1887

Journal of General Virology header logo

Volume 83, Issue 9

Susceptibility of sensory neurons to apoptosis following infection by bovine herpesvirus type 1 Free

Abstract

Like other members of the alpha subfamily of herpesviruses, bovine herpesvirus type 1 (BHV-1) establishes latent infections in sensory neurons. BHV-1 induces apoptosis in lymphoid cells and in epithelial cell lines, but the ability of BHV-1 to induce apoptosis in sensory neurons remains unknown. In this report, the susceptibility of rabbit ganglionic neurons to infection by BHV-1 was examined and . Following infection of cultured neurons with BHV-1, hallmarks of apoptosis such as chromatin condensation, DNA fragmentation and membrane blebbing were detected. The appearance of these changes was preceded by active viral DNA replication as determined by hybridization. When viral DNA replication was blocked by treatment of cultures with an inhibitor of eukaryotic DNA polymerases, apoptosis but not virus attachment to neurons or bICP0 gene expression was completely prevented. Taken together, these results demonstrate that sensory neurons are not intrinsically resistant to BHV-1-induced apoptosis and that viral DNA replication plays a role in triggering the apoptotic programme. Infection of rabbits with BHV-1 resulted in pathological changes in the trigeminal ganglia (TG) which included mononuclear cell infiltration and neuronophagia. Morphological evidence of apoptosis was not detected in neurons, even in cells with advanced cytophatology. Furthermore, whereas DNA fragmentation was common in infiltrating cells, it was very rare and sporadic in neurons. Therefore, mechanisms in the TG should exist to prevent neuronal apoptosis upon BHV-1 infection.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-9-2257
2002-09-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/9/0832257a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-9-2257&mimeType=html&fmt=ahah

