Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About IAI
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Infection and Immunity
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About IAI
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Molecular Pathogenesis

Expression of Phosphorylcholine by Histophilus somni Induces BovinePlatelet Aggregation

Christopher J. Kuckleburg, Shaadi F. Elswaifi, Thomas J. Inzana, Charles J. Czuprynski
Christopher J. Kuckleburg
1Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Shaadi F. Elswaifi
2Center for Molecular Medicine and Infectious Diseases, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, Virginia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Thomas J. Inzana
2Center for Molecular Medicine and Infectious Diseases, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, Virginia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Charles J. Czuprynski
1Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Madison, Wisconsin
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: czuprync@svm.vetmed.wisc.edu
DOI: 10.1128/IAI.01177-06
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Histophilus somni-induced platelet aggregation was inhibited by antagonists of the platelet-activating factor (PAF) receptor but not inhibitors of PAF synthesis. In addition, H. somni cells expressing phosphorylcholine (ChoP) induced aggregation, while ChoP−H. somni cells did not. This suggests that H. somni ChoP may induce platelet aggregation via interactions with the PAF receptor.

Histophilus somni is a gram-negative pleomorphic bacillus that causes respiratory disease primarily in cattle. Clinical signs of H. somni infection can include pneumonia, abortion, arthritis, septicemia, myocarditis, vasculitis, and an acute condition known as thrombotic meningoencephalitis (1, 3, 8, 10, 13).

The ability of H. somni to modify its lipooligosaccharide (LOS) composition and structure is thought to play an important role in its virulence. H. somni can incorporate sialic acid into the outer core of the LOS molecule, and this event has been shown to be critical for resistance to serum-mediated killing (14). It has been reported that some strains of H. somni that do not incorporate sialic acid are unable to produce disease (5). Another modification is the addition of phosphorylcholine (ChoP) to the outer core of the LOS (12).

H. somni exhibits extensive intrastrain variability in ChoP incorporation into the LOS molecule (12). The possible contribution of ChoP to H. somni pathogenesis is unknown. For other species of bacteria, ChoP can be incorporated into bacterial structures such as fibrillar proteins and cell wall components that are important for bacterial adherence to host cells. For example, the expression of ChoP by Streptococcus pneumoniae has been reported to contribute to pneumococcal adherence and invasion in the lung (6, 30) and the brain (20). Similarly, the expression of ChoP on the LOS of Haemophilus influenzae contributes to its binding and internalization by human epithelial cells (27, 28). This adherence was demonstrated to be due to an interaction between ChoP expressed on LOS and the platelet-activating factor (PAF) receptor on epithelial cells. ChoP has also been found in Actinobacillus actinomycetemcomitans, which facilitates binding to the PAF receptor on human vascular endothelial cells, followed by internalization of the bacteria (7, 23, 24). ChoP has also been detected in Bacillus spp. and Clostridium spp., and the lipopolysaccharide of Escherichia coli O26:B6 was found to activate human platelets through a PAF receptor-dependent pathway (9, 19).

Our laboratory has previously reported that H. somni and its LOS can activate bovine platelets (16). We also found that H. somni, but not its LOS, could induce platelet aggregation. The mechanism by which H. somni induces platelet aggregation is unknown. It has previously been demonstrated that endotoxin and bacteria can adhere to and activate platelets from several different mammalian species (2, 11, 18, 21, 22, 31-33). For this study, we sought to investigate the interaction between H. somni and bovine platelets and determine if bacterial expression of ChoP affects platelet activation.

We first wanted to ascertain whether platelet aggregation was induced by ChoP-expressing H. somni cells. Using colony immunoblotting with an anti-phosphorylcholine antibody (15), two H. somni variants of strain 7735 were selected for either high or low expression of ChoP. These populations were enriched through selective passage in culture. Bovine platelets (2.5 × 108 platelets) (isolation procedures were described previously [16]) were incubated with one of the two H. somni variants (multiplicity of infection [MOI] of 5:1) for 10 min in a Chronolog aggregometer. As a positive control, platelets were treated with PAF (10−6 M; Calbiochem) to induce irreversible aggregation within 5 min. It was found that ChoP+H. somni induced platelet aggregation, while ChoP−H. somni did not (Fig. 1A and B). ChoP+H. somni consistently induced approximately 15% aggregation, which was not reversible within a 30-min incubation period (data not shown). Upon microscopic examination, platelet aggregates could be observed following incubation with ChoP+ but not with ChoP−H. somni (Fig. 1C and D). In addition, we observed ChoP+H. somni within bovine platelet aggregates. Pretreatment of ChoP+H. somni with polymyxin B (10μ g/ml; Sigma) for 10 min resulted in a modest decrease in the ability of H. somni to induce aggregation (Fig. 1E).

