Comprehensive molecular characterization and comparison of venom proteins and transcripts in three Gloydius species from South Korea

comprehensive-molecular-characterization-and-comparison-of-venom-proteins-and-transcripts-in-three-gloydius-species-from-south-korea
Comprehensive molecular characterization and comparison of venom proteins and transcripts in three Gloydius species from South Korea

References

  1. WHO. Snakebite envenoming: a strategy for prevention and control. WHO Neglected Tropical (2019).

  2. Tasoulis, T. & Isbister, G. K. A review and database of snake venom proteomes. Toxins (Basel). 9. https://doi.org/10.3390/toxins9090290 (2017).

  3. Tan, K. Y., Tan, N. H. & Tan, C. H. Venom proteomics and antivenom neutralization for the Chinese Eastern russell’s viper, Daboia siamensis from Guangxi and Taiwan. Sci. Rep. 8, 8545. https://doi.org/10.1038/s41598-018-25955-y (2018).

    Google Scholar 

  4. Calvete, J. J. Snake venomics: from the inventory of toxins to biology. Toxicon 75, 44–62. https://doi.org/10.1016/j.toxicon.2013.03.020 (2013).

    Google Scholar 

  5. Serok Lee, M. D. W. J. M. D. Epidemiology of patients with snake bite or envenomation in emergency department: NEDIS (National emergency department information System). Journal Korean Soc. Clin. Toxicology 20(2) (2022).

  6. Shim, J. S., Kang, H., Cho, Y., Shin, H. & Lee, H. Adverse reactions after administration of antivenom in Korea. Toxins (Basel). 12. https://doi.org/10.3390/toxins12080507 (2020).

  7. Li, L., Huang, J. Z. & Lin, Y. Snake venoms in cancer therapy: Past, present and future. Toxins 10 https://doi.org/10.3390/toxins10090346 (2018).

  8. Debono, J., Bos, M. H. A., Do, M. S. & Fry, B. G. Clinical implications of coagulotoxic variations in Mamushi (Viperidae: Gloydius) snake venoms. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 225, 108567. https://doi.org/10.1016/j.cbpc.2019.108567 (2019).

    Google Scholar 

  9. Shin, Y., Jang, Y. & Borzee, A. Snakebite envenomings in the Republic of Korea from the 1970s to the 2020s: A review. Toxicon 196, 8–18. https://doi.org/10.1016/j.toxicon.2021.03.013 (2021).

    Google Scholar 

  10. Gao, J. F. et al. Proteomic and biochemical analyses of short-tailed pit Viper (Gloydius brevicaudus) venom: age-related variation and composition-activity correlation. J. Proteom. 105, 307–322. https://doi.org/10.1016/j.jprot.2014.01.019 (2014).

    Google Scholar 

  11. Yang, Z. M. et al. Transcriptome and proteome of the highly neurotoxic venom of gloydius intermedius. Toxicon 107, 175–186. https://doi.org/10.1016/j.toxicon.2015.08.010 (2015).

    Google Scholar 

  12. Slagboom, J. et al. Haemotoxic snake venoms: their functional activity, impact on snakebite victims and pharmaceutical promise. Br. J. Haematol. 177 (6), 947–959 (2017).

    Google Scholar 

  13. Gutierrez, J. M. et al. Snakebite envenoming. Nat. Rev. Dis. Primers. 3, 17079. https://doi.org/10.1038/nrdp.2017.79 (2017).

    Google Scholar 

  14. Oliveira, A. L. et al. The chemistry of snake venom and its medicinal potential. Nat. Rev. Chem. 6, 451–469. https://doi.org/10.1038/s41570-022-00393-7 (2022).

    Google Scholar 

  15. Anas Bedraoui, M. S. et al. Rachid El Fatimy, Tariq Daouda,. Therapeutic potential of snake venom: toxin distribution and opportunities in deep learning for novel drug discovery. Medicine Drug Discovery 21 (2024).

