Vertebrate protein glycosylation: Diversity, synthesis and function

Nature Reviews Molecular Cell Biology

Volumn 13, Issue 7, 2012, Pages 448-462

  Moremen, Kelley W ^a   Tiemeyer, Michael ^a   Nairn, Alison V ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CATABOLISM; CELL MIGRATION; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS; QUALITY CONTROL; REVIEW; VERTEBRATE;

ANIMALS; CELL MEMBRANE; CYTOSOL; ENDOPLASMIC RETICULUM; GLYCOPROTEINS; GLYCOSYLATION; GOLGI APPARATUS; HUMANS; METABOLISM; MODELS, BIOLOGICAL; POLYSACCHARIDES; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS;

EID: 84862728161     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3383     Document Type: Review

References (158)

1. Varki, A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3, 97-130 (1993). (Pubitemid 23132602)
2. Haltiwanger, R. S. & Lowe, J. B. Role of glycosylation in development. Annu. Rev. Biochem. 73, 491-537 (2004). (Pubitemid 39050378)
3. Dennis, J. W., Lau, K. S., Demetriou, M. & Nabi, I. R. Adaptive regulation at the cell surface by N-glycosylation. Traffic 10, 1569-1578 (2009).
4. Hoseki, J., Ushioda, R. & Nagata, K. Mechanism and components of endoplasmic reticulum-associated degradation. J. Biochem. 147, 19-25 (2010).
5. Kollmann, K. et al. Mannose phosphorylation in health and disease. Eur. J. Cell Biol. 89, 117-123 (2010).
6. Hart, G. W., Slawson, C., Ramirez-Correa, G. & Lagerlof, O. Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825-858 (2011).
7. Cummings, R. D. The repertoire of glycan determinants in the human glycome. Mol. Biosyst. 5, 1087-1104 (2009).
8. Rothman, J. E. & Fine, R. E. Coated vesicles transport newly synthesized membrane glycoproteins from endoplasmic reticulum to plasma membrane in two successive stages. Proc. Natl Acad. Sci. USA 77, 780-784 (1980). (Pubitemid 10108384)
9. Roth, J. Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. Chem. Rev. 102, 285-303 (2002). (Pubitemid 35381634)
10. Peanne, R. et al. Differential effects of lobe A and lobe B of the Conserved Oligomeric Golgi complex on the stability of β1,4- galactosyltransferase 1 and α2,6-sialyltransferase 1. Glycobiology 21, 864-876 (2011).
11. Nairn, A. V. & Moremen, K. W. in Handbook of Glycomics (eds Cummings, R. & Pierce, J.M.) 95-136 (Academic Press, 2009).
12. Nairn, A. V. et al. Regulation of glycan structures in animal tissues: transcript profiling of glycan-related genes. J. Biol. Chem. 283, 17298-17313 (2008).
13. Spiro, R. G. Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R-56R (2002). (Pubitemid 34760066)
14. Schachter, H. The joys of HexNAc. The synthesis and function of N-and O-glycan branches. Glycoconj. J. 17, 465-483 (2000). (Pubitemid 32480339)
15. Schachter, H. The 'yellow brick road' to branched complex N-glycans. Glycobiology 1, 453-461 (1991).
16. Zaia, J. Mass spectrometry and glycomics. Omics: J. Integrative Biol. 14, 401-418 (2010).
17. Apweiler, R., Hermjakob, H. & Sharon, N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8 (1999).
18. Kornfeld, R. & Kornfeld, S. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54, 631-664 (1985). (Pubitemid 15073660)
19. Lizak, C., Gerber, S., Numao, S., Aebi, M. & Locher, K. P. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474, 350-355 (2011).
20. Kelleher, D. J. & Gilmore, R. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16, 47R-62R (2006).
21. Zielinska, D. F., Gnad, F., Wisniewski, J. R. & Mann, M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907 (2010).
22. Schreiner, R., Schnabel, E. & Wieland, F. Novel N-glycosylation in eukaryotes: laminin contains the linkage unit β-glucosylasparagine. J. Cell Biol. 124, 1071-1081 (1994).
23. Valliere-Douglass, J. F. et al. Glutamine-linked and non-consensus asparagine-linked oligosaccharides present in human recombinant antibodies define novel protein glycosylation motifs. J. Biol. Chem. 285, 16012-16022 (2010).
