Arabidopsis μ-adaptin subunit AP1M of adaptor protein complex 1 mediates late secretory and vacuolar traffic and is required for growth

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 25, 2013, Pages 10318-10323

  Park, Misoon ^a   Song, Kyungyoung ^a   Reichardt, Ilka ^a,c   Kim, Hyeran ^a,d   Mayer, Ulrike ^a,b   Stierhof, York Dieter ^b   Hwang, Inhwan ^a   Jürgens, Gerd ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Adaptor complex 1; Development; Membrane traffic; Secretory pathway

Indexed keywords

ADAPTOR PROTEIN; ALPHA ADAPTIN; ARABIDOPSIS PROTEIN; GAMMA ADAPTIN; MU ADAPTIN;

ARABIDOPSIS; ARTICLE; CELL DIVISION; CELL MIGRATION; CELL VACUOLE; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CYTOKINESIS; GENE INSERTION; INTERPHASE; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; POLLEN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANS GOLGI NETWORK;

ADAPTOR COMPLEX 1; DEVELOPMENT; MEMBRANE TRAFFIC; SECRETORY PATHWAY;

ADAPTOR PROTEIN COMPLEX 1; ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ADAPTOR PROTEIN COMPLEX GAMMA SUBUNITS; ADAPTOR PROTEIN COMPLEX MU SUBUNITS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; CYTOKINESIS; GOLGI APPARATUS; INTERPHASE; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS, INSERTIONAL; PROTEIN TRANSPORT; SECRETORY VESICLES; TRANS-GOLGI NETWORK; VACUOLES;

ARABIDOPSIS; MAMMALIA;

EID: 84879308012     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300460110     Document Type: Article

References (44)

