- About this Journal ·
- Abstracting and Indexing ·
- Aims and Scope ·
- Annual Issues ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 153045, 8 pages
Snake Venom PLA2s Inhibitors Isolated from Brazilian Plants: Synthetic and Natural Molecules
1Chemistry, Biotechnology and Bioprocess Department, Federal University of São João Del Rei, 36420-000 Ouro Branco, MG, Brazil
2Molecular Biology Department, Federal University of Paraíba, 58051-900 João Pessoa, PB, Brazil
3Biochemistry Department, State University of Campinas, 13083-970 Campinas, SP, Brazil
4Chemistry Department, Federal University of Lavras, 37200-000 Lavras, MG, Brazil
5Oswaldo Cruz Foundation, Federal University of Rondonia, 76812-245 Porto Velho, RO, Brazil
Received 31 May 2013; Accepted 19 August 2013
Academic Editor: Fernando Albericio
Copyright © 2013 B. M. A. Carvalho et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- D. C. I. Koh, A. Armugam, and K. Jeyaseelan, “Snake venom components and their applications in biomedicine,” Cellular and Molecular Life Sciences, vol. 63, no. 24, pp. 3030–3041, 2006.
- R. K. Arni and R. J. Ward, “Phospholipase A2—a structural review,” Toxicon, vol. 34, no. 8, pp. 827–841, 1996.
- C. D. Funk, “Prostaglandins and Leukotrienes: advances in eicosanoid biology,” Science, vol. 294, no. 5548, pp. 1871–1875, 2001.
- F. S. Markland Jr, “Snake venoms and the hemostatic system,” Toxicon, vol. 36, no. 12, pp. 1749–1800, 1998.
- S. L. da Silva, M. Comar Jr., K. M. T. Oliveira et al., “Molecular modeling of the inhibition of enzyme PLA2 from snake venom by dipyrone and 1-phenyl-3-methyl-5-pyrazolone,” International Journal of Quantum Chemistry, vol. 108, no. 13, pp. 2576–2585, 2008.
- Z. Mallat, G. Lambeau, and A. Tedgui, “Lipoprotein-associated and secreted phospholipases A2 in cardiovascular disease: roles as biological effectors and biomarkers,” Circulation, vol. 122, no. 21, pp. 2183–2200, 2010.
- D. de Luca, A. Minucci, P. Cogo et al., “Secretory phospholipase A2 pathway during pediatric acute respiratory distress syndrome: a preliminary study,” Pediatric Critical Care Medicine, vol. 12, no. 1, pp. e20–e24, 2011.
- R. Ezzeddini, M. Darabi, B. Ghasemi et al., “Circulating phospholipase A2 activity in obstructive sleep apnea and recurrent tonsillitis,” International Journal of Pediatric Otorhinolaryngology, vol. 76, no. 4, pp. 471–474, 2012.
- S. Chalbot, H. Zetterberg, K. Blennow et al., “Blood-cerebrospinal fluid barrier permeability in Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 25, no. 3, pp. 505–515, 2011.
- A. A. Farooqui, M. L. Litsky, T. Farooqui, and L. A. Horrocks, “Inhibitors of intracellular phospholipase A2 activity: their neurochemical effects and therapeutical importance for neurological disorders,” Brain Research Bulletin, vol. 49, no. 3, pp. 139–153, 1999.
- S. S. Teixeira, L. B. Silveira, F. M. N. da Silva et al., “Molecular characterization of an acidic phospholipase A2 from Bothrops pirajai snake venom: synthetic C-terminal peptide identifies its antiplatelet region,” Archives of Toxicology, vol. 85, no. 10, pp. 1219–1233, 2011.
- L. Romero, S. Marcussi, D. P. Marchi-Salvador et al., “Enzymatic and structural characterization of a basic phospholipase A2 from the sea anemone Condylactis gigantea,” Biochimie, vol. 92, no. 8, pp. 1063–1071, 2010.