  16. El-Aziz, M. A., Garcia Soares, T., Stockand, J. D. & A. & Snake venoms in drug discovery: valuable therapeutic tools for life saving. Toxins (Basel). 11. https://doi.org/10.3390/toxins11100564 (2019).

  17. Messadi, E. Snake venom components as therapeutic drugs in ischemic heart disease. Biomolecules 13 https://doi.org/10.3390/biom13101539 (2023).

  18. Ferreira, S. H., Bartelt, D. C. & Greene, L. J. Isolation of bradykinin-potentiating peptides from Bothrops Jararaca venom. Biochemistry 9, 2583–2593. https://doi.org/10.1021/bi00815a005 (1970).

    Google Scholar 

  19. Venoms to Drugs: Venom as a Source for the Development of Human Therapeutics. (2015).

  20. Canas, C. A., Castano-Valencia, S., Castro-Herrera, F., Canas, F. & Tobon, G. J. Biomedical applications of snake venom: from basic science to autoimmunity and rheumatology. J. Transl Autoimmun. 4, 100076. https://doi.org/10.1016/j.jtauto.2020.100076 (2021).

    Google Scholar 

  21. Macêdo, J. K. A., Fox, J. W. & Castro, M. D. Disintegrins from snake venoms and their applications in cancer research and therapy. Curr. Protein Pept. Sci. 16, 532–548. https://doi.org/10.2174/1389203716666150515125002 (2015).

    Google Scholar 

  22. Alomran, N. et al. Exploring the utility of Recombinant snake venom Serine protease toxins as immunogens for generating experimental snakebite antivenoms. Toxins 14 https://doi.org/10.3390/toxins14070443 (2022).

  23. Luddecke, T. et al. Venom biotechnology: casting light on nature’s deadliest weapons using synthetic biology. Front. Bioeng. Biotechnol. 11, 1166601. https://doi.org/10.3389/fbioe.2023.1166601 (2023).

    Google Scholar 

  24. Rivera-de-Torre, E. et al. Strategies for heterologous Expression, Synthesis, and purification of animal venom toxins. Front. Bioeng. Biotechnol. 9 https://doi.org/10.3389/fbioe.2021.811905 (2022).

  25. Vyas, V. K., Brahmbhatt, K., Bhatt, H. & Parmar, U. Therapeutic potential of snake venom in cancer therapy: current perspectives. Asian Pac. J. Trop. Biomed. 3, 156–162. https://doi.org/10.1016/S2221-1691(13)60042-8 (2013).

    Google Scholar 

  26. Rao, W. Q. et al. The rise of genomics in snake venom research: recent advances and future perspectives. Gigascience 11 https://doi.org/10.1093/gigascience/giac024 (2022).

  27. Durban, J. et al. Profiling the venom gland transcriptomes of Costa Rican snakes by 454 pyrosequencing. BMC Genom. 12 https://doi.org/10.1186/1471-2164-12-259 (2011).

  28. Rokyta, D. R., Wray, K. P., Lemmon, A. R., Lemmon, E. M. & Caudle, S. B. A high-throughput venom-gland transcriptome for the Eastern Diamondback rattlesnake and evidence for pervasive positive selection across toxin classes. Toxicon 57, 657–671. https://doi.org/10.1016/j.toxicon.2011.01.008 (2011).

    Google Scholar 

  29. Casewell, N. R. et al. Medically important differences in snake venom composition are dictated by distinct postgenomic mechanisms. Proc. Natl. Acad. Sci. U.S.A. 111, 9205–9210. https://doi.org/10.1073/pnas.1405484111 (2014).

    Google Scholar 

  30. Tan, K. Y., Tan, C. H., Chanhome, L. & Tan, N. H. Comparative venom gland transcriptomics of (monocled cobra) from Malaysia and thailand: elucidating geographical venom variation and insights into sequence novelty. Peerj 5 https://doi.org/10.7717/peerj.3142 (2017).

  31. Moon, J., Chun, B., Cho, Y. & Park, K. Clinical characteristics of snake envenomation-related acute kidney injury in South Korea. Sci. Rep. 14, 23503. https://doi.org/10.1038/s41598-024-74142-9 (2024).

