Crystal structure of crotoxin reveals key residues involved in the stability and toxicity of this potent heterodimeric β-neurotoxin

Journal of Molecular Biology

Volumn 412, Issue 2, 2011, Pages 176-191

  Faure, Grazyna ^a,b   Xu, Haijin ^a   Saul, Frederick A ^a  

^a INSTITUT PASTEUR   (France)

^b Département de Biologie Structurale et Chimie   (France)

Author keywords

crotoxin; crystal structure; heterodimer interface; snake venom neurotoxin

Indexed keywords

AMINO ACID; CROTOXIN; NEUROTOXIN; PHOSPHOLIPASE A2; POLYPEPTIDE;

ALPHA CHAIN; ARTICLE; BETA CHAIN; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN STABILITY; SNAKE; TOXICITY;

CROTALUS DURISSUS TERRIFICUS;

EID: 80052029834     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.07.027     Document Type: Article

References (62)

1. Slotta K.H., and Fraenkel-Conrat H. Schlangengifte III: Mitteilung: Reinigung und Krystallisation des Klapperschlangen-Giftes Ber. Dtsch. Chem. Ges. 71 1938 1076 1081
2. 2 crotapotin complex isolated from the venom of the South American rattlesnake Br. J. Pharmacol. 61 1977 597 606 (Pubitemid 8233442)
3. Hendon R.A., and Fraenkel-Conrat H. Biological role of the two components of crotoxin Proc. Natl Acad. Sci. USA 68 1971 1560 1563
4. 2-like precursor Biochem. Biophys. Acta 1088 1991 401 408
5. 2 neurotoxin from Crotalus durissus terrificus: venom, results from post-translational modifications Biochemistry 30 1991 8074 8083
6. Jeng T., Hendon R.A., and Fraenkel-Conrat H. Search for relationships among the haemolytic, phospholipolytic and neurotoxic activities of snake venoms Proc. Natl Acad. Sci. USA 75 1987 600 604
7. Bon C., Changeux J.P., Jeng T.W., and Fraenkel-Conrat H. Postsynaptic effects of crotoxin and its isolated subunits Eur. J. Biochem. 99 1979 471 481
8. 2 FEBS Lett. 445 1999 440 444
9. 2 neurotoxins on Torpedo synaptosomes Biochemistry 32 1993 10708 10713
10. Faure G., Copic A., Le Porrier S., Gubensek F., Bon C., and Krizaj I. Crotoxin acceptor protein isolated from Torpedo electric organ: binding properties to crotoxin by surface plasmon resonance Toxicon 41 2003 509 517 (Pubitemid 36351319)
11. 2 F. Goudey-Perrière, C. Bon, S. Puiseux-Dao, M. Sauviat, Toxines et recherches biomédicales. SFET collection, "Rencontres en toxinologie" 2002 Elsevier Paris, France 305 313
12. 2 from Viperidae snake venom by affinity binding studies and molecular bioinformatics BMC Struct. Biol. 7 2007 82
13. Gopalakrishnakone P., and Hawgood B.J. Morphological changes induced by crotoxin in murine nerve and neuromuscular junction Toxicon 22 1984 791 804 (Pubitemid 14024682)
14. Mebs D., and Ownby C.L. Myotoxic components of snake venom: their biochemical and biological activities Pharmacol. Ther. 48 1990 223 236
15. 2 homologue Toxicon 51 2008 80 92
16. Costa L.A., Miles H., Araujo C.E., Gonzales S., and Villarrubia V.G. Tumor regression of advanced carcinomas following intra- and/or peri-tumoral inoculation with VRCTC-310 in humans: preliminary report of two cases Immunopharmacol. Immunotoxicol. 20 1998 15 25 (Pubitemid 28157288)
17. 2 toxin: a novel growth inhibitory mechanism Biochem. Pharmacol. 51 1996 1535 1543
18. Rudd C.J., Visckatis L.J., Vidal J.C., and Etcheverry M.A. In vitro comparison of cytotoxic effects of crotoxin against three human tumors and a normal human epidermal keratinocyte cell line Invest. New Drugs 12 1994 183 184 (Pubitemid 24376402)
