Molecular Interactions that Enable Movement of the Lyme Disease Agent from the Tick Gut into the Hemolymph

English version České info

Borrelia burgdorferi, the causative agent of Lyme disease, is transmitted to humans by bite of Ixodes scapularis ticks. The mechanisms by which the bacterium is transmitted from vector to host are poorly understood. In this study, we show that the F(ab)₂ fragments of BBE31, a B.burgdorferi outer-surface lipoprotein, interfere with the migration of the spirochete from tick gut into the hemolymph during tick feeding. The decreased hemolymph infection results in lower salivary glands infection, and consequently attenuates mouse infection by tick-transmitted B. burgdorferi. Using a yeast surface display approach, a tick gut protein named TRE31 was identified to interact with BBE31. Silencing tre31 also decreased the B. burgdorferi burden in the tick hemolymph. Delineating the specific spirochete and arthropod ligands required for B. burgdorferi movement in the tick may lead to new strategies to interrupt the life cycle of the Lyme disease agent.

Vyšlo v časopise: Molecular Interactions that Enable Movement of the Lyme Disease Agent from the Tick Gut into the Hemolymph. PLoS Pathog 7(6): e32767. doi:10.1371/journal.ppat.1002079
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002079

Souhrn

Zdroje

1. BarbourAGFishD 1993 The biological and social phenomenon of Lyme disease. Science 260 1610 1616

2. SteereAC 2001 Lyme disease. N Engl J Med 345 115 125

3. PiesmanJ 1989 Transmission of Lyme disease spirochetes (Borrelia burgdorferi). Exp Appl Acarol 7 71 80

4. NarasimhanSSantiagoFKoskiRABreiBAndersonJF 2002 Examination of the Borrelia burgdorferi transcriptome in Ixodes scapularis during feeding. J Bacteriol 184 3122 3125

5. KumarMYangXColemanASPalU 2010 BBA52 facilitates Borrelia burgdorferi transmission from feeding ticks to murine hosts. J Infect Dis 201 1084 1095

6. GilmoreRDJrMbowMLStevensonB 2001 Analysis of Borrelia burgdorferi gene expression during life cycle phases of the tick vector Ixodes scapularis. Microbes Infect 3 799 808

7. XuHHeMHeJJYangXF 2010 Role of the surface lipoprotein BBA07 in the enzootic cycle of Borrelia burgdorferi. Infect Immun 78 2910 2918

8. FikrigEFengWBartholdSWTelfordSR3rdFlavellRA 2000 Arthropod -⁠ and host-specific Borrelia burgdorferi bbk32 expression and the inhibition of spirochete transmission. J Immunol 164 5344 5351

9. De SilvaAMFikrigE 1995 Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am J Trop Med Hyg 53 397 404

10. PalULiXWangTMontgomeryRRRamamoorthiN 2004 TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119 457 468

11. RamamoorthiNNarasimhanSPalUBaoFYangXF 2005 The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436 573 577

12. GuoBPBrownELDorwardDWRosenbergLCHookM 1998 Decorin-binding adhesins from Borrelia burgdorferi. Mol Microbiol 30 711 723

13. ProbertWSJohnsonBJ 1998 Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol Microbiol 30 1003 1015

14. GuoBPNorrisSJRosenbergLCHookM 1995 Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect Immun 63 3467 3472

15. von LackumKOllisonKMBykowskiTNowalkAJHughesJL 2007 Regulated synthesis of the Borrelia burgdorferi inner-membrane lipoprotein IpLA7 (P22, P22-A) during the Lyme disease spirochaete's mammal-tick infectious cycle. Microbiology 153 1361 1371

16. de SilvaAMZeidnerNSZhangYDolanMCPiesmanJ 1999 Influence of outer surface protein A antibody on Borrelia burgdorferi within feeding ticks. Infect Immun 67 30 35

17. PalUYangXChenMBockenstedtLKAndersonJF 2004 OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113 220 230

18. BendtsenJDNielsenHvon HeijneGBrunakS 2004 Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 783 795

19. Dunham-EmsSMCaimanoMJPalUWolgemuthCWEggersCH 2009 Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest 119 3652 3665

20. JohnsROhnishiJBroadwaterASonenshineDEDe SilvaAM 2001 Contrasts in tick innate immune responses to Borrelia burgdorferi challenge: immunotolerance in Ixodes scapularis versus immunocompetence in Dermacentor variabilis (Acari: Ixodidae). J Med Entomol 38 99 107

21. GilmoreRDJrHowisonRRDietrichGPattonTGCliftonDR 2010 The bba64 gene of Borrelia burgdorferi, the Lyme disease agent, is critical for mammalian infection via tick bite transmission. Proc Natl Acad Sci U S A 107 7515 7520

22. JohnsRHSonenshineDEHynesWL 2000 Enhancement of OspC expression by Borrelia burgdorferi in the presence of tick hemolymph. FEMS Microbiol Lett 193 137 141

23. LiXLiuXBeckDSKantorFSFikrigE 2006 Borrelia burgdorferi lacking BBK32, a fibronectin-binding protein, retains full pathogenicity. Infect Immun 74 3305 3313

24. YangXFPalUAlaniSMFikrigENorgardMV 2004 Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J Exp Med 199 641 648

25. LiXNeelakantaGLiuXBeckDSKantorFS 2007 Role of outer surface protein D in the Borrelia burgdorferi life cycle. Infect Immun 75 4237 4244

26. PalUWangPBaoFYangXSamantaS 2008 Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. J Exp Med 205 133 141

27. StrotherKOde SilvaA 2005 Role of Borrelia burgdorferi linear plasmid 25 in infection of Ixodes scapularis ticks. J Bacteriol 187 5776 5781

28. GrimmDEggersCHCaimanoMJTillyKStewartPE 2004 Experimental assessment of the roles of linear plasmids lp25 and lp28-1 of Borrelia burgdorferi throughout the infectious cycle. Infect Immun 72 5938 5946

29. StrotherKOBroadwaterADe SilvaA 2005 Plasmid requirements for infection of ticks by Borrelia burgdorferi. Vector Borne Zoonotic Dis 5 237 245

30. PurserJELawrenzMBCaimanoMJHowellJKRadolfJD 2003 A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48 753 764

31. RevelATBlevinsJSAlmazanCNeilLKocanKM 2005 bptA (bbe16) is essential for the persistence of the Lyme disease spirochete, Borrelia burgdorferi, in its natural tick vector. Proc Natl Acad Sci U S A 102 6972 6977

32. PalUMontgomeryRRLusitaniDVoetPWeynantsV 2001 Inhibition of Borrelia burgdorferi-tick interactions in vivo by outer surface protein A antibody. J Immunol 166 7398 7403

33. NarasimhanSSukumaranBBozdoganUThomasVLiangX 2007 A tick antioxidant facilitates the Lyme disease agent's successful migration from the mammalian host to the arthropod vector. Cell Host Microbe 2 7 18

34. ChaoGLauWLHackelBJSazinskySLLippowSM 2006 Isolating and engineering human antibodies using yeast surface display. Nat Protoc 1 755 768