Apoptosis in lymphoid tissues of calves inoculated with non-cytopathic bovine viral diarrhea virus genotype 1: Activation of effector caspase-3 and role of macrophages

Journal of General Virology

Volumn 90, Issue 11, 2009, Pages 2650-2659

  Pedrera, Miriam ^a   Gómez Villamandos, José C ^a   Romero Trevejo, José L ^a   Risalde, María A ^a   Molina, Verónica ^a   Sánchez Cordón, Pedro J ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; INTERLEUKIN 1ALPHA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BOVINE DIARRHEA VIRUS; CELL FUNCTION; CELL SECRETION; CONTROLLED STUDY; COW; ENZYME ACTIVATION; GENOTYPE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LYMPH FOLLICLE; LYMPHOCYTE DEPLETION; LYMPHOID TISSUE; MACROPHAGE; MACROPHAGE FUNCTION; MALE; NICK END LABELING; NONHUMAN; PATHOGENESIS; PEYER PATCH; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; VIRUS INFECTION; VIRUS STRAIN; ANIMAL; CATTLE; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; TIME;

BOVINAE; BOVINE VIRAL DIARRHEA VIRUS 1;

ANIMALS; APOPTOSIS; CASPASE 3; CATTLE; DIARRHEA VIRUS 1, BOVINE VIRAL; IN SITU NICK-END LABELING; MACROPHAGES; MALE; PEYER'S PATCHES; TIME FACTORS;

EID: 70350470005     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.012021-0     Document Type: Article

References (55)

