Expression of type I interferon-induced antiviral state and pro-apoptosis markers during experimental infection with low or high virulence bovine viral diarrhea virus in beef calves

Virus Research

Volumn 173, Issue 2, 2013, Pages 260-269

  Palomares, Roberto A ^a   Walz, Heather G ^b   Brock, Kenny V ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b AUBURN UNIVERSITY   (United States)

Author keywords

Antiviral state; Bovine viral diarrhea virus; Cytokines; Gene expression; Interferon

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CASPASE 3; CASPASE 8; CASPASE 9; INTERFERON; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BOVINE DIARRHEA VIRUS; BOVINE VIRAL DIARRHEA; CALF (BOVINE); CONTROLLED STUDY; CULTURE MEDIUM; EXPERIMENTAL INFECTION; GENE EXPRESSION; GENE TARGETING; LYMPH NODE; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; UPREGULATION; VIRUS VIRULENCE;

ANIMALS; APOPTOSIS; CATTLE; CATTLE DISEASES; DIARRHEA VIRUS 1, BOVINE VIRAL; DIARRHEA VIRUS 2, BOVINE VIRAL; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; INTERFERON TYPE I; LYMPH NODES; PESTIVIRUS INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPLEEN;

BOVINE VIRAL DIARRHEA VIRUS 1;

EID: 84876864218     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2013.02.010     Document Type: Article

References (81)

