Highlighted Text:
Show |
Hide
Full text loading...
Chapter 2 : Effects of Hydrostatic Pressure on Viruses
Authors:
Andréa C. Oliveira1,
Andre M. O. Gomes2,
Sheila M. B. Lima3,
Rafael B. Gonçalves4,
Waleska D. Schwarcz5,
Ana Cristina B. Silva6,
Juliana R. Cortines7,
Jerson L. Silva8
VIEW AFFILIATIONS
HIDE AFFILIATIONS
Affiliations:
1: Programa de Biologia Estrutural, Instituto de Bioquímica Médica and Centro Nacional de Ressonância Magnética Nuclear Jiri Jonas, Universi-dade Federal do Rio de Janeiro, 21941-590, Rio de Janeiro, RJ, Brazil;
2: Programa de Biologia Estrutural, Instituto de Bioquímica Médica and Centro Nacional de Ressonância Magnética Nuclear Jiri Jonas, Universi-dade Federal do Rio de Janeiro, 21941-590, Rio de Janeiro, RJ, Brazil;
3: Fundação Oswaldo Cruz, Instituto de Tecnologia em Imunobiológicos, Programa de Vacinas Virais, Rio de Janeiro, RJ 21045-900, Brazil;
4: Centro de Pesquisa em Ciência e Tecnologia do Leite, Universidade Norte do Paraná, Fazenda Experimental da UNOPAR, 86125-000, Tamarana, PR, Brazil;
5: Centro de Pesquisa em Ciência e Tecnologia do Leite, Universidade Norte do Paraná, Fazenda Experimental da UNOPAR, 86125-000, Tamarana, PR, Brazil;
6: Programa de Biologia Estrutural, Instituto de Bioquímica Médica and Centro Nacional de Ressonância Magnética Nuclear Jiri Jonas, Universi-dade Federal do Rio de Janeiro, 21941-590, Rio de Janeiro, RJ, Brazil;
7: Programa de Biologia Estrutural, Instituto de Bioquímica Médica and Centro Nacional de Ressonância Magnética Nuclear Jiri Jonas, Universi-dade Federal do Rio de Janeiro, 21941-590, Rio de Janeiro, RJ, Brazil;
8: Programa de Biologia Estrutural, Instituto de Bioquímica Médica and Centro Nacional de Ressonância Magnética Nuclear Jiri Jonas, Universi-dade Federal do Rio de Janeiro, 21941-590, Rio de Janeiro, RJ, Brazil
Content Type: Monograph
Publication Year:
2008
Category: Applied and Industrial Microbiology
Book DOI:
10.1128/9781555815646
Chapter DOI:
10.1128/9781555815646.ch2
MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Preview this chapter:
Effects of Hydrostatic Pressure on Viruses, Page 1 of 2
< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815646/9781555814236_Chap02-1.gif /docserver/preview/fulltext/10.1128/9781555815646/9781555814236_Chap02-2.gif
Abstract:
In several animal viruses, hydrostatic pressure causes inactivation with maintenance of immunogenicity. This chapter describes in detail how high pressure has been used to tackle basic and applied problems in virus biology. The contribution of protein folding and protein-nucleic acid interactions to virus assembly has been evaluated in many bacterial, plant, and animal viruses. Upon interaction with host cells, the conformations of the coat proteins and envelope glycoproteins have to change, which on one hand leads to noninfectious particles and on the other may lead to the exposure of previously occult epitopes, important for vaccine development. These irreversible conformational changes evoked by high pressure that resemble the changes that occur in vivo are discussed in the chapter for most of the viruses. It has been found that high pressure inactivates the enveloped influenza and Sindbis viruses by trapping the particles in the fusion intermediate state. The high titers of the neutralizing antibodies elicited by pressure-inactivated viruses indicate that hydrostatic pressure can be used to prepare whole-virus immunogens. The substantial evidence that high pressure traps viruses in the fusion intermediate states (found with alphaviruses, influenza virus, retroviruses, etc.), not infectious but highly immunogenic, is very promising for vaccine development.
