Tick saliva affects both proliferation and distribution of Borrelia burgdorferi spirochetes in mouse organs and increases transmission of spirochetes to ticks

International Journal of Medical Microbiology

Volumn 299, Issue 5, 2009, Pages 373-380

  Horká, Helena ^a   Černá Kýčková, Kateřina ^a   Skallová, Anna ^a   Kopecký, Jan ^a  

^a INSTITUTE OF PARASITOLOGY   (Czech Republic)

Author keywords

Borrelia burgdorferi; Ixodes ricinus; Real time PCR; Saliva activated transmission

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSMISSION; BLADDER; BORRELIA BURGDORFERI; C3H MOUSE; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; EXPERIMENTAL INFECTION; FEEDING; FEMALE; HEART; HOST; INNATE IMMUNITY; INOCULATION; IXODES RICINUS; MALE; MOUSE; NONHUMAN; NYMPH; PREVALENCE; REAL TIME POLYMERASE CHAIN REACTION; SALIVA; SALIVARY GLAND; SKIN; SPIROCHETE; TICK;

ANIMALS; BORRELIA BURGDORFERI; COLONY COUNT, MICROBIAL; FEMALE; HEART; IXODES; LYME DISEASE; MICE; MICE, INBRED C3H; SALIVA; SKIN; URINARY BLADDER;

EID: 67349254700     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2008.10.009     Document Type: Article

References (53)

