C-terminal armadillo repeats are essential and sufficient for association of the plant U-box armadillo E3 ubiquitin ligase SAUL1 with the plasma membrane

Journal of Experimental Botany

Volumn 62, Issue 2, 2011, Pages 775-785

  Drechsel, Gabriele ^a   Bergler, Johannes ^a   Wippel, Kathrin ^a   Sauer, Norbert ^a   Vogelmann, Katja ^a   Hoth, Stefan ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

ARM repeat; Armadillo repeat; E3 ubiquitin ligase; plasma membrane; SAUL1; U box

Indexed keywords

ARABIDOPSIS PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TRANSPORT; UBIQUITINATION;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; PROTEIN BINDING; PROTEIN TRANSPORT; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

ARMADILLO;

EID: 78650649279     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq313     Document Type: Article

References (68)

1. Abel S, Theologis A. 1994. Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. The Plant Journal 5, 421-427.
2. Aberle H, Butz S, Stappert J, Weissig H, Kemler R, Hoschuetzky H. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. Journal of Cell Science 107, 3655-3663.
3. Amador V, Monte E, Garcia-Martinez JL, Prat S. 2001. Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo. Cell 106, 343-354.
4. Aravind L, Koonin EV. 2000. The U box is a modified RING finger-a common domain in ubiquitination. Current Biology 10, R132-R134.
5. Azevedo C, Santos-Rosa MJ, Shirasu K. 2001. The U-box protein family in plants. Trends in Plant Science 6, 354-358.
6. Behrens J. 2000. Control of beta-catenin signaling in tumor development. Annals of the New York Academy of Sciences 910, 21-33: discussion 33-25.
7. Bhattacharjee S, Lee LY, Oltmanns H, Cao H, Veena Cuperus J, Gelvin SB. 2008. IMPa-4, an Arabidopsis importin alpha isoform, is preferentially involved in agrobacterium-mediated plant transformation. The Plant Cell 20, 2661-2680.
8. Cho SK, Ryu MY, Song C, Kwak JM, Kim WT. 2008. Arabidopsis PUB22 and PUB23 are homologous U-box E3 ubiquitin ligases that play combinatory roles in response to drought stress. The Plant Cell 20, 1899-1914.
9. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
10. Coates JC. 2003. Armadillo repeat proteins: beyond the animal kingdom. Trends in Cell Biology 13, 463-471.
11. Coates JC, Laplaze L, Haseloff J. 2006. Armadillo-related proteins promote lateral root development in Arabidopsis. Proceedings of the National Academy of Sciences, USA 103, 1621-1626.
12. Conti E, Kuriyan J. 2000. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha. Structure 8, 329-338.
13. Curtis MD, Grossniklaus U. 2003. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133, 462-469.
14. Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, Van Montagu M, Leemans J. 1985. Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Research 13, 4777-4788.
15. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. The Plant Journal 45, 616-629.
16. Fleckenstein D, Rohde M, Klionsky DJ, Rudiger M. 1998. Yel013p (Vac8p), an armadillo repeat protein related to plakoglobin and importin alpha is associated with the yeast vacuole membrane. Journal of Cell Science 111, 3109-3118.
17. Froissard M, Keller AM, Cohen J. 2001. ND9P, a novel protein with armadillo-like repeats involved in exocytosis: physiological studies using allelic mutants in paramecium. Genetics 157, 611-620.
18. Gebert M, Dresselhaus T, Sprunck S. 2008. F-actin organization and pollen tube tip growth in Arabidopsis are dependent on the gametophyte-specific Armadillo repeat protein ARO1. The Plant Cell 20, 2798-2814.
19. Gonzalez-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD. 2006. The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. The Plant Cell 18, 1067-1083.