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
Key Concept Ranking
- Infectious bursal disease virus
- 0.44667196
- Nuclear Magnetic Resonance Spectroscopy
- 0.42488477
0.44667196
Figures
Effects of Hydrostatic Pressure on Viruses
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-1,webId=/content/author/10.1128/9781555815646.ch02-1,properties={foaf_givenname=Andréa C., foaf_name=Andréa C. Oliveira, foaf_surname=Oliveira, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-2,webId=/content/author/10.1128/9781555815646.ch02-2,properties={foaf_givenname=Andre M. O., foaf_name=Andre M. O. Gomes, foaf_surname=Gomes, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-3,webId=/content/author/10.1128/9781555815646.ch02-3,properties={foaf_givenname=Sheila M. B., foaf_name=Sheila M. B. Lima, foaf_surname=Lima, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-4,webId=/content/author/10.1128/9781555815646.ch02-4,properties={foaf_givenname=Rafael B., foaf_name=Rafael B. Gonçalves, foaf_surname=Gonçalves, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-5,webId=/content/author/10.1128/9781555815646.ch02-5,properties={foaf_givenname=Waleska D., foaf_name=Waleska D. Schwarcz, foaf_surname=Schwarcz, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff5]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-6,webId=/content/author/10.1128/9781555815646.ch02-6,properties={foaf_givenname=Ana Cristina B., foaf_name=Ana Cristina B. Silva, foaf_surname=Silva, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff6]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-7,webId=/content/author/10.1128/9781555815646.ch02-7,properties={foaf_givenname=Juliana R., foaf_name=Juliana R. Cortines, foaf_surname=Cortines, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff7]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815646.ch02-8,webId=/content/author/10.1128/9781555815646.ch02-8,properties={foaf_givenname=Jerson L., foaf_name=Jerson L. Silva, foaf_surname=Silva, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815646.ch02-aff8]]}]]
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
/content/10.1128/9781555815646.ch02.ch02fig01
Figure 1.
Cavity increase occurring in the M88V mutant. Using the program VMD and a probe radius of 1.4 Å, we analyzed the pdb coordinates of WT bacteriophage and the M88V mutant for the existence of internal cavities in this region. Shown is the region on coat protein in the asymmetric unit of the capsid around residue 88. For the WT phage structure (A), a significant cavity was identified in the neighboring region of the Met88 residue (B). After the replacement of this residue with valine (C), the cavity volume increased to 43 Å3 (D), reflecting a reduction in the surface area of the residue (59 Å2) and in the interactions occurring there (from reference
24
).
10.1128/9781555815646/f0022-01_thmb.gif
10.1128/9781555815646/f0022-01.gif
Figure 1.
Cavity increase occurring in the M88V mutant. Using the program VMD and a probe radius of 1.4 Å, we analyzed the pdb coordinates of WT bacteriophage and the M88V mutant for the existence of internal cavities in this region. Shown is the region on coat protein in the asymmetric unit of the capsid around residue 88. For the WT phage structure (A), a significant cavity was identified in the neighboring region of the Met88 residue (B). After the replacement of this residue with valine (C), the cavity volume increased to 43 Å3 (D), reflecting a reduction in the surface area of the residue (59 Å2) and in the interactions occurring there (from reference 24 ).
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
/content/10.1128/9781555815646.ch02.ch02fig02
Figure 2.
Proposed model for the disassembly of picornaviruses by denaturing high concentrations of urea (A) or by pressure and low temperature (B). In panel A, a high urea concentration elicits complete dissociation and denaturation, with separation of the RNA from the coat protein (urea-unfolded subunits are represented as elongated random coils). In panel B, in contrast, pressure plus low temperature disrupts the icosahedral structure, but the capsid proteins (VP1, VP2, and VP3) still remain bound to the RNA. This particle loses infectivity upon returning to atmospheric pressure and room temperature. This infectivity loss may be due to release of VP4 and the pocket factor (from reference
29
).
10.1128/9781555815646/f0025-01_thmb.gif
10.1128/9781555815646/f0025-01.gif
Figure 2.
Proposed model for the disassembly of picornaviruses by denaturing high concentrations of urea (A) or by pressure and low temperature (B). In panel A, a high urea concentration elicits complete dissociation and denaturation, with separation of the RNA from the coat protein (urea-unfolded subunits are represented as elongated random coils). In panel B, in contrast, pressure plus low temperature disrupts the icosahedral structure, but the capsid proteins (VP1, VP2, and VP3) still remain bound to the RNA. This particle loses infectivity upon returning to atmospheric pressure and room temperature. This infectivity loss may be due to release of VP4 and the pocket factor (from reference 29 ).
