Toxicity and potency evaluation of pertussis vaccines

Expert Review of Vaccines

Volumn 3, Issue 1, 2004, Pages 89-101

  Corbel, Michael J ^a   Xing, Dorothy K L ^a  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Acellular; Immune response; Pertussis; Potency assay; Safety test; Toxins; Vaccines

Indexed keywords

ACELLULAR VACCINE; ADENYLATE CYCLASE TOXIN; CYTOTOXIN; FIMBRIA PROTEIN; HEMAGGLUTININ; HEMOLYSIN; HISTAMINE; LIPOOLIGOSACCHARIDE; NITRIC OXIDE; PERTACTIN; PERTUSSIS TOXIN; PERTUSSIS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CHO CELL; CONTROLLED STUDY; DNA MICROARRAY; DRUG TOXICITY; IMMUNOGENICITY; MOUSE; NONHUMAN; PATHOGENICITY; PERTUSSIS; PRIORITY JOURNAL; PROVOCATION TEST; R FACTOR; RECEPTOR BINDING; REVIEW; WEIGHT GAIN; WORLD HEALTH ORGANIZATION;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL TOXINS; BORDETELLA PERTUSSIS; FIMBRIAE, BACTERIAL; HEMAGGLUTININS; HISTAMINE; LIPOPOLYSACCHARIDES; PERTUSSIS TOXIN; PERTUSSIS VACCINE; TOXICITY TESTS; TRANSGLUTAMINASES; VIRULENCE FACTORS, BORDETELLA;

EID: 1042291316     PISSN: 14760584     EISSN: None     Source Type: Journal    
DOI: 10.1586/14760584.3.1.89     Document Type: Review

References (127)

1. Madsen T. Vaccination against whooping cough. J. Am. Med. Assoc., 101, 187-188 (1933).
2. McFarlan AM, Topley E, Fisher M. Trial of whooping cough vaccine in city and residential nursery groups. Br. Med. J. 2, 205-208 (1945).
3. Kendrick PL, Eldering G. Significance of bacteriological methods in the diagnosis and control of whooping cough. Am. J. Public Health. 25, 147-155 (1935).
4. Kendrick PL, Eldering G. A study on active immunisation against pertussis. Am. J. Hyg. (Sect B). 29,133-153 (1939).
5. Kendrick PL, Eldering G, Dixon MK, Misner J. Mouse protection tests in the study of pertussis vaccines: a comparative series using the intracerebral route of challenge. Am. J. Public. Health. 37, 803-810 (1947). Describes the development of the potency assay for whole-cell vaccine.
6. Medical Research Council: The prevention of whooping cough by, vaccination. Br. Med. J. 1, 1463-1471 (1951).
7. Medical Research Council: Vaccination against whooping cough: Relation between protection in children and results of laboratory tests. Br. Med. J. 2, 454-462 (1956). Describes the trial results which confirmed the value of the Kendrick potency assay.
8. Medical Research Council: Vaccination against whooping cough: The final report. Br. Med. J. 1, 994-1000 (1959).
9. Cameron J. Pertussis vaccine: control testing problems. In: International Symposium on Pertussis Proceedings. Manclark CR., Hill JC (Eds), DHEW publication, DC, USA, 200-207 (1978).
10. Cameron J. Pertussis vaccine: mouse-weight-gain (toxicity) test. Dev. Biol. Stand. 34, 213-215 (1976). Describes the use of the mouse weight gain toxicity test.
11. van Ramshorst JD. Toxicity control of pertussis vaccines by the mouse-weight-gain test. Prog. Immunobiol. Stand. 3, 324-326 (1969).
12. Corbel MJ, Xing DKL. The current status of acellular pertussis vaccines: Editorial, J. Med. Microbiol. 46, 817-818 (1997).
13. Corbel MJ, Xing DKL. A consideration of control requirements for acellular pertussis vaccines. Dev. Biol. Stand. 89, 283-287 (1997).
14. Corbel MJ, Xing DKL, Kreeftenberg JG. Informal Consultation with Manufacturers and WHO Ad Hoc Working Group on Mouse Protection Models for Acellular Pertussis Vaccines. Meeting Report, Biologicals 27, 189-193 (1999). Summarizes recent WHO initiatives to improve the standardization of acellular pertussis vaccines.
