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Antigenic modulation of Bordetella pertussis

Published online by Cambridge University Press:  15 May 2009

B. W. Lacey
B. W. Lacey
Affiliation:
The Department of Bacteriology, Westminster Medical School, London, S. W. 1
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The antigenic structure of Bordetella pertussis varies continuously with environmental conditions of growth and, under suitable conditions, any of three forms (or modes) with markedly different antigenic surfaces may be developed. High temperatures and certain ions, such as sodium, potassium, halides, formate and nitrate, favour growth like that on Bordet and Gengou's medium at 35° C. Low temperatures and other ions, such as magnesium, sulphate and mono- and dicarboxylic acids with more than two carbon atoms, favour growth with a markedly different antigenic structure and character. These two extreme forms have been called X mode and C mode respectively. A third mode (called I mode) is induced within a narrow range of intermediate temperatures and ion ratios. Bacterial cells in C mode, unlike those in X mode, do not agglutinate red-blood cells, are not haemolytic or agglutinable by heavy metal salts, have no surface antigen related to Bordetella parapertussis or B. bronchiseptica and are serotypically homogeneous.

The influence of ions is a function of their species and ratios and not of their absolute concentrations or total ionic strength. A number of ions has been arranged in a pattern. In this the influence of any salt is represented at the centre of a line joining its component ions, and a measure of the influence of any salt mixture is given by the position of its imaginary centre of inertia. (For calculating this, mass is represented by the product of salt concentration and conductance ratio and radius of gyration by distance.) The influences of ions and temperature appear not to interact since their combined influence is proportional to the sum of their separate influences.

The change from one mode to another (modulation) occurs without mutation or selection, is complete within 7–15 cell divisions and appears to stem from altered rates of synthesis of at least three kinds of antigen molecule. During the process of modulation, antigens not detectable by agglutination in any of the three equilibrium modes (X, I and C) may appear transiently at the surface.

Mutants may or may not modulate. Modulatable mutants may be distinguishable from the wild type in only one mode. Almost all convalescent antibodies are directed against X mode, but C-mode antibodies have been found in several adults with persistent cough and infection.

I wish particularly to thank Dr E. K. Andersen for her generous gifts of sera, Drs P. L. Kendrick, H. Proom, A. F. B. Standfast and A. J. H. Tomlinson for gifts of cultures and Mr M. Breach for his invaluable help in the preparation of media and sera. I am also indebted to the University of London Central Research Fund and the Governors of Westminster Hospital for grants towards the purchase of materials.

Type
Research Article
Information
Journal of Hygiene , Volume 58 , Issue 1 , March 1960 , pp. 57 - 93
Copyright
Copyright © Cambridge University Press 1960

