Folia Parasitologica 52[4] 279-294 (2005) | DOI: 10.14411/fp.2005.039

Lyme borreliosis: insights into tick- / host-borrelia relations

Libor Grubhoffer1, Maryna Golovchenko1, Marie Vancová1, Klára Zacharovová-Slavíčková1, Nataliia Rudenko1, James H. Oliver Jr.2
1 Institute of Parasitology, Academy of Sciences of the Czech Republic and Faculty of Biological Sciences, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
2 Institute of Arthropodology and Parasitology, Georgia Southern University, Statesboro, Georgia 30460-8056, USA

Lyme borreliosis (LB) is a serious infectious disease of humans and some domestic animals in temperate regions of the Northern Hemisphere. It is caused by certain spirochetes in the Borrelia burgdorferi sensu lato (s.l.) species complex. The complex consists of 11 species (genospecies). Borrelia burgdorferi sensu stricto (s.s.), Borrelia garinii and Borrelia afzelii are the major agents of human disease. Borrelia burgdorferi s.l. species are transmitted mainly by ticks belonging to the Ixodes ricinus species complex plus a few additional species not currently assigned to the complex. B. burgdorferi infections may produce an acute or chronic disease with a wide array of clinical symptoms such as erythema migrans (EM), carditis, arthritis, neuroborreliosis, and acrodermatitis chronica atrophicans (ACA). Differences in LB spirochetes 'genospecies' and strains/isolates determine the occurrence and severity of this multi-system disease. Accurate and reliable identification of the LB spirochetes in ticks as well as knowledge of their prevalence are essential for prevention against the disease and development of an effective vaccine. An overview of the knowledge of molecular factors with emphasis on potential protein-carbohydrate interactions in the tick-borrelia system is the main focus of this review.

Keywords: borrelia spirochete, Lyme borreliosis, ticks, vectors, interactions, glycoproteins

Received: January 18, 2005; Accepted: June 23, 2005; Published: September 1, 2005  Show citation

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Grubhoffer, L., Golovchenko, M., Vancová, M., Zacharovová-Slavíčková, K., Rudenko, N., & Oliver, J.H. (2005). Lyme borreliosis: insights into tick- / host-borrelia relations. Folia Parasitologica, 52(4), 279-294. doi: 10.14411/fp.2005.039
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    References

    1. ASSOUS M., POSTIC D., PAUL G., NEVOT P., BARANTON G. 1993: Western blot analysis of sera from Lyme borreliosis patients according to the genomic species of the Borrelia strains used as antigen. J. Clin. Microbiol. Infect. Dis. 12: 261-268 Go to original source... Go to PubMed...
    2. BABB K., El-HAGE N., MILLER J.C., CARROL J.A., STEVENSON B. 2001: Distinct regulatory pathway control expression of Borrelia burgdorferi infection-associated OspC and Erp surface proteins. Infect. Immun. 69: 4146- 4153 Go to original source... Go to PubMed...
    3. BARANTON G., ASSOUS M., POSTIC D. 1992: Three bacterial species associated with Lyme borreliosis. Clinical and diagnostic implications Bull. Acad. Natl. Med. 176: 1075-1085 Go to PubMed...
    4. BARANTON G., POSTIC D., SAINT GIRONS I., BOERLING P., PIFFARETTI J.C., ASSOUS M., BUNIKIS J., LUKE C.J., BUNIKIENE E., BERGSTROeM, BARBOUR A.G. 1998: A surface-exposed region of a novel outer membrane protein (P66) of Borrelia spp. is variable in size and sequence. J. Bacteriol. 180: 1618 -1623 Go to original source... Go to PubMed...
    5. BARANTON G., SEINOST G., THEODORE G., POSTIC D., DYKHUIYEN D. 2001: Distinct levels of genetic diversity of Borrelia burgdorferi are associated with different aspects of pathogenicity. Res. Microbiol. 152: 149-156 Go to original source... Go to PubMed...
    6. BARBOUR A.G. 1988: Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent. J. Clin. Microbiol. 26: 475- 478 Go to original source... Go to PubMed...
    7. BARBOUR A.G., HAYES S.F. 1986: Biology of Borrelia species. Microbiol. Rev. 50: 381-400 Go to original source... Go to PubMed...
    8. BARILLAS-MURY C., WIZEL B., HAN Y.S. 2000: Mosquito immune responses and malaria transmission: lessons from insect model systems and implications for vertebrate innate immunity and vaccine development. Insect Biochem. Mol. Biol. 30: 429-442 Go to original source... Go to PubMed...
    9. BENACH J.L., COLEMAN J.L., SKINNER R.A., BOSLER E.M. 1987: Adult Ixodes dammini on rabbits: hypothesis for the development and transmission of Borrelia burgdorferi. J. Infect. Dis. 155: 1300-1306 Go to original source... Go to PubMed...
    10. BEN-MENACHEM G., KUBLER-KIELB J., COXON B., YERGEY A., SCHNEERSON R. 2003: A newly discovered cholesteryl galactoside from Borrelia burgdorferi. Proc. Natl. Acad. Sci. U.S.A. 100: 7913-7918 Go to original source... Go to PubMed...
    11. BERGSTROeM S., NOPPA L., GYLFE A., OeSTBERG Y. 2002: Molecular and cellular biology of Borrelia burgdorferi sensu lato. In: O. Kahl, J.S. Gray, R.S. Lane and G. Stanek (Eds.), Lyme Borreliosis: Biology, Epidemiology and Control. CABI Publishing, Oxford, United Kingdom, pp. 47-90 Go to original source...
