Non-26S Proteasome Proteolytic Role of Ubiquitin in Plant Endocytosis and Endosomal Trafficking

Journal of Integrative Plant Biology

Volumn 55, Issue 1, 2013, Pages 54-63

  Tian, Miaomiao ^a   Xie, Qi ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

Endocytosis; Endosomal trafficking; Ubiquitin

Indexed keywords

PROTEASOME; UBIQUITIN;

AMINO ACID; CELL ORGANELLE; CYTOLOGY; DEGRADATION; PLANT; PROTEIN;

ARTICLE; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOME; METABOLISM; PROTEIN DEGRADATION; PROTEIN TRANSPORT;

CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; PROTEOLYSIS; UBIQUITIN;

EUKARYOTA; MAMMALIA;

EID: 84872801028     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12007     Document Type: Article

References (87)

1. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8, 249-256.
2. Adhikari A, Chen ZJ (2009) Diversity of polyubiquitin chains. Dev. Cell 16, 485-486.
3. Bachmair A, Novatchkova M, Potuschak T, Eisenhaber F (2001) Ubiquitylation in plants: A post-genomic look at a post-translational modification. Trends Plant Sci. 6, 463-470.
4. Bader M, Steller H (2009) Regulation of cell death by the ubiquitin-proteasome system. Curr. Opin. Cell Biol. 21, 878-884.
5. Barberon M, Zelazny E, Robert S, Conejero G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl. Acad. Sci. USA 108, E450-458.
6. Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11, 643-660.
7. Chen X, Irani NG, Friml J (2011) Clathrin-mediated endocytosis: The gateway into plant cells. Curr. Opin. Plant Biol. 14, 674-682.
8. Ciechanover A, Finley D, Varshavsky A (1984) The ubiquitin-mediated proteolytic pathway and mechanisms of energy-dependent intracellular protein degradation. J. Cell Biochem. 24, 27-53.
9. Clague MJ, Urbe S (2010) Ubiquitin: Same molecule, different degradation pathways. Cell 143, 682-685.
10. Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin B, Wu Y, Tang S, Xie Q (2012) Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell 24, 233-244.
11. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520-527.
12. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat. Cell Biol. 5, 410-421.
13. Duncan LM, Piper S, Dodd RB, Saville MK, Sanderson CM, Luzio JP, Lehner PJ (2006) Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J. 25, 1635-1645.
14. 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 (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13, 853-859.
15. Egner R, Kuchler K (1996) The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett. 378, 177-181.
16. Feraru E, Feraru MI, Kleine-Vehn J, Martiniere A, Mouille G, Vanneste S, Vernhettes S, Runions J, Friml J (2011) PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol 21, 338-343.
17. Floyd BE, Morriss SC, MacIntosh GC, Bassham DC (2012) What to Eat: Evidence for Selective Autophagy in Plants. J. Integr. Plant Biol. 54, 907-920.
18. Forestan C, Varotto S (2012) The role of PIN auxin efflux carriers in polar auxin transport and accumulation and their effect on shaping maize development. Mol. Plant 5, 787-798.
19. Fujimoto M, Arimura S, Ueda T, Takanashi H, Hayashi Y, Nakano A, Tsutsumi N (2010) Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc. Natl. Acad. Sci. USA 107, 6094-6099.
20. Galan JM, Haguenauer-Tsapis R (1997) Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16, 5847-5854.
21. Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21, 1598-1602.
22. Gu Y, Innes RW (2011) The KEEP ON GOING protein of Arabidopsis recruits the ENHANCED DISEASE RESISTANCE1 protein to trans-Golgi network/early endosome vesicles. Plant Physiol. 155, 1827-1838.
23. Hadlington JL, Denecke J (2000) Sorting of soluble proteins in the secretory pathway of plants. Curr. Opin. Plant Biol. 3, 461-468.
24. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466.
25. Hansen CG, Nichols BJ (2009) Molecular mechanisms of clathrin-independent endocytosis. J. Cell Sci. 122, 1713-1721.