19. Yan C.H., Yang Y.P., Qin Z.H., Gu Z.L., Reid P., and Liang Z.Q. Autophagy is involved in cytotoxic effects of crotoxin in human breast cancer cell line MCF-7 cells Acta Pharmacol. Sin. 28 2007 540 548 (Pubitemid 46496084)
20. 2 NSC-624 244) in patients with advanced cancer Clin. Cancer Res. 8 2002 1033 1041 (Pubitemid 35177352)
21. 2 isolated from Crotalus durissus terrificus venom on macrophage function Toxicon 45 2005 671 676 (Pubitemid 40381027)
22. Zambelli V.O., Sampaio S.C., Sudo-Hayashi L.S., Greco K., Britto L.R.G., and Alves A.S. Crotoxin alters lymphocyte distribution in rats: involvement of adhesion molecules and lipoxygenase-derived mediators Toxicon 51 2008 1357 1367
23. Sampaio S.C., Hyslop S., Fontes M.R., Prado-Franceschi J., Zambelli V.O., and Magro A.J. Crotoxin: novel activities for a classic beta-neurotoxin Toxicon 55 2010 1045 1060
24. Zhang H.L., Han R., Chen Z.X., Chen B.W., Gu Z.L., and Reid P.F. Opiate and acetylcholine-independent analgesic actions of crotoxin isolated from Crotalus durissus terrificus venom Toxicon 48 2006 175 182 (Pubitemid 44093678)
25. Gutierrez V.P., Konno K., Chacur M., Sampaio C., Picolo G., and Brigatte P. Crotalphine induces potent antinociception in neuropathic pain by acting at peripheral opioid receptors Eur. J. Pharmacol. 594 2008 84 92
26. Faure G., and Bon C. Several isoforms of crotoxin are present in individual venoms from the South American rattlesnake, Crotalus durissus terrificus Toxicon 25 1987 229 234 (Pubitemid 17025096)
27. 2 neurotoxin from the South American rattlesnake Crotalus durissus terrificus Biochemistry 27 1988 730 738
28. Faure G., Harvey A.L., Thomson E., Saliou B., Radvanyi F., and Bon C. Comparison of crotoxin isoforms reveals the stability of the complex plays a major role in its pharmacological action Eur. J. Biochem. 214 1993 491 496 (Pubitemid 23173800)
29. Faure G., Choumet V., Bouchier C., Camoin L., Guillaume J.L., and Monegier B. The origin of the diversity of crotoxin isoforms in the venom of Crotalus durissus terrificus Eur. J. Biochem. 223 1994 161 164 (Pubitemid 24221658)
30. Krizaj I., Faure G., Gubensek F., and Bon C. Re-examination of crotoxin-membrane interactions Toxicon 34 1996 1003 1009 (Pubitemid 26320010)
31. 2 ammodytoxin and crotoxin bind to distinct high-affinity protein acceptors in Torpedo marmorata electric organ Biochemistry 36 1997 2779 2787 (Pubitemid 27138559)
32. Hendon R.A., and Tu A.T. The role of crotoxin subunits in tropical rattlesnake neurotoxic action Biochim. Biophys. Acta 578 1979 243 252 (Pubitemid 9181445)
33. Radvanyi F., and Bon C. Catalytic activity and reactivity with p-bromophenacyl bromide of the phospholipase subunit of crotoxin; influence of dimerization and association with the noncatalytic subunit J. Biol. Chem. 257 1982 12616 12632
34. Hawgood B., and Bon C. Snake venom presynaptic toxins A.T. Tu, Handbook of Natural Toxins, Reptile and Amphibian Venoms 1991 Marcel Dekker New York, NY 3 52
35. Bieber A., Bon C., and Faure G. Rattlesnake venom neurotoxins: crotoxin related proteins R. Rappuoli, C. Montecucco, Guidebook to Protein Toxins and Their Use in Cell Biology 1997 Oxford University Press Oxford, UK 221 224
36. 2 formed by two isoforms of crotoxin B from Crotalus durissus terrificus venom Proteins 72 2008 883 891 (Pubitemid 352000866)