24. Kelleher, D. J., Karaoglu, D., Mandon, E. C. & Gilmore, R. Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell 12, 101-111 (2003). (Pubitemid 36945039)
25. Imperiali, B. & Hendrickson, T. L. Asparagine-linked glycosylation: specificity and function of oligosaccharyl transferase. Bioorg. Med. Chem. 3, 1565-1578 (1995). (Pubitemid 26022435)
26. Larkin, A. & Imperiali, B. The expanding horizons of asparagine-linked glycosylation. Biochemistry 50, 4411-4426 (2011).
27. Schwarz, F. & Aebi, M. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol. 21, 576-582 (2011).
28. Weerapana, E. & Imperiali, B. Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16, 91R-101R (2006). (Pubitemid 43779042)
29. Mohorko, E., Glockshuber, R. & Aebi, M. Oligosaccharyltransferase: the central enzyme of N-linked protein glycosylation. J. Inherit. Metab. Dis. 34, 869-878 (2011).
30. Helenius, A. & Aebi, M. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049 (2004). (Pubitemid 39050393)
31. Lederkremer, G. Z. Glycoprotein folding, quality control and ER-associated degradation. Curr. Opin. Struct. Biol. 19, 515-523 (2009).
32. D'Alessio, C., Caramelo, J. J. & Parodi, A. J. UDP-GlC:glycoprotein glucosyltransferase-glucosidase II, the ying-yang of the ER quality control. Semin. Cell Dev. Biol. 21, 491-499 (2010).
33. Clerc, S. et al. Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J. Cell Biol. 184, 159-172 (2009).
34. Gauss, R., Kanehara, K., Carvalho, P., Ng, D. T. & Aebi, M. A complex of pdi1p and the mannosidase htm1p initiates clearance of unfolded glycoproteins from the endoplasmic reticulum. Mol. Cell 42, 782-793 (2011).
35. Mast, S. W. & Moremen, K. W. Family 47 α-mannosidases in N-glycan processing. Methods Enzymol. 415, 31-46 (2006).
36. Moremen, K. W. & Molinari, M. N-linked glycan recognition and processing: the molecular basis of endoplasmic reticulum quality control. Curr. Opin. Struct. Biol. 16, 592-599 (2006). (Pubitemid 44472609)
37. Aebi, M., Bernasconi, R., Clerc, S. & Molinari, M. N-glycan structures: recognition and processing in the ER. Trends Biochem. Sci. 35, 74-82 (2010).
38. Xie, W., Kanehara, K., Sayeed, A. & Ng, D. T. Intrinsic conformational determinants signal protein misfolding to the Hrd1/Htm1 endoplasmic reticulum-associated degradation system. Mol. Biol. Cell 20, 3317-3329 (2009).
39. Kanehara, K., Xie, W. & Ng, D. T. Modularity of the Hrd1 ERAD complex underlies its diverse client range. J. Cell Biol. 188, 707-716 (2010).
40. An, H. J. et al. Extensive determination of glycan heterogeneity reveals an unusual abundance of high mannose glycans in enriched plasma membranes of human embryonic stem cells. Mol. Cell. Proteomics 11, M111.010660 (2012).
41. Rabouille, C. et al. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108, 1617-1627 (1995).
42. Stanley, P. Golgi glycosylation. Cold Spring Harb. Perspect. Biol. 3, a005199 (2011).
43. Mogelsvang, S., Marsh, B. J., Ladinsky, M. S. & Howell, K. E. Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5, 338-345 (2004). (Pubitemid 38660200)
44. Papanikou, E. & Glick, B. S. The yeast Golgi apparatus: insights and mysteries. FEBS Lett. 583, 3746-3751 (2009).
45. Ripoche, J., Link, B., Yucel, J. K., Tokuyasu, K. & Malhotra, V. Location of Golgi membranes with reference to dividing nuclei in syncytial Drosophila embryos. Proc. Natl Acad. Sci. USA 91, 1878-1882 (1994). (Pubitemid 24080309)
46. Velasco, A. et al. Cell type-dependent variations in the subcellular distribution of α-mannosidase I and II. J. Cell Biol. 122, 39-51 (1993). (Pubitemid 23188797)
47. Nilsson, T. et al. Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells. J. Cell Biol. 120, 5-13 (1993). (Pubitemid 23014061)
48. Chou, C. F. & Omary, M. B. Mitotic arrest with anti-microtubule agents or okadaic acid is associated with increased glycoprotein terminal GlcNAc's. J. Cell Sci. 107, 1833-1843 (1994). (Pubitemid 24226434)
49. Haltiwanger, R. S. & Philipsberg, G. A. Mitotic arrest with nocodazole induces selective changes in the level of O-linked N-acetylglucosamine and accumulation of incompletely processed N-glycans on proteins from HT29 cells. J. Biol. Chem. 272, 8752-8758 (1997). (Pubitemid 27147845)
50. Klausner, R. D., Donaldson, J. G. & Lippincott-Schwartz, J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071-1080 (1992).