FIG. 1.
  • Open in new tab
  • Download powerpoint
FIG. 1.

ChoP+ but not ChoP−H. somni induces bovine platelet aggregation. Platelets (500 μl, 2.5 × 108 platelets/ml) were placed in siliconized glass cuvettes and incubated with ChoP+ or ChoP−H. somni (MOI of 5:1) or with PAF (10−6 M) as a positive control. Platelet aggregation was measured for 10 min using the turbidimetric method in a Chrono-Log Model 560-Ca Dual Sample Lumi-Ionized Calcium aggregometer, and the percent aggregation was calculated using AGGRO/LINK software. The aggregation plot in A is a representative experiment of four separate experiments that were performed. The data in B illustrate the means ± standard errors of the means (SEM) of four separate experiments showing the percent aggregation induced at 10 min (*, P < 0.05 compared to ChoP+H. somni-treated platelets). For some aggregation experiments, platelets were removed from the cuvette and transferred onto glass coverslips using a Cytospin centrifuge before being fixed and stained with Diff-Quick. These platelets were then observed by light microscopy for the presence platelet-bacterium aggregates (C and D). We observed such aggregates in the presence of ChoP+ but not ChoP−H. somni. Preincubation of ChoP+H. somni for 10 min with polymyxin B (PB) (10 μg/ml) inhibited platelet aggregation (E). These data represent the means ± SEM of four separate experiments (*, P < 0.05 compared to ChoP+-treated platelets). PBS, phosphate-buffered saline.

We next considered the possibility that H. somni may interact with the PAF receptor on platelets. To exclude the contribution of platelet-derived PAF, we incubated platelets with previously described selective inhibitors of phospholipase A2, AACOCF3 (10 μM; Calbiochem) or cPLA (10 μM; Calbiochem), for 10 min prior to the addition of ChoP+H. somni (17, 26). Some platelets were preincubated with the PAF receptor antagonist WEB 2170 (10μ g/ml) at a concentration that was previously demonstrated to inhibit platelet activation by PAF (29). Platelets preincubated with WEB 2170 but not inhibitors of PAF synthesis demonstrated a significant diminution in platelet aggregation following incubation with ChoP+H. somni (Fig. 2).

FIG. 2.
  • Open in new tab
  • Download powerpoint
FIG. 2.

Platelet aggregation is inhibited by the PAF receptor antagonist WEB 2170. Platelets (500 μl, 2.5 × 108 platelets/ml) were pretreated for 10 min with the PAF receptor antagonist WEB 2170 (10 μg/ml) or the PAF synthesis inhibitor AACOCF (10μ M) or cPLA (10 μM) before incubation with ChoP+H. somni (MOI of 5:1). Platelet aggregation was then measured as described in the legend of Fig. 1. The data represent the means ± SEM of four separate experiments (*, P< 0.05 compared to platelets incubated with ChoP+H. somni alone).

To study PAF receptor signaling, we used an inhibitor of downstream signaling through phospholipase Cβ (D609, 200μ M; Calbiochem) and the PAF receptor antagonist WEB 2170 (10μ g/ml). Using an antibody against P-selectin as a marker of platelet activation (BD Bioscience), we observed low baseline P-selectin levels in unstimulated platelets. Following incubation with PAF (10−7 M) or ChoP+H. somni (MOI of 5:1), we observed a significant increase in platelet activation (Fig. 3A and B). However, neither PAF antagonist resulted in a significant decrease in platelet P-selectin expression induced by ChoP+H. somni, suggesting that PAF receptor activation is not required for platelet activation by ChoP+H. somni. In addition, D609 inhibited PAF-induced aggregation but not aggregation induced by ChoP+H. somni (data not shown). We next compared platelet activation in response to ChoP+ or ChoP−H. somni as determined by flow cytometry evaluation of P-selectin expression and fibrinogen binding. The latter event, which is required for platelet aggregation, was detected using an antibody against platelet-bound fibrinogen (American Diagnostica, Stamford, CT). We found that both ChoP+ and ChoP−H. somni cells induced significant platelet P-selectin expression (Fig. 3C). Surprisingly, ChoP+H. somni did not induce a significant level of platelet fibrinogen binding compared to platelets stimulated with PAF. The lack of fibrinogen binding suggests that H. somni may induce platelet aggregate formation using a mechanism distinct from activation induced by PAF.

