Borrelia pathogenesis research in the post-genomic and post-vaccine era

Current Opinion in Microbiology

Volumn 3, Issue 1, 2000, Pages 86-92

  Nordstrand, Annika ^a   Barbour, Alan G ^b   Bergström, Sven ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYME DISEASE VACCINE;

BACTERIAL GENE; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; BORRELIA INFECTION; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; LYME DISEASE; NONHUMAN; PATHOGENESIS; REVIEW;

BACTERIA (MICROORGANISMS); BORRELIA; BORRELIA BURGDORFERI;

EID: 0033952252     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(99)00056-9     Document Type: Review

References (71)

1. Fraser C.M., Casjens S., Huang W.M., Sutton G.G., Clayton R., Lathigra R., White O., Ketchum K.A., Dodson R., Hickey E.k.et al. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature. 390:1997;580-586.
2. Casjens S., Palmer N., van Vugt R., Huang W-M., Stevenon B., Rosa P., Lathigra R., Sutton G., Peterson J., Dodson R.J.et al. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol. 2000;. in press. This study completed the sequencing and analysis of all the plasmids of B. burgdorferi.
3. •].
4. •] of OspA vaccine in endemic areas demonstrated 70-90% efficacy after three immunizations.
5. Casjens S. Evolution of the linear DNA replicons of the Borrelia spirochetes. Curr Opin Microbiol. 2:1999;529-534.
6. Seiler K.P., Weis J.J. Immunity to Lyme disease: protection, pathology and persistence. Curr Opin Immunol. 8:1996;502-509.
7. Sigal L.H. Lyme disease: a review of aspects of its immunity and immunopathogenesis. Annu Rev Immunol. 15:1997;63-92.
8. Schwan T.G., Piesman J., Golde W.T., Dolan M.C., Rosa P.A. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci USA. 92:1995;2909-2913.
9. Schwan T.G., Hinnebusch B.J. Bloodstream-versus tick-associated variants of a relapsing fever bacterium. Science. 280:1998;1938-1940. This paper demonstrates how the expression of different surface proteins depends on whether they are in the tick vector or the mammalian host. An OspC paralog of B. hermsii is expressed in the tick but not in the host. Another protein is expressed in the mammalian host but not in the tick.
10. de Silva A.M., Fikrig E. Arthropod- and host-specific gene expression by Borrelia burgdorferi. J Clin Invest. 99:1997;377-379.
11. de Silva A.M., Zeidner N.S., Zhang Y., Dolan M.C., Piesman J., Fikrig E. Influence of outer surface protein A antibody on Borrelia burgdorferi within feeding ticks. Infect Immun. 67:1999;30-35. This is one of several papers by de Silva, Fikrig, and colleagues that demonstrated differences in expression of different B. burgdorferi proteins in the tick and in the mammalian host.
12. Akin E., McHugh G.L., Flavell R.A., Fikrig E., Steere A.C. The immunoglobulin (IgG) antibody response to OspA and OspB correlates with severe and prolonged Lyme arthritis and the IgG response to P35 correlates with mild and brief arthritis. Infect Immun. 67:1999;173-181.
13. Padula S.J., Dias F., Sampieri A., Craven R.B., Ryan R.W. Use of recombinant OspC from Borrelia burgdorferi for serodiagnosis of early Lyme disease. J Clin Microbiol. 32:1994;1733-1738.
14. Wilske B., Jauris-Heipke S., Lobentanzer R., Pradel I., Preac-Mursic V., Rössler D., Soutschek E., Johnson R.C. Phenotypic analysis of outer surface protein C (OspC) of Borrelia burgdorferi sensu lato by monoclonal antibodies: relationship to genospecies and OspA serotype. J Clin Microbiol. 33:1995;103-109.
15. Wang I.N., Dykhuizen D.E., Qiu W., Dunn J.J., Bosler E.M., Luft B.J. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics. 151:1999;15-30.
16. Sohaskey C.D., Zuckert W.R., Barbour A.G. The extended promoters for two outer membrane lipoprotein genes of Borrelia spp. uniquely include a T-rich region. Mol Microbiol. 33:1999;41-51.
17. Bunikis J., Luke C.J., Bunikiene E., Bergström S., Barbour A.G. A surface-exposed region of a novel outer membrane protein (P66) of Borrelia spp. is variable in size and sequence. J Bacteriol. 180:1998;1618-1623.
18. Bunikis J., Barbour A.G. Access of antibody or trypsin to an integral outer membrane protein (P66) of Borrelia burgdorferi is hindered by Osp lipoproteins. Infect Immun. 67:1999;2874-2883. OspA and other outer membrane lipoproteins hinder access of antibodies and proteases to an integral membrane protein of B. burgdorferi.
