1887

Abstract

Non-human primate herpesviruses establish and maintain a lifelong persistent infection in immunocompetent hosts in the absence of clinical signs of disease. A fundamental issue for understanding the natural history of non-human primate herpesviruses is whether the viruses are maintained in a truly latent state or one characterized by a low level of chronic expression. To address this issue, a real-time PCR assay was developed to quantify (B virus) DNA in mucosal fluids of rhesus macaques. This assay was rapid, sensitive (10 genome copies) and specific for B virus obtained from multiple species of macaques. The shedding profile of B virus was compared to another endemic herpesvirus, rhesus cytomegalovirus (RhCMV), in colony-reared monkeys. Mucosal swabs or saliva samples were taken daily from two groups of seropositive monkeys undergoing either a stressful relocation (group 1) or daily chair restraint (group 2). B virus DNA was detected in mucosal fluids from four animals relocated during the breeding season (group 1) but not from 10 animals moved at other times of the year. No B virus DNA was detected in any group 2 monkey. In contrast, RhCMV DNA was detected in the majority of animals of both groups 1 and 2. Detection of B virus DNA shedding is a relatively rare event associated with the breeding season, while RhCMV DNA is persistently detected in mucosal fluids of most monkeys.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18808-0
2003-01-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/1/vir840083.html?itemId=/content/journal/jgv/10.1099/vir.0.18808-0&mimeType=html&fmt=ahah

References

  1. Alford, C. A. & Britt, W. J. ( 1993; ). Cytomegalovirus. In The Human Herpesviruses, pp. 227–255. Edited by B. Roizman, R. J. Whitley & C. Lopez. New York: Raven Press.
  2. Augenbraun, M., Feldman, J., Chirgwin, K., Zenilman, J., Clarke, L., DeHovitz, J., Landesman, S. & Minkoff, H. ( 1995; ). Increased genital shedding of herpes simplex virus type 2 in HIV-seropositive women. Ann Intern Med 123, 845–847.[CrossRef]
    [Google Scholar]
  3. Baroncelli, S., Barry, P. A., Capitanio, J. P., Lerche, N. W., Otsyula, M. & Mendoza, S. P. ( 1997; ). Cytomegalovirus and simian immunodeficiency virus coinfection: longitudinal study of antibody responses and disease progression. J Acquir Immune Defic Syndr Human Retrovirol 15, 5–15.[CrossRef]
    [Google Scholar]
  4. Barry, P. A., Alcendor, D. J., Power, M. D., Kerr, H. & Luciw, P. A. ( 1996; ). Nucleotide sequence and molecular analysis of the rhesus cytomegalovirus immediate-early gene and the UL121–117 open reading frames. Virology 215, 61–72.[CrossRef]
    [Google Scholar]
  5. Benedetti, J., Corey, L. & Ashley, R. ( 1994; ). Recurrence rates in genital herpes after symptomatic first-episode infection. Ann Intern Med 121, 847–854.[CrossRef]
    [Google Scholar]
  6. Benedetti, J. K., Zeh, J. & Corey, L. ( 1999; ). Clinical reactivation of genital herpes simplex virus infection decreases in frequency over time. Ann Intern Med 131, 14–20.[CrossRef]
    [Google Scholar]
  7. Black, D. H. & Eberle, R. ( 1997; ). Detection and differentiation of primate alpha-herpesviruses by PCR. J Vet Diagn Invest 9, 225–231.[CrossRef]
    [Google Scholar]
  8. Capitanio, J. P. & Lerche, N. W. ( 1998; ). Social separation, housing relocation, and survival in simian AIDS: a retrospective analysis. Psychosom Med 60, 235–244.
