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. 1991 Sep;173(17):5585–5588. doi: 10.1128/jb.173.17.5585-5588.1991

Analysis of outer membrane ultrastructure of pathogenic Treponema and Borrelia species by freeze-fracture electron microscopy.

E M Walker 1, L A Borenstein 1, D R Blanco 1, J N Miller 1, M A Lovett 1
PMCID: PMC208278  PMID: 1885536

Abstract

We analyzed the outer membrane (OM) ultrastructure of four pathogenic members of the family Spirochaetaceae by freeze fracture. The OM of Treponema pallidum subsp. pertenue contained a low intramembranous particle concentration, indicating that it contains few OM transmembrane proteins. The concave OM fracture faces of Treponema hyodysenteriae and Borrelia burgdorferi contained dense populations of particles, typical of gram-negative organisms. A relatively low concentration of particles which were evenly divided between a small and a large species was present in the concave OM fracture face of Borrelia hermsii; the convex OM fracture face contained only small particles. As for gram-negative bacteria, the convex OM fracture face particle concentrations of these pathogens were low. These spirochetes cleaved preferentially within the OM, in contrast to typical gram-negative bacteria, which tend to fracture within the inner membrane. The OM ultrastructure of T. pallidum subsp. pertenue provides an explanation for the lack of antigenicity of the treponemal surface and may reflect a mechanism by which this pathogen evades the host immune response.