51. Peyroche, A. et al. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol. Cell 3, 275-285 (1999). (Pubitemid 29290668)
52. Rogalski, A. A., Bergmann, J. E. & Singer, S. J. Effect of microtubule assembly status on the intracellular processing and surface expression of an integral protein of the plasma membrane. J. Cell Biol. 99, 1101-1109 (1984). (Pubitemid 14043368)
53. Sampath, D., Varki, A. & Freeze, H. H. The spectrum of incomplete N-linked oligosaccharides synthesized by endothelial cells in the presence of brefeldin A. J. Biol. Chem. 267, 4440-4455 (1992).
54. Balch, W. E., Dunphy, W. G., Braell, W. A. & Rothman, J. E. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell 39, 405-416 (1984). (Pubitemid 15191223)
55. Glick, B. S. & Luini, A. Models for Golgi traffic: a critical assessment. Cold Spring Harb. Perspect. Biol. 3, a005215 (2011).
56. Goud, B. & Gleeson, P. A. TGN golgins, Rabs and cytoskeleton: regulating the Golgi trafficking highways. Trends Cell Biol. 20, 329-336 (2010).
57. Jackson, C. L. Mechanisms of transport through the Golgi complex. J. Cell Sci. 122, 443-452 (2009).
58. Jamieson, J. D. & Palade, G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. 3. Dissociation of intracellular transport from protein synthesis. J. Cell Biol. 39, 580-588 (1968).
59. Kartberg, F., Elsner, M., Froderberg, L., Asp, L. & Nilsson, T. Commuting between Golgi cisternae-mind the GAP! Biochim. Biophys. Acta 1744, 351-363 (2005). (Pubitemid 40848253)
60. Marchi, F. & Leblond, C. P. Radioautographic characterization of successive compartments along the rough endoplasmic reticulum-Golgi pathway of collagen precursors in foot pad fibroblasts of [3H] proline-injected rats. J. Cell Biol. 98, 1705-1709 (1984). (Pubitemid 14102596)
61. Reynders, E., Foulquier, F., Annaert, W. & Matthijs, G. How Golgi glycosylation meets and needs trafficking: the case of the COG complex. Glycobiology 21, 853-863 (2011).
62. Munro, S. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14, 4695-4704 (1995).
63. Patterson, G. H. et al. Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133, 1055-1067 (2008). (Pubitemid 351795609)
64. Sharpe, H. J., Stevens, T. J. & Munro, S. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158-169 (2010).
65. Schmitz, K. R. et al. Golgi localization of glycosyltransferases requires a Vps74p oligomer. Dev. Cell 14, 523-534 (2008). (Pubitemid 351479939)
66. Tu, L., Tai, W. C., Chen, L. & Banfield, D. K. Signal-mediated dynamic retention of glycosyltransferases in the Golgi. Science 321, 404-407 (2008). (Pubitemid 352029976)
67. Aoki, D., Lee, N., Yamaguchi, N., Dubois, C. & Fukuda, M. N. Golgi retention of a trans-Golgi membrane protein, galactosyltransferase, requires cysteine and histidine residues within the membrane-anchoring domain. Proc. Natl Acad. Sci. USA 89, 4319-4323 (1992).
68. Colley, K. J. Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 7, 1-13 (1997). (Pubitemid 27091315)
69. Colley, K. J., Lee, E. U. & Paulson, J. C. The signal anchor and stem regions of the β-galactoside α2,6-sialyltransferase may each act to localize the enzyme to the Golgi apparatus. J. Biol. Chem. 267, 7784-7793 (1992).
