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Haemophilus somnus virulence factors and resistance to host immunity

Published online by Cambridge University Press:  28 February 2007

Shivakumara Siddaramppa  and
Thomas J. Inzana
Shivakumara Siddaramppa
Affiliation:
Center for Molecular Medicine and Infectious Diseases, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA
Thomas J. Inzana*
Affiliation:
Center for Molecular Medicine and Infectious Diseases, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA
*
*1410 Price's Fork Road, Blacksburg, VA 24061, USA. E-mail: [email protected]
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Abstract

Haemophilus somnus (‘Histophilus somni’) is a Gram-negative bacterium and opportunistic pathogen associated with multisystemic diseases of bovines. Some strains of H. somnus are relatively avirulent, but are biochemically and antigenically similar to the virulent strains. Several virulence factors have been identified in H. somnus, of which lipo-oligosaccharide phase variation, induction of apoptosis, intraphagocytic survival and immunoglobulin Fc binding proteins have been well studied. The sequencing of the genomes of two strains of H. somnus has facilitated the identification of genes responsible for distinctive attributes within this species and related bacteria. The genetic characterization of this bacterium will enhance our understanding of H. somnus virulence factors and facilitate the development of new and improved vaccines. This review presents an overview of H. somnus virulence factors, their role in resistance to host defenses and pathogenesis, and the host immune response to this bacterium. Current areas of investigation in the post-genomic era and recent insights into new pathogenic mechanisms are also discussed.

Keywords

HaemophilusHistophilusHaemophilus somnusHistophilus somnivirulencepathogenesishost resistanceimmunity
Type
Review Article
Information
Animal Health Research Reviews , Volume 5 , Issue 1 , June 2004 , pp. 79 - 93
Copyright
Copyright © CAB International 2004

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References

Akira, S, Takeda, K and Kaisho, T (2001). Toll-like receptors: critical proteins linking innate and acquired immunity. Nature Immunology 2: 675–680.CrossRefGoogle ScholarPubMed
Angen, O, Ahrens, P, Kuhnert, P, Christensen, H and Mutters, R (2003). Proposal of Histophilus somni gen. nov., sp. nov. for the three species incertae sedis “Haemophilus somnus”, “Haemophilus agni” and “Histophilus ovis”. International Journal of Systematic and Evolutionary Microbiology 53: 1449–1456.CrossRefGoogle Scholar
Appuhamy, S, Low, JC, Coote, JG and Parton, R (1998). PCR methods and plasmid profile analysis for characterisation of Histophilus ovis strains. Journal of Medical Microbiology 47: 987–992.CrossRefGoogle ScholarPubMed
Asmussen, MD and Baugh, CL (1981). Thiamine pyrophosphate (cocarboxylase) as a growth factor for Haemophilus somnus. Journal of Clinical Microbiology 14: 178–183.CrossRefGoogle ScholarPubMed
Bannerman, DD and Goldblum, SE (2003). Mechanisms of bacterial lipopolysaccharide-induced endothelial apoptosis. American Journal of Physiology Lung Cellular and Molecular Physiology 284: L899–914CrossRefGoogle ScholarPubMed
Bassler, BL (1999). How bacteria talk to each other: regulation of gene expression by quorum sensing. Current Opinion in Microbiology 2: 582–587.CrossRefGoogle ScholarPubMed
Bastida-Corcuera, FD, Butler, JE, Yahiro, S and Corbeil, LB (1999a). Differential complement activation by bovine IgG2 allotypes. Veterinary Immunology and Immunopathology 71: 115–123.CrossRefGoogle ScholarPubMed
