Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T22:09:54.265Z Has data issue: false hasContentIssue false
  • English
  • Français

Immune response to bovine viral diarrhea virus—looking at newly defined targets

Published online by Cambridge University Press:  08 June 2015

Christopher C. L. Chase ,
Neelu Thakur ,
Mahmoud F. Darweesh ,
Susan E. Morarie-Kane  and
Mrigendra K. Rajput
Christopher C. L. Chase*
Affiliation:
Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD, USA
Neelu Thakur
Affiliation:
Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD, USA
Mahmoud F. Darweesh
Affiliation:
Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD, USA South Valley University, Qena, Egypt
Susan E. Morarie-Kane
Affiliation:
Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD, USA Wenatchee Valley College, Wenatchee, WA, USA
Mrigendra K. Rajput
Affiliation:
Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD, USA Medgene LLC, Brookings, SD, USA
*
*Corresponding author. E-mail: Christopher.Chase@sdstate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Bovine viral diarrhea virus (BVDV) has long been associated with a wide variety of clinical syndromes and immune dysregulation, many which result in secondary bacterial infections. Current understanding of immune cell interactions that result in activation and tolerance are explored in light of BVDV infection including: depletion of lymphocytes, effects on neutrophils, natural killer cells, and the role of receptors and cytokines. In addition, we review some new information on the effect of BVDV on immune development in the fetal liver, the role of resident macrophages, and greater implications for persistent infection.

Keywords

bovine viral diarrhea virusBVDVmacrophagesdendritic cellsneutrophilsnatural killer cellsKupffer cellspersistent infectionliver tolerance
Type
Review Article
Information
Animal Health Research Reviews , Volume 16 , Issue 1 , June 2015 , pp. 4 - 14
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bertolino, P, McCaughan, GW and Bowen, DG (2002). Role of primary intrahepatic T-cell activation in the ‘liver tolerance effect’. Immunology and Cell Biology 80(1): 84–92. doi: 10.1046/j.0818-9641.2001.01048.xCrossRefGoogle ScholarPubMed
Bolin, SR, McClurkin, AW and Coria, MF (1985). Effects of bovine viral diarrhea virus on the percentages and absolute numbers of circulating 3 and T lymphocytes in cattle. American Journal of Veterinary Research 46: 884–886.Google Scholar
Borca, MV, Gudmundsdottir, I, Fernández-Sainz, IJ, Holinka, LG and Risatti, GR (2008). Patterns of cellular gene expression in swine macrophages infected with highly virulent classical swine fever virus strain Brescia. Virus Research 138(1–2): 89–96. doi: 10.1016/j.virusres.2008.08.009.CrossRefGoogle ScholarPubMed
Bowen, DG, Zen, M, Holz, L, Davis, T, McCaughan, GW and Bertolino, P (2004). The site of primary T cell activation is a determinant of the balance between intrahepatic tolerance and immunity. Journal of Clinical Investigation 114(5): 701–712. doi: 10.1172/JCI21593CrossRefGoogle ScholarPubMed
Boysen, P and Storset, AK (2009). Bovine natural killer cells. Veterinary Immunology and Immunopathology 130(3–4): 163–177. doi: 10.1016/j.vetimm.2009.02.017.CrossRefGoogle ScholarPubMed
Boysen, P, Olsen, I, Berg, I, Kulberg, S, Johansen, GM and Storset, AK (2006). Bovine CD2-/NKp46+ cells are fully functional natural killer cells with a high activation status. BMC Immunology 7: 10. doi: 10.1186/1471-2172-7-10.CrossRefGoogle ScholarPubMed
