Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-17T00:44:54.859Z Has data issue: false hasContentIssue false
  • English
  • Français

Host response to bovine respiratory pathogens

Published online by Cambridge University Press:  15 December 2009

Charles J. Czuprynski
Charles J. Czuprynski*
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI 53706, USA
*
E-mail: czuprync@svm.vetmed.wisc.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Bovine respiratory disease (BRD) involves complex interactions amongst viral and bacterial pathogens that can lead to intense pulmonary inflammation (fibrinous pleuropneumonia). Viral infection greatly increases the susceptibility of cattle to secondary infection of the lung with bacterial pathogens like Mannheimia haemolytica and Histophilus somni. The underlying reason for this viral/bacterial synergism, and the manner in which cattle respond to the virulence strategies of the bacterial pathogens, is incompletely understood. Bovine herpesvirus type 1 (BHV-1) infection of bronchial epithelial cells in vitro enhances the binding of M. haemolytica and triggers release of inflammatory mediators that attract and enhance binding of neutrophils. An exotoxin (leukotoxin) released from M. haemolytica further stimulates release of inflammatory mediators and causes leukocyte death. Cattle infected with H. somni frequently display vasculitis. Exposure of bovine endothelial cells to H. somnii or its lipooligosaccharide (LOS) increases endothelium permeability, and makes the surface of the endothelial cells pro-coagulant. These processes are amplified in the presence of platelets. The above findings demonstrate that bovine respiratory pathogens (BHV-1, M. haemolytica and H. somni) interact with leukocytes and other cells (epithelial and endothelial cells) leading to the inflammation that characterizes BRD.

Keywords

Mannheimia haemolyticaHistophilus somnileukotoxinviral–bacterial synergismleukotoxin
Type
Review Article
Information
Animal Health Research Reviews , Volume 10 , Issue 2 , December 2009 , pp. 141 - 143
Copyright
Copyright © Cambridge University Press 2009

