Haemolysin A and listeriolysin - Two vaccine delivery tools for the induction of cell-mediated immunity

International Journal for Parasitology

Volumn 33, Issue 5-6, 2003, Pages 495-505

  Dietrich, Guido ^a   Viret, Jean Francois ^a   Gentschev, Ivaylo ^b  

^a Berna Biotech AG   (Switzerland)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Attenuated live bacterial vaccines; Haemolysin secretion system; Listeriolysin; Vaccine delivery

Indexed keywords

85B ANTIGEN; BACTERIAL ANTIGEN; BCG VACCINE; CHOLERA VACCINE; CLOSTRIDIUM DIFFICILE TOXIN A; CYTOLYSIN; EARLY SECRETORY ANTIGENIC TARGET 6; HEMOLYSIN; HEMOLYSIN A; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; HYBRID PROTEIN; LISTERIOLYSIN; LIVE VACCINE; MALARIA VACCINE; MEASLES VACCINE; MYCOBACTERIUM ANTIGEN; PROTEIN E7; PROTEIN P60; PROTEIN P67; PROTEIN SSP 2; PROTOZOAL VACCINE; SHIGA TOXIN; SPOROZOITE VACCINE; SUPEROXIDE DISMUTASE; TUMOR VACCINE; TYPHOID VACCINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRULENCE FACTOR; VIRUS NUCLEOPROTEIN;

IMMUNE SYSTEM;

ANTIGEN EXPRESSION; BACTERIAL VIRULENCE; CANCER IMMUNOTHERAPY; CATTLE DISEASE; CELLULAR IMMUNITY; DRUG COST; DRUG DELIVERY SYSTEM; DRUG RESEARCH; ESCHERICHIA COLI; GRAM NEGATIVE INFECTION; HETEROLOGOUS EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; INFLUENZA VIRUS; LEISHMANIASIS; LISTERIA MONOCYTOGENES; MALARIA FALCIPARUM; MICROBIAL ATTENUATION; MORBIDITY; MORTALITY; MYCOBACTERIUM BOVIS; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN SECRETION; PROTOZOAL INFECTION; PROTOZOON; REVIEW; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SIDE EFFECT; SPOROZOITE; THEILERIA PARVA; TUBERCULOSIS; TUMOR; TYPHOID FEVER; VACCINATION; VIBRIO CHOLERAE; WART VIRUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA; LISTERIA MONOCYTOGENES; PROTOZOA;

EID: 0038362550     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0020-7519(03)00058-4     Document Type: Review

References (109)

1. Alexander J.E., Andrew P.W., Jones D., Roberts I.S. Characterization of an aromatic amino acid-dependent Listeria monocytogenes mutant: attenuation, persistence, and ability to induce protective immunity in mice. Infect. Immun. 61:1993;2245-2248.
2. Alfonso L.C., Scharton T.M., Vieira L.Q., Wysocka M., Trinchieri G., Scott P. The adjuvant effect of interleukin-12 in a vaccine against Leihmania major. Science. 263:1994;235-237.
3. Angelakopoulos H., Loock K., Sisul D.M., Jensen E.R., Miller J.F., Hohmann E.L. Safety and shedding of an attenuated strain of Listeria monocytogenes with a deletion of actA/plcB in adult volunteers: a dose escalation study of oral inoculation. Infect. Immun. 70:2002;3592-3601.
4. Bachmann M.F., Kopf M. The role of B cells in acute and chronic infections. Curr. Opin. Immunol. 11:1999;332-339.
5. Barry R.A., Bouwer H.G., Portnoy D.A., Hinrichs D.J. Pathogenicity and immunogenicity of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect. Immun. 60:1992;1625-1632.
6. Blight M.A., Chervaux C., Holland I.B. Protein secretion pathway in Escherichia coli. Curr. Opin. Biotechnol. 5:1994;468-474.
7. Blight M.A., Holland I.B. Heterologous protein secretion and the versatile Escherichia coli haemolysin translocator. Trends Biotechnol. 12:1994;450-455.
