Comparative proteomics of human monkeypox and vaccinia intracellular mature and extracellular enveloped virions.

Orthopoxviruses are among the largest and most complex of the animal viruses. In response to the recent emergence of monkeypox in Africa and the threat of smallpox bioterrorism, two orthopoxviruses with different pathogenic potentials, human monkeypox virus and vaccinia virus, were proteomically compared with the goal of identifying proteins required for pathogenesis. Orthopoxviruses were grown in HeLa cells to two different viral forms (intracellular mature virus and extracellular enveloped virus), purified by sucrose gradient ultracentrifugation, denatured using RapiGest surfactant, and digested with trypsin. Unfractionated samples and strong cation exchange HPLC fractions were analyzed by high-resolution reversed-phase nano-LC-MS/MS, and analyses of the MS/MS spectra using SEQUEST and X! Tandem resulted in the confident identification of hundreds of monkeypox, vaccinia, and copurified host-cell proteins. The unfractionated samples were additionally analyzed by LC-MS using an LTQ-Orbitrap, and the accurate mass and elution time tag approach was used to perform quantitative comparisons. Possible pathophysiological roles of differentially abundant Orthopoxvirus proteins are discussed. Data, processed results, and protocols are available at http://www.proteomicsresource.org/.

[1]  Joshua N. Adkins,et al.  MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC-MS(/MS) features , 2008, Comput. Biol. Chem..

[2]  A. Sahu,et al.  Viral mimicry of the complement system , 2003, Journal of Biosciences.

[3]  Navdeep Jaitly,et al.  Accurate Mass Measurements in Proteomics , 2007 .

[4]  Navdeep Jaitly,et al.  VIPER: an advanced software package to support high-throughput LC-MS peptide identification , 2007, Bioinform..

[5]  Vladislav A Petyuk,et al.  Spatial mapping of protein abundances in the mouse brain by voxelation integrated with high-throughput liquid chromatography-mass spectrometry. , 2007, Genome research.

[6]  Ronald J. Moore,et al.  Protein composition of the vaccinia virus mature virion. , 2007, Virology.

[7]  Richard D. Smith,et al.  Mass measurement accuracy in analyses of highly complex mixtures based upon multidimensional recalibration. , 2006, Analytical chemistry.

[8]  Richard D. Smith,et al.  Robust algorithm for alignment of liquid chromatography-mass spectrometry analyses in an accurate mass and time tag data analysis pipeline. , 2006, Analytical chemistry.

[9]  Fred Heffron,et al.  Analysis of the Salmonella typhimurium Proteome through Environmental Response toward Infectious Conditions* , 2006, Molecular & Cellular Proteomics.

[10]  Ying Xu,et al.  Improved peptide elution time prediction for reversed-phase liquid chromatography-MS by incorporating peptide sequence information. , 2006, Analytical chemistry.

[11]  Richard D. Smith,et al.  Advances in proteomics data analysis and display using an accurate mass and time tag approach. , 2006, Mass spectrometry reviews.

[12]  Nikola Tolić,et al.  PRISM: A data management system for high‐throughput proteomics , 2006, Proteomics.

[13]  C. Maier,et al.  Pox proteomics: mass spectrometry analysis and identification of Vaccinia virion proteins , 2006, Virology Journal.

[14]  Chung-Lin Liao,et al.  Vaccinia Virus Proteome: Identification of Proteins in Vaccinia Virus Intracellular Mature Virion Particles , 2006, Journal of Virology.

[15]  Matthew E Monroe,et al.  Estimating probabilities of peptide database identifications to LC-FTICR-MS observations , 2006, Proteome Science.

[16]  P. Formenty,et al.  A tale of two clades: monkeypox viruses. , 2005, The Journal of general virology.

[17]  Gilbert S Omenn,et al.  An evaluation, comparison, and accurate benchmarking of several publicly available MS/MS search algorithms: Sensitivity and specificity analysis , 2005, Proteomics.

[18]  G. Poland,et al.  The US smallpox vaccination program: a review of a large modern era smallpox vaccination implementation program. , 2005, Vaccine.

[19]  Richard D. Smith,et al.  Proteomics by FTICR mass spectrometry: top down and bottom up. , 2005, Mass spectrometry reviews.

[20]  Ronald J Moore,et al.  Comparative proteome analyses of human plasma following in vivo lipopolysaccharide administration using multidimensional separations coupled with tandem mass spectrometry , 2005, Proteomics.

[21]  Chris Upton,et al.  Poxvirus Bioinformatics Resource Center: a comprehensive Poxviridae informational and analytical resource , 2004, Nucleic Acids Res..

