Selected prfA* mutations in recombinant attenuated Listeria monocytogenes strains augment expression of foreign immunogens and enhance vaccine-elicited humoral and cellular immune responses

Infection and Immunity

Volumn 76, Issue 8, 2008, Pages 3439-3450

  Yan, Lin ^a   Qiu, Jin ^a   Chen, Jianbo ^a,b   Ryan Payseur, Bridgett ^a   Huang, Dan ^a   Wang, Yunqi ^a   Rong, Lijun ^a   Melton Witt, Jody A ^c   Freitag, Nancy E ^a   Chen, Zheng W ^a,d  

^a UNIVERSITY OF ILLINOIS   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MC790 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; LIVE VACCINE; RECOMBINANT LISTERIA MONOCYTOGENES VACCINE; VIRUS ANTIGEN; BACTERIUM ANTIBODY; GAMMA INTERFERON; PEPTIDE CHAIN TERMINATION RELEASE FACTOR 1; PEPTIDE CHAIN-TERMINATION RELEASE FACTOR 1; RECOMBINANT PROTEIN; TRANSLATION TERMINATION FACTOR; VIRUS ANTIBODY;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CELLULAR IMMUNITY; GENE ACTIVATION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMORAL IMMUNITY; LISTERIA MONOCYTOGENES; MUTATION; NONHUMAN; PRFA GENE; PRIORITY JOURNAL; UPREGULATION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BLOOD; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETICS; IMMUNIZATION; IMMUNOLOGY; MOUSE; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, VIRAL; BACTERIAL VACCINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNIZATION, SECONDARY; INTERFERON TYPE II; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED BALB C; MUTATION; PEPTIDE TERMINATION FACTORS; RECOMBINANT PROTEINS; T-LYMPHOCYTES; VACCINES, ATTENUATED;

EID: 48849107349     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00245-08     Document Type: Article

References (57)