15. Corbel MJ, Mastrantonio P, Kreeftenberg JG. Ad Hoc Working Group on Acellular Pertussis Vaccines, WHO, Meeting Report, Vaccine 20, 288-291 (2002). Summarizes recent WHO initiatives to improve the standardization of acellular pertussis vaccines.
16. Corbel MJ, Knezevic I, Kreeftenberg JG. Ad Hoc Working Group on Acellular Pertussis Vaccines, WHO, Meeting Report, Vaccine 22, 293-300 (2004). Summarizes recent WHO initiatives to improve the standardization of acellular pertussis vaccines.
17. Coote JG. Antigenic switching and pathogenicity: environmental effects on virulence gene expression in Bordetella pertussis. J. Gen. Microbiol. 137, 2493-2503 (1991).
18. Manetti R, Arico B, Rappuoli R, Scarlato V. Mutations in the linker region of BvgS abolish response to environmental signals for the regulation of the virulence factors in Bordetella pertussis. Gene 150, 123-127 (1994).
19. Smith AM, Guzman CA, Walker MJ. The virulence factors of Bordetella pertussis: a matter of control. FEMS Microbiology Reviews 25, 309-333 (2001).
20. Pittman M. Pertussis toxin: the cause of harmful effects and prolonged immunity of whooping cough. A hypothesis. Rev. Infect. Dis. 1, 401-412 (1979).
21. Vysoka B. The epidemiology of pertussis and parapertussis. J. Hyg. Epidemiol. Microbiol. Immunol. II, 196-204 (1958).
22. Katada T, Ui M. Direct modification of the membrane adenyl cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein. Proc. Natl Acad. Sci. USA 79, 3129-33 (1982).
23. Tammura M, Nogimori K, Murai S et al. Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry 21, 5516-5522 (1982).
24. Munoz J. Biological activities of pertussigen (pertussis toxin) In: Pertussis Toxin. Sekura, R. Moss J, Vaughan M. (Eds), Academic Press, London, UK, 1-18 (1985).
25. Xing D, Canthaboo C, Corbel MJ. Effect of pertussis toxin on induction of nitric oxide in murine macrophages and protection in vivo. Vaccine. 18, 2110-2119 (2000).
26. Pittman M, Cox C. Pertussis vaccine testing for freedom from toxicity. Appl. Microbiol. 13, 447-456 (1965).
27. Cameron J, Desormeaux Y, Desormeaux ML, Leclerc J. Toxicity testing of pertussis vaccines: effect of increased sensitivity of mice to Bordetella pertussis. J. Biol. Stand. 12, 19-24 (1984).
28. Van Straaten, Van de Kappelle I, Wiertz EJHJ et al. The modified leukocytosis promoting factor (LPF)-test: a valuable supplement to the mouse weight gain (MWG)-test in toxicity control of whole-cell pertussis vaccine. Biologicals 20, 277-282 (1992).
29. Burns D, Kenimer J, Manclark C. Role of the A subunit of pertussis toxin in alteration of Chinese hamster ovary cell morphology. Infect. Immun. 55, 24-28 (1987). Describes the application of the CHO-cell assay to pertussis toxin detection.
30. Cyr T, Menzies J, Calver J, Whitehouse L. A quantitative analysis for the ADP-ribosylation activity of pertussis toxin: an enzymatic-HPLC coupled assay applicable to formulated whole-cell and acellular pertussis vaccine products. Biologicals 29, 81-95 (2001). Development of a physico-chemical ribosyl transferase assay.
31. Horiguchi Y, Inoue N, Masuda M et al. Bordetella bronchiseptica dermonecrotizing toxin induces reorganization of actin stress fibers through deamination of Gln-63 of the GTP-binding protein Rho. Proc. Natl Acad. Sci. USA 94, 11623-11626 (1997).
32. Minako M, Massyoshi M, Hiroaki S, Matsuzawa T, Horiguchi Y. In vivo modifications of small GTPase Rac and Cdc42 by Bordetella dermonecrotic toxin. Infect. Immun. 70, 998-1001 (2002).
