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A comparison of N-glycan profiles in human plasma and vitreous fluid

  • Basic Science
  • Published:
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Abstract

Purpose

To investigate the concentration and composition of N-glycans in plasma and vitreous samples obtained from patients with non-proliferative vitreoretinal diseases.

Methods

Plasma and vitreous samples were collected from 11 patients with idiopathic macular hole (MH) and 9 patients with epiretinal membrane (ERM). The samples were pretreated for enzymatic cleaving, and subsequently glycans released from proteins were captured on BlotGlyco H beads. Sialic acids were methyl-esterified. Processed glycans were tagged with aminooxy-functionalized peptide reagent (aoWR) and released from the beads, followed by detection by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF-MS). The concentration and composition of N-glycans in the samples were assessed.

Results

Concentration of N-glycans in vitreous samples (132 ± 29 pmol/100 μg protein) was significantly lower compared with those in plasma samples (714 ± 29 pmol/100 μg protein, p < 0.001). Predominant N-glycan in both plasma (39.7 ± 1.1 %) and vitreous fluid (37.2 ± 3.1 %) was identical, and the composition was presumed as [(Hex)2(HexNAc)2(NeuAc)2+ (Man)3(GlcNAc)2]. By contrast, the second-ranked N-glycan in vitreous samples (15.6 ± 1.5 %) was the seventh in plasma (2.3 ± 0.2 %).

Conclusions

The current data provide useful information on N-glycan profile in the vitreous fluid, which is distinct from that in the plasma.

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References

  1. Hashimoto K, Takigawa I, Shiga M, Kanehisa M, Mamitsuka H (2008) Mining significant tree patterns in carbohydrate sugar chains. Bioinformatics 24:i167–i173. doi:10.1093/bioinformatics/btn293

    Article  PubMed  Google Scholar 

  2. Schwarz F, Aebi M (2011) Mechanisms and principles of N-linked protein glycosylation. Curr Opin Struct Biol 21:576–582. doi:10.1016/j.sbi.2011.08.005

    Article  CAS  PubMed  Google Scholar 

  3. Varki A (1999) Essentials of glycobiology. Cold Spring Harbor Laboratory Press [Bethesda National Center for Biotechnology Information], Cold Spring Harbor, NY

    Google Scholar 

  4. Kamiyama T, Yokoo H, Furukawa J, Kurogochi M, Togashi T, Miura N, Nakanishi K, Kamachi H, Kakisaka T, Tsuruga Y, Fujiyoshi M, Taketomi A, Nishimura S, Todo S (2013) Identification of novel serum biomarkers of hepatocellular carcinoma using glycomic analysis. Hepatology 57:2314–2325. doi:10.1002/hep.26262

    Article  CAS  PubMed  Google Scholar 

  5. Kimura A, Sogawa K, Satoh M, Kodera Y, Yokosuka O, Tomonaga T, Nomura F (2012) The application of a three-step serum proteome analysis for the discovery and identification of novel biomarkers of hepatocellular carcinoma. Int J Proteomics 2012:623190. doi:10.1155/2012/623190

    Article  PubMed Central  PubMed  Google Scholar 

  6. Chen C, Schmilovitz-Weiss H, Liu XE, Pappo O, Halpern M, Sulkes J, Braun M, Cohen M, Barak N, Tur-Kaspa R, Vanhooren V, Van Vlierberghe H, Libert C, Contreras R, Ben-Ari Z (2009) Serum protein N-glycans profiling for the discovery of potential biomarkers for nonalcoholic steatohepatitis. J Proteome Res 8:463–470. doi:10.1021/pr800656e

    Article  CAS  PubMed  Google Scholar 

  7. Lu JP, Knezevic A, Wang YX, Rudan I, Campbell H, Zou ZK, Lan J, Lai QX, Wu JJ, He Y, Song MS, Zhang L, Lauc G, Wang W (2011) Screening novel biomarkers for metabolic syndrome by profiling human plasma N-glycans in Chinese Han and Croatian populations. J Proteome Res 10:4959–4969. doi:10.1021/pr2004067

    Article  CAS  PubMed  Google Scholar 

  8. Abeijon C, Hirschberg CB (1992) Topography of glycosylation reactions in the endoplasmic reticulum. Trends Biochem Sci 17:32–36

