Mycoplasma Interaction with Eukaryotic Cells

  • Shlomo Rottem
  • David Yogev
Part of the Subcellular Biochemistry book series (SCBI, volume 33)

Abstract

Mollicutes are the smallest and simplest self-replicating prokaryotes. These microorganisms lack a rigid cell wall and are bound by a single membrane, the plasma membrane (Razin et al., 1998). Wall-less prokaryotes were first described 100 years ago and now over 180 species, widely distributed among humans, animals, insects and plants are known (Razin et al., 1998). The lack of a cell wall is used to distinguish these microorganisms from ordinary bacteria and to include them in a separate class named Mollicutes. Most human and animal mollicutes are Mycoplasma and Ureaplasma species of the family Mycoplasmataceae. The trivial name mycoplasmas will be used by us to denote any organisms within this family. Mycoplasmas have an extremely small genome size of 0.58–1.35 mb (compared with the 4.64 mb of E. coli). Over the last three years the genomes of Mycoplasma genitalium (0.58mb) and Mycoplasma pneumoniae (0.816mb) have been sequenced (Himmelreich et al., 1996; Fraser et al., 1995), showing only 470 and 500 protein coding regions respectively. Their small genomes impose on these organisms limited metabolic options for replication and survival (Himmelreich et a1.,1997; Pollack et al., 1997).

Keywords

Antigenic Variation Mycoplasma Pneumoniae Phenotypic Switching Ureaplasma Urealyticum Mycoplasma Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Almagor, M., Kahane, I., Gilon, C., and Yatziv, S., 1986, Protective effects of the glutathione redox cycle and vitamin E on cultured fibroblasts infected by Mycoplasma pneumoniae, Infect. Immun. 52: 240–244.Google Scholar
  2. Andreev J., Borovsky, Z., Rosenshine, I., and Rottem, S., 1995, Invasion of HeLa cells by-Mycoplasma penetrans and the induction of tyrosine phosphorylation of a 145 kDa host cell protein, FEMS Leu. 132: 189–194.CrossRefGoogle Scholar
  3. Baseggio, N., Glew, M.D., Markham, P.R. Whithear, K.G., and Browning, G.F., 1996, Size and genomic location of the pMGA multigene family of Mycoplasma gallisepticum, Microbiology 142: 1429–1435.Google Scholar
  4. Baseman, J.B., 1993, The cytadhesins of Mycoplasma pneumoniae and Mycoplasma genitalium, in Subcellular Biochemistry, Volume 20 ( S. Rottem, and I. Kahane, eds), Plenum Press, New York, pp. 243–259.Google Scholar
  5. Baseman, J.B., Lange, M., Criscimagna, N.L., Giron, J.A., and Thomas, C.A., 1995, Interplay between mycoplasmas and host target cells, Microb. Pathog. 19: 105–116.PubMedCrossRefGoogle Scholar
  6. Baseman, J.B., Reddy, S.P., and Dallo, S.F. 1996, Interplay between mycoplasma surface proteins, airway cells, and the protein manifestations of mycoplasma-mediated human infections, Am. J. Resp. Crit. Care Med. 154: S137 — S144.PubMedGoogle Scholar
  7. Baseman, J.B., and Tülly, J.G., 1997, Mycoplasmas: sophisticated, reemerging, and burdened by their notoriety, Emerg. Infect. Dis. 3: 21–32.Google Scholar
  8. 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, Infect. Immun. 62: 5075–5084.Google Scholar
  9. Bhugra, B., and Dybvig, K., 1992, High-frequency rearrangements in the chromosome of Mycoplasma pulmonis correlate with phenotypic switching, Mol. Microbiol. 6: 1149–1154.PubMedCrossRefGoogle Scholar
  10. Bhugra, B., Voelker, L.L., Zou, N., Yu, H., and Dybvig, K., 1995, Mechanism of antigenic variation in Mycoplasma pulmonis: interwoven, site-specific DNA inversions, Mol. Microbiol. 18: 703–714.PubMedCrossRefGoogle Scholar