33. Horiguchi Y, Sugimoto N, Matsuda M. Stimulation of DNA synthesis in osteoblast-like MC3T3-E1 cells by Bordetella bronchiseptica dermonecrotizing toxin. Infect. Immun. 61, 3611-3615 (1993).
34. Maskell D, Allen AG. The identification cloning and mutagenesis of a genetic locus required for lipopolysaccharide biosynthesis in Bordetella pertussis. Mol. Microbiol. 19, 37-52 (1996).
35. Yuk MH, Harvill ET, Miller JF. The BvgAS virulence control system regulates Type III secretion in Bordetella bronchiseptica. Mol. Microbiol. 28, 945-959 (1998). Regulation of pathogenicity in B. pertussis.
36. Gupta RK, Saxena SN, Sharma SB. The effects of purified pertussis components and lipopolysaccharide in the results of the mouse weight gain test. J. Biol. Stand. 16, 321-331 (1988).
37. Redhead K, Seagroatt V. The effects of purified components of Bordetella pertussis in the weight gain test for the toxicity testing of pertussis vaccines. J. Biol. Stand. 14, 57-65, (1986)
38. Bacterial endotoxins. In: European Pharmacopeia 4, European Pharmacopeia Commission, France 140-147 (2002).
39. Cookson BT, Tyler AN, Goldman WE. Primary structure of the peptidoglycan-derived tracheal cytotoxin of Bordetella pertussis. Biochemistry 28, 1744-1749 (1989).
40. Cookson BT, CHO HL, Herwaldt LA, Goldman WE. Biological activities and chemical composition of purified tracheal cytotoxin of Bordetella pertussis. Infect. Immun. 57, 2223-2229 (1989).
41. Glaser P, Ladant D, Sezer O, Pichot F, Ullmann A, Danchin A. The calmodulin-sensitive adenyl cyclase of Bordetella pertussis: cloning and expression in Escherichia coli. Mol. Microbiol. 2, 19-30 (1988).
42. Ladant D. Interaction of Bordetella pertussis adenyl cyclase with calmodulin. Identification of two separated calmodulin-binding domains. J. Biol. Chem. 263, 2612-2618 (1988).
43. Friedman RL, Fiederlein RL, Glasser L, Galgiani JN. Bordetella pertussis adenyl cyclase: effects of affinity-purified adenyl cyclase on human polymorphonuclear leukocyte functions. Infect. Immun. 55, 135-40 (1987).
44. Khelef N, Guiso N. Induction of macrophage apoptosis by Bordetella pertussis adenyl cylase-hemolysin. FEMS Microbiol. Lett. 134, 27-32 (1995)
45. Novotny P, Chubb AP, Cownley K, Monterez JA. Adenyl cyclase activity of a 68,000-molecular-weight protein isolated from the outer membrane of Bordetella bronchiseptica. Infect. Immun. 50, 199-206, (1985).
46. Wolff J, Hope CG, Goldhammer AL, Berkowitz SA. Calmodulin activates prokaryotic adenyl cyclase. Proc. Natl Acad. Sci. USA 77, 3841-3844 (1980).
47. Prior S, Xing D, Auda G, Corbel M. Evaluation of the toxicity of recombinant Bordetella pertussis adenyl cyclase toxin preparations. In: Advancing Science and Elimination of the use of laboratory animals for development and control of vaccines and hormones. Brown F, Hendriksen C, Sesardic D. Eds). S. Karger AG, Basel 111, 119-129 (2002).
48. Menozzi FD, Mutombo R, Renauld G et al. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect. Immun. 62, 769-778 (1994).
49. Prasad SA, Yin Y, Rodzinski E, Tuomanen EI, Masure HR. Identification of a carbohydrate recognition domain in filamentous hemagglutinin from Bordetella pertussis. Infect. Immun. 61, 2780-2785 (1993).
50. Relman D, Tuomanen EI, Falkow S. Recognition of a bacterial adhesion by an integrin: macrophage CR3 (_Mβ2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61, 1375-1382 (1990).
51. McGuirk P, McCann C, Mills KHG. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin-10 production by dendritic cells: a novel strategy for evasion of protective T-helper Type 1 responses by Bordetella pertussis. J. Exp. Med. 195, 221-231 (2002).
