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Pharmacological Characterization of Mouse Hind Paw Edema Induced by Parachartergus fraternus Venom

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Abstract

Stings from the wasp Parachartergus fraternus occur throughout Latin America, and edema followed by pain is the main symptom presented by victims. This often limited inflammatory event has not been characterized for this species. In this work, we identified the mechanisms and possible mediators involved in this response. P. fraternus venom (100, 200, and 400 μg/kg) was injected into the hind paws of mice, and edema was evaluated at intervals of 10 min for up to 60 min and at 120, 240, and 1440 min using a digital plethysmometer. The peak of edema was observed at 10 min with a dose of 200 μg/kg. A reduction in edema was observed with indomethacin (58.1%), celecoxib (44.5%), MK886 (30.8%), and dexamethasone (53.2%). Loratadine, cimetidine, and cyproheptadine treatment reduced the edema by 54.2%, 63.9%, and 84.4%, respectively, compared with the control. Captopril and l-NAME inhibited 42.5% and 69.8%, respectively, of the edema. These results showed that the edema induced in mice by P. fraternus venom occurs early and is mediated by arachidonic acid derivatives, vasoactive amines, and nitric oxide. Together, these mediators amplify the inflammatory process, with emphasis on histamine and serotonin in triggering the edematogenic response, being more effective the use of cyproheptadine in the therapeutic approach.

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References

  1. Carpenter, J.M., and O.M. Marques. 2001. Contribuição ao estudo dos vespídeos do Brasil. Bahia: UFB.

    Google Scholar 

  2. Somavilla, A., and M.L. Oliveira. 2017. Social wasps (Vespidae: Polistinae) from an Amazon rainforest fragment: Ducke Reserve. Sociobiology. 64: 125. https://doi.org/10.13102/sociobiology.v64i1.1215.

    Article  Google Scholar 

  3. Edery, H., J. Ishay, S. Gitter, and H. Joshua. 2013. Venoms of vespidae. In Arthropod venoms, ed. S. Bettini, 691–771. New York: Springer-Verlag Berlin Heidelberg.

    Google Scholar 

  4. Umakanth, M. 2017. Acute pancreatitis following multiple wasps stung. Saudi Journal of Medical and Pharmaceutical Sciences 3: 441–443.

    Google Scholar 

  5. Forrester, J.A., T.G. Weiser, and J.D. Forrester. 2018. An update on fatalities due to venomous and nonvenomous animals in the United States (2008–2015). Wilderness & Environmental Medicine 29: 36–44. https://doi.org/10.1016/j.wem.2017.10.004.

    Article  Google Scholar 

  6. Richards, O.W. 1978. Social wasps of America excluding the Vespinae. London: British Museum Press.

    Google Scholar 

  7. Olson, E.J. 2000. Parachartergus fraternus (Gribodo) (Hymenoptera: Vespidae: Polistinae) uses venom when taking caterpillar prey. Psyche. 103: 85–93. https://doi.org/10.1155/2000/62738.

    Article  Google Scholar 

  8. Mateus, S. 2011. Observations on forced colony emigration in Parachartergus fraternus (Hymenoptera: Vespidae: Epiponini): new nest site marked with sprayed venom. Psyche. 2011: 1–8. https://doi.org/10.1155/2011/157149.

    Article  Google Scholar 

  9. Nakajima, T. 1986. Pharmacological biochemistry of vespid venoms. In Venoms of the Hymenoptera: biochemical, pharmacological and behavioural aspects, ed. T. Piek, 309–327. London: Academic Press.

    Chapter  Google Scholar 

  10. Fitzgerald, K.T., and A.A. Flood. 2006. Hymenoptera stings. Clinical Techniques in Small Animal Practice 21: 194–204. https://doi.org/10.1053/j.ctsap.2006.10.002.

    Article  PubMed  Google Scholar 

  11. Mortari, M.R., L.L. Couto, L.A. Carneiro, C.B.F. Mourao, T.S. Camargo, J.A.G. Vargas, F.N. Oliveira, C.D.C. Gati, C.A. Schwartz, and E.F. Schwartz. 2012. Pharmacological characterization of Synoeca cyanea venom: an aggressive social wasp widely distributed in the Neotropical region. Toxicon. 59: 163–170. https://doi.org/10.1016/j.toxicon.2011.11.002.

