Spirochaetal lipoproteins and pathogenesis

Microbiology

Volumn 146, Issue 7, 2000, Pages 1491-1504

  Haake, David A ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bacterial outer membrane; Lipoprotein; Pathogenesis

Indexed keywords

ACYLTRANSFERASE; ANTIGEN; APOLIPOPROTEIN; BACTERIAL PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE; BINDING PROTEIN; CARRIER PROTEIN; CD14 ANTIGEN; GLOBOMYCIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPROTEIN; MEMBRANE PROTEIN; OCTOXINOL; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPID; POLYPEPTIDE ANTIBIOTIC AGENT; SCLEROPROTEIN; SIGNAL PEPTIDASE; SIGNAL RECOGNITION PARTICLE;

ADAPTATION; ANTIGENIC VARIATION; BACTERIAL GENE; BORRELIA BURGDORFERI; CONTROLLED STUDY; ESCHERICHIA COLI; GENE SEQUENCE; IMMUNE RESPONSE; IMMUNITY; INFLAMMATION; LEPTOSPIRA; LIPOPROTEIN SECRETION; NONHUMAN; OUTER MEMBRANE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SPIROCHETE; TREPONEMA PALLIDUM;

EID: 0033910411     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-146-7-1491     Document Type: Review

References (108)

1. Akins, D. R., Bourell, K. W., Caimano, M. J., Norgard, M. V. & Radolf, J. D. (1998). A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J Clin Invest 101, 2240-2250.
2. Aliprantis, A. O., Yang, R. B., Mark, M. R., Suggett, S., Devaux, B., Radolf, J. D., Kumpel, G. R., Godowski, P. & Zychlinsky, A. (1999). Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 285, 736-739.
3. Anderson, D. M. & Schneewind, O. (1999). Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol Microbiol 31, 1139-1148.
4. Barbour, A. G., Tessier, S. L. & Hayes, S. F. (1984). Variation in a major surface protein of Lyme disease spirochetes. Infect Immun 45, 94-100.
5. Barnett, J. K., Barnett, D., Bolin, C. A., Summers, T. A., Wagar, E. A., Cheville, N. F., Hartskeerl, R. A. & Haake, D. A. (1999). Expression and distribution of leptospiral outer membrane components during renal infection of hamsters. Infect Immun 67, 853-861.
6. Barthold, S. W., Beck, D. S., Hansen, G. M., Terwilliger, G. A. & Moody, K. D. (1990). Lyme borreliosis in selected strains and ages of laboratory mice. J Infect Dis 162, 133-138.
7. Belisle, J. T., Brandt, M. E., Radolf, J. D. & Norgard, M. V. (1994). Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J Bacteriol 176, 2151-2157.
8. Blanco, D. R., Reimann, K., Skare, J., Champion, C. I., Foley, D., Exner, M. M., Hancock, R. E., Miller, J. N. & Lovett, M. A. (1994). Isolation of the outer membranes from Treponema pallidum and Treponema vincentii. J Bacteriol 176, 6088-6099.
9. Brandt, M. E., Riley, B. S., Radolf, J. D. & Norgard, M. V. (1990). Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins. Infect Immun 58, 983-991.
10. Brown, E. L., Guo, B. P., O'Neal, P. & Hook, M. (1999). Adherence of Borrelia burgdorferi : identification of critical lysine residues in DhpA required for decorin binding. J Biol Chem 274, 26272-26278.
11. Brusca, J. S., McDowall, A. W., Norgard, M. V. & Radolf, J. D. (1991). Localization of outer surface proteins A and B in both the outer membrane and intracellular compartments of Borrelia burgdorferi. J Bacteriol 173, 8004-8008.
12. Bunikis, J. & Barbour, A. G. (1999). Access of antibody or trypsin to an integral outer membrane protein (P66) of Burrelia burgdorferi is hindered by Osp lipoproteins. Inject Immun 67, 2874-2883.
13. Burkot, T. R., Piesman, J. & Wirtz, R. A. (1994). Quantitation of the Borrelia burgdorferi outer surface protein A in Ixodes scapularis: fluctuations during the tick life cycle, doubling times, and loss while feeding. J Infect Dis 170, 883-889.
14. Cadavid, D., Thomas, D. D., Crawley, R. & Barbour, A. G. (1994). Variability of a bacterial surface protein and disease expression in a possible mouse model of systemic Lyme borreliosis. J Exp Med 179, 631-642.
