1887

Abstract

Herpes simplex virus type 1 (HSV-1) replicates in various cell types and induces early cell death, which limits viral replication in certain cell types. Axin is a scaffolding protein that regulates Wnt signalling and participates in various cellular events, including cellular proliferation and cell death. The effects of axin expression on HSV-1 infection were investigated based on our initial observation that Wnt3a treatment or axin knockdown reduced HSV-1 replication. L929 cells expressed the axin protein in a doxycycline-inducible manner (L-axin) and enhanced HSV-1 replication in comparison to control cells (L-EV). HSV-1 infection induced cell death as early as 6 h after infection through the necrotic pathway and required protein synthesis in L929 cells. Subsequent analysis of viral protein expression suggested that axin expression led to suppression of HSV-1-induced premature cell death, resulting in increased late gene expression. In analysis of axin deletion mutants, the regulators of the G-protein signalling (RGS) domain were involved in the axin-mediated enhancement of viral replication and reduction in cell death. These results suggest that viral replication enhancement might be mediated by the axin RGS domain.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.051540-0
2013-07-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/7/1636.html?itemId=/content/journal/jgv/10.1099/vir.0.051540-0&mimeType=html&fmt=ahah

References

  1. Ahmed Y., Hayashi S., Levine A., Wieschaus E. 1998; Regulation of armadillo by a Drosophila APC inhibits neuronal apoptosis during retinal development. Cell 93:1171–1182 [View Article][PubMed]
    [Google Scholar]
  2. Alexander D. E., Ward S. L., Mizushima N., Levine B., Leib D. A. 2007; Analysis of the role of autophagy in replication of herpes simplex virus in cell culture. J Virol 81:12128–12134 [View Article][PubMed]
    [Google Scholar]
  3. Aubert M., Blaho J. A. 2003; Viral oncoapoptosis of human tumor cells. Gene Ther 10:1437–1445 [View Article][PubMed]
    [Google Scholar]
  4. Aubert M., O’Toole J., Blaho J. A. 1999; Induction and prevention of apoptosis in human HEp-2 cells by herpes simplex virus type 1. J Virol 73:10359–10370[PubMed]
    [Google Scholar]
  5. Behrens J., Jerchow B.-A., Würtele M., Grimm J., Asbrand C., Wirtz R., Kühl M., Wedlich D., Birchmeier W. 1998; Functional interaction of an axin homolog, conductin, with β-catenin, APC, and GSK3β. Science 280:596–599 [View Article][PubMed]
    [Google Scholar]
  6. Bryant K. F., Yan Z., Dreyfus D. H., Knipe D. M. 2012; Identification of a divalent metal cation binding site in herpes simplex virus 1 (HSV-1) ICP8 required for HSV replication. J Virol 86:6825–6834 [View Article][PubMed]
    [Google Scholar]
  7. Chen S.-Y, Chiu L.-Y., Maa M.-C., Wang J.-S., Chien C.-L., Lin W.-W. 2011; zVAD-induced autophagic cell death requires c-Src-dependent ERK and JNK activation and reactive oxygen species generation. Autophagy 7:217–228 [View Article][PubMed]
    [Google Scholar]
  8. Choi E.-J., Kim S.-M., Song K.-J., Lee J.-M., Kee S.-H. 2011; Axin1 expression facilitates cell death induced by aurora kinase inhibition through PARP activation. J Cell Biochem 112:2392–2402 [View Article][PubMed]
    [Google Scholar]
  9. Degterev A., Huang Z., Boyce M., Li Y., Jagtap P., Mizushima N., Cuny G. D., Mitchison T. J., Moskowitz M. A., Yuan J. 2005; Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1:112–119 [View Article][PubMed]
    [Google Scholar]
  10. Dupont P., Besson M.-T., Devaux J., Liévens J.-C. 2012; Reducing canonical Wingless/Wnt signaling pathway confers protection against mutant Huntingtin toxicity in Drosophila . Neurobiology Dis 47:237–247 [View Article][PubMed]
    [Google Scholar]
  11. Egger-Adam D., Katanaev V. L. 2008; Trimeric G protein-dependent signaling by Frizzled receptors in animal development. Front Biosci 13:4740–4755 [View Article][PubMed]
    [Google Scholar]
  12. Egger-Adam D., Katanaev V. L. 2010; The trimeric G protein Go inflicts a double impact on axin in the Wnt/frizzled signaling pathway. Dev Dyn 239:168–183 [View Article][PubMed]
    [Google Scholar]
  13. English L., Chemali M., Duron J., Rondeau C., Laplante A., Gingras D., Alexander D., Leib D., Norbury C. other authors 2009; Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat Immunol 10:480–487 [View Article][PubMed]
    [Google Scholar]
