In-Depth Venome of the Brazilian Rattlesnake Crotalus durissus terrificus: An Integrative Approach Combining Its Venom Gland Transcriptome and Venom Proteome
Wiezel, G. A.; Shibao, P. Y. T.; Cologna, C. T.et al.
2018 • In Journal of Proteome Research, 17 (11), p. 3941-3958
Wiezel, G. A.; Department of Physics and Chemistry, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Av. do Café, s/n, Ribeirão Preto, 14040-903, Brazil
Shibao, P. Y. T.; Department of Physics and Chemistry, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Av. do Café, s/n, Ribeirão Preto, 14040-903, Brazil
Cologna, C. T.; Department of Physics and Chemistry, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Av. do Café, s/n, Ribeirão Preto, 14040-903, Brazil
Morandi Filho, R.; Laboratory of Genetics, Biotechnology Institute, Federal University of Uberlândia, Rua Acre, s/n, Uberlândia, 38400-902, Brazil
Ueira-Vieira, C.; Laboratory of Genetics, Biotechnology Institute, Federal University of Uberlândia, Rua Acre, s/n, Uberlândia, 38400-902, Brazil
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie analytique inorganique
Quinton, Loïc ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie biologique
Arantes, E. C.; Department of Physics and Chemistry, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Av. do Café, s/n, Ribeirão Preto, 14040-903, Brazil
Language :
English
Title :
In-Depth Venome of the Brazilian Rattlesnake Crotalus durissus terrificus: An Integrative Approach Combining Its Venom Gland Transcriptome and Venom Proteome
Santoro, M. L.; Sousa-e-Silva, M. C. C.; Gonçalves, L. R. C.; Almeida-Santos, S. M.; Cardoso, D. F.; Laporta-Ferreira, I. L. L.; Saiki, M.; Peres, C. A.; Sano-Martins, I. S. Comparison of the biological activities in venoms from three subspecies of the South American rattlesnake (Crotalus durissus terrificus, C. durissus cascavella and C. durissus collilineatus). Comp. Biochem. Physiol., Part C: Pharmacol., Toxicol. Endocrinol. 1999, 122 (1), 61-73, 10.1016/S0742-8413(98)10079-8
Boldrini-França, J.; Corrêa-Netto, C.; Silva, M. M.; Rodrigues, R. S.; De La Torre, P.; Pérez, A.; Soares, A. M.; Zingali, R. B.; Nogueira, R. A.; Rodrigues, V. M.; Sanz, L.; Calvete, J. J. Snake venomics and antivenomics of Crotalus durissus subspecies from Brazil: assessment of geographic variation and its implication on snakebite management. J. Proteomics 2010, 73 (9), 1758-76, 10.1016/j.jprot.2010.06.001
Faure, G.; Choumet, V.; Bouchier, C.; Camoin, L.; Guillaume, J. L.; Monegier, B.; Vuilhorgne, M.; Bon, C. The origin of the diversity of crotoxin isoforms in the venom of Crotalus durissus terrificus. Eur. J. Biochem. 1994, 223 (1), 161-4, 10.1111/j.1432-1033.1994.tb18978.x
Georgieva, D.; Ohler, M.; Seifert, J.; von Bergen, M.; Arni, R. K.; Genov, N.; Betzel, C. Snake venomic of Crotalus durissus terrificus - correlation with pharmacological activities. J. Proteome Res. 2010, 9 (5), 2302-16, 10.1021/pr901042p
Calvete, J. J.; Sanz, L.; Cid, P.; de la Torre, P.; Flores-Díaz, M.; Dos Santos, M. C.; Borges, A.; Bremo, A.; Angulo, Y.; Lomonte, B.; Alape-Girón, A.; Gutiérrez, J. M. Snake venomics of the Central American rattlesnake Crotalus simus and the South American Crotalus durissus complex points to neurotoxicity as an adaptive paedomorphic trend along Crotalus dispersal in South America. J. Proteome Res. 2010, 9 (1), 528-44, 10.1021/pr9008749
Melani, R. D.; Araujo, G. D. T.; Carvalho, P. C.; Goto, L.; Nogueira, F. C. S.; Junqueira, M.; Domont, G. B. Seeing beyond the tip of the iceberg: A deep analysis of the venome of the Brazilian Rattlesnake, Crotalus durissus terrificusSeeing beyond the tip of the iceberg: A deep analysis of the venome of the Brazilian Rattlesnake, Crotalus durissus terrificus. EuPa Open Proteomics 2015, 8, 144-156, 10.1016/j.euprot.2015.05.006
