Carbohydrates act as sorting determinants in ER-associated degradation of tyrosinase

Journal of Cell Science

Volumn 117, Issue 14, 2004, Pages 2937-2949

  Svedine, Sherri ^a   Wang, Tao ^a   Halaban, Ruth ^b   Hebert, Daniel N ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Molecular chaperones; N linked glycans; Protein aggregation; Quality control

Indexed keywords

CALNEXIN; CARBOHYDRATE; CHAPERONE; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; LECTIN; MANNOSE; MONOPHENOL MONOOXYGENASE; MUTANT PROTEIN; PROTEASOME; PROTEIN DISULFIDE ISOMERASE;

ALBINISM; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL PERMEABILIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME DEGRADATION; ENZYME SUBSTRATE; GLYCOSYLATION; MELANOCYTE; MOLECULAR STABILITY; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALNEXIN; CARBOHYDRATE METABOLISM; CELLS, CULTURED; ENDOPLASMIC RETICULUM; GLUCOSE; HEAT-SHOCK PROTEINS; MANNOSE; MELANOCYTES; MICE; MOLECULAR CHAPERONES; MONOPHENOL MONOOXYGENASE; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN DISULFIDE-ISOMERASE; PROTEIN TRANSPORT;

ANIMALIA;

EID: 4344568526     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01154     Document Type: Article

References (71)