  11. Borovsky, Z., Tarshis, M., Zhang, P., and Rottem, S., 1998, Mycoplasma penetrans invasion of HeLa cells induces protein kinase C activation and vacuolation in the host cells, J. Med. Microbiol. 47: 915–922.Google Scholar
  12. Brenner, C., Neyrolles, O., and Blanchard, A., 1996, Mycoplasmas and HIV infection: From epidemiology to their interaction with immune cells, Front. Biosci. 1: 42–54.Google Scholar
  13. Citti, C., and Wise, K.S., 1995, Mycoplasma hyorhinis yip gene transcription: critical role in phase variation and expression of surface lipoproteins, Mol. Microbiol. 18: 649–660.Google Scholar
  14. Citti, C., Kim, M.F., and Wise, K.S., 1997, Elongated versions of Vlp surface lipoproteins protect Mycoplasma hyorhinis escape variants from growth-inhibiting host antibodies, Infect. Immun. 65: 1773–1785.PubMedGoogle Scholar
  15. Citovsky, V., Rottem, S., Nussbaum, O., Rott, R., and Loyter, A., 1987, Animal viruses are able to fuse with prokaryotic cells: fusion between Sendai or Influenza virions and Mycoplasma, J. Biol. Chem. 263: 461–468.Google Scholar
  16. Cole, B.C., Knudtson, K.L., Oliphant, A., Sawitzke, A.D., Pole, A., Manohar, M., Benson, L.S., Ahmed, E., and Atkin, C.L., 1996, The sequence of the Mycoplasma arthritidis superanti-gen, MAM: identification of functional domains and comparison with microbial super-antigens and plant lectin mitogens, J. Exp. Med. 183: 1105–1110.PubMedCrossRefGoogle Scholar
  17. Dallo, S.F., Chavoya, A., and Baseman, J.B., 1990, Characterization of the gene for a 30kDa adhesin-related protein of Mycoplasma pneumoniae, Infect. Immun. 58: 4163–4165.PubMedGoogle Scholar
  18. DeBey, M.C., and Ross R.F., 1994, Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ cultures, Infect. Immun. 62: 5312–5318.PubMedGoogle Scholar
  19. DiRita, V.J., and Mekalanos, J.J., 1989, Genetic regulation of bacterial virulence, Annu. Rev.Genet. 23: 455–482.PubMedCrossRefGoogle Scholar
  20. Dong, Q., Sadouk, A., van der Lelie, D., Taghavi, A., Ferhat, A., Mutten, A., Borremans, B., Mergeay, M., and Toussaint, A., 1992, Cloning and sequencing of IS1086, an Alcaligenes eutrophus insertion element related to IS30 and íS4351, J. Bacteriol. 174: 8133–8138.PubMedGoogle Scholar
  21. Dramsi, S., Dehoux, P., and Cossart, P., 1993, Common features of gram-positive bacterial proteins involved in cell recognition, Mol. Microbiol. 9: 1119–1121.PubMedCrossRefGoogle Scholar
  22. Dybvig, K., 1993, DNA rearrangements and phenotypic switching in prokaryotes, Mol. Microbiol. 10: 465–471.PubMedCrossRefGoogle Scholar
  23. Elsinghorst, E.A., 1994, Measurement of invasion by gentamicin resistance, Methods Enzymol. 236: 405–420.PubMedCrossRefGoogle Scholar
  24. Finlay, B.B., and Falkow, S., 1988, Comparison of the invasion strategies used by Salmonella choleraesuis. Shigelia flexneri and Yersina enterocolitica to enter cultured animal cells: endosomic acidification is not required for bacterial invasion or intracellular replication, Biochimie 80: 248–254.Google Scholar
  25. Finlay, B.B., Ruschkowski, S., and Dedhar, S., 1991, Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells, J. Cell Sci. 99: 283–296.PubMedGoogle Scholar
  26. Franzoso, G., Dimitrov, D.S., Blumenthal, R., Barile, M.F., and Rottem, S., 1992, Fusion of M. fermentans, strain incognitus, with T-lymphocytes, FEBS Lett. 303: 251–254.PubMedCrossRefGoogle Scholar
  27. Franzoso, G., Hu, P-C., Meloni, G., and Barile, M.R., 1994, Immunoblot analysis of chimpanzee sera after infection and after immunization and challenge with Mycoplasma pneumoniae, Infect. Immun. 62: 1008–1014.PubMedGoogle Scholar
