Genetic Determination of Bacterial Virulence, with Special Reference to Salmonella

  • B. A. D. Stocker
  • P. H. Mäkelä
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 124)


“Virulence factor” or “virulence determinant” is often used to refer to bacterial traits, such as production of a surface component hindering phagocytosis, whose presence is noted to be correlated with virulence and whose loss, by mutation, etc., causes loss or great reduction in virulence in an experimental system. Logically any bacterial property indispensable for bacterial growth in the relevant compartment of the host, such as ability to grow at the temperature there prevalent, should be considered a virulence factor; we shall discuss such properties, as well as those commonly called virulence factors.


Phagocytic Cell Genetic Determination Capsular Polysaccharide Enteric Bacterium Live Vaccine 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson RP, Roth JR (1977) Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol 31: 473–505PubMedCrossRefGoogle Scholar
  2. Babior BM (1978) Oxygen-dependent microbial killing by phagocytes. New Engl J Med 298:659–668; 721–725PubMedCrossRefGoogle Scholar
  3. Bacon GA, Burrows TW, Yates M (1950a) The effects of biochemical mutation on the virulence of Bacterium typhosum: the induction and isolation of mutants. Br J Exp Pathol 31: 703–713PubMedGoogle Scholar
  4. Bacon GA, Burrows TW, Yates M (1950 b) The effect of biochemical mutation on the virulence of Bacterium typhosum: the virulence of mutants. Br J Exp Pathol 31: 714–724Google Scholar
  5. Bacon GA, Burrows TW, Yates M (1951) The effects of biochemical mutation on the virulence of Bacterium typhosum: the loss of virulence of certain mutants. Br J Exp Pathol 32: 85–96PubMedGoogle Scholar
  6. Benjamin WH Jr, Turnbough CL Jr, Posey BS, Briles DE (1985) The ability of Salmonella typhimurium to produce the iron gathering siderophore, enterobactin, is not a virulence factor in mouse typhoid. Infect Immun 50: 392–397PubMedGoogle Scholar
  7. Berche PA, Carter PB (1982) Calcium requirement and virulence of Yersinia enterocolitica. J Med Microbiol 15: 277–284PubMedCrossRefGoogle Scholar
  8. Bhakdi S, Tranum-Jensen J, Klump O (1980) The terminal membrane C5b-9 complex of human complement. Evidence for the existence of multiple protease-resistant polypeptides that form the transmembrane complement channel. J Immunol 124: 2451–2457PubMedGoogle Scholar
  9. Björnson AB, Björnson HS (1977) Activation of complement by opportunist pathogens and chemo-types of Salmonella minnesota. Infect Immun 16: 748–753PubMedGoogle Scholar
  10. Blanden RV, MacKaness GB, Collins FM (1966) Mechanisms of acquired resistance in mouse typhoid. J Exp Med 124: 585–600PubMedCrossRefGoogle Scholar
  11. Blumenstock E, Jann K (1981) Natural resistance of mice to Salmonella typhimurium: bactericidal activity and chemiluminescence response of murine peritoneal macrophages. J Gen Microbiol 125: 173–179PubMedGoogle Scholar
  12. Bölin I, Norlander L, Wolf-Watz H (1982) Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun 37: 506–512PubMedGoogle Scholar
  13. Brinton CC (1959) Non-flagellar appendages of bacteria. Nature 183: 782–786PubMedCrossRefGoogle Scholar
  14. Brubaker RR (1972) The genus Yersinia: biochemistry and genetics of virulence. Curr Top Microbiol Immunol 57: 111–158PubMedCrossRefGoogle Scholar
  15. Carsiotis M, Weinstein DL, Karch H, Holder I A, O’Brien AD (1984) Flagella of Salmonella typhimurium are a virulence factor in infected C57BL/6J mice. Infect Immun 46: 814–818PubMedGoogle Scholar