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
/content/10.1128/9781555815646.ch02.ch02fig03
Figure 3.
Pressure sensitivity of WT and cleavage-defective FHV VLPs. The pressure stability of FHV WT (circles) and D75N mutant (triangles) VLPs was analyzed by the shift of intrinsic fluorescence spectra (the spectral center of mass [A]) and particle average-size analysis (light scattering [B]). To better appreciate the effect of pressure, the reaction was poised by adding 1 M urea, a subdissociating concentration. Reassembly was evaluated by size exclusion high-performance liquid chromatography for WT FHV (C) and the mutant after decompression (D) (from reference
28
). One bar is equal to 105 Pa.
10.1128/9781555815646/f0026-01_thmb.gif
10.1128/9781555815646/f0026-01.gif
Figure 3.
Pressure sensitivity of WT and cleavage-defective FHV VLPs. The pressure stability of FHV WT (circles) and D75N mutant (triangles) VLPs was analyzed by the shift of intrinsic fluorescence spectra (the spectral center of mass [A]) and particle average-size analysis (light scattering [B]). To better appreciate the effect of pressure, the reaction was poised by adding 1 M urea, a subdissociating concentration. Reassembly was evaluated by size exclusion high-performance liquid chromatography for WT FHV (C) and the mutant after decompression (D) (from reference 28 ). One bar is equal to 105 Pa.
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
/content/10.1128/9781555815646.ch02.ch02fig04
Figure 4.
Disassembly/denaturation of FHV by chemical and physical treatments. Shown is the proposed model for the reversible disassembly of FHV by pressure (a) and complete dissociation by high denaturing concentrations of urea (b). (c) Dissociation effect of high pressure and subdenaturing urea concentrations. (d and e) Effect of high temperature without and with subdenaturing (2 M) urea concentration, respectively. The high-temperature treatment induced aggregation of protein subunits. In panels b, c, and e, the treatments led to complete dissociation and denaturation with separation of the RNA from the capsid proteins, whereas high pressure induced disassembly of the particle, with the coat proteins remaining bound to the RNA (from reference
35
).
10.1128/9781555815646/f0027-01_thmb.gif
10.1128/9781555815646/f0027-01.gif
Figure 4.
Disassembly/denaturation of FHV by chemical and physical treatments. Shown is the proposed model for the reversible disassembly of FHV by pressure (a) and complete dissociation by high denaturing concentrations of urea (b). (c) Dissociation effect of high pressure and subdenaturing urea concentrations. (d and e) Effect of high temperature without and with subdenaturing (2 M) urea concentration, respectively. The high-temperature treatment induced aggregation of protein subunits. In panels b, c, and e, the treatments led to complete dissociation and denaturation with separation of the RNA from the capsid proteins, whereas high pressure induced disassembly of the particle, with the coat proteins remaining bound to the RNA (from reference 35 ).
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
/content/10.1128/9781555815646.ch02.ch02fig05
Figure 5.
pg 28 Gibbs free-energy and volume diagrams for enveloped viruses. Free-energy (A) and volume (B) diagrams showing the conversion between native nonfusogenic state (N) and fusogenic state (FG). The transition intermediate state (T) is also shown (from reference
16
).
10.1128/9781555815646/f0028-01_thmb.gif
10.1128/9781555815646/f0028-01.gif
Figure 5.
pg 28 Gibbs free-energy and volume diagrams for enveloped viruses. Free-energy (A) and volume (B) diagrams showing the conversion between native nonfusogenic state (N) and fusogenic state (FG). The transition intermediate state (T) is also shown (from reference 16 ).
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
/content/10.1128/9781555815646.ch02.ch02fig06
Figure 6.
