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Archives of Virology

, Volume 152, Issue 10, pp 1885–1900 | Cite as

Dual enteric and respiratory tropisms of winter dysentery bovine coronavirus in calves

  • S. J. Park
  • G. Y. Kim
  • H. E. Choy
  • Y. J. Hong
  • L. J. Saif
  • J. H. Jeong
  • S. I. Park
  • H. H. Kim
  • S. K. Kim
  • S. S. Shin
  • M. I. Kang
  • K. O. Cho
Article

Summary

Although winter dysentery (WD), which is caused by the bovine coronavirus (BCoV) is characterized by the sudden onset of diarrhea in many adult cattle in a herd, the pathogenesis of the WD-BCoV is not completely understood. In this study, colostrum-deprived calves were experimentally infected with a Korean WD-BCoV strain and examined for viremia, enteric and nasal virus shedding as well as for viral antigen expression and virus-associated lesions in the small and large intestines and the upper and lower respiratory tract from 1 to 8 days after an oral infection. The WD-BCoV-inoculated calves showed gradual villous atrophy in the small intestine and a gradual increase in the crypt depth of the large intestine. The WD-BCoV-infected animals showed epithelial damage in nasal turbinates, trachea and lungs, and interstitial pneumonia. The WD-BCoV antigen was detected in the epithelium of the small and large intestines, nasal turbinates, trachea and lungs. WD-BCoV RNA was detected in the serum from post-inoculation day 3. These results show that the WD-BCoV has dual tropism and induces pathological changes in both the digestive and respiratory tracts of calves. To our knowledge, this is the first detailed report of dual enteric and respiratory tropisms of WD-BCoV in calves. Comprehensive studies of the dual tissue pathogenesis of the BCoV might contribute to an increased understanding of similar pneumoenteric CoV infections in humans.