  14. Galvan V., Roizman B. 1998; Herpes simplex virus 1 induces and blocks apoptosis at multiple steps during infection and protects cells from exogenous inducers in a cell-type-dependent manner. Proc Natl Acad Sci U S A 95:3931–3936 [View Article][PubMed]
    [Google Scholar]
  15. Galvan V., Brandimarti R., Roizman B. 1999; Herpes simplex virus 1 blocks caspase-3-independent and caspase-dependent pathways to cell death. J Virol 73:3219–3226[PubMed]
    [Google Scholar]
  16. Godin J. D., Poizat G., Hickey M. A., Maschat F., Humbert S. 2010; Mutant huntingtin-impaired degradation of β-catenin causes neurotoxicity in Huntington’s disease. EMBO J 29:2433–2445 [View Article][PubMed]
    [Google Scholar]
  17. Grondin B., DeLuca N. 2000; Herpes simplex virus type 1 ICP4 promotes transcription preinitiation complex formation by enhancing the binding of TFIID to DNA. J Virol 74:11504–11510 [View Article][PubMed]
    [Google Scholar]
  18. Hanson C. A., Miller J. R. 2005; Non-traditional roles for the adenomatous polyposis coli (APC) tumor suppressor protein. Gene 361:1–12 [View Article][PubMed]
    [Google Scholar]
  19. Huang S.-M. A., Mishina Y. M., Liu S., Cheung A., Stegmeier F., Michaud G. A., Charlat O., Wiellette E., Zhang Y. other authors 2009; Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461:614–620 [View Article][PubMed]
    [Google Scholar]
  20. Ishidate T., Matsumine A., Toyoshima K., Akiyama T. 2000; The APC-hDLG complex negatively regulates cell cycle progression from the G0/G1 to S phase. Oncogene 19:365–372 [View Article][PubMed]
    [Google Scholar]
  21. Itoh K., Krupnik V. E., Sokol S. Y. 1998; Axis determination in Xenopus involves biochemical interactions of axin, glycogen synthase kinase 3 and β-catenin. Curr Biol 8:591–594 [View Article][PubMed]
    [Google Scholar]
  22. Jeon S. H., Yoon J. Y., Park Y. N., Jeong W. J., Kim S., Jho E. H., Surh Y. J., Choi K. Y. 2007; Axin inhibits extracellular signal-regulated kinase pathway by Ras degradation via β-catenin. J Biol Chem 282:14482–14492 [View Article][PubMed]
    [Google Scholar]
  23. Kim S.-M., Choi E.-J., Song K.-J., Kim S., Seo E., Jho E.-H., Kee S.-H. 2009; Axin localizes to mitotic spindles and centrosomes in mitotic cells. Exp Cell Res 315:943–954 [View Article][PubMed]
    [Google Scholar]
  24. Kishida S., Yamamoto H., Ikeda S., Kishida M., Sakamoto I., Koyama S., Kikuchi A. 1998; Axin, a negative regulator of the Wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of β-catenin. J Biol Chem 273:10823–10826 [View Article][PubMed]
    [Google Scholar]
  25. Koval A., Purvanov V., Egger-Adam D., Katanaev V. L. 2011; Yellow submarine of the Wnt/Frizzled signaling: submerging from the G protein harbor to the targets. Biochem Pharmacol 82:1311–1319 [View Article][PubMed]
    [Google Scholar]
  26. Koyama A. H., Adachi A. 1997; Induction of apoptosis by herpes simplex virus type 1. J Gen Virol 78:2909–2912[PubMed]
    [Google Scholar]
  27. Kraft R. M., Nguyen M. L., Yang X.-H., Thor A. D., Blaho J. A. 2006; Caspase 3 activation during herpes simplex virus 1 infection. Virus Res 120:163–175 [View Article][PubMed]
    [Google Scholar]
  28. Lee E., Salic A., Krüger R., Heinrich R., Kirschner M. W. 2003; The roles of APC and axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol 1:e10 [View Article][PubMed]
    [Google Scholar]
  29. Li Q., Wang X., Wu X., Rui Y., Liu W., Wang J., Wang X., Liou Y.-C., Ye Z., Lin S.-C. 2007; Daxx cooperates with the axin/HIPK2/p53 complex to induce cell death. Cancer Res 67:66–74 [View Article][PubMed]
    [Google Scholar]
  30. Li Q., Lin S., Wang X., Lian G., Lu Z., Guo H., Ruan K., Wang Y., Ye Z. other authors 2009; Axin determines cell fate by controlling the p53 activation threshold after DNA damage. Nat Cell Biol 11:1128–1134 [View Article][PubMed]
    [Google Scholar]
  31. McCartney B. M., Näthke I. S. 2008; Cell regulation by the Apc protein: Apc as master regulator of epithelia. Curr Opin Cell Biol 20:186–193 [View Article][PubMed]
    [Google Scholar]
  32. McFarlane S., Aitken J., Sutherland J. S., Nicholl M. J., Preston V. G., Preston C. M. 2011; Early induction of autophagy in human fibroblasts after infection with human cytomegalovirus or herpes simplex virus 1. J Virol 85:4212–4221 [View Article][PubMed]
    [Google Scholar]
  33. Morin P. J., Vogelstein B., Kinzler K. W. 1996; Apoptosis and APC in colorectal tumorigenesis. Proc Natl Acad Sci U S A 93:7950–7954 [View Article][PubMed]
    [Google Scholar]
