1887

Journal of General Virology

Volume 91, Issue 9

Changes in the porcine peripheral blood mononuclear cell proteome induced by infection with highly virulent classical swine fever virus Free

Abstract

Leukopenia and immunosuppression are characteristic clinical manifestations of classical swine fever and peripheral blood mononuclear cells (PBMCs) are major targets of classical swine fever virus. To investigate proteomic expression changes in swine PBMCs during lethal CSFV infection, proteins of PBMCs from five lethally CSFV-infected pigs were resolved by two-dimensional electrophoresis followed by mass spectrometry. Quantitative intensity analysis revealed that 66 protein spots showed altered expression, 44 of which were identified as 34 unique proteins by MALDI-TOF-MS/MS. Cellular functions of these proteins included cytoskeletal, energy metabolism, protein translation and processing, antioxidative stress, heat shock and blood clotting. Western blot analysis confirmed the upregulation of annexin A1 and downregulation of cofilin. Identification of these changed levels of expression provides an understanding at the molecular level of the response of target cells to CSFV infection and of the pathogenic mechanisms of leukopenia and immunosuppression induced by the virus.

  • Received:
  • Accepted:
  • Published Online:
© SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.022020-0
2010-09-01
2021-01-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/9/2254.html?itemId=/content/journal/jgv/10.1099/vir.0.022020-0&mimeType=html&fmt=ahah

