267
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Lipidomic profiling of the Brazilian yellow scorpion venom: new insights into inflammatory responses following Tityus serrulatus envenomation

, ORCID Icon, , &

References

  • Acunha, T., V. Nardini, and L. H. Faccioli. 2021. A lipidomics approach reveals new insights into Crotalus Durissus Terrificus and Bothrops Moojeni snake venoms. Arch. Toxicol. 95 (1):345–53. doi:10.1007/s00204-020-02896-y.
  • Ahmadi, S., J. M. Knerr, L. Argemi, K. C. F. Bordon, M. B. Pucca, F. A. Cerni, E. C. Arantes, F. Çalışkan, and A. H. Laustsen. 2020. Scorpion venom: Detriments and benefits. Biomedicines 8 (5):118. doi:10.3390/biomedicines8050118.
  • Almaaytah, A., and Q. Albalas. 2014. Scorpion venom peptides with no disulfide bridges: A review. Peptides 51:35–45. doi:10.1016/j.peptides.2013.10.021.
  • Almeida, A. C. C., Y. F. Mise, F. M. Carvalho, and R. M. L. Silva. 2021. Associação ecológica entre fatores socioeconômicos, ocupacionais e de saneamento e a ocorrência de escorpionismo no Brasil, 2007-2019. Epidemiologia e Serviços de Saúde 30 (4):e2021009. doi:10.1590/S1679-49742021000400021.
  • Andrieu-Abadie, N., and T. Levade. 2002. Sphingomyelin hydrolysis during apoptosis. Biochim. Biophys. Acta 1585 (2–3):126–34. doi:10.1016/S1388-1981(02)00332-3.
  • Bolt, H. M. 2021. New aspects in snake venom toxicology. Arch. Toxicol. 95 (6):1865–66. doi:10.1007/s00204-021-03066-4.
  • Borges, A., M. R. Graham, D. M. Cândido, and P. P. O. Pardal. 2021. Amazonian scorpions and scorpionism: Integrating toxinological, clinical, and phylogenetic data to combat a human health crisis in the world’s most diverse rainforest. J. Venom. Anim. Toxins Incl. Trop. Dis 27:e20210028. doi:10.1590/1678-9199-jvatitd-2021-0028.
  • BRASIL ACIDENTE POR ANIMAIS PEÇONHENTOS - Notificações Registradas No Sistema de Informação de Agravos de Notificação. Datasus; Tabnet; Sinan. 2019.
  • Braverman, N. E., and A. B. Moser. 2012. Functions of plasmalogen lipids in health and disease. Biochim. Biophys. Acta 1822 (9):1442–52. doi:10.1016/j.bbadis.2012.05.008.
  • Byeon, S. K., J. Y. Lee, and M. H. Moon. 2012. Optimized extraction of phospholipids and lysophospholipids for nanoflow liquid chromatography-electrospray ionization-tandem mass spectrometry. Analyst. (Lond) 137 (2):451–58. doi:10.1039/c1an15920h.
  • Carmo, A. A. F., B. R. C. Costa, J. P. Vago, L. C. de Oliveira, L. P. Tavares, C. R. C. Nogueira, A. L. C. Ribeiro, C. C. Garcia, A. S. Barbosa, B. S. A. F. Brasil, et al. 2014. Plasmin induces in vivo monocyte recruitment through protease-activated receptor-1–, MEK/ERK-, and CCR2-mediated signaling. J. Immunol. 193(7):3654–63. doi:10.4049/jimmunol.1400334.
  • Carmo, É. A., A. A. Nery, C. L. Nascimento Sobrinho, and C. A. Casotti. 2019. Clinical and epidemiological aspects of scorpionism in the interior of the state of Bahia, Brazil: Retrospective epidemiological study. Sao Paulo Med. J. 137 (2):162–68. Published 2019 Jul 15. doi:10.1590/1516-3180.2018.0388070219.
