Lipopolysaccharide of Coxiella burnetii

  • Craig T. Narasaki
  • Rudolf Toman
Part of the Advances in Experimental Medicine and Biology book series (volume 984)


A lipopolysaccharide (LPS) is considered to be one of the major determinants of virulence expression and infection of virulent Coxiella burnetii. The LPSs from virulent phase I (LPS I) and from avirulent phase II (LPS II) bacteria were investigated for their chemical composition, structure and biological properties. LPS II is of rough (R) type in contrast to LPS I, which is phenotypically smooth (S) and contains a noticeable amount of two sugars virenose (Vir) and dihydrohydroxystreptose (Strep), which have not been found in other LPSs and can be considered as unique biomarkers of the bacterium. Both sugars were suggested to be located mostly in terminal positions of the O-specific chain of LPS I (O-PS I) and to be involved in the immunobiology of Q fever. There is a need to establish a more detailed chemical structure of LPS I in connection with prospective, deeper studies on mechanisms of pathogenesis and immunity of Q fever, its early and reliable diagnosis, and effective prophylaxis against the disease. This will also help to better understanding of host-pathogen interactions and contribute to improved modulation of pathological reactions which in turn are prerequisite for research and development of vaccines of new type. A fundamental understanding of C. burnetii LPS biosynthesis is still lacking. The intracellular nature of the bacterium, lack of genetic tools and its status as a selected agent have made elucidating basic physiological mechanisms challenging. The GDP-β-D-Vir biosynthetic pathway proposed most recently is an important initial step in this endeavour. The current advanced technologies providing the genetic tools necessary to screen C. burnetii mutants and propagate isogenic mutants might speed the discovery process.


Coxiella burnetii Biosynthesis Function Lipopolysaccharide Q fever Structure 



This research was supported in part by the grant 2/0026/12 from the Scientific Grant Agency of Ministry of Education of Slovak Republic and the Slovak Academy of Sciences.


  1. Alexander C, Rietschel ET (2001) Bacterial lipopolysaccharides and innate immunity. J Endotoxin Res 7:167–202PubMedGoogle Scholar
  2. Al-Hendy A, Toivanen P, Skurnik M (1991) Expression cloning of Yersinia enterocolitica O:3 rfb gene cluster in Escherichia coli K12. Microb Pathog 10:47–59PubMedGoogle Scholar
  3. Amano K, Williams JC (1984) Chemical and immunological characterization of lipopolysaccharides from phase I and phase II Coxiella burnetii. J Bacteriol 160:994–1002PubMedGoogle Scholar
  4. Amano K, Williams JC, Missler SR et al (1987) Structure and biological relationships of Coxiella burnetii lipopolysaccharides. J Biol Chem 262:4740–4747PubMedGoogle Scholar
  5. Aschauer H, Grob A, Hildebrandt J et al (1990) Highly purified lipid X is devoid of immunostimulatory activity. Isolation and characterization of immunostimulating contaminants in a batch of synthetic lipid X. J Biol Chem 265:9159–9164PubMedGoogle Scholar
  6. Awomoyi AA, Rallabhandi P, Pollin TI et al (2007) Association of TLR4 polymorphisms with asymptomatic respiratory syncytial virus infection in high-risk infants and young children. J Immunol 179:3171–3177PubMedGoogle Scholar
  7. Baca OG, Martinez IL, Aragon AS et al (1980) Isolation and partial characterization of a lipopolysaccharide from phase II Coxiella burnetii. Can J Microbiol 26:819–826Google Scholar
  8. Bisercic M, Feutrier JY, Reeves PR (1991) Nucleotide sequences of the gnd genes from nine natural isolates of Escherichia coli: evidence of intragenic recombination as a contributing factor in the evolution of the polymorphic gnd locus. J Bacteriol 173:3894–3900PubMedGoogle Scholar
