Potential Ancestral Conoidean Toxins in the Venom Cocktail of the Carnivorous Snail Raphitoma purpurea (Montagu, 1803) (Neogastropoda: Raphitomidae)
Abstract
:1. Introduction
2. Results
2.1. Bioinformatics Analyses
2.2. The Venom Cocktail of Raphitoma purpurea
2.2.1. Post-Translational Modification
2.2.2. Regulation
2.2.3. Biosynthesis
2.3. Venom Evolutionary Patterns in Conoidea
3. Discussion
4. Materials and Methods
4.1. Dataset
4.2. Bioinformatic Analyses
4.3. Venom Cocktail Characterisation
4.4. Venom Evolutionary Patterns in Conoidea
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Nelsen, D.R.; Nisani, Z.; Cooper, A.M.; Fox, G.A.; Gren, E.C.K.; Corbit, A.G.; Hayes, W.K. Poisons, Toxungens, and Venoms: Redefining and Classifying Toxic Biological Secretions and the Organisms That Employ Them. Biol. Rev. 2014, 89, 450–465. [Google Scholar] [CrossRef] [PubMed]
- 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. The Toxicogenomic Multiverse: Convergent Recruitment of Proteins into Animal Venoms. Annu. Rev. Genom. Hum. Genet. 2009, 10, 483–511. [Google Scholar] [CrossRef] [PubMed]
- Edstrom, A. Venomous and Poisonous Animals; Krieger Publishing Company: Malabar, FL, USA, 1992; ISBN 0894646273. [Google Scholar]
- Arbuckle, K. Evolutionary Context of Venom in Animals. In Evolution of Venomous Animals and Their Toxins; Malhotra, A., Gopalakrishnakone, P., Eds.; Springer: Dordrecht, The Netherlands, 2017; pp. 3–31. ISBN 978-94-007-6458-3. [Google Scholar]
- Phuong, M.A.; Mahardika, G.N.; Alfaro, M.E. Dietary Breadth Is Positively Correlated with Venom Complexity in Cone Snails. BMC Genom. 2016, 17, 401. [Google Scholar] [CrossRef] [PubMed]
- Gorson, J.; Fassio, G.; Lau, E.S.; Holford, M. Diet Diversity in Carnivorous Terebrid Snails Is Tied to the Presence and Absence of a Venom Gland. Toxins 2021, 13, 108. [Google Scholar] [CrossRef] [PubMed]
- Casewell, N.R.; Wüster, W.; Vonk, F.J.; Harrison, R.A.; Fry, B.G. Complex Cocktails: The Evolutionary Novelty of Venoms. Trends Ecol. Evol. 2013, 28, 219–229. [Google Scholar] [CrossRef] [PubMed]
- Modica, M.V.; Lombardo, F.; Franchini, P.; Oliverio, M. The Venomous Cocktail of the Vampire Snail Colubraria reticulata (Mollusca, Gastropoda). BMC Genom. 2015, 16, 441. [Google Scholar] [CrossRef] [PubMed]
- Remigio, E.A.; Duda, T.F., Jr. Evolution of Ecological Specialization and Venom of a Predatory Marine Gastropod. Mol. Ecol. 2008, 17, 1156–1162. [Google Scholar] [CrossRef] [PubMed]
- Furtado, M.F.D.; Travaglia-Cardoso, S.R.; Rocha, M.M.T. Sexual Dimorphism in Venom of Bothrops jararaca (Serpentes: Viperidae). Toxicon 2006, 48, 401–410. [Google Scholar] [CrossRef] [PubMed]
- Dutertre, S.; Jin, A.-H.; Vetter, I.; Hamilton, B.; Sunagar, K.; Lavergne, V.; Dutertre, V.; Fry, B.G.; Antunes, A.; Venter, D.J.; et al. Evolution of Separate Predation- and Defence-Evoked Venoms in Carnivorous Cone Snails. Nat. Commun. 2014, 5, 3521. [Google Scholar] [CrossRef]
- Olivera, B.M. Conus Peptides: Biodiversity-Based Discovery and Exogenomics. J. Biol. Chem. 2006, 281, 31173–31177. [Google Scholar] [CrossRef]
- Kaas, Q.; Westermann, J.-C.; Craik, D.J. Conopeptide Characterization and Classifications: An Analysis Using ConoServer. Toxicon 2010, 55, 1491–1509. [Google Scholar] [CrossRef] [PubMed]
- Puillandre, N.; Koua, D.; Favreau, P.; Olivera, B.M.; Stöcklin, R. Molecular Phylogeny, Classification and Evolution of Conopeptides. J. Mol. Evol. 2012, 74, 297–309. [Google Scholar] [CrossRef] [PubMed]
- Dao, F.-Y.; Yang, H.; Su, Z.-D.; Yang, W.; Wu, Y.; Hui, D.; Chen, W.; Tang, H.; Lin, H. Recent Advances in Conotoxin Classification by Using Machine Learning Methods. Molecules 2017, 22, 1057. [Google Scholar] [CrossRef] [PubMed]
- Safavi-Hemami, H.; Gajewiak, J.; Karanth, S.; Robinson, S.D.; Ueberheide, B.; Douglass, A.D.; Schlegel, A.; Imperial, J.S.; Watkins, M.; Bandyopadhyay, P.K.; et al. Specialized Insulin Is Used for Chemical Warfare by Fish-Hunting Cone Snails. Proc. Natl. Acad. Sci. USA 2015, 112, 1743–1748. [Google Scholar] [CrossRef] [PubMed]
- Jami, S.; Erickson, A.; Brierley, S.M.; Vetter, I. Pain-Causing Venom Peptides: Insights into Sensory Neuron Pharmacology. Toxins 2018, 10, 15. [Google Scholar] [CrossRef] [PubMed]
- Garrison, J.L.; Macosko, E.Z.; Bernstein, S.; Pokala, N.; Albrecht, D.R.; Bargmann, C.I. Oxytocin/Vasopressin-Related Peptides Have an Ancient Role in Reproductive Behavior. Science 2012, 338, 540–543. [Google Scholar] [CrossRef] [PubMed]
- Mendel, H.C.; Kaas, Q.; Muttenthaler, M. Neuropeptide Signalling Systems—An Underexplored Target for Venom Drug Discovery. Biochem. Pharmacol. 2020, 181, 114129. [Google Scholar] [CrossRef] [PubMed]
- Lewis, R.J.; Dutertre, S.; Vetter, I.; Christie, M.J. Conus Venom Peptide Pharmacology. Pharmacol. Rev. 2012, 64, 259. [Google Scholar] [CrossRef] [PubMed]
- Prashanth, J.R.; Lewis, R.J.; Dutertre, S. Towards an Integrated Venomics Approach for Accelerated Conopeptide Discovery. Toxicon 2012, 60, 470–477. [Google Scholar] [CrossRef]
- Duda, T.F.; Palumbi, S.R. Molecular Genetics of Ecological Diversification: Duplication and Rapid Evolution of Toxin Genes of the Venomous Gastropod Conus. Proc. Natl. Acad. Sci. USA 1999, 96, 6820–6823. [Google Scholar] [CrossRef]
- Safavi-Hemami, H.; Li, Q.; Jackson, R.L.; Song, A.S.; Boomsma, W.; Bandyopadhyay, P.K.; Gruber, C.W.; Purcell, A.W.; Yandell, M.; Olivera, B.M.; et al. Rapid Expansion of the Protein Disulfide Isomerase Gene Family Facilitates the Folding of Venom Peptides. Proc. Natl. Acad. Sci. USA 2016, 113, 3227–3232. [Google Scholar] [CrossRef] [PubMed]
