Identification of N-Glycosites in Chicken Egg White Proteins Using an Omics Strategy

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 26, 2017, Pages 5357-5364

  Geng, Fang ^a   Wang, Jinqiu ^a   Liu, Dayu ^a   Jin, Yongguo ^b   Ma, Meihu ^b  

^a CHENGDU UNIVERSITY   (China)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

chicken egg white; clusterin; glycoproteins; mass spectrometry; N glycosylation site

Indexed keywords

ANIMALS; BIOACTIVITY; ELECTROPHORESIS; GLYCOSYLATION; MASS SPECTROMETRY; PROTEINS; SPECTROMETRY;

CHICKEN EGG WHITE; CLUSTERIN; FUNCTIONAL PROPERTIES; GLYCOPEPTIDES; ISO-ELECTRIC POINTS; N-GLYCOSYLATION SITES; NATURAL PROTEINS; TWO DIMENSIONAL ELECTROPHORESIS;

GLYCOPROTEINS;

EGG PROTEIN; GLYCOPROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHICKEN; GLYCOSYLATION; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; MOLECULAR GENETICS; PEPTIDE MAPPING; PROTEOMICS;

AMINO ACID SEQUENCE; ANIMALS; CHICKENS; EGG PROTEINS; GLYCOPROTEINS; GLYCOSYLATION; MOLECULAR SEQUENCE DATA; PEPTIDE MAPPING; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 85021883584     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.7b01706     Document Type: Article

References (35)