    12. BRORSON O., BRORSON S.H. 1998: In vitro conversion of Borrelia burgdorferi to cystic forms in spinal fluid, and transformation to mobile spirochetes by incubation in BSK-H medium. Infection 26: 144-150 Go to original source... Go to PubMed...
    13. BURGDORFER W. 2001: Arthropod-borne spirochetosis: a historical perspective. Eur. J. Clin. Microbiol. Dis. 20: 1- 5 Go to original source...
    14. BURGDORFER W., BARBOUR A.G., HAYES S.F., BENACH J.L., GRUNDWALDT E., DAVIS J.P. 1982: Lyme disease: a tick-borne spirochetosis? Science 216: 1317- 1319 Go to original source... Go to PubMed...
    15. BURGDORFER W., HAYES S.F., CORWIN D. 1989: Pathophysiology of the Lyme disease spirochete Borrelia burgdorferi, in ixodid ticks. Rev. Infect. Dis. 6: 127-150 Go to original source...
    16. CANICA M.M., NATO F., DU MERLE L., MAZIE J.C., BARANTON G., POSTIC D. 1993: Monoclonal antibodies for identification of Borrelia afzelii sp. nov. associated with late cutaneous manifestations of Lyme borreliosis. Scand. J. Infect. Dis. 25: 441-448 Go to original source... Go to PubMed...
    17. CHRISTOPHIDES G.K., VLACHOU D., KAFATOS F.C. 2004: Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol. Rev. 198: 127-148 Go to original source... Go to PubMed...
    18. COLEMAN J.L., GEBBIA J.A., PIESMAN J., DEGEN J., BUGGE T.H., BENACH J.L. 1997: Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89: 1111-1119 Go to original source... Go to PubMed...
    19. COLEMAN J.L., ROEMER E.J., BENACH J.L. 1999: Plasmin-coated Borrelia burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immun. 67: 3929-3936 Go to original source... Go to PubMed...
    20. COLLARES-PEREIRA M., COUCEIRO S., FRANCA I., KURTENBACH K., SCHAeFER S.M., VITORINO L., GONCALVES L., BAPTISTA S., VIEIRA M.L., CUNHA C. 2004: First isolation of Borrelia lusitaniae from a human patient. J. Clin. Microbiol. 42: 1316-1318 Go to original source... Go to PubMed...
    21. DE SILVA A.M., FIKRIG E. 1997: Borrelia burgdorferi genes selectively expressed in ticks and mammals. Parasitol. Today 13: 267-270 Go to original source... Go to PubMed...
    22. DEFOE G., COBURN J. 2001: Delineation of Borrelia burgdorferi p66 sequences required for integrin alpha(IIb)beta(3) recognition. Infect. Immun. 69: 3455- 3459 Go to original source... Go to PubMed...
    23. DEMAERSCHALCK I., MESSAOUD A.B., KESEL M. De, HOYOIS B., LOBET Y., HOET P., BIGAIGNON G., BOLLEN A., GODFROID E. 1995: Simultaneous presence of different Borrelia burgdorferi sensu lato genospecies in biological fluids of Lyme disease patients. J. Clin. Microbiol. 33: 602-608 Go to original source... Go to PubMed...
    24. DENNIS D.T., HAYES E.B. 2002: Epidemiology of Lyme borreliosis. In: O. Kahl, J.S. Gray, R.S. Lane and G. Stanek (Eds.), Lyme Borreliosis: Biology, Epidemiology and Control. CABI Publishing, Oxford, United Kingdom, pp. 251-280 Go to original source... Go to PubMed...
    25. DERDAKOVA M., BEATI L., PET'KO B., STANKO M., FISH D. 2003: Genetic variability within Borrelia burgdorferi sensu lato genospecies established by PCRsingle-strand conformation polymorphism analysis of the rrfA-rrlB intergenic spacer in Ixodes ricinus ticks from the Czech Republic. Appl. Environ. Microbiol. 69: 509-516 Go to original source... Go to PubMed...
    26. DOLAN M.C., PIESMAN J., MBOW M.L., MAUPIN G.O., PETER O., BROSSARD M., GOLDE W.T. 1998: Vector competence of Ixodes scapularis and Ixodes ricinus (Acari: Ixodidae) for three genospecies of Borrelia burgdorferi. J. Med. Entomol. 35: 465-470. Go to original source... Go to PubMed...
    27. DORWARD D.W., GARON C.F. 1990: Glycosylation of proteins associated with extra cellular membrane vesicles in Borrelia burgdorferi. IV. Int. Conf. Lyme Borreliosis, Stockholm, June 18-21, 1990, Abstract M/TU-P-12
    28. DURNOVA E. 1998: [Midgut agglutinins (lectins) of common sheep tick, Ixodes ricinus L. (Ixodida, Ixodidae): isolation and partial characterization.] MSc thesis, University of South Bohemia, Ceske Budejovice, 44 pp. (In Czech, unpubl.)
    29. EGGENBERGER L.R., LAMOREAUX W.J., COONS L.B. 1990: Hemocytic encapsulation of implants in the tick Dermacentor variabilis. Exp. Appl. Acarol. 9: 279-287 Go to original source... Go to PubMed...
    30. ELIAS A.F., STEWART P.E., GRIMM D., CAIMANO M.J., EGGERS C.H., TILLY K., BONO J.L., AKINS D.R., RADOLF J.D., SCHWAN T.G., ROSA P. 2002: Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect. Immun. 70: 2139-2150 Go to original source... Go to PubMed...