70. Fenteany, F. H. & Colley, K. J. Multiple signals are required for α2,6-sialyltransferase (ST6Gal I) oligomerization and Golgi localization. J. Biol. Chem. 280, 5423-5429 (2005). (Pubitemid 40280017)
71. Nilsson, T., Lucocq, J. M., Mackay, D. & Warren, G. The membrane spanning domain of β-1,4-galactosyltransferase specifies trans Golgi localization. EMBO J. 10, 3567-3575 (1991). (Pubitemid 21905382)
72. Nilsson, T., Rabouille, C., Hui, N., Watson, R. & Warren, G. The role of the membrane-spanning domain and stalk region of N- acetylglucosaminyltransferase I in retention, kin recognition and structural maintenance of the Golgi apparatus in HeLa cells. J. Cell Sci. 109, 1975-1989 (1996). (Pubitemid 26248643)
73. Banfield, D. K. Mechanisms of protein retention in the Golgi. Cold Spring Harb. Perspect. Biol. 3, a005264 (2011).
74. Tu, L. & Banfield, D. K. Localization of Golgi-resident glycosyltransferases. Cell. Mol. Life Sci. 67, 29-41 (2010).
75. Nilsson, T., Slusarewicz, P., Hoe, M. H. & Warren, G. Kin recognition. A model for the retention of Golgi enzymes. FEBS Lett. 330, 1-4 (1993). (Pubitemid 23263028)
76. Hassinen, A., Rivinoja, A., Kauppila, A. & Kellokumpu, S. Golgi N-glycosyltransferases form both homo-and heterodimeric enzyme complexes in live cells. J. Biol. Chem. 285, 17771-17777 (2010).
77. Daniotti, J. L., Martina, J. A., Giraudo, C. G., Zurita, A. R. & Maccioni, H. J. GM3 α2,8-sialyltransferase (GD3 synthase): protein characterization and sub-golgi location in CHO-K1 cells. J. Neurochem. 74, 1711-1720 (2000). (Pubitemid 30163994)
78. Giraudo, C. G. & Maccioni, H. J. Ganglioside glycosyltransferases organize in distinct multienzyme complexes in CHO-K1 cells. J. Biol. Chem. 278, 40262-40271 (2003). (Pubitemid 37248594)
79. Yano, H. et al. Distinct functional units of the Golgi complex in Drosophila cells. Proc. Natl Acad. Sci. USA 102, 13467-13472 (2005). (Pubitemid 41420871)
80. Freeze, H. H. Congenital disorders of glycosylation: CDG-I, CDG-II, and beyond. Curr. Mol. Med. 7, 389-396 (2007). (Pubitemid 46979703)
81. Foulquier, F. COG defects, birth and rise! Biochim. Biophys. Acta 1792, 896-902 (2009).
82. Pokrovskaya, I. D. et al. Conserved oligomeric Golgi complex specifically regulates the maintenance of Golgi glycosylation machinery. Glycobiology 21, 1554-1569 (2011).
83. Smith, R. D. & Lupashin, V. V. Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr. Res. 343, 2024-2031 (2008).
84. Wu, X. et al. Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder. Nature Med. 10, 518-523 (2004). (Pubitemid 38667911)
85. Oka, T., Ungar, D., Hughson, F. M. & Krieger, M. The COG and COPI complexes interact to control the abundance of GEARs, a subset of Golgi integral membrane proteins. Mol. Biol. Cell 15, 2423-2435 (2004). (Pubitemid 38580657)
86. Gill, D. J., Chia, J., Senewiratne, J. & Bard, F. Regulation of O-glycosylation through Golgi-to-ER relocation of initiation enzymes. J. Cell Biol. 189, 843-858 (2010).
87. Baas, S. et al. Sugar-free frosting, a homolog of SAD kinase, drives neural-specific glycan expression in the Drosophila embryo. Development 138, 553-563 (2011).
88. Farhan, H. et al. MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189, 997-1011 (2010).
89. Lowe, M. et al. Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis. Cell 94, 783-793 (1998). (Pubitemid 28436010)
90. Muniz, M., Alonso, M., Hidalgo, J. & Velasco, A. A regulatory role for cAMP-dependent protein kinase in protein traffic along the exocytic route. J. Biol. Chem. 271, 30935-30941 (1996). (Pubitemid 26404120)
91. Colley, K. J. Structural basis for the polysialylation of the neural cell adhesion molecule. Adv. Exp. Med. Biol. 663, 111-126 (2010).
92. Rana, N. A. & Haltiwanger, R. S. Fringe benefits: functional and structural impacts of O-glycosylation on the extracellular domain of Notch receptors. Curr. Opin. Struct. Biol. 21, 583-589 (2011).
