Phylogenetic Diversity, Virulence and Comparative Genomics

Chapter
Part of the Advances in Experimental Medicine and Biology book series (volume 984)

Abstract

Coxiella burnetii, the causative agent of Q fever, has remained a public health concern since the identification of this organism in 1935 by E. H. Derrick in Australia and at the Rocky Mountain Laboratory in the USA by H.R. Cox and G. Davis. Human Q fever has been described in most countries where C. burnetii is ubiquitous in the environment except in New Zealand where no cases have been described. Most human infections are acquired through inhalation of contaminated aerosols that can lead to acute self-limiting febrile illness or more severe chronic cases of hepatitis or endocarditis. It is estimated that the actual incidence of human infection is under-reported as a result of imprecise tools for differential diagnosis. An intracellular lifestyle, low infectious dose, and ease of transmission have resulted in the classification of C. burnetii as a category B bio-warfare agent. The recent outbreaks in Europe are a reminder that there is much to learn about this unique intracellular pathogen, especially with the speculation of a hyper-virulent strain contributing to an outbreak in the Netherlands where over 4,000 human cases were reported. A new era in C. burnetii research has begun with the recent description of an axenic media making this an exciting time to study this bacterial pathogen.

Keywords

Coxiella burnetii Isolates Phylogeny Genomics Pathogenecity Virulence Virulence factors 

References

  1. Abu-Zant A, Jones S, Asare R, Suttles J, Price C, Graham J, Kwaik YA (2007) Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell Microbiol 9:246–264. %U http://dx.doi.org/10.1111/j.1462-5822.2006.00785.x Google Scholar
  2. Aguilera M, Salinas R, Rosales E, Carminati S, Colombo MI, Beron W (2009) Actin dynamics and Rho GTPases regulate the size and formation of parasitophorous vacuoles containing Coxiella burnetii. Infect Immun 77:4609–4620. %U http://iai.asm.org/cgi/content/abstract/77/10/4609 Google Scholar
  3. Akporiaye ET, Stefanovich D, Tsosie V, Baca G (1990) Coxiella burnetii fails to stimulate human neutrophil superoxide anion production. Acta Virol 34:64–70PubMedGoogle Scholar
  4. Al-Khodor S, Price CT, Kalia A, Abu Kwaik Y (2010) Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol 18:132–139. %U http://www.sciencedirect.com/science/article/B6TD0-4XVGGCC-2/2/9f35429b076db88abfd89cb482b24b77 Google Scholar
  5. Amano K, Williams JC, Missler SR, Reinhold VN (1987) Structure and biological relationships of Coxiella burnetii lipopolysaccharides. J Biol Chem 262:4740–4747PubMedGoogle Scholar
  6. Arricau-Bouvery N, Hauck Y, Bejaoui A, Frangoulidis D, Bodier CC, Souriau A, Meyer H, Neubauer H, Rodolakis A, Vergnaud G (2006) Molecular characterization of Coxiella burnetii isolates by infrequent restriction site-PCR and MLVA typing. BMC Microbiol 6:38PubMedCrossRefGoogle Scholar
  7. Ayers M, Howell PL, Burrows LL (2010) Architecture of the type II secretion and type IV pilus machineries. Future Microbiol 5:1203–1218PubMedCrossRefGoogle Scholar
  8. Baca OG, Klassen DA, Aragon AS (1993) Entry of Coxiella burnetti into host cells. Acta Virol 37:143–155PubMedGoogle Scholar