Bastida-Corcuera, FD, Nielsen, KH and Corbeil, LB (1999b). Binding of bovine IgG2a and IgG2b allotypes to protein A, protein G, and Haemophilus somnus IgBPs. Veterinary Immunology and Immunopathology 71: 143–149.CrossRefGoogle ScholarPubMed
Beaman, L and Beaman, BL (1984). The role of oxygen and its derivatives in microbial pathogenesis and host defense. Annual Review of Microbiology 38: 27–48.CrossRefGoogle ScholarPubMed
Beutler, B (2003). Innate immune responses to microbial poisons: discovery and function of the Toll-like receptors. Annual Review of Pharmacology and Toxicology 43: 609–628.CrossRefGoogle ScholarPubMed
Bisgaard, M (1993). Ecology and significance of Pasteurellaceae in animals. Zentralblatt fur Bakteriologie 279: 7–26.CrossRefGoogle ScholarPubMed
Blood, DC and Radostits, OM (1989). Haemophilus septicemia of cattle. In: Blood, DC and Radostits, OM, editors. Veterinary Medicine. London: Bailliere Tindall, pp. 700–704.Google Scholar
Buchvarova, I (1985). Isolation of Haemophilus somnus from cattle. Veterinarno Meditsinski Nauki 22: 15–21.Google ScholarPubMed
Butt, BM, Besser, TE, Senger, PL and Widders, PR (1993). Specific antibody to Haemophilus somnus in the bovine uterus following intramuscular immunization. Infection and Immunity 61: 2558–2562.CrossRefGoogle ScholarPubMed
Canto, GJ and Biberstein, EL (1982). Serological diversity in Haemophilus somnus. Journal of Clinical Microbiology 15: 1009–1015.CrossRefGoogle ScholarPubMed
Chen, X, Schauder, S, Potier, N, Van Dorsselaer, A, Pelczer, I, Bassler, BL and Hughson, FM (2002). Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545–549.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.CrossRefGoogle ScholarPubMed
Chladek, DW (1975). Bovine abortion associated with Haemophilus somnus. American Journal of Veterinary Research 36: 1041.Google ScholarPubMed
Cole, SP, Guiney, DG and Corbeil, LB (1992). Two linked genes for outer membrane proteins are absent in four non-disease strains of Haemophilus somnus. Molecular Microbiology 6: 1895–1902.CrossRefGoogle ScholarPubMed
Corbeil, LB, Blau, K, Prieur, DJ and Ward, ACS (1985). Serum susceptibility of Haemophilus somnus from bovine clinical cases and carriers. Journal of Clinical Microbiology 22: 192–198.CrossRefGoogle Scholar
Corbeil, LB, Gogolewski, RP, Stephens, LR and Inzana, TJ (1995). Haemophilus somnus: antigen analysis and immune responses. In: Donachie, W, Lainson, FA and Hodgson, JC, editors. Haemophilus, Actinobacillus, and Pasteurella. New York: Plenum Press, pp. 63–73.CrossRefGoogle Scholar
Corbeil, LB, Bastida-Corcuera, FD and Beveridge, TJ (1997a). Haemophilus somnus immunoglobulin binding proteins and surface fibrils. Infection and Immunity 65: 4250–4257.CrossRefGoogle ScholarPubMed
Corbeil, LB, Gogolewski, RP, Kacskovics, I, Nielsen, KH, Corbeil, RR, Morrill, JL, Greenwood, R and Butler, JE (1997b). IgG2a antibodies to Haemophilus somnus and allotype expression. Canadian Journal of Veterinary Research 61: 207–213.Google ScholarPubMed
Cornelissen, CN and Sparling, PF (1994). Iron piracy: acquisition of transferrin-bound iron by bacterial pathogens. Molecular Microbiology 14: 843–850.CrossRefGoogle ScholarPubMed
Cox, AD, Howard, MD, Brisson, JR, van der Zwan, M, Thibault, P, Perry, MB and Inzana, TJ (1998). Structural analysis of the phase-variable lipooligosaccharide from Haemophilus somnus strain 738. European Journal of Biochemistry 253: 507–516.CrossRefGoogle ScholarPubMed
