Abstract
Hemorrhagic enteritis virus (HEV), a type II avian adenovirus, causes intestinal hemorrhages and immunosuppression in turkeys. In this study, we exposed turkeys to virulent HEV and examined fractionated spleen cells for the presence of viral DNA by in situ hybridization and amplification of DNA extracted from virus-infected cells by PCR. HEV replication was detected only in the immunoglobulin M-bearing B lymphocytes and macrophage-like cells but not in the CD4+ or CD8+ T lymphocytes. The inability to infect T cells distinguishes type II avian adenoviruses from lymphotropic mammalian adenoviruses which infect and replicate in T cells. Furthermore, these data suggested that HEV-induced immunosuppression in turkeys may be due to the effect of the virus on B lymphocytes and macrophages. We also examined tissue tropism of HEV by in situ hybridization conducted on sections of lymphoid and nonlymphoid tissues. Large numbers of HEV-positive cells were detected in spleen and cecal tonsils. Diminutive viral activity was present in the intestines, the principal site of HEV-induced pathology. Thus, intestinal pathology was not associated with local cytopathic viral replication. This result and our previous observation that cyclosporin A abrogated intestinal hemorrhaging in HEV-infected turkeys strongly suggested that intestinal lesion induced by this virus may be immune system mediated.
Full Text
The Full Text of this article is available as a PDF (1.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Allefs J. J., Salentijn E. M., Krens F. A., Rouwendal G. J. Optimization of non-radioactive Southern blot hybridization: single copy detection and reuse of blots. Nucleic Acids Res. 1990 May 25;18(10):3099–3100. doi: 10.1093/nar/18.10.3099. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blacklow N. R., Greenberg H. B. Viral gastroenteritis. N Engl J Med. 1991 Jul 25;325(4):252–264. doi: 10.1056/NEJM199107253250406. [DOI] [PubMed] [Google Scholar]
- Fadly A. M., Winterfield R. W. Isolation and some characteristics of an agent associated with inclusion body hepatitis, hemorrhages, and aplastic anemia in chickens. Avian Dis. 1973 Jan-Mar;17(1):182–193. [PubMed] [Google Scholar]
- Fasina S. O., Fabricant J. Immunofluorescence studies on the early pathogenesis of hemorrhagic enteritis virus infection in turkeys and chickens. Avian Dis. 1982 Jan-Mar;26(1):158–163. [PubMed] [Google Scholar]
- Fujiwara H., Tanaami S., Yamaguchi M., Yoshino T. Histopathology of hemorrhagic enteritis in turkeys. Natl Inst Anim Health Q (Tokyo) 1975 Summer;15(2):68–75. [PubMed] [Google Scholar]
- Heiles H. B., Genersch E., Kessler C., Neumann R., Eggers H. J. In situ hybridization with digoxigenin-labeled DNA of human papillomaviruses (HPV 16/18) in HeLa and SiHa cells. Biotechniques. 1988 Nov-Dec;6(10):978–981. [PubMed] [Google Scholar]
- Hussain I., Choi C. U., Rings B. S., Shaw D. P., Nagaraja K. V. Pathogenesis of hemorrhagic enteritis virus infection in turkeys. Zentralbl Veterinarmed B. 1993 Dec;40(9-10):715–726. doi: 10.1111/j.1439-0450.1993.tb00196.x. [DOI] [PubMed] [Google Scholar]
- Itakura C., Carlson H. C. Electron microscopic findings of cells with inclusion bodies in experimental hemorrhagic enteritis of turkeys. Can J Comp Med. 1975 Jul;39(3):299–304. [PMC free article] [PubMed] [Google Scholar]
- McLean I. W., Nakane P. K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem. 1974 Dec;22(12):1077–1083. doi: 10.1177/22.12.1077. [DOI] [PubMed] [Google Scholar]
- Nazerian K., Fadly A. M. Propagation of virulent and avirulent turkey hemorrhagic enteritis virus in cell culture. Avian Dis. 1982 Oct-Dec;26(4):816–827. [PubMed] [Google Scholar]
- Neil G. A., Summers R. W., Cheyne B. A., Carpenter C., Huang W. L., Waldschmidt T. J. Analysis of T-lymphocyte subpopulations in inflammatory bowel diseases by three-color flow cytometry. Dig Dis Sci. 1994 Sep;39(9):1900–1908. doi: 10.1007/BF02088123. [DOI] [PubMed] [Google Scholar]