  9. Bowen RA (2008) Protein hydrophobicity plots.
  10. Bulut Y, Faure E, Thomas L et al (2002) Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J Immunol 168:1435–1440PubMedGoogle Scholar
  11. Burns SM, Hull SI (1998) Comparison of loss of serum resistance by defined lipopolysaccharide mutants and an acapsular mutant of uropathogenic Escherichia coli O75:K5. Infect Immun 66:4244–4253PubMedGoogle Scholar
  12. Capo C, Zugun F, Stein A et al (1996) Upregulation of tumor necrosis factor-α and interleukin-1β in Q fever endocarditis. Infect Immun 64:1638–1642PubMedGoogle Scholar
  13. Capo C, Amirayan N, Ghigo E et al (1999) Circulating cytokine balance and activation markers of leucocytes in Q fever. Clin Exp Immunol 115:120–123PubMedGoogle Scholar
  14. Caroff M, Brisson JR, Martin A et al (2000) Structure of the Bordetella pertussis 1414 endotoxin. FEBS Lett 477:8–14PubMedGoogle Scholar
  15. Chen MM, Glover KJ, Imperiali B (2007) From peptide to protein: comparative analysis of the substrate specificity of N-linked glycosylation in Campylobacter jejuni. Biochemistry 46:5579–5585PubMedGoogle Scholar
  16. Clarke BR, Cuthbertson L, Whitfield C (2004) Nonreducing terminal modifications determine the chain length of polymannose O-antigens of Escherichia coli and couple chain termination to polymer export via an ATP-binding cassette transporter. J Biol Chem 279:35709–35718PubMedGoogle Scholar
  17. Coleman SA, Fischer ER, Howe D et al (2004) Temporal analysis of Coxiella burnetii morphological differentiation. J Bacteriol 186:7344–7352PubMedGoogle Scholar
  18. Coleman SA, Fischer ER, Cockrell DC et al (2007) Proteome and antigen profiling of Coxiella burnetii developmental forms. Infect Immun 75:290–298PubMedGoogle Scholar
  19. Darveau RP, Pham TT, Lemley K et al (2004) Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both toll-like receptors 2 and 4. Infect Immun 72:5041–5051PubMedGoogle Scholar
  20. Dellacasagrande J, Capo C, Raoult D et al (1999) IFN-γ-mediated control of Coxiella burnetii survival in monocytes: the role of cell apoptosis and TNF. J Immunol 162:2259–2265PubMedGoogle Scholar
  21. Dellacasagrande J, Ghigo E, Capo C et al (2000a) Coxiella burnetii survives in monocytes from patients with Q fever endocarditis: involvement of tumor necrosis factor. Infect Immun 68:160–164PubMedGoogle Scholar
  22. Dellacasagrande J, Ghigo E, Machergui-El Hammami S et al (2000b) Alpha(v)beta(3) integrin and bacterial lipopolysaccharide are involved in Coxiella burnetii-stimulated production of tumor necrosis factor by human monocytes. Infect Immun 68:5673–5678PubMedGoogle Scholar
  23. Demerec M, Adelberg EA, Clark AJ et al (1966) A proposal for a uniform nomenclature in bacterial genetics. Genetics 54:61–76PubMedGoogle Scholar
  24. Denison AM, Massung RF, Thompson HA (2007) Analysis of the O-antigen biosynthesis regions of phase II isolates of Coxiella burnetii. FEMS Microbiol Lett 267:102–107PubMedGoogle Scholar
  25. Diaz QM, Lukacova M (1998) Immunological consequences of Coxiella burnetii phase variation. Acta Virol 42:181–185Google Scholar
  26. Dotson SB, Rush JS, Ricketts AD et al (1995) Mannosylphosphoryldolichol-mediated O-mannosylation of yeast glycoproteins: stereospecificity and recognition of the alpha-isoprene unit by a purified mannosyltransferase. Arch Biochem Biophys 316:773–779PubMedGoogle Scholar
  27. Doyle SL, O’ Neill LA (2006) Toll-like receptors from the discovery of NF-χB to new insights into transcriptional regulations in innate imunity. Biochem Pharmacol 72:1102–1113PubMedGoogle Scholar
