Non-lysosomal degradation pathway for N-linked glycans and dolichol-linked oligosaccharides

Biochemical and Biophysical Research Communications

Volumn 453, Issue 2, 2014, Pages 213-219

  Suzuki, Tadashi ^a   Harada, Yoichiro ^a  

^a RIKEN   (Japan)

Author keywords

Free oligosaccharides; Non lysosomal degradation; Oligosaccharyltransferase; Peptide:N glycanase; Phosphorylated oligosaccharides; Pyrophosphatase

Indexed keywords

ASPARAGINE; DOLICHOL; GLYCAN; GLYCOSYLATED PROTEIN; N GLYCOSYLATED PROTEIN; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; INORGANIC PYROPHOSPHATASE; POLYSACCHARIDE;

CAMPYLOBACTER JEJUNI; DEGLYCOSYLATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GLYCOPROTEIN SYNTHESIS; IN VIVO STUDY; LYSOSOME; MAMMAL CELL; MICROSOME MEMBRANE; NONHUMAN; PROTEIN DEGRADATION; QUALITY CONTROL; REGULATORY MECHANISM; REVIEW; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; ACTIVE TRANSPORT; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CYTOSOL; GLYCOSYLATION; HUMAN; METABOLISM; PROTEIN FOLDING;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CYTOSOL; DOLICHOL; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HUMANS; MODELS, BIOLOGICAL; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEIN FOLDING; PYROPHOSPHATASES;

EID: 84908455205     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2014.05.075     Document Type: Review

References (85)

