Phospholipase A2 isolated from the venom of Crotalus durissus terrificus inactivates dengue virus and other enveloped viruses by disrupting the viral envelope

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Muller, Vanessa Danielle ^a,b   Soares, Ricardo Oliveira ^a   Santos Junior, Nilton Nascimento Dos ^a   Trabuco, Ama Cristina ^a   Cintra, Adelia Cristina ^a   Figueiredo, Luiz Tadeu ^a   Caliri, Antonio ^a   Sampaio, Suely Vilela ^a   Aquino, Victor Hugo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF ALAGOAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CROTOXIN; GENOMIC RNA; GLYCEROPHOSPHOLIPID; PHOSPHOLIPASE A2 CROTOXIN B; UNCLASSIFIED DRUG; LIPID BILAYER; PHOSPHOLIPASE A2; SNAKE VENOM;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL DISRUPTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; COXSACKIE VIRUS B; CROTALUS; CROTALUS DURISSUS; DENGUE VIRUS; DRUG STRUCTURE; LIPID BILAYER; MAYARO VIRUS; NONHUMAN; OROPOUCHE VIRUS; ROCIO VIRUS; VIRUS; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS INACTIVATION; ANIMAL; CHLOROCEBUS AETHIOPS; DRUG EFFECTS; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; VERO CELL LINE; VIRION;

CROTALUS DURISSUS TERRIFICUS; DENGUE VIRUS;

ANIMALS; ANTIVIRAL AGENTS; CERCOPITHECUS AETHIOPS; CROTALID VENOMS; CROTALUS; DENGUE VIRUS; LIPID BILAYERS; PHOSPHOLIPASES A2; VERO CELLS; VIRION; VIRUS INACTIVATION;

EID: 84911413300     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112351     Document Type: Article

References (83)

1. Wendt A, Adhoute X, Castellani P, Oules V, Ansaldi C, et al. (2014) Chronic hepatitis C: future treatment. Clin Pharmacol 6: 1-17.
2. Ray D, Shi PY (2006) Recent advances in flavivirus antiviral drug discovery and vaccine development. Recent Pat Antiinfect Drug Discov 1: 45-55.
3. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, et al. (2013) The global distribution and burden of dengue. Nature 496: 504-507.
4. Hales S, de Wet N, Maindonald J, Woodward A (2002) Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet 360: 830-834.
5. Kyle JL, Harris E (2008) Global spread and persistence of dengue. Annu Rev Microbiol 62: 71-92.
6. Letson GW, Singhasivanon P, Fernandez E, Abeysinghe N, Amador JJ, et al. (2010) Dengue vaccine trial guidelines and role of large-scale, post proof-ofconcept demonstration projects in bringing a dengue vaccine to use in dengue endemic areas. Hum Vaccin 6: 802-809.
7. Lim SP, Wang Q-Y, Noble CG, Chen Y-L, Dong H, et al. (2013) Ten years of dengue drug discovery: Progress and prospects. Antiviral Research 100: 500-519.
8. th ed.Philadelphia: Lippincot Williams & Wilkins. pp. 1101-1151.
9. KING H (1948) Curare alkaloids; constitution of dextro-tubocurarine chloride. J Chem Soc 174: 265.
10. Ganesan A (2008) The impact of natural products upon modern drug discovery. Curr Opin Chem Biol 12: 306-317.
11. Butler MS (2005) Natural products to drugs: natural product derived compounds in clinical trials. Nat Prod Rep 22: 162-195.
12. Butler MS (2008) Natural products to drugs: natural product-derived compounds in clinical trials. Nat Prod Rep 25: 475-516.
13. Bailey P, Wilce J (2001) Venom as a source of useful biologically active molecules. Emerg Med (Fremantle) 13: 28-36.
14. Ferreira SH, Bartelt DC, Greene LJ (1970) Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 9: 2583-2593.
15. Ondetti MA, Williams NJ, Sabo EF, Pluscec J, Weaver ER, et al. (1971) Angiotensin-converting enzyme inhibitors from the venom of Bothrops jararaca. Isolation, elucidation of structure, and synthesis. Biochemistry 10: 4033-4039.
