Combined venomics, venom gland transcriptomics, bioactivities, and antivenomics of two Bothrops jararaca populations from geographic isolated regions within the Brazilian Atlantic rainforest

Journal of Proteomics - Tập 135 - Trang 73-89 - 2016
Larissa Gonçalves Machado1,2,3, Davinia Plá3, Líbia Sanz3, Roberta Jeane Bezerra Jorge4, Moema Leitão-de-Araújo5, Maria Lúcia Machado Alves5, Diego Janisch Alvares6, Joari De Miranda7, Jenifer Nowatzki7, Karen de Morais-Zani8, Wilson Roberto Fernandes8, Anita Mitico Tanaka-Azevedo8, Julián Fernández9, Russolina B. Zingali1,2, José Marı́a Gutiérrez9, Carlos Corrêa-Netto1,10,2, Juan J. Calvete3
1Instituto Nacional de Biologia Estrutural e Bioimagem, Rede Proteomica do Rio de Janeiro, Universidade Federal do Rio de Janeiro (UFRJ), Brazil
2Instituto de Bioquímica Médica, Programa de Biologia Estrutural, Laboratório de Hemostase e Venenos, Universidade Federal do Rio de Janeiro (UFRJ), Brazil
3Laboratorio de Venómica Estructural y Funcional, Instituto de Biomedicina de Valencia, CSIC, Valencia, Spain
4Departamento de Fisiologia e Farmacologia, Universidade Federal do Ceará (UFC), Fortaleza 60430-270, Brazil
5Fundação Zoobotânica do Rio Grande do Sul, Museu de Ciências Naturais, Núcleo Regional de Ofiologia de Porto Alegre, RS, Brazil
6Laboratorio de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçãlves 9500, Agronomia, 91501-970 Porto Alegre, RS, Brazil
7Hygeia Biotecnologia Aplicada S.A., Fundação Bio-Rio, Rio de Janeiro, Brazil
8Laboratorio de Herpetologia, Instituto Butantan, Avenida Vital Brazil 1500, São Paulo 05503-900, SP, Brazil
9Instituto Clodomiro Picado, Facultad de Microbiología, Universidad de Costa Rica, San José, Costa Rica
10Instituto Vital Brazil, Niterói, Rio de Janeiro, Brazil

Tóm tắt

Từ khóa


Tài liệu tham khảo

Campbell, 2004

Sazima, 1992, Natural history of the jararaca pitviper, Bothrops jararaca, in Southeastern Brazil, 199

Grazziotin, 2006, Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic Forest, Mol Ecol, 15, 3969, 10.1111/j.1365-294X.2006.03057.x

Martins, 2002, Ecological and phylogenetic correlates of feeding habits in Neotropical pitvipers of the genus Bothrops, 1

Cardoso, 1990, Bothropic accidents, Mem Inst Butantan, 52, 43

Ministério da Saúde do Brasil, 1996, Normas de Produção e Controle de Qualidade de Soros Antiofıdicos, 23491

Ministério da Saúde do Brasil/FUNASA (Fundação Nacional de Saúde)., 1998, Manual de diagnóstico e tratamento de acidentes por animais peçonhentos. COMED/ASPLAN/FNS, Brasília, 1

Warrell, 2004, Snakebites in Central and South America: epidemiology, clinical features, and clinical management, 709

Brown, 1973

Rosenfeld, 1971, Symptomatology, pathology and treatment of snake bites in South America, 1971, 345

França, 2003, Acidente botrópico, 81

Gibbs, 2009, Functional basis of a molecular adaptation: prey-specific toxic effects of venom from Sistrurus rattlesnakes, Toxicon, 53, 672, 10.1016/j.toxicon.2009.01.034

Fry, 2012, The structural and functional diversification of the Toxicofera reptile venom system, Toxicon, 60, 434, 10.1016/j.toxicon.2012.02.013

Casewell, 2013, Complex cocktails: the evolutionary novelty of venoms, Trends Ecol Evol, 28, 219, 10.1016/j.tree.2012.10.020

Calvete, 2013, Snake venomics: from the inventory of toxins to biology, Toxicon, 75, 44, 10.1016/j.toxicon.2013.03.020

Vonk, 2013, The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system, Proc Natl Acad Sci U S A, 110, 20651, 10.1073/pnas.1314702110

Schield, 2015, A role for genomics in rattlesnake research — current knowledge and future potential

Shaney, 2015, Squamate reptile genomics and evolution

Fox, 2006, Comparison of indirect and direct approaches using ion-trap and Fourier transform ion cyclotron resonance mass spectrometry for exploring viperid venom proteomes, Toxicon, 47, 700, 10.1016/j.toxicon.2006.01.022