1. Anguita J., Ramamoorthi N., Hovius J.W.R., Das S., Thomas V., Persinski R., Conze D., Askenase P.W., Rincón M., Kantor F.S., and Fikrig E. Salp15, an Ixodes scapularis salivary protein, inhibits CD4+ T cell activation. Immunity 16 (2002) 849-859
2. Brossard M., and Wikel S.K. Tick immunobiology. Parasitology 129 (2004) S161-S176
3. Caimano M.J., Iyer R., Eggers C.H., Gonzalez C., Morton E.A., Gilbert M.A., Schwartz I., and Radolf J.D. Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol. Microbiol. 65 (2007) 1193-1217
4. Coleman J.L., Sellati T.J., Testa J.E., Kew R.R., Furie M.B., and Benach J.L. Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers. Infect. Immun. 63 (1995) 2478-2484
5. Danielová V., Rudenko N., Daniel M., Holubová J., Materna J., Golovchenko M., and Schwarzová L. Extension of Ixodes ricinus ticks and agents of tick-borne diseases to mountain areas in the Czech Republic. Int. J. Med. Microbiol. Suppl. 40 (2006) 48-53
6. Dennis D.T., and Hayes E.B. Epidemiology of Lyme borreliosis. In: Kahl O., Gray J.S., Lane R.S., and Stanek G. (Eds). Lyme Borreliosis: Biology, Epidemiology and Control (2002), CABI Publishing, Oxford 251-280
7. Ferreira B.R., and Silva J.S. Saliva of Rhipicephalus sanguineus tick impairs T cell proliferation and IFN-gamma-induced macrophage microbicidal activity. Vet. Immunol. Immunopathol. 64 (1998) 279-293
8. Ferreira B.R., and Silva J.S. Successive tick infestations selectively promote a T-helper 2 cytokine profile in mice. Immunology 96 (1999) 434-439
9. Frauenschuh A., Power C.A., Déruaz M., Ferreira B.R., Silva J.S., Teixeira M.M., Dias J.M., Martin T., Wells T.N., and Proudfoot A.E. Molecular cloning and characterization of a highly selective chemokine-binding protein from the tick Rhipicephalus sanguineus. J. Biol. Chem. 282 (2007) 27250-27258
10. Garg R., Juncadella I.J., Ramamoorthi N., Ashish, Ananthanarayanan S.K., Thomas V., Rincón M., Krueger J.K., Fikrig E., Yengo C.M., and Anguita J. Cutting edge: CD4 is the receptor for the tick saliva immunosuppressor, Salp15. J. Immunol. 177 (2006) 6579-6583
11. Gillespie R.D., Dolan M.C., Piesman J., and Titus R.G. Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick Ixodes scapularis. J. Immunol. 166 (2001) 4319-4327
12. Goodman J.L., Jurkovich P., Kodner C., and Johnson R.C. Persistent cardiac and urinary tract infections with Borrelia burgdorferi in experimentally infected Syrian hamsters. J. Clin. Microbiol. 29 (1991) 894-896
13. Hagman K.E., Yang X., Wikel S.K., Schoeler G.B., Caimano M.J., Radolf J.D., and Norgard M.V. Decorin-binding protein A (DbpA) of Borrelia burgdorferi is not protective when immunized mice are challenged via tick infestation and correlates with the lack of DbpA expression by B. burgdorferi in ticks. Infect. Immun. 68 (2000) 4759-4764
14. Hajnická V., Kocáková P., Slovák M., Labuda M., Fuchsberger N., and Nuttall P.A. Inhibition of the antiviral action of interferon by tick salivary gland extract. Parasite Immunol. 22 (2000) 201-206
15. Hovius J.W., de Jong M.A., den Dunnen J., Litjens M., Fikrig E., van der Poll T., Gringhuis S.I., and Geijtenbeek T.B. Salp15 binding to DC-SIGN inhibits cytokine expression by impairing both nucleosome remodeling and mRNA stabilization. PLoS Pathog. 4 (2008) e31
16. Hovius J.W., Ramamoorthi N., Van't Veer C., de Groot K.A., Nijhof A.M., Jongejan F., van Dam A.P., and Fikrig E. Identification of Salp15 homologues in Ixodes ricinus ticks. Vector Borne Zoonotic Dis. 7 (2007) 296-303
17. Hu{combining double acute accent}bner A., Yang X., Nolen D.M., Popova T.G., Cabello F.C., and Norgard M.V. Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc. Natl. Acad. Sci. USA 98 (2001) 12724-12729
18. Jones L.D., Hodgson E., and Nuttall P.A. Enhancement of virus transmission by tick salivary glands. J. Gen. Virol. 70 (1989) 1895-1898
19. Kopecký J., Kuthejlová M., and Pechová J. Salivary gland extract from Ixodes ricinus ticks inhibits production of interferon-γ by the upregulation of interleukin-10. Parasite Immunol. 21 (1999) 351-356
20. Kročová Z., Macela A., Hernychová L., Kroča M., Pechová J., and Kopecký J. Tick salivary gland extract accelerates proliferation of Franciscella tularensis in the host. J. Parasitol. 89 (2003) 14-20
21. Kuthejlová M., Kopecký J., Štěpánová G., and Macela A. Tick salivary gland extract inhibits killing of Borrelia afzelii spirochetes by mouse macrophages. Infect. Immun. 69 (2001) 575-578
22. Kýčková K., and Kopecký J. Effect of tick saliva on mechanisms of innate immune response against Borrelia afzelii. J. Med. Entomol. 43 (2006) 1208-1214
23. Labuda M., Jones L.D., Williams T., and Nuttall P.A. Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Med. Vet. Entomol. 7 (1993) 193-196
24. Lloyd C.M., and Walker A.R. Salivary glands and saliva of Amblyomma variegatum ticks: comparison of immatures and adults in relation to the pathogenesis of dermatophilosis. Vet. Parasitol. 59 (1995) 59-67
25. Macháčková M., Kopecký J., and Oborník M. Effect of salivary gland extract from Ixodes ricinus ticks on the proliferation of Borrelia burgdorferi sensu stricto in vivo. Folia Parasitol. 53 (2006) 153-158
26. Magnuson H.J., Capel Hill N.C., Eagle H., and Fleischman R. The minimal infectious inoculum of Spirochaeta pallida (Nichols strain), and a consideration of its rate of multiplication in vivo. Am. J. Syph. Gonorrhoea Vener. Dis. 32 (1948) 1-18