52. Ad hoc group for the study of pertussis vaccines. Placebo-controlled trial of two acellular pertussis vaccines in Sweden-protective efficacy and adverse events. Lancet 1, 955-960 (1988). Clinical trial comparing one and two component acellular vaccines.
53. Tuomanen EI, Prasad SM, George JS et al. Reversible opening of the blood-brain barrier by antibacterial antibodies. Proc. Natl Acad. Sci. USA 90, 7824-7828 (1993).
54. Willems RJ, Geuijen C, van der Heide HG et al. Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol. Microbiol. 11, 337-347 (1994).
55. Robinson A, Irons LI, Seabrook RN et al. Structure-function studies of Bordetella pertussis fimbriae. In: Proceedings of sixth International Symposium on pertussis. Manclark CR (Ed), FDA, MD, USA (1991).
56. Preston NW. Type-specific immunity against whooping cough. Br. Med. J. 3, 724-726 (1963).
57. Robinson A, Gorringe AR, Funnell SG. Fernandez M. Serospecific protection of mice against intranasal infection with Bordetella pertussis. Vaccine 7, 321-324 (1989).
58. Mattoo S, Miller JF, Cotter PA. Role of Bordetella bronchiseptica fimbriae in tracheal colonisation and development of a humoral immune response. Infect. Immun. 68, 2024-2033 (2000).
59. Hynes RO. Integrins: a family of cell surface receptors. Cell 48, 549-554 (1987).
60. Luker KE, Tyler AN, Marshall GR, Goldman WE. Tracheal cytotoxin structural requirements for respiratory epithelial damage in pertussis. Mol. Microbiol. 16, 733-743 (1995).
61. Finn TM, Stevens LA. Tracheal colonisation factor: a Bordetella pertussis secreted virulence determinant. Mol. Microb. 16, 625-634 (1995).
62. Fernandez RC, Weiss AA. Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect Immun. 62, 4727-4738 (1994).
63. Fernandez RC, Weiss AA. Serum resistance in bvg-regulated mutants of Bordetella pertussis. FEMS Microb. Lett. 163, 57-63 (1998).
64. De Serres G, Shadmani R, Duval B et al. Morbidity of pertussis in adolescents and adults. J. Infect Dis. 182, 174-179 (2000).
65. Ausiello CM, Lande R, Urbani F et al. Cell-mediated immune responses in four-year old children after primary immunization with acellular pertussis vaccines. Infect. Immun. 67, 4064-4071 (1999).
66. Esposito S, Agliardi T, Giammanco A et al. Long-term pertussis-specific immunity after primary vaccination with a combined diphtheria, tetanus, tricomponent acellular pertussis and hepatitis B vaccine in comparison with that after natural infection. Infect. Immun. 69, 4516-4520 (2001). Assessment of duration of immunity to pertussis.
67. Di Tommaso A, Bartalini M, Peppoloni S et al. Acellular pertussis vaccines containing genetically detoxified pertussis toxin induce long lasting humoral and cellular responses in adults. Vaccine 15, 1218-1224 (1997).
68. Mahon BP, Brady MT, Mills KHG. Protection against Bordetella pertussis in mice in the absence of detectable circulating antibody: implications for long-term immunity in children. J. Infect. Dis. 181, 2087-2091 (2000).
69. Ryan EJ, Nilsson L, Kjellman NIM, Gothefors L, Mills KHG. Booster immunization of children with an acellular pertussis vaccine enhances Th2 cytokine production and serum IgE responses against pertussis toxin but not against common allergens. Clin. Exp. Immunol. 121, 193-200 (2000).
70. Zepp F, Knuf M, Habermehl P et al. Pertussis-specific cell-mediated immunity in infants after vaccination with a tricomponent acellular pertussis vaccine. Infect. Immun. 64, 4078-7084 (1996).
71. Locht C, Bertin P, Menozzi FD, Renauld G. The filamentous haemagglutinin, a multifaceted adhesin produced by virulent Bordetella spp. Mol. Microb. 9, 653-660 (1993).