- Turner, A.H.; Craik, D.J.; Kaas, Q.; Schroeder, C.I. Bioactive Compounds Isolated from Neglected Predatory Marine Gastropods. Mar. Drugs 2018, 16, 118. [Google Scholar] [CrossRef] [PubMed]
- Von Reumont, B.M.; Campbell, L.I.; Jenner, R.A. Quo Vadis Venomics? A Roadmap to Neglected Venomous Invertebrates. Toxins 2014, 6, 3488–3551. [Google Scholar] [CrossRef] [PubMed]
- Puillandre, N.; Fedosov, A.E.; Kantor, Y.I. Systematics and Evolution of the Conoidea. In Evolution of Venomous Animals and Their Toxins; Malhotra, A., Gopalakrishnakone, P., Eds.; Springer: Dordrecht, The Netherlands, 2017; pp. 367–398. ISBN 978-94-007-6458-3. [Google Scholar]
- Prashanth, J.R.; Dutertre, S.; Lewis, R.J. Revising the Role of Defense and Predation in Cone Snail Venom Evolution. In Evolution of Venomous Animals and Their Toxins; Malhotra, A., Gopalakrishnakone, P., Eds.; Springer: Dordrecht, The Netherlands, 2017; pp. 105–123. ISBN 978-94-007-6458-3. [Google Scholar]
- Prashanth, J.R.; Brust, A.; Jin, A.-H.; Alewood, P.F.; Dutertre, S.; Lewis, R.J. Cone Snail Venomics: From Novel Biology to Novel Therapeutics. Future Med. Chem. 2014, 6, 1659–1675. [Google Scholar] [CrossRef] [PubMed]
- Bouchet, P.; Kantor, Y.I.; Sysoev, A.; Puillandre, N. A New Operational Classification of the Conoidea (Gastropoda). J. Molluscan Stud. 2011, 77, 273–308. [Google Scholar] [CrossRef]
- Kantor, Y.I.; Taylor, J.D. Foregut Anatomy and Relationships of Raphitomine Gastropods (Gastropoda: Conoidea: Raphitominae). Boll. Malacol. 2002, 38 (Suppl. S4), 83–110. [Google Scholar]
- Abdelkrim, J.; Aznar-Cormano, L.; Fedosov, A.E.; Kantor, Y.I.; Lozouet, P.; Phuong, M.A.; Zaharias, P.; Puillandre, N. Exon-Capture-Based Phylogeny and Diversification of the Venomous Gastropods (Neogastropoda, Conoidea). Mol. Biol. Evol. 2018, 35, 2355–2374. [Google Scholar] [CrossRef] [PubMed]
- Lozouet, P. Les Conoidea de l’Oligocène Supérieur (Chattien) Du Bassin de l’Adour (Sud-Ouest de La France). Cossmanniana 2017, 19, 3–180. [Google Scholar]
- Prkić, J.; Giannuzzi-Savelli, R.; Pusateri, F.; Russini, V.; Fassio, G.; Oliverio, M. Three New Species of Raphitoma Bellardi 1847 (Mollusca, Gastropoda, Raphitomidae) from Croatian Waters (NE Adriatic Sea). Zoosystema 2020, 42, 215–238. [Google Scholar] [CrossRef]
- Giannuzzi-Savelli, R.; Pusateri, F.; Bartolini, S. A Revision of the Mediterranean Raphitomidae (Gastropoda, Conoidea), 7: On the Sibling Species Raphitoma densa (Monterosato, 1884) and R. Griseomaculata n. sp. Biodivers. J. 2018, 9, 429–440. [Google Scholar] [CrossRef]
- Kontadakis, C.; Ovalis, P.; Zaminos, G.; Manousis, T. Description of Raphitoma minae sp. Nov. (Mollusca, Gastropoda, Raphitomidae) from the Mediterranean (Aegean Sea, Greece). Xenophora Taxon. 2024, 43, 23–26. [Google Scholar]
- Giannuzzi-Savelli, R.; Pusateri, F.; Bartolini, S. A Revision of the Mediterranean Raphitomidae (Gastropoda: Conoidea) 5: Loss of Planktotrophy and Pairs of Species, with the Description of Four New Species. Boll. Malacol. 2018, 54, 1–77. [Google Scholar]
- Pusateri, F.; Giannuzzi-Savelli, R.; Bartolini, S. A Revision of the Mediterranean Raphitomidae, 3: On the Raphitoma pupoides (Monterosato, 1884) Complex, with the Description of a New Species (Mollusca Gastropoda). Biodivers. J. 2016, 7, 103–115. [Google Scholar]
- Russini, V.; Giannuzzi-Savelli, R.; Pusateri, F.; Prkić, J.; Fassio, G.; Modica, M.V.; Oliverio, M. Candidate Cases of Poecilogony in Neogastropoda: Implications for the Systematics of the Genus Raphitoma Bellardi, 1847. Invertebr. Syst. 2020, 34, 293–318. [Google Scholar] [CrossRef]
- Fassio, G.; Russini, V.; Pusateri, F.; Giannuzzi-Savelli, R.; Høisaeter, T.; Puillandre, N.; Modica, M.V.; Oliverio, M. An Assessment of Raphitoma and Allied Genera (Neogastropoda: Raphitomidae). J. Molluscan Stud. 2019, 85, 414–425. [Google Scholar] [CrossRef]
- Rolán, E.; Otero-Schmitt, J.; Fernandes, F. The Family Turridae s.l. (Mollusca, Gastropoda) in Angola (West Africa), 1. Subfamily Daphnellinae. Iberus 1998, 16, 95–118. [Google Scholar]
- von Reumont, B.M.; Anderluh, G.; Antunes, A.; Ayvazyan, N.; Beis, D.; Caliskan, F.; Crnković, A.; Damm, M.; Dutertre, S.; Ellgaard, L.; et al. Modern Venomics—Current Insights, Novel Methods, and Future Perspectives in Biological and Applied Animal Venom Research. Gigascience 2022, 11, giac048. [Google Scholar] [PubMed]
- Ringeval, A.; Farhat, S.; Fedosov, A.; Gerdol, M.; Greco, S.; Mary, L.; Modica, M.V.; Puillandre, N. DeTox: A Pipeline for the Detection of Toxins in Venomous Organisms. Brief. Bioinform. 2024, 25, bbae094. [Google Scholar] [CrossRef] [PubMed]
- Dutertre, S.; Biass, D.; Stöcklin, R.; Favreau, P. Dramatic Intraspecimen Variations within the Injected Venom of Conus consors: An Unsuspected Contribution to Venom Diversity. Toxicon 2010, 55, 1453–1462. [Google Scholar] [CrossRef]
- Hargreaves, A.D.; Tucker, A.S.; Mulley, J.F. A Critique of the Toxicoferan Hypothesis. In Evolution of Venomous Animals and Their Toxins; Malhotra, A., Gopalakrishnakone, P., Eds.; Springer: Dordrecht, The Netherlands, 2017; pp. 69–86. ISBN 978-94-007-6458-3. [Google Scholar]
- Butte, A.J.; Dzau, V.J.; Glueck, S.B. Further Defining Housekeeping, or “Maintenance,” Genes Focus on “A Compendium of Gene Expression in Normal Human Tissues”. Physiol. Genom. 2001, 7, 95–96. [Google Scholar] [CrossRef]
- RStudio Team. RStudio: Integrated Development Environment for R 2020; RStudio Team: Boston, MA, USA, 2020. [Google Scholar]