Calvete, J. J.; Pérez, A.; Lomonte, B.; Sánchez, E. E.; Sanz, L. Snake venomics of Crotalus tigris: the minimalist toxin arsenal of the deadliest Nearctic rattlesnake venom. Evolutionary Clues for generating a pan-specific antivenom against crotalid type II venoms [corrected]. J. Proteome Res. 2012, 11 (2), 1382-90, 10.1021/pr201021d
Shu, Y. Z. Recent natural products based drug development: a pharmaceutical industry perspective. J. Nat. Prod. 1998, 61 (8), 1053-1071, 10.1021/np9800102
Calvete, J. J. Venomics, what else?. Toxicon 2012, 60, 427-33, 10.1016/j.toxicon.2012.05.012
Brahma, R. K.; McCleary, R. J.; Kini, R. M.; Doley, R. Venom gland transcriptomics for identifying, cataloging, and characterizing venom proteins in snakes. Toxicon 2015, 93, 1-10, 10.1016/j.toxicon.2014.10.022
Boldrini-França, J.; Rodrigues, R. S.; Fonseca, F. P.; Menaldo, D. L.; Ferreira, F. B.; Henrique-Silva, F.; Soares, A. M.; Hamaguchi, A.; Rodrigues, V. M.; Otaviano, A. R.; Homsi-Brandeburgo, M. I. Crotalus durissus collilineatus venom gland transcriptome: analysis of gene expression profile. Biochimie 2009, 91 (5), 586-95, 10.1016/j.biochi.2009.02.001
Junqueira-de-Azevedo, I. L.; Campos, P. F.; Ching, A. T.; Mackessy, S. P. Colubrid Venom Composition: An -Omics Perspective. Toxins 2016, 8 (8), 1-24, 10.3390/toxins8080230
Schuster, S. C. Next-generation sequencing transforms today's biology. Nat. Methods 2008, 5, 16-8, 10.1038/nmeth1156
Escoubas, P.; Quinton, L.; Nicholson, G. M. Venomics: unravelling the complexity of animal venoms with mass spectrometry. J. Mass Spectrom. 2008, 43 (3), 279-95, 10.1002/jms.1389
Escoubas, P.; King, G. F. Venomics as a drug discovery platform. Expert Rev. Proteomics 2009, 6 (3), 221-4, 10.1586/epr.09.45
Sunagar, K.; Morgenstern, D.; Reitzel, A. M.; Moran, Y. Ecological venomics: How genomics, transcriptomics and proteomics can shed new light on the ecology and evolution of venom. J. Proteomics 2016, 135, 62-72, 10.1016/j.jprot.2015.09.015
Blankenberg, D.; Gordon, A.; Von Kuster, G.; Coraor, N.; Taylor, J.; Nekrutenko, A.; Team, G. Manipulation of FASTQ data with Galaxy. Bioinformatics 2010, 26 (14), 1783-5, 10.1093/bioinformatics/btq281
Bolger, A. M.; Lohse, M.; Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30 (15), 2114-20, 10.1093/bioinformatics/btu170
Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data; Babraham Bioinformatics, 2010.
Grabherr, M. G.; Haas, B. J.; Yassour, M.; Levin, J. Z.; Thompson, D. A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q. D.; Chen, Z. H.; Mauceli, E.; Hacohen, N.; Gnirke, A.; Rhind, N.; di Palma, F.; Birren, B. W.; Nusbaum, C.; Lindblad-Toh, K.; Friedman, N.; Regev, A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29 (7), 644-U130, 10.1038/nbt.1883
Smith-Unna, R.; Boursnell, C.; Patro, R.; Hibberd, J. M.; Kelly, S. TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res. 2016, 26 (8), 1134-44, 10.1101/gr.196469.115
Haas, B. J.; Papanicolaou, A.; Yassour, M.; Grabherr, M.; Blood, P. D.; Bowden, J.; Couger, M. B.; Eccles, D.; Li, B.; Lieber, M.; MacManes, M. D.; Ott, M.; Orvis, J.; Pochet, N.; Strozzi, F.; Weeks, N.; Westerman, R.; William, T.; Dewey, C. N.; Henschel, R.; LeDuc, R. D.; Friedman, N.; Regev, A. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013, 8 (8), 1494-512, 10.1038/nprot.2013.084
Kim, D.; Pertea, G.; Trapnell, C.; Pimentel, H.; Kelley, R.; Salzberg, S. L. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013, 14 (4), R36, 10.1186/gb-2013-14-4-r36
Buchfink, B.; Xie, C.; Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015, 12, 59-60
Patro, R.; Duggal, G.; Love, M. I.; Irizarry, R. A.; Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 2017, 14 (4), 417-419, 10.1038/nmeth.4197
Wagner, G. P.; Kin, K.; Lynch, V. J. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 2012, 131 (4), 281-5, 10.1007/s12064-012-0162-3
Consortium, U. UniProt: a hub for protein information. Nucleic Acids Res. 2015, 43, D204-12, 10.1093/nar/gku989