1. Ayalon-Soffer, M., Shenkman, M. and Lederkremer, G. Z. (1999). Differential roles of mannose and glucose trimming in the ER degradation of asialoglycoprotein receptor subunits. J. Cell Sci. 112, 3309-3318.
2. Beckers, C. J. M., Keller, D. S. and Balch, W. E. (1987). Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex. Cell 50, 523-534.
3. Ben-Zeev, O., Mao, H. Z. and Doolittle, M. H. (2002). Maturation of lipoprotein lipase in the endoplasmic reticulum. Concurrent formation of functional dimers and inactive aggregates. J. Biol. Chem. 277, 10727-10738.
4. Bennett, D. C., Cooper, P. J., Dexter, T. J., Devlin, L. M., Heasman, J. and Nester, B. (1989). Cloned mouse melanocyte lines carrying the germline mutations albino and brown: complementation in culture. Development 105, 379-385.
5. Berson, J. F., Frank, D. W., Calvo, P. A., Bieler, B. M. and Marks, M. S. (2000). A common temperature-sensitive allelic form of human tyrosinase is retained in the endoplasmic reticulum at the nonpermissive temperature. J. Biol. Chem. 275, 12281-12289.
6. Bonifacino, J. S. and Weissman, A. M. (1998). Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev. Cell Dev. Biol. 14, 19-57.
7. Branza-Nichita, N., Petrescu, A. J., Dwek, R. A., Wormald, M. R., Platt, F. M. and Petrescu, S. M. (1999). Tyrosinase folding and copper loading in vivo: a crucial role for calnexin and alpha-glucosidase II. Biochem. Biophy. Res. Commun. 261, 720-725.
8. Cabral, C. M., Choudhury, P., Liu, Y. and Sifers, R. N. (2000). Processing by endoplasmic reticulum mannosidases partitions a secretion-impaired glycoprotein into distinct disposal pathways. J Biol. Chem. 275, 25015-25022.
9. Cabral, C. M., Liu, Y. and Sifers, R. N. (2001). Dissecting glycoprotein quality control in the secretory pathway. Trends Biochem. Sci. 26, 619-624.
10. Cabral, C. M., Liu, Y., Moreman, K. W. and Sifers, R. N. (2002). Organizational diversity among distinct glycoprotein endoplasmic reticulum-associated degradation programs. Mol. Biol. Cell 13, 2639-2650.
11. Daniels, R., Svedine, S. and Hebert, D. N. (2004). N-linked carbohydrates act as lumenal maturation and quality control protein tags. Cell. Biochem. Biophys. (in press).
12. Dick, L. R., Cruikshank, A. A., Grenier, L., Melandri, F. D., Nunes, S. L. and Stein, R. L. (1996). Mechanistic studies on the inactivation of the proteasome by lactacystin: a central role for clasto-lactacystin beta-lactone. J. Biol. Chem. 271, 7273-7276.
13. Elbein, A. D. (1991). Glucosidase inhibitors: inhibitors of N-linked oligosaccharide processing. FASEB J. 5, 3055-3063.
14. Ellgaard, L. and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 4, 181-191.
15. Fagioli, C. and Sitia, R. (2001). Glycoprotein quality control in the endoplasmic reticulum. J. Biol. Chem. 276, 12885-12892.
16. Francis, E., Wang, N., Parag, H., Halaban, R. and Hebert, D. N. (2003). Tyrosinase maturation and oligomerization in the endoplasmic reticulum requires a melanocyte specific factor. J. Biol. Chem. 278, 25607-25617.
17. Frenkel, Z., Gregory, W., Kornfeld, S. and Lederkremer, G. Z. (2003). Endoplasmic reticulum-associated degradation of mammalian glycoproteins involves sugar chain trimming to Man6-5GlcNAc2. J. Biol. Chem. 278, 34119-34124.
18. Garcia-Mata, R., Gao, Y. and Sztul, E. (2002). Hassles with taking out the garbage: aggravating aggresomes. Traffic 3, 388-396.
19. Halaban, R., Chang, E., Zhang, Y., Moellmann, G., Hanlon, D., Michalak, M., Setaluri, V. and Hebert, D. N. (1997). Aberrant retention of tyrosinase in the endoplasmic reticulum mediates accelerated degradation of the enzyme and contributes to the dedifferentiated phenotype of amelanotic melanoma cells. Proc. Natl. Acad. Sci. USA 94, 6210-6215.
20. Halaban, R., Svedine, S., Cheng, E., Smicun, Y., Aron, R. and Hebert, D. N. (2000). Endoplasmic reticulum retention is a common defect associated with tyrosinase-negative albinism. Proc. Natl. Acad. Sci. USA 97, 5889-5894.
21. Hammond, C., Braakman, I. and Helenius, A. (1994). Role of N-linked oligosaccharides, glucose trimming and calnexin during glycoprotein folding in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 91, 913-917.
22. Hebert, D. N., Foellmer, B. and Helenius, A. (1995). Glucose trimming and reglucosylation determines glycoprotein association with calnexin. Cell 81, 425-433.
23. Hebert, D. N., Foellmer, B. and Helenius, A. (1996). Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes. EMBO J. 15, 2961-2968.