- Bose, U.; Wang, T.; Zhao, M.; Motti, C.A.; Hall, M.R.; Cummins, S.F. Multiomics Analysis of the Giant Triton Snail Salivary Gland, a Crown-of-Thorns Starfish Predator. Sci. Rep. 2017, 7, 6000. [Google Scholar] [CrossRef] [PubMed]
- Breddam, K. Serine Carboxypeptidases. A Review. Carlsberg Res. Commun. 1986, 51, 83. [Google Scholar] [CrossRef]
- Li, R.; Zhang, L.; Fang, Y.; Han, B.; Lu, X.; Zhou, T.; Feng, M.; Li, J. Proteome and Phosphoproteome Analysis of Honeybee (Apis mellifera) Venom Collected from Electrical Stimulation and Manual Extraction of the Venom Gland. BMC Genom. 2013, 14, 766. [Google Scholar] [CrossRef] [PubMed]
- Knight, P.J.K.; Crickmore, N.; Ellar, D.J. The Receptor for Bacillus thuringiensis CrylA(c) Delta-Endotoxin in the Brush Border Membrane of the Lepidopteran Manduca Sexta Is Aminopeptidase N. Mol. Microbiol. 1994, 11, 429–436. [Google Scholar] [CrossRef] [PubMed]
- Gasparello-Clemente, E.; Silveira, P.F. Fluorometric Assay Using Naphthylamide Substrates for Assessing Novel Venom Peptidase Activities. Toxicon 2002, 40, 1617–1626. [Google Scholar] [CrossRef] [PubMed]
- 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 Negl. Trop. Dis. 2010, 4, e796. [Google Scholar] [CrossRef] [PubMed]
- Luo, H.; Hallen-Adams, H.E.; Scott-Craig, J.S.; Walton, J.D. Colocalization of Amanitin and a Candidate Toxin-Processing Prolyl Oligopeptidase in Amanita basidiocarps. Eukaryot. Cell 2010, 9, 1891–1900. [Google Scholar] [CrossRef] [PubMed]
- Gorres, K.L.; Raines, R.T. Prolyl 4-Hydroxylase. Crit. Rev. Biochem. Mol. Biol. 2010, 45, 106–124. [Google Scholar] [CrossRef] [PubMed]
- Buczek, O.; Bulaj, G.; Olivera, B.M. Conotoxins and the Posttranslational Modification of Secreted Gene Products. Cell Mol. Life Sci. 2005, 62, 3067–3079. [Google Scholar] [CrossRef]
- Vijayasarathy, M.; Balaram, P. Cone Snail Prolyl-4-Hydroxylase α-Subunit Sequences Derived from Transcriptomic Data and Mass Spectrometric Analysis of Variable Proline Hydroxylation in C. amadis Venom. J. Proteom. 2019, 194, 37–48. [Google Scholar] [CrossRef]
- Fassio, G.; Modica, M.V.; Mary, L.; Zaharias, P.; Fedosov, A.E.; Gorson, J.; Kantor, Y.I.; Holford, M.; Puillandre, N. Venom Diversity and Evolution in the Most Divergent Cone Snail Genus Profundiconus. Toxins 2019, 11, 623. [Google Scholar] [CrossRef]
- Calvete, J.J.; Fasoli, E.; Sanz, L.; Boschetti, E.; Righetti, P.G. Exploring the Venom Proteome of the Western Diamondback Rattlesnake, Crotalus atrox, via Snake Venomics and Combinatorial Peptide Ligand Library Approaches. J. Proteome Res. 2009, 8, 3055–3067. [Google Scholar] [CrossRef] [PubMed]
- Isomoto, A.; Shoguchi, E.; Hisata, K.; Inoue, J.; Sun, Y.; Inaba, K.; Satoh, N.; Ogawa, T.; Shibata, H. Active Expression of Genes for Protein Modification Enzymes in Habu Venom Glands. Toxins 2022, 14, 300. [Google Scholar] [CrossRef] [PubMed]
- Attenborough, R.M.F.; Hayward, D.C.; Kitahara, M.V.; Miller, D.J.; Ball, E.E. A “Neural” Enzyme in Nonbilaterian Animals and Algae: Preneural Origins for Peptidylglycine α-Amidating Monooxygenase. Mol. Biol. Evol. 2012, 29, 3095–3109. [Google Scholar] [CrossRef]
- Ul-Hasan, S.; Burgess, D.M.; Gajewiak, J.; Li, Q.; Hu, H.; Yandell, M.; Olivera, B.M.; Bandyopadhyay, P.K. Characterization of the Peptidylglycine α-Amidating Monooxygenase (PAM) from the Venom Ducts of Neogastropods, Conus bullatus and Conus geographus. Toxicon 2013, 74, 215–224. [Google Scholar] [CrossRef]
- Katiyar, S.; Till, E.A.; Lennarz, W.J. Studies on the Function of Yeast Protein Disulfide Isomerase in Renaturation of Proteins. Biochim. Biophys. Acta (BBA)-Protein Struct. Mol. Enzymol. 2001, 1548, 47–56. [Google Scholar] [CrossRef]
- Wang, L.; Wang, X.; Ren, Z.; Tang, W.; Zou, Q.; Wang, J.; Chen, S.; Zhang, H.; Xu, A. Oxidative Folding of Conopeptides Modified by Conus Protein Disulfide Isomerase. Protein J. 2017, 36, 407–416. [Google Scholar] [CrossRef] [PubMed]
- Krücken, J.; Greif, G.; von Samson-Himmelstjerna, G. In Silico Analysis of the Cyclophilin Repertoire of Apicomplexan Parasites. Parasit. Vectors 2009, 2, 27. [Google Scholar] [CrossRef]
- Barik, S. Immunophilins: For the Love of Proteins. Cell Mol. Life Sci. 2006, 63, 2889–2900. [Google Scholar] [CrossRef]
- Violette, A.; Leonardi, A.; Piquemal, D.; Terrat, Y.; Biass, D.; Dutertre, S.; Noguier, F.; Ducancel, F.; Stöcklin, R.; Križaj, I.; et al. Recruitment of Glycosyl Hydrolase Proteins in a Cone Snail Venomous Arsenal: Further Insights into Biomolecular Features of Conus Venoms. Mar. Drugs 2012, 10, 258–280. [Google Scholar] [CrossRef]
- Yuasa, H.J.; Furuta, E.; Nakamura, A.; Takagi, T. Cloning and Sequencing of Three C-Type Lectins from Body Surface Mucus of the Land Slug, Incilaria fruhstorferi. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1998, 119, 479–484. [Google Scholar] [CrossRef]
- Zelensky, A.N.; Gready, J.E. The C-Type Lectin-like Domain Superfamily. FEBS J. 2005, 272, 6179–6217. [Google Scholar] [CrossRef] [PubMed]
- Clemetson, K.J.; Lu, Q.; Clemetson, J.M. Snake C-Type Lectin-Like Proteins and Platelet Receptors. Pathophysiol. Haemost. Thromb. 2006, 34, 150–155. [Google Scholar] [CrossRef]
- Bland, N.D.; Pinney, J.W.; Thomas, J.E.; Turner, A.J.; Isaac, R.E. Bioinformatic Analysis of the Neprilysin (M13) Family of Peptidases Reveals Complex Evolutionary and Functional Relationships. BMC Evol. Biol. 2008, 8, 16. [Google Scholar] [CrossRef]
- Turner, A.J.; Isaac, R.E.; Coates, D. The Neprilysin (NEP) Family of Zinc Metalloendopeptidases: Genomics and Function. BioEssays 2001, 23, 261–269. [Google Scholar] [CrossRef] [PubMed]