1. Ali, Z., L. Shao, L. Halliday, A. Reichenberg, M. Hintz, H. Jomaa, and Z. W. Chen. 2007. Prolonged (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate-driven antimicrobial and cytotoxic responses of pulmonary and systemic Vγ2Vδ2 T cells in macaques. J. Immunol. 179:8287-8296.
2. Angelakopoulos, H., K. Loock, D. M. Sisul, E. R. Jensen, J. F. Miller, and E. L. Hohmann. 2002. 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. 70:3592-3601.
3. + T cell response to Listeria monocytogenes in the absence of perforin and IFN-gamma. J. Immunol. 164:6444-6452.
4. + T cells after infection. Nat. Immunol. 3:619-626.
5. Behari, J., and P. Youngman. 1998. Regulation of hly expression in Listeria monocytogenes by carbon sources and pH occurs through separate mechanisms mediated by PrfA. Infect. Immun. 66:3635-3642.
6. Bouwer, H. G., H. Shen, X. Fan, J. F. Miller, R. A. Barry, and D. J. Hinrichs. 1999. Existing antilisterial immunity does not inhibit the development of a Listeria monocytogenes-specific primary cytotoxic T-lymphocyte response. Infect. Immun. 67:253-258.
7. Boyer, J. D., T. M. Robinson, P. C. Maciag, X. Peng, R. S. Johnson, G. Pavlakis, M. G. Lewis, A. Shen, R. Siliciano, C. R. Brown, D. B. Weiner, and Y. Paterson. 2005. DNA prime Listeria boost induces a cellular immune response to SIV antigens in the rhesus macaque model that is capable of limited suppression of SIV239 viral replication. Virology 333:88-101.
8. Brockstedt, D. G., M. A. Giedlin, M. L. Leong, K. S. Bahjat, Y. Gao, W. Luckett, W. Liu, D. N. Cook, D. A. Portnoy, and T. W. Dubensky, Jr. 2004. Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc. Natl. Acad. Sci. USA 101:13832-13837.
9. Bron, P. A., I. R. Monk, S. C. Corr, C. Hill, and C. G. Gahan. 2006. Novel luciferase reporter system for in vitro and organ-specific monitoring of differential gene expression in Listeria monocytogenes. Appl. Environ. Microbiol. 72:2876-2884.
10. Bruhn, K. W., N. Craft, and J. F. Miller. 2007. Listeria as a vaccine vector. Microbes Infect. 9:1226-1235.
11. Brundage, R. A., G. A. Smith, A. Camilli, J. A. Theriot, and D. A. Portnoy. 1993. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc. Natl. Acad. Sci. USA 90:11890- 11894.
12. Bubert, A., Z. Sokolovic, S. K. Chun, L. Papatheodorou, A. Simm, and W. Goebel. 1999. Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Mol. Gen. Genet. 261:323-336.
13. Busch, D. H., I. M. Pilip, S. Vijh, and E. G. Pamer. 1998. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity 8:353-362.
14. Cossart, P. 2002. Molecular and cellular basis of the infection by Listeria monocytogenes: an overview. Int. J. Med. Microbiol. 291:401-409.
15. Cote, C. K., C. A. Rossi, A. S. Kang, P. R. Morrow, J. S. Lee, and S. L. Welkos. 2005. The detection of protective antigen (PA) associated with spores of Bacillus anthracis and the effects of anti-PA antibodies on spore germination and macrophage interactions. Microb. Pathog. 38:209-225.
16. Darji, A., W. Mohamed, E. Domann, and T. Chakraborty. 2003. Induction of immune responses by attenuated isogenic mutant strains of Listeria monocytogenes. Vaccine 21(Suppl. 2):S102-S109.
17. Davies, D. H., M. M. McCausland, C. Valdez, D. Huynh, J. E. Hernandez, Y. Mu, S. Hirst, L. Villarreal, P. L. Feigner, and S. Crotty. 2005. Vaccinia virus H3L envelope protein is a major target of neutralizing antibodies in humans and elicits protection against lethal challenge in mice. J. Virol. 79:11724-11733.
18. Domann, E., J. Wehland, M. Rohde, S. Pistor, M. Hartl, W. Goebel, M. Leimeister-Wachter, M. Wuenscher, and T. Chakraborty. 1992. A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J. 11:1981-1990.
19. Dussurget, O., J. Pizarro-Cerda, and P. Cossart. 2004. Molecular determinants of Listeria monocytogenes virulence. Annu. Rev. Microbiol. 58:587-610.
20. Edelson, B. T., and E. R. Unanue. 2000. Immunity to Listeria infection. Curr. Opin. Immunol. 12:425-431.
21. Eiting, M., G. Hageluken, W. D. Schubert, and D. W. Heinz. 2005. The mutation G145S in PrfA, a key virulence regulator of Listeria monocytogenes, increases DNA-binding affinity by stabilizing the HTH motif. Mol. Microbiol. 56:433-446.
22. Freitag, N. E. 2006. From hot dogs to host cells: how the bacterial pathogen Listeria monocytogenes regulates virulence gene expression. Future Microbiol. 1:89-101.
23. Freitag, N. E., L. Rong, and D. A. Portnoy. 1993. Regulation of the PrfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cell-to-cell spread. Infect. Immun. 61:2537-2544.
24. Freitag, N. E., P. Youngman, and D. A. Portnoy. 1992. Transcriptional activation of the Listeria monocytogenes hemolysin gene in Bacillus subtilis. J. Bacteriol. 174:1293-1298.
25. Gray, M. J., N. E. Freitag, and K. J. Boor. 2006. How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect. Immun. 74:2505-2512.
26. Hamon, M., H. Bierne, and P. Cossart. 2006. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4:423-434.
27. Harty, J. T., and M. J. Bevan. 1995. Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 3:109-117.
28. Huang, D., Y. Shen, L. Qiu, C. Y. Chen, L. Shen, J. Estep, R. Hunt, D. Vasconcelos, G. Du, P. Aye, A. A. Lackner, M. H. Larsen, W. R. Jacobs, Jr., B. F. Haynes, N. L. Letvin, and Z. W. Chen. 2008. Immune distribution and localization of phosphoantigen-specific Vγ2Vδ2 T cells in lymphoid and nonlymphoid tissues in Mycobacterium tuberculosis infection. Infect. Immun. 76:426-436.