FIG. 3.
  • Open in new tab
  • Download powerpoint
FIG. 3.

H. somni-induced platelet activation is independent of PAF receptor signaling. Bovine platelets (2.5 × 108) were incubated for 10 min at 37°C with ChoP+ or ChoP−H. somni (MOI of 5:1) or PAF (10−7 M). The platelets were then fixed in paraformaldehyde (0.4% final volume) and stained with antibodies for P-selectin or fibrinogen before being analyzed by flow cytometry. The results reflect the means± SEM of percent positive platelets from at least three separate experiments. (A) Platelets preincubated with the PAF receptor antagonist WEB 2170 or the phospholipase Cβ inhibitor D609 expressed significantly less P-selectin after PAF stimulation than platelets treated with PAF alone (*, P < 0.05 compared to untreated platelets). (B) Pretreatment of platelets with WEB 2170 or D609 resulted in a modest decrease in P-selection expression in platelets challenged with H. somni; however, this decrease was not significant (P > 0.05 compared to platelets incubated with ChoP+H. somni alone). Panel C illustrates that platelets incubated with either ChoP+ or ChoP−H. somni significantly up-regulated platelet P-selectin expression. However, neither strain was able to induce significant levels of platelet fibrinogen binding compared to untreated platelets (*, P < 0.05 compared to untreated platelets).

Transmission electron microscopy (TEM) was used to visualize whether the expression of ChoP by H. somni affected the adherence of the bacteria to platelets or platelet morphology. Bovine platelets were incubated with ChoP+ or ChoP−H. somni for 10 min before being fixed and embedded for TEM. Unactivated platelets demonstrated their characteristic discoid shape, with no significant changes in morphology (Fig. 4A). Following incubation with ChoP+ or ChoP−H. somni, bovine platelets exhibited spreading, pseudopod formation, and changes in morphology indicative of platelet activation (Fig. 4B). Although platelet spreading and pseudopod formation were observed following exposure to either ChoP+ or ChoP−H. somni, only ChoP+H. somni cells were capable of inducing platelet aggregation (Fig. 4C and D). In addition, obvious binding of platelets to ChoP+H. somni only was observed. Closer examination of this interaction revealed surface structures on ChoP+H. somni that appeared to facilitate the adherence of the bacteria to the platelets (Fig. 4E and F).

FIG. 4.
  • Open in new tab
  • Download powerpoint
FIG. 4.

Transmission electron microscopy of platelets activated by H. somni. Platelets (500 μl, 2.5 × 108 platelets/ml) were placed in siliconized glass cuvettes and incubated with ChoP+ or ChoP−H. somni (MOI of 5:1) in a Chrono-Log Model 560-Ca Dual Sample Lumi-Ionized Calcium aggregometer. After a 10-min incubation, the platelet-rich plasma was fixed with a 25% volume of Karnovsky's solution (2.5% glutaraldehyde, 4% paraformaldehyde) for 10 min at room temperature and then centrifuged onto glass coverslips at 1,500 × g for 10 min to facilitate TEM processing. (A) Unactivated bovine platelets exhibit the typical discoid or “plate” morphology. (B) Shape change and pseudopod formation but no aggregate formation by bovine platelets incubated with ChoP−H. somni. (C and D) Aggregates of bovine platelets incubated with ChoP+H. somni. (E and F) Platelets incubated with ChoP+H. somni at greater magnification, with arrows indicating areas of attachment between bovine platelets and H. somni. These results are representative of three separate experiments.

