Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Structures of N-Glycans of Bothrops Venoms Revealed as Molecular Signatures that Contribute to Venom Phenotype in Viperid Snakes.
Andrade-Silva D
,
Ashline D
,
Tran T
,
Lopes AS
,
Travaglia Cardoso SR
,
Reis MDS
,
Zelanis A
,
Serrano SMT
,
Reinhold V
.
???displayArticle.abstract???
The complexity of snake venoms has long been investigated to explore a myriad of biologically active proteins and peptides that are used for immobilizing or killing prey, and are responsible for the pathological effects observed on envenomation. Glycosylation is the main post-translational modification (PTM) of viperid venoms but currently there is little understanding of how protein glycosylation impacts the variation of venom proteomes. We have previously reported that Bothrops venom glycoproteomes contain a core of components that markedly define their composition and parallel their phylogenetic classification. Here we extend those observations to eight Bothrops species evaluating the N-glycomes by LC-MS as assigned cartoon structures and detailing those structures separately as methylated analogs using ion-trap mass spectrometry (MSn). Following ion disassembly through multiple steps provided sequence and linkage isomeric details that characterized 52 unique compositions in Bothrops venoms. These occurred as 60 structures, of which 26 were identified in the venoms of the Jararaca Complex (B. alcatraz, B. insularis, and B. jararaca), 20 in B. erythromelas, B. jararacussu, B. moojeni and B. neuwiedi venoms, and 22 in B. cotiara venom. Further, quantitative analysis of these N-glycans showed variable relative abundances in the venoms. For the first time a comprehensive set of N-glycan structures present in snake venoms are defined. Despite the fact that glycosylation is not template-defined, the N-glycomes of these venoms mirror the phylogeny cladograms of South American bothropoid snakes reported in studies on morphological, molecular data and feeding habits, exhibiting distinct molecular signatures for each venom. Considering the complexity of N-glycan moieties generally found in glycoproteins, characterized by different degrees of branching, isomer structures, and variable abundances, our findings point to these factors as another level of complexity in Bothrops venoms, features that could dramatically contribute to their distinct biological activities.
Aird,
Snake venoms are integrated systems, but abundant venom proteins evolve more rapidly.
2015, Pubmed
Aird,
Snake venoms are integrated systems, but abundant venom proteins evolve more rapidly.
2015,
Pubmed
Andrade-Silva,
Proteomic and Glycoproteomic Profilings Reveal That Post-translational Modifications of Toxins Contribute to Venom Phenotype in Snakes.
2016,
Pubmed
,
Echinobase
Apweiler,
On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database.
1999,
Pubmed
Ashline,
Structural documentation of glycan epitopes: sequential mass spectrometry and spectral matching.
2014,
Pubmed
Bernardoni,
Functional variability of snake venom metalloproteinases: adaptive advantages in targeting different prey and implications for human envenomation.
2014,
Pubmed
Bigge,
Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid.
1995,
Pubmed
Casewell,
Dynamic evolution of venom proteins in squamate reptiles.
2012,
Pubmed
Chen,
Glycoengineering approach to half-life extension of recombinant biotherapeutics.
2012,
Pubmed
Chen,
New insights into the functions and N-glycan structures of factor X activator from Russell's viper venom.
2008,
Pubmed
Cooper,
GlycoMod--a software tool for determining glycosylation compositions from mass spectrometric data.
2001,
Pubmed
Deshimaru,
Accelerated evolution of crotalinae snake venom gland serine proteases.
1996,
Pubmed
Doley,
Protein complexes in snake venom.
2009,
Pubmed
Fernández,
Snake venomics of Micrurus alleni and Micrurus mosquitensis from the Caribbean region of Costa Rica reveals two divergent compositional patterns in New World elapids.
2015,
Pubmed
Fox,
Exploring snake venom proteomes: multifaceted analyses for complex toxin mixtures.
2008,
Pubmed
Fox,
Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity.
2008,
Pubmed
Fry,
Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia).
2008,
Pubmed
Gavel,
Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering.
1990,
Pubmed
Geyer,
Structure and characterization of the glycan moiety of L-amino-acid oxidase from the Malayan pit viper Calloselasma rhodostoma.
2001,
Pubmed
Gonçalves-Machado,
Combined venomics, venom gland transcriptomics, bioactivities, and antivenomics of two Bothrops jararaca populations from geographic isolated regions within the Brazilian Atlantic rainforest.
2016,
Pubmed
Gowda,
Factor X-activating glycoprotein of Russell's viper venom. Polypeptide composition and characterization of the carbohydrate moieties.
1994,
Pubmed
Gowda,
Structure of the major oligosaccharide of cobra venom factor.
1992,
Pubmed
Gowda,
N-linked oligosaccharides of cobra venom factor contain novel alpha(1-3)galactosylated Le(x) structures.
2001,
Pubmed
Grazziotin,
Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic Forest.
2006,
Pubmed
Gutiérrez,
Snakebite envenoming from a global perspective: Towards an integrated approach.
2010,
Pubmed
Guércio,
Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox.
2006,
Pubmed
Huang,
Cobra venom proteome and glycome determined from individual snakes of Naja atra reveal medically important dynamic range and systematic geographic variation.
2015,
Pubmed
Igarashi,
Crystal structures of catrocollastatin/VAP2B reveal a dynamic, modular architecture of ADAM/adamalysin/reprolysin family proteins.
2007,
Pubmed
Isaji,
Functional roles of the bisecting GlcNAc in integrin-mediated cell adhesion.