    [Google Scholar]
  9. Capitanio, J. P., Mendoza, S. P. & Lerche, N. W. ( 1998a; ). Individual differences in peripheral blood immunological and hormonal measures in adult male rhesus macaques (Macaca mulatta): evidence for temporal and situational consistency. Am J Primatol 44, 29–41.[CrossRef]
    [Google Scholar]
  10. Capitanio, J. P., Mendoza, S. P., Lerche, N. W. & Mason, W. A. ( 1998b; ). Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proc Natl Acad Sci U S A 95, 4714–4719.[CrossRef]
    [Google Scholar]
  11. Chellman, G. J., Lukas, V. S., Eugui, E. M., Altera, K. P., Almquist, S. J. & Hilliard, J. K. ( 1992; ). Activation of B virus (Herpesvirus simiae) in chronically immunosuppressed cynomolgus monkeys. Lab Anim Sci 42, 146–151.
    [Google Scholar]
  12. Cohen, J. ( 2000; ). AIDS research. Vaccine studies stymied by shortage of animals. Science 287, 959–960.[CrossRef]
    [Google Scholar]
  13. Cone, R. W., Hobson, A. C., Brown, Z., Ashley, R., Berry, S., Winter, C. & Corey, L. ( 1994; ). Frequent detection of genital herpes simplex virus DNA by polymerase chain reaction among pregnant women. JAMA (J Am Med Assoc) 272, 792–796.[CrossRef]
    [Google Scholar]
  14. Cook, S. D., Paveloff, M. J., Doucet, J. J., Cottingham, A. J., Sedarati, F. & Hill, J. M. ( 1991; ). Ocular herpes simplex virus reactivation in mice latently infected with latency-associated transcript mutants. Invest Ophthalmol Vis Sci 32, 1558–1561.
    [Google Scholar]
  15. Coyle, P. V., Desai, A., Wyatt, D., McCaughey, C. & O'Neill, H. J. ( 1999; ). A comparison of virus isolation, indirect immunofluorescence and nested multiplex polymerase chain reaction for the diagnosis of primary and recurrent herpes simplex type 1 and type 2 infections. J Virol Methods 83, 75–82.[CrossRef]
    [Google Scholar]
  16. Daniel, Y., Gull, I., Peyser, M. R. & Lessing, J. B. ( 1995; ). Congenital cytomegalovirus infection. Eur J Obstet Gynecol Reprod Biol 63, 7–16.[CrossRef]
    [Google Scholar]
  17. Diamond, C., Speck, C., Huang, M. L., Corey, L., Coombs, R. W. & Krieger, J. N. ( 2000; ). Comparison of assays to detect cytomegalovirus shedding in the semen of HIV-infected men. J Virol Methods 90, 185–191.[CrossRef]
    [Google Scholar]
  18. do Canto, C. L., Granato, C. F., Garcez, E., Villas Boas, L. S., Fink, M. C., Estevam, M. P. & Pannuti, C. S. ( 2000; ). Cytomegalovirus infection in children with Down syndrome in a day-care center in Brazil. Rev Inst Med Trop Sao Paulo 42, 179–183.[CrossRef]
    [Google Scholar]
  19. Eberle, R. & Hilliard, J. K. ( 1984; ). Replication of simian herpesvirus SA8 and identification of viral polypeptides in infected cells. J Virol 50, 316–324.
    [Google Scholar]
  20. Fidouh-Houhou, N., Duval, X., Bissuel, F. & 7 other authors ( 2001; ). Salivary cytomegalovirus (CMV) shedding, glycoprotein B genotype distribution, and CMV disease in human immunodeficiency virus-seropositive patients. Clin Infect Dis 33, 1406–1411.[CrossRef]
    [Google Scholar]
  21. Flo, R. W., Haukenes, G., Nilsen, A., Skjaerven, R., Forsgren, R. & Fehniger, T. E. ( 1995; ). Longitudinal study of cytomegalovirus antibodies in individuals infected with the human immunodeficiency virus. Eur J Clin Microbiol Infect Dis 14, 504–511.[CrossRef]
    [Google Scholar]
  22. Glaser, R. & Kiecolt-Glaser, J. K. ( 1997; ). Chronic stress modulates the virus-specific immune response to latent herpes simplex virus type 1. Ann Behav Med 19, 78–82.[CrossRef]
    [Google Scholar]
  23. Glaser, R., Friedman, S. B., Smyth, J. & 8 other authors ( 1999; ). The differential impact of training stress and final examination stress on herpesvirus latency at the United States Military Academy at West Point. Brain Behav Immun 13, 240–251.[CrossRef]
    [Google Scholar]
  24. Gradilone, A., Vercillo, R., Napolitano, M., Cardinali, G., Gazzaniga, P., Silvestri, I., Gandini, O., Tomao, S. & Agliano, A. M. ( 1996; ). Prevalence of human papillomavirus, cytomegalovirus, and Epstein–Barr virus in the cervix of healthy women. J Med Virol 50, 1–4.[CrossRef]
    [Google Scholar]
  25. Hahn, G., Jores, R. & Mocarski, E. S. ( 1998; ). Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc Natl Acad Sci U S A 95, 3937–3942.[CrossRef]
    [Google Scholar]
  26. Hilliard, J. K. & Ward, J. A. ( 1999; ). B-virus specific-pathogen-free breeding colonies of macaques (Macaca mulatta): retrospective study of seven years of testing. Lab Anim Sci 49, 144–148.