    31. FENG S., HODZIC E., STEVENSON B., BARTHOLD S. 1998: Humoral immunity to Borrelia burgdorferi N40 decorin binding proteins during infection of laboratory mice. Infect. Immun. 66: 2827-2835 Go to original source... Go to PubMed...
    32. FRASER C.M., CASJENS S., HUANG W., SUTTON G., CLAYTON R., LATHIGRA R., WHITE O., KETCHUM K.A., DODSON R., HICKEY E.K., GWINN M., DOUGHERTY B., TOMB J.F., FLEISCHMANN R.D., RICHARDSON D., PETERSON J., KERLAVAGE A.R., QUACKENBUSH J., SALZBERG S., HANSON M., et al. 1997: Genome of Lyme disease pathogen. Nature 390: 580-586 Go to original source... Go to PubMed...
    33. FRIEDHOFF K.T. 1990: Interaction between parasite and tick vector. Int. J. Parasitol. 20: 525-535 Go to original source... Go to PubMed...
    34. FRIEDLANDER A.M., WELKOS S.L., WORSHAM P.L., ANDREWS G.P., HEATH D.G., ANDERSON G.W. Jr., PITT M.L., ESTEP J., DAVIS K. 1995: Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin. Infect. Dis. 21: S178-S181 Go to original source... Go to PubMed...
    35. FUCHS H., WALLICH R., SIMON M.M., KRAMER M.D. 1994: The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc. Natl. Acad. Sci. U.S.A. 91: 12594-12598 Go to original source... Go to PubMed...
    36. FUKUNAGA M., HAMASE A., OKADA K., NAKAO M. 1996: Borrelia tanukii sp. nov. and Borrelia turdae sp. nov. found from ixodid ticks in Japan: rapid species identification by 16S rRNA gene-targeted PCR analysis. Microbiol. Immunol. 40: 877-881 Go to original source... Go to PubMed...
    37. FUKUNAGA M., TAKAHASHI Y., TSURUTA Y., MATSUSHITA O., RALPH D., McCLELLAND M., NAKAO M. 1995: Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int. J. Syst. Bacteriol. 45: 804-810 Go to original source... Go to PubMed...
    38. GARCIA-MONCO J.C.G., FERNANDEZ VILLAR B., ROGERS R.C., SZCZEPANSKI A., WHEELER C.M., BENACH J.L. 1992: Borrelia burgdorferi and other related spirochetes bind to galactocerebroside. Neurology 42: 1341-1348 Go to original source... Go to PubMed...
    39. GARON C.F., DORWARD D.W., CORWIN M.D. 1989: Structural features of Borrelia burgdorferi - the Lyme disease spirochete: silver staining for nucleic acid. Scann. Microsc. 3: 109-115
    40. GE Y., CORUM L., SLAUGHTER C.A., CHARON N.W. 1998: Structure and expression of the FlaA periplasmic flagellar protein of Borrelia burgdorferi. J. Bacteriol. 180: 2418-2425 Go to original source... Go to PubMed...
    41. GERN L., HU C.M., KOCIANOVA E., VYROSTEKOVA V., REHACEK J. 1999: Genetic diversity of Borrelia burgdorferi sensu lato isolates obtained from Ixodes ricinus ticks collected in Slovakia. Eur. J. Epidemiol. 15: 665-669 Go to original source... Go to PubMed...
    42. GILMORE R.D. Jr., MURPHREE R.L., JAMES A.M., SULLIVAN S.A., JOHNSON B.J.B. 1999: The Borrelia burgdorferi 37-kilodalton immunoblot band (P37) used in serodiagnosis of early Lyme disease is the flaA gene product. J. Clin. Microbiol. 37: 548-552 Go to original source... Go to PubMed...
    43. GRIMM D., TILLY K., BYRAM R., STEWART P.E., KRUM J.G., BUESCHEL D.M., SCHWAN T.G., POLICASTRO P.F., ELIAS A.F., ROSA P.A. 2004: Outersurface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc. Natl. Acad. Sci. U.S.A. 101: 3142-3147 Go to original source... Go to PubMed...
    44. GRUBHOFFER L., DURNOVA E. 1996: A lectin in salivary glands of tick Ixodes ricinus: detection and partial characterization. XX Int. Congr. Entomol., Firenze, Italy, 1996, Proceedings, p. 746
    45. GRUBHOFFER L., HYPSA V., VOLF P. 1997: Lectins (hemagglutinins) in the gut of the important disease vectors. Parasite 4: 203-216 Go to original source... Go to PubMed...
    46. GRUBHOFFER L., KOVAR V. 1998: Arthropod lectins: affinity approaches in the analysis and preparation of carbohydrate binding proteins. In: A. Wiesner et al. (Eds.), Techniques in Insect Immunology. FITC-5, SOS Publications, Fair Haven, NJ, pp. 47-57
    47. GRUBHOFFER L., RUDENKO N., KOVAR V. 2004: Tick lectins: structural and functional properties. Parasitology 129 (Suppl.): S113-S126 Go to original source... Go to PubMed...
    48. GRUBHOFFER L., VERES J., DUSBABEK F. 1991: Lectins as the molecular factors of recognition and defence reactions of ticks. In: F. Dusbabek and V. Bukva (Eds.), Modern Acarology. Vol. 2. Academia Prague and SPB Academic, The Hague, pp. 381-388
    49. GRUBHOFFER L., UHLIR J., VOLF P. 1992: Hemagglutination activity of Borrelia burgdorferi and B. recurrentis. 1st International Conference on Lyme Borreliosis, Prague, October 1992, Abstract 22
    50. GRUBHOFFER L., UHLIR J., VOLF P. 1993: Functional and structural identification of a new lectin activity of Borrelia recurrentis spirochetes. Comp. Biochem. Physiol. 105B: 535-540 Go to original source...