8. Brehm K., Haas A., Goebel W., Kreft J. A gene encoding a superoxide dismutase of the facultative intracellular bacterium Listeria monocytogenes. Gene. 118:1992;121-125.
9. + T cells requires secretion of haemolysin and intracellular bacterial growth. J. Immunol. 145:1990;3540-3546.
10. Calmette A. La Vaccination Preventive Contre la Tuberculose. 1927;Masson et Cie, Paris.
11. Cardenas L., Clements J.D. Oral immunisation using live attenuated Salmonella spp. as carriers of foreign antigens. Clin. Microbiol. Rev. 5:1992;328-342.
12. Casadevall A. Antibody-mediated protection against intracellular pathogens. Trends Microbiol. 6:1998;102-107.
13. Catic A., Dietrich G., Gentschev I., Goebel W., Kaufmann S.H.E., Hess J. Introduction of protein or DNA delivered via recombinant Salmonella typhimurium into the major histocompatibility complex class I presentation pathway of macrophages. Microbes Infect. 2:1999;111-121.
14. Chatfield S.N., Dougan G. Attenuated Salmonella as a live vector for expression of foreign antigens. Levine M.M., Woodrow G.C., Kaper J.B., Cobon G.S. New Generation Vaccines. 2nd ed. 1997;331-341 Marcel Dekker, New York, NY.
15. Chervaux C., Sauvonnet N., Le Clainche A., Kenny B., Hung A.L., Broome-Smith J.K., Holland I.B. Secretion of active beta-lactamase to the medium mediated by the Escherichia coli haemolysin transport pathway. Mol. Gen. Genet. 249:1995;237-245.
16. Davis H.L., Brazolot Millan C.L., Watkins S.C. Immune-mediated destruction of transfected muscle fibers after direct gene transfer with antigen-expressing plasmid DNA. Gene Ther. 4:1997;181-188.
17. Decatur A.L., Portnoy D.A. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science. 290:2000;992-995.
18. Dietrich G., Bubert A., Gentschev I., Sokolovic Z., Simm A., Catic A., Kaufmann S.H.E., Hess J., Szalay A.A., Goebel W. Delivery of antigen-encoding plasmid DNA into the cytosol of macrophages by attenuated suicide Listeria monocytogenes. Nat. Biotechnol. 16:1998;181-185.
19. Dietrich G., Gentschev I., Hess J., Knapp B., Kaufmann S.H.E., Goebel W. From evil to good: a cytolysin in vaccine development. Trends Microbiol. 9:2001;23-28.
20. Dobbelaere D.A., Fernandez P.C., Heussler V.T. Theileria parva: taking control of host cell proliferation and survival mechanisms. Cell. Microbiol. 2:2000;91-99.
21. + cell-, interferon gamma-, and nitric oxide-dependent immunity. J. Exp. Med. 183:1996;1739-1746.
22. Edelman R., Palmer K., Russ K.G., Secrest H.P., Becker J.A., Bodison S.A., Perry J.G., Sills A.R., Barbour A.G., Luke C.J., Hanson M.S., Stover C.K., Burlein J.E., Bansal G.P., Connor E.M., Koenig S. Safety and immunogenicity of recombinant Bacille Calmette-Guerin (rBCG) expressing Borrelia burgdorferi outer surface protein A (OspA) lipoprotein in adult volunteers: a candidate Lyme disease vaccine. Vaccine. 17:1999;904-914.
23. Fenner F. The eradication of smallpox. Prog. Med. Virol. 23:1979;1-21.
24. Frankel F.R., Hegde S., Lieberman J., Paterson Y. Induction of cell-mediated immune responses to human immunodeficiency virus type 1 Gag protein by using Listeria monocytogenes as a live vaccine vector. J. Immunol. 155:1995;4775-4782.
25. Friedman R.S., Frankel F.R., Xu Z., Lieberman J. Induction of human immunodeficiency virus (HIV)-specific CD8 T-cell responses by Listeria monocytogenes and a hyperattenuated Listeria strain engineered to express HIV antigens. J. Virol. 74:2000;9987-9993.