  9. Baker S, Hanage WP, Holt KE (2010) Navigating the future of bacterial molecular epidemiology. Curr Opin Microbiol 13:640–645. %U http://www.sciencedirect.com/science/article/B6VS2-511KRNF-1/2/3507c23bc681b509a4ffd1a78df53743 Google Scholar
  10. Bansal A (2005) Bioinformatics in microbial biotechnology – a mini review. Microb Cell Fact 4:19. %U http://www.microbialcellfactories.com/content/4/1/19
  11. Beare PA, Samuel JE, Howe D, Virtaneva K, Porcella SF, Heinzen RA (2006) Genetic diversity of the Q fever agent, Coxiella burnetii, assessed by microarray-based whole-genome comparisons. J Bacteriol 188:2309–2324PubMedCrossRefGoogle Scholar
  12. Beare PA, Unsworth N, Andoh M, Voth DE, Omsland A, Gilk SD, Williams KP, Sobral BW, Kupko JJ, Porcella SF, Samuel JE, Heinzen RA (2009) Comparative genomics reveal extensive transposon-mediated genomic plasticity and diversity among potential effector proteins within the genus Coxiella. Infect Immun 77:642–656. %U http://iai.asm.org/cgi/content/abstract/77/2/642 Google Scholar
  13. Beare P, Sandoz K, Omsland A, Rockey D, Heinzen R (2011) Advances in genetic manipulation of obligate intracellular bacterial pathogens. Front Microbiol 2:97PubMedGoogle Scholar
  14. Beron W, Gutierrez MG, Rabinovitch M, Colombo MI (2002) Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun 70:5816–5821. %U http://iai.asm.org/cgi/content/abstract/70/10/5816 Google Scholar
  15. Boyle EC, Finlay BB (2003) Bacterial pathogenesis: exploiting cellular adherence. Curr Opin Cell Biol 15:633–639. %U http://www.sciencedirect.com/science/article/B6VRW-495VP58-1/2/3044a9c7b18bdda19a8987ae516255e4 Google Scholar
  16. Brodsky FM, Lem L, Solache A, Bennett EM (1999) Human pathogen subversion of antigen presentation. Immunol Rev 168:199–215. %U http://dx.doi.org/10.1111/j.1600-065X.1999.tb01294.x Google Scholar
  17. Campoy EM, Zoppino FCM, Colombo MI (2010) The early secretory pathway contributes to the growth of the Coxiella-replicative niche. Infect Immun. doi: 10.1128/IAI.00688-10. %U http://iai.asm.org/cgi/content/abstract/IAI.00688-10v1
  18. Capo C, Lindberg FP, Meconi S, Zaffran Y, Tardei G, Brown EJ, Raoult D, Mege J-L (1999) Subversion of monocyte functions by Coxiella burnetii: impairment of the cross-talk between αvß3 integrin and CR3. J Immunol 163:6078–6085. %U http://jimmunol.org/content/163/11/6078.abstract Google Scholar
  19. Capo C, Moynault A, Collette Y, Olive D, Brown EJ, Raoult D, Mege J-L (2003) Coxiella burnetii avoids macrophage phagocytosis by interfering with spatial distribution of complement receptor 3. J Immunol 170:4217–4225. %U http://jimmunol.org/content/170/8/4217.abstract Google Scholar
  20. Carey KL, Newton HJ, Lührmann A, Roy CR (2011) The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication. PLoS Pathog 7:e1002056PubMedCrossRefGoogle Scholar
  21. Casadevall A (2008) Evolution of intracellular pathogens. Annu Rev Microbiol 62:19–33PubMedCrossRefGoogle Scholar
  22. Chakraborty S, Monfett M, Maier TM, Benach JL, Frank DW, Thanassi DG (2008) Type IV pili in Francisella tularensis: roles of pilF and pilT in fiber assembly, host cell adherence, and virulence. Infect Immun 76:2852–2861. %U http://iai.asm.org/cgi/content/abstract/76/7/2852 Google Scholar