Czuprynski, CJ and Hamilton, HL (1985). Bovine neutrophils ingest but do not kill Haemophilus somnus. Infection and Immunity 50: 431–436.CrossRefGoogle Scholar
Descarga, CO, Piscitelli, HG, Zielinski, GC and Cipolla, AL (2002). Thromboembolic meningoencephalitis due to Haemophilus somnus in feedlot cattle in Argentina. Veterinary Record 150: 817.CrossRefGoogle ScholarPubMed
Dewey, KJ and Little, PB (1984). The pathogenicity of Haemophilus somnus in various laboratory animal species. Canadian Journal of Comparative Medicine 48: 27–29.Google ScholarPubMed
Donlan, RM and Costerton, JW (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews 15: 167–193.CrossRefGoogle ScholarPubMed
Duncan, A, Magee, C and Inzana, T (2002). Molecular characterization of a DNA locus involved in lipooligosaccharide biosynthesis in Haemophilus somnus. In: Abstracts of the 102nd Abstract D-104 General Meeting of the American Society for Microbiology.Google Scholar
Dyer, NW (2001). Haemophilus somnus bronchopneumonia in American bison (Bison bison). Journal of Veterinary Diagnostic Investigation 13: 419–421.CrossRefGoogle ScholarPubMed
Elsbach, P and Weiss, J (1985). Oxygen-dependent and oxygen-independent mechanisms of microbicidal activity of neutrophils. Immunology Letters 11: 159–163.CrossRefGoogle ScholarPubMed
Elswaifi, S, Howard, M, Scarratt, WK and Inzana, T (2003). Phase variation of Haemophilus somnus phosphorylcholine (ChoP) expression and the role of ChoP in bacterial colonization of the bovine respiratory tract. In: Abstracts of the 103rd General Meeting of the American Society for Microbiology Abstract B-447.Google Scholar
Erridge, C, Bennett-Guerrero, E and Poxton, IR (2002). Structure and function of lipopolysaccharides. Microbes and Infection 4: 837–851.CrossRefGoogle ScholarPubMed
Federle, MJ and Bassler, BL (2003). Interspecies communication in bacteria. Journal of Clinical Investigation 112: 1291–1299.CrossRefGoogle ScholarPubMed
Fong, KP, Gao, L and Demuth, DR (2003). luxS and arcB control aerobic growth of Actinobacillus actinomycetemcomitans under iron limitation. Infection and Immunity 71: 298–308.CrossRefGoogle ScholarPubMed
Frey, EA and Finlay, BB (1998). Lipopolysaccharide induces apoptosis in a bovine endothelial cell line via a soluble CD14 dependent pathway. Microbial Pathogenesis 24: 101–109.CrossRefGoogle Scholar
Fussing, V and Wegener, HC (1993). Characterization of bovine Haemophilus somnus by biotyping, plasmid profiling, REA-patterns and ribotyping. Zentralblatt fur Bakteriologie 279: 60–74.CrossRefGoogle ScholarPubMed
Galanos, C and Luderitz, O (1984). Lipopolysaccharide: properties of an amphipathic molecule. In: Rietschel, ET editor. Chemistry of Endotoxin. Amsterdam: Elsevier Science Publishers, pp. 46–58.Google Scholar
Garcia-Delgado, GA, Little, PB and Barnum, DA (1977). A comparison of various Haemophilus somnus strains. Canadian Journal of Comparative Medicine 41: 380–388.Google ScholarPubMed
Gogolewski, RP, Kania, SA, Inzana, TJ, Widders, PR, Liggitt, HD and Corbeil, LB (1987). Protective ability and specificity of convalescent serum from calves with Haemophilus somnus pneumonia. Infection and Immunity 55: 1403–1411.CrossRefGoogle ScholarPubMed
Gogolewski, RP, Kania, SA, Liggitt, HD and Corbeil, LB (1988). Protective ability of antibodies against 78- and 40-kilodalton outer membrane antigens of Haemophilus somnus. Infection and Immunity 56: 2307–2316.CrossRefGoogle ScholarPubMed
Gogolewski, RP, Schaefer, DC, Wasson, SK, Corbeil, RR and Corbeil, LB (1989). Pulmonary persistence of Haemophilus somnus in the presence of specific antibody. Journal of Clinical Microbiology 27: 1767–1774.CrossRefGoogle ScholarPubMed