  34. Neo S. Y., Zhang Y., Yaw L. P., Li P., Lin S.-C. 2000; Axin-induced apoptosis depends on the extent of its JNK activation and its ability to down-regulate β-catenin levels. Biochem Biophys Res Commun 272:144–150 [View Article][PubMed]
    [Google Scholar]
  35. Nguyen M. L., Blaho J. A. 2006; Apoptosis during herpes simplex virus infection. In Advances in Virus Research pp. 67–97 Edited by Karl M., Aaron J. S. San Diego, CA: Academic Press;
    [Google Scholar]
  36. Nguyen M. L., Kraft R. M., Blaho J. A. 2005; African green monkey kidney Vero cells require de novo protein synthesis for efficient herpes simplex virus 1-dependent apoptosis. Virology 336:274–290 [View Article][PubMed]
    [Google Scholar]
  37. Orvedahl A., Alexander D., Tallóczy Z., Sun Q., Wei Y., Zhang W., Burns D., Leib D. A., Levine B. 2007; HSV-1 ICP34.5 confers neurovirulence by targeting the beclin 1 autophagy protein. Cell Host Microbe 1:23–35 [CrossRef]
    [Google Scholar]
  38. Pei Y., Chen Z.-P., Ju H.-Q., Komatsu M., Ji Y. H., Liu G., Guo C. W., Zhang Y.-J., Yang C.-R. other authors 2011; Autophagy is involved in anti-viral activity of pentagalloylglucose (PGG) against herpes simplex virus type 1 infection in vitro . Biochem Biophys Res Commun 405:186–191 [View Article][PubMed]
    [Google Scholar]
  39. Ravikumar B., Imarisio S., Sarkar S., O’Kane C. J., Rubinsztein D. C. 2008; Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J Cell Sci 121:1649–1660 [View Article][PubMed]
    [Google Scholar]
  40. Roizman B. 1974; Herpesviruses, latency and cancer: a biochemical approach. J Reticuloendothel Soc 15:312–321[PubMed]
    [Google Scholar]
  41. Salahshor S., Woodgett J. R. 2005; The links between axin and carcinogenesis. J Clin Pathol 58:225–236 [View Article][PubMed]
    [Google Scholar]
  42. Shin J. H., Kim H. W., Rhyu I. J., Song K. J., Kee S. H. 2012; Axin expression reduces staurosporine-induced mitochondria-mediated cell death in HeLa cells. Exp Cell Res 318:2022–2033 [View Article][PubMed]
    [Google Scholar]
  43. Van Noorden C. J. 2001; The history of Z-VAD-FMK, a tool for understanding the significance of caspase inhibition. Acta Histochem 103:241–251 [View Article][PubMed]
    [Google Scholar]
  44. Vercammen D., Beyaert R., Denecker G., Goossens V., Van Loo G., Declercq W., Grooten J., Fiers W., Vandenabeele P. 1998a; Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 187:1477–1485 [View Article][PubMed]
    [Google Scholar]
  45. Vercammen D., Brouckaert G., Denecker G., Van de Craen M., Declercq W., Fiers W., Vandenabeele P. 1998b; Dual signaling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J Exp Med 188:919–930 [View Article][PubMed]
    [Google Scholar]
  46. Wang X., Patenode C., Roizman B. 2011; US3 protein kinase of HSV-1 cycles between the cytoplasm and nucleus and interacts with programmed cell death protein 4 (PDCD4) to block apoptosis. Proc Natl Acad Sci U S A 108:14632–14636 [View Article][PubMed]
    [Google Scholar]
  47. Whitley R. J., Roizman B. 2001; Herpes simplex virus infections. Lancet 357:1513–1518 [View Article][PubMed]
    [Google Scholar]
  48. Wood L. W., Shillitoe E. J. 2011; Effect of a caspase inhibitor, zVADfmk, on the inhibition of breast cancer cells by herpes simplex virus type 1. Cancer Gene Ther 18:685–694 [View Article][PubMed]
    [Google Scholar]
  49. Wu Y. T., Tan H. L., Huang Q., Sun X. J., Zhu X., Shen H. M. 2011; zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFα mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ 18:26–37 [View Article][PubMed]
    [Google Scholar]
  50. Ye Y. C., Yu L., Wang H. J., Tashiro S., Onodera S., Ikejima T. 2011; TNFα-induced necroptosis and autophagy via supression of the p38-NF-κB survival pathway in L929 cells. J Pharmacol Sci 117:160–169 [View Article][PubMed]
    [Google Scholar]
  51. Zeng L., Fagotto F., Zhang T., Hsu W., Vasicek T. J., Perry W. L. III, Lee J. J., Tilghman S. M., Gumbiner B. M., Costantini F. 1997; The mouse Fused locus encodes axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90:181–192 [View Article][PubMed]
    [Google Scholar]
  52. Zhang Y. G., Wu S., Xia Y., Chen D., Petrof E. O., Claud E. C., Hsu W., Sun J. 2012; Axin1 prevents Salmonella invasiveness and inflammatory response in intestinal epithelial cells. PLoS ONE 7:e34942 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.051540-0
Loading
/content/journal/jgv/10.1099/vir.0.051540-0
Loading

Data & Media loading...

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