Boysen, P, Gunnes, G, Pende, D, Valheim, M and Storset, AK (2008). Natural killer cells in lymph nodes of healthy calves express CD16 and show both cytotoxic and cytokine-producing properties. Developmental and Comparative Immunology 32(7): 773–783. doi: 10.1016/j.dci.2007.11.006.Google Scholar
Brackenbury, LS, Carr, BV and Charleston, B (2003). Aspects of the innate and adaptive immune responses to acute infections with BVDV. Veterinary Microbiology 96(4): 337–344.CrossRefGoogle ScholarPubMed
Brock, KV (2003). The persistence of bovine viral diarrhea virus. Biologicals 31(2): 133–135.CrossRefGoogle ScholarPubMed
Cantor, HM and Dumont, AE (1967). Hepatic suppression of sensitization to antigen absorbed into the portal system. Nature 215(5102): 744–745.CrossRefGoogle ScholarPubMed
Chase, CCL (2013). The impact of BVDV infection on adaptive immunity. Biologicals 41(1): 52–60. doi: 10.1016/j.biologicals.2012.09.009CrossRefGoogle ScholarPubMed
Chase, CCL, Elmowalid, G and Yousif, AAA (2004). The immune response to bovine viral diarrhea virus: a constantly changing picture. Veterinary Clinics of North America: Food Animal Practice 20(1): 95–114. doi: 10.1016/j.cvfa.2003.11.004Google Scholar
Choi, C, Hwang, K-K and Chae, C (2004). Classical swine fever virus induces tumor necrosis factor-alpha and lymphocyte apoptosis. Archives of Virology 149(5): 875–889. doi: 10.1007/s00705-003-0275-6CrossRefGoogle ScholarPubMed
Darweesh, M (2013). Using genetic and pathogenesis studies to develop antiviral and BVDV vaccine targets. PhD Dissertation 2013, South Dakota State University, Brookings, SD.Google Scholar
Decker, K (1990). Biologically active products of stimulated liver macrophages (Kupffer cells). European Journal of Biochemistry 192(2): 245–261. doi: 10.1111/j.1432-1033.1990.tb19222.xCrossRefGoogle ScholarPubMed
Decker, K (1998). The response of liver macrophages to inflammatory stimulation. Keio Journal of Medicine 47(1): 1–9.CrossRefGoogle ScholarPubMed
Dobromylskyj, M and Ellis, S (2007). Complexity in cattle KIR genes: transcription and genome analysis. Immunogenetics 59(6): 463–472. doi: 10.1007/s00251-007-0215-9CrossRefGoogle ScholarPubMed
Finlay, BB and Hancock, REW (2004). Can innate immunity be enhanced to treat microbial infections? Nature Reviews Microbiology 2(6): 497–504. doi: 10.1038/nrmicro908CrossRefGoogle ScholarPubMed
Endsley, JJ, Furrer, JL, Endsley, MA, McIntosh, MA, Maue, AC, Waters, WR, Lee, DR and Estes, DM (2004). Characterization of bovine homologues of granulysin and NK-lysin. Journal of Immunology (Baltimore, Md.: 1950) 173(4): 2607–2614.CrossRefGoogle ScholarPubMed
Endsley, JJ, Endsley, MA and Estes, DM (2006). Bovine natural killer cells acquire cytotoxic/effector activity following activation with IL-12/15 and reduce Mycobacterium bovis BCG in infected macrophages. Journal of Leukocyte Biology 79(1): 71–79. doi: 10.1189/jlb.0505239CrossRefGoogle ScholarPubMed
Gabriel, C, Her, Z and Ng, LFP (2013). Neutrophils: neglected players in viral diseases. DNA and Cell Biology 32(12), 665–675. doi: 10.1089/dna.2013.2211CrossRefGoogle ScholarPubMed
Gånheim, C, Johannisson, A, Ohagen, P and Persson Waller, K (2005). Changes in peripheral blood leucocyte counts and subpopulations after experimental infection with BVDV and/or Mannheimia haemolytica. Journal of Veterinary Medicine B, Infectious Diseases and Veterinary Public Health 52(9): 380–385. doi: 10.1111/j.1439-0450.2005.00882.xGoogle Scholar
Graham, EM, Thom, ML, Howard, CJ, Boysen, P, Storset, AK, Sopp, P and Hope, JC (2009). Natural killer cell number and phenotype in bovine peripheral blood is influenced by age. Veterinary Immunology and Immunopathology 132(2–4): 101–108. doi: 10.1016/j.vetimm.2009.05.002CrossRefGoogle ScholarPubMed