- Liu, G.; Zhou, Y.; Liu, D.; Wang, Q.; Ruan, Z.; He, Q.; Zhang, L. Global Transcriptome Analysis of the Tentacle of the Jellyfish Cyanea capillata Using Deep Sequencing and Expressed Sequence Tags: Insight into the Toxin- and Degenerative Disease-Related Transcripts. PLoS ONE 2015, 10, e0142680. [Google Scholar] [CrossRef]
- do Nascimento, S.M.; de Oliveira, U.C.; Nishiyama-Jr, M.Y.; Tashima, A.K.; Silva Junior, P.I. da Presence of a Neprilysin on Avicularia juruensis (Mygalomorphae: Theraphosidae) Venom. Toxin Rev. 2022, 41, 370–379. [Google Scholar] [CrossRef]
- Knowles, A.F. The GDA1_CD39 Superfamily: NTPDases with Diverse Functions. Purinergic Signal 2011, 7, 21–45. [Google Scholar] [CrossRef]
- Kirkitadze, M.D.; Barlow, P.N. Structure and Flexibility of the Multiple Domain Proteins That Regulate Complement Activation. Immunol. Rev. 2001, 180, 146–161. [Google Scholar] [CrossRef]
- O’Keeffe, A.H.; Green, J.L.; Grainger, M.; Holder, A.A. A Novel Sushi Domain-Containing Protein of Plasmodium falciparum. Mol. Biochem. Parasitol. 2005, 140, 61–68. [Google Scholar] [CrossRef]
- Krishnarjuna, B.; Sunanda, P.; Seow, J.; Tae, H.-S.; Robinson, S.D.; Belgi, A.; Robinson, A.J.; Safavi-Hemami, H.; Adams, D.J.; Norton, R.S. Characterisation of Elevenin-Vc1 from the Venom of Conus victoriae: A Structural Analogue of α-Conotoxins. Mar. Drugs 2023, 21, 81. [Google Scholar] [CrossRef] [PubMed]
- Zuo, W.; Tian, M.; Qi, J.; Zhang, G.; Hu, J.; Wang, S.; Bao, Y. The Functions of EF-Hand Proteins from Host and Zoonotic Pathogens. Microbes Infect. 2023, 105276. [Google Scholar] [CrossRef] [PubMed]
- Junqueira-de-Azevedo, I.d.L.M.; Pertinhez, T.; Spisni, A.; Carreño, F.R.; Farah, C.S.; Ho, P.L. Cloning and Expression of Calglandulin, a New EF-Hand Protein from the Venom Glands of Bothrops insularis Snake in E. Coli. Biochim. Biophys. Acta (BBA)-Proteins Proteom. 2003, 1648, 90–98. [Google Scholar] [CrossRef]
- Pardos-Blas, J.R.; Irisarri, I.; Abalde, S.; Tenorio, M.J.; Zardoya, R. Conotoxin Diversity in the Venom Gland Transcriptome of the Magician’s Cone, Pionoconus magus. Mar. Drugs 2019, 17, 553. [Google Scholar] [CrossRef] [PubMed]
- Nagata, S. Chapter 41—Neuropeptide F. In Handbook of Hormones; Takei, Y., Ando, H., Tsutsui, K., Eds.; Academic Press: San Diego, CA, USA, 2016; pp. 355–356. ISBN 978-0-12-801028-0. [Google Scholar]
- Mancuso, D.J.; Tuley, E.A.; Westfield, L.A.; Worrall, N.K.; Shelton-Inloes, B.B.; Sorace, J.M.; Alevy, Y.G.; Sadler, J.E. Structure of the Gene for Human von Willebrand Factor. J. Biol. Chem. 1989, 264, 19514–19527. [Google Scholar] [CrossRef] [PubMed]
- Matsui, T.; Hamako, J. Structure and Function of Snake Venom Toxins Interacting with Human von Willebrand Factor. Toxicon 2005, 45, 1075–1087. [Google Scholar] [CrossRef] [PubMed]
- Thomazini, C.M.; Sachetto, A.T.A.; de Albuquerque, C.Z.; de Moura Mattaraia, V.G.; de Oliveira, A.K.; Serrano, S.M.d.T.; Lebrun, I.; Barbaro, K.C.; Santoro, M.L. Involvement of von Willebrand Factor and Botrocetin in the Thrombocytopenia Induced by Bothrops jararaca Snake Venom. PLoS Negl. Trop. Dis. 2021, 15, e0009715. [Google Scholar] [CrossRef] [PubMed]
- Pihlajamaa, T.; Kajander, T.; Knuuti, J.; Horkka, K.; Sharma, A.; Permi, P. Structure of Plasmodium falciparum TRAP (Thrombospondin-Related Anonymous Protein) A Domain Highlights Distinct Features in Apicomplexan von Willebrand Factor A Homologues. Biochem. J. 2013, 450, 469–476. [Google Scholar] [CrossRef] [PubMed]
- Small, D.H.; Nurcombe, V.; Reed, G.; Clarris, H.; Moir, R.; Beyreuther, K.; Masters, C.L. A Heparin-Binding Domain in the Amyloid Protein Precursor of Alzheimer’s Disease Is Involved in the Regulation of Neurite Outgrowth. J. Neurosci. 1994, 14, 2117. [Google Scholar] [CrossRef]
- Floden, M.A.; Sohrabi, M.; Nookala, S.; Cao, J.J.; Combs, K.C. Salivary Aβ Secretion and Altered Oral Microbiome in Mouse Models of AD. Curr. Alzheimer Res. 2020, 17, 1133–1144. [Google Scholar] [CrossRef]
- Huan, P.; Liu, G.; Wang, H.; Liu, B. Multiple Ferritin Subunit Genes of the Pacific Oyster Crassostrea gigas and Their Distinct Expression Patterns during Early Development. Gene 2014, 546, 80–88. [Google Scholar] [CrossRef] [PubMed]
- Zhang, G.; Schmidt, O.; Asgari, S. A Calreticulin-like Protein from Endoparasitoid Venom Fluid Is Involved in Host Hemocyte Inactivation. Dev. Comp. Immunol. 2006, 30, 756–764. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Wang, B.; Qiu, L.; Wan, B.; Yang, Y.; Liu, M.; Wang, F.; Fang, Q.; Stanley, D.; Ye, G. Functional Characterization of a Venom Protein Calreticulin in the Ectoparasitoid Pachycrepoideus vindemiae. Insects 2020, 11, 29. [Google Scholar]
- Kriegler, T.; Kiburg, G.; Hessa, T. Translocon-Associated Protein Complex (TRAP) Is Crucial for Co-Translational Translocation of Pre-Proinsulin. J. Mol. Biol. 2020, 432, 166694. [Google Scholar] [CrossRef]
- Dlakić, M. Functionally Unrelated Signalling Proteins Contain a Fold Similar to Mg2+-Dependent Endonucleases. Trends Biochem. Sci. 2000, 25, 272–273. [Google Scholar] [CrossRef] [PubMed]
- Pons, B.J.; Vignard, J.; Mirey, G. Cytolethal Distending Toxin Subunit B: A Review of Structure–Function Relationship. Toxins 2019, 11, 595. [Google Scholar] [CrossRef] [PubMed]
- Xu, E.-R.; Blythe, E.E.; Fischer, G.; Hyvönen, M. Structural Analyses of von Willebrand Factor C Domains of Collagen 2A and CCN3 Reveal an Alternative Mode of Binding to Bone Morphogenetic Protein-2. J. Biol. Chem. 2017, 292, 12516–12527. [Google Scholar] [CrossRef] [PubMed]
