1887

Journal of General Virology header logo

Volume 75, Issue 9

Oral-oesophageal inoculation of mice with herpes simplex virus type 1 causes latent infection of the vagal sensory ganglia (nodose ganglia) Free

Abstract

Herpes simplex virus type 1 (HSV-1) gingivostomatitis during childhood is known to result in a latent infection of the trigeminal ganglion neurons, which innervate the oral mucosa. During latency the viral genome is maintained in a non-infectious state. However, stimuli such as stress, fever or localized trauma can cause HSV-1 to reactivate in neurons and produce recrudescent disease in the peripheral tissues. Recently, HSV-1 proteins and nucleic acids have been detected in biopsies from human duodenal and gastric ulcers, raising the possibility that HSV-1 latency within the enteric nervous system is involved in this chronic recurrent gastrointestinal disorder. The studies in mice described here were done to determine whether HSV-1 latency could be established in neurons that innervate the murine gut. We found that after either intraperitoneal or oral-oesophageal inoculation of mice, HSV-1 establishes a latent infection in nodose ganglia of the vagus nerve, whose sensory neurons project to the gastrointestinal tract. This animal model of HSV-1 latency in the vagal sensory ganglia will be useful to examine the possible relationship between HSV-1 and recurrent gastrointestinal disease.

  • Received:
  • Accepted:
  • Published Online:
© The Journal of General Virology 1994
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-75-9-2379
1994-09-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/75/9/JV0750092379.html?itemId=/content/journal/jgv/10.1099/0022-1317-75-9-2379&mimeType=html&fmt=ahah