29. Kocks, C., E. Gouin, M. Tabouret, P. Berche, H. Ohayon, and P. Cossart. 1992. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68:521-531.
30. Kreft, J., and J. A. Vazquez-Boland. 2001. Regulation of virulence genes in Listeria. Int. J. Med. Microbiol. 291:145-157.
31. Lauer, P., M. Y. Chow, M. J. Loessner, D. A. Portnoy, and R. Calendar. 2002. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184:4177-4186.
32. Lecuit, M., S. Vandonnael-Pournin, J. Lefort, M. Huerre, P. Gounon, C. Dupuy, C. Babinet, and P. Cossart. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292:1722-1725.
33. Leimeister-Wachter, M., C. Haffner, E. Domann, W. Goebel, and T. Chakraborty. 1990. Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc. Natl. Acad. Sci. USA 87:8336-8340.
34. Li, Z., X. Zhao, D. E. Higgins, and F. R. Frankel. 2005. Conditional lethality yields a new vaccine strain of Listeria monocytogenes for the induction of cell-mediated immunity. Infect. Immun. 73:5065-5073.
35. Mercado, R., S. Vp, S. E. Allen, K. Kerksiek, I. M. Pilip, and E. G. Pamer. 2000. Early programming of T cell populations responding to bacterial infection. J. Immunol. 165:6833-6839.
36. Moors, M. A., B. Levitt, P. Youngman, and D. A. Portnoy. 1999. Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect. Immun. 67:131-139.
37. Mueller, K. J., and N. E. Freitag. 2005. Pleiotropic enhancement of bacterial pathogenesis resulting from the constitutive activation of the Listeria monocytogenes regulatory factor PrfA. Infect. Immun. 73:1917-1926.
38. Orr, M. T., N. N. Orgun, C. B. Wilson, and S. S. Way. 2007. Cutting edge: recombinant Listeria monocytogenes expressing a single immune-dominant peptide confers protective immunity to herpes simplex virus-1 infection. J. Immunol. 178:4731-1735.
39. Pamer, E. G. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. 4:812-823.
40. Pan, Z. K., G. Ikonomidis, A. Lazenby, D. Pardoll, and Y. Paterson. 1995. 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. 1:471-477.
41. Paterson, Y., and R. S. Johnson. 2004. Progress towards the use of Listeria monocytogenes as a live bacterial vaccine vector for the delivery of HIV antigens. Expert Rev. Vaccines 3:S119-S134.
42. Peters, C., E. Domann, A. Darbouche, T. Chakraborty, and M. E. Mielke. 2003. Tailoring host immune responses to Listeria by manipulation of virulence genes - the interface between innate and acquired immunity. FEMS Immunol. Med. Microbiol. 35:243-253.
43. Pym, A. S., P. Brodin, L. Majlessi, R. Brosch, C. Demangel, A. Williams, K. E. Griffiths, G. Marchai, C. Leclerc, and S. T. Cole. 2003. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 9:533-539.
44. Ripio, M. T., G. Dominguez-Bernal, M. Lara, M. Suarez, and J. A. Vazquez-Boland. 1997. A Gly145Ser substitution in the transcriptional activator PrfA causes constitutive overexpression of virulence factors in Listeria monocytogenes. J. Bacteriol. 179:1533-1540.
45. Ripio, M. T., G. Dominguez-Bernal, M. Suarez, K. Brehm, P. Berche, and J. A. Vazquez-Boland. 1996. Transcriptional activation of virulence genes in wild-type strains of Listeria monocytogenes in response to a change in the extracellular medium composition. Res. Microbiol. 147:371-384.
46. Scortti, M., H. J. Monzo, L. Lacharme-Lora, D. A. Lewis, and J. A. Vazquez-Boland. 2007. The PrfA virulence regulon. Microbes Infect. 9:1196-1207.
47. Shen, Y., L. Shen, P. Sehgal, D. Huang, L. Qiu, G. Du, N. L. Letvin, and Z. W. Chen. 2004. Clinical latency and reactivation of AIDS-related mycobacterial infections. J. Virol. 78:14023-14032.
48. + T cells during mycobacterial infections. Science 295:2255-2258.
49. Shetron-Rama, L. M., K. Mueller, J. M. Bravo, H. G. Bouwer, S. S. Way, and N. E. Freitag. 2003. Isolation of Listeria monocytogenes mutants with high-level in vitro expression of host cytosol-induced gene products. Mol. Microbiol. 48:1537-1551.
50. Skoble, J., D. A. Portnoy, and M. D. Welch. 2000. Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J. Cell Biol. 150:527-538.
51. Slifka, M. K., H. Shen, M. Matloubian, E. R. Jensen, J. F. Miller, and R. Ahmed. 1996. Antiviral cytotoxic T-cell memory by vaccination with recombinant Listeria monocytogenes. J. Virol. 70:2902-2910.
52. Starks, H., K. W. Bruhn, H. Shen, R. A. Barry, T. W. Dubensky, D. Brockstedt, D. J. Hinrichs, D. E. Higgins, J. F. Miller, M. Giedlin, and H. G. Bouwer. 2004. Listeria monocytogenes as a vaccine vector: virulence attenuation or existing antivector immunity does not diminish therapeutic efficacy. J. Immunol. 173:420-427.
53. Stevens, R., A. Lavoy, S. Nordone, M. Burkhard, and G. A. Dean. 2005. Pre-existing immunity to pathogenic Listeria monocytogenes does not prevent induction of immune responses to feline immunodeficiency virus by a novel recombinant Listeria monocytogenes vaccine. Vaccine 23:1479-1490.
54. + T-cell priming against a nonsecreted Listeria monocytogenes antigen is independent of the antimicrobial activities of gamma interferon. Infect. Immun. 68:2196-2204.
55. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. Dominguez-Bernal, W. Goebel, B. Gonzalez-Zorn, J. Wehland, and J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
56. Weiskirch, L. M., and Y. Paterson. 1997. Listeria monocytogenes: a potent vaccine vector for neoplastic and infectious disease. Immunol. Rev. 158:159-169.
57. Zhao, X., Z. Li, B. Gu, and F. R. Frankel. 2005. Pathogenicity and immunogenicity of a vaccine strain of Listeria monocytogenes that relies on a suicide plasmid to supply an essential gene product. Infect. Immun. 73:5789-5798.