- Nesmelova, I.V.; Hackett, P.B. DDE Transposases: Structural Similarity and Diversity. Adv. Drug Deliv. Rev. 2010, 62, 1187–1195. [Google Scholar] [CrossRef] [PubMed]
- Munford, R.S.; Sheppard, P.O.; O’Hara, P.J. Saposin-like Proteins (SAPLIP) Carry out Diverse Functions on a Common Backbone Structure. J. Lipid Res. 1995, 36, 1653–1663. [Google Scholar] [CrossRef]
- Friedland, N.; Liou, H.-L.; Lobel, P.; Stock, A.M. Structure of a Cholesterol-Binding Protein Deficient in Niemann–Pick Type C2 Disease. Proc. Natl. Acad. Sci. USA 2003, 100, 2512–2517. [Google Scholar] [CrossRef]
- Turk, B.; Turk, D.; Turk, V. Lysosomal Cysteine Proteases: More than Scavengers. Biochim. Biophys. Acta (BBA)-Protein Struct. Mol. Enzymol. 2000, 1477, 98–111. [Google Scholar] [CrossRef]
- Sartim, M.A.; Sampaio, S.V. Snake Venom Galactoside-Binding Lectins: A Structural and Functional Overview. J. Venom. Anim. Toxins Incl. Trop. Dis. 2015, 21, 35. [Google Scholar] [CrossRef] [PubMed]
- Dai, S.-X.; Zhang, A.-D.; Huang, J.-F. Evolution, Expansion and Expression of the Kunitz/BPTI Gene Family Associated with Long-Term Blood Feeding in Ixodes scapularis. BMC Evol. Biol. 2012, 12, 4. [Google Scholar] [CrossRef] [PubMed]
- Bayrhuber, M.; Vijayan, V.; Ferber, M.; Graf, R.; Korukottu, J.; Imperial, J.; Garrett, J.E.; Olivera, B.M.; Terlau, H.; Zweckstetter, M.; et al. Conkunitzin-S1 Is the First Member of a New Kunitz-Type Neurotoxin Family: Structural and Functional Characterization. J. Biol. Chem. 2005, 280, 23766–23770. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.S.; Kim, B.Y.; Yoon, H.J.; Choi, Y.S.; Jin, B.R. Secapin, a Bee Venom Peptide, Exhibits Anti-Fibrinolytic, Anti-Elastolytic, and Anti-Microbial Activities. Dev. Comp. Immunol. 2016, 63, 27–35. [Google Scholar] [CrossRef]
- Taylor, J.W.; Bidard, J.N.; Lazdunski, M. The Characterization of High-Affinity Binding Sites in Rat Brain for the Mast Cell-Degranulating Peptide from Bee Venom Using the Purified Monoiodinated Peptide. J. Biol. Chem. 1984, 259, 13957–13967. [Google Scholar] [CrossRef] [PubMed]
- Skinner, W.S.; Adams, M.E.; Quistad, G.B.; Kataoka, H.; Cesarin, B.J.; Enderlin, F.E.; Schooley, D.A. Purification and Characterization of Two Classes of Neurotoxins from the Funnel Web Spider, Agelenopsis aperta. J. Biol. Chem. 1989, 264, 2150–2155. [Google Scholar] [CrossRef] [PubMed]
- Andersen, J.F. Structure and Mechanism in Salivary Proteins from Blood-Feeding Arthropods. Toxicon 2010, 56, 1120–1129. [Google Scholar] [CrossRef] [PubMed]
- Cabezas-Cruz, A.; Valdés, J.J. Are Ticks Venomous Animals? Front. Zool. 2014, 11, 47. [Google Scholar] [CrossRef]
- Strube, K.H.; Kröger, B.; Bialojan, S.; Otte, M.; Dodt, J. Isolation, Sequence Analysis, and Cloning of Haemadin. An Anticoagulant Peptide from the Indian Leech. J. Biol. Chem. 1993, 268, 8590–8595. [Google Scholar] [CrossRef]
- Acquasaliente, L.; Pierangelini, A.; Pagotto, A.; Pozzi, N.; De Filippis, V. From Haemadin to Haemanorm: Synthesis and Characterization of Full-Length Haemadin from the Leech Haemadipsa sylvestris and of a Novel Bivalent, Highly Potent Thrombin Inhibitor (Haemanorm). Protein Sci. 2023, 32, e4825. [Google Scholar] [CrossRef]
- Lee, I.H.; Zhao, C.; Cho, Y.; Harwig, S.S.L.; Cooper, E.L.; Lehrer, R.I. Clavanins, α-Helical Antimicrobial Peptides from Tunicate Hemocytes. FEBS Lett. 1997, 400, 158–162. [Google Scholar] [CrossRef] [PubMed]
- Robinson, S.D.; Norton, R.S. Conotoxin Gene Superfamilies. Mar. Drugs 2014, 12, 6058–6101. [Google Scholar] [CrossRef]
- Changeux, J.-P.; Taly, A. Nicotinic Receptors, Allosteric Proteins and Medicine. Trends Mol. Med. 2008, 14, 93–102. [Google Scholar] [CrossRef] [PubMed]
- Castañeda, O.; Sotolongo, V.; Amor, A.M.; Stöcklin, R.; Anderson, A.J.; Harvey, A.L.; Engström, Å.; Wernstedt, C.; Karlsson, E. Characterization of a Potassium Channel Toxin from the Caribbean Sea Anemone Stichodactyla helianthus. Toxicon 1995, 33, 603–613. [Google Scholar] [CrossRef]
- Möller, C.; Melaun, C.; Castillo, C.; Díaz, M.E.; Renzelman, C.M.; Estrada, O.; Kuch, U.; Lokey, S.; Marí, F. Functional Hypervariability and Gene Diversity of Cardioactive Neuropeptides. J. Biol. Chem. 2010, 285, 40673–40680. [Google Scholar] [CrossRef]
- Schlimgen, A.K.; Helms, J.A.; Vogel, H.; Perin, M.S. Neuronal Pentraxin, a Secreted Protein with Homology to Acute Phase Proteins of the Immune System. Neuron 1995, 14, 519–526. [Google Scholar] [CrossRef] [PubMed]
- Nihei, K.; Peigneur, S.; Tytgat, J.; Lange, A.B.; Konno, K. Isolation and Characterization of FMRFamide-like Peptides in the Venoms of Solitary Sphecid Wasps. Peptides 2021, 142, 170575. [Google Scholar] [CrossRef] [PubMed]
- Fedosov, A.; Tucci, C.F.; Kantor, Y.; Farhat, S.; Puillandre, N. Collaborative Expression: Transcriptomics of Conus virgo Suggests Contribution of Multiple Secretory Glands to Venom Production. J. Mol. Evol. 2023, 91, 837–853. [Google Scholar] [CrossRef]
- Abalde, S.; Tenorio, M.J.; Afonso, C.M.L.; Zardoya, R. Conotoxin Diversity in Chelyconus ermineus (Born, 1778) and the Convergent Origin of Piscivory in the Atlantic and Indo-Pacific Cones. Genome Biol. Evol. 2018, 10, 2643–2662. [Google Scholar] [CrossRef]
- Li, R.; Bekaert, M.; Wu, L.; Mu, C.; Song, W.; Migaud, H.; Wang, C. Transcriptomic Analysis of Marine Gastropod Hemifusus Tuba Provides Novel Insights into Conotoxin Genes. Mar. Drugs 2019, 17, 466. [Google Scholar] [CrossRef] [PubMed]
