Skip to main content
SpringerLink
Log in

Photobiostimulation reduces edema formation induced in mice by Lys-49 phospholipases A2 isolated from Bothrops moojeni venom

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The prominent local myotoxic effects induced by Bothrops snake venom are due, in part, to myotoxins This effect is not neutralized by antivenom, which is the main therapy for victims of snakebite. Two basic myotoxins named MjTX-I and MjTX-II were isolated from Bothrops moojeni venom. Both myotoxins have a Lys-49 phospholipase A2 structure devoid of enzymatic activity, but are highly myonecrotic and edema-inducing. In this study, we analyzed the effect of a low-level laser (LLL) at 685 nm, an energy density of 2.2 J cm−2, and the irradiation time of 15 s, and a light emitting diode (LED) at 635 or 945 nm at energy densities of 4 and 3.8 J cm−2, and irradiation times of 41 and 38 s, respectively, applied 30 min and 3 h after edema formation in mice caused by MjTX-I or MjTX-II. MjTX-I or MjTX-II caused a significant edema formation in envenomed paws. LLL and LED irradiation significantly reduced the edema formation by both myotoxins from 1 up to 6 hours after the injection. Both LLL and LEDs were similar in reducing the edema formation induced by myotoxins. The combined photobiostimulation with antivenom had the same effect in reducing edema as treatment with the LLL or LEDs alone. In conclusion, the results of this study indicate that photobiostimulation could be used in association with antivenom therapy for treatment of local effects of Bothrops species venom.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. H. W. Fan and J. L. C. Cardoso, Clinical toxicology of snakebite in South America, in Handbook of Clinical Toxicology of Animal, Venoms and Poisons, ed. J. Meier and J. White, CRC Press, Boca Raton, FL, USA, 1995, pp. 667–688.

    Google Scholar 

  2. J. M. Gutierrez, Clinical toxicology of snakebite in Central America, in Handbook of Clinical Toxicology of Animal, Venoms and Poisons, ed. J. Meier and J. White, CRC Press, Boca Raton, FL, USA, 1995, pp. 645–665.

    Google Scholar 

  3. J. M. Gutierrez, H. W. Fan, C. L. M. Silvera and Y. Angulo, Stability, distribution and use of antivenoms for snakebite envenomation in Latin America: report of a workshop, Toxicon, 2009, 53, 625–630.

    Article  CAS  Google Scholar 

  4. R. Mora, B. Lomonte and J. M. Gutierrez, Effects of Bothrops asper Snake Venom on Lymphatic Vessels: Insights into a Hidden Aspect of Envenomation, PLOs Neglected Diseases, 2008, 2, 318.

    Article  Google Scholar 

  5. R. Otero, J. M. Gutierrez, M. B. Mesa, E. Duque, O. Rodriguez, J. L. Arango, F. Gomez, A. Toro, F. Cano, L. M. Rodriguez, E. Caro, J. Martinez, W. Cornejo, L. M. Gomez, F. L. Uribe, S. Cardenas, V. Nunez and A. Diaz, Complications of Bothrops, Porthidium, and Bothrie-chis snakebites in Colombia. A clinical and epidemiological study of 39 cases attended in a university hospital, Toxicon, 2002, 40, 1107–1114.

    Article  CAS  Google Scholar 

  6. J. M. Gutierrez and B. Lomonte, Phospholipase A2 myotoxins from Bothrops snake venoms, Toxicon, 1995, 33, 1405–1424.

    Article  CAS  Google Scholar 

  7. G. H. Salvador, W. L. Cavalcante, J. I. Dos Santos, M. Gallacci, A. M. Soares and M. R. Fontes, Structural and functional studies with mytoxin 11 from Bothrops moojeni reveal remarkable similarities and differences compared to other catalytically inactive phospholipases A2-like, Toxicon, 2013, 72, 52–63.

    Article  CAS  Google Scholar 

  8. R. M. Kini, in Venom Phospholipase A2 Enzymes. Structure, Function and Mechanism, ed. M. R. Kini, John Wiley & Sons, New York, 1997.

  9. J. C. Villalobos, R. Mora, B. Lomonte, J. M. Gutierrez and Y. Angulo, Cytotoxicity induced in myotubes by a Lys49 phospholipase A2 homologue from the venom of the snake Bothrops asper asper: evidence of rapid plasma membrane damage and a dual role for extracellular calcium, Toxicol In Vitro, 2007, 21(8), 1382–1389.

    Article  CAS  Google Scholar 

  10. B. Lomonte, Y. Angulo and L. Calderon, An overview of Iysine-49 phospholipase A2 myotoxins from crotalid snake venoms and their structural determinants of myotoxic action, Toxicon, 2003, 42, 885–901.