  28. D’Souza-Schorey C, McLachlan KR, Krag SS et al (1994) Mammalian glycosyltransferases prefer glycosyl phosphoryl dolichols rather than glycosyl phosphoryl polyprenols as substrates for oligosaccharyl synthesis. Arch Biochem Biophys 308:497–503PubMedGoogle Scholar
  29. Emmerson JR, Gally DL, Roe AJ (2006) Generation of gene deletions and gene replacements in Escherichia coli O157:H7 using a temperature sensitive allelic exchange system. Biol Proced Online 8:153–162PubMedGoogle Scholar
  30. Erridge C, Bennett-Guerrero E, Poxton IR (2002) Structure and function of lipopolysaccharides. Microbes Infect 4:837–851PubMedGoogle Scholar
  31. Flebbe LM, Chapes SK, Morrison DC (1990) Activation of C3H/HeJ macrophage tumoricidal activity and cytokine release by R-chemotype lipopolysaccharide preparations. J Immunol 145:505–514Google Scholar
  32. Ftacek P, Skultety L, Toman R (2000) Phase variation of Coxiella burnetii strain Priscilla: influence of this phenomenon on biochemical features of its lipopolysaccharide. J Endotoxin Res 6:369–376PubMedGoogle Scholar
  33. Gajdosova E, Kovacova E, Toman R et al (1994) Immunogenicity of Coxiella burnetii whole cells and their outer membrane components. Acta Virol 38:339–344PubMedGoogle Scholar
  34. Girard R, Pedron T, Uematsu S et al (2003) Lipopolysaccharides from Legionella and Rhizobium stimulate mouse bone marrow granulocytes via toll-like receptor 2. J Cell Sci 116:293–302PubMedGoogle Scholar
  35. Golenbock DT, Hampton RY, Qureshi N et al (1991) Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J Biol Chem 266:19490–19498PubMedGoogle Scholar
  36. Gunn JS, Ernst RK (2007) The structure and function of Francisella lipopolysaccharide. Ann NY Acad Sci 1105:202–218PubMedGoogle Scholar
  37. Hackstadt T (1986) Antigenic variation in the phase I lipopolysaccharide of Coxiella burnetii isolates. Infect Immun 52:337–340PubMedGoogle Scholar
  38. Hackstadt T, Peacock MG, Hitchcock PJ et al (1985) Lipopolysaccharide variation in Coxiella burnetii: intrastrain heterogeneity in structure and antigenicity. Infect Immun 48:359–365PubMedGoogle Scholar
  39. Hajjar AM, O’Mahony DS, Ozinsky A et al (2001) Cutting edge: functional interactions between toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J Immunol 166:15–19PubMedGoogle Scholar
  40. Heinrichs DE, Whitfield C, Valvano MA (1999) Biosynthesis and genetics of lipopolysaccharide core. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York/Basel, pp 305–330Google Scholar
  41. Heinzen RA, Hackstadt T (1996) A developmental stage-specific histone H1 homolog of Coxiella burnetii. J Bacteriol 178:5049–5052PubMedGoogle Scholar
  42. Helbig JH, Luck PC, Knirel YA et al (1995) Molecular characterization of a virulence-associated epitope on the lipopolysaccharide of Legionella pneumophila serogroup 1. Epidemiol Infect 115:71–78PubMedGoogle Scholar
  43. Hirschfeld M, Weiss JJ, Toshchakov V et al (2001) Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect Immun 69:1477–1482PubMedGoogle Scholar
  44. Hobbs M, Reeves PR (1994) The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Mol Microbiol 12:855–856PubMedGoogle Scholar
  45. Hollenstein K, Dawson RJ, Locher KP (2007) Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17:412–418PubMedGoogle Scholar
  46. Holst O (1999) Chemical structure of the core region of lipopolysaccharides. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York/Basel, pp 115–154Google Scholar