  • Castoldi, A., L. B. Monteiro, N. van Teijlingen Bakker, D. E. Sanin, N. Rana, M. Corrado, A. M. Cameron, F. Hässler, M. Matsushita, G. Caputa, et al. 2020. Triacylglycerol synthesis enhances macrophage inflammatory function. Nat. Commun. 11(1):4107. doi:10.1038/s41467-020-17881-3.
  • Checa, A., C. Bedia, and J. Jaumot. 2015. Lipidomic data analysis: Tutorial, practical guidelines and applications. Anal. Chim. Acta 885:1–16. doi:10.1016/j.aca.2015.02.068.
  • Cid-Uribe, J. I., J. I. Veytia-Bucheli, T. Romero-Gutierrez, E. Ortiz, and L. D. Possani. 2019. Scorpion venomics: An overview. Expert Rev. Proteomics 17 (1):67–83. doi:10.1080/14789450.2020.1705158.
  • Freire-Maia, L., and I. M. de Matos. 1993. Heparin or a PAF antagonist (BN-52021) prevents the acute pulmonary edema induced by Tityus serrulatus scorpion venom in the rat. Toxicon 31:1207–10. doi:10.1016/0041-0101(93)90137-8.
  • Furtado, A. A., A. Daniele-Silva, A. A. Silva-Júnior, and M. F. Fernandes-Pedrosa. 2020. Biology, venom composition, and scorpionism induced by Brazilian scorpion Tityus stigmurus (Thorell, 1876) (Scorpiones: Buthidae): A mini-review. Toxicon 185:36–45. doi:10.1016/j.toxicon.2020.06.015.
  • Ghezellou, P., K. Jakob, J. Atashi, A. Ghassempour, and B. Spengler. 2022. Mass-spectrometry-based lipidome and proteome profiling of Hottentotta saulcyi (Scorpiones: Buthidae) venom. Toxins 14:370. doi:10.3390/toxins14060370.
  • Hannun, Y. A., and L. M. Obeid. 2002. The ceramide-centric universe of lipid-mediated cell regulation: Stress encounters of the lipid kind. J. Biol. Chem. 277 (29):25847–50. doi:10.1074/jbc.R200008200.
  • Hetz, C. A., M. Hunn, P. Rojas, V. Torres, L. Leyton, and A. F. G. Quest. 2002. Caspase-dependent initiation of apoptosis and necrosis by the Fas receptor in lymphoid cells: Onset of necrosis is associated with delayed ceramide increase. J. Cell. Sci. 115 (23):4671–863. doi:10.1242/jcs.00153.
  • Holčapek, M., G. Liebisch, and K. Ekroos. 2018. Lipidomic analysis. Anal. Chem. 90 (7):4249–57. doi:10.1021/acs.analchem.7b05395.
  • Ikram, S., J. Ahmad, I. U. Rehman, and S. Durdagi. 2020. Potent novel inhibitors against hepatitis C virus NS3 (HCV NS3 GT-3a) protease domain. J. Mol. Graph. Model. 101:107727. doi:10.1016/j.jmgm.2020.107727.
  • Iverson, S. J., S. L. Lang, and M. H. Cooper. 2001. Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids. 36 (11):1283–87. doi:10.1007/s11745-001-0843-0.
  • Iwasaki, Y., Y. Sakurai, and J. Damnjanović. 2020. A simple chemo-enzymatic synthesis of alkyl-acyl (plasmanyl) phospholipids. Biocatal. Agric. Biotechnol. 26:101625. doi:10.1016/j.bcab.2020.101625.
  • Jamaluddin, M., S. Wang, I. Boldogh, B. Tian, and A. R. Brasier. 2007. TNF-α-induced NF-κB/RelA Ser276 phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway. Cell. Signal. 19 (7):1419–33. doi:10.1016/j.cellsig.2007.01.020.
  • Khalil, M. B., W. Hou, L. A. Elisma, F. Swayne, A. P. Blanchard, S. A. L. Yao, Z. Bennett, and D. Figeys. 2010. Lipidomics era: Accomplishments and challenges. Mass Spectrom. Rev. 29 (6):877–929. doi:10.1002/mas.20294.