References

  1. Altschuler S, Bao X., Bieger D., Hopkins D. A., Miselis R. R. 1989; Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. Journal of Comparative Neurology 283:248–268
     [Google Scholar]
  2. Andrews P. L. R. 1986; Vagal afferent innervation of the gastrointestinal tract. Progressive Brain Research 67:65–86
     [Google Scholar]
  3. Baringer J. R., Swoveland P. 1973; Recovery of herpes simplex virus from human trigeminal ganglions. New England Journal of Medicine 288:648–650
     [Google Scholar]
  4. Bastian F. O., Rabson A. S., Yee C. L., Tralka T. S. 1972; Herpesvirus hominis: isolation from human trigeminal ganglion. Science 178:306–307
     [Google Scholar]
  5. Becker Y., Hadar J., Tabor E., Ben-Hur T., Raibstein I., Rosen A., Darai G. 1986; A sequence in Hpal-P fragment of herpes simplex virus-1 DNA determines intraperitoneal virulence in mice. Virology 149:255–259
     [Google Scholar]
  6. Berthoud H. R., Powley T. L. 1992; Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. Journal of Comparative Neurology 319:261–276
     [Google Scholar]
  7. Berthoud H. R., Jedrzejewska A., Powley T. L. 1990; Simultaneous labeling of vagal innervation of the gut and afferent projections from the visceral forebrain with dil injected into the dorsal vagal complex in the rat. Journal of Comparative Neurology 301:65–79
     [Google Scholar]
  8. Brown S. M., Ritchie D. A., Subak-Sharpe J. H. 1973; Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. Journal of General Virology 18:329–346
     [Google Scholar]
  9. Buddingh G. J., Schrum D. I., Lanier J. C., Guidry D. J. 1953; Studies of the natural history of herpes simplex virus infections. Pediatrics 11:595–610
     [Google Scholar]
  10. Buss D. H., Scharyl M. 1979; Herpesvirus infection of the esophagus and other visceral organs in adults. American Journal of Medicine 66:457–462
     [Google Scholar]
  11. Card J. P., Rinaman L., Schwaber J. S., Miselis R. R., Whealy M. E., Robbins A. K., Enquist L. W. 1990; Neutrotrophic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. Journal of Neuroscience 10:1974–1994
     [Google Scholar]
  12. Corey L., Spear P. G. 1986a; Infections with herpes simplex viruses. New England Journal of Medicine 314:686–691
     [Google Scholar]
  13. Corey L., Spear P. G. 1986b; Infections with herpes simplex viruses. New England Journal of Medicine 314:749–757
     [Google Scholar]
  14. Deatly A. M., Spivack J. G., Lavi E., O’Boyle D. R.II Fraser N. W. 1988; Latent herpes simplex virus type 1 transcripts in peripheral and central nervous system tissues of mice map to similar regions of the viral genome. Journal of Virology 62:749–756
     [Google Scholar]
  15. Deshmukh M., Shah R., McCallum R. N. 1984; Experience with herpes esophagitis in otherwise healthy patients. American Journal of Gastroenterology 79:173–176
     [Google Scholar]
  16. Dix R. D., McKendall R. R., Baringer J. R. 1983; Comparative neurovirulence of herpes simplex virus type 1 strain after peripheral or intracerebral inoculation of BALB/c mice. Infection and Immunity 40:103–112
     [Google Scholar]
  17. Ejercito P. M., Kieff E. D., Roizman B. 1968; Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. Journal of General Virology 2:357–364
     [Google Scholar]
  18. Fawl R. L., Roizman B. 1993; Induction of reactivation of herpes simplex virus in murine sensory ganglia in vivo by cadmium. Journal of Virology 67:7025–7031
     [Google Scholar]
  19. Fraser N. W., Spivack J. G., Wroblewska Z., Block T., Deshmane S. L., Valyi-Nagy T., Natarajan R., Gesser R. M. 1991; A review of the molecular mechanism of HSV-1 latency. Current Eye Research 10: Supplement 1–14
     [Google Scholar]
  20. Ginaldi S., Burgert W., Paulk T. 1987; Herpes esophagitis in immunocompetent patients. American Family Physician 36:160–164
     [Google Scholar]
  21. Hale B. D., Rendtorff R. C., Walker L. C., Roberts A. N. 1963; Epidemic hepetic stomatitis in an orphanage nursery. Journal of the American Medical Association 183:1068–1072
     [Google Scholar]
  22. Henken D. B., Martin J. R. 1991; Herpes simplex virus infection in populations of mouse dorsal root ganglion neurons: effects of inoculation route and virus strain. Journal of Neurological Science 105:29–36
     [Google Scholar]
  23. Hsu S. M., Raine L., Fanger H. 1981; Use of avidin- biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled (PAP) procedures. Journal of Histochemistry & Cytochemistry 29:577–580
     [Google Scholar]
  24. Irie H., Harada Y., Kataoka M., Nagamuta M., Moriya Y., Handa M., Saito M., Matsubara S., Kohima K., Sugawara Y. 1992; Efficacy of oral administration of live herpes simplex virus type 1 as a vaccine. Journal of Virology 66:2428–2434
     [Google Scholar]
  25. Irie H., Shimeld C., Williams N., Hill T. 1993; Protection against ocular and cutaneous infection with herpes simplex virus type 1 by intragastric immunization with live virus. Journal of General Virology 74:1357–1362
