-adaptin ear domains. J. Biol. Chem. 279, 8018-8028.
42. Meyer, C., Zizioli, D., Lausmann, S., Eskelinen, E. L., Hamann, J., Saftig, P., von Figura, K., and Schu, P. (2000). mu1A-adaprin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19, 2193-2203.
43. Miller, G. J., Mattera, R., Bonifacino, J. S., and Hurley, J. H. (2003). Recognition of accessory protein motifs by the gamma-adaptin ear domain of GGA3. Nat. Struct. Biol. 10, 599-606.
44. Mills, I. G., Praefcke, G. J., Vallis, Y., Peter, B. J., Olesen, L. E., Gallop, J. L., Butler, P. J., Evans, P. R., and McMahon, H. T. (2003). EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J. Cell Biol. 160, 213-222.
45. Mullins, C., and Bonifacino, J. S. (2001). The molecular machinery for lysosome biogenesis, Bioessays 23, 333-343.
46. Nakagawa, T., Setou, M., Seog, D., Ogasawara, K., Dohmae, N., Takio, K., and Hirokawa, N. (2000). A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex. Cell 103, 569-581.
47. Neubrand, V. E., Will, R. D., Mobius, W., Poustka, A., Wiemann, S., Schu, P., Dotti, C. G., Pepperkok, R., and Simpson, J. C. (2005). Gamma-BAR, a novel AP-1-interacting protein involved in post-Golgi trafficking. EMBO J. 24, 1122-1133.
48. Nogi, T. et al. (2002). Structural basis for the accessory protein recruitment by the gamma-adaptin ear domain. Nat. Struct. Biol. 9, 527-531.
49. Owen, D. J., Collins, B. M., and Evans, P. R. (2004). Adaptors for clathrin coats: structure and function. Annu. Rev. Cell Dev. Biol. 20, 153-191.
50. Page, L. J., Sowerby, P. J., Lui, W. W., and Robinson, M. S. (1999). Gamma-synergin: an EH domain-containing protein that interacts with gamma-adaptin. J. Cell Biol. 146, 993-1004.
51. Polishchuk, R. S., San Pietro, E., Di Pentima, A., Tete, S., and Bonifacino, J. S. (2006). Ultrastructure of long-range transport carriers moving from the trans Golgi network to peripheral endosomes. Traffic 7, 1092-1103.
52. Poussu, A., Lohi, O., and Lehto, V. P. (2000). Vear, a novel Golgi-associated protein with VHS and gamma-adaptin "ear" domains. J. Biol. Chem. 275, 7176-7183.
53. Puertollano, R., Aguilar, R. C., Gorshkova, I., Crouch, R. J., and Bonifacino, J. S. (2001). Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292, 1712-1716.
54. Puertollano, R., and Bonifacino, J. S. (2004). Interactions of GGA3 with the ubiquitin sorting machinery. Nat. Cell Biol. 6, 244-251.
55. Puertollano, R., van der Wei, N. N., Greene, L. E., Eisenberg, E., Peters, P. J., and Bonifacino, J. S. (2003). Morphology and dynamics of clathrin/GGA1-coated carriers budding from the trans-Golgi network. Mol. Biol. Cell 14, 1545-1557.
56. Rasband, W. S. (1997-2007). ImageJ. Bethesda, MD: US National Institutes of Health. USA http://rsb.info.nih.gov/ij/.
57. Ritter, B., Philie, J., Girard, M., Tung, E. C., Blondeau, F., and McPherson, P. S. (2003). Identification of a family of endocytic proteins that define a new alpha-adaptin ear-binding motif. EMBO Rep. 4, 1089-1095.
58. Rizzo, M. A., Springer, G. H., Granada, B., and Piston, D. W. (2004). An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449.
59. Robinson, M. S. (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167-174.
60. Shiba, Y., Takatsu, H., Shin, H. W., and Nakayama, K. (2002). Gamma-adaptin interacts directly with Rabaptin-5 through its ear domain. J. Biochem. (Tokyo) 131, 327-336.
61. Takatsu, H., Katoh, Y., Shiba, Y., and Nakayama, K. (2001). Golgi-localizing, gamma-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J. Biol. Chem. 276, 28541-28545.
62. Takatsu, H., Yoshino, K., and Nakayama, K. (2000). Adaptor gamma ear homology domain conserved in gamma-adaptin and GGA proteins that interact with gamma-synergin. Biochem. Biophys. Res. Commun. 271, 719-725.
63. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
64. Traub, L. M. (2005). Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta 1744, 415-437.
65. Waguri, S., Dewitte, F., Le Borgne, R., Rouillé, Y., Uchiyama, Y., Dubremetz, J. F., and Hoflack, B. (2002). Visualization of TGN to endosomes trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell 14, 142-155.
66. Wahle, T., Prager, K., Raffler, N., Haass, C., Famulok, M., and Walter, J. (2005). GGA proteins regulate retrograde transport of BACE1 from endosomes to the trans-Golgi network. Mol. Cell. Neurosci. 29, 453-461.
67. Wasiak, S., Legendre-Guillemin, V., Puertollano, R., Blondeau, F., Girard, M., de Heuvel, E., Boismenu, D., Bell, A. W., Bonifacino, J. S., and McPherson, P. S. (2002). Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics. J. Cell Biol. 158, 855-862.
68. Wettey, F. R., Hawkins, S. F., Stewart, A., Luzio, J. P., Howard, J. C., and Jackson, A. P. (2002). Controlled elimination of clathrin heavy-chain expression in DT40 lymphocytes. Science 297, 1521-1525.
69. Wu, X., Zhao, X., Puertollano, R., Bonifacino, J. S., Eisenberg, E., and Greene, L. E. (2003). Adaptor and clathrin exchange at the plasma membrane and trans-Golgi network. Mol. Biol. Cell 14, 516-528.
70. Zhu, Y., Doray, B., Poussu, A., Lehto, V. P., and Kornfeld, S. (2001). Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6- phosphate receptor. Science 292, 1716-1718.
71. Zola, H., and Brooks, D. A. (1981). Techniques for production and characterization of monoclonal hybridoma antibodies. In: Monoclonal Hybridoma Antibodies: Techniques and Applications, ed. J.G.R. Hurrell, Boca Raton, FL: CRC Press, 1-57.