Toxins of the venom of tarantulas (Theraphosidae, Arachnida) in interspecies interactions
https://doi.org/10.35885/1684-7318-2024-4-410-430
Abstract
Spiders are the most important entomophages in ecosystems. They are the most numerous poisonous animals on the planet, indispensable regulators of populations’ numbers by killing mainly insects and other small arthropods. Spiders are an integral part of the food chain; they produce venom serving to immobilize the prey. Spider venoms are a “natural combinatorial library” of biologically active substances, with varying effectiveness and specificity. A feature of the biological effect of spider’s venom is a unique combination of the low toxicity of the whole venom, for both animals and humans, with high selectivity of the interaction of the neurotoxins, which are part of the venom, with the molecular structures of ion channels and synaptic receptors of the nervous system. The present review introduces the reader to new fundamental facts, ideas and perspective of the practical application of spider’s venoms in biomedical research and drug design. The current state of research on a unique set of polypeptide toxins which serve as chemical factors (allomons) of the interspecific (allelochemical) interactions of spiders of the family Thetaphosidae is considered. Modern information on the structure of spiders’ venom toxins is analyzed using the UniProt database. The latest bioecological and toxicological characteristics of tarantulas are presented. The chemical nature and mechanism of action of some unique toxins selectively acting on key processes in the nervous system are considered. The toxins act upon synaptic transmission and the functioning ion channels, which allow spiders not only to interact with various molecular targets of the prey or predator, but also to implement various life strategies, gaining an evolutionary advantage.
About the Authors
David B. Gelashvili
Lobachevsky State University of Nizhni Novgorod
Russian Federation
Russian Federation
23 Gagarin Avenue, Nizhni Novgorod 603950
Elena B. Romanova
Lobachevsky State University of Nizhni Novgorod
Russian Federation
Russian Federation
23 Gagarin Avenue, Nizhni Novgorod 603950
References
1. Agwa A. J., Lawrence N., Deplazes E., Cheneval O., Chen R. M., Craik D. J., Schroeder C. I., Henriques S.T. Spider peptide toxin HwTx-IV engineered to bind to lipid membranes has an increased inhibitory potency at human voltage-gated sodium channel hNav1.7. Biochimica et Biophysica Acta, 2017, vol. 1859, no. 5, pp. 835–844. https://doi.org/10.1016/j.bbamem.2017.01.020
2. Ardisson-Araújo D. M. P., Morgado F. D. S., Schwartz E. F., Corzo G., Ribeiro B. M. A new theraphosid spider toxin causes early insect cell death by necrosis when expressed in vitro during recombinant baculovirus infection. PLoS ONE, 2013, vol. 12, no. 8, article no. e84404. https://doi.org/10.1371/journal.pone.0084404
3. Bowman C. L., Gottlieb P. A., Suchyna T. M., Murphy Y. K., Sachs F. Mechanosensitive ion channels and the peptide inhibitor GsMTx-4: History, properties, mechanisms and pharmacology. Toxicon, 2007, vol. 49, iss. 2, pp. 249–270. https://doi.org/10.1016/j.toxicon.2006.09.030
4. Chan T. K., Geren C. R., Howell D. E., Odell G. V. Adenosine triphosphate in tarantula spider venoms and its synergistic effect with the venom toxin. Toxicon, 1975, vol. 13, iss. 1, pp. 61–66.
5. Chen J., Deng M., He Q., Meng E., Jiang L., Liao Z., Rong M., Liang S. Molecular diversity and evolution of cystine knot toxins of the tarantula Chilobrachys jingzhao. Cellular and Molecular Life Sciences, 2008, vol. 65, iss. 15, pp. 2431–2444. https://doi.org/10.1007/s00018-008-8135-x
6. Cheng T.-C., Long R.-W., Wu Y.-Q., Guo Y.-B., Liu D.-L., Peng L., Li D.-Q., Yang D.-W., Xu X., Liu F.-X., Хia Q.-Y. Identification and characterization of toxins in the venom gland of the Chinese bird spider, Haplopelma hainanum, by transcriptomic analysis. Insect Science, 2016, vol. 23, iss. 3, pp. 487–499. https://doi.org/10.1111/1744-7917.12305