27. Masuzawa T., Beppu Y., Kawabata H., Yanagihara Y., Iwamoto Y., Shimizu T., and Johnson R.C. Experimental Borrelia burgdorferi infection of outbred mice. J. Clin. Microbiol. 30 (1992) 3016-3018
28. Mejri N., Franscini N., Rutti B., and Brossard M. Th2 polarization of the immune response of BALB/c mice to Ixodes ricinus instars, importance of several antigens in activation of specific Th2 subpopulations. Parasite Immunol. 23 (2001) 61-69
29. Narasimhan S., Deponte K., Marcantonio N., Liang X., Royce T.E., Nelson K.F., Booth C.J., Koski B., Anderson J.F., Kantor F., and Fikrig E. Immunity against Ixodes scapularis salivary proteins expressed within 24 hours of attachment thwarts tick feeding and impairs Borrelia transmission. PLoS ONE 2 (2007) e451
30. Nuttall P.A., and Jones L.D. Non-viraemic tick-borne virus transmission: mechanisms and significance. In: Dusbabek F., and Bukva V. (Eds). Modern Acarology vol. 2 (1991), Academia Prague and SPB Academic Publishing bv, The Hague 3-6
31. Nuttall P.A., and Labuda M. Tick-host interactions: saliva-activated transmission. Parasitology 129 (2004) S177-S189
32. Ogden N.H., Barker I.K., Beauchamp G., Brazeau S., Charron D.F., Maarouf A., Morshed M.G., O'Callaghan C.J., Thompson R.A., Waltner-Toews D., Waltner-Toews M., and Lindsay L.R. Investigation of ground level and remote-sensed data for habitat classification and prediction of survival of Ixodes scapularis in habitats of southeastern Canada. J. Med. Entomol. 43 (2006) 403-414
33. Pachner A.R., Ricalton N., and Delaney E. Comparison of polymerase chain reaction with culture and serology for diagnosis of murine experimental Lyme borreliosis. J. Clin. Microbiol. 31 (1993) 208-214
34. Paesen G.C., Adams P.L., Harlos K., Nuttall P.A., and Stuart D.I. Tick histamine-binding proteins: isolation, cloning and three-dimensional structure. Mol. Cell 3 (1999) 661-671
35. Pechová J., Štěpánová G., Kovář L., and Kopecký J. Tick salivary gland extract-activated transmission of Borrelia afzelii spirochaetes. Folia Parasitol. 49 (2002) 153-159
36. Pfister H.W., Wilske B., and Weber K. Lyme borreliosis: basic science and clinical aspects. Lancet 343 (1994) 1013-1016
37. Ramachandra R.N., and Wikel S.K. Modulation of host-immune responses to ticks (Acari: Ixodidae): effect of salivary gland extracts on host macrophages and lymphocyte cytokine production. J. Med. Entomol. 29 (1992) 818-826
38. Ramamoorthi N., Narasimhan S., Pal U., Bao F., Yang X.F., Fish D., Anguita J., Norgard M.V., Kantor F.S., Anderson J.F., Koski R.A., and Fikrig E. Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436 (2005) 573-577
39. Rauter C., and Hartung T. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl. Environ. Microbiol. 71 (2005) 7203-7216
40. Ribeiro J.M.C. Ixodes dammini: salivary anti-complement activity. Exp. Parasitol. 64 (1987) 347-353
41. Ribeiro J.M.C., and Spielman A. Ixodes dammini: salivary anaphylatoxin inactivating activity. Exp. Parasitol. 62 (1986) 292-297
42. Ribeiro J.M.C., Weiss J.J., and Telford III S.R. Saliva of the tick Ixodes dammini inhibits neutrophil function. Exp. Parasitol. 70 (1990) 382-388
43. Schoeler G.B., Manweiler S.A., and Wikel S.K. Ixodes scapularis: effects of repeated infestations with pathogen-free nymphs on macrophage and T lymphocyte cytokine responses of BALB/c and C3H/HeN mice. Exp. Parasitol. 92 (1999) 239-248
44. Schroeder H., Daix V., Gillet L., Renault J.C., and Vanderplasschen A. The paralogous salivary anti-complement proteins IRAC I and IRAC II encoded by Ixodes ricinus ticks have broad and complementary inhibitory activities against the complement of different host species. Microbes Infect. 9 (2007) 247-250
45. Schuijt T.J., Hovius J.W., van Burgel N.D., Ramamoorthi N., Fikrig E., and van Dam A.P. The tick salivary protein Salp15 inhibits the killing of serum-sensitive Borrelia burgdorferi sensu lato isolates. Infect. Immun. 76 (2008) 2888-2894
46. Schwan T.G., Burgdorfer W., Schrumpf M.E., and Karstens R.H. The urinary bladder, a consistent source of Borrelia burgdorferi in experimentally infected white-footed mice (Peromyscus leucopus). J. Clin. Microbiol. 26 (1988) 893-895
47. Shi Y., Xu Q., McShan K., and Liang F.T. Both decorin-binding proteins A and B are critical for the overall virulence of Borrelia burgdorferi. Infect. Immun. 76 (2008) 1239-1246
48. Skallová A., Iezzi G., Ampenberger F., Kopf M., and Kopecký J. Tick saliva inhibits dendritic cell migration, maturation, and function while promoting development of Th2 responses. J. Immunol. 180 (2008) 6186-6192
49. Tyson K., Elkins C., Patterson H., Fikrig E., and de Silva A. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect Mol. Biol. 16 (2007) 469-479
50. Valenzuela J.G., Charlab R., Mather T.N., and Ribeiro J.M. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J. Biol. Chem. 275 (2000) 18717-18723
51. van Dam A.P., Kuiper H., Vos K., Widjojokusumo A., de Jongh B.M., Spanjaard L., Ramselaar A.C., Kamer M.D., and Dankert J. Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin. Infect. Dis. 17 (1993) 708-717
52. Wilske B., Fingerle V., and Schulte-Spechtel U. Microbiological and serological diagnosis of Lyme borreliosis. FEMS Immunol. Med. Microbiol. 49 (2007) 13-21
53. Zeidner N.S., Schneider B.S., Nuncio M.S., Gern L., and Piesman J. Co-inoculation of Borrelia spp. with tick salivary gland lysate enhances spirochaete load in mice and is tick species-specific. J. Parasitol. 88 (2002) 1276-1278