    Article  CAS  PubMed  Google Scholar 

  12. Winter, C.A., E.A. Risley, and G.W. Nuss. 1962. Carrageenin-induced edema in hind paw of the rat as an assay for anti-inflammatory drugs. Proceedings of the Society for Experimental Biology and Medicine 111: 544–547.

    Article  CAS  Google Scholar 

  13. Albuquerque, T.M., N.M. Alencar, J.G. Figueiredo, I.S. Figueiredo, C.M. Teixeira, F.S. Bitencourt, D.D. Secco, E.F. Araújo, A.M. Leão, and M.V. Ramos. 2009. Vascular permeability, neutrophil migration and edematogenic effects induced by the latex of Cryptostegia grandiflora. Toxicon. 53: 15–23. https://doi.org/10.1016/j.toxicon.2008.10.009.

    Article  CAS  PubMed  Google Scholar 

  14. Barbosa, A.M., R.O. Amaral, C.F.P. Teixeira, S. Hyslop, and J.C. Cogo. 2003. Pharmacological characterization of mouse hind paw oedema induced by Bothrops insularis (jararaca ilhoa) snake venom. Toxicon. 42: 515–523. https://doi.org/10.1016/S0041-0101(03)00230-7.

    Article  CAS  PubMed  Google Scholar 

  15. Lopes, P.H., M.M.T. Rocha, A.K. Kuniyoshi, F.C.V. Portaro, and L.R.C. Gonçalves. 2017. Edema and nociception induced by Philodryas patagoniensis venom in mice: a pharmacological evaluation with implications for the accident treatment. The Journal of Pharmacology and Experimental Therapeutics. 361: 349–354. https://doi.org/10.1124/jpet.116.239640.

    Article  CAS  PubMed  Google Scholar 

  16. Paula, L., W.G. Santos, A. Malheiro, D. Carlos, and L.H. Faccioli. 2006. Differential modulation of cell recruitment and acute edema in a model of Polybia paulista venom-induced inflammation. International Immunopharmacology 6: 182–189. https://doi.org/10.1016/j.intimp.2005.08.002.

    Article  CAS  PubMed  Google Scholar 

  17. Sharma, J.N., A.M. Samud, and M.Z. Asmawi. 2004. Comparison between plethysmometer and micrometer methods to measure acute paw oedema for screening anti-inflammatory activity in mice. Inflammopharmacology. 12: 89–94. https://doi.org/10.1163/156856004773121400.

    Article  CAS  PubMed  Google Scholar 

  18. Shivkar, Y.M., and V.L. Kumar. 2003. Histamine mediates the proinflammatory effect of latex of Calotropis procera in rats. Mediators of Inflammation 12: 299–302. https://doi.org/10.1080/096293503310001619708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Toni, L.G.B., D.L. Menaldo, A.C.O. Cintra, M.J. Figueiredo, A.R. Souza, W.M.A. Maximiano, M.C. Jamur, G.E.P. Souza, and S.V. Sampaio. 2015. Inflammatory mediators involved in the paw edema and hyperalgesia induced by Batroxase, a metalloproteinase isolated from Bothrops atrox snake venom. International Immunopharmacology 28: 199–207. https://doi.org/10.1016/j.intimp.2015.06.001.

    Article  CAS  PubMed  Google Scholar 

  20. Wanderley, C.W.S., C.M.S. Silva, D.V.T. Wong, R.M. Ximenes, D.F.C. Morelo, F. Cosker, K.S. Aragão, C. Fernandes, R.C. Palheta-Júnior, A. Havt, G.A.C. Brito, F.Q. Cunha, R.A. Ribeiro, and R.C.P. Lima-Júnior. 2014. Bothrops jararacussu snake venom-induces a local inflammatory response in a prostanoid- and neutrophil-dependent manner. Toxicon. 90: 134–147. https://doi.org/10.1016/j.toxicon.2014.08.001.