  47. Honstettre A, Ghigo E, Moynnault A et al (2004) Lipopolysaccharide from Coxiella burnetii is involved in bacterial phagocytosis, filamentous actin reorganization, and inflammatory responses through toll-like receptor 4. J Immunol 172:3695–3703PubMedGoogle Scholar
  48. Hoover TA, Culp DW, Vodkin MH et al (2002) Chromosomal DNA deletions explain phenotypic characteristics of two antigenic variants, phase II and RSA 514 (Crazy), of the Coxiella burnetii nine mile strain. Infect Immun 70:6726–6733PubMedGoogle Scholar
  49. Hussein A, Kovacova E, Toman R (2001) Isolation and evaluation of Coxiella burnetii O-polysaccharide antigen as immunodiagnostic reagent. Acta Virol 45:173–180PubMedGoogle Scholar
  50. Jimenez de Bagues MP, Gross A, Terraza A et al (2005) Cellular bioterrorism: how Brucella corrupts macrophage physiology to promote invasion and proliferation. Clin Immunol 114:227–238PubMedGoogle Scholar
  51. Joiner KA (1988) Complement evasion by bacteria and parasites. Ann Rev Microbiol 42:201–230Google Scholar
  52. Kawai T, Akira S (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann NY Acad Sci 1143:1–20PubMedGoogle Scholar
  53. Kean EL, Rush JS, Waechter CJ (1994) Activation of GlcNAc-P-P-dolichol synthesis by mannosylphosphoryldolichol is stereospecific and requires a saturated alpha-isoprene unit. Biochemistry 33:10508–10512PubMedGoogle Scholar
  54. Keenleyside WJ, Whitfield C (1999) Genetics and biosynthesis of lipopolysaccharide O-antigens. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York/Basel, pp 331–358Google Scholar
  55. King JD, Kocincova D, Westman EL et al (2009) Review: lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Innate Immun 15:261–312PubMedGoogle Scholar
  56. Knirel YA, Rietschel ET, Marre R et al (1994) The structure of the O-specific chain of Legionella pneumophila serogroup 1 lipopolysaccharide. Eur J Biochem 221:239–245PubMedGoogle Scholar
  57. Kubes M, Kuzmova Z, Gajdosova E et al (2006) Induction of tumor necrosis factor alpha in murine macrophages with various strains of Coxiella burnetii and their lipopolysaccharides. Acta Virol 50:93–99PubMedGoogle Scholar
  58. Lien E, Sellati TJ, Yoshimura A et al (1999) Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J Biol Chem 274:33419–33425PubMedGoogle Scholar
  59. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501PubMedGoogle Scholar
  60. Lorenz E, Mira JP, Cornish KL et al (2000) A novel polymorphism in the toll-like receptor 2 gene and its potential association with staphylococcal infection. Infect Immun 68:6398–6401PubMedGoogle Scholar
  61. Lu YC, Yeh WC, Ohashi PS (2008) LPS/TLR4 signal transduction pathway. Cytokine 42:145–151PubMedGoogle Scholar
  62. Luck PC, Freier T, Steudel C et al (2001) Point mutation in the active site of Legionella pneumophila O-acetyltransferase results in modified lipopolysaccharide but does not influence virulence. Int J Med Microbiol 291:345–352PubMedGoogle Scholar
  63. Luneberg E, Zahringer U, Knirel YA et al (1998) Phase-variable expression of lipopolysaccharide contributes to the virulence of Legionella pneumophila. J Exp Med 188:49–60PubMedGoogle Scholar
  64. Luneberg E, Zetzmann N, Alber D et al (2000) Cloning and functional characterization of a 30 kb gene locus required for lipopolysaccharide biosynthesis in Legionella pneumophila. Int J Med Microbiol 290:37–49PubMedGoogle Scholar
  65. Luneberg E, Mayer B, Daryab N et al (2001) Chromosomal insertion and excision of a 30 kb unstable genetic element is responsible for phase variation of lipopolysaccharide and other virulence determinants in Legionella pneumophila. Mol Microbiol 39:1259–1271PubMedGoogle Scholar
