Analysis of site-specific N-glycan remodeling in the endoplasmic reticulum and the Golgi

Glycobiology

Volumn 25, Issue 12, 2015, Pages 1335-1349

  Hang, Ivan ^a   Lin, Chia Wei ^a   Grant, Oliver C ^b   Fleurkens, Susanna ^a   Villiger, Thomas K ^a   Soos, Miroslav ^a   Morbidelli, Massimo ^a   Woods, Robert J ^b   Gauss, Robert ^a   Aebi, Markus ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Endoplasmic reticulum glycosylation; Golgi; Golgi glycosylation; Site specific glycosylation

Indexed keywords

GLYCAN; PDI1 PROTEIN, S CEREVISIAE; POLYSACCHARIDE; PROTEIN DISULFIDE ISOMERASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; IN VITRO STUDY; INSECT CELL; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SECRETORY PATHWAY; ANIMAL; GLYCOSYLATION; METABOLISM; SF9 CELL LINE; SPODOPTERA;

ANIMALS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GOLGI APPARATUS; POLYSACCHARIDES; PROTEIN DISULFIDE-ISOMERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SACCHAROMYCES CEREVISIAE PROTEINS; SF9 CELLS; SPODOPTERA;

EID: 84959339855     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv058     Document Type: Article

References (62)