  16. Clegg S (1982) Cloning of genes determining the production of mannose-resistant fimbriae in a uropathogenic strain of Escherichia coli belonging to serogroup 06. Infect Immun 38: 739–744PubMedGoogle Scholar
  17. Coleman W, Leive L (1979) Two mutations which affect the barrier function of the Escherichia coli K-12 outer membrane. J Bacteriol 139: 899–910PubMedGoogle Scholar
  18. Collins FM (1969) Effect of immune mouse serum on the growth of Salmonella enteritidis in non-vaccinated mice challenged by various routes. J Bacteriol 97: 667–675PubMedGoogle Scholar
  19. Cooper GN, Fahey KJ (1970) Oral immunization in experimental salmonellosis. III. Behavior of virulent and temperature-sensitive mutant strains in the intestinal tissues of rats. Infect Immun 2: 192–200PubMedGoogle Scholar
  20. de Graaf FK, Klaasen-Boor P, van Hees JE (1980) Biosynthesis of the K99 surface antigen is repressed by alanine. Infect Immun 30: 125–128PubMedGoogle Scholar
  21. Droge W, Ruschman E, Lüderitz O, Westphal O (1968) Biochemical studies on lipopolysaccharides of Salmonella R mutants. 4. Phosphate groups linked to heptose units and their absence in some R lipopolysaccharides. Eur J Biochem 4: 134–138PubMedCrossRefGoogle Scholar
  22. Duguid JP, Gillies RR (1958) Fimbriae and haemagglutinating activity in Salmonella, Klebsiella, Proteus and Chromobacterium. J Pathol Bacteriol 75: 519–520Google Scholar
  23. Duguid JP, Darekar MR, Wheater DWF (1976) Fimbriae and infectivity in Salmonella typhimurium. J Med Microbiol 9: 459–473PubMedCrossRefGoogle Scholar
  24. Edwang TG, Befus AD (1984) The role of complement in the induction and regulation of immune responses. Immunology 51: 207–224Google Scholar
  25. Eisenstein B (1981) Phase variation of Type 1 fimbriae in Escherichia coli is under transcriptional control. Science 214: 337–339PubMedCrossRefGoogle Scholar
  26. Elsbach P, Weiss J (1983) A reevaluation of the roles of the O2-dependent and O2 independent microbicidal systems of phagocytes. Rev Infect Dis 5: 843–853PubMedCrossRefGoogle Scholar
  27. Finne J, Leinonen M, Makela PH (1983) Antigenic similarities between brain components and bacteria causing meningitis. Lancet 2: 354–357Google Scholar
  28. Gaastra W, de Graaf FK (1982) Host-specific fimbrial adhesins of noninvasive enterotoxigenic Escherichia coli strains. Microbiol Rev 46: 129–161Google Scholar
  29. Gemski P, Lazere JR, Casey T (1980) Plasmid associated with pathogenicity and calcium dependency of Yersinia enterocolitica. Infect Immun 27: 682–685PubMedGoogle Scholar
  30. Girardeau JP, Dubourguier HC, Gouet Ph (1982) Effect of glucose and amino acids on expression of K99 antigen in Escherichia coli. J Gen Microbiol 128: 2243–2249PubMedGoogle Scholar
  31. Göransson M, Uhlin BE (1984) Environmental temperature regulates transcription of a virulence pili operon in E. coli. EMBO J 3: 2885–2888Google Scholar
  32. Griffin FM Jr, Mullinax PJ (1981) Augmentation of macrophage complement receptor function in vitro. III. C3b receptors that promote phagocytosis migrate within the plane of the macrophage plasma membrane. J Exp Med 154: 291–305PubMedCrossRefGoogle Scholar
  33. Grossman N, Leive L (1984) Complement activation via the alternative pathway by purified Salmonella lipopolysaccharide is affected by its structure but not its O-antigen length. J Immunol 132: 376–385PubMedGoogle Scholar
  34. Gutteridge WE, Coombes GH (1977) Biochemistry of parasitic protozoa. University Park Press, BaltimoreGoogle Scholar
  35. Hackstadt T, Williams JC (1981) Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc Natl Acad Sci USA 78: 3240–3244PubMedCrossRefGoogle Scholar