    Google Scholar 

  32. Moon, J. M., Chun, B. J. & Koo, Y. J. The association between the neutrophil lymphocyte ratio and local edema after Viper snake envenomation in South Korea. Toxicon 240 https://doi.org/10.1016/j.toxicon.2024.107635 (2024).

  33. Roman-Ramos, H. & Ho, P. L. Current technologies in snake venom analysis and applications. Toxins (Basel). 16. https://doi.org/10.3390/toxins16110458 (2024).

  34. Sanchez, E. F., Flores-Ortiz, R. J., Alvarenga, V. G. & Eble, J. A. Direct fibrinolytic snake venom metalloproteinases affecting hemostasis: Structural, biochemical features and therapeutic potential. Toxins (Basel). 9. https://doi.org/10.3390/toxins9120392 (2017).

  35. Akesson, J. et al. Proteomics reveal biomarkers for diagnosis, disease activity and long-term disability outcomes in multiple sclerosis. Nat. Commun. 14, 6903. https://doi.org/10.1038/s41467-023-42682-9 (2023).

    Google Scholar 

  36. Frantzi, M., Bhat, A. & Latosinska, A. Clinical proteomic biomarkers: relevant issues on study design & technical considerations in biomarker development. Clin. Transl Med. 3, 7. https://doi.org/10.1186/2001-1326-3-7 (2014).

    Google Scholar 

  37. Serrano, S. M., Shannon, J. D., Wang, D., Camargo, A. C. & Fox, J. W. A multifaceted analysis of Viperid snake venoms by two-dimensional gel electrophoresis: an approach to Understanding venom proteomics. Proteomics 5, 501–510. https://doi.org/10.1002/pmic.200400931 (2005).

    Google Scholar 

  38. Modahl, C. M., Brahma, R. K., Koh, C. Y., Shioi, N. & Kini, R. M. Omics technologies for profiling toxin diversity and evolution in snake venom: impacts on the discovery of therapeutic and diagnostic agents. Annu. Rev. Anim. Biosci. 8, 91–116. https://doi.org/10.1146/annurev-animal-021419-083626 (2020).

    Google Scholar 

  39. Modahl, C. M., Saviola, A. J. & Mackessy, S. P. Integration of transcriptomic and proteomic approaches for snake venom profiling. Expert Rev. Proteom. 18, 827–834. https://doi.org/10.1080/14789450.2021.1995357 (2021).

    Google Scholar 

  40. Machado Marinho, A. C. et al. The role of venom proteomics and single-domain antibodies for antivenoms: progress in snake envenoming treatment. Drug Discov Today. 29, 103967. https://doi.org/10.1016/j.drudis.2024.103967 (2024).

    Google Scholar 

  41. Willard, N. K. et al. Proteomic identification and quantification of snake venom biomarkers in venom and plasma extracellular vesicles. Toxins (Basel). 13. https://doi.org/10.3390/toxins13090654 (2021).

  42. Lau, J. L. & Dunn, M. K. Therapeutic peptides: historical perspectives, current development trends, and future directions. Bioorg. Med. Chem. 26, 2700–2707. https://doi.org/10.1016/j.bmc.2017.06.052 (2018).

    Google Scholar 

  43. Mirzaei, S. et al. Venom peptides in cancer therapy: an updated review on cellular and molecular aspects. Pharmacol. Res. 164 https://doi.org/10.1016/j.phrs.2020.105327 (2021).

  44. Moon, J. M., Chun, B. J. & Cho, Y. S. Clinical features of snake envenomation in South Korea. Clin. Toxicol. (Phila). 61, 276–282. https://doi.org/10.1080/15563650.2022.2160341 (2023).

    Google Scholar 

  45. Jae-Han Shim, Y. J. S., Lee, S. S., Park, K. S. & Oh, H. B. Young-Do Park. Ecological study on poisonous snake and investigation of the venom Characteristics, snakebiting frequenty in Korea. Korean Soc. Environ. Ecol. 12, 58–77 (1998).