26. Galen J.E., Levine M.M. Can a 'flawless' live vector vaccine strain be engineered? Trends Microbiol. 9:2001;372-376.
27. Gentschev I., Sokolovic Z., Köhler S., Krohne G.F., Hof H., Wagner J., Goebel W. Identification of p60 antibodies in human sera and presentation of this listerial antigen on the surface of attenuated salmonellae by the HlyB-HlyD secretion system. Infect. Immun. 60:1992;5091-5098.
28. Gentschev I., Mollenkopf H.-J., Sokolovic Z., Ludwig A., Tengel C., Gross R., Hess J., Demuth A., Goebel W. Synthesis and secretion of bacterial antigens by attenuated Salmonela via the Escherichia coli haemolysin system. Behring Inst. Mitt. 95:1994;57-66.
29. Gentschev I., Sokolovic Z., Mollenkopf H.-J., Hess J., Kaufmann S.H.E., Kuhn M., Krohne G.F., Goebel W. Salmonella secreting active listeriolysin changes its intracellular localization. Infect. Immun. 63:1995;4202-4205.
30. Gentschev I., Maier G., Kranig A., Goebel W. Mini-TnhlyAs: a new tool for the construction of secreted fusion proteins. Mol. Gen. Genet. 252:1996;266-274.
31. Gentschev I., Mollenkopf H., Sokolovic Z., Hess J., Kaufmann S.H.E., Goebel W. Development of antigen-delivery systems, based on the Escherichia coli haemolysin secretion pathway. Gene. 179:1996;133-140.
32. Gentschev I., Dietrich G., Mollenkopf H.-J., Sokolovic Z., Hess J., Kaufmann S.H.E., Goebel W. The Escherichia coli haemolysin secretion apparatus - a versatile anti-gen delivery system in attenuated Salmonella. Behring Inst. Mitt. 98:1997;103-113.
33. Gentschev I., Glaser I., Goebel W., McKeever D.J., Heussler V. Delivery of the p67 sporozoite antigen of Theileria parva using recombinant Salmonella: secretion of the product enhances specific antibody responses in cattle. Infect. Immun. 66:1998;2060-2064.
34. Gentschev I., Dietrich G., Spreng S., Kolb-Mäurer A., Daniels J., Hess J., Kaufmann S.H.E., Goebel W. Bacterial antigen and DNA delivery systems. J. Biotechnol. 83:2000;19-26.
35. Gentschev I., Dietrich G., Spreng S., Kolb-Mäurer A., Brinkmann V., Grode L., Kaufmann S.H.E., Hess J., Goebel W. Recombinant attenuated bacteria for the delivery of subunit vaccines. Vaccine. 19:2001;2621-2628.
36. Gentschev I., Dietrich G., Goebel W. The E. coli alpha-haemolysin secretion system and its use in vaccine development. Trends Microbiol. 10:2002;39-45.
37. Gomez-Duarte O.G., Pasetti M.F., Santiago A., Sztein M.B., Hoffman S.L., Levine M.M. Expression, extracellular secretion, and immunogenicity of the Plasmodium falciparum sporozoite surface protein 2 in Salmonella vaccine strains. Infect. Immun. 69:2001;1192-1198.
38. Goddeeris B., Morrison I., Teale A., Bensaid A., Baldwin C. Bovine cytotoxic T-cell clones specific for cells infected with the protozoan parasite Theileria parva: parasite strain specificity and class I major histocompatibility complex restriction. Proc. Natl Acad. Sci. USA. 83:1996;5238-5242.
39. + T lymphocytes by an attenuated Listeria monocytogenes actA mutant. Int. Immunol. 4:1992;1413-1418.
40. Grillot-Courvalin C., Goussard S., Huetz F., Ojcius D.M., Courvalin P. Functional gene transfer from intracellular bacteria to mammalian cells. Nat. Biotechnol. 16:1998;862-866.
41. Grillot-Courvalin C., Goussard S., Courvalin P. Wild-type intracellular bacteria deliver DNA into mammalian cells. Cell. Microbiol. 4:2002;177-186.