93. Hanisch, F. G. & Breloy, I. Protein-specific glycosylation: signal patches and cis-controlling peptidic elements. Biol. Chem. 390, 619-626 (2009).
94. Luther, K. B. & Haltiwanger, R. S. Role of unusual O-glycans in intercellular signaling. Int. J. Biochem. Cell Biol. 41, 1011-1024 (2009).
95. Muntoni, F., Torelli, S., Wells, D. J. & Brown, S. C. Muscular dystrophies due to glycosylation defects: diagnosis and therapeutic strategies. Curr. Opin. Neurol. 24, 437-442 (2011).
96. Stanley, P. & Okajima, T. Roles of glycosylation in Notch signaling. Curr. Top. Dev. Biol. 92, 131-164 (2010).
97. Wopereis, S., Lefeber, D. J., Morava, E. & Wevers, R. A. Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects: a review. Clin. Chem. 52, 574-600 (2006).
98. Sakaidani, Y. et al. O-linked-N-acetylglucosamine modification of mammalian Notch receptors by an atypical O-GlcNAc transferase Eogt1. Biochem. Biophys. Res. Commun. 419, 14-19 (2012).
99. Shao, L., Moloney, D. J. & Haltiwanger, R. Fringe modifies O-fucose on mouse Notch1 at epidermal growth factor-like repeats within the ligand-binding site and the Abruptex region. J. Biol. Chem. 278, 7775-7782 (2003). (Pubitemid 36800510)
100. Wang, Y. et al. Modification of epidermal growth factor-like repeats with O-fucose. Molecular cloning and expression of a novel GDP-fucose protein O-fucosyltransferase. J. Biol. Chem. 276, 40338-40345 (2001).
101. Okajima, T. & Irvine, K. D. Regulation of Notch signaling by O-linked fucose. Cell 111, 893-904 (2002). (Pubitemid 36109160)
102. Shi, S. & Stanley, P. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc. Natl Acad. Sci. USA 100, 5234-5239 (2003). (Pubitemid 36542688)
103. Yao, D. et al. Protein O-fucosyltransferase 1 (Pofut1) regulates lymphoid and myeloid homeostasis through modulation of Notch receptor ligand interactions. Blood 117, 5652-5662 (2011).
104. Acar, M. et al. Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132, 247-258 (2008). (Pubitemid 351172433)
105. Sethi, M. K. et al. Identification of glycosyltransferase 8 family members as xylosyltransferases acting on O-glucosylated notch epidermal growth factor repeats. J. Biol. Chem. 285, 1582-1586 (2010).
106. Sethi, M. K. et al. Molecular cloning of a xylosyltransferase that transfers the second xylose to O-glucosylated epidermal growth factor repeats of notch. J. Biol. Chem. 287, 2739-2748 (2012).
107. Rana, N. A. et al. O-Glucose trisaccharide is present at high but variable stoichiometry at multiple sites on mouse Notch1. J. Biol. Chem. 286, 31623-31637 (2011).
108. Fernandez-Valdivia, R. et al. Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development 138, 1925-1934 (2011).
109. Sakaidani, Y. et al. O-linked-N-acetylglucosamine on extracellular protein domains mediates epithelial cell-matrix interactions. Nature Commun. 2, 583 (2011).
110. Matsuura, A. et al. O-linked N-acetylglucosamine is present on the extracellular domain of notch receptors. J. Biol. Chem. 283, 35486-35495 (2008).
111. Hofsteenge, J. et al. C-mannosylation and O-fucosylation of the thrombospondin type 1 module. J. Biol. Chem. 276, 6485-6498 (2001).