Pressure-induced fusogenic state of Sindbis virus. (A) Schematic representation of pressure-induced membrane fusion activation of Sindbis virus with ghosts. (B) Fusion assay of Sindbis virus with ghosts as measured by means of pyrene excimer/monomer fluorescence ratio intensity. Fusion was measured over a period of 1 h following addition of ghost vesicles to a final concentration of 0.5 mg/ml. □, native virus in the absence of ghosts at pH 7.5; 0, native virus in the presence of ghosts at pH 7.5;■, pressurized virus in the absence of ghosts at pH 7.5;▲, pressurized virus in the presence of ghosts at pH 7.5;●, virus in the presence of ghosts at pH 6.0. (C) Average values : standard deviations (error bars) after three 1-h experiments for all conditions described for panel (B). Column 1, native virus in the absence of ghosts at pH 7.5; column 2, native virus in the presence of ghosts at pH 7.5; column 3, pressurized virus in the absence of ghosts at pH 7.5; column 4, pressurized virus in the presence of ghosts at pH 7.5; column 5, virus in the presence of ghosts at pH 6.0. The pyrene-labeled lipids in the virus were excited at 330 nm, and the spectra were recorded at wavelengths from 360 to 530 nm. The fluorescence intensities of excimer and monomer emissions were determined at 470 and 389 nm, respectively. The virus concentration was 100 μg/ml (from reference
16
).
10.1128/9781555815646/f0029-01_thmb.gif
10.1128/9781555815646/f0029-01.gif
Figure 6.
Pressure-induced fusogenic state of Sindbis virus. (A) Schematic representation of pressure-induced membrane fusion activation of Sindbis virus with ghosts. (B) Fusion assay of Sindbis virus with ghosts as measured by means of pyrene excimer/monomer fluorescence ratio intensity. Fusion was measured over a period of 1 h following addition of ghost vesicles to a final concentration of 0.5 mg/ml. □, native virus in the absence of ghosts at pH 7.5; 0, native virus in the presence of ghosts at pH 7.5;■, pressurized virus in the absence of ghosts at pH 7.5;▲, pressurized virus in the presence of ghosts at pH 7.5;●, virus in the presence of ghosts at pH 6.0. (C) Average values : standard deviations (error bars) after three 1-h experiments for all conditions described for panel (B). Column 1, native virus in the absence of ghosts at pH 7.5; column 2, native virus in the presence of ghosts at pH 7.5; column 3, pressurized virus in the absence of ghosts at pH 7.5; column 4, pressurized virus in the presence of ghosts at pH 7.5; column 5, virus in the presence of ghosts at pH 6.0. The pyrene-labeled lipids in the virus were excited at 330 nm, and the spectra were recorded at wavelengths from 360 to 530 nm. The fluorescence intensities of excimer and monomer emissions were determined at 470 and 389 nm, respectively. The virus concentration was 100 μg/ml (from reference 16 ).
Citation:
Oliveira A, Gomes A, Lima S, Gonçalves R, Schwarcz W, Silva A, Cortines J, Silva J.
2008.
Effects of Hydrostatic Pressure on Viruses,
p 19-34.
In
Michiels C, Bartlett D, Aersten A (ed),
High-Pressure Microbiology.
ASM Press, Washington, DC.
doi: 10.1128/9781555815646.ch2
References
/content/book/10.1128/9781555815646.ch02
1.
Bloom, B. R. 1996. A perspective on AIDS vaccines. Science 272: 1888– 1890.
2.
Bonafe, C. F.,, C. M. Vital,, R. C. Telles,, M. C. Gonçalves,, M. S. Matsuura,, F. B. Pessine,, D. R. Freitas, and, J. Vega. 1998. Tobacco mosaic virus disassembly by high hydrostatic pressure in combination with urea and low temperature. Biochemistry 37: 11097– 11105.
3.
Bradley, D. W.,, R. A. Hess,, F. Tao,, L. Sciaba-Lentz,, A. T. Remaley,, J. Laugharn, Jr., and, M. Manak. 2000. Pressure cycling technology: a novel approach to virus inactivation in plasma. Transfusion 40: 193– 200.
4.
Bullough, P. A.,, F. M. Hughson,, J. J. Skehel, and, D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371: 37– 43.
5.
Carr, C. M., and, P. S. Kim. 1993. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73: 823– 832.
6.
Cooper, A. 1976. Thermodynamic fluctuations in protein molecules. Proc. Natl. Acad. Sci. USA 73: 2740– 2741.
7.
Da Poian, A. T.,, A. M. O. Gomes,, R. J. N. Oliveira, and, J. L. Silva. 1996. Migration of vesicular stomatitis virus glycoprotein to the nucleus of infected cells. Proc. Natl. Acad. Sci. USA 93: 8268– 8273.
8.
