Refolding by high pressure of a toxin containing seven disulfide bonds: Bothropstoxin-1 from Bothrops jararacussu

Molecular Biotechnology

Volumn 48, Issue 3, 2011, Pages 228-234

  Balduino, Keli N ^a   Spencer, Patrick J ^a   Malavasi, Natalia V ^a   Chura Chambi, Rosa M ^a   Lemke, Laura S ^a   Morganti, Ligia ^a  

^a INSTITUTO DE PESQUISAS ENERGÉTICAS E NUCLEARES   (Brazil)

Author keywords

Aggregation; High hydrostatic pressure; K49 phospholipase; Myotoxin; Refolding

Indexed keywords

AGGREGATED PROTEIN; BACTERIAL CULTURES; CYTOTOXIC ACTIVITIES; DISAGGREGATION; DISULFIDE BONDS; DOSE-DEPENDENT; E. COLI; GUANIDINE HYDROCHLORIDE; HETEROLOGOUS PROTEINS; HIGH HYDROSTATIC PRESSURE; HIGH PRESSURE; INCLUSION BODIES; MUSCLE CELL; MYOTOXIN; OPTIMAL CONDITIONS; PHOSPHOLIPASES; PROTEIN CONCENTRATIONS; RECOMBINANT BACTERIA; REFOLDING; SPHERICAL PARTICLE;

BACTERIOLOGY; CELL CULTURE; COVALENT BONDS; CYTOTOXICITY; ESCHERICHIA COLI; HYDRAULICS; HYDRODYNAMICS; HYDROSTATIC PRESSURE; PROTEINS; SCANNING ELECTRON MICROSCOPY;

PH EFFECTS;

BOTHROPSTOXIN 1; DISULFIDE; GUANIDINE; TOXIN; UNCLASSIFIED DRUG; BOTHROPSTOXIN; GLUTATHIONE; RECOMBINANT PROTEIN; SNAKE VENOM;

ANIMAL CELL; ARTICLE; BACTERIUM CULTURE; BOTHROPS JARARACUSSU; COMPRESSION; CONTROLLED STUDY; CYTOTOXICITY; DISULFIDE BOND; HIGH PRESSURE PRESSURE; MORPHOLOGY; MOUSE; MUSCLE CELL; NONHUMAN; PH; PRESSURE; PROTEIN FOLDING; SCANNING ELECTRON MICROSCOPY; SNAKE; ANIMAL; CELL DEATH; CELL INCLUSION; CELL LINE; CHEMISTRY; DRUG EFFECT; ESCHERICHIA COLI; GENETICS; HYDROSTATIC PRESSURE; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN REFOLDING; PROTEIN STABILITY;

BACTERIA (MICROORGANISMS); BOTHROPS JARARACUSSU;

ANIMALS; BOTHROPS; CELL DEATH; CELL LINE; CROTALID VENOMS; DISULFIDES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GLUTATHIONE; GUANIDINE; HYDROGEN-ION CONCENTRATION; HYDROSTATIC PRESSURE; INCLUSION BODIES; MICE; MICROSCOPY, ELECTRON, SCANNING; PROTEIN REFOLDING; PROTEIN STABILITY; RECOMBINANT PROTEINS;

EID: 80054050339     PISSN: 10736085     EISSN: 15590305     Source Type: Journal    
DOI: 10.1007/s12033-010-9363-5     Document Type: Article

References (36)