    51. GUIGNOT J., MOCK M., FOUET A. 1997: AtxA activates the transcription of genes harbored by both Bacillus anthracis virulence plasmids. FEMS Microbiol. Lett. 147: 203-207 Go to original source... Go to PubMed...
    52. GUO B.P., BROWN E.L., DORWARD D.W., ROSENBERG L.C., HOOK M. 1998: Decorin-binding adhesins from Borrelia burgdorferi. Mol. Microbiol. 30: 711-723 Go to original source... Go to PubMed...
    53. GUO B.P., NORRIS S.J., ROSENBERG L.C., HOOK M. 1995: Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect. Immun. 63: 3467-3472. Go to original source... Go to PubMed...
    54. HAGMAN K.E., LAHDANNE P., POPOVA P., PORCELLA T.G., AKINS S.F., RADOLF D.R., NORGARD M. 1998: Decorin-binding protein of Borrelia burgdorferi is encoded within a two-gene operon and is protective in the murine model of Lyme borreliosis. Infect. Immun. 66: 2674-2683 Go to original source... Go to PubMed...
    55. HELLWAGE J., MERI T., HEIKKILAe T., ALITALO A., PANELIUS J., LAHDENNE P., SEPPAeLAe I.J.T., MERI S. 2001: The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276: 8427-8435 Go to original source... Go to PubMed...
    56. HENGGE U.R., TANNAPFEL A., TYRING S.K., ERBEL R., ARENDT G., RUZICKA T. 2003: Lyme borreliosis. Lancet Infect. Dis. 3: 489-500 Go to original source... Go to PubMed...
    57. HOSSAIN H., WELLENSIEK H.J., GEYER R., LOCHNIT G. 2001: Structural analysis of glycolipids from Borrelia burgdorferi. Biochimie 83: 683-692 Go to original source... Go to PubMed...
    58. HUBALEK Z. 2003: Emerging human infectious diseases: anthroponoses, zoonoses, and sapronoses. Emerg. Infect. Dis. 9: 403-404 Go to original source... Go to PubMed...
    59. HUBALEK Z., HALOUZKA J. 1998: Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitol. Res. 84: 167-172 Go to original source... Go to PubMed...
    60. HULINSKA D., VOLF P., GRUBHOFFER L. 1991: Surface carbohydrates of Borrelia burgdorferi. In: F. Dusbabek and V. Bukva (Eds.), Modern Acarology. Vol. 2. Academia Prague and SPB Academic, The Hague, pp. 73-78
    61. HULINSKA D., VOLF P., GRUBHOFFER L. 1992: Study of Borrelia burgdorferi glycoproteins and surface carbohydrates by lectin conjugates. Zentralbl. Bakteriol. 276: 473- 480 Go to original source... Go to PubMed...
    62. ISAACS R.D. 1994: Borrelia burgdorferi bind to epithelial cell proteoglycans. J. Clin. Invest. 93: 809-819 Go to original source... Go to PubMed...
    63. JOHNS R., OHNISHI J., BROADWATER A., SONENSHINE D.E., DE SILVA A.M., HYNES W.L. 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 Go to original source... Go to PubMed...
    64. JOHNS R., SONENSHINE D.E., HYNES W.L. 1998: Control of bacterial infections in the hard tick Dermacentor variabilis (Acari: Ixodidae): evidence for the existence of antimicrobial proteins in tick hemolymph. J. Med. Entomol. 37: 265-270 Go to original source... Go to PubMed...
    65. JOHNS R., SONENSHINE D.E., HYNES W.L. 2000: Response of the tick Dermacentor variabilis (Acari: Ixodidae) to hemocoelic inoculation of Borrelia burgdorferi (Spirochetales). J. Med. Entomol. 37: 265-270 Go to original source... Go to PubMed...
    66. JOHNSON R.C., SCHMID G.P., HYDE F.M., STEIGERWALT A.G., BRENNER D.J. 1984: Borrelia burgdorferi sp. nov.: etiological agent of Lyme disease. Int. J. Syst. Bacteriol. 34: 496-497 Go to original source...
    67. KAMRADT T. 2002: Lyme disease and current aspects of immunization. Arthritis Res. 4: 20-29 Go to original source... Go to PubMed...
    68. KAMWENDO S.P., INGRAM G.A., MUSISI F.L., MOLYNEUX D.H. 1993: Haemagglutinin activity in tick (Rhipicephalus appendiculatus) haemolymph and extracts of gut and salivary gland. Ann. Trop. Med. Parasitol. 87: 303-305 Go to original source... Go to PubMed...
    69. KAMWENDO S.P., MUSISI F.L., TREES A.J., MOLYNEUX D.H. 1995: Effect of haemagglutinin (lectin) inhibitory sugars in Theileria parva infection in Rhipicephalus appendiculatus. Int. J. Parasitol. 25: 29-35 Go to original source... Go to PubMed...
    70. KAWABATA H., MASUZAWA T., YANAGIHARA Y. 1993: Genomic analysis of Borrelia japonica sp. nov. isolated from Ixodes ovatus in Japan. Microbiol. Immunol. 37: 843-848 Go to original source... Go to PubMed...
