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BioMed Research International
Volume 2013 (2013), Article ID 391389, 9 pages
Antitumoral Potential of Tunisian Snake Venoms Secreted Phospholipases A2
1Laboratoire des Venins et Biomolecules Therapeutiques, Institut Pasteur de Tunis, 13, Place Pasteur, 1002 Tunis, Tunisia
2Université de Tunis el Manar, 1068 Tunis, Tunisia
3Centre de Recherche en Oncologie Biologique et Oncopharmacologie (CRO2), INSERM UMR 911, Marseille, France
4Université d'Aix-Marseille, Marseille, France
5Faculté de Médecine de Tunis, 1007 Tunis, Tunisia
Received 19 July 2012; Accepted 4 September 2012
Academic Editor: Luis A. Ponce Soto
Copyright © 2013 Raoudha Zouari-Kessentini 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.
- R. Doley and R. M. Kini, “Protein complexes in snake venom,” Cellular and Molecular Life Sciences, vol. 66, no. 17, pp. 2851–2871, 2009.
- 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.
- M. F. El-Refaei and N. H. Sarkar, “Snake venom inhibits the growth of mouse mammary tumor cells in vitro and in vivo,” Toxicon, vol. 54, pp. 33–41, 2009.
- V. Guimarães-Gomes, A. L. Oliveira-Carvalho, I. D. L. M. Junqueira-De-Azevedo et al., “Cloning, characterization, and structural analysis of a C-type lectin from Bothrops insularis (BiL) venom,” Archives of Biochemistry and Biophysics, vol. 432, no. 1, pp. 1–11, 2004.
- K. Stocker, “Use of snake venom proteins in medicine,” Schweizerische Medizinische Wochenschrift, vol. 129, no. 6, pp. 205–216, 1999.
- R. C. De Paula, H. C. Castro, C. R. Rodrigues, P. A. Melo, and A. L. Fuly, “Structural and pharmacological features of phospholipases A2 from snake venoms,” Protein and Peptide Letters, vol. 16, no. 8, pp. 899–907, 2009.
- R. Lakshminarayanan, S. Valiyaveettil, V. S. Rao, and R. M. Kini, “Purification, characterization, and in vitro mineralization studies of a novel goose eggshell matrix protein, ansocalcin,” Journal of Biological Chemistry, vol. 278, no. 5, pp. 2928–2936, 2003.
- R. Doley, X. Zhou, and R. M. Kini, Venoms and Toxins of Reptiles, edited by S. P. Mackessy, University of Northern Colorado, Greeley, Colo, USA, 2010.
- P. H. C. Ciscotto, B. Rates, D. A. F. Silva et al., “Venomic analysis and evaluation of antivenom cross-reactivity of South American Micrurus species,” Journal of Proteomics, vol. 74, pp. 1810–1825, 2011.
- J. M. Maraganore, G. Merutka, and W. Cho, “A new class of phospholipases A2 with lysine in place of aspartate 49. Functional consequences for calcium and substrate binding,” Journal of Biological Chemistry, vol. 259, no. 22, pp. 13839–13843, 1984.
- J. Polgár, E. M. Magnenat, M. C. Peitsch, T. N. C. Wells, and K. J. Clemetson, “Asp-49 is not an absolute prerequisite for the enzymic activity of low-Mr phospholipases A2: purification, characterization and computer modelling of an enzymically active Ser-49 phospholipase A2, ecarpholin S, from the venom of Echis carinatus sochureki (saw-scaled viper),” Biochemical Journal, vol. 319, no. 3, pp. 961–968, 1996.
- I. H. Tsai, Y. M. Wang, Y. H. Chen, T. S. Tsai, and M. C. Tu, “Venom phospholipases A2 of bamboo viper (Trimeresurus stejnegeri): molecular characterization, geographic variations and evidence of multiple ancestries,” Biochemical Journal, vol. 377, no. 1, pp. 215–223, 2004.
