Korean Journal of Agricultural Science (농업과학연구)

Institute of Agricultural Science, CNU (충남대학교 농업과학연구소)
권호 표지
DOI QR코드

DOI QR Code

Evaluation of immune responses in dairy cows immunized with an inactivated vaccine for bovine respiratory disease

  • Aganja, Ram Prasad (Division of Biotechnology, College of Environmental and Bioresource Sciences, Jeonbuk National University) ;
  • Seo, Kangseok (Department of Animal Science and Technology, Sunchon National University) ;
  • Ha, Seungmin (National Institute of Animal Science, Rural Development Administration) ;
  • Yi, Young-Joo (Department of Agricultural Education, College of Education, Sunchon National University) ;
  • Lee, Sang-Myeong (College of Veterinary Medicine, Chungbuk National University)
  • Received : 2021.02.22
  • Accepted : 2021.04.27
  • Published : 2021.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Bovine respiratory syncytial virus (BRSV) and bovine viral diarrhea virus (BVDV) are the main viral contributors to bovine respiratory disease (BRD) with high mortality and morbidity. BRD control measures include vaccination that modulates immunological profiles reflected in blood cells, serum, and body secretions, such as milk. This study evaluated the immune responses to an inactivated BRD vaccine in lactating cows reared in a natural environment on a dairy farm. The cows were intramuscularly inoculated with the vaccine, and serum, blood, and milk were collected pre-and post-vaccination. Our study revealed a prominent increase in BRSV-specific antibodies both in serum and milk, while the change in BVDV-specific antibodies was insignificant. Serum interleukin (IL)-1β and IL-6 levels significantly decreased, but this change was not reflected in milk. Evaluation of pattern recognition receptors (PRRs) via RT-qPCR revealed downregulation of nucleotide-binding oligomerization domain 2 (NOD2). The concentrations of BRSV antibodies, BVDV antibodies, IL-2, and IL-17A in serum and milk were strongly correlated, implying a concurrent influence on both body fluids. Thus, immunological factors modulated as a result of vaccination generally measured in serum were reflected in milk, demonstrating the suitability of milk evaluation as an alternative approach for immunological observations. Furthermore, the correlation between BRSV antibodies and NOD2 and that between BVDV antibodies and toll-like receptor (TLR) 2, TLR3, TLR4, and TLR5 imply the possible role of PRRs for the assessment of the immune response developed in immunized cows reared on the farm.

Keywords

Acknowledgement

This work was supported by the Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ012704012019), Rural Development Administration, Republic of Korea.

