Isolation, enzymatic characterization and antiedematogenic activity of the first reported rattlesnake hyaluronidase from Crotalus durissus terrificus venom

Biochimie

Volumn 94, Issue 12, 2012, Pages 2740-2748

  Bordon, Karla C F ^a   Perino, Márcio G ^a   Giglio, José R ^a   Arantes, Eliane C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antiedematogenic activity; Crotalus durissus terrificus; Hyaluronidase; Kinetic studies

Indexed keywords

AMINO ACID; CALCIUM ION; CHONDROITIN 4 SULFATE; CHONDROITIN 6 SULFATE; CROTOXIN; DERMATAN; HYALURONIC ACID; HYALURONIDASE; MAGNESIUM ION; PHOSPHOLIPASE A2; SNAKE VENOM; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIEDEMATOGENIC ACTIVITY; CATION EXCHANGE; CHROMATOGRAPHY; CONTROLLED STUDY; CROTALUS; DEGRADATION; DIFFUSION; DRUG ACTIVITY; ENZYME ACTIVITY; ENZYME PURIFICATION; GEL FILTRATION; HYDROPHOBIC CHROMATOGRAPHY; ISOLATION PROCEDURE; MALE; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE PHASE FAST PROTEIN LIQUID CHROMATOGRAPHY; REVERSED PHASE LIQUID CHROMATOGRAPHY; REVIEW; TURBIDITY;

EID: 84868206952     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.08.014     Document Type: Article

References (69)