2010,
Pubmed
Jitsuhara,
Chaperone-like functions of high-mannose type and complex-type N-glycans and their molecular basis.
2002,
Pubmed
Jones,
Controlling N-linked glycan site occupancy.
2005,
Pubmed
Jorge,
Venomics and antivenomics of Bothrops erythromelas from five geographic populations within the Caatinga ecoregion of northeastern Brazil.
2015,
Pubmed
Joseph,
Occurrence of O-linked Xyl-GlcNAc and Xyl-Glc disaccharides in trocarin, a factor Xa homolog from snake venom.
2003,
Pubmed
Junqueira-de-Azevedo,
Venom-related transcripts from Bothrops jararaca tissues provide novel molecular insights into the production and evolution of snake venom.
2015,
Pubmed
Lannoo,
Review/N-glycans: The making of a varied toolbox.
2015,
Pubmed
Leymarie,
Effective use of mass spectrometry for glycan and glycopeptide structural analysis.
2012,
Pubmed
Lin,
Terminal disialylated multiantennary complex-type N-glycans carried on acutobin define the glycosylation characteristics of the Deinagkistrodon acutus venom.
2011,
Pubmed
Lochnit,
Carbohydrate structure analysis of batroxobin, a thrombin-like serine protease from Bothrops moojeni venom.
1995,
Pubmed
Lomonte,
Venoms of Micrurus coral snakes: Evolutionary trends in compositional patterns emerging from proteomic analyses.
2016,
Pubmed
Menezes,
Sex-based individual variation of snake venom proteome among eighteen Bothrops jararaca siblings.
2006,
Pubmed
Miwa,
The bisecting GlcNAc in cell growth control and tumor progression.
2012,
Pubmed
Nagae,
Recognition of bisecting N-acetylglucosamine: structural basis for asymmetric interaction with the mouse lectin dendritic cell inhibitory receptor 2.
2013,
Pubmed
Nawarak,
Analysis of lectin-bound glycoproteins in snake venom from the Elapidae and Viperidae families.
2004,
Pubmed
Nikai,
Primary structure and functional characterization of bilitoxin-1, a novel dimeric P-II snake venom metalloproteinase from Agkistrodon bilineatus venom.
2000,
Pubmed
O'Sullivan,
N-linked glycan truncation causes enhanced clearance of plasma-derived von Willebrand factor.
2016,
Pubmed
Ohno,
Molecular evolution of myotoxic phospholipases A2 from snake venom.
2003,
Pubmed
Pabst,
Comparison of fluorescent labels for oligosaccharides and introduction of a new postlabeling purification method.
2009,
Pubmed
Pfeiffer,
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.
1992,
Pubmed
Pla,
Proteomic analysis of venom variability and ontogeny across the arboreal palm-pitvipers (genus Bothriechis).
2017,
Pubmed
Prien,
The high mannose glycans from bovine ribonuclease B isomer characterization by ion trap MS.
2009,
Pubmed
Roth,
Protein N-glycosylation, protein folding, and protein quality control.
2010,
Pubmed
Rydz,
The C-type lectin receptor CLEC4M binds, internalizes, and clears von Willebrand factor and contributes to the variation in plasma von Willebrand factor levels.
2013,
Pubmed
Rägo,
Treating snake bites--a call for partnership.
2015,
Pubmed
Sanz,
Insights into the Evolution of a Snake Venom Multi-Gene Family from the Genomic Organization of Echis ocellatus SVMP Genes.
2016,
Pubmed
Serrano,
Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved.
2005,
Pubmed
Smirnov,
Chemical Polysialylation of Recombinant Human Proteins.
2015,
Pubmed
Sousa,
Comparison of phylogeny, venom composition and neutralization by antivenom in diverse species of bothrops complex.
2013,
Pubmed
Steirer,
The asialoglycoprotein receptor regulates levels of plasma glycoproteins terminating with sialic acid alpha2,6-galactose.
2009,
Pubmed
Takahashi,
Core fucose and bisecting GlcNAc, the direct modifiers of the N-glycan core: their functions and target proteins.
2009,
Pubmed
Tanaka,
Novel structure of the N-acetylgalactosamine containing N-glycosidic carbohydrate chain of batroxobin, a thrombin-like snake venom enzyme.
1992,
Pubmed
Tashima,
Peptidomics of three Bothrops snake venoms: insights into the molecular diversification of proteomes and peptidomes.
2012,
Pubmed
Tian,
Characterization of disease-associated N-linked glycoproteins.
2013,
Pubmed
Varki,
Sialic acids in human health and disease.
2008,
Pubmed
Varki,
2009,
Pubmed
Varki,
Cellular Organization of Glycosylation
2009,
Pubmed
Wang,
Correlation between the glycan variations and defibrinogenating activities of acutobin and its recombinant glycoforms.
2014,
Pubmed
Wormald,
Glycoproteins: glycan presentation and protein-fold stability.
1999,
Pubmed
Wujek,
N-glycosylation is crucial for folding, trafficking, and stability of human tripeptidyl-peptidase I.
2004,
Pubmed
Yamashiro,
Proteoforms of the platelet-aggregating enzyme PA-BJ, a serine proteinase from Bothrops jararaca venom.
2014,
Pubmed
Zelanis,
Proteomic identification of gender molecular markers in Bothrops jararaca venom.
2016,
Pubmed
Zelanis,
Analysis of the ontogenetic variation in the venom proteome/peptidome of Bothrops jararaca reveals different strategies to deal with prey.
2010,
Pubmed
Zelanis,
N-glycome profiling of Bothrops jararaca newborn and adult venoms.
2012,
Pubmed