The DOI matches its Crossref record; 44 of the 45 references it cites were found in a registry or an index.
From genome to “venome”: Molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins
Open accessAbstract
This study analyzed the origin and evolution of snake venom proteome by means of phylogenetic analysis of the amino acid sequences of the toxins and related nonvenom proteins. The snake toxins were shown to have arisen from recruitment events of genes from within the following protein families: acetylcholinesterase, ADAM (disintegrin/metalloproteinase), AVIT, complement C3, crotasin/β defensin, cystatin, endothelin, factor V, factor X, kallikrein, kunitz-type proteinase inhibitor, LYNX/SLUR, L-amino oxidase, lectin, natriuretic peptide, βnerve growth factor, phospholipase A 2, SPla/Ryanodine, vascular endothelial growth factor, and whey acidic protein/secretory leukoproteinase inhibitor. Toxin recruitment events were found to have occurred at least 24 times in the evolution of snake venom. Two of these toxin derivations (CRISP and kallikrein toxins) appear to have been actually the result of modifications of existing salivary proteins rather than gene recruitment events. One snake toxin type, the waglerin peptides from Tropidolaemus wagleri (Wagler's Viper), did not have a match with known proteins and may be derived from a uniquely reptilian peptide. All of the snake toxin types still possess the bioactivity of the ancestral proteins in at least some of the toxin isoforms. However, this study revealed that the toxin types, where the ancestral protein was extensively cysteine cross-linked, were the ones that flourished into functionally diverse, novel toxin multigene families.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Notably, duplications in each of the b -defensin, C-type natriuretic peptide and nerve growth factor gene families have also occurred independently in reptiles during the evolution of their venom 47 .”
From Genome analysis of the platypus reveals unique signatures of evolution (2008) · cites this paper as [47]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 38,685
MrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 29,194
MRBAYES: Bayesian inference of phylogenetic trees.
Huelsenbeck, J. P., & Ronquist, F. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.8.754 · Cited by 21,937
PHYLIP-Phylogeny inference package (Version 3.2)
Felsenstein, J. (1989) · Cladistics · Cited by 17,682
MRBAYES: Bayesian inference of phylogeny
Huelsenbeck, J. P., & Ronquist, F. (2001) · Bioinformatics · Cited by 4,892
Snakes : The Evolution of Mystery in Nature
Greene, H. W. (1997) · Cited by 654
Greene, H. W. (1997) · University of California Press eBooks · doi:10.1525/9780520935433 · Cited by 545
Molecular Evolution and Phylogeny of Elapid Snake Venom Three-Finger Toxins
Fry, B. G., W�ster, W., Kini, R. M., Brusić, V., Khan, A. M., Venkataraman, D., & Rooney, A. P. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-2461-2 · Cited by 367
Self-citationMesozoic Birds: Above the Heads of Dinosaurs
Clarke, J. A. (2003) · Journal of Paleontology · doi:10.1666/0022-3360(2003)077 · Cited by 320
lynx1, an Endogenous Toxin-like Modulator of Nicotinic Acetylcholine Receptors in the Mammalian CNS
Miwa, J. M., Ibáñez-Tallon, I., Crabtree, G. W., Sánchez, R., Šali, A., Role, L. W., & Heintz, N. (1999) · Neuron · doi:10.1016/s0896-6273(00)80757-6 · Cited by 287
Chimienti, F. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg320 · Cited by 247
Fry, B. G. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh091 · Cited by 236
Self-citationThe origin of snakes and evolution of the venom apparatus
Kochva, E. (1987) · Toxicon · doi:10.1016/0041-0101(87)90150-4 · Cited by 231
Schweitz, H., Bruhn, T., Guillemare, E., Moinier, D., Lancelin, J., Béress, L., & Lazdunski, M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.42.25121 · Cited by 216