15. Cameron, C. E., Castro, C., Lukehart, S. A. & Van Voorhis, W. C. (1998). Function and protective capacity of Treponema pallidum subsp. pallidum lycerophosphodiester phosphodiesterase. Infect Immun 66, 5763-5770.
16. Carroll, J. A., Garon, C. F. & Schwan, T. G. (1999). Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect Immun 67, 3181-3187.
17. Carter, C. J., Bergstrom, S., Norris, S. J. & Barbour, A. G. (1994). A family of surface-exposed proteins of 20 kilodaltons in the genus Borrelia. Infect Immun 62, 2792-2799.
18. Chamberlain, N. R., Brandt, M. E., Erwin, A. L., Radolf, J. D. & Norgard, M. V. (1989a). Major integral membrane protein immunogens of Treponema pallidum are proteolipids. Infect Immun 57, 2872-2877.
19. Chamberlain, N. R., DeOgny, L., Slaughter, C., Radolf, J. D. & Norgard, M. V. (1989b). Acylation of the 47-kilodalton major membrane immimogen of Treponema pallidum determines its hydrophobicity. Infect Immun 57, 2878-2885.
20. Champion, C. I., Miller, J. N., Borenstein, L. A., Lovett, M. A. & Blanco, D. R. (1990). Immunization with Treponema pallidum endoflagella alters the course of experimental rabbit syphilis. Infect Immun 58, 3158-3161.
21. Chi, B., Chauhan, S. & Kuramitsu, H. (1999). Development of a system for expressing heterologous genes in the oral spirochete Treponema denticola and its use in expression of the Treponema pallidum flaA gene. Infect Immun 67, 3653-3656.
22. Cox, D. L., Chang, P., McDowall, A. W. & Radolf, J. D. (1992). The outer membrane, not a eoat of host proteins, limits antigenicity of virulent Treponema pallidum. Infect Immun 60, 1076-1083.
23. Cox, D. L., Akins, D. R., Porcella, S. F., Norgard, M. V. & Radolf, J. D. (1995). Treponema pallidum in gel microdroplets: a novel strategy for investigation of treponemal molecular architecture. Mol Microbiol 15, 1151-1164.
24. Cox, D. L., Akins, D. R., Bourell, K. W., Lahdenne, P., Norgard, M. V. & Radolf, J. D. (1996). Limited surface exposure of Borrelia burgdorferi outer surface lipoproteins. Proc Natl Acad Sci USA 93, 7973-7978.
25. Duong, F., Eichler, J., Price, A., Leonard, M. R. & Wickner, W. (1997). Biogenesis of the gram-negative bacterial envelope. Cell 91, 567-573.
26. El Hage, N., Lieto, L. D. & Stevenson, B. (1999). Stability of erp loci during Borrelia burgdorferi infection: recombination is not required for chronic infection of immunocompetent mice. Infect Immun 67, 3146-3150.
27. Erdile, L. F., Brandt, M. A., Warakomski, D. J., Westrack, G. J., Sadziene, A., Barbour, A. G. & Mays, J. P. (1993). Role of attached lipid in immunogenicity of Borrelia burgdorferi OspA. Infect Immun 61, 81-90.
28. Feng, S., Hodzic, E., Stevenson, B. & Barthold, S.W. (1998). Humoral immunity to Borrelia burgdorferi N40 decorin-binding proteins during infection of laboratory mice. Infect Immun 66, 2827-2835.
29. Fikrig, E., Barthold, S.W., Kantor, F. S. & Flavell, R. A. (1990). Protection of mice against the Lyme disease agent by immunizing with recombinant OspA. Science 250, 553-556.
30. Fikrig, E., Barthold, S. W., Sun, W., Feng, W., Telford, S. R., III & Flavell, R. A. (1997). Borrelia burgdorferi P35 and P37 proteins, expressed in vivo, elicit protective immunity. Immunity 6, 531-539.
31. Foley, D. M., Wang, Y. P., Wu, X. Y., Blanco, D. R., Lovett, M. A. & Miller, J. N. (1997). Acquired resistance to Borrelia burgdorferi infection in the rabbit: comparison between outer surface protein A vaccine- and infection-derived immunity. J Clin Invest 99, 2030-2035.
32. Fraser, C. M., Casjens, S., Huang, W. M. & 35 other authors (1997). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586.