Menezes, 2006, Sex-based individual variation of snake venom proteome among eighteen Bothrops jararaca siblings, Toxicon, 47, 304, 10.1016/j.toxicon.2005.11.007

Pimenta, 2007, Mass spectrometric analysis of the individual variability of Bothrops jararaca venom peptide fraction. Evidence for sex-based variation among the bradykinin-potentiating peptides, Rapid Commun Mass Spectrom, 21, 1034, 10.1002/rcm.2931

Zelanis, 2010, Analysis of the ontogenetic variation in the venom proteome/peptidome of Bothrops jararaca reveals different strategies to deal with prey, J Proteome Res, 9, 2278, 10.1021/pr901027r

Zelanis, 2011, Bothrops jararaca venom proteome rearrangement upon neonate to adult transition, Proteomics, 11, 4218, 10.1002/pmic.201100287

Zelanis, 2012, N-glycome profiling of Bothrops jararaca newborn and adult venoms, J Proteomics, 75, 774, 10.1016/j.jprot.2011.09.017

Tashima, 2012, Peptidomics of three Bothrops snake venoms: insights into the molecular diversification of proteomes and peptidomes, Mol Cell Proteomics, 11, 1245, 10.1074/mcp.M112.019331

Dias, 2013, Individual variability in the venom proteome of juvenile Bothrops jararaca specimens, J Proteome Res, 12, 4585, 10.1021/pr4007393

Sousa, 2013, Comparison of phylogeny, venom composition and neutralization by antivenom in diverse species of bothrops complex, PLoS Negl Trop Dis, 7, e2442, 10.1371/journal.pntd.0002442

Cidade, 2006, Bothrops jararaca venom gland transcriptome: analysis of the gene expression pattern, Toxicon, 48, 437, 10.1016/j.toxicon.2006.07.008

Zelanis, 2012, A transcriptomic view of the proteome variability of newborn and adult Bothrops jararaca snake venoms, PLoS Negl Trop Dis, 6, e1554, 10.1371/journal.pntd.0001554

Vellard, 1937, Variation géographique du venin de Bothrops atrox, C. R Acad Sci, 204, 1369

Vellard, 1939, Variation géographique du venin de Crotalus terrificus, C R Soc Biol, 130, 463

Chippaux, 1991, Snake venom variability: methods of study, results and interpretation, Toxicon, 29, 1279, 10.1016/0041-0101(91)90116-9

Glenn, 1978, Mojave rattlesnake Crotalus scutulatus scutulatus venom: variation in toxicity with geographical origin, Toxicon, 16, 81, 10.1016/0041-0101(78)90065-X

Massey, 2012, Venom variability and envenoming severity outcomes of the Crotalus scutulatus scutulatus (Mojave rattlesnake) from Southern Arizona, J Proteomics, 75, 2576, 10.1016/j.jprot.2012.02.035

Calvete, 2011, Snake population venomics and antivenomics of Bothrops atrox: paedomorphism along its transamazonian dispersal and implications of geographic venom variability on snakebite management, J Proteomics, 74, 510, 10.1016/j.jprot.2011.01.003

Furtado, 1991, Mem Inst Butantan, 53, 149

Calvete, 2014, Omics meets biology: application to the design and preclinical assessment of antivenoms, Toxins, 6, 3388, 10.3390/toxins6123388

WHO, 2010

Pla, 2012, Second generation snake antivenomics: comparing immunoaffinity and immunodepletion protocols, Toxicon, 60, 688, 10.1016/j.toxicon.2012.04.342

Raw, 1991, Antivenins in Brazil: preparation, 557

Angulo, 1997, Clinical and laboratory alterations in horses during immunization with snake venoms for the production of polyvalent (Crotalinae) antivenom, Toxicon, 35, 81, 10.1016/S0041-0101(96)00077-3

Rojas, 1994, Caprylic acid fractionation of hyperimmune horse plasma: description of a simple procedure for antivenom production, Toxicon, 32, 59, 10.1016/0041-0101(94)90087-6

Paine, 1992, Gene expression in Echis carinatus (carpet viper) venom glands following milking, Toxicon, 30, 379, 10.1016/0041-0101(92)90534-C

Margulies, 2005, Genome sequencing in microfabricated high-density picolitre reactors, Nature, 437, 376, 10.1038/nature03959

Altschul, 1990, Basic local alignment search tool, J Mol Biol, 215, 403, 10.1016/S0022-2836(05)80360-2