- T. Chijiwa, E. Tokunaga, R. Ikeda et al., “Discovery of novel [Arg49]phospholipase A2 isozymes from Protobothrops elegans venom and regional evolution of Crotalinae snake venom phospholipase A2 isozymes in the southwestern islands of Japan and Taiwan,” Toxicon, vol. 48, no. 6, pp. 672–682, 2006.
- J. M. Maraganore and R. L. Heinrikson, “The role of lysyl residues of phospholipase A2 in the formation of the catalytic complex,” Biochemical and Biophysical Research Communications, vol. 131, no. 1, pp. 129–138, 1985.
- J. I. Dos Santos, M. Cintra-Francischinelli, R. J. Borges et al., “Structural, functional, and bioinformatics studies reveal a new snake venom homologue phospholipase A2 class,” Proteins, vol. 79, no. 1, pp. 61–78, 2011.
- K. Shimuta, M. Ohnishi, S. Iyoda, N. Gotoh, N. Koizumi, and H. Watanabe, “The hemolytic and cytolytic activities of Serratia marcescens phospholipase A(PhlA) depend on lysophospholipid production by PhlA,” BMC Microbiology, vol. 9, article 261, 2009.
- 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.
- M. T. Murakami, M. R. Lourenzoni, E. Z. Arruda et al., “Biochemical and structural investigations of bothropstoxin-II, a myotoxic Asp49 phospholipase A2 from Bothrops jararacussu venom,” Protein and Peptide Letters, vol. 15, no. 9, pp. 1002–1008, 2008.
- C. Barja-Fidalgo, A. L. J. Coelho, R. Saldanha-Gama, E. Helal-Neto, A. Mariano-Oliveira, and M. S. de Freitas, “Disintegrins: integrin selective ligands which activate integrin-coupled signaling and modulate leukocyte functions,” Brazilian Journal of Medical and Biological Research, vol. 38, no. 10, pp. 1513–1520, 2005.
- V. L. Karbovskiy, O. M. Savchuk, G. L. Volkov, N. V. Zaichko, and T. Buchan, “Influence of proteins from the Agkistrodon blomhoffii ussuriensis snake venom on platelets,” Ukrain'skyi Biokhimichnyi Zhurnal, vol. 79, no. 4, pp. 82–89, 2007.
- R. Zouari-Kessentini, J. Luis, A. Karray et al., “Two purified and characterized phospholipases A2 from Cerastes cerastes venom, that inhibit cancerous cell adhesion and migration,” Toxicon, vol. 53, no. 4, pp. 444–453, 2009.
- R. P. Samy, P. Gopalakrishnakone, M. M. Thwin et al., “Antibacterial activity of snake, scorpion and bee venoms: a comparison with purified venom phospholipase A2 enzymes,” Journal of Applied Microbiology, vol. 102, no. 3, pp. 650–659, 2007.
- D. Fenard, G. Lambeau, E. Valentin, J. C. Lefebvre, M. Lazdunski, and A. Doglio, “Secreted phospholipases A2, a new class of HIV inhibitors that block virus entry into host cells,” Journal of Clinical Investigation, vol. 104, no. 5, pp. 611–618, 1999.
- C. Deregnaucourt and J. Schrével, “Bee venom phospholipase A2 induces stage-specific growth arrest of the intraerythrocytic Plasmodium falciparum via modifications of human serum components,” Journal of Biological Chemistry, vol. 275, no. 51, pp. 39973–39980, 2000.
- D. Jerusalinsky, E. Kornisiuk, R. Bernabeu, I. Izquierdo, and C. Cervenanskyl, “Muscarinic toxins from the venom of Dendroaspis snakes with agonist-like actions,” Toxicon, vol. 33, no. 4, pp. 389–397, 1995.
- J. Jebali, A. Bazaa, S. Sarray et al., “C-type lectin protein isoforms of Macrovipera lebetina: cDNA cloning and genetic diversity,” Toxicon, vol. 53, no. 2, pp. 228–237, 2009.
