Terminal disialylated multiantennary complex-type N-glycans carried on acutobin define the glycosylation characteristics of the Deinagkistrodon acutus venom

Glycobiology

Volumn 21, Issue 4, 2011, Pages 530-542

  Lin, Chia Wei ^a   Chen, Jin Mei ^b   Wang, Ying Ming ^b   Wu, Sz Wei ^b   Tsai, Inn Ho ^a,b   Khoo, Kay Hooi ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

Author keywords

acutobin; disialyl; glycosylation analysis; mass spectrometry; snake venom

Indexed keywords

GLYCAN; GLYCOPEPTIDASE; GLYCOPROTEIN; SNAKE VENOM; THROMBIN;

ARTICLE; DEINAGKISTRODON ACUTUS; ENZYME GLYCOSYLATION; ENZYME PURIFICATION; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; SNAKE;

AMINO ACID SEQUENCE; AMINO SUGARS; ANIMALS; CARBOHYDRATE SEQUENCE; CROTALID VENOMS; CROTALUS; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; OLIGOSACCHARIDES, BRANCHED-CHAIN; POLYSACCHARIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIALIC ACIDS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY; THROMBIN;

CROTALINAE; DEINAGKISTRODON ACUTUS; MAMMALIA;

EID: 79952558225     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwq195     Document Type: Article

References (49)