Gomis, SM, Godson, DL, Beskorwayne, T, Wobeser, GA and Potter, AA (1997a). Modulation of phagocytic function of bovine mononuclear phagocytes by Haemophilus somnus. Microbial Pathogenesis 22: 13–21.CrossRefGoogle ScholarPubMed
Gomis, SM, Godson, DL, Wobeser, GA and Potter, AA (1997b). Effect of Haemophilus somnus on nitric oxide production and chemiluminescence response of bovine blood monocytes and alveolar macrophages. Microbial Pathogenesis 23: 327–333.CrossRefGoogle ScholarPubMed
Gomis, SM, Godson, DL, Wobeser, GA and Potter, AA (1998). Intracellular survival of Haemophilus somnus in bovine blood monocytes and alveolar macrophages. Microbial Pathogenesis 25: 227–235.CrossRefGoogle ScholarPubMed
Gotschlich, EC (1994). Genetic locus for the biosynthesis of the variable portion of Neisseria gonorrhoeae lipooligosaccharide. Journal of Experimental Medicine 180: 2181–2190.CrossRefGoogle ScholarPubMed
Hajishengallis, G, Martin, M, Schifferle, RE and Genco, RJ (2002). Counteracting interactions between lipopolysaccharide molecules with differential activation of toll-like receptors. Infection and Immunity 70: 6658–6664.CrossRefGoogle ScholarPubMed
Harris, FW and Janzen, ED (1989). The Haemophilus somnus disease complex (haemophilosis): a review. Canadian Journal of Veterinary Research 30: 816–822.Google Scholar
Hazlett, MJ, Little, PB, Barnum, DA, Maxie, MG, Leslie, KE and Miller, RB (1985). Haemophilus somnus: investigations of its potential role in bovine mastitis. American Journal of Veterinary Research 46: 2229–2234.Google ScholarPubMed
Henderson, IR, Owen, P and Nataro, JP (1999). Molecular switches-the ON and OFF of bacterial phase variation. Molecular Microbiology 33: 919–932.CrossRefGoogle ScholarPubMed
Hitchcock, PJ, Leive, L, Makela, PH, Rietschel, ET, Strittmatter, W and Morrison, DC (1986). Lipopolysaccharide nomenclature-past, present, and future. Journal of Bacteriology 166: 699–705.CrossRefGoogle ScholarPubMed
Howard, MD, Cox, AD, Weiser, JN, Schurig, GG and Inzana, TJ (2000). Antigenic diversity of Haemophilus somnus lipooligosaccharide: phase-variable accessibility of the phosphorylcholine epitope. Journal of Clinical Microbiology 38: 4412–4419.CrossRefGoogle ScholarPubMed
Howard, M, Duncan, A, Cox, A, Wakarchuk, W and Inzana, T (2003). Identification of putative genes involved in lipooligosaccharide sialylation in Haemophilus somnus. In: Abstracts of the 103rd General Meeting of the American Society for Microbiology, Abstract Z-003.Google Scholar
Hubbard, RD, Kaeberle, ML, Roth, JA and Chiang, YW (1986). Haemophilus somnus-induced interference with bovine neutrophil functions. Veterinary Microbiology 12: 77–85.CrossRefGoogle ScholarPubMed
Humphrey, JD and Stephens, L (1983). Haemophilus somnus: a review. Veterinary Bulletin 53: 987–1004.Google Scholar
Inzana, TJ (1999). The Haemophilus somnus complex. In: Howard, JL and Smith, RA, editors. Current Veterinary Therapy: Food Animal Practice, Vol. 4. Philadelphia: W. B. Saunders, pp. 358–361.Google Scholar
Inzana, TJ and Corbeil, LB (1987). Development of a defined medium for Haemophilus somnus isolated from cattle. American Journal of Veterinary Research 48: 366–369.Google ScholarPubMed
Inzana, TJ and Corbeil, LB (2004). Haemophilus. In: Gyles, C, Thoen, C, Prescott, JF and Songer, G, editors. Pathogenesis of Bacterial Infections of Animals 3rd edition. Ames (IA): Iowa State University Press. In press.Google Scholar