    Article  CAS  PubMed  Google Scholar 

  21. Witharana, E.W.R.A., S.K.J. Wijesinghe, K.S.M. Pradeepa, W.A.I.P. Karunaratne, and S. 2015. Bee and wasp stings in Deniyaya; a series of 322 cases. The Ceylon Medical Journal 60: 5–9. https://doi.org/10.4038/cmj.v60i1.7406.

    Article  CAS  PubMed  Google Scholar 

  22. Mortari, M.R., A.O.S. Cunha, O. Oliveira, E.A. Gelfuso, E.B. Vieira, and W.F. Santos. 2005. Comparative toxic effects of the venoms from three wasp species of the genus Polybia (Hymenoptera, Vespidae). Journal of Biological Sciences 5: 449–454.

    Article  Google Scholar 

  23. Yshii, L.M., G.H.M.F. Souza, E.A. Camargo, M.N. Eberlin, M.T.C.P. Ribela, M.N. Muscara, S. Hyslop, and S.K.P. Costa. 2009. Characterization of the mechanisms underlying the inflammatory response to Polistes lanio lanio (paper wasp) venom in mouse dorsal skin. Toxicon. 53: 42–52. https://doi.org/10.1016/j.toxicon.2008.10.006.

    Article  CAS  PubMed  Google Scholar 

  24. Eno, A.E. 1997. Pharmacological investigation of oedema induced by venom from the wasp Polistes fuscatus. Toxicon 35: 1691–1698.

    Article  CAS  Google Scholar 

  25. Dias, N.B., B.M. Souza, P.C. Gomes, P. Brigatte, and M.S. Palma. 2015. Peptidome profiling of venom from the social wasp Polybia paulista. Toxicon. 107: 290–303. https://doi.org/10.1016/j.toxicon.2015.08.013.

    Article  CAS  PubMed  Google Scholar 

  26. Gonçalves, J., M. Rangel, A. Biolchi, E. Alves, K. Moreira, L. Silva, and M. Mortari. 2016. Antinociceptive properties of the mastoparan peptide Agelaia-MPI isolated from social wasps. Toxicon. 120: 15–21. https://doi.org/10.1016/j.toxicon.2016.07.009.

    Article  CAS  PubMed  Google Scholar 

  27. Mendes, M.A., B.M. Souza, and M.S. Palma. 2005. Structural and biological characterization of three novel mastoparan peptides from the venom of the neotropical social wasp Protopolybia exigua (Saussure). Toxicon. 45: 101–106. https://doi.org/10.1016/j.toxicon.2004.09.015.

    Article  CAS  PubMed  Google Scholar 

  28. Griesbacher, T., P. Althuber, M. Zenz, I. Rainer, S. Griengl, and F. Lembeck. 1998. Vespula vulgaris venom: role of kinins and release of 5-hydroxytryptamine from skin mast cells. European Journal of Pharmacology 351: 95–104. https://doi.org/10.1016/S0014-2999(98)00276-3.

    Article  CAS  PubMed  Google Scholar 

  29. Khanapure, S.P., D.S. Garvey, D.R. Janero, and L.G. Letts. 2007. Eicosanoids in inflammation: biosynthesis, pharmacology, and therapeutic frontiers. Current Topics in Medicinal Chemistry 7: 311–340.

    Article  CAS  Google Scholar 

  30. Morimoto, K., N. Shirata, Y. Taketomi, S. Tsuchiya, E. Segi-Nishida, T. Inazumi, K. Kabashima, S. Tanaka, M. Murakami, X.S. Narumiya, and Y. Sugimoto. 2014. Prostaglandin E2–EP3 signaling induces inflammatory swelling by mast cell activation. Journal of Immunology 192: 1130–1137. https://doi.org/10.4049/jimmunol.1300290.

    Article  CAS  Google Scholar 

  31. Olivo, R.A., C.F.P. Teixeira, J.L. Wallace, J.M. Gutierrez, and S.R. Zamuner. 2007. Role of cyclooxygenases in oedema-forming activity of bothropic venoms. Toxicon. 49: 670–677. https://doi.org/10.1016/j.toxicon.2006.11.006.