  • Kim, S., J. Chen, T. Cheng, A. Gindulyte, J. He, S. He, Q. Li, B. A. Shoemaker, P. A. Thiessen, B. Yu, et al. 2019. PubChem 2019 update: Improved access to chemical data. Nucl. Acids Res. 47(D1):D1102–29. doi:10.1093/nar/gky1033.
  • Kim, J. H., H. J. Na, C. K. Kim, J. Y. Kim, K. S. Ha, H. Lee, H. T. Chung, H. J. Kwon, Y. G. Kwon, and Y. M. Kim. 2008. The non-provitamin a carotenoid, lutein, inhibits NF-ΚB-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/pten/akt and NF-ΚB-inducing kinase pathways: Role of H2O2 in NF-ΚB activation. Free Radic. Biol. Med. 45 (6):885–96. doi:10.1016/j.freeradbiomed.2008.06.019.
  • Kimura, T., W. Jennings, and R. M. Epand. 2016. Roles of specific lipid species in the cell and their molecular mechanism. Prog. Lipid Res. 62:75–92. doi:10.1016/j.plipres.2016.02.001.
  • Kim, S. C., and X. Wang. 2020. Phosphatidic acid: An emerging versatile class of cellular mediators. Essays Biochem. 64 (3):533–46. doi:10.1042/EBC20190089.
  • Kind, T., K. H. Liu, D. Y. Lee, B. DeFelice, J. K. Meissen, and O. Fiehn. 2013. LipidBlast in silico tandem mass spectrometry database for lipid identification. Nat. Meth 10 (8):755–58. doi:10.1038/nmeth.2551.
  • Kinoshita, M., K. G. N. Suzuki, M. Murata, and N. Matsumori. 2018. Evidence of lipid rafts based on the partition and dynamic behavior of sphingomyelins. Chem. Phys. Lipids 215:84–95. doi:10.1016/j.chemphyslip.2018.07.002.
  • Lacerda, A. B., C. Lorenz, T. S. Azevedo, D. M. Cândido, F. H. Wen, L. J. Eloy, and F. Chiaravalloti-Neto. 2022. Detection of areas vulnerable to scorpionism and its association with environmental factors in São Paulo, Brazil. Acta Trop. 230:106390. doi:10.1016/j.actatropica.2022.106390.
  • Lavieu, G., F. Scarlatti, G. Sala, S. Carpentier, T. Levade, R. Ghidoni, J. Botti, and P. Codogno. 2006. Regulation of autophagy by sphingosine kinase 1 and its role in cell survival during nutrient starvation. J. Biol. Chem. 281 (13):8518–27. doi:10.1074/jbc.M506182200.
  • Löfgren, L., M. Ståhlman, M. B. Forsberg, S. Saarinen, R. Nilsson, and G. I. Hansson. 2012. The BUME method: A novel automated chloroform-free 96-well total lipid extraction method for blood plasma. J. Lipid Res. 53 (8):1690–700. doi:10.1194/jlr.D023036.
  • Lu, J., Y. Xu, J. Wang, S. D. Singer, and G. Chen. 2020. The role of triacylglycerol in plant stress response. Plants 9:472. doi:10.3390/plants9040472.
  • Lv, W., X. Shi, S. Wang, and G. Xu. 2019. Multidimensional liquid chromatography-mass spectrometry for metabolomic and lipidomic analyses. Trends Anal. Chem 120:115302. doi:10.1016/j.trac.2018.11.001.
  • Marchi, F. C., E. Mendes-Silva, L. Rodrigues-Ribeiro, L. G. Bolais-Ramos, and T. Verano-Braga. 2022. Toxinology in the proteomics era: A review on arachnid venom proteomics. J. Venom. Anim. Toxins Incl. Trop. Dis 28:20210034. doi:10.1590/1678-9199-jvatitd-2021-0034.
