Novel microbial virulence factor triggers murine lyme arthritis

Journal of Infectious Diseases

Volumn 207, Issue 6, 2013, Pages 907-918

  Yang, Xiuli ^a   Qin, Jinhong ^a   Promnares, Kamoltip ^a   Kariu, Toru ^a   Anderson, John F ^b   Pal, Utpal ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b Northeast Regional Center for Excellence in Vector Borne Diseases   (United States)

Author keywords

Borrelia burgdorferi; inflammation; Lyme disease; virulence

Indexed keywords

BACTERIAL PROTEIN; BBA57 PROTEIN; CHEMOKINE; CHEMOKINE RECEPTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BBA57 GENE; BORRELIA BURGDORFERI; DISEASE TRANSMISSION; IN VIVO STUDY; LYME DISEASE; MEMBRANE VESICLE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; UPREGULATION; WILD TYPE;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; DOUBLE-BLIND METHOD; GENES, BACTERIAL; JOINTS; LIPOPROTEINS; LYME DISEASE; MICE; MICE, INBRED C3H; MYOCARDIUM; NEUTROPHILS; RECEPTORS, CHEMOKINE; SEQUENCE DELETION; UP-REGULATION; VIRULENCE FACTORS;

EID: 84874286509     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jis930     Document Type: Article

References (50)