- Fedosov, A.; Zaharias, P.; Puillandre, N. A Phylogeny-Aware Approach Reveals Unexpected Venom Components in Divergent Lineages of Cone Snails. Proc. R. Soc. B 2021, 288, 20211017. [Google Scholar] [CrossRef] [PubMed]
- Gerdol, M.; Cervelli, M.; Oliverio, M.; Modica, M.V. Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia Reticulata. Mol. Biol. Evol. 2018, 35, 2654–2668. [Google Scholar] [CrossRef] [PubMed]
- Olivera, B.M.; Watkins, M.; Bandyopadhyay, P.; Imperial, J.S.; de la Cotera, E.P.H.; Aguilar, M.B.; Vera, E.L.; Concepcion, G.P.; Lluisma, A. Adaptive Radiation of Venomous Marine Snail Lineages and the Accelerated Evolution of Venom Peptide Genes. Ann. N. Y. Acad. Sci. 2012, 1267, 61–70. [Google Scholar] [CrossRef]
- Rogalski, A.; Himaya, S.W.A.; Lewis, R.J. Coordinated Adaptations Define the Ontogenetic Shift from Worm- to Fish-Hunting in a Venomous Cone Snail. Nat. Commun. 2023, 14, 3287. [Google Scholar] [CrossRef]
- Duda, T.F., Jr.; Kohn, A.J.; Palumbi, S.R. Origins of Diverse Feeding Ecologies within Conus, a Genus of Venomous Marine Gastropods. Biol. J. Linn. Soc. 2001, 73, 391–409. [Google Scholar] [CrossRef]
- Dutertre, S.; Griffin, J.; Lewis, R.J. Phyla Molluska: The Venom Apparatus of Cone Snails. In Marine and Freshwater Toxins; Gopalakrishnakone, P., Haddad, V., Jr., Tubaro, A., Kim, E., Kem, W.R., Eds.; Springer: Dordrecht, The Netherlands, 2016; pp. 327–340. ISBN 978-94-007-6419-4. [Google Scholar]
- Himaya, S.W.A.; Jin, A.-H.; Hamilton, B.; Rai, S.K.; Alewood, P.; Lewis, R.J. Venom Duct Origins of Prey Capture and Defensive Conotoxins in Piscivorous Conus striatus. Sci. Rep. 2021, 11, 13282. [Google Scholar] [CrossRef]
- Dobson, R.; Collodoro, M.; Gilles, N.; Turtoi, A.; De Pauw, E.; Quinton, L. Secretion and Maturation of Conotoxins in the Venom Ducts of Conus textile. Toxicon 2012, 60, 1370–1379. [Google Scholar] [CrossRef]
- Hu, H.; Bandyopadhyay, P.K.; Olivera, B.M.; Yandell, M. Elucidation of the Molecular Envenomation Strategy of the Cone Snail Conus geographus through Transcriptome Sequencing of Its Venom Duct. BMC Genom. 2012, 13, 284. [Google Scholar] [CrossRef] [PubMed]
- Prashanth, J.R.; Dutertre, S.; Rai, S.K.; Lewis, R.J. Venomics Reveals a Non-Compartmentalised Venom Gland in the Early Diverged Vermivorous Conus distans. Toxins 2022, 14, 226. [Google Scholar] [CrossRef]
- Page, L.R. Developmental Modularity and Phenotypic Novelty within a Biphasic Life Cycle: Morphogenesis of a Cone Snail Venom Gland. Proc. R. Soc. B Biol. Sci. 2011, 279, 77–83. [Google Scholar] [CrossRef] [PubMed]
- Bompiani, E.; Petrillo, U.F.; Lasinio, G.J.; Palini, F. High-Performance Computing with Terastat. In Proceedings of the 2020 IEEE Intl Conf on Dependable, Autonomic and Secure Computing, Intl Conf on Pervasive Intelligence and Computing, Intl Conf on Cloud and Big Data Computing, Intl Conf on Cyber Science and Technology Congress (DASC/PiCom/CBDCom/CyberSciTech), Calgary, AB, Canada, 17–22 August 2020; IEEE: New York, NY, USA, 2020; pp. 499–506. [Google Scholar]
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Full-Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef] [PubMed]
- Robinson, M.D.; Oshlack, A. A Scaling Normalization Method for Differential Expression Analysis of RNA-Seq Data. Genome Biol. 2010, 11, R25. [Google Scholar] [CrossRef] [PubMed]
- Love, M.I.; Huber, W.; Anders, S. Moderated Estimation of Fold Change and Dispersion for RNA-Seq Data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed]
- Peng, C.; Yao, G.; Gao, B.-M.; Fan, C.-X.; Bian, C.; Wang, J.; Cao, Y.; Wen, B.; Zhu, Y.; Ruan, Z.; et al. High-Throughput Identification of Novel Conotoxins from the Chinese Tubular Cone Snail (Conus betulinus) by Multi-Transcriptome Sequencing. Gigascience 2016, 5, s13742-016-0122-9. [Google Scholar] [CrossRef] [PubMed]
- Barghi, N.; Concepcion, G.P.; Olivera, B.M.; Lluisma, A.O. Comparison of the Venom Peptides and Their Expression in Closely Related Conus Species: Insights into Adaptive Post-Speciation Evolution of Conus Exogenomes. Genome Biol. Evol. 2015, 7, 1797–1814. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Barghi, N.; Lu, A.; Fedosov, A.E.; Bandyopadhyay, P.K.; Lluisma, A.O.; Concepcion, G.P.; Yandell, M.; Olivera, B.M.; Safavi-Hemami, H. Divergence of the Venom Exogene Repertoire in Two Sister Species of Turriconus. Genome Biol. Evol. 2017, 9, 2211–2225. [Google Scholar] [CrossRef]
- Chase, K.; Watkins, M.; Safavi-Hemami, H.; Olivera, B.M. Integrating Venom Peptide Libraries into a Phylogenetic and Broader Biological Framework. Front. Mol. Biosci. 2022, 9, 784419. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Chen, W.; Zhangsun, D.; Luo, S. Diversity of Conopeptides and Their Precursor Genes of Conus litteratus. Mar. Drugs 2020, 18, 464. [Google Scholar] [CrossRef]
- Singh, U.; Wurtele, E.S. Orfipy: A Fast and Flexible Tool for Extracting ORFs. Bioinformatics 2021, 37, 3019–3020. [Google Scholar] [CrossRef]
- Fu, L.; Niu, B.; Zhu, Z.; Wu, S.; Li, W. CD-HIT: Accelerated for Clustering the next-Generation Sequencing Data. Bioinformatics 2012, 28, 3150–3152. [Google Scholar] [CrossRef] [PubMed]
- Buchfink, B.; Xie, C.; Huson, D.H. Fast and Sensitive Protein Alignment Using DIAMOND. Nat. Methods 2015, 12, 59–60. [Google Scholar] [CrossRef] [PubMed]
- Almagro Armenteros, J.J.; Tsirigos, K.D.; Sønderby, C.K.; Petersen, T.N.; Winther, O.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 5.0 Improves Signal Peptide Predictions Using Deep Neural Networks. Nat. Biotechnol. 2019, 37, 420–423. [Google Scholar] [CrossRef] [PubMed]