1. Abbas A.K., Lithman A.H. Cellular and Molecular Immunology 2005, Elsevier Saunders, Philadelphia, 564 pp. 5th ed.
2. Adler B., Adler H., Pfister H., Jungi T.W., Peterhans E. Macrophages infected with cytopathic bovine viral diarrhea virus release a factor(s) capable of priming uninfected macrophages for activation-induced apoptosis. Journal of Virology 1997, 71:3255-3258.
3. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413(6857):732-738.
4. Baigent S.J., Goodbourn S., McCauley J.W. Differential activation of interferon regulatory factors-3 and -7 by non-cytopathogenic and cytopathogenic bovine viral diarrhoea virus. Veterinary Immunology and Immunopathology 2004, 100(3-4):135-144.
5. Baigent S.J., Zhang G., Fray M.D., Flick-Smith H., Goodbourn S., McCauley J.W. Inhibition of beta interferon transcription by noncytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor 3-dependent mechanism. Journal of Virology 2002, 76(18):8979-8988.
6. Baker J. The clinical manifestation of bovine viral diarrhea infection. Veterinary Clinics of North America. Food Animal Practice 1995, 11:425-445.
7. Baldwin C. U.S. Veterinary Immune Reagent Network. Primer Pairs Used for Cloning Target Sequences 2008, University of Massachusetts, Amherst. C. Baldwin (Ed.).
8. Bandyopadhyay S.K., Leonard G.T., Bandyopadhyay T., Stark G.R., Sen G.C. Transcriptional induction by double-stranded RNA is mediated by interferon-stimulated response elements without activation of interferon-stimulated gene factor 3. Journal of Biological Chemistry 1995, 270:19624-19629.
9. Bolin S.R., Ridpath J.F. Differences in virulence between two noncytopathic bovine viral diarrhea viruses in calves. American Journal of Veterinary Research 1992, 53(11):2157-2163.
10. Brackenbury L.S., Carr B.V., Stamataki Z., Prentice H., Lefevre E.A., Howard C.J., Charleston B. Identification of a cell population that produces alpha/beta interferon in vitro and in vivo in response to noncytopathic bovine viral diarrhea virus. Journal of Virology 2005, 79(12):7738-7744.
11. Brock K.V., Widel P., Walz P., Walz H.L. Onset of protection from experimental infection with type 2 bovine viral diarrhea virus following vaccination with a modified-live vaccine. Veterinary Therapeutics 2007, 8(1):88-96.
12. Carman S., van Dreumel T., Ridpath J., Hazlett M., Alves D., Dubovi E., Tremblay R., Bolin S., Godkin A., Anderson N. Severe acute bovine viral diarrhea in Ontario, 1993-1995. Journal of Veterinary Diagnostic Investigation 1998, 10(1):27-35.
13. Charleston B., Brackenbury L.S., Carr B.V., Fray M.D., Hope J.C., Howard C.J., Morrison W.I. Alpha/beta and gamma interferons are induced by infection with noncytopathic bovine viral diarrhea virus in vivo. Journal of Virology 2002, 76(2):923-927.
14. Charleston B., Fray M.D., Baigent S., Carr B.V., Morrison W.I. Establishment of persistent infection with non-cytopathic bovine viral diarrhea virus in cattle is associated with a failure to induce type I interferon. Journal of General Virology 2001, 82(8):1893-1897.
15. Colonna M., Trinchieri G., Liu Y.J. Plasmacytoid dendritic cells in immunity. Nature Immunology 2004, 5(12):1219-1226.
16. Deng R., Brock K.V. Molecular cloning and nucleotide sequence of a pestivirus genome, noncytopathic bovine viral diarrhea virus strain SD-1. Virology 1992, 191:867-879.
17. Di Domizio J., Blum A., Gallagher-Gambarelli M., Molens J.P., Chaperot L., Plumas J. TLR7 stimulation in human plasmacytoid dendritic cells leads to the induction of early IFN-inducible genes in the absence of type I IFN. Blood 2009, 114:1794-1802.
18. Ellis J.A., West K.H., Cortese V.S., Myers S.L., Carman S., Martin K.M., Haines D.M. Lesions and distribution of viral antigen following an experimental infection of young seronegative calves with virulent bovine virus diarrhea virus-type II. Canadian Journal of Veterinary Research 1998, 62(3):161-169.
19. Fray M.D., Mann G.E., Charleston B. Validation of an Mx/CAT reporter gene assay for the quantification of bovine type-I interferon. Journal of Immunological Methods 2001, 249(1-2):235-244.
20. Gånheim C., Hultén C., Carlsson U., Kindahl H., Niskanen R., Waller K.P. The acute phase response in calves experimentally infected with bovine viral diarrhoea virus and/or Mannheimia haemolytica. Journal of Veterinary Medicine B: Infectious Diseases and Veterinary Public Health 2003, 50(4):183-190.