    Article  CAS  Google Scholar 

  32. Toriyabe, M., K. Omote, T. Kawamata, and A. Namiki. 2004. Contribution of interaction between nitric oxide and cyclooxygenases to the production of prostaglandins in carrageenan-induced inflammation. Anesthesiology 101: 983–990.

    Article  CAS  Google Scholar 

  33. King, T.P., S.Y. Jim, and K.M. Wittkowski. 2003. Inflammatory role of two venom components of yellow jackets (Vespula vulgaris): a mast cell degranulating peptide mastoparan and phospholipase A1. International Archives of Allergy and Immunology 131: 25–32. https://doi.org/10.1159/000070431.

    Article  CAS  PubMed  Google Scholar 

  34. Rao, N.L., P.J. Dunford, X. Xue, X. Jiang, K.A. Lundeen, F. Coles, J.P. Riley, K.N. Williams, C.A. Grice, J.P. Edwards, L. Karlsson, and A.M. Fourie. 2007. Anti-inflammatory activity of a potent, selective leukotriene A4 hydrolase inhibitor in comparison with the 5-lipoxygenase inhibitor zileuton. The Journal of Pharmacology and Experimental Therapeutics 321: 1154–1160. https://doi.org/10.1124/jpet.106.115436.

    Article  CAS  PubMed  Google Scholar 

  35. Sousa, P.L., Y.P. Quinet, L.A.C. Brizeno, T.L. Sampaio, A.F.C. Torres, A.M.C. Martins, and A.M.S. Assreuy. 2016. The acute inflammatory response induced in mice by the venom of the giant ant Dinoponera quadriceps involves macrophage and interleukin-1 β. Toxicon. 117: 22–29. https://doi.org/10.1016/j.toxicon.2016.03.009.

    Article  CAS  PubMed  Google Scholar 

  36. Tommasini, I., and O. Cantoni. 2004. Dexamethasone promotes toxicity in U937 cells exposed to otherwise nontoxic concentrations of peroxynitrite: pivotal role for lipocortin 1-mediated inhibition of cytosolic phospholipase A2. Molecular Pharmacology 65: 964–972. https://doi.org/10.1124/mol.65.4.964.

    Article  CAS  PubMed  Google Scholar 

  37. Hall, S.E., S. Lim, I.R. Witherden, T.D. Tetley, P.J. Barnes, A.M. Kamal, and S.F. Smith. 1999. Lung type II cell and macrophage annexin I release: differential effects of two glucocorticoids. The American Journal of Physiology 276: L114–L121. https://doi.org/10.1152/ajplung.1999.276.1.L114.

    Article  CAS  PubMed  Google Scholar 

  38. Bartko, J., L. Stiebellehner, U. Derhaschnig, C. Schoergenhofer, M. Schwameis, H. Prosch, and B. Jilma. 2016. Dissociation between systemic and pulmonary anti-inflammatory effects of dexamethasone in humans. British Journal of Clinical Pharmacology 81: 865–877. https://doi.org/10.1111/bcp.12857.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Al-Harbi, N.O., F. Imam, M.M. Al-Harbi, M.A. Ansari, K.M. Zoheir, H.M. Korashy, M.M. Sayed-Ahmed, S.M. Attia, O.A. Shabanah, and S.F. Ahamad. 2016. Dexamethasone attenuates LPS-induced acute lung injury through inhibition of NF-κB, COX-2, and pro-inflammatory mediators. Immunological Investigations 45: 349–369. https://doi.org/10.3109/08820139.2016.1157814.

    Article  CAS  PubMed  Google Scholar 

  40. Oropeza, A.R., S. Mikkelsen, C. Bindslev-Jensen, and C.G. Mortz. 2017. Pre-hospital treatment of bee and wasp induced anaphylactic reactions: a retrospective study. Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine 25: 4. https://doi.org/10.1186/s13049-016-0344-y.

    Article  Google Scholar 

  41. Calixto, M.C., K.M. Trichês, and J.B. Calixto. 2003. Analysis of the inflammatory response in the rat paw caused by the venom of Apis melifera bee. Inflammation Research 52: 132–139.

    Article  CAS  Google Scholar 

  42. Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature. 454: 428–435. https://doi.org/10.1038/nature07201.

