Anomalous N -glycan structures with an internal fucose branched to GlcA and GlcN residues isolated from a mollusk shell-forming fluid

Journal of Proteome Research

Volumn 12, Issue 10, 2013, Pages 4547-4555

  Zhou, Hui ^a,c,d   Hanneman, Andrew J ^a,b   Chasteen, N Dennis ^c   Reinhold, Vernon N ^a,b  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b Glycan Connections LLC   (United States)

^c Univ of New Hampshire   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

(+) MSn; ( ) MSn; 4 O methyl GlcA(1 4) GlcNAc(1 3) Fuc(1 4)GlcNAc; branched fucose; extrapallial fluid; GC MS; HRMS; ITMSn; Mytilus edulis; N glycans; O methyl Fuc(1 2) 4 O methyl GlcA(1 4) GlcNAc(1 3) Fuc(1 4) GlcNAc; sequential disassembly

Indexed keywords

CALCIUM CARBONATE; FUCOSE; GLUCURONIC ACID; GLYCAN DERIVATIVE; HEAVY METAL; PENTASACCHARIDE; TETRASACCHARIDE;

AMINO ACID SEQUENCE; ANIMAL SHELL; ARTICLE; CALCIUM BINDING; CAPILLARY CHROMATOGRAPHY; COLLISIONALLY ACTIVATED DISSOCIATION; GROWTH; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; METHYLATION; MYTILUS EDULIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; STEREOISOMERISM;

ACETYLGLUCOSAMINE; ANIMAL SHELLS; ANIMALS; BODY FLUIDS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; FUCOSE; GLYCOPROTEINS; METHYLATION; METHYLGLUCOSIDES; MYTILUS EDULIS; POLYSACCHARIDES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84885220290     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4006734     Document Type: Article

References (54)

