Decoration of Histophilus somni lipooligosaccharide with N-acetyl-5-neuraminic acid enhances bacterial binding of complement factor H and resistance to killing by serum and polymorphonuclear leukocytes

Veterinary Microbiology

Volumn 161, Issue 1-2, 2012, Pages 113-121

  Inzana, Thomas J ^a   Balyan, Rajiv ^a   Howard, Michael D ^a  

^a CENTER FOR MOLECULAR MEDICINE AND INFECTIOUS DISEASES   (United States)

Author keywords

Complement; Factor H; Histophilus somni; Lipooligosaccharide; N acetyl 5 neuraminic acid; Polymorphonuclear leucocytes; Sialic acid; Sialylation; Virulence

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT IC3B; COMPLEMENT FACTOR H; LIPOOLIGOSACCHARIDE; N ACETYLNEURAMINIC ACID; THYMIDINE; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; COW; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; FETAL CALF SERUM; HEMOLYSIS; HISTOPHILUS SOMNI; HOST RESISTANCE; INNATE IMMUNITY; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PROTEIN BINDING; SIALYLATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, BACTERIAL; CATTLE; COMPLEMENT ACTIVATION; COMPLEMENT FACTOR H; CYTIDINE MONOPHOSPHATE N-ACETYLNEURAMINIC ACID; ENZYME-LINKED IMMUNOSORBENT ASSAY; HAEMOPHILUS SOMNUS; LIPOPOLYSACCHARIDES; N-ACETYLNEURAMINIC ACID; NEUTROPHILS; PHAGOCYTOSIS; PROTEIN BINDING; SERUM;

BACTERIA (MICROORGANISMS); BOVINAE; HISTOPHILUS SOMNI;

EID: 84869884697     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.07.008     Document Type: Article

References (36)