Da Poian, A. T.,, J. E. Johnson, and, J. L. Silva. 1994. Differences in pressure stability of the three components of cowpea mosaic virus: implications for virus assembly and disassembly. Biochemistry 33: 8339– 8346.
9.
Da Poian, A. T.,, A. C. Oliveira, and, J. L. Silva. 1995. Cold denaturation of an icosahedral virus. The role of entropy in virus assembly. Biochemistry 34: 2672– 2677.
10.
De Souza, P. C., Jr.,, R. Tuma,, P. E. Prevelige,, J. L. Silva, and, D. Foguel. 1999. Cavity defects in the procapsid of bacteriophage P22 and the mechanism of capsid maturation. J. Mol. Biol. 287: 527– 538.
11.
Fiers, W. 1979. Structure and function of RNA bacteriophages, p. 69– 204. In H. Fraenkel-Conrat-and, R. R. Wagner (ed.), Comprehensive Virology. Plenum, New York, NY.
12.
Foguel, D., and, J. L. Silva. 1994. Cold denaturation of a repressor-operator complex: the role of entropy in protein-DNA recognition. Proc. Natl. Acad. Sci. USA 91: 8244– 8247.
13.
Foguel, D.,, C. M. Teschke,, P. E. Prevelige, and, J. L. Silva. 1995. Role of entropic interactions in viral capsids: single amino acid substitutions in P22 bacteriophage coat protein resulting in loss of capsid stability. Biochemistry 34: 1120– 1126.
14.
Freitas, M. S.,, A. T. Da Poian,, O. M. Barth,, M. A. Rebello,, J. L. Silva, and, L. P. Gaspar. 2006. The fusogenic state of Mayaro virus induced by low pH and by hydrostatic pressure. Hydrostatic pressure induces the fusion-active state of enveloped viruses. Cell Biochem. Biophys. 44: 325– 335.
15.
Gaspar, L. P.,, J. E. Johnson,, J. L. Silva, and, A. T. Da Poian. 1997. Partially folded states of the capsid protein of cowpea severe mosaic virus in the disassembly pathway. J. Mol. Biol. 273: 456– 466.
16.
Gaspar, L. P.,, A. C. B. Silva,, A. M. O. Gomes,, M. S. Freitas,, A. P. Ano Bom,, W. D. Schwarcz,, J. Mestecky,, M. J. Novak,, D. Foguel, and, J. L. Silva. 2002. Hydrostatic pressure induces the fusion-active state of enveloped viruses. J. Biol. Chem. 277: 8433– 8439.
17.
Golmohammadi, R.,, K. Valegard,, K. Fridborg, and, L. Liljas. 1993. The refined structure of bacteriophage MS2 at 2.8 A resolution. J. Mol. Biol. 234: 620– 639.
18.
Humphrey, W.,, A. Dalke, and, K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14: 33– 38.
19.
Ishimaru, D.,, D. Sa-Carvalho, and, J. L. Silva. 2004. Pressure-inactivated FMDV: a potential vaccine. Vaccine 22: 2334– 2339.
20.
Johnson, J. E. 1996. Functional implications of protein-protein interactions in icosahedral viruses. Proc. Natl. Acad. Sci. USA 93: 27– 33.
21.
Jurkiewicz, E.,, M. Villas-Boas,, J. L. Silva,, G. Weber,, G. Hunsmann, and, R. M. Clegg. 1995. Inactivation of simian immunodeficiency virus by hydrostatic pressure. Proc. Natl. Acad. Sci. USA 92: 6935– 6937.
22.
Lauffer, M. A., and, R. B. Dow. 1941. The denaturation of tobacco mosaic virus at high pressures. J. Biol. Chem. 140: 509– 518.
23.
Leimkuhler, M.,, A. Goldbeck,, M. D. Lechner, and, J. Witz. 2000. Conformational changes preceding decapsidation of bromegrass mosaic virus under hydrostatic pressure: a small-angle neutron scattering study. J. Mol. Biol. 296: 1295– 1305.
24.
Lima, S. M. B.,, D. S. Peabody,, J. L. Silva, and, A. C. Oliveira. 2004. Mutations in the hydrophobic core and in the protein-RNA interface affect the packing and stability of icosahedral viruses. Eur. J. Biochem. 271: 135– 145.
25.