  36. Halula M, Stocker BAD (1984) Cloning mannose-resistant hemagglutination gene(s) in Salmonella typhimurium. Abstr Annu Meet Am Soc Microbiol p 24Google Scholar
  37. Halula M, Stocker BAD (1985) Mannose-resistant haemagglutination gene(s) of Salmonella typhimurium. Abstr Annu Meet Am Soc Microbiol p 34Google Scholar
  38. Hammer CH, Shin ML, Abramovitz AS, Mayer MM (1977) On the mechanism of cell membrane damage by complement: evidence on insertion of polypeptide chains from C8 and C9 into the lipid bilayer of erythrocytes. J Immunol 119: 1–8PubMedGoogle Scholar
  39. Herzberg M (1962) Living organisms as immunizing agents against experimental salmonellosis in mice. I. Virulence of auxotrophic mutants. J Infect Dis 111: 192–203CrossRefGoogle Scholar
  40. Hoiseth SK, Stocker BAD (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238–239PubMedCrossRefGoogle Scholar
  41. Hull RA, Gill RE, Hsu P, Minshew BH, Falkow S (1981) Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli. Infect Immun 33: 933–938PubMedGoogle Scholar
  42. Ivanovics G, Marjai E, Dobozy A (1968) The growth of purine mutants of Bacillus anthracis in the body of the mouse. J Gen Microbiol 53: 147–162PubMedGoogle Scholar
  43. Joiner KA, Hammer CH, Brown EJ, Cole RJ, Frank MM (1982a) Studies on the mechanism of bacterial resistance to complement-mediated killing. I. Terminal complement components are deposited and released from Salmonella minnesota S218 without causing bacterial death. J Exp Med 155: 797–808PubMedCrossRefGoogle Scholar
  44. Joiner KA, Hammer CH, Brown EJ, Frank MM (1982 b) Studies on the mechanism of bacterial resistance to complement-mediated killing. II. C8 and C9 release C5b67 from the surface of Salmonella minnesota S218 because the terminal complex does not insert into the bacterial outer membrane. J Exp Med 155: 809–819CrossRefGoogle Scholar
  45. Joiner KA, Schmetz MA, Goldman RC, Leive L, Frank MM (1984) Mechanism of bacterial resistance to complement-mediated killing: inserted C5b-9 correlates with killing for Escherichia coli 0111B4 varying in O-antigen capsule and O-polysaccharide coverage of lipid A core oligosaccharide. Infect Immun 45: 113–117PubMedGoogle Scholar
  46. Jones GW, Rutter JM (1972) Role of the K88 antigen in the pathogenesis of neonatal diarrhea caused by Escherichia coli in piglets. Infect Immun 6: 918–927PubMedGoogle Scholar
  47. Jones GW, Rabert DK, Svinarich DM, Whitfield HJ (1982) Association of adhesive, invasive, and virulent phenotypes of Salmonella typhimurium with autonomous 60-megadalton plasmids. Infect Immun 38: 476–486PubMedGoogle Scholar
  48. Källenius G, Mollby R, Svenson SB, Winberg J, Hultberg H (1980) Identification of a carbohydrate receptor recognized by uropathogenic Escherichia coli. Infection 8: S288–S293CrossRefGoogle Scholar
  49. Kauffmann F (1941) A typhoid variant and a new serological variation in the Salmonella group. J Bacteriol 41: 127–140PubMedGoogle Scholar
  50. Korhonen TK, Valtonen MV, Parkkinen J, Väisänen-Rhen V, Finne J, Ørskov F, Ørskov I, Svenson SB, Mäkelä PH (1985) Escherichia coli strains associated with neonatal sepsis and meningitis: serotypes, hemolysin production and receptor recognition. Infect Immun 48: 386–491Google Scholar
  51. Labigne-Roussel AF, Lark D, Schoolnik G, Falkow S (1984) Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect Immun 46: 251–259PubMedGoogle Scholar
  52. Langenberg M-L, Tytgat GNJ, Schipper MEI, Rietra PJGM, Zanen HC (1984) Campylobacter-like organisms in the stomach of patients and healthy individuals. Lancet 1: 1348CrossRefGoogle Scholar