1. Adler, B., Adler, H., Pfister, H., Jungi, T. W. & Peterhans, E. (1997). Macrophages infected with cytopathic bovine viral diarrhea virus release a factor(s) capable of priming uninfected macrophages for activation-induced apoptosis. J Virol 71, 3255-3258.
2. Archambault, D., Beliveau, C., Couture, Y. & Carman, S. (2000). Clinical response and immunomodulation following experimental challenge of calves with type 2 noncytopathogenic bovine viral diarrhea virus. Vet Res 31, 215-227.
3. Baigent, S. J., Zhang, G., Fray, M. D., Flick-Smith, H., Goodbourn, S. & McCauley, J. W. (2002). Inhibition of beta interferon transcription by noncytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor 3-dependent mechanism. J Virol 76, 8979-8988.
4. Bielefeldt Ohmann, H. & Babiuk, L. A. (1988). Influence of interferons alpha I1 and gamma and of tumour necrosis factor on persistent infection with bovine viral diarrhoea virus in vitro. J Gen Virol 69, 1399-1403.
5. Bendfeldt, S., Grummer, B. & Greiser-Wilke, I. (2003). No caspase activation but overexpression of Bcl-2 in bovine cells infected with noncytopathic bovine virus diarrhoea virus. Vet Microbiol 96, 313-326.
6. Bendfeldt, S., Ridpath, J. F. & Neill, J. D. (2007). Activation of cell signaling pathways is dependant on the biotype of bovine viral diarrhea viruses type 2. Virus Res 126, 96-105.
7. Brock, K. V. (2003). The persistence of bovine viral diarrhea virus. Biologicals 31, 133-135.
8. Clem, R. J. & Miller, L. K. (1994). Control of programmed cell death by the baculovirus genes p35 and iap. Mol Cell Biol 14, 5212-5222.
9. Dukers, D. F., Oudejans, J. J., Vos, W., ten Berge, R. L. & Meijer, C. J. (2002). Apoptosis in B-cell lymphomas and reactive lymphoid tissues always involves activation of caspase 3 as determined by a new in situ detection method. J Pathol 196, 307-315.
10. Ellis, J. A., West, K. H., Cortese, V. S., Myers, S. L., Carman, S., Martin, K. M. & Haines, D. M. (1998). Lesions and distribution of viral antigen following an experimental infection of young seronegative calves with virulent bovine virus diarrhea virus-type II. Can J Vet Res 62, 161-169.
11. Fauquet, C. M., Mayo, M. A. & Maniloff, J. (2005). Classification and nomenclature of viruses. In Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses, pp. 135-143, 981-998. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego: Elsevier Academic Press.
12. Fulton, R. W., Ridpath, J. F., Confer, A. W., Saliki, J. T., Burge, L. J. & Payton, M. E. (2003). Bovine viral diarrhoea virus antigenic diversity: impact on disease and vaccination programmes. Biologicals 31, 89-95.
13. Gómez del Moral, M., Ortuño, E., Fernández-Zapatero, P., Alonso, F., Alonso, C., Ezquerra, A. & Domínguez, J. (1999). African swine fever virus infection induces tumor necrosis factor alpha production: implications in pathogenesis. J Virol 73, 2173-2180.
14. Gómez-Villamandos, J. C., Ruiz-Villamor, E., Bautista, M. J., Sánchez, C. P., Sánchez-Cordón, P. J., Salguero, F. J. & Jover, A. (2001). Morphological and immunohistochemical changes in splenic macrophages of pigs infected with classical swine fever. J Comp Pathol 125, 98-109.
15. Grummer, B., Moenning, V. & Greiser-Wilke, I. (1998). Cytopathogenic bovine viral diarrhea viruses induce apoptosis in bovine cell cultures. Dtsch Tierarztl Wochenschr 105, 29-31.
16. Grummer, B., Bendfeldt, S. & Greiser-Wilke, I. (2002a). Apoptosis inhibitors delay the cytopathic effect of bovine viral diarrhoea virus (BVDV). J Vet Med B Infect Dis Vet Public Health 49, 298-303.
17. Grummer, B., Bendfeldt, S., Wagner, B. & Greiser-Wilke, I. (2002b). Induction of the intrinsic apoptotic pathway in cells infected with cytopathic bovine virus diarrhoea virus. Virus Res 90, 143-153.
18. Hengartner, M. O. (2000). The biochemistry of apoptosis. Nature 407, 770-776.
19. Huppertz, B., Frank, H. G. & Kaufmann, P. (1999). The apoptosis cascade - morphological and immunohistochemical methods for its visualization. Anat Embryol (Berl) 200, 1-18.
20. Jensen, J. & Schultz, R. D. (1991). Effect of infection by bovine viral diarrhea virus (BVDV) in vitro on interleukin-1 activity of bovine monocytes. Vet Immunol Immunopathol 29, 251-265.
21. Kelling, C. L., Steffen, D. J., Topliff, C. L., Eskridge, K. M., Donis, R. O. & Higuchi, D. S. (2002). Comparative virulence of isolates of bovine viral diarrhea virus type II in experimentally inoculated six- to nine-month- old calves. Am J Vet Res 63, 1379-1384.
22. Kerr, J. F., Wyllie, A. H. & Currie, A. R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26, 239-257.
23. Labat-Moleur, F., Guillermet, C., Lorimier, P., Robert, C., Lantuejoul, S., Brambilla, E. & Negoescu, A. (1998). TUNEL apoptotic cell detection in tissue sections: critical evaluation and improvement. J Histochem Cytochem 46, 327-334.
24. Lambot, M., Hanon, E., Lecomte, C., Hamers, C., Letesson, J. J. & Pastoret, P. P. (1998). Bovine viral diarrhoea virus induces apoptosis in blood mononuclear cells by a mechanism largely dependent on monocytes. J Gen Virol 79, 1745-1749.
25. Le, J. & Vilcek, J. (1987). Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities. Lab Invest 56, 234-248.
26. Liebler-Tenorio, E. M., Ridpath, J. E. & Neill, J. D. (2002). Distribution of viral antigen and development of lesions after experimental infection with highly virulent bovine viral diarrhea virus type 2 in calves. Am J Vet Res 63, 1575-1584.
27. Liebler-Tenorio, E. M., Ridpath, J. F. & Neill, J. D. (2003a). Distribution of viral antigen and development of lesions after experimental infection of calves with a BVDV 2 strain of low virulence. J Vet Diagn Invest 15, 221-232.
28. Liebler-Tenorio, E. M., Ridpath, J. F. & Neill, J. D. (2003b). Lesions and tissue distribution of viral antigen in severe acute versus subclinical acute infection with BVDV2. Biologicals 31, 119-122.