1. Boehm M, Bonifacino JS (2001) Adaptins: The final recount. Mol Biol Cell 12(10):2907-2920.
2. Glyvuk N, et al. (2010) AP-1/sigma1B-adaptin mediates endosomal synaptic vesicle recycling, learning and memory. EMBO J 29(8):1318-1330.
3. Stepp JD, Pellicena-Palle A, Hamilton S, Kirchhausen T, Lemmon SK (1995) A late Golgi sorting function for Saccharomyces cerevisiae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol Biol Cell 6(1):41-58.
4. Klumperman J, Kuliawat R, Griffith JM, Geuze HJ, Arvan P (1998) Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J Cell Biol 141(2):359-371.
5. Dwyer ND, Adler CE, Crump JG, L'Etoile ND, Bargmann CI (2001) Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31(2):277-287.
6. Fölsch H, Ohno H, Bonifacino JS, Mellman I (1999) A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99(2):189-198.
7. Kita A, et al. (2004) Loss of Apm1, the micro1 subunit of the clathrin-associated adaptor-protein-1 complex, causes distinct phenotypes and synthetic lethality with calcineurin deletion in fission yeast. Mol Biol Cell 15(6):2920-2931.
8. Meyer C, et al. (2000) mu1A-adaptin-deficient mice: Lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J 19(10):2193-2203.
9. Aguilar RC, Ohno H, Roche KW, Bonifacino JS (1997) Functional domain mapping of the clathrin-associated adaptor medium chains mu1 and mu2. J Biol Chem 272(43):27160-27166.
10. Owen DJ, Evans PR (1998) A structural explanation for the recognition of tyrosinebased endocytotic signals. Science 282(5392):1327-1332.
11. Motley A, Bright NA, Seaman MN, Robinson MS (2003) Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162(5):909-918.
12. Huang F, Khvorova A, Marshall W, Sorkin A (2004) Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 279(16):16657-16661.
13. Zizioli D, et al. (1999) Early embryonic death of mice deficient in gamma-adaptin. J Biol Chem 274(9):5385-5390.
14. Cowles CR, Odorizzi G, Payne GS, Emr SD (1997) The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91(1):109-118.
15. Mullins C, Hartnell LM, Bonifacino JS (2000) Distinct requirements for the AP-3 adaptor complex in pigment granule and synaptic vesicle biogenesis in Drosophila melanogaster. Mol Gen Genet 263(6):1003-1014.
16. Simmen T, Höning S, Icking A, Tikkanen R, Hunziker W (2002) AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nat Cell Biol 4(2):154-159.
17. Hirst J, et al. (2011) The fifth adaptor protein complex. PLoS Biol 9(10):e1001170.
18. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18(3):715-730.
19. Park M, Jürgens G (2011) Membrane traffic and fusion at post-Golgi compartments. Front Plant Sci 2:111, 10.3389/fpls.2011.00111.
20. Happel N, et al. (2004) Arabidopsis mu A-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J 37(5):678-693.
21. Feraru E, et al. (2010) The AP-3 β adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22(8):2812-2824.
22. Zwiewka M, et al. (2011) The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Res 21(12):1711-1722.
23. Wolfenstetter S, Wirsching P, Dotzauer D, Schneider S, Sauer N (2012) Routes to the tonoplast: The sorting of tonoplast transporters in Arabidopsis mesophyll protoplasts. Plant Cell 24(1):215-232.
24. Niihama M, Takemoto N, Hashiguchi Y, Tasaka M, Morita MT (2009) ZIP genes encode proteins involved in membrane trafficking of the TGN-PVC/vacuoles. Plant Cell Physiol 50(12):2057-2068.
25. Sanderfoot AA, Kovaleva V, Bassham DC, Raikhel NV (2001) Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biol Cell 12(12):3733-3743.
26. Johnson MA, et al. (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics 168(2):971-982.
27. Nesterov A, Carter RE, Sorkina T, Gill GN, Sorkin A (1999) Inhibition of the receptorbinding function of clathrin adaptor protein AP-2 by dominant-negative mutant mu2 subunit and its effects on endocytosis. EMBO J 18(9):2489-2499.
28. Verdaguer B, de Kochko A, Beachy RN, Fauquet C (1996) Isolation and expression in transgenic tobacco and rice plants, of the cassava vein mosaic virus (CVMV) promoter. Plant Mol Biol 313(6):1129-1139.
29. French AP, Mills S, Swarup R, Bennett MJ, Pridmore TP (2008) Colocalization of fluorescent markers in confocal microscope images of plant cells. Nat Protoc 3(4):619-628.
30. Stierhof YD, El Kasmi F (2010) Strategies to improve the antigenicity, ultrastructure preservation and visibility of trafficking compartments in Arabidopsis tissue. Eur J Cell Biol 89(2-3):285-297.
31. Geldner N, et al. (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112(2):219-230.
32. Lee GJ, Sohn EJ, Lee MH, Hwang I (2004) The Arabidopsis rab5 homologs rha1 and ara7 localize to the prevacuolar compartment. Plant Cell Physiol 45(9):1211-1220.
33. Tse YC, et al. (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16(3):672-693.
34. Song K, et al. (2012) An A/ENTH domain-containing protein functions as an adaptor for clathrin-coated vesicles on the growing cell plate in Arabidopsis root cells. Plant Physiol 159(3):1013-1025.
35. Lee GJ, et al. (2007) EpsinR2 interacts with clathrin, adaptor protein-3, AtVTI12, and phosphatidylinositol-3-phosphate. Implications for EpsinR2 function in protein trafficking in plant cells. Plant Physiol 143(4):1561-1575.
36. Kim H, Park M, Kim SJ, Hwang I (2005) Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell 17(3):888-902.
37. Jung C, et al. (2011) Identification of sorting motifs of AtβFruct4 for trafficking from the ER to the vacuole through the Golgi and PVC. Traffic 12(12):1774-1792.
38. Batoko H, Zheng HQ, Hawes C, Moore I (2000) A rab1 GTPase is required for transport between the endoplasmic reticulum and golgi apparatus and for normal golgi movement in plants. Plant Cell 12(11):2201-2218.
39. Ahmed SU, et al. (2000) The plant vacuolar sorting receptor AtELP is involved in transport of NH (2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J Cell Biol 149(7):1335-1344.
40. Niemes S, et al. (2010) Sorting of plant vacuolar proteins is initiated in the ER. Plant J 62(4):601-614.
41. Robinson DG, Albrecht S, Moriysu Y (2004) The V-ATPase inhibitors concanamycin A and bafilomycin A lead to Golgi swelling in tobacco BY-2 cells. Protoplasma 224(3-4):255-260.
42. Abas L, et al. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxinefflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8(3):249-256.
43. Reichardt I, et al. (2007) Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr Biol 17(23):2047-2053.
44. Albertson R, Riggs B, Sullivan W (2005) Membrane traffic: A driving force in cytokinesis. Trends Cell Biol 15(2):92-101.