24. Helenius, A. and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291, 2364-2369.
25. Herscovics, A., Romero, P. A. and Tremblay, L. O. (2002). The specificity of the yeast and human class I ER alpha 1,2-mannosidase involved in ER quality control is not as strict as previously reported. Glycobiology 12, 14G-15G.
26. Hosokawa, N., Wada, I., Hasegawa, K., Yorihuzi, T., Tremblay, L. O., Herscovics, A. and Nagata, K. (2001). A novel ER a-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep. 2, 415-422.
27. Hosokawa, N., Tremblay, L. O., You, Z., Herscovics, A., Wada, I. and Nagata, K. (2003). Enhancement of endoplasmic reticulum (ER) degradation of misfolded null Hong Kong alpha1-antitrypsin by human ER mannosidase I. J. Biol. Chem. 278, 26287-26294.
28. Jakob, C. A., Burda, P., Roth, J. and Aebi, M. (1998). Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J. Cell Biol. 142, 1223-1233.
29. Jakob, C. A., Bodmer, D., Spirig, U., Battig, P., Marcil, A., Dignard, D., Bergeron, J. J., Thomas, D. Y. and Aebi, M. (2001). Htm1p, a mannosidase-like protein, is involved in glycoprotein degradation in yeast. EMBO Rep. 2, 423-430.
30. Jensen, T.J., Loo, M. A., Pind, S., Williams, D. B., Goldberg, A. L. and Riordan, J. R. (1995). Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135.
31. Katz, J. and Wals, P. A. (1985). Studies with digitonin-treated rat hepatocytes (nude cells). J. Cell. Biochem. 28, 207-228.
32. Kopito, R. R. and Sitia, R. (2000). Aggresomes and russell bodies. EMBO Rep. 1, 225-231.
33. Lee, D. H. and Goldberg, A. L. (1998). Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 10, 397-403.
34. Lehrman, M. A. (2001). Oligosaccharide-based information in the endoplasmic reticulum quality control and other biological systems. J. Biol. Chem. 276, 8623-8626.
35. Lerner, A. B., Fitzpatrick, T. B., Calkins, E. and Summerson, W. H. (1949). Mammalian tyrosinase: preparation and properties. J. Biol. Chem. 178, 185-195.
36. Liu, Y., Choudhury, P., Cabral, C. M. and Sifers, R. N. (1999). Oligosaccharide modification in the early secretory pathway directs the selection of a misfolded glycoprotein for degradation by the proteasome. J. Biol. Chem. 274, 5861-5867.
37. Lomas, D. A., Evans, D. L., Finch, J. T. and Carrell, R. W. (1992). The mechanisms of Z a1-antitrypsin accumulation in the liver. Nature 357, 605-607.
38. Marcus, N. M. and Perlmutter, D. H. (2000). Glucosidase and mannosidase inhibitors mediate increased secretion of mutant alpha-1 antitrypsin Z. J. Biol. Chem. 275, 1987-1992.
39. McCracken, A. A. and Brodsky, J. L. (1996). Assembly of ER-associated protein degradation in vitro: dependence of cytosol, calnexin and ATP. J. Cell Biol. 132, 291-298.
40. Molinari, M., Galli, C., Piccaluga, V., Pieren, M. and Paganetti, P. (2002). Sequential assistance of molecular chaperones and transient formation of covalent complexes during protein degradation from the ER. J. Cell Biol. 158, 247-257.
41. Molinari, M., Calanca, V., Galli, C., Lucca, P. and Pagnetti, P. (2003). Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299, 1397-1400.
42. Moore, S. E. H. and Spiro, R. G. (1993). Inhibition of glucose trimming by castanospermine results in rapid degradation of unsassembled major hitsocompatibility complex Class I molecules. J. Biol. Chem. 268, 3809-3812.
43. Mosse, C. A., Meadows, L., Luckey, C. J., Kittlesen, D. J., Huczko, E. L., Slingluff, C. L., Shabanowitz, J., Hunt, D. R and Engelhard, V. H. (1998). The class I antigen-processing pathway for the membrane protein tyrosinase involves translation in the endoplasmic reticulum and processing in the cytosol. J. Exp. Med. 187, 37-48.
44. Moussali, M., Pipe, S. W. and Hauri, H. P. (1999). Mannose-dependent endoplasmic reticulum (ER)-Golgi intermediate compartment-53 mediated ER to Golgi trafficking of coagulation factors V and VIII. J. Biol. Chem. 274, 32539-32542.
45. Nakatsukasa, K., Nishikawa, S. I., Hosokawa, N., Nagata, K. and Endo, T. (2001). Mnl1p, an alpha-mannosidase-like protein in yeast Saccharomyces cerevisiae, is required for endoplasmic reticulum-associated degradation of glycoproteins. J. Biol. Chem. 276, 8635-8638.
46. Oberdorf, J. and Skach, W. (2002). In vitro reconstitution of CFTR biogenesis and degradation. Methods. Mol. Med. 70, 295-310.
47. Oda, Y., Hosokawa, N., Wada, I. and Nagata, K. (2003). EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299, 1394-1397.