42. Gunn G.R., Zubair A., Peters C., Pan Z.K., Wu T.C., Paterson Y. Two Listeria monocytogenes vaccine vectors that express different molecular forms of human papilloma virus-16 (HPV-16) E7 induce qualitatively different T cell immunity that correlates with their ability to induce regression of established tumors immortalized by HPV-16. J. Immunol. 167:2001;6471-6479.
43. Gunn G.R., Peters C., Paterson Y. Listeriolysin - a useful cytolysin. Trends Microbiol. 9:2001;161-162.
44. + T cells. Eur. J. Immunol. 28:1998;1807-1814.
45. Hahn H.P., Hess C., Gabelsberger J., Domdey H., von Specht B.U.A. Salmonella typhimurium strain genetically engineered to secrete effectively a bioactive human interleukin (hIL)-6 via the Escherichia coli hemolysin secretion apparatus. FEMS Immunol. Med. Microbiol. 20:1998;111-119.
46. Harty J.T., Bevan M.J. CD8+ T cells specific for a single nonamer epitope of Listeria monocytogenes are protective in vivo. J. Exp. Med. 175:1992;1531-1538.
47. Hense M., Domann E., Krusch S., Wacholz P., Dittmar K.E.J., Rohde M., Wehland J., Chakraborty T., Weiss S. Eukaryotic expression plasmid transfer from the intracellular bacterium Listeria monocytogenes to host cells. Cell. Microbiol. 3:2001;599-609.
48. Hess J., Gentschev I., Goebel W., Jarchau T. Analysis of the haemolysin secretion system by PhoA-HlyA fusion proteins. Mol. Gen. Genet. 224:1990;201-208.
49. Hess J., Gentschev I., Szalay G., Ladel C., Bubert A., Goebel W., Kaufmann S.H.E. Listeria monocytogenes p60 supports host cell invasion by and in vivo survival of attenuated Salmonella typhimurium. Infect. Immun. 63:1995;2047-2053.
50. Hess J., Gentschev I., Miko D., Welzel M., Ladel C., Goebel W., Kaufmann S.H.E. Superior efficacy of secreted over somatic antigen display in recombinant Salmonella vaccine induced protection against listeriosis. Proc. Natl Acad. Sci. USA. 93:1996;1458-1463.
51. Hess J., Dietrich G., Gentschev I., Miko D., Goebel W., Kaufmann S.H.E. Protection against murine listeriosis by an attenuated recombinant Salmonella typhimurium vaccine strain that secretes the naturally somatic antigen superoxide dismutase. Infect. Immun. 65:1997;1286-1292.
52. Hess J., Miko D., Catic A., Lehmensiek V., Russel D.G., Kaufmann S.H.E. Mycobacterium bovis Bacille Calmette-Guerin strains secreting listeriolysin of Listeria monocytogenes. Proc. Natl Acad. Sci. USA. 95:1998;5299-5304.
53. Hess J., Grode L., Gentschev I., Hellwig J., Fensterle J., Brinkmann J., Dietrich G., Krohne G.F., Goebel W., Kaufmann S.H.E. Secretion of different listeriolysin cognates by recombinant attenuated Salmonella typhimurium: superior efficacy of haemolytic over non-haemolytic constructs after oral vaccination. Microbes Infect. 2:2000;1799-1806.
54. Hess J., Grode L., Hellwig J., Gentschev I., Goebel W., Ladel C., Kaufmann S.H.E. Protection against murine tuberculosis by an attenuated recombinant Salmonella typhimurium vaccine strain that secretes the 30 kDa-antigen of Mycobacterium bovis BCG. FEMS Immunol. Med. Microbiol. 27:2000;283-289.
55. Hormaeche C., Khan C. Recombinant bacteria as vaccine carriers of heterologous antigens. Kaufmann S.H.E. Concept in Vaccine Development. 1996;327-349 Walter de Gruyter, Berlin/New York, NY.
56. Ikonomidis G., Paterson Y., Kos F.J., Portnoy D.A. Delivery of a viral antigen to the class I processing and presentation pathway by Listeria monocytogenes. J. Exp. Med. 180:1994;2209-2218.