Keywords

Nasal Swab Nasal Turbinate Adult Cattle Bovine Respiratory Disease Feedlot Cattle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. An, S, Chen, CJ, Yu, X, Leibowitz, JL, Makino, S 1999Induction of apoptosis in murine coronavirus-infected cultured cells and demonstration of E protein as an apoptosis inducerJ Virol7378537859PubMedGoogle Scholar
  2. Azevedo, MS, Yuan, L, Jeong, KI, Gonzalez, A, Nguyen, TV, Pouly, S, Gochnuer, M, Zhang, W, Azevedo, A, Saif, LJ 2005Viremia and nasal and rectal shedding of rotavirus in gnotobiotic pigs inoculated with Wa human rotavirusJ Virol7954285436PubMedCrossRefGoogle Scholar
  3. Baranowski, E, Ruiz-Jarabo, CM, Pariente, N, Verdaguer, N, Domingo, E 2003Evolution of cell recognition by viruses: a source of biological novelty with medical implicationsAdv Virus Res6219111PubMedCrossRefGoogle Scholar
  4. Cheville, NF 1994Interpretation of acute cell injury: degenerationCheville, NF eds. Ultrastructural pathology: an introduction to interpretationIowa State University PressIowa5179Google Scholar
  5. Cho, KO, Hoet, AE, Loerch, SC, Wittum, TE, Saif, LJ 2001Evaluation of concurrent shedding of bovine coronavirus via the respiratory tract and enteric route in feedlot cattleAm J Vet Rec6214361441CrossRefGoogle Scholar
  6. Cho, KO, Hasoksuz, M, Nielsen, PR, Chang, KO, Lathrop, S, Saif, LJ 2001Cross-protection studies between respiratory and calf diarrhea and winter dysentery coronavirus strains in calves and RT-PCR and nested PCR for their detectionArch Virol14624012419PubMedCrossRefGoogle Scholar
  7. Cho, KO, Halbur, PG, Bruna, JD, Sorden, SD, Yoon, KJ, Janke, BH, Chang, KO, Saif, LJ 2000Detection and isolation of coronavirus from feces of three herds of feedlot cattle during outbreaks of winter dysentery-like diseaseJ Am Vet Med Assoc21711911194PubMedCrossRefGoogle Scholar
  8. Cho, KO, Ohashi, K, Onuma, M 1999Electron microscopic and immunohistochemical localization of Marek’s disease (MD) herpesvirus particles in MD skin lymphomasVet Pathol36314320PubMedCrossRefGoogle Scholar
  9. Chouljenko, VN, Kousoulas, KG, Lin, X, Storz, J 1998Nucleotide and predicted amino acid sequences of all genes encoded by the 3′ genomic portion (9.5 kb) of respiratory bovine coronaviruses and comparisons among respiratory and enteric coronavirusesVirus Genes173342PubMedCrossRefGoogle Scholar
  10. Dungworth, DL 1993The respiratory systemJubb, KVFKennedy, PCPalmer, N eds. Pathology of domestic animalsAcademic PressSan Diego539699Google Scholar
  11. Dyer, RM 1981The bovine respiratory disease complex: infectious agentsCompend Contin Educ Pract Vet3S374S382Google Scholar
  12. Eleouet, JF, Chilmonczyk, S, Besnardeau, L, Laude, H 1998Transmissible gastroenteritis coronavirus indues programmed cell death in infected cells through a caspase-dependent pathwayJ Virol7249184924PubMedGoogle Scholar
  13. El-Kanawati, ZRH, Tsunemitsu, H, Smith, DR, Saif, LJ 1996Infection and cross-protection studies of winter dysentery and calf diarrhea bovine coronavirus strains in colostrum-deprived and gnotobiotic calvesAm J Vet Res574853PubMedGoogle Scholar
  14. Flynn, WT, Saif, LJ, Moorhead, PG 1988Pathogenesis of porcine enteric calicivirus in four-day-old gnotobiotic pigletsAm J Vet Res49819825PubMedGoogle Scholar
  15. Gallagher, TM, Buchmeier, MJ 2001Coronavirus spike proteins in viral entry and pathogenesisVirology279371374PubMedCrossRefGoogle Scholar
  16. Hasoksuz, M, Sreevatsan, S, Cho, KO, Hoet, AE, Saif, LJ 2002Molecular analysis of the S1 subunit of the spike glycoprotein of respiratory and enteric bovine coronavirus isolatesVirus Res84101109PubMedCrossRefGoogle Scholar
  17. Hussain, KA, Storz, J, Kousoulas, KG 1991Comparison of bovine coronavirus (BCV) antigens: monoclonal antibodies to the spike glycoprotein distinguish between vaccine and wild-type strainsVirology183442445PubMedCrossRefGoogle Scholar
  18. Jeong, JH, Kim, GY, Yoon, SS, Park, SJ, Kim, YJ, Sung, CM, Shin, SS, Lee, BJ, Kang, MI, Park, NY, Koh, HB, Cho, KO 2005Molecular analysis of S gene of spike glycoprotein of winter dysentery bovine coronavirus circulated in Korea during 2002–2003Virus Res108207212PubMedCrossRefGoogle Scholar
  19. Jeong, JH, Kim, GY, Yoon, SS, Park, SJ, Kim, YJ, Sung, CM, Shin, SS, Koh, HB, Lee, BJ, Lee, CY, Kang, MI, Kim, HJ, Park, NY, Cho, KO 2005Detection and isolation of winter dysentery bovine coronavirus circulated in Korea during 2002–2004J Vet Med Sci67187189PubMedCrossRefGoogle Scholar
  20. Kapil, S, Ttrent, AM, Goyal, SM 1990Excretion and persistence of bovine coronavirus in neonatal calvesArch Virol115127132PubMedCrossRefGoogle Scholar
  21. Kipar, A, May, H, Menger, S, Weber, M, Leukert, W, Reinacher, M 2005Morphologic features and development of granulomatous vasculitis in feline infectious peritonitisVet Pathol42321330PubMedCrossRefGoogle Scholar
  22. Kyuwa, S, Cohen, M, Nelson, G, Tahara, SM, Stohlman, SA 1994Modulation of cellular macromolecular synthesis by coronavirus: implication for pathogenesisJ Virol6868156819PubMedGoogle Scholar