19. Finlay B.B., Cossart P. Exploitation of mammalian host cell functions by bacterial pathogens. Science. 276:1997;718-725.
20. 3 on human platelets. Infect Immun. 62:1994;5559-5567.
21. 1 mediate attachment of Lyme disease spirochetes to human cells. Infect Immun. 66:1998;1946-1952.
22. Leong J.M., Morrissey P.E., Ortega-Barria E., Pereira M.E., Coburn J. Hemagglutination and proteoglycan binding by the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun. 63:1995;874-883.
23. Guo B.P., Norris S.J., Rosenberg L.C., Hook M. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect Immun. 63:1995;3467-3472.
24. Leong J.M., Robbins D., Rosenfeld L., Lahiri B., Parveen N. Structural requirements for glycosaminoglycan recognition by the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun. 66:1998;6045-6048.
25. Leong J.M., Wang H., Magoun L., Field J.A., Morrissey P.E., Robbins D., Tatro J.B., Coburn J., Parveen N. Different classes of proteoglycans contribute to the attachment of Borrelia burgdorferi to cultured endothelial and brain cells. Infect Immun. 66:1998;994-999.
26. Parveen N., Robbins D., Leong J.M. Strain variation in glycosaminoglycan recognition influences cell-type-specific binding by lyme disease spirochetes. Infect Immun. 67:1999;1743-1749.
27. Burman N., Shamaei-Tousi A., Bergström S. The spirochete Borrelia crocidurae causes erythrocyte rosetting during relapsing fever. Infect Immun. 66:1998;815-819. This paper describes the aggregation of erythrocytes on B. crocidurae and discusses a new immune evasion strategy employed by this spirochete.
28. Duray P.H. Target organs of Borrelia burgdorferi infections: functional responses and histology. Schutzer S.E. Lyme Disease: Molecular and Immunologic Approaches, vol 6. 1992;11-30 Cold Spring Harbor Press, Plainview.
29. Hanson M.S., Cassatt D.R., Guo B.P., Patel N.K., McCarthy M.P., Dorward D.W., Hook M. Active and passive immunity against Borrelia burgdorferi decorin binding protein A (DbpA) protects against infection. Infect Immun. 66:1998;2143-2153.
30. Hagman K.E., Lahdenne P., Popova T.G., Porcella S.F., Akins D.R., Radolf J.D., Norgard M.V. 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. 66:1998;2674-2683.
31. Cassatt D.R., Patel N.K., Ulbrandt N.D., Hanson M.S. DbpA, but not OspA, is expressed by Borrelia burgdorferi during spirochetemia and is a target for protective antibodies. Infect Immun. 66:1998;5379-5387.
32. Guo B.P., Brown E.L., Dorward D.W., Rosenberg L.C., Hook M. Decorin binding adhesins from Borrelia burgdorferi. Mol Microbiol. 30:1998;711-723. The genes for two decorin binding proteins, DbpA and DbpB, were cloned and sequenced, and properties of the proteins were characterized. The study shows that the proteins are surface exposed and can mediate attachment to a fibroblast matrix using decorin as a ligand. The authors propose that Dbps are adhesins of B. burgdorferi that belong to the MSCRAMM family and mediate attachment to the extracellular matrix of the host.
33. Klempner M.S., Noring R., Rogers R.A. Invasion of human skin fibroblasts by the Lyme disease spirochete, Borrelia burgdorferi. J Infect Dis. 167:1993;1074-1081.
34. Grab D.J., Givens C., Kennedy R. Fibronectin-binding activity in Borrelia burgdorferi. Biochim Biophys Acta. 1407:1998;135-145.
35. Grab D.J., Lanners H-N., Martin L.N., Chesney J., Cai C., Adkisson H.D., Bucala R. Interaction of Borrelia burgdorferi with peripheral blood fibrocytes, antigen-presenting cells with the potential for connective tissue targeting. Mol Med. 5:1999;46-54.
36. th General Meeting of the American Society for Microbiology: 1997 May 4-8. 1997;D-133 ASM Press, Miami Beach, FL, Washington, DC.
37. Montgomery R.R., Malawista S.E. Entry of Borrelia burgdorferi into macrophages is end-on and leads to degradation in lysosomes. Infect Immun. 64:1996;2867-2872.
38. Rittig M.G., Jagoda J.C., Wilske B., Murgia R., Cinco M., Repp R., Burmester G.R., Krause R. Coiling phagocytosis discriminates between different spirochetes and is enhanced by phorbol myristate acetate and granulocyte-macrophage colony-stimulating factor. Infect Immun. 66:1998;627-635.