    Article  CAS  PubMed  Google Scholar 

  9. Chu CS, Ninonuevo MR, Clowers BH, Perkins PD, An HJ, Yin H, Killeen K, Miyamoto S, Grimm R, Lebrilla CB (2009) Profile of native N-linked glycan structures from human serum using high-performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. Proteomics 9:1939–1951. doi:10.1002/pmic.200800249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Miura Y, Hato M, Shinohara Y, Kuramoto H, Furukawa J, Kurogochi M, Shimaoka H, Tada M, Nakanishi K, Ozaki M, Todo S, Nishimura S (2008) BlotGlycoABCTM, an integrated glycoblotting technique for rapid and large scale clinical glycomics. Mol Cell Proteomics 7:370–377. doi:10.1074/mcp.M700377-MCP200

    Article  CAS  PubMed  Google Scholar 

  11. Miyahara K, Nouso K, Saito S, Hiraoka S, Harada K, Takahashi S, Morimoto Y, Kobayashi S, Ikeda F, Miyake Y, Shiraha H, Takaki A, Okada H, Amano M, Hirose K, Nishimura S, Yamamoto K (2013) Serum glycan markers for evaluation of disease activity and prediction of clinical course in patients with ulcerative colitis. PLoS One 8:e74861. doi:10.1371/journal.pone.0074861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Nouso K, Amano M, Ito YM, Miyahara K, Morimoto Y, Kato H, Tsutsumi K, Tomoda T, Yamamoto N, Nakamura S, Kobayashi S, Kuwaki K, Hagihara H, Onishi H, Miyake Y, Ikeda F, Shiraha H, Takaki A, Nakahara T, Nishimura S, Yamamoto K (2013) Clinical utility of high-throughput glycome analysis in patients with pancreatic cancer. J Gastroenterol 48:1171–1179. doi:10.1007/s00535-012-0732-7

    Article  CAS  PubMed  Google Scholar 

  13. Seales EC, Jurado GA, Brunson BA, Wakefield JK, Frost AR, Bellis SL (2005) Hypersialylation of beta1 integrins, observed in colon adenocarcinoma, may contribute to cancer progression by up-regulating cell motility. Cancer Res 65:4645–4652. doi:10.1158/0008-5472.CAN-04-3117

    Article  CAS  PubMed  Google Scholar 

  14. Tanaka F, Otake Y, Nakagawa T, Kawano Y, Miyahara R, Li M, Yanagihara K, Nakayama J, Fujimoto I, Ikenaka K, Wada H (2000) Expression of polysialic acid and STX, a human polysialyltransferase, is correlated with tumor progression in non-small cell lung cancer. Cancer Res 60:3072–3080

    CAS  PubMed  Google Scholar 

  15. Itoh N, Sakaue S, Nakagawa H, Kurogochi M, Ohira H, Deguchi K, Nishimura S, Nishimura M (2007) Analysis of N-glycan in serum glycoproteins from db/db mice and humans with type 2 diabetes. Am J Physiol Endocrinol Metab 293:E1069–E1077. doi:10.1152/ajpendo.00182.2007

    Article  CAS  PubMed  Google Scholar 

  16. Nishimura S, Niikura K, Kurogochi M, Matsushita T, Fumoto M, Hinou H, Kamitani R, Nakagawa H, Deguchi K, Miura N, Monde K, Kondo H (2004) High-throughput protein glycomics: combined use of chemoselective glycoblotting and MALDI-TOF/TOF mass spectrometry. Angew Chem Int Ed Engl 44:91–96. doi:10.1002/anie.200461685

    Article  PubMed  Google Scholar 

  17. Miura Y, Shinohara Y, Furukawa J, Nagahori N, Nishimura S (2007) Rapid and simple solid-phase esterification of sialic acid residues for quantitative glycomics by mass spectrometry. Chemistry 13:4797–4804. doi:10.1002/chem.200601872

    Article  CAS  PubMed  Google Scholar 

  18. Yamane K, Minamoto A, Yamashita H, Takamura H, Miyamoto-Myoken Y, Yoshizato K, Nabetani T, Tsugita A, Mishima HK (2003) Proteome analysis of human vitreous proteins. Mol Cell Proteomics 2:1177–1187. doi:10.1074/mcp.M300038-MCP200