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Selected References

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  1. Barbour A. G., Hayes S. F. Biology of Borrelia species. Microbiol Rev. 1986 Dec;50(4):381–400. doi: 10.1128/mr.50.4.381-400.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barbour A. G. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984 Jul-Aug;57(4):521–525. [PMC free article] [PubMed] [Google Scholar]
  3. Barbour A. G., Tessier S. L., Stoenner H. G. Variable major proteins of Borrellia hermsii. J Exp Med. 1982 Nov 1;156(5):1312–1324. doi: 10.1084/jem.156.5.1312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beveridge T. J. Ultrastructure, chemistry, and function of the bacterial wall. Int Rev Cytol. 1981;72:229–317. doi: 10.1016/s0074-7696(08)61198-5. [DOI] [PubMed] [Google Scholar]
  5. Bishop N. H., Miller J. N. Humoral immunity in experimental syphilis. II. The relationship of neutralizing factors in immune serum to acquired resistance. J Immunol. 1976 Jul;117(1):197–207. [PubMed] [Google Scholar]
  6. Blanco D. R., Walker E. M., Haake D. A., Champion C. I., Miller J. N., Lovett M. A. Complement activation limits the rate of in vitro treponemicidal activity and correlates with antibody-mediated aggregation of Treponema pallidum rare outer membrane protein. J Immunol. 1990 Mar 1;144(5):1914–1921. [PubMed] [Google Scholar]
  7. Boyden D. A., Albert F. G., Robinson C. S. Cloning and characterization of Treponema hyodysenteriae antigens and protection in a CF-1 mouse model by immunization with a cloned endoflagellar antigen. Infect Immun. 1989 Dec;57(12):3808–3815. doi: 10.1128/iai.57.12.3808-3815.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brandt M. E., Riley B. S., Radolf J. D., Norgard M. V. Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins. Infect Immun. 1990 Apr;58(4):983–991. doi: 10.1128/iai.58.4.983-991.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Burman N., Bergström S., Restrepo B. I., Barbour A. G. The variable antigens Vmp7 and Vmp21 of the relapsing fever bacterium Borrelia hermsii are structurally analogous to the VSG proteins of the African trypanosome. Mol Microbiol. 1990 Oct;4(10):1715–1726. doi: 10.1111/j.1365-2958.1990.tb00549.x. [DOI] [PubMed] [Google Scholar]
  10. Chamberlain N. R., Brandt M. E., Erwin A. L., Radolf J. D., Norgard M. V. Major integral membrane protein immunogens of Treponema pallidum are proteolipids. Infect Immun. 1989 Sep;57(9):2872–2877. doi: 10.1128/iai.57.9.2872-2877.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cunningham T. M., Walker E. M., Miller J. N., Lovett M. A. Selective release of the Treponema pallidum outer membrane and associated polypeptides with Triton X-114. J Bacteriol. 1988 Dec;170(12):5789–5796. doi: 10.1128/jb.170.12.5789-5796.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greer J. M., Wannemuehler M. J. Comparison of the biological responses induced by lipopolysaccharide and endotoxin of Treponema hyodysenteriae and Treponema innocens. Infect Immun. 1989 Mar;57(3):717–723. doi: 10.1128/iai.57.3.717-723.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hanff P. A., Norris S. J., Lovett M. A., Miller J. N. Purification of Treponema pallidum, Nichols strain, by Percoll density gradient centrifugation. Sex Transm Dis. 1984 Oct-Dec;11(4):275–286. doi: 10.1097/00007435-198410000-00003. [DOI] [PubMed] [Google Scholar]
  14. Holt S. C. Anatomy and chemistry of spirochetes. Microbiol Rev. 1978 Mar;42(1):114–160. doi: 10.1128/mr.42.1.114-160.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hovind-Hougen K., Birch-Andersen A., Nielsen H. A. Electron microscopy of treponemes subjected to the Treponema pallidum immobilization (TPI) test. II. Immunoelectron microscopy. Acta Pathol Microbiol Scand C. 1979 Aug;87C(4):263–268. [PubMed] [Google Scholar]
  16. KHAN A. S., NELSON R. A., Jr, TURNER T. B. Immunological relationships among species and strains of virulent treponemes as determined with the treponemal immobilization test. Am J Hyg. 1951 May;53(3):296–316. doi: 10.1093/oxfordjournals.aje.a119455. [DOI] [PubMed] [Google Scholar]
  17. Kochi S. K., Johnson R. C. Role of immunoglobulin G in killing of Borrelia burgdorferi by the classical complement pathway. Infect Immun. 1988 Feb;56(2):314–321. doi: 10.1128/iai.56.2.314-321.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lugtenberg B., Van Alphen L. Molecular architecture and functioning of the outer membrane of Escherichia coli and other gram-negative bacteria. Biochim Biophys Acta. 1983 Mar 21;737(1):51–115. doi: 10.1016/0304-4157(83)90014-x. [DOI] [PubMed] [Google Scholar]
  19. METZGER M., RUCZKOWSKA J. INFLUENCE OF LYSOZYME UPON THE REACTIVITY OF TREPONEMA PALLIDUM IN THE FLUORESCENT ANTIBODY REACTION. Arch Immunol Ther Exp (Warsz) 1964;12:702–708. [PubMed] [Google Scholar]
  20. MILLER J. N., FAZZAN F. P., WHANG S. J. STUDIES ON IMMUNITY IN EXPERIMENTAL SYPHILIS. II. TREPONEMA PALLIDUM IMMOBILIZATION (TPI) ANTIBODY AND THE IMMUNE RESPONSE. Br J Vener Dis. 1963 Sep;39:199–203. doi: 10.1136/sti.39.3.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Miao R. M., Fieldsteel A. H. Genetic relationship between Treponema pallidum and Treponema pertenue, two noncultivable human pathogens. J Bacteriol. 1980 Jan;141(1):427–429. doi: 10.1128/jb.141.1.427-429.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Norris S. J., Sell S. Antigenic complexity of Treponema pallidum: antigenicity and surface localization of major polypeptides. J Immunol. 1984 Nov;133(5):2686–2692. [PubMed] [Google Scholar]
  23. Penn C. W., Cockayne A., Bailey M. J. The outer membrane of Treponema pallidum: biological significance and biochemical properties. J Gen Microbiol. 1985 Sep;131(9):2349–2357. doi: 10.1099/00221287-131-9-2349. [DOI] [PubMed] [Google Scholar]
  24. Radolf J. D., Chamberlain N. R., Clausell A., Norgard M. V. 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. 1988 Feb;56(2):490–498. doi: 10.1128/iai.56.2.490-498.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Radolf J. D., Fehniger T. E., Silverblatt F. J., Miller J. N., Lovett M. A. The surface of virulent Treponema pallidum: resistance to antibody binding in the absence of complement and surface association of recombinant antigen 4D. Infect Immun. 1986 May;52(2):579–585. doi: 10.1128/iai.52.2.579-585.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Radolf J. D., Norgard M. V., Schulz W. W. Outer membrane ultrastructure explains the limited antigenicity of virulent Treponema pallidum. Proc Natl Acad Sci U S A. 1989 Mar;86(6):2051–2055. doi: 10.1073/pnas.86.6.2051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sellwood R., Kent K. A., Burrows M. R., Lysons R. J., Bland A. P. Antibodies to a common outer envelope antigen of Treponema hyodysenteriae with antibacterial activity. J Gen Microbiol. 1989 Aug;135(8):2249–2257. doi: 10.1099/00221287-135-8-2249. [DOI] [PubMed] [Google Scholar]
  28. Stanton T. B., Cornell C. P. Erythrocytes as a source of essential lipids for Treponema hyodysenteriae. Infect Immun. 1987 Feb;55(2):304–308. doi: 10.1128/iai.55.2.304-308.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Takayama K., Rothenberg R. J., Barbour A. G. Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun. 1987 Sep;55(9):2311–2313. doi: 10.1128/iai.55.9.2311-2313.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Walker E. M., Zampighi G. A., Blanco D. R., Miller J. N., Lovett M. A. Demonstration of rare protein in the outer membrane of Treponema pallidum subsp. pallidum by freeze-fracture analysis. J Bacteriol. 1989 Sep;171(9):5005–5011. doi: 10.1128/jb.171.9.5005-5011.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wannemuehler M. J., Hubbard R. D., Greer J. M. Characterization of the major outer membrane antigens of Treponema hyodysenteriae. Infect Immun. 1988 Dec;56(12):3032–3039. doi: 10.1128/iai.56.12.3032-3039.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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