References

  1. Ahmed M., Lock M., Miller C. G., Fraser N. W. 2002; Regions of the herpes simplex virus type 1 latency-associated transcript that protect cells from apoptosis in vitro and protect neuronal cells in vivo. Journal of Virology 76:717–729
     [Google Scholar]
  2. Aleman N., Quiroga M. I., Lopez Peña M., Vázquez S., Guerrero F. H., Nieto J. M. 2001; Induction and inhibition of apoptosis by pseudorabies virus in the trigeminal ganglion during acute infection of swine. Journal of Virology 75:469–479
     [Google Scholar]
  3. Allsopp T. E., Fazakerley J. K. 2000; Altruistic cell suicide and the specialized case of the virus-infected nervous system. Trends in Neurosciences 23:284–290
     [Google Scholar]
  4. Chao C. C., Hu S., Ehrlich L., Peterson P. K. 1995; Interleukin-1 and tumor necrosis factor-α synergistically mediate neurotoxicity: involvement of nitric oxide and of N-methyl-d-aspartate receptors. Brain Behavior and Immunity 9:355–365
     [Google Scholar]
  5. Ciacci-Zanella J., Stone M., Henderson G., Jones C. 1999; The latency-related gene of bovine herpesvirus 1 inhibits programmed cell death. Journal of Virology 73:9734–9740
     [Google Scholar]
  6. Delhon G. 1990; In vitro interactions between bovine herpesvirus type 1 and sensory neurons . MS thesis University of Nebraska–Lincoln; USA:
     [Google Scholar]
  7. Devireddy L. R., Jones C. 1999; Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. Journal of Virology 73:3778–3788
     [Google Scholar]
  8. Dyanov H. M., Dzitoeva S. G. 1995; Isolation of DNA-free RNA from a very small number of cells. Biotechniques 18:559–562
     [Google Scholar]
  9. Eskra L., Splitter G. A. 1997; Bovine herpesvirus-1 infects activated CD4+ lymphocytes. Journal of General Virology 78:2159–2166
     [Google Scholar]
  10. Freeman R. S., Estus S., Johnson E. M. 1994; Analysis of cell cycle-related gene expression in post mitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12:343–355
     [Google Scholar]
  11. Hannon E., Vanderplasschen A., Lyaku J., Keil G., Denis M., Pastoret P. P. 1996; Inactivated bovine herpesvirus 1 induces apoptotic cell death of mitogen-stimulated bovine peripheral blood mononuclear cells. Journal of Virology 70:4116–4120
     [Google Scholar]
  12. Hannon E., Hoornaert S., Dequiedt F., Vanderplasschen A., Lyaku J., Willems L., Pastoret P. P. 1997; Bovine herpesvirus 1-induced apoptosis occurs at the G0/G1 phase of the cell cycle. Virology 232:351–358
     [Google Scholar]
  13. Hannon E., Meyer G., Vanderplasschen A., Dessy-Doizé C., Thiry E., Pastoret P. P. 1998; Attachment but not penetration of bovine herpesvirus 1 is necessary to induce apoptosis in target cells. Journal of Virology 72:7638–7641
     [Google Scholar]
  14. Homan E. J., Easterday B. C. 1980; Isolation of bovine herpes virus 1 from trigeminal ganglia of clinically normal cattle. American Journal of Veterinary Research 41:1212–1213
     [Google Scholar]
  15. Hossain A., Schang L. M., Jones C. 1995; Identification of gene products encoded by the latency-related gene of bovine herpesvirus 1. Journal of Virology 69:5345–5352
     [Google Scholar]
  16. Inman M., Zhang Y., Geiser V., Jones C. 2001; The zinc ring finger in the bICP0 protein encoded by bovine herpesvirus-1 mediates toxicity and activates productive infection. Journal of General Virology 82:483–492
     [Google Scholar]
  17. Jones C. 1998; Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Advances in Virus Research 51:81–133
     [Google Scholar]
  18. Jones C., Delhon G., Bratanich A., Kutish G., Rock D. 1990; Analysis of the transcriptional promoter which regulates the latency-related transcript of bovine herpesvirus 1. Journal of Virology 64:1164–1170
     [Google Scholar]
  19. Kosz-Vnenchak M., Coen D. M., Knipe D. M. 1990; Restricted expression of herpes simplex virus lytic genes during establishment of latent infection by thymidine kinase-negative mutant viruses. Journal of Virology 64:5396–5402
     [Google Scholar]
  20. Kosz-Vnenchak M., Jacobson J., Coen D. M., Knipe D. M. 1993; Evidence for a novel regulatory pathway for herpes simplex virus gene expression in trigeminal ganglion neurons. Journal of Virology 67:5383–5393
     [Google Scholar]
  21. Lee E. Y.-H. P., Hu N., Yuan S.-S. F., Cox L. A., Bradley A., Lee W.-H., Herrup K. 1994; Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes & Development 8:2008–2021
     [Google Scholar]
  22. Marheineke K., Hyrien O. 2001; Aphidicolin triggers a block to replication origin in Xenopus egg extracts. Journal of Biological Chemistry 276:17092–17100
     [Google Scholar]
  23. Martin S. J., Reutelingsperger C. P., McGahon A. J., Rader J. A., van Schie R. C., LaFace D. M., Green D. R. 1995; Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. Journal of Experimental Medicine 182:1545–1556
     [Google Scholar]