33. Fraser, C. M., Norris, S. J., Weinstock, G. M. & 30 other authors (1998). Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281, 375-388.
34. Giambartolomei, G. H., Dennis, V. A., Lasater, B. L & Philipp, M. T. (1999). Induction of pro- and anti-inflammatory cytokines by Borrelia burgdorferi lipoproteins in monocytes is mediated by CD14. Infect Immun 67, 140-147.
35. Greene, S. R., Stamm, L. V., Hardham, J. M., Young, N. R. & Frye, J. G. (1997). Identification, sequences, and expression of Treponema pallidum chemotaxis genes. DNA Seq 7, 267-284.
36. 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.
37. 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.
38. Haake, D. A., Walker, E. M., Blanco, D. R., Bolin, C. A., Miller, M. N. & Lovett, M. A. (1991). Changes in the surface of Leptospira interrogans serovar grippotyphosa during in vitro cultivation. Infect Immun 59, 1131-1140.
39. Haake, D. A., Champion, C. L., Martinich, C., Shang, E. S., Blanco, D. R., Miller, J. N. & Lovett, M. A. (1993). Molecular cloning and sequence analysis of the gene encoding OmpL1, a transmembrane outer membrane protein of pathogenic Leptospira spp. J Bacteriol 175, 4225-1234.
40. Haake, D. A., Martinich, C., Summers, T. A., Shang, E. S., Pruetz, J. D., McCoy, A. M., Mazel, M. K. & Bolin, C. A. (1998). Characterization of leptospiral outer membrane lipoprotein LipL36: downregulation associated with late log-phase growth and mammalian infection. Infect Immun 66, 1579-1587.
41. Haake, D. A., Mazel, M. K., McCoy, A. M., Milward, F., Chao, G., Matsunaga, J. & Wagar, E. A. (1999). Leptospiral outer membrane proteins OmpL1 and LipL41 exhibit synergistic immunoprotection. Infect Immun 67, 6572-6582.
42. Haake, D. A., Chao, G., Zuerner, R. L., Barnett, J. K., Barnett, D., Mazel, M., Matsunaga, J., Levett, P. N. & Bolin, C. A. (2000). The leptospiral major outer membrane protein LipL32 is a lipoprotein expressed during mammalian infection. Infect Immun 68, 2276-2285.
43. Hagman, K. E., Porcella, S. F., Popova, T. G. & Norgard, M. V. (1997). Evidence for a methyl-accepting chemotaxis protein gene (mcp1) that encodes a putative sensory transducer in virulent Treponema pallidum. Infect Immun 65, 1701-1709.
44. Hagman, K. E., Lahdenne, P., Popova, T. G., Porcella, S. F., Akins, D. R., Radolf, J. D. & Norgard, M. V. (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.
45. Hanson, M. S., Cassatt, D. R., Guo, B. P., Patel, N. K., McCarthy, M. P., Dorward, D. W. & Hook, M. (1998). Active and passive immunity against Borrelia burgdorferi decorin binding protein A (DbpA) protects against infection. Infect Immun 66, 2143-2153.
46. Hinnebusch, B. J., Barbour, A. G., Restrepo, B. I. & Schwan, T. G. (1998). Population structure of the relapsing fever spirochete Borrelia bermsii as indicated by polymorphism of two multigene families that encode immunogenic outer surface lipoproteins. Infect Immun 66, 432-440.
47. Hirschfeld, M., Kirschning, C. I., Schwandner, R., Wesche, H., Weis, J. H., Wooten, R. M. & Weis, J. J. (1999). Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 163, 2382-2386.
48. Indest, K. J., Ramamoorthy, R., Sole, M., Gilmore, R. D., Johnson, B. J. & Philipp, M. T. (1997). Cell-density-dependent expression of Borrelia burgdorferi lipoproteins in vitro. Infect Immun 65, 1165-1171.
49. Johnson, R. C., Kodner, C. & Russell, M. (1987). In vitro and in vivo susceptibility of the Lyme disease spirochete, Borrelia burgdorferi, to four antimicrobial agents. Antimicrob Agents Chemother 31, 164-167 (erratum 34, 1622).
50. Johnson, B. J., Sviat, S. L., Happ, C. M., Dunn, J. J., Frantz, J. C., Mayer, L W. & Piesman, J. (1995). Incomplete protection of hamsters vaccinated with unlipidated OspA from Borrelia burgdorferi infection is associated with low levels of antibody to an epitope defined by mAb LA-2. Vaccine 13, 1086-1094.