48. Oetting, W. S. and King, R. A. (1999). Molecular basis of albinism: mutations and polymorphisms of pigmentation genes associated with albinism. Hum. Mutat. 13, 99-115.
49. Ou, W. J., Cameron, P. H., Thomas, D. Y. and Bergeron, J. J. M. (1993). Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature 364, 771-776.
50. Petrescu, S. M., Petrescu, A. J., Titu, H. N., Dwek, R. A. and Platt, F. M. (1997). Inhibition of N-Glycan processing in B 16 melanoma cells results in inactivation of tyrosinase but does not prevent its transport to the melanosome. J. Biol. Chem. 272, 15796-15803.
51. Plemper, R. K. and Wolf, D. H. (1999). Endoplasmic reticulum degradation. Reverse protein transport and its end in the proteasome. Mol. Biol. Rep. 26, 125-130.
52. Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A. and Dwek, R. A. (2001). Glycosylation and the immune system. Science 291, 2370-2376.
53. Rutishauser, J. and Speiss, M. (2002). Endoplasmic reticulum storage disease. Swiss Med. Wkly. 132, 211-222.
54. Sifers, R. N. (1992). Z and the insoluble answer. Nature 357, 541-542.
55. Sousa, M. and Parodi, A. J. (1995). The molecular basis for the recognition of misfolded glycoproteins by the UDP-Glc: glycoprotein glucosyltransferase. EMBO J. 14, 4196-4203.
56. Spiro, R. G. (2000). Glucose residues as key determinants in the biosynthesis and quality control of glycoproteins with N-linked oligosaccharides. J. Biol. Chem. 275, 35657-35660.
57. Tamura, A., Halaban, R., Moellman, G., Cowan, J. M., Lerner, M. R. and Lerner, A. B. (1987). Normal routine melanocytes in culture. In Vitro Cell. Dev. Biol. 23, 519-522.
58. Thomas, P. J., Que, B. H. and Pedersen, P. L. (1995). Defective protein folding as a basis of human disease. Trends Biochem. Sci. 20, 456-459.
59. Tokunaga, F., Brostrom, C., Koide, T. and Arvan, P. (2000). Endoplasmic reticulum (ER)-associated degradation of misfolded N-linked glycoproteins is suppressed upon inhibition of ER mannosidase I. J. Biol. Chem. 275, 40757-40764.
60. Toyofuku, K., Wada, I., Hirosaki, K., Park, J. S., Hori, Y. and Jimbow, K. (1999). Promotion of tyrosinase folding in COS 7 cells by calnexin. J. Biochem. (Tokyo) 125, 82-89.
61. Toyofuku, K., Wada, I., Spritz, R. A. and Hearing, V. J. (2001). The molecular basis of oculocutaneous albinism type 1 (OCA1): sorting failure and degradation of mutant tyrosinases results in a lack of pigmentation. Biochem. J. 355, 259-269.
62. Újvári, A., Aron, R., Eisenhaure, T., Cheng, E., Parag, H. A., Smicun, Y., Halaban, R. and Hebert, D. N. (2001). Translation rate of human tyrosinase determines its N-linked glycosylation level. J. Biol. Chem. 276, 5924-5931.
63. Vassilakos, A., Cohen-Doyle, M. E, Peterson, P. A., Jackson, M. R. and Williams, D. B. (1996). The molecular chaperone calnexin facilitates folding and assembly of class I histocompatibility molecules. EMBO J. 15, 1495-1506.
64. Wang, J. and White, A. L. (2000). Role of calnexin, calreticulin, and endoplasmic reticulum mannosidase I in apolipoprotein (a) intracellular targeting. Biochemistry 39, 8993-9000.
65. Wang, Y. and Androlewicz, M. J. (2000). Oligosaccharide trimming plays a role in the endoplasmic reticulum-associated degradation of tyrosinase. Biochem. Biophys. Res. Commun. 271, 22-27.
66. Ward, C. L., Omura, S. and Kopito, R. R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
67. Wiertz, E. J. H. J., Jones, T. R., Sun, L., Bogyo, M., Geuze, H. J. and Ploegh, H. L. (1996). The human cytomegalovirus US11 gene product dislocated MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779.
68. Wilson, C. M., Farmery, M. R. and Bulleid, N. J. (2000). Pivotal role of calnexin and mannose trimming in regulating the endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain. J. Biol. Chem. 275, 21224-21232.
69. Wilson, R., Allen, A. J., Oliver, J., Brookman, J. L., High, S. and Bulleid, N. J. (1995). The translocation, folding, assembly and redox-dependent degradation of secretory and membrane proteins in semi-permeabilized mammalian cells. Biochem. J. 307, 679-687.
70. Xiong, X., Chong, E. and Skach, W. R. (1999). Evidence that endoplasmic reticulum (ER)-associated degradation of cystic fibrosis transmembrane conductance regulator is linked to retrograde translocation from the ER membrane. J. Biol. Chem. 274, 2616-2624.
71. Yang, M., Omura, S., Bonifacino, J. S. and Weissman, A. M. (1998). Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing, ubiquitination and proteasome-dependent removal from ER membranes. J. Exp. Med. 187, 835-846.