    Article  CAS  PubMed  Google Scholar 

  19. Gu W, Fukuda T, Isaji T, Hashimoto H, Wang Y, Gu J (2013) alpha1,6-Fucosylation regulates neurite formation via the activin/phospho-Smad2 pathway in PC12 cells: the implicated dual effects of Fut8 for TGF-beta/activin-mediated signaling. FASEB J 27:3947–3958. doi:10.1096/fj.12-225805

    Article  CAS  PubMed  Google Scholar 

  20. Jaeken J, Schachter H, Carchon H, De Cock P, Coddeville B, Spik G (1994) Carbohydrate-deficient glycoprotein syndrome type II: a deficiency in Golgi localised N-acetyl-glucosaminyltransferase II. Arch Dis Child 71:123–127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Shinkawa T, Nakamura K, Yamane N, Shoji-Hosaka E, Kanda Y, Sakurada M, Uchida K, Anazawa H, Satoh M, Yamasaki M, Hanai N, Shitara K (2003) The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J Biol Chem 278:3466–3473. doi:10.1074/jbc.M210665200

    Article  CAS  PubMed  Google Scholar 

  22. Wang Y, Tan J, Sutton-Smith M, Ditto D, Panico M, Campbell RM, Varki NM, Long JM, Jaeken J, Levinson SR, Wynshaw-Boris A, Morris HR, Le D, Dell A, Schachter H, Marth JD (2001) Modeling human congenital disorder of glycosylation type IIa in the mouse: conservation of asparagine-linked glycan-dependent functions in mammalian physiology and insights into disease pathogenesis. Glycobiology 11:1051–1070

    Article  CAS  PubMed  Google Scholar 

  23. Knezevic A, Gornik O, Polasek O, Pucic M, Redzic I, Novokmet M, Rudd PM, Wright AF, Campbell H, Rudan I, Lauc G (2010) Effects of aging, body mass index, plasma lipid profiles, and smoking on human plasma N-glycans. Glycobiology 20:959–969. doi:10.1093/glycob/cwq051

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by JSPS KAKENHI Grant Number 24659754, 26670749 and 25462745, the Charitable Trust Fund for Ophthalmic Research in Commemoration of Santen Pharmaceutical's Founder (KN and AK), and “Development of Systems and Technology for Advanced Measurement and Analysis” by JST-SENTAN. The authors wish to thank Ikuyo Hirose, Shiho Yoshida, Erdal Tan Ishizuka, and Kazue Okada for their skillful technical assistance in this project.

Conflict of interest

The authors declare that they have no conflicts of interest.

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Authors and Affiliations

  1. Laboratory of Ocular Cell Biology and Visual Science, Hokkaido University Graduate School of Medicine, Sapporo, Japan

    Saori Inafuku, Kousuke Noda, Atsuhiro Kanda & Susumu Ishida

  2. Department of Ophthalmology, Hokkaido University Graduate School of Medicine, North 15, West 7, Kita-ku, Sapporo, Hokkaido, 060-8638, Japan

    Saori Inafuku, Kousuke Noda, Chikako Yoshizawa, Wataru Saito, Atsuhiro Kanda & Susumu Ishida

  3. Field of Drug Discovery Research, Faculty of Advanced Life Science, Graduate School of Life Sciences, Hokkaido University, Sapporo, Japan

    Saori Inafuku, Maho Amano, Tetsu Ohashi & Shin-Ichiro Nishimura

  4. Medicinal Chemistry Pharmaceuticals, Co. Ltd, Sapporo, Japan

    Maho Amano & Shin-Ichiro Nishimura

Authors
  1. Saori Inafuku
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  2. Kousuke Noda
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  3. Maho Amano
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  4. Tetsu Ohashi
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  8. Shin-Ichiro Nishimura
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  9. Susumu Ishida
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Correspondence to Kousuke Noda.

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Inafuku, S., Noda, K., Amano, M. et al. A comparison of N-glycan profiles in human plasma and vitreous fluid. Graefes Arch Clin Exp Ophthalmol 252, 1235–1243 (2014). https://doi.org/10.1007/s00417-014-2671-x

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  • DOI: https://doi.org/10.1007/s00417-014-2671-x

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