Sievers, F.; Wilm, A.; Dineen, D.; Gibson, T. J.; Karplus, K.; Li, W. Z.; Lopez, R.; McWilliam, H.; Remmert, M.; Soding, J.; Thompson, J. D.; Higgins, D. G. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011, 7, 6, 10.1038/msb.2011.75
Corpet, F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988, 16 (22), 10881-90, 10.1093/nar/16.22.10881
Robert, X.; Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014, 42, W320-4, 10.1093/nar/gku316
Letunic, I.; Doerks, T.; Bork, P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2015, 43, D257-60, 10.1093/nar/gku949
Cotto-Rios, X. M.; Békés, M.; Chapman, J.; Ueberheide, B.; Huang, T. T. Deubiquitinases as a signaling target of oxidative stress. Cell Rep. 2012, 2 (6), 1475-84, 10.1016/j.celrep.2012.11.011
Zybailov, B.; Mosley, A. L.; Sardiu, M. E.; Coleman, M. K.; Florens, L.; Washburn, M. P. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 2006, 5 (9), 2339-47, 10.1021/pr060161n
Edman, P.; Begg, G. A PROTEIN SEQUENATOR. Eur. J. Biochem. 1967, 1 (1), 80, 10.1111/j.1432-1033.1967.tb00047.x
Kaas, Q.; Craik, D. J. Bioinformatics-Aided Venomics. Toxins 2015, 7 (6), 2159-2187, 10.3390/toxins7062159
Nesvizhskii, A. I. Protein identification by tandem mass spectrometry and sequence database searching. Methods Mol. Biol. 2006, 367, 87-119, 10.1385/1-59745-275-0:87
Bantscheff, M.; Lemeer, S.; Savitski, M. M.; Kuster, B. Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal. Bioanal. Chem. 2012, 404 (4), 939-65, 10.1007/s00216-012-6203-4
Calderón-Celis, F.; Encinar, J. R.; Sanz-Medel, A. Standardization approaches in absolute quantitative proteomics with mass spectrometry. Mass Spectrom. Rev. 2018, 37, 715, 10.1002/mas.21542
Zhang, J.; Xin, L.; Shan, B.; Chen, W.; Xie, M.; Yuen, D.; Zhang, W.; Zhang, Z.; Lajoie, G. A.; Ma, B. PEAKS DB: de novo sequencing assisted database search for sensitive and accurate peptide identification. Mol. Cell. Proteomics 2012, 11 (4), M111.010587, 10.1074/mcp.M111.010587
Han, Y.; Ma, B.; Zhang, K. SPIDER: software for protein identification from sequence tags with de novo sequencing error. J. Bioinf. Comput. Biol. 2005, 3 (3), 697-716, 10.1142/S0219720005001247
Nesvizhskii, A. I.; Aebersold, R. Interpretation of shotgun proteomic data: the protein inference problem. Mol. Cell. Proteomics 2005, 4 (10), 1419-40, 10.1074/mcp.R500012-MCP200
Melani, R. D.; Skinner, O. S.; Fornelli, L.; Domont, G. B.; Compton, P. D.; Kelleher, N. L. Mapping Proteoforms and Protein Complexes From King Cobra Venom Using Both Denaturing and Native Top-down Proteomics. Mol. Cell. Proteomics 2016, 15 (7), 2423-34, 10.1074/mcp.M115.056523
Morgenstern, D.; King, G. F. The venom optimization hypothesis revisited. Toxicon 2013, 63, 120-8, 10.1016/j.toxicon.2012.11.022
Paine, M. J. I.; Desmond, H. P.; Theakston, R. D. G.; Crampton, J. M. Gene expression in Echis carinatus (carpet viper) venom glands following milking. Toxicon 1992, 30 (4), 379-386, 10.1016/0041-0101(92)90534-C
Luna, M. S.; Valente, R. H.; Perales, J.; Vieira, M. L.; Yamanouye, N. Activation of Bothrops jararaca snake venom gland and venom production: a proteomic approach. J. Proteomics 2013, 94, 460-72, 10.1016/j.jprot.2013.10.026
Margres, M. J.; McGivern, J. J.; Wray, K. P.; Seavy, M.; Calvin, K.; Rokyta, D. R. Linking the transcriptome and proteome to characterize the venom of the eastern diamondback rattlesnake (Crotalus adamanteus). J. Proteomics 2014, 96, 145-58, 10.1016/j.jprot.2013.11.001
Doery, H. M.; Pearson, J. E. Phospholipase B in snake venoms and bee venom. Biochem. J. 1964, 92 (3), 599-602, 10.1042/bj0920599
Mohamed, A. H.; Kamel, A.; Ayobe, M. H. Studies of phospholipase A and B activities of Egyptian snake venoms and a scorpion toxin. Toxicon 1969, 6 (4), 293-8, 10.1016/0041-0101(69)90099-3