1. Aebi M, Bernasconi R, Clerc S, Molinari M. 2010. N-Glycan structures: Recognition and processing in the ER. Trends Biochem Sci. 35:74-82.
2. Antoniewicz MR. 2013. Dynamic metabolic flux analysis - Tools for probing transient states of metabolic networks. Curr Opin Biotechnol. 24:973-978.
3. Case DA, Babin V, Berryman JT, Betz RM, Cai Q, Cerutti DS, Cheatham TE, Darden TA, Duke RE, Gohlke H, et al. 2014. AMBER 14. San Francisco: University of California.
4. Darden T, York D, Pedersen L. 1993. Particle mesh Ewald: An N·log (N) method for Ewald sums in large systems. J Chem Phys. 98:10089.
5. Dell A, Galadari A, Sastre F, Hitchen P. 2010. Similarities and differences in the glycosylation mechanisms in prokaryotes and eukaryotes. Int J Microbiol. 2010:148178.
6. Dell A, Reason AJ, Khoo KH, Panico M, McDowell RA, Morris HR. 1994. Mass spectrometry of carbohydrate-containing biopolymers. Methods Enzymol. 230:108-132.
7. Domon B, Vath JE, Costello CE. 1990. Analysis of derivatized ceramides and neutral glycosphingolipids by high-performance tandem mass spectrometry. Anal Biochem. 184:151-164.
8. Faid V, Evjen G, Tollersrud OK, Michalski JC, Morelle W. 2006. Site-specific glycosylation analysis of the bovine lysosomal alpha-mannosidase. Glycobiology. 16:440-461.
9. Ferrara C, Grau S, Jager C, Sondermann P, Brunker P, Waldhauer I, Hennig M, Ruf A, Rufer AC, Stihle M, et al. 2011. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci USA. 108:12669-12674.
10. Gauss R, Kanehara K, Carvalho P, Ng DT, Aebi M. 2011. A complex of Pdi1p and the mannosidase Htm1p initiates clearance of unfolded glycoproteins from the endoplasmic reticulum. Mol Cell. 42:782-793.
11. Geisler C, Jarvis DL. 2012. Substrate specificities and intracellular distributions of three N-glycan processing enzymes functioning at a key branch point in the insect N-glycosylation pathway. J Biol Chem. 287:7084-7097.
12. Go EP, Irungu J, Zhang Y, Dalpathado DS, Liao HX, Sutherland LL, Alam SM, Haynes BF, Desaire H. 2008. Glycosylation site-specific analysis of HIV envelope proteins (JR-FL and CON-S) reveals major differences in glycosylation site occupancy, glycoform profiles, and antigenic epitopes' accessibility. J Proteome Res. 7:1660-1674.
13. Gotz AW, Williamson MJ, Xu D, Poole D, Le Grand S, Walker RC. 2012. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized Born. J Chem Theory Comput. 8:1542-1555.
14. Hebert DN, Garman SC, Molinari M. 2005. The glycan code of the endoplasmic reticulum: Asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol. 15:364-370.
15. Heikinheimo P, Helland R, Leiros HK, Leiros I, Karlsen S, Evjen G, Ravelli R, Schoehn G, Ruigrok R, Tollersrud OK, et al. 2003. The structure of bovine lysosomal alpha-mannosidase suggests a novel mechanism for low-pH activation. J Mol Biol. 327:631-644.
16. Hosokawa N, Tremblay LO, Sleno B, Kamiya Y, Wada I, Nagata K, Kato K, Herscovics A. 2010. EDEM1 accelerates the trimming of alpha1,2-linked mannose on the C branch of N-glycans. Glycobiology. 20:567-575.
17. Hsieh P, Rosner MR, Robbins PW. 1983a. Host-dependent variation of asparagine-linked oligosaccharides at individual glycosylation sites of Sindbis virus glycoproteins. J Biol Chem. 258:2548-2554.
18. Hsieh P, Rosner MR, Robbins PW. 1983b. Selective cleavage by endo-beta-N-acetylglucosaminidase H at individual glycosylation sites of Sindbis virion envelope glycoproteins. J Biol Chem. 258:2555-2561.
19. Hua S, Nwosu CC, Strum JS, Seipert RR, An HJ, Zivkovic AM, German JB, Lebrilla CB. 2012. Site-specific protein glycosylation analysis with glycan isomer differentiation. Anal Bioanal Chem. 403:1291-1302.
20. Hubbard SC. 1988. Regulation of glycosylation. The influence of protein structure on N-linked oligosaccharide processing. J Biol Chem. 263:19303-19317.
21. Hubbard SJ, Thornton JM. 1993. "NACCESS", Computer Program. Department of Biochemistry and Molecular Biology, University College London
22. Jelinek-Kelly S, Akiyama T, Saunier B, Tkacz JS, Herscovics A. 1985. Characterization of a specific alpha-mannosidase involved in oligosaccharide processing in Saccharomyces cerevisiae. J Biol Chem. 260:2253-2257.
23. Jimenez del Val I, Nagy JM, Kontoravdi C. 2011. A dynamic mathematical model for monoclonal antibody N-linked glycosylation and nucleotide sugar donor transport within a maturing Golgi apparatus. Biotechnol Progr. 27:1730-1743.
24. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 79:926-935.
25. Karaveg K, Moremen KW. 2005. Energetics of substrate binding and catalysis by class 1 (glycosylhydrolase family 47) alpha-mannosidases involved in N-glycan processing and endoplasmic reticulum quality control. J Biol Chem. 280:29837-29848.
26. Kelleher DJ, Gilmore R. 2006. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology. 16:47R-62R.
27. Kemmink J, Darby NJ, Dijkstra K, Nilges M, Creighton TE. 1996. Structure determination of the N-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy. Biochemistry. 35:7684-7691.
28. Kemmink J, Dijkstra K, Mariani M, Scheek RM, Penka E, Nilges M, Darby NJ. 1999. The structure in solution of the b domain of protein disulfide isomerase. J Biomol NMR. 13:357-368.
29. Kirschner KN, Yongye AB, Tschampel SM, Gonzalez-Outeirino J, Daniels CR, Foley BL, Woods RJ. 2008. GLYCAM06: A generalizable biomolecular force field. Carbohydrates. J Comput Chem. 29:622-655.
30. Krambeck FJ, Bennun SV, Narang S, Choi S, Yarema KJ, Betenbaugh MJ. 2009. A mathematical model to derive N-glycan structures and cellular enzyme activities from mass spectrometric data. Glycobiology. 19:1163-1175.