72. Canthaboo C, Williams L, Xing DKL, Corbel MJ. Investigation of cellular and humoral immune responses to whole-cell and acellular pertussis vaccines. Vaccine 19, 637-643 (2001). Laboratory evaluation of immune responses to acellular vaccines.
73. Canthaboo C, Xing D, Wei XQ, Corbel MJ. Investigation of role of nitric oxide in protection from Bordetella pertussis respiratory challenge. Infect. Immun. 70, 679-684 (2002). Demonstration of role of nitric oxide in immunity to experimental pertussis.
74. Xing DKL, Canthaboo C, Corbel MJ. Nitric oxide induction in murine macrophages and spleen cells by whole-cell Bordetella pertussis vaccine. Vaccine 16, 16-23 (1998).
75. Greco D, Salmaso S, Mastrantonio P et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. N. Engl. J. Med. 334, 341-348 (1996).
76. Gustafsson L, Hallander HO, Olin P, Reizenstein E, Storsaeter J. A controlled trial of a two component acellular, a five component acellular and a whole-cell pertussis vaccine. N. Engl. J. Med. 334, 349-355 (1996). Clinical trial comparing acellular and whole-cell vaccines.
77. Heiniger U, Cherry JD, Christenson PD et al. Comparative study of Lederle Takeda acellular and Lederle whole-cell pertussis-component diphtheria-tetanus pertussis vaccines in infants in Germany. Vaccine 12, 81-86 (1994).
78. Trollfors B, Taranger J, Lagergard T et al. A placebo-controlled trial of a pertussis-toxoid vaccine. N. Engl. J. Med. 333, 1045-1050 (1995).
79. Simondon F, Preziosi MP, Yam A et al. Randomized double-blind trial comparing a two-component acellular to a whole-cell pertussis vaccine in Senegal. Vaccine 15, 1606-1612 (1997).
80. Hedenskog S, Granstrom M, Olin P, Tiru M, Sato Y. A clinical trial of a monocomponent pertussis toxoid vaccine. Am. J. Dis. Chil. 141, 844-847 (1987).
81. Stainer DW, Scholte MJ. A simple chemically defined medium for the production of Phase I Bordetella pertussis. J. Gen. Microbiol. 63, 211-220 (1971).
82. Guiso N, Wirsing von Konig CH, Becker C, Hallander H. Fimbrial typing of Bordetella pertussis isolates; agglutination with polyclonal and monoclonal antisera. J. Clin. Microbiol. 39, 1684-1685 (2001).
83. Xing DKL, Ramakrishnan S, Newland P, Corbel MJ. Fimbrial typing of Bordetella pertussis isolates: agglutination with polyclonal and monoclonal antibodies. J. Clin. Microb. 39, 4220 (2001).
84. Requirements for diphtheria, tetanus, pertussis and combined vaccines. In: WHO technical Report Series No. 800. 87-149 (1990). WHO recommendations for whole-cell pertussis vaccines.
85. Diphtheria, tetanus and pertussis vaccine (adsorbed). In: European Pharmacopeia (4th ed.), 2178-2200 (2002)
86. Xing D, Das RG, O'Neill T et al. and participants. Laboratory testing of whole-cell pertussis vaccine: a WHO proficiency study using the Kendrick test. Vaccine 20, 342-51 (2002). Inter-laboratory comparison of Kendrick potency test.
87. Chazono M, Yoshida I, Konobe T, Fukai F. The purification and characterisation of an acellular pertussis vaccine. J. Biol. Stand. 16, 630-689 (1988).
88. Aoyama T, Murase Y, Kato T. Efficacy of an acellular pertussis vaccine in Japan. J. Ped. 107, 180-183 (1985).
89. Rappuoli R. Toxin inactivation and antigen stabilisation: two different uses of formaldehyde. Vaccine 12, 579-581 (1994).
90. Diphtheria-pertussis-tetanus combination vaccine, In: Minimum requirements for Biological products. Association of Biologicals Manufacturers of Japan, 41-49 (1986). Japanese requirements for pertussis vaccines.
91. Guidelines for the production and control of the acellular pertussis component of monovalent or combined vaccines. In: WHO Technical Report Series. 878, 57-72 (1998). WHO recommendations for acellular vaccines.