57. Ikonomidis G., Portnoy D.A., Gerhard W., Paterson Y. Influenza-specific immunity induced by recombinant Listeria monocytogenes vaccines. Vaccine. 15:1997;433-440.
58. Jarchau T., Chakraborty T., Garcia F., Goebel W. Selection for transport competence of C-terminal polypeptides from Escherichia coli haemolysin: the shortest peptide capable of autonomous HlyB/HlyD-dependent secretion comprises the 62 C-terminal amino acids of HlyA. Mol. Gen. Genet. 245:1994;53-60.
59. Jensen E.R., Selvakumar R., Shen H., Ahmed R., Wettstein F.O., Miller J.F. Recombinant Listeria monocytogenes vaccination eliminates papillomavirus-induced tumors and prevents papilloma formation from viral DNA. J. Virol. 71:1997;8467-8474.
60. Jondal M., Schirmbeck R., Reimann J. MHC class I-restricted CTL responses to exogenous antigens. Immunity. 5:1996;295-302.
61. Kaufmann S.H.E. Immunity to intracellular bacteria. Paul W.E. Fundamental Immunology. 1998;1335-1371 Lippincott-Raven, Philadelphia, PA.
62. Kern I., Ceglowski P. Secretion of streptokinase fusion proteins from Escherichia coli cells through the haemolysin transporter. Gene. 163:1995;53-57.
63. Kolb-Mäurer A., Gentschev I., Fries H.W., Fiedler F., Bröcker E.B., Kämpgen E., Goebel W. Listeria monocytogenes-infected human dendritic cells: invasion and host cell response. Infect. Immun. 66:2000;3680-3688.
64. Lauvau G., Vijh S., Kong P., Horng T., Kerksiek K., Serbina N., Tuma R.A., Pamer E.G. Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science. 294:2001;1735-1739.
65. Levine M.M., Ferreccio C., Black R.E., Germanier R. Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet. 1:1987;1049-1052.
66. Levine M.M., Kaper J.B. Live oral vaccines against cholera: an update. Vaccine. 11:1993;207-212.
67. Levine M.M., Galen J.E., Sztein M.B., Beier M., Noriega F. Attenuated Salmonella as a live vector for expression of foreign antigens. Part iii: Salmonella expressing protozoal antigens. Levine M.M., Woodrow G.C., Kaper J.B., Cobon G.S. New Generation Vaccines. 2nd ed. 1997;351-361 Marcel Dekker, New York, NY.
68. Lindberg A.A. Vaccination against enteric pathogens: from science to vaccine trials. Curr. Opin. Microbiol. 1:1998;116-124.
69. Lindberg A.A., Karnell A., Stocker B.A.D., Katakura S., Sweiha H., Reinholt F.P. Development of an auxotrophic oral live Shigella flexneri vaccine. Vaccine. 6:1988;146-150.
70. Ludwig A. Cytolytic toxins from gram-negative bacteria. Microbiologia. 12:1996;281-296.
71. Mata M., Travers P.J., Liu Q., Frankel F.R., Paterson Y. The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D. J. Immunol. 161:1998;2985-2993.
72. Mata M., Paterson Y. Th1 T cell responses to HIV-1 Gag protein delivered by a Listeria monocytogenes vaccine are similar to those induced by endogenous listerial antigens. J. Immunol. 163:1999;1449-1456.
73. Mata M., Paterson Y. Listeria monocytogenes as an alternative vaccine vector for HIV. Arch. Immunol. Ther. Exp. (Warsz). 48:2000;151-162.
74. Mata M., Yao Z., Zubair A., Syres K., Paterson Y. Evaluation of a recombinant Listeria monocytogenes expressing an HIV protein that protects mice against viral challenge. Vaccine. 19:2001;1435-1445.
75. Matsumoto S., Yukitake H., Kanbara H., Yamada T. Recombinant Mycobacterium bovis Bacillus Calmette-Guerin secreting merozoite surface protein 1 (MSP1) induces protection against rodent malaria parasite infection depending on MSP1-stimulated interferon gamma and parasite-specific antibodies. J. Exp. Med. 188:1998;845-854.