31. Krokhin O, Ens W, Standing KG, Wilkins J, Perreault H. 2004. Site-specific N-glycosylation analysis: Matrix-assisted laser desorption/ionization quadrupole-quadrupole time-of-flight tandem mass spectral signatures for recognition and identification of glycopeptides. Rapid Commun Mass Spectrom. 18:2020-2030.
32. Mast SW, Moremen KW. 2006. Family 47 alpha-mannosidases in N-glycan processing. Methods Enzymol. 415:31-46.
33. Moremen KW, Tiemeyer M, Nairn AV. 2012. Vertebrate protein glycosylation: Diversity, synthesis and function. Nat Rev Mol Cell Biol. 13:448-462.
34. Nagae M, Yamaguchi Y. 2012. Function and 3D structure of the N-glycans on glycoproteins. Int J Mol Sci. 13:8398-8429.
35. Niwa R, Shoji-Hosaka E, Sakurada M, Shinkawa T, Uchida K, Nakamura K, Matsushima K, Ueda R, Hanai N, Shitara K. 2004. Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res. 64:2127-2133.
36. North SJ, Huang HH, Sundaram S, Jang-Lee J, Etienne AT, Trollope A, Chalabi S, Dell A, Stanley P, Haslam SM. 2010. Glycomics profiling of Chinese hamster ovary cell glycosylation mutants reveals N-glycans of a novel size and complexity. J Biol Chem. 285:5759-5775.
37. Parekh RB, Tse AG, Dwek RA, Williams AF, Rademacher TW. 1987. Tissue-specific N-glycosylation, site-specific oligosaccharide patterns and lentil lectin recognition of rat Thy-1. EMBO J. 6:1233-1244.
38. Powell AK, Harvey DJ. 1996. Stabilization of sialic acids in N-linked oligosaccharides and gangliosides for analysis by positive ion matrix-assisted laser desorption/ionization mass spectrometry. Rapid Commun Mass Spectrom. 10:1027-1032.
39. Raykhel I, Alanen H, Salo K, Jurvansuu J, Nguyen VD, Latva-Ranta M, Ruddock L. 2007. A molecular specificity code for the three mammalian KDEL receptors. J Cell Biol. 179:1193-1204.
40. Roe DR, Cheatham TE. 2013. PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. J Chem Theory Comput. 9:3084-3095.
41. Roepstorff P, Fohlman J. 1984. Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed Mass Spectrom. 11:601.
42. Ryckaert J-P, Ciccotti G, Berendsen HJC. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J Comput Phys. 23:327-341.
43. Salomon-Ferrer R, Götz AW, Poole D, Le Grand S, Walker RC. 2013. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh Ewald. J Chem Theory Comput. 9:3878-3888.
44. Sazinsky SL, Ott RG, Silver NW, Tidor B, Ravetch JV, Wittrup KD. 2008. Aglycosylated immunoglobulin G1 variants productively engage activating Fc receptors. Proc Natl Acad Sci USA. 105:20167-20172.
45. Scallon BJ, Tam SH, McCarthy SG, Cai AN, Raju TS. 2007. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol. 44:1524-1534.
46. Schachter H. 1991. The 'yellow brick road' to branched complex N-glycans. Glycobiology. 1:453-461.
47. Segu ZM, Mechref Y. 2010. Characterizing protein glycosylation sites through higher-energy C-trap dissociation. Rapid Commun Mass Spectrom. 24:1217-1225.
48. Shental-Bechor D, Levy Y. 2009. Folding of glycoproteins: Toward understanding the biophysics of the glycosylation code. Curr Opin Struct Biol. 19:524-533.
49. Shi X, Jarvis DL. 2007. Protein N-glycosylation in the baculovirus-insect cell system. Curr Drug Targets. 8:1116-1125.
50. Sparbier K, Asperger A, Resemann A, Kessler I, Koch S, Wenzel T, Stein G, Vorwerg L, Suckau D, Kostrzewa M. 2007. Analysis of glycoproteins in human serum by means of glycospecific magnetic bead separation and LC-MALDI-TOF/TOF analysis with automated glycopeptide detection. J Biomol Tech. 18:252-258.
51. Stanley P. 2011. Golgi glycosylation. Cold Spring Harb Perspect Biol. 3:1-13.
52. Tian G, Xiang S, Noiva R, Lennarz WJ, Schindelin H. 2006. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell. 124:61-73.
53. Titz A, Butschi A, Henrissat B, Fan YY, Hennet T, Razzazi-Fazeli E, Hengartner MO, Wilson IB, Kunzler M, Aebi M. 2009. Molecular basis for galactosylation of core fucose residues in invertebrates: Identification of caenorhabditis elegans N-glycan core alpha1,6-fucoside beta1, 4-galactosyltransferase GALT-1 as a member of a novel glycosyltransferase family. J Biol Chem. 284:36223-36233.
54. Trimble RB, Maley F, Chu FK. 1983. GlycoProtein biosynthesis in yeast. Protein conformation affects processing of high mannose oligosaccharides on carboxypeptidase Y and invertase. J Biol Chem. 258:2562-2567.
55. Vallée F, Lipari F, Yip P, Sleno B, Herscovics A, Howell PL. 2000. Crystal structure of a class I alpha1,2-mannosidase involved in N-glycan processing and endoplasmic reticulum quality control. EMBO J. 19:581-588.
56. van Kooyk Y, Rabinovich GA. 2008. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol. 9:593-601.
57. Varki A. 1998. Factors controlling the glycosylation potential of the Golgi apparatus. Trends Cell Biol. 8:34-40.
58. Wilkinson B, Gilbert HF. 2004. Protein disulfide isomerase. Biochim Biophys Acta. 1699:35-44.
59. Wisniewski JR, Zougman A, Nagaraj N, Mann M. 2009. Universal sample preparation method for proteome analysis. Nat Methods. 6:359-362.
60. Woods Group. (2005-2014). GLYCAM Web. Athens, GA: Complex Carbohydrate Research Center, University of Georgia (http://www.glycam.com).
61. Yu X, Baruah K, Harvey DJ, Vasiljevic S, Alonzi DS, Song BD, Higgins MK, Bowden TA, Scanlan CN, Crispin M. 2013. Engineering hydrophobic protein-carbohydrate interactions to fine-tune monoclonal antibodies. J Am Chem Soc. 135:9723-9732.
62. Ziegler FD, Trimble RB. 1991. Glycoprotein biosynthesis in yeast: Purification and characterization of the endoplasmic reticulum Man9 processing alpha-mannosidase. Glycobiology. 1:605-614.