1887

Journal of General Virology

Volume 99, Issue 10

Differences in the effects of mutations in GP131, a guinea pig cytomegalovirus homologue of pentameric complex component UL130, on macrophage and epithelial cell infection Free

Abstract

As congenital cytomegalovirus (CMV) infection is the major cause of developmental abnormalities in children, the development of effective vaccines is critical to public health. Recent studies have demonstrated that the pentameric complex (Pentamer) of glycoproteins, which is required for human CMV infection of endothelial and epithelial cells, could be a potent vaccine antigen. As guinea pig CMV (GPCMV) infects congenitally and encodes homologues of all Pentamer components, GPCMV models are considered to be useful for the development of vaccine strategies. Here, to clarify the precise requirement of GP131, one of the GPCMV Pentamer components, for the infection of epithelial cells and macrophages, we prepared several mutants with a charged amino acid-to-alanine alteration in GP131 and found some differences in the effects of the mutations on the infection of the two cell types, suggesting the existence of cell type-dependent recognition or function of Pentamer in GPCMV infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): cell tropism , cytomegalovirus , entry , epithelial cells , guinea pig and macrophage
© 2018 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001137
2018-08-16
2020-07-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/10/1425.html?itemId=/content/journal/jgv/10.1099/jgv.0.001137&mimeType=html&fmt=ahah