29. Liebler-Tenorio, E. M., Ridpath, J. E. & Neill, J. D. (2004). Distribution of viral antigen and tissue lesions in persistent and acute infection with the homologous strain of noncytopathic bovine viral diarrhea virus. J Vet Diagn Invest 16, 388-396.
30. Marshall, D. J., Moxley, R. A. & Kelling, C. L. (1996). Distribution of virus and viral antigen in specific pathogen-free calves following inoculation with noncytopathic bovine viral diarrhea virus. Vet Pathol 33, 311-318.
31. Noteborn, M. H., Todd, D., Verschueren, C. A., de Gauw, H. W., Curran, W. L., Veldkamp, S., Douglas, A. J., McNulty, M. S., van der EB, A. J. & Koch, G. (1994). A single chicken anemia virus protein induces apoptosis. J Virol 68, 346-351.
32. Odeón, A. C., Kelling, C. L., Marshall, D. J., Estela, E. S., Dubovi, E. J. & Donis, R. O. (1999). Experimental infection of calves with bovine viral diarrhea virus genotype II (NY-93). J Vet Diagn Invest 11, 221-228.
33. Pedrera, M., Sánchez-Cordón, P. J., Romero-Trevejo, J. L., Risalde, M. A., Greiser-Wilke, I., Núñez, A. & Gómez-Villamandos, J. C. (2009). Morphological changes and viral distribution in the ileum of colostrum-deprived calves inoculated with noncytopathic bovine viral diarrhea virus genotype-1. J Comp Pathol 141, 52-62.
34. Rathmell, J. C. & Thompson, C. B. (2002). Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell 109 (Suppl.), S97-S107.
35. Ridpath, J. F., Bolin, S. R. & Dubovi, E. J. (1994). Segregation of bovine viral diarrhea virus into genotypes. Virology 205, 66-74.
36. Ridpath, J. F., Neill, J. D. & Peterhans, E. (2007). Impact of variation in acute virulence of BVDV1 strains on design of better vaccine efficacy models. Vaccine 25, 8058-8066.
37. Saldeen, J. (2000). Cytokines induce both necrosis and apoptosis via a common Bcl-2-inhibitable pathway in rat insulin-producing cells. Endocrinology 141, 2003-2010.
38. Sánchez-Cordón, P. J., Romanini, S., Salguero, F. J., Núñez, A., Bautista, M. J., Jover, A. & Gómez-Villamos, J. C. (2002). Apoptosis of thymocytes related to cytokine expression in experimental classical swine fever. J Comp Pathol 127, 239-248.
39. Sánchez-Cordón, P. J., Romanini, S., Salguero, F. J., Ruiz-Villamor, E., Carrasco, L. & Góomez-Villamandos, J. C. (2003). A histopathologic, immunohistochemical, and ultrastructural study of the intestine in pigs inoculated with classical swine fever virus. Vet Pathol 40, 254-262.
40. Sánchez-Cordón, P. J., Núñez, A., Salguero, F. J., Pedrera, M., Fernández de Marco, M. & Gómez-Villamandos, J. C. (2005). Lymphocyte apoptosis and thrombocytopenia in spleen during classical swine fever: role of macrophages and cytokines. Vet Pathol 42, 477-488.
41. Savill, J., Fadok, V., Henson, P. & Haslett, C. (1993). Phagocyte recognition of cells undergoing apoptosis. Immunol Today 14, 131-136.
42. Schweizer, M. & Peterhans, E. (1999). Oxidative stress in cells infected with bovine viral diarrhoea virus: a crucial step in the induction of apoptosis. J Gen Virol 80, 1147-1155.
43. Schweizer, M. & Peterhans, E. (2001). Noncytopathic bovine viral diarrhea virus inhibits double-stranded RNA-induced apoptosis and interferon synthesis. J Virol 75, 4692-4698.
44. Stahelin, B. J., Marti, U., Solioz, M., Zimmermann, H. & Reichen, J. (1998). False positive staining in the TUNEL assay to detect apoptosis in liver and intestine is caused by endogenous nucleases and inhibited by diethyl pyrocarbonate. Mol Pathol 51, 204-208.
45. Stennicke, H. R., Jurgensmeier, J. M., Shin, H., Deveraux, Q., Wolf, B. B., Yang, X., Zhon, Q., Ellerby, H. M., Ellerby, L. M. & other authors (1998). Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 273, 27084-27090.
46. Stoffregen, B., Bolin, S. R., Ridpath, J. F. & Pohlenz, J. (2000). Morphologic lesions in type 2 BVDV infections experimentally induced by strain BVDV2-1373 recovered from a field case. Vet Microbiol 77, 157-162.
47. Teichmann, U., Liebler-Tenorio, E. M. & Pohlenz, J. F. (2000). Ultrastructural changes in follicles of small-intestinal aggregated lymphoid nodules in early and advanced phases of experimentally induced mucosal diseases in calves. Am J Vet Res 61, 174-182.
48. Tolskaya, E. A., Romanova, L. I., Kolesnikova, M. S., Ivannikova, T. A., Smirnova, E. A., Raikhlin, N. T. & Agol, V. I. (1995). Apoptosis-inducing and apoptosis-preventing functions of poliovirus. J Virol 69, 1181-1189.
49. Vassilev, V. B. & Donis, R. O. (2000). Bovine viral diarrhea virus induced apoptosis correlates with increased intracellular viral RNA accumulation. Virus Res 69, 95-107.
50. Walz, P. H., Bell, T. G., Wells, J. L., Gooms, D. L., Kaiser, L., Maes, R. K. & Baker, J. C. (2001). Relationship between degree of viremia and disease manifestations in calves with experimentally induced bovine viral diarrhoea virus infection. Am J Vet Res 62, 1095-1103.
51. Wilhelmsen, C. L., Bolin, S. R., Ridpath, J. F., Cheville, N. F. & Kluge, J. P. (1990). Experimental primary postnatal bovine viral diarrhea viral infections in six-month-old calves. Vet Pathol 27, 235-243.
52. Yamane, D., Nagai, M., Ogawa, Y., Tohya, Y. & Akashi, H. (2005). Enhancement of apoptosis via an extrinsic factor, TNF-α, in cells infected with cytopathic bovine viral diarrhea virus. Microbes Infect 7, 1482-1491.
53. Zhang, G., Aldridge, S., Clarke, M. C. & McCauley, J. W. (1996). Cell death induced by cytopathic bovine viral diarrhoea virus is mediated by apoptosis. J Gen Virol 77, 1677-1681.
54. Zheng, L., Fisher, G., Miller, R. E., Peschon, J., Lynch, D. H. & Lenardo, M. J. (1995). Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377, 348-351.
55. Zhuang, S. M., Shvarts, A., van Ormondt, H., Jochemsen, A. G., van der Eb, A. J. & Noteborn, M. H. (1995). Apoptin, a protein derived from chicken anemia virus, induces p53-independent apoptosis in human osteosarcoma cells. Cancer Res 55, 486-489.