1887

Abstract

The GP129, GP131 and GP133 genes of guinea pig cytomegalovirus (GPCMV) are homologues of human cytomegalovirus UL128, UL130 and UL131A, respectively, which are essential for infection of endothelial and epithelial cells, and for viral transmission to leukocytes. Our previous study demonstrated that a GPCMV strain lacking the 1.6 kb locus that contains the GP129, GP131 and GP133 genes had a growth defect in animals. Here, we demonstrated that the WT strain, but not the 1.6 kb-deleted strain, formed capsids in macrophages prepared from the peritoneal fluid. To understand the mechanism, we prepared GPCMV strains defective in each of GP129, GP131 and GP133, and found that they were all essential for the infection of peritoneal, splenic and PBMC-derived macrophages/monocytes, and for expression of immediate-early antigens in the macrophages/monocytes, although they were dispensable for infection of fibroblasts. Monocyte/macrophage tropism could be one of the important determinants for viral dissemination .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.064527-0
2014-06-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/6/1376.html?itemId=/content/journal/jgv/10.1099/vir.0.064527-0&mimeType=html&fmt=ahah

References

  1. Adler B., Scrivano L., Ruzcics Z., Rupp B., Sinzger C., Koszinowski U. 2006; Role of human cytomegalovirus UL131A in cell type-specific virus entry and release. J Gen Virol 87:2451–2460 [View Article][PubMed]
    [Google Scholar]
  2. Auerbach M., Yan D., Fouts A., Xu M., Estevez A., Austin C. D., Bazan F., Feierbach B. 2013; Characterization of the guinea pig CMV gH/gL/GP129/GP131/GP133 complex in infection and spread. Virology 441:75–84 [View Article][PubMed]
    [Google Scholar]
  3. Cui X., McGregor A., Schleiss M. R., McVoy M. A. 2008; Cloning the complete guinea pig cytomegalovirus genome as an infectious bacterial artificial chromosome with excisable origin of replication. J Virol Methods 149:231–239 [View Article][PubMed]
    [Google Scholar]
  4. Cui X., McGregor A., Schleiss M. R., McVoy M. A. 2009; The impact of genome length on replication and genome stability of the herpesvirus guinea pig cytomegalovirus. Virology 386:132–138 [View Article][PubMed]
    [Google Scholar]
  5. Hahn G., Revello M. G., Patrone M., Percivalle E., Campanini G., Sarasini A., Wagner M., Gallina A., Milanesi G.other authors 2004; Human cytomegalovirus UL131–128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 78:10023–10033 [View Article][PubMed]
    [Google Scholar]
  6. Hashimoto K., Yamada S., Katano H., Fukuchi S., Sato Y., Kato M., Yamaguchi T., Moriishi K., Inoue N. 2013; Effects of immunization of pregnant guinea pigs with guinea pig cytomegalovirus glycoprotein B on viral spread in the placenta. Vaccine 31:3199–3205 [View Article][PubMed]
    [Google Scholar]
  7. Hirt B. 1967; Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol 26:365–369 [View Article][PubMed]
    [Google Scholar]
  8. Jarvis M. A., Nelson J. A. 2007; Human cytomegalovirus tropism for endothelial cells: not all endothelial cells are created equal. J Virol 81:2095–2101 [View Article][PubMed]
    [Google Scholar]
  9. Kanai K., Yamada S., Yamamoto Y., Fukui Y., Kurane I., Inoue N. 2011; Re-evaluation of the genome sequence of guinea pig cytomegalovirus. J Gen Virol 92:1005–1020 [View Article][PubMed]
    [Google Scholar]
  10. Katano H., Sato Y., Tsutsui Y., Sata T., Maeda A., Nozawa N., Inoue N., Nomura Y., Kurata T. 2007; Pathogenesis of cytomegalovirus-associated labyrinthitis in a guinea pig model. Microbes Infect 9:183–191 [View Article][PubMed]
    [Google Scholar]
  11. Kern E. R. 2006; Pivotal role of animal models in the development of new therapies for cytomegalovirus infections. Antiviral Res 71:164–171 [View Article][PubMed]
    [Google Scholar]
  12. Koyano S., Inoue N., Nagamori T., Yan H., Asanuma H., Yagyu K., Osaki M., Seiwa C., Fujieda K. 2009; Dried umbilical cords in the retrospective diagnosis of congenital cytomegalovirus infection as a cause of developmental delays. Clin Infect Dis 48:e93–e95 [View Article][PubMed]
    [Google Scholar]
  13. Koyano S., Inoue N., Oka A., Moriuchi H., Asano K., Ito Y., Yamada H., Yoshikawa T., Suzutani T.Japanese Congenital Cytomegalovirus Study Group 2011; Screening for congenital cytomegalovirus infection using newborn urine samples collected on filter paper: feasibility and outcomes from a multicentre study. BMJ Open 1:e000118 [View Article][PubMed]
    [Google Scholar]
  14. Lafemina R. L., Hayward G. S. 1988; Differences in cell-type-specific blocks to immediate early gene expression and DNA replication of human, simian and murine cytomegalovirus. J Gen Virol 69:355–374 [View Article][PubMed]
    [Google Scholar]
  15. MacDonald M. R., Burney M. W., Resnick S. B., Virgin H. M. IV. 1999; Spliced mRNA encoding the murine cytomegalovirus chemokine homolog predicts a beta chemokine of novel structure. J Virol 73:3682–3691[PubMed]
    [Google Scholar]
  16. Manning W. C., Stoddart C. A., Lagenaur L. A., Abenes G. B., Mocarski E. S. 1992; Cytomegalovirus determinant of replication in salivary glands. J Virol 66:3794–3802[PubMed]
