Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-22T20:03:28.290Z Has data issue: false hasContentIssue false

6 - Evasion of antibody responses: Bacterial phase variation

from Part II - Evasion of humoral immunity

Published online by Cambridge University Press:  13 August 2009

By
Nigel J. Saunders
Edited by
Brian Henderson  and
Petra C. F. Oyston
Nigel J. Saunders
Affiliation:
Molecular Infectious Diseases Group, Institute of Molecular, Medicine University of Oxford, Headington, OX3 9DS, UK
Brian Henderson
Affiliation:
University College London
Petra C. F. Oyston
Affiliation:
Defence Science and Technology Laboratory, Salisbury
Get access

Summary

INTRODUCTION

The generation of diversity within bacterial populations is important in the evolution and development of bacterial species and also in the adaptability of bacteria to their changing environments. Diversity is generated by a combination of programmed and random events that occur at different rates and confer different types of variability on the population. At one extreme there are random point mutations that occur throughout the coding and intergenic sequences that alter the expression, structure, and function of bacterial components. At the other extreme, there are regulated responses that allow bacteria to control the expression of genes whenever the appropriate environmental conditions are encountered. Between these there is a variety of processes that adds to the capacity of a population to diversify, including the presence and movement of insertion sequences that affect expression, mobile genetic elements that can move within and between populations, and the horizontal transfer of DNA between individual bacteria. One process that lies between the mutations that occur randomly throughout the genome and the programmed regulation of environmentally responsive genes is phase variation. This process involves alterations in the cell at the level of DNA but in a way that generates predictable and predetermined adaptability for the bacterial population.

SECTION 1: PHASE VARIATION, ITS CHARACTERISTICS AND HOW IT WORKS

Phase variation has been recognised as a process associated with diversification since the early days of medical bacteriology (Andrewes, 1922).

Type
Chapter
Information
Bacterial Evasion of Host Immune Responses , pp. 103 - 124
Publisher: Cambridge University Press
Print publication year: 2003

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Achtman, M., Neibert, M., Crowe, B. A., Strittmatter, W., Kusecek, B., Weyse, E., Walsh, M. J., Slawig, B., Morelli, G., Moll, A., and Blake, M. (1988). Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. Journal of Experimental Medicine 168, 507–525CrossRefGoogle ScholarPubMed
Andrewes, F. W. (1922). Studies in group-agglutination. I. The Salmonella group and its antigenic structure. Journal of Pathology and Bacteriology 25, 505–521CrossRefGoogle Scholar
Apicella, M. A., Shero, M., Jarvis, G. A., Griffiss, J. M., Mandrell, R. E., and Schneider, H. (1987). Phenotypic variation in epitope expression of the Neisseria gonorrhoeae lipooligosaccharide. Infection and Immunity 55, 1755–1761Google ScholarPubMed
Barbour, A. G., Tessier, S. L., and Stoenner, H. G. (1982). Variable major proteins of Borrelia hermsii. Journal of Experimental Medicine 156, 1312–1324CrossRefGoogle Scholar
Barbour, A. G., Barrera, O., and Judd, R. C. (1983). Structural analysis of the variable major proteins of Borrelia hermsii. Journal of Experimental Medicine 158, 2127–2140CrossRefGoogle ScholarPubMed