7. Cromer B. A., McIntyre P. Painful toxins acting at TRPV1. Toxicon, 2008, vol. 51, iss. 2, pp. 163–173.
8. Dawson R. J., Benz J., Stohler P., Tetaz T., Joseph C., Huber S., Schmid G., Hügin D., Pflimlin P., Trube G., Rudolph M.G., Hennig M., Ruf A. Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1. Nature Communications, 2012, no. 3, article no. 936. https://doi.org/10.1038/ncomms1917
9. Deng M., Luo X., Xiao Y., Sun Z., Jiang L., Liu Z., Zeng X., Chen H., Tang J., Zeng W., Liang S. Huwentoxin-XVI, an analgesic, highly reversible mammalian N-type calcium channel antagonist from Chinese tarantula Ornithoctonus huwena. Neuropharmacology, 2014, vol. 79, pp. 657–667. https://doi.org/10.1016/j.neuropharm.2014.01.017
10. Escoubas P., Bernard C., Lambeau G., Lazdunski M., Darbon H. Recombinant production and solution structure of PcTx1, the specific peptide inhibitor of ASIC1a proton-gated cation channels. Protein Science, 2003, vol. 12, iss. 7, pp. 1332–1343. https://doi.org/10.1110/ps.0307003
11. Escoubas P., De Weille J. R., Lecoq A., Diochot S., Waldmann R., Champigny G., Moinier D., Ménez A., Lazdunski M. Isolation of a tarantula toxin specific for a class of proton-gated Na+channels. Journal of Biological Chemistry, 2000, vol. 275, iss. 33, pp. 25116–25121. https://doi.org/10.1074/jbc.M003643200
12. Escoubas P., Diochot S., Celerier M.-L., Nakajima T., Lazdunski M. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Molecular Pharmacology, 2002, vol. 62, iss. 1, pp. 48–57. https://doi.org/10.1124/mol.62.1.48
13. Escoubas P., Rash L. Tarantulas: Eight-legged pharmacists and combinatorial chemists. Toxicon, 2004, vol. 43, iss. 5, pp. 555–574. https://doi.org/10.1016/j.toxicon.2004.02.007
14. Fletcher J. I., Wang X., Connor M., Christie M. J., King G. F., Nicholson G. M. Spider toxins: A new group of potassium channel modulators. Perspectives in Drug Discovery and Design, 1999, vol. 15, iss. 1, pp. 61–69.
15. Gelashvili D. B., Krylov V. N., Romanova E. B. Zootoxinology: Bioecological and Biomedical Aspects. Nizhnij Novgorod, Lobachevsky State University of Nizhni Novgorod Publ., 2015. 770 p. (in Russian).
16. Gladkikh I. N., Sintsova O. V., Leychenko E. V., Kozlov S. A. TRPV1 ion channel: Structural features, activity modulators, and therapeutic potential. Biochemistry, 2021, vol. 86, supll. 1, pp. 50–70. https://doi.org/10.1134/S0006297921140054
17. Herrington J. Gating modifier peptides as probes of pancreatic β-cell physiology. Toxicon, 2007, vol. 49, iss. 2, pp. 231–238. https://doi.org/10.1016/j.toxicon.2006.09.012
18. Herzig V. Arthropod assassins: Crawling biochemists with diverse toxin pharmacopeias. Toxicon, 2019, vol. 158, pp. 33–37. https://doi.org/10.1016/j.toxicon.2018.11.312
19. Hesselberg T., Galvez D. Spider ecology and behaviour–spiders as model organisms. Insects, 2023, vol. 14, no. 4, article no. 330. https://doi.org/10.3390/insects14040330
20. Khan S. A., Zafar Y., Briddon R. W., Malik K. A., Mukhtar Z. Spider venom toxin protects plants from insect attack. Transgenic Research, 2006, vol. 15, iss. 3, pp. 349–357. https://doi.org/10.1007/s11248-006-0007-2
21. King G. F., Gentz M. C., Escoubas P., Graham M. N. A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon, 2008, vol. 52, iss. 2, pp. 264–276. https://doi.org/10.1016/j.toxicon.2008.05.020
22. Kuhn-Nentwig L., Stocklin R., Nentwig W. Venom composition and strategies in spiders: Is everything possible? Advances in Insect Physiology, 2011, vol. 40, pp. 1–86. https://doi.org/10.1016/B978-0-12-387668-3.00001-5
23. Lampe R. A., Defeo P. A., Davison M. D., Young J., Herman J. L., Spreen R. C., Horn M. B., Mangano T. J., Keith R. A. Isolation and pharmacological characterization of omega-grammotoxin SIA, a novel peptide inhibitor of neuronal voltage-sensitive calcium channel responses. Molecular Pharmacology, 1993, vol. 44, iss. 2, pp. 451–460.