- A. Bazaa, E. Pasquier, C. Defilles et al., “MVL-PLA2, a snake venom phospholipase A2, inhibits angiogenesis through an increase in microtubule dynamics and disorganization of focal adhesions,” PLoS ONE, vol. 5, no. 4, Article ID e10124, 2010.
- R. Kessentini-Zouari, J. Jebali, S. Taboubi et al., “CC-PLA2-1 and CC-PLA2-2, two Cerastes cerastes venom-derived phospholipases A2, inhibit angiogenesis both in vitro and in vivo,” Laboratory Investigation, vol. 90, no. 4, pp. 510–519, 2010.
- D. Fujisawa, Y. Yamazaki, B. Lomonte, and T. Morita, “Catalytically inactive phospholipase A2 homologue binds to vascular endothelial growth factor receptor-2 via a C-terminal loop region,” Biochemical Journal, vol. 411, no. 3, pp. 515–522, 2008.
- R. Majunatha Kini and H. J. Evans, “A model to explain the pharmacological effects of snake venom phospholipases A2,” Toxicon, vol. 27, no. 6, pp. 613–635, 1989.
- L. Cupillard, R. Mulherkar, N. Gomez et al., “Both group IB and group IIA secreted phospholipases A2 are natural ligands of the mouse 180-kDa M-type receptor,” Journal of Biological Chemistry, vol. 274, no. 11, pp. 7043–7051, 1999.
- H. Rehm, T. Schafer, and H. Betz, “β-Bungarotoxin-induced cell-death of neurons in chick retina,” Brain Research, vol. 250, no. 2, pp. 309–319, 1982.
- H. Rehm, “Molecular aspects of neuronal voltage-dependent K+ channels,” European Journal of Biochemistry, vol. 202, no. 3, pp. 701–713, 1991.
- G. Lambeau, P. Ancian, J. P. Nicolas, L. Cupillard, E. Zvaritch, and M. Lazdunski, “A family of receptors for secretory phospholipases A2,” Comptes Rendus des Séances de la Société de Biologie et de ses Filiales, vol. 190, no. 4, pp. 425–435, 1996.
- G. Lambeau, J. Barhanin, H. Schweitz, J. Qar, and M. Lazdunski, “Identification and properties of very high affinity brain membrane-binding sites for a neurotoxic phospholipase from the taipan venom,” Journal of Biological Chemistry, vol. 264, no. 19, pp. 11503–11510, 1989.
- K. Hanasaki and H. Arita, “Phospholipase A2 receptor: a regulator of biological functions of secretory phospholipase A2,” Prostaglandins and Other Lipid Mediators, vol. 68-69, pp. 71–82, 2002.
- T. F. Huang, “What have snakes taught us about integrins?” Cellular and Molecular Life Sciences, vol. 54, no. 6, pp. 527–540, 1998.
- A. Bazaa, N. Marrakchi, M. El Ayeb, L. Sanz, and J. J. Calvete, “Snake venomics: comparative analysis of the venom proteomes of the Tunisian snakes Cerastes cerastes, Cerastes vipera and Macrovipera lebetina,” Proteomics, vol. 5, no. 16, pp. 4223–4235, 2005.
- M. A. McLane, T. Joerger, and A. Mahmoud, “Disintegrins in health and disease,” Frontiers in Bioscience, vol. 13, pp. 6617–6637, 2008.
- K. J. Clemetson, Q. Lu, and J. M. Clemetson, “Snake C-type lectin-like proteins and platelet receptors,” Pathophysiology of Haemostasis and Thrombosis, vol. 34, no. 4-5, pp. 150–155, 2006.
- L. C. Wijeyewickrema, M. C. Berndt, and R. K. Andrews, “Snake venom probes of platelet adhesion receptors and their ligands,” Toxicon, vol. 45, no. 8, pp. 1051–1061, 2005.