References

REFERENCES

Andersen, E. K. (1952). Some observations made during experiments on mice inoculated with H. pertussis. Acta path. microbiol. scand. 31, 546.CrossRefGoogle ScholarPubMed
Andersen, E. K. (1953). Serological studies on H. pertussis, H. parapertussis and H. bronchisepticus. Acta path. microbiol. scand. 33, 202.CrossRefGoogle Scholar
Arkwright, J. A. (1930). Variation. In A System of Bacteriology in Relation to Medicine, vol. I, pp. 311–74. Medical Research Council. London: H.M. Stationery Office.Google Scholar
Atwood, K. C., Schneider, L. K. & Ryan, F. J. (1951). Periodic selection in Escherichia coli. Proc. nat. Acad. Sci., Wash., 37, 146.CrossRefGoogle ScholarPubMed
Bloom, W. (1937). Cellular differentiation and tissue culture. Physiol. Rev. 17, 589.CrossRefGoogle Scholar
Bordet, J. (1912). Note complémentaire sur le microbe de la coqueluche et sa variabiité au point de vue sérodiagnostic et de la toxicité. Zbl. Bakt. (I. Orig.), 66, 276.Google Scholar
Bordet, J. & Sleeswyk, (1910). Sérodiagnostic et variabilité des microbes suivant le milieu de culture. Ann. Inst. Pasteur, 24, 476.Google Scholar
Braun, W., Kraft, M., Mead, D. D. & Goodlow, R. J. (1952). The effect of penicillin on genetic changes and temporary modifications in populations of Brucellae. J. Bact. 64, 41.CrossRefGoogle ScholarPubMed
Briody, B. A. (1948). Haemagglutination by influenza virus: III. The XO phase of influenza A virus. J. infect. Dis. 83, 293.CrossRefGoogle Scholar
Brodie, B. B. & Hogben, C. A. M. (1957). Some physico-chemical factors in drug action. J. Pharm., Lond., 9, 345.CrossRefGoogle ScholarPubMed
Burnet, F. M. (1953). Virus classification and nomenclature. Ann. N.Y. Acad. Sci. 56, 383.CrossRefGoogle Scholar
Calaresu, F., Spurrier, W. & Schwartz, S. O. (1956). Studies in Leukemia. V. Antigenic differences between leukemic and non leukemic red blood cells. J. Lab. clin. Med. 48, 102.Google Scholar
Cashman, A. J. (1955). Early immunization against whooping cough. Brit. med. J. ii, 589.Google Scholar
Cole, L. J. & Wright, W. H. (1916). Application of the pure-line concept to bacteria. J. infect. Dis. 19, 209.CrossRefGoogle Scholar
Cruickshank, J. C. & Freeman, G. G. (1937). Immunising fractions isolated from Haemophilus pertussis. Lancet, ii, 567.CrossRefGoogle Scholar
Dobell, C. (1912). Some recent work on mutation in micro-organisms. II. Mutations in bacteria. J. Genet. 2, 325.CrossRefGoogle Scholar
Eisenberg, P. (1912). Untersuchungen über die Variabilität der Bakterien. II. Über sogenannte Mutationsvorgänge bei Choleravibrionen. Zbl. Bakt. (I. Orig.), 66, 1.Google Scholar
Eisenberg, P. (1918). Untersuchungen über spezifische Desinfektionsvorgänge. II. Mitteilung: Über die Wirkung von Salzen und Ionen auf Bakterien. Zbl. Bakt. (I. Orig.), 82, 69.Google Scholar
Eldering, G. & Kendrick, P. L. (1936). Some practical considerations in B. pertussis vaccine preparation. Amer. J. publ. Hlth, 26, 506.CrossRefGoogle Scholar
Evans, D. G. & Perkins, F. T. (1953). An agglutinin-production test in the study of pertussis vaccines. J. Path. Bact. 66, 479.CrossRefGoogle Scholar
Evans, D. G. & Perkins, F. T. (1954). An improved method for testing the ability of pertussis vaccines to produce agglutinin. J. Path. Bact. 68, 251.CrossRefGoogle ScholarPubMed
Felix, A., Bhatnagar, S. S. & Pitt, R. M. (1934). Observations on the properties of the Vi antigen of B. typhosus. Brit. J. exp. Path. 15, 346.Google Scholar
Fell, H. B. (1954). The effect of environmental factors on the differentiation of the allantoic endoderm in organ culture. J. Embryol. exp. Morph. 2, 348.Google Scholar
Freund, J. & Bonanto, M. V. (1944). The effect of paraffin oil, lanolin-like substances and killed tubercle bacilli on immunization with diphtheric toxoid and Bact. typhosum. J. Immunol. 48, 325.CrossRefGoogle Scholar
Goldschmidt, R. (1938). Physiological Genetics. New York: McGraw Hill.CrossRefGoogle Scholar
Hartely, H. & Raikes, H. R. (1927). The mobilities of the elementary ions in methyl alcohol. Trans. Faraday Soc. 23, 393.CrossRefGoogle Scholar
Hektoen, L. (1918). The production of precipitins by the fowl. J. infect. Dis. 22, 561.CrossRefGoogle Scholar
Hilleman, M. R. (1954). Antigenic variation of influenza viruses. Annu. Rev. Microbiol. 8, 311.CrossRefGoogle ScholarPubMed