    Article  CAS  Google Scholar 

  11. J. P. Zuliani, C. M. Fernandes, S. R. Zamuner, J. M. Gutierrez and C. F. P. Teixeira, Inflammatory events induced by Lys-49 and Asp-49 phospholipases A2 isolated form Bothrops asper snake venom: role of catalytic activity, Toxicon, 2005, 45, 335–346.

    Article  CAS  Google Scholar 

  12. R. G. Stabeli, S. F. Amui, C. D. Sant’ana, M. G. Pires, A. Nomizo, M. C. Monteiro, P. R. Romao, R. Guerrasa, C. A. Vieira, J. R. Giglio, M. P. Fontes and A. M. Soares, Atividades Biologicas induzidas pela MjTX-II isolada do veneno de Bothrops moojeni, Comp. Biochem. Physiol, Part C: Toxicol. Pharmacol, 2006, 142, 371–381.

    Google Scholar 

  13. A. M. Soares, S. H. Andriao-Escarso, Y. Angulo, B. Lomonte, J. M. Gutierrez, S. Marangoni, M. H. Toyama, R. K. Ami and J. R. Giglio, Structural and Functional Characterization of Myotoxin I, a Lys49 Phospholipase A2 Homologue from Bothrops moojeni (Caissaca) Snake Venom, Arch. Biochem. Biophys., 2000, 373, 7–15.

    Article  CAS  Google Scholar 

  14. B. Lomonte, A. Tarkowski and L. A. Hanson, Broad cytolytic specificity of myotoxin ll, a Iysine-49 phospholipase A2 of Bothrops asper snake venom, Toxicon, 1994, 32, 1359–1369.

    Article  CAS  Google Scholar 

  15. A. M. Soares, V. M. Rodrigues, M. I. Homsi-Brandeburgo, M. H. Toyama, F. R. Lombardi, R. K. Ami and J. R. Giglio, A rapid procedure for the isolation of the Lys-49 myotoxin ll from Bothrops moojeni(Caissaca) venom: Biochemical characterization, crystallization, myotoxic and edemato-genic activity, Toxicon, 1998, 36, 503–514.

    Article  CAS  Google Scholar 

  16. A. M. Soares, M. R. M. Fontes and J. R. Giglio, Phospholipases A2 myotoxins from Bothrops snake venoms: structure-function relationship, Curr. Org. Chem., 2004, 8, 1677–1690.

    Article  CAS  Google Scholar 

  17. J. M. Gutierrez, B. Lomonte, G. Leon, A. Rucavado, F. Chaves and Y. Angulo, Trends in snakebite envenoma-tion therapy: scientific, Technol.ogical and public health considerations, Curr. Pharm. Des., 2007, 13, 2935–2950.

    Article  CAS  Google Scholar 

  18. D. M. Dourado, S. Favero, V. Baranauskas and M. A. Cruz-Hofling, Effects of the GaAs laser irradiation on myonecrosis caused by Bothrops moojeni snake venom, Lasers Surg. Med., 2003, 33, 352–357.

    Article  Google Scholar 

  19. A. M. Barbosa, A. B. Villaverde, L. G. Sousa, E. Munin, C. M. Fernandez, J. C. Cogo and S. R. Zamuner, Effect of low level laser Theraphy in the myonecrosis induced by Bothrops jararacussu snake venom, Photomed and Laser Surgery, 2009, 27(3), 1–7.

    Google Scholar 

  20. A. M. Barbosa, A. B. Villaverde, L. Guimaraes-Souza, W. Ribeiro, J. C. Cogo and S. R. Zamuner, Effect of low level laser therapy in the inflammatory response induced by Bothrops jararacussu snake venom, Toxicon, 2008, 51, 1236–1244.

    Article  CAS  Google Scholar 

  21. L. Guimaraes-Souza, C. S. Dale, N. Nadur-Andrade, A. M. Barbosa, J. C. Cogo and S. R. Zamuner, Low-level laser therapy reduces edema, leukocyte influx and hyperalgesia induced by Bothrops jararacussu snake venom, Clin. Exp. Med. Lett., 2011, 52(3-4), 97–102.

    Google Scholar 

  22. N. Nadur-Andrade, A. M. Barbosa, F. P. Carlos, C. J. Lima, J. C. Cogo and S. R. Zamuner, Effects of photobiostimula-tion on edema and hemorrhage induced by Bothrops moojeni venom, Lasers Med. Sci., 2011, 27, 65–70.

    Article  Google Scholar 

  23. N. Nadur-Andrade, S. R. Zamuner, E. F. Toniolo, C. J. De Lima, J. C. Cogo and C. S. Dale, Analgesic Effect of Light-Emitting Diode (LED) Therapy at Wavelengths of 635 and 945 nm on Bothrops moojeni Venom-Induced Hyperalgesia, Photochem. Photobiol, 2014, 90, 207–213.

