Quantitative analysis of Borrelia burgdorferi gene expression in naturally (tick) infected mouse strains

Medical Microbiology and Immunology

Volumn 194, Issue 1-2, 2005, Pages 81-90

  Lederer, Sharon ^a   Brenner, Christiane ^b   Stehle, Thomas ^a   Gern, Lise ^c   Wallich, Reinhard ^b   Simon, Markus M ^a  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Borrelia burgdorferi; Gene expression; Tick infection; Tissue tropism

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BORRELIA BURGDORFERI; BORRELIA INFECTION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; DOWN REGULATION; EAR; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART; IMMUNE DEFICIENCY; IMMUNE STATUS; IMMUNOCOMPETENCE; INFLAMMATION; JOINT; LYME DISEASE; MOUSE; MOUSE STRAIN; NONHUMAN; OSPC GENE; PLASMID; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPIROCHETE; SPLEEN; TICK;

ANIMALS; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; DNA, BACTERIAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; IXODES; LYME DISEASE; MICE; MICE, INBRED AKR; MICE, INBRED BALB C; MICE, SCID; ORGAN SPECIFICITY; POLYMERASE CHAIN REACTION;

EID: 11244308148     PISSN: 03008584     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00430-004-0218-1     Document Type: Article

References (67)

1. Akins DR, Porcella SF, Popova TG, Shevchenko D, Baker SI, Li M, Norgard MV, Radolf JD (1995) Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homologue. Mol Microbiol 18:507-520
2. Akins DR, Bourell KW, Caimano MJ, Norgard MV, Radolf JD (1998) A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J Clin Invest 101:2240-2250
3. Anderson JF (1989) Epizootiology of Borrelia in Ixodes tick vectors and reservoir hosts. Rev Infect Dis 11:1451-1459
4. Backenson PB, Coleman JL, Benach JL (1995) Borrelia burgdorferi shows specificity of binding to glycosphingolipids. Infect Immun 63:2811-2817
5. Barthold SW, Bockenstedt LK (1993) Passive immunizing activity of sera from mice infected with Borrelia burgdorferi. Infect Immun 61:4696-4702
6. Brooks CS, Hefty PS, Jolliff SE, Akins DR (2003) Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect Immun 71:3371-3383
7. Brown CR, Reiner SL (1999) Experimental Lyme arthritis in the absence of interleukin-4 or gamma interferon. Infect Immun 67:3329-3333
8. Brown CR, Reiner SL (1999) Genetic control of experimental Lyme arthritis in the absence of specific immunity. Infect Immun 67:1967-1973
9. Brown JP, Zachary JF, Teuscher C, Weis JJ, Wooten RM (1999) Dual role of interleukin-10 in murine Lyme disease: regulation of arthritis severity and host defense. Infect Immun 67:5142-5150
10. Champion CI, Blanco DR, Skare JT, Haake DA, Giladi M, Foley D, Miller JN, Lovett MA (1994) A 9.0-kilobase-pair circular plasmid of Borrelia burgdorferi encodes an exported protein: evidence for expression only during infection. Infect Immun 62:2653-2661
11. Coburn J, Magoun L, Bodary SC, Leong JM (1998) Integrins alpha5beta3 and alpha5beta1 mediate attachment of Lyme disease spirochetes to human cells. Infect Immun 66:1946-1952
12. Coleman JL, Gebbia JA, Piesman J, Degen JL, Bugge TH, Benach JL (1997) Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89:1111-1119
13. Crowley H, Huber BT (2003) Host-adapted Borrelia burgdorferi in mice expresses OspA during inflammation. Infect Immun 71:4003-4010
14. Das S, Barthold SW, Giles SS, Montgomery RR, Telford SR 3rd, Fikrig E (1997) Temporal pattern of Borrelia burgdorferi p21 expression in ticks and the mammalian host. J Clin Invest 99:987-995
15. de Silva AM, Fikrig E (1997) Arthropod- and host-specific gene expression by Borrelia burgdorferi. J Clin Invest 99:377-379
16. de Silva AM, Telford SR 3rd, Brunet LR, Barthold SW, Fikrig E (1996) Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine. J Exp Med 183:271-275
17. Feng S, Hodzic E, Stevenson B, Barthold SW (1998) Humoral immunily to Borrelia burgdorferi N40 decorin binding proteins during infection of laboratory mice. Infect Immun 66:2827-2835
18. Feng S, Hodzic E, Barthold SW (2000) Lyme arthritis resolution with antiserum to a 37-kilodalton Borrelia burgdorferi protein. Infect Immun 68:4169-4173
19. Fikrig E, Feng W, Barthold SW, Telford SR 3rd, Flavell RA (2000) Arthropod- and host-specific Borrelia burgdorferi bbk32 expression and the inhibition of spirochete transmission. J Immunol 164:5344-5351
20. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb JF, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, van Vugt R, Palmer N, Adams MD, Gocayne J, Venter JC, et al (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586