- L. C. Corrêa, D. P. Marchi-Salvador, A. C. O. Cintra, S. V. Sampaio, A. M. Soares, and M. R. M. Fontes, “Crystal structure of a myotoxic Asp49-phospholipase A2 with low catalytic activity: insights into Ca2+ independent catalytic mechanism,” Biochimica et Biophysica Acta, vol. 1784, no. 4, pp. 591–599, 2008.
- D. P. Marchi-Salvador, L. C. Corrêa, A. J. Magro, C. Z. Oliveira, A. M. Soares, and M. R. M. Fontes, “Insights into the role of oligomeric state on the biological activities of crotoxin: crystal structure of a tetrameric phospholipase A2 formed by two isoforms of crotoxin B from Crotalus durissus terrificus venom,” Proteins, vol. 72, no. 3, pp. 883–891, 2008.
- D. P. Marchi-Salvador, C. A. H. Fernandes, L. B. Silveira, A. M. Soares, and M. R. M. Fontes, “Crystal structure of a phospholipase A2 homolog complexed with p-bromophenacyl bromide reveals important structural changes associated with the inhibition of myotoxic activity,” Biochimica et Biophysica Acta, vol. 1794, no. 11, pp. 1583–1590, 2009.
- C. A. H. Fernandes, D. P. Marchi-Salvador, G. H. M. Salvador et al., “Comparison between apo and complexed structures of bothropstoxin-I reveals the role of Lys122 and Ca2+-binding loop region for the catalytically inactive Lys49-PLA2s,” Journal of Structural Biology, vol. 171, no. 1, pp. 31–43, 2010.
- J. L. C. Cardoso, F. O. S. França, F. H. Wen, C. M. S. Málaque, and V. Haddad Jr, Animais peçonhentos no Brasil: biologia clinica e terapêutica dos acidentes, Sarvier, São Paulo, Brazil, 2003.
- D. C. S. Damico, M. A. C. Höfling, M. Cintra et al., “Pharmacological study of edema and myonecrosis in mice induced by venom of the bushmaster snake (Lachesis muta muta) and its basic Asp49 phospholipase A2 (LmTX-I),” The Protein Journal, vol. 27, no. 6, pp. 384–391, 2008.
- D. C. S. Damico, T. Vassequi-Silva, F. D. Torres-Huaco et al., “LmrTX, a basic PLA2 (D49) purified from Lachesis muta rhombeata snake venom with enzymatic-related antithrombotic and anticoagulant activity,” Toxicon, vol. 60, pp. 773–781, 2012.
- M. Ohno, R. Ménez, T. Ogawa et al., “Molecular evolution of snake toxins: is the functional diversity of snake toxins associated with a mechanism of accelerated evolution?” Progress in Nucleic Acid Research and Molecular Biology, vol. 59, pp. 307–364, 1998.
- E. Valentin and G. Lambeau, “What can venom phospholipases A2 tell us about the functional diversity of mammalian secreted phospholipases A2?” Biochimie, vol. 82, no. 9-10, pp. 815–831, 2000.
- W. L. G. Cavalcante, T. O. Campos, M. dal Pai-Silva et al., “Neutralization of snake venom phospholipase A2 toxins by aqueous extract of Casearia sylvestris (Flacourtiaceae) in mouse neuromuscular preparation,” Journal of Ethnopharmacology, vol. 112, no. 3, pp. 490–497, 2007.
- S. Marcussi, C. D. Sant'Ana, C. Z. Oliveira et al., “Snake venom phospholipase A2 inhibitors: medicinal chemistry and therapeutic potential,” Current Topics in Medicinal Chemistry, vol. 7, no. 8, pp. 743–756, 2007.
- C. Z. Oliveira, D. L. Menaldo, S. Marcussi et al., “An α-type phospholipase A2 inhibitor from Bothrops jararacussu snake plasma: structural and functional characterization,” Biochimie, vol. 90, no. 10, pp. 1506–1514, 2008.