- X. Lu, D. Lu, M. F. Scully, and V. V. Kakkar, “Integrins in drug targeting-RGD templates in toxins,” Current Pharmaceutical Design, vol. 12, no. 22, pp. 2749–2769, 2006.
- S. Sarray, E. Delamarre, J. Marvaldi, M. E. Ayeb, N. Marrakchi, and J. Luis, “Lebectin and lebecetin, two C-type lectins from snake venom, inhibit α5β1 and αv-containing integrins,” Matrix Biology, vol. 26, no. 4, pp. 306–313, 2007.
- S. Sarray, J. Luis, M. El Ayeb, and N. Marrakchi, “Snake venoms C-type lectins and their receptors on platelets and cancerous cells,” Archives de l'Institut Pasteur de Tunis, vol. 85, no. 1–4, pp. 69–80, 2008.
- R. K. Andrews and M. C. Berndt, “Snake venom modulators of platelet adhesion receptors and their ligands,” Toxicon, vol. 38, no. 6, pp. 775–791, 2000.
- K. Z. Olfa, L. José, D. Salma et al., “Lebestatin, a disintegrin from Macrovipera venom, inhibits integrin-mediated cell adhesion, migration and angiogenesis,” Laboratory Investigation, vol. 85, no. 12, pp. 1507–1516, 2005.
- R. J. Carbajo, L. Sanz, S. Mosulén et al., “NMR structure and dynamics of recombinant wild type and mutated jerdostatin, a selective inhibitor of integrin α1β1,” Proteins, vol. 79, no. 8, pp. 2530–2542, 2011.
- B. B. Vargaftig, J. Prado-Franceschi, and M. Chignard, “Activation of guinea-pig platelets induced by convulxin, a substance extracted from the venom of Crotalus durissus cascavella,” European Journal of Pharmacology, vol. 68, no. 4, pp. 451–464, 1980.
- B. B. Vargaftig, D. Joseph, G. Marlas, and L. G. Chevance, “Degranulation of rabbit platelets with PAF-acether: a new procedure for unravelling the mode of action of platelet-activating substances,” Thrombosis and Haemostasis, vol. 48, no. 1, pp. 67–71, 1982.
- J. Polgár, J. M. Clemetson, B. E. Kehrel et al., “Platelet activation and signal transduction by convulxin, a C-type lectin from Crotalus durissus terrificus (Tropical rattlesnake) venom via the p62/GPVI collagen receptor,” Journal of Biological Chemistry, vol. 272, no. 21, pp. 13576–13583, 1997.
- S. Sarray, N. Srairi, J. Luis, J. Marvaldi, M. El Ayeb, and N. Marrakchi, “Lebecetin, a C-lectin protein from the venom of Macrovipera lebetina that inhibits platelet aggregation and adhesion of cancerous cells,” Haemostasis, vol. 31, no. 3–6, pp. 173–176, 2001.
- A. Pilorget, M. Conesa, S. Sarray et al., “Lebectin, a Macrovipera lebetina venom-derived C-type lectin, inhibits angiogenesis both in vitro and in vivo,” Journal of Cellular Physiology, vol. 211, no. 2, pp. 307–315, 2007.
- J. J. Calvete, J. W. Fox, A. Agelan, S. Niewiarowski, and C. Marcinkiewicz, “The presence of the WGD motif in CC8 heterodimeric disintegrin increases its inhibitory effect on αIIbβ3, αvβ3, and α5β1 integrins,” Biochemistry, vol. 41, no. 6, pp. 2014–2021, 2002.
- R. M. Kini and H. J. Evans, “Structure-function relationships of phospholipases. The anticoagulant region of phospholipases A2,” Journal of Biological Chemistry, vol. 262, no. 30, pp. 14402–14407, 1987.
- R. M. Kini, “Anticoagulant proteins from snake venoms: structure, function and mechanism,” Biochemical Journal, vol. 397, no. 3, pp. 377–387, 2006.