    Article  CAS  Google Scholar 

  24. A. M. Barbosa, A. B. Villaverde, L. Guimaraes-Souza, A. M. Soares, S. F. Zamuner, J. C. Cogo and S. R. Zamuner, Low-level laser therapy decreases local effects induced by myotoxins isolated from Bothrops jararacussu snake venom, J. Venom. Anim. Toxins Including Trop. Dis. (Online), 2010, 16, 470–479.

    Article  CAS  Google Scholar 

  25. C. G. Van Arman, A. J. Begany, L. M. Miller and H. H. Pless, Some details of inflammation caused by yeast and carra-geenan, J. Pharm. Exp. Ther., 1965, 150, 328–334.

    Google Scholar 

  26. J. M. Gutierrez, D. Williams, H. W. Fan and D. A. Warrell, Snakebite envenoming from a global perspective: Towards an integrated approach, Toxicon, 2010, 56(7), 1223–1235.

    Article  CAS  Google Scholar 

  27. G. H. M. Salvador, C. A. H. Fernandes, A. J. Magro, D. P. Marchi-Salvador, W. L. G. Cavalcante, R. M. Fernandez, M. Gallacci, A. M. Soares, C. L. P. Oliveira and M. R. M. Fontes, Structural and Phylogenetic Studies with MjTX-I Reveal a Multi-Oligomeric Toxin - a Novel Feature in Lys49-PLA2 s Protein Class, PLoS One, 2013, 8, e60610.

    Article  CAS  Google Scholar 

  28. C. F. Teixeira, E. C. Landucci, E. Antunes, M. Chacur and Y. Cury, Inflammatory effects of snake venom myotoxic phospholipases A2, Toxicon, 2003, 42(8), 947–962.

    Article  CAS  Google Scholar 

  29. I. L. Bonta and M. J. Parnham, Time-dependent stimulatory and inhibitory effects of prostaglandin El on exudative and tissue components of granulomatous inflammation in rats, Br. J. Pharmacol, 1979, 65(3), 465–472.

    Article  CAS  Google Scholar 

  30. A. Ohsaka, M. Motota, N. Izumi and H. Kondo, The use of differential thermal analysis and thermogravimetry to study the free and bound water of edema induced in rat skin by the toxin of Clostridium oedematiens, Jpn. J. Med. Sci. Biol., 1979, 32(2), 124–125.

    CAS  PubMed  Google Scholar 

  31. N. Galvao Nascimento, M. C. Sampaio, R. Amaral Olivo and C. F. Teixeira, Contribution of mast cells to the oedema induced by Bothrops moojeni snake venom and a pharmacological assessment of the inflammatory mediators involved, Toxicon, 2010, 55(2-3), 343–343.

    Article  Google Scholar 

  32. N. Shimizu, M. Yamaguchi, T. Goseki, Y. Shibata, H. Takiguchi, T. Iwasawa and Y. Abiko, Inhibition of prostaglandin E2 and interleukin 1 beta production by low-power laser irradiation in stretched human periodontal ligament cells, J. Dent. Res., 1995, 74, 1382–1388.

    Article  CAS  Google Scholar 

  33. L. Assis, A. I. S. Moretti, T. B. Abrahao, V. Cury, H. P. Souza, M. R. Hamblin and N. A. Parizotto, Low level laser therapy (880 nm) reduces inflammatory response and oxidative stress in rats tibialis anterior muscle after cryolesion, Lasers Surg. Med., 2012, 44(9), 726–735.

    Article  Google Scholar 

  34. F. Bortone, H. A. Santos, R. Albertini, J. B. Pesquero, M. S. Costa and J. A. Silva Jr., Low level laser therapy modulates kinin receptors mRNA expression in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation, Int. ImmunopharmacoL, 2008, 8, 206–210.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Universidade Nove dejulho, São Paulo, SP, Brazil

    Nikele Nadur-Andrade, Adriano Silvio dos Santos & Stella Regina Zamuner

  2. Department of Anatomy, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, Brazil

    Camila Squarzone Dale

  3. Oswaldo Cruz Foundation, Federal University of Rondonia, 76812-245, Porto Velho, RO, Brazil

    Andreimar M. Soares

  4. Laboratory of Biomedical Instrumentation, Camilo Castelo Branco University, São Jose dos Campos, Brazil

    Carlos J. de Lima

Authors
  1. Nikele Nadur-Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camila Squarzone Dale
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adriano Silvio dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andreimar M. Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos J. de Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stella Regina Zamuner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stella Regina Zamuner.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nadur-Andrade, N., Dale, C.S., Silvio dos Santos, A. et al. Photobiostimulation reduces edema formation induced in mice by Lys-49 phospholipases A2 isolated from Bothrops moojeni venom. Photochem Photobiol Sci 13, 1561–1567 (2014). https://doi.org/10.1039/c4pp00111g

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c4pp00111g

Search

Navigation