The adaptor complex AP-4 regulates vacuolar protein sorting at the trans-golgi network by interacting with VACUOLAR SORTING RECEPTOR11

Plant Physiology

Volumn 170, Issue 1, 2016, Pages 211-219

  Fuji, Kentaro ^a,c   Shirakawa, Makoto ^a,d   Shimono, Yuki ^a   Kunieda, Tadashi ^a,d   Fukao, Yoichiro ^b,e   Koumoto, Yasuko ^a   Takahashi, Hideyuki ^a,b   Hara Nishimura, Ikuko ^a   Shimada, Tomoo ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^c RIKEN   (Japan)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ARABIDOPSIS PROTEIN; ELP PROTEIN, ARABIDOPSIS; GREEN FLUORESCENT PROTEIN;

ARABIDOPSIS; CELL VACUOLE; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PLANT SEED; PROTEIN MOTIF; PROTEIN TRANSPORT; TRANS GOLGI NETWORK; TRANSGENIC PLANT;

ADAPTOR PROTEIN COMPLEX 4; AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GREEN FLUORESCENT PROTEINS; MUTATION; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; SEEDS; TRANS-GOLGI NETWORK; VACUOLES;

EID: 84953211124     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00869     Document Type: Article

References (47)

1. Bassham DC, Brandizzi F, Otegui MS, Sanderfoot AA (2008) The secretory system of Arabidopsis. The Arabidopsis Book 6: e0116, doi/ 10.1199/tab.0116
2. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15: 441-447
3. Burgos PV, Mardones GA, Rojas AL, daSilva LL, Prabhu Y, Hurley JH, Bonifacino JS (2010) Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev Cell 18: 425-436
4. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
5. Dell'Angelica EC (2009) AP-3-dependent trafficking and disease: the first decade. Curr Opin Cell Biol 21: 552-559
6. Dell'Angelica EC, Mullins C, Bonifacino JS (1999) AP-4, a novel protein complex related to clathrin adaptors. J Biol Chem 274: 7278-7285
7. De Marcos Lousa C, Gershlick DC, Denecke J (2012) Mechanisms and concepts paving the way towards a complete transport cycle of plant vacuolar sorting receptors. Plant Cell 24: 1714-1732
8. Fuji K, Shimada T, Takahashi H, Tamura K, Koumoto Y, Utsumi S, Nishizawa K, Maruyama N, Hara-Nishimura I (2007) Arabidopsis vacuolar sorting mutants (green fluorescent seed) can be identified efficiently by secretion of vacuole-targeted green fluorescent protein in their seeds. Plant Cell 19: 597-609
9. Geldner N, Dénervaud-Tendon V, Hyman DL, Mayer U, Stierhof YD, Chory J (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59: 169-178
10. Gershlick DC, Lousa CdeM, Foresti O, Lee AJ, Pereira EA, daSilva LL, Bottanelli F, Denecke J (2014) Golgi-dependent transport of vacuolar sorting receptors is regulated by COPII, AP1, and AP4 protein complexes in tobacco. Plant Cell 26: 1308-1329
11. Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MN, Dacks JB, Robinson MS (2011) The fifth adaptor protein complex. PLoS Biol 9: e1001170
12. Hirst J, Borner GH, Antrobus R, Peden AA, Hodson NA, Sahlender DA, Robinson MS (2012) Distinct and overlapping roles for AP-1 and GGAs revealed by the "knocksideways" system. Curr Biol 22: 1711-1716
13. Hirst J, Bright NA, Rous B, Robinson MS (1999) Characterization of a fourth adaptor-related protein complex. Mol Biol Cell 10: 2787-2802
14. Hirst J, Irving C, Borner GH (2013) Adaptor protein complexes AP-4 and AP-5: new players in endosomal trafficking and progressive spastic paraplegia. Traffic 14: 153-164
15. Isono E, Katsiarimpa A, Müller IK, Anzenberger F, Stierhof YD, Geldner N, Chory J, Schwechheimer C (2010) The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell 22: 1826-1837
16. Jaillais Y, Fobis-Loisy I, Miège C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443: 106-109
17. Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I (2001) A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13: 1511-1526
18. Li L, Shimada T, Takahashi H, Koumoto Y, Shirakawa M, Takagi J, Zhao X, Tu B, Jin H, Shen Z, et al (2013) MAG2 and three MAG2- INTERACTING PROTEINs form an ER-localized complex to facilitate storage protein transport in Arabidopsis thaliana. Plant J 76: 781-791
19. Mano S, Hayashi M, Nishimura M (1999) Light regulates alternative splicing of hydroxypyruvate reductase in pumpkin. Plant J 17: 309-320
20. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533
21. Miao Y, Li KY, Li HY, Yao X, Jiang L (2008) The vacuolar transport of aleurain-GFP and 2S albumin-GFP fusions is mediated by the same prevacuolar compartments in tobacco BY-2 and Arabidopsis suspension cultured cells. Plant J 56: 824-839
22. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007a) Development of series of Gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41
23. Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Tanaka K, Niwa Y, et al (2007b) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71: 2095-2100
24. Nesterov A, Carter RE, Sorkina T, Gill GN, Sorkin A (1999) Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant mu2 subunit and its effects on endocytosis. EMBO J 18: 2489-2499
25. Niemes S, Langhans M, Viotti C, Scheuring D, San Wan Yan M, Jiang L, Hillmer S, Robinson DG, Pimpl P (2010) Retromer recycles vacuolar sorting receptors from the trans-Golgi network. Plant J 61: 107-121
26. Nishizawa K, Maruyama N, Satoh R, Fuchikami Y, Higasa T, Utsumi S (2003) A C-terminal sequence of soybean b-conglycinin a9 subunit acts as a vacuolar sorting determinant in seed cells. Plant J 34: 647-659
27. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269: 1872-1875
28. Owen DJ, Evans PR (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282: 1327-1332
29. Park M, Song K, Reichardt I, Kim H, Mayer U, Stierhof YD, Hwang I, Jürgens G (2013) Arabidopsis m-adaptin subunit AP1M of adaptor protein complex 1 mediates late secretory and vacuolar traffic and is required for growth. Proc Natl Acad Sci USA 110: 10318-10323
30. Pimpl P, Hanton SL, Taylor JP, Pinto-daSilva LL, Denecke J (2003) The GTPase ARF1p controls the sequence-specific vacuolar sorting route to the lytic vacuole. Plant Cell 15: 1242-1256
31. Pourcher M, Santambrogio M, Thazar N, Thierry AM, Fobis-Loisy I, Miège C, Jaillais Y, Gaude T (2010) Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22: 3980-3991
32. Robinson DG, Pimpl P (2014) Clathrin and post-Golgi trafficking: a very complicated issue. Trends Plant Sci 19: 134-139
33. Robinson MS (2004) Adaptable adaptors for coated vesicles. Trends Cell Biol 14: 167-174
34. Rossignol P, Collier S, Bush M, Shaw P, Doonan JH (2007) Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase. J Cell Sci 120: 3678-3687
35. Sanmartín M, Ordóñez A, Sohn EJ, Robert S, Sánchez-Serrano JJ, Surpin MA, Raikhel NV, Rojo E (2007) Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. ProcNatl Acad Sci USA 104: 3645-3650
36. Shimada T, Fuji K, Tamura K, KondoM, Nishimura M, Hara-Nishimura I (2003a) Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 16095-16100
37. Shimada T, Koumoto Y, Hara-Nishimura I (2014) Evaluation of defective endosomal trafficking to the vacuole by monitoring seed storage proteins in Arabidopsis thaliana. Methods Mol Biol 1209: 131-142
38. Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y, Kuroyanagi M, Tabata S, Kato T, Shinozaki K, Seki M, et al (2003b) Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J Biol Chem 278: 32292-32299
39. Shirakawa M, Ueda H, Koumoto Y, Fuji K, Nishiyama C, Kohchi T, Hara- Nishimura I, Shimada T (2014) CONTINUOUS VASCULAR RING (COV1) is a trans-Golgi network-localized membrane protein required for Golgi morphology and vacuolar protein sorting. Plant Cell Physiol 55: 764-772
40. Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22: 4084-4097
41. Tamura K, Shimada T, Kondo M, Nishimura M, Hara-Nishimura I (2005) KATAMARI1/MURUS3 is a novel Golgi membrane protein that is required for endomembrane organization in Arabidopsis. Plant Cell 17: 1764-1776
42. Teh OK, Shimono Y, Shirakawa M, Fukao Y, Tamura K, Shimada T, Hara-Nishimura I (2013) The AP-1 m adaptin is required for KNOLLE localization at the cell plate to mediate cytokinesis in Arabidopsis. Plant Cell Physiol 54: 838-847
43. Uemura T, Kim H, Saito C, Ebine K, Ueda T, Schulze-Lefert P, Nakano A (2012) Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc Natl Acad Sci USA 109: 1784-1789
44. Xiang L, Etxeberria E, Van den Ende W (2013) Vacuolar protein sorting mechanisms in plants. FEBS J 280: 979-993
45. Yamada K, Fuji K, Shimada T, Nishimura M, Hara-Nishimura I (2005) Endosomal proteases facilitate the fusion of endosomes with vacuoles at the final step of the endocytotic pathway. Plant J 41: 888-898
46. Yamazaki M, Shimada T, Takahashi H, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I (2008) Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence. Plant Cell Physiol 49: 142-156
47. Zouhar J, Muñoz A, Rojo E (2010) Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. Plant J 64: 577-588