112. Luo, Y., Koles, K., Vorndam, W., Haltiwanger, R. S. & Panin, V. M. Protein O-fucosyltransferase 2 adds O-fucose to thrombospondin type 1 repeats. J. Biol. Chem. 281, 9393-9399 (2006). (Pubitemid 43864655)
113. Martinez-Duncker, I., Mollicone, R., Candelier, J. J., Breton, C. & Oriol, R. A new superfamily of protein-O-fucosyltransferases, α2-fucosyltransferases, and α6-fucosyltransferases: phylogeny and identification of conserved peptide motifs. Glycobiology 13, 1C-5C (2003). (Pubitemid 37508892)
114. Kozma, K. et al. Identification and characterization of a β1,3-glucosyltransferase that synthesizes the Glc-β1,3-Fuc disaccharide on thrombospondin type 1 repeats. J. Biol. Chem. 281, 36742-36751 (2006). (Pubitemid 46042141)
115. Sato, T. et al. Molecular cloning and characterization of a novel human β1,3-glucosyltransferase, which is localized at the endoplasmic reticulum and glucosylates O-linked fucosylglycan on thrombospondin type 1 repeat domain. Glycobiology 16, 1194-1206 (2006). (Pubitemid 44811583)
116. Ricketts, L. M., Dlugosz, M., Luther, K. B., Haltiwanger, R. S. & Majerus, E. M. O-fucosylation is required for ADAMTS13 secretion. J. Biol. Chem. 282, 17014-17023 (2007). (Pubitemid 47093216)
117. Du, J. et al. O-fucosylation of thrombospondin type 1 repeats restricts epithelial to mesenchymal transition (EMT) and maintains epiblast pluripotency during mouse gastrulation. Dev. Biol. 346, 25-38 (2010).
118. Doucey, M. A., Hess, D., Cacan, R. & Hofsteenge, J. Protein C-mannosylation is enzyme-catalysed and uses dolichyl-phosphate-mannose as a precursor. Mol. Biol. Cell 9, 291-300 (1998). (Pubitemid 28084125)
119. Krieg, J. et al. Recognition signal for C-mannosylation of Trp-7 in RNase 2 consists of sequence Trp-x-x-Trp. Mol. Biol. Cell 9, 301-309 (1998). (Pubitemid 28084126)
120. Wang, L. W., Leonhard-Melief, C., Haltiwanger, R. S. & Apte, S. S. Post-translational modification of thrombospondin type-1 repeats in ADAMTS-like 1/punctin-1 by C-mannosylation of tryptophan. J. Biol. Chem. 284, 30004-30015 (2009).
121. Barresi, R. & Campbell, K. P. Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207 (2006). (Pubitemid 43210689)
122. Stalnaker, S. H. et al. Glycomic analyses of mouse models of congenital muscular dystrophy. J. Biol. Chem. 286, 21180-21190 (2011).
123. Stalnaker, S. H. et al. Site mapping and characterization of O-glycan structures on α-dystroglycan isolated from rabbit skeletal muscle. J. Biol. Chem. 285, 24882-24891 (2010).
124. Combs, A. C. & Ervasti, J. M. Enhanced laminin binding by α-dystroglycan after enzymatic deglycosylation. Biochem. J. 390, 303-309 (2005). (Pubitemid 41192256)
125. Hara, Y. et al. A dystroglycan mutation associated with limb-girdle muscular dystrophy. N. Engl. J. Med. 364, 939-946 (2011).
126. Yoshida-Moriguchi, T. et al. O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 327, 88-92 (2010).
127. Inamori, K. et al. Dystroglycan function requires xylosyl-and glucuronyltransferase activities of LARGE. Science 335, 93-96 (2012).
128. Zhang, Z., Zhang, P. & Hu, H. LARGE expression augments the glycosylation of glycoproteins in addition to α-dystroglycan conferring laminin binding. PLoS ONE 6, e19080 (2011).
129. Nairn, A. V., dela Rosa, M. & Moremen, K. W. Transcript analysis of stem cells. Methods Enzymol. 479, 73-91 (2010).
130. Hua, S. et al. Comprehensive native glycan profiling with isomer separation and quantitation for the discovery of cancer biomarkers. Analyst 136, 3663-3671 (2011).
131. An, H. J., Kronewitter, S. R., de Leoz, M. L. & Lebrilla, C. B. Glycomics and disease markers. Curr. Opin. Chem. Biol. 13, 601-607 (2009).
132. Bielik, A. M. & Zaia, J. Historical overview of glycoanalysis. Methods Mol. Biol. 600, 9-30 (2010).
133. Aoki, K. et al. The diversity of O-linked glycans expressed during Drosophila melanogaster development reflects stage-and tissue-specific requirements for cell signaling. J. Biol. Chem. 283, 30385-30400 (2008).
134. Haab, B. B. Antibody-lectin sandwich arrays for biomarker and glycobiology studies. Expert Rev. Proteom. 7, 9-11 (2010).
135. Yue, T. et al. The prevalence and nature of glycan alterations on specific proteins in pancreatic cancer patients revealed using antibody-lectin sandwich arrays. Mol. Cell. Proteomics 8, 1697-1707 (2009).