The phylogeny of varanoid lizards and the affinities of snakes
Lee, M. S. Y. (1997) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1997.0005 · Cited by 204
Ibañez-Tallon, I., Miwa, J. M., Wang, H.-L., Adams, N. C., Crabtree, G. W., Sine, S. M., & Heintz, N. (2002) · Neuron · doi:10.1016/s0896-6273(02)00632-3 · Cited by 200
Bv8, a small protein from frog skin and its homologue from snake venom induce hyperalgesia in rats
Mollay, C., Wechselberger, C., Mignogna, G., Negri, L., Melchiorri, P., Barra, D., & Kreil, G. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00229-0 · Cited by 188
Schweitz, H., Heurteaux, C., Bois, P., Moinier, D., Romey, G., & Lazdunski, M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.3.878 · Cited by 167
Fry, B. G., Wüster, W., Ramjan, S. F. R., Jackson, T., Martelli, P., & Kini, R. M. (2003) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.1148 · Cited by 167
Self-citationPrimary structure and properties of helothermine, a peptide toxin that blocks ryanodine receptors
Morrissette, J. M., Krätzschmar, J., Haendler, B., El-Hayek, R., Mochca-Morales, J., Martin, B. M., Patel, J. R., Moss, R. L., Schleuning, W.-D. D., & Coronado, R. (1995) · Biophysical Journal · doi:10.1016/s0006-3495(95)80410-8 · Cited by 166
Fry, B. G., Lumsden, N. G., W�ster, W., Wickramaratna, J. C., Hodgson, W. C., & Kini, R. M. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-2497-3 · Cited by 154
Self-citationCloning and characterization of novel snake venom proteins that block smooth muscle contraction
Yamazaki, Y., Koike, H., Sugiyama, Y., Motoyoshi, K., Wada, T., Hishinuma, S., Mita, M., & Morita, T. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.02940.x · Cited by 148
Forstner, M. R. J., Davis, S. K., & Arévalo, E. (1995) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.1995.1010 · Cited by 141
The evolution of venom-delivery systems in snakes
Jackson, K. (2003) · Zoological Journal of the Linnean Society · doi:10.1046/j.1096-3642.2003.00052.x · Cited by 131
Vidal, N. (2002) · Journal of Toxicology Toxin Reviews · doi:10.1081/txr-120004740 · Cited by 121
On the affinities of the burrowing asps Atractaspis (Serpentes: Atractaspididae)
Underwood, G., & Kochva, E. (1993) · Zoological Journal of the Linnean Society · doi:10.1111/j.1096-3642.1993.tb01252.x · Cited by 108
Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes
Vidal, N., & Hedges, S. B. (2002) · Comptes Rendus Biologies · doi:10.1016/s1631-0691(02)01509-3 · Cited by 106
Mochca-Morales, J., Martin, B. M., & Possani, L. D. (1990) · Toxicon · doi:10.1016/0041-0101(90)90065-f · Cited by 99
Helothermine, a lizard venom toxin, inhibits calcium current in cerebellar granules
Nobile, M., Noceti, F., Prestipino, G., & Possani, L. D. (1996) · Experimental Brain Research · doi:10.1007/bf00241369 · Cited by 94
Venomous Snakes: Ecology, Evolution and Snakebite
Ernst, C. H., Thorpe, R. S., Wüster, W., Malhotra, A., & Wüster, W. (1997) · Copeia · doi:10.2307/1447318 · Cited by 82
The toxin helothermine affects potassium currents in newborn rat cerebellar granule cells
Nobile, M., Magnelli, V., Lagostena, L., Mochca-Morales, J., Possani, L. D., & Prestipino, G. (1994) · The Journal of Membrane Biology · doi:10.1007/bf00232674 · Cited by 70
Structure activity in the atrial natriuretic peptide (ANP) family
Bovy, P. R. (1990) · Medicinal Research Reviews · doi:10.1002/med.2610100105 · Cited by 65
Utaisincharoen, P., Mackessy, S. P., Miller, R. A., & Tu, A. T. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)80636-x · Cited by 63
Kochva, E. (1965) · Copeia · doi:10.2307/1440716 · Cited by 51
Szeto, T. H., Wang, X., Smith, R., Connor, M. A., Christie, M. J., Nicholson, G. M., & King, G. F. (2000) · Toxicon · doi:10.1016/s0041-0101(99)00174-9 · Cited by 45
DEVELOPMENT OF THE VENOM GLAND AND TRIGEMINAL MUSCLES IN VIPERA PALAESTINAE
Kochva, E. (2008) · Acta Anatomica · doi:10.1159/000142338 · Cited by 45