24. Lee S., Milescu M., Jung H. H., Lee J. Y., Bae C. H., Lee C. W., Kim H. H., Swartz K. J., Kim J. I. Solution structure of GxTX-1E, a high-affinity tarantula toxin interacting with voltage sensors in Kv2.1 potassium channels. Biochemistry, 2010, vol. 49, iss. 25, pp. 5134–5142. https://doi.org/10.1021/bi100246u
25. Li D., Xiao Y., Hu W., Xie J., Bosmans F., Tytgat J., Liang S. Function and solution structure of hainantoxin-I, a novel insect sodium channel inhibitor from the Chinese bird spider Selenocosmia hainana. FEBS Letters, 2003, vol. 555, iss.3, pp. 616–622. https://doi.org/10.1016/s00145793(03)01303-6
26. Liang S. An overview of peptide toxins from the venom of the Chinese bird spider Selenocosmia huwena Wang [=Ornithoctonus huwena (Wang)]. Toxicon, 2004, vol. 43, iss. 5, pp. 575–585. https://doi.org/10.1016/j.toxicon.2004.02.005
27. Liao Z., Cao J., Li S., Yan X., Hu W., He Q., Chen J., Tang J., Xie J., Liang S. Proteomic and peptidomic analysis of the venom from Chinese tarantula Chilobrachys jingzhao. Proteomics, 2007, vol. 7, iss. 11, pp. 1892–1907. https://doi.org/10.1002/pmic.200600785
28. Liu Z., Cai T., Zhu Q., Deng M., Li J., Zhou X., Zhang F., Li D., Liu Y., Hu W., Liang S. Structure and function of hainantoxin-III, a selective antagonist of neuronal tetrodotoxin-sensitive voltage-gated sodium channels isolated from the chinese bird spider Ornithoctonus hainana. Journal of Biological Chemistry, 2013, vol. 288, iss. 28, pp. 20392–20403. https://doi.org/10.1074/jbc.m112.426627
29. Lüddecke T., Herzig V., von Reumont B. M., Vilcinskas A. The biology and evolution of spider venoms. Biological Reviews, 2022, vol. 97, pp. 163–178. https://doi.org/10.1111/brv.12793
30. Middleton R. E., Warren V. A., Kraus R. L., Hwang J. C., Liu C. J., Dai G., Brochu R. M., Kohler M. G., Gao Y.-D., Garsky V. M., Bogusky M. J., Mehl J. T., Cohen C. J., Smith M. M. Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry, 2002, vol. 41, iss. 50, pp. 14734–14747. https://doi.org/10.1021/bi026546a
31. Odell G. V., Ownby C. L., Christian C. D., Hudiburg S. A., Herrero V., Swartz P. D., Hooper K. P. A review of research on tarantula colony maintenance, venom collection, composition and toxicity. Toxicon, 1987, vol. 25, iss. 2, pp. 151. https://doi.org/10.1016/0041-0101(87)90219-4 Osteen J. D., Herzig V., Gilchrist J., Emrick J. J., Zhang C., Wang X., Castro J., GarciaCaraballo S., Grundy L., Rychkov G. Y. Selective spider toxins reveal a role for the Nav1.1 channel in mechanical pain. Nature, 2016, vol. 534, no. 7680, pp. 494–499. https://doi.org/10.1038/nature17976
32. Ostrow K. L., Mammoser A., Suchyna T., Sachs F., Oswald R., Kubo S., Chino N., Gottlieb P. A. cDNA sequence and in vitro folding of GsMTx4, a specific peptide inhibitor of mechanosensitive channels. Toxicon, 2003, vol. 42, iss. 3, pp. 263–274. https://doi.org/10.1016/s00410101(03)00141-7