21. Gillespie J.H., Baker J.A., McEntee K. A cytopathogenic strain of virus diarrhoea virus. Cornell Veterinarian 1960, 50:73-79.
22. Glew E.J., Carr B.V., Brackenbury L.S., Hope J.C., Charleston B., Howard C.J. Differential effects of bovine viral diarrhoea virus on monocytes and dendritic cells. Journal of General Virology 2003, 84(7):1771-1780.
23. Goetschy J.F., Zeller H., Content J., Horisberger M.A. Regulation of the interferon-inducible IFI-78K gene, the human equivalent of the murine Mx gene, by interferons, double-stranded RNA, certain cytokines, and viruses. Journal of Virology 1989, 63(6):2616-2622.
24. Groebner A.E., Schulke K., Unterseer S., Reichenbach H.D., Reichenbach M., Büttner M., Wolf E., Meyer H.H.D., Ulbrich S.E. Enhanced proapoptotic gene expression of XAF1, CASP8 and TNFSF10 in the bovine endometrium during early pregnancy is not correlated with augmented apoptosis. Placenta 2010, 31(3):168-177.
25. Grummer B., Bendfeldt S., Wagner B., Greiser-Wilke I. Induction of the intrinsic apoptotic pathway in cells infected with cytopathic bovine virus diarrhoea virus. Virus Research 2002, 90:143-153.
26. Hamers C., Dehan P., Couvreur B., Letellier C., Kerkhofs P., Pastoret P.P. Diversity among bovine pestiviruses. The Veterinary Journal 2001, 161:112-122.
27. Houe H. Epidemiology of bovine viral diarrhea virus. Veterinary Clinics of North America. Food Animal Practice 1995, 11(3):521-547.
28. Houe H. Epidemiological features and economical importance of bovine virus diarrhoea virus (BVDV) infections. Veterinary Microbiology 1999, 64:89-107.
29. Hug H., Costas M., Staeheli P., Aebi M., Weissmann C. Organization of the murine Mx gene and characterization of its interferon- and virus-inducible promoter. Molecular and Cellular Biology 1988, 8(8):3065-3079.
30. Jensen J., Schultz R.D. Effect of infection by bovine viral diarrhea virus (BVDV) in vitro on interleukin-1 activity of bovine monocytes. Veterinary Immunology and Immunopathology 1991, 29(3-4):251-265.
31. Jordan R., Wang L., Graczyk T., Block T., Romano P. Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells. Journal of Virology 2002, 76(19):9588-9599.
32. Kapil S., Walz P., Wilkerson M., Minocha H. Immunity and immunosuppression. Bovine Viral Diarrhea Virus: Diagnosis, Management and Control 2005, 157-170. Blackwell Publishing, Ames. 1st ed. S.M. Goyal, J.F. Ridpath (Eds.).
33. Katze M.G., He Y., Gale M.J. Viruses and interferon: a fight for supremacy. Nature Reviews Immunology 2002, 2(9):675-687.
34. Kelling C.L., Steffen D.J., Topliff C.L., Eskridge K.M., Donis R.O., Higuchi D.S. Comparative virulence of isolates of bovine viral diarrhea virus type II in experimentally inoculated six- to nine-month-old calves. American Journal of Veterinary Research 2002, 63(10):1379-1384.
35. Kliem H., Berisha B., Meyer H.H.D., Schams D. Regulatory changes of apoptotic factors in the bovine corpus luteum after induced luteolysis. Molecular Reproduction and Development 2009, 76(3):220-230.
36. Lamontagne L., Lafortune P., Fournel M. Modulation of the cellular immune responses to T-cell-dependent and T cell-independent antigens in lambs with induced bovine viral diarrhea virus infection. American Journal of Veterinary Research 1989, 50(9):1604-1608.
37. Lee K.M., Gillespie J.H. Propagation of virus diarrhea virus of cattle in tissue culture. American Journal of Veterinary Research 1957, 18:952-953.
38. Lenschow D.J., Lai C., Frias-Staheli N., Giannakopoulos N.V., Lutz A., Wolff T., Osiak A., Levine B., Schmidt R.E., García-Sastre A., Leib D., Pekosz A., Knobeloch K.P., Horak I., Virgin H.t. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(4):1371-1376.
39. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91(4):479-489.
40. Liebler-Tenorio E.M., Ridpath J.E., Neill J.D. Distribution of viral antigen and development of lesions after experimental infection with highly virulent bovine viral diarrhea virus type 2 in calves. American Journal of Veterinary Research 2002, 63(11):1575-1584.
41. Liebler-Tenorio E.M., Ridpath J.F., Neill J.D. Distribution of viral antigen and development of lesions after experimental infection of calves with a BVDV 2 strain of low virulence. Journal of Veterinary Diagnostic Investigation 2003, 15(3):221-232.