    [Google Scholar]
  27. Hilliard, J. K., Eberle, R., Lipper, S. L., Munoz, R. M. & Weiss, S. A. ( 1987; ). Herpesvirus simiae (B virus): replication of the virus and identification of viral polypeptides in infected cells. Arch Virol 93, 185–198.[CrossRef]
    [Google Scholar]
  28. Hirano, M., Nakamura, S., Okada, M., Ueda, M. & Mukai, R. ( 2000; ). Rapid discrimination of monkey B virus from human herpes simplex viruses by PCR in the presence of betaine. J Clin Microbiol 38, 1255–1257.
    [Google Scholar]
  29. Holmes, G. P., Chapman, L. E., Stewart, J. A., Straus, S. E., Hilliard, J. K. & Davenport, D. S. ( 1995; ). Guidelines for the prevention and treatment of B-virus infections in exposed persons. The B virus Working group. Clin Infect Dis 20, 421–439.[CrossRef]
    [Google Scholar]
  30. Kaufman, H. E., Varnell, E. D. & Thompson, H. W. ( 1999; ). Latanoprost increases the severity and recurrence of herpetic keratitis in the rabbit. Am J Ophthalmol 127, 531–536.[CrossRef]
    [Google Scholar]
  31. Kessler, M. J. & Hilliard, J. K. ( 1990; ). Seroprevalence of B virus (Herpesvirus simiae) in a naturally formed group of rhesus macaques. J Med Primatol 19, 155–160.
    [Google Scholar]
  32. Koelle, D. M. & Wald, A. ( 2000; ). Herpes simplex virus: the importance of asymptomatic shedding. J Antimicrob Chemother 45, 1–8.
    [Google Scholar]
  33. Koelle, D. M., Benedetti, J., Langenberg, A. & Corey, L. ( 1992; ). Asymptomatic reactivation of herpes simplex virus in women after the first episode of genital herpes. Ann Intern Med 116, 433–437.[CrossRef]
    [Google Scholar]
  34. Koelle, D. M., Posavad, C. M., Barnum, G. R., Johnson, M. L., Frank, J. M. & Corey, L. ( 1998; ). Clearance of HSV-2 from recurrent genital lesions correlates with infiltration of HSV-specific cytotoxic T lymphocytes. J Clin Invest 101, 1500–1508.[CrossRef]
    [Google Scholar]
  35. Kravitz, R. H., Sciabica, K. S., Cho, K., Luciw, P. A. & Barry, P. A. ( 1997; ). Cloning and characterization of rhesus cytomegalovirus glycoprotein B. J Gen Virol 78, 2009–2013.
    [Google Scholar]
  36. Krech, U. & Lewis, I. J. ( 1954; ). Propagation of B-virus in tissue cultures. Proc Soc Exp Biol Med 87, 174–178.[CrossRef]
    [Google Scholar]
  37. Lees, D. N., Baskerville, A., Cropper, L. M. & Brown, D. W. ( 1991; ). Herpesvirus simiae (B virus) antibody response and virus shedding in experimental primary infection of cynomolgus macaques. Lab Anim Sci 41, 360–364.