  28. Fraser, C.M., Gocayne, J.D., White, O., Adams, M.D., Clayton, R.A., Fleischmann, R.D., Bult, C.J., Kerlavage, A.R., Sutton, G., Kelly, J.M., Fritchman, J.L., Weidman, J.F., Small, K.V., Sandusky, M., Fuhrmann, J., Nguyen, D., Utterback, T.R., Saudek, D.M., Phillips, C.A., Merrick, J.M., Tomb, J.-E, Dougherty, B.A., Bott, K.F., Hu, P.-C., Lucier, T.S., Petterson, S.N., Smith, H.O., Hutchison, C.A. III, and Venter, J.C., 1995, The minimal gene complement of Mycoplasma genitalium, Science 270: 397–403.PubMedCrossRefGoogle Scholar
  29. Geary, S.J., and Gabridge, M.G., 1987, Characterization of a human lung fibroblast receptor site for Mycoplasma pneumoniae, Isr. J. Med. Sci. 23: 462–468.PubMedGoogle Scholar
  30. Geary, S.J., Gabridge, M.G., Intres, R., D.L., Draper, R., and Gladd, M.F., 1990, Identification of mycoplasma binding proteins utilizing a 100 kilodalton lung fibroblast receptor, J. Rec. Res. 9: 465–478.Google Scholar
  31. Girón, J.A., Lange, M., and Baseman, J.B., 1996, Adherence, fibronectin binding, and induction of cytoskeleto reorganization in cultured human cells by Mycoplasma penetrans, Infect. Immun. 64: 197–208.Google Scholar
  32. Glew, M.D., Markham, P.F., Browning, G.E. and Walker, í.D.,1995, Expression studies on four members of the pMGA multigene family in Mycoplasma gallisepticum S6, Microbiology 141: 3005–3014.Google Scholar
  33. Glew, M.D., 1997, Gene expression studies of pMGA, A surface protein of Mycoplasma gallisepticum, Ph. D. Thesis, The University of Melbourne.Google Scholar
  34. Guzman, C.A., Rohde, M., and Timmis, K.N., 1994, Mechanisms involved in uptake of Bordetella bronchiseptica by mouse dendritic cells, Infect. Immun. 62: 5538–5544.Google Scholar
  35. Hahn, T.-W, Willby, M.J., and Krause, D.C., 1998, HMW1 is required for cytadhesin P1 trafficking to the attachment organelle in Mycoplasma pneumoniae, J. Bacteriol. 180: 1270–1276.PubMedGoogle Scholar
  36. Henderson, B., Poole, S., and Wilson, M., 1996, Bacterial modulins: a novel class of virulence factors which cause host tissue pathology by inducing cytokine synthesis, Microbiol. Rev. 60: 316–341.PubMedGoogle Scholar
  37. Himmelreich, R., Hilbert, H., Plagens, H., Pirkl, E., Li, B.-C., and Herrmann, R., 1996, Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae, Nucleic Acids Res. 24: 4420–4449.PubMedCrossRefGoogle Scholar
  38. Himmelreich, R., Plagens, H., Hilbert, H., Reiner, B., and Herrman, R., 1997, Comparative analysis of the genomes of the bacteria Mycoplasma pneumoniae and Mycoplasma genitalium, Nucleic Acids Res. 25: 701–712.PubMedCrossRefGoogle Scholar
  39. Hollingshead, S.K., Fischetti, V.A., and Scott, J.R., 1987, Size variation in group A streptococcal M protein is generated by homologous recombination between intragenic repeats, Mol. Gen. Genet. 207: 196–203.PubMedCrossRefGoogle Scholar
  40. Inamine, J.M., Denny, TP., Loechel, S., Schaper, U., Huang, C.-H., Bott, K.F., and Hu, P.-C., 1988, Nucleotide sequence of the P1 attachment-protein gene of Mycoplasma pneumoniae, Gene 64: 217–229.PubMedCrossRefGoogle Scholar
  41. Kehoe, M.A., 1994, Cell-wall-associated proteins in gram-positive bacteria, in: Bacterial cell wall ( J-M. Ghuysen, and R. Hakenbeck, eds.), Elsevier Biomedical Press, Amsterdam, pp. 217–261.CrossRefGoogle Scholar
  42. Kelly, R.B., 1990, Microtubules, membrane traffic, and cell organization, Cell 61: 5–7.PubMedCrossRefGoogle Scholar
