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

Volumn 171, Issue 1, 2010, Pages 31-43

  Fernandes, Carlos A H ^a,b   Marchi Salvador, Daniela P ^a,c   Salvador, Guilherme M ^a,b   Silva, Mabel C O ^a   Costa, Tássia R ^b,c   Soares, Andreimar M ^b,c   Fontes, Marcos R M ^a,b  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b CNPq   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Ca2+ binding loop; Homologue phospholipase A2 (Lys49 PLA2s); Myotoxicity; Phospholipase A2; X ray crystallography

Indexed keywords

4 BROMOFENACIL BROMIDE; ASPARTIC ACID; BOTHROPSTOXIN 1; CALCIUM ION; CARBOXYL GROUP; GLYCINE; LYSINE; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; SNAKE VENOM; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM BINDING; CATALYSIS; CHEMICAL MODIFICATION; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME STRUCTURE; HYDROPHOBICITY; LIGHT SCATTERING; NONHUMAN; PRIORITY JOURNAL; SNAKE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BOTHROPS; CALCIUM; CROTALID VENOMS; CRYSTALLOGRAPHY, X-RAY; LYSINE; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

BOTHROPS; SERPENTES;

EID: 77953613264     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.03.019     Document Type: Article

References (49)

1. Angulo Y., Gutierrez J.M., Soares A.M., Cho W., Lomonte B. Myotoxic and cytolytic activities of dimeric Lys49 phospholipase A2 homologues are reduced, but not abolished, by a pH-induced dissociation. Toxicon 2005, 46:291-296.
2. Arni R.K., Ward R.J., Gutierrez J.M., Tulinsky A. Structure of a calcium-independent phospholipase-like myotoxic protein from Bothrops asper venom. Acta Crystallogr. D Biol. Crystallogr. 1995, 51:311-317.
3. Arni R.K., Fontes M.R.M., Barberato C., Gutierrez J.M., Diaz C., Ward R.J. Crystal structure of myotoxin II, a monomeric Lys49-phospholipase A2 homologue isolated from the venom of Cerrophidion (Bothrops) godmani. Arch. Biochem. Biophys. 1999, 366:177-182.
4. de Azevedo W.F., Ward R.J., Gutierrez J.M., Arni R.K. Structure of a Lys49 phospholipase A2 homologue isolated from the venom of Bothrops nummifer (jumping viper). Toxicon 1999, 37:371-384.
5. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., Read R.J., Rice L.M., Simonson T., Warren G.L. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D - Biol. Crystallogr. 1998, 54:905-921.
6. Chandra V., Kaur P., Jasti J., Betzel C., Singh T.P. Regulation of catalytic function by molecular association: structure of phospholipase A2 from Daboia russelli pulchella (DPLA2) at 1.9 Å resolution. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:1793-1798.
7. Chioato L., Aragao E.A., Ferreira T.L., de Medeiros A.I., Faccioli L.H., Ward R.J. Mapping of the structural determinants of artificial and biological membrane damaging activities of a Lys49 phospholipase A2 by scanning alanine mutagenesis. Biochim. Biophys. Acta - Biomembr. 2007, 1768:1247-1257.
8. Correa L.C., Marchi-Salvador D.P., Cintra A.C.O., Sampaio S.V., Soares A.A., Fontes M.R.M. Crystal structure of a myotoxic Asp49-phospholipase A2 with low catalytic activity: insights into Ca2+-independent catalytic mechanism. Biochim. Biophys. Acta - Proteins Proteomics 2008, 1784:591-599.
9. DeLano, W.L., 2002. The PyMOL Molecular Graphics System, DeLano Scientific LLC, San Carlos, CA.
10. Diaz-Oreiro C., Gutierrez J.M. Chemical modification of histidine and lysine residues of myotoxic phospholipases A2 isolated from Bothrops asper and Bothrops godmani snake venoms: effects on enzymatic and pharmacological properties. Toxicon 1997, 35:241-252.
11. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