26. Happel N, Honing S, Neuhaus JM, Paris N, Robinson DG, Holstein SE (2004) Arabidopsis mu A-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J. 37, 678-693.
27. Herberth S, Shahriari M, Bruderek M, Hessner F, Muller B, Hulskamp M, Schellmann S (2012) Artificial ubiquitylation is sufficient for sorting of a plasma membrane ATPase to the vacuolar lumen of Arabidopsis cells. Planta 236, 63-77.
28. Hershko A (1983) Ubiquitin: Roles in protein modification and breakdown. Cell 34, 11-12.
29. Hershko A (1988) Ubiquitin-mediated protein degradation. J. Biol. Chem. 263, 15237-15240.
30. Hicke L, Riezman H (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287.
31. Hochstrasser M (2009) Origin and function of ubiquitin-like proteins. Nature 458, 422-429.
32. Holstein SE (2002) Clathrin and plant endocytosis. Traffic 3, 614-620.
33. Ikeda F, Dikic I (2008) Atypical ubiquitin chains: New molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep. 9, 536-542.
34. Irani NG, Di Rubbo S, Mylle E, Van den Begin J, Schneider-Pizon J, Hnilikova J, Sisa M, Buyst D, Vilarrasa-Blasi J, Szatmari AM, Van Damme D, Mishev K, Codreanu MC, Kohout L, Strnad M, Cano-Delgado AI, Friml J, Madder A, Russinova E (2012) Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat. Chem. Biol. 8, 583-589.
35. Jiang X, Litkowski PE, Taylor AA, Lin Y, Snider BJ, Moulder KL (2010) A role for the ubiquitin-proteasome system in activity-dependent presynaptic silencing. J. Neurosci. 30, 1798-1809.
36. Jurgens G (2004) Membrane trafficking in plants. Annu. Rev. Cell Dev. Biol. 20, 481-504.
37. Kasai K, Takano J, Miwa K, Toyoda A, Fujiwara T (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J. Biol. Chem. 286, 6175-6183.
38. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
39. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL (2000) Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell 6, 1365-1375.
40. Kitakura S, Vanneste S, Robert S, Lofke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23, 1920-1931.
41. Kolling R, Hollenberg CP (1994) The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13, 3261-3271.
42. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 10, 249.
43. Lai EC, Deblandre GA, Kintner C, Rubin GM (2001) Drosophila neuralized is a ubiquitin ligase that promotes the internalization and degradation of delta. Dev. Cell 1, 783-794.
44. Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L (2007) Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19, 296-319.
45. Legendre-Guillemin V, Wasiak S, Hussain NK, Angers A, McPherson PS (2004) ENTH/ANTH proteins and clathrin-mediated membrane budding. J. Cell Sci. 117, 9-18.
46. Li W, Ye Y (2008) Polyubiquitin chains: Functions, structures, and mechanisms. Cell Mol. Life Sci. 65, 2397-2406.
47. Liu L, Cui F, Li Q, Yin B, Zhang H, Lin B, Wu Y, Xia R, Tang S, Xie Q (2011) The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res. 21, 957-969.
48. Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332, 1439-1442.
49. Matsumoto ML, Wickliffe KE, Dong KC, Yu C, Bosanac I, Bustos D, Phu L, Kirkpatrick DS, Hymowitz SG, Rape M, Kelley RF, Dixit VM (2010) K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 39, 477-484.
50. Matsuoka K, Bednarek SY (1998) Protein transport within the plant cell endomembrane system: An update. Curr. Opin. Plant Biol. 1, 463-469.
51. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533.
52. Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205.
53. Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MC, Fukuda H, Friml J (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc. Natl. Acad. Sci. USA 107, 21890-21895.
54. Oliviusson P, Heinzerling O, Hillmer S, Hinz G, Tse YC, Jiang L, Robinson DG (2006) Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 18, 1239-1252.