    Google Scholar 

  46. Frangieh, J. et al. Snake venom components: tools and cures to target cardiovascular diseases. Molecules 26 https://doi.org/10.3390/molecules26082223 (2021).

  47. Ochoa-Mosquera, J., Montoya-Gómez, A. & Jiménez-Charris, E. Snake venom toxins as potential therapeutic agents in the treatment of prostate cancer. Mol. Biol. Rep. 51 https://doi.org/10.1007/s11033-024-09970-z (2024).

  48. Roy, A. & Bharadvaja, N. Venom-Derived bioactive compounds as potential anticancer agents: A review. Int. J. Pept. Res. Ther. 27, 129–147. https://doi.org/10.1007/s10989-020-10073-z (2021).

    Google Scholar 

  49. Capone, P., Chiarella, P. & Sisto, R. Advanced technologies in genomic toxicology: current trend and future directions. Curr. Opin. Toxicol. 37 https://doi.org/10.1016/j.cotox.2023.100444 (2024).

  50. Zhao, H. Y. et al. Venom-gland transcriptomic, venomic, and antivenomic profiles of the spine-bellied sea snake (Hydrophis curtus) from the South China sea. BMC Genom. 22, 520. https://doi.org/10.1186/s12864-021-07824-7 (2021).

    Google Scholar 

  51. Laustsen, A. H. Guiding Recombinant antivenom development by omics technologies. N Biotechnol. 45, 19–27. https://doi.org/10.1016/j.nbt.2017.05.005 (2018).

    Google Scholar 

  52. Suryamohan, K. et al. The Indian Cobra reference genome and transcriptome enables comprehensive identification of venom toxins. Nat. Genet. 52, 106. https://doi.org/10.1038/s41588-019-0559-8 (2020).

    Google Scholar 

  53. Offor, B. C. & Piater, L. A. Snake venom toxins: potential anticancer therapeutics. J. Appl. Toxicol. 44, 666–685. https://doi.org/10.1002/jat.4544 (2024).

    Google Scholar 

  54. Li, L., Huang, J. & Lin, Y. Snake venoms in cancer therapy: Past, present and future. Toxins (Basel). 10. https://doi.org/10.3390/toxins10090346 (2018).

  55. Rubio, D. C. Z., Aragón, D. M. & Alves, I. A. Innovations in snake Venom-Derived therapeutics: A systematic review of global patents and their Pharmacological applications. Toxins 17 https://doi.org/10.3390/toxins17030136 (2025).

  56. Choi, B. K., Cho, Y. M., Bae, S. H., Zoubaulis, C. C. & Paik, Y. K. Single-step perfusion chromatography with a throughput potential for enhanced peptide detection by matrix-assisted laser desorption/ ionization-mass spectrometry. Proteomics 3, 1955–1961. https://doi.org/10.1002/pmic.200300558 (2003).

    Google Scholar 

  57. Rokyta, D. R., Margres, M. J., Ward, M. J. & Sanchez, E. E. The genetics of venom ontogeny in the eastern diamondback rattlesnake (Crotalus adamanteus). PeerJ 5, e3249 (2017). https://doi.org/10.7717/peerj.3249

  58. Andrews, S. FastQC: A Quality Control tool for High Throughput Sequence Data https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (.

  59. Grabherr, M. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652. https://doi.org/10.1038/nbt.1883 (2011). https://doi.org:

    Google Scholar 

  60. Simao, 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 31, 3210–3212. https://doi.org/10.1093/bioinformatics/btv351 (2015).

    Google Scholar 

  61. Barrell, D. et al. The GOA database in 2009–an integrated gene ontology annotation resource. Nucleic Acids Res. 37, D396–403. https://doi.org/10.1093/nar/gkn803 (2009).

    Google Scholar 

  62. Yang, S. H., Kim, S. W., Lee, S. J. & Koo, Y. Optimized protocols for protoplast isolation, transfection, and regeneration in the solanum genus for the CRISPR/Cas-mediated transgene-free genome editing. Appl. Biol. Chem. 67 https://doi.org/10.1186/s13765-024-00870-1 (2024).

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