  53. Law SK, Lichtenberg NA, Levine RP (1979) Evidence for an ester linkage between the labile binding site of C3b and receptive surfaces. J Immunol 123: 1388–1394PubMedGoogle Scholar
  54. Lederberg J, lino T (1956) Phase variation in Salmonella. Genetics 41: 744–757Google Scholar
  55. Leffler H, Svanborg Eden C (1980) Chemical identification of a glycosphingolipid receptor for Escherichia coli attaching to human urinary tract epithelial cells and agglutinating human erythrocytes. FEMS Microbiol Lett 8: 127–134CrossRefGoogle Scholar
  56. Liang-Takasaki C-J, Mäkelä PH, Leive L (1982) Phagocytosis of bacteria by macrophages: changing the carbohydrate of lipopolysaccharide alters interaction with complement and macrophages. J Immunol 128: 1229–1235PubMedGoogle Scholar
  57. Liang-Takasaki C-J, Grossman N, Leive L (1983) Salmonellae activate complement differentially via the alternative pathway depending on the structure of their lipopolysaccharide O-antigen. J Immunol 130: 1867–1870PubMedGoogle Scholar
  58. Linde K, Keller H, Ezold R, Blatz B, Gericke B, Koch H, Kittlick M, Schmidt S (1974) Live vaccines against infections with Enterobacteriaceae: problems of selection of attenuated mutants and their genetic stability. Acta Microbiol Acad Sei Hung 21: 11–27Google Scholar
  59. Lysko PG, Morse SA (1981) Neisseria gonorrhoeae cell envelope: permeability to hydrophobic molecules. J Bacteriol 145:946–952PubMedGoogle Scholar
  60. MacKaness GB, BlandenRV,CollinsFM (1966) Host-parasite relations in mouse typhoid. J Exp Med 124: 573–583PubMedCrossRefGoogle Scholar
  61. Mäkelä PH, Mäkelä O (1966) Salmonella antigen 122: genetics of form variation. Ann Med Exp Fenn 44: 310–317PubMedGoogle Scholar
  62. Mäkelä PH, Stocker BAD (1984) Genetics of lipopolysaccharide. In: Rietschel ET (ed) Handbook of endotoxin, vol 1: chemistry of endotoxin. Elsevier, Amsterdam, pp 50–137Google Scholar
  63. Mekalanos JJ (1983) Duplication and amplification of toxin genes in Vibrio cholerae. Cell 35:253– 263PubMedCrossRefGoogle Scholar
  64. Modrzakowski MC, Spitznagel JK (1979) Bactericidal activity of fractionated granule contents from human polymorphonuclear leukocytes: antagonism of granule cationic proteins by lipopolysaccharide. Infect Immun 25: 597–602PubMedGoogle Scholar
  65. Moll A, Manning PA, Timmis KN (1980) Plasmid-determined resistance to serum bactericidal activity: a major outer membrane protein, the traT gene product, is responsible for plasmid-specified serum resistance in Escherichia coli. Infect Immun 28: 359–367PubMedGoogle Scholar
  66. Moon HW, Nagy B, Isaacson RE, Ørskov I (1977) Occurrence of K99 antigen on Escherichia coli isolated from pigs and colonization of pig ileum by K99+ enterotoxigenic Escherichia coli from calves and pigs. Infect Immun 15: 614–620PubMedGoogle Scholar
  67. Morrison DC, Kline LF (1977) Activation of the classical and properdin pathways of complement by bacterial lipopolysaccharides (LPS). J Immunol 118: 362–368PubMedGoogle Scholar
  68. Nevola JJ, Stocker BAD, Laux DC, Cohen PS (1985) Colonization of the mouse intestine by an avirulent Salmonella typhimurium strain and its lipopolysaccharide-defective mutants. Infect Immun 50: 152–159PubMedGoogle Scholar
  69. Normark S (1969) Mutation in Escherichia coli K-12 mediating spherelike envelopes and changed tolerance to ultraviolet irradiation and some antibiotics. J Bacteriol 98: 1274–1277PubMedGoogle Scholar
  70. Normark S, Lark D, Hull R, Norgren M, Baga M, O’Hanley P, Schoolnik G, Falkow S (1983) Genetics of digalactoside-binding adhesin from uropathogenic Escherichia coli strain. Infect Immun 41: 942–949PubMedGoogle Scholar