  43. Krause, D.C., Leith, D.K., Wilson, R.M., and Baseman, J.B., 1982, Identification of Mycoplasma pneumoniae proteins associated with hemadsorption and virulence, Infect. Immun. 35: 809–817.PubMedGoogle Scholar
  44. Krause, D.C., 1996, Mycoplasma pneumoniae cytadherence: unravelling the tie that binds, Mol. Microbiol. 20: 247–253.Google Scholar
  45. Krivan, H.C., Olson, L.D., Barile, M.F., Ginsburg, V., and Roberts, D.D., 1989, Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate, J. Biol. Chem. 264: 9283–9288.PubMedGoogle Scholar
  46. Layh-Schmitt, G., and Herrmann, R., 1994, Spatial arrangement of gene products of the P1 operon in the membrane of Mycoplasma pneumoniae, Infect. Immun. 62: 974–979.PubMedGoogle Scholar
  47. Levinson, G., and Gutman, G.A., 1987, Slipped-strand mispairing: A major mechanism for DNA sequence evolution, Mol. Biol. Evol. 4: 203–221.PubMedGoogle Scholar
  48. Lysnyansky, L, Rosengarten, R., and Yogev, D., 1996, Phenotypic switching of variable surface lipoproteins in Mycoplasma bovis involves high-frequency chromosomal rearrangements, J. Bacteriol. 178: 5395–5401.PubMedGoogle Scholar
  49. Lo, S.C., 1992, Mycoplasmas in AIDS, in Mycoplasmas: molecular biology and pathogenesis ( J. Maniloff, R.N. McElhaney, L.R. Finch, and J.B. Baseman, eds.), American Society for Microbiology, Washington, D.C., pp. 525–548.Google Scholar
  50. Lo, S.C., Hayes, M.M., and Kotani, H., Pierce, P.F., Wear, D.J., Newton, P.B., Tully, J.G., and Shih, J.W-K., 1993, Adhesion onto and invasion into mammalian cells by Mycoplasma pene-trans: a newly isolated mycoplasma from patients with AIDS., Mod. Pathol. 6: 276–280.Google Scholar
  51. Loveless, R.W., and Feizi, T., 1989, Sialo-oligosaccharide receptors for Mycoplasma pneumoniae and related oligosaccharides of poly-N-acetyllactosamine series are polarized at the cilia and apicalmicrovillar domains of the ciliated cells in human bronchial epithelium, Infect. Immun. 57: 1285–1289.PubMedGoogle Scholar
  52. Markham, P.F., Glew, M.D., Sykes, J.E., Bowden, T.R., Pollocks, T.D., Browning, G.F., Whithear, K.G., and Walker, I.D., 1994, The organization of the multigene family which encodes the major cell surface protein, pMGA, of Mycoplasma gallisepticum, FEBS Lett. 352: 347–352.PubMedCrossRefGoogle Scholar
  53. Marshall, A.J., Miles, R.J., and Richards, L., 1995, The phagocytosis of mycoplasmas, J. Med. Microbiol. 43: 239–250.PubMedCrossRefGoogle Scholar
  54. Metzger, J.W., Beck-Sickinger, A.G., Loleit, M., Eckert, M., Bessler, W.G., Jung, G., 1995, Synthetic S-(2,3-dihydroxypropyl)-cysteinyl peptides derived from the N-terminus of the cytochrome subunit of the photoreaction centre of Rhodopseudomonas viridis enhance murine splenocyte proliferation, J. Pept. Sci. 3: 184–190.CrossRefGoogle Scholar
  55. Miihlradt, P.F., and Frisch, M., 1994, Purification and partial biochemical characterization of a Mycoplasma fermentans derived substance that activates macrophages to release nitric oxide, tumor necrosis factor, and interleukin-6, Infect. Immun. 62: 3801–3807.Google Scholar
  56. Milhlradt, P.F., Meyer, H., and Jansen, R., 1996, Identification of S-(2,3-dihydroxypropyl) cystein in a macrophage-activating lipopeptide from Mycoplasma fermentans, Biochemistry 35: 7781–7786.CrossRefGoogle Scholar
  57. Pollack, J.D., Williams, M.V., and McElhaney, R.N., 1997, The comparative metabolism of the mollicutes (mycoplasmas): The utility for taxonomic classification and the relationship of putative gene annotation and phylogeny to enzymatic function, Crit. Rev. Microbiol. 23: 269–354.PubMedCrossRefGoogle Scholar