92. Pertussis vaccine, In: US Code of Federal Regulations. Government Printing Office, DC, USA. 58-61 (1983).
93. Pertussis vaccine (acellular, component, adsorbed), In: European Pharmacopeia Supplement 1050-1052 (2000).
94. Cohen H, van Ramshorst JD, Drion FE. Relation between toxicity tests in mice and reactions in children using four lots of quadruple vaccine (DTP-polio). Sym. Series Immunobiol. Stand. 10, 53-62 (1969).
95. Butler NR, Voyce MA, Burland WL, Hilton ML. Advantages of aluminium hydroxide adsorbed combined diphtheria, tetanus and pertussis vaccine for the immunisation of infants. Br. Med. J. 1, 663-666 (1969).
96. Hilton ML, Burland WL. Pertussis-containing vaccines: The relationship between laboratory toxicity tests and reactions in children. Sym. Series Immunobiol. Stand. 13, 150-156 (1970).
97. Perkins FT, Sheffield F, Miller CL, Skegg JL. The comparison of toxicity of pertussis vaccines in children and mice. Sym. Series Immunobiol. Stand. 13, 41-49 (1970).
98. Kappelle IS, Gun JW, Marsman FR, Hendriksen C, Donk H. Collaborative study on test systems to assess toxicity of whole-cell pertussis vaccine. Biologicals 25, 41-57 (1997).
99. Locht C, Antoine R. Bordetella pertussis protein toxins. In: Bacterial Protein Toxins. Alouf JE, Freer JH (Eds.), (2nd ed.), Academic press, London, UK, 130-146 (1999).
100. Ibsen PH. The effect of formaldehyde, hydrogen peroxide and genetic detoxification of pertussis toxin on epitope recognition by murine monoclonal antibodies. Vaccine 14, 359-368 (1996).
101. Gillenius P, Jaatmaa E, Askelof P, Granstrom M, Tiru M. The standardization of an assay for pertussis toxin and antitoxin in microplate culture of Chinese hamster ovary cells. J. Biol. Stand. 13, 61-66 (1985).
102. Kataoka M, Toyoizumi H, Yamamoto A, Ochiai M, Horiuchi Y. Chinese Hamster Ovary (CHO) cell clustering does not correlate with in vivo histamine-sensitisation when measuring residual activity of aldehyde-treated pertussis toxin (PT). Biologicals 30, 297-302 (2002).
103. Yuen CT, Canthaboo C, Menzies JA et al. An enzymatic-HPLC coupled assay for determination of ribosylation activity of pertussis toxin and its correlation with toxic effect in vivo. Vaccine 21, 44-52 (2002).
104. Chaby R, Caroff M. Lipopolysaccharides of Bordetella pertussis endotoxin. In: Pathogenesis and immunity in pertussis Wardlaw AC, Parton R (Eds.), John Wiley and Sons, UK, 247-271 (1988).
105. Poole S, Musset MV. The International Standard for endotoxin: evaluation in an international collaborative study. J. Biol. Stand. 17, 161-171 (1989).
106. Ochiai M, Kataoka M, Toyoizumi H et al. Evaluation of endotoxin content of diphtheria tetanus acellular pertussis combined (DTaP) vaccines that interfere with the bacterial endotoxin test. Vaccine 21, 1862-1866 (2003).
107. Nakagawa Y, Maeda H, Murai T. Evaluation of the in vitro pyrogen test system based on pro-inflammatory cytokine release from human monocytes: Comparison with a human whole blood culture test svstem and with the rabbit pyrogen test. Clin. Diag. Lab. Immun. 9, 588-597 (2002).
108. Westrop GD, Campbell G, Kazi Y et al. A new assay for the invasive adenyl cyclase toxin of Bordetella pertussis based on its morphological effects on the fibronectin-stimulated spreading of BHK21 cells. Microbiology 140, 245-253 (1994).
109. Horiguchi Y, Sugimoto N, Matsuda M. Bordetella bronchiseptica dermonecrotizing toxin stimulates protein synthesis in an osteoblastic clone, MC3T3-E1 cells. FEMS Microbiol. Lett. 120, 19-22 (1994).