  71. Normark S, Båga M, Göransson M, Lindberg F, Lund B, Norgren M, Uhlin B-E (1985) Genetics of bacterial adhesins. In: Korhonen TK, Dawes EA, Mäkelä PH (eds) Enterobacterial surface antigens: methods for molecular characterization. Elsevier, AmsterdamGoogle Scholar
  72. Nowicki B, Rhen M, Väisänen-Rhen V, Pere A, Korhonen TK (1984) Immunofluorescence study of fimbrial phase variation in Escherichia coli KS71. J Bacteriol 160: 691–695PubMedGoogle Scholar
  73. O’Brien AD, Scher I, Formal SB (1979) Effect of silica on the innate resistance of inbred mice to Salmonella typhimurium infection. Infect Immun 25: 513–520PubMedGoogle Scholar
  74. O’Brien AD, Newland JW, Miller SF, Holmes RK (1984) Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226: 694–696PubMedCrossRefGoogle Scholar
  75. Old DC (1972) Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. J Gen Microbiol 71: 149–157PubMedGoogle Scholar
  76. Orndorff PE, Falkow S (1984) Identification and characterization of a gene product that regulates Type 1 piliation in Escherichia coli. J Bacteriol 160: 61–66PubMedGoogle Scholar
  77. Ørskov F, Ørskov I, Sutton A, Schneerson R, Lin W, Egan W, Hoff GE, Robbins JB (1979) Form variation in Escherichia coli Kl: determined by O-acetylation of the capsular polysaccharide. J Exp Med 149: 669–685PubMedCrossRefGoogle Scholar
  78. Ørskov I, Ferenc A, Ørskov F (1980) Tamm-Horsfall protein or uromucoid is the normal urinary slime that traps type 1 fimbriated Escherichia coli. Lancet 1: 887PubMedCrossRefGoogle Scholar
  79. Pangburn MK, Müller-Eberhard HJ (1980) Relation of a putative thioester bond in C3 to activation of the alternative pathway and the binding of C3b to biological targets of complement. J Exp Med 152: 1102PubMedCrossRefGoogle Scholar
  80. Parkkinen J, Finne J, Achtman M, Väisänen V, Korhonen TK (1983) Escherichia coli strains binding neuraminyl 2–3 galactosides. Biochem Biophys Res Commun 111: 456–461PubMedCrossRefGoogle Scholar
  81. Pluschke G, Achtman M (1984) Degree of antibody-independent activation of the classical complement pathway by K1 Escherichia coli differs with O antigen type and correlates with virulence of meningitis in newborns. Infect Immun 43: 684–692PubMedGoogle Scholar
  82. Pluschke G, Mayden J, Achtman M, Levine RP (1983 a) Role of the capsule and the O antigen in resistance of 018:K1 Escherichia coli to complement-mediated killing. Infect Immun 42: 907–913Google Scholar
  83. Pluschke G, Mercer A, Kusecek B, Pohl A, Achtman M (1983 b) Induction of bacteremia in newborn rats by Escherichia coli Kl is correlated with only certain O (lipopolysaccharide) antigen types. Infect Immun 39: 599–608Google Scholar
  84. Portnoy DA, Blank HF, Kingsbury DT, Falkow S (1983) Genetic analysis of essential plasmid determinants of pathogenicity in Yersinia pestis. J Infect Dis 148: 297–304PubMedCrossRefGoogle Scholar
  85. Rhen M, Knowles J, Penttilä ME, Sarvas M, Korhonen TK (1983 a) P fimbriae of Escherichia coli: molecular cloning of DNA fragments containing the structural genes. FEMS Microbiol Lett 19: 119–123CrossRefGoogle Scholar
  86. Rhen M, Mäkelä PH, Korhonen TK (1983 b) P fimbriae of Escherichia coli are subject to phase variation. FEMS Microbiol Lett 19: 267–271CrossRefGoogle Scholar
  87. Robertsson JA, Lindberg AA, Hoiseth SK, Stocker BAD (1983) Salmonella typhimurium infection in calves: evaluation of protection and survival of virulent S. typhimurium challenge bacteria after immunization with live or inactivated S. typhimurium vaccines. Infect Immun 41: 742–750PubMedGoogle Scholar
  88. Rutter JM, Jones GW (1973) Protection against enteric disease caused by Escherichia coli: a model for vaccination with a virulence determinant. Nature 242: 531–533PubMedCrossRefGoogle Scholar