- B. S. Cummings, J. McHowat, and R. G. Schnellmann, “Phospholipase A2s in cell injury and death,” The Journal of Pharmacology and Experimental Therapeutics, vol. 294, no. 3, pp. 793–799, 2000.
- C. Araya and B. Lomonte, “Antitumor effects of cationic synthetic peptides derived from Lys49 phospholipase A2 homologues of snake venoms,” Cell Biology International, vol. 31, no. 3, pp. 263–268, 2007.
- B. Lomonte, Y. Angulo, and E. Moreno, “Synthetic peptides derived from the C-Terminal region of Lys49 phospholipase A2 homologues from viperidae snake venoms: biomimetic activities and potential applications,” Current Pharmaceutical Design, vol. 16, no. 28, pp. 3224–3230, 2010.
- R. Perumal Samy and P. Gopalakrishnakone, “Therapeutic potential of plants as anti-microbials for drug discovery,” Evidence-Based Complementary and Alternative Medicine, vol. 7, no. 3, pp. 283–294, 2010.
- C. Z. Oliveira, N. A. Santos-Filho, D. L. Menaldo et al., “Structural and functional characterization of a γ-type phospholipase A2 inhibitor from Bothrops jararacussu Snake Plasma,” Current Topics in Medicinal Chemistry, vol. 11, no. 20, pp. 2509–2519, 2011.
- J. M. Gutiérrez, B. Lomonte, G. León, A. Rucavado, F. Chaves, and Y. Angulo, “Trends in snakebite envenomation therapy: scientific, technological and public health considerations,” Current Pharmaceutical Design, vol. 13, no. 28, pp. 2935–2950, 2007.
- M. García, M. Monge, G. León et al., “Effect of preservatives on IgG aggregation, complement-activating effect and hypotensive activity of horse polyvalent antivenom used in snakebite envenomation,” Biologicals, vol. 30, no. 2, pp. 143–151, 2002.
- J. M. Schmidt, “Antivenom therapy for snakebites in children: is there evidence?” Current Opinion in Pediatrics, vol. 17, no. 2, pp. 234–238, 2005.
- J. A. F. P. Villar, F. T. D. Lima, C. L. Veber et al., “Synthesis and evaluation of nitrostyrene derivative compounds, new snake venom phospholipase A2 inhibitors,” Toxicon, vol. 51, no. 8, pp. 1467–1478, 2008.
- A. M. Soares, A. H. Januário, M. V. Lourenço, A. M. S. Pereira, and P. S. Pereira, “Neutralizing effects of Brazilian plants against snake venoms,” Drugs of the Future, vol. 29, no. 11, pp. 1105–1117, 2004.
- M. L. da Silva, S. Marcussi, R. S. Fernandes et al., “Anti-snake venom activities of extracts and fractions from callus cultures of Sapindus saponaria,” Pharmaceutical Biology, vol. 50, no. 3, pp. 366–375, 2012.
- F. K. Ticli, L. I. S. Hage, R. S. Cambraia et al., “Rosmarinic acid, a new snake venom phospholipase A2 inhibitor from Cordia verbenacea (Boraginaceae): antiserum action potentiation and molecular interaction,” Toxicon, vol. 46, no. 3, pp. 318–327, 2005.
- W. B. Mors, M. C. Nascimento, B. M. R. Pereira, and N. A. Pereira, “Plant natural products active against snake bite—the molecular approach,” Phytochemistry, vol. 55, no. 6, pp. 627–642, 2000.
- M. H. Borges, A. M. Soares, V. M. Rodrigues et al., “Effects of aqueous extract of Casearia sylvestris (Flacourtiaceae) on actions of snake and bee venoms and on activity of phospholipases A2,” Comparative Biochemistry and Physiology B, vol. 127, no. 1, pp. 21–30, 2000.