51. Lam, T. T., Nguyen, T. P., Montgomery, R. R., Kantor, F. S., Fikrig, E. & Flavell, R. A. (1994). Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease. Infect Immun 62, 290-298.
52. Li, H., Ruby, J., Charon, N. & Kuramitsu, H. (1996). Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant. J Bacteriol 178, 3664-3667.
53. Li, H., Dunn, J. J., Luft, B. J. & Lawson, C. L. (1997). Crystal structure of Lyme disease antigen outer surface protein A complexed with an FAb. Proc Natl Acad Sci USA 94, 3584-3589.
54. Matsuyama, S., Yokota, N. & Tokuda, H. (1997). A novel outer membrane lipoprotein, LolB (He mM), involved in the LolA (p20)-dependent localization of lipoproteins to the outer membrane of Escherichia coli. EMBO J 16, 6947-6955.
55. Montgomery, R. R., Malawista, S. E., Feen, K. J. & Bockenstedt, L. K. (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.
56. Nguyen, T. P., Lam, T. T., Barthold, S. W., Telford, S. R., III, Flavell, R. A. & Fikrig, E. (1994). Partial destruction of Borrelia burgdorferi within ticks that engorged on OspE- or OspF-immunized mice. Infect Immun 62, 2079-2084.
57. Norgard, M. V., Riley, B. S., Richardson, J. A. & Radolf, J. D. (1995). Dermal inflammation elicited by synthetic analogs of Treponema pallidum and Borrelia burgdorferi lipoproteins. Infect Immun 63, 1507-1515.
58. Norris, S.J. (1993). Polypeptides of Treponema pallidum: progress toward understanding their structural, functional, and immunologic roles. Microbiol Rev 57, 750-779 (erratum 58, 291).
59. Norris, S. J., Carter, C. J., Howell, J. K. & Barbour, A. G. (1992). Low-passage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein. Infect Immun 60, 4662-4672.
60. Nowling, J. M. & Philipp, M. T. (1999). Killing of Borrelia burgdorferi by antibody elicited by OspA vaccine is inefficient in the absence of complement. Infect Immun 67, 443-44.5.
61. Obonyo, M., Munderloh, U. G., Fingerle, V., Wilske, B. & Kurtti, T. J. (1999). Borrelia burgdorferi in tick cell culture modulates expression of outer surface proteins A and C in response to temperature. J Clin Microbiol 37, 2137-2141.
62. Pennington, P. M., Cadavid, D. & Barbour, A. G. (1999). Characterization of VspB of Borrelia turicatae, a major outer membrane protein expressed in blood and tissues of mice. Infect Immun 67, 4637-4645.
63. Persing, D.H., Mathiesen, D., Podzorski, D. & Barthold, S.W. (1994). Genetic stability of Borrelia burgdorferi recovered from chronically infected immunocompetent mice. Infect Immun 62, 3521-3527.
64. Probert, W. S. & Johnson, B. J. (1998). Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol Microbiol 30, 1003-1015.
65. Probert, W. S. & LeFebvre, R. B. (1994). Protection of C3H/HeN mice from challenge with Borrelia burgdorferi through active immunization with OspA, OspB, or OspC, but not with OspD or the 83-kilodalton antigen. Infect Immun 62, 1920-1926.
66. Purcell, B. K., Swancutt, M. A. & Radolf, J. D. (1990). Lipid modification of the 15 kilodalton major membrane immunogen of Treponema pallidum. Mol Microbiol 4, 1371-1379.
67. Radolf, J. D., Chamberlain, N. R., Clausell, A. & Norgard, M. V. (1988). Identification and localization of integral membrane proteins of virulent Treponema pallidum subsp. pallidum by phase partitioning with the nonionic detergent triton X-114. Infect Immun 56, 490-498.
68. Radolf, J. D., Norgard, M. V. & Schulz, W. W. (1989). Outer membrane ultrastructure explains the limited antigenicity of virulent Treponema pallidum. Proc Natl Acad Sci USA 86, 2051-2055.
69. Radolf, J. D., Robinson, E. J., Bourell, K. W., Akins, D. R., Porcella, S. F., Weigel, L. M., Jones, J. D. &Norgard, M. V. (1995a). Characterization of outer membranes isolated from Treponema pallidum, the syphilis spirochete. Infect Immun 63, 4244-4252.