  89. Saier MH, Schmidt MR, Leibowitz M (1978) Cyclic AMP-dependent synthesis of fimbriae in Salmonella typhimurium: effects of cya and pts mutations. J Bacteriol 134: 356–358PubMedGoogle Scholar
  90. Sansonetti PJ, Kopecko DJ, Formal SB (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun 35: 852–860PubMedGoogle Scholar
  91. Sansonetti PJ, Hale TL, Dammin GJ, Kapfer C, Collins HH, Formal SB (1983) Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun 39: 1392–1402PubMedGoogle Scholar
  92. Saxen H (1984) Mechanism of the protective action of anti-Salmonella IgM in experimental mouse salmonellosis. J Gen Microbiol 130: 2277–2283PubMedGoogle Scholar
  93. Saxen H, Hovi M, Mäkelä PH (1984) Lipopolysaccharide and mouse virulence of Salmonella: O antigen is important after intraperitoneal but not intravenous challenge. FEMS Microbiol Lett 24: 63–66CrossRefGoogle Scholar
  94. Schlecht S, Schmidt G (1969) Möglichkeiten zur Differenzierung von Salmonella-R-Formen mittels Antibiotica und antibakterieller Farbstoffe. Zentralbl Bakteriol Parasitenk Infektionskr Hyg Abt 1, Orig. 212: 505–511Google Scholar
  95. Schreiber RD, Morrison DC, Podack ER, Müller-Eberhard J (1979) Bactericidal activity of the alternative complement pathway generated from 11 isolated plasma proteins. J Exp Med 149: 870–882PubMedCrossRefGoogle Scholar
  96. Schweizer M, Schwarz H, Sonntag I, Henning U (1976) Mutational change of membrane architecture. Mutants of Escherichia coli Kl2 missing major proteins of the outer cell envelope membrane. Biochim Biophys Acta 448: 474–491PubMedCrossRefGoogle Scholar
  97. Seilwood R, Gibbons RA, Jones GW, Rutter JM (1975) Adhesion of enteropathogenic Escherichia coli to pig intestinal brush borders: the existence of two pig phenotypes. J Med Microbiol 8: 405–411CrossRefGoogle Scholar
  98. Simonet M, Mazigh D, Berche P (1984) Growth of Yersinia pseudotuberculosis in mouse spleen despite loss of a virulence plasmid of mol. wt. 47 x 106. J Med Microbiol 18: 371–375PubMedCrossRefGoogle Scholar
  99. Skurnik M, Bölin I, Heikkinen H, Piha S, Wolf-Watz H (1984) Virulence plasmid-associated autoagg-lutination in Yersinia spp. J Bacteriol 158: 1033–1036PubMedGoogle Scholar
  100. Smith BP, Reina-Guerra M, Hoiseth SK, Stocker BAD, Habasha F, Johnson E, Meritt F (1983) Safety and efficacy of aromatic-dependent Salmonella typhimurium as live vaccine for calves. Am J Vet Res 45: 59–66Google Scholar
  101. Smith BP, Reina-Guerra M, Stocker BAD, Hoiseth SK, Johnson E (1984) Aromatic-dependent Salmonella dublin as a parenteral modified live vaccine for calves. Am J Vet Res 45: 2231–2235PubMedGoogle Scholar
  102. Smith HW, Huggins MB (1980) The association of the 018, K1 and H7 antigens and the ColV plasmid of a strain of Escherichia coli with its virulence and immunogenicity. J Gen Microbiol 121: 387–400PubMedGoogle Scholar
  103. Smith HW, Linggood MA (1971) Observations on the pathogenic properties of the K88 hly and ent plasmids of Escherichia coli with particular reference to porcine diarrhea. J Med Microbiol 4: 467–485PubMedCrossRefGoogle Scholar
  104. Smith HW, Tucker JF (1976) The virulence of trimethoprim-resistant thymine-requiring strains of Salmonella. J Hyg 76: 97–108CrossRefGoogle Scholar
  105. Stevens P, Young LS, Adamu S (1983) Opsonization of various capsular (K) E. coli by the alternative complement pathway. Immunology 50: 497–502PubMedGoogle Scholar
  106. Stocker BAD, Hoiseth SK, Smith BP (1983) Aromatic-dependent Salmonella sp. as live vaccine, in mice and calves. Dev Biol Stand 53: 47–62PubMedGoogle Scholar
