The arabidopsis homolog of the mammalian os-9 protein plays a key role in the endoplasmic reticulum-associated degradation of misfolded receptor-like kinases

Molecular Plant

Volumn 5, Issue 4, 2012, Pages 929-940

  Su, Wei ^a,b   Liu, Yidan ^a   Xia, Yang ^a   Hong, Zhi ^a,c   Li, Jianming ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b FUDAN UNIVERSITY   (China)

^c NANJING UNIVERSITY   (China)

Author keywords

Brassinosteroid receptor; EMS mutagenized bri1 9 suppressor; ER quality control; Lectin; MRH domain; N glycan

Indexed keywords

ARABIDOPSIS; BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 84866410154     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss042     Document Type: Article

References (59)

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. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657 (Pubitemid 36927950)
3. Arnold, S.M., Fessler, L.I., Fessler, J.H., and Kaufman, R.J. (2000). Two homologues encoding human UDP-glucose:glycoprotein glucosyltransferase differ in mRNA expression and enzymatic activity. Biochemistry. 39, 2149-2163 (Pubitemid 30130063)
4. Bechtold, N., and Pelletier, G. (1998). In planta Agrobacteriummediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259-266
5. Caramelo, J.J., and Parodi, A.J. (2007). How sugars convey information on protein conformation in the endoplasmic reticulum. Semin. Cell. Dev. Biol. 18, 732-742 (Pubitemid 350138447)
6. Ceriotti, A., and Roberts, L.M. (2006). Endoplasmic reticulumassociated protein degradation in plant cells. In The Plant Endoplasmic Reticulum, Robinson D.G., ed. (Berlin Heidelberg: Springer-Verlag), pp. 75-98
7. Chakrabarty, R., Banerjee, R., Chung, S.M., Farman, M., Citovsky, V., Hogenhout, S.A., Tzfira, T., and Goodin, M. (2007). PSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. Mol. Plant-Microbe Interact. 20, 740-750 (Pubitemid 46944968)
8. 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
9. Clouse, S.D., Langford, M., and McMorris, T.C. (1996). A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111, 671-678 (Pubitemid 126450540)
10. 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 Cell. 24, 233-244
11. Curtis, M.D., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469 (Pubitemid 37325657)
12. Denic, V., Quan, E.M., and Weissman, J.S. (2006). A luminal surveillance complex that selects misfolded glycoproteins for ERassociated degradation. Cell. 126, 349-359 (Pubitemid 44092967)
13. Elbein, A.D. (1981). The tunicamycins-useful tools for studies on glycoproteins. Trends Biochem. Sci. 6, 219-221
14. Elbein, A.D., Tropea, J.E., Mitchell, M., and Kaushal, G.P. (1990). Kifunensine, a potent inhibitor of the glycoprotein processing mannosidase I. J. Biol. Chem. 265, 15599-15605
15. Friedrichsen, D.M., Joazeiro, C.A., Li, J., Hunter, T., and Chory, J. (2000). Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol. 123, 1247-1256
16. 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 (Pubitemid 44151588)
17. Guan, K.L., and Dixon, J.E. (1991). Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192, 262-267
18. Hajdukiewicz, P., Svab, Z., and Maliga, P. (1994). The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989-994 (Pubitemid 2152867)
19. Hampton, R.Y., Gardner, R.G., and Rine, J. (1996). Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol. Biol. Cell. 7, 2029-2044 (Pubitemid 26415008)
20. Hauri, H.P., Nufer, O., Breuza, L., Tekaya, H.B., and Liang, L. (2002). Lectins and protein traffic early in the secretory pathway. Biochem. Soc. Symp. 69, 73-82 (Pubitemid 135689843)
21. Helenius, A., and Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049 (Pubitemid 39050393)
22. 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
23. Hong, Z., Jin, H., Tzfira, T., and Li, J. (2008). Multiple mechanismmediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell. 20, 3418-3429
24. Hosokawa, N., Kamiya, Y., and Kato, K. (2010). The role of MRH domain-containing lectins in ERAD. Glycobiology. 20, 651-660
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 mannosetrimmed N-glycans. J. Biol. Chem. 284, 17061-17068
26. Huttner, 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
27. 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
28. Jin, H., Yan, Z., Nam, K.H., 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 (Pubitemid 46921004)