1. Piesman J, Eisen L. Prevention of tick-borne Diseases. Annu Rev Entomol 2008; 53:323-43.
2. Barthold SW, DeSouza M, Fikrig E, Persing DH. Lyme borreliosis in the laboratory mouse. In: Schuster SE, ed. Lyme disease. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1992:223-42.
3. Steere AC, Coburn J, Glickstein L. The emergence of Lyme disease. J Clin Invest 2004; 113:1093-101.
4. Steere AC, Glickstein L. Elucidation of Lyme arthritis. Nat Rev Immunol 2004; 4:143-52.
5. Barthold SW, Diego C, Philipp MT. Animal models of borreliosis. In: Samuels DS, Radolf JD, eds. Borrelia, molecular biology, host interaction and pathogenesis. Norfolk, UK: Caister Academic Press, 2010:353-405.
6. Buckland J. Lyme arthritis: Direct and indirect actions of Borrelia burgdorferi. Nat Rev Rheumatol 2010; 6:615.
7. Brown CR, Blaho VA, Loiacono CM. Treatment of mice with the neutrophil-depleting antibody RB6-8C5 results in early development of experimental Lyme arthritis via the recruitment of Gr-1-polymorphonuclear leukocyte-like cells. Infect Immun 2004; 72:4956-65.
8. Ritzman AM, Hughes-Hanks JM, Blaho VA, Wax LE, Mitchell WJ, Brown CR. The chemokine receptor CXCR2 ligand KC (CXCL1) mediates neutrophil recruitment and is critical for development of experimental Lyme arthritis and carditis. Infect Immun 2010; 78:4593-600.
9. Weis JJ, Bockenstedt LK. Host response. In: Samuels DS, Radolf JD, eds. Borrelia, molecular biology, host interaction and pathogenesis. Norfolk, UK: Caister Academic Press, 2010:413-41.
10. Xu Q, Seemanapalli SV, Reif KE, Brown CR, Liang FT. Increasing the recruitment of neutrophils to the site of infection dramatically attenuates Borrelia burgdorferi infectivity. J Immunol 2007; 178:5109-15.
11. Brown CR, Blaho VA, Loiacono CM. Susceptibility to experimental Lyme arthritis correlates with KC and monocyte chemoattractant protein-1 production in joints and requires neutrophil recruitment via CXCR2. J Immunol 2003; 171:893-901.
12. Armstrong A, Barthold SW, Persing D, Beck D. Carditis in Lyme disease susceptible and resistant strains of laboratory mice infected with Borrelia burgdorferi. Am J Trop Med Hyg 1992; 47:249-58.
13. Bateman H, Sigal L. Update on Lyme carditis. Curr Infect Dis Rep 2000; 2:299-301.
14. Grzesik P, Oczko-Grzesik B, Kepa L. Cardiac manifestations of Lyme borreliosis. Przegl Epidemiol 2004; 58:589-96.
15. Haddad FA, Nadelman RB. Lyme disease and the heart. Front Biosci 2003; 8:s769-82.
16. McAlister HF, Klementowicz PT, Andrews C, Fisher JD, Feld M, Furman S. Lyme carditis: an important cause of reversible heart block. Ann Int Med 1989; 110:339-45.
17. Montgomery RR, Booth CJ, Wang X, Blaho VA, Malawista SE, Brown CR. Recruitment of macrophages and polymorphonuclear leukocytes in Lyme carditis. Infect Immun 2007; 75:613-20.
18. Ruderman EM, Kerr JS, Telford SR, Spielman A, Glimcher LH, Gravallese EM. Early murine Lyme carditis has a macrophage predominance and is independent of major histocompatibility complex class II-CD4+ T cell interactions. J Infect Dis 1995; 171:362-70.
19. Strle K, Drouin EE, Shen S, et al. Borrelia burgdorferi stimulates macrophages to secrete higher levels of cytokines and chemokines than Borrelia afzelii or Borrelia garinii. J Infect Dis 2009; 200:1936-43.
20. Yang X, Coleman AS, Anguita J, Pal U. A chromosomally encoded virulence factor protects the Lyme disease pathogen against host-adaptive immunity. PLoS Pathog 2009; 5:e1000326.
21. Zhang X, Yang X, Kumar M, Pal U. BB0323 function is essential for Borrelia burgdorferi virulence and persistence through tick-rodent transmission cycle. J Infect Dis 2009; 200:1318-30.
22. Kumar M, Kaur S, Kariu T, et al. Borrelia burgdorferi BBA52 is a potential target for transmission blocking Lyme disease vaccine. Vaccine 2011; 29:9012-9.
23. Pal U, Wang P, Bao F, et al. Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. J Exp Med 2008; 205:133-41.
24. Skare JT, Shang ES, Foley DM, et al. Virulent strain associated outer membrane proteins of Borrelia burgdorferi. J Clin Invest 1995; 96:2380-92.
25. Yang X, Lenhart TR, Kariu T, Anguita J, Akins DR, Pal U. Characterization of unique regions of Borrelia burgdorferi surface-located membrane protein 1. Infect Immun 2010; 78:4477-87.
26. Mulay V, Caimano MJ, Liveris D, Desrosiers DC, Radolf JD, Schwartz I. Borrelia burgdorferi BBA74, a periplasmic protein associated with the outer membrane, lacks porin-like properties. J Bacteriol 2007; 189:2063-8.
27. Frank KL, Bundle SF, Kresge ME, Eggers CE, Samuels DS. aadA confers streptomycin resistance in Borrelia burgdorferi. J Bacteriol 2003; 185:6723-7.