  66. Malley R, Hennecke P, Morse SC et al (2003) Recognition of pneumolysin by toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci USA 100:1966–1971PubMedGoogle Scholar
  67. Marrie TJ, Raoult D (1997) Q fever – a review and issues for the next century. J Antimicrob Agents 8:145–161Google Scholar
  68. Mayer H, Radziejewska-Lebrecht J, Schramek S (1988) Chemical and immunochemical studies on lipopolysaccharides of Coxiella burnetii phase I and phase II. Adv Exp Med Biol 228:577–591PubMedGoogle Scholar
  69. McCaul TF, Banerjee-Bhatnagar N, Williams JC (1991) Antigenic differences between Coxiella burnetii cells revealed by postembedding immunoelectron microscopy and immunoblotting. Infect Immun 59:3243–3253PubMedGoogle Scholar
  70. McLachlan KR, Krag SS (1994) Three enzymes involved in oligosaccharide-lipid assembly in Chinese hamster ovary cells differ in lipid substrate preference. J Lipid Res 35:1861–1868PubMedGoogle Scholar
  71. Meghari S, Honstettre A, Lepidi H et al (2005) TLR2 is necessary to inflammatory response in Coxiella burnetii infection. Ann NY Acad Sci 1063:161–166PubMedGoogle Scholar
  72. Moran AP, Zähringer U, Seydel U et al (1991) Structural analysis of the lipid A component of Campylobacter jejuni CCUG 10936 (serotype O:2) lipopolysaccharide. Description of a lipid A containing a hybrid backbone of 2-amino-2-deoxy-D-glucose and 2,3-diamino-2,3-dideoxy-D-glucose. Eur J Biochem 198:459–469PubMedGoogle Scholar
  73. Nagy G, Palkovics T, Otto A et al (2008) “Gently rough”: the vaccine potential of a Salmonella enterica regulatory lipopolysaccharide mutant. J Infect Dis 198:1699–1706PubMedGoogle Scholar
  74. Narasaki CT, Mertens K, Samuel JE (2011) Characterization of the GDP-D-mannose biosynthesis pathway in Coxiella burnetii: the initial steps for GDP-β-D-virenose biosynthesis. PLoS One 6(10):e25514PubMedGoogle Scholar
  75. Nelson K, Selander RK (1994) Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria. Proc Natl Acad Sci USA 91:10227–10231PubMedGoogle Scholar
  76. Nesper J, Lauriano CM, Klose KE et al (2001) Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect Immun 69:435–445PubMedGoogle Scholar
  77. O’Neill LA (2006) How toll-like receptors signal: what we know and what we don’t know. Curr Opin Immunol 18:3–9PubMedGoogle Scholar
  78. Palkovicova K, Ihnatko R, Vadovic P et al (2009) A monoclonal antibody specific for a unique biomarker virenose in a lipopolysaccharide of Coxiella burnetii. Clin Microbiol Infect 15:183–184PubMedGoogle Scholar
  79. Pretat L, Toman R, Vadovic P et al (2009) Intracellular trafficking of the Coxiella burnetii lipopolysaccharide. Clin Microbiol Infect 15:185–187PubMedGoogle Scholar
  80. Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Ann Rev Biochem 71:635–700PubMedGoogle Scholar
  81. Reeves PR, Hobbs M, Valvano MA et al (1996) Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol 4:495–503PubMedGoogle Scholar
  82. Rietschel ET, Brade H, Brade L et al (1987) Lipid A, the endotoxic centre of bacterial lipopolysaccharides: relation of chemical structure to biological activity. Prog Clin Biol Res 231:25–53PubMedGoogle Scholar
  83. Rietschel ET, Kirikae T, Schade U et al (1993) The chemical structure of bacterial endotoxin in relation to bioactivity. Immunobiology 187:169–190PubMedGoogle Scholar
  84. Rocchetta HL, Burrows LL, Lam JS (1999) Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 63:523–553PubMedGoogle Scholar