  23. Chen C, Banga S, Mertens K, Weber MM, Gorbaslieva I, Tan Y, Luo Z-Q, Samuel JE (2010) Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii. Proc Natl Acad Sci USA 107:21755–21760. %U http://www.pnas.org/content/107/50/21755.abstract Google Scholar
  24. Chiang P, Burrows LL (2003) Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J Bacteriol 185:2374–2378. %U http://jb.asm.org/cgi/content/abstract/185/7/2374 Google Scholar
  25. Coleman SA, Fischer ER, Howe D, Mead DJ, Heinzen RA (2004) Temporal analysis of Coxiella burnetii morphological differentiation. J Bacteriol 186:7344–7352. %U http://jb.asm.org/cgi/content/abstract/186/21/7344 Google Scholar
  26. Coleman SA, Fischer ER, Cockrell DC, Voth DE, Howe D, Mead DJ, Samuel JE, Heinzen RA (2007) Proteome and antigen profiling of Coxiella burnetii developmental forms. Infect Immun 75:290–298. %U http://iai.asm.org/cgi/content/abstract/75/1/290 Google Scholar
  27. Dellacasagrande J, Ghigo E, Machergui-el S, Hammami Toman R, Raoult D, Capo C, Mege J-L (2000) Alpha vbeta 3 integrin and bacterial lipopolysaccharide are involved in Coxiella burnetii-stimulated production of tumor necrosis factor by human monocytes. Infect Immun 68:5673–5678. %U http://iai.asm.org/cgi/content/abstract/68/10/5673 Google Scholar
  28. Denison A, Thompson H, Massung R (2007) IS1111 insertion sequences of Coxiella burnetii: characterization and use for repetitive element PCR-based differentiation of Coxiella burnetii isolates. BMC Microbiol 7:91. %U http://www.biomedcentral.com/1471-2180/7/91
  29. Forsberg Å, Guina T (2007) Type II secretion and type IV pili of Francisella. Ann NY Acad Sci 1105:187–201. %U http://dx.doi.org/10.1196/annals.1409.016
  30. Gimenez DF (1964) Staining Rickettsiae in yolk-sac cultures. Stain Technol 39:135–140PubMedGoogle Scholar
  31. Glazunova O, Roux V, Freylikman O, Sekeyova Z, Fournous G, Tyczka J, Tokarevich N, Kovacava E, Marrie TJ, Raoult D (2005) Coxiella burnetii genotyping. Emerg Infect Dis 11:1211–1217PubMedGoogle Scholar
  32. Gutierrez MG, Vázquez CL, Munafó DB, Zoppino FCM, Berón W, Rabinovitch M, Colombo MI (2005) Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol 7:981–993. %U http://dx.doi.org/10.1111/j.1462-5822.2005.00527.x Google Scholar
  33. Hackstadt T (1983) Estimation of the cytoplasmic pH of Coxiella burnetii and effect of substrate oxidation on proton motive force. J Bacteriol 154:591–597. %U http://jb.asm.org/cgi/content/abstract/154/2/591
  34. Hackstadt T (1986) Antigenic variation in the phase I lipopolysaccharide of Coxiella burnetii isolates. Infect Immun 52:337–340. %U http://iai.asm.org/cgi/content/abstract/52/1/337
  35. Hackstadt T (1988) Steric hindrance of antibody binding to surface proteins of Coxiella burnetti by phase I lipopolysaccharide. Infect Immun 56: 802–807. %U http://iai.asm.org/cgi/content/abstract/56/4/802
  36. Hackstadt T, Williams JC (1981) Stability of the adenosine 5′-triphosphate pool in Coxiella burnetii: influence of pH and substrate. J Bacteriol 148:419–425. %U http://jb.asm.org/cgi/content/abstract/148/2/419 Google Scholar
  37. Hager AJ, Bolton DL, Pelletier MR, Brittnacher MJ, Gallagher LA, Kaul R, Skerrett SJ, Miller, SI, Guina T (2006) Type IV pili-mediated secretion modulates Francisella virulence. Mol Microbiol 62:227–237. %U http://dx.doi.org/10.1111/j.1365-2958.2006.05365.x Google Scholar
