Genetics and molecular specificity of sialylation of Histophilus somni lipooligosaccharide (LOS) and the effect of LOS sialylation on Toll-like receptor-4 signaling

Veterinary Microbiology

Volumn 153, Issue 1-2, 2011, Pages 163-172

  Howard, Michael D ^a   Willis, Lisa ^b   Wakarchuk, Warren ^b   St Michael, Frank ^b   Cox, Andrew ^b   Horne, William T ^c   Hontecillas, Raquel ^c   Bassaganya Riera, Josep ^c   Lorenz, Eva ^d   Inzana, Thomas J ^a  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Histophilus somni; NF B; Phase variation; Sialic acid; Sialyltransferase; TLR 4

Indexed keywords

BACTERIAL PROTEIN; EPITOPE; HSST I PROTEIN; HSST II PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOOLIGOSACCHARIDE; MONOCLONAL ANTIBODY; N ACETYLLACTOSAMINE SYNTHASE; NEU5AC SYNTHETASE; SIALYLTRANSFERASE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVITY; GENE FUNCTION; HISTOPHILUS SOMNI; HOST RESISTANCE; IMMUNOREACTIVITY; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE HOMOLOGY; SIALYLATION; SIGNAL TRANSDUCTION;

ANIMALS; HAEMOPHILUS DUCREYI; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HAEMOPHILUS SOMNUS; IMMUNE EVASION; LIPOPOLYSACCHARIDES; MACROPHAGES; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIALYLTRANSFERASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

BOVINAE; HAEMOPHILUS DUCREYI; HAEMOPHILUS INFLUENZAE; HISTOPHILUS SOMNI; MUS;

EID: 80052542883     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2011.02.054     Document Type: Article

References (50)