76. McGhee J.R., Mestecky J., Dertzbaugh M.T., Eldridge J.H., Hirasawa M., Kiyono H. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine. 10:1992;75-88.
77. McKeever D.J., Morrison W.I. Theileria parva: the nature of the immune response and its significance for immunoprophylaxis. Rev. Sci. Technol. 9:1990;405-421.
78. Michel E., Reich K.A., Favier R., Berche P., Cossart P. Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol. Microbiol. 4:1990;2167-2178.
79. Mielke M.E., Peters C., Hahn H. Cytokines in the induction and expression of T-cell-mediated granuloma formation and protection in the murine model of listeriosis. Immunol. Rev. 158:1997;79-93.
80. Mollenkopf H.J., Gentschev I., Goebel W. Conversion of bacterial gene products to secretion-competent fusion proteins. Biotechniques. 21:1996;854-860.
81. Mollenkopf H.J., Groine-Triebkorn D., Andersen P., Hess J., Kaufmann S.H.E. Protective efficacy against tuberculosis of ESAT-6 secreted by a live Salmonella typhimurium vaccine carrier strain and expressed by naked DNA. Vaccine. 19:2001;4028-4035.
82. Musoke A.J., Morzaria S., Nkonge C., Jones E., Nene V. A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proc. Natl Acad. Sci. USA. 89:1992;514-518.
83. Nakano H., Kawakami Y., Nishimura H. Secretion of genetically-engineered dihydrofolate reductase from Escherichia coli using an E. coli alpha-haemolysin membrane translocation system. Appl. Microbiol. Biotechnol. 37:1992;765-771.
84. Norval R.A.I., Perry B.P., Young A.S. The Epidemiology of Theileriosis in Africa. 1992;235-236 Academic Press, San Diego, CA.
85. Paglia P., Arioli I., Frahm N., Chakraborty T., Colombo M.P., Guzman C.A. The defined attenuated Listeria monocytogenes delta mp12 mutant is an effective oral vaccine carrier to trigger a long-lasting immune response against a mouse fibrosarcoma. Eur. J. Immunol. 27:1997;1570-1575.
86. Pan American Health Organization, 1994. EPI Newsletter. 16, 1-3.
87. Pan Z.K., Ikonomidis G., Lazenby A., Pardoll D., Paterson Y. A recombinant Listeria monocytogenes vaccine expressing a model tumour antigen protects mice against lethal tumour cell challenge and causes regression of established tumours. Nat. Med. 1:1995;471-477.
88. Pan Z.K., Ikonomidis G., Pardoll D., Paterson Y. Regression of established tumors in mice mediated by the oral administration of a recombinant Listeria monocytogenes vaccine. Cancer Res. 55:1995;4776-4779.
89. Pan Z.K., Weiskirch L.M., Paterson Y. Regression of established B16F10 melanoma with a recombinant Listeria monocytogenes vaccine. Cancer Res. 59:1999;5264-5269.
90. Paschen A., Dittmar K.E., Grenningloh R., Rohde M., Schadendorf D., Domann E., Chakraborty T., Weiss S. Human dendritic cells infected by Listeria monocytogenes: induction of maturation, requirements for phagolysosomal escape and antigen presentation capacity. Eur. J. Immunol. 30:2000;3447-3456.
91. Portnoy D.A., Chakraborty T., Goebel W., Cossart P. Molecular determinants of Listeria monocytogenes pathogenesis. Infect. Immun. 60:1992;1263-1267.
92. Rayevskaya M.V., Frankel F.R. Systemic immunity and mucosal immunity are induced against human immunodeficiency virus gag protein in mice by a new hyperattenuated strain of Listeria monocytogenes. J. Virol. 76:2001;2786-2791.
93. Robson K.J., Frevert U., Reckmann I., Cowan G., Beier J., Scragg I.G., Takehara K., Bishop D.H., Pradel G., Sinden R. Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J. 14:1995;3883-3894.