1. J. Boldrini-França, C. Correa-Netto, M.M.S. Silva, R.S. Rodrigues, P. De La Torre, A. Perez, A.M. Soares, R.B. Zingali, R.A. Nogueira, V.M. Rodrigues, L. Sanz, and J.J. Calvete Snake venomics and antivenomics of Crotalus durissus subspecies from Brazil: assessment of geographic variation and its implication on snakebite management J. Proteomics 73 2010 1758 1776
2. M.M. Azevedo-Marques, P. Cupo, T.M. Coimbra, S.E. Hering, M.A. Rossi, and C.J. Laure Myonecrosis, myoglobinuria and acute renal-failure induced by south-american rattlesnake (Crotalus durissus terrificus) envenomation in Brazil Toxicon 23 1985 631 636 (Pubitemid 15020880)
3. R. Frezzatti, and P.F. Silveira Allopurinol reduces the lethality associated with acute renal failure induced by Crotalus durissus terrificus snake venom: comparison with probenecid Plos Negl. Trop. Dis. 5 2011
4. K.S. Girish, R. Shashidharamurthy, S. Nagaraju, T.V. Gowda, and K. Kemparaju Isolation and characterization of hyaluronidase a "spreading factor" from Indian cobra (Naja naja) venom Biochimie 86 2004 193 202 (Pubitemid 38591508)
5. D.A. Warrell Clinical toxicology of snakebite in Africa and the Middle East/Arabian Peninsula J. Meier, J. White, Handbook of Clinical Toxicology of Animal Venoms and Poisons 1995 CRC Press Boca Raton 433 492
6. J. Maria Gutierrez, A. Rucavado, T. Escalante, B. Lomonte, Y. Angulo, and J.W. Fox Tissue pathology induced by snake venoms: how to understand a complex pattern of alterations from a systems biology perspective? Toxicon 55 2010 166 170
7. S. Iwanaga, and T. Suzuki Enzymes in snake venom C.Y. LEE, Snake Venoms 1979 Springer-Verlag 99
8. A.T. Tu, and R.R. Hendon Characterization of lizard venom hyaluronidase and evidence for its action as a spreading factor Comp. Biochem. Physiol. 76B 1983 377 383
9. S. Yingprasertchai, S. Bunyasrisawat, and K. Ratanabanangkoon Hyaluronidase inhibitors (sodium cromoglycate and sodium auro-thiomalate) reduce the local tissue damage and prolong the survival time of mice injected with Naja kaouthia and Calloselasma rhodostoma venoms Toxicon 42 2003 635 646 (Pubitemid 37346231)
10. X. Xu, X. Wang, X. Xi, J. Liu, J. Huang, and Z. Lu Purification and partial characterization of hyaluronidase from five pace snake (Agkistrodon acutus) venom Toxicon 20 1982 973 981 (Pubitemid 13189873)
11. S. Pukrittayakamee, D. Warrell, V. Desakorn, A. McMichael, N. White, and D. Bunnag The hyaluronidase activities of some Southeast Asian snake venoms Toxicon 26 1988 629 637
12. R.A. Harrison, F. Ibison, D. Wilbraham, and S.C. Wagstaff Identification of cDNAs encoding viper venom hyaluronidases: cross-generic sequence conservation of full-length and unusually short variant transcripts Gene 392 2007 22 33 (Pubitemid 46482833)
13. K. Kudo, and A.T. Tu Characterization of hyaluronidase isolated from Agkistrodon contortrix contortrix (southern copperhead) venom Arch. Biochem. Biophys. 386 2001 154 162 (Pubitemid 32989304)
14. N.H. Tan, and G. Ponnudurai A comparative-study of the biological-activities of rattlesnake (genera Crotalus and Sistrurus) venoms Comp. Biochem. Physiol. Part C Pharmacol. Toxicol. Endocrinol. 98 1991 455 461
15. K.S. Girish, H. Mohanakumari, S. Nagaraju, B. Vishwanath, and K. Kemparaju Hyaluronidase and protease activities from Indian snake venoms: neutralization by Mimosa pudica root extract Fitoterapia 75 2004 378 380 (Pubitemid 38670572)
16. K.S. Girish, and K. Kemparaju Inhibition of Naja naja venom hyaluronidase by plant-derived bioactive components and polysaccharides Biochemistry (Mosc) 70 2005 948 952 (Pubitemid 41274506)
17. K.S. Girish, and K. Kemparaju Inhibition of Naja naja venom hyaluronidase: role in the management of poisonous bite Life Sci. 78 2006 1433 1440 (Pubitemid 43233810)
18. K.S. Girish, K. Kemparaju, S. Nagaraju, and B.S. Vishwanath Hyaluronidase inhibitors: a biological and therapeutic perspective Curr. Med. Chem. 16 2009 2261 2288
19. K.S. Girish, and K. Kemparaju Overlooked issues of snakebite management: time for strategic approach Curr. Top. Med. Chem. 11 2011 2494 2508