1. A. Helenius, and M. Aebi Intracellular functions of N-linked glycans Science 291 2001 2364 2369
2. A. Helenius, and M. Aebi Roles of N-linked glycans in the endoplasmic reticulum Annu. Rev. Biochem. 73 2004 1019 1049
3. D.J. Kelleher, and R. Gilmore An evolving view of the eukaryotic oligosaccharyltransferase Glycobiology 16 2006 47R 62R
4. M. Chavan, and W. Lennarz The molecular basis of coupling of translocation and N-glycosylation Trends Biochem. Sci. 31 2006 17 20
5. M. Aebi N-linked protein glycosylation in the ER Biochim. Biophys. Acta 2013 1833 2430 2437
6. A. Varki Biological roles of oligosaccharides: all of the theories are correct Glycobiology 3 1993 97 130
7. T. Suzuki, Q. Yan, and W.J. Lennarz Complex, two-way traffic of molecules across the membrane of the endoplasmic reticulum J. Biol. Chem. 273 1998 10083 10086
8. T. Suzuki, H. Park, K. Kitajima, and W.J. Lennarz Peptides glycosylated in the endoplasmic reticulum of yeast are subsequently deglycosylated by a soluble peptide: N-glycanase activity J. Biol. Chem. 273 1998 21526 21530
9. T. Suzuki, and W.J. Lennarz In yeast the export of small glycopeptides from the endoplasmic reticulum into the cytosol is not affected by the structure of their oligosaccharide chains Glycobiology 10 2000 51 58
10. T. Suzuki, H. Park, N.M. Hollingsworth, R. Sternglanz, and W.J. Lennarz PNG1, a yeast gene encoding a highly conserved peptide:N-glycanase J. Cell Biol. 149 2000 1039 1052
11. H. Park, T. Suzuki, and W.J. Lennarz Identification of proteins that interact with mammalian peptide:N-glycanase and implicate this hydrolase in the proteasome-dependent pathway for protein degradation Proc. Natl. Acad. Sci. U.S.A. 98 2001 11163 11168
12. T. Suzuki, H. Park, M.A. Kwofie, and W.J. Lennarz Rad23 provides a link between the Png1 deglycosylating enzyme and the 26 S proteasome in yeast J. Biol. Chem. 276 2001 21601 21607
13. T. Suzuki, H. Park, E.A. Till, and W.J. Lennarz The PUB domain: a putative protein-protein interaction domain implicated in the ubiquitin-proteasome pathway Biochem. Biophys. Res. Commun. 287 2001 1083 1087
14. S. Katiyar, T. Suzuki, B.J. Balgobin, and W.J. Lennarz Site-directed mutagenesis study of yeast peptide:N-glycanase. Insight into the reaction mechanism of deglycosylation J. Biol. Chem. 277 2002 12953 12959
15. T. Suzuki, H. Park, and W.J. Lennarz Cytoplasmic peptide:N-glycanase (PNGase) in eukaryotic cells: occurrence, primary structure, and potential functions FASEB J. 16 2002 635 641
16. T. Suzuki, and W.J. Lennarz Glycopeptide export from the endoplasmic reticulum into cytosol is mediated by a mechanism distinct from that for export of misfolded glycoprotein Glycobiology 12 2002 803 811
17. T. Suzuki, K. Yano, S. Sugimoto, K. Kitajima, W.J. Lennarz, S. Inoue, Y. Inoue, and Y. Emori Endo-beta-N-acetylglucosaminidase, an enzyme involved in processing of free oligosaccharides in the cytosol Proc. Natl. Acad. Sci. U.S.A. 99 2002 9691 9696
18. T. Suzuki, M.A. Kwofie, and W.J. Lennarz Ngly1, a mouse gene encoding a deglycosylating enzyme implicated in proteasomal degradation: expression, genomic organization, and chromosomal mapping Biochem. Biophys. Res. Commun. 304 2003 326 332
19. T. Suzuki, and W.J. Lennarz Hypothesis: a glycoprotein-degradation complex formed by protein-protein interaction involves cytoplasmic peptide:N-glycanase Biochem. Biophys. Res. Commun. 302 2003 1 5
20. M. Chavan, T. Suzuki, M. Rekowicz, and W. Lennarz Genetic, biochemical, and morphological evidence for the involvement of N-glycosylation in biosynthesis of the cell wall beta1,6-glucan of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U.S.A. 100 2003 15381 15386
21. Y. Harada, H. Li, and W.J. Lennarz Oligosaccharyltransferase directly binds to ribosome at a location near the translocon-binding site Proc. Natl. Acad. Sci. U.S.A. 106 2009 6945 6949
22. Y. Harada, H. Li, J.S. Wall, and W.J. Lennarz Structural studies and the assembly of the heptameric post-translational translocon complex J. Biol. Chem. 286 2011 2956 2965
23. R. Cacan, B. Hoflack, and A. Verbert Fate of oligosaccharide-lipid intermediates synthesized by resting rat-spleen lymphocytes Eur. J. Biochem. 106 1980 473 479