28. Brown CR, Lai AY, Callen ST, Blaho VA, Hughes JM, Mitchell WJ. Adenoviral delivery of interleukin-10 fails to attenuate experimental Lyme disease. Infect Immun 2008; 76:5500-7.
29. Vieira SM, Lemos HP, Grespan R, et al. A crucial role for TNF-alpha in mediating neutrophil influx induced by endogenously generated or exogenous chemokines, KC/CXCL1 and LIX/CXCL5. Br J Pharmacol 2009; 158:779-89.
30. Kumar M, Yang X, Coleman AS, Pal U. BBA52 facilitates Borrelia burgdorferi transmission from feeding ticks to murine hosts. J Infect Dis 2010; 201:1084-95.
31. Barthold SW, Beck DS, Hansen GM, Terwilliger GA, Moody KD. Lyme borreliosis in selected strains and ages of laboratory mice. J Infect Dis 1990; 162:133-8.
32. Wooten RM, Modur VR, McIntyre TM, Weis JJ. Borrelia burgdorferi outer membrane protein A induces nuclear translocation of nuclear factor-kappa B and inflammatory activation in human endothelial cells. J Immunol 1996; 157:4584-90.
33. Akins DR, Porcella SF, Popova TG, et al. Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homologue. Mol Microbiol 1995; 18:507-20.
34. Alexopoulou L, Thomas V, Schnare M, et al. Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1-and TLR2-deficient mice. Nat Med 2002; 8:878-84.
35. Hirschfeld M, Kirschning CJ, Schwandner R, et al. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 1999; 163:2382-6.
36. Sellati TJ, Bouis DA, Caimano MJ, et al. Activation of human monocytic cells by Borrelia burgdorferi and Treponema pallidum is facilitated by CD14 and correlates with surface exposure of spirochetal lipoproteins. J Immunol 1999; 163:2049-56.
37. Bolz DD, Sundsbak RS, Ma Y, et al. MyD88 plays a unique role in host defense but not arthritis development in Lyme disease. J Immunol 2004; 173:2003-10.
38. Coburn J, Cugini C. Targeted mutation of the outer membrane protein P66 disrupts attachment of the Lyme disease agent, Borrelia burgdorferi, to integrin alpha-v-beta-3. Proc Natl Acad Sci USA 2003; 100:7301-6.
39. Behera AK, Durand E, Cugini C, et al. Borrelia burgdorferi BBB07 interaction with integrin alpha3beta1 stimulates production of pro-inflammatory mediators in primary human chondrocytes. Cell Microbiol 2008; 10:320-31.
40. Talkington J, Nickell SP. Role of Fc gamma receptors in triggering host cell activation and cytokine release by Borrelia burgdorferi. Infect Immun 2001; 69:413-9.
41. Brusca JS, McDowall AW, Norgard MV, Radolf JD. Localization of outer surface proteins A and B in both the outer membrane and intracellular compartments of Borrelia burgdorferi. J Bacteriol 1991; 173:8004-8.
42. Liang FT, Nelson FK, Fikrig E. DNA microarray assessment of putative Borrelia burgdorferi Lipoprotein Genes. Infect Immun 2002; 70:3300-3.
43. Shin OS, Isberg RR, Akira S, Uematsu S, Behera AK, Hu LT. Distinct roles for MyD88 and Toll-like receptors 2, 5, and 9 in phagocytosis of Borrelia burgdorferi and cytokine induction. Infect Immun 2008; 76:2341-51.
44. Cervantes JL, Dunham-Ems SM, La Vake CJ, et al. Phagosomal signaling by Borrelia burgdorferi in human monocytes involves Toll-like receptor (TLR) 2 and TLR8 cooperativity and TLR8-mediated induction of IFN-beta. Proc Natl Acad Sci USA 2011; 108:3683-8.
45. Moore MW, Cruz AR, LaVake CJ, et al. Phagocytosis of Borrelia burgdorferi and Treponema pallidum potentiates innate immune activation and induces gamma interferon production. Infect Immun 2007; 75:2046-62.
46. Radolf JD, Salazar JC, Dattwyler RJ. Lyme disease in humans. In: Samuels DS, Radolf JD, eds. Borrelia, molecular biology, host interaction and pathogenesis. Norfolk, UK: Caister Academic Press, 2010:487-533.
47. Sellati TJ, Burns MJ, Ficazzola MA, Furie MB. Borrelia burgdorferi upregulates expression of adhesion molecules on endothelial cells and promotes transendothelial migration of neutrophils in vitro. Infect Immun 1995; 63:4439-47.
48. Chintakuntlawar AV, Chodosh J. Chemokine CXCL1/KC and its receptor CXCR2 are responsible for neutrophil chemotaxis in adenoviral keratitis. J Interferon Cytokine Res 2009; 29:657-66.
49. Radstake TR, van der Voort R, ten Brummelhuis M, et al. Increased expression of CCL18, CCL19, and CCL17 by dendritic cells from patients with rheumatoid arthritis, and regulation by Fc gamma receptors. Ann Rheum Dis 2005; 64:359-67.
50. Tanida S, Yoshitomi H, Nishitani K, et al. CCL20 produced in the cytokine network of rheumatoid arthritis recruits CCR6+ mononuclear cells and enhances the production of IL-6. Cytokine 2009; 47:112-8.