136. Li, C. et al. Pancreatic cancer serum detection using a lectin/glyco-antibody array method. J. Proteome Res. 8, 483-492 (2009).
137. Adamczyk, B., Tharmalingam, T. & Rudd, P. M. Glycans as cancer biomarkers. Biochim. Biophys. Acta 9 Dec 2011 (doi:10.1016/j.bbagen.2011.12.001) .
138. Lauc, G. et al. Genomics meets glycomics-the first GWAS study of human N-glycome identifies HNF1α as a master regulator of plasma protein fucosylation. PLoS Genet. 6, e1001256 (2010).
139. Huffman, J. E. et al. Polymorphisms in B3GAT1, SLC9A9 and MGAT5 are associated with variation within the human plasma N-glycome of 3533 European adults. Hum. Mol. Genet. 20, 5000-5011 (2011).
140. Esko, J. D. & Selleck, S. B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471 (2002). (Pubitemid 34800227)
141. Wang, A., de la Motte, C., Lauer, M. & Hascall, V. Hyaluronan matrices in pathobiological processes. FEBS J. 278, 1412-1418 (2011).
142. Tian, E. & Ten Hagen, K. G. Recent insights into the biological roles of mucin-type O-glycosylation. Glycoconj. J. 26, 325-334 (2009).
143. Issoglio, F. M., Carrizo, M. E., Romero, J. M. & Curtino, J. A. Mechanisms of monomeric and dimeric glycogenin autoglucosylation. J. Biol. Chem. 287, 1955-1961 (2012).
144. Schegg, B., Hulsmeier, A. J., Rutschmann, C., Maag, C. & Hennet, T. Core glycosylation of collagen is initiated by two β(1-O) galactosyltransferases. Mol. Cell. Biol. 29, 943-952 (2009).
145. Pontier, S. M. & Schweisguth, F. Glycosphingolipids in signaling and development: from liposomes to model organisms. Dev. Dyn. 241, 92-106 (2012).
146. Farquhar, M. G. & Palade, G. E. The Golgi apparatus: 100 years of progress and controversy. Trends Cell Biol. 8, 2-10 (1998). (Pubitemid 28040839)
147. Perry, R. J. & Ridgway, N. D. Molecular mechanisms and regulation of ceramide transport. Biochim. Biophys. Acta 1734, 220-234 (2005). (Pubitemid 40805079)
148. van Meer, G. & de Kroon, A. I. Lipid map of the mammalian cell. J. Cell Sci. 124, 5-8 (2011).
149. Smith, M. H., Ploegh, H. L. & Weissman, J. S. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334, 1086-1090 (2011).
150. Seemann, J., Jokitalo, E., Pypaert, M. & Warren, G. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407, 1022-1026 (2000).
151. Slusarewicz, P., Nilsson, T., Hui, N., Watson, R. & Warren, G. Isolation of a matrix that binds medial Golgi enzymes. J. Cell Biol. 124, 405-413 (1994). (Pubitemid 24064454)
152. Ramirez, I. B. & Lowe, M. Golgins and GRASPs: holding the Golgi together. Semin. Cell Dev. Biol. 20, 770-779 (2009).
153. Maccioni, H. J., Quiroga, R. & Spessott, W. Organization of the synthesis of glycolipid oligosaccharides in the Golgi complex. FEBS Lett. 585, 1691-1698 (2011).
154. Gerken, T. A. et al. Emerging paradigms for the initiation of mucin-type protein O-glycosylation by the polypeptide GalNAc transferase family of glycosyltransferases. J. Biol. Chem. 286, 14493-14507 (2011).
155. Gupta, R. & Brunak, S. Prediction of glycosylation across the human proteome and the correlation to protein function. Pac. Symp. Biocomput. 2002, 310-322 (2002).
156. Roch, C., Kuhn, J., Kleesiek, K. & Gotting, C. Differences in gene expression of human xylosyltransferases and determination of acceptor specificities for various proteoglycans. Biochem. Biophys. Res. Commun. 391, 685-691 (2010).
157. Manya, H. et al. Regulation of mammalian protein O-mannosylation: preferential amino acid sequence for O-mannose modification. J. Biol. Chem. 282, 20200-20206 (2007). (Pubitemid 47100010)
158. Pierleoni, A., Martelli, P. L. & Casadio, R. PredGPI: a GPI-anchor predictor. BMC Bioinformat. 9, 392 (2008).