Conesa, 2005, Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research, Bioinformatics, 21, 3674, 10.1093/bioinformatics/bti610

Mortazavi, 2008, Mapping and quantifying mammalian transcriptomes by RNA-Seq, Nat Methods, 5, 621, 10.1038/nmeth.1226

Durban, 2013, Integrated “omics” profiling indicates that miRNAs are modulators of the ontogenetic venom composition shift in the Central American rattlesnake Crotalus simus simus, BMC Genomics, 14, 234, 10.1186/1471-2164-14-234

Jorge, 2015, Venomics and antivenomics of Bothrops erythromelas from five geographic populations within the Caatinga ecoregion of northeastern Brazil, J Proteomics, 114, 93, 10.1016/j.jprot.2014.11.011

Calvete, 2011, Proteomic tools against the neglected pathology of snake bite envenoming, Expert Rev Proteomics, 8, 739, 10.1586/epr.11.61

Calvete, 2014, Next-generation snake venomics: protein-locus resolution through venom proteome decomplexation, Expert Rev Proteomics, 11, 315, 10.1586/14789450.2014.900447

Gutiérrez, 1985, Neutralization of proteolytic and hemorrhagic activities of Costa Rican snake venoms by a polyvalent antivenom, Toxicon, 23, 887, 10.1016/0041-0101(85)90380-0

Theakston, 1983, Development of simple standard procedures for the characterisation of snake venom, Bull World Health Organ, 61, 949

Gené, 1989, Comparative study on coagulant, defibrinating, fibrinolytic and fibrinogenolytic activities of Costa Rican crotaline snake venoms and their neutralization by a polyvalent antivenom, Toxicon, 27, 841, 10.1016/0041-0101(89)90096-2

Holzer, 1996, An aqueous endpoint assay of snake venom phospholipase A2, Toxicon, 34, 1149, 10.1016/0041-0101(96)00057-8

Wang, 2004, A novel P-I class metalloproteinase with broad substrate-cleaving activity, agkislysin, from Agkistrodon acutus venom, Biochem Biophys Res Commun, 324, 224, 10.1016/j.bbrc.2004.09.031

Johnstone, 1987

Tiffin, 2014, Advances and limits of using population genetics to understand local adaptation, Trends Ecol Evol, 29, 673, 10.1016/j.tree.2014.10.004

Savolainen, 2013, Ecological genomics of local adaptation, Nat Rev Genet, 14, 807, 10.1038/nrg3522

Lynch, 2010, Evolution of the mutation rate, Trends Genet, 26, 345, 10.1016/j.tig.2010.05.003

Casewell, 2014, Medically important differences in snake venom composition are dictated by distinct postgenomic mechanisms, Proc Natl Acad Sci U S A, 111, 9205, 10.1073/pnas.1405484111

Schenberg, 1959, Geographical pattern of crotamine distribution in the same rattlesnake subspecies, Science, 129, 1361, 10.1126/science.129.3359.1361

Wooldridge, 2001, Mojave rattlesnakes (Crotalus scutulatus scutulatus) lacking the acidic subunit DNA sequence lack Mojave toxin in their venom, Comp Biochem Physiol B Biochem Mol Biol, 130, 169, 10.1016/S1096-4959(01)00422-5

Wang, 2010, Absence of phospholipase A2 in most Crotalus horridus venom due to translation blockage: comparison with Crotalus horridus atricaudatus venom, Toxicon, 56, 93, 10.1016/j.toxicon.2010.03.015

Alape-Girón, 2008, Snake venomics of the lancehead pitviper Bothrops asper. Geographic, individual and ontogenetic variations, J Proteome Res, 7, 3556, 10.1021/pr800332p

Madrigal, 2012, Snake venomics across genus Lachesis Ontogenetic changes in the venom composition of L. stenophrys and comparative proteomics of the venoms of adult L. melanocephala and L. acrochorda, J. Proteomics, 77, 280, 10.1016/j.jprot.2012.09.003

Cogo, 2006, Purification, sequencing and structural analysis of two acidic phospholipases A2 from the venom of Bothrops insularis (jararaca ilhoa), Biochimie, 88, 1947, 10.1016/j.biochi.2006.10.006

de Azevedo IL, 2001, Molecular cloning and expression of a functional snake venom vascular endothelium growth factor (VEGF) from the Bothrops insularis pit viper. A new member of the VEGF family of proteins, J Biol Chem, 276, 39836, 10.1074/jbc.M106531200