16. Scarborough RM, Rose JW, Hsu MA, Phillips DR, Fried VA, et al. (1991) Barbourin. A GPIIb-IIIa-specific integrin antagonist from the venom of Sistrurus m. barbouri. J Biol Chem 266: 9359-9362.
17. Egbertson MS, Chang CT, Duggan ME, Gould RJ, Halczenko W, et al. (1994) Non-peptide fibrinogen receptor antagonists. 2. Optimization of a tyrosine template as a mimic for Arg-Gly-Asp. J Med Chem 37: 2537-2551.
18. Petricevich VL, Mendonça RZ (2003) Inhibitory potential of Crotalus durissus terrificus venom on measles virus growth. Toxicon 42: 143-153.
19. Borkow G, Ovadia M (1999) Selective lysis of virus-infected cells by cobra snake cytotoxins: A sendai virus, human erythrocytes, and cytotoxin model. Biochem Biophys Res Commun 264: 63-68.
20. Zhang XG, Mason PW, Dubovi EJ, Xu X, Bourne N, et al. (2009) Antiviral activity of geneticin against dengue virus. Antiviral Res 83: 21-27.
21. 2 from Crotalus durissus terrificus showed antiviral activity against dengue and yellow fever viruses. Toxicon 59: 507-515.
22. Fenard D, Lambeau G, Valentin E, Lefebvre JC, Lazdunski M, et al. (1999) Secreted phospholipases A(2), a new class of HIV inhibitors that block virus entry into host cells. J Clin Invest 104: 611-618.
23. J.E. Fletcher AHSS, C.L Ownby (1997) Molecular events in the myotoxic action of phospholipases. In: Kini RM, editor. Venom phospholipase A2 enzymes: structure, function, and mechanism. Chichester; New York: John Wiley. pp. xii, 511 p.
24. Furukawa Y, Matsunaga Y, Hayashi K (1976) Purification and Characterization of a Coagulant Protein from Venom of Russells Viper. Biochimica Et Biophysica Acta 453: 48-61.
25. Huang HC, Lee CY (1984) Isolation and Pharmacological Properties of Phospholipases A2 from Vipera-Russelli (Russell Viper) Snake-Venom. Toxicon 22: 207-217.
26. Vishwanath BS, Kini RM, Gowda TV (1988) Purification and Partial Biochemical-Characterization of an Edema Inducing Phospholipase-A2 from Vipera-Russelli (Russells Viper) Snake-Venom. Toxicon 26: 713-720.
27. Thwin MM, Gopalakrishnakone P, Yuen R, Tan CH (1995) A Major Lethal Factor of the Venom of Burmese Russells Viper (Daboia-Russelli-Siamensis) - Isolation, N-Terminal Sequencing and Biological-Activities of Daboiatoxin. Toxicon 33: 63-76.
28. Mukherjee AK, Ghosal SK, Maity CR (1997) Lysosomal membrane stabilization by alpha-tocopherol against the damaging action of Vipera russelli venom phospholipase A(2). Cellular and Molecular Life Sciences 53: 152-155.
29. Fenard D, Lambeau G, Maurin T, Lefebvre JC, Doglio A (2001) A peptide derived from bee venom-secreted phospholipase A2 inhibits replication of T-cell tropic HIV-1 strains via interaction with the CXCR4 chemokine receptor. Mol Pharmacol 60: 341-347.
30. Kim JO, Chakrabarti BK, Guha-Niyogi A, Louder MK, Mascola JR, et al. (2007) Lysis of human immunodeficiency virus type 1 by a specific secreted human phospholipase A2. J Virol 81: 1444-1450.
31. Mitsuishi M, Masuda S, Kudo I, Murakami M (2006) Group V and X secretory phospholipase A2 prevents adenoviral infection in mammalian cells. Biochem J 393: 97-106.
32. Kohn A, Klibansky C (1967) Studies on the inactivation of cell-fusing property of Newcastle disease virus by phospholipase A. Virology 31: 385-388.