Bernheimer, A. W.; Linder, R.; Weinstein, S. A.; Kim, K. S. Isolation and characterization of a phospholipase B from venom of Collett's snake, Pseudechis colletti. Toxicon 1987, 25 (5), 547-54, 10.1016/0041-0101(87)90290-X
Rokyta, D. R.; Wray, K. P.; Lemmon, A. R.; Lemmon, E. M.; Caudle, S. B. A high-throughput venom-gland transcriptome for the Eastern Diamondback Rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes. Toxicon 2011, 57 (5), 657-71, 10.1016/j.toxicon.2011.01.008
Aird, S. D.; Watanabe, Y.; Villar-Briones, A.; Roy, M. C.; Terada, K.; Mikheyev, A. S. Quantitative high-throughput profiling of snake venom gland transcriptomes and proteomes (Ovophis okinavensis and Protobothrops flavoviridis). BMC Genomics 2013, 14, 790, 10.1186/1471-2164-14-790
Sanchez, E. F.; Felicori, L. F.; Chavez-Olortegui, C.; Magalhaes, H. B.; Hermogenes, A. L.; Diniz, M. V.; Junqueira-de-Azevedo, I. L.; Magalhaes, A.; Richardson, M. Biochemical characterization and molecular cloning of a plasminogen activator proteinase (LV-PA) from bushmaster snake venom. Biochim. Biophys. Acta, Gen. Subj. 2006, 1760 (12), 1762-71, 10.1016/j.bbagen.2006.08.023
Serrano, S. M.; Maroun, R. C. Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved. Toxicon 2005, 45 (8), 1115-32, 10.1016/j.toxicon.2005.02.020
Castro, H. C.; Zingali, R. B.; Albuquerque, M. G.; Pujol-Luz, M.; Rodrigues, C. R. Snake venom thrombin-like enzymes: from reptilase to now. Cell. Mol. Life Sci. 2004, 61 (7-8), 843-56, 10.1007/s00018-003-3325-z
Fox, J. W.; Serrano, S. M. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J. 2008, 275 (12), 3016-30, 10.1111/j.1742-4658.2008.06466.x
Portes-Junior, J. A.; Yamanouye, N.; Carneiro, S. M.; Knittel, P. S.; Sant'Anna, S. S.; Nogueira, F. C. S.; Junqueira, M.; Magalhaes, G. S.; Domont, G. B.; Moura-da-Silva, A. M. Unraveling the Processing and Activation of Snake Venom Metalloproteinases. J. Proteome Res. 2014, 13 (7), 3338-3348, 10.1021/pr500185a
Rokyta, D. R.; Lemmon, A. R.; Margres, M. J.; Aronow, K. The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics 2012, 13, 312, 10.1186/1471-2164-13-312
Soto, J. G.; Powell, R. L.; Reyes, S. R.; Wolana, L.; Swanson, L. J.; Sanchez, E. E.; Perez, J. C. Genetic variation of a disintegrin gene found in the American copperhead snake (Agkistrodon contortrix). Gene 2006, 373, 1-7, 10.1016/j.gene.2005.11.039
Calvete, J. J.; Marcinkiewicz, C.; Monleón, D.; Esteve, V.; Celda, B.; Juárez, P.; Sanz, L. Snake venom disintegrins: evolution of structure and function. Toxicon 2005, 45 (8), 1063-74, 10.1016/j.toxicon.2005.02.024
Lomonte, B.; Calvete, J. J. Strategies in 'snake venomics' aiming at an integrative view of compositional, functional, and immunological characteristics of venoms. J. Venomous Anim. Toxins Incl. Trop. Dis. 2017, 23, 26, 10.1186/s40409-017-0117-8
Oliveira, I. S.; Cardoso, I. A.; Bordon, K. C. F.; Carone, S. E. I.; Boldrini-França, J.; Pucca, M. B.; Zoccal, K. F.; Faccioli, L. H.; Sampaio, S. V.; Rosa, J. C.; Arantes, E. C. Global proteomic and functional analysis of Crotalus durissus collilineatus individual venom variation and its impact on envenoming. J. Proteomics 2018, 10.1016/j.jprot.2018.02.020
Chen, R. Q.; Jin, Y.; Wu, J. B.; Zhou, X. D.; Lu, Q. M.; Wang, W. Y.; Xiong, Y. L. A new protein structure of P-II class snake venom metalloproteinases: it comprises metalloproteinase and disintegrin domains. Biochem. Biophys. Res. Commun. 2003, 310 (1), 182-7, 10.1016/j.bbrc.2003.09.009
Cologna, C. T.; Rodrigues, R. S.; Santos, J.; de Pauw, E.; Arantes, E. C.; Quinton, L. Peptidomic investigation of Neoponera villosa venom by high-resolution mass spectrometry: seasonal and nesting habitat variations. J. Venomous Anim. Toxins Incl. Trop. Dis. 2018, 24, 6, 10.1186/s40409-018-0141-3
Wiezel, G. A.; dos Santos, P. K.; Cordeiro, F. A.; Bordon, K. C. F.; Selistre-de-Araujo, H. S.; Ueberheide, B.; Arantes, E. C. Identification of hyaluronidase and phospholipase B in Lachesis muta rhombeata venom. Toxicon 2015, 107, 359-368, 10.1016/j.toxicon.2015.08.029
