Molecular Analysis and Localization of CaARA7 a Conventional RAB5 GTPase from Characean Algae

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Volumn 16, Issue 5, 2015, Pages 534-554

  Hoepflinger, Marion C ^a   Geretschlaeger, Anja ^a   Sommer, Aniela ^a   Hoeftberger, Margit ^a   Hametner, Christina ^a   Ueda, Takashi ^b   Foissner, Ilse ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

ARA7; Chara australis; Endosomal trafficking; Multivesicular endosome; RAB5 GTPase; RABF2

Indexed keywords

AMINO ACID; EPITOPE; GUANOSINE TRIPHOSPHATASE; POLYPEPTIDE; PROTEIN ATARA7; PROTEIN CAARA6; PROTEIN CAARA7; UNCLASSIFIED DRUG; WORTMANNIN; ALGAL PROTEIN; ARA7 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; RAB PROTEIN;

ANTIBODY LABELING; ARA7 GENE; ARTICLE; BINDING SITE; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CHARA AUSTRALIS; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; ENZYME LOCALIZATION; EPIDERMIS CELL; GENE; GREEN ALGA; MEMBRANE TRANSPORT; MOLECULAR WEIGHT; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT LEAF; PRIORITY JOURNAL; AMINO ACID SEQUENCE; ARABIDOPSIS; CHAROPHYTA; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; POINT MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

ALGAL PROTEINS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHARACEAE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT LEAVES; POINT MUTATION; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84929995596     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12267     Document Type: Article

References (72)

1. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A. Rab GTPases at a glance. J Cell Sci 2007;120:3905-3910.
2. Fujimoto M, Ueda T. Conserved and plant-unique mechanisms regulating plant post-Golgi traffic. Front Plant Sci 2012;3:197.
3. Saito C, Ueda T. Chapter 4 Functions of RAB and SNARE proteins in plant life. In: Kwang WJ, editor. International Review of Cell and Molecular Biology. Burlington: Academic Press; 2009, pp. 183-233.
4. Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A. VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. Plant Cell 2007;19:3504-3515.
5. 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.
6. Ueda T, Uemura T, Sato MH, Nakano A. Functional differentiation of endosomes in Arabidopsis cells. Plant J 2004;40:783-789.
7. Bolte S, Schiene K, Dietz K-J. Characterization of a small GTP-binding protein of the rab 5 family in Mesembryanthemum crystallinum with increased level of expression during early salt stress. Plant Mol Biol 2000;42:923-935.
8. Ebine K, Fujimoto M, Okatani Y, Nishiyama T, Goh T, Ito E, Dainobu T, Nishitani A, Uemura T, Sato MH, Thordal-Christensen H, Tsutsumi N, Nakano A, Ueda T. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 2011;13:853-859.
9. Ebine K, Miyakawa N, Fujimoto M, Uemura T, Nakano A, Ueda T. Endosomal trafficking pathway regulated by ARA6, a RAB5 GTPase unique to plants. Small GTPases 2012;3:23-27.
10. Bottanelli F, Foresti O, Hanton S, Denecke J. Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell 2011;23:3007-3025.
11. Ebine K, Ueda T. Unique mechanism of plant endocytic/vacuolar transport pathways. J Plant Res 2009;122:21-30.
12. Hoepflinger MC, Geretschlaeger A, Sommer A, Hoeftberger M, Nishiyama T, Sakayama H, Hammerl P, Tenhaken R, Ueda T, Foissner I. Molecular and biochemical analysis of the first ARA6 homologue, a RAB5 GTPase, from green algae. J Exp Bot 2013;64:5553-5568.
13. Hoepflinger M, Hametner C, Ueda T, Foissner I. Vesicular trafficking in characean green algae and the possible involvement of a VAMP72-family protein. Plant Signal Behav 2014;9:e28466.
14. Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TWJ. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 2006;10:137-150.
15. Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 2012;24:4205-4219.
16. Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS. The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 2007;19:1295-1312.
17. Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, Hawes C. AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Sci 2004;117:6377-6389.
18. Wodniok S, Brinkmann H, Glockner G, Heidel A, Philippe H, Melkonian M, Becker B. Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 2011;11:104.
19. Braun M, Foissner I, Lühring H, Schubert H, Thiel G. Characean algae: still a valid model system to examine fundamental principles in plants. Prog Bot 2007;68:193-220.
20. Tazawa M, Shimmen T. How characean cells have contributed to the progress of plant membrane biophysics. Aust J Plant Physiol 2001;28:523-539.
21. Foissner I, Wasteneys GO. Characean internodal cells as a model system for the study of cell organization. In: Kwang WJ, editor. International Review of Cell and Molecular Biology. Burlington: Academic Press; 2014, pp. 307-364.
22. Foissner I, Wasteneys GO. The characean internodal cell as a model system for studying wound healing. J Microsc 2012;247:10-22.
23. Li G, Barbieri A, Colombo MI, Stahl PD. Structural features of the GTP-binding defective Rab5 mutants required for their inhibitory activity on endocytosis. J Biol Chem 1994;269:14631-14635.
24. Hoffenberg S, Sanford JC, Liu S, Daniel DS, Tuvin M, Knoll BJ, Wessling-Resnick M, Dickey BF. Biochemical and functional characterization of a recombinant GTPase, Rab5, and two of its mutants. J Biol Chem 1995;270:5048-5056.
25. Anand B, Majumdar S, Prakash B. Structural basis unifying diverse GTP hydrolysis mechanisms. Biochemistry 2013;52:1122-1130.
26. Olkkonen VM, Stenmark H. Role of rab GTPases in membrane traffic. In: Jeon KW, editor. International Review of Cytology - A Survey of Cell Biology. Burlington: Academic Press Inc; 1997, pp. 1-85.
27. Kleuss C, Raw AS, Lee E, Sprang SR, Gilman AG. Mechanism of GTP hydrolysis by G-protein alpha subunits. Proc Natl Acad Sci USA 1994;91:9828-9831.
28. Li G, Stahl PD. Structure-function relationship of the small GTPase rab5. J Biol Chem 1993;268:24475-24480.
29. Scheuring D, Viotti C, Kräger F, Känzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K. Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 2011;23:3463-3481.
30. Klima A, Foissner I. FM dyes label sterol-rich plasma membrane domains and are internalized independently of the cytoskeleton in characean internodal cells. Plant Cell Physiol 2008;49:1508-1521.
31. Schmoelzer PM, Hoeftberger M, Foissner I. Plasma membrane domains participate in pH banding of Chara internodal cells. Plant Cell Physiol 2011;52:1274-1288.
32. Wang JQ, Cai Y, Miao YS, Lam SK, Jiang LW. Wortmannin induces homotypic fusion of plant prevacuolar compartments. J Exp Bot 2009;60:3075-3083.
33. Lam SK, Tse YC, Miao YS, Li H, Wang J, Lo SW, Jiang CJ. Molecular characterization of plant prevacuolar and endosomal compartments. J Integr Plant Biol 2007;49:1119-1128.
34. Norris SR, Meyer SE, Callis J. The intron of Arabidopsis thaliana polyubiquitin genes is conserved in location and is a quantitative determinant of chimeric gene expression. Plant Mol Biol 1993;21:895-906.
35. Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc Natl Acad Sci USA 2012;109:15942-15946.
36. Martiniere A, Bassil E, Jublanc E, Alcon C, Reguera M, Sentenac H, Blumwald E, Paris N. In vivo intracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. Plant Cell 2013;25:4028-4043.
37. Nelson BK, Cai X, Nebenfuhr A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 2007;51:1126-1136.
38. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH. Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi network in plant cells. Cell Struct Funct 2004;29:49-65.
39. Ceresa BP, Lotscher M, Schmid SL. Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q79l)-induced changes in endosome geometry. J Biol Chem 2001;276:9649-9654.
40. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992;70:715-728.
41. Bucci C, Lutcke A, Steele-Mortimer O, Olkkonen VM, Dupree P, Chiariello M, Bruni CB, Simons K, Zerial M. Co-operative regulation of endocytosis by three Rab5 isoforms. FEBS Lett 1995;366:65-71.
42. Dinneen JL, Ceresa BP. Expression of dominant negative rab5 in HeLa cells regulates endocytic trafficking distal from the plasma membrane. Exp Cell Res 2004;294:509-522.
43. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature 1991;349:117-127.
44. Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 2002;317:41-72.
45. Araki S, Kaibuchi K, Sasaki T, Hata Y, Takai Y. Role of the C-terminal region of smg p25A in its interaction with membranes and the GDP/GTP exchange protein. Mol Cell Biol 1991;11:1438-1447.
46. Musha T, Kawata M, Takai Y. The geranylgeranyl moiety but not the methyl moiety of the smg-25A/rab3A protein is essential for the interactions with membrane and its inhibitory GDP/GTP exchange protein. J Biol Chem 1992;267:9821-9825.
47. Soldati T, Riederer MA, Pfeffer SR. Rab GDI: a solubilizing and recycling factor for rab9 protein. Mol Biol Cell 1993;4:425-434.
48. Ueda T, Matsuda N, Uchimiya H, Nakano A. Modes of interaction between the Arabidopsis Rab protein, Ara4, and its putative regulator molecules revealed by a yeast expression system. Plant J 2000;21:341-349.
49. Chavrier P, Gorvel JP, Stelzer E, Simons K, Gruenberg J, Zerial M. Hypervariable C-terminal domain of rab proteins acts as a targeting signal. Nature 1991;353:769-772.
50. Brennwald P, Novick P. Interactions of three domains distinguishing the Ras-related GTP-binding proteins Ypt1 and Sec4. Nature 1993;362:560-563.
51. Aivazian D, Serrano RL, Pfeffer S. TIP47 is a key effector for Rab9 localization. J Cell Biol 2006;173:917-926.
52. Wu Y-W, Oesterlin LK, Tan K-T, Waldmann H, Alexandrov K, Goody RS. Membrane targeting mechanism of Rab GTPases elucidated by semisynthetic protein probes. Nat Chem Biol 2010;6:534-540.
53. Ali BR, Wasmeier C, Lamoreux L, Strom M, Seabra MC. Multiple regions contribute to membrane targeting of Rab GTPases. J Cell Sci 2004;117(Pt 26):6401-6412.
54. Beranger F, Paterson H, Powers S, de Gunzburg J, Hancock JF. The effector domain of Rab6, plus a highly hydrophobic C terminus, is required for Golgi apparatus localization. Mol Cell Biol 1994;14:744-758.
55. Li F, Yi L, Zhao L, Itzen A, Goody RS, Wu Y. The role of the hypervariable C-terminal domain in Rab GTPases membrane targeting. Proc Natl Acad Sci USA 2014;111:2572-2577.
56. Li G, Barbieri MA, Stahl PD. Myristoylation cannot functionally replace the isoprenylation of Rab5. Arch Biochem Biophys 1995;316:529-534.
57. Jia TR, Gao CJ, Cui Y, Wang JQ, Ding Y, Cai Y, Ueda T, Nakano A, Jiang LW. ARA7(Q69L) expression in transgenic Arabidopsis cells induces the formation of enlarged multivesicular bodies. J Exp Bot 2013;64:2817-2829.
58. Glez-Pena D, Gomez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D. ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Res 2010;38:W14-W18.
59. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012;9:772.
60. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003;52:696-704.
61. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007;7:214.
62. Rambaut A, Drummond AJ. Tracer v1.4; 2007. Available from http://beast.bio.ed.ac.uk/Tracer.
63. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006;22:2688-2690.
64. Silvestro D, Michalak I. raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 2012;12:335-337.
65. Rambaut A. FigTree: tree figure drawing tool; 2006-2009. Version 1.3.1. http://tree.bio.ed.ac.uk/software/figtree/
66. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403-410.
67. Weigel D, Glazebrook J. Arabidopsis: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press; 2002.
68. Curtis M, Grossniklaus U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 2003;133:462-469.
69. Littlejohn GR, Gouveia JD, Edner C, Smirnoff N, Love J. Perfluorodecalin enhances in vivo confocal microscopy resolution of Arabidopsis thaliana mesophyll. New Phytol 2010;186:1018-1025.
70. French AP, Mills S, Swarup R, Bennett MJ, Pridmore TP. Colocalization of fluorescent markers in confocal microscope images of plant cells. Nat Protocols 2008;3:619-628.
71. Foissner I. Induction of exocytosis in characean internodal cells by locally restricted application of chlortetracycline and the effect of cytochalasin B, depolarizing and hyperpolarizing agents. Plant Cell Environ 1991;14:907-915.
72. Foissner I, Hoeftberger M. Immuno-gold labeling of resin-embedded electron microscopical sections. In: Žárský V, Cvrčková F, editors. Plant Cell Morphogenesis: Methods and Protocols. New York: Springer Science Business Media; 2014, pp. 183-193.