  58. Popham, P.L., Hahn, T.-W., Krebes, K.A., and Krause, D.C., 1997, Loss of HMW1 and HMW3 in noncytadhering mutants of Mycoplasma pneumoniae occurs posttranslationally, Proc. NatL Acad. ScL USA 94: 13979–13984.CrossRefGoogle Scholar
  59. Rainey, P.B., Moxon, E.R., and Thompson, I.P., 1993, Intraclonal polymorphism in bacteria, Advan. Microb. Ecol. 13: 263–300.CrossRefGoogle Scholar
  60. Razin, S., and Jacobs, E., 1992, Mycoplasma adhesion, J. Gen. Microbiol. 138: 407–422.PubMedGoogle Scholar
  61. Razin, S., Yogev, D., and Naot, Y., 1998, Molecular biology and pathogenicity of mycoplasmas, MicrobioL. Rev. 62: 1094–1156.Google Scholar
  62. Roberts, D.D., Olson, L.D., Barile, M.F., Ginsburg, V., and Krivan, H.C., 1989, Sialic acid-dependent adhesion of Mycoplasma pneumoniae to purified glycoproteins, J. Biol. Chem. 264: 9289–9293.PubMedGoogle Scholar
  63. Robertson, B.D., and Meyer, T.F., 1992, Genetic variation in pathogenic bacteria, Trends Genet. 8: 422–427.PubMedGoogle Scholar
  64. Rosengarten, R., and Wise, K., 1990, Phenotypic switching in mycoplasmas: Phase variation of diverse surface lipoproteins, Science 247: 315–318.PubMedCrossRefGoogle Scholar
  65. Rosengarten, R., and Wise, K., 1991, The Vlp system of Mycoplasma hyorhinis: combinatorial expression of distinct size variant lipoproteins generating high-frequency surface antigenic variation, J. Bacteriol. 173: 4782–4793.PubMedGoogle Scholar
  66. Rosengarten, R., Behrens, A., Stetefeld, A., Heller, M., Ahrens, M., Sachse, K., Yogev, D., and Kirchhoff, H., 1994, Antigen heterogeneity among isolates of Mycoplasma bovis is generated by high-frequency variation of diverse membrane surface proteins, Infect. Immun. 62: 5066–5074.PubMedGoogle Scholar
  67. Rosenshine, I., and Finlay, B.B., 1993, Exploitation of host signal transduction pathways and cytoskeletal functions by invasive bacteria, BioEssays 15: 17–24.PubMedCrossRefGoogle Scholar
  68. Rottem, S., and Barile, M.F., 1993, Beware of mycoplasmas, Trends Biotechnol. 11: 143–151.PubMedCrossRefGoogle Scholar
  69. Rottem, S., and Naot, Y., 1998, Subversion and exploitation of host cells by mycoplasmas, Trends Microbiol. 6: 436–440.PubMedCrossRefGoogle Scholar
  70. Salman, M., Deutsch, I., Tarshis, M., Naot, Y., and Rottem, S., 1994, Membrane lipids of Mycoplasma fermentans, FEMS Microbiol. Leu. 123: 255–260.CrossRefGoogle Scholar
  71. Salman, M., and Rottem, S., 1995, The cell membrane of Mycoplasma penetrans: Lipid composition and phospholipase AI activity, Biochim. Biophys. Acta 1235: 369–377.PubMedCrossRefGoogle Scholar
  72. Salman, M., Borovsky, Z., and Rottem, S., 1998, Mycoplasma penetrans invasion of Molt-3 lymphocytes induces changes in the lipid composition of host cells, Microbiology 144: 3447–3454.Google Scholar
  73. Shaw, J.H., and Falkow, S., 1988, Model for invasion of human tissue culture cells by Neisseria ghonorrhoeae, Infect. Immun. 56: 1625–1632.PubMedGoogle Scholar
  74. Shibata, K.-I., Mamoru, N., Yoshihiko, S., and Tsuguo, W, 1994, Acid phosphatase purified from Mycoplasma fermentans has protein tyrosine phosphatase-like activity, Infect. Immun. 62: 313–315.PubMedGoogle Scholar
  75. Shibata, K.-I., Sasaki, T., and Watanabe, T., 1995, AIDS-Associated mycoplasmas possess phospholipases C in the membrane, Infect. Immun. 63: 4174–4177.PubMedGoogle Scholar
  76. Simmons, W.L., Zuhua, C., Glass, J.I., Simecke, J.W., Cassell, G.H., and Watson, H.L., 1996, Sequence analysis of the chromosomal region around and within the V-1-encoding gene of Mycoplasma pulmonis: Evidence for DNA inversion as a mechanis for V-1 variation, Infect. Immun. 64: 472–479.PubMedGoogle Scholar