24. J.A. Hanover, and W.J. Lennarz Transmembrane assembly of membrane and secretory glycoproteins Arch. Biochem. Biophys. 211 1981 1 19
25. K.R. Anumula, and R.G. Spiro Release of glucose-containing polymannose oligosaccharides during glycoprotein biosynthesis. Studies with thyroid microsomal enzymes and slices J. Biol. Chem. 258 1983 15274 15282
26. N. Gao, J. Shang, and M.A. Lehrman Analysis of glycosylation in CDG-Ia fibroblasts by fluorophore-assisted carbohydrate electrophoresis: implications for extracellular glucose and intracellular mannose 6-phosphate J. Biol. Chem. 280 2005 17901 17909
27. Y. Harada, R. Buser, E.M. Ngwa, H. Hirayama, M. Aebi, and T. Suzuki Eukaryotic oligosaccharyltransferase generates free oligosaccharides during N-glycosylation J. Biol. Chem. 288 2013 32673 32684
28. H. Nothaft, X. Liu, D.J. McNally, J. Li, and C.M. Szymanski Study of free oligosaccharides derived from the bacterial N-glycosylation pathway Proc. Natl. Acad. Sci. U.S.A. 106 2009 15019 15024
29. I. Chantret, M. Fasseu, K. Zaoui, C. Le Bizec, H.S. Yaye, T. Dupre, and S.E. Moore Identification of roles for peptide: N-glycanase and endo-beta-N-acetylglucosaminidase (Engase1p) during protein N-glycosylation in human HepG2 cells PLoS One 5 2010 e11734
30. H. Hirayama, J. Seino, T. Kitajima, Y. Jigami, and T. Suzuki Free oligosaccharides to monitor glycoprotein endoplasmic reticulum-associated degradation in Saccharomyces cerevisiae J. Biol. Chem. 285 2010 12390 12404
31. S.E. Moore Oligosaccharide transport: pumping waste from the ER into lysosomes Trends Cell Biol. 9 1999 441 446
32. S.E. Moore, and R.G. Spiro Intracellular compartmentalization and degradation of free polymannose oligosaccharides released during glycoprotein biosynthesis J. Biol. Chem. 269 1994 12715 12721
33. S.E. Moore, C. Bauvy, and P. Codogno Endoplasmic reticulum-to-cytosol transport of free polymannose oligosaccharides in permeabilized HepG2 cells EMBO J. 14 1995 6034 6042
34. S.E. Moore Transport of free polymannose-type oligosaccharides from the endoplasmic reticulum into the cytosol is inhibited by mannosides and requires a thapsigargin-sensitive calcium store Glycobiology 8 1998 373 381
35. Y. Haga, K. Totani, Y. Ito, and T. Suzuki Establishment of a real-time analytical method for free oligosaccharide transport from the ER to the cytosol Glycobiology 19 2009 987 994
36. D. Kmiecik, V. Herman, C.J. Stroop, J.C. Michalski, A.M. Mir, O. Labiau, A. Verbert, and R. Cacan Catabolism of glycan moieties of lipid intermediates leads to a single Man5GlcNAc oligosaccharide isomer: a study with permeabilized CHO cells Glycobiology 5 1995 483 494
37. D. Peric, C. Durrant-Arico, C. Delenda, T. Dupre, P. De Lonlay, H.O. de Baulny, C. Pelatan, B. Bader-Meunier, O. Danos, I. Chantret, and S.E. Moore The compartmentalisation of phosphorylated free oligosaccharides in cells from a CDG Ig patient reveals a novel ER-to-cytosol translocation process PLoS One 5 2010 e11675
38. W. Vleugels, S. Duvet, R. Peanne, A.M. Mir, R. Cacan, J.C. Michalski, G. Matthijs, and F. Foulquier Identification of phosphorylated oligosaccharides in cells of patients with a congenital disorders of glycosylation (CDG-I) Biochimie 93 2011 823 833
39. M. Belard, R. Cacan, and A. Verbert Characterization of an oligosaccharide-pyrophosphodolichol pyrophosphatase activity in yeast Biochem. J. 255 1988 235 242
40. Y. Harada, K. Nakajima, Y. Masahara-Negishi, H.H. Freeze, T. Angata, N. Taniguchi, and T. Suzuki Metabolically programmed quality control system for dolichol-linked oligosaccharides Proc. Natl. Acad. Sci. U.S.A. 110 2013 19366 19371
41. C. Thiel, M. Schwarz, J. Peng, M. Grzmil, M. Hasilik, T. Braulke, A. Kohlschutter, K. von Figura, L. Lehle, and C. Korner A new type of congenital disorders of glycosylation (CDG-Ii) provides new insights into the early steps of dolichol-linked oligosaccharide biosynthesis J. Biol. Chem. 278 2003 22498 22505
42. M.K. O'Reilly, G. Zhang, and B. Imperiali In vitro evidence for the dual function of Alg2 and Alg11: essential mannosyltransferases in N-linked glycoprotein biosynthesis Biochemistry 45 2006 9593 9603