In this study, we demonstrated that ChoP expression by H. somni plays a role in its interactions with bovine platelets. Preincubation of platelets with the PAF receptor antagonist WEB 2170 prevented platelet aggregation. However, the ineffectiveness of downstream PAF receptor signaling inhibitors suggests that PAF receptor signaling was not required for platelet activation or aggregation. One possible explanation may reflect the location of the ChoP molecule on H. somni LOS, where it is coupled to the primary glucose residue that is bound to heptose I (4). Steric interference from sugars in the outer core may make ChoP less accessible to interactions with the extracellular environment. In contrast, the ChoP group on H. influenza LOS is located on a terminal glycose on either heptose I or heptose III, where it may be more accessible for PAF receptor binding (25). Our findings suggest that H. somni may interact with the PAF receptor, but the resulting events are dissimilar to those by which PAF activates platelets. Upon careful examination, we conclude that aggregation reflected cross-linking between platelets and bacteria, a response that was not observed in bacteria that lacked ChoP (Fig. 1C and D and 4B to D). Future work will be directed at determining if H. somni ChoP interacts directly with the PAF receptor or through another platelet receptor and how these interactions may contribute to platelet activation.

Statistical analysis.

An unbalanced one-way analysis of variance was used to determine if significant variation existed between group means. Pairwise comparisons of group means were performed using Tukey's test (P < 0.05) with the Prism 4 statistical package (GraphPad, San Diego, CA).

ACKNOWLEDGMENTS

This work was supported by funding from the University of Wisconsin School of Veterinary Medicine, the Wisconsin Agriculture Experiment Station (project 3094), and the United States Department of Agriculture National Research Initiative (2005-35204-16169 to C.J.C. and 2003-35204-13637 to T.J.I.).

We thank Yongjing Li for help in preparing samples for transmission electron microscopy. WEB 2170 was generously provided by Boehringer-Ingelheim (Ridgefield, CT).

FOOTNOTES

    • Received 26 July 2006.
    • Returned for modification 13 September 2006.
    • Accepted 9 November 2006.
  • Copyright © 2007 American Society for Microbiology