  77. Stevens, M.K., and Krause, D.C., 1991, Localization of the Mycoplasma pneumoniae cytadherence-accessory proteins HMW1 and HMW4 in the cytoskeleton like triton shell, J. Bacteriol. 173: 1041–1050.PubMedGoogle Scholar
  78. Stevens, M.K., and Krause, D.C., 1992, Mycoplasma pneumoniae cytadherence phase-variable protein HMW3 is a component of the attachment organelle, J. Bacteriol. 174: 4265–4274.Google Scholar
  79. Su, C.J., Chavoya, A., and Baseman, J.B., 1989, Spontaneous mutation results in loss of the cytadhesin (P1) of Mycoplasma pneumoniae, Infect. Immun. 57: 3237–3239.PubMedGoogle Scholar
  80. Sutcliffe, I.C., and Russell, R.R., 1995, Lipoproteins of gram-positive bacteria, J. Bacteriol. 177: 1123–1128.PubMedGoogle Scholar
  81. Swanson, J., Belland, R.J., and Hill., S.A., 1992, Neisserial surface variation: how and why?, Curr. Opin. Genet. Develop. 2: 805–811.CrossRefGoogle Scholar
  82. Tarshis, M., Salman, M., and Rottem, S., 1993, Cholesterol is required for the fusion of single unilamellar vesicles with M. capricolum., Biophys. J. 64: 709–715.PubMedCrossRefGoogle Scholar
  83. Taylor-Robinson, D., Davies, H.A., Sarathchandra, P., and Furr, P.M., 1991, Intracellular location of mycoplasmas in cultured cells demonstrated by immunocytochemistry and electron microscopy, Inn. J. Exp. Patito!. 72: 705–714.Google Scholar
  84. Theiss, P., and Wise, K.S., 1997, Localized frameshift mutation generates selective, high-frequency phase variation of a surface lipoprotein encoded by a mycoplasma ABC transporter operon, J. Bacteriol. 179: 4013–4022.PubMedGoogle Scholar
  85. Wise, K.S., Yogev, D., and Rosengarten, R., 1992, Antigenic variation, in: Mycoplasmas: molecular biology and pathogenesis ( J. Maniloff, R.N. McElhaney, L.R. Finch, and J.B. Baseman, eds.), American Society for Microbiology, Washington, D.C., pp. 473–489.Google Scholar
  86. Wise, K.S.,1993, Adaptive surface variation in mycoplasmas, Trends. Microbiol. 1: 59–63.Google Scholar
  87. 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, EMBO J. 10: 4069–4079.PubMedGoogle Scholar
  88. Yogev, D., Watson, M.R., Rosengarten, R., Im, J., and Wise, K.M., 1995, Increased structural and combinatorial diversity in an extended family of genes encoding Vlp surface proteins of Mycoplasma hyorhinis, J. Bacteriol. 177: 5636–5643.PubMedGoogle Scholar
  89. Zähringer, U., Wagner, E, Rietschel, E.Th., Ben-Menachem, G., Deutsch, J., and Rottem, S., 1997, Primary structure of a new phosphocholine-containing glycoglycerolipid of Mycoplasma fermentans, J. Biol. Chem. 272: 26262–26270.PubMedCrossRefGoogle Scholar
  90. Zhang, Q., and Wise, K.S., 1996, Molecular basis of size and antigenic variation of a Mycoplasma hominis adhesin encoded by divergent vaa genes, Infect. Immun. 64: 2737–2744.PubMedGoogle Scholar
  91. Zhang, Q., and Wise, K.S., 1997, Localized reversible frameshift mutation in an adhesin gene confers a phase-variable adherence phenotype in mycoplasma, Mol. Microbiol. 25: 859–869.PubMedCrossRefGoogle Scholar
  92. Zheng, X., Teng, L.J., Watson, H.L., Glass, J.I., Blanchard, A., and Cassell, G.H., 1995, Small repeating units within the Ureaplasma urealyticum MB antigen gene encode serovar specificity and are associated with antigen size variation, Infect. Immun. 63: 891–898.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Shlomo Rottem
    • 1
  • David Yogev
    • 1
  1. 1.Department of Membrane and Ultrastructure ResearchThe Hebrew University-Hadassah Medical SchoolJerusalemIsrael

Personalised recommendations