39. Suhonen J., Hartiala K., Viljanen M.K. Tube phagocytosis, a novel way for neutrophils to phagocytize Borrelia burgdorferi. Infect Immun. 66:1998;3433-3435.
40. Zhang J.R., Hardham J.M., Barbour A.G., Norris S.J. Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell. 89:1997;275-285.
41. Zhang J.R., Norris S.J. Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect Immun. 66:1998;3689-3697.
42. Zhang J.R., Norris S.J. Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect Immun. 66:1998;3698-3704. This paper, together with [40,41], describes the novel finding of vmp-like antigenic variation in the Lyme disease agent Borrelia burgdorferi.
43. Kang I., Barthold S.W., Persing D.H., Bockenstedt L.K. T-helper-cell cytokines in the early evolution of murine Lyme arthritis. Infect Immun. 65:1997;3107-3111.
44. Straubinger R.K., Straubinger A.F., Harter L., Jacobson R.H., Chang Y.F., Summers B.A., Erb H.N., Appel M.J. Borrelia burgdorferi migrates into joint capsules and causes an up-regulation of interleukin-8 in synovial membranes of dogs experimentally infected with ticks. Infect Immun. 65:1997;1273-1285.
45. Cadavid D., Barbour A.G. Neuroborreliosis during relapsing fever: review of the clinical manifestations, pathology, and treatment of infections in humans and experimental animals. Clin Infect Dis. 26:1998;151-164. This review includes many articles from before 1970 that are not easily accessible through computer searches. These early clinical and experimental studies showed that neuroinvasion and neurological complications are as common with tick-borne relapsing fever as with Lyme borreliosis.
46. Garcia-Monco J.C., Miller N.S., Backenson P.B., Anda P., Benach J.L. A mouse model of Borrelia meningitis after intradermal injection. J Infect Dis. 175:1997;1243-1245.
47. Cadavid D., Thomas D.D., Crawley R., Barbour A.G. Variability of a bacterial surface protein and disease expression in a possible mouse model of systemic Lyme borreliosis. J Exp Med. 179:1994;631-642.
48. Pennington P.M., Allred C.D., West C.S., Alvarez R., Barbour A.G. Arthritis severity and spirochete burden are determined by serotype in the Borrelia turicatae-mouse model of Lyme disease. Infect Immun. 65:1997;285-292.
49. Pennington P.M., Cadavid D., Barbour A.G. Characterization of VspB of Borrelia turicatae, a major outer membrane protein expressed in blood and tissues of mice. Infect Immun. 67:1999;4637-4645.
50. Pennington P.M., Cadavid D., Bunikis J., Norris S.J., Barbour A.G. Extensive interplasmidic duplications change the virulence phenotype of the relapsing fever agent Borrelia turicatae. Mol Microbiol. 34:1999;1120-1132.
51. Cadavid D., Pennington P.M., Kerentseva T.A., Bergström S., Barbour A.G. Immunologic and genetic analyses of VmpA of a neurotropic strain of Borrelia turicatae. Infect Immun. 65:1997;3352-3360.
52. Boyle M.D.P., Lottenberg R. Plasminogen activation by invasive human pathogens. Thromb Haemost. 77:1997;1-10.
53. Fuchs H., Wallich R., Simon M.M., Kramer M.D. The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc Natl Acad Sci USA. 91:1994;12594-12598.
54. Coleman J.L., Sellati T.J., Testa J.E., Kew R.R., Furie M.B., Benach J.L. Borrelia burgdorferi binds plasminogen, resulting in enhanced penetration of endothelial monolayers. Infect Immun. 63:1995;2478-2484.
55. Coleman J.L., Roemer E.J., Benach J.L. Plasmin-coated Borrelia burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect Immun. 67:1999;3929-3936.
56. Coleman J.L., Gebbia J.A., Piesman J., Degen J.L., Bugge T.H., Benach J.L. Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell. 89:1997;1111-1119.
57. Gebbia J.A., Monco J.C., Degen J.L., Bugge T.H., Benach J.L. The plasminogen activation system enhances brain and heart invasion in murine relapsing fever borreliosis. J Clin Invest. 103:1999;81-87. The authors tested the hypothesis that invasion in the mammalian host is dependent upon or enhanced by the utilization of host-derived plasminogen by the spirochete. Transgenic mice allowed for testing the in vivo relevance of in vitro observations regarding plasminogen acquisition by spirochetes.