REFERENCES

  1. 1.↵
    Andrews, J. J., T. D. Anderson, L. N. Slife, and G. W. Stevenson. 1985. Microscopic lesions associated with the isolation of Haemophilus somnus from pneumonic bovine lungs. Vet. Pathol.22:131-136.
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    Clawson, C. C., J. G. White, and M. C. Herzberg. 1980. Platelet interaction with bacteria. VI. contrasting the role of fibrinogen and fibronectin.Am. J. Hematol.9:43-53.
    OpenUrlPubMedWeb of Science
  3. 3.↵
    Corbeil, L. B., J. E. Arthur, P. R. Widders, J. W. Smith, and A. F. Barbet. 1987 . Antigenic specificity of convalescent serum from cattle with Haemophilus somnus-induced experimental abortion.Infect. Immun.55:1381-1386.
    OpenUrlAbstract/FREE Full Text
  4. 4.↵
    Cox, A. D., M. D. Howard, J. R. Brisson, M. van der Zwan, P. Thibault, M. B. Perry, and T. J. Inzana. 1998. Structural analysis of the phase-variable lipooligosaccharide from Haemophilus somnus strain 738. Eur. J. Biochem.253:507-516.
    OpenUrlPubMed
  5. 5.↵
    Cox, A. D., M. D. Howard, and T. J. Inzana. 2003. Structural analysis of the lipooligosaccharide from the commensal Haemophilus somnus strain 1P. Carbohydr. Res.338:1223-1228.
    OpenUrlCrossRefPubMed
  6. 6.↵
    Cundell, D. R., N. P. Gerard, C. Gerard, I. Idanpaan-Heikkila, and E. I. Tuomanen. 1995. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature377:435-438.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    Fillon, S., K. Soulis, S. Rajasekaran, H. Benedict-Hamilton, J. N. Radin, C. J. Orihuela, K. C. El Kasmi, G. Murti, D. Kaushal, M. W. Gaber, J. R. Weber, P. J. Murray, and E. I. Tuomanen. 2006. Platelet-activating factor receptor and innate immunity: uptake of gram-positive bacterial cell wall into host cells and cell-specific pathophysiology. J. Immunol.177:6182-6191.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    Gogolewski, R. P., C. W. Leathers, H. D. Liggitt, and L. B. Corbeil. 1987. Experimental Haemophilus somnus pneumonia in calves and immunoperoxidase localization of bacteria. Vet. Pathol.24:250-256.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    Harnett, W., and M. M. Harnett. 1999. Phosphorylcholine: friend or foe of the immune system? Immunol. Today20:125-129.
    OpenUrlCrossRefPubMedWeb of Science
  10. 10.↵
    Harris, F. W., and E. D. Janzen. 1984. The Haemophilus somnus disease complex (haemophilosis): a review.Can. Vet. J.30:816-822.
    OpenUrl
  11. 11.↵
    Houlihan, R. B., and A. L. Copley. 1946. The adhesion of rabbit platelets to bacteria. J. Bacteriol.52:439-448.
    OpenUrlFREE Full Text
  12. 12.↵
    Howard, M. D., A. D. Cox, J. N. Weiser, G. G. Schurig, and T. J. Inzana. 2000 . Antigenic diversity of Haemophilus somnus lipooligosaccharide: phase-variable accessibility of the phosphorylcholine epitope. J. Clin. Microbiol.38:4412-4419.
    OpenUrlAbstract/FREE Full Text
  13. 13.↵
    Humphrey, J. D., P. B. Little, D. A. Barnum, P. A. Doig, L. R. Stephens, and J. Thorsen. 1982. Occurrence of “Haemophilus somnus” in bovine semen and in the prepuce of bulls and steers. Can. J. Comp. Med.46:215-217.
    OpenUrlPubMedWeb of Science
  14. 14.↵
    Inzana, T. J., G. Glindemann, A. D. Cox, W. Wakarchuk, and M. D. Howard. 2002. Incorporation of N-acetylneuraminic acid into Haemophilus somnus lipooligosaccharide (LOS): enhancement of resistance to serum and reduction of LOS antibody binding. Infect. Immun.70:4870-4879.
    OpenUrlAbstract/FREE Full Text
  15. 15.↵
    Inzana, T. J., R. P. Gogolewski, and L. B. Corbeil. 1992. Phenotypic phase variation in Haemophilus somnus lipooligosaccharide during bovine pneumonia and after in vitro passage. Infect. Immun.60:2943-2951.
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    Kuckleburg, C. J., M. J. Sylte, T. J. Inzana, L. B. Corbeil, B. J. Darien, and C. J. Czuprynski. 2005. Bovine platelets activated by Haemophilus somnus and its LOS induce apoptosis in bovine endothelial cells. Microb. Pathog.38:23-32.
    OpenUrlCrossRefPubMed
  17. 17.↵
    Lockhart, L. K., C. Pampolina, B. R. Nickolaychuk, and A. McNicol. 2001. Evidence for a role for phospholipase C, but not phospholipase A2, in platelet activation in response to low concentrations of collagen. Thromb. Haemost.85:882-889.
    OpenUrlPubMed
  18. 18.↵
    Malhotra, R., R. Priest, M. R. Foster, and M. I. Bird. 1998 . P-selectin binds to bacterial lipopolysaccharide.Eur. J. Immunol.28:983-988.
    OpenUrlCrossRefPubMed
  19. 19.↵
    Nystrom, M. L., M. A. Barradas, J. Y. Jeremy, and D. P. Mikhailidis. 1994. Platelet shape change in whole blood: differential effects of endotoxin.Thromb. Haemost.71:646-650.
    OpenUrlPubMedWeb of Science