33. DRAYTON HA (1961) Inactivation of Rous virus by phospholipase A. Nature 192: 896.
34. Yasumura Y, Kawakita Y (1963) Studies on SV40 in tissue culture-preliminary step for cancer research in vitro. Nihon rinsho 21: 15.
35. Igarashi A (1978) Isolation of a Singh's Aedes albopictus cell clone sensitive to Dengue and Chikungunya viruses. J Gen Virol 40: 531-544.
36. Dos Santos HW, Poloni TR, Souza KP, Muller VD, Tremeschin F, et al. (2008) A simple one-step real-time RT-PCR for diagnosis of dengue virus infection. J Med Virol 80: 1426-1433.
37. Aquino VH, Anatriello E, Goncalves PF, da Silva EV, Vasconcelos PFC, et al. (2006) Molecular epidemiology of dengue type 3 virus in Brazil and Paraguay, 2002-2004. American Journal of Tropical Medicine and Hygiene 75: 710-715.
38. Kaptein SJ, De Burghgraeve T, Froeyen M, Pastorino B, Alen MM, et al. (2010) A derivate of the antibiotic doxorubicin is a selective inhibitor of dengue and yellow fever virus replication in vitro. Antimicrob Agents Chemother 54: 5269-5280.
39. Bernstein FC, Koetzle TF, Williams GJ, Meyer EF, Brice MD, et al. (1977) The Protein Data Bank. A computer-based archival file for macromolecular structures. Eur J Biochem 80: 319-324.
40. Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, et al. (2013) Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci U S A 110: 6795-6799.
41. Modis Y, Ogata S, Clements D, Harrison SC (2003) A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci U S A 100: 6986-6991.
42. Jo S, Kim T, Iyer VG, Im W (2008) CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem 29: 1859-1865.
43. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J Chem Theory Comput 4: 435-447.
44. Zhang Q, Hunke C, Yau YH, Seow V, Lee S, et al. (2012) The stem region of premembrane protein plays an important role in the virus surface protein rearrangement during dengue maturation. J Biol Chem 287: 40525-40534.
45. Marchi-Salvador DP, Corrêa LC, Magro AJ, Oliveira CZ, Soares AM, et al. (2008) 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 72: 883-891.
46. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 27-38.
47. Delano W (2002) The PyMOL Molecular Graphics System. In: LLC DS, editor. San Carlos, CA, USA.
48. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926.
49. Miyamoto S, Kollman PA (1992) Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. Journal of Computational Chemistry 13: 952-962.
50. Klauda JB, Venable RM, Freites JA, O'Connor JW, Tobias DJ, et al. (2010) Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J Phys Chem B 114: 7830-7843.
51. Piggot TJ, Piñ eiro Á, Khalid S (2012) Molecular Dynamics Simulations of Phosphatidylcholine Membranes: A Comparative Force Field Study. J Chem Theory Comput 8: 4593-4609.
52. Nozaki Y, Tanford C (1967) Examination of titration behavior. In: CHW H, editor.Methods in Enzymology. 11 ed.New York: Academic Press. pp. 715-734.
53. Parrinello M, Rahman A (1980) Crystal Structure and Pair Potentials: A Molecular-Dynamics Study. Phys Rev Lett 45: 1196-1199.
54. Nosé S (1984) A unified formulation of the constant temperature molecular dynamics methods. J Chem Phys 81: 511-519.
55. Hoover WG (1985) Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A 31: 1695-1697.
56. Hess B (2008) P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation. J Chem Theory Comput 4: 116-122.
57. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
58. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32: W665-667.
59. Li H, Robertson AD, Jensen JH (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins 61: 704-721.
60. Soares RO, Caliri A (2013) Stereochemical features of the envelope protein Domain III of dengue virus reveals putative antigenic site in the five-fold symmetry axis. Biochim Biophys Acta 1834: 221-230.
61. Pan YH, Epstein TM, Jain MK, Bahnson BJ (2001) Five coplanar anion binding sites on one face of phospholipase A2: relationship to interface binding. Biochemistry 40: 609-617.
62. Hendon RA, Fraenkel-Conrat H (1971) Biological roles of the two components of crotoxin. Proc Natl Acad Sci U S A 68: 1560-1563.