Rocha, 2014, Seasonal, daily activity, and habitat use by three sympatric pit vipers (Serpentes, Viperidae) from southern Brazil, An Acad Bras Cienc, 86, 695, 10.1590/0001-37652014119013

Salomão, 1999, mtDNA phylogeny of neotropical pitvipers of the genus Bothrops (Squamata: Serpentes: Viperidae), Kaupia, 8, 127

Fenwick, 2009, Morphological and molecular evidence for phylogeny and classification of South American pitvipers, genera Bothrops, Bothriopsis, and Bothrocophias (Serpentes: Viperidae), Zool J Linn Soc, 156, 617, 10.1111/j.1096-3642.2008.00495.x

Carrasco, 2012, Morphology, phylogeny and taxonomy of South American bothropoid pitvipers (Serpentes, Viperidae), Zool Scr, 41, 109, 10.1111/j.1463-6409.2011.00511.x

Antunes, 2010, Comparative analysis of newborn and adult Bothrops jararaca snake venoms, Toxicon, 56, 1443, 10.1016/j.toxicon.2010.08.011

Berger, 2008, Purification and functional characterization of bothrojaractivase, a prothrombin-activating metalloproteinase isolated from Bothrops jararaca snake venom, Toxicon, 51, 488, 10.1016/j.toxicon.2007.09.005

Nishida, 1994, Purification and characterization of bothrombin, a fibrinogen-clotting serine protease from the venom of Bothrops jararaca, Biochemistry, 33, 1843, 10.1021/bi00173a030

Serrano, 1999, A novel phospholipase A2, BJ-PLA2, from the venom of the snake Bothrops jararaca: purification, primary structure analysis, and its characterization as a platelet aggregation-inhibiting factor, Arch Biochem Biophys, 367, 26, 10.1006/abbi.1999.1230

Homsi-Brandeburgo, 1988, Fractionation of Bothrops jararacussu snake venom: partial chemical characterization and biological activity of bothropstoxin, Toxicon, 26, 615, 10.1016/0041-0101(88)90244-9

Andrião-Escarso, 2000, Myotoxic phospholipases A2 in Bothrops snake venoms: effect of chemical modifications on the enzymatic and pharmacological properties of bothropstoxins from Bothrops jararacussu, Biochimie, 82, 755, 10.1016/S0300-9084(00)01150-0

Neto, 2005, Microvessel damage by B. jararacussu snake venom: pathogenesis and influence on muscle regeneration, Toxicon, 46, 814, 10.1016/j.toxicon.2005.08.013

Oshima-Franco, 2004, The presynaptic activity of bothropstoxin-I, a myotoxin from Bothrops jararacussu snake venom, Basic Clin Pharmacol Toxicol, 95, 175, 10.1111/j.1742-7843.2004.pto_950405.x

Marques, 2002, A new insular species of pitviper from Brazil, with comments on evolutionary biology and conservation of the Bothrops jararaca group (Serpentes, Viperidae), Herpetologica, 58, 303, 10.1655/0018-0831(2002)058[0303:ANISOP]2.0.CO;2

Wüster, 2005, Morphological correlates of incipient arboreality and ornithophagy in island pitvipers, and the phylogenetic position of Bothrops insularis, J Zool, 266, 1, 10.1017/S0952836904006247

Duarte, 1995, A biological survey of the pitviper Bothrops insularis Amaral (Serpentes: Viperidae): an endemic and threatened offshore island snake of Southeastern Brazil, Stud Neotropical Fauna Environ, 30, 1, 10.1080/01650529509360936

Marques, 2012, The Golden Lancehead Bothrops insularis (Serpentes: Viperidae) relies on two seasonally plentiful bird species visiting its island habitat, J Nat Hist, 46, 885, 10.1080/00222933.2011.654278

Daltry, 1996, Diet and snake venom evolution, Nature, 379, 537, 10.1038/379537a0

Cogo, 1998, An unusual presynaptic action of Bothrops insularis snake venom mediated by phospholipase A2 fraction, Toxicon, 36, 1323, 10.1016/S0041-0101(97)00174-8

Queiroz, 2008, Interspecific variation in venom composition and toxicity of Brazilian snakes from Bothrops genus, Toxicon, 52, 842, 10.1016/j.toxicon.2008.10.002

Oshima-Franco, 2000, Neutralizing capacity of commercial bothropic antivenom against Bothrops jararacussu venom and bothropstoxin-I, Muscle Nerve, 23, 1832, 10.1002/1097-4598(200012)23:12<1832::AID-MUS6>3.0.CO;2-F