1. Anderson P., Johnston R.B., Smith D.H. Human serum activities against Haemophilus influenzae type b. J. Clin. Invest. 1972, 51:31-38.
2. Apicella M.A., Mandrell R.E., Shero M., Wilson M.E., Griffiss J.M., Brooks G.F., Lammel C., Breen J.F., Rice P.A. Modification by sialic acid of Neisseria gonorrhoeae lipooligosaccharide epitope expression in human urethral exudates: an immunoelectron microscopic analysis. J. Infect. Dis. 1990, 162:506-512.
3. Brown E.J. Complement receptors and phagocytosis. Curr. Opin. Immunol. 1991, 3:76-82.
4. Challacombe J.F., Duncan A.J., Brettin T.S., Bruce D., Chertkov O., Detter J.C., Han C.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.
5. Coligan J.E., Kruisbeek A.M., Margulies D.M., Shevach E.M., Strober W. Complement. Current Protocols in Immunology 1994, John Wiley & Sons, Inc. R. Coico (Ed.).
6. Corbeil L.B., Widders P.R., Gogolewski R.P., Arthur J., Inzana T.J., Ward A.C.S. Haemophilus somnus: bovine reproductive and respiratory disease. Can. Vet. J. 1986, 26:90-93.
7. Czuprynski C.J., Hamilton H.L. Bovine neutrophils ingest but do not kill Haemophilus somnus in vitro. Infect. Immun. 1985, 50:431-436.
8. Fearon D.T., Austen K.F. Activation of the alternative complement pathway due to resistance of zymosan-bound amplification convertase to endogenous regulatory mechanisms. PNAS 1977, 74:1683-1687.
9. Figueira M.A., Ram S., Goldstein R., Hood D.W., Moxon E.R., Pelton S.I. Role of complement in defense of the middle ear revealed by restoring the virulence of nontypeable Haemophilus influenzae siaB mutants. Infect. Immun. 2007, 75:325-333.
10. Fischer S.H., Rest R.F. Gonococci possessing only certain P.II outer membrane proteins interact with human neutrophils. Infect. Immun. 1988, 56:1574-1579.
11. Gill M.J., McQuillen D.P., van Putten J.P., Wetzler L.M., Bramley J., Crooke H., Parsons N.J., Cole J.A., Smith H. Functional characterization of a sialyltransferase-deficient mutant of Neisseria gonorrhoeae. Infect. Immun. 1996, 64:3374-3378.
12. Gogolewski R.P., Leathers C.W., Liggitt H.D., Corbeil L.B. Experimental Haemophilus somnus pneumonia in calves and immunoperoxidase localization of bacteria. Vet. Pathol. 1987, 24:250-256.
13. Gulati S., Cox A., Lewis L.A., Michael F.S., Li J., Boden R., Ram S., Rice P.A. Enhanced factor H binding to sialylated gonococci is restricted to the sialylated lacto-N-neotetraose lipooligosaccharide species: implications for serum resistance and evidence for a bifunctional lipooligosaccharide sialyltransferase in gonococci. Infect. Immun. 2005, 73:7390-7397.
14. Harvey H.A., Swords W.E., Apicella M.A. The mimicry of human glycolipids and glycosphingolipids by the lipooligosaccharides of pathogenic Neisseria and Haemophilus. J. Autoimmun. 2001, 16:257-262.
15. Hood D.W., Makepeace K., Deadman M.E., Rest R.F., Thibault P., Martin A., Richards J.C., Moxon E.R. Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol. Microbiol. 1999, 33:679-692.
16. Howard M.D., Boone J.H., Buechner-Maxwell V., Schurig G.G., Inzana T.J. Inhibition of bovine macrophage and polymorphonuclear leukocyte superoxide anion production by Haemophilus somnus. Microb. Pathogen. 2004, 37:263-271.
17. Howard M.D., Willis L., Wakarchuk W., St.Michael F., Cox A., Horne W.T., Hontecilas R., Bassaganya-Riera J., Lorenz E., Inzana T.J. Genetics and molecular specificity of sialylation of Histophilus somni lipooligosaccharide (LOS) and the effect of LOS sialylation on Toll-like receptor-4 signaling. Vet. Microbiol. 2011, 153:163-172.
18. 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.
19. Inzana T.J., Iritani B., Gogolewski R.P., Kania S.A., Corbeil L.B. Purification and characterization of lipooligosaccharides from four strains of " Haemophilus somnus" Infect. Immun. 1988, 56:2830-2837.
20. Inzana T.J., Tosi M.F., Kaplan S.L., Anderson D.C., Mason E.O., Williams R.P. Effect of Haemophilus influenzae type b lipopolysaccharide on complement activation and polymorphonuclear leukocyte function. Pediatr. Res. 1987, 22:659-666.
21. Madico G., Ngampasutadol J., Gulati S., Vogel U., Rice P.A., Ram S. Factor H binding and function in sialylated pathogenic neisseriae is influenced by gonococcal, but not meningococcal, porin. J. Immunol. 2007, 178:4489-4497.
22. Madico G., Welsch J.A., Lewis L.A., McNaughton A., Perlman D.H., Costello C.E., Ngampasutadol J., Vogel U., Granoff D.M., Ram S. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 2006, 177:501-510.
23. 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.
24. 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.
25. Riches D., Stanworth D. A simple new method of measuring the capacity to activate the alternative complement pathway. Immunol. Lett. 1980, 1:363-366.
26. Sandal I., Inzana T.J. A genomic window into the virulence of Histophilus somni. Trends Microbiol. 2010, 18:90-99.
27. Sandal I., Inzana T.J., Molinaro A., De Castro C., Shao J.Q., Apicella M.A., Cox A.D., St Michael F., Berg G. Identification, structure, and characterization of an exopolysaccharide produced by Histophilus somni during biofilm formation. BMC Microbiol. 2011, 11:186.
28. Severi E., Hood D.W., Thomas G.H. Sialic acid utilization by bacterial pathogens. Microbiology 2007, 153:2817-2822.
29. 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.
30. Tullius M.V., Munson R.S., Wang J., Gibson B.W. Purification, cloning, and expression of a cytidine 5'-monophosphate N-acetylneuraminic acid synthetase from Haemophilus ducreyi. J. Biol. Chem. 1996, 271:15373-15380.
31. Vimr E.R. Microbial sialidases: does bigger always mean better?. Trends Microbiol. 1994, 2:271-277.
32. 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.
33. Vogel U., Weinberger A., Frank R., Muller A., Kohl J., Atkinson J.P., Frosch M. Complement factor C3 deposition and serum resistance in isogenic capsule and lipooligosaccharide sialic acid mutants of serogroup B Neisseria meningitidis. Infect. Immun. 1997, 65:4022-4029.
34. Ward C.K., Inzana T.J. Identification and characterization of a DNA region involved in the export of capsular polysaccharide by Actinobacillus pleuropneumoniae serotype 5a. Infect. Immun. 1997, 65:2491-2496.
35. Wetzler L.M., Barry K., Blake M.S., Gotschlich E.C. Gonococcal lipooligosaccharide sialylation prevents complement-dependent killing by immune sera. Infect. Immun. 1992, 60:39-43.
36. Yamasaki R., Bacon B.E., Nasholds W., Schneider H., Griffiss J.M. Structural determination of oligosaccharides derived from lipooligosaccharide of Neisseria gonorrhoeae F62 by chemical, enzymatic, and two-dimensional NMR methods. Biochemistry 1991, 30:10566-10575.