Inzana, TJ and Todd, J (1992). Immune response of cattle to an Haemophilus somnus lipid A-protein conjugate vaccine and efficacy in a mouse abortion model. American Journal of Veterinary Research 53: 175–179.CrossRefGoogle Scholar
Inzana, TJ, Iritani, B, Gogolewski, RP, Kania, SA and Corbeil, LB (1988). Purification and characterization of lipooligosaccharides from four strains of Haemophilus somnus. Infection and Immunity 56: 2830–2837.CrossRefGoogle ScholarPubMed
Inzana, TJ, Gogolewski, RP and Corbeil, LB (1992). Phenotypic phase variation in Haemophilus somnus lipooligosaccharide during bovine pneumonia and after in vitro passage. Infection and Immunity 60: 2943–2951.CrossRefGoogle ScholarPubMed
Inzana, TJ, Hensley, J, McQuiston, J, Lesse, AJ, Campagnari, AA, Boyle, SM and Apicella, MA (1997). Phase variation and conservation of lipooligosaccharide epitopes in Haemophilus somnus. Infection and Immunity 65: 4675–4681.CrossRefGoogle ScholarPubMed
Inzana, TJ, Cox, A and Glindemann, G (2002a). Exopolysaccharide production by Haemophilus somnus. In: American Society for Microbiology, 102nd General Meeting, Salt Lake City, Utah, Abstract Z-26.Google Scholar
Inzana, TJ, Glindemann, G, Cox, AD, Wakarchuk, W and Howard, MD (2002b). Incorporation of N-acetylneuraminic acid into Haemophilus somnus lipooligosaccharide (LOS): enhancement of resistance to serum and reduction of LOS antibody binding. Infection and Immunity 70: 4870–4879.CrossRefGoogle ScholarPubMed
Inzana, TJ, Glindemann, G, Larson, J and Siddaramappa, S (2003). Biofilm formation by Haemophilus somnus. In: Proceedings of the 84th Annual Meeting of The Conference of Research Workers in Animal Diseases, Chicago, IL Oxford: Blackwell Publishing. Abstract 12Google Scholar
Ishikawa, Y, Tsukuda, S, Nakajima, Y and Ohshima, K (1984). Atypical nervous lesion in Haemophilus somnus infection of cattle. Cornell Veterinarian 74: 349–353.Google ScholarPubMed
Ismail, M (1991). Haemophilus somnus as a bacterial cause of pneumonia in buffalo calves in Egypt. Archives of Experimental Veterinary Medicine 45: 161–164.Google ScholarPubMed
Jackson, JA, Andrews, JJ and Hargis, JW (1987). Experimental Haemophilus somnus pneumonia in calves. Veterinary Pathology 24: 129–134.CrossRefGoogle ScholarPubMed
Kilian, M and Biberstein, EL (1984). Genus II. Haemophilus, In: Krieg, NR editor. Bergey's Manual of Systematic Bacteriology, Vol. 1. Baltimore: Williams & Wilkins, pp. 558–569.Google Scholar
Kwiecien, JM and Little, PB (1991). Haemophilus somnus and reproductive disease in the cow: a review. Canadian Veterinary Journal 32: 595–601.Google ScholarPubMed
Last, RD, Macfarlane, MD and Jarvis, CJ (2001). Isolation of Haemophilus somnus from dairy cattle in kwaZulu-Natal. An emerging cause of “dirty cow syndrome” and infertility? Journal of the South African Veterinary Association 72: 95.CrossRefGoogle ScholarPubMed
Lederer, JA, Brown, JF and Czuprynski, CJ (1987). “Haemophilus somnus”, a facultative intracellular pathogen of bovine mononuclear phagocytes. Infection and Immunity 55: 381–387.CrossRefGoogle ScholarPubMed
Lees, VW, Yates, WD and Corbeil, LB (1994). Ovine Haemophilus somnus: experimental intracisternal infection and antigenic comparison with bovine Haemophilus somnus. Canadian Journal of Veterinary Research 58: 202–210.Google ScholarPubMed
Malott, RJ and Lo, RYC (2002). Studies on the production of quorum-sensing signal molecules in Mannheimia haemolytica A1 and other Pasteurellaceae species. FEMS Microbiology Letters 206: 25–30.CrossRefGoogle ScholarPubMed
Mandrell, RE and Apicella, MA (1993). Lipooligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS. Immunobiology 187: 382–402.CrossRefGoogle ScholarPubMed