Hilleman, M. R. & Gordon, F. B. (1943). A protective antiserum against mouse pneumonitis virus. Science, 98, 347.CrossRefGoogle ScholarPubMed
Hinshelwood, C. N. (1957). Ageing in Bacteria. In: The Biology of Ageing (eds. Yapp, W. B. and Bourne, G. H.), pp. 1–7. London: Institute of Biology.Google Scholar
Huxley, J. S. (1955). Morphism and evolution. Heredity, 9, 1.CrossRefGoogle Scholar
Jones, K. L. (1954). Variations in Streptomyces. Ann. N.Y. Acad. Sci. 60, 124.CrossRefGoogle ScholarPubMed
Jordan, E. O. (1915). Variation in bacteria. Proc. nat. Acad. Sci., Wash., 1, 160.CrossRefGoogle ScholarPubMed
Jude, A. & Nicolle, P. (1952). Persistence, à l'état potentiel, de la capacité d'élaborer 1' antigène Vi chez le bacille typhique cultivé en série à basse température. C.R. Acad. Sci., Paris, 234, 1718.Google Scholar
Krumwiede, C., Mishulow, L. & Oldenbusch, C. (1923). The existence of more than one immunologic type of B. pertussis. J. infect. Dis. 32, 22.CrossRefGoogle Scholar
Lacey, B. W. (1951). Antigenic modulation of Haemophilus pertussis. J. gen. Microbiol. 5, xxi.Google ScholarPubMed
Lacey, B. W. (1953 a). Three dimensional patterns of antigenic modulation of Haemophilus pertussis, H. parapertussis and H. bronchisepticus. J. gen. Microbiol. 8, iii.Google ScholarPubMed
Lacey, B. W. (1953 b). The influence of growth conditions on the antigenic structure of Haemophilus pertussis, parapertussis and bronchisepticus. Atti del Congresso Internazionale di microbiologica, 2, sez. vi–vii, 331.Google Scholar
Lacey, B. W. (1954). A new selective medium for Haemophilus pertussis, containing a diamidine, sodium fluoride and penicillin. J. Hyg., Camb., 52, 273.CrossRefGoogle Scholar
Landauer, W. (1948). Hereditary abnormalities and their chemically induced phenocopies. Growth, 12 (Suppl), p. 171.Google Scholar
Le Bouvier, G. L. (1955). The modification of poliovirus antigens by heat and ultraviolet light. Lancet, ii, 1013.CrossRefGoogle Scholar
Leslie, P. H. & Gardner, A. D. (1931). The phases of Haemophilus pertussis. J. Hyg., Camb., 31, 423.CrossRefGoogle ScholarPubMed
Luria, S. E. & Delbrück, M. (1943). Mutations of bacteria from virus sensitivity to virus resistance. Genetics, 28, 491.CrossRefGoogle ScholarPubMed
MacDougall, F. H. (1952). Physical Chemistry, 3rd ed.New York: Macmillan.Google Scholar
MacInnes, D. A. (1939). The Principles of Electrochemistry. New York: Rheinhold Publishing Corporation.Google Scholar
Magill, T. P. & Sugg, J. Y. (1948). The reversibility of the O-D type of influenza virus variation. J. exp. Med. 87, 535.CrossRefGoogle ScholarPubMed
Maitland, H. B., Kohn, R. & Macdonald, A. D. (1955). The histamine-sensitizing property of Haemophilus pertussis. J. Hyg., Camb., 53, 196.CrossRefGoogle ScholarPubMed
Mellon, R. R. & Hagan, M. L. (1942). The polyphasic potencies of the bacterial cell; general biologic and chemotherapeutic significance. J. Bact. 44, 1.CrossRefGoogle ScholarPubMed
Miles, A. A. (1939). The antigenic surface of smooth Brucella abortus and melitensis. Brit. J. exp. Path. 20, 63.Google Scholar
Miller, J. J. Jr, & Silverberg, R. J. (1939). The agglutinative reaction in relation to pertussis and to prophylactic vaccination against pertussis with description of a new technic. J. Immunol. 37, 207.CrossRefGoogle Scholar
Monod, J. (1947). The phenomenon of enzymatic adaptation and its bearing on problems of genetics and cellular differentiation. Growth, 11, 223.Google Scholar
Murray, J. (1944). Rh antenatal testing. A suggested nomenclature. Lancet, ii, 594.CrossRefGoogle Scholar
Neter, E., Westphal, O., Lüderitz, O., Gorzynski, E. A. & Eichenberger, E. (1955). Studies of the enterobacterial lipopolysaccharides. Effects of heat and chemicals on erythrocyte-modifying, antigenic, toxic and pyrogenic properties. J. Immunol. 76, 377.CrossRefGoogle Scholar
Phair, J. J., Smith, D. G. & Root, C. M. (1943). Use of chicken serum in the species and type identification of Neisseria. Proc. Soc. exp. Biol., N.Y., 52, 72.CrossRefGoogle Scholar
Pillemer, L., Blum, L. & Lepow, I. H. (1954). Protective antigen of Haemophilus pertussis. Lancet, i, 1257.CrossRefGoogle Scholar