Phylogeny and classification of the Orussidae (Insecta: Hymenoptera), a basal parasitic wasp taxon
Vilhelmsen, L. (2003) · Zoological Journal of the Linnean Society · doi:10.1046/j.1096-3642.2003.00080.x · Cited by 45
Ducancel, F., Matre, V., Dupont, C., Lajeunesse, E. C., Wollberg, Z., Bdolah, A., Kochva, E., Boulain, J., & Ménèz, A. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53658-9 · Cited by 44
Plater, G. M. D., Martin, R. L., & Milburn, P. J. (1998) · Toxicon · doi:10.1016/s0041-0101(97)00176-1 · Cited by 43
Kolbe, H. V. J., Huber, A., Cordier, P., Rasmussen, U. B., Bouchon, B., Jaquinod, M., Vlasak, R., Délot, E. C., & Kreil, G. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85442-x · Cited by 38
Plater, G. M. D., Martin, R. L., & Milburn, P. J. (1998) · Comparative Biochemistry and Physiology Part C Pharmacology Toxicology and Endocrinology · doi:10.1016/s0742-8413(98)00030-9 · Cited by 37
Rádis‐Baptista, G., Kubo, T., Oguiura, N., Svartman, M., Almeida, T. M. B., Batistic, R. F., Oliveira, E. B., Vianna‐Morgante, A. M., & Yamane, T. (2003) · Toxicon · doi:10.1016/j.toxicon.2003.10.019 · Cited by 34
Aiken, S. P., Sellin, L. C., Schmidt, J. J., Weinstein, S. A., & McArdle, J. J. (1992) · Pharmacology & Toxicology · doi:10.1111/j.1600-0773.1992.tb00508.x · Cited by 22
Snake Venom Toxins: The Evolution of Some of the Toxins Found in Snake Venoms
Strydom, D. J. (1973) · Systematic Zoology · doi:10.2307/2412964 · Cited by 21
Research works printed but not linked: 4
- 1978, Biology of the Reptilia, 8, 43
- 1994, J. Membr. Biol., 139, 49
- 1996, Exp. Brain Res., 110, 15
- 2003, Crotalus durissus terrificus Toxicon, 42, 747
Cited by
Sorted by citations
Complex cocktails: the evolutionary novelty of venoms
Casewell, N. R., Wüster, W., Vonk, F. J., Harrison, R. A., & Fry, B. G. (2012) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.10.020 · Cited by 998
Self-citationThe Toxicogenomic Multiverse: Convergent Recruitment of Proteins Into Animal Venoms
Fry, B. G., Roelants, K., Champagne, D. E., Scheib, H., Tyndall, J. D. A., King, G. F., Nevalainen, T. J., Norman, J. A., Lewis, R. J., Norton, R. S., et al. (2009) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.9.081307.164356 · Cited by 840
Self-citationWarrell, D. A. (2010) · The Lancet · doi:10.1016/s0140-6736(09)61754-2 · Cited by 776
Genome analysis of the platypus reveals unique signatures of evolution
paper, A. L. O. A. A. T. A. A. A. T. E. O. T. (2008) · Nature · doi:10.1038/nature06936 · Cited by 719
A Review and Database of Snake Venom Proteomes
Tasoulis, T., & Isbister, G. K. (2017) · Toxins · doi:10.3390/toxins9090290 · Cited by 618
Metadata
- Authors
- Fry, B. G.
- Affiliations
- European Bioinformatics Institute (GB)
- Corresponding author
- Fry, Bryan G.
- ORCID
- Fry, Bryan G.
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2005-03
- Volume
- 15
- Issue
- 3
- Pages
- 403-420
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC551567
- OpenAlex
- W2073555092
- Cited by
- 486
- References
- 45
- Citations by year
- 2026: 9 · 2025: 19 · 2024: 14 · 2023: 9 · 2022: 20 · 2021: 20 · 2020: 27 · 2019: 23 · 2018: 14 · 2017: 30 · 2016: 29 · 2015: 23 · 2014: 40 · 2013: 30 · 2012: 21
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Bioinformatics Institute
- Australian Academy of Science
- University of Melbourne
- Australian Research Council (DP0451663)
- Topics
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Venomous Animal Envenomation and Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Amphibian and Reptile Biology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- snake venom proteome, gene recruitment, acetylcholinesterase, Adam, kallikrein, phospholipase A2, cysteine cross-linking, salivary proteins
- MeSH terms
- Animals, Phylogeny, Snake Venoms, Snakes, Tissue Distribution, Evolution, Molecular, Proteome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