43. M. Kampf, B. Absmanner, M. Schwarz, and L. Lehle Biochemical characterization and membrane topology of Alg2 from Saccharomyces cerevisiae as a bifunctional alpha1,3- and 1,6-mannosyltransferase involved in lipid-linked oligosaccharide biosynthesis J. Biol. Chem. 284 2009 11900 11912
44. P.G. Needham, and J.L. Brodsky How early studies on secreted and membrane protein quality control gave rise to the ER associated degradation (ERAD) pathway: the early history of ERAD Biochim. Biophys. Acta 2013 1833 2447 2457
45. J. Merulla, E. Fasana, T. Solda, and M. Molinari Specificity and regulation of the endoplasmic reticulum-associated degradation machinery Traffic 14 2013 767 777
46. G. Thibault, and D.T. Ng The endoplasmic reticulum-associated degradation pathways of budding yeast Cold Spring Harb. Perspect. Biol. 4 2012
47. C.M. Cabral, Y. Liu, and R.N. Sifers Dissecting glycoprotein quality control in the secretory pathway Trends Biochem. Sci. 26 2001 619 624
48. J.J. Caramelo, and A.J. Parodi Getting in and out from calnexin/calreticulin cycles J. Biol. Chem. 283 2008 10221 10225
49. G.Z. Lederkremer Glycoprotein folding, quality control and ER-associated degradation Curr. Opin. Struct. Biol. 19 2009 515 523
50. M. Aebi, R. Bernasconi, S. Clerc, and M. Molinari N-glycan structures: recognition and processing in the ER Trends Biochem. Sci. 35 2010 74 82
51. N. Hosokawa, Y. Kamiya, and K. Kato The role of MRH domain-containing lectins in ERAD Glycobiology 20 2010 651 660
52. M.H. Smith, H.L. Ploegh, and J.S. Weissman Road to ruin: targeting proteins for degradation in the endoplasmic reticulum Science 334 2011 1086 1090
53. T. Suzuki, and Y. Funakoshi Free N-linked oligosaccharide chains: formation and degradation Glycoconj. J. 23 2006 291 302
54. T. Suzuki Cytoplasmic peptide:N-glycanase and catabolic pathway for free N-glycans in the cytosol Semin. Cell Dev. Biol. 18 2007 762 769
55. T. Suzuki Introduction to "Glycometabolome" Trends Glycosci. Glyc. 21 2009 219 227
56. A.C. Need, V. Shashi, Y. Hitomi, K. Schoch, K.V. Shianna, M.T. McDonald, M.H. Meisler, and D.B. Goldstein Clinical application of exome sequencing in undiagnosed genetic conditions J. Med. Genet. 49 2012 353 361
57. G.M. Enns, V. Shashi, M. Bainbridge, M.J. Gambello, F.R. Zahir, T. Bast, R. Crimian, K. Schoch, J. Platt, R. Cox, J.A. Bernstein, M. Scavina, R.S. Walter, A. Bibb, M. Jones, M. Hegde, B.H. Graham, A.C. Need, A. Oviedo, C.P. Schaaf, S. Boyle, A.J. Butte, R. Chen, M.J. Clark, R. Haraksingh, T.M. Cowan, P. He, S. Langlois, H.Y. Zoghbi, M. Snyder, R.A. Gibbs, H.H. Freeze, and D.B. Goldstein Mutations in NGLY1 cause an inherited disorder of the endoplasmic reticulum-associated degradation pathway Genet. Med. 2014 10.1038/gim.2014.22
58. T. Kato, K. Fujita, M. Takeuchi, K. Kobayashi, S. Natsuka, K. Ikura, H. Kumagai, and K. Yamamoto Identification of an endo-beta-N-acetylglucosaminidase gene in Caenorhabditis elegans and its expression in Escherichia coli Glycobiology 12 2002 581 587
59. T. Kato, K. Kitamura, M. Maeda, Y. Kimura, T. Katayama, H. Ashida, and K. Yamamoto Free oligosaccharides in the cytosol of Caenorhabditis elegans are generated through endoplasmic reticulum-golgi trafficking J. Biol. Chem. 282 2007 22080 22088
60. R.J. Chalkley, A. Thalhammer, R. Schoepfer, and A.L. Burlingame Identification of protein O-GlcNAcylation sites using electron transfer dissociation mass spectrometry on native peptides Proc. Natl. Acad. Sci. U.S.A. 106 2009 8894 8899
61. J.C. Trinidad, D.T. Barkan, B.F. Gulledge, A. Thalhammer, A. Sali, R. Schoepfer, and A.L. Burlingame Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse Mol. Cell. Proteomics 11 2012 215 229
62. J.C. Trinidad, R. Schoepfer, A.L. Burlingame, and K.F. Medzihradszky N- and O-glycosylation in the murine synaptosome Mol. Cell. Proteomics 12 2013 3474 3488
63. Y.C. Kim, N. Jahren, M.D. Stone, N.D. Udeshi, T.W. Markowski, B.A. Witthuhn, J. Shabanowitz, D.F. Hunt, and N.E. Olszewski Identification and origin of N-linked beta-D-N-acetylglucosamine monosaccharide modifications on Arabidopsis proteins Plant Physiol. 161 2013 455 464
64. I. Chantret, J.P. Frenoy, and S.E. Moore Free-oligosaccharide control in the yeast Saccharomyces cerevisiae: roles for peptide:N-glycanase (Png1p) and vacuolar mannosidase (Ams1p) Biochem. J. 373 2003 901 908