Behrens, A., Heller, M., Kirchhoff, H., Yogev, D., and Rosengarten, R. (1994). A family of phase- and size-variant membrane surface lipoprotein antigens (Vsps) of Mycoplasma bovis. Infection and Immunity 62, 5075–5084Google ScholarPubMed
Bhat, K. S., Gibbs, C. P., Barrera, O., Morrison, S. G., Jahnig, F., Stern, A., Kupsch, E.-M., Meyer, T. F., and Swanson, J. (1991). The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Molecular Microbiology 5, 1889–1901. Also see erratum: Molecular Microbiology 6, 1073–1076CrossRefGoogle ScholarPubMed
Chen, C.-J., Sparling, P. F., Lewis, L. A., Dyer, D. W., and Elkins, C. (1996). Identification and purification of a hemoglobin-binding outer membrane protein from Neisseria gonorrhoeae. Infection and Immunity 64, 5008–5014Google ScholarPubMed
Chen, C. J., Elkins, C., and Sparling, P. F. (1998). Phase variation of hemoglobin utilization in Neisseria gonorrhoeae. Infection and Immunity 66, 987–993Google ScholarPubMed
Citti, C., Kim, M. F., and Wise, K. S. (1997). Elongated versions of Vlp surface lipoproteins protect Mycoplasma hyrhinis escape variants from growth-inhibiting host antibodies. Infection and Immunity 65, 1773–1785Google ScholarPubMed
Coffey, E. M. and Eveland, W. C. (1967). Experimental relapsing fever initiated by Borrelia hermsii. II. Sequential appearance of major serotypes in the rat. Journal of Infectious Diseases 177, 29–34CrossRefGoogle Scholar
Danaher, R. J., Levin, J. C., Arking, D., Burch, C. L., Sandlin, R., and Stein, D. C. (1995). Genetic basis of Neisseria gonorrhoeae lipooligosaccharide antigenic variation. Journal of Bacteriology 177, 7275–7279CrossRefGoogle ScholarPubMed
Paz, H., Cooke, S. J., and Heckels, J. E. (1995). Effect of sialylation of lipopolysaccharide of Neisseria gonorrhoeae on recognition and complementmediated killing by monoclonal antibodies directed against different outer-membrane antigens. Microbiology 141, 913–920CrossRefGoogle Scholar
DeVoe, I. W. (1982). The meningococcus and mechanisms of pathogenicity. Microbiology Reviews 46, 162–190Google ScholarPubMed
Fearon, D. T. (1978). Regulation by membrane sialic acid of ß1H-dependent decay-dissociation of amplification C3 convertase of the alternative complement pathway. Proceedings of the National Academy of Sciences USA 75, 1971–1975CrossRefGoogle ScholarPubMed
Finlay, B. B. and Falkow, S. (1989). Common themes in microbial pathogenicity. Microbiology Reviews 53, 210–230Google ScholarPubMed
Finne, J., Leinonen, M., and Makela, P. H. (1983). Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 2, 355–357CrossRefGoogle ScholarPubMed
Finne, J., Bitter-Suermann, D., Goridis, C., and Finne, U. (1987). An IgG monoclonal antibody to group B meningococci cross-reacts with developmentally regulated polysialic acid units of glycoproteins in neural and extraneural tissues. Journal of Immunology 138, 4402–4407Google Scholar
Gill, M. J., McQuillen, D. P., Putten, J. P. M., Wetzler, L. M., Bramley, J., Crooke, H., Parsons, N. J., Cole, J. A., and Smith, H. (1996). Functional characterization of a sialyltranferase-deficient mutant of Neisseria gonorrhoeae. Infection and Immunity 64, 3374–3378Google ScholarPubMed
Gilsdorf, J. R. and Ferrieri, P. (1986). Susceptibility of phenotypic variants of Haemophilus influenzae type b to serum bactericidal activity: relationship to surface lipopolysaccharide. Journal of Infectious Diseases 153, 223–231CrossRefGoogle Scholar