- M. H. Borges, A. M. Soares, V. M. Rodrigues et al., “Neutralization of proteases from Bothrops snake venoms by the aqueous extract from Casearia sylvestris (Flacourtiaceae),” Toxicon, vol. 39, no. 12, pp. 1863–1869, 2001.
- R. Biondo, A. M. S. Pereira, S. Marcussi, P. S. Pereira, S. C. França, and A. M. Soares, “Inhibition of enzymatic and pharmacological activities of some snake venoms and toxins by Mandevilla velutina (Apocynaceae) aqueous extract,” Biochimie, vol. 85, no. 10, pp. 1017–1025, 2003.
- R. Biondo, A. M. Soares, B. W. Bertoni, S. C. França, and A. M. S. Pereira, “Direct organogenesis of Mandevilla illustris (Vell) Woodson and effects of its aqueous extract on the enzymatic and toxic activities of Crotalus durissus terrificus snake venom,” Plant Cell Reports, vol. 22, no. 8, pp. 549–552, 2004.
- J. O. da Silva, J. S. Coppede, V. C. Fernandes et al., “Antihemorrhagic, antinucleolytic and other antiophidian properties of the aqueous extract from Pentaclethra macroloba,” Journal of Ethnopharmacology, vol. 100, no. 1-2, pp. 145–152, 2005.
- L. Almeida, A. C. O. Cintra, E. L. G. Veronese et al., “Anticrotalic and antitumoral activities of gel filtration fractions of aqueous extract from Tabernaemontana catharinensis (Apocynaceae),” Comparative Biochemistry and Physiology C, vol. 137, no. 1, pp. 19–27, 2004.
- E. L. G. Veronese, L. E. Esmeraldino, A. P. F. Trombone et al., “Inhibition of the myotoxic activity of Bothrops jararacussu venom and its two major myotoxins, BthTX-I and BthTX-II, by the aqueous extract of Tabernaemontana catharinensis A. DC. (Apocynaceae),” Phytomedicine, vol. 12, no. 1-2, pp. 123–130, 2005.
- C. Z. Oliveira, V. A. Maiorano, S. Marcussi et al., “Anticoagulant and antifibrinogenolytic properties of the aqueous extract from Bauhinia forficata against snake venoms,” Journal of Ethnopharmacology, vol. 98, no. 1-2, pp. 213–216, 2005.
- M. M. Mendes, C. F. Oliveira, D. S. Lopes et al., “Anti-snake venom properties of Schizolobium parahyba (Caesalpinoideae) aqueous leaves extract,” Phytotherapy Research, vol. 22, no. 7, pp. 859–866, 2008.
- I. C. Pereira, A. M. Barbosa, M. J. Salvador et al., “Anti-inflammatory activity of Blutaparon portulacoides ethanolic extract against the inflammatory reaction induced by Bothrops jararacussu venom and isolated myotoxins BthTX-I and II,” Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 15, no. 3, pp. 527–545, 2009.
- V. A. Maiorano, S. Marcussi, M. A. F. Daher et al., “Antiophidian properties of the aqueous extract of Mikania glomerata,” Journal of Ethnopharmacology, vol. 102, no. 3, pp. 364–370, 2005.
- R. S. Floriano, R. M. B. Nogueira, M. Sakate et al., “Effect of Mikania glomerata (Asteraceae) leaf extract combined with anti-venom serum on experimental Crotalus durissus (Squamata: Viperidae) envenomation in rats,” Revista de Biología Tropical, vol. 57, no. 4, pp. 929–937, 2009.
- V. S. Nazato, L. Rubem-Mauro, N. A. G. Vieira et al., “In vitro antiophidian properties of Dipteryx alataVogel bark extracts,” Molecules, vol. 15, no. 9, pp. 5956–5970, 2010.