McQuiston, JH, McQuiston, JR, Cox, AD, Wu, Y, Boyle, SM and Inzana, TJ (2000). Characterization of a DNA region containing 5'-(CAAT)(n)-3' DNA sequences involved in lipooligosaccharide biosynthesis in Haemophilus somnus. Microbial Pathogenesis 28: 301–312.CrossRefGoogle ScholarPubMed
Merino, M and Biberstein, EL (1982). Growth requirements of Haemophilus somnus. Journal of Clinical Microbiology 16: 798–802.CrossRefGoogle ScholarPubMed
Miller, RJ, Renshaw, HW and Evans, JA (1975). Haemophilus somnus complex: antigenicity and specificity of fractions of Haemophilus somnus. American Journal of Veterinary Research 36: 1123–1128.Google ScholarPubMed
Nivard, JL, Ward, GE, Stevens, JB and Maheswaran, SK (1982). Model infection of the chicken embryo with Haemophilus somnus. American Journal of Veterinary Research 43: 1790–1792.Google ScholarPubMed
Pennell, JR and Renshaw, HW (1977). Haemophilus somnus complex: in vitro interactions of Haemophilus somnus, leukocytes, complement, and antiserums produced from vaccination of cattle with fractions of the organism. American Journal of Veterinary Research 38: 759–769.Google ScholarPubMed
Pfeifer, CG, Campos, M, Beskorwayne, T, Babiuk, LA and Potter, AA (1992). Effect of Haemophilus somnus on phagocytosis and hydrogen peroxide production by bovine polymorphonuclear leukocytes. Microbial Pathogenesis 13: 191–202.CrossRefGoogle ScholarPubMed
Pritchard, DG, Shreeve, J and Bradley, R (1979). The experimental infection of calves with a British strain of Haemophilus somnus. Research in Veterinary Science 26: 7–11.CrossRefGoogle ScholarPubMed
Ram, S, Sharma, AK, Simpson, SD, Gulati, S, McQuillen, DP, Pangburn, MK and Rice, PA (1998). A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. Journal of Experimental Medicine 187: 743–752.CrossRefGoogle ScholarPubMed
Ruby, KW, Griffith, RW and Kaeberle, ML (2002). Histamine production by Haemophilus somnus. Comparative Immunology, Microbiology & Infectious Diseases 25: 13–20.CrossRefGoogle ScholarPubMed
Salaun, L, Snyder, LA and Saunders, NJ (2003). Adaptation by phase variation in pathogenic bacteria. Advances in Applied Microbiology 52: 263–301.CrossRefGoogle ScholarPubMed
Sample, AK and Czuprynski, CJ (1991). Elimination of hydrogen peroxide by Haemophilus somnus, a catalase-negative pathogen of cattle. Infection and Immunity 59: 2239–2244.CrossRefGoogle ScholarPubMed
Sanders, JD, Bastida-Corcuera, FD, Arnold, KF, Wunderlich, AC and Corbeil, LB (2003). Genetic manipulation of immunoglobulin binding proteins of Haemophilus somnus. Microbial Pathogenesis 34: 131–139.CrossRefGoogle ScholarPubMed
Schilling, B, Goon, S, Samuels, NM, Gaucher, SP, Leary, JA, Bertozzi, CR and Gibson, BW (2001). Biosynthesis of sialylated lipooligosaccharides in Haemophilus ducreyi is dependent on exogenous sialic acid and not mannosamine. Incorporation studies using N-acylmannosamine analogues, N-glycolylneuraminic acid, and 13 C-labeled N-acetylneuraminic acid. Biochemistry 40: 12666–12677.CrossRefGoogle Scholar
Schuh, JCL, Harland, RJ, and Janzen, ED (1991). Haemophilus somnus infection in the bovine heart-chronic sequelae. In: Abstracts of the 42nd Annual Meeting of the American College of Veterinary Pathology, Abstract M-5.Google Scholar
Silva, SVPS and Little, PB (1990). The protective effect of vaccination against experimental pneumonia in cattle with Haemophilus somnus outer membrane antigens and interference by lipopolysaccharides. Canadian Journal of Veterinary Research 54: 326–330.Google Scholar
