Alg13p, the catalytic subunit of the endoplasmic reticulum UDP-GlcNAc glycosyltransferase, is a target for proteasomal degradation

Molecular Biology of the Cell

Volumn 19, Issue 5, 2008, Pages 2169-2178

  Averbeck, Nicole ^a   Gao, Xiao Dong ^b   Nishimura, Shin Ichiro ^a   Dean, Neta ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; DOLICHOL; GLYCOSYLTRANSFERASE; OLIGOSACCHARIDE; PROTEASOME; PROTEIN A1G13P; PROTEIN A1G14P; PROTEIN SUBUNIT; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE GLYCOSYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CARBOHYDRATE SYNTHESIS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CATALYST; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

CATALYTIC DOMAIN; CELL DEATH; CELL MEMBRANE; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME STABILITY; GLYCOSYLATION; MUTATION; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 48249097100     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-10-1077     Document Type: Article

References (41)

1. Abeijon, C., and Hirschberg, C. B. (1992). Topography of glycosylation reactions in the endoplasmic reticulum. Trends Biochem. Sci. 17, 32-36.
2. Alvarado, E., Ballou, L., Hernandez, L. M., and Ballou, C. E. (1990). Localization of alpha 1-3-linked mannoses in the N-linked oligosaccharides of Saccharomyces cerevisiae mnn mutants. Biochemistry 29, 2471-2482.
3. Asher, G., Reuven, N., and Shaul, Y. (2006). 20S proteasomes and protein degradation "by default." Bioessays 28, 844-849.
4. Averbeck, N., Keppler-Ross, S., and Dean, N. (2007). Membrane topology of the Alg14 ER UDP-GlcNAc transferase subunit. J. Biol. Chem. (in press).
5. Bachmair, A., Finley, D., and Varshavsky, A. (1986). In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186.
6. Bercovich, Z., Rosenberg-Hasson, Y., Ciechanover, A., and Kahana, C. (1989). Degradation of ornithine decarboxylase in reticulocyte lysate is ATP-dependent but ubiquitin-independent. J. Biol. Chem. 264, 15949-15952.
7. Bickel, T., Lehle, L., Schwarz, M., Aebi, M., and Jakob, C. A. (2005). Biosynthesis of lipid-linked oligosaccharides in Saccharomyces cerevisiae: Alg13p and Alg14p form a complex required for the formation of GlcNAc(2)-PP-dolichol. J. Biol. Chem. 280, 34500-34506.
8. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
9. Buchler, N. E., Gerland, U., and Hwa, T. (2005). Nonlinear protein degradation and the function of genetic circuits. Proc. Natl. Acad. Sci. USA 102, 9559-9564.
10. Chantret, I., Dancourt, J., Barbat, A., and Moore, S. E. (2005). Two proteins homologous to the N- and C-terminal domains of the bacterial glycosyltransferase MurG are required for the second step of dolichyl-linked oligosaccharide synthesis in S. cerevisiae. J. Biol. Chem. 280, 9236-9242.
11. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K., and Varshavsky, A. (1989). A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583.
12. Dean, N., and Pelham, H.R.B. (1990). Recycling of proteins from the Golgi compartment to the ER in yeast. J. Cell Biol. 111, 369-377.
13. Dyson, H. J., and Wright, P. E. (2005). Intrinsically unstructured proteins and their functions. Nat. Rev. 6, 197-208.
14. Ferdous, A., Gonzalez, F., Sun, L., Kodadek, T., and Johnston, S. A. (2001). The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol. Cell 7, 981-991.
15. Forsthoefel, A. M., Peña, M. M., Xing, Y. Y., Rafique, Z., and Berger, F. G. (2004). Structural determinants for the intracellular degradation of human thymidylate synthase. Biochemistry 43, 1972-1979.
16. Frickel, E. M., Frei, P., Bouvier, M., Stafford, W. F., Helenius, A., Glockshuber, R., and Ellgaard, L. (2004). ERp57 is a multifunctional thiol-disulfide oxidoreductase. J. Biol. Chem. 279, 18277-18287.
17. Gandre, S., Bercovich, Z., and Kahana, C. (2003). Mitochondrial localization of antizyme is determined by context-dependent alternative utilization of two AUG initiation codons. Mitochondrion 2, 245-256.