  38. Heinzen R, Stiegler GL, Whiting LL, Schmitt SA, Mallavia LP, Frazier ME (1990) Use of pulsed field gel electrophoresis to differentiate Coxiella burnetii Strainsa. Ann NY Acad Sci 590:504–513. %U http://dx.doi.org/10.1111/j.1749-6632.1990.tb42260.x
  39. Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T (1996) Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun 64:796–809. %U http://iai.asm.org/cgi/content/abstract/64/3/796
  40. Hendrix LR, Samuel JE, Mallavia LP (1991) Differentiation of Coxiella burnetii isolates by analysis of restriction-endonuclease-digested DNA separated by SDS-PAGE. J Gen Microbiol 137:269–276. %U http://mic.sgmjournals.org/cgi/content/abstract/137/2/269 Google Scholar
  41. Hill J, Samuel JE (2010) Coxiella burnetii acid phosphatase: inhibiting the release of reactive oxygen intermediates in polymorphonuclear leukocytes. Infect Immun. doi:10.1128/IAI.01011-10. %U http://iai.asm.org/cgi/content/abstract/IAI.01011-10v1
  42. Hodivala-Dilke KM, Mchugh KP, Tsakiris DA, Rayburn H, Crowley D, Ullman-Culleré M, Ross FP, Coller BS, Teitelbaum S, Hynes RO (1999) β3-integrin–deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 103:229–238. %U http://www.jci.org/articles/view/5487 Google Scholar
  43. Honstettre A, Ghigo E, Moynault A, Capo C, Toman R, Akira S, Takeuchi O, Lepidi H, Raoult D, Mege J-L (2004) Lipopolysaccharide from Coxiella burnetii is involved in bacterial phagocytosis, filamentous actin reorganization, and inflammatory responses through toll-like receptor 4. J Immun 172:3695–3703. %U http://www.jimmunol.org/content/172/6/3695.abstract Google Scholar
  44. Hoover TA, Culp DW, Vodkin MH, Williams JC, Thompson HA (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 70:6726–6733PubMedCrossRefGoogle Scholar
  45. Howe D, Heinzen RA (2006) Coxiella burnetii inhabits a cholesterol-rich vacuole and influences cellular cholesterol metabolism. Cell Microbiol 8:496–507PubMedCrossRefGoogle Scholar
  46. Howe D, Melnicáková J, Barák I, Heinzen RA (2003) Maturation of the Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication. Cell Microbiol 5:469–480. %U http://dx.doi.org/10.1046/j.1462-5822.2003.00293.x Google Scholar
  47. Howe D, Shannon JG, Winfree S, Dorward DW, Heinzen RA (2010) Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages. Infect Immun 78:3465–3474. %U http://iai.asm.org/cgi/content/abstract/78/8/3465
  48. Huijsmans CJJ, Schellekens JJA, Wever PC, Toman R, Savelkoul PHM, Janse I, Hermans MHA (2011) SNP-genotyping of a Coxiella burnetii outbreak in the Netherlands. Appl Environ Microbiol. doi:10.1128/AEM.02293-10. %U http://aem.asm.org/cgi/content/abstract/AEM.02293-10v1
  49. Jäger C, Willems H, Thiele D, Baljer G (1998) Molecular characterization of Coxiella burnetii isolates. Epidemiol Infect 120:157–164. %U http://www.jstor.org/stable/3864204 Google Scholar
  50. Jager C, Lautenschlager S, Willems H, Baljer G (2002) Coxiella burnetii plasmid types QpDG and QpH1 are closely related and likely identical. Vet Microbiol 89:161–166PubMedCrossRefGoogle Scholar