  20. 20.↵
    Ring, A., J. N. Weiser, and E. I. Tuomanen. 1998 . Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway.J. Clin. Investig.102:347-360.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Salden, H. J., and B. M. Bas. 1994. Endotoxin binding to platelets in blood from patients with a sepsis syndrome. Clin. Chem.40:1575-1579.
    OpenUrlAbstract/FREE Full Text
  22. 22.↵
    Saluk-Juszczak, J., B. Wachowicz, and W. Kaca. 2000. Endotoxins stimulate generation of superoxide radicals and lipid peroxidation in blood platelets. Microbios103:17-25.
    OpenUrlPubMed
  23. 23.↵
    Schenkein, H. A., S. E. Barbour, C. R. Berry, B. Kipps, and J. G. Tew. 2000. Invasion of human vascular endothelial cells by Actinobacillus actinomycetemcomitans via the receptor for platelet-activating factor. Infect. Immun.68:5416-5419.
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    Schenkein, H. A., C. R. Berry, D. Purkall, J. A. Burmeister, C. N. Brooks, and J. G. Tew. 2001 . Phosphorylcholine-dependent cross-reactivity between dental plaque bacteria and oxidized low-density lipoproteins.Infect. Immun.69:6612-6617.
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    Schweda, E. K., J. R. Brisson, G. Alvelius, A. Martin, J. N. Weiser, D. W. Hood, E. R. Moxon, and J. C. Richards. 2000. Characterization of the phosphocholine-substituted oligosaccharide in lipopolysaccharides of type b Haemophilus influenzae.Eur. J. Biochem.267:3902-3913.
    OpenUrlPubMed
  26. 26.↵
    Seno, K., T. Okuno, K. Nishi, Y. Murakami, F. Watanabe, T. Matsuura, M. Wada, Y. Fujii, M. Yamada, T. Ogawa, T. Okada, H. Hashizume, M. Kii, S. Hara, S. Hagishita, S. Nakamoto, K. Yamada, Y. Chikazawa, M. Ueno, I. Teshirogi, T. Ono, and M. Ohtani. 2000. Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J. Med. Chem.43:1041-1044.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    Swords, W. E., B. A. Buscher, K. Ver Steeg Ii, A. Preston, W. A. Nichols, J. N. Weiser, B. W. Gibson, and M. A. Apicella. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol.37:13-27.
    OpenUrlCrossRefPubMedWeb of Science
  28. 28.↵
    Swords, W. E., M. R. Ketterer, J. Shao, C. A. Campbell, J. N. Weiser, and M. A. Apicella. 2001 . Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell. Microbiol.3:525-536.
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.↵
    Teng, C. M., S. M. Yu, F. N. Ko, C. C. Chen, W. C. Wang, K. Y. Chen, Y. L. Huang, and T. F. Huang. 1991. Comparison of the actions of some platelet-activating factor antagonists on platelets and aortic smooth muscles. Eur. J. Pharmacol.205:151-156.
    OpenUrlCrossRefPubMed
  30. 30.↵
    Tuomanen, E. 1999. Molecular and cellular biology of pneumococcal infection. Curr. Opin. Microbiol.2:35-39.
    OpenUrlCrossRefPubMedWeb of Science
  31. 31.↵
    Wachowicz, B., J. Saluk, and W. Kaca. 1998. Response of blood platelets to Proteus mirabilis lipopolysaccharide.Microbiol. Immunol.42:47-49.
    OpenUrlPubMed
  32. 32.
    Washida, S. 1978. Endotoxin receptor site. I. Binding of endotoxin to platelets. Acta Med. Okayama32:159-167.
    OpenUrlPubMed
  33. 33.↵
    Washida, S. 1978. Endotoxin receptor site. II. Specificity of endotoxin receptor of platelets and sensitivity to endotoxin in vivo.Acta Med. Okayama32:217-223.
    OpenUrlPubMed
PreviousNext
Back to top
Download PDF
Citation Tools
Expression of Phosphorylcholine by Histophilus somni Induces BovinePlatelet Aggregation
Christopher J. Kuckleburg, Shaadi F. Elswaifi, Thomas J. Inzana, Charles J. Czuprynski
Infection and Immunity Jan 2007, 75 (2) 1045-1049; DOI: 10.1128/IAI.01177-06

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Infection and Immunity article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Expression of Phosphorylcholine by Histophilus somni Induces BovinePlatelet Aggregation
(Your Name) has forwarded a page to you from Infection and Immunity
(Your Name) thought you would be interested in this article in Infection and Immunity.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Expression of Phosphorylcholine by Histophilus somni Induces BovinePlatelet Aggregation
Christopher J. Kuckleburg, Shaadi F. Elswaifi, Thomas J. Inzana, Charles J. Czuprynski
Infection and Immunity Jan 2007, 75 (2) 1045-1049; DOI: 10.1128/IAI.01177-06
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • Statistical analysis.
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

Pasteurellaceae
phosphorylcholine
Platelet Aggregation

Related Articles

Cited By...

About

  • About IAI
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #IAIjournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0019-9567; Online ISSN: 1098-5522