1. Avril T, North SJ, Haslam SM, Willison HJ, Crocker PR. 2006. Probing the cis interactions of the inhibitory receptor Siglec-7 with α2,8- disialylated ligands on natural killer cells and other leukocytes using glycan-specific antibodies and by analysis of α2,8-sialyltransferase gene expression. J Leukoc Biol. 80:787-796. (Pubitemid 44835897)
2. Birrell GW, Earl S, Masci PP, de Jersey J, Wallis TP, Gorman JJ, Lavin MF. 2006. Molecular diversity in venom from the Australian Brown snake, Pseudonaja textilis. Mol Cell Proteomics. 5:379-389. (Pubitemid 43329315)
3. Birrell GW, Earl ST, Wallis TP, Masci PP, de Jersey J, Gorman JJ, Lavin MF. 2007. The diversity of bioactive proteins in Australian snake venoms. Mol Cell Proteomics. 6:973-986. (Pubitemid 47019399)
4. Canis K, McKinnon TA, Nowak A, Panico M, Morris HR, Laffan M, Dell A. 2010. The plasma von Willebrand factor O-glycome comprises a surprising variety of structures including ABH antigens and disialosyl motifs. J Thromb Haemost. 8:137-145.
5. Chang LY, Harduin-Lepers A, Kitajima K, Sato C, Huang CJ, Khoo KH, Guerardel Y. 2009. Developmental regulation of oligosialylation in zebra-fish. Glycoconj J. 26:247-261.
6. Chen HS, Chen JM, Lin CW, Khoo KH, Tsai IH. 2008. New insights into the functions and N-glycan structures offactor X activator from Russell's viper venom. FEBS J. 275:3944-3958.
7. Crocker PR, Paulson JC, Varki A. 2007. Siglecs and their roles in the immune system. Nat Rev Immunol. 7:255-266. (Pubitemid 46480955)
8. Dell A, Reason AJ, Khoo KH, Panico M, McDowell RA, Morris HR. 1994. Mass spectrometry of carbohydrate-containing biopolymers. Methods Enzymol. 230:108-132. (Pubitemid 24080130)
9. Fox JW, Serrano SM. 2008. Exploring snake venom proteomes: Multifaceted analyses for complex toxin mixtures. Proteomics. 8:909-920. (Pubitemid 351362943)
10. Fukuda M, Dell A, Fukuda MN. 1984. Structure offetal lactosaminoglycan: The carbohydrate moiety of Band 3 isolated from human umbilical cord erythrocytes. J Biol Chem. 259:4782-4791. (Pubitemid 14150015)
11. Fukuda MN, Dell A, Oates JE, Fukuda M. 1985. Embryonal lactosaminoglycan: The structure of branched lactosaminoglycans with novel disialosyl (sialyl α 2-9 sialyl) terminals isolated from PA1 human embryonal carcinoma cells. J Biol Chem. 260:6623-6631.
12. Fukuda M, Lauffenburger M, Sasaki H, Rogers ME, Dell A. 1987. Structures of novel sialylated O-linked oligosaccharides isolated from human erythro-cyte glycophorins. J Biol Chem. 262:11952-11957.
13. Funakoshi Y, Taguchi T, Sato C, Kitajima K, Inoue S, Morris HR, Dell A, Inoue Y. 1997. Occurrence of terminal α2-8-linked disialylated poly-N-acetyllactosamine chains with Le(X) and I antigenic glycotopes in tetraantennary arms of an N-linked glycoprotein isolated from rainbow trout ovarian fluid. Glycobiology. 7:195-205. (Pubitemid 27168774)
14. Gowda DC, Davidson EA. 1992. Structural features of carbohydrate moieties in snake venom glycoproteins. Biochem Biophys Res Commun. 182:294-301.
15. Gowda DC, Davidson EA. 1994. Isolation and characterization of novel mucin-like glycoproteins from cobra venom. J Biol Chem. 269:20031-20039. (Pubitemid 24250924)
16. Gowda DC, Jackson CM, Hensley P, Davidson EA. 1994. Factor X-activating glycoprotein of Russell's viper venom: Polypeptide composition and characterization of the carbohydrate moieties. J Biol Chem. 269:10644-10650.
17. Gowda DC, Schultz M, Bredehorst R, Vogel CW. 1992. Structure of the major oligosaccharide of cobra venom factor. Mol Immunol. 29:335-342.
18. Grewal PK. 2010. The Ashwell-Morell receptor. Methods Enzymol. 479:223-241.
19. Gutierrez JM, Lomonte B, Leon G, Alape-Giron A, Flores-Diaz M, Sanz L, Angulo Y, Calvete JJ. 2009. Snake venomics and antivenomics: Proteomic tools in the design and control of antivenoms for the treatment of snakebite envenoming. J Proteomics. 72:165-182.
20. Joseph JS, Valiyaveettil M, Gowda DC, Kini RM. 2003. Occurrence of O-linked Xyl-GlcNAc and Xyl-Glc disaccharides in trocarin, a factor Xa homolog from snake venom. J Thromb Haemost. 1:545-550.
21. Kiang WL, Krusius T, Finne J, Margolis RU, Margolis RK. 1982. Glycoproteins and proteoglycans of the chromaffin granule matrix. J Biol Chem. 257:1651-1659. (Pubitemid 12157113)
22. Klein A, Roussel P. 1998. O-acetylation of sialic acids. Biochimie. 80:49-57. (Pubitemid 28211653)
23. Kordis D, Gubensek F. 2000. Adaptive evolution of animal toxin multigene families. Gene. 261:43-52. (Pubitemid 32106652)
24. Krusius T, Fukuda M, Dell A, Ruoslahti E. 1985. Structure of the carbohydrate units of human amniotic fluid fibronectin. J Biol Chem. 260:4110-4116. (Pubitemid 15091953)
25. Lin SY, Chen YY, Fan YY, Lin CW, Chen ST, Wang AH, Khoo KH. 2008. Precise mapping of increased sialylation pattern and the expression of acute phase proteins accompanying murine tumor progression in BALB/c mouse by integrated sera proteomics and glycomics. J Proteome Res. 7:3293-3303.
26. Lochnit G, Geyer R. 1995. Carbohydrate structure analysis of batroxobin, a thrombin-like serine protease from Bothrops moojeni venom. Eur J Biochem. 228:805-816.