1. Gutierrez, J. M., & Lomonte, B. (1995). Phospholipase a(2), myotoxins from bothrops snake-venoms. Toxicon, 33, 1405-1424.
2. Bober, M. A., Glenn, J. L., Straight, R. C., & Ownby, C. L. (1988). Detection of myotoxin alpha-like proteins in various snake venoms. Toxicon, 26, 665-673.
3. Fletcher, J. E., & Jiang, M. S. (1998). Lys49 phospholipase A(2) myotoxins lyse cell cultures by two distinct mechanisms. Tox-icon, 36, 1549-1555. (Pubitemid 28511069)
4. Pungercar, J., Krizaj, I., Liang, N. S., & Gubensek, F. (1999). An aromatic, but not a basic, residue is involved in the toxicity of group-II phospholipase A(2) neurotoxins. Biochemical Journal, 341, 139-145. (Pubitemid 29359058)
5. Wang, Y. M., Lu, P. J., Ho, C. L., & Tsai, I. H. (1992). Characterization and molecular-cloning of neurotoxic phospholipases-a(2) from Taiwan viper (Vipera-russelli-formosensis). European Journal of Biochemistry, 209, 635-641.
6. Arni, R. K., & Gutierrez, J. M. (1993). Crystallization and preliminary diffraction data of two myotoxins isolated from the venoms of Bothrops asper (Terciopelo) and Bothrops nummifer (jumping viper). Toxicon, 31, 1061-1064.
7. Cintra, A. C. O., Marangoni, S., Oliveira, B., & Giglio, J. R. (1993). Bothropstoxin-I-amino-acid-sequence and function. Journal of Protein Chemistry, 12, 57-64.
8. Lomonte, B., Angulo, Y., Rufini, S., Cho, W. H., Giglio, J. R., Ohno, M., et al. (1999). Comparative study of the cytolytic activity of myotoxic phospholipases A(2) on mouse endothelial (tEnd) and skeletal muscle (C2C12) cells in vitro. Toxicon, 37, 145-158. (Pubitemid 28512994)
9. Swietnicki, W. (2006). Folding aggregated proteins into functionally active forms. Current Opinion in Biotechnology, 17, 367-372. (Pubitemid 44163450)
10. Paladini, A. A., Jr., & Weber, G. (1981). Pressure-induced reversible dissociation of enolase. Biochemistry, 20, 2587-2593.
11. Silva, J. L., Foguel, D., Da Poian, A. T., & Prevelige, P. E. (1996). The use of hydrostatic pressure as a tool to study viruses and other macromolecular assemblages. Current Opinion in Structural Biology, 6, 166-175. (Pubitemid 26128820)
12. Robinson, C. R., & Sligar, S. G. (1995). Hydrostatic and osmotic pressure as tools to study macromolecular recognition. Methods in Enzymology, 259, 395-427.
13. Silva, J. L., & Weber, G. (1993). Pressure stability of proteins. Annual Review of Physical Chemistry, 44, 89-113.
14. Lefebvre, B. G., Gage, M. J., & Robinson, A. S. (2004). Maximizing recovery of native protein from aggregates by optimizing pressure treatment. Biotechnology Progress, 20, 623-629. (Pubitemid 38459171)
15. St John, R. J., Carpenter, J. F., & Randolph, T. W. (1999). High pressure fosters protein refolding from aggregates at high concentrations. Proceedings of the National Academy of Sciences of the United States of America, 96, 13029-13033.
16. St John, R. J., Carpenter, J. F., & Randolph, T. W. (2002). High-pressure refolding of disulfide-cross-linked lysozyme aggregates: Thermodynamics and optimization. Biotechnology Progress, 18, 565-571. (Pubitemid 34623232)
17. Foguel, D., Robinson, C. R., de Sousa, P. C., Jr., Silva, J. L., & Robinson, A. S. (1999). Hydrostatic pressure rescues native protein from aggregates. Biotechnology and Bioengineering, 63, 552-558. (Pubitemid 29193949)
18. St John, R. J., Carpenter, J. F., Balny, C., & Randolph, T. W. (2001). High pressure refolding of recombinant human growth hormone from insoluble aggregates. Structural transformations, kinetic barriers, and energetics. The Journal of Biological Chemistry, 276, 46856-46863.
19. Seefeldt, M. B., Ouyang, J., Froland, W. A., Carpenter, J. F., & Randolph, T. W. (2004). High-pressure refolding of bikunin: Efficacy and thermodynamics. Protein Science, 13, 2639-2650. (Pubitemid 39274632)