37. Achari A., Radvanyi F.R., Scott D., Bon C., and Sigler P.B. Crystals of crotoxin suitable for high resolution X-ray diffraction analysis J. Biol. Chem. 260 1985 9385 9387 (Pubitemid 16238323)
38. 2 Acta Crystallogr., Sect. F 63 2007 287 290
39. 3, subunit of crotoxin Toxicon 31 1993 530
40. Perbandt M., Tsai I.H., Fuchs A., Banumathi S., Rajashankar K.R., and Georgieva D. Structure of hetero dimeric neurotoxic complex viperotoxin F (RV-4/RV-7) from the venom of Vipera russelli formosensis at 1.9 Å resolution Acta Crystallogr., Sect. D: Biol. Crystallogr. 59 2003 1679 1687 (Pubitemid 37245120)
41. Perband M., Wilson J.C., Eschenburg S., Mancheva I., Aleksiev B., and Genov N. Crystal structure of vipoxin at 2.0 Å: an example of regulation of a toxic function generated by molecular evolution FEBS Lett. 412 1997 573 577 (Pubitemid 27337112)
42. Krissinel E., and Henrick K. Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
43. Lawrence M.C., and Colman P.M. Shape complementarity at protein/protein interfaces J. Mol. Biol. 234 1993 946 950 (Pubitemid 24027225)
44. 2 from bovine pancreas and Crotalus atrox venom J. Biol. Chem. 260 1985 11627 11634 (Pubitemid 16250819)
45. 2 from Vipera ammodytes which differ in neurotoxicity and anticoagulant activity J. Struct. Biol. 169 2010 360 369
46. 2 at 2.2 Å resolution Nature 352 1991 79 82 (Pubitemid 21896703)
47. Mascarenhas Y.P., Stouten P.F., Beltran J.R., Laure C.J., and Vriend G. Structure-function relationship for the highly toxic crotoxin from Crotalus durissus terrificus Eur. Biophys. J. 21 1992 199 205
48. 2 in a complex with a transition-state analogue Science 250 1990 1560 1563 (Pubitemid 120034366)
49. 2 Biochemistry 36 1997 14325 14333 (Pubitemid 27509924)
50. 2s Biochim. Biophys. Acta 1761 2006 1260 1269 (Pubitemid 44738707)
51. 2 with the crotoxin inhibitor from Crotalus serum Eur. J. Biochem. 267 2000 4799 4808 (Pubitemid 30619471)
52. 2 Biochimie 82 2000 833 840
53. Fortes-Dias C.L., Santos R.M., Magro A.J., Fontes M.R., Chávez-Olórtegui C., and Granier C. Identification of continuous interaction sites in PLA(2)-based protein complexes by peptide arrays Biochimie 91 2009 1482 1492
54. 2 (PLI) du sang de serpent. Homologie structurale avec des protéines de la réponse immunitaire innée (Chapitre 2) G. Mion, S. Larréché, Goyffon Aspects cliniques et thérapeutiques des envenimations graves 2010 Urgence Pratique Editions Grenges, France
55. Kabsch W. Integration, scaling, space-group assignment and post-refinement Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 133 144
56. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., and Evans P.R. Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D: Biol. Crystallogr. 67 2011 235 242
57. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
58. Matthews B.W. Solvent content of protein crystals J. Mol. Biol. 33 1968 491 497
59. Vaguine A.A., Richelle J., and Wodak S.J. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 1999 191 205 (Pubitemid 29053816)
60. Pannu N.S., Murshudov G.N., Dodson E.J., and Read R.J. Incorporation of prior phase information strengthens maximum-likelihood structure refinement Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 1998 1285 1294
61. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
62. DeLano W.L. The PyMOL Molecular Graphic System 2002 Delano Scientific LLC San Carlos, CA Available at http://www.pymol.org