Pittman, M. (1951). Comparison of the histamine-sensitizing property with the protective activity of pertussis vaccines for mice. J. infect. Dis. 89, 300.CrossRefGoogle ScholarPubMed
Pittman, M. (1952). Influence of preservatives, of heat, and of irradiation on mouse protective activity and detoxification of pertussis vaccine. J. Immunol. 69, 201.CrossRefGoogle ScholarPubMed
Povitzky, O. R. & Worth, E. (1916). Agglutination in pertussis. Its characteristics and its comparative value in clinical diagnosis, and in determination of genus and species. Arch. int. Med. 17, 279.CrossRefGoogle Scholar
Ravin, A. W. (1953). The nature of variations affecting bacterial adaptability. Symp. Soc. gen. Microbiol. 3, 46.Google Scholar
Schmitt, F. O. (1956). Patterns of interaction of biological macromolecules in relation to cell function. Proc. nat. Acad. Sci., Wash., 42, 806.CrossRefGoogle Scholar
Schütze, H. (1932). Studies in B. pestis antigens. I. The antigens and immunity reactions of B. pestis. Brit. J. exp. Path. 13, 284.Google Scholar
Shepherd, C. J. (1957). The genome as a component of the ecosystem. Symp. Soc. gen. Microbiol. 7, 1.Google Scholar
Shibayama, G. (1905). Über die Agglutination des Pestbacillus. Zbl. Bakt. (I. Orig.), 38, 482.Google Scholar
Shimojo, H. & Ishii, T. (1954). Studies on the K antigen of H. pertussis. Its existence and a method of detection. Jap. J. exp. Med. 24, 51.Google Scholar
Slavin, D. (1950). Production of antisera in rabbits using calcium alginate as an antigen depot. Nature, Lond., 165, 115.CrossRefGoogle ScholarPubMed
Spiegelman, S. & Landman, O. E. (1954). Genetics of micro-organisms. Annu. Rev. Microbiol. 8, 181.CrossRefGoogle Scholar
Stamp, Lord, (1947). The preservation of bacteria by drying. J. gen. Microbiol. 1, 251.CrossRefGoogle ScholarPubMed
Stanier, R. Y. (1953). Adaptation, evolutionary and physiological: or Darwinism among the micro-organisms. Symp. Soc. gen. Microbiol. 3, 1.Google Scholar
Toenniessen, E. (1915). Über Vererbung und Variabilität bei Bakterien. Ein Beitrag zur Entwicklungslehre. Biol. Zbl. 35, 281.Google Scholar
Ungar, J. & Muggleton, P. W. (1949). The relationship of the aluminium phosphate precipitation of organisms of Haemophilus pertussis strains to their other biological properties. J. gen. Microbiol. 3, 353.CrossRefGoogle ScholarPubMed
Waddington, C. H. (1948). The genetic control of development. Symp. Soc. exp. Biol. 2, 145.Google Scholar
Waddington, C. H. (1953). In discussion of: Observations on bacterial adaptation by S. C. R. Dean and C. Hinshelwood. Symp. Soc. gen. Microbiol. 3, 21.Google Scholar
Wallace, J. H., Dodd, M. C. & Wright, C-S. (1955). Antigenic studies of virus and trypsin-treated erythocytes. J. Immunol. 74, 89.CrossRefGoogle Scholar
Weiner, W., Lewis, H. B. M., Moores, P., Sanger, R. & Race, R. R. (1957). A gene, y, modifying the blood group antigen A. Vox sanguinis, 2, 25.CrossRefGoogle ScholarPubMed
Weiss, P. (1939). Principles of Development. New York: Henry Holt.Google Scholar
Weiss, P. (1947). The problem of specificity in growth and development. Yale J. Biol. Med. 19, 235.Google ScholarPubMed
Weiss, P. (1949). Growth and differentiation on the cellular and molecular levels. Exp. Cell Res. (Suppl. 1), p. 475.Google Scholar
Weiss, P. (1953). Some introductory remarks on the cellular basis of differentiation. J. Embryol. exp. Morph. 1, 181.Google Scholar
Westergaard, M. (1957). Chemical mutagenesiS in relation to the concept of the gene. Experientia, 13, 224.CrossRefGoogle Scholar
Wilson, G. S. & Miles, A. A. (1955). Topley and Wilson's Principles of Bacteriology and Immunity, 4th ed.London: Edward Arnold.Google Scholar
Winslow, C. E. A. & Walker, L. T. (1909). A case of non-inheritance of fluctuating variations among bacteria. J. infect. Dis. 6, 90.CrossRefGoogle Scholar
Wolfe, H. R. (1942). Precipitin-production in chickens. I. Interfacial titers as affected by quantity of antigen injected and aging of antisera. J. Immunol. 44, 135.CrossRefGoogle Scholar
World Health Organisation (1953). Diphtheria and pertussis vaccination. Report of a conference of heads of laboratories producing diphtheria and pertussis vaccines. Wld Hlth Org. tech. Rep. Ser. 61.Google Scholar
Zuckerman, S. (1957). The human breeding season. New Scientist, no. 20, p. 12.Google Scholar