    71. KOVAR V., KOPACEK P., GRUBHOFFER L. 2000: Isolation and characterization of Dorin M, a lectin from plasma of the soft tick Ornithodoros moubata. Insect Biochem. Mol. Biol. 30: 195-205 Go to original source... Go to PubMed...
    72. KUHN K.H., RITTIG M., HAeUPL T., BURMESTER G.R. 1994: Haemocytes of the hard tick Ixodes ricinus express coiling phagocytosis of Borrelia burgdorferi. Dev. Comp. Immunol. 18 (Suppl. 1): S115 Go to original source...
    73. KUHN K.H., UHLIR J., GRUBHOFFER L. 1996: Ultrastructural localization of a sialic acid-specific hemolymph lectin in the hemocytes and other tissues of the hard tick Ixodes ricinus (Acari: Chelicerata). Parasitol. Res. 82: 215-221 Go to original source... Go to PubMed...
    74. KUMARAN D., ESWARAMOORTHY S., LUFT B.J., KOIDE S., DUNN J.J., LAWSON C.L., SWAMINATHAN S. 2001: Crystal structure of outer surface protein C (OspC) from the Lyme disease spirochete, Borrelia burgdorferi. EMBO J. 20: 971-978 Go to original source... Go to PubMed...
    75. KURTENBACH K., PEACEY M., RIJPKEMA S.G.T., HOODLESS A.N., NUTTALL P.A., RANDOLPH S.E. 2002: Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game bird and small rodents in England. Appl. Environ. Microbiol. 64: 1169- 1174 Go to original source...
    76. LeFLECHE, A., POSTIC D., GIRARDET K., PETER O., BARANTON G. 1997: Characterization of Borrelia lusitaniae sp. nov. by 16S ribosomal DNA sequence analysis. Int. J. Syst. Bacteriol. 47: 921-925 Go to original source... Go to PubMed...
    77. LEONG J.M., MORRISSEY P.E., ORTEGA-BARRIA E., PEREIRA M.E.A., COBURN J. 1995: Hemagglutination and proteoglycan binding by the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63: 874-883 Go to original source... Go to PubMed...
    78. LI H., DUNN J.J., LUFT B.J., LAWSON C.L. 1997: Crystal structure of Lyme disease antigen outer protein A complexed with an Fab. Proc. Natl. Acad. Sci. U.S.A. 94: 3584-3589 Go to original source... Go to PubMed...
    79. LIN T., OLIVER J.H. Jr., GAO L. 2002: Genetic diversity of the outer surface protein C gene of southern Borrelia isolates and its possible epidemiological, clinical, and pathogenetic implications. J. Clin. Microbiol. 40: 2572-2583 Go to original source... Go to PubMed...
    80. LIVEY I., GIBBS C.P., SCHUSTER R., DORNER F. 1995: Evidence for lateral transfer and recombination of OspC variation in Lyme disease. Mol. Microbiol. 18: 257-269 Go to original source... Go to PubMed...
    81. MARCONI R.T., LIVERIS D., SCHWARTZ I. 1995: Identification of novel insertion elements, restriction fragments length polymorphism pattern and discontinuous 23S rRNA in Lyme disease spirochetes: phylogenetic analyses of rRNA genes and their intergenic spacers in Borrelia japonica sp. nov. and genomic group 21038 (Borrelia andersonii sp. nov.) isolates. J. Clin. Microbiol. 33: 2427- 2434. Go to original source... Go to PubMed...
    82. MASUZAWA T. 2004: Terrestrial distribution of the Lyme borreliosis agent Borrelia burgdorferi sensu lato in East Asia. Jpn. J. Infect. Dis. 57: 229-235
    83. MASUZAWA T., TAKADA N., KUDEKEN M., FUKUI T., YANO Y., ISHIGURO F., KAWAMURA Y., IMAI Y., EZAKI T. 2001: Borrelia sinica sp. nov., a Lyme diseaserelated Borrelia species isolated in China. Int. J. Syst. Evol. Microbiol. 51: 1817-1824 Go to original source... Go to PubMed...
    84. MATLOVA L., HALOUZKA J., JURICOVA Z., HUBALEK Z. 1996: Comparative experimental infection of Ixodes ricinus and Dermacentor reticulatus (Acari: Ixodidae) with Borrelia burgdorferi sensu lato. Folia Parasitol. 43: 159-160
    85. McDOWELL J.V., SUNG S.Z., PRICE G., MARCONI R.T. 2001: Demonstration of the genetic stability and temporal expression of select members of the Lyme disease spirochete OspF protein family during infection in mice. Infect. Immun. 69: 4831-4838 Go to original source... Go to PubMed...
    86. McGOWEN M.M., VIONNET J., VANNW.F. 2001: Elongation of alpha 2,8/2,9 polysialic acid by the Escherichia coli K92. Glycobiology 11: 613-620 Go to original source... Go to PubMed...
    87. NAKAJIMA Y., NATERS-YASUI A., TAYLOR D., YAMAKAWA M. 2001: Two isoforms of the arthropod defensin family from the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Biochem. Mol. Biol. 31: 747- 751 Go to original source... Go to PubMed...
    88. NOPPA L., OeSTBERG Y., LAVRINOVICHA M., BERGSTROeM S. 2001: P13, an integral membrane protein of Borrelia burgdorferi, is C-terminally processed and contains surface-exposed domains. Infect. Immun. 69: 3323- 3334 Go to original source... Go to PubMed...