References

  1. Berggren, M. I., Husbeck, B., Samulitis, B., Baker, A. F., Gallegos, A. & Powis, G. ( 2001; ). Thioredoxin peroxidase-1 (peroxiredoxin-1) is increased in thioredoxin-1 transfected cells and results in enhanced protection against apoptosis caused by hydrogen peroxide but not by other agents including dexamethasone, etoposide, and doxorubicin. Arch Biochem Biophys 392, 103–109.[CrossRef]
    [Google Scholar]
  2. Buchkovich, N. J., Maguire, T. G., Yu, Y., Paton, A. W., Paton, J. C. & Alwine, J. C. ( 2008; ). Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly. J Virol 82, 31–39.[CrossRef]
    [Google Scholar]
  3. Bukrinsky, M. ( 2008; ). How to engage cofilin. Retrovirology 5, 85 [CrossRef]
    [Google Scholar]
  4. Burridge, K. & Connell, L. ( 1983; ). Talin: a cytoskeletal component concentrated in adhesion plaques and other sites of actin-membrane interaction. Cell Motil 3, 405–417.[CrossRef]
    [Google Scholar]
  5. Burridge, K. & Mangeat, P. ( 1984; ). An interaction between vinculin and talin. Nature 308, 744–746.[CrossRef]
    [Google Scholar]
  6. Choi, C., Hwang, K. K. & Chae, C. ( 2004; ). Classical swine fever virus induces tumor necrosis factor-alpha and lymphocyte apoptosis. Arch Virol 149, 875–889.[CrossRef]
    [Google Scholar]
  7. Dastoor, Z. & Dreyer, J. L. ( 2001; ). Potential role of nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase in apoptosis and oxidative stress. J Cell Sci 114, 1643–1653.
     [Google Scholar]
  8. Davis, W. G., Blackwell, J. L., Shi, P. Y. & Brinton, M. A. ( 2007; ). Interaction between the cellular protein eEF1A and the 3′-terminal stem–loop of West Nile virus genomic RNA facilitates viral minus-strand RNA synthesis. J Virol 81, 10172–10187.[CrossRef]
    [Google Scholar]
  9. De Nova-Ocampo, M., Villegas-Sepúlveda, N. & del Angel, R. M. ( 2002; ). Translation elongation factor-1α, La, and PTB interact with the 3′ untranslated region of dengue 4 virus RNA. Virology 295, 337–347.[CrossRef]
    [Google Scholar]
  10. Gerke, V. & Moss, S. E. ( 2002; ). Annexins: from structure to function. Physiol Rev 82, 331–371.
     [Google Scholar]
  11. Heinz, F. X., Collett, M. S., Purcell, R. H., Gould, E. A. & Howard, C. R., Houghton M., Moormann, R. J. M., Rice, C. M. & Thiel, H. J. ( 2004; ). Family Flaviviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 981–998. Edited by C. M. Fauquet, M. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego, CA: Academic Press.
  12. Huang, Y., Jin, Y., Yan, C. H., Yu, Y., Bai, J., Che, F., Zhao, Y. Z. & Fu, S. B. ( 2008; ). Involvement of annexin A2 in p53 induced apoptosis in lung cancer. Mol Cell Biochem 309, 117–123.[CrossRef]
    [Google Scholar]
  13. Ishitani, R. & Chuang, D. M. ( 1996; ). Glyceraldehyde-3-phosphate dehydrogenase antisense oligodeoxynucleotides protect against cytosine arabinonucleoside-induced apoptosis in cultured cerebellar neurons. Proc Natl Acad Sci U S A 93, 9937–9941.[CrossRef]
    [Google Scholar]
  14. Johnson, C. M., Perez, D. R., French, R., Merrick, W. C. & Donis, R. O. ( 2001; ). The NS5A protein of bovine viral diarrhoea virus interacts with the alpha subunit of translation elongation factor-1. J Gen Virol 82, 2935–2943.
     [Google Scholar]
  15. Kim, S. Y., Kim, T. J. & Lee, K. Y. ( 2008; ). A novel function of peroxiredoxin 1 (Prx-1) in apoptosis signal-regulating kinase 1 (ASK1)-mediated signaling pathway. FEBS Lett 582, 1913–1918.[CrossRef]
    [Google Scholar]
  16. Kou, Y. H., Chou, S. M., Wang, Y. M., Chang, Y. T., Huang, S. Y., Jung, M. Y., Huang, Y. H., Chen, M. R., Chang, M. F. & Chang, S. C. ( 2006; ). Hepatitis C virus NS4A inhibits cap-dependent and the viral IRES-mediated translation through interacting with eukaryotic elongation factor 1A. J Biomed Sci 13, 861–874.[CrossRef]
    [Google Scholar]
  17. Lee, W. C., Wang, C. S. & Chien, M. S. ( 1999; ). Virus antigen expression and alterations in peripheral blood mononuclear cell subpopulations after classical swine fever virus infection. Vet Microbiol 67, 17–29.[CrossRef]
    [Google Scholar]
  18. Li, Z., Calzada, M. J., Sipes, J. M., Cashel, J. A., Krutzsch, H. C., Annis, D. S., Mosher, D. F. & Roberts, D. D. ( 2002; ). Interactions of thrombospondins with α4β1 integrin and CD47 differentially modulate T cell behavior. J Cell Biol 157, 509–519.[CrossRef]
    [Google Scholar]
  19. Manevich, Y. & Fisher, A. B. ( 2005; ). Peroxiredoxin 6, a 1-Cys peroxiredoxin, functions in antioxidant defense and lung phospholipids metabolism. Free Radic Biol Med 38, 1422–1432.[CrossRef]
    [Google Scholar]
  20. Mathesius, U., Keijzers, G., Natera, S. H., Weinman, J. J., Diordjevic, M. A. & Rolfe, B. G. ( 2001; ). Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 1, 1424–1440.[CrossRef]
    [Google Scholar]
  21. Moennig, V. & Plagemann, P. G. W. ( 1992; ). The pestiviruses. Adv Virus Res 41, 53–98.
     [Google Scholar]
  22. Naghavi, M. H., Valente, S., Hatziioannou, T., de Los Santos, K., Wen, Y., Mott, C., Gundersen, G. G. & Goff, S. P. ( 2007; ). Moesin regulates stable microtubule formation and limits retroviral infection in cultured cells. EMBO J 26, 41–52.[CrossRef]
    [Google Scholar]
  23. Pauly, T., König, M., Thiel, H. J. & Saalmüller, A. ( 1998; ). Infection with classical swine fever virus: effects on phenotype and immune responsiveness of porcine T lymphocytes. J Gen Virol 79, 31–40.
     [Google Scholar]
  24. Peluso, R. W., Lamb, R. A. & Choppin, P. W. ( 1978; ). Infection with paramyxoviruses stimulates synthesis of cellular polypeptides that are also stimulated in cells transformed by Rous sarcoma virus or deprived of glucose. Proc Natl Acad Sci U S A 75, 6120–6124.[CrossRef]
    [Google Scholar]