Lima, S. M. B.,, A. C. Q. Vaz,, T. L. F. Souza,, D. S. Peabody,, J. L. Silva, and, A. C. Oliveira. 2006. Dissecting the role of protein-protein and protein-nucleic acid interactions in MS2 bacteriophage stability. FEBS J. 273: 1463– 1475.
26.
Mozhaev, V. V.,, K. Heremans,, J. Frank,, P. Masson, and, C. Balny. 1996. High pressure effects on protein structure and function. Proteins 24: 81– 91.
27.
Nakagami, T.,, H. Ohno,, T. Shigehisa,, T. Otake,, H. Mori,, T. Kawahata,, M. Morimoto, and, N. Ueba. 1996. Inactivation of human immunodeficiency virus by high hydrostatic pressure. Transfusion 36: 475– 476.
28.
Oliveira, A. C.,, A.M. O. Gomes,, F.C. L. Almeida,, R. Mohana-Borges,, A. P. Valente,, V. S. Reddy,, J. E. Johnson, and, J. L. Silva. 2000. Virus maturation targets the protein capsid to concerted disassembly and unfolding. J. Biol. Chem. 275: 16037– 16043.
29.
Oliveira, A. C.,, D. Ishimaru,, R. B. Goncalves,, T. J. Smith,, P. Mason,, D. Sa-Carvalho, and, J. L. Silva. 1999. Low temperature and pressure stability of picornaviruses: implications for virus uncoating. Biophys. J. 76: 1270– 1279.
30.
Oliveira, A. C.,, A. P. Valente,, F.C. L. Almeida,, S.M. B. Lima,, D. Ishimaru,, R. B. Gonçalves,, D. Peabody,, D. Foguel, and, J. L. Silva. 1999. Hydrostatic pressure as a tool to study virus assembly: inactivated vaccines and antiviral drugs. NATO ASI Ser. E 358: 497– 513.
31.
Pontes, L.,, Y. Cordeiro,, V. Giongo,, M. Villas-Boas,, A. Barreto,, J. R. Araujo, and, J. L. Silva. 2001. Pressure-induced formation of inactive triple-shelled rotavirus particles is associated with changes in the spike protein Vp4. J. Mol. Biol. 307: 1171– 1179.
32.
Prevelige, P. E.,, J. King, and, J. L. Silva. 1994. Pressure denaturation of the bacteriophage P22 coat protein and its entropic stabilization in icosahedral shells. Biophys. J. 66: 1631– 1641.
33.
Rossmann, M. G. 1994. The beginnings of structural biology. Recollections, special section in honor of Max Perutz. Protein Sci. 3: 1712– 1725.
34.
Rueckert, R. R. 1996. Picornaviridae: the viruses and their replication, p. 609– 645. In B. N. Fields,, D. M. Knipe, and, P. M. Howley (ed.), Fields Virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, PA.
35.
Schwarcz, W. D.,, S. P. C. Barroso,, A. M. O. Gomes,, J. E. Johnson,, A. Schneemann,, A. C. Oliveira, and, J. L. Silva. 2004. Virus stability and protein-nucleic acid interaction as studied by high-pressure effects on nodaviruses. Cell. Mol. Biol. 50: 419– 427.
36.
Silva, C. C.,, V. Giongo,, A. J. Simpson,, E. R. Camargos,, J. L. Silva, and, M. C. Koury. 2001. Effects of hydrostatic pressure on the Leptospira interrogans: high immunogenicity of the pressure-inactivated serovar hardjo. Vaccine 19: 1511– 1514.
37.
Silva, J. L.,, D. Foguel,, A. T. Da Poian, and, P. E. Prevelige. 1996. The use of hydrostatic pressure as a tool to study viruses and other macromolecular assemblages. Curr. Opin. Struct. Biol. 6: 166– 175.
38.
Silva, J. L.,, P. Luan,, M. Glaser,, E. W. Voss, and, G. Weber. 1992. Effects of hydrostatic pressure on a membrane-enveloped virus: high immunogenicity of the pressure-inactivated virus. J. Virol. 66: 2111– 2117.
39.
Skehel, J. J., and, D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69: 531– 569.
40.
Tian, S. M.,, K. C. Ruan,, J. F. Qian,, G. Q. Shao, and, C. Balny. 2000. Effects of hydrostatic pressure on the structure and biological activity of infectious bursal disease virus. Eur. J. Biochem. 267: 4486– 4494.