1. Bassaganya-Riera J., Reynolds K., Martino-Catt S., Cui Y., Hennighausen L., Gonzalez F., Rohrer J., Benninghoff A.U., Hontecillas R. Activation of PPAR γ and Δ by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology 2004, 127:777-791.
2. Challacombe J.F., Duncan A.J., Brettin T.S., Bruce D., Chertkov O., Detter J.C., Han D.S., Misra M., Richardson P., Tapia R., Thayer N., Xie G., Inzana T.J. Complete genome sequence of Haemophilus somnus (Histophilus somni) strain 129Pt and comparison to Haemophilus ducreyi 35000HP and Haemophilus influenzae Rd. J. Bacteriol. 2007, 189:1890-1898.
3. Corbeil L.B., Gogolewski R.P., Stephens L.R., Inzana T.J. Haemophilus somnus: antigen analysis and immune responses. Haemophilus, Actinobacillus, and Pasteurella 1995, 63-73. Plenum Press, New York. W. Donachie, F.A. Lainson, J.C. Hodgson (Eds.).
4. Cox A.D., Howard M.D., Brisson J.-R., Van Der Zwan M., Thibault P., Perry M.B., Inzana T.J. Structural analysis of the phase-variable lipooligosaccharide from Haemophilus somnus strain 738. Eur. J. Biochem. 1998, 253:507-516.
5. Czuprynski C.J., Hamilton H.L. Bovine neutrophils ingest but do not kill Haemophilus somnus in vitro. Infect. Immun. 1985, 50:431-436.
6. Danaher R.J., Levin J.C., Arking D., Burch C.L., Sandlin R., Stein D.C. Genetic basis of Neisseria gonorrhoeae lipooligosaccharide antigenic variation. J. Bacteriol. 1995, 177:7275-7279.
7. Doyle S.L., O'Neill L.A. Toll-like receptors: from the discovery of NF-κB to new insights into transcriptional regulations in innate immunity. Biochem. Pharmacol. 2006, 72:1102-1113.
8. Elswaifi S.F., St.Michael F., Sreenivas A., Cox A.D., Carman G.M., Inzana T.J. Molecular characterization of phosphorylcholine expression on the lipooligosaccharide of Histophilus somni. Microb. Pathog. 2009, 47:223-230.
9. Estabrook M.M., Christopher N.C., Griffiss J.M., Baker C.J., Mandrell R.E. Sialylation and human neutrophil killing of group C Neisseria meningitidis. J. Infect. Dis. 1992, 166:1079-1088.
10. Estabrook M.M., Griffiss J.M., Jarvis G.A. Sialylation of Neisseria meningitidis lipooligosaccharide inhibits serum bactericidal activity by masking lacto-N-neotetraose. Infect. Immun. 1997, 65:4436-4444.
11. Gao L., Linden L., Parsons N.J., Cole J.A., Smith H. Uptake of metabolites by gonococci grown with lactate in a medium containing glucose: evidence for a surface location of the sialyltransferase. Microb. Pathog. 2000, 28:257-266.
12. Gilbert M., Cunningham A.M., Watson D.C., Martin A., Richards J.C., Wakarchuk W.W. Characterization of a recombinant Neisseria meningitidis α-2,3-sialyltransferase and its acceptor specificity. Eur. J. Biochem. FEBS 1997, 249:187-194.
13. Gilbert M., Watson D.C., Cunningham A.M., Jennings M.P., Young N.M., Wakarchuk W.W. Cloning of the lipooligosaccharide α-2,3-sialyltransferase from the bacterial pathogens Neisseria meningitidis and Neisseria gonorrhoeae. J. Biol. Chem. 1996, 271:28271-28276.
14. Hirschfeld M., Ma Y., Weis J.H., Vogel S.N., Weis J.J. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J. Immunol. 2000, 165:618-622.
15. Hood D.W., Cox A.D., Gilbert M., Makepeace K., Walsh S., Deadman M.E., Cody A., Martin A., Mansson M., Schweda E.K., Brisson J.R., Richards J.C., Moxon E.R., Wakarchuk W.W. Identification of a lipopolysaccharide α-2,3-sialyltransferase from Haemophilus influenzae. Mol. Microbiol. 2001, 39:341-350.
16. Howard, M.D., 2005. Investigation of Haemophilus somnus virulence factors: lipooligosaccharide sialylation and inhibition of superoxide anion production. Doctoral dissertation. Virginia Tech, Blacksburg, VA.
17. Howard M.D., Cox A.D., Weiser J.N., Schurig G.G., Inzana T.J. Antigenic diversity of Haemophilus somnus lipooligosaccharide: phase-variable accessibility of the phosphorylcholine epitope. J. Clin. Microbiol. 2000, 38:4412-4419.
18. Inzana T.J. Electrophoretic heterogeneity and interstrain variation of the lipopolysaccharide of Haemophilus influenzae. J. Infect. Dis. 1983, 148:492-499.
19. Inzana T.J., Corbeil L.B. Haemophilus. Pathogenesis of Bacterial Infections of Animals 2004, 243-258. Iowa State University Press, Ames, Iowa. C. In, C.T. Gyles, J. Prescott, G. Songer (Eds.).
20. Inzana T.J., Glindemann G., Cox A.D., Wakarchuk W., Howard M.D. Incorporation of N-acetylneuraminic acid into Haemophilus somnus lipooligosaccharide (LOS): enhancement of resistance to serum and reduction of LOS antibody binding. Infect. Immun. 2002, 70:4870-4879.
21. Inzana T.J., Gogolewski R.P., Corbeil L.B. Phenotypic phase variation in Haemophilus somnus lipooligosaccharide during bovine pneumonia and after in vitro passage. Infect. Immun. 1992, 60:2943-2951.
22. Inzana T.J., Hensley J., McQuiston J., Lesse A.J., Campagnari A.A., Boyle S.M., Apicella M.A. Phase variation and conservation of lipooligosaccharide epitopes in Haemophilus somnus. Infect. Immun. 1997, 65:4675-4681.
23. Ish-Horowicz D., Burke J.F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981, 9:2989-2998.