29. 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 (Pubitemid 40979315)
30. Kelleher, D.J., and Gilmore, R. (2006). An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology. 16, 47R-62R.
31. Kinoshita, T., Cano-Delgado, A., Seto, H., Hiranuma, S., Fujioka, S., Yoshida, S., and Chory, J. (2005). Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature. 433, 167-171
32. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. (2004). The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell. 16, 3496-3507 (Pubitemid 41096021)
33. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 90, 929-938 (Pubitemid 27381631)
34. Li, J., and Chory, J. (1998). Preparation of DNA from Arabidopsis. Methods Mol. Biol. 82, 55-60
35. Li, J.,Nam, K.H.,Vafeados,D., and Chory, J. (2001). BIN2, a newbrassinosteroid-insensitivelocusinArabidopsis.PlantPhysiol.127,14-22
36. Li, J., Zhao-Hui, C., Batoux, M., Nekrasov, V., Roux, M., Chinchilla, D., Zipfel, C., and Jones, J.D. (2009). Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl Acad. Sci. U S A. 106, 15973-15978
37. Liu, J.X., and Howell, S.H. (2010). Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell. 22, 2930-2942
38. 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
39. Lu, X., Tintor, N., Mentzel, T., Kombrink, E., Boller, T., Robatzek, S., Schulze-Lefert, P., and Saijo, Y. (2009). Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl Acad. Sci. U S A. 106, 22522-22527
40. Martinez, I.M., and Chrispeels, M.J. (2003). Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell. 15, 561-576 (Pubitemid 36230005)
41. Mikami, K., et al. (2010). The sugar-binding ability of human OS-9 and its involvement in ER-associated degradation. Glycobiology. 20, 310-321
42. Mora-Garcia, S., Vert, G., Yin, Y., Cano-Delgado, A., Cheong, H., and Chory, J. (2004). Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448-460 (Pubitemid 38316351)
43. Neff, M.M., Neff, J.D., Chory, J., and Pepper, A.E. (1998). dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J. 14, 387-392 (Pubitemid 28236003)
44. Nekrasov, V., et al. (2009). Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28, 3428-3438
45. Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Yoshida, S., Yuan, H., Feldmann, K.A., and Tax, F.E. (1999). Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol. 121, 743-752
46. Quan, E.M., Kamiya, Y., Kamiya, D., Denic, V., Weibezahn, J., Kato, K., andWeissman, J.S. (2008). Defining the glycan destruction signal for endoplasmic reticulum-associated degradation. Mol. Cell. 32, 870-877
47. Robbins, P.W., Trimble, R.B., Wirth, D.F., Hering, C., Maley, F., Maley, G.F., Das, R., Gibson, B.W., Royal, N., and Biemann, K. (1984). Primary structure of the Streptomyces enzyme endo-beta-N-acetylglucosaminidase H. J. Biol. Chem. 259, 7577-7583 (Pubitemid 14081164)
48. Saijo, Y. (2010). ER quality control of immune receptors and regulators in plants. Cell Microbiol. 12, 716-724
49. Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K., Haweker, H., Dong, X., Robatzek, S., and Schulze-Lefert, P. (2009). Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28, 3439-3449
50. Satoh, T., Chen, Y., Hu, D., Hanashima, S., Yamamoto, K., and Yamaguchi, Y. (2010). Structural basis for oligosaccharide recognition of misfolded glycoproteins by OS-9 in ER-associated degradation. Mol. Cell. 40, 905-916
51. 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
52. 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
53. 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 (Pubitemid 41316671)
54. Vembar, S.S., and Brodsky, J.L. (2008). One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9, 944-957
55. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956 (Pubitemid 36339384)
56. Williams,D.B. (2006). Beyondlectins: the calnexin/calreticulinchaperone systemof the endoplasmic reticulum. J. Cell. Sci. 119, 615-623
57. Yin, Y.,Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell. 109, 181-191 (Pubitemid 34518257)
58. Zhao, J., Peng, P., Schmitz, R.J., Decker, A.D., Tax, F.E., and Li, J. (2002). Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol. 130, 1221-1229 (Pubitemid 35352950)
59. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D., Boller, T., and Felix, G. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell. 125, 749-760.