Localization and Trafficking of an Isoform of the AtPRA1 Family to the Golgi Apparatus Depend on Both N- and C-Terminal Sequence Motifs

Traffic

Volumn 12, Issue 2, 2011, Pages 185-200

  Jung, Chan Jin ^a   Hui Lee, Myoung ^a   Ki Min, Myung ^a   Hwang, Inhwan ^a  

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

Author keywords

AtPRA1 isoform; ER exit signals; Golgi apparatus; Trafficking and localization

Indexed keywords

ATPRA1 PROTEIN; ISOPROTEIN; PROTEIN; RAB PROTEIN; UNCLASSIFIED DRUG; VALINE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LEVEL; ENDOSOME; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; PROTOPLAST; RESIDUE ANALYSIS; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; TRANSGENIC PLANT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PLANTS, GENETICALLY MODIFIED; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN ISOFORMS; PROTEIN PRENYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTOPLASTS; RAB GTP-BINDING PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 78651075537     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01140.x     Document Type: Article

References (63)

1. Chavrier P, Goud B. The role of ARF and Rab GTPases in membrane transport. Curr Opin Cell Biol 1999;11:466-475.
2. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
3. Pasqualato S, Renault L, Cherfils J. Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication. EMBO Rep 2002;3:1035-1041.
4. Collins RN. Rab and ARF GTPase regulation of exocytosis. Mol Membr Biol 2003;20:105-115.
5. Memon AR. The role of ADP-ribosylation factor and SAR1 in vesicular trafficking in plants. Biochim Biophys Acta 2004;1664:9-30.
6. Molendijk AJ, Ruperti B, Palme K. Small GTPases in vesicle trafficking. Curr Opin Plant Biol 2004;7:694-700.
7. Pfeffer S. A model for Rab GTPase localization. Biochem Soc Trans 2005;33:627-630.
8. Novick P, Zerial M. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 1997;9:496-504.
9. Somsel Rodman J, Wandinger-Ness A. Rab GTPases coordinate endocytosis. J Cell Sci 2000;113:183-192.
10. Waters MG, Hughson FM. Membrane tethering and fusion in the secretory and endocytic pathways. Traffic 2000;1:588-597.
11. Pfeffer SR. Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol 2001;11:487-491.
12. Segev N. Ypt and Rab GTPases: insight into functions through novel interactions. Curr Opin Cell Biol 2001;13:500-511.
13. Ueda T, Nakano A. Vesicular traffic: an integral part of plant life. Curr Opin Plant Biol 2002;5:513-517.
14. Prekeris R, Klumperman J, Scheller RH. A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol Cell 2000;6:1437-1448.
15. Rutherford S, Moore I. The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 2002;5:518-528.
16. Bernards A. GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim Biophys Acta 2003;1603:47-82.
17. Vernoud V, Horton AC, Yang Z, Nielsen E. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 2003;131: 1191-1208.
18. Spang A. Vesicle transport: a close collaboration of Rabs and effectors. Curr Biol 2004;14:R33-R34.
19. Pfeffer S, Aivazian D. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 2004;5:886-896.
20. Sevier CS, Weisz OA, Davis M, Machamer CE. Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol Biol Cell 2000;11:13-22.
21. Shisheva A, Sudhof TC, Czech MP. Cloning, characterization, and expression of a novel GDP dissociation inhibitor isoform from skeletal muscle. Mol Cell Biol 1994;14:3459-3468.
22. Wada M, Nakanishi H, Satoh A, Hirano H, Obaishi H, Matsuura Y, Takai Y. Isolation and characterization of a GDP/GTP exchange protein specific for the Rab3 subfamily small G proteins. J Biol Chem 1997;272:3875-3878.
23. Yang X, Matern HT, Gallwitz D. Specific binding to a novel and essential Golgi membrane protein (Yip1p) functionally links the transport GTPases Ypt1p and Ypt31p. EMBO J 1998;17:4954-4963.
24. Calero M, Winand NJ, Collins RN. Identification of the novel proteins Yip4p and Yip5p as Rab GTPase interacting factors. FEBS Lett 2002;515:89-98.
25. Calero M, Collins RN. Saccharomyces cerevisiae Pra1p/Yip3p interacts with Yip1p and Rab proteins. Biochem Biophys Res Commun 2002;290:676-681.
26. Martincic I, Peralta ME, Ngsee JK. Isolation and characterization of a dual prenylated Rab and VAMP2 receptor. J Biol Chem 1997;272:26991-26998.
27. Bucci C, Chiariello M, Lattero D, Maiorano M, Bruni CB. Interaction cloning and characterization of the cDNA encoding the human prenylated rab acceptor (PRA1). Biochem Biophys Res Commun 1999;258:657-662.
28. Liang Z, Li G. Mouse prenylated Rab acceptor is a novel Golgi membrane protein. Biochem Biophys Res Commun 2000;275:509-516.
29. Figueroa C, Taylor J, Vojtek AB. Prenylated Rab acceptor protein is a receptor for prenylated small GTPases. J Biol Chem 2001;276:28219-28225.
30. Geng J, Shin ME, Gilbert PM, Collins RN, Burd CG. Saccharomyces cerevisiae Rab-GDI displacement factor ortholog Yip3p forms distinct complexes with the Ypt1 Rab GTPase and the reticulon Rtn1p. Eukaryot Cell 2005;4:1166-1174.
31. Sivars U, Aivazian D, Pfeffer SR. Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 2003;425:856-859.