Bordon, K. C. F.; Wiezel, G. A.; Amorim, F. G.; Arantes, E. C. Arthropod venom Hyaluronidases: biochemical properties and potential applications in medicine and biotechnology. J. Venomous Anim. Toxins Incl. Trop. Dis. 2015, 21, 43, 10.1186/s40409-015-0042-7
Bordon, K. C.; Perino, M. G.; Giglio, J. R.; Arantes, E. C. Isolation, enzymatic characterization and antiedematogenic activity of the first reported rattlesnake hyaluronidase from Crotalus durissus terrificus venom. Biochimie 2012, 94 (12), 2740-8, 10.1016/j.biochi.2012.08.014
Boldrini-França, J.; Cologna, C. T.; Pucca, M. B.; de Castro Figueiredo Bordon, K.; Amorim, F. G.; Anjolette, F. A.; Cordeiro, F. A.; Wiezel, G. A.; Cerni, F. A.; Pinheiro-Junior, E. L.; Shibao, P. Y.; Ferreira, I. G.; de Oliveira, I. S.; Cardoso, I. A.; Arantes, E. C. Minor snake venom proteins: structure, function and potential applications. Biochim. Biophys. Acta, Gen. Subj. 2017, 1861 (4), 824-838, 10.1016/j.bbagen.2016.12.022
Cherr, G. N.; Yudin, A. I.; Overstreet, J. W. The dual functions of GPI-anchored PH-20: hyaluronidase and intracellular signaling. Matrix Biol. 2001, 20 (8), 515-25, 10.1016/S0945-053X(01)00171-8
Mio, K.; Stern, R. Inhibitors of the hyaluronidases. Matrix Biol. 2002, 21 (1), 31-7, 10.1016/S0945-053X(01)00185-8
Zelanis, A.; Tashima, A. K.; Rocha, M. M. T.; Furtado, M. F.; Camargo, A. C. M.; Ho, P. L.; Serrano, S. M. T. Analysis of the Ontogenetic Variation in the Venom Proteome/Peptidome of Bothrops jararaca Reveals Different Strategies to Deal with Prey. J. Proteome Res. 2010, 9 (5), 2278-2291, 10.1021/pr901027r
Castanheira, L. E.; Rodrigues, R. S.; Boldrini-França, J.; Fonseca, F. P.; Henrique-Silva, F.; Homsi-Brandeburgo, M. I.; Rodrigues, V. M. Molecular cloning of a hyaluronidase from Bothrops pauloensis venom gland. J. Venomous Anim. Toxins Incl. Trop. Dis. 2014, 20, 25, 10.1186/1678-9199-20-25
Earl, S. T.; Birrell, G. W.; Wallis, T. P.; St Pierre, L. D.; Masci, P. P.; de Jersey, J.; Gorman, J. J.; Lavin, M. F. Post-translational modification accounts for the presence of varied forms of nerve growth factor in Australian elapid snake venoms. Proteomics 2006, 6 (24), 6554-65, 10.1002/pmic.200600263
Otrock, Z. K.; Makarem, J. A.; Shamseddine, A. I. Vascular endothelial growth factor family of ligands and receptors: review. Blood Cells, Mol., Dis. 2007, 38 (3), 258-68, 10.1016/j.bcmd.2006.12.003
Takahashi, H.; Hattori, S.; Iwamatsu, A.; Takizawa, H.; Shibuya, M. A novel snake venom vascular endothelial growth factor (VEGF) predominantly induces vascular permeability through preferential signaling via VEGF receptor-1. J. Biol. Chem. 2004, 279 (44), 46304-14, 10.1074/jbc.M403687200
Nakamura, H.; Murakami, T.; Imamura, T.; Toriba, M.; Chijiwa, T.; Ohno, M.; Oda-Ueda, N. Discovery of a novel vascular endothelial growth factor (VEGF) with no affinity to heparin in Gloydius tsushimaensis venom. Toxicon 2014, 86, 107-15, 10.1016/j.toxicon.2014.05.003
Yamazaki, Y.; Matsunaga, Y.; Tokunaga, Y.; Obayashi, S.; Saito, M.; Morita, T. Snake venom Vascular Endothelial Growth Factors (VEGF-Fs) exclusively vary their structures and functions among species. J. Biol. Chem. 2009, 284 (15), 9885-91, 10.1074/jbc.M809071200
Cebe-Suarez, S.; Zehnder-Fjallman, A.; Ballmer-Hofer, K. The role of VEGF receptors in angiogenesis; complex partnerships. Cell. Mol. Life Sci. 2006, 63 (5), 601-615, 10.1007/s00018-005-5426-3
Joukov, V.; Pajusola, K.; Kaipainen, A.; Chilov, D.; Lahtinen, I.; Kukk, E.; Saksela, O.; Kalkkinen, N.; Alitalo, K. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 1996, 15 (7), 1751, 10.1002/j.1460-2075.1996.tb00521.x
Dunn, R. D.; Broady, K. W. Snake inhibitors of phospholipase A2 enzymes. Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2001, 1533 (1), 29-37, 10.1016/S1388-1981(01)00138-X