He, F, Chen, Z, Xu, S, Cai, M, Wu, M, Li, H and Chen, X (2009). Increased CD4+CD25+Foxp3+ regulatory T cells in tolerance induced by portal venous injection. Surgery 145(6): 663–674. doi: 10.1016/j.surg.2009.01.016CrossRefGoogle ScholarPubMed
Kärre, K, Ljunggren, HG, Piontek, G and Kiessling, R (1986). Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319(6055): 675–678. doi: 10.1038/319675a0CrossRefGoogle ScholarPubMed
Knolle, P, Schlaak, J, Uhrig, A, Kempf, P, Meyer zum, Büschenfelde KH and Gerken, G (1995). Human Kupffer cells secrete IL-10 in response to lipopolysaccharide (LPS) challenge. Journal of Hepatology 22(2): 226–229.CrossRefGoogle ScholarPubMed
Knolle, PA and Gerken, G (2000). Local control of the immune response in the liver. Immunological Reviews 174: 21–34.CrossRefGoogle ScholarPubMed
Laskin, DL and Pendino, KJ (1995). Macrophages and inflammatory mediators in tissue injury. Annual Review of Pharmacology and Toxicology 35: 655–677. doi: 10.1146/annurev.pa.35.040195.003255CrossRefGoogle ScholarPubMed
Ley, K, Laudanna, C, Cybulsky, MI and Nourshargh, S (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nature Reviews Immunology 7(9): 678–689. doi: 10.1038/nri2156Google Scholar
Li, F and Tian, Z (2013). The liver works as a school to educate regulatory immune cells. Cellular and Molecular Immunology 10(4): 292–302. doi: 10.1038/cmi.2013.7CrossRefGoogle ScholarPubMed
Liebler-Tenorio, EM, Ridpath, JF and Neill, JD (2002). 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 63(11): 1575–1584. doi: 10.2460/ajvr.2002.63.1575CrossRefGoogle ScholarPubMed
Liebler-Tenorio, EM, Ridpath, JF and Neill, JD (2003). 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 15(3): 221–232.CrossRefGoogle ScholarPubMed
Ljunggren, HG and Kärre, K (1990). In search of the ‘missing self’: MHC molecules and NK cell recognition. Immunology Today 11(7): 237–44.CrossRefGoogle ScholarPubMed
Lund, H, Boysen, P, Dean, GA, Davis, WC, Park, KT and Storset, AK (2012). Interleukin-15 activated bovine natural killer cells express CD69 and produce interferon-γ. Veterinary Immunology and Immunopathology 150(1–2): 79–89. doi: 10.1016/j.vetimm.2012.08.011.CrossRefGoogle ScholarPubMed
Lund, H, Boysen, P, Hope, JC, Sjurseth, SK and Storset, AK (2013). Natural killer cells in afferent lymph express an activated phenotype and readily produce IFN-γ. Frontiers in Immunology 4: Article 392: 1–8. doi: 10.3389/fimmu.2013.00395.CrossRefGoogle ScholarPubMed
Menge, C, Neufeld, B, Hirt, W, Schmeer, N, Bauerfeind, R, Baljer, G and Wieler, LH (1998). Compensation of preliminary blood phagocyte immaturity in the newborn calf. Veterinary Immunology and Immunopathology 62(4): 309–321.CrossRefGoogle ScholarPubMed
Molina, V, Risalde, MA, Sánchez-Cordón, PJ, Romero-Palomo, F, Pedrera, M, Garfia, B and Gómez-Villamandos, JC (2014). Cell-mediated immune response during experimental acute infection with bovine viral diarrhoea virus: evaluation of blood parameters. Transboundary and Emerging Diseases 61(1): 44–59. doi: 10.1111/tbed.12002.CrossRefGoogle ScholarPubMed
Morarie, S (2012). Unraveling the biology of bovine viral diarrhea virus (BVDV) persistent infections: integrating field and laboratory studies. PhD Dissertation 2012, South Dakota State University, Brookings, SD.Google Scholar
Morarie, S, Braun, L, Smirnova, N, Hansen, T and Chase, C (2012). Liver tolerance may serve a role in the development of BVDV persistent infection. Abstract W33-9. 31st Annual Meeting of the American Society of Virology, Madison, WI, 21–25 July 2012.Google Scholar