32. Abdul-Ghani M, Gougeon PY, Prosser DC, Da-Silva LF, Ngsee JK. PRA isoforms are targeted to distinct membrane compartments. J Biol Chem 2001;276:6225-6233.
33. Seabra MC, Wasmeier C. Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 2004;16:451-457.
34. Heidtman M, Chen CZ, Collins RN, Barlowe C. A role for Yip1p in COPII vesicle biogenesis. J Cell Biol 2003;163:57-69.
35. Calero M, Whittaker GR, Collins RN. Yop1p, the yeast homolog of the polyposis locus protein 1, interacts with Yip1p and negatively regulates cell growth. J Biol Chem 2001;276:12100-12112.
36. Heidtman M, Chen CZ, Collins RN, Barlowe C. Yos1p is a novel subunit of the Yip1p-Yif1p complex and is required for transport between the endoplasmic reticulum and the Golgi complex. Mol Biol Cell 2005;16:1673-1683.
37. Brands A, Ho TH. Function of a plant stress-induced gene, HVA22. Synthetic enhancement screen with its yeast homolog reveals its role in vesicular traffic. Plant Physiol 2002;130:1121-1131.
38. Alvim Kamei CL, Boruc J, Vandepoele K, Van den Daele H, Maes S, Russinova E, Inze D, De Veylder L. The PRA1 gene family in Arabidopsis. Plant Physiol 2008;147:1735-1749.
39. Liang Z, Veeraprame H, Bayan N, Li G. The C-terminus of prenylin is important in forming a dimer conformation necessary for endoplasmic-reticulum-to-Golgi transport. Biochem J 2004;380:43-49.
40. Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I. A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 2001;13:1511-1526.
41. Kim DH, Eu YJ, Yoo CM, Kim YW, Pih KT, Jin JB, Kim SJ, Stenmark H, Hwang I. Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 2001;13:287-301.
42. Pimpl P, Movafeghi A, Coughlan S, Denecke J, Hillmer S, Robinson DG. In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 2000;12:2219-2236.
43. Lee MH, Min MK, Lee YJ, Jin JB, Shin DH, Kim DH, Lee KH, Hwang I. ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol 2002;129: 1507-1520.
44. Sohn EJ, Kim ES, Zhao M, Kim SJ, Kim H, Kim YW, Lee YJ, Hillmer S, Sohn U, Jiang L, Hwang I. Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 2003;15:1057-1070.
45. Lee GJ, Sohn EJ, Lee MH, Hwang I. The Arabidopsis rab5 homologs rha1 and ara7 localize to the prevacuolar compartment. Plant Cell Physiol 2004;45:1211-1220.
46. Ueda T, Yamaguchi M, Uchimiya H, Nakano A. Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 2001;20:4730-4741.
47. Aoyama T, Chua NH. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 1997;11:605-612.
48. Hanton SL, Renna L, Bortolotti LE, Chatre L, Stefano G, Brandizzi F. Diacidic motifs influence the export of transmembrane proteins from the endoplasmic reticulum in plant cells. Plant Cell 2005;17:3081-3093.
49. Okada K, Saito T, Nakagawa T, Kawamukai M, Kamiya Y. Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol 2000;122:1045-1056.
50. Miao Y, Yan PK, Kim H, Hwang I, Jiang L. Localization of green fluorescent protein fusions with the seven Arabidopsis vacuolar sorting receptors to prevacuolar compartments in tobacco BY-2 cells. Plant Physiol 2006;142:945-962.
51. Paulhe F, Imhof BA, Wehrle-Haller B. A specific endoplasmic reticulum export signal drives transport of stem cell factor (Kitl) to the cell surface. J Biol Chem 2004;279:55545-55555.
52. Zaarour N, Demaretz S, Defontaine N, Mordasini D, Laghmani K. A highly conserved motif at the COOH terminus dictates endoplasmic reticulum exit and cell surface expression of NKCC2. J Biol Chem 2009;284:21752-21764.
53. Fiedler K, Veit M, Stamnes MA, Rothman JE. Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science 1996;273:1396-1399.
54. Nishimura N, Balch WE. A di-acidic signal required for selective export from the endoplasmic reticulum. Science 1997;277:556-558.
55. Hanton SL, Chatre L, Renna L, Matheson LA, Brandizzi F. De novo formation of plant endoplasmic reticulum export sites is membrane cargo induced and signal mediated. Plant Physiol 2007;143:1640-1650.
56. Zelazny E, Miecielica U, Borst JW, Hemminga MA, Chaumont F. An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 2009;57:346-355.
57. Gomord V, Denmat LA, Fitchette-Laine AC, Satiat-Jeunemaitre B, Hawes C, Faye L. The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J 1997;11:313-325.
58. Prosser DC, Tran D, Gougeon PY, Verly C, Ngsee JK. FFAT rescues VAPA-mediated inhibition of ER-to-Golgi transport and VAPB-mediated ER aggregation. J Cell Sci 2008;121:3052-3061.
59. Frigerio L, de Virgilio M, Prada A, Faoro F, Vitale A. Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. Plant Cell 1998;10:1031-1042.
60. Park M, Lee D, Lee GJ, Hwang I. AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J Cell Biol 2005;170:757-767.
61. Wee EG, Sherrier DJ, Prime TA, Dupree P. Targeting of active sialyltransferase to the plant Golgi apparatus. Plant Cell 1998;10: 1759-1768.
62. Kircher S, Wellmer F, Nick P, Rugner A, Schafer E, Harter K. Nuclear import of the parsley bZIP transcription factor CPRF2 is regulated by phytochrome photoreceptors. J Cell Biol 1999;144:201-211.
63. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998;16: 735-743.