  • Matyash, V., G. Liebisch, T. V. Kurzchalia, A. Shevchenko, and D. Schwudke. 2008. Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. J. Lipid Res. 49 (5):1137–46. doi:10.1194/jlr.D700041-JLR200.
  • Milhas, D., C. J. Clarke, and Y. A. Hannun. 2010. Sphingomyelin metabolism at the plasma membrane: Implications for bioactive sphingolipids. FEBS Lett. 584 (9):1887–94. doi:10.1016/j.febslet.2009.10.058.
  • Monteiro, W. M., J. Gomes, N. Fé, I. M. da Silva, M. Lacerda, A. Alencar, A. S. de Farias, F. Val, V. de Souza Sampaio, G. C. de Melo, et al. 2019. Perspectives and recommendations towards evidence-based health care for scorpion sting envenoming in the Brazilian Amazon: A comprehensive review. Toxicon 169:68–80. doi:10.1016/j.toxicon.2019.09.003.
  • Mouchbahani-Constance, S., and R. Sharif-Naeini. 2021. Proteomic and transcriptomic techniques to decipher the molecular evolution of venoms. Toxins 13:154. doi:10.3390/toxins13020154.
  • Nencioni, A. L. A., E. B. Neto, L. A. de Freitas, and V. A. C. Dorce. 2018. Effects of Brazilian scorpion venoms on the central nervous system. J. Venom. Anim. Toxins Incl. Trop. Dis 24 (1):3. doi:10.1186/s40409-018-0139-x.
  • Nixon, G. F. 2009. Sphingolipids in inflammation: Pathological implications and potential therapeutic targets. Br. J. Pharmacol. 158 (4):982–93. doi:10.1111/j.1476-5381.2009.00281.x.
  • Ortiz, E., G. B. Gurrola, E. F. Schwartz, and L. D. Possani. 2015. Scorpion venom components as potential candidates for drug development. Toxicon 93:125–35. doi:10.1016/j.toxicon.2014.11.233.
  • Paul, S., G. I. Lancaster, and P. J. Meikle. 2019. Plasmalogens: A potential therapeutic target for neurodegenerative and cardiometabolic disease. Prog. Lipid Res. 74:186–95. doi:10.1016/j.plipres.2019.04.003.
  • Pucca, M. B., F. A. Cerni, E. L. Pinheiro Junior, K. C. F. Bordon, F. G. Amorim, F. A. Cordeiro, H. T. Longhim, C. M. Cremonez, G. H. Oliveira, and E. C. Arantes. 2015. Tityus serrulatus venom – a lethal cocktail. Toxicon 108:272–84. doi:10.1016/j.toxicon.2015.10.015.
  • Quintero-Hernández, V., E. Ortiz, M. Rendón-Anaya, E. F. Schwartz, B. Becerril, G. Corzo, and L. D. Possani. 2011. Scorpion and spider venom peptides: Gene cloning and peptide expression. Toxicon 58:644–63. doi:10.1016/j.toxicon.2011.09.015.
  • Reckziegel, G. C., and V. L. Pinto Jr. 2014. Scorpionism in Brazil in the years 2000 to 2012. J. Venom Anim. Toxins Incl. Trop. Dis 20 (1):46. doi:10.1186/1678-9199-20-46.
  • Reis, M. B., F. L. Rodrigues, N. Lautherbach, A. Kanashiro, C. A. Sorgi, A. Meirelles, C. Silva, K. F. Zoccal, C. Souza, S. G. Ramos, et al. 2020. Interleukin-1 receptor-induced PGE2 production controls acetylcholine-mediated cardiac dysfunction and mortality during scorpion envenomation. Nat. Commun. 11(1):5433. doi:10.1038/s41467-020-19232-8.
  • Reis, A., A. Rudnitskaya, G. J. Blackburn, N. Mohd Fauzi, A. R. Pitt, and C. M. Spickett. 2013. A comparison of five lipid extraction solvent systems for lipidomic studies of human LDL. J. Lipid Res. 54 (7):1812–24. doi:10.1194/jlr.M034330.