70. Radolf, J. D., Arndt, L. L., Akins, D. R., Curetty, L. L., Levi, M. E., Shen, Y., Davis, L. S. & Norgard, M. V. (1995b). Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J Immunol 154, 2866-2877.
71. Roberts, W. C., Mullikin, B. A., Lathigra, R. & Hanson, M. S. (1998). Molecular analysis of sequence heterogeneity among genes encoding decorin binding proteins A and B of Borrelia burgdorferi sensu lato. Infect Immun 66, 5275-5285.
72. Rosey, E. L., Kennedy, M. J., Petrella, D. K., Ulrich, R. G. & Yancey, R. J., Jr (1995). Inactivation of Serpulina hyodysenteriae flaA1 and flaB1 periplasmic flagellar genes by electroporation-mediated allelic exchange. J Bacteriol 177, 5959-5970.
73. Sadziene, A., Thompson, P. A. & Barbour, A. G. (1993). In vitro inhibition of Borrelia burgdorferi growth by antibodies. J Infect Dis 167, 165-172.
74. Sadziene, A., Thomas, D. D. & Barbour, A. G. (1995). Borrelia burgdorferi mutant lacking Osp: biological and immunological characterization. Infect Immun 63, 1573-1580.
75. Schwan, T. G. & Hinnebusch, B. J. (1998). Bloodstream- versus tick-associated variants of a relapsing fever bacterium. Science 280, 1938-1940.
76. Schwan, T. G., Piesman, J., Golde, W. T., Dolan, M. C. & Rosa, P. A. (1995). Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci USA 92, 2909-2913.
77. Sears, J. E., Fikrig, E., Nakagawa, T. Y., Deponte, K., Marcantonio, N., Kantor, F. S. & Flavell, R. A. (1991). Molecular mapping of Osp-A mediated immunity against Borrelia burgdorferi, the agent of Lyme disease. J Immunol 147, 1995-2000.
78. Sellati, T. J., Abrescia, L. D., Radolf, J. D. & Furie, M. B. (1996). Outer surface lipoproteins of Borrelia burgdorferi activate vascular endotheliuni in vitro. Infect Immun 64, 3180-3187.
79. Sellati, T. J., Bouis, D. A., Kitchens, R. L. & 7 other authors (1998). 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, 5455-5464.
80. Shang, E. S., Exner, M. M., Summers, T. A., Martinich, C., Champion, C. I., Hancock, R. E. W. & Haake, D. A. (1995). The rare outer membrane protein, OmpL1, of pathogenic Leptospira species is a heat-modifiable porin. Infect Immun 63, 3174-3181.
81. Shang, E. S., Summers, T. A. & Haake, D. A. (1996). Molecular cloning and sequence analysis of the gene encoding LipL41, a surface-exposed lipoprotein of pathogenic Leptospira species. Infect Immun 64, 2322-2330.
82. Shevchenko, D. V., Akins, D. R., Robinson, E. J., Li, M., Shevchenko, O. V. & Radolf, J. D. (1997). Identification of homologs for thioredoxin, peptidyl prolyl cis-trans isomerase, and glycerophosphodiester phosphodiesterase in outer membrane fractions from Treponema pallidum, the syphilis spirochete. Infect Immun 65, 4179-4189.
83. Shevchenko, D. V., Sellati, T. J., Cox, D. L., Shevchenko, O. V., Robinson, E. J. & Radolf, J. D. (1999). Membrane topology and cellular location of the Treponema pallidum glycerophosphodiester phosphodiesterase (GlpQ) ortholog. Infect Immun 67, 2266-2276.
84. de Silva, A. M., Zeidner, N. S., Zhang, Y., Dolan, M. C., Piesman, J. & Fikrig, E. (1999). Influence of outer surface protein A antibody on Borrelia burgdorferi within feeding ticks. Infect Immun 67, 30-35.
85. Skare, J. T., Foley, D. M., Hernandez, S. R., Moore, D. C., Blanco, D. R., Miller, J. N. & Lovett, M. A. (1999). Cloning and molecular characterization of plasmid-encoded antigens of Borrelia burgdorferi. Infect Immun 67, 4407-4417.
86. Stevenson, B., Bockenstedt, L. K. & Barthold, S.W. (1994). Expression and gene sequence of outer surface protein C of Borrelia burgdorferi reisolated from chronically infected mice. Infect Immun 62, 3568-3571.