- Käll, L.; Krogh, A.; Sonnhammer, E.L.L. Advantages of Combined Transmembrane Topology and Signal Peptide Prediction—The Phobius Web Server. Nucleic Acids Res. 2007, 35 (Suppl. S2), W429–W432. [Google Scholar] [CrossRef] [PubMed]
- Käll, L.; Krogh, A.; Sonnhammer, E.L.L. A Combined Transmembrane Topology and Signal Peptide Prediction Method. J. Mol. Biol. 2004, 338, 1027–1036. [Google Scholar] [CrossRef] [PubMed]
- Horton, P.; Park, K.-J.; Obayashi, T.; Fujita, N.; Harada, H.; Adams-Collier, C.J.; Nakai, K. WoLF PSORT: Protein Localization Predictor. Nucleic Acids Res. 2007, 35, W585–W587. [Google Scholar] [CrossRef] [PubMed]
- Simão, F.A.; Waterhouse, R.M.; Ioannidis, P.; Kriventseva, E.V.; Zdobnov, E.M. BUSCO: Assessing Genome Assembly and Annotation Completeness with Single-Copy Orthologs. Bioinformatics 2015, 31, 3210–3212. [Google Scholar] [CrossRef] [PubMed]
- Koua, D.; Ebou, A.; Dutertre, S. Improved Prediction of Conopeptide Superfamilies with ConoDictor 2.0. Bioinform. Adv. 2021, 1, vbab011. [Google Scholar] [CrossRef] [PubMed]
- Mistry, J.; Finn, R.D.; Eddy, S.R.; Bateman, A.; Punta, M. Challenges in Homology Search: HMMER3 and Convergent Evolution of Coiled-Coil Regions. Nucleic Acids Res. 2013, 41, e121. [Google Scholar] [CrossRef]
- Huerta-Cepas, J.; Forslund, K.; Coelho, L.P.; Szklarczyk, D.; Jensen, L.J.; von Mering, C.; Bork, P. Fast Genome-Wide Functional Annotation through Orthology Assignment by EggNOG-Mapper. Mol. Biol. Evol. 2017, 34, 2115–2122. [Google Scholar] [CrossRef]
- Huerta-Cepas, J.; Szklarczyk, D.; Forslund, K.; Cook, H.; Heller, D.; Walter, M.C.; Rattei, T.; Mende, D.R.; Sunagawa, S.; Kuhn, M.; et al. EggNOG 4.5: A Hierarchical Orthology Framework with Improved Functional Annotations for Eukaryotic, Prokaryotic and Viral Sequences. Nucleic Acids Res. 2016, 44, D286–D293. [Google Scholar] [CrossRef] [PubMed]
- Gabler, F.; Nam, S.-Z.; Till, S.; Mirdita, M.; Steinegger, M.; Söding, J.; Lupas, A.N.; Alva, V. Protein Sequence Analysis Using the MPI Bioinformatics Toolkit. Curr. Protoc. Bioinform. 2020, 72, e108. [Google Scholar] [CrossRef]
- Remmert, M.; Biegert, A.; Hauser, A.; Söding, J. HHblits: Lightning-Fast Iterative Protein Sequence Searching by HMM-HMM Alignment. Nat. Methods 2012, 9, 173–175. [Google Scholar] [CrossRef] [PubMed]
- Zimmermann, L.; Stephens, A.; Nam, S.-Z.; Rau, D.; Kübler, J.; Lozajic, M.; Gabler, F.; Söding, J.; Lupas, A.N.; Alva, V. A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at Its Core. J. Mol. Biol. 2018, 430, 2237–2243. [Google Scholar] [CrossRef]
- Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic Local Alignment Search Tool. J. Mol. Biol. 1990, 215, 403–410. [Google Scholar] [CrossRef]
- Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T.L. BLAST+: Architecture and Applications. BMC Bioinform. 2009, 10, 421. [Google Scholar] [CrossRef]
- Jumper, J.; Evans, R.; Pritzel, A.; Green, T.; Figurnov, M.; Ronneberger, O.; Tunyasuvunakool, K.; Bates, R.; Žídek, A.; Potapenko, A.; et al. Highly Accurate Protein Structure Prediction with AlphaFold. Nature 2021, 596, 583–589. [Google Scholar] [CrossRef] [PubMed]
- Evans, R.; O’Neill, M.; Pritzel, A.; Antropova, N.; Senior, A.; Green, T.; Žídek, A.; Bates, R.; Blackwell, S.; Yim, J.; et al. Protein Complex Prediction with AlphaFold-Multimer. bioRxiv 2022. [Google Scholar] [CrossRef]
- Mirdita, M.; Schütze, K.; Moriwaki, Y.; Heo, L.; Ovchinnikov, S.; Steinegger, M. ColabFold: Making Protein Folding Accessible to All. Nat. Methods 2022, 19, 679–682. [Google Scholar] [CrossRef]
- Kaas, Q.; Westermann, J.C.; Halai, R.; Wang, C.K.; Craik, D.J. ConoServer, a database for conopeptide sequences and structures. Bioinformatics 2008, 24, 445–446. [Google Scholar] [CrossRef]
- Kaas, Q.; Yu, R.; Jin, A.H.; Dutertre, S.; Craik, D.J. ConoServer: Updated content, knowledge, and discovery tools in the conopeptide database. Nucleic Acids Res. 2012, 40, D325–D330. [Google Scholar] [CrossRef] [PubMed]
- Trifinopoulos, J.; Nguyen, L.-T.; von Haeseler, A.; Minh, B.Q. W-IQ-TREE: A Fast Online Phylogenetic Tool for Maximum Likelihood Analysis. Nucleic Acids Res. 2016, 44, W232–W235. [Google Scholar] [CrossRef] [PubMed]
- Rambaut, A.; Drummond, A.J. FigTree, version 1.4.4; Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, UK, 2018. [Google Scholar]
ID | C | SG | VD | pVD | dVD | len | Matching Domains | Rating |
---|---|---|---|---|---|---|---|---|
Post-translational modification | ||||||||
PVC-01 | 488 | Peptidase S10 serine carboxypeptidase | SBCD | |||||
PVC-02 | x | 943 | Aminopeptidase M1, ERAP1 | SCD | ||||
PVC-03 | x | 725 | Peptidase S9 prolyl oligopeptidase | SBD | ||||
PVC-04 | x | 716 | Peptidase S9 prolyl oligopeptidase | SBCD | ||||
PVC-05 | x | 573 | Prolyl-4-hydroxylase, tetratricopeptide | SBCD | ||||
PVC-06 | x | 564 | Prolyl-4-hydroxylase, tetratricopeptide | SBCD | ||||
PVC-07 | 253 | Peroxiredoxin IV | SBCD | |||||
PVC-08 | 445 | Copper type II PAM monooxygenase (2) | SCD | |||||
PVC-09 | ! | 500 | Disulfide isomerase | SBCD | ||||
PVC-10 | ! | 492 | Disulfide isomerase | SBCD | ||||
PVC-11 | ! | 211 | Cyclophilin CeCYP16 | SBD | ||||
PVC-12 | ! | 353 | Glycoside hydrolase 47 | SBD | ||||
Regulation | ||||||||
PVC-13 | x | 148 | Attractin-like C-lectin | SCD | ||||
PVC-14 | x | 136 | Peptidase M13 neprilysin | SCD | ||||
PVC-15 | x | 369 | Peptidase M13 neprilysin | SCD | ||||
PVC-16 | x | 446 | GDA1/CD39 nucleoside phosphatase | SCD | ||||
PVC-17 | x | 197 | SUSHI repeat (2) | SCD | ||||
PVC-18 | x | 113 | Elevenin | SB | ||||