  • Reis, M. B., K. F. Zoccal, L. G. Gardinassi, and L. H. Faccioli. 2019. Scorpion envenomation and inflammation: Beyond neurotoxic effects. Toxicon 167:174–79. doi:10.1016/j.toxicon.2019.06.219.
  • Rodríguez de la Vega, R. C., E. F. Schwartz, and L. D. Possani. 2010. Mining on scorpion venom biodiversity. Toxicon 56:1155–61. doi:10.1016/j.toxicon.2009.11.010.
  • Saidoune-Malek, I., A. Ait-Lounis, and F. Laraba-Djebari. 2018. TNF-α antagonist improves oxidative stress and lipid disorders induced by scorpion venom in the intestinal tissue. Acta Trop. 185:307–13. doi:10.1016/j.actatropica.2018.06.013.
  • Santos, L., C. Oliveira, B. M. Vasconcelos, D. Vilela, L. Melo, L. Ambrósio, A. da Silva, L. Murback, J. Kurissio, J. Cavalcante, et al. 2021. Good management practices of venomous snakes in captivity to produce biological venom-based medicines: Achieving replicability and contributing to pharmaceutical industry. J. Toxicol. Environ. Health B 24 (1):30–50. doi:10.1080/10937404.2020.1855279.
  • Santos, M. S. V., C. G. L. Silva, B. S. Neto, C. R. P. Grangeiro Júnior, V. H. G. Lopes, A. G. Teixeira Júnior, D. A. Bezerra, J. V. C. P. Luna, J. B. Cordeiro, J. G. Júnior, et al. 2016. Clinical and epidemiological aspects of scorpionism in the world: A systematic review. Wilderness Environ. Med. 27(4):504–18. doi:10.1016/j.wem.2016.08.003.
  • Slotte, J. P. 2013. Biological functions of sphingomyelins. Prog. Lipid Res. 52 (4):424–37. doi:10.1016/j.plipres.2013.05.001.
  • Snider, A. J., K. Alexa Orr Gandy, and L. M. Obeid. 2010. Sphingosine kinase: Role in regulation of bioactive sphingolipid mediators in inflammation. Biochimie. 92:707–15. doi:10.1016/j.biochi.2010.02.008.
  • Spiegel, S., and S. Milstien. 2002. Sphingosine 1-phosphate, a key cell signaling molecule. J. Biol. Chem. 277 (29):25851–54. doi:10.1074/jbc.R200007200.
  • Suasnábar, S., C. Godoy, A. Forchino, and G. Armando. 2022. Pediatric scorpionism: A descriptive, cross-sectional, and retrospective study of predictors of severity. Arch. Argent. Pediatr. 120:377–83. doi:10.5546/aap.2022.eng.377.
  • Tan, C. H. 2022. Snake venomics: Fundamentals, recent updates, and a look to the next decade. Toxins 14:247. doi:10.3390/toxins14040247.
  • Taniele-Silva, J., L. G. Martins, M. B. Sousa, L. M. Souza, R. M. B. Cardoso, S. R. U. Velasco, G. D. S. Ramos, C. T. Miranda, A. Á. Moura, L. Anderson, et al. 2020. Retrospective clinical and epidemiological analysis of scorpionism at a referral hospital for the treatment of accidents by venomous animals in Alagoas State, Northeast Brazil, 2007-2017. Rev. Inst. Med. Trop. Sao Paulo 62:e26. doi:10.1590/s1678-9946202062026.
  • Tobassum, S., H. M. Tahir, M. Arshad, M. T. Zahid, S. Ali, and M. M. Ahsan. 2020. Nature and applications of scorpion venom: An overview. Toxin Rev. 39 (3):214–25. doi:10.1080/15569543.2018.1530681.
  • Torrez, P. P. Q., F. S. Dourado, R. Bertani, P. Cupo, and F. O. S. França. 2019. Scorpionism in Brazil: Exponential growth of accidents and deaths from scorpion stings. Rev. Soc. Bras. Med. Trop. 52:e20180350. doi:10.1590/0037-8682-0350-2018.