  85. Rojas G, Saldias S, Bittner M et al (2001) The rfaH gene, which affects lipopolysaccharide synthesis in Salmonella enterica serovar Typhi, is differentially expressed during the bacterial growth phase. FEMS Microbiol Lett 204:123–128PubMedGoogle Scholar
  86. Rush JS, Shelling JG, Zingg NS et al (1993) Mannosylphosphoryldolichol-mediated reactions in oligosaccharide-P-P-dolichol biosynthesis. Recognition of the saturated alpha-isoprene unit of the mannosyl donor by pig brain mannosyltransferases. J Biol Chem 268:13110–13117PubMedGoogle Scholar
  87. Rush JS, Rick PD, Waechter CJ (1997) Polyisoprenyl phosphate specificity of UDP-GlcNAc: undecaprenyl phosphate N-acetylglucosaminyl 1-P transferase from E.coli. Glycobiology 7:315–322PubMedGoogle Scholar
  88. Rush JS, Alaimo C, Robbiani R et al (2010) A novel epimerase that converts GlcNAc-P-P-undecaprenol to GalNAc-P-P-undecaprenol in Escherichia coli O157. J Biol Chem 285:1671–1680PubMedGoogle Scholar
  89. Samuel G, Reeves P (2003) Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res 338:2503–2519PubMedGoogle Scholar
  90. Sandlin RC, Lampel KA, Keasler SP et al (1995) Avirulence of rough mutants of Shigella flexneri: requirement of O antigen for correct unipolar localization of IcsA in the bacterial outer membrane. Infect Immun 63:229–237PubMedGoogle Scholar
  91. Sandlin RC, Goldberg MB, Maurelli AT (1996) Effect of O side-chain length and composition on the virulence of Shigella flexneri 2a. Mol Microbiol 22:63–73PubMedGoogle Scholar
  92. Schramek S, Mayer H (1982) Different sugar composition of lipopolysaccharides isolated from phase I and pure phase II cells of Coxiella burnetii. Infect Immun 38:53–57PubMedGoogle Scholar
  93. Schramek S, Radziejewska-Lebrecht J, Mayer H (1985) 3-C-branched aldoses in lipopolysaccharide of phase I Coxiella burnetii and their role as immunodominant factors. Eur J Biochem 148:445–461Google Scholar
  94. Seshadri R, Hendrix LR, Samuel JE (1999) Differential expression of translational elements by life cycle variants of Coxiella burnetii. Infect Immun 67:6026–6033PubMedGoogle Scholar
  95. Seshadri R, Paulsen IT, Eisen JA et al (2003) Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci USA 100:5455–5460PubMedGoogle Scholar
  96. Seydel U, Wiese A, Schromm AB et al (1999) A biophysical view on the function and activity of endotoxins. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York/Basel, pp 195–219Google Scholar
  97. Shannon JG, Howe D, Heinzen RA (2005) Virulent Coxiella burnetii does not activate human dendritic cells: role of lipopolysaccharide as a shielding molecule. Proc Natl Acad Sci USA 102:8722–8727PubMedGoogle Scholar
  98. Shimazu R, Akashi S, Ogata H et al (1999) MD-2, a molecule that confers lipopolysaccharide responsiveness on toll-like receptor 4. J Exp Med 189:1777–1782PubMedGoogle Scholar
  99. Skultety L, Toman R, Patoprsty V (1998) A comparative study of lipopolysaccharides from two Coxiella burnetii strains considered to be associated with acute and chronic Q fever. Carbohydr Polymers 35:189–194Google Scholar
  100. Skultety L, Hernychova L, Toman R et al (2005) Coxiella burnetii whole cell lysate protein identification by mass spectrometry and tandem mass spectrometry. Ann NY Acad Sci 1063:115–122PubMedGoogle Scholar
  101. Skurnik M, Toivanen P (1993) Yersinia enterocolitica lipopolysaccharide: genetics and virulence. Trends Microbiol 1:148–152PubMedGoogle Scholar