42. Liebler-Tenorio E.M., Ridpath J.F., Neill J.D. Lesions and tissue distribution of viral antigen in severe acute versus subclinical acute infection with BVDV2. Biologicals 2003, 31(2):119-122.
43. Lin Q., Dong C., Cooper M. Impairment of T and B cell development by treatment with a type I interferon. Journal of Experimental Medicine 1998, 187:79-87.
44. Lindenbach B.D., Rice C.M. Flaviviridae: the viruses and their replication. Fields Virology 2001, vol. 1:991-1041. Lippincott-Raven Publishers, Philadelphia, PA. 4th ed.
45. Liu L., Lehmkuhl H.D., Kaeberle M.L. Synergistic effects of bovine respiratory syncytial virus and non-cytopathic bovine viral diarrhea virus infection on selected bovine alveolar macrophage functions. Canadian Journal of Veterinary Research 1999, 63(1):41-48.
46. Livak K., Schmittgen T. Analysis of relative gene expression data using RTqPCR and the 2DD CT method. Methods 2001, 25(4):402-428.
47. Müller-Doblies D., Arquint A., Schaller P., Heegaard P.M., Hilbe M., Albini S., Abril C., Tobler K., Ehrensperger F., Peterhans E., Ackermann M., Metzler A. Innate immune responses of calves during transient infection with a noncytopathic strain of bovine viral diarrhea virus. Clinical and Diagnostic Laboratory Immunology 2004, 11(2):302-312.
48. Nakaya T., Sato M., Hata N., Asagiri M., Suemori H., Noguchi S., Tanaka N., Taniguchi T. Gene induction pathways mediated by distinct IRFs during viral infection. Biochemical and Biophysical Research Communications 2001, 283:1150-1156.
49. Ning S., Huye L.E., Pagano J.S. Regulation of the transcriptional activity of the IRF7 promoter by a pathway independent of interferon signaling. Journal of Biological Chemistry 2005, 280:12262-12270.
50. Norgaard J.V., Theil P.K., Sorensen M.T., Sejrsen K. Cellular mechanisms in regulating mammary cell turnover during lactation and dry period in dairy cows. Journal of Dairy Science 2008, 91(6):2319-2327.
51. Pedrera M., Gómez-Villamandos J.C., Risalde M.A., Molina V., Sánchez-Cordón P.J. Characterization of apoptosis pathways (intrinsic and extrinsic) in lymphoid tissues of calves inoculated with non-cytopathic bovine viral diarrhoea virus genotype-1. Journal of Comparative Pathology 2012, 146(1):30-39.
52. Pedrera M., Gómez-Villamandos J.C., Romero-Trevejo J.L., Risalde M.A., Molina V., Sánchez-Cordón P.J. 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 2009, 90(11):2650-2659.
53. Perler L., Schweizer M., Jungi T.W., Peterhans E. Bovine viral diarrhoea virus and bovine herpesvirus-1 prime uninfected macrophages for lipopolysaccharide-triggered apoptosis by interferon-dependent and -independent pathways. Journal of General Virology 2000, 81(4):881-887.
54. Peterhans E., Jungi T.W., Schweizer M. BVDV and innate immunity. Biologicals 2003, 31(2):107-112.
55. Potgieter L. Immunology of bovine viral diarrhea virus. Veterinary Clinics of North America. Food Animal Practice 1995, 11(3):501-520.
56. Rasper D.M., Vaillancourt J.P., Hadano S., Houtzager V.M., Seiden I., Keen S.L., Tawa P., Xanthoudakis S., Nasir J., Martindale D., Koop B.F., Peterson E.P., Thornberry N.A., Huang J., MacPherson D.P., Black S.C., Hornung F., Lenardo M.J., Hayden M.R., Roy S., Nicholson D.W. Cell death attenuation by 'Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death and Differentiation 1998, 5(4):271-288.
57. Richards K.H., Macdonald A. Putting the brakes on the anti-viral response: negative regulators of type I interferon (IFN) production. Microbes and Infection 2011, 13(4):291-302.
58. Ridpath J. BVDV genotypes and biotypes: practical implications for diagnosis and control. Biologicals 2003, 31(2):127-131.
59. Ridpath J.F., Bendfeldt S., Neill J., Liebler-Tenorio E. Lymphocytopathogenic activity in vitro correlates with high virulence in vivo for BVDV type 2 strains: criteria for a third biotype of BVDV. Virus Research 2006, 118:62-69.
60. Ridpath J.F., Bolin S.R., Dubovi E.J. Segregation of bovine viral diarrhea virus into genotypes. Virology 1994, 205:66-74.
61. Ronni T., Matikainen S., Sareneva T., Melén K., Pirhonen J., Keskinen P., Julkunen I. Regulation of IFN-alpha/beta, MxA, 2',5'-oligoadenylate synthetase, and HLA gene expression in influenza A-infected human lung epithelial cells. Journal of Immunology 1997, 158(5):2363-2374.