- P. Puebla, Y. Oshima-Franco, L. M. Franco et al., “Chemical constituents of the bark of Dipteryx alata vogel, an active species against Bothrops jararacussu venom,” Molecules, vol. 15, no. 11, pp. 8193–8204, 2010.
- M. Assafim, E. C. Coriolano, S. E. Benedito et al., “Hypericum brasiliense plant extract neutralizes some biological effects of Bothrops jararaca snake venom,” Journal of Venom Research, vol. 2, pp. 11–16, 2011.
- A. Dey and J. N. De, “Phytopharmacology of antiophidian botanicals: a review,” International Journal of Pharmacology, vol. 8, no. 2, pp. 62–79, 2012.
- R. P. Samy, P. Gopalakrishnakone, and V. T. Chow, “Therapeutic application of natural inhibitors against snake venom phospholipase A2,” Bioinformation, vol. 8, pp. 48–57, 2012.
- A. M. Soares, F. K. Ticli, S. Marcussi et al., “Medicinal plants with inhibitory properties against snake venoms,” Current Medicinal Chemistry, vol. 12, no. 22, pp. 2625–2641, 2005.
- J. Lättig, M. Böhl, P. Fischer et al., “Mechanism of inhibition of human secretory phospholipase A2 by flavonoids: rationale for lead design,” Journal of Computer-Aided Molecular Design, vol. 21, no. 8, pp. 473–483, 2007.
- L. C. Diogo, R. S. Fernandes, S. Marcussi et al., “Inhibition of snake venoms and phospholipases A2 by extracts from native and genetically modified Eclipta alba: isolation of active coumestans,” Basic & Clinical Pharmacology & Toxicology, vol. 104, no. 4, pp. 293–299, 2009.
- A. J. M. da Silva, P. A. Melo, N. M. V. Silva et al., “Synthesis and preliminary pharmacological evaluation of coumestans with different patterns of oxygenation,” Bioorganic & Medicinal Chemistry Letters, vol. 11, no. 3, pp. 283–286, 2001.
- R. C. S. Nunomura, V. G. Oliveira, S. L. da Silva, and S. M. Nunomura, “Characterization of bergenin in Endopleura uchi bark and its anti-inflammatory activity,” Journal of the Brazilian Chemical Society, vol. 20, no. 6, pp. 1060–1064, 2009.
- M. F. Batina, A. C. O. Cintra, E. L. G. Veronese et al., “Inhibition of the lethal and myotoxic activities of Crotalus durissus terrificus venom by Tabernaemontana catharinensis: identification of one of the active components,” Planta Medica, vol. 66, no. 5, pp. 424–428, 2000.
- L. A. F. Ferreira, O. B. Henriques, A. A. S. Andreoni et al., “Antivenom and biological effects of ar-turmerone isolated from Curcuma longa (Zingiberaceae),” Toxicon, vol. 30, no. 10, pp. 1211–1218, 1992.
- V. Núñez, V. Castro, R. Murillo, L. A. Ponce-Soto, I. Merfort, and B. Lomonte, “Inhibitory effects of Piper umbellatum and Piper peltatum extracts towards myotoxic phospholipases A2 from Bothrops snake venoms: isolation of 4-nerolidylcatechol as active principle,” Phytochemistry, vol. 66, no. 9, pp. 1017–1025, 2005.
- S. L. da Silva, A. K. Calgarotto, J. S. Chaar, and S. Marangoni, “Isolation and characterization of ellagic acid derivatives isolated from Casearia sylvestris SW aqueous extract with anti-PLA2 activity,” Toxicon, vol. 52, no. 6, pp. 655–666, 2008.
- B. S. Vishwanath and T. V. Gowda, “Interaction of aristolochic acid with Vipera russelli phospholipase A2: its effect on enzymatic and pathological activities,” Toxicon, vol. 25, no. 9, pp. 929–937, 1987.