  • Tumanov, S., and J. J. Kamphorst. 2017. Recent advances in expanding the coverage of the lipidome. Curr. Opin. Biotechnol. 43:127–33. doi:10.1016/j.copbio.2016.11.008.
  • Wang, R., B. Li, S. M. Lam, and G. Shui. 2020. Integration of lipidomics and metabolomics for in-depth understanding of cellular mechanism and disease progression. J. Genet. Genom. 47 (2):69–83. doi:10.1016/j.jgg.2019.11.009.
  • Yoon, H., J. L. Shaw, M. C. Haigis, and A. Greka. 2021. Lipid metabolism in sickness and in health: Emerging regulators of lipotoxicity. Mol. Cell 81 (18):3708–30. doi:10.1016/j.molcel.2021.08.027.
  • Young, M. M., M. Kester, and H. G. Wang. 2013. Sphingolipids: Regulators of crosstalk between apoptosis and autophagy. J. Lipid Res. 54 (1):5–19. doi:10.1194/jlr.R031278.
  • Zhang, J., G. Johnston, B. Stebler, and E. T. Keller. 2001. Hydrogen peroxide activates NF κ B and the interleukin-6 promoter through NF κ B-inducing kinase. Antioxid. Redox Signal. 3 (3):493–504. doi:10.1089/15230860152409121.
  • Zhao, Y. Y., S. P. Wu, S. Liu, Y. Zhang, and R. C. Lin. 2014. Ultra-performance liquid chromatography–mass spectrometry as a sensitive and powerful technology in lipidomic applications. Chem. Biol. Interact. 220:181–92. doi:10.1016/j.cbi.2014.06.029.
  • Zoccal, K. F., C. Bitencourt, F. W. Paula-Silva, C. A. Sorgi, K. de Castro Figueiredo Bordon, E. C. Arantes, L. H. Faccioli, and P. Talamas-Rohana. 2014. TLR2, TLR4 and CD14 recognize venom-associated molecular patterns from Tityus serrulatus to induce macrophage-derived inflammatory mediators. PloS One 9 (2):e88174. doi:10.1371/journal.pone.0088174.
  • Zoccal, K. F., L. G. Gardinassi, K. C. F. Bordon, E. C. Arantes, S. Marleau, H. Ong, and L. H. Faccioli. 2019. EP80317 restrains inflammation and mortality caused by scorpion envenomation in mice. Front Pharmacol. 10:171. doi:10.3389/fphar.2019.00171.
  • Zoccal, K. F., L. G. Gardinassi, C. A. Sorgi, A. Meirelles, K. Bordon, I. Glezer, P. Cupo, A. K. Matsuno, V. R. Bollela, E. C. Arantes, et al. 2018. CD36 shunts eicosanoid metabolism to repress CD14 licensed interleukin-1β release and inflammation. Front Immunol. 9:890. doi:10.3389/fimmu.2018.00890.
  • Zoccal, K. F., F. W. Paula-Silva, C. Bitencourt, C. A. Sorgi, K. Bordon, E. C. Arantes, and L. H. Faccioli. 2015. PPAR-γ activation by Tityus serrulatus venom regulates lipid body formation and lipid mediator production. Toxicon 93:90–97. doi:10.1016/j.toxicon.2014.11.226.
  • Zoccal, K. F., C. A. Sorgi, J. I. Hori, F. W. G. Paula-Silva, E. C. Arantes, C. H. Serezani, D. S. Zamboni, and L. H. Faccioli. 2016. Opposing roles of LTB4 and PGE2 in regulating the inflammasome-dependent scorpion venom-induced mortality. Nat. Commun. 7 (1):10760. doi:10.1038/ncomms10760.
  • Züllig, T., and H. C. Köfeler. 2021. High resolution mass spectrometry in lipidomics. Mass Spectrom. Rev 40:162–76. doi:10.1002/mas.21627.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.