87. Stevenson, B., Schwan, T. G. & Rosa, P. A. (1995). Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun 63, 4535-4539.
88. Stevenson, B., Tilly, K. & Rosa, P. A. (1996). A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J Bacteriol 178, 3508-3516.
89. Stevenson, B., Bono, J. L., Schwan, T. G. & Rosa, P. (1998a). Borrelia burgdorferi erp proteins are immunogenic in mammals infected by tick bite, and their synthesis is inducible in cultured bacteria. Infect Immun 66, 2648-2654.
90. Stevenson, B., Bono, J. L., Elias, A., Tilly, K. & Rosa, P. (1998b). Transformation of the Lyme disease spirochete Borrelia burgdorferi with heterologous DNA. J Bacteriol 180, 4850-4855.
91. Suk, K., Das, S., Sun, W., Jwang, B., Barthold, S. W., Flavell, R. A. & Fikrig, E. (1995). Borrelia burgdorferi genes selectively expressed in the infected host. Proc Natl Acad Sci USA 92, 4269-4273.
92. Sutcliffe, I. C. & Russell, R. R. (1995). Lipoproteins of gram-positive bacteria. J Bacteriol 177, 1123-1128.
93. Swancutt, M. A., Radolf, J. D. & Norgard, M. V. (1990). The 34-kilodalton membrane immunogen of Treponema pallidum is a lipoprotein. Infect Immun 58, 384-392.
94. Thomas, W. & Sellwood, R. (1993). Molecular cloning, expression, and DNA sequence analysis of the gene that encodes the 16-kilodalton outer membrane lipoprotein of Serpulina hyodysenteriae. Infect Immun 61, 1136-1140.
95. The Institute for Genomic Research (2000). Trends Genet Microbial Database: A listing of microbial genomes and chromosomes completed and in progress. http://www.tigr.org/ tdb/mdb/mdb.html.
96. Ulevitch, R. J. (1999). Endotoxin opens the Tollgates to innate immunity. Nature Med 5, 144-145.
97. Vincent, M. S., Roessner, K., Sellati, T., Huston, C. D., Sigal, L. H., Behar, S. M., Radolf, J. D. & Budd, R. C. (1998). Lyme arthritis synovial gamma delta T cells respond to Borrelia burgdorferi lipoproteins and lipidated hexapeptides. J Immunol 161, 5762-5771.
98. Walker, E. M., Zampighi, G. A., Blanco, D. R., Miller, J. N. & Lovett, M. A. (1989). Demonstration of rare protein in the outer membrane of Treponema pallidum subsp. pallidum by freeze-fracture analysis. J Bacteriol 171, 5005-5011.
99. Walker, E. M., Borenstein, L. A., Blanco, D. R., Miller, J. N. & Lovett, M. A. (1991). Analysis of outer membrane ultrastructure of pathogenic Treponema and Borrelia species by freeze-fracture electron microscopy. J Bacteriol 173, 5585-5588.
100. Wallich, R., Brenner, C., Kramer, M. D. & Simon, M. M. (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.
101. Weis. J. J., McCracken, B. A., Ma, Y. & 7 other authors (1999). Identification of quantitative trait loci governing arthritis severity and humoral responses in the murine model of Lyme disease. J Immunol 162, 948-956.
102. Wilske, B., Preac-Mursic, V., Jauris, S., Hofmann, A., Pradel, I., Soutschek, E., Schwab, E., Will, G. & Wanner, G. (1993). Immunological and molecular polymorphisms of OspC, an immunodominant major outer surface protein of Borrelia burgdorferi. Infect Immun 61, 2182-2191.
103. Wooten, R. M., Morrison, T. B., Weis, J. H., Wright S. D., Thieringer, R. & Weis, J. J. (1998). The role of CD14 in signaling mediated by outer membrane lipoproteins of Borrelia burgdorferi. J Immunol 160, 5485-5492.
104. Wu, H. C. (1996). Biosynthesis of lipoproteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 1005-1014. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
105. Yamaguchi, K., Yu, F. & Inouye, M. (1988). A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53, 423-432.
106. Zhang, J. R. & Norris, S. J. (1998a). Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect Immun 66, 3698-3704.
107. Zhang, J. R. & Norris, S. J. (1998b). Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect Immun 66, 3689-3697 (erratum 67, 468).
108. Zhang, J. R., Hardham, J. M., Barbour, A. G. & Norris, S. J. (1997). Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89, 275-285.