    [Google Scholar]
  17. McGregor A., Schleiss M. R. 2001; Molecular cloning of the guinea pig cytomegalovirus (GPCMV) genome as an infectious bacterial artificial chromosome (BAC) in Escherichia coli . Mol Genet Metab 72:15–26 [View Article][PubMed]
    [Google Scholar]
  18. Nozawa N., Yamamoto Y., Fukui Y., Katano H., Tsutsui Y., Sato Y., Yamada S., Inami Y., Nakamura K.other authors 2008; Identification of a 1.6 kb genome locus of guinea pig cytomegalovirus required for efficient viral growth in animals but not in cell culture. Virology 379:45–54 [View Article][PubMed]
    [Google Scholar]
  19. Ogawa H., Suzutani T., Baba Y., Koyano S., Nozawa N., Ishibashi K., Fujieda K., Inoue N., Omori K. 2007; Etiology of severe sensorineural hearing loss in children: independent impact of congenital cytomegalovirus infection and GJB2 mutations. J Infect Dis 195:782–788 [View Article][PubMed]
    [Google Scholar]
  20. Pass R. F. 2001; Cytomegalovirus. In Fields Virology vol. 2 pp. 2675–2705 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  21. Ryckman B. J., Jarvis M. A., Drummond D. D., Nelson J. A., Johnson D. C. 2006; Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J Virol 80:710–722 [View Article][PubMed]
    [Google Scholar]
  22. Ryckman B. J., Rainish B. L., Chase M. C., Borton J. A., Nelson J. A., Jarvis M. A., Johnson D. C. 2008; Characterization of the human cytomegalovirus gH/gL/UL128–131 complex that mediates entry into epithelial and endothelial cells. J Virol 82:60–70 [View Article][PubMed]
    [Google Scholar]
  23. Saederup N., Lin Y. C., Dairaghi D. J., Schall T. J., Mocarski E. S. 1999; Cytomegalovirus-encoded beta chemokine promotes monocyte-associated viremia in the host. Proc Natl Acad Sci U S A 96:10881–10886 [View Article][PubMed]
    [Google Scholar]
  24. Schleiss M. R. 2006; Nonprimate models of congenital cytomegalovirus (CMV) infection: gaining insight into pathogenesis and prevention of disease in newborns. ILAR J 47:65–72 [View Article][PubMed]
    [Google Scholar]
  25. Smith M. S., Bentz G. L., Alexander J. S., Yurochko A. D. 2004; Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence. J Virol 78:4444–4453 [View Article][PubMed]
    [Google Scholar]
  26. Stoddart C. A., Cardin R. D., Boname J. M., Manning W. C., Abenes G. B., Mocarski E. S. 1994; Peripheral blood mononuclear phagocytes mediate dissemination of murine cytomegalovirus. J Virol 68:6243–6253[PubMed]
    [Google Scholar]
  27. Straschewski S., Patrone M., Walther P., Gallina A., Mertens T., Frascaroli G. 2011; Protein pUL128 of human cytomegalovirus is necessary for monocyte infection and blocking of migration. J Virol 85:5150–5158 [View Article][PubMed]
    [Google Scholar]
  28. Tang Q., Maul G. G. 2006; Mouse cytomegalovirus crosses the species barrier with help from a few human cytomegalovirus proteins. J Virol 80:7510–7521 [View Article][PubMed]
    [Google Scholar]
  29. Taylor-Wiedeman J., Sissons P., Sinclair J. 1994; Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J Virol 68:1597–1604[PubMed]
    [Google Scholar]
  30. van der Strate B. W., Hillebrands J. L., Lycklama à Nijeholt S. S., Beljaars L., Bruggeman C. A., Van Luyn M. J., Rozing J., The T. H., Meijer D. K.other authors 2003; Dissemination of rat cytomegalovirus through infected granulocytes and monocytes in vitro and in vivo . J Virol 77:11274–11278 [View Article][PubMed]
    [Google Scholar]
  31. Voigt S., Sandford G. R., Hayward G. S., Burns W. H. 2005; The English strain of rat cytomegalovirus (CMV) contains a novel captured CD200 (vOX2) gene and a spliced CC chemokine upstream from the major immediate-early region: further evidence for a separate evolutionary lineage from that of rat CMV Maastricht. J Gen Virol 86:263–274 [View Article][PubMed]
    [Google Scholar]
  32. Vomaske J., Denton M., Kreklywich C., Andoh T., Osborn J. M., Chen D., Messaoudi I., Orloff S. L., Streblow D. N. 2012; Cytomegalovirus CC chemokine promotes immune cell migration. J Virol 86:11833–11844 [View Article][PubMed]
    [Google Scholar]
  33. Wagner F. M., Brizic I., Prager A., Trsan T., Arapovic M., Lemmermann N. A., Podlech J., Reddehase M. J., Lemnitzer F., other authors. 2013; The viral chemokine MCK-2 of murine cytomegalovirus promotes infection as part of a gH/gL/MCK-2 complex. PLoS Pathog 9:e1003493 [View Article][PubMed]
    [Google Scholar]
  34. Wang D., Shenk T. 2005a; Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J Virol 79:10330–10338 [View Article][PubMed]
    [Google Scholar]
  35. Wang D., Shenk T. 2005b; Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci U S A 102:18153–18158 [View Article][PubMed]
    [Google Scholar]
  36. Yamada S., Nozawa N., Katano H., Fukui Y., Tsuda M., Tsutsui Y., Kurane I., Inoue N. 2009; Characterization of the guinea pig cytomegalovirus genome locus that encodes homologs of human cytomegalovirus major immediate-early genes, UL128, and UL130. Virology 391:99–106 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.064527-0
Loading
/content/journal/jgv/10.1099/vir.0.064527-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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