    Article  CAS  PubMed  Google Scholar 

  43. Tiligada, E., and M. Ennis. 2018. Histamine pharmacology: from Sir Henry Dale to the 21st century. British Journal of Pharmacology. https://doi.org/10.1111/bph.14524.

  44. Lamraoui, A., S. Adi-Bessalem, and F. Laraba-Djebari. 2014. Modulation of tissue inflammatory response by histamine receptors in scorpion envenomation pathogenesis: involvement of H4 receptor. Inflammation. 37: 1689–1704. https://doi.org/10.1007/s10753-014-9898-x.

    Article  CAS  PubMed  Google Scholar 

  45. Welsh, A.L., and M. Ede. 1962. Further studies of cyproheptadine as an antiallergic, antipruritic agent. The Journal of New Drugs 2: 88–93.

    Article  CAS  Google Scholar 

  46. Wernersson, S., and G. Pejler. 2014. Mast cell secretory granules: armed for battle. Nature Reviews. Immunology 14: 478–494. https://doi.org/10.1038/nri3690.

    Article  CAS  PubMed  Google Scholar 

  47. Decarie, A., A. Adam, and J. Couture. 1996. Effects of captopril and icatibant on bradykinin (BK) and des[Arg9]BK in carrageenan-induced edema. Peptides 17: 1009–1015.

    CAS  PubMed  Google Scholar 

  48. Lim, H.W., R. Kamide, and I. Gigli. 1984. Effect of captopril on the vascular permeability changes induced by C5a, histamine and compound 48/80. British Journal of Dermatology 112: 43–45.

    Article  Google Scholar 

  49. Sun, N., L. Zhai, H. Li, L. Shia, Z. Yao, and B. Zhang. 2016. Angiotensin-converting enzyme inhibitor (ACEI)-mediated amelioration in renal fibrosis involves suppression of mast cell degranulation. Kidney & Blood Pressure Research 41: 108–118. https://doi.org/10.1159/000368549.

    Article  CAS  Google Scholar 

  50. Sebia-Amrane, F., and F. Laraba-Djebari. 2013. Pharmaco-modulations of induced edema and vascular permeability changes by Vipera lebetina venom: inflammatory mechanisms. Inflammation. 36: 434–443. https://doi.org/10.1007/s10753-012-9563-1.

    Article  CAS  PubMed  Google Scholar 

  51. Laurindo, F.R.M., M. Liberman, D.C. Fernandes, and P.F. Leite. 2018. Endothelium-dependent vasodilation: nitric oxide and other mediators. In Endothelium and cardiovascular diseases: vascular biology and clinical syndromes, ed. P.L. Luz, P. Libby, F.R.M. Laurindo, and A.C.P. Chagas, 97–113. London: Academic Press.

    Chapter  Google Scholar 

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Acknowledgments

Acknowledgment is given to Andreia Biolchi Mayer for the assistance in the collection of the P. fraternus specimens.

Funding

This study was funded by the Federal University of Mato Grosso do Sul and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance Code 001 and scholarship 1655328.

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Authors and Affiliations

  1. Laboratory of Pharmacology and Inflammation, FACFAN/Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil

    Jéssica de Araujo Isaias Muller, Iluska Senna Bonfá Moslaves & Mônica Cristina Toffoli-Kadri

  2. Multicenter Program of Post-Graduation in Biochemistry and Molecular Biology, INBIO/Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil

    Jéssica de Araujo Isaias Muller

  3. Laboratory of Neuropharmacology, ICB/University of Brasilia, Brasilia, Brazil

    Márcia Renata Mortari

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  1. Jéssica de Araujo Isaias Muller
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Correspondence to Jéssica de Araujo Isaias Muller.

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All experiments were approved by the Ethics Committee on Animal Experimentation of the UFMS (protocol 764/2016) and were conducted in accordance with the National Institutes of Health Regulations on the Use and Care of Animals for Scientific Purposes.

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de Araujo Isaias Muller, J., Mortari, M.R., Moslaves, I.S.B. et al. Pharmacological Characterization of Mouse Hind Paw Edema Induced by Parachartergus fraternus Venom. Inflammation 42, 2011–2019 (2019). https://doi.org/10.1007/s10753-019-01062-6

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