21. Fuchs H, Wallich R, Simon MM, Kramer MD (1994) The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc Natl Acad Sci USA 91:12594-12598
22. Gern L, Toutoungi LN, Hu CM, Aeschlimann A (1991) Ixodes (Pholeoixodes) hexagonus, an efficient vector of Borrelia burgdorferi in the laboratory. Med Vet Entomol 5:431-435
23. Gern L, Schaible UE, Simon MM (1993) Mode of inoculation of the Lyme disease agent Borrelia burgdorferi influences infection and immune responses in inbred strains of mice. J Infect Dis 167:971-975
24. Gilmore RD Jr, Mbow ML, Stevenson B (2001) Analysis of Borrelia burgdorferi gene expression during life cycle phases of the tick vector Ixodes scapularis. Microbes Infect 3:799-808
25. Golde WT, Kappel KJ, Dequesne G, Feron C, Plainchamp D, Capiau C, Lobet Y (1994) Tick transmission of Borrelia burgdorferi to inbred strains of mice induces an antibody response to P39 but not to outer surface protein A. Infect Immun 62:2625-2627
26. Grab DJ, Givens C, Kennedy R (1998) Fibronectin-binding activity in Borrelia burgdorferii. Biochim Biophys Acta 1407:135-145
27. Hodzic E, Feng S, Freet KJ, Borjesson DL, Barthold SW (2002) Borrelia burgdorferi population kinetics and selected gene expression at the host-vector interface. Infect Immun 70:3382-3388
28. Hodzic E, Feng S, Freet KJ, Barthold SW (2003) Borrelia burgdorferi population dynamics and prototype gene expression during infection of immunocompetent and immunodeficient mice. Infect Immun 71:5042-5055
29. Isaacs RD (1994) Borrelia burgdorferi bind to epithelial cell proteoglycans. J Clin Invest 93:809-819
30. Iyer R, Kalu O, Purser J, Norris S, Stevenson B, Schwartz I (2003) Linear and circular plasmid content in Borrelia burgdorferi clinical isolates. Infect Immun 71:3699-3706
31. Kraiczy P, Skerka C, Kirschfink M, Brade V, Zipfel PF (2001) Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and Factor H. Eur J Immunol 31:1674-1684
32. Kraiczy P, Hellwage J, Skerka C, Becker H, Kirschfink M, Simon MM, Brade V, Zipfel PF, Wallich R (2004) Complement resistance of Borrelia burgdorferi correlates with expression of BbCRASP-1, a novel linear plasmid-encoded surface protein that interacts with human factor H and FHL-1 and is unrelated to Erp proteins. J Biol Chem 279:2421-2429
33. Kramer MD, Schaible UE, Wallich R, Moter SE, Petzoldt D, Simon MM (1990) Characterization of Borrelia burgdorferi associated antigens by monoclonal antibodies. Immunobiology 181:357-366
34. Lahdenne P, Porcella SF, Hagman KE, Akins DR, Popova TG, Cox DL, Katona LI, Radolf JD, Norgard MV (1997) Molecular characterization of a 6.6-kilodalton Borrelia burgdorferi outer membrane-associated lipoprotein (lp6.6) which appears to be down-regulated during mammalian infection. Infect Immun 65:412-421
35. Leong JM, Morrissey PE, Ortega-Barria E, Pereira ME, Coburn J (1995) Hemagglutination and proteoglycan binding by the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun 63:874-883
36. Liang FT, Jacobs MB, Bowers LC, Philipp MT (2002) An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J Exp Med 195:415-422
37. Liang FT, Nelson FK, Fikrig E (2002) DNA microarray assessment of putative Borrelia burgdorferi lipoprotein genes. Infect Immun 70:3300-3303
38. Liang FT, Nelson FK, Fikrig E (2002) Molecular adaptation of Borrelia burgdorferi in the murine host. J Exp Med 196:275-280
39. Ma Y, Seiler KP, Eichwald EJ, Weis JH, Teuscher C, Weis JJ (1998) Distinct characteristics of resistance to Borrelia burgdorferi-induced arthritis in C57BL/6N mice. Infect Immun 66:161-168
40. Marconi RT, Samuels DS, Garon CF (1993) Transcriptional analyses and mapping of the ospC gene in Lyme disease spirochetes. J Bacteriol 175:926-932
41. Montgomery RR, Malawista SE, Feen KJ, Bockenstedt LK (1996) Direct demonstration of antigenic substitution of Borrelia burgdorferi ex vivo: exploration of the paradox of the early immune response to outer surface proteins A and C in Lyme disease. J Exp Med 183:261-269
42. Morrison TB, Ma Y, Weis JH, Weis JJ (1999) Rapid and sensitive quantification of Borrelia burgdorferi-infected mouse tissues by continuous fluorescent monitoring of PCR. J Clin Microbiol 37:987-992
43. Nowakowski J, Schwartz I, Liveris D, Wang G, Aguero-Rosenfeld ME, Girao G, McKenna D, Nadelman RB, Cavaliere LF, Wormser GP (2001) Laboratory diagnostic techniques for patients with early Lyme disease associated with erythema migrans: a comparison of different techniques. Clin Infect Dis 33:2023-2027
44. Ohnishi J, Piesman J, de Silva AM (2001) Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc Natl Acad Sci USA 98:670-675