94. Ryan E.T., Butterton J.R., Smith R.N., Carroll P.A., Crean T.I., Calderwood S.B. Protective immunity against Clostridium difficile toxin A induced by oral immunisation with a live, attenuated Vibrio cholerae vector strain. Infect. Immun. 65:1997;2941-2949.
95. Shata M.T., Stevceva L., Agwale S., Lewis G.K., Hone D.M. Recent advances with recombinant bacterial vaccine vectors. Mol. Med. Today. 6:2000;66-71.
96. Sirard J.C., Fayolle C., de Chastellier C., Mock M., Leclerc C., Berche P. Intracytoplasmic delivery of listeriolysin O by a vaccinal strain of Bacillus anthracis induces CD8-mediated protection against Listeria monocytogenes. J. Immunol. 159:1997;4435-4443.
97. Shen H., Slifka M.K., Matloubian M., Jensen E.R., Ahmed R., Miller J.F. Recombinant Listeria monocytogenes as a live vaccine vehicle for the induction of protective anti-viral cell-mediated immunity. Proc. Natl Acad. Sci. USA. 92:1995;3987-3991.
98. Soussi N., Milon G., Colle J.H., Mougneau E., Glaichenhaus N., Goossens P.L. Listeria monocytogenes as a short-lived delivery system for the induction of type 1 cell-mediated immunity against the p36/LACK antigen of Leishmania major. Infect. Immun. 68:2000;1498-1506.
99. Soussi N., Saklani-Jusforgues H., Colle J.H., Milon G., Glaichenhaus N., Goossens P.L. Effect of intragastric and intraperitoneal immunisation with attenuated and wild-type LACK-expressing Listeria monocytoenes on control of murine Leishmania major infection. Vaccine. 20:2002;2702-2712.
100. Spreng S., Dietrich G., Goebel W., Gentschev I. The Escherichia coli haemolysin secretion apparatus: a potential universal antigen delivery system in gram-negative bacterial vaccine carriers. Mol. Microbiol. 31:1999;1596-1598.
101. Spreng S., Gentschev I., Goebel W., Weidinger G., ter Meulen V., Niewiesk S. Salmonella vaccines secreting measles virus epitopes induce protective immune responses against measles virus encephalitis. Microbes Infect. 2:2000;1687-1689.
102. Spreng S., Dietrich G., Niewiesk S., ter Meulen V., Gentschev I., Goebel W. Novel bacterial systems for the delivery of recombinant protein or DNA. FEMS Immunol. Med. Microbiol. 27:2000;299-304.
103. Thompson R.J., Bouwer H.G., Portnoy D.A., Frankel F.R. Pathogenicity and immunogenicity of a Listeria monocytogenes strain that requires D-alanine for growth. Infect. Immun. 66:1998;3552-3561.
104. Tzschaschel B.D., Guzman C.A., Timmis K.N., de Lorenzo V. An Escherichia coli haemolysin transport system-based vector for the export of polypeptides: export of Shiga-like toxin IIeB subunit by Salmonella typhimurium aroA. Nat. Biotechnol. 14:1996;765-769.
105. Tzschaschel B.D., Klee S.R., de Lorenzo V., Timmis K.N., Guzman C.A. Towards a vaccine candidate against Shigella dysenteriae 1: expression of the Shiga toxin B-subunit in an attenuated Shigella flexneri aroD carrier strain. Microb. Pathog. 21:1996;277-288.
106. Vijh S., Pamer E.G. Immunodominant and subdominant CTL responses to Listeria monocytogenes infection. J. Immunol. 158:1997;3366-3371.
107. Wagner W., Vogel M., Goebel W. Transport of haemolysin across the outer membrane of Escherichia coli requires two functions. J. Bacteriol. 154:1983;200-210.
108. Wandersman C., Delepelaire P. TolC, an Escherichia coli outer membrane protein required for haemolysin secretion. Proc. Natl Acad. Sci. USA. 87:1990;4776-4780.
109. Weiskirch L.M., Paterson Y. Listeria monocytogenes: a potent vaccine vector for neoplastic and infectious disease. Immunol. Rev. 158:1997;159-169.