18. Gao, X. D., and Dean, N. (2000). Distinct protein domains of the yeast Golgi GDP-mannose transporter mediate oligomer assembly and export from the endoplasmic reticulum. J. Biol. Chem. 275, 17718-17727.
19. Gao, X. D., Tachikawa, H., Sato, T., Jigami, Y., and Dean, N. (2005). Alg14 recruits Alg13p to the cytoplasmic face of the endoplasmic reticulum to form a novel bipartite UDP-N-acetylglucosamine transferase required for the second step of N-linked glycosylation. J. Biol. Chem. 280, 36254-36262.
20. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
21. Gonzalez, F., Delahodde, A., Kodadek, T., and Johnston, S. A. (2002). Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 296, 548-550.
22. Guthrie, C., and Fink, G. R. (1991). Guide to yeast genetics and molecular biology. Methods Enzymol. 194, 3-20.
23. Heinemeyer, W., Gruhler, A., Mohrle, V., Mahe, Y., and Wolf, D. H. (1993). PRE2, highly homologous to the human major histocompatibility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chrymotryptic activity and degradation of ubiquitinated proteins. J. Biol. Chem. 268, 5115-5120.
24. Hoyt, M. A., and Coffino, P. (2004). Ubiquitin-free routes into the proteasome. Cell Mol. Life Sci. 61, 1596-1600.
25. Hoyt, M. A., Zhang, M., and Coffino, P. (2005). Probing the ubiquitin/ proteasome system with ornithine decarboxylase, a ubiquitin-independent substrate. Methods Enzymol. 398, 399-413.
26. Keleher, C. A., Goutte, C., and Johnson, A. D. (1988). The yeast cell-type-specific repressor alpha 2 acts cooperatively with a non-cell-type-specific protein. Cell 53, 927-936.
27. Li, X., and Coffino, P. (1993). Degradation of ornithine decarboxylase: exposure of the C-terminal target by a polyamine-inducible inhibitory protein. Mol. Cell. Biol. 13, 2377-2383.
28. Liu, Y., Mathius, N., Stuessy, C. N., and Goebl, M. G. (1995). Intragenic suppression among CDC34 (UBC3) mutations defines a class of ubiquitin-conjugating catalytic domains. Mol. Cell. Biol. 15, 5635-5644.
29. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
30. Matsuzawa, S., Cuddy, M., Fukushima, T., and Reed, J. C. (2005). Method for targeting protein destruction by using a ubiquitin-independent, proteasome-mediated degradation pathway. Proc. Natl. Acad. Sci. USA 102, 14982-14987.
31. Miller, J. H. (1972). Experiments in Molecular Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
32. Odani, T., Shimma, Y., Wang, X. H., and Jigami, Y. (1997). Mannosylphosphate transfer to cell wall mannan is regulated by the transcriptional level of the MNN4 gene in Saccharomyces cerevisiae. FEBS Lett. 420, 186-190.
33. Orlowski, M., and Wilk, S. (2003). Ubiquitin-independent proteolytic functions of the proteasome. Arch. Biochem. Biophys. 415, 1-5.
34. Peña, M. M., Xing, Y. Y., Koli, S., and Berger, F. G. (2006). Role of N-terminal residues in the ubiquitin-independent degradation of human thymidylate synthase. Biochem. J. 394, 355-363.
35. Perez, M., and Hirschberg, C. B. (1986). Transport of sugar nucleotides and adenosine 3′-phosphate 5′-phosphosulfate into vesicles derived from the Golgi apparatus. Biochim. Biophys. Acta 864, 213-222.
36. Rubin, D. M., Glickman, M. H., Larsen, C. N., Dhruvakumar, S., and Finley, D. (1998). Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 17, 4909-4919.
37. Sikorski, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
38. Snider, M. D., and Rogers, O. C. (1984). Transmembrane movement of oligosaccharide-lipids during glycoprotein synthesis. Cell 36, 753-761.
39. Swanson, R., and Hochstrasser, M. (2000). A viable ubiquitin-activating enzyme mutant for evaluating ubiquitin system function in Saccharomyces cerevisiae. FEBS Lett. 477, 193-198.
40. Thomas, B. J., and Rothstein, R. (1989). The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination at GAL10, a transcriptionally regulated gene. Genetics 123, 725-738.
41. Weerapana, E., and Imperiali, B. (2006). Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16, 91R-101R.