  51. Kinchen JM, Ravichandran KS (2008) Phagosome maturation: going through the acid test. Nat Rev Mol Cell Biol 9:781–795. %U http://dx.doi.org/10.1038/nrm2515 Google Scholar
  52. Luhrmann A, Roy CR (2007) Coxiella burnetii inhibits activation of host cell apoptosis through a mechanism that involves preventing Cytochrome c release from mitochondria. Infect Immun 75:5282–5289. %U http://iai.asm.org/cgi/content/abstract/75/11/5282 Google Scholar
  53. Lührmann A, Nogueira CV, Carey KL, Roy CR (2010) Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc Natl Acad Sci USA107:18997–19001. %U http://www.pnas.org/content/107/44/18997.abstract Google Scholar
  54. Marrie TJ (2010) Q fever pneumonia. Infect Dis Clin North Am 24:27–41. %U http://www.sciencedirect.com/science/article/B75J9-4YDSNYG-7/2/d375c369e8de324f6cf9fe0057dea99e
  55. Maurin M, Raoult D (1999) Q fever. Clin Microbiol Rev 12:518–553. %U http://cmr.asm.org/cgi/content/abstract/12/4/518 Google Scholar
  56. Mccaul TF, Williams JC (1981) Developmental cycle of Coxiella burnetii: structure and morphogenesis of vegetative and sporogenic differentiations. J Bacteriol 147:1063–1076. %U http://jb.asm.org/cgi/content/abstract/147/3/1063 Google Scholar
  57. Mccaul TF, Banerjee-Bhatnagar N, Williams JC (1991) Antigenic differences between Coxiella burnetii cells revealed by postembedding immunoelectron microscopy and immunoblotting. Infect Immun 59:3243–3253. %U http://iai.asm.org/cgi/content/abstract/59/9/3243 Google Scholar
  58. Meconi S, Capo C, Remacle-Bonnet M, Pommier G, Raoult D, Mege J-L (2001) Activation of protein tyrosine kinases by Coxiella burnetii: role in actin cytoskeleton reorganization and bacterial phagocytosis. Infect Immun 69:2520–2526. %U http://iai.asm.org/cgi/content/abstract/69/4/2520 Google Scholar
  59. Mertens K, Lantsheer L, Ennis DG, Samuel JE (2008) Constitutive SOS expression and damage-inducible addAB-mediated recombinational repair systems for Coxiella burnetii as potential adaptations for survival within macrophages. Mol Microbiol 69:1411–1426. %U http://dx.doi.org/10.1111/j.1365-2958.2008.06373.x
  60. Miller JD, Curns AT, Thompson HA (2004) A growth study of Coxiella burnetii Nine Mile phase I and phase II in fibroblasts. FEMS Immunol Med Microbiol 42:291–297PubMedCrossRefGoogle Scholar
  61. Mohapatra NP, Soni S, Rajaram MVS, Dang PM-C, Reilly TJ, El-Benna J, Clay CD, Schlesinger LS, Gunn JS (2010) Francisella acid phosphatases inactivate the NADPH oxidase in human phagocytes. J Immunol 184:5141–5150. %U http://jimmunol.org/content/184/9/5141.abstract Google Scholar
  62. Mollet C, Drancourt M, Raoult D (1998) Determination of Coxiella burnetii rpoB sequence and its use for phylogenetic analysis. Gene 207:97–103. %U http://www.sciencedirect.com/science/article/B6T39-3S1PY3W-F/2/db7d6374f04a8b7083a1c0c35617665f Google Scholar
  63. Moos A, Hackstadt T (1987) Comparative virulence of intra- and interstrain lipopolysaccharide variants of Coxiella burnetii in the guinea pig model. Infect Immun 55:1144–1150. %U http://iai.asm.org/cgi/content/abstract/55/5/1144
  64. Nguyen SV, Hirai K (1999) Differentiation of Coxiella burnetii isolates by sequence determination and PCR-restriction fragment length polymorphism analysis of isocitrate dehydrogenase gene. FEMS Microbiol Lett 180:249–254. %U http://www.sciencedirect.com/science/article/B6T2W-3XT6BRP-M/2/a24324a06b91710f585b988e1b67adc9