  25. Pervushina, O., Scheuerer, B., Reiling, N., Behnke, L., Schröder, J. M., Kasper, B., Brandt, E., Bulfone-Paus, S. & Petersen, F. ( 2004; ). Platelet factor 4/CXCL4 induces phagocytosis and the generation of reactive oxygen metabolites in mononuclear phagocytes independently of Gi protein activation or intracellular calcium transients. J Immunol 173, 2060–2067.[CrossRef]
    [Google Scholar]
  26. Sánchez-Cordón, P. J., Romanini, S., Salguero, F. J., Núñez, A., Bautista, M. J., Jover, A. & Gómez-Villamos, J. C. ( 2002; ). Apoptosis of thymocytes related to cytokine expression in experimental classical swine fever. J Comp Pathol 127, 239–248.[CrossRef]
    [Google Scholar]
  27. Sánchez-Cordón, P. J., Núñez, A., Salguero, F. J., Pedrera, M., Fernández de Marco, M. & Gómez-Villamandos, J. C. ( 2005; ). Lymphocyte apoptosis and thrombocytopenia in spleen during classical swine fever: role of macrophages and cytokines. Vet Pathol 42, 477–488.[CrossRef]
    [Google Scholar]
  28. Sarnow, P. ( 1989; ). Translation of glucose-regulated protein 78/immunoglobulin heavy-chain binding protein mRNA is increased in poliovirus-infected cells at a time when cap-dependent translation of cellular mRNAs is inhibited. Proc Natl Acad Sci U S A 86, 5795–5799.[CrossRef]
    [Google Scholar]
  29. Saunders, P. A., Chen, R. W. & Chuang, D. M. ( 1999; ). Nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase isoforms during neuronal apoptosis. J Neurochem 72, 925–932.
     [Google Scholar]
  30. Sawa, A., Khan, A., Hester, L. & Snyder, S. ( 1997; ). Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and non-neuronal cell death. Proc Natl Acad Sci U S A 94, 11669–11674.[CrossRef]
    [Google Scholar]
  31. Shi, Z., Sun, J., Guo, H. & Tu, C. ( 2009; ). Genomic expression profiling of peripheral blood leukocytes of pigs infected with highly virulent classical swine fever virus strain Shimen. J Gen Virol 90, 1670–1680.[CrossRef]
    [Google Scholar]
  32. Sirover, M. A. ( 1997; ). Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J Cell Biochem 66, 133–140.[CrossRef]
    [Google Scholar]
  33. Solito, E., de Coupade, C., Canaider, S., Goulding, N. J. & Perretti, M. ( 2001; ). Transfection of annexin 1 in monocytic cells produces a high degree of spontaneous and stimulated apoptosis associated with caspase-3 activation. Br J Pharmacol 133, 217–228.[CrossRef]
    [Google Scholar]
  34. Stoeckle, M. Y., Sugano, S., Hampe, A., Vashistha, A., Pellman, D. & Hanafusa, H. ( 1988; ). 78-kilodalton glucose-regulated protein is induced in Rous sarcoma virus-transformed cells independently of glucose deprivation. Mol Cell Biol 8, 2675–2680.
     [Google Scholar]
  35. Summerfield, A., Knötig, S. M. & McCullough, K. C. ( 1998a; ). Lymphocyte apoptosis during classical swine fever: implication of activation-induced cell death. J Virol 72, 1853–1861.
     [Google Scholar]
  36. Summerfield, A., Hofmann, M. A. & McCullough, K. C. ( 1998b; ). Low density blood granulocytic cells induced during classical swine fever are targets for virus infection. Vet Immunol Immunopathol 63, 289–301.[CrossRef]
    [Google Scholar]
  37. Summerfield, A., Knoetig, S. M., Tschudin, R. & McCullough, K. C. ( 2000; ). Pathogenesis of granulocytopenia and bone marrow atrophy during classical swine fever involves apoptosis and necrosis of uninfected cells. Virology 272, 50–60.[CrossRef]
    [Google Scholar]
  38. Summerfield, A., Zingle, K., Inumaru, S. & McCullough, K. C. ( 2001; ). Induction of apoptosis in bone marrow neutrophil-lineage cells by classical swine fever virus. J Gen Virol 82, 1309–1318.
     [Google Scholar]
  39. Sun, J., Jiang, Y., Shi, Z., Yan, Y., Guo, H., He, F. & Tu, C. ( 2008; ). Proteomic alteration of PK-15 cells after infection by classical swine fever virus. J Proteome Res 7, 5263–5269.[CrossRef]
    [Google Scholar]
  40. Susa, M., König, M., Saalmüller, A., Reddehase, M. J. & Thiel, H. J. ( 1992; ). Pathogenesis of classical swine fever: B-lymphocyte deficiency caused by hog cholera virus. J Virol 66, 1171–1176.
     [Google Scholar]
  41. Tabe, Y., Jin, L., Contractor, R., Gold, D., Ruvolo, P., Radke, S., Xu, Y., Tsutusmi-Ishii, Y., Miyake, K. & other authors ( 2007; ). Novel role of HDAC inhibitors in AML1/ETO AML cells: activation of apoptosis and phagocytosis through induction of annexin A1. Cell Death Differ 14, 1443–1456.[CrossRef]
    [Google Scholar]
  42. Thiel, H. J., Plagemann, P. G. W. & Moennig, V. ( 1996; ). Pestiviruses. In Fields Virology, 3rd edn, pp. 1059–1073. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott–Raven.
  43. Tuszynski, G. P., Rothman, V. L., Murphy, A., Siegler, K. & Knudsen, K. A. ( 1988; ). Thrombospondin promotes platelet aggregation. Blood 72, 109–115.
     [Google Scholar]
  44. Vallejo, A. N., Mügge, L. O., Klimiuk, P. A., Weyand, C. M. & Goronzy, J. J. ( 2000; ). Central role of thrombospondin-1 in the activation and clonal expansion of inflammatory T cells. J Immunol 164, 2947–2954.[CrossRef]
    [Google Scholar]
  45. Waxman, S. & Wurmbach, E. ( 2007; ). De-regulation of common housekeeping genes in hepatocellular carcinoma. BMC Genomics 8, 243 [CrossRef]
    [Google Scholar]
  46. White, S. R., Williams, P., Wojcik, K. R., Sun, S., Hiemstra, P. S., Rabe, K. F. & Dorscheid, D. R. ( 2001; ). Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells. Am J Respir Cell Mol Biol 24, 282–294.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.022020-0
Loading
Changes in the porcine peripheral blood mononuclear cell proteome induced by infection with highly virulent classical swine fever virus
J. Gen. Virol. 91, 2254 (2010); https://doi.org/10.1099/vir.0.022020-0
/content/journal/jgv/10.1099/vir.0.022020-0
/content/journal/jgv/10.1099/vir.0.022020-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error