20. C.R. DeVries, A.K. Miller, and M.G. Packer Reduction of paraphimosis with hyaluronidase Urology 48 1996 464 465 (Pubitemid 26317491)
21. K.H. Venkatesk, and G.S.U. Rao Treatment of supraglottic airway edema by local hyaluronidase Anesthesiology 106 2007 1254 1255 (Pubitemid 46828196)
22. G. Javey, S.G. Schwartz, and H.W. Flynn Jr. Emerging pharmacotherapies for diabetic macular edema Exp. Diabetes Res. 2012 548732
23. B. McGuire, A.E. Brannigan, and P.R. O'Connell Hyaluronidase assisted reduction of intestinal intussusception; a novel application Ir. Med. J. 98 2005 146 147 (Pubitemid 40916451)
24. C. Johnsson, R. Hallgren, A. Elvin, B. Gerdin, and G. Tufveson Hyaluronidase ameliorates rejection-induced edema Transpl. Int. 12 1999 235 243 (Pubitemid 29423660)
25. D. Zhong, Q. Meng, J. Li, Y. Wang, X. Zhang, S. Wang, and H. Zhu A hyaluronidase from the snake venom of Agkistrodon blomhoffii ussurensis of Changbai Mountain: isolation and characterization Int. J. Biol. 2 2010 171 180
26. Y.H. Mahadeswaraswamy, B. Manjula, S. Devaraja, K.S. Girish, and K. Kemparaju Daboia russelli venom hyaluronidase: purification, characterization and inhibition by beta-3-(3-hydroxy-4-oxopyridyl) alpha-amino-propionic acid Curr. Top. Med. Chem. 11 2011 2556 2565
27. 2 Toxicon 42 2003 947 962 (Pubitemid 38201494)
28. 2) isolated from Crotalus durissus collilineatus venom Toxicon 53 2009 417 426
29. A.C. Pessini, T.T. Takao, E.C. Cavalheiro, W. Vichnewski, S.V. Sampaio, J.R. Giglio, and E.C. Arantes A hyaluronidase from Tityus serrulatus scorpion venom: isolation, characterization and inhibition by flavonoids Toxicon 39 2001 1495 1504 (Pubitemid 32722036)
30. C.H. Poh, R. Yuen, M.C.M. Chung, and H.E. Khoo Purification and partial characterization of hyaluronidase from Stone fish (Synanceja horrida) venom Comp. Biochem. Physiol. (B) 101 1992 159 163
31. M.M. Bradford Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding Anal. Biochem. 72 1976 248 254
32. R.K. Scopes Measurement of protein by spectrophotometry at 205-nm Anal. Biochem. 59 1974 277 282
33. M.A. Cevallos, C. Navarroduque, M. Varelajulia, and A.C. Alagon Molecular mass determination and assay of venom hyaluronidases by sodium dodecyl sulfate-poliacrylamide gel electrophoresis Toxicon 30 1992 925 930
34. U.K. Laemmli Cleavage of structural proteins during assembly of head of bacteriophage T4 Nature 227 1970 680 685
35. K.C. Doerner, and B.A. White Detection of glycoproteins separated by nondenaturing polyacrylamide-gel electrophoresis using the periodic acid-schiff stain Anal. Biochem. 187 1990 147 150 (Pubitemid 20157532)
36. P. Edman, and G. Begg A protein sequenator Eur. J. Biochem. 1 1967 80 91
37. F. Corpet Multiple sequence alignment with hierarchical-clustering Nucleic Acids Res. 16 1988 10881 10890
38. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308 (Pubitemid 29213756)
39. R. Stern, and M.J. Jedrzejas Hyaluronidases: their genomics, structures, and mechanisms of action Chem. Rev. 106 2006 818 839
40. M.R. Magalhães, N.J. da Silva, and C.J. Ulhoa A hyaluronidase from Potamotrygon motoro (freshwater stingrays) venom: isolation and characterization Toxicon 51 2008 1060 1067
41. M. Ramanaiah, P.R. Parthasarathy, and B. Venkaiah Isolation and characterization of hyaluronidase from scorpion (Heterometrus fulvipes) venom Biochem. Int. 20 1990 301 310 (Pubitemid 20071954)
42. F. Costal-Oliveira, R. Machado de Avila, M.M. Melo, K.C.F. Bordon, E.C. Arantes, N.C. Paredes, B. Tintaya, C. Bonilla, R.E. Bonilla, W.S. Suarez, A. Yarleque, J.M. Fernandez, E. Kalapothakis, and C. Chávez-Olórtegui General biochemical and immunological characteristics of the venom from Peruvian scorpion Hadruroides lunatus Toxicon 60 2012 934 942
43. D.M. Kemeny, N. Dalton, A.J. Lawrence, F.L. Pearce, and C.A. Vernon The purification and characterization of hyaluronidase from the venom of the honey bee, Apis mellifera Eur. J. Biochem. 139 1984 217 223 (Pubitemid 14160994)
44. G.L. Frost, T. Csoka, and R. Stern The hyaluronidases: a chemical, biological and clinical overview Trends Glycosc. Glycotechnol. 8 1996 419 434