References

  1. Kenneson A, Cannon MJ. Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol 2007;17:253–276 [CrossRef][PubMed]
     [Google Scholar]
  2. Pass RF. Cytomegalovirus. In Knipe DM, Howley PM. (editors) Fields Virology Philadelphia, PA: Lippincott Williams & Wilkins; 2001; pp.2675–2705
     [Google Scholar]
  3. Ogawa H, Suzutani T, Baba Y, Koyano S, Nozawa N et al. Etiology of severe sensorineural hearing loss in children: independent impact of congenital cytomegalovirus infection and GJB2 mutations. J Infect Dis 2007;195:782–788 [CrossRef][PubMed]
     [Google Scholar]
  4. Koyano S, Inoue N, Nagamori T, Yan H, Asanuma H et al. Dried umbilical cords in the retrospective diagnosis of congenital cytomegalovirus infection as a cause of developmental delays. Clin Infect Dis 2009;48:e93e95 [CrossRef][PubMed]
     [Google Scholar]
  5. Koyano S, Inoue N, Oka A, Moriuchi H, Asano K et al. Screening for congenital cytomegalovirus infection using newborn urine samples collected on filter paper: feasibility and outcomes from a multicentre study. BMJ Open 2011;1:e000118 [CrossRef][PubMed]
     [Google Scholar]
  6. Adler B, Scrivano L, Ruzcics Z, Rupp B, Sinzger C et al. Role of human cytomegalovirus UL131A in cell type-specific virus entry and release. J Gen Virol 2006;87:2451–2460 [CrossRef][PubMed]
     [Google Scholar]
  7. Hahn G, Revello MG, Patrone M, Percivalle E, Campanini G et al. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 2004;78:10023–10033 [CrossRef][PubMed]
     [Google Scholar]
  8. Ryckman BJ, Jarvis MA, Drummond DD, Nelson JA, Johnson DC. Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J Virol 2006;80:710–722 [CrossRef][PubMed]
     [Google Scholar]
  9. Wang D, Shenk T. Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci USA 2005;102:18153–18158 [CrossRef][PubMed]
     [Google Scholar]
  10. Wang D, Shenk T. Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J Virol 2005;79:10330–10338 [CrossRef][PubMed]
     [Google Scholar]
  11. Ryckman BJ, Rainish BL, Chase MC, Borton JA, Nelson JA et al. Characterization of the human cytomegalovirus gH/gL/UL128-131 complex that mediates entry into epithelial and endothelial cells. J Virol 2008;82:60–70 [CrossRef][PubMed]
     [Google Scholar]
  12. Wussow F, Chiuppesi F, Martinez J, Campo J, Johnson E et al. Human cytomegalovirus vaccine based on the envelope gH/gL pentamer complex. PLoS Pathog 2014;10:e1004524 [CrossRef][PubMed]
     [Google Scholar]
  13. Fouts AE, Chan P, Stephan JP, Vandlen R, Feierbach B. Antibodies against the gH/gL/UL128/UL130/UL131 complex comprise the majority of the anti-cytomegalovirus (anti-CMV) neutralizing antibody response in CMV hyperimmune globulin. J Virol 2012;86:7444–7447 [CrossRef][PubMed]
     [Google Scholar]
  14. Cui X, Meza BP, Adler SP, McVoy MA. Cytomegalovirus vaccines fail to induce epithelial entry neutralizing antibodies comparable to natural infection. Vaccine 2008;26:5760–5766 [CrossRef][PubMed]
     [Google Scholar]
  15. Wen Y, Monroe J, Linton C, Archer J, Beard CW et al. Human cytomegalovirus gH/gL/UL128/UL130/UL131A complex elicits potently neutralizing antibodies in mice. Vaccine 2014;32:3796–3804 [CrossRef][PubMed]
     [Google Scholar]
  16. Fu TM, An Z, Wang D. Progress on pursuit of human cytomegalovirus vaccines for prevention of congenital infection and disease. Vaccine 2014;32:2525–2533 [CrossRef][PubMed]
     [Google Scholar]
  17. Schleiss MR. Comparison of vaccine strategies against congenital CMV infection in the guinea pig model. J Clin Virol 2008;41:224–230 [CrossRef][PubMed]
     [Google Scholar]
  18. Schleiss MR. Developing a vaccine against congenital cytomegalovirus (CMV) infection: what have we learned from animal models? where should we go next?. Future Virol 2013;8:1161–1182 [CrossRef][PubMed]
     [Google Scholar]
  19. Hashimoto K, Yamada S, Katano H, Fukuchi S, Sato Y et al. Effects of immunization of pregnant guinea pigs with guinea pig cytomegalovirus glycoprotein B on viral spread in the placenta. Vaccine 2013;31:3199–3205 [CrossRef][PubMed]
     [Google Scholar]
  20. Auerbach M, Yan D, Fouts A, Xu M, Estevez A et al. Characterization of the guinea pig CMV gH/gL/GP129/GP131/GP133 complex in infection and spread. Virology 2013;441:75–84 [CrossRef][PubMed]
     [Google Scholar]
  21. Coleman S, Choi KY, Root M, McGregor A. A homolog pentameric complex dictates viral epithelial tropism, pathogenicity and congenital infection rate in guinea pig cytomegalovirus. PLoS Pathog 2016;12:e1005755 [CrossRef][PubMed]
     [Google Scholar]
  22. Yamada S, Fukuchi S, Hashimoto K, Fukui Y, Tsuda M et al. Guinea pig cytomegalovirus GP129/131/133, homologues of human cytomegalovirus UL128/130/131A, are necessary for infection of monocytes and macrophages. J Gen Virol 2014;95:1376–1382 [CrossRef][PubMed]
     [Google Scholar]
  23. Yamada S, Nozawa N, Katano H, Fukui Y, Tsuda M et al. Characterization of the guinea pig cytomegalovirus genome locus that encodes homologs of human cytomegalovirus major immediate-early genes, UL128, and UL130. Virology 2009;391:99–106 [CrossRef][PubMed]
     [Google Scholar]
  24. Nozawa N, Yamamoto Y, Fukui Y, Katano H, Tsutsui Y et al. 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 2008;379:45–54 [CrossRef][PubMed]
     [Google Scholar]
  25. McVoy MA, Wang JB, Dittmer DP, Bierle CJ, Swanson EC et al. Repair of a mutation disrupting the guinea pig cytomegalovirus pentameric complex acquired during fibroblast passage restores pathogenesis in immune-suppressed guinea pigs and in the context of congenital infection. J Virol 2016;90:7715–7727 [CrossRef][PubMed]
     [Google Scholar]
  26. Miller AD, Rosman GJ. Improved retroviral vectors for gene transfer and expression. Biotechniques 1989;7:980–990[PubMed]
     [Google Scholar]
  27. Katano H, Sato Y, Tsutsui Y, Sata T, Maeda A et al. Pathogenesis of cytomegalovirus-associated labyrinthitis in a guinea pig model. Microbes Infect 2007;9:183–191 [CrossRef][PubMed]
     [Google Scholar]
  28. Nogalski MT, Chan GC, Stevenson EV, Collins-McMillen DK, Yurochko AD. The HCMV gH/gL/UL128-131 complex triggers the specific cellular activation required for efficient viral internalization into target monocytes. PLoS Pathog 2013;9:e1003463 [CrossRef][PubMed]
     [Google Scholar]
  29. Ciferri C, Chandramouli S, Donnarumma D, Nikitin PA, Cianfrocco MA et al. Structural and biochemical studies of HCMV gH/gL/gO and pentamer reveal mutually exclusive cell entry complexes. Proc Natl Acad Sci USA 2015;112:1767–1772 [CrossRef][PubMed]
     [Google Scholar]
  30. Ciferri C, Chandramouli S, Leitner A, Donnarumma D, Cianfrocco MA et al. Antigenic characterization of the HCMV gH/gL/gO and pentamer cell entry complexes reveals binding sites for potently neutralizing human antibodies. PLoS Pathog 2015;11:e1005230 [CrossRef][PubMed]
     [Google Scholar]
  31. Schuessler A, Sampaio KL, Scrivano L, Sinzger C. Mutational mapping of UL130 of human cytomegalovirus defines peptide motifs within the C-terminal third as essential for endothelial cell infection. J Virol 2010;84:9019–9026 [CrossRef][PubMed]
     [Google Scholar]
  32. Coleman S, Choi KY, McGregor A. Cytomegalovirus UL128 homolog mutants that form a pentameric complex produce virus with impaired epithelial and trophoblast cell tropism and altered pathogenicity in the guinea pig. Virology 2017;509:205–221 [CrossRef][PubMed]
     [Google Scholar]
  33. Stoddart CA, Cardin RD, Boname JM, Manning WC, Abenes GB et al. Peripheral blood mononuclear phagocytes mediate dissemination of murine cytomegalovirus. J Virol 1994;68:6243–6253[PubMed]
     [Google Scholar]
  34. van der Strate BW, Hillebrands JL, Lycklama À Nijeholt SS, Beljaars L, Bruggeman CA et al. Dissemination of rat cytomegalovirus through infected granulocytes and monocytes in vitro and in vivo. J Virol 2003;77:11274–11278 [CrossRef][PubMed]
     [Google Scholar]
  35. Smith MS, Bentz GL, Alexander JS, Yurochko AD. Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence. J Virol 2004;78:4444–4453 [CrossRef][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001137
Loading
Differences in the effects of mutations in GP131, a guinea pig cytomegalovirus homologue of pentameric complex component UL130, on macrophage and epithelial cell infection
J. Gen. Virol. 99, 1425 (2018); https://doi.org/10.1099/jgv.0.001137
/content/journal/jgv/10.1099/jgv.0.001137
/content/journal/jgv/10.1099/jgv.0.001137
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

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