55. Otegui MS, Spitzer C (2008) Endosomal functions in plants. Traffic 9, 1589-1598.
56. Pattison RJ, Catala C (2012) Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/ΞAΛ gene families. Plant J 70, 585-598.
57. Qiu QS (2012) Plant and yeast NHX antiporters: Roles in membrane trafficking. J. Integr. Plant Biol. 54, 66-72.
58. Raiborg C, Stenmark H (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452.
59. Reyes FC, Buono R, Otegui MS (2011) Plant endosomal trafficking pathways. Curr. Opin. Plant Biol. 14, 666-673.
60. Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jurgens G (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448, 488-492.
61. Richter S, Muller LM, Stierhof YD, Mayer U, Takada N, Kost B, Vieten A, Geldner N, Koncz C, Jurgens G (2011) Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat. Cell Biol. 14, 80-86.
62. Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542.
63. Robert S, Chary SN, Drakakaki G, Li S, Yang Z, Raikhel NV, Hicks GR (2008) Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc. Natl. Acad. Sci. USA 105, 8464-8469.
64. Robinson DG, Jiang L, Schumacher K (2008) The endosomal system of plants: Charting new and familiar territories. Plant Physiol. 147, 1482-1492.
65. Roth AF, Davis NG (2000) Ubiquitination of the PEST-like endocytosis signal of the yeast a-factor receptor. J. Biol. Chem. 275, 8143-8153.
66. Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, Chory J, de Vries SC (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216-3229.
67. Saito C, Ueda T (2009) Chapter 4: Functions of RAB and SNARE proteins in plant life. Int. Rev. Cell Mol. Biol. 274, 183-233.
68. Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J. 61, 1029-1040.
69. Schellmann S, Pimpl P (2009) Coats of endosomal protein sorting: Retromer and ESCRT. Curr. Opin. Plant Biol. 12, 670-676.
70. Scheuring D, Viotti C, Kruger F, Kunzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K (2011) Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23, 3463-3481.
71. Schlossarek S, Carrier L (2011) The ubiquitin-proteasome system in cardiomyopathies. Curr. Opin. Cardiol. 26, 190-195.
72. Schmidt O, Teis D (2012) The ESCRT machinery. Curr. Biol. 22, 116-120.
73. Shields SB, Piper RC (2011) How ubiquitin functions with ESCRTs. Traffic 12, 1306-1317.
74. Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590.
75. Song L, Shi QM, Yang XH, Xu ZH, Xue HW (2009) Membrane steroid-binding protein 1 (MSBP1) negatively regulates brassinosteroid signaling by enhancing the endocytosis of BAK1. Cell Res. 19, 864-876.
76. Spitzer C, Schellmann S, Sabovljevic A, Shahriari M, Keshavaiah C, Bechtold N, Herzog M, Muller S, Hanisch FG, Hulskamp M (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133, 4679-4689.
77. Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18, 3415-3428.
78. Su W, Liu Y, Xia Y, Hong Z, Li J (2011) Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. Proc. Natl. Acad. Sci. USA 108, 870-875.
79. Takano J, Miwa K, Fujiwara T (2008) Boron transport mechanisms: Collaboration of channels and transporters. Trends Plant Sci. 13, 451-457.
80. Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl. Acad. Sci. USA 102, 12276-12281.
81. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223-1233.
82. Vierstra RD (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135-142.
83. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397.
84. Wiemuth D, Ke Y, Rohlfs M, McDonald FJ (2007) Epithelial sodium channel (ENaC) is multi-ubiquitinated at the cell surface. Biochem. J. 405, 147-155.
85. Wollert T, Yang D, Ren X, Lee HH, Im YJ, Hurley JH (2009) The ESCRT machinery at a glance. J. Cell Sci. 122, 2163-2166.
86. Worden N, Park E, Drakakaki G (2012) Trans-Golgi Network-An Intersection of Trafficking Cell Wall Components. J. Integr. Plant Biol. 54, 875-886.
87. Ye Y, Rape M (2009) Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755-764.