    89. OLIVER J.H. Jr., OWSLEY M.R., HUTCHESON H.J., JAMES A.M., CHEN C., IRBY W.S., DOTSON E.M., McLAIN D.K. 1993: Conspecificity of the ticks Ixodes scapularis and I. dammini (Acari: Ixodidae). J. Med. Entomol. 30: 54-63 Go to original source... Go to PubMed...
    90. OYSTON P.C., PAYNE D.W., HAVARD H.L., WILLIAMSON E.D., TITBALL R.W. 1998: Production of a nontoxic site-directed mutant of Clostridium perfringens epsilon-toxin, which induces protective immunity in mice. Microbiology 144: 333-341 Go to original source... Go to PubMed...
    91. PACHNER A.R. 1989: Neurologic manifestation of Lyme disease, the new "great imitator". Rev. Infect. Dis. 11: 1482-1486 Go to original source...
    92. PAL U., DE SILVA A.M., MONTGOMERY R.R., FISH D., ANGUITA J., ANDERSON J.F., LOBET Y., FIKRIG E. 2000: Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. J. Clin. Invest. 106: 561-569 Go to original source... Go to PubMed...
    93. PAL U., LI X., WANG T., MONTGOMERY R.R., RAMAMOORTHI N., DESILVA A.M., BAO F., YANG X., PYPAERT M., PRADHAN D., KANTOR F.S., TELFORD S., ANDERSON J.F., FIKRIG E. 2004b: TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119: 457-468 Go to original source... Go to PubMed...
    94. PAL U., YANG X., CHEN M., BOCKENSTEDT L.K., ANDERSON J.F., FLAVELL R.A., NORGARD M.V., FIKRIG E. 2004a: OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest. 113: 220-230 Go to original source... Go to PubMed...
    95. PARVEEN N., CAIMANO M., RADOLF J.D., LEONG J.M. 2003: Adaptation of the Lyme disease spirochaete to the mammalian host environment results in enhanced glycosaminoglycan and host cell binding. Mol. Microbiol. 47: 1433-1444 Go to original source... Go to PubMed...
    96. PARVEEN N., LEONG J.M. 2000: Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35: 1220-1234 Go to original source... Go to PubMed...
    97. PARVEEN N., ROBBINS D., LEONG J.M. 1999: Strain variation in glycosaminoglycan recognition influences cell-type-specific binding by Lyme disease spirochetes. Infect. Immun. 67: 1743-1749 Go to original source... Go to PubMed...
    98. PERSING D.H., MATHIESEN D., PODZORSKI D., BARTHOLD A.W. 1994: Genetic stability of Borrelia burgdorferi recovered from chronically infected immunocompetent mice. Infect. Immun. 62: 3521-3527 Go to original source... Go to PubMed...
    99. PICKEN R.N., CHENG Y., STRLE F., PICKEN M.M. 1996: Patient isolates of Borrelia burgdorferi sensu lato with genomic and phenotypic similarities of strain 25015. J. Infect. Dis. 174: 1112-1115 Go to original source... Go to PubMed...
    100. POSTIC D., RAS N.M., LANE R.S., HENDSON M., BARANTON G. 1998: Expanded diversity among Californian Borrelia isolates and description of Borrelia bissettii sp. nov. (formerly Borrelia group DN127). J. Clin. Microbiol. 36: 3497-3504 Go to original source... Go to PubMed...
    101. PROBERT W.S., KIM J.H., HOeOeK M., JOHNSON B.J.B. 2001: Mapping the ligand-binding region of Borrelia burgdorferi fibronectin-binding protein BBK32. Infect. Immun. 69: 4129-4133 Go to original source... Go to PubMed...
    102. PURSER J.E., NORRIS S.J. 2000: Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc. Natl. Acad. Sci. U.S.A. 97: 13865-13870 Go to original source... Go to PubMed...
    103. QIU W.G., DYKHUIZEN D.E., ACOSTA M.S., LUFT B.J. 2002: Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the Northeastern United States. Genetics 16: 833-849 Go to original source...
    104. QIU W.G., SCHUTZER S.E., BRUNO J.F., ATTIE O., XU Y., DUNN J.J., FRASER C.M., CASJENS S.R., LUFT B.J. 2004: Genetic exchange and plasmid transfers in Borrelia burgdorferi sensu stricto revealed by three-way genome comparisons and multilocus sequence typing. Proc. Natl. Acad. Sci. U.S.A. 101:14150-14155 Go to original source... Go to PubMed...
    105. REGO R.O.M., HAJDUSEK O., KOVAR V., KOPACEK P., GRUBHOFFER L., HYPSA V. 2005a: Molecular cloning and comparative analysis of fibrinogen-related proteins from the soft tick Ornithodoros moubata and the hard tick Ixodes ricinus. Insect Biochem. Mol. Biol. 35: 991-1000 Go to original source... Go to PubMed...
    106. REGO R.O.M., KOVAR V., KOPACEK P., WEISE C., MAN P., SAUMAN I., GRUBHOFFER L. 2005b: The tick plasma lectin, Dorin M, is a fibrinogen-related molecule. Insect Biochem. Mol. Biol. (In press.)
    107. RIBEIRO J.M.C., MATHER T.N., PIESMAN J., SPIELMAN A. 1987: Dissemination and salivary gland delivery of Lyme disease spirochetes in vector ticks (Acari, Ixodidae). J. Med. Entomol. 24: 201-205 Go to original source... Go to PubMed...
    108. RICHTER D., SCHLEE D.B., ALLGOWER R., MATUSCHKA F.R. 2004: Relationships of a novel Lyme disease spirochete, Borrelia spielmani sp. nov., with its hosts in Central Europe. Appl. Environ. Microbiol. 70: 6414-6419 Go to original source... Go to PubMed...