References

  1. Bochniarz M, Zdzisinska B, Wawron W, Szczubial M, Dabrowski R. 2017. Milk and serum IL-4, IL-6, IL-10, and amyloid A concentrations in cows with subclinical mastitis caused by coagulase-negative staphylococci. Journal of Dairy Science 100:9674-9680. https://doi.org/10.3168/jds.2017-13552
  2. Brodersen BW. 2010. Bovine respiratory syncytial virus. Veterinary Clinics North America Food Animal Practice 26:323-333. https://doi.org/10.1016/j.cvfa.2010.04.010
  3. Bryson DG, McFerran JB, Ball HJ, Neill SD. 1978. Observations on outbreaks of respiratory disease in housed calves--(2) Pathological and microbiological findings. The Veterinary Record 103:503-509. https://doi.org/10.1136/vr.103.23.503
  4. Cakebread JA, Humphrey R, Hodgkinson AJ. 2015. Immunoglobulin A in bovine milk: A potential functional food? Journal of Agricultural and Food Chemistry 63:7311-7316. https://doi.org/10.1021/acs.jafc.5b01836
  5. Carvalho CA, Sousa Jr IP, Silva JL, Oliveira AC, Goncalves RB, Gomes AM. 2014. Inhibition of Mayaro virus infection by bovine lactoferrin. Virology 452:297-302. https://doi.org/10.1016/j.virol.2014.01.022
  6. Cheng JB, Wang JQ, Bu DP, Liu GL, Zhang CG, Wei HY, Zhou LY, Wang JZ. 2008. Factors affecting the lactoferrin concentration in bovine milk. Journal of Dairy Science 91:970-976. https://doi.org/10.3168/jds.2007-0689
  7. Cronin JG, Turner ML, Goetze L, Bryant CE, Sheldon IM. 2012. Toll-like receptor 4 and MYD88-dependent signaling mechanisms of the innate immune system are essential for the response to lipopolysaccharide by epithelial and stromal cells of the bovine endometrium. Biology of Reproduction 86:51. https://doi.org/10.1095/biolreprod.111.092718
  8. Downey ED, Tait Jr RG, Mayes MS, Park CA, Ridpath JF, Garrick DJ, Reecy JM. 2013. An evaluation of circulating bovine viral diarrhea virus type 2 maternal antibody level and response to vaccination in Angus calves. Journal of Animal Science 91:4440-4450. https://doi.org/10.2527/jas.2012-5890
  9. Elvander M, Edwards S, Naslund K, Linde N. 1995. Evaluation and application of an indirect ELISA for the detection of antibodies to bovine respiratory syncytial virus in milk, bulk milk, and serum. Journal of Veterinary Diagnostic Investigation 7:177-182. https://doi.org/10.1177/104063879500700202
  10. Griffin D. 1997. Economic impact associated with respiratory disease in beef cattle. Veterinary Clinics North America Food Animal Practice 13:367-377. https://doi.org/10.1016/S0749-0720(15)30302-9
  11. Grooms DL. 2004. Reproductive consequences of infection with bovine viral diarrhea virus. Veterinary Clinics North America Food Animal Practice 20:5-19. https://doi.org/10.1016/j.cvfa.2003.11.006
  12. Guzman E, Taylor G. 2015. Immunology of bovine respiratory syncytial virus in calves. Molecular Immunology 66:48-56. https://doi.org/10.1016/j.molimm.2014.12.004
  13. Hagiwara K, Kataoka S, Yamanaka H, Kirisawa R, Iwai H. 2000. Detection of cytokines in bovine colostrum. Veterinary Immunology and Immunopathology 76:183-190. https://doi.org/10.1016/S0165-2427(00)00213-0
  14. Hao L, Shan Q, Wei J, Ma F, Sun P. 2019. Lactoferrin: Major physiological functions and applications. Current Protein and Peptide Science 20:139-144. https://doi.org/10.2174/1389203719666180514150921
  15. Ibeagha-Awemu EM, Lee JW, Ibeagha AE, Bannerman DD, Paape MJ, Zhao X. 2008. Bacterial lipopolysaccharide induces increased expression of toll-like receptor (TLR) 4 and downstream TLR signaling molecules in bovine mammary epithelial cells. Veterinary Research 39:11. https://doi.org/10.1051/vetres:2007047
  16. Janeway Jr CA, Medzhitov R. 2002. Innate immune recognition. Annual Review of Immunology 20:197-216. https://doi.org/10.1146/annurev.immunol.20.083001.084359