20. Gorlich D, Kutay U. 1999. Transport between the cell nucleus and the cytoplasm. Annual Review of Cell and Developmental Biology 15, 607-660.
21. Graham TA, Weaver C, Mao F, Kimelman D, Xu W. 2000. Crystal structure of a beta-catenin/Tcf complex. Cell 103, 885-896.
22. Gruss OJ, Carazo-Salas RE, Schatz CA, Guarguaglini G, Kast J, Wilm M, Le Bot N, Vernos I, Karsenti E, Mattaj IW. 2001. Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 104, 83-93.
23. Hachet V, Kocher T, Wilm M, Mattaj IW. 2004. Importin alpha associates with membranes and participates in nuclear envelope assembly in vitro. EMBO Journal 23, 1526-1535.
24. Hatakeyama S, Yada M, Matsumoto M, Ishida N, Nakayama KI. 2001. U box proteins as a new family of ubiquitin-protein ligases. Journal of Biological Chemistry 276, 33111-33120.
25. Hoppe T, Rape M, Jentsch S. 2001. Membrane-bound transcription factors: regulated release by RIP or RUP. Current Opinion in Cell Biology 13, 344-348.
26. Huber AH, Nelson WJ, Weis WI. 1997. Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90, 871-882.
27. Huber AH, Weis WI. 2001. The structure of the beta-catenin/ E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 105, 391-402.
28. Hulsken J, Birchmeier W, Behrens J. 1994. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. Journal of Cell Biology 127, 2061-2069.
29. Iwata Y, Koizumi N. 2005. An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proceedings of the National Academy of Sciences, USA 102, 5280-5285.
30. Jin Z, Li Y, Pitti R, Lawrence D, Pham VC, Lill JR, Ashkenazi A. 2009. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 137, 721-735.
31. Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
32. Kerscher O, Felberbaum R, Hochstrasser M. 2006. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell and Developmental Biology 22, 159-180.
33. Kim S, Choi HI, Ryu HJ, Park JH, Kim MD, Kim SY. 2004. ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiology 136, 3639-3648.
34. Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM. 2006. A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. The Plant Cell 18, 3132-3144.
35. Koegl M, Hoppe T, Schlenker S, Ulrich HD, Mayer TU, Jentsch S. 1999. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 96, 635-644.
36. Lin SS, Martin R, Mongrand S, Vandenabeele S, Chen KC, Jang IC, Chua NH. 2008. RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. The Plant Journal 56, 550-561.
37. Masuda HP, Cabral LM, De Veylder L, Tanurdzic M, de Almeida Engler J, Geelen D, Inze D, Martienssen RA, Ferreira PC, Hemerly AS. 2008. ABAP1 is a novel plant Armadillo BTB protein involved in DNA replication and transcription. EMBO Journal 27, 2746-2756.
38. Mudgil Y, Shiu SH, Stone SL, Salt JN, Goring DR. 2004. A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiology 134, 59-66.
39. Nambara E, McCourt P. 1999. Protein farnesylation in plants: a greasy tale. Current Opinion in Plant Biology 2, 388-392.
40. Nusslein-Volhard C, Wieschaus E. 1980. Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
41. Pai LM, Kirkpatrick C, Blanton J, Oda H, Takeichi M, Peifer M. 1996. Drosophila alpha-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. Journal of Biological Chemistry 271, 32411-32420.
42. Pan X, Goldfarb DS. 1998. YEB3/VAC8 encodes a myristylated armadillo protein of the Saccharomyces cerevisiae vacuolar membrane that functions in vacuole fusion and inheritance. Journal of Cell Science 111, 2137-2147.
43. Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, Hoth S. 2009. Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. The Plant Journal 59, 39-51.
44. Riggleman B, Wieschaus E, Schedl P. 1989. Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes and Development 3, 96-113.
45. Samuel MA, Mudgil Y, Salt JN, Delmas F, Ramachandran S, Chilelli A, Goring DR. 2008. Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiology 147, 2084-2095.