  23. Lai, MMC, Holmes, KV 2001Coronaviridae: the viruses and their replicationFields, BNKnipe, DMHowley, PM eds. Fields virologyLippincott-RavenPhiladephia11631185Google Scholar
  24. Lathrop, SL, Wittum, TE, Loerch, SC, Perino, LJ, Saif, LJ 2000Antibody titers against bovine coronavirus and shedding of the virus via the respiratory tract in feedlot cattleAm J Vet Res6110571061PubMedCrossRefGoogle Scholar
  25. Mebus, CA 1978Pathogenesis of coronaviral infection in calvesJ Am Vet Med Assoc173631632PubMedGoogle Scholar
  26. Mebus, CA, Stair, EL, Rhodes, MB, Twiehaus, MJ 1973Pathology of neonatal calf diarrhea induced by a coronavirus-like agentVet Pathol104564PubMedGoogle Scholar
  27. Park, SJ, Jeong, C, Yoon, SS, Choy, HE, Saif, LJ, Park, SH, Kim, YJ, Jeong, JH, Park, SI, Kim, HH, Lee, BJ, Cho, HS, Kim, SK, Kang, MI, Cho, KO 2006Detection and characterization of bovine coronaviruses in fecal specimens of adult cattle with diarrhea during the warmer seasonsJ Clin Microbiol4431783188PubMedCrossRefGoogle Scholar
  28. Poon, LL, Leung, CS, Chan, KH, Yuen, KY, Guan, Y, Peiris, JS 2005Recurrent mutations associated with isolation and passage of SARS coronavirus in cells from non-human primatesJ Med Virol76435440PubMedCrossRefGoogle Scholar
  29. Saif, LJ, Wesley, RD 1999Transmissible gastroenteritis and porcine respiratory coronavirusStraw, BED’Allaire, SMengeling, WLTaylor, DI eds. Diseases of swineIowa State University PressAmes, Iowa295325Google Scholar
  30. Saif, LJ 1990A review of evidence implicating bovine coronavirus in the etiology of winter dysentery in cows: an enigma resolved?Cornell Vet80303311PubMedGoogle Scholar
  31. Saif, LJ, Redman, DR, Moorhead, PD, Theil, KW 1986Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tractsAm J Vet Res4714261432PubMedGoogle Scholar
  32. Schultze, B, Herrler, G 1993Recognition of N-acetyl-9-O-acetylneuraminic acid by bovine coronavirus and hemagglutinating encephalomyelitis virusAdv Exp Med Biol342299304PubMedGoogle Scholar
  33. Schultze, B, Gross, HJ, Brossmer, R, Herrler, G 1991The S protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinantJ Virol6562326237PubMedGoogle Scholar
  34. Shi, X, Gong, E, Gao, D, Zhang, B, Zheng, J, Gao, Z, Zhong, Y, Zou, W, Wu, B, Fang, W, Liao, S, Wang, S, Xie, Z, Lu, M, Hou, L, Zhong, H, Shao, B, Li, N, Liu, C, Pei, F, Yang, J, Wang, Y, Han, Z, Shi, X, Zhang, Q, You, J, Zhu, X 2005Severe acute respiratory syndrome associated coronavirus is detected in intestinal tissues of fatal casesAm J Gastroenterol100169176PubMedCrossRefGoogle Scholar
  35. Silim, A, Elazhary, MA 1983Detection of infectious rhinotracheitis and bovine viral diarrhea virus in the nasal epithelial cells by the direct immunofluorescence techniqueCan J Com Med471822Google Scholar
  36. Smith, DR, Tsunemitsu, H, Heckert, RA, Saif, LJ 1996Evaluation of two antigen-capture ELISAs using polyclonal or monoclonal antibodies for the detection of bovine coronavirusJ Vet Diagn Invest899105PubMedGoogle Scholar
  37. Storz, J, Zhang, XM, Rott, R 1992Comparison of hemagglutinating, receptor destroying, and acetylesterase activities of avirulent and virulent bovine coronavirus strainsArch Virol125193204PubMedCrossRefGoogle Scholar
  38. Straub, OC 1995Viral respiratory infections of cattleBovine Pract296670Google Scholar
  39. Traven, M, Naslund, K, Linde, N, Linde, B, Silvan, A, Fossum, C, Hedlund, KO, Sarsson, B 2001Experimental reproduction of winter dysentery in lactating cows using BCV – comparison with BCV infection in milk-fed calvesVet Microbiol81127151PubMedCrossRefGoogle Scholar
  40. Tsunemitsu, H, Saif, LJ 1995Antigenic and biological comparisons of bovine coronaviruses derived from neonatal calf diarrhea and winter dysentery of adult cattleArch Virol14013031311PubMedCrossRefGoogle Scholar
  41. Welch, SK, Saif, LJ 1988Monoclonal antibodies to a virulent strain of transmissible gastroenteritis virus: comparison of reactivity with virulent and attenuated virusArch Virol101221235PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • S. J. Park
    • 1
  • G. Y. Kim
    • 2
  • H. E. Choy
    • 3
  • Y. J. Hong
    • 3
  • L. J. Saif
    • 4
  • J. H. Jeong
    • 1
  • S. I. Park
    • 1
  • H. H. Kim
    • 1
  • S. K. Kim
    • 1
  • S. S. Shin
    • 1
  • M. I. Kang
    • 1
  • K. O. Cho
    • 1
  1. 1.Biotherapy Human Resources Center, College of Veterinary MedicineChonnam National UniversityGwangjuSouth Korea
  2. 2.College of Health and Well FareDongshin UniversityNajuSouth Korea
  3. 3.Genome Research Center for Enteropathogenic BacteriaChonnam National University Medical CollegeGwangjuSouth Korea
  4. 4.Ohio Agricultural Research and Development Center, Food Animal Health Research Program, Department of Veterinary Preventive MedicineThe Ohio State UniversityWoosterUSA

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