  65. Omsland A, Cockrell DC, Fischer ER, Heinzen RA (2008) Sustained axenic metabolic activity by the obligate intracellular bacterium Coxiella burnetii. J Bacteriol 190:3203–3212. %U http://jb.asm.org/cgi/content/abstract/190/9/3203 Google Scholar
  66. Omsland A, Cockrell DC, Howe D, Fischer ER, Virtaneva K, Sturdevant DE, Porcella SF, Heinzen RA (2009) Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc Natl Acad Sci USA 106:4430–4434. %U http://www.pnas.org/content/106/11/4430.abstract
  67. Omsland A, Beare PA, Hill J, Cockrell DC, Howe D, Hansen B, Samuel JE, Heinzen RA (2011a). Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl Environ Microbiol 77:3720–3725. %U http://aem.asm.org/cgi/content/abstract/77/11/3720
  68. Omsland A, Beare PA, Hill J, Cockrell DC, Howe D, Hansen B, Samuel JE, Heinzen RA (2011b) Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl Environ Microbiol 77:3720–3725PubMedCrossRefGoogle Scholar
  69. Ormsbee RA, Peacock MG (1964) Metabolic activity in Coxiella burnetii. J Bacteriol 88:1205–1210. %U http://jb.asm.org/cgi/content/abstract/88/5/1205 Google Scholar
  70. Peacock MG, Philip RN, Williams JC, Faulkner RS (1983) Serological evaluation of O fever in humans: enhanced phase I titers of immunoglobulins G and A are diagnostic for Q fever endocarditis. Infect Immun 41:1089–1098.%U http://iai.asm.org/cgi/content/abstract/41/3/1089
  71. Raghavan R, Hicks LD, Minnick, MF (2008) Toxic introns and parasitic intein in Coxiella burnetii: legacies of a promiscuous past. J Bacteriol 190:5934–5943. %U http://jb.asm.org/cgi/content/abstract/190/17/5934 Google Scholar
  72. Rohmer L, Fong C, Abmayr S, Wasnick M, Larson Freeman T, Radey M, Guina T, Svensson K, Hayden H, Jacobs, M, Gallagher L, Manoil C, Ernst R, Drees B, Buckley D, Haugen E, Bovee D, Zhou Y, Chang J, Levy R, Lim R, Gillett W, Guenthener D, Kang A, Shaffer S, Taylor G, Chen J, Gallis B, D’argenio D, Forsman M, Olson M, Goodlett D, Kaul R, Miller S, Brittnacher M (2007) Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains Genome Biol 8:R102. %U http://genomebiology.com/2007/8/6/R102
  73. Romano PS, Gutierrez MG, Berón W, Rabinovitch M, Colombo MI (2007) The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol 9:891–909. %U http://dx.doi.org/10.1111/j.1462-5822.2006.00838.x Google Scholar
  74. Roux V, Bergoin M, Lamaze N, Raoult D (1997) Reassessment of the taxonomic position of Rickettsiella grylli. Int J Sys Bacteriol 47:1255–1257. %U http://ijs.sgmjournals.org/cgi/content/abstract/47/4/1255 Google Scholar
  75. Russell-Lodrigue KE, Andoh M, Poels MWJ, Shive HR, Weeks BR, Zhang GQ, Tersteeg C, Masegi T, Hotta A, Yamaguchi T, Fukushi H, Hirai K, Mcmurray DN, Samuel JE (2009) Coxiella burnetii isolates cause genogroup-specific virulence in mouse and guinea pig models of acute Q fever. Infect Immun 77:5640–5650. %U http://iai.asm.org/cgi/content/abstract/77/12/5640 Google Scholar
  76. Samuel JE, Frazier ME, Mallavia LP (1985) Correlation of plasmid type and disease caused by Coxiella burnetii. Infect Immun 49:775–779. %U http://iai.asm.org/cgi/content/abstract/49/3/775