  107. Sukupolvi S, Vaara M, Heiander IM, Viljanen P, Mäkelä PH (1984) New Salmonella typhimurium mutants with altered outer membrane permeability. J Bacteriol 159: 704–712PubMedGoogle Scholar
  108. Takeuchi A (1967) Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am J Pathol 50: 109–136PubMedGoogle Scholar
  109. Tenner AJ, Ziccardi RJ, Cooper NR (1984) Antibody-independent CI activation by E. coli. J Immunol 133: 886–891PubMedGoogle Scholar
  110. Tidmarsh GF, Rosenberg LT (1981) Aquisition of iron from transferrin by Salmonella paratyphi B. Current Microbiol 6: 217–220CrossRefGoogle Scholar
  111. Vaara M, Nikaido H (1984) Molecular organization of bacterial outer membrane. In: Rietschel ET (ed) Handbook of endotoxin, vol 1: chemistry of endotoxin. Elsevier, Amsterdam, pp 1–45Google Scholar
  112. Vaara M, Vaara T (1983) Sensitization of Gram-negative bacteria to antibiotics and complement by a nontoxic oligopeptide. Nature 133: 526–527CrossRefGoogle Scholar
  113. Vaara M, Viljanen P, Vaara T, Mäkelä PH (1984) An outer membrane-disorganizing peptide PMBN sensitizes E. coli strains to serum bactericidal action. J Immunol 132: 2582–2589PubMedGoogle Scholar
  114. Väisänen V, Elo J, Tallgren LG, Siitonen A, Mäkelä PH, Svanborg Eden C, Källenius G, Svenson SB, Hultberg H, Korhonen TK (1981) Mannose-resistant hemagglutination and P antigen recognition are characteristic of Escherichia coli causing primary pyelonephritis. Lancet 11: 1366–1369CrossRefGoogle Scholar
  115. Valtonen MV (1977) Role of phagocytosis in mouse virulence of Salmonella typhimurium recombinants with O-antigen 6, 7 or 4, 12. Infect Immun 18: 574–578PubMedGoogle Scholar
  116. Valtonen VV (1970) Mouse virulence of Salmonella strains: the effect of different smooth-type O side-chains. J Gen Microbiol 64: 255–268PubMedGoogle Scholar
  117. Weinstein DL, Carsiotis M, Lissner CR, O’Brien AD (1984) Flagella help Salmonella typhimurium survive within murine macrophages. Infect Immun 46: 819–825PubMedGoogle Scholar
  118. Weiss J, Victor M, Elsbach P (1983) Role of charge and hydrophobic interaction in the action of the bactericidal/permeability-increasing protein of neutrophils on gram-negative bacteria. J Clin Invest 71: 540–549PubMedCrossRefGoogle Scholar
  119. Williams PH, Warner PJ (1980) ColV plasmid-mediated, colicin V-independent iron uptake system of invasive strains of Escherichia coli. Infect Immun 29: 411–416PubMedGoogle Scholar
  120. Wright SD, Levine RP (1981) How complement kills E. coli. I. Location of the lethal lesion. J Immunol 127: 1146–1151PubMedGoogle Scholar
  121. Yancey RJ, Breeding SAL, Lankford CE (1979) Enterochelin (enterobactin): virulence factor for Salmonella typhimurium. Infect Immun 24: 174–180PubMedGoogle Scholar
  122. Zaleska M, Lounatmaa K, Nurminen M, Wahlström E, Mäkelä PH (1985) A novel virulence- associated cell surface structure composed of 47 Kdal protein subunits in Yersinia enterocolitica. EMBO J 4: 1013–1018PubMedGoogle Scholar
  123. Zieg J, Silverman M, Hilmen M, Simon M (1977) Recombinational switch for gene expression. Science 196: 170–172PubMedCrossRefGoogle Scholar
  124. Zinc DL, Feeley JC, Wells JG, Vanderzant C, Vickery JC, Roof WD, O’Donoran GA (1980) Plasmid- mediated tissue invasiveness in Yersinia enterocolitica. Nature 283: 224–226CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1986

Authors and Affiliations

  • B. A. D. Stocker
    • 1
  • P. H. Mäkelä
    • 2
  1. 1.Department of Medical MicrobiologyStanford University School of MedicineStanfordUSA
  2. 2.National Public Health InstituteHelsinkiFinland

Personalised recommendations