58. Shamaei-Tousi A., Martin P., Bergh A., Burman N., Brännström T., Bergström S. Erythrocyte aggregating relapsing fever Borrelia crocidurae induces microemboli formation. J Infect Dis. 180:1999;1929-1938. In this study, the pathological effects of erythrocyte rosetting by the relapsing fever spirochete B. crocidurae were investigated. The presence of extravascular B. crocidurae indicates a novel route for these bacteria to spread in the mammalian host.
59. Radolf J.D., Arndt L.L., Akins D.R., Curetty L.L., Levi M.E., Shen Y., Davis L.S., Norgard M.V. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J Immunol. 154:1995;2866-2877.
60. Vidal V., Scragg I.G., Cutler S.J., Rockett K.A., Fekade D., Warrell D.A., Wright D.J., Kwiatkowski D. Variable major lipoprotein is a principal TNF-inducing factor of louse-borne relapsing fever. Nat Med. 4:1998;1416-1420.
61. Rittig M.G., Häupl T., Krause A., Kressel M., Groscurth P., Burmester G.R. Borrelia burgdorferi-induced ultrastructural alterations in human phagocytes: a clue to pathogenicity? J Pathol. 173:1994;269-282.
62. Sprenger H., Krause A., Kaufmann A., Priem S., Fabian D., Burmester G.R., Gemsa D., Rittig M.G. Borrelia burgdorferi induces chemokines in human monocytes. Infect Immun. 65:1997;4384-4388.
63. Ebnet K., Simon M.M., Shaw S. Regulation of chemokine gene expression in human endothelial cells by proinflammatory cytokines and Borrelia burgdorferi. Ann NY Acad Sci. 797:1996;107-117.
64. Wooten R.M., Modur V.R., McIntyre T.M., Weis J.J. Borrelia burgdorferi outer membrane protein A induces nuclear translocation of nuclear factor-κB and inflammatory activation in human endothelial cells. J Immunol. 157:1996;4584-4590.
65. Wooten R.M., Morrison T.B., Weis J.H., Wright S.D., Thieringer R., Weis J.J. The role of CD14 in signaling mediated by outer membrane lipoproteins of Borrelia burgdorferi. J Immunol. 160:1998;5485-5492. The findings of this study, using HUVEC and neutrophils, suggest that CD14 plays a role in facilitating lipoprotein-mediated signaling by B. burgdorferi in mammalian cells. As CD14 appears not to be the receptor directly responsible for transducing lipoprotein-mediated signaling, is was suggested that lipoproteins shuttled to cell membranes, where they can subsequently interact with the ligand-specific receptor(s).
66. Sellati T.J., Bouis D.A., Kitchens R.L., Darveau R.P., Pugin J., Ulevitch R.J., Gangloff S.C., Goyert S.M., Norgard M.V., Radolf J.D. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J Immunol. 160:1998;5455-5464. The report demonstrates that activation of monocytic cells by spirochetal lipoproteins and lipopeptides proceeds predominantly via CD14, although a CD14-independent pathway also was discernible. These spirochetal constituents use a CD14-dependent pathway that differs in at least two fundamental respects from the lipopolysaccharide recognition pathway.
67. Giambartolomei G.H., Dennis V.A., Lasater B.L., Phillipp M.T. Induction of pro- and antiinflammatory cytokines by Borrelia burgdorferi lipoproteins in monocytes is mediated by CD14. Infect Immun. 67:1999;140-147.
68. Sellati T.J., Bouis D.A., Caimano M.J., Feulner J.A., Ayers C., Lien E., Radolf J.D. 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. 163:1999;2049-2056.
69. Giambartolomei G.H., Dennis V.A., Philipp M.T. Borrelia burgdorferi stimulates the production of interleukin-10 in peripheral blood mononuclear cells from uninfected humans and rhesus monkeys. Infect Immun. 66:1998;2691-2697.
70. Hirschfeld M., Kirschning C.J., Schwandner R., Wesche H., Weis J.H., Wooten R.M., Weis J.J. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol. 163:1999;2382-2386. Transfection of Toll-like receptor 2 (TLR2) into cell lines conferred responsiveness to lipoproteins, lipopeptides, and sonicated B. burgdorferi, as measured by nuclear translocation of NF-κB and cytokine production. The TLR2-dependent signaling by lipoprotein was facilitated by CD14. The widespread expression of lipoproteins by other bacterial species suggests that this interaction may have broad implications in microbial inflammation.
71. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R-B., Belisle J.T., Bleharski J.R., Maitland M., Norgard M.V., Plevy S.E., Smale S.T.et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science. 285:1999;732-736.