  24. Nichol P. F., Chang J. Y., Johnson E. M., Olivo P. D. 1996; Herpes simplex virus gene expression in neurons: viral DNA synthesis is a critical regulatory event in the branch point between the lytic and latent pathways. Journal of Virology 70:5476–5486
     [Google Scholar]
  25. Nishiyama Y., Suzuki S., Yamauchi M., Maeno K., Yoshida S. 1984; Characterization of an aphidicolin-resistant mutant of herpes simplex virus type 2 which induces an altered viral DNA polymerase. Virology 135:87–96
     [Google Scholar]
  26. Perng G., Jones C., Ciacci-Zanella J., Stone M., Henderson G., Yukht A., Slanina S. M., Hofman F. M., Ghiasi H., Nesburn A. B., Wechsler S. L. 2000; Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript. Science 287:1500–1503
     [Google Scholar]
  27. Rock D. L. 1993; Latent infection with bovine herpesvirus type 1. Seminars in Virology 5:233–240
     [Google Scholar]
  28. Rock D. L. 1994; The molecular basis of latent infections by alphaherpesviruses. Seminars in Virology 4:157–165
     [Google Scholar]
  29. Rock D. L., Hagemoser W. A., Osorio F. A., Reed D. E. 1987; Detection of bovine herpesvirus type 1 RNA in trigeminal ganglia of latently infected rabbits by in situ hybridization. Journal of General Virology 67:2515–2520
     [Google Scholar]
  30. Rock D. L., Lokensgard J. R., Lewis T. L., Kutish G. F. 1992; Molecular characterization of dexamethasone induced reactivation of latent bovine herpesvirus type 1 infection. Journal of Virology 66:2484–2490
     [Google Scholar]
  31. Ross M. E. 1996; Cell division and the nervous system: regulating the cycle from neural differentiation to death. Trends in Neurosciences 19:62–68
     [Google Scholar]
  32. Schang L. M., Jones C. 1997; Analysis of bovine herpesvirus 1 transcripts during a primary infection of trigeminal ganglia of cattle. Journal of Virology 71:6786–6795
     [Google Scholar]
  33. Schang L. M., Hossain A., Jones C. 1996; The latency-related gene of bovine herpesvirus 1 encodes a product which inhibits cell cycle progression. Journal of Virology 70:3807–3814
     [Google Scholar]
  34. Sei Y., Vitkovic L., Yokoyama M. M. 1995; Cytokines in the central nervous system: regulatory roles in neuronal function, cell death and repair. Neuroimmunomodulation 2:121–133
     [Google Scholar]
  35. Shen Y., Shenk T. 1995; Viruses and apoptosis. Current Opinion in Genetics & Development 5:105–111
     [Google Scholar]
  36. Shimeld C., Easty D. L., Hill T. J. 1999; Reactivation of herpes simplex virus type 1 in the mouse trigeminal ganglion: an in vivo study of virus antigen and cytokines. Journal of Virology 73:1767–1773
     [Google Scholar]
  37. Snowdon W. A. 1965; The IBR-IPV: reaction to infection and intermittent recovery of virus from experimentally infected cattle. Australian Veterinary Journal 41:135–142
     [Google Scholar]
  38. Stevens J. G., Wagner E. K., Devi-Rao G. B., Cook M. L., Feldman L. 1987; RNA complementary to a herpesvirus alpha gene mRNA is prominent in latently infected neurons. Science 235:1056–1059
     [Google Scholar]
  39. Teodoro J. G., Branton P. E. 1997; Regulation of apoptosis by viral gene products. Journal of Virology 71:1739–1746
     [Google Scholar]
  40. Thompson R. L., Sawtell N. M. 2001; Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. Journal of Virology 75:6660–6675
     [Google Scholar]
  41. Trump B. F., Berezesky I. K. 1998; The reactions of cells to lethal injury: oncosis and necrosis. The role of calcium. In When Cells Die. A Comprehensive Evaluation of Apoptosis and Programmed Cell Death pp 57–96 Edited by Lockshim R. A., Zakeri Z., Tilly J. L. New York: Wiley–Liss;
     [Google Scholar]
  42. Winkler M. T. C., Doster A., Jones C. 1999; Bovine herpesvirus 1 can infect CD4+ T lymphocytes and induce programmed cell death during acute infection of cattle. Journal of Virology 73:8657–8668
     [Google Scholar]
  43. Winkler M. T., Schang L. M., Doster A., Holt T., Jones C. 2000; Analysis of cyclins in trigeminal ganglia of calves infected with bovine herpesvirus-1. Journal of General Virology 81:2993–2998
     [Google Scholar]
  44. Wirth U. V., Gunkel K., Engels M., Schwyzer M. 1989; Spatial and temporal distribution of bovine herpesvirus 1 transcripts. Journal of Virology 63:4882–4889
     [Google Scholar]
  45. Wirth U. V., Fraefel C., Vogt B., Vlcek C., Paces V., Schwyzer M. 1992; Immediate-early RNA 2.9 and early 2.6 of bovine herpesvirus 1 are 3′ coterminal and encode a putative zinc finger transactivation protein. Journal of Virology 66:2763–2772
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-9-2257
Loading
Susceptibility of sensory neurons to apoptosis following infection by bovine herpesvirus type 1
J. Gen. Virol. 83, 2257 (2002); https://doi.org/10.1099/0022-1317-83-9-2257
/content/journal/jgv/10.1099/0022-1317-83-9-2257
/content/journal/jgv/10.1099/0022-1317-83-9-2257
Loading

Data & Media loading...

Most cited 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