110. Senda T, Horiguchi Y, Umemoto M, Sugimoto N, Matsuda M. Bordetella bronchiseptica dermonecrotizing toxin, which activates a small GTP-binding protein rho, induces membrane organelle proliferation and caveolae formation. Exp. Cell Res. 230, 163-168 (1997).
111. Zhang YL, Sekura RD. Purification and charaterisation of the heat-labile toxin of Bordetella pertussis. Infect. Immun. 59, 3754-3759 (1991).
112. Goldman WE, Klapper DG, Baseman JB. Detection, isolation and analysis of a released Bordetella pertussis product toxic to cultured tracheal cells. Infect. Immun. 36, 782-794 (1982).
113. Cookson BT, Cho HL, Herwaldt LA, Goldman WE. Biological activities and chemical composition of purified tracheal cytotoxin of Bordetella pertussis. Infect. Immun. 57, 2223-2229 (1989).
114. Flak TA, Goldman WE. Muramyl peptide probes derived from tracheal cytotoxin of Bordetella pertussis. Anal. Biochem. 264, 41-46 (1998).
115. Ark A, Kappelle I, Akkermans A, Hendriksen C, Donk H, Development of pertussis serological potency test. Biological 22, 233-242 (1994).
116. Sakural S, Kamachi K, Konda T et al. Nitric oxide induction by pertussis toxin in mouse spleen cells via gamma interferon. Infect. Immun. 64, 1309-1313 (1996).
117. Xing DKL, Canthaboo C, Corbel MJ. Development of a nitric oxide induction assay as a potential replacement for the intracerebral mouse protection test for potency assay of pertussis whole-cell vaccines. Dev. Biol. Stand. 101, 95-103 (1999).
118. Sato H, Sato Y. Pertussis vaccine. In: Vaccine Handbook, Researcher's Associates, The National Institute of Health (Ed.), Maruzen Co. Ltd, Tokyo, Japan 39-51 (1996).
119. Mills KHG, Ryan M, Ryan E, Mahon BP. A murine model in which protection correlates with pertussis vaccine efficacy in children reveals complementary roles for humoral and cell-mediated immunity in protection agains Bordetella pertussis. Infect. Immun. 66, 594-602 (1998). Laboratory evaluation of mechanisms of immunity to pertussis vaccines.
120. Syukuda Y, Watanabe H, Suehara A et al. Aerosol infection test for evaluation of pertussis vaccine. Tokai J. Exp. Med. 13, 71-77 (1988).
121. Guiso N, Capiau C, Poolman J, Hauser P. Intranasal murine model of Bordetella pertussis infection. I. Prediction of protection in human infants by acellular vaccines. Vaccine 17, 2366-2376 (1999). A challenge model for acellular vaccines.
122. Sato Y, Izzumiya K, Sato H, Cowell JL, Manclark CR. Aerosol infection of mice with Bordetella pertussis. Infect. Immun. 29, 261-266 (1980).
123. Peterson JP, Ibsen PH, Hasløv K, Heron I. Proliferative responses and gamma interferon and tumor necrosis factor production by lymphocytes isolated from tracheobroncheal lymph nodes and spleens of mice aerosol infected with Bordetella pertussis. Infect. Immun. 60, 4563-4570 (1992).
124. Canthaboo C, Xing D, Douglas A, Corbel MJ. Investigation of an aerosol challenge model as alternative to the intracerebral mouse protection test for potency assay of whole-cell pertussis vaccines. Biologicals 28, 241-246 (2000).
125. Xing DKL, Das RG, Williams L et al. An aerosol challenge model of Bordetella pertussis infection as a potential bioassay for acellular pertussis vaccines. Vaccine 17, 565-576 (1999). Description of an improved aerosol challenge model for evaluating acellular vaccines.
126. Belcher CE, Drenkow J, Kehoe B et al. The transcriptional responses of respiratory epithelial cells to Bordetella pertussis reveal host defensive and pathogen counter-defensive strategies. Proc. Natl Acad. Sci. 97, 13847-13852 (2000). Use of gene microarrays for assessing toxic effects of B. pertussis components.
127. Boldrick JC, Alizadeh AA, Diehn M et al. Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc. Natl Acad. Sci. 99, 972-977 (2002).