Hammerschmidt, S., Birkholtz, C., Zahringer, U., Robertson, B. D., Putten, J., Ebeling, O., and Frosch, M. (1994). Contribution of genes from the capsule gene cluster complex (cps) to lipopolysaccharide biosynthesis and serum resistance in Neisseria meningitidis. Molecular Microbiology 11, 885–896CrossRefGoogle ScholarPubMed
Hammerschmidt, S., Hilse, R., Putten, JPM., Gerardy-Schahn, R., Unkmeir, A., and Frosch, M. (1996). Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. European Molecular Biology Organisation Journal 15, 192–198Google Scholar
Harnett, W. and Harnett, M. M. (1999). Phosphorylcholine: friend or foe of the immune system?Immmunology Today 20, 125–129CrossRefGoogle ScholarPubMed
Hood, D. W., Deadman, M. E., Jennings, M. P., Biscercic, M., Fleischmann, R. D., Venter, J. C., and Moxon, E. R. (1996). DNA repeats identify novel virulence genes in Haemophilus influenzae. Proceedings of the National Academy of Sciences USA 93, 11,121–11,125CrossRefGoogle ScholarPubMed
Hopman, C. T. P., Dankert, J., and van Putten, J. P. M. (1994). Variable expression of the class 1 protein of Neisseria meningitidis, In, ed. C. J. Conde-Glez, S. Morse, P. Rice, F. Sparling, and E. Calderon. pp. 513–517. Pathology and immunobiology of Neisseriaceae, Instituto Nacional de Salud Publica Cuernavaca, Mexico
Inzana, T. J., Gogolewski, R. P., and Corbeil, L. B. (1992). Phenotypic phase variation in Haemophilus somnus lipopolysaccharide during bovine pneumonia and after in vitro passage. Infection and Immunity 60, 2943–2951Google ScholarPubMed
Inzana, T. J., Hensley, J., McQuiston, J., Lesse, A. J., Campagnari, A. A., Boyle, S. M., and Apicella, M. A. (1997). Phase variation and conservation of lipopolysaccharide epitopes in Haemophilus somnus. Infection and Immunity 65, 4675–4681Google ScholarPubMed
Jarvis, G. A. (1995). Recognition and control of neisserial infection by antibody and complement. Trends in Microbiology 3, 198–201CrossRefGoogle ScholarPubMed
Jennings, H. J., Bhattacharjee, A. K., Bundle, D. R., Kenny, C. P., Martin, A., and Smith, I. C. (1977). Structures of the capsular polysaccharides of Neisseria meningitidis as determined by 13C-nuclear magnetic resonance spectroscopy. Journal of Infectious Diseases 136, S78–S83CrossRefGoogle Scholar
Jennings, M. P., Virji, M., Evans, D., Foster, V., Srikhanta, Y. N., Steeghs, L., Ley, P., and Moxon, E. R. (1998). Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Molecular Microbiology 29, 975–984CrossRefGoogle ScholarPubMed
Jennings, M. P., Srithanta, Y. N., Moxon, E. R., Kramer, M., Poolman, J. T., Kuipers, B., and Ley, P. (1999). The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology 145, 3013–3021CrossRefGoogle ScholarPubMed
Judd, R. S. and Shafer, W. M. (1989). Topographical alterations in proteins I of Neisseria gonorrhoeae correlated with lipooligosaccharide variation. Molecular Microbiology 3, 637–642CrossRefGoogle ScholarPubMed
Kasper, D. L., Winkelhake, J. L., Zollinger, W. D., Brandt, B. L., and Artenstein, M. S. (1973). Immunological similarity between polysaccharide antigens of Escherichia coli O7:K1 (L): NM and group B Neisseria meningitidis. Journal of Immunology 110, 262–268Google Scholar
Kasper, D. L., Baker, C. J., Galdes, B., Katzenellenbogen, E., and Jennings, H. J. (1983). Immunological analysis and immunogenicity of the type II group B streptococccal capsular polysaccharide. Journal of Clinical Investigation 72, 260–269CrossRefGoogle Scholar
Kim, J. J., Zhau, D., Mandrell, R. E., and Griffiss, J. M. (1992). Effects of endogenous sialylation of the lipooligosaccharide of Neisseria gonorrhoeae on opsonophagocytosis. Infection and Immunity 60, 4439–4442Google Scholar