45. S.A. Mohamed Hyaluronidase isoforms from developing embryos of the camel tick Hyalomma dromedarii Comp. Biochem. Physiol. B Biochem. Mol. Biol. 142 2005 164 171 (Pubitemid 41262555)
46. N.K. Dutta, and K.G.A. Narayanan Release of histamine from rat diaphragm by cobra venom Nature 169 1952 1064 1065
47. A. Weisel-Eichler, and F. Libersat Venom effects on monoaminergic systems J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190 2004 683 690 (Pubitemid 40876353)
48. M. Metz, A.M. Piliponsky, C.C. Chen, V. Lammel, M. Abrink, G. Pejler, M. Tsai, and S.J. Galli Mast cells can enhance resistance to snake and honeybee venoms Science 313 2006 526 530 (Pubitemid 44148458)
49. M. Gautam, C.J. Benson, and K.A. Sluka Increased response of muscle sensory neurons to decreases in pH after muscle inflammation Neuroscience 170 2010 893 900
50. M.H. Schmid-Wendtner, and H.C. Korting The pH of the skin surface and its impact on the barrier function Skin Pharmacol. Physiol. 19 2006 296 302 (Pubitemid 44808083)
51. W.B. Elliott Chemistry and immunology of reptilian venoms C. Gans, K.A. Gans, Biology of the Reptilia Physiology B vol. 8 1978 Academic Press London 163 436
52. L.J. Zaneveld, K.L. Polakoski, and G.F. Schumacher Properties of acrosomal hyaluronidase from bull spermatozoa - evidence for its similarity to testicular hyaluronidase J. Biol. Chem. 248 1973 564 570
53. N.S. El-Safory, A.E. Fazary, and C.K. Lee Hyaluronidases, a group of glycosidases: current and future perspectives Carbohydr. Polym. 81 2010 165 181
54. S.D. Gorham, A.H. Olavesen, and K.S. Dodgson Effect of ionic-strength and pH on properties of purified bovine testicular hyaluronidase Connect. Tissue Res. 3 1975 17 25
55. A. Dorfman, and M.L. Ott A turbidimetric method for the assay of hyaluronidase J. Biol. Chem. 172 1948 367 375
56. S. Nagaraju, S. Devaraja, and K. Kemparaju Purification and properties of hyaluronidase from Hippasa partita (funnel web spider) venom gland extract Toxicon 50 2007 383 393 (Pubitemid 47094881)
57. Z. Hadidian, and N.W. Pirie The effects of serum and of hyaluronic acid derivatives on the action of hyaluronidase Biochem. J. 42 1948 266 274
58. K. Kemparaju, and K.S. Girish Snake venom hyaluronidase: a therapeutic target Cell. Biochem. Funct. 24 2006 7 12 (Pubitemid 43171003)
59. C. Bon, J.P. Changeux, T.W. Jeng, and H. Fraenkelconrat Postsynaptic effects of crotoxin and of its isolated subunits Eur. J. Biochem. 99 1979 471 481
60. 2 and crotoxin complex Toxicon 14 1976 221 233
61. R.A. Hendon, and H. Fraenkel Biological roles of two components of crotoxin Proc. Natl. Acad. Sci. U. S. A. 68 1971 1560 1563
62. S. Stair, K.W. Carlson, S. Shuster, E.T. Wei, and R. Stern Mystixin peptides reduce hyaluronan deposition and edema formation Eur. J. Pharmacol. 450 2002 291 296 (Pubitemid 35246072)
63. C.S. Bitencourt, P.A. Pereira, S.G. Ramos, S.V. Sampaio, E.C. Arantes, D.M. Aronoff, and L.H. Faccioli Hyaluronidase recruits mesenchymal-like cells to the lung and ameliorates fibrosis Fibrog. Tissue Repair 4 2011 3
64. R.J. Lewis, and M.L. Garcia Therapeutic potential of venom peptides Nat. Rev. Drug Discov. 2 2003 790 802 (Pubitemid 37361811)
65. P. Favreau, L. Menin, S. Michalet, F. Perret, O. Cheyneval, M. Stocklin, P. Bulet, and R. Stocklin Mass spectrometry strategies for venom mapping and peptide sequencing from crude venoms: case applications with single arthropod specimen Toxicon 47 2006 676 687 (Pubitemid 44308190)
66. T.E. Heinen, and A.B. Gorini da Veiga Arthropod venoms and cancer Toxicon 57 2011 497 511
67. 2 neurotoxin from the south-american rattlesnake Crotalus durissus terrificus - purification of several isoforms and comparison of their molecular-structure and of their biological activities Biochemistry 27 1988 730 738
68. A.L. Harvey Toxins 'R'Us: more pharmacological tools from nature's superstore Trends Pharmacol. Sci. 23 2002 201 203 (Pubitemid 34465533)
69. J.S.P. Yee, N.L. Gong, F. Afifiyan, D.H. Ma, P.S. Lay, A. Armugam, and K. Jeyaseelan Snake postsynaptic neurotoxins: gene structure, phylogeny and applications in research and therapy Biochimie 86 2004 137 149 (Pubitemid 38317463)