1. Marin, F.; Luquet, G.; Marie, B.; Medakovic, D. Molluscan Shell Proteins: Primary Structure, Origin, And Evolution Curr. Top. Dev. Biol. 2008, 80, 209-276
2. Colfen, H. Biomineralization: A Crystal-Clear View Nat. Mater. 2010, 9 (12) 960-961
3. Zuykov, M.; Pelletier, E.; Demers, S. Colloidal Complexed Silver and Silver Nanoparticles in Extrapallial Fluid of Mytilus edulis Mar. Environ. Res. 2011, 71 (1) 17-21
4. Muller, W. E. G.; Xie, L.-p.; Zhu, F.-j.; Zhou, Y.-j.; Yang, C.; Zhang, R.-q., Molecular Approaches to Understand Biomineralization of Shell Nacreous Layer. In Molecular Biomineralization; Springer: Berlin/Heidelberg, 2011; pp 331-352.
5. Hu, B.; Xue, Z.; Du, Z. The Biomimetic Mineralization Closer to a Real Biomineralization. In Advances in Biomimetics; Cavrak, M., Ed.; Intech Open Books: New York, 2011.
6. Ma, Z.; Huang, J.; Sun, J.; Wang, G.; Li, C.; Xie, L.; Zhang, R. A Novel Extrapallial Fluid Protein Controls the Morphology of Nacre Lamellae in the Pearl Oyster, Pinctada fucata J. Biol. Chem. 2007, 282 (32) 23253-23263
7. Misogianes, M. J.; Chasteen, N. D. A Chemical and Spectral Characterization of the Extrapallial Fluid of Mytilus edulis Anal. Biochem. 1979, 100 (2) 324-34
8. Hattan, S. J.; Laue, T. M.; Chasteen, N. D. Purification and Characterization of a Novel Calcium-Binding Protein from the Extrapallial Fluid of the Mollusc, Mytilus edulis J. Biol. Chem. 2001, 276 (6) 4461-4468
9. Yin, Y.; Huang, J.; Paine, M. L.; Reinhold, V. N.; Chasteen, N. D. Structural Characterization of the Major Extrapallial Fluid Protein of the Mollusc Mytilus edulis: Implications for Function Biochemistry 2005, 44 (31) 10720-31
10. Lopes-Lima, M.; Ribeiro, I.; Pinto, R. A.; Machado, J. Isolation, Purification and Characterization of Glycosaminoglycans in the Fluids of the Mollusc Anodonta cygnea Comp. Biochem. Physiol. A: Mol. Int. Physiol. 2005, 141 (3) 319-26
11. Moura, G.; Vilarinho, L.; Santos, A. C.; Machado, J. Organic Compounds in the Extrapalial Fluid and Haemolymph of Anodonta cygnea (L.) with Emphasis On The Seasonal Biomineralization Process Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2000, 125 (3) 293-306
12. Moura, G.; Vilarinho, L.; Machado, J. The Action of Cd, Cu, Cr, Zn, and Pb on Fluid Composition of Anodonta cygnea (L.): Organic Components Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2000, 127 (1) 105-112
13. Nair, P. S.; Robinson, W. E. Calcium Speciation and Exchange between Blood and Extrapallial Fluid of the Quahog Mercenaria mercenaria (L.) Biol. Bull. 1998, 195 (1) 43-51
14. Nair, P. S.; Robinson, W. E. Purification and Characterization of a Histidine-Rich Glycoprotein That Binds Cadmium from the Blood Plasma of the Bivalve Mytilus edulis Arch. Biochem. Biophys. 1999, 366 (1) 8-14
15. Abebe, A. T.; Devoid, S. J.; Sugumaran, M.; Etter, R.; Robinson, W. E. Identification and Quantification of Histidine-Rich Glycoprotein (HRG) in the Blood Plasma of Six Marine Bivalves Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2007, 147 (1) 74-81
16. Devoid, S. J.; Etter, R.; Sugumaran, M.; Wallace, G. T.; Robinson, W. E. Histidine-Rich Glycoprotein from the Hemolymph of the Marine Mussel Mytilus edulis L. binds Class A, Class B, and Borderline Metals Environ. Toxicol. Chem. 2007, 26 (5) 872-877
17. Nair, P. S.; Robinson, W. E. Cadmium Speciation and Transport in the Blood of the Bivalve Mytilus edulis Mar. Environ. Res. 2000, 50 (1-5) 99-102
18. Satish Nair, P.; Robinson, W. E. Histidine-Rich Glycoprotein in the Blood of the Bivalve Mytilus edulis: Role in Cadmium Speciation and Cadmium Transfer to the Kidney Aquat. Toxicol. 2001, 52 (2) 133-142