62. Ronni T., Sareneva T., Pirhonen J., Julkunen I. Activation of IFN-alpha, IFN-gamma, MxA, and IFN regulatory factor 1 genes in influenza A virus-infected human peripheral blood mononuclear cells. Journal of Immunology 1995, 154(6):2764-2774.
63. Sadler A.J., Williams B.R.G. Interferon-inducible antiviral effectors. Nature 2008, 8:559-568.
64. Samuel C.E. Antiviral actions of interferons. Clinical Microbiology Reviews 2001, 14(4):778-809.
65. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., Rice C.M. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472(7344):481-485.
66. Schweizer M., Matzener P., Pfaffen G., Stalder H., Peterhans E. Self and "nonself" manipulation of interferon defense during persistent infection: bovine viral diarrhea virus resists alpha/beta interferon without blocking antiviral activity against unrelated viruses replicating in its host cells. Journal of Virology 2006, 80(14):6926-6935.
67. Schweizer M., Peterhans E. Noncytopathic bovine viral diarrhea virus inhibits double-stranded RNA-induced apoptosis and interferon synthesis. Journal of Virology 2001, 75:4692-4698.
68. Shoemaker M.L., Smirnova N.P., Bielefeldt-Ohmann H., Austin K.J., van Olphen A., Clapper J.A., Hansen T.R. Differential expression of the type I interferon pathway during persistent and transient bovine viral diarrhea virus infection. Journal of Interferon and Cytokine Research 2009, 1:23-35.
69. Simon A., Fäh J., Haller O., Staeheli P. Interferon-regulated Mx genes are not responsive to interleukin-1, tumor necrosis factor, and other cytokines. Journal of Virology 1991, 65(2):968-971.
70. Sin W.X., Li P., Yeong J.P.S., Chin K.C. Activation and regulation of interferon-β in immune responses. Immunologic research 2012, 53:25-40.
71. Slee E.A., Harte M.T., Kluck R.M., Wolf B.B., Casiano C.A., Newmeyer D.D., Wang H.G., Reed J.C., Nicholson D.W., Alnemri E.S., Green D.R., Martin S.J. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. Journal of Cell Biology 1999, 144(2):281-292.
72. Smirnova N.P., Bielefeldt-Ohmann H., Van Campen H., Austin K.J., Han H., Montgomery D.L., Shoemaker M.L., van Olphen A.L., Hansen T.R. Acute non-cytopathic bovine viral diarrhea virus infection induces pronounced type I interferon response in pregnant cows and fetuses. Virus Research 2008, 132(1-2):49-58.
73. Stennicke H.R., Jürgensmeier J.M., Shin H., Deveraux Q., Wolf B.B., Yang X., Zhou Q., Ellerby H.M., Ellerby L.M., Bredesen D., Green D.R., Reed J.C., Froelich C.J., Salvesen G.S. Pro-caspase-3 is a major physiologic target of caspase-8. Journal of Biological Chemistry 1998, 273(42):27084-27090.
74. Tråvén M., Alenius S., Fossum C., Larsson B. Primary bovine viral diarrhoea virus infection in calves following direct contact with a persistently viraemic calf. Zentralblatt fur Veterinarmedizin. Reihe B 1991, 38(6):453-462.
75. Vassilev V.B., Donis R.O. Bovine viral diarrhea virus induced apoptosis correlates with increased intracellular viral RNA accumulation. Virus Research 2000, 69:95-107.
76. von Wussow P., Jakschies D., Hochkeppel H.K., Fibich C., Penner L., Deicher H. The human intracellular Mx-homologous protein is specifically induced by type I interferons. European Journal of Immunology 1990, 20(9):2015-2019.
77. Wathelet M.G., Berr P.M., Huez G.A. Regulation of gene expression by cytokines and virus in human cells lacking the type-I interferon locus. European Journal of Biochemistry 1992, 206:901-910.
78. Yamane D., Kato K., Tohya Y., Akashi H. The double-stranded RNA-induced apoptosis pathway is involved in the cytopathogenicity of cytopathogenic Bovine viral diarrhea virus. Journal of General Virology 2006, 87:2961-2970.
79. Yamane D., Kato K., Tohya Y., Akashi H. The relationship between the viral RNA level and upregulation of innate immunity in spleen of cattle persistently infected with bovine viral diarrhea virus. Veterinary Microbiology 2008, 129(1-2):69-79.
80. Yamane D., Zahoor M.A., Mohamed Y.M., Azab W., Kato K., Tohya Y., Akashi H. Microarray analysis reveals distinct signaling pathways transcriptionally activated by infection with bovine viral diarrhea virus in different cell types. Virus Research 2009, 142(1-2):188-199.
81. Zhang G., Aldridge S., Clarke M.C., McCauley J.W. Cell death induced by cytopathic bovine viral diarrhoea virus is mediated by apoptosis. Journal of General Virology 1996, 77:1677-1681.