33. Pekar S., Coddington J. A., Blackledge T. A. Evolution of stenophagy in spiders (Araneae): Evidence based on the comparative analysis of spider diets. Evolution, 2011, vol. 66, iss. 3, pp. 776–778. https://doi.org/10.1111/j.1558-5646.2011.01471.x
34. Pérez-Miles F. Introduction to the Theraphosidae. In: Pérez-Miles F., ed. New World Tarantulas: Taxonomy, Biogeography and Evolutionary Biology of Theraphosidae. Cham, Springer Nature, 2020, pp. 1–24. https://doi.org/10.1007/978-3-030-48644-0_1
35. Pineda S. S., Chin Y. K. Y., Undheim E. A. B., King G. F. Structural venomics reveals evolution of a complex venom by duplication and diversification of an ancient peptide-encoding gene. Proceedings of the National Academy of Sciences, 2020, vol. 117, no. 21, pp. 11399–11408. https://doi.org/10.1073/pnas.1914536117
36. Piser T. M., Lampe R. A., Keith R. A., Thayer S. A. Complete and reversible block by ωgrammotoxin SIA of glutamatergic synaptic transmission between cultured rat hippocampal neurons. Neuroscience Letters, 1995, vol. 201, iss. 2, pp. 135–138. https://doi.org/10.1016/03043940(95)12169-2
37. Platnick N. I., ed. Spiders of the World: A Natural History. Princeton, Princeton University Press, 2020. 257 p. https://doi.org/10.1525/9780691204987
38. Priest B. T., Blumenthal K. M., Smith J. J., Warren V. A., Smith M. M. ProTx-I and ProTxII: Gating modifiers of voltage-gated sodium channels. Toxicon, 2007, vol. 49, iss. 2, pp. 194–201. https://doi.org/10.1016/j.toxicon.2006.09.014
39. Richards K. L., Milligan C., Richardson R. J., Jancovski N., Grunnet M., Jacobson L. H., Undheim E. A. B., Mobli M. Selective Nav1.1 activation rescues Dravet syndrome mice from seizures and premature death. Proceedings of the National Academy of Sciences, 2018, vol. 115, no. 34, pp. 8077–8085. https://doi.org/10.1073/pnas.1804764115
40. Saez N. J., Mobli M., Bieri M., Chassagnon I. R., Malde A. K., Gamsjaeger R., Mark A. E., Gooley P. R., Rash L. D., King G. F. A dynamic pharmacophore drives the interaction between Psalmotoxin-1 and the putative drug target acid-sensing ion channel 1a. Molecular Pharmacology, 2011, vol. 80, iss. 5, pp. 796–808. https://doi.org/10.1073/pnas.180476411510.1124/mol.111.072207
41. Saez N. J., Senff S., Jensen J. E., Er S. Y., Herzig V., Rash L. D., King G. F. Spider-venom peptides as therapeutics. Toxins, 2010, vol. 2, iss. 12, pp. 2851–2871. https://doi.org/10.3390/toxins2122851
42. Schanbacher F. L., Lee C. K., Wilson I. B., Howell D. E., Odell G. V. Purification and characterization of tarantula, Dugesiella hentzi (Girard) venom hyaluronidase. Comparative Biochemistry &Physiology, 1973, vol. 44, iss. 2, pp. 389–396.
43. Siemens J., Zhou S., Piskorowski R., Nikai T., Lumpkin E. A., Basbaum A. I., King D., Julius D. Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature, 2006, vol. 444, pp. 208–212.