  17. Johnson RW. 1997. Inhibition of growth by pro-inflammatory cytokines: an integrated view. Journal of Animal Science 75:1244-1255. https://doi.org/10.2527/1997.7551244x
  18. Kawai T, Akira S. 2006. Innate immune recognition of viral infection. Nature Immunology 7:131-137. https://doi.org/10.1038/ni1303
  19. Kimman TG, Zimmer GM, Westenbrink F, Mars J, van Leeuwen E. 1988. Epidemiological study of bovine respiratory syncytial virus infections in calves: Influence of maternal antibodies on the outcome of disease. The Veterinary Record 123:104-109. https://doi.org/10.1136/vr.123.4.104
  20. Klem TB, Tollersrud T, Osteras O, Stokstad M. 2014. Association between the level of antibodies in bulk tank milk and bovine respiratory syncytial virus exposure in the herd. The Veterinary Record 175:47. https://doi.org/10.1136/vr.102403
  21. Lee SR, Pharr GT, Boyd BL, Pinchuk LM. 2008. Bovine viral diarrhea viruses modulate toll-like receptors, cytokines and co-stimulatory molecules genes expression in bovine peripheral blood monocytes. Comparative Immunology, Microbiology and Infectious Diseases 31:403-418. https://doi.org/10.1016/j.cimid.2007.06.006
  22. Lindberg AL, Alenius S. 1999. Principles for eradication of bovine viral diarrhoea virus (BVDV) infections in cattle populations. Veterinary Microbiology 64:197-222. https://doi.org/10.1016/S0378-1135(98)00270-3
  23. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  24. McGill JL, Kelly SM, Kumar P, Speckhart S, Haughney SL, Henningson J, Narasimhan B, Sacco RE. 2018. Efficacy of mucosal polyanhydride nanovaccine against respiratory syncytial virus infection in the neonatal calf. Scientific Reports 8:3021. https://doi.org/10.1038/s41598-018-21292-2
  25. McGill JL, Sacco RE. 2020. The immunology of bovine respiratory disease: Recent advancements. Veterinary Clinics North America Food Animal Practice 36:333-348. https://doi.org/10.1016/j.cvfa.2020.03.002
  26. Menzies M, Ingham A. 2006. Identification and expression of Toll-like receptors 1-10 in selected bovine and ovine tissues. Veterinary Immunology and Immunopathology 109:23-30. https://doi.org/10.1016/j.vetimm.2005.06.014
  27. Meyer G, Deplanche M, Schelcher F. 2008. Human and bovine respiratory syncytial virus vaccine research and development. Comparative Immunology, Microbiology and Infectious Diseases 31:191-225. https://doi.org/10.1016/j.cimid.2007.07.008
  28. Morales-Aguilar A, Lopez-Reyes Y, Regalado-Huitron M, Sarmiento-Silva RE, Arriaga-Pizano L, Benitez-Guzman A. 2020. The NADL strain of bovine viral diarrhea virus induces the secretion of IL-1beta through caspase 1 in bovine macrophages. Research in Veterinary Science 131:131-136. https://doi.org/10.1016/j.rvsc.2020.04.014
  29. Nakajima Y, Mikami O, Yoshioka M, Motoi Y, Ito T, Ishikawa Y, Fuse M, Nakano K, Yasukawa K. 1997. Elevated levels of tumor necrosis factor-alpha (TNF-alpha) and interleukin-6 (IL-6) activities in the sera and milk of cows with naturally occurring coliform mastitis. Research in Veterinary Science 62:297-298. https://doi.org/10.1016/S0034-5288(97)90209-5
  30. Ohlson A, Blanco-Penedo I, Fall N. 2014. Comparison of bovine coronavirus-specific and bovine respiratory syncytial virus-specific antibodies in serum versus milk samples detected by enzyme-linked immunosorbent assay. Journal of Veterinary Diagnostic Investigation 26:113-116. https://doi.org/10.1177/1040638713509377
  31. Oliveira TES, Pelaquim IF, Flores EF, Massi RP, Valdiviezo MJJ, Pretto-Giordano LG, Alfieri AA, Saut JPE, Headley SA. 2020. Mycoplasma bovis and viral agents associated with the development of bovine respiratory disease in adult dairy cows. Transboundary and Emergerging Diseases 67:82-93. https://doi.org/10.1111/tbed.13223