  102. Slaba K, Hussein A, Palkovic P et al (2003) Studies on immunological role of virenose and dihydrohydroxystreptose present in the Coxiella burnetii phase I lipopolysaccharide. Ann NY Acad Sci 990:505–509PubMedGoogle Scholar
  103. Stoker MG, Fiset P (1956) Phase variation of the Nine Mile and other strains of Rickettsia burneti. Can J Microbiol 2:310–321PubMedGoogle Scholar
  104. Stroeher UH, Jedani KE, Manning PA (1998) Genetic organization of the regions associated with surface polysaccharide synthesis in Vibrio cholerae O1, O139 and Vibrio anguillarum O1 and O2: a review. Gene 223:269–282PubMedGoogle Scholar
  105. Svraka S, Toman R, Skultety L et al (2006) Establishment of a genotyping scheme for Coxiella burnetii. FEMS Microbiol Lett 254:268–274PubMedGoogle Scholar
  106. Szkopinska A, Swiezewska E, Chojnacki T (1992) On the specificity of dolichol kinase and DolPMan synthase towards isoprenoid alcohols of different chain length in rat liver micro-somal membrane. Int J Biochem 24:1151–1157PubMedGoogle Scholar
  107. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14PubMedGoogle Scholar
  108. Thompson HA, Hoover TA, Vodkin MH et al (2003) Do chromosomal deletions in the lipopolysaccharide biosynthetic regions explain all cases of phase variation in Coxiella burnetii strains? An update. Ann NY Acad Sci 990:664–670PubMedGoogle Scholar
  109. Toman R (1991) Basic structural features of a lipopolysaccharide from the Coxiella burnetii strain Nine Mile in the virulent phase I. Acta Virol 35:224Google Scholar
  110. Toman R, Kazar J (1991) Evidence for the structural heterogeneity of the polysaccharide component of Coxiella burnetii strain Nine Mile lipopolysaccharide. Acta Virol 35:531–537PubMedGoogle Scholar
  111. Toman R, Skultety L (1994) Analysis of the 3-deoxy-D-manno-2-octulosonic acid region in a lipopolysaccharide isolated from Coxiella burnetii strain Nine Mile in phase II. Acta Virol 38:241–243PubMedGoogle Scholar
  112. Toman R, Skultety L (1996) Structural study on a lipopolysaccharide from Coxiella burnetii strain Nine Mile in avirulent phase II. Carbohydr Res 283:175–185PubMedGoogle Scholar
  113. Toman R, Skultety L, Kazar J (1993) On the determination of “Kdo-like substance” in the lipopolysaccharide from Coxiella burnetii strain Nine Mile in phase II. Acta Virol 37:196–198PubMedGoogle Scholar
  114. Toman R, Skultety L, Ftacek P et al (1998) NMR study of virenose and dihydrohydroxystreptose isolated from Coxiella burnetii phase I lipopolysaccharide. Carbohydr Res 306:291–296PubMedGoogle Scholar
  115. Toman R, Hussein A, Palkovic P et al (2003a) Structural properties of lipopolysaccharides from Coxiella burnetii strains Henzerling and S. Ann NY Acad Sci 990:563–567PubMedGoogle Scholar
  116. Toman R, Hussein A, Slaba K et al (2003b) Further structural characteristics of the lipopolysaccharide from Coxiella burnetii strain Nine Mile in low virulent phase II. Acta Virol 47:129–130PubMedGoogle Scholar
  117. Toman R, Garidel P, Andra J et al (2004) Physicochemical characterization of the endotoxins from Coxiella burnetii strain Priscilla in relation to their bioactivities. BMC Biochem 5:1 Google Scholar
  118. Toman R, Skultety L, Ihnatko R (2009) Coxiella burnetii glycomics and proteomics – tools for linking structure to function. Ann NY Acad Sci 1166:67–78PubMedGoogle Scholar
  119. Trefzer A, Salas JA, Bechthold A (1999) Genes and enzymes involved in deoxysugar biosynthesis in bacteria. Nat Prod Rep 16:283–299PubMedGoogle Scholar
  120. Tujulin E, Lilliehook B, Macellaro A et al (1999) Early cytokine induction in mouse P388D1 macrophages infected by Coxiella burnetii. Vet Immunol Immunopathol 68:159–168PubMedGoogle Scholar