Moretta, A, Bottino, C, Vitale, M, Pende, D, Cantoni, C, Mingari, MC, Biassoni, R and Moretta, L (2001). Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annual Review of Immunology 19: 197–223. doi: 10.1146/annurev.immunol.19.1.197.Google Scholar
Paape, MJ, Bannerman, DD, Zhao, X and Lee, J-W (2003). The bovine neutrophil: structure and function in blood and milk. Veterinary Research 34(5): 597–627. doi: 10.1051/vetres:2003024Google ScholarPubMed
Palomares, RA, Brock, KV and Walz, PH (2014). Differential expression of pro-inflammatory and anti-inflammatory cytokines during experimental infection with low or high virulence bovine viral diarrhea virus in beef calves. Veterinary Immunology and Immunopathology 157(3–4): 149–154. doi: 10.1016/j.vetimm.2013.12.002.CrossRefGoogle ScholarPubMed
Peterhans, E and Schweizer, M (2010). Pestiviruses: how to outmaneuver your hosts. Veterinary Microbiology 142(1–2): 18–25. doi: 10.1016/j.vetmic.2009.09.038.CrossRefGoogle ScholarPubMed
Peterhans, E and Schweizer, M (2013). BVDV: a pestivirus inducing tolerance of the innate immune response. Biologicals, 41(1): 39–51. doi: 10.1016/j.biologicals.2012.07.006.CrossRefGoogle ScholarPubMed
Peterhans, E, Jungi, TW and Schweizer, M (2003). BVDV and innate immunity. Biologicals 31(2): 107–112. doi: 10.1016/S1045-1056(03)00024-1CrossRefGoogle ScholarPubMed
Rai, RM, Loffreda, S, Karp, CL, Yang, SQ, Lin, HZ and Diehl, AM (1997). Kupffer cell depletion abolishes induction of interleukin-10 and permits sustained overexpression of tumor necrosis factor alpha messenger RNA in the regenerating rat liver. Hepatology 25(4): 889–895. doi: 10.1002/hep.510250417CrossRefGoogle ScholarPubMed
Rajput, MK, Darweesh, MF, Park, K, Braun, LJ, Mwangi, W, Young, AJ and Chase, CC (2014). The effect of bovine viral diarrhea virus (BVDV) strains on bovine monocyte-derived dendritic cells (Mo-DC) phenotype and capacity to produce BVDV. Virology Journal 11(1): 44. doi: 10.1186/1743-422X-11-44CrossRefGoogle ScholarPubMed
Rebhun, WC, French, TW, Perdrizet, JA, Dubovi, EJ, Dill, SG and Karcher, LF (1989). Thrombocytopenia associated with acute bovine virus diarrhea infection in cattle. Journal of Veterinary Internal Medicine 3(1): 42–46.CrossRefGoogle ScholarPubMed
Ridpath, JF, Bendfeldt, S, Neill, JD and Liebler-Tenorio, E (2006). Lymphocytopathogenic activity in vitro correlates with high virulence in vivo for BVDV type 2 strains: criteria for a third biotype of BVDV. Virus Research 118(1–2): 62–69. doi: 10.1016/j.virusres.2005.11.014CrossRefGoogle ScholarPubMed
Risalde, MA, Gómez-Villamandos, JC, Pedrera, M, Molina, V, Cerón, JJ, Martínez-Subiela, S and Sánchez-Cordón, PJ (2011). Hepatic immune response in calves during acute subclinical infection with bovine viral diarrhoea virus type 1. Veterinary Journal (London, England: 1997) 190(2): e110–e116. doi: 10.1016/j.tvjl.2011.03.003Google Scholar
Risalde, MA, Molina, V, Sánchez-Cordón, PJ, Romero-Palomo, F, Pedrera, M and Gómez-Villamandos, JC (2014). Effects of preinfection with bovine viral diarrhea virus on immune cells from the lungs of calves inoculated with bovine herpesvirus 1.1. Veterinary Pathology. doi: 10.1177/0300985814551579Google ScholarPubMed
Roland, CR, Mangino, MJ, Duffy, BF and Flye, MW (1993). Lymphocyte suppression by Kupffer cells prevents portal venous tolerance induction: a study of macrophage function after intravenous gadolinium. Transplantation 55(5): 1151–1158.CrossRefGoogle ScholarPubMed
Roth, JA and Kaeberle, ML (1983). Suppression of neutrophil and lymphocyte function induced by a vaccinal strain of bovine viral diarrhea virus with and without the administration of ACTH. American Journal of Veterinary Research 44(12): 2366–2372.Google ScholarPubMed