45. Pahl A, Kuhlbrandt U, Brune K, Rollinghoff M, Gessner A (1999) Quantitative detection of Borrelia burgdorferi by real-time PCR. J Clin Microbiol 37:1958-1963
46. Piesman J, Schneider BS, Zeidner NS (2001) Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J Clin Microbiol 39:4145-4148
47. Pietila J, He Q, Oksi J, Viljanen MK (2000) Rapid differentiation of Borrelia garinii from Borrelia afzelii and Borrelia burgdorferi sensu stricto by LightCycler fluorescence melting curve analysis of a PCR product of the recA gene. J Clin Microbiol 38:2756-2759
48. Rauter C, Oehme R, Diterich I, Engele M, Hartung T (2002) Distribution of clinically relevant Borrelia genospecies in ticks assessed by a novel, single-run, real-time PCR. J Clin Microbiol 40:36-43
49. Sadziene A, Thomas DD, Barbour AG (1995) Borrelia burgdorferi mutant lacking Osp: biological and immunological characterization. Infect Immun 63:1573-1580
50. Schaible UE, Kramer MD, Justus CW, Museteanu C, Simon MM (1989) Demonstration of antigen-specific T cells and histopathological alterations in mice experimentally inoculated with Borrelia burgdorferi. Infect Immun 57:41-47
51. Schaible UE, Kramer MD, Museteanu C, Zimmer G, Mossmann H, Simon MM (1989) The severe combined immunodeficiency (scid) mouse. A laboratory model for the analysis of Lyme arthritis and carditis. J Exp Med 170:1427-1432
52. Schaible UE, Gay S, Museteanu C, Kramer MD, Zimmer G, Eichmann K, Museteanu U, Simon MM (1990) Lyme borreliosis in the severe combined immunodeficiency (scid) mouse manifests predominantly in the joints, heart, and liver. Am J Pathol 137:811-820
53. Schaible UE, Kramer MD, Wallich R, Tran T, Simon MM (1991) Experimental Borrelia burgdorferi infection in inbred mouse strains: antibody response and association of H-2 genes with resistance and susceptibility to development of arthritis. Eur J Immunol 21:2397-2405
54. Schaible UE, Gern L, Wallich R, Kramer MD, Prester M, Simon MM (1993) Distinct patterns of protective antibodies are generated against Borrelia burgdorferi in mice experimentally inoculated with high and low doses of antigen. Immunol Lett 36:219-226
55. Schaible UE, Wallich R, Kramer MD, Gern L, Anderson JF, Museteanu C, Simon MM (1993) Immune sera to individual Borrelia burgdorferi isolates or recombinant OspA thereof protect SCID mice against infection with homologous strains but only partially or not at all against those of different OspA/OspB genotype. Vaccine 11:1049-1054
56. Schwan TG, Piesman J, Golde WT, Dolan MC, Rosa PA (1995) Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci USA 92:2909-2913
57. Sigal LH (1997) Lyme disease: a review of aspects of its immunology and immunopathogenesis. Annu Rev Immunol 15:63-92
58. Straubinger RK (2000) PCR-based quantification of Borrelia burgdorferi organisms in canine tissues over a 500-day postinfection period. J Clin Microbiol 38:2191-2199
59. Suk K, Das S, Sun W, Jwang B, Barthold SW, Flavell RA, Fikrig E (1995) Borrelia burgdorferi genes selectively expressed in the infected host. Proc Natl Acad Sci USA 92:4269-4273
60. Wallich R, Brenner C, Kramer MD, Simon MM (1995) Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo. Infect Immun 63:3327-3335
61. Wallich R, Jahraus O, Stehle T, Tran TT, Brenner C, Hofmann H, Gern L, Simon MM (2003) Artificial-infection protocols allow immunodetection of novel Borrelia burgdorferi antigens suitable as vaccine candidates against Lyme disease. Eur J Immunol 33:708-719
62. Wang G, Ojaimi C, Iyer R, Saksenberg V, McClain SA, Wormser GP, Schwartz I (2001) Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/HeJ mice. Infect Immun 69:4303-4312
63. Yang L, Weis JH, Eichwald E, Kolbert CP, Persing DH, Weis JJ (1994) Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues. Infect Immun 62:492-500
64. Zeidner NS, Schneider BS, Dolan MC, Piesman J (2001) An analysis of spirochete load, strain, and pathology in a model of tick-transmitted Lyme borreliosis. Vector Borne Zoonotic Dis 1:35-44
65. Zhang JR, Hardham JM, Barbour AG, Norris SJ (1997) Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89:275-285
66. Zhong W, Stehle T, Museteanu C, Siebers A, Gern L, Kramer M, Wallich R, Simon MM (1997) Therapeutic passive vaccination against chronic Lyme disease in mice. Proc Natl Acad Sci USA 94:12533-12538
67. Zhong W, Gern L, Stehle T, Museteanu C, Kramer M, Wallich R, Simon MM (1999) Resolution of experimental and tick-borne Borrelia burgdorferi infection in mice by passive, but not active immunization using recombinant OspC. Eur J Immunol 29:946-957