    109. RIJPKEMA S.G., TAZELAARD D., MOLKENBOER M., NOORDHOEK G., PLANTINGA G., SCHOULS L., SCHELLEKENS J. 1997: Detection of Borrelia afzelii, Borrelia burgdorferi sensu stricto, Borrelia garinii and group VS116 by PCR in skin biopsies of patients with erythema migrans and acrodermatitis chronica atrophicans. Clin. Microbiol. Infect. 3: 109-116 Go to original source... Go to PubMed...
    110. RITTIG M.G., KUHN K.-H., DECHANT C.A., GAUCKLER A., MODOLELL M., RICCIARDI-CASTAGNOLI P., KRAUSE I.A., BURMESTER G.R. 1996: Phagocytes from both vertebrate and invertebrate species use "coiling" phagocytosis. Dev. Comp. Immunol. 20: 393-406 Go to original source... Go to PubMed...
    111. RUDEL T., SCHEURERPFLUG I., MEYER T.F. 1995: Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373: 357-359 Go to original source... Go to PubMed...
    112. RUDENKO N., GOLOVCHENKO M., GRUBHOFFER L. 1999: Lectin-like sequences in genome of Borrelia burgdorferi. Folia Parasitol. 46: 81-90 Go to PubMed...
    113. RUDENKO N., GOLOVCHENKO M., GRUBHOFFER L. 2001: Lectin of Borrelia burgdorferi, a new factor of spirochetal virulence? Rev. Infect. Dis. (Suppl. 3): 102-104
    114. RUDOLF I., HUBALEK Z. 2003: Effect of the salivary gland and midgut extracts from Ixodes ricinus and Dermacentor reticulatus (Acari: Ixodidae) on the growth of Borrelia garinii in vitro. Folia Parasitol. 50:159-160 Go to original source... Go to PubMed...
    115. RUZIC-SABLJIC E., LOTRIC-FURLAN S., MARASPIN V., CIMPERMAN J., PLETERSKI-RIGLER D., STRLE F. 2001: Analysis of Borrelia sensu lato isolated from cerebrospinal fluid. APMIS 109: 707-713 Go to original source... Go to PubMed...
    116. RYFFEL K., PETER O., RUTTI B., SUARD A., DAYER E. 1999: Scored antibody reactivity determined by immunoblotting shows an association between clinical manifestations and presence of Borrelia burgdorferi sensu stricto, B. garinii, B. afzelii, and B. valaisiana in humans. J. Clin. Microbiol. 37: 4086-4092 Go to original source... Go to PubMed...
    117. SAMBRI V., MASSARIA F., ARDIZZONI M., STEFANELLI C., CEVENINI R. 1993: Glycoprotein patterns in Borrelia spp. Zentralbl. Bakteriol. 279: 330-335 Go to original source... Go to PubMed...
    118. SAMBRI V., STEFANELLI C., CEVENINI R. 1992: Detection of glycoproteins in Borrelia burgdorferi. Arch. Microbiol. 157: 205-208 Go to original source... Go to PubMed...
    119. SCHAeFFER C., GRANINGER M., MESSNER P. 2001: Prokaryotic glycosylation. Proteomics 1: 248-261 Go to original source... Go to PubMed...
    120. SCHROeDER N.W.J., SCHOMBEL U., HEINE H., GOeBEL U.B., ZAeHRINGER U., SCHUMANN R.R. 2003: Acylated cholesteryl galactoside as a novel immunogenic motif in Borrelia burgdorferi sensu stricto. J. Biol. Chem. 278: 33645-33653 Go to original source... Go to PubMed...
    121. SCHWAN T.G., PIESMAN J. 2002: Vector interaction and molecular adaptation of Lyme disease and relapsing fever spirochetes associated with transmission by ticks. Emerg. Infect. Dis. 2: 15-21 Go to original source... Go to PubMed...
    122. SCHWAN T.G., PIESMAN J., GOLDE W.T., DOLAN M.N., ROSA P.A. 1995: Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. U.S.A. 92: 2909-2913 Go to original source... Go to PubMed...
    123. SEINOST G., DYKHUIZEN D.E., DATTWYLER R.J., GOLDE W.T., DUNN J.J., WANG I.N., WORMSER G.P., SCHRIEFER M.E., LUFT B.J. 1999: Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect. Immun. 67: 3518-3524 Go to original source... Go to PubMed...
    124. SHOBERG R.J., THOMAS D.D. 1995: Borrelia burgdorferi vesicle production occurs via a mechanism independent of immunoglobulin M involvement. Infect. Immun. 63: 4857-4861 Go to original source... Go to PubMed...
    125. SLAVICKOVA K. 2004: [Interaction of Ixodes ricinus tick haemocytes with Lyme borreliosis spirochetes and characterization of the glycan structures of ticks salivary glands.] MSc Thesis, University of South Bohemia, Ceske Budejovice, Czech Republic, 51 pp. (In Czech, unpubl.)
    126. STANEK G. 1997: Biology of Borrelia burgdorferi, risk of infection with Lyme borreliosis. In: J. Sus and O. Kahl (Eds.), Tick-borne Encephalitis and Lyme Borreliosis. Pabst Scientific Publications, Germany, pp. 230- 237
    127. STOITSOVA S.R., GRUBHOFFER L., NEBESAROVA J. 2003: Exposed and hidden lectin-binding epitopes at the surface of Borrelia burgdorferi. Folia Microbiol. 48: 654- 658 Go to original source... Go to PubMed...
