Endoplasmic reticulum-associated degradation of glycoproteins in plants

Frontiers in Plant Science

Volumn 3, Issue APR, 2012, Pages

  Hüttner, Silvia ^a   Strasser, Richard ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Endoplasmic reticulum; Protein degradation; Protein glycosylation; Protein quality control; Ubiquitin proteasome

Indexed keywords

EID: 84890550268     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00067     Document Type: Review

References (56)

1. Aebi, M., Bernasconi, R., Clerc, S., and Molinari, M. (2010). N-glycan structures: recognition and processing in the ER. Trends Biochem. Sci. 35, 74-82.
2. Bernasconi, R., Galli, C., Calanca, V., Nakajima, T., and Molinari, M. (2010). Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates. J. Cell Biol. 188, 223-235.
3. Bernasconi, R., Pertel, T., Luban, J., and Molinari, M. (2008). A dual task for the Xbp1-responsive OS-9 variants in the mammalian endoplasmic reticulum: inhibiting secretion of misfolded protein conformers and enhancing their disposal. J. Biol. Chem. 283, 16446-16454.
4. Bhamidipati, A., Denic, V., Quan, E. M., and Weissman, J. S. (2005). Exploration of the topological requirements of ERAD identifies Yos9p as a lectin sensor of misfolded glycoproteins in the ER lumen. Mol. Cell 19, 741-751.
5. Brandizzi, F., Hanton, S., DaSilva, L., Boevink, P., Evans, D., Oparka, K., Denecke, J., and Hawes, C. (2003). ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J. 34, 269-281.
6. Caramelo, J., and Parodi, A. (2008). Getting in and out from calnexin/calreticulin cycles. J. Biol. Chem. 283, 10221-10225.
7. Ceriotti, A. (2011). Waste disposal in the endoplasmic reticulum, ROS production and plant salt stress response. Cell Res. 21, 555-557.
8. Che, P., Bussell, J. D., Zhou, W., Estavillo, G. M., Pogson, B. J., and Smith, S. M. (2010). Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci. Signal. 3, ra69.
9. Chen, X., Tukachinsky, H., Huang, C. H., Jao, C., Chu, Y. R., Tang, H. Y., Mueller, B., Schulman, S., Rapoport, T. A., and Salic, A. (2011). Processing and turnover of the Hedgehog protein in the endoplasmic reticulum. J. Cell Biol.192, 825-838.
10. Chiang, W. C., Messah, C., and Lin, J. H. (2012). IRE1 directs proteasomal and lysosomal degradation of misfolded rhodopsin. Mol. Biol. Cell 23, 758-770.
11. Christianson, J. C., Olzmann, J. A., Shaler, T. A., Sowa, M. E., Bennett, E. J., Richter, C. M., Tyler, R. E., Greenblatt, E. J., Harper, J. W., and Kopito, R. R. (2012). Defining human ERAD networks through an integrative mapping strategy. Nat. Cell Biol. 14, 93-105.
12. Christianson, J. C., Shaler, T. A., Tyler, R. E., and Kopito, R. R. (2008). OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10, 272-282.
13. Clerc, S., Hirsch, C., Oggier, D. M., Deprez, P., Jakob, C., Sommer, T., and Aebi, M. (2009). Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J. Cell Biol. 184, 159-172.
14. Cui, F., Liu, L., Zhao, Q., Zhang, Z., Li, Q., Lin, B., Wu, Y., Tang, S., and Xie, Q. (2012). Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell24, 233-244.
15. Denic, V., Quan, E. M., and Weissman, J. S. (2006). A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126, 349-359.
16. Di Cola, A., Frigerio, L., Lord, J. M., Ceriotti, A., and Roberts, L. M. (2001). Ricin A chain without its partner B chain is degraded after retrotranslocation from the endoplasmic reticulum to the cytosol in plant cells. Proc. Natl. Acad. Sci. U.S.A. 98, 14726-14731.
17. Di Cola, A., Frigerio, L., Lord, J. M., Roberts, L., and Ceriotti, A. (2005). Endoplasmic reticulum-associated degradation of ricin A chain has unique and plant-specific features. Plant Physiol. 137, 287-296.
18. Foresti, O., De Marchis, F., de Virgilio, M., Klein, E. M., Arcioni, S., Bellucci, M., and Vitale, A. (2008). Protein domains involved in assembly in the endoplasmic reticulum promote vacuolar delivery when fused to secretory GFP, indicating a protein quality control pathway for degradation in the plant vacuole. Mol. Plant 1, 1067-1076.
19. Gauss, R., Jarosch, E., Sommer, T., and Hirsch, C. (2006). A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat. Cell Biol. 8, 849-854.
20. Hebert, D. N., Bernasconi, R., and Molinari, M. (2010). ERAD substrates: which way out? Semin. Cell Dev. Biol. 21, 526-532.
21. Hegde, R. S., and Ploegh, H. L. (2010). Quality and quantity control at the endoplasmic reticulum. Curr. Opin. Cell Biol. 22, 437-446.
22. Helenius, A., and Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem.73, 1019-1049.
23. Hong, Z., Jin, H., Fitchette, A.-C., Xia, Y., Monk, A. M., Faye, L., and Li, J. (2009). Mutations of an alpha1,6 mannosyltransferase inhibit endoplasmic reticulum-associated degradation of defective brassinosteroid receptors in Arabidopsis. Plant Cell 21, 3792-3802.
24. Hong, Z., Jin, H., Tzfira, T., and Li, J. (2008). Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20, 3418-3429.
25. Hosokawa, N., Kamiya, Y., Kamiya, D., Kato, K., and Nagata, K. (2009). Human OS-9, a lectin required for glycoprotein endoplasmic reticulum-associated degradation, recognizes mannose-trimmed N-glycans. J. Biol. Chem. 284, 17061-17068.
26. Hosokawa, N., Kamiya, Y., and Kato, K. (2010). The role of MRH domain-containing lectins in ERAD. Glycobiology20, 651-660.