46. Santner A, Estelle M. 2009. Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071-1078.
47. Sauer N, Stadler R. 1993. A sink-specific H+/monosaccharide co-transporter from Nicotiana tabacum: cloning and heterologous expression in baker's yeast. The Plant Journal 4, 601-610.
48. Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flugge UI, Kunze R. 2003. ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiology 131, 16-26.
49. Schwechheimer C, Calderon Villalobos LI. 2004. Cullin-containing E3 ubiquitin ligases in plant development. Current Opinion in Plant Biology 7, 677-686.
50. Seo PJ, Kim SG, Park CM. 2008. Membrane-bound transcription factors in plants. Trends in Plant Science 13, 550-556.
51. Sigismund S, Polo S, Di Fiore PP. 2004. Signaling through monoubiquitination. Current Topics in Microbioogy andl Immunology 286, 149-185.
52. Stone SL, Anderson EM, Mullen RT, Goring DR. 2003. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. The Plant Cell 15, 885-898.
53. Stone SL, Callis J. 2007. Ubiquitin ligases mediate growth and development by promoting protein death. Current Opinion in Plant Biology 10, 624-632.
54. Trujillo M, Ichimura K, Casais C, Shirasu K. 2008. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Current Biology 18, 1396-1401.
55. Vierstra RD. 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nature Reviews Molecular Cell Biology 10, 385-397.
56. Von Kries JP, Winbeck G, Asbrand C, Schwarz-Romond T, Sochnikova N, Dell'Oro A, Behrens J, Birchmeier W. 2000. Hot spots in beta-catenin for interactions with LEF-1, conductin and APC. Nature Structural Biology 7, 800-807.
57. Wahl R, Wippel K, Goos S, Kämper J, Sauer N. 2010. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biology 8, e1000303.
58. Wang YX, Catlett NL, Weisman LS. 1998. Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. Journal of Cell Biology 140, 1063-1074.
59. Wang Z, Yuan T, Yuan C, Niu Y, Sun D, Cui S. 2009. LFR, which encodes a novel nuclear-localized Armadillo-repeat protein, affects multiple developmental processes in the aerial organs in Arabidopsis. Plant Molecular Biology 69, 121-131.
60. Wiborg J, O'Shea C, Skriver K. 2008. Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin-protein ligases. Biochemical Journal 413, 447-457.
61. Xing Y, Clements WK, Kimelman D, Xu W. 2003. Crystal structure of a beta-catenin/axin complex suggests a mechanism for the beta-catenin destruction complex. Genes and Development 17, 2753-2764.
62. Xing Y, Clements WK, Le Trong I, Hinds TR, Stenkamp R, Kimelman D, Xu W. 2004. Crystal structure of a beta-catenin/APC complex reveals a critical role for APC phosphorylation in APC function. Molecular Cell 15, 523-533.
63. Yalovsky S, Rodr?́guez-Concepcion M, Gruissem W. 1999. Lipid modifications of proteins-slipping in and out of membranes. Trends in Plant Science 4, 439-445.
64. Yang CW, Gonzalez-Lamothe R, Ewan RA, Rowland O, Yoshioka H, Shenton M, Ye H, O'Donnell E, Jones JD, Sadanandom A. 2006. The E3 ubiquitin ligase activity of arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. The Plant Cell 18, 1084-1098.
65. Yang G, Gao P, Zhang H, Huang S, Zheng ZL. 2007. A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS One 2, e1074.
66. Yap AS, Brieher WM, Gumbiner BM. 1997. Molecular and functional analysis of cadherin-based adherens junctions. Annual Reviews of Cell and Devopmental Biology 13, 119-146.
67. Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL. 2004. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. The Plant Cell 16, 2795-2808.
68. Zhurinsky J, Shtutman M, Ben-Ze'ev A. 2000. Plakoglobin and beta-catenin: protein interactions, regulation and biological roles. Journal of Cell Science 113, 3127-3139.