  77. Savinelli EA, Mallavia LP (1990) Comparison of Coxiella burnetii plasmids to homologous chromosomal sequences present in a plasmidless endocarditis-causing isolate. Ann NY Acad Sci 590:523–533PubMedCrossRefGoogle Scholar
  78. Schromm A, Brandenburg K, Loppnow H, Moran AP, Koch MHJ, Rietschel E, Seydel U (2000) Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem 267:2008–2013PubMedCrossRefGoogle Scholar
  79. Sekeyová Z, Roux V, Raoult D (1999) Intraspecies diversity of Coxiella burnetii as revealed by com1 and mucZ sequence comparison. FEMS Microbiol Lett 180:61–67PubMedCrossRefGoogle Scholar
  80. Seshadri R, Samuel J (2005) Genome analysis of Coxiella burnetii species: insights into pathogenesis and evolution and implications for biodefense. Ann NY Acad Sci 1063:442–450. %U http://dx.doi.org/10.1196/annals.1355.063 Google Scholar
  81. Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, Nelson WC, Ward NL, Tettelin H, Davidsen TM, Beanan MJ, Deboy RT, Daugherty SC, Brinkac LM, Madupu R, Dodson RJ, Khouri HM, Lee KH, Carty HA, Scanlan D, Heinzen RA, Thompson HA, Samuel JE, Fraser CM, Heidelberg JF (2003) Complete genome sequence of the Q-fever pathogen Coxiella burnetii. ProcNatl Acad Sci USA 100:5455–5460. %U http://www.pnas.org/content/100/9/5455.abstract
  82. 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 102:8722–8727. %U http://www.pnas.org/content/102/24/8722.abstract Google Scholar
  83. Siemsen DW, Kirpotina LN, Jutila MA, Quinn MT (2009) Inhibition of the human neutrophil NADPH oxidase by Coxiella burnetii. Microbes Infect 11:671–679PubMedCrossRefGoogle Scholar
  84. 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 Polym 35:189–194CrossRefGoogle Scholar
  85. Stein A, Saunders NA, Taylor AG, Raoult D (1993) Phylogenic homogeneity of Coxiella burnetii strains as determinated by 16S ribosomal RNA sequencing. FEMS Microbiol Lett 113:339–344. %U http://www.sciencedirect.com/science/article/B6T2W-476HN4R-15/2/5f67777b44bc4d8ddfc89c8a15f7ad10
  86. Svraka S, Toman R, Skultety L, Slaba K, Homan WL (2006) Establishment of a genotyping scheme for Coxiella burnetii. FEMS Microbiol Lett 254:268–274. %U http://dx.doi.org/10.1111/j.1574-6968.2005.00036.x
  87. Thiele D, Willems H (1994) Is plasmid based differentiation of Coxiella burnetii in ‘Acute’ and ‘Chronic’ isolates still valid? Eur J Epidemiol 10:427–434. %U http://www.jstor.org/stable/3520970 Google Scholar
  88. Thompson HA, Hoover TA, Vodkin MH, Shaw EI (2003) Do chromosomal deletions in the lipopolysaccharide biosynthetic regions explain all cases of phase variation in Coxiella burnetii strains? Ann NY Acad Sci 990:664–670. %U http://dx.doi.org/10.1111/j.1749-6632.2003.tb07441.x
  89. 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
  90. Tujulin E, Lilliehöök B, Macellaro A, Sjöstedt A, Norlander L (1999) Early cytokine induction in mouse P388D1 macrophages infected by Coxiella burnetii. Vet Immunol Immunopathol 68:159–168. %U http://www.sciencedirect.com/science/article/pii/S0165242799000239
  91. Vazquez CL, Colombo MI (2009) Coxiella burnetii modulates Beclin 1 and Bcl-2, preventing host cell apoptosis to generate a persistent bacterial infection. Cell Death Differ 17:421–438. %U http://dx.doi.org/10.1038/cdd.2009.129