12. Gutierrez J.M., Lomonte B. Phospholipase A2 myotoxins from Bothrops snake venoms. Toxicon 1995, 33:1405-1424.
13. Holland D.R., Clancy L.L., Muchmore S.W., Ryde T.J., Einspahr H.M., Finzel B.C., Heinrikson R.L., Watenpaugh K.D. The crystal structure of a lysine 49 phospholipase A2 from the venom of the cottonmouth snake at 2.0 Å resolution. J Biol Chem 1990, 265:17649-17656.
14. Homsi-Brandeburgo M.I., Queiroz L.S., Santo-Neto H., Rodrigues-Simioni L., Giglio J.R. Fractionation of Bothrops jararacussu snake venom: partial chemical characterization and biological activity of bothropstoxin. Toxicon 1988, 26:615-627.
15. Jancarik J., Kim S.H. Sparse-matrix sampling - a screening method for crystallization of proteins. J. Appl. Crystallogr. 1991, 24:409-411.
16. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
17. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
18. Kwong P.D., McDonald N.Q., Sigler P.B., Hendrickson W.A. Structure of beta 2-bungarotoxin: potassium channel binding by Kunitz modules and targeted phospholipase action. Structure 1995, 3:1109-1119.
19. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 26:283-291.
20. Lee W.H., da Silva Giotto M.T., Marangoni S., Toyama M.H., Polikarpov I., Garratt R.C. Structural basis for low catalytic activity in Lys49 phospholipases A2 - a hypothesis: the crystal structure of piratoxin II complexed to fatty acid. Biochemistry 2001, 40:28-36.
21. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., Richardson J.S., Richardson D.C. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003, 50:437-450.
22. Magro A.J., Soares A.M., Giglio J.R., Fontes M.R.M. Crystal structures of BnSP-7 and BnSP-6, two Lys49-phospholipases A2: quaternary structure and inhibition mechanism insights. Biochem. Biophys. Res. Commun. 2003, 311:713-720.
23. Magro A.J., Takeda A.A., Soares A.M., Fontes M.R.M. Structure of BthA-I complexed with p-bromophenacyl bromide: possible correlations with lack of pharmacological activity. Acta Crystallogr. D Biol. Crystallogr. 2005, 61:1670-1677.
24. Magro A.J., Fernandes C.A., dos Santos J.I., Fontes M.R. Influence of quaternary conformation on the biological activities of the Asp49-phospholipases A2s from snake venoms. Protein Pept. Lett. 2009, 16:852-859.
25. Marchi-Salvador D.P., Fernandes C.A., Silveira L.B., Soares A.M., Fontes M.R. Crystal structure of a phospholipase A2 homolog complexed with p-bromophenacyl bromide reveals important structural changes associated with the inhibition of myotoxic activity. Biochim. Biophys. Acta 2009, 1794:1583-1590.
26. McPherson, A., 2003. Introduction to Macromolecular Crystallography, Wiley-Liss, Hoboken.
27. Moolenaar W.H., van Meeteren L.A., Giepmans B.N. The ins and outs of lysophosphatidic acid signaling. BioEssays 2004, 26:870-881.
28. Murakami M.T., Arruda E.Z., Melo P.A., Martinez A.B., Calil-Elias S., Tomaz M.A., Lomonte B., Gutierrez J.M., Arni R.K. Inhibition of myotoxic activity of Bothrops asper myotoxin II by the anti-trypanosomal drug surarnin. J. Mol. Biol. 2005, 350:416-426.
29. Murakami M.T., Vicoti M.M., Abrego J.R.B., Lourenzoni M.R., Cintra A.C.O., Arruda E.Z., Tomaz M.A., Melo P.A., Arni R.K. Interfacial surface charge and free accessibility to the PLA2-active site-like region are essential requirements for the activity of Lys49 PLA2 homologues. Toxicon 2007, 49:378-387.
30. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
31. Navaza J. Amore - an automated package for molecular replacement. Acta Crystallogr. A 1994, 50:157-163.
32. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. Pt A 1997, 276:307-326.
33. Prescott S.M., Zimmerman G.A., Stafforini D.M., McIntyre T.M. Platelet-activating factor and related lipid mediators. Annu. Rev. Biochem. 2000, 69:419-445.
34. Rogers J., Yu B.Z., Serves S.V., Tsivgoulis G.M., Sotiropoulos D.N., Ioannou P.V., Jain M.K. Kinetic basis for the substrate specificity during hydrolysis of phospholipids by secreted phospholipase A2. Biochemistry 1996, 35:9375-9384.
35. dos Santos J.I., Soares A.M., Fontes M.R.M. Comparative structural studies on Lys49-phospholipases A2 from Bothrops genus reveal their myotoxic site. J. Struct. Biol. 2009, 167:106-116.
36. Schaloske R.H., Dennis E.A. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 2006, 1761:1246-1259.
37. Scott D.L., White S.P., Otwinowski Z., Yuan W., Gelb M.H., Sigler P.B. Interfacial catalysis: the mechanism of phospholipase A2. Science 1990, 250:1541-1546.
38. Scott D.L., Achari A., Vidal J.C., Sigler P.B. Crystallographic and biochemical studies of the (inactive) Lys49 phospholipase A2 from the venom of Agkistrodon piscivorus piscivorus. J. Biol. Chem. 1992, 267:22645-22657.
39. da Silva Giotto M.T., Garratt R.C., Oliva G., Mascarenhas Y.P., Giglio J.R., Cintra A.C.O., de Azevedo W.F., Arni R.K., Ward R.J. Crystallographic and spectroscopic characterization of a molecular hinge: conformational changes in bothropstoxin I, a dimeric Lys49 phospholipase A2 homologue. Proteins-Struct. Funct. Bioinform. 1998, 30:442-454.
40. Soares A.M., Guerra-Sa R., Borja-Oliveira C.R., Rodrigues V.M., Rodrigues-Simioni L., Rodrigues V., Fontes M.R.M., Lomonte B., Gutierrez J.M., Giglio J.R. Structural and functional characterization of BnSP-7, a Lys49 myotoxic phospholipase A(2) homologue from Bothrops neuwiedi pauloensis venom. Arch. Biochem. Biophys. 2000, 378:201-209.
41. Steiner R.A., Rozeboom H.K., de Vrires A., Kalk K.H., Murshudov G.N., Wilson K.S., Dijkstra B.W. X-ray structure of bovine pancreatic phospholipase A2 at atomic resolution. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:516-526.
42. Tsuboi K., Sugimoto Y., Ichikawa A. Prostanoid receptor subtypes. Prostaglandins Other Lipid Mediat. 2002, 68-69:535-556.
43. Wallace A.C., Laskowski R.A., Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 1995, 8:127-134.
44. Wang X.Q., Yang J., Gui L.L., Lin Z.J., Chen Y.C., Zhou Y.C. Crystal structure of an acidic phospholipase A2 from the venom of Agkistrodon halys pallas at 2.0 Å resolution. J. Mol. Biol. 1996, 255:669-676.
45. Ward R.J., Chioato L., de Oliveira A.H.C., Ruller R., Sa J.M. Active-site mutagenesis of a Lys(49)-phospholipase A2: biological and membrane-disrupting activities in the absence of catalysis. Biochem. J. 2002, 362:89-96.
46. Watanabe L., Soares A.M., Ward R.J., Fontes M.R.M., Arni R.K. Structural insights for fatty acid binding in a Lys49-phospholipase A2: crystal structure of myotoxin II from Bothrops moojeni complexed with stearic acid. Biochimie 2005, 87:161-167.
47. Yu B.Z., Berg O.G., Jain M.K. The divalent cation is obligatory for the binding of ligands to the catalytic site of secreted phospholipase A2. Biochemistry 1993, 32:6485-6492.
48. Yu B.Z., Rogers J., Nicol G.R., Theopold K.H., Seshadri K., Vishweshwara S., Jain M.K. Catalytic significance of the specificity of divalent cations as KS* and kcat* cofactors for secreted phospholipase A2. Biochemistry 1998, 37:12576-12587.
49. Zhou X., Tan T.C., Valiyaveettil S., Go M.L., Kini R.M., Velazquez-Campoy A., Sivaraman J. Structural characterization of myotoxic ecarpholin S from Echis carinatus venom. Biophys. J. 2008, 95:3366-3380.