19. Nair, P. S.; Robinson, W. E. Cadmium Binding to a Histidine-Rich Glycoprotein from Marine Mussel Blood Plasma: Potentiometric Titration and Equilibrium Speciation Modeling Environ. Toxicol. Chem. 2001, 20 (7) 1596-1604
20. n Anal. Chem. 2005, 77 (19) 6250-6262
21. Gutternigg, M.; Ahrer, K.; Grabher-Meier, H.; Burgmayr, S.; Staudacher, E. Neutral N -Glycans of the Gastropod Arion lusitanicus Eur. J. Biochem. 2004, 271 (7) 1348-1356
22. Puanglarp, N.; Oxley, D.; Currie, G. J.; Bacic, A.; Craik, D. J.; Yellowlees, D. Structure of the N-Linked Oligosaccharides from Tridacnin, A Lectin Found in the Haemolymph of the Giant Clam Hippopus hippopus Eur. J. Biochem. 1995, 232 (3) 873-880
23. Khoo, K. H.; Maizels, R. M.; Page, A. P.; Taylor, G. W.; Rendell, N. B.; Dell, A. Characterization of Nematode Glycoproteins: The Major O -Glycans of Toxocara Excretory-Secretory Antigens Are O-Methylated Trisaccharides Glycobiology 1991, 1 (2) 163-171
24. Huang, Y.; Konse, T.; Mechref, Y.; Novotny, M. V. Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Compatible Beta-Elimination of O-Linked Oligosaccharides Rapid Commun. Mass Spectrom. 2002, 16 (12) 1199-204
25. Shimizu, Y.; Nakata, M.; Kuroda, Y.; Tsutsumi, F.; Kojima, N.; Mizuochi, T. Rapid and Simple Preparation of N-Linked Oligosaccharides by Cellulose-Column Chromatography Carbohydr. Res. 2001, 332 (4) 381-388
26. Ciucanu, I.; Costello, C. E. Elimination of Oxidative Degradation during the Per- O -methylation of Carbohydrates J. Am. Chem. Soc. 2003, 125 (52) 16213-16219
27. Mechref, Y.; Kang, P.; Novotny, M. V. Solid-Phase Permethylation for Glycomic Analysis Methods Mol. Biol. 2009, 534, 53-64
28. Jiao, J.; Zhang, H.; Reinhold, V. N. High Performance IT-MS Sequencing of Glycans (Spatial Resolution of Ovalbumin Isomers) Int. J. Mass Spectrom. 2011, 303 (2-3) 109-117
29. Sweeley, C. C.; Bentley, R.; Makita, M.; Wells, W. W. Gas-Liquid Chromatography of Trimethylsilyl Derivatives of Sugars and Related Substances J. Am. Chem. Soc. 1963, 85
30. Becker, D. J.; Lowe, J. B. Fucose: Biosynthesis and Biological Function in Mammals Glycobiology 2003, 13 (7) 41R-53R
31. Scarsdale, J. N.; Prestegard, J. H.; Ando, S.; Hori, T.; Yu, R. K. 1H-2D-nuclear magnetic Resonance Applied to the Primary Structure Determination of a Novel Octasaccharide Glycolipid Isolated from the Spermatozoa of Bivalves Carbohydr. Res. 1986, 155, 45-56
32. Hori, T.; Sugita, M.; Ando, S.; Tsukada, K.; Shiota, K.; Tsuzuki, M.; Itasaka, O. Isolation and Characterization of a 4-O-methylglucuronic Acid-Containing Glycosphingolipid from Spermatozoa of a Fresh Water Bivalve, H y r i o p s i s s c h l e g e l i i J. Biol. Chem. 1983, 258 (4) 2239-2245
33. Hori, T.; Sugita, M.; Ando, S.; Kuwahara, M.; Kumauchi, K.; Sugie, E.; Itasaka, O. Characterization of a Novel Glycosphingolipid, Ceramide Nonasaccharide, Isolated from Spermatozoa of the Fresh Water Bivalve, Hyriopsis schlegelii J. Biol. Chem. 1981, 256 (21) 10979-10985
34. Yu, R. K.; Koerner, T. A.; Scarsdale, J. N.; Prestegard, J. H. Elucidation of Glycolipid Structure by Proton Nuclear Magnetic Resonance Spectroscopy Chem. Phys. Lipids 1986, 42 (1-3) 27-48
35. Gielens, C.; Idakieva, K.; Van den Bergh, V.; Siddiqui, N. I.; Parvanova, K.; Compernolle, F. Mass Spectral Evidence for N-Glycans with Branching on Fucose in a Molluscan Hemocyanin Biochem. Biophys. Res. Commun. 2005, 331 (2) 562-570
36. Idakieva, K.; Stoeva, S.; Voelter, W.; Gielens, C. Glycosylation of Rapana thomasiana Hemocyanin. Comparison with Other Prosobranch (Gastropod) Hemocyanins Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2004, 138 (3) 221-228