1. Raman, R.; Raguram, S.; Venkataraman, G.; Paulson, J. C.; Sasisekharan, R. Glycomics: an integrated systems approach to structure-function relationships of glycans Nat. Methods 2005, 2, 817-824 10.1038/nmeth807
2. Arnold, J. N.; Wormald, M. R.; Sim, R. B.; Rudd, P. M.; Dwek, R. A. The impact of glycosylation on the biological function and structure of human immunoglobulins Annu. Rev. Immunol. 2007, 25, 21-50 10.1146/annurev.immunol.25.022106.141702
3. Sun, X.; Gänzle, M. G.; Wu, J. Identification and Characterization of Glycopeptides from Egg Protein Ovomucin with Anti-Agglutinating Activity against Porcine K88 Enterotoxigenic Escherichia coli Strains J. Agric. Food Chem. 2017, 65, 777 10.1021/acs.jafc.6b04299
4. Offengenden, M.; Wu, J. Egg white ovomucin gels: structured fluids with weak polyelectrolyte properties RSC Adv. 2013, 3, 910-917 10.1039/C2RA22501H
5. Mine, Y.; Yang, M. Recent advances in the understanding of egg allergens: basic, industrial, and clinical perspectives J. Agric. Food Chem. 2008, 56, 4874-4900 10.1021/jf8001153
6. Benede, S.; Lopez-Exposito, I.; Molina, E.; Lopez-Fandino, R. Egg proteins as allergens and the effects of the food matrix and processing Food Funct. 2015, 6, 694-713 10.1039/C4FO01104J
7. KATO, A.; OGINO, K.; KURAMOTO, Y.; KOBAYASHI, K. DEGRADATION OF THE O-GLYCOSIDICALLY LINKED CARBOHYDRATE UNITS OF OVOMUCIN DURING EGG WHITE THINNING J. Food Sci. 1979, 44, 1341-1344 10.1111/j.1365-2621.1979.tb06434.x
8. Shan, Y.; Xu, Q.; Ma, M. Mg 2+ binding affects the structure and activity of ovomucin Int. J. Biol. Macromol. 2014, 70, 230-235 10.1016/j.ijbiomac.2014.06.056
9. Rupa, P.; Nakamura, S.; Katayama, S.; Mine, Y. Effects of ovalbumin glycoconjugates on alleviation of orally induced egg allergy in mice via dendritic-cell maturation and T-cell activation Mol. Nutr. Food Res. 2014, 58, 405-417 10.1002/mnfr.201300067
10. Rupa, P.; Nakamura, S.; Katayama, S.; Mine, Y. Attenuation of Allergic Immune Response Phenotype by Mannosylated Egg White in Orally Induced Allergy in Balb/c Mice J. Agric. Food Chem. 2014, 62, 9479-9487 10.1021/jf503109r
11. Mine, Y.; D'Silva, I. Bioactive components in egg white. In Egg bioscience and biotechnology; Mine, Y., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, 2008; pp 141-184.
12. Geng, F.; Jin, Y. Chicken Egg White Glycoproteins and Its Allergenic Mechanism: A Review China Poultry 2016, 38, 1-8
13. Qiu, N.; Ma, M.; Cai, Z.; Jin, Y.; Huang, X.; Huang, Q.; Sun, S. Proteomic analysis of egg white proteins during the early phase of embryonic development J. Proteomics 2012, 75, 1895-1905 10.1016/j.jprot.2011.12.037
14. Qiu, N.; Ma, M.; Zhao, L.; Liu, W.; Li, Y.; Mine, Y. Comparative Proteomic Analysis of Egg White Proteins under Various Storage Temperatures J. Agric. Food Chem. 2012, 60, 7746-7753 10.1021/jf302100m
15. Zielinska, D. F.; Gnad, F.; Wiśniewski, J. R.; Mann, M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints Cell 2010, 141, 897-907 10.1016/j.cell.2010.04.012
16. Zielinska, D. F.; Gnad, F.; Schropp, K.; Wiśniewski, J. R.; Mann, M. Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery Mol. Cell 2012, 46, 542-548 10.1016/j.molcel.2012.04.031
17. Offengenden, M.; Fentabil, M. A.; Wu, J. N-glycosylation of ovomucin from hen egg white Glycoconjugate J. 2011, 28, 113-123 10.1007/s10719-011-9328-3
18. Jiang, K.; Wang, C. J.; Sun, Y. J.; Liu, Y.; Zhang, Y.; Huang, L. J.; Wang, Z. F. Comparison of Chicken and Pheasant Ovotransferrin N-Glycoforms via Electrospray Ionization Mass Spectrometry and Liquid Chromatography Coupled with Mass Spectrometry J. Agric. Food Chem. 2014, 62, 7245-7254 10.1021/jf501352j
19. Geng, F.; Huang, X.; Majumder, K.; Zhu, Z.; Cai, Z.; Ma, M. Mass spectrometry and two-dimensional electrophoresis to characterize the glycosylation of hen egg white ovomacroglobulin J. Agric. Food Chem. 2015, 63, 8209-8215 10.1021/acs.jafc.5b02618
20. Li, S.; Geng, F.; Wang, P.; Lu, J.; Ma, M. Proteome analysis of the almond kernel (Prunus dulcis) J. Sci. Food Agric. 2016, 96, 3351 10.1002/jsfa.7514
21. Geng, F.; Huang, X.; Yan, N.; Jia, L.; Ma, M. Purification of hen egg white ovomacroglobulin using one-step chromatography J. Sep. Sci. 2013, 36, 3717-3722 10.1002/jssc.201300425
22. Hu, S.; Qiu, N.; Liu, Y.; Zhao, H.; Gao, D.; Song, R.; Ma, M. Identification and comparative proteomic study of quail and duck egg white protein using 2-dimensional gel electrophoresis and matrix-assisted laser desorption/ionization time-of-flight tandem mass spectrometry analysis Poult. Sci. 2016, 95, 1137 10.3382/ps/pew033
23. Crooks, G. E.; Hon, G.; Chandonia, J.-M.; Brenner, S. E. WebLogo: a sequence logo generator Genome Res. 2004, 14, 1188-1190 10.1101/gr.849004
24. Robinson, D.; Monsey, J. Studies on the composition of egg-white ovomucin Biochem. J. 1971, 121, 537-547 10.1042/bj1210537
25. Zhu, F.; Trinidad, J. C.; Clemmer, D. E. Glycopeptide site heterogeneity and structural diversity determined by combined lectin affinity chromatography/IMS/CID/MS techniques J. Am. Soc. Mass Spectrom. 2015, 26, 1092-1102 10.1007/s13361-015-1110-5
26. Benedé, S.; López-Fandiño, R.; Reche, M.; Molina, E.; López-Expósito, I. Influence of the carbohydrate moieties on the immunoreactivity and digestibility of the egg allergen ovomucoid PLoS One 2013, 8, e80810 10.1371/journal.pone.0080810
27. Asperger, A.; Marx, K.; Albers, C.; Molin, L.; Pinato, O. Low abundant N-linked glycosylation in hen egg white lysozyme is localized at nonconsensus sites J. Proteome Res. 2015, 14, 2633-2641 10.1021/acs.jproteome.5b00175
28. Jones, S. E.; Jomary, C. Clusterin Int. J. Biochem. Cell Biol. 2002, 34, 427-431 10.1016/S1357-2725(01)00155-8
29. Mann, K.; Gautron, J.; Nys, Y.; McKee, M. D.; Bajari, T.; Schneider, W. J.; Hincke, M. T. Disulfide-linked heterodimeric clusterin is a component of the chicken eggshell matrix and egg white Matrix Biol. 2003, 22, 397-407 10.1016/S0945-053X(03)00072-6
30. Araki, S.; Israel, S.; Leskov, K.; Criswell, T.; Beman, M.; Klokov, D.; Sampalth, L.; Reinicke, K.; Cataldo, E.; Mayo, L. Clusterin proteins: stress-inducible polypeptides with proposed functions in multiple organ dysfunction Br. J. Radiol. 2005, 27, 106 10.1259/bjr/18105113
31. Makkar, S.; Liyanage, R.; Kannan, L.; Packialakshmi, B.; Lay, J. O., Jr; Rath, N. C. Chicken egg shell membrane associated proteins and peptides J. Agric. Food Chem. 2015, 63, 9888-9898 10.1021/acs.jafc.5b04266
32. Réhault-Godbert, S.; Labas, V.; Helloin, E.; Hervé-Grépinet, V.; Slugocki, C.; Berges, M.; Bourin, M.-C.; Brionne, A.; Poirier, J.-C.; Gautron, J. Ovalbumin-related protein X is a heparin-binding ov-serpin exhibiting antimicrobial activities J. Biol. Chem. 2013, 288, 17285-17295 10.1074/jbc.M113.469759
33. Liu, Y.; Qiu, N.; Ma, M. Comparative proteomic analysis of egg white proteins during the rapid embryonic growth period by combinatorial peptide ligand libraries Poult. Sci. 2015, 94, 2495-2505 10.3382/ps/pev176
34. Bousfield, G. R.; Butnev, V. Y.; Rueda-Santos, M. A.; Brown, A.; Hall, A. S.; Harvey, D. J. Macro-and micro-heterogeneity in pituitary and urinary follicle-stimulating hormone glycosylation. J. Glycomics Lipidomics 2014, 4 10.4172/2153-0637.1000125
35. Sunryd, J. C.; Cheon, B.; Graham, J. B.; Giorda, K. M.; Fissore, R. A.; Hebert, D. N. TMTC1 and TMTC2 are novel endoplasmic reticulum tetratricopeptide repeat-containing adapter proteins involved in calcium homeostasis J. Biol. Chem. 2014, 289, 16085-16099 10.1074/jbc.M114.554071