    [Google Scholar]
  38. Lee-Wing, M. W., Hodge, W. G. & Diaz-Mitoma, F. ( 1999; ). The prevalence of herpes family virus DNA in the conjunctiva of patients positive and negative for human immunodeficiency virus using the polymerase chain reaction. Ophthalmology 106, 350–354.[CrossRef]
    [Google Scholar]
  39. Lockridge, K. M., Sequar, G., Zhou, S. S., Yue, Y., Mandell, C. P. & Barry, P. A. ( 1999; ). Pathogenesis of experimental rhesus cytomegalovirus infection. J Virol 73, 9576–9583.
    [Google Scholar]
  40. Loomis-Huff, J. E., Eberle, R., Lockridge, K. M., Rhodes, G. & Barry, P. A. ( 2001; ). Immunogenicity of a DNA vaccine against herpes B virus. Vaccine 19, 4865–4873.[CrossRef]
    [Google Scholar]
  41. Lucht, E., Brytting, M., Bjerregaard, L., Julander, I. & Linde, A. ( 1998; ). Shedding of cytomegalovirus and herpesviruses 6, 7, and 8 in saliva of human immunodeficiency virus type 1-infected patients and healthy controls. Clin Infect Dis 27, 137–141.[CrossRef]
    [Google Scholar]
  42. Madhavan, H. N., Priya, K., Anand, A. R. & Therese, K. L. ( 1999; ). Detection of herpes simplex virus (HSV) genome using polymerase chain reaction (PCR) in clinical samples comparison of PCR with standard laboratory methods for the detection of HSV. J Clin Virol 14, 145–151.[CrossRef]
    [Google Scholar]
  43. Mosimann, F., Cuenoud, P. F., Steinhauslin, F. & Wauters, J. P. ( 1994; ). Herpes simplex esophagitis after renal transplantation. Transplant Int 7, 79–82.[CrossRef]
    [Google Scholar]
  44. Mostad, S. B., Kreiss, J. K., Ryncarz, A., Chohan, B., Mandaliya, K., Ndinya-Achola, J., Bwayo, J. J. & Corey, L. ( 2000; ). Cervical shedding of herpes simplex virus and cytomegalovirus throughout the menstrual cycle in women infected with human immunodeficiency virus type 1. Am J Obstet Gynecol 183, 948–955.[CrossRef]
    [Google Scholar]
  45. Ohsawa, K., Lehenbauer, T. W. & Eberle, R. ( 1999; ). Herpesvirus papio 2: alternative antigen for use in monkey B virus diagnostic assays. Lab Anim Sci 49, 605–616.
    [Google Scholar]
  46. Pachner, A. R., Amemiya, K., Bartlett, M., Schaefer, H., Reddy, K. & Zhang, W. F. ( 2001; ). Lyme borreliosis in rhesus macaques: effects of corticosteroids on spirochetal load and isotype switching of anti-Borrelia burgdorferi antibody. Clin Diagn Lab Immunol 8, 225–232.
    [Google Scholar]
  47. Padgett, D. A., Sheridan, J. F., Dorne, J., Berntson, G. G., Candelora, J. & Glaser, R. ( 1998; ). Social stress and the reactivation of latent herpes simplex virus type 1. Proc Natl Acad Sci U S A 95, 7231–7235.[CrossRef]
    [Google Scholar]
  48. Palmer, A. E. ( 1987; ). B virus, Herpesvirus simiae: historical perspective. J Med Primatol 16, 99–130.
    [Google Scholar]
  49. Posavad, C. M., Koelle, D. M., Shaughnessy, M. F. & Corey, L. ( 1997; ). Severe genital herpes infections in HIV-infected individuals with impaired herpes simplex virus-specific CD8+ cytotoxic T lymphocyte responses. Proc Natl Acad Sci U S A 94, 10289–10294.[CrossRef]
    [Google Scholar]
  50. Posavad, C. M., Koelle, D. M. & Corey, L. ( 1998; ). Tipping the scales of herpes simplex virus reactivation: the important responses are local. Nat Med 4, 381–382.[CrossRef]
    [Google Scholar]
  51. Roizman, B. & Sears, A. ( 1996; ). Herpes simplex viruses and their replication. In Fields Virology, 3rd edn, pp. 2231–2295. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott– Raven.