- Opengart K., Eyre P., Domermuth C. H. Increased numbers of duodenal mucosal mast cells in turkeys inoculated with hemorrhagic enteritis virus. Am J Vet Res. 1992 May;53(5):814–819. [PubMed] [Google Scholar]
- Ossa J. E., Alexander J., Schurig G. G. Role of splenectomy in prevention of hemorrhagic enteritis and death from hemorrhagic enteritis virus in turkeys. Avian Dis. 1983 Oct-Dec;27(4):1106–1111. [PubMed] [Google Scholar]
- Ossa J. E., Bates R. C., Schurig G. G. Hemorrhagic enteritis in turkeys: purification and quantification of the virus. Avian Dis. 1983 Jan-Mar;27(1):235–245. [PubMed] [Google Scholar]
- Sampaio E. P., Sarno E. N., Galilly R., Cohn Z. A., Kaplan G. Thalidomide selectively inhibits tumor necrosis factor alpha production by stimulated human monocytes. J Exp Med. 1991 Mar 1;173(3):699–703. doi: 10.1084/jem.173.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scott-Taylor T. H., Hammond G. W. Conserved sequences of the adenovirus genome for detection of all human adenovirus types by hybridization. J Clin Microbiol. 1992 Jul;30(7):1703–1710. doi: 10.1128/jcm.30.7.1703-1710.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharma J. M. Response of specific-pathogen-free turkeys to vaccines derived from marble spleen disease virus and hemorrhagic enteritis virus. Avian Dis. 1994 Jul-Sep;38(3):523–530. [PubMed] [Google Scholar]
- Sponenberg D. P., Domermuth C. H., Larsen C. T. Field outbreaks of colibacillosis of turkeys associated with hemorrhagic enteritis virus. Avian Dis. 1985 Jul-Sep;29(3):838–842. [PubMed] [Google Scholar]
- Suresh M., Sharma J. M., Belzer S. W. Studies on lymphocyte subpopulations and the effect of age on immune competence in turkeys. Dev Comp Immunol. 1993 Nov-Dec;17(6):525–535. doi: 10.1016/s0145-305x(05)80008-4. [DOI] [PubMed] [Google Scholar]
- Suresh M., Sharma J. M. Hemorrhagic enteritis virus induced changes in the lymphocyte subpopulations in turkeys and the effect of experimental immunodeficiency on viral pathogenesis. Vet Immunol Immunopathol. 1995 Mar;45(1-2):139–150. doi: 10.1016/0165-2427(94)05323-k. [DOI] [PubMed] [Google Scholar]
- Tracey K. J., Beutler B., Lowry S. F., Merryweather J., Wolpe S., Milsark I. W., Hariri R. J., Fahey T. J., 3rd, Zentella A., Albert J. D. Shock and tissue injury induced by recombinant human cachectin. Science. 1986 Oct 24;234(4775):470–474. doi: 10.1126/science.3764421. [DOI] [PubMed] [Google Scholar]
- Tracey K. J., Lowry S. F., Fahey T. J., 3rd, Albert J. D., Fong Y., Hesse D., Beutler B., Manogue K. R., Calvano S., Wei H. Cachectin/tumor necrosis factor induces lethal shock and stress hormone responses in the dog. Surg Gynecol Obstet. 1987 May;164(5):415–422. [PubMed] [Google Scholar]
- Wheelock E. F., Toy S. T. Participation of lymphocytes in viral infections. Adv Immunol. 1973;16:123–184. doi: 10.1016/s0065-2776(08)60297-7. [DOI] [PubMed] [Google Scholar]
- Wu M. X., Daley J. F., Rasmussen R. A., Schlossman S. F. Monocytes are required to prime peripheral blood T cells to undergo apoptosis. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1525–1529. doi: 10.1073/pnas.92.5.1525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- YATES V. J., FRY D. E. Observations on a chicken embryo lethal orphan (CELO) virus. Am J Vet Res. 1957 Jul;18(68):657–660. [PubMed] [Google Scholar]
- Zhang C., Nagaraja K. V. Differentiation of avian adenovirus type-II strains by restriction endonuclease fingerprinting. Am J Vet Res. 1989 Sep;50(9):1466–1470. [PubMed] [Google Scholar]
- Zinkernagel R. M., Hengartner H. Virally induced immunosuppression. Curr Opin Immunol. 1992 Aug;4(4):408–412. doi: 10.1016/s0952-7915(06)80031-2. [DOI] [PubMed] [Google Scholar]
- van den Hurk J. V. Propagation of group II avian adenoviruses in turkey and chicken leukocytes. Avian Dis. 1990 Jan-Mar;34(1):12–25. [PubMed] [Google Scholar]