Kimura, A. and Hansen, E. J. (1986). Antigenic and phenotypic variations of Haemophilus influenzae type b lipopolysaccharide and their relationship to virulence. Infection and Immunity 51, 69–79Google ScholarPubMed
Kupsch, E.-M., Knepper, B., Kuroki, T., Heuer, I., and Meyer, T. F. (1993). Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. European Molecular Biology Organisation Journal 12, 641–650Google ScholarPubMed
Lewis, L. A., Gipson, M., Hartman, K., Ownbey, T., Vaughn, J., and Dyer, D. W. (1999). Phase variation of HpuAB and HmbR, two distinct haemoglobin receptors of Neisseria meningitidis DNM2. Molecular Microbiology 32, 977–989CrossRefGoogle ScholarPubMed
McNeil, G., Virji, M., and Moxon, E. R. (1994). Interactions of Neisseria meningitidis with human monocytes. Microbial Pathogenesis 16, 153–163CrossRefGoogle ScholarPubMed
Meleney, H. E. (1928). Relapse phenomena of Spironema recurrentis. Journal of Experimental Medicine 48, 65–82CrossRefGoogle ScholarPubMed
Mertsola, J., Cope, L. D., Saez-Lorenz, X., Ramilo, O., Kennedy, W., McCraken, G. H. Jr., and Hansen, E. J. (1991). In vivo and in vitro expression of Haemophilus influenzae type b lipooligosaccharide epitopes. Journal of Infectious Diseases 164, 555–563CrossRefGoogle ScholarPubMed
Moxon, E. R., Rainey, P. B., Nowak, M. A., and Lenski, R. E. (1994). Adaptive evolution of highly mutable loci in pathogenic bacteria. Current Biology 4, 24–33CrossRefGoogle ScholarPubMed
Munkley, A., Tinsley, R., Virji, M., and Heckels, J. E. (1991). Blocking of bactericidal killing of Neisseria meningitidis by antibodies directed against class 4 outer membrane protein. Microbial Pathogenesis 11, 447–452CrossRefGoogle ScholarPubMed
Nassif, X., Beretti, J.-L., Lowy, J., Stenberg, P., O'Gaora, P., Pfeifer, J., Normark, S., and So, M. (1994). Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proceedings of the National Academy of Sciences USA 91, 3769–3773CrossRefGoogle ScholarPubMed
Nicholson, A. and Lepow, I. H. (1979). Host defence against Neisseria meningitidis requires a complement-dependent bactericidal activity. Science 205, 298–299CrossRefGoogle Scholar
Nicholson, T. L. and Baumler, A. J. (2001). Salmonella enterica serotype typhimurium elicits cross-immunity against a Salmonella enterica serotype enteritidis strain expressing LP fimbriae from the lac promoter. Infection and Immunity 69, 204–212CrossRefGoogle ScholarPubMed
Nikaido, H. (1996). Outer membrane. In Escherichia coli and Salmonella, 2nd ed., ed. F. C. Neidhardt. pp. 29–47. Washington, DC: ASM Press
Norris, T. L. and Baumler, A. J. (1999). Phase variation of the lpf operon is a mechanism to evade cross-immunity between Salmonella serotypes. Proceedings of the National Academy of Sciences USA 96, 13,393–13,398CrossRefGoogle ScholarPubMed
Parsons, N. J., Andrade, J. R. C., Patel, P. V., Cole, J. A., and Smith, H. (1989). Sialylation of lipopolysaccharide and loss of absorption of bactericidal antibody during conversion of gonococci to serum resistance by cytidine 5′-monophospho-N-acetyl neuraminic acid. Microbial Pathogenesis 7, 63–72CrossRefGoogle ScholarPubMed
Parsons, N. J., Cole, J. A., and Smith, H. (1990). Resistance to human serum of gonococci in urethral exudates is reduced by neuraminidase. Proceedings of Royal Society of London B 241, 3–5CrossRefGoogle ScholarPubMed
Poolman, J. T., Marie, S., and Zanen, H. C. (1980). Variability of low-molecular-weight, heat-modifiable outer membrane proteins of Neisseria meningitidis. Infection and Immunity 30, 642–648Google ScholarPubMed