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

Ambagala, TC, Ambagala, APN and Srikumaran, S (1999). The leukotoxin of Pasteurella haemolytica binds to β-integrins on bovine leukocytes. FEMS Microbiology Letters 179: 161–167.Google ScholarPubMed
Atapattu, DN and Czuprynski, CJ (2005). Mannheimia haemolytica leukotoxin induces apoptosis of bovine lymphoblastoid cells (BL-3) via a caspase-9-dependent mitochondrial pathway. Infection and Immunity 73: 5504–5513.CrossRefGoogle Scholar
Atapattu, DN, Albrecht, RM, McClenahan, DJ and Czuprynski, CJ (2008). Dynamin-2-dependent targeting of Mannheimia haemolytica leukotoxin to mitochondrial cyclophilin D in bovine lymphoblastoid cells. Infection and Immunity 76: 5357–5565.Google Scholar
Ayalew, S, Confer, AW and Blackwood, ER (2004). Characterization of immunodominant and potentially protective epitopes of Mannheimia haemolytica serotype 1 outer membrane lipoprotein PlpE. Infection and Immunity 72: 7265–7274.Google Scholar
Behling-Kelly, E, Vonderheid, H, Kim, KS, Corbeil, LB and Czuprynski, CJ (2006). Roles of cellular activation and sulfated glycans in Haemophilus somnus adherence to bovine brain microvascular endothelial cells. Infection and Immunity 74: 5311–5318.CrossRefGoogle ScholarPubMed
Behling-Kelly, E, Kim, KS and Czuprynski, CJ (2007a). Haemophilus somnus activation of brain endothelial cells: potential role for local cytokine production and thrombosis in central nervous system (CNS) infection. Thrombosis and Haemostasis 98: 823–830.CrossRefGoogle ScholarPubMed
Behling-Kelly, E, McClenahan, D, Kim, KS and Czuprynski, CJ (2007b). Viable “Haemophilus somnus” induces myosin light-chain kinase-dependent decrease in brain endothelial cell monolayer resistance. Infection and Immunity 75: 4572–4581.CrossRefGoogle ScholarPubMed
Chiang, YW, Kaeberle, ML and Roth, JA (1986). Identification of suppressive components in “Haemophilus somnus” fractions which inhibit bovine polymorphonuclear leukocyte function. Infection and Immunity 52: 792–797.Google Scholar
Czuprynski, CJ, Hamilton, HL and Noel, EJ (1987). Ingestion and killing of Pasteurella haemolytica A1 by bovine neutrophils in vitro. Veterinary Microbiology 14: 61–74.CrossRefGoogle ScholarPubMed
Czuprynski, CJ, Noel, EJ, Ortiz-Carranza, O and Srikumaran, S (1991). Activation of bovine neutrophils by partially purified Pasteurella haemolytica leukotoxin. Infection and Immunity 59: 3126–3133.CrossRefGoogle ScholarPubMed
Dassanayake, RP, Maheswaran, SK and Srikumaran, S (2007). Monomeric expression of bovine beta2-integrin subunits reveals their role in Mannheimia haemolytica leukotoxin-induced biological effects. Infection and Immunity 75: 5004–5010.CrossRefGoogle ScholarPubMed
Gershwin, LJ, Berghaus, LJ, Arnold, K, Anderson, ML and Corbeil, LB (2005). Immune mechanisms of pathogenetic synergy in concurrent bovine pulmonary infection with Haemophilus somnus and bovine respiratory syncytial virus. Veterinary Immunology and Immunopathology 107: 119–130.CrossRefGoogle ScholarPubMed
Gogolewski, RP, Leathers, CW, Liggitt, HD and Corbeil, LB (1987). Experimental Haemophilus somnus pneumonia in calves and immunoperoxidase localization of bacteria. Veterinary Pathology 24: 250–256.CrossRefGoogle ScholarPubMed
Gomis, SM, Godson, DL, Beskorwayne, T, Wobeser, GA and Potter, AA (1997). Modulation of phagocytic function of bovine mononuclear phagocytes by Haemophilus somnus. Microbial Pathogenesis 22: 13–21.Google Scholar
Hodgson, PD, Aich, P, Manuja, A, Hokamp, K, Roche, FM, Brinkman, FS, Potter, A, Babiuk, LA and Griebel, PJ (2005). Effect of stress on viral-bacterial synergy in bovine respiratory disease: novel mechanisms to regulate inflammation. Comparative and Functional Genomics 6: 244–250.CrossRefGoogle ScholarPubMed
Jeyaseelan, S, Sreevatsan, S and Maheswaran, SK (2002). Role of Mannheimia haemolytica leukotoxin in the pathogenesis of bovine pneumonic pasteurellosis. Animal Health Research Reviews 3: 69–82.CrossRefGoogle ScholarPubMed
Kisiela, D and Czuprynski, CJ (2009). Outer membrane proteins of Mannheimia haemolytica bind to bovine bronchial epithelial cells. Infection and Immunity 77: 446–455.CrossRefGoogle ScholarPubMed
Kuckleburg, CJ, Sylte, MJ, Inzana, TJ, Corbeil, LB, Darien, BJ and Czuprynski, CJ (2005). Bovine platelets activated by Haemophilus somnus and its LOS induce apoptosis in bovine endothelial cells. Microbial Pathogenesis 38: 23–32.Google Scholar
Kuckleburg, CJ, Elswaifi, SF, Inzana, TJ and Czuprynski, CJ (2007). Expression of phosphorylcholine by Histophilus somni induces bovine platelet aggregation. Infection and Immunity 75: 1045–1049.CrossRefGoogle ScholarPubMed
Kuckleburg, CJ, McClenahan, DJ and Czuprynski, CJ (2008). Platelet activation by Histophilus somni and its lipooligosaccharide induces endothelial cell proinflammatory responses and platelet internalization. Shock 29: 189–196.CrossRefGoogle ScholarPubMed
McClenahan, D, Hellenbrand, K, Atapattu, D, Aulik, N, Carlton, D, Kapur, A and Czuprynski, CJ (2008). Effects of lipopolysaccharide and Mannheimia haemolytica leukotoxin on bovine lung microvascular endothelial cells and alveolar epithelial cells. Clinical Vaccine Immunology 15: 338–347.CrossRefGoogle ScholarPubMed
Rivera, J, Kisiela, D and Czuprynski, CJ (2009). Bovine herpesvirus type 1 infection of bovine bronchial epithelial cells increases neutrophil adhesion and activation. Veterinary Immunology and Immunopathology 131: 167–176.CrossRefGoogle Scholar
Shanthalingam, S and Srikumaran, S (2009). Intact signal peptide of CD18, the beta-subunit of beta2-integrins, renders ruminants susceptible to Mannheimia haemolytica leukotoxin. Proceedings of the National Academy of Sciences, USA 106: 15448–15453.CrossRefGoogle ScholarPubMed
Stevens, P and Czuprynski, C (1996). Pasteurella haemolytica leukotoxin induces bovine leukocytes to undergo morphologic changes consistent with apoptosis in vitro. Canadian Journal of Veterinary Research 59: 110–117.Google Scholar
Tiwari, R, Sullivan, J and Czuprynski, CJ (2009). PECAM-1 is involved in neutrophil transmigration across Histophilus somni treated bovine brain endothelial cells. Microbial Pathogenesis 47: 164–170.Google Scholar
Wartha, F, Beiter, K, Normark, S and Henriques-Normark, B (2007). Neutrophil extracellular traps: casting the NET over pathogenesis. Current Opinion in Microbiology 10: 52–56.Google Scholar