44. Suchyna T. M., Johnson J. H., Hamer K., Joseph F., Leykam D. A., Gage H. F., Clive C., Baumgarten M., Sachs F. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. Journal of General Physiology, 2000, vol. 115, iss. 5, pp. 583–598. https://doi.org/10.1085/jgp.115.5.583
45. Swartz K. J., MacKinnon R. Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites. Neuron, 1997, vol. 18, iss. 4, pp. 665–673. https://doi.org/10.1016/s0896-6273(00)80306-2
46. Takahashi H., Kim J. I., Min H. J., Sato K., Swartz K. J., Shimada I. Solution structure of hanatoxin1, a gating modifier of voltage-dependent K+ channels: Common surface features of gating modifier toxins. Journal of Molecular Biology, 2000, vol. 297, iss. 3, pp. 771–780. https://doi.org/10.1006/jmbi.2000.3609
47. Takeuchi K., Park E. J., Lee C. W., Takeuchi K., Park E. J., Lee C. W., Kim J. I., Takahashi H., Swartz K. J., Shimada I. Solution structure of ω-grammotoxin SIA, a gating modifier of P/Q and N-type Ca2+ channel. Journal of Molecular Biology, 2002, vol. 321, iss. 3, pp. 517–526. https://doi.org/10.1016/s0022-2836(02)00595-8
48. Tilley D. C., Angueyra J. M., Eum K. S., Kim H., Chao L.H., Peng A.W., Sack J.T. The tarantula toxin GxTx detains K+ channel gating charges in their resting conformation. Journal of General Physiology, 2019, vol. 151, iss. 3, pp. 292–315. https://doi.org/10.1085/jgp.201812213
49. Vassilevski A. A., Kozlov S. A., Grishin E. V. Molecular diversity of spider venom. Biochemistry, 2009, vol. 74, no. 13, pp. 1505–1534. https://doi.org/10.1134/S0006297909130069
50. Whittaker R. H., Feeny P. P. Allelochemics: Chemical interactions between species. Science, 1971, vol. 17, no. 3973, pp. 757–770. https://doi.org/10.1126/science.171.3973.757
51. Wigger E., Kuhn-Nentwig L., Nentwig W. The venom optimisation hypothesis: A spider injects large venom quantities only into difficult prey types. Toxicon, 2002, vol. 40, iss. 6, pp. 749–752. https://doi.org/10.1016/s0041-0101(01)00277-x
52. World Spider Catalog. Version 25.0. Bern, Natural History Museum, 2024. Available at: http://wsc.nmbe.ch/ (accessed January 21, 2024). https://doi.org/10.24436/2
53. Wright Z. V. F., McCarthy S., Dickman R., Reyes F. E., Sanchez-Martinez S., Cryar A., Kilford I., Hall A. The role of disulfide bond replacements in analogues of the tarantula toxin ProTxII and their effects on inhibition of the voltage-gated sodium ion channel Nav1.7. J. Journal of the American Chemical Society, 2017, vol. 139, no. 37, pp. 13063–13075. https://doi.org/10.1021/jacs.7b06506
54. Xiao Y., Tang J., Hu W., Xie J., Maertens C., Tytgat J., Liang S. Jingzhaotoxin-I, a novel spider neurotoxin preferentially inhibiting cardiac sodium channel inactivation. Journal of Biological Chemistry, 2004, vol. 280, iss. 13, pp. 12069–12076. https://doi.org/10.1074/jbc.m411651200
55. Yuan C. H., He Q. Y., Peng K., Diao J.-B., Jiang L.-P., Tang X., Liang S.-P. Discovery of a distinct superfamily of Kunitz-type toxin (KTT) from tarantulas. PLoS ONE, 2008, vol. 3, no. 10, article no. e3414. https://doi.org/10.1371/journal.pone.0003414
Review
For citations:
Gelashvili D.B., Romanova E.B. Toxins of the venom of tarantulas (Theraphosidae, Arachnida) in interspecies interactions. Povolzhskiy Journal of Ecology. 2024;(4):410 – 430. (In Russ.) https://doi.org/10.35885/1684-7318-2024-4-410-430
Views:
1219
Email this article 