Cardoso, 1993, Randomized comparative trial of three antivenoms in the treatment of envenoming by lance-headed vipers (Bothrops jararaca) in São Paulo Brazil, Q J Med, 86, 315

Greene, 1997

Shine, 2000, Snakes: a new ‘model organism’ in ecological research?, Trends Ecol Evol, 15, 221, 10.1016/S0169-5347(00)01853-X

Connell, 1980, Diversity and the coevolution of competitors, or the ghost of competition past, Oikos, 35, 131, 10.2307/3544421

Steen, 2014, Snake co-occurrence patterns are best explained by habitat and hypothesized effects of interspecific interactions, J Anim Ecol, 83, 286, 10.1111/1365-2656.12121

Reinert, 1984, Habitat separation between sympatric snake populations, Ecology, 65, 478, 10.2307/1941410

Luiselli, 2006, Resource partitioning and interspecific competition in snakes: the search for general geographical and guild patterns, Oikos, 114, 193, 10.1111/j.2006.0030-1299.14064.x

Sih, 1985, Predation, competition, and prey communities: a review of field experiments, Annu Rev Ecol Syst, 16, 269, 10.1146/annurev.es.16.110185.001413

Diz, 2012, Proteomics in evolutionary ecology: linking the genotype with the phenotype, Mol Ecol, 21, 1060, 10.1111/j.1365-294X.2011.05426.x

Salomão, 1996, DNA evolution of South American pitvipers of the genus Bothrops (Reptilia: Serpentes: Viperidae), 89, 10.1093/oso/9780198549864.003.0007

Amaro, 2012, Demographic processes in the montane Atlantic rainforest: molecular and cytogenetic evidence from the endemic frog Proceratophrys boiei, Mol Phylogenet Evol, 62, 880, 10.1016/j.ympev.2011.11.004

Carnaval, 2009, Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot, Science, 323, 785, 10.1126/science.1166955

Bickford, 2007, Cryptic species as a window on diversity and conservation, Trends Ecol Evol, 22, 148, 10.1016/j.tree.2006.11.004

Malhotra, 2004, Maximising information in systematic revisions: a combined molecular and morphological analysis of a cryptic green pitviper complex (Trimeresurus stejnegeri), Biol J Linn Soc, 82, 219, 10.1111/j.1095-8312.2004.00354.x

Sanders, 2006, Combining molecular, morphological and ecological data to infer species boundaries in a cryptic tropical pitviper, Biol J Linn Soc, 87, 343, 10.1111/j.1095-8312.2006.00568.x

Malhotra, 2011, Phylogenetic structure and species boundaries in the mountain pitviper Ovophis monticola (Serpentes: Viperidae: Crotalinae) in Asia, Mol Phylogenet Evol, 59, 444, 10.1016/j.ympev.2011.02.010

Gutiérrez, 2008, Snake venomics of the Lesser Antillean pit vipers Bothrops caribbaeus and Bothrops lanceolatus: correlation with toxicological activities and immunoreactivity of a heterologous antivenom, J Proteome Res, 7, 4396, 10.1021/pr8003826

Calvete, 2009, Snake venomics and antivenomics of Bothrops colombiensis, a medically important pitviper of the Bothrops atrox-asper complex endemic to Venezuela: contributing to its taxonomy and snakebite management, J Proteomics, 72, 227, 10.1016/j.jprot.2009.01.005

Gutiérrez, 2014, Immunological profile of antivenoms: preclinical analysis of the efficacy of a polyspecific antivenom through antivenomics and neutralization assays, J Proteomics, 105, 340, 10.1016/j.jprot.2014.02.021

Bogarín, 2000, Neutralization of crotaline snake venoms from Central and South America by antivenoms produced in Brazil and Costa Rica, Toxicon, 38, 1429, 10.1016/S0041-0101(99)00236-6

Wüster, 2008, A nesting of vipers: phylogeny and historical phylogeography of the Viperidae (Squamata: Serpentes), Mol Phylogenet Evol, 49, 445, 10.1016/j.ympev.2008.08.019

Castoe, 2006, Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes), Mol Phylogenet Evol, 39, 91, 10.1016/j.ympev.2005.12.014

Machado, 2014, Phylogenetic relationships within Bothrops neuwiedi group (Serpentes, Squamata): geographically highly-structured lineages, evidence of introgressive hybridization and Neogene/Quaternary diversification, Mol Phylogenet Evol, 71, 1, 10.1016/j.ympev.2013.10.003

Sousa, 2001, Proteolytic action of Bothrops jararaca venom upon its own constituents, Toxicon, 39, 787, 10.1016/S0041-0101(00)00208-7