Gimenes, S. N.; Ferreira, F. B.; Silveira, A. C.; Rodrigues, R. S.; Yoneyama, K. A.; Izabel Dos Santos, J.; Fontes, M. R.; de Campos Brites, V. L.; Santos, A. L.; Borges, M. H.; Lopes, D. S.; Rodrigues, V. M. Isolation and biochemical characterization of a γ-type phospholipase A2 inhibitor from Crotalus durissus collilineatus snake serum. Toxicon 2014, 81, 58-66, 10.1016/j.toxicon.2014.01.012
Soares, A. M.; Marcussi, S.; Stábeli, R. G.; França, S. C.; Giglio, J. R.; Ward, R. J.; Arantes, E. C. Structural and functional analysis of BmjMIP, a phospholipase A2 myotoxin inhibitor protein from Bothrops moojeni snake plasma. Biochem. Biophys. Res. Commun. 2003, 302 (2), 193-200, 10.1016/S0006-291X(03)00155-4
Junqueira-de-Azevedo, I. L.; Ching, A. T.; Carvalho, E.; Faria, F.; Nishiyama, M. Y.; Ho, P. L.; Diniz, M. R. Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of cobra (Elapidae) venoms: implications for snake toxin repertoire evolution. Genetics 2006, 173 (2), 877-89, 10.1534/genetics.106.056515
Gao, J. F.; Qu, Y. F.; Zhang, X. Q.; He, Y.; Ji, X. Neonate-to-adult transition of snake venomics in the short-tailed pit viper, Gloydius brevicaudus. J. Proteomics 2013, 84, 148-57, 10.1016/j.jprot.2013.04.003
Pla, D.; Petras, D.; Saviola, A. J.; Modahl, C. M.; Sanz, L.; Pérez, A.; Juárez, E.; Frietze, S.; Dorrestein, P. C.; Mackessy, S. P.; Calvete, J. J. Transcriptomics-guided bottom-up and top-down venomics of neonate and adult specimens of the arboreal rear-fanged Brown Treesnake, Boiga irregularis, from Guam. J. Proteomics 2018, 174, 71-84, 10.1016/j.jprot.2017.12.020
Cidade, D. A.; Simão, T. A.; Dávila, A. M.; Wagner, G.; Junqueira-de-Azevedo, I. L.; Ho, P. L.; Bon, C.; Zingali, R. B.; Albano, R. M. Bothrops jararaca venom gland transcriptome: analysis of the gene expression pattern. Toxicon 2006, 48 (4), 437-61, 10.1016/j.toxicon.2006.07.008
Salazar-Valenzuela, D.; Mora-Obando, D.; Fernández, M. L.; Loaiza-Lange, A.; Gibbs, H. L.; Lomonte, B. Proteomic and toxicological profiling of the venom of Bothrocophias campbelli, a pitviper species from Ecuador and Colombia. Toxicon 2014, 90, 15-25, 10.1016/j.toxicon.2014.07.012
Aird, S. D. Ophidian envenomation strategies and the role of purines. Toxicon 2002, 40 (4), 335-93, 10.1016/S0041-0101(01)00232-X
Dhananjaya, B. L.; D'Souza, C. J. An overview on nucleases (DNase, RNase, and phosphodiesterase) in snake venoms. Biochemistry (Moscow) 2010, 75 (1), 5-11, 10.1134/S0006297910010013
Nicolau, C. A.; Carvalho, P. C.; Junqueira-de-Azevedo, I. L.; Teixeira-Ferreira, A.; Junqueira, M.; Perales, J.; Neves-Ferreira, A. G.; Valente, R. H. An in-depth snake venom proteopeptidome characterization: Benchmarking Bothrops jararaca. J. Proteomics 2017, 151, 214, 10.1016/j.jprot.2016.06.029
Ogawa, Y.; Kanai-Azuma, M.; Akimoto, Y.; Kawakami, H.; Yanoshita, R. Exosome-like vesicles in Gloydius blomhoffii blomhoffii venom. Toxicon 2008, 51 (6), 984-93, 10.1016/j.toxicon.2008.02.003
Carneiro, S. M.; Fernandes, W.; Sant'Anna, S. S.; Yamanouye, N. Microvesicles in the venom of Crotalus durissus terrificus (Serpentes, Viperidae). Toxicon 2007, 49 (1), 106-10, 10.1016/j.toxicon.2006.04.020
Souza-Imberg, A.; Carneiro, S. M.; Giannotti, K. C.; Sant'Anna, S. S.; Yamanouye, N. Origin and characterization of small membranous vesicles present in the venom of Crotalus durissus terrificus. Toxicon 2017, 136, 27-33, 10.1016/j.toxicon.2017.06.013
Frobert, Y.; Créminon, C.; Cousin, X.; Rémy, M. H.; Chatel, J. M.; Bon, S.; Bon, C.; Grassi, J. Acetylcholinesterases from Elapidae snake venoms: biochemical, immunological and enzymatic characterization. Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1997, 1339 (2), 253-67, 10.1016/S0167-4838(97)00009-5
Ferreira, I. G. Caracterização estrutural e funcional de um fator de crescimento endotelial vascular, VEGF, da peçonha da serpente Crotalus durissus collilineatus; University of São Paulo: Ribeirão Preto, 2017.