Poolman, J. T., Timmermans, H. A. M., Hopman, C. T. P., Teerlink, T., van Vught, P. A. M., Witvliet, M. H., and Beuvery, E. C. (1988). In Gonococci and Meningococci, ed. J. T. Poolman, H. C. Znen, T. F. Meyer, J. E. Heckels, P. R. H. Makela, H. Smith and E. C. Bauvery. pp. 159–166. Dortrecht: Kluwer Academic
Read, R. C., Zimmerli, S., Broaddus, V. C., Sanan, D. A., Stephens, D. S., and Ernst, J. D. (1996). The (α2 → 8)-linked polysialic acid capsule of group B Neisseria meningitidis modifies multiple steps during interaction with human macrophages. Infection and Immunity 64, 3210–3217Google Scholar
Rest, R. F. and Frangipane, J. V. (1992). Growth of Neisseria gonorrhoeae in CMP-N-acetylneuraminic acid inhibits nonopsonic (opacity-associated outer membrane protein-mediated) interactions with human neutrophils. Infection and Immunity 60, 989–997Google ScholarPubMed
Risberg, A., Schweda, E. K. H., and Jansson, P.-E. (1997). Stuctural studies of the cell-envelop oligosaccharide from lipopolysaccharide of Haemophilus influenzae strain RM 118–28. European Journal of Biochemistry 243, 701–707CrossRefGoogle Scholar
Rosengarten, R. and Wise, K. S. (1990). Phenotypic switching in Mycoplasmas: Phase variation of diverse surface lipoproteins. Science 247, 315–318CrossRefGoogle ScholarPubMed
Rosengarten, R. and Wise, K. S. (1991). The Vlp system of Mycoplasma hyorhinis: combinatorial expression of distinct size variant lipoproteins generating high-frequency surface antigenic variation. Journal of Bacteriology 173, 4782–4793CrossRefGoogle ScholarPubMed
Rosengarten, R., Behrens, A., Stetefeld, A., Heller, M., Ahrens, M., Sachse, K., Yogev, D., and Kirchhoff, H. (1994). Antigenic heterogeneity among isolates of Mycoplasma bovis is generated by high-frequency variation of diverse membrane surface proteins. Infection and Immunity 62, 5066–5074Google ScholarPubMed
Rudel, T., Putten, J. P. M., Gibbs, C. P., Haas, R., and Meyer, T. F. (1992). Interaction of two variable proteins (PilE and PilC) required for pilus mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Molecular Microbiology 6, 3439–3450CrossRefGoogle ScholarPubMed
Rudel, T., Boxberger, H.-J., and Meyer, T. F. (1995). Pilus biogenesis and epithelial adherence of Neisseria gonorrhoeae pilC double knock-out mutants. Molecular Microbiology 17, 1057–1071CrossRefGoogle ScholarPubMed
Sarkari, J., Pandit, N., Moxon, E. R., and Achtman, M. (1994). Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Molecular Microbiology 13, 207–217CrossRefGoogle ScholarPubMed
Saunders, N. J., Peden, J. F., Hood, D. W., and Moxon, E. R. (1998). Simple sequence repeats in the Helicobacter pylori genome. Molecular Microbiology 27, 1091–1098CrossRefGoogle ScholarPubMed
Saunders, N. J., Jeffries, A. C., Peden, J. F., Hood, D. W., Tettelin, H., Rappouli, R., and Moxon, E. R. (2000). Repeat associated phase variable genes in the complete genome sequence of Neisseria meningitidis. Molecular Microbiology 37, 207–215CrossRefGoogle ScholarPubMed
Saunders, N. J., Moxon, E. R., and Gravenor, M. (2002a). The determination of mutation rates associated with phase variation. – submitted
Saunders, N. J., Moxon, E. R., and Gravenor, M. (2002b). The influence of phase variation and selection on population structure. – submitted
Schneider, H., Hammack, C. A., Apicella, M. A., and Griffiss, J. M. (1988). Instability of expression of lipooligosaccharides and their epitopes in Neisseria gonorrhoeae. Infection and Immunity 56, 942–946Google ScholarPubMed