Simonson, RR and Maheswaran, SK (1982). Host humoral factors in natural resistance to Haemophilus somnus. American Journal of Veterinary Research 43: 1160–1164.Google ScholarPubMed
Smith, H, Parsons, NJ and Cole, JA (1995). Sialylation of neisserial lipopolysaccharide: a major influence on pathogenicity. Microbial Pathogenesis 19: 365–377.CrossRefGoogle ScholarPubMed
Stephens, LR and Little, PB (1981). Ultrastructure of Haemophilus somnus, causative agent of bovine infectious thromboembolic meningoencephalitis. American Journal of Veterinary Research 42: 1638–1640.Google ScholarPubMed
Stephens, L, Little, RPB, Wilkie, BN and Barnum, A (1981). Infectious thromboembolic meningoencephalitis in cattle: a review. Journal of American Veterinary Medical Association 178: 378–384.Google ScholarPubMed
Stephens, LR, Humphrey, JD, Little, PB and Barnum, DA (1983). Morphological, biochemical, antigenic, and cytochemical relationships among Haemophilus somnus, Haemophilus agni, Haemophilus haemoglobinophilus, Histophilus ovis, and Actinobacillus seminis. Journal of Clinical Microbiology 17: 728–737.CrossRefGoogle ScholarPubMed
Stephens, LR, Slee, KJ, Poulton, P, Larcombe, M and Kosior, E (1986). Investigation of purulent vaginal discharge in cows, with particular reference to Haemophilus somnus. Australian Veterinary Journal 63: 182–185.CrossRefGoogle ScholarPubMed
Stephens, LR, Aukema, R and Murray, LJ (1987). Antigenic heterogeneity of Haemophilus somnus. Australian Veterinary Journal 64: 113.CrossRefGoogle ScholarPubMed
Svastova, A (1988). Haemophilus somnus as a cause of bronchopneumonia in calves. Veterinary Medicine (Praha) 33: 193–200.Google ScholarPubMed
Swords, WE, Buscher, BA, Ver Steeg Ii, K, Preston, A, Nichols, WA, Weiser, JN, Gibson, BW and Apicella, MA (2000). Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Molecular Microbiology 37: 13–27.CrossRefGoogle ScholarPubMed
Sylte, MJ, Corbeil, LB, Inzana, TJ and Czuprynski, CJ (2001). Haemophilus somnus induces apoptosis in bovine endothelial cells in vitro. Infection and Immunity 69: 1650–1660.CrossRefGoogle ScholarPubMed
Sylte, MJ, Leite, FP, Kuckleburg, CJ, Inzana, TJ and Czuprynski, CJ (2003). Caspase activation during Haemophilus somnus lipooligosaccharide-mediated apoptosis of bovine endothelial cells. Microbial Pathogenesis 35: 285–291.CrossRefGoogle ScholarPubMed
Sylte, MJ, Inzana, TJ and Czuprynski, CJ (2004). Reactive oxygen and nitrogen intermediates contribute to Haemophilus somnus lipooligosaccharide-mediated apoptosis of bovine endothelial cells. Veterinary Immunology and Immunopathology 97: 207–217.CrossRefGoogle ScholarPubMed
Tagawa, Y, Bastida-Corcuera, F and Corbeil, LB (2000). Immunological characterization of the major outer membrane protein of Haemophilus somnus. Veterinary Microbiology 71: 245–254.CrossRefGoogle ScholarPubMed
Tegtmeier, C, Angen, O and Ahrens, P (2000). Comparison of bacterial cultivation, PCR, in situ hybridization and immunohistochemistry as tools for diagnosis of Haemophilus somnus pneumonia in cattle. Veterinary Microbiology 76: 385–394.CrossRefGoogle ScholarPubMed
Thompson, KG and Little, PB (1981). Effect of Haemophilus somnus on bovine endothelial cells in organ culture. American Journal of Veterinary Research 42: 748–754.Google ScholarPubMed
Thompson, KG, Vickers, MC, Stevenson, BJ and Davidson, GW (1987). Thromboembolic meningocephalitis caused by Haemophilus somnus infection in a bull calf—a new disease in New Zealand. New Zealand Veterinary Journal 35: 5–7.CrossRefGoogle Scholar
Vaara, M and Nikaido, H (1984). Molecular organization of bacterial outer membrane. In: Rietschel, ET editor. Chemistry of Endotoxin. Amsterdam: Elsevier Science Publishers, pp. 1–45.Google Scholar