Mashiko, H.; Takahashi, H. Cysteine proteinase inhibitors in elapid and hydrophiid snake venoms. Toxicon 2002, 40 (9), 1275-81, 10.1016/S0041-0101(02)00133-2
Vaiyapuri, S.; Wagstaff, S. C.; Watson, K. A.; Harrison, R. A.; Gibbins, J. M.; Hutchinson, E. G. Purification and functional characterisation of rhiminopeptidase A, a novel aminopeptidase from the venom of Bitis gabonica rhinoceros. PLoS Neglected Trop. Dis. 2010, 4 (8), e796, 10.1371/journal.pntd.0000796
Rawlings, N. D.; Barrett, A. J. Evolution of proteins of the cystatin superfamily. J. Mol. Evol. 1990, 30 (1), 60-71, 10.1007/BF02102453
Richards, R.; St Pierre, L.; Trabi, M.; Johnson, L. A.; de Jersey, J.; Masci, P. P.; Lavin, M. F. Cloning and characterisation of novel cystatins from elapid snake venom glands. Biochimie 2011, 93 (4), 659-68, 10.1016/j.biochi.2010.12.008
Campos, P. F.; Andrade-Silva, D.; Zelanis, A.; Paes Leme, A. F.; Rocha, M. M.; Menezes, M. C.; Serrano, S. M.; Junqueira-de-Azevedo, I. e. L. Trends in the Evolution of Snake Toxins Underscored by an Integrative Omics Approach to Profile the Venom of the Colubrid Phalotris mertensi. Genome Biol. Evol. 2016, 8 (8), 2266-87, 10.1093/gbe/evw149
Inagaki, H.; Kimoto, H.; Yamauchi, Y.; Toriba, M.; Kubo, T. Functional characterization of Kunitz-type protease inhibitor Pr-mulgins identified from New Guinean Pseudechis australis. Toxicon 2012, 59 (1), 74-80, 10.1016/j.toxicon.2011.10.005
Cheng, Y. C.; Yan, F. J.; Chang, L. S. Taiwan cobra chymotrypsin inhibitor: cloning, functional expression and gene organization. Biochim. Biophys. Acta, Proteins Proteomics 2005, 1747 (2), 213-20, 10.1016/j.bbapap.2004.11.006
Reeks, T. A.; Fry, B. G.; Alewood, P. F. Privileged frameworks from snake venom. Cell. Mol. Life Sci. 2015, 72 (10), 1939-1958, 10.1007/s00018-015-1844-z
Guo, J.; Chen, S.; Huang, C.; Chen, L.; Studholme, D. J.; Zhao, S.; Yu, L. MANSC: a seven-cysteine-containing domain present in animal membrane and extracellular proteins. Trends Biochem. Sci. 2004, 29 (4), 172-4, 10.1016/j.tibs.2004.02.007
Bycroft, M.; Bateman, A.; Clarke, J.; Hamill, S. J.; Sandford, R.; Thomas, R. L.; Chothia, C. The structure of a PKD domain from polycystin-1: implications for polycystic kidney disease. EMBO J. 1999, 18 (2), 297-305, 10.1093/emboj/18.2.297
Fernández, J.; Gutiérrez, J. M.; Calvete, J. J.; Sanz, L.; Lomonte, B. Characterization of a novel snake venom component: Kazal-type inhibitor-like protein from the arboreal pitviper Bothriechis schlegelii. Biochimie 2016, 125, 83-90, 10.1016/j.biochi.2016.03.004
Bordon, K. C. F.; Wiezel, G. A.; Cabral, H.; Arantes, E. C. Bordonein-L, a new L-amino acid oxidase from Crotalus durissus terrificus snake venom: isolation, preliminary characterization and enzyme stability. J. Venomous Anim. Toxins Incl. Trop. Dis. 2015, 21, 26, 10.1186/s40409-015-0025-8
Wiezel, G. A. Caracterização bioquímica e avaliação in vitro da ativação de fibroblastos e do potencial leishmanicida de uma L-aminoácido oxidase (LAAO) da peçonha de Crotalus durissus terrificus; Universidade de São Paulo: Ribeirão Preto, 2016.