  52. Sainz, B., Loutsch, J. M., Marquart, M. E. & Hill, J. M. ( 2001; ). Stress-associated immunomodulation and herpes simplex virus infections. Med Hypotheses 56, 348–356.[CrossRef]
    [Google Scholar]
  53. Schacker, T., Zeh, J., Hu, H. L., Hill, E. & Corey, L. ( 1998; ). Frequency of symptomatic and asymptomatic herpes simplex virus type 2 reactivations among human immunodeficiency virus-infected men. J Infect Dis 178, 1616–1622.[CrossRef]
    [Google Scholar]
  54. Scinicariello, F., Eberle, R. & Hilliard, J. K. ( 1993; ). Rapid detection of B virus (Herpesvirus simiae) DNA by polymerase chain reaction. J Infect Dis 168, 747–750.[CrossRef]
    [Google Scholar]
  55. Sequar, G., Britt, W. J., Lakeman, F. D., Lockridge, K. M., Tarara, R. P., Canfield, D. R., Zhou, S. S., Gardner, M. B. & Barry, P. A. ( 2002; ). Experimental coinfection of rhesus macaques with rhesus cytomegalovirus and simian immunodeficiency virus: pathogenesis. J Virol 76, 7661–7671.[CrossRef]
    [Google Scholar]
  56. Shane, S. A., Wollman, M. & Claassen, D. ( 1994; ). Herpes simplex dissemination following glucocorticoids for upper airway obstruction in an adolescent girl. Pediatr Emerg Care 10, 160–162.[CrossRef]
    [Google Scholar]
  57. Shen, C. Y., Chang, B. L., Chang, S. F., Yang, S. L., Tseng, S. L., Chen, C. Y. & Wu, C. W. ( 1996; ). Molecular epidemiology of cytomegalovirus infection in kindergarten children. J Med Virol 48, 33–37.[CrossRef]
    [Google Scholar]
  58. Slomka, M. J., Brown, D. W., Clewley, J. P., Bennett, A. M., Harrington, L. & Kelly, D. C. ( 1993; ). Polymerase chain reaction for detection of herpesvirus simiae (B virus) in clinical specimens. Arch Virol 131, 89–99.[CrossRef]
    [Google Scholar]
  59. Smith, A. L., Black, D. H. & Eberle, R. ( 1998; ). Molecular evidence for distinct genotypes of monkey B virus (Herpesvirus simiae) which are related to the macaque host species. J Virol 72, 9224–9232.
    [Google Scholar]
  60. Soderberg-Naucler, C. & Nelson, J. Y. ( 1999; ). Human cytomegalovirus latency and reactivation – a delicate balance between the virus and its host's immune system. Intervirology 42, 314–321.[CrossRef]
    [Google Scholar]
  61. Stagno, S., Pass, R. F., Dworsky, M. E., Henderson, R. E., Moore, E. G., Walton, P. D. & Alford, C. A. ( 1982; ). Congenital cytomegalovirus infection: the relative importance of primary and recurrent maternal infection. New Engl J Med 306, 945–949.[CrossRef]
    [Google Scholar]
  62. Tarantal, A. F., Salamat, S., Britt, W. J., Luciw, P. A., Hendrickx, A. G. & Barry, P. A. ( 1998; ). Neuropathogenesis induced by rhesus cytomegalovirus in fetal rhesus monkeys (Macaca mulatta). J Infect Dis 177, 446–450.[CrossRef]
    [Google Scholar]
  63. Thompson, S. A., Hilliard, J. K., Kittel, D., Lipper, S., Giddens, W. E., Jr, Black, D. H. & Eberle, R. ( 2000; ). Retrospective analysis of an outbreak of B virus infection in a colony of DeBrazza's monkeys (Cercopithecus neglectus). Comp Med 50, 649–657.