  92. Vishwanath S, Hackstadt T (1988) Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii. Infect Immun 56:40–44. %U http://iai.asm.org/cgi/content/abstract/56/1/40
  93. Vodkin MH, Williams JC, Stephenson EH (1986) Genetic heterogeneity among isolates of Coxiella burnetii. J Gen Microbiol 132:455–463PubMedGoogle Scholar
  94. Voth DE, Heinzen RA (2007) Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9:829–840. %U http://dx.doi.org/10.1111/j.1462-5822.2007.00901.x Google Scholar
  95. Voth DE, Heinzen RA (2009) Sustained activation of Akt and Erk1/2 is required for Coxiella burnetii antiapoptotic activity. Infect Immun 77:205–213. %U http://iai.asm.org/cgi/content/abstract/77/1/205
  96. Voth DE, Howe D, Beare PA, Vogel JP, Unsworth N, Samuel JE, Heinzen RA (2009) The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot/Icm-mediated secretion. J Bacteriol 191:4232–4242. %U http://jb.asm.org/cgi/content/abstract/191/13/4232 Google Scholar
  97. Weisburg WG, Dobson ME, Samuel JE, Dasch GA, Mallavia LP, Baca O, Mandelco L, Sechrest JE, Weiss E, Woese CR (1989) Phylogenetic diversity of the Rickettsiae. J Bacteriol 171:4202–4206. %U http://jb.asm.org/cgi/content/abstract/171/8/4202 Google Scholar
  98. Willems H, Ritter M, Jager C, Thiele D (1997) Plasmid-homologous sequences in the chromosome of plasmidless Coxiella burnetii Scurry Q217. J Bacteriol 179:3293–3297PubMedGoogle Scholar
  99. Williams JC (1991) Infectivity, virulence, and pathogenicity of Coxiella burnetti for various hosts. In: Williams JC, Thompson HA (eds) Q fever: the biology of Coxiella burnetii. CRC Press, Boca RatonGoogle Scholar
  100. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng T-I, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129–1132. %U http://www.sciencemag.org/content/275/5303/1129.abstract Google Scholar
  101. Zamboni DS, Mortara RA, Freymuller E, Rabinovitch M (2002) Mouse resident peritoneal macrophages partially control in vitro infection with Coxiella burnetii phase II. Microbes Infect 4:591–598. %U http://www.sciencedirect.com/science/article/B6VPN-45JPMBJ-2/2/e343d26d0e629d99e221099e0e20e1f8
  102. Zamboni DS, Mcgrath S, Rabinovitch M, Roy CR (2003) Coxiella burnetii express type IV secretion system proteins that function similarly to components of the Legionella pneumophila Dot/Icm system. Mol Microbiol 49:965–976. %U http://dx.doi.org/10.1046/j.1365-2958.2003.03626.x
  103. Zamboni DS, Campos MA, Torrecilhas ACT, Kiss K, Samuel JE, Golenbock DT, Lauw FN, Roy CR, Almeida IC, Gazzinelli RT (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 279:54405–54415. %U http://www.jbc.org/content/279/52/54405.abstract Google Scholar
  104. Zhang GQ, To H, Yamaguchi T, Fukushi H, Hirai K (1997) Differentiation of Coxiella burnetii by sequence analysis of the gene (com1) encoding a 27-kDa outer membrane protein. Microbiol Immunol 41:871–877PubMedGoogle Scholar
  105. Zogaj X, Chakraborty S, Liu J, Thanassi D G, Klose KE (2008) Characterization of the Francisella tularensis subsp. novicida type IV pilus. Microbiology 154:2139–2150. %U http://mic.sgmjournals.org/cgi/content/abstract/154/7/2139 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Department of Microbial and Molecular Pathogenesis, College of MedicineTexas A&M Health Science CenterBryanUSA

Personalised recommendations