20. Chura-Chambi, R. M., Genova, L. A., Affonso, R., & Morganti, L. (2008). Refolding of endostatin from inclusion bodies using high hydrostatic pressure. Analytical Biochemistry, 379, 32-39.
21. Lee, S. H., Carpenter, J. F., Chang, B. S., Randolph, T. W., & Kim, Y. S. (2006). Effects of solutes on solubilization and refolding of proteins from inclusion bodies with high hydrostatic pressure. Protein Science, 15, 304-313. (Pubitemid 43145002)
22. Schoner, B. E., Bramlett, K. S., Guo, H., & Burris, T. P. (2005). Reconstitution of functional nuclear receptor proteins using high pressure refolding. Molecular Genetics and Metabolism, 85, 318-322. (Pubitemid 41074116)
23. Ward, R. J., de Oliveira, A. H., Bortoleto, R. K., Rosa, J. C., Faca, V. M., & Greene, L. J. (2001). Refolding and purification of Bothropstoxin-I, a Lys49-phospholipase A2 homologue, expressed as inclusion bodies in Escherichia coli. Protein Expression and Purification, 21, 134-140. (Pubitemid 32614506)
24. Angulo, Y., & Lomonte, B. (2005). Differential susceptibility of C2C12 myoblasts and myotubes to group II phospholipase A2 myotoxins from crotalid snake venoms. Cell Biochemistry and Function, 23, 307-313. (Pubitemid 41330284)
25. Clark, E. D. B. (1998). Refolding of recombinant proteins. Current Opinion in Biotechnology, 9, 157-163.
26. Ami, D., Natalello, A., Taylor, G., Tonon, G., & Maria Doglia, S. (2006). Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochimica et Biophysica Acta, 1764, 793-799.
27. Garcia-Fruitos, E., Aris, A., & Villaverde, A. (2007). Localization of functional polypeptides in bacterial inclusion bodies. Applied and Environmental Microbiology, 73, 289-294. (Pubitemid 46079961)
28. Singh, S. M., & Panda, A. K. (2005). Solubilization and refolding of bacterial inclusion body proteins. Journal of Bioscience and Bioengineering, 99, 303-310. (Pubitemid 40740579)
29. Patra, A. K., Mukhopadhyay, R., Mukhija, R., Krishnan, A., Garg, L. C., & Panda, A. K. (2000). Optimization of inclusion body solubilization and renaturation of recombinant human growth hormone from Escherichia coli. Protein Expression and Purification, 18, 182-192. (Pubitemid 30172224)
30. da Silva Giotto, M. T., Garratt, R. C., Oliva, G., Mascarenhas, Y. P., Giglio, J. R., Cintra, A. C. O., et al. (1998). Crystallographic and spectroscopic characterization of a molecular hinge: Con-formational changes in bothropstoxin I, a dimeric Lys49 phos-pholipase A2 homologue. Proteins, 30, 442-454. (Pubitemid 28117664)
31. Middelberg, A. P. (2002). Preparative protein refolding. Trends in Biotechnology, 20, 437-443. (Pubitemid 35239937)
32. Tsumoto, K., Umetsu, M., Kumagai, I., Ejima, D., Philo, J. S., & Arakawa, T. (2004). Role of arginine in protein refolding, solu-bilization, and purification. Biotechnology Progress, 20, 1301-1308. (Pubitemid 39351313)
33. Prijatelj, P., Pranznikar, Z. J., Petan, T., Krizaj, I., & Pungercar, J. (2008). Mapping the structural determinants of presynaptic neurotoxicity of snake venom phospholipases A(2). Toxicon, 51, 1520-1529.
34. Aragao, E. A., Chioato, L., & Ward, R. J. (2008). Permeabili-zation of E. coli K12 inner and outer membranes by bothrops-toxin-I, A LYS49 phospholipase A2 from Bothrops jararacussu. Toxicon, 51, 538-546.
35. Leite, R. S., Giuliani, C. D., Lomonte, B., Franco, W., & Selistre-de-Araujo, H. S. (2004). Effect of a recombinant Lys49PLA2 myotoxin and Lys49PLA2-derived synthetic peptides from Agkistrodon species on membrane permeability to water. Tox-icon, 44, 157-159. (Pubitemid 38891544)
36. Yang, W. L., Peng, L. S., Zhong, X. F., Wei, J. W., Jiang, X. Y., Ye, L. T., et al. (2003). Functional expression and characterization of a recombinant phospholipase A2 from sea snake Lapemis hardwickii as a soluble protein in E. coli. Toxicon, 41, 713-721.