    [Google Scholar]
  64. Vogel, P., Weigler, B. J., Kerr, H., Hendrickx, A. & Barry, P. A. ( 1994; ). Seroepidemiologic studies of cytomegalovirus infection in a breeding population of rhesus macaques. Lab Anim Sci 44, 25–30.
    [Google Scholar]
  65. Wald, A., Zeh, J., Selke, S., Ashley, R. L. & Corey, L. ( 1995; ). Virologic characteristics of subclinical and symptomatic genital herpes infections. New Engl J Med 333, 770–775.[CrossRef]
    [Google Scholar]
  66. Wald, A., Corey, L., Cone, R., Hobson, A., Davis, G. & Zeh, J. ( 1997; ). Frequent genital herpes simplex virus 2 shedding in immunocompetent women. Effect of acyclovir treatment. J Clin Invest 99, 1092–1097.[CrossRef]
    [Google Scholar]
  67. Ward, J. A. & Hilliard, J. K. ( 1994; ). B virus-specific pathogen-free (SPF) breeding colonies of macaques: issues, surveillance, and results in 1992. Lab Anim Sci 44, 222–228.
    [Google Scholar]
  68. Weigler, B. J. ( 1992; ). Biology of B virus in macaques and human hosts: a review. Clin Infect Dis 14, 555–567.[CrossRef]
    [Google Scholar]
  69. Weigler, B. J., Roberts, J. A., Hird, D. W., Lerche, N. W. & Hilliard, J. K. ( 1990; ). A cross sectional survey for B virus antibody in a colony of group housed rhesus macaques. Lab Anim Sci 40, 257–261.
    [Google Scholar]
  70. Weigler, B. J., Hird, D. W., Hilliard, J. K., Lerche, N. W., Roberts, J. A. & Scott, L. M. ( 1993; ). Epidemiology of Cercopithecine herpesvirus 1 (B virus) infection and shedding in a large breeding cohort of rhesus macaques. J Infect Dis 167, 257–263.[CrossRef]
    [Google Scholar]
  71. Weigler, B. J., Scinicariello, F. & Hilliard, J. K. ( 1995; ). Risk of venereal B virus (Cercopithecine herpesvirus 1) transmission in rhesus monkeys using molecular epidemiology. J Infect Dis 171, 1139–1143.[CrossRef]
    [Google Scholar]
  72. Weir, E. C., Bhatt, P. N., Jacoby, R. O., Hilliard, J. K. & Morgenstern, S. ( 1993; ). Infrequent shedding and transmission of herpesvirus simiae from seropositive macaques. Lab Anim Sci 43, 541–544.
    [Google Scholar]
  73. Whitley, R. J. ( 1996; ). Cercopithecine herpesvirus 1 (B virus). In Fields Virology, 3rd edn, pp. 2623–2635. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott–Raven.
  74. Wilson, A. P. & Boelkins, R. C. ( 1970; ). Evidence for seasonal variation in aggressive behaviour by Macaca mulatta. Anim Behav 18, 719–724.[CrossRef]
    [Google Scholar]
  75. Yang, Y. S., Ho, H. N., Chen, H. F., Chen, S. U., Shen, C. Y., Chang, S. F., Huang, E. S. & Wu, C. W. ( 1995; ). Cytomegalovirus infection and viral shedding in the genital tract of infertile couples. J Med Virol 45, 179–182.[CrossRef]
    [Google Scholar]
  76. Zwartouw, H. T. & Boulter, E. A. ( 1984; ). Excretion of B virus in monkeys and evidence of genital infection. Lab Anim 18, 65–70.[CrossRef]
    [Google Scholar]
  77. Zwartouw, H. T., MacArthur, J. A., Boulter, E. A., Seamer, J. H., Marston, J. H. & Chamove, A. S. ( 1984; ). Transmission of B virus infection between monkeys especially in relation to breeding colonies. Lab Anim 18, 125–130.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18808-0
Loading
/content/journal/jgv/10.1099/vir.0.18808-0
Loading

Data & Media loading...

Most Cited This Month

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