Roth, JA, Kaeberle, ML and Griffith, RW (1981). Effects of bovine viral diarrhea virus infection on bovine polymorphonuclear leukocyte function. American Journal of Veterinary Research 42(2): 244–250.Google ScholarPubMed
Sánchez-Cordón, PJ, NUNez, A, Salguero, FJ, Pedrera, M, Fernández de Marco, M and Gómez-Villamandos, JC (2005). Lymphocyte apoptosis and thrombocytopenia in spleen during classical swine fever: role of macrophages and cytokines. Veterinary Pathology 42(4): 477–488. doi: 10.1354/vp.42-4-477CrossRefGoogle ScholarPubMed
Schultz, RD, Dunne, HW and Heist, CE (1973). Ontogeny of the bovine immune response. Infection and Immunity, 7(6): 981–991.CrossRefGoogle ScholarPubMed
Shuster, DE, Kehrli, ME, Ackermann, MR and Gilbert, RO (1992). Identification and prevalence of a genetic defect that causes leukocyte adhesion deficiency in Holstein cattle. Proceedings of the National Academy of Sciences of the United States of America 89(19): 9225–9229.CrossRefGoogle ScholarPubMed
Sladek, Z and Rysanek, D (2006). The role of CD14 during resolution of experimentally induced Staphylococcus aureus and Streptococcus uberis mastitis. Comparative Immunology, Microbiology and Infectious Diseases 29(4): 243–262. doi: 10.1016/j.cimid.2006.06.006CrossRefGoogle ScholarPubMed
Smirnova, NP, Webb, BT, Bielefeldt-Ohmann, H, Van Campen, H, Antoniazzi, AQ, Morarie, SE and Hansen, TR (2012). Development of fetal and placental innate immune responses during establishment of persistent infection with bovine viral diarrhea virus. Virus Research 167(2): 329–36. doi: 10.1016/j.virusres.2012.05.018Google Scholar
Smirnova, NP, Webb, BT, McGill, JL, Schaut, RG, Bielefeldt-Ohmann, H, Van Campen, H, Sacco, RE and Hansen, TR (2014). Induction of interferon-gamma and downstream pathways during establishment of fetal persistent infection with bovine viral diarrhea virus. Virus Research 183: 95–106. doi: 10.1016 /j.virusres.2014.02.002CrossRefGoogle ScholarPubMed
Sohn, EJ, Paape, MJ, Bannerman, DD, Connor, EE, Fetterer, RH and Peters, RR (2007). Shedding of sCD14 by bovine neutrophils following activation with bacterial lipopolysaccharide results in down-regulation of IL-8. Veterinary Research 38(1): 95–108. doi: 10.1051/vetres:2006052CrossRefGoogle ScholarPubMed
Storset, AK, Kulberg, S, Berg, I, Boysen, P, Hope, JC and Dissen, E (2004). NKp46 defines a subset of bovine leukocytes with natural killer cell characteristics. European Journal of Immunology 34(3): 669–676. doi: 10.1002/eji.200324504CrossRefGoogle ScholarPubMed
Thakur, N, Braun, L and Chase, CCL (2014). Effect of bovine viral diarrhea virus (BVDV) infection on neutrophil survival and surface marker expression. Abstract 71P. 95th Annual Meeting of the Conference for Research Workers in Animal Diseases, Chicago IL, 7–9 December, 2014.Google Scholar
Tiegs, G and Lohse, AW (2010). Immune tolerance: what is unique about the liver. Journal of Autoimmunity 34(1): 1–6. Review. PubMed PMID: 19717280.CrossRefGoogle ScholarPubMed
Triger, DR, Cynamon, MH and Wright, R (1973). Studies on hepatic uptake of antigen: I. Comparison of inferior vena cava and portal vein routes of immunization. Immunology 25(6): 941.Google Scholar
Vivier, E, Tomasello, E, Baratin, M, Walzer, T and Ugolini, S (2008). Functions of natural killer cells. Nature Immunology 9(5): 503–510. doi: 10.1038/ni1582CrossRefGoogle ScholarPubMed
Zeldin, DC, Eggleston, P, Chapman, M, Piedimonte, G, Renz, H and Peden, D (2006). How exposures to biologics influence the induction and incidence of asthma. Environmental Health Perspectives, 620–626. doi: 10.1289/ehp.8379CrossRefGoogle ScholarPubMed