Schneider, H., Griffiss, J. M., Boslego, J. W., Hitchcock, P. J., Zahos, K. M., and Apicella, M. A. (1991). Expression of paragloboside-like lipooligosaccharides may be a necessary component of gonococcal pathogenesis in men. Journal of Experimental of Medicine 174, 1601–1605CrossRefGoogle ScholarPubMed
Schryvers, A. B. and Stojiljkovic, I. (1999). Iron acquisition systems in the pathogenic Neisseria. Molecular Microbiology 32, 1117–1123CrossRefGoogle ScholarPubMed
Schweda, E. K. H., Masoud, H., Martin, A., Risberg, A., Hood, D. W., Moxon, E. R., Weiser, J. N., and Richards, J. C. (1997). Phase variable expression and characterisation of phosphorylcholine oligosaccharide epitopes in Haemophilus influenzae lipopolysaccharides. Glycoconjugate Journal 14 (Suppl), S23Google Scholar
Smith, H. (1991). The Leeuwenhoek Lecture, 1991. The influence of the host on microbes that cause disease. Proceedings of Royal Society of London B 246, 97–105CrossRefGoogle ScholarPubMed
Sparling, P., Cannon, J., and So, M. (1986). Phase and antigenic variation of pili and outer membrane protein II of Neisseria gonorrhoeae. Journal of Infectious Diseases 153, 196–201CrossRefGoogle ScholarPubMed
Stephens, D. S. and McGee, Z. A. (1981). Attachment of Neisseria meningitidis to human mucosal surfaces: influence of pili and type of receptor cell. Journal of Infectious Diseases 143, 525–532CrossRefGoogle ScholarPubMed
Stephens, D. S., Spellman, P. A., and Swartley, J. S. (1993). Effect of the (α2→8) -linked polysialic acid capsule on adherence of Neisseria meningitidis to human mucosal cells. Journal of Infectious Diseases 167, 475–479CrossRefGoogle Scholar
Stern, A., Nickel, P., Meyer, T., and So, M. (1984). Opacity determinants of Neisseria gonorrhoeae: gene expression and chromosomal linkage to the gonoccocal pilus gene. Cell 37, 447–456CrossRefGoogle Scholar
Stern, A., Brown, M., Nickel, P., and Meyer, T. (1986). Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47, 61–71CrossRefGoogle ScholarPubMed
Stoenner, H. G., Dodd, T., and Larsen, C. (1982). Antigenic variation in B. hermsii. Journal of Experimental Medicine 156, 1297–1311CrossRefGoogle Scholar
Tettelin, H., Saunders, N. J., Heidelberg, J., Jeffries, A. C., Nelson, K. E., and 37 other authors. (2000). The complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287, 1809–1815CrossRefGoogle ScholarPubMed
Tommassen, J., Vermeij, P., Struyve, M., Benz, R., and Poolman, J. T. (1990). Isolation of Neisseria meningitidis mutants deficient in class 1 (PorA) and class 3 (PorB) outer membrane proteins. Infection and Immunity 58, 1355–1359Google ScholarPubMed
Belkum, A., Scherer, S., Leeuwen, W., Willemse, D., Alphen, L., and Verbrugh, H. (1997a). Variable number of tandem repeats in clinical strains of Haemophilus influenzae. Infection and Immunity 65, 5017–5027Google Scholar
Belkum, A., Melchers, W. J. G., Ijsseldijk, C., Nohlmans, L., Verbuch, H., and Meis, J. F. G. M. (1997b). Outbreak of amoxycillin-resistant Haemophilus influenzae type b: variable number of tandem repeats as novel molecular markers. Journal of Clinical Microbiology 35, 1517–1520Google Scholar
Ende, A., Hopman, C. T. P., Zaat, S., Oude, Essink B. B., Berkhout, B., and Dankert, J. (1995). Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the – 10 and – 35 regions of the promoter. Journal of Bacteriology 177, 2475–2480CrossRefGoogle ScholarPubMed
Putten, J. P. M. (1993). Phase variation of lipopolysaccharide directs interconversion of invasive and immuno-resistant phenotypes of Neisseria gonorrhoeae. European Molecular Biology Organisation Journal 12, 4043–4051Google ScholarPubMed