- G. Lambeau, P. Ancian, J. P. Nicolas et al., “Structural elements of secretory phospholipases A2 involved in the binding to M-type receptors,” Journal of Biological Chemistry, vol. 270, no. 10, pp. 5534–5540, 1995.
- G. A. Boffa, M. C. Boffa, and J. J. Winchenne, “A phospholipase A2 with anticoagulant activity. I. Isolation from Vipera berus venom and properties,” Biochimica et Biophysica Acta, vol. 429, no. 3, pp. 828–838, 1976.
- R. T. Kerns, R. M. Kini, S. Stefansson, and H. J. Evans, “Targeting of venom phospholipases: the strongly anticoagulant phospholipase A2 from Naja nigricollis venom binds to coagulation factor Xa to inhibit the prothrombinase complex,” Archives of Biochemistry and Biophysics, vol. 369, no. 1, pp. 107–113, 1999.
- R. Manjunatha Kini and H. J. Evans, “The role of enzymatic activity in inhibition of the extrinsic tenase complex by phospholipase A2 isoenzymes from Naja nigricollis venom,” Toxicon, vol. 33, no. 12, pp. 1585–1590, 1995.
- S. Lizano, Y. Angulo, B. Lomonte et al., “Two phospholipase A2 inhibitors from the plasma of Cerrophidion (Bothrops) godmani which selectively inhibit two different group-II phospholipase A2 myotoxins from its own venom: isolation, molecular cloning and biological properties,” Biochemical Journal, vol. 346, no. 3, pp. 631–639, 2000.
- J. Fernández, J. M. Gutiérrez, Y. Angulo et al., “Isolation of an acidic phospholipase A2 from the venom of the snake Bothrops asper of Costa Rica: biochemical and toxicological characterization,” Biochimie, vol. 92, no. 3, pp. 273–283, 2010.
- D. A. Higuchi, C. M. V. Barbosa, C. Bincoletto et al., “Purification and partial characterization of two phospholipases A2 from Bothrops leucurus (white-tailed-jararaca) snake venom,” Biochimie, vol. 89, no. 3, pp. 319–328, 2007.
- S. Kashima, P. G. Roberto, A. M. Soares et al., “Analysis of Bothrops jararacussu venomous gland transcriptome focusing on structural and functional aspects: I-gene expression profile of highly expressed phospholipases A2,” Biochimie, vol. 86, no. 3, pp. 211–219, 2004.
- M. Z. Huang, P. Gopalakrishnakone, and R. M. Kini, “Role of enzymatic activity in the antiplatelet effects of a phospholipase A2 from Ophiophagus hannah snake venom,” Life Sciences, vol. 61, no. 22, pp. 2211–2217, 1997.
- G. Maity, S. Mandal, P. Bhattacharjee, and D. Bhattacharyya, “Thermal detoxification of the venom from Daboia russelli russelli of Eastern India with restoration of fibrinolytic activity,” Toxicon, vol. 57, no. 5, pp. 747–754, 2011.
- J. Folkman, “Angiogenesis: an organizing principle for drug discovery?” Nature Reviews Drug Discovery, vol. 6, no. 4, pp. 273–286, 2007.
- P. Ernsberger, M. E. Graves, L. M. Graff et al., “I1-imidazoline receptors—definition, characterization, distribution, and transmembrane signaling,” Annals of the New York Academy of Sciences, vol. 763, pp. 22–42, 1995.
- J. D. Watson and E. J. Milner-White, “The conformations of polypeptide chains where the main-chain parts of successive residues are enantiomeric. Their occurrence in cation and anion-binding regions of proteins,” Journal of Molecular Biology, vol. 315, no. 2, pp. 183–191, 2002.