27. Luo X, Yang H, Liang C, Jin S. 2010. Structural characterization of N-linked oligosaccharides of Defibrase from Agikistrodon acutus by sequential exo-glycosidase digestion and MALDI-TOF mass spectrometry. Toxicon. 55:421-429.
28. Nawarak J, Phutrakul S, Chen ST. 2004. Analysis of lectin-bound glyco-proteins in snake venom from the Elapidae and Viperidae families. J Proteome Res. 3:383-392. (Pubitemid 39207341)
29. Nikandrov NN, Deshimaru M, Tani A, Chijiwa T, Shibata H, Chang CC, Fukumaki Y, Ito T, Ohno M. 2005. Purification, primary structures and evolution of coagulant proteases from Deinagkistrodon actus venom. Toxicon. 46:907-917. (Pubitemid 41735141)
30. O'Reilly MK, Paulson JC. 2009. Siglecs as targets for therapy in immune-cell-mediated disease. Trends Pharmacol Sci. 30:240-248.
31. Pfeiffer G, Dabrowski U, Dabrowski J, Stirm S, Strube KH, Geyer R. 1992. Carbohydrate structure of a thrombin-like serine protease from Agkistrodon rhodostoma: Structure elucidation of oligosaccharides by methylation analysis, liquid secondary-ion mass spectrometry and proton magnetic resonance. Eur J Biochem. 205:961-978.
32. Powlesland AS, Hitchen PG, Parry S, Graham SA, Barrio MM, Elola MT, Mordoh J, Dell A, Drickamer K, Taylor ME. 2009. Targeted glyco-proteomic identification of cancer cell glycosylation. Glycobiology. 19:899-909.
33. Sato C. 2004. Chain length diversity of sialic acids and its biological significance. Trends Glycosci Glycotechnol. 16:331-344. (Pubitemid 39539988)
34. Sato C, Fukuoka H, Ohta K, Matsuda T, Koshino R, Kobayashi K, Troy FA, II, Kitajima K. 2000. Frequent occurrence of pre-existing α2-8-linked dis-ialic and oligosialic acids with chain lengths up to 7 Sia residues in mammalian brain glycoproteins: Prevalence revealed by highly sensitive chemical methods and anti-di-, oligo-, and poly-Sia antibodies specific for defined chain lengths. J Biol Chem. 275:15422-15431. (Pubitemid 30337273)
35. Sato C, Inoue S, Matsuda T, Kitajima K. 1998. Development of a highly sensitive chemical method for detecting α2-8-linked oligo/polysialic acid residues in glycoproteins blotted on the membrane. Anal Biochem. 261:191-197. (Pubitemid 28406938)
36. Sato C, Matsuda T, Kitajima K. 2002. Neuronal differentiation-dependent expression of the disialic acid epitope on CD166 and its involvement in neurite formation in Neuro2A cells. J Biol Chem. 277:45299-45305. (Pubitemid 36159136)
37. Sato C, Yasukawa Z, Honda N, Matsuda T, Kitajima K. 2001. Identification and adipocyte differentiation-dependent expression of the unique disialic acid residue in an adipose tissue-specific glycoprotein, adipo Q. J Biol Chem. 276:28849-28856.
38. Sjoberg ER, Powell LD, Klein A, Varki A. 1994. Natural ligands of the B cell adhesion molecule CD22 beta can be masked by 9-O-acetylation of sialic acids. J Cell Biol. 126:549-562.
39. Soares SG, Oliveira LL. 2009. Venom-sweet-venom: N-linked glycosylation in snake venom toxins. Protein Pept Lett. 16:913-919.
40. Tanaka N, Nakada H, Itoh N, Mizuno Y, Takanishi M, Kawasaki T, Tate S, Inagaki F, Yamashina I. 1992. Novel structure of the N-acetylgalactosamine containing N-glycosidic carbohydrate chain of batroxobin, a thrombin-like snake venom enzyme. J Biochem. 112:68-74.
41. Wang YM, Wang SR, Tsai IH. 2001. Serine protease isoforms of Deinagkistrodon acutus venom: Cloning, sequencing and phylogenetic analysis. Biochem J. 354:161-168.
42. Wei JN, Wang QC, Liu GF, Ezell EL, Quast MJ. 2004. Reduction of brain injury by antithrombotic agent acutobin after middle cerebral artery ischemia/reperfusion in the hyperglycemic rat. Brain Res. 1022: 234-243. (Pubitemid 39195004)
43. Yasukawa Z, Sato C, Kitajima K. 2005. Inflammation-dependent changes in alpha2,3-, alpha2,6-, and alpha2,8-sialic acid glycotopes on serum glyco-proteins in mice. Glycobiology. 15:827-837. (Pubitemid 41222472)
44. Yasukawa Z, Sato C, Kitajima K. 2007. Identification of an inflammation-inducible serum protein recognized by anti-disialic acid antibodies as carbonic anhydrase II. J Biochem. 141:429-441. (Pubitemid 46770395)
45. Yasukawa Z, Sato C, Sano K, Ogawa H, Kitajima K. 2006. Identification of disialic acid-containing glycoproteins in mouse serum: A novel modification of immunoglobulin light chains, vitronectin, and plasminogen. Glycobiology. 16:651-665. (Pubitemid 43985506)
46. Yu SY, Khoo KH, Yang Z, Herp A, Wu AM. 2008. Glycomic mapping of O-and N-linked glycans from major rat sublingual mucin. Glycoconj J. 25:199-212. (Pubitemid 351406286)
47. Yu SY, Wu SW, Khoo KH. 2006. Distinctive characteristics of MALDI-Q/ TOF and TOF/TOF tandem mass spectrometry for sequencing of per-methylated complex type N-glycans. Glycoconj J. 23:355-369.
48. Zhang B, Liu Q, Yin W, Zhang X, Huang Y, Luo Y, Qiu P, Su X, Yu J, Hu S, Yan G. 2006. Transcriptome analysis of Deinagkistrodon acutus venomous gland focusing on cellular structure and functional aspects using expressed sequence tags. BMC Genomics. 7:152.
49. Zhao Y, Zhao G, Chen Q. 2000. Evaluation of acutobin injection in the treatment of acute cerebral infarction. Chin New Drugs J. 9:266-267.