  32. Ploegaert TC, Tijhaar E, Lam TJ, Taverne-Thiele A, van der Poel JJ, van Arendonk JA, Savelkoul HF, Parmentier HK. 2011. Natural antibodies in bovine milk and blood plasma: Variability among cows, repeatability within cows, and relation between milk and plasma titers. Veterinary Immunology and Immunopathology 144:88-94. https://doi.org/10.1016/j.vetimm.2011.07.008
  33. Russell CD, Widdison S, Leigh JA, Coffey TJ. 2012. Identification of single nucleotide polymorphisms in the bovine Tolllike receptor 1 gene and association with health traits in cattle. Veterinary Research 43:17. https://doi.org/10.1186/1297-9716-43-17
  34. Sabbah A, Chang TH, Harnack R, Frohlich V, Tominaga K, Dube PH, Xiang Y, Bose S. 2009. Activation of innate immune antiviral responses by Nod2. Nature Immunology 10:1073-1080. https://doi.org/10.1038/ni.1782
  35. Schlender J, Hornung V, Finke S, Gunthner-Biller M, Marozin S, Brzozka K, Moghim S, Endres S, Hartmann G, Conzelmann KK. 2005. Inhibition of toll-like receptor 7- and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. Journal of Virology 79:5507-5515. https://doi.org/10.1128/JVI.79.9.5507-5515.2005
  36. Snowder GD, Van Vleck LD, Cundiff LV, Bennett GL. 2006. Bovine respiratory disease in feedlot cattle: Environmental, genetic, and economic factors. Journal of Animal Science 84:1999-2008. https://doi.org/10.2527/jas.2006-046
  37. Theurer ME, Larson RL, White BJ. 2015. Systematic review and meta-analysis of the effectiveness of commercially available vaccines against bovine herpesvirus, bovine viral diarrhea virus, bovine respiratory syncytial virus, and parainfluenza type 3 virus for mitigation of bovine respiratory disease complex in cattle. Journal of the American Veterinary Medical Association 246:126-142. https://doi.org/10.2460/javma.246.1.126
  38. Tizard IR. 2004. Veterinary immunology. p. 247. SAUNDERS, Philadelpia, USA.
  39. Tizioto PC, Kim J, Seabury CM, Schnabel RD, Gershwin LJ, Van Eenennaam AL, Toaff-Rosenstein R, Neibergs HL, Bovine Respiratory Disease Complex Coordinated Agricultural Project Research Team, Taylor JF. 2015. Immunological response to single pathogen challenge with agents of the bovine respiratory disease complex: An RNA-sequence analysis of the bronchial lymph node transcriptome. PLoS One 10:e0131459. https://doi.org/10.1371/journal.pone.0131459
  40. van der Strate BW, Beljaars L, Molema G, Harmsen MC, Meijer DK. 2001. Antiviral activities of lactoferrin. Antiviral Research 52:225-239. https://doi.org/10.1016/S0166-3542(01)00195-4
  41. Verhoeff J, Van der Ban M, van Nieuwstadt AP. 1984. Bovine respiratory syncytial virus infections in young dairy cattle: Clinical and haematological findings. The Veterinary Record 114:9-12. https://doi.org/10.1136/vr.114.1.9
  42. Weng XG, Song QJ, Wu Q, Liu MC, Wang ML, Wang JF. 2015. Genetic characterization of bovine viral diarrhea virus strains in Beijing, China and innate immune responses of peripheral blood mononuclear cells in persistently infected dairy cattle. Journal of Veterinary Science 16:491-500. https://doi.org/10.4142/jvs.2015.16.4.491
  43. Werling D, Collins RA, Taylor G, Howard CJ. 2002. Cytokine responses of bovine dendritic cells and T cells following exposure to live or inactivated bovine respiratory syncytial virus. Journal of Leukocyte Biology 72:297-304.
  44. Werling D, Hope JC, Siddiqui N, Widdison S, Russell C, Sopp P, Coffey TJ. 2017. Subset-specific expression of toll-like receptors by bovine afferent lymph dendritic cells. Frontiers in Veterinary Science 4:44. https://doi.org/10.3389/fvets.2017.00044