[22]  Matthew E Monroe,et al.  Probability-based evaluation of peptide and protein identifications from tandem mass spectrometry and SEQUEST analysis: the human proteome. , 2005, Journal of proteome research.

[23]  G. McFadden.  Poxvirus tropism , 2005, Nature Reviews Microbiology.

[24]  M. Law,et al.  The exit of vaccinia virus from infected cells. , 2004, Virus research.

[25]  Alexandra Lucas,et al.  Secreted Immunomodulatory Viral Proteins as Novel Biotherapeutics12 , 2004, The Journal of Immunology.

[26]  Richard D. Smith,et al.  Application of peptide LC retention time information in a discriminant function for peptide identification by tandem mass spectrometry. , 2004, Journal of proteome research.

[27]  E. Birney,et al.  The International Protein Index: An integrated database for proteomics experiments , 2004, Proteomics.

[28]  Thomas L. Madden,et al.  BLAST: at the core of a powerful and diverse set of sequence analysis tools , 2004, Nucleic Acids Res..

[29]  Daniel C. Desrosiers,et al.  The ankyrin repeat as molecular architecture for protein recognition , 2004, Protein science : a publication of the Protein Society.

[30]  S. Lewis-jones.  Zoonotic poxvirus infections in humans , 2004, Current opinion in infectious diseases.

[31]  P. Eckburg,et al.  Human monkeypox: an emerging zoonosis , 2004, The Lancet. Infectious diseases.

[32]  E. A. Uvarova,et al.  Multiple Genetic Differences between the Monkeypox and Variola Viruses , 2002, Doklady Biochemistry and Biophysics.

[33]  P. Kellam,et al.  Poxvirus genomes: a phylogenetic analysis. , 2004, The Journal of general virology.

[34]  R. Beavis,et al.  A method for reducing the time required to match protein sequences with tandem mass spectra. , 2003, Rapid communications in mass spectrometry : RCM.

[35]  G. Rutherford,et al.  Risks of serious complications and death from smallpox vaccination: A systematic review of the United States experience, 1963–1968 , 2003, BMC public health.

[36]  R. Aebersold,et al.  A statistical model for identifying proteins by tandem mass spectrometry. , 2003, Analytical chemistry.

[37]  G. McFadden,et al.  Poxvirus Immunomodulatory Strategies: Current Perspectives , 2003, Journal of Virology.

[38]  M. Law,et al.  The formation and function of extracellular enveloped vaccinia virus. , 2002, The Journal of general virology.

[39]  E. A. Uvarova,et al.  Analysis of the Monkeypox Virus Genome , 2002, Virology.

[40]  A. Kemper,et al.  Expected adverse events in a mass smallpox vaccination campaign. , 2002, Effective clinical practice : ECP.

[41]  B. Sodeik,et al.  Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host? , 2002, Trends in microbiology.

[42]  John Quackenbush,et al.  Genesis: cluster analysis of microarray data , 2002, Bioinform..

[43]  E. A. Uvarova,et al.  Human monkeypox and smallpox viruses: genomic comparison , 2001, FEBS letters.

[44]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[45]  B. Moss,et al.  Orthopoxvirus IL-18 binding proteins: affinities and antagonist activities. , 2001, Virology.

[46]  B. Moss,et al.  The Vaccinia Virus A33R Protein Provides a Chaperone Function for Viral Membrane Localization and Tyrosine Phosphorylation of the A36R Protein , 2001, Journal of Virology.

[47]  D. Tscharke,et al.  Vaccinia virus gene B7R encodes an 18-kDa protein that is resident in the endoplasmic reticulum and affects virus virulence. , 2000, Virology.

[48]  B. Moss,et al.  The Vaccinia Virus A 33 R Protein Provides a Chaperone Function for Viral Membrane Localization and Tyrosine Phosphorylation of the A 36 R Protein , 2000 .

[49]  A. Alcamí,et al.  Vaccinia virus strains Lister, USSR and Evans express soluble and cell-surface tumour necrosis factor receptors. , 1999, The Journal of general virology.

[50]  C. Smith,et al.  Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. , 1994, Virology.

[51]  S. Shchelkunov,et al.  Ankyrin‐like proteins of variola and vaccinia viruses , 1993, FEBS letters.

[52]  H. W. Chang,et al.  The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[53]  R. Doms,et al.  Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane , 1990, Journal of virology.

[54]  D. Baxby.  Jenner's smallpox vaccine : the riddle of vaccinia virus and its origin , 1982 .

[55]  L. Payne.  Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. , 1980, The Journal of general virology.