63. Samy RP, Gopalakrishnakone P, Stiles BG, Girish KS, Swamy SN, et al. (2012) Snake venom phospholipases A(2): a novel tool against bacterial diseases. Curr Med Chem 19: 6150-6162.
64. Ward RJ, de Azevedo WF, Arni RK (1998) At the interface: crystal structures of phospholipases A2. Toxicon 36: 1623-1633.
65. de Paula RC, Castro HC, Rodrigues CR, Melo PA, Fuly AL (2009) Structural and pharmacological features of phospholipases A2 from snake venoms. Protein Pept Lett 16: 899-907.
66. Kini RM (2003) Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42: 827-840.
67. 2 crotoxin B isolated from the venom of Crotalus durissus terrificus exert antiviral effect against Dengue virus and Yellow fever virus through its catalytic activity. J Virol Antivir Res 3: 1.
68. Jain MK, Ranadive G, Yu BZ, Verheij HM (1991) Interfacial catalysis by phospholipase A2: monomeric enzyme is fully catalytically active at the bilayer interface. Biochemistry 30: 7330-7340.
69. Faure G, Harvey AL, Thomson E, Saliou B, Radvanyi F, et al. (1993) Comparison of crotoxin isoforms reveals that stability of the complex plays a major role in its pharmacological action. Eur J Biochem 214: 491-496.
70. Burke JE, Dennis EA (2009) Phospholipase A2 structure/function, mechanism, and signaling. J Lipid Res 50 Suppl: S237-242.
71. Lee CH, Bell JD, Zimmerman SS (1997) A binding study of phospholipase A2 with lecithin, lysolecithin and their tetrahedral intermediates using molecular modeling. J Pept Res 50: 25-33.
72. van Deenen L, de Haas G, Heemskerk CH (1963) Hydrolysis of synthetic mixedacid phosphatides by phospholipase A from human pancreas. Biochim Biophys Acta 67: 295-304.
73. Tsai IH, Liu HC, Chang T (1987) Toxicity domain in presynaptically toxic phospholipase A2 of snake venom. Biochim Biophys Acta 916: 94-99.
74. Nakashima K, Nobuhisa I, Deshimaru M, Nakai M, Ogawa T, et al. (1995) Accelerated evolution in the protein-coding regions is universal in crotalinae snake venom gland phospholipase A2 isozyme genes. Proc Natl Acad Sci U S A 92: 5605-5609.
75. Ahyayauch H, Villar AV, Alonso A, Goñ i FM (2005) Modulation of PI-specific phospholipase C by membrane curvature and molecular order. Biochemistry 44: 11592-11600.
76. Berg OG, Yu BZ, Rogers J, Jain MK (1991) Interfacial catalysis by phospholipase A2: determination of the interfacial kinetic rate constants. Biochemistry 30: 7283-7297.
77. Kensil CR, Dennis EA (1985) Action of cobra venom phospholipase A2 on large unilamellar vesicles: comparison with small unilamellar vesicles and multibilayers. Lipids 20: 80-83.
78. Yeagle PL (2011) The Structure of Biological Membranes. Boca Raton, USA: CRC Press.
79. Grainger DW, Reichert A, Ringsdorf H, Salesse C (1990) Hydrolytic action of phospholipase A2 in monolayers in the phase transition region: direct observation of enzyme domain formation using fluorescence microscopy. Biochim Biophys Acta 1023: 365-379.
80. Grandbois M, Clausen-Schaumann H, Gaub H (1998) Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A2. Biophys J 74: 2398-2404.
81. Wilschut JC, Regts J, Scherphof G (1979) Action of phospholipase A2 on phospholipid vesicles. Preservation of the membrane permeability barrier during asymmetric bilayer degradation. FEBS Lett 98: 181-186.
82. Davidsen J, Mouritsen OG, Jørgensen K (2002) Synergistic permeability enhancing effect of lysophospholipids and fatty acids on lipid membranes. Biochim Biophys Acta 1564: 256-262.
83. Jain MK, De Haas GH (1983) Activation of phospholipase A2 by freshly added lysophospholipids. Biochim Biophys Acta 736: 157-162.