24. Johnston J.W., Zaleski A., Allen S., Mootz J.M., Armbruster D., Gibson B.W., Apicella M.A., Munson R.S. Regulation of sialic acid transport and catabolism in Haemophilus influenzae. Mol. Microbiol. 2007, 66:26-39.
25. Lederer J.A., Brown J.F., Czuprynski C.J. " Haemophilus somnus" , a facultative intracellular pathogen of bovine mononuclear phagocytes. Infect. Immun. 1987, 55:381-387.
26. Lorenz E., Chemotti D.C., Vandal K., Tessier P.A. Toll-like receptor 2 represses nonpilus adhesin-induced signaling in acute infections with the Pseudomonas aeruginosa pilA mutant. Infect. Immun. 2004, 72:4561-4569.
27. Lorenz E., Patel D.D., Hartung T., Schwartz D.A. Toll-like receptor 4 (TLR4)-deficient murine macrophage cell line as an in vitro assay system to show TLR4-independent signaling of Bacteroides fragilis lipopolysaccharide. Infect. Immun. 2002, 70:4892-4896.
28. Mandrell R.E., Lesse A.J., Sugai J.V., Shero M., Griffiss J.M., Cole J.A., Parsons N.J., Smith H., Morse S.A., Apicella M.A. In vitro and in vivo modification of Neisseria gonorrhoeae lipooligosaccharide epitope structure by sialylation. J. Exp. Med. 1990, 171:1649-1664.
29. Mandrell R.E., Smith H., Jarvis G.A., Griffiss J.M., Cole J.A. Detection and some properties of the sialyltransferase implicated in the sialylation of lipopolysaccharide of Neisseria gonorrhoeae. Microb. Pathog. 1993, 14:307-313.
30. Manthey C.L., Perera P.Y., Henricson B.E., Hamilton T.A., Qureshi N., Vogel S.N. Endotoxin-induced early gene expression in C3H/HeJ (Lpsd) macrophages. J. Immunol. 1994, 153:2653-2663.
31. Miller S.I., Ernst R.K., Bader M.W. LPS, TLR4 and infectious disease diversity. Nat. Rev. 2005, 3:36-46.
32. Moran A.P., Prendergast M.M., Appelmelk B.J. Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol. Med. Microbiol. 1996, 16:105-115.
33. Palsson-McDermott E.M., O'Neill L.A. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 2004, 113:153-162.
34. Pollard A., St Michael F., Connor L., Nichols W., Cox A. Structural characterization of Haemophilus parainfluenzae lipooligosaccharide and elucidation of its role in adherence using an outer core mutant. Can. J. Microbiol. 2008, 54:906-917.
35. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
36. Pridmore A.C., Jarvis G.A., John C.M., Jack D.L., Dower S.K., Read R.C. Activation of toll-like receptor 2 (TLR2) and TLR4/MD2 by Neisseria is independent of capsule and lipooligosaccharide (LOS) sialylation but varies widely among LOS from different strains. Infect. Immun. 2003, 71:3901-3908.
37. Ram S., Sharma A.K., Simpson S.D., Gulati S., McQuillen D.P., Pangburn M.K., Rice P.A. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 1998, 187:743-752.
38. Rest R.F., Frangipane J.V. Growth of Neisseria gonorrhoeae in CMP-N-acetylneuraminic acid inhibits nonopsonic (opacity-associated outer membrane protein-mediated) interactions with human neutrophils. Infect. Immun. 1992, 60:989-997.
39. Sandal I., Hong W., Swords W.E., Inzana T.J. Characterization and comparison of biofilm development by pathogenic and commensal isolates of Histophilus somni. J. Bacteriol. 2007, 189:8179-8185.
40. Sandal I., Shao J.Q., Annadata S., Apicella M.A., Boye M., Saunders G.K., Inzana T.J. Histophilus somni biofilm formation in cardiopulmonary tissue of the bovine host following respiratory challenge. Microbes Infect. 2009, 11:254-263.
41. Shell D.M., Chiles L., Judd R.C., Seal S., Rest R.F. The Neisseria lipooligosaccharide-specific α-2,3-sialyltransferase is a surface-exposed outer membrane protein. Infect. Immun. 2002, 70:3744-3751.
42. St Michael F., Li J., Howard M.D., Duncan A.J., Inzana T.J., Cox A.D. Structural analysis of the oligosaccharide of Histophilus somni (Haemophilus somnus) strain 2336 and identification of several lipooligosaccharide biosynthesis gene homologues. Carbohydr. Res. 2005, 340:665-672.
43. Stephens L.R., Little P.B., Wilkie B.N., Barnum D.A. Infectious thromboembolic meningoencephalitis in cattle: a review. J. Am. Vet. Med. Assoc. 1981, 178:378-384.
44. Sylte M.J., Corbeil L.B., Inzana T.J., Czuprynski C.J. Haemophilus somnus induces apoptosis in bovine endothelial cells in vitro. Infect. Immun. 2001, 69:1650-1660.
45. Tagawa Y., Sanders J.D., Uchida I., Bastida-Corcuera F.D., Kawashima K., Corbeil L.B. Genetic and functional analysis of Haemophilus somnus high molecular weight-immunoglobulin binding proteins. Microb. Pathog. 2005, 39:159-170.
46. Vimr E., Lichtensteiger C. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 2002, 10:254-257.
47. Vimr E., Lichtensteiger C., Steenbergen S. Sialic acid metabolism's dual function in Haemophilus influenzae. Mol. Microbiol. 2000, 36:1113-1123.
48. Vimr E.R., Kalivoda K.A., Deszo E.L., Steenbergen S.M. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 2004, 68:132-153.
49. Weiser J.N., Love J.M., Moxon E.R. The molecular mechanism of phase variation of Haemophilus influenzae lipopolysaccharide. Cell 1989, 59:657-665.
50. Yamasaki R., Nasholds W., Schneider H., Apicella M.A. Epitope expression and partial structural characterization of F62 lipooligosaccharide (LOS) of Neisseria gonorrhoeae. Mol. Immunol. 1991, 28:1233-1242.