Putten, J. P. M. and Robertson, B. D. (1995). Molecular mechanisms and implication for infection of lipopolysaccharide variation in Neisseria. Molecular Microbiology 16, 847–853CrossRefGoogle Scholar
Virji, M., Kayhty, H., Fergusson, D. J. P., Alexandrescu, C., Heckles, J. E., and Moxon, E. R. (1991). The role of pilin in the interactions of pathogenic Neisseria with cultured human endothelial cells. Molecular Microbiology 5, 1831–1841CrossRefGoogle Scholar
Virji, M., Alexandrescu, C., Fergusson, D. J. P., Saunders, J. R., and Moxon, E. R. (1992). Variations in the expression of pili: the effect on adherence of Neisseria meningitidis to human epithelial and endothelial cells. Molecular Microbiology 6, 1271–1279CrossRefGoogle ScholarPubMed
Virji, M., Makepeace, K., Ferguson, D. J., Achtman, M., and Moxon, E. R. (1993a). Menigococcal Opa and Opc proteins: their role in colonisation and invasion of human epithelial and endothelial cells. Molecular Microbiology 10, 499–510CrossRefGoogle Scholar
Virji, M., Saunders, J. R., Sims, G., Makepeace, K., Maskell, D., and Ferguson, D. J. P. (1993b). Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in the primary amino acid sequence and the glycosylation status of pilin. Molecular Microbiology 10, 1013–1028CrossRefGoogle Scholar
Waldbeser, L. S., Ajioka, R. S., Merz, A. J., Puaoi, D., Lin, L., Thomas, M., and So, M. (1994). The OpaH locus of Neisseria gonorrhoeae MS11A is involved in epithelial cell invasion. Molecular Microbiology 13, 919–928CrossRefGoogle ScholarPubMed
Weel, J. F. L., Hopman, C. T. P., and Putten, J. P. M. (1989). Stable expression of lipooligosaccharide antigens during attachment, internalization, and intracellular processing of Neisseria gonorrhoeae in infected epithelial cells. Infection and Immunity 57, 3395–3402Google ScholarPubMed
Weiser, J. N., Lindberg, A. A., Manning, E. J., Hansen, E. J., and Moxon, E. R. (1989). Identification of a chromosomal locus for expression of lipopolysaccharide epitopes in Haemophilus influenzae. Infection and Immunity 57, 3945–3052Google ScholarPubMed
Weiser, J. N., Shchepetov, M., and Chong, S. T. H. (1997). Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infection and Immunity 65, 943–950Google ScholarPubMed
Weiser, J. N. and Pan, N. (1998). Adaptation of Haemophilus influenzae to acquired and innate humoral immunity based on phase variation of lipopolysaccharide. Molecular Microbiology 30, 767–775CrossRefGoogle ScholarPubMed
Weiser, J. N., Pan, N., McGowan, K. L., Musher, D., Martin, A., and Richards, J. (1998a). Phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae contributes to persistance in the respiratory tract and sensitivity to serum killing mediated by C-reactive protein. Journal of Experimental Medicine 187, 631–640CrossRefGoogle Scholar
Wise, K. S. (1993). Adaptive surface variation in mycoplasmas. Trends in Microbiology 1, 59–63CrossRefGoogle ScholarPubMed
Yogev, D., Rosengarten, R., Watson-McKown, R., and Wise, K. S. (1991). Molecular basis of Mycoplasma surface antigenic variation: a novel set of divergent genes undergo spontaneous mutation of periodic coding regions and 5′ regulatory sequences. European Molecular Biology Organisation Journal 10, 4069–4079Google ScholarPubMed
Yogev, D., Watson-McKown, R., Rosenbgarten, R., Im, J., and Wise, K. S. (1995). Increased structural and combinatorial diversity in an extended family of genes encoding Vlp surface proteins of Mycoplasma hyorhinis. Journal of Bacteriology 177, 5636–5643CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×