    128. STRLE F., PICKEN R.N., CHENG Y., CIMPERMAN J., MARASPIN V., LOTRIC-FURLAN S., RUZICSABLJIC E., PICKEN M.M. 1997: Clinical findings for patients with Lyme borreliosis caused by Borrelia burgdorferi sensu lato with genomic and phenotypic similarities of strain 25015. Clin. Infect. Dis. 25: 273-280 Go to original source... Go to PubMed...
    129. SWARTLEY J.S., MARFIN A.A., EDUPUGASTI S., LIU L.J., CIESLAK P., PERKINS B., WENGER J.D., STEPHENS D.S. 1997: Capsule switching of Neisseria meningitidis. Proc. Natl. Acad. Sci. U.S.A. 94: 271-276 Go to original source... Go to PubMed...
    130. SZCZEPANSKI A., FURIE M.B., BENACH J.L., LANE B.P., FLEIT H.B. 1990: Interaction between Borrelia burgdorferi and endothelium in vitro. J. Clin. Invest. 85: 1637-1647 Go to original source... Go to PubMed...
    131. TAKADA N., MASUZAWA T., ISHIGURO F., FUJITA H., KUDEKEN M., MITANI H., FUKUNAGA M., TSUCHIYA K., YANO Y., MA X.-H. 2001: Lyme disease Borrelia spp. in ticks and rodents from northwestern China. Appl. Environ. Microbiol. 67: 5161-5165 Go to original source... Go to PubMed...
    132. TENOVER F.C., ARBEIT R.D., GOERING R.V., MICKELSEN P.A., MURRAY B.E., PERSING D.H., SWAMINATHAN B. 1995: Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33: 2233-2239 Go to original source... Go to PubMed...
    133. UHLIR J., GRUBHOFFER L., BORSKY I., DUSBABEK F. 1994: Antigens and glycoproteins of larvae, nymphs and adults of the tick Ixodes ricinus. Med. Vet. Entomol. 8: 141-150 Go to original source... Go to PubMed...
    134. UHLIR J., GRUBHOFFER L., VOLF P. 1996: Novel agglutinin in the midgut of the tick Ixodes ricinus. Folia Parasitol. 43: 233-239 Go to PubMed...
    135. ULBRANDT N.D., CASSATT D.R., PATEL N.K., ROBERTS W.C., BACHY C.M., FAYENBAKER C.A., HANSON M.S. 2001: Conformational nature of the Borrelia burgdorferi decorin binding protein A epitopes that elicit protective antibodies 69. Infect. Immun. 69: 4799- 4807 Go to original source... Go to PubMed...
    136. VAN DAM A., KUIPER H., VOS K., WIDJOJOKUSUMO A., DE JONGH B., SPANJAARD L., RAMSELLAR A., KRAMER M., DANKERT J. 1993: Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestation of Lyme borreliosis. Clin. Infect. Dis. 17: 708-717 Go to original source... Go to PubMed...
    137. VANCOVA M., NEBESAROVA J., GRUBHOFFER L. 2005: Lectin-binding characteristics of a Lyme borreliosis spirochete Borrelia burgdorferi sensu stricto. Folia Microbiol. 50: 229-238 Go to original source... Go to PubMed...
    138. VASTA G.R., MARCHALONIS J.J. 1983: Humoral recognition factors in the arthropods. The specificity of chelicerate serum lectins. Am. Zool. 23: 157-171 Go to original source...
    139. WALKER A.R., FLETCHER J.D. 1990: Rhipicephalus appendiculatus feeding on rabbits and cattle: salivary-gland responses to varying host resistance. Exp. Appl. Acarol. 8: 285-290 Go to original source... Go to PubMed...
    140. WANG G., VAN DAM A.P., DANKERT J. 1999: Phenotypic and genetic characterization of a novel Borrelia burgdorferi sensu lato isolate from patient with Lyme borreliosis. J. Clin. Microbiol. 37: 3025-3028 Go to original source... Go to PubMed...
    141. WATT D.M., WALKER A.R., LAMZA K.A., AMBROSE N.C. 2001: Tick-Theileria interactions in response to immune activation of the vector. Exp. Parasitol. 97: 89-94 Go to original source... Go to PubMed...
    142. WEBER K. 2001: Aspects of Lyme borreliosis in Europe. Eur. J. Clin. Microbiol. Dis. 20: 6-13 Go to original source...
    143. WEBER K., PFISTER H.-W. 1993: History of Lyme borreliosis in Europe, In: K. Weber and W. Burgdorfer (Eds.), Aspects of Lyme Borreliosis. Springer-Verlag KG, Berlin, Germany, pp. 1-20 Go to original source...
    144. WELKOS S.L. 1991: Plasmid-associated virulence factors of non-toxigenic (pX01-) Bacillus anthracis. Microb. Pathog. 10: 183-198 Go to original source... Go to PubMed...
    145. ZEIDNER N.S., NUNCIO M.S., SCHNEIDER B.S., GERN L., PIESMAN J., BRANDAO O., FILIPE A.R. 2001: A Portuguese isolate of Borrelia lusitaniae induces disease in C3H/HeN mice. J. Med. Microbiol. 50: 1055-1060 Go to original source... Go to PubMed...
    146. ZUNG J.L., LEWENGRUB S., RUDZINSKA M.A. 1989: Fine structural evidence for the penetration of the Lyme disease spirochete Borrelia burgdorferi through the gut and salivary tissues of Ixodes dammini. Can. J. Zool. 67: 1737-1748 Go to original source...

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