Van Belkum, A, Scherer, S, van Alphen, L and Verbrugh, H (1998). Short-sequence DNA repeats in prokaryotic genomes. Microbiology and Molecular Biology Reviews 62: 275–293.CrossRefGoogle ScholarPubMed
Vimr, E and Lichtensteiger, C (2002). To sialylate, or not to sialylate: that is the question. Trends in Microbiology 10: 254–257.CrossRefGoogle ScholarPubMed
Vimr, E, Lichtensteiger, C and Steenbergen, S (2000). Sialic acid metabolism's dual function in Haemophilus influenzae. Molecular Microbiology 36: 1113–1123.CrossRefGoogle ScholarPubMed
Walker, RL, Biberstein, EL, Pritchett, RF and Kirkham, C (1985). Deoxyribonucleic acid relatedness among “Haemophilus somnus”, “Haemophilus agni”, “Histophilus ovis”, “Actinobacillus seminis” and Haemophilus influenzae. International Journal of Systemic Bacteriology 35: 46–49.CrossRefGoogle Scholar
Ward, AC, Dyer, NW and Corbeil, LB (1999). Characterization of putative Haemophilus somnus isolates from tonsils of American bison (Bison bison). Canadian Journal of Veterinary Research 63: 166–169.Google ScholarPubMed
Weiser, JN, Shchepetov, M and Chong, ST (1997). Decoration of lipopolysaccharide with phosphorylcholine: phase-variable characteristic of Haemophilus influenzae. Infection and Immunity 65: 943–950CrossRefGoogle ScholarPubMed
Weiser, JN, Pan, NMcGowan, KL, Musher, D, Martin, A and Richards, J (1998). Phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae contributes to persistence in the respiratory tract and sensitivity to serum killing mediated by C-reactive protein. Journal of Experimental Medicine 187: 631–640.CrossRefGoogle ScholarPubMed
Widders, PR, Paisley, LG, Gogolewski, RP, Evermann, JF, Smith, JW and Corbeil, LB (1986). Experimental abortion and the systemic immune response to “Haemophilus somnus” in cattle. Infection and Immunity 54: 555–560.CrossRefGoogle ScholarPubMed
Widders, PR, Smith, JW, Yarnall, M, McGuire, TC and Corbeil, LB (1988). Non-immune immunoglobulin binding of Haemophilus somnus. Journal of Medical Microbiology 26: 307–311.CrossRefGoogle ScholarPubMed
Widders, PR, Dorrance, LA, Yarnall, M and Corbeil, LB (1989a). Immunoglobulin-binding activity among pathogenic and carrier isolates of Haemophilus somnus. Infection and Immunity 57: 639–42.CrossRefGoogle ScholarPubMed
Widders, PR, Dowling, SC, Gogolewski, RP, Smith, JW and Corbeil, LB (1989b). Isotypic antibody responses in cattle infected with Haemophilus somnus. Research in Veterinary Science 46: 212–217.CrossRefGoogle ScholarPubMed
Won, J and Griffith, RW (1993). Cloning and sequencing of the gene encoding a 31 kilodalton antigen of Haemophilus somnus. Infection and Immunity 61: 2813–2821.CrossRefGoogle ScholarPubMed
Wu, Y, McQuiston, JH, Cox, A, Pack, TD and Inzana, TJ (2000). Molecular cloning and mutagenesis of a DNA locus involved in lipooligosaccharide biosynthesis in Haemophilus somnus. Infection and Immunity 68: 310–319.CrossRefGoogle ScholarPubMed
Xavier, KB and Bassler, BL (2003). LuxS quorum sensing: more than just a numbers game. Current Opinion in Microbiology 6: 191–197.CrossRefGoogle ScholarPubMed
Yang, YF, Sylte, MJ and Czuprynski, CJ (1998). Apoptosis: a possible tactic of Haemophilus somnus for evasion of killing by bovine neutrophils? Microbial Pathogenesis 24: 351–359.CrossRefGoogle ScholarPubMed
Yarnall, M, Widders, PR and Corbeil, LB (1988). Isolation and characterization of Fc receptors from Haemophilus somnus. Scandinavian Journal of Immunology 28: 129–137.CrossRefGoogle ScholarPubMed