PVC-19 | 214 | EF-hand protein | SD | |||||
PVC-20 | 81 | Neuropeptide F | SBD | |||||
PVC-21 | 122 | Elevenin | SB | |||||
PVC-22 | 436 | vWFA-like (2) | SBCD | |||||
PVC-23 | 263 | Heparin, amyloid A4 precursor | SCD | |||||
PVC-24 | ! | 90 | Ferritin | BD | ||||
PVC-25 | ! | 111 | Ferritin | BD | ||||
PVC-26 | ! | 414 | Calreticulin | SD | ||||
PVC-27 | ! | 172 | TRAP-delta | SD | ||||
PVC-28 | ! | 596 | Exonuclease-Endonuclease-Phosphatase | SCD | ||||
PVC-29 | ! | 1407 | vWFC-like, collagen | SCD | ||||
PVC-30 | ! | 165 | Transposase, PAX domain | SCD | ||||
PVC-31 | ! | 155 | ML domain | SCD | ||||
PVC-32 | ! | 598 | Saposin (7) | SCD | ||||
PVC-33 | ! | 560 | Peptidases C1 cathepsin, cathepsin inhibitor, cystatin (2) | SBCD | ||||
PVC-34 | ! | 351 | Peptidases C1 cathepsin, cathepsin inhibitor | SBCD | ||||
PVC-35 | ! | 291 | Galactose-binding lectin (2) | SCD | ||||
Biosynthesis | ||||||||
PVC-36 | x | 56 | - | S | ||||
PVC-37 | x | 78 | Beta flower 3, DUF3931 | S | ||||
PVC-38 | x | 65 | DUF3530 | S | ||||
PVC-39 | x | 71 | tick salivary peptide | S | ||||
PVC-40 | x | 91 | tick salivary peptide | SC | ||||
PVC-41 | x | 67 | Conotoxin, DUF2756, Clavanin, haemadin | SC | ||||
PVC-42 | 94 | Conotoxin, spider neurotoxin | SC | |||||
PVC-43 | x | 93 | Conotoxin | SC | ||||
PVC-44 | x | 92 | tick salivary peptide | SC | ||||
PVC-45 | x | 55 | Conotoxin | S | ||||
PVC-46 | x | 80 | Conotoxin, Clavanin, haemadin | SC | ||||
PVC-47 | x | 51 | - | S | ||||
PVC-48 | x | 78 | Conotoxin, secapin, haemadin | SC | ||||
PVC-49 | x | 71 | Conotoxin, heavy metal binding | SC | ||||
PVC-50 | x | 48 | - | S | ||||
PVC-51 | x | 36 | Defensin propeptide | S | ||||
PVC-52 | 72 | Conotoxin | SC | |||||
PVC-53 | x | 95 | tick salivary peptide, Defensin | SC | ||||
PVC-54 | x | 136 | Kunitz/BPTI | SCD | ||||
PVC-55 | x | 105 | DUF3931 | SC | ||||
PVC-56 | x | 143 | Kunitz/BPTI (2) | SBCD | ||||
PVC-57 | x | 74 | Secapin | SC | ||||
PVC-58 | x | 38 | - | S | ||||
PVC-59 | x | 47 | tick salivary peptide | S | ||||
PVC-60 | 88 | Conotoxin | SC | |||||
PVC-61 | x | 53 | - | S | ||||
PVC-62 | x | 45 | - | SC | ||||
PVC-63 | x | 45 | - | SC | ||||
PVC-64 | x | 46 | Transmembrane 219 | S | ||||
PVC-65 | x | 69 | Conotoxin, tick salivary peptide | SC | ||||
PVC-66 | x | 81 | - | S | ||||
PVC-67 | x | 187 | Apolipoprotein M | SBC | ||||
PVC-68 | x | 88 | Conotoxin | SC | ||||
PVC-69 | x | 154 | Kunitz/BPTI | SCD | ||||
PVC-70 | x | 69 | tick salivary peptide | SC | ||||
PVC-71 | x | 90 | tick salivary peptide | SC | ||||
PVC-72 | x | 64 | - | S | ||||
PVC-73 | x | 110 | Conotoxin, macin | SC | ||||
PVC-74 | x | 47 | Beta flower 3, DU3931 | S | ||||
PVC-75 | x | 36 | - | S | ||||
PVC-76 | 94 | Myticin preproprotein | SBC | |||||
PVC-77 | x | 232 | Kunitz/BPTI (2) | BD | ||||
PVC-78 | x | 55 | - | S | ||||
PVC-79 | 41 | Pleurocidin antimicrobial 12 | SB | |||||
PVC-80 | x | 157 | Kunitz/BPTI (2) | SBCD | ||||
PVC-81 | 41 | Pleurocidin antimicrobial 12 | SB | |||||
PVC-82 | 100 | Conotoxin, spider neurotoxin | SCD | |||||
PVC-83 | x | 606 | DUF885, nucleoporin FG2, tyrosine carboxypeptidase | SD | ||||
PVC-84 | 143 | Kunitz/BPTI (2) | SBCD | |||||
PVC-85 | x | 235 | Nicotinic acetylcholine receptor | SCD | ||||
PVC-86 | 115 | Conotoxin, chitin-binding | SCD | |||||
PVC-87 | 97 | Conotoxin, chitin-binding | SB | |||||
PVC-88 | 120 | Chitin-binding | SB | |||||
PVC-89 | 457 | CRISP, ShK toxin (3) | SBCD | |||||
PVC-90 | 99 | Conotoxin | SB | |||||
PVC-91 | 920 | Tumour necrosis factor | SCD | |||||
PVC-92 | 311 | Cardio active peptide (2) | SBC | |||||
PVC-93 | 434 | Chitin-binding (3), pentraxin | SCD | |||||
PVC-94 | x | 203 | Insulin-like growth factor, conotoxin | SCD | ||||
PVC-95 | 391 | FMRFamide | SD | |||||
PVC-96 | 417 | Chitin-binding (3), pentraxin | SCD | |||||
PVC-97 | ! | 116 | Conotoxin precursor | SBC | ||||
PVC-98 | ! | 108 | Conotoxin precursor | SBC | ||||
PVC-99 | ! | 86 | - | SC | ||||
PVC-100 | ! | 70 | Conotoxin, Kunitz/BPTI | SBCD | ||||
PVC-101 | ! | 185 | Insulin-homologue binding site, Thyroglobulin | SCD | ||||
PVC-102 | ! | 409 | Kunitz/BPTI, WAP (3) | SBCD | ||||
PVC-103 | ! | 219 | CRISP | SBCD | ||||
PVC-104 | ! | 139 | Conotoxin, Kunitz/BPTI, Kunitz/BPTI | SCD |
Sample ID | Sampling Data | Date | C | SG | VD | pVD | dVD | GC |
---|---|---|---|---|---|---|---|---|
BAU 4602 | France, Brittany, Ploubazlanec, Pointe de l’Arcouest 48.8209, −3.0100 | 1 June | x | |||||
BAU 4604 | 1 June | x | x | |||||
BAU 4605 | 1 June | x | ||||||
BAU 4607 | 6 June | x | x | x | x | |||
BAU 4609 | 14 June | x | x | |||||
BAU 4611 | 16 June | x | x | x | x | x |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Chiappa, G.; Fassio, G.; Modica, M.V.; Oliverio, M. Potential Ancestral Conoidean Toxins in the Venom Cocktail of the Carnivorous Snail Raphitoma purpurea (Montagu, 1803) (Neogastropoda: Raphitomidae). Toxins 2024, 16, 348. https://doi.org/10.3390/toxins16080348
Chiappa G, Fassio G, Modica MV, Oliverio M. Potential Ancestral Conoidean Toxins in the Venom Cocktail of the Carnivorous Snail Raphitoma purpurea (Montagu, 1803) (Neogastropoda: Raphitomidae). Toxins. 2024; 16(8):348. https://doi.org/10.3390/toxins16080348
Chicago/Turabian StyleChiappa, Giacomo, Giulia Fassio, Maria Vittoria Modica, and Marco Oliverio. 2024. "Potential Ancestral Conoidean Toxins in the Venom Cocktail of the Carnivorous Snail Raphitoma purpurea (Montagu, 1803) (Neogastropoda: Raphitomidae)" Toxins 16, no. 8: 348. https://doi.org/10.3390/toxins16080348