- B. S. Vishwanath, R. M. Kini, and T. V. Gowda, “Characterization of three edema-inducing phospholipase A2 enzymes from habu (Trimeresurus flavoviridis) venom and their interaction with the alkaloid aristolochic acid,” Toxicon, vol. 25, no. 5, pp. 501–515, 1987.
- V. Chandra, J. Jasti, P. Kaur, A. Srinivasan, C. H. Betzel, and T. P. Singh, “Structural basis of phospholipase A2 inhibition for the synthesis of prostaglandins by the plant alkaloid aristolochic acid from a 1.7 Å crystal structure,” Biochemistry, vol. 41, no. 36, pp. 10914–10919, 2002.
- P. S. Shimabuku, C. A. H. Fernandes, A. J. Magro, T. R. Costa, A. M. Soares, and M. R. M. Fontes, “Crystallization and preliminary X-ray diffraction analysis of a Lys49-phospholipase A2 complexed with caffeic acid, a molecule with inhibitory properties against snake venoms,” Acta Crystallographica F, vol. 67, no. 2, pp. 249–252, 2011.
- J. I. Santos, F. F. Cardoso, A. M. Soares, M. dal Pai Silva, M. Gallacci, and M. R. M. Fontes, “Structural and functional studies of a bothropic myotoxin complexed to rosmarinic acid: new insights into Lys49-PLA2 inhibition,” PLoS One, vol. 6, no. 12, Article ID e28521, pp. 1–11, 2011.
- A. D. L. Souza, E. Rodrigues-Filho, A. Q. L. Souza et al., “Koninginins, phospholipase A2 inhibitors from endophytic fungus Trichoderma koningii,” Toxicon, vol. 51, no. 2, pp. 240–250, 2008.
- W. B. Mors, M. C. do Nascimento, J. P. Parente, M. H. da Silva, P. A. Melo, and G. Suarez-Kurtz, “Neutralization of lethal and myotoxic activities of South American rattlesnake venom by extracts and constituents of the plant Eclipta prostrata (Asteraceae),” Toxicon, vol. 27, no. 9, pp. 1003–1009, 1989.
- A. H. Januário, S. L. Santos, S. Marcussi et al., “Neo-clerodane diterpenoid, a new metalloprotease snake venom inhibitor from Baccharis trimera (Asteraceae): anti-proteolytic and anti-hemorrhagic properties,” Chemico-Biological Interactions, vol. 150, no. 3, pp. 243–251, 2004.
- A. J. M. da Silva, A. L. Coelho, A. B. C. Simas et al., “Synthesis and pharmacological evaluation of prenylated and benzylated pterocarpans against snake venom,” Bioorganic & Medicinal Chemistry Letters, vol. 14, no. 2, pp. 431–435, 2004.
- D. N. Georgieva, W. Rypniewski, M. Perbandt, M. Jain, N. Genov, and C. Betzel, “Crystallization and preliminary X-ray diffraction studies of a toxic phospholipase A2 from the venom of Vipera ammodytes meridionalis complexed to a synthetic inhibitor,” Biochimica et Biophysica Acta, vol. 1650, no. 1-2, pp. 1–3, 2003.
- D. N. Georgieva, W. Rypniewski, A. Gabdoulkhakov, N. Genov, and C. Betzel, “Asp49 phospholipase A2-elaidoylamide complex: a new mode of inhibition,” Biochemical and Biophysical Research Communications, vol. 319, no. 4, pp. 1314–1321, 2004.
- S. L. da Silva, A. K. Calgarotto, V. Maso et al., “Molecular modeling and inhibition of phospholipase A2 by polyhydroxy phenolic compounds,” European Journal of Medicinal Chemistry, vol. 44, no. 1, pp. 312–321, 2009.
- E. S. de Alvarenga, S. A. Silva, L. C. A. Barosa et al., “Synthesis and evaluation of sesquiterpene lactone inhibitors of phospholipase A2 from Bothrops jararacussu,” Toxicon, vol. 57, no. 1, pp. 100–108, 2011.