  121. Ulmer AJ, Heine H, Feist W et al (1992) Biological activity of synthetic phosphono-oxyethyl analogues of lipid A and lipid A partial structures. Infect Immun 60:3309–3314PubMedGoogle Scholar
  122. Vadovic P, Slaba K, Fodorova M et al (2005) Structural and functional characterization of the glycan antigens involved in immunobiology of Q fever. Ann NY Acad Sci 1063:149–153PubMedGoogle Scholar
  123. Vadovic P, Fodorova M, Toman R (2007) Structural studies of lipid A of Piscirickettisa salmonis, the etiological agent of the salmonid rickettsial septicemia. Acta Virol 51:249–259PubMedGoogle Scholar
  124. Vadovic P, Fuleova A, Ihnatko R et al (2009) Structural studies of lipid A from a lipopolysaccharide of the Coxiella burnetii isolate RSA 514 (Crazy). Clin Microbiol Infect 15:198–199PubMedGoogle Scholar
  125. Van den Bosch L, Manning PA, Morona R (1997) Regulation of O-antigen chain length is required for Shigella flexneri virulence. Mol Microbiol 23:765–775PubMedGoogle Scholar
  126. Van der Woude MW, Baumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17:581–611PubMedGoogle Scholar
  127. Vishwanath S, Hackstadt T (1988) Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii. Infect Immun 56:40–44PubMedGoogle Scholar
  128. Vodkin MH, Williams JC (1986) Overlapping deletion in two spontaneous phase variants of Coxiella burnetii. J Gen Microbiol 132:2587–2594PubMedGoogle Scholar
  129. Wang L, Jensen S, Hallman R et al (1998) Expression of the O antigen gene cluster is regulated by RfaH through the JUMPstart sequence. FEMS Microbiol Lett 165:201–206PubMedGoogle Scholar
  130. Weiser JN, Love JM, Moxon ER (1989) The molecular mechanism of phase variation of Haemophilus influenzae lipopolysaccharide. Cell 59:657–665PubMedGoogle Scholar
  131. Weisman LS, Ballou CE (1984) Biosynthesis of the mycobacterial methylmannose polysaccharide. Identification of a 3-O-methyltransferase. J Biol Chem 259:3464–3469PubMedGoogle Scholar
  132. Weiss J, Hutzler M, Kao L (1986) Environmental modulation of lipopolysaccharide chain length alters the sensitivity of Escherichia coli to the neutrophil bactericidal/permeability-increasing protein. Infect Immun 51:594–599PubMedGoogle Scholar
  133. Williams JC, Waag DM (1991) Antigens, virulence factors, and biological response modifiers of Coxiella burnetii: strategies for vaccine development. In: Williams JC, Thompson HA (eds) Q fever: the biology of Coxiella burnetii. CRC Press, Boca Raton, pp 175–222Google Scholar
  134. Wollenweber HW, Schramek S, Moll H et al (1985) Nature and linkage of fatty acids present in lipopolysaccharides of phase I and phase II Coxiella burnetii. Arch Microbiol 142:6–11PubMedGoogle Scholar
  135. Zamboni DS, Campos MA, Torrecilhas ACT et al (2004) Stimulation of toll-like receptor 2 by Coxiella burnetii is required for macrophage production of pro-inflammatory cytokines and resistance to infection. J Biol Chem 279:54405–54415PubMedGoogle Scholar
  136. Zhang G, Russell-Lodrigue KE, Andoh M et al (2007) Mechanisms of vaccine-induced protective immunity against Coxiella burnetii infection in BALB/c mice. J Immunol 179:8372–8380PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Center Department of Microbial and Molecular PathogenesisTexas A&M University Health ScienceCollege StationUSA
  2. 2.Laboratory for Diagnosis and Prevention of Rickettsial and Chlamydial InfectionsInstitute of Virology, Slovak Academy of SciencesBratislavaSlovakia

Personalised recommendations