37. Stanley, P.; Schachter, H.; Taniguchi, N., N-Glycans. In Essentials of Glycobiology, 2 nd ed.; Varki, A.; Cummings, R. D.; Esko, J. D.; Freeze, H. H.; Stanley, P.; Bertozzi, C. R.; Hart, G. W.; Etzler, M. E., Eds.; Cold Spring Harbor: New York, 2009.
38. Bleton, J.; Mejanelle, P.; Sansoulet, J.; Goursaud, S.; Tchapla, A. Characterization of Neutral Sugars and Uronic Acids after Methanolysis and Trimethylsilylation for Recognition of Plant Gums J. Chromatogr. A 1996, 720, 27-49
39. Stumpo, K. A.; Reinhold, V. N. The N-Glycome of Human Plasma J. Proteome Res. 2010, 9 (9) 4823-4830
40. Ashline, D. J.; Lapadula, A. J.; Liu, Y. H.; Lin, M.; Grace, M.; Pramanik, B.; Reinhold, V. N. Carbohydrate Structural Isomers Analyzed by Sequential Mass Spectrometry Anal. Chem. 2007, 79 (10) 3830-3842
41. Harvey, D. J. Fragmentation of Negative Ions from Carbohydrates: Part 1. Use of Nitrate and Other Anionic Adducts for the Production of Negative Ion Electrospray Spectra from N-Linked Carbohydrates J. Am. Soc. Mass Spectrom. 2005, 16 (5) 622-630
42. Harvey, D. J. Fragmentation of Negative Ions from Carbohydrates: Part 2. Fragmentation of High-Mannose N-Linked Glycans J. Am. Soc. Mass Spectrom. 2005, 16 (5) 631-646
43. Harvey, D. J. Fragmentation of Negative Ions from Carbohydrates: Part 3. Fragmentation of Hybrid and Complex N-Linked Glycans J. Am. Soc. Mass Spectrom. 2005, 16 (5) 647-659
44. Harvey, D. J. Collision-Induced Fragmentation of Negative Ions from N-Linked Glycans Derivatized with 2-Aminobenzoic Acid J. Mass Spectrom.: JMS 2005, 40 (5) 642-653
45. Harvey, D. J.; Baruah, K.; Scanlan, C. N. Application of Negative Ion MS/MS to the Identification of N-Glycans Released from Carcinoembryonic Antigen Cell Adhesion Molecule 1 (CEACAM1) J. Mass Spectrom.: JMS 2009, 44 (1) 50-60
46. Harvey, D. J.; Jaeken, J.; Butler, M.; Armitage, A. J.; Rudd, P. M.; Dwek, R. A. Fragmentation of Negative Ions from N-Linked Carbohydrates, Part 4. Fragmentation of Complex Glycans Lacking Substitution on the 6-Antenna J. Mass Spectrom.: JMS 2010, 45 (5) 528-535
47. Harvey, D. J.; Royle, L.; Radcliffe, C. M.; Rudd, P. M.; Dwek, R. A. Structural and Quantitative Analysis of N-Linked Glycans by Matrix-Assisted Laser Desorption Ionization and Negative Ion Nanospray Mass Spectrometry Anal. Biochem. 2008, 376 (1) 44-60
48. Ritchie, G.; Harvey, D. J.; Stroeher, U.; Feldmann, F.; Feldmann, H.; Wahl-Jensen, V.; Royle, L.; Dwek, R. A.; Rudd, P. M. Identification of N-Glycans from Ebola Virus Glycoproteins by Matrix-Assisted Laser Desorption/Ionisation Time-of-Flight and Negative Ion Electrospray Tandem Mass Spectrometry Rapid Commun. Mass Spectrom.: RCM 2010, 24 (5) 571-585
49. Hart, G. W.; Copeland, R. J. Glycomics Hits the Big Time Cell 2010, 143 (5) 672-676
50. Bertozzi, C. R.; Rabuka, D., Structural Basis of Glycan Diversity. In Essentials of Glycobiology, 2 nd ed.; Varki, A.; Cummings, R. D.; Esko, J. D.; Freeze, H. H.; Stanley, P.; Bertozzi, C. R.; Hart, G. W.; Etzler, M. E., Eds.; Cold Spring Harbor: New York, 2009.
51. Marino, K.; Bones, J.; Kattla, J. J.; Rudd, P. M. A Systematic Approach to Protein Glycosylation Analysis: A Path through the Maze Nat. Chem. Biol. 2010, 6 (10) 713-723
52. Reinhold, V.; Zhang, H.; Hanneman, A.; Ashline, D. Toward a Platform for Comprehensive Glycan Sequencing Mol. Cell. Proteomics 2013, 12 (4) 866-873
53. Maduzia, L. L.; Yu, E.; Zhang, Y. Caenorhabditis elegans Galectins LEC-6 and LEC-10 Interact with Similar Glycoconjugates in the Intestine. J. Biol. Chem. 286, (6), 4371-4381.
54. Hanneman, A. J.; Rosa, J. C.; Ashline, D.; Reinhold, V. N. Isomer and Glycomer Complexities of Core GlcNAcs in Caenorhabditis elegans Glycobiology 2006, 16 (9) 874-890