     [Google Scholar]
  26. Kaufman H. E. 1978; Herpetic keratitis: Proctor lecture. Investigative Ophthalmology and Visual Science 17:941–957
     [Google Scholar]
  27. Knotts F. B., Cook M. L., Stevens J. G. 1974; Pathogenesis of herpetic encephalitis in mice after ophthalmic inoculation. Journal of Infectious Diseases 130:16–27
     [Google Scholar]
  28. Krinke G. J., Dietrich F. M. 1990; Transneuronal spread of intraperitoneally administered herpes simplex virus type 1 from the abdomen via the vagus nerve to the brains of mice. Journal of Comparative Pathology 103:301–306
     [Google Scholar]
  29. Lohr J. M., Nelson J. A., Oldstone M. B. A. 1990; Is herpes simplex virus associated with peptic ulcer disease. Journal of Virology 64:2168–2174
     [Google Scholar]
  30. McBane R. D., Gross J. B. 1991; Herpes esophagitis: clinical syndrome, endoscopic appearance and diagnosis in 23 patients. Gastrointestinal Endoscopy 37:600–603
     [Google Scholar]
  31. McLennan J. L., Darby G. 1980; Herpes simplex virus latency: the cellular location of virus in dorsal root ganglia and the fate of the infected cell following virus activation. Journal of General Virology 51:233–243
     [Google Scholar]
  32. Nahmias A. J., Roizman B. 1973; Infection with herpes simplex viruses 1 and 2. New England Journal of Medicine 289:781–789
     [Google Scholar]
  33. Roizman B., Sears A. E. 1987; An inquiry into the mechanisms of herpes simplex virus latency. Annual Review of Microbiology 41:543–571
     [Google Scholar]
  34. Sedarati F., Stevens J. G. 1987; Biological basis for virulence of three strains of herpes simplex virus type 1. Journal of General Virology 68:2389–2395
     [Google Scholar]
  35. Sedarati F., Margolis T. P., Stevens J. G. 1993; Latent infection can be established with drastically restricted transcription and replication of the HSV-1 genome. Virology 192:687–691
     [Google Scholar]
  36. Spruance S. L. 1984; Pathogenesis of herpes simplex virus labialis: excretion of virus in the oral cavity. Journal of Clinical Microbiology 19:675–679
     [Google Scholar]
  37. Steiner I., Spivack J. G., Deshmane S. L., Ace C. I., Preston C. M., Fraser N. W. 1990; A herpes simplex virus type 1 mutant containing a non-transinducing Vmw65 protein establishes latent infection in vivo in the absence of viral replication and reactivates efficiently from explanted trigeminal ganglia. Journal of Virology 64:1630–1638
     [Google Scholar]
  38. Stoker M. G. P., Ross R. W. 1958; Quantitative studies on the growth of herpesvirus in HeLa cells. Journal of General Microbiology 19:250–266
     [Google Scholar]
  39. Thompson R. L., Cook M. L., Devi-Rao G. B., Wagner E. K., Stevens J. G. 1986; Function and molecular analysis of the avirulent wild-type herpes simplex virus type 1 strain KOS. Journal of Virology 58:203–211
     [Google Scholar]
  40. Ugolini G. 1992; Transneuronal transfer of herpes simplex virus type 1 (HSV-1) from mixed limb nerves to CNS. I. Sequence of transfer from sensory, motor and sympathetic nerve fibers to the spinal cord. Journal of Comparative Neurology 326:527–548
     [Google Scholar]
  41. Ugolini G., Kuypers H. G. J. M., Strick P. L. 1989; Transneuronal transfer of herpes virus from peripheral nerves to cortex and brainstem. Science 243:89–91
     [Google Scholar]
  42. Valyi-Nagy T., Deshmane S. L., Raengsakulrach B., Nicosia M., Gesser R. M., Wysocka M., Dillner A., Fraser N. W. 1992; Herpes simplex virus type 1 mutant strain ml814 establishes a unique, slowly progressing infection in SCID mice. Journal of Virology 66:7336–7345
     [Google Scholar]
  43. Warren K. G., Gilden D. H., Brown S. M., Devlin M., Wroblewska Z., Subak-Sharpe J., Koprowski H. 1977; Isolation of latent herpes simplex virus from human trigeminal ganglia including ganglia from one patient with multiple sclerosis. Lancet ii:637–639
     [Google Scholar]
  44. Warren K. G., Brown S. M., Wroblewska Z., Gilden D., Koprowski H., Subak-Sharpe J. 1978; Isolation of latent herpes simplex virus from the superior cervical and vagus ganglions of human beings. New England Journal of Medicine 298:1068–1069
     [Google Scholar]
  45. Whitley R. J. 1990; Herpes simplex viruses. In Fields Virology 2 pp. 1843–1887 Fields B. N., Knipe D. M., Chanock R. M. Edited by New York: Raven Press;
     [Google Scholar]
  46. Wildy P. 1954; The growth of herpes simplex virus. Australian Journal of Experimental Biology and Medical Science 32:605–620
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-75-9-2379
Loading
Oral-oesophageal inoculation of mice with herpes simplex virus type 1 causes latent infection of the vagal sensory ganglia (nodose ganglia)
J. Gen. Virol. 75, 2379 (1994); https://doi.org/10.1099/0022-1317-75-9-2379
/content/journal/jgv/10.1099/0022-1317-75-9-2379
/content/journal/jgv/10.1099/0022-1317-75-9-2379
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