- Y. Yamazaki, Y. Matsunaga, Y. Nakano, and T. Morita, “Identification of vascular endothelial growth factor receptor-binding protein in the venom of eastern cottonmouth: a new role of snake venom myotoxic LYS49-phospholipase A2,” Journal of Biological Chemistry, vol. 280, no. 34, pp. 29989–29992, 2005.
- M. L. Gardel, B. Sabass, L. Ji, G. Danuser, U. S. Schwarz, and C. M. Waterman, “Traction stress in focal adhesions correlates biphasically with actin retrograde fl ow speed,” Journal of Cell Biology, vol. 183, no. 6, pp. 999–1005, 2008.
- B. Wehrle-Haller and B. A. Imhof, “Actin, microtubules and focal adhesion dynamics during cell migration,” International Journal of Biochemistry and Cell Biology, vol. 35, no. 1, pp. 39–50, 2003.
- D. H. Madsen, S. Ingvarsen, H. J. Jürgensen et al., “The non-phagocytic route of collagen uptake: a distinct degradation pathway,” Journal of Biological Chemistry, vol. 286, no. 30, pp. 26996–27010, 2011.
- K. Zaoui, K. Benseddik, P. Daou, D. Salaün, and A. Badache, “ErbB2 receptor controls microtubule capture by recruiting ACF7 to the plasma membrane of migrating cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 43, pp. 18517–18522, 2010.
- S. Elifio-Esposito, L. Tomazeli, C. Schwartz et al., “Human neutrophil migration and activation by BJcuL, a galactose binding lectin purified from Bothrops jararacussu venom,” BMC Immunology, vol. 12, article 10, 2011.
- J. Folkman, “Tumor angiogenesis: therapeutic implications,” New England Journal of Medicine, vol. 285, no. 21, pp. 1182–1186, 1971.
- F. P. Silva, G. M. C. Alexandre, C. H. I. Ramos, and S. G. De-Simone, “On the quaternary structure of a C-type lectin from Bothrops jararacussu venom—BJ-32 (BjcuL),” Toxicon, vol. 52, no. 8, pp. 944–953, 2008.
- I. Y. Torshin, “Structural criteria of biologically active RGD-sites for analysis of protein cellular function—a bioinformatics study,” Medical Science Monitor, vol. 8, no. 8, pp. BR301–BR312, 2002.
- D. H. F. Souza, M. R. C. Iemma, L. L. Ferreira et al., “The disintegrin-like domain of the snake venom metalloprotease alternagin inhibits α2β1 integrin-mediated cell adhesion,” Archives of Biochemistry and Biophysics, vol. 384, no. 2, pp. 341–350, 2000.
- U. Hersel, C. Dahmen, and H. Kessler, “RGD modified polymers: biomaterials for stimulated cell adhesion and beyond,” Biomaterials, vol. 24, no. 24, pp. 4385–4415, 2003.
- J. J. Calvete, M. P. Moreno-Murciano, R. D. G. Theakston, D. G. Kisiel, and C. Marcinkiewicz, “Snake venom disintegrins: novel dimeric disintegrins and structural diversification by disulphide bond engineering,” Biochemical Journal, vol. 372, no. 3, pp. 725–734, 2003.
- R. L. Heinrikson, E. T. Krueger, and P. S. Keim, “Amino acid sequence of phospholipase A2α from the venom of Crotalus adamanteus. A new classification of phospholipases A2 based upon structural determinants,” Journal of Biological Chemistry, vol. 252, no. 14, pp. 4913–4921, 1977.
- G. Lambeau, J. Barhanin, and M. Lazdunski, “Identification of different receptor types for toxic phospholipases A2 in rabbit skeletal muscle,” FEBS Letters, vol. 293, no. 1-2, pp. 29–33, 1991.
- E. C. T. Landucci, R. C. Castro, M. F. Pereira et al., “Mast cell degranulation induced by two phospholipase A2 homologues: dissociation between enzymatic and biological activities,” European Journal of Pharmacology, vol. 343, no. 2-3, pp. 257–263, 1998.