27. Hüttner, S., Veit, C., Schoberer, J., Grass, J., and Strasser, R. (2012). Unraveling the function of Arabidopsis thaliana OS9 in the endoplasmic reticulum-associated degradation of glycoproteins. Plant Mol. Biol. doi:10.1007/s11103-012-9891-4
28. Iida, Y., Fujimori, T., Okawa, K., Nagata, K., Wada, I., and Hosokawa, N. (2011). SEL1L protein critically determines the stability of the HRD1-SEL1L endoplasmic reticulum-associated degradation (ERAD) complex to optimize the degradation kinetics of ERAD substrates. J. Biol. Chem. 286, 16929-16939.
29. Jaenicke, L. A., Brendebach, H., Selbach, M., and Hirsch, C. (2011). Yos9p assists in the degradation of certain nonglycosylated proteins from the endoplasmic reticulum. Mol. Biol. Cell 22, 2937-2945.
30. Jin, H., Hong, Z., Su, W., and Li, J. (2009). A plant-specific calreticulin is a key retention factor for a defective brassinosteroid receptor in the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 106, 13612-13617.
31. Jin, H., Yan, Z., Nam, K., and Li, J. (2007). Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control. Mol. Cell 26, 821-830.
32. Kamauchi, S., Nakatani, H., Nakano, C., and Urade, R. (2005). Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 272, 3461-3476.
33. Kawaguchi, S., Hsu, C.-L., and Ng, D. T. W. (2010). Interplay of substrate retention and export signals in endoplasmic reticulum quality control. PLoS ONE 5, e15532. doi:10.1371/journal.pone.0015532
34. Kikkert, M., Doolman, R., Dai, M., Avner, R., Hassink, G., van Voorden, S., Thanedar, S., Roitelman, J., Chau, V., and Wiertz, E. (2004). Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J. Biol. Chem. 279, 3525-3534.
35. Kim, W., Spear, E. D., and Ng, D. T. W. (2005). Yos9p detects and targets misfolded glycoproteins for ER-associated degradation. Mol. Cell 19, 753-764.
36. Kincaid, M. M., and Cooper, A. A. (2007). Misfolded proteins traffic from the endoplasmic reticulum (ER) due to ER export signals. Mol. Biol. Cell 18, 455-463.
37. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.
38. Liebminger, E., Hüttner, S., Vavra, U., Fischl, R., Schoberer, J., Grass, J., Blaukopf, C., Seifert, G. J., Altmann, F., Mach, L., and Strasser, R. (2009). Class I alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. Plant Cell 21, 3850-3867.
39. Liu, J.-X., Srivastava, R., Che, P., and Howell, S. H. (2007). Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J. 51, 897-909.
40. Liu, J.-X., and Howell, S. H. (2010a). bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22, 782-796.
41. Liu, J.-X., and Howell, S. H. (2010b). Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22, 2930-2942.
42. Liu, L., Cui, F., Li, Q., Yin, B., Zhang, H., Lin, B., Wu, Y., Xia, R., Tang, S., and Xie, Q. (2011). The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res. 21, 957-969.
43. Marshall, R. S., Jolliffe, N. A., Ceriotti, A., Snowden, C. J., Lord, J. M., Frigerio, L., and Roberts, L. M. (2008). The role of CDC48 in the retro-translocation of non-ubiquitinated toxin substrates in plant cells. J. Biol. Chem. 283, 15869-15877.
44. Martínez, I., and Chrispeels, M. (2003). Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15, 561-576.
45. Müller, J., Piffanelli, P., Devoto, A., Miklis, M., Elliott, C., Ortmann, B., Schulze-Lefert, P., and Panstruga, R. (2005). Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell 17, 149-163.
46. Nagashima, Y., Mishiba, K., Suzuki, E., Shimada, Y., Iwata, Y., and Koizumi, N. (2011). Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci. Rep. 1, 29.
47. Pedrazzini, E., Giovinazzo, G., Bielli, A., de Virgilio, M., Frigerio, L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A., and Vitale, A. (1997). Protein quality control along the route to the plant vacuole. Plant Cell 9, 1869-1880.
48. Pimpl, P., Taylor, J. P., Snowden, C., Hillmer, S., Robinson, D. G., and Denecke, J. (2006). Golgi-mediated vacuolar sorting of the endoplasmic reticulum chaperone BiP may play an active role in quality control within the secretory pathway. Plant Cell 18, 198-211.
49. Quan, E., Kamiya, Y., Kamiya, D., Denic, V., Weibezahn, J., Kato, K., and Weissman, J. S. (2008). Defining the glycan destruction signal for endoplasmic reticulum-associated degradation. Mol. Cell 32, 870-877.
50. Russinova, E., Borst, J.-W., Kwaaitaal, M., Caño-Delgado, A., Yin, Y., Chory, J., and de Vries, S. C. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216-3229.
51. Sato, B. K., Schulz, D., Do, P. H., and Hampton, R. Y. (2009). Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol. Cell 34, 212-222.
52. Smith, M. H., Ploegh, H. L., and Weissman, J. S. (2011). Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334, 1086-1090.
53. Su, W., Liu, Y., Xia, Y., Hong, Z., and Li, J. (2011). Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 870-875.
54. Szathmary, R., Bielmann, R., Nita-Lazar, M., Burda, P., and Jakob, C. A. (2005). Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. Mol. Cell 19, 765-775.
55. Vashist, S., and Ng, D. T. W. (2004). Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 165, 41-52.
56. Vitale, A., and Boston, R. S. (2008). Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9, 1581-1588.