Rádis-Baptista, G.; Kubo, T.; Oguiura, N.; Prieto da Silva, A. R.; Hayashi, M. A.; Oliveira, E. B.; Yamane, T. Identification of crotasin, a crotamine-related gene of Crotalus durissus terrificus. Toxicon 2004, 43 (7), 751-9, 10.1016/j.toxicon.2004.02.023
Pung, Y. F.; Wong, P. T.; Kumar, P. P.; Hodgson, W. C.; Kini, R. M. Ohanin, a novel protein from king cobra venom, induces hypolocomotion and hyperalgesia in mice. J. Biol. Chem. 2005, 280 (13), 13137-47, 10.1074/jbc.M414137200
Pung, Y. F.; Kumar, S. V.; Rajagopalan, N.; Fry, B. G.; Kumar, P. P.; Kini, R. M. Ohanin, a novel protein from king cobra venom: its cDNA and genomic organization. Gene 2006, 371 (2), 246-56, 10.1016/j.gene.2005.12.002
Kini, R. M.; Doley, R. Structure, function and evolution of three-finger toxins: mini proteins with multiple targets. Toxicon 2010, 56 (6), 855-67, 10.1016/j.toxicon.2010.07.010
Falcao, C. B.; de La Torre, B. G.; Pérez-Peinado, C.; Barron, A. E.; Andreu, D.; Rádis-Baptista, G. Vipericidins: a novel family of cathelicidin-related peptides from the venom gland of South American pit vipers. Amino Acids 2014, 46 (11), 2561-71, 10.1007/s00726-014-1801-4
de Oliveira, N. G.; Cardoso, M.; Franco, O. L. Snake venoms: attractive antimicrobial proteinaceous compounds for therapeutic purposes. Cell. Mol. Life Sci. 2013, 70 (24), 4645-4658, 10.1007/s00018-013-1345-x
Nair, D. G.; Fry, B. G.; Alewood, P.; Kumar, P. P.; Kini, R. M. Antimicrobial activity of omwaprin, a new member of the waprin family of snake venom proteins. Biochem. J. 2007, 402 (1), 93-104, 10.1042/BJ20060318
Falcao, C. B.; Pérez-Peinado, C.; de la Torre, B. G.; Mayol, X.; Zamora-Carreras, H.; Jiménez, M.; Rádis-Baptista, G.; Andreu, D. Structural Dissection of Crotalicidin, a Rattlesnake Venom Cathelicidin, Retrieves a Fragment with Antimicrobial and Antitumor Activity. J. Med. Chem. 2015, 58 (21), 8553-63, 10.1021/acs.jmedchem.5b01142
Bandeira, I. C. J.; Bandeira-Lima, D.; Mello, C. P.; Pereira, T. P.; De Menezes, R. R. P. P.; Sampaio, T. L.; Falcão, C. B.; Rádis-Baptista, G.; Martins, A. M. C. Antichagasic effect of crotalicidin, a cathelicidin-like vipericidin, found in Crotalus durissus terrificus rattlesnake's venom gland. Parasitology 2018, 145, 1-6, 10.1017/S0031182017001846
Aird, S. D. Snake venom dipeptidyl peptidase IV: taxonomic distribution and quantitative variation. Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 2008, 150 (2), 222-8, 10.1016/j.cbpb.2008.03.005
Rawlings, N. D.; Barrett, A. J. Evolutionary families of peptidases. Biochem. J. 1993, 290, 205-218, 10.1042/bj2900205
Chaim, O. M.; da Silveira, R. B.; Trevisan-Silva, D.; Ferrer, V. P.; Sade, Y. B.; Bóia-Ferreira, M.; Gremski, L. H.; Gremski, W.; Senff-Ribeiro, A.; Takahashi, H. K.; Toledo, M. S.; Nader, H. B.; Veiga, S. S. Phospholipase-D activity and inflammatory response induced by brown spider dermonecrotic toxin: endothelial cell membrane phospholipids as targets for toxicity. Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2011, 1811 (2), 84-96, 10.1016/j.bbalip.2010.11.005
Tambourgi, D. V.; Magnoli, F. C.; van den Berg, C. W.; Morgan, B. P.; de Araujo, P. S.; Alves, E. W.; Da Silva, W. D. Sphingomyelinases in the venom of the spider Loxosceles intermedia are responsible for both dermonecrosis and complement-dependent hemolysis. Biochem. Biophys. Res. Commun. 1998, 251 (1), 366-73, 10.1006/bbrc.1998.9474
Vonk, F. J.; Casewell, N. R.; Henkel, C. V.; Heimberg, A. M.; Jansen, H. J.; McCleary, R. J.; Kerkkamp, H. M.; Vos, R. A.; Guerreiro, I.; Calvete, J. J.; Wüster, W.; Woods, A. E.; Logan, J. M.; Harrison, R. A.; Castoe, T. A.; de Koning, A. P.; Pollock, D. D.; Yandell, M.; Calderon, D.; Renjifo, C.; Currier, R. B.; Salgado, D.; Pla, D.; Sanz, L.; Hyder, A. S.; Ribeiro, J. M.; Arntzen, J. W.; van den Thillart, G. E.; Boetzer, M.; Pirovano, W.; Dirks, R. P.; Spaink, H. P.; Duboule, D.; McGlinn, E.; Kini, R. M.; Richardson, M. K. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (51), 20651-6, 10.1073/pnas.1314702110
Brown, W. M.; Dziegielewska, K. M. Friends and relations of the cystatin superfamily - new members and their evolution. Protein Sci. 1997, 6 (1), 5-12, 10.1002/pro.5560060102
Tsuchida-Straeten, N.; Ensslen, S.; Schäfer, C.; Wöltje, M.; Denecke, B.; Moser, M.; Gräber, S.; Wakabayashi, S.; Koide, T.; Jahnen-Dechent, W. Enhanced blood coagulation and fibrinolysis in mice lacking histidine-rich glycoprotein (HRG). J. Thromb. Haemostasis 2005, 3 (5), 865-72, 10.1111/j.1538-7836.2005.01238.x
Casewell, N. R.; Harrison, R. A.; Wüster, W.; Wagstaff, S. C. Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics 2009, 10, 564, 10.1186/1471-2164-10-564