65. H. Hirayama, and T. Suzuki Metabolism of free oligosaccharides is facilitated in the och1Delta mutant of Saccharomyces cerevisiae Glycobiology 21 2011 1341 1348
66. I. Chantret, V.P. Kodali, C. Lahmouich, D.J. Harvey, and S.E. Moore Endoplasmic reticulum-associated degradation (ERAD) and free oligosaccharide generation in Saccharomyces cerevisiae J. Biol. Chem. 286 2011 41786 41800
67. T. Suzuki, I. Hara, M. Nakano, M. Shigeta, T. Nakagawa, A. Kondo, Y. Funakoshi, and N. Taniguchi Man2C1, an alpha-mannosidase, is involved in the trimming of free oligosaccharides in the cytosol Biochem. J. 400 2006 33 41
68. E. Costanzi, C. Balducci, R. Cacan, S. Duvet, A. Orlacchio, and T. Beccari Cloning and expression of mouse cytosolic alpha-mannosidase (Man2c1) Biochim. Biophys. Acta 1760 2006 1580 1586
69. E. Kuokkanen, W. Smith, M. Makinen, H. Tuominen, M. Puhka, E. Jokitalo, S. Duvet, T. Berg, and P. Heikinheimo Characterization and subcellular localization of human neutral class II alpha-mannosidase [corrected] Glycobiology 17 2007 1084 1093
70. T.D. Butters, D.S. Alonzi, N.V. Kukushkin, Y. Ren, and Y. Bleriot Novel mannosidase inhibitors probe glycoprotein degradation pathways in cells Glycoconj. J. 26 2009 1109 1116
71. C. Bernon, Y. Carre, E. Kuokkanen, M.C. Slomianny, A.M. Mir, F. Krzewinski, R. Cacan, P. Heikinheimo, W. Morelle, J.C. Michalski, F. Foulquier, and S. Duvet Overexpression of Man2C1 leads to protein underglycosylation and upregulation of endoplasmic reticulum-associated degradation pathway Glycobiology 21 2011 363 375
72. A. Kato, L. Wang, K. Ishii, J. Seino, N. Asano, and T. Suzuki Calystegine B3 as a specific inhibitor for cytoplasmic alpha-mannosidase, Man2C1 J. Biochem. 149 2011 415 422
73. L. Wang, and T. Suzuki Dual functions for cytosolic alpha-mannosidase (Man2C1): its down-regulation causes mitochondria-dependent apoptosis independently of its alpha-mannosidase activity J. Biol. Chem. 288 2013 11887 11896
74. S. Paciotti, E. Persichetti, K. Klein, A. Tasegian, S. Duvet, D. Hartmann, V. Gieselmann, and T. Beccari Accumulation of free oligosaccharides and tissue damage in cytosolic alpha-mannosidase (Man2c1)-deficient mice J. Biol. Chem. 289 2014 9611 9622
75. H. Oku, and S. Hase Studies on the substrate specificity of neutral alpha-mannosidase purified from Japanese quail oviduct by using sugar chains from glycoproteins J. Biochem. 110 1991 982 989
76. T. Grard, A. Saint-Pol, J.F. Haeuw, C. Alonso, J.M. Wieruszeski, G. Strecker, and J.C. Michalski Soluble forms of alpha-D-mannosidases from rat liver. Separation and characterization of two enzymic forms with different substrate specificities Eur. J. Biochem. 223 1994 99 106
77. M. Kumano, K. Omichi, and S. Hase Substrate specificity of bovine liver cytosolic neutral alpha-mannosidase activated by Co2+ J. Biochem. 119 1996 991 997
78. A. Saint-Pol, C. Bauvy, P. Codogno, and S.E. Moore Transfer of free polymannose-type oligosaccharides from the cytosol to lysosomes in cultured human hepatocellular carcinoma HepG2 cells J. Cell Biol. 136 1997 45 59
79. A. Saint-Pol, P. Codogno, and S.E. Moore Cytosol-to-lysosome transport of free polymannose-type oligosaccharides. Kinetic and specificity studies using rat liver lysosomes J. Biol. Chem. 274 1999 13547 13555
80. J. Seino, L. Wang, Y. Harada, C. Huang, K. Ishii, N. Mizushima, and T. Suzuki Basal autophagy is required for the efficient catabolism of sialyloligosaccharides J. Biol. Chem. 288 2013 26898 26907
81. J.F. Haeuw, J.C. Michalski, G. Strecker, G. Spik, and J. Montreuil Cytosolic glycosidases: do they exist? Glycobiology 1 1991 487 492
82. Y. Funakoshi, and T. Suzuki Glycobiology in the cytosol: the bitter side of a sweet world Biochim. Biophys. Acta 1790 2009 81 94
83. T. Suzuki, K. Kitajima, S. Inoue, and Y. Inoue Occurrence and biological roles of 'proximal glycanases' in animal cells Glycobiology 4 1994 777 789
84. T. Suzuki, K. Kitajima, S. Inoue, and Y. Inoue N-glycosylation/deglycosylation as a mechanism for the post-translational modification/remodification of proteins Glycoconj. J. 12 1995 183 193
85. R. Cacan, S. Duvet, D. Kmiecik, O. Labiau, A.M. Mir, and A. Verbert 'Glyco-deglyco' processes during the synthesis of N-glycoproteins Biochimie 80 1998 59 68