Listeriolysin O is strongly immunogenic independently of its cytotoxic activity

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Carrero, Javier A ^a   Vivanco Cid, Hector ^b   Unanue, Emil R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSIDAD VERACRUZANA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; LISTERIOLYSIN O; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MUTANT PROTEIN; RECOMBINANT PROTEIN; TRYPTOPHAN; BACTERIAL TOXIN; HEAT SHOCK PROTEIN; HEMOLYSIN; HLYA PROTEIN, LISTERIA MONOCYTOGENES;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; ENDOSOME; IMMUNOCYTOTOXICITY; IMMUNOGENICITY; IN VIVO STUDY; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN TRANSPORT; T LYMPHOCYTE ACTIVATION; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; ANTIGEN PRESENTING CELL; CHEMISTRY; CYTOLOGY; DRUG EFFECT; IMMUNIZATION; IMMUNOLOGY; METABOLISM;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; BACTERIAL TOXINS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; ENDOSOMES; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; IMMUNIZATION; MICE; PROTEIN TRANSPORT;

EID: 84857741923     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032310     Document Type: Article

References (52)

1. Gilbert RJ, (2010) Cholesterol-dependent cytolysins. Adv Exp Med Biol 677: 56-66.
2. Schnupf P, Portnoy DA, (2007) Listeriolysin O: a phagosome-specific lysin. Microb and Infect 9: 1176-1187.
3. Barsig J, Kaufmann SH, (1997) The mechanism of cell death in Listeria monocytogenes-infected murine macrophages is distinct from apoptosis. Infect Immun 65: 4075-4081.
4. Carrero JA, Unanue ER, (2006) Lymphocyte apoptosis as an immune subversion strategy of microbial pathogens. Trends Immunol 27: 497-503.
5. Carrero JA, Unanue ER, (2007) Impact of lymphocyte apoptosis on the innate immune stages of infection. Immunol Res 38: 333-341.
6. Carrero JA, Vivanco-Cid H, Unanue ER, (2008) Granzymes drive a rapid listeriolysin O-induced T cell apoptosis. J Immunol 181: 1365-1374.
7. Guzman CA, Domann E, Rohde M, Bruder D, Darji A, et al. (1996) Apoptosis of mouse dendritic cells is triggered by listeriolysin, the major virulence determinant of Listeria monocytogenes. Mol Microbiol 20: 119-126.
8. Sauer JD, Witte CE, Zemansky J, Hanson B, Lauer P, et al. (2010) Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7: 412-419.
9. Berche P, Gaillard JL, Geoffroy C, Alouf JE, (1987) T cell recognition of listeriolysin O is induced during infection with Listeria monocytogenes. J Immunol 139: 3813-3821.
10. Gaillard JL, Berche P, Sansonetti P, (1986) Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun 52: 50-55.
11. Hamilton SE, Badovinac VP, Khanolkar A, Harty JT, (2006) Listeriolysin O-deficient Listeria monocytogenes as a vaccine delivery vehicle: antigen-specific CD8 T cell priming and protective immunity. J Immunol 177: 4012-4020.
12. Portnoy DA, Jacks PS, Hinrichs DJ, (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
13. Decatur AL, Portnoy DA, (2000) A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 290: 992-995.
14. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, et al. (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110: 551-561.
15. Leimeister-Wachter M, Haffner C, Domann E, Goebel W, Chakraborty T, (1990) Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of listeria monocytogenes. Proc Natl Acad Sci U S A 87: 8336-8340.
16. Glomski IJ, Decatur AL, Portnoy DA, (2003) Listeria monocytogenes mutants that fail to compartmentalize listerolysin O activity are cytotoxic, avirulent, and unable to evade host extracellular defenses. Infect Immun 71: 6754-6765.
17. Beattie IA, Swaminathan B, Ziegler HK, (1990) Cloning and characterization of T-cell-reactive protein antigens from Listeria monocytogenes. Infect Immun 58: 2792-2803.
18. Geginat G, Schenk S, Skoberne M, Goebel W, Hof H, (2001) A novel approach of direct ex vivo epitope mapping identifies dominant and subdominant CD4 and CD8 T cell epitopes from Listeria monocytogenes. J Immunol 166: 1877-1884.
19. Pamer EG, Harty JT, Bevan MJ, (1991) Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes. Nature 353: 852-855.
20. Safley SA, Cluff CW, Marshall NE, Ziegler HK, (1991) Role of listeriolysin-O (LLO) in the T lymphocyte response to infection with Listeria monocytogenes. Identification of T cell epitopes of LLO. J Immunol 146: 3604-3616.
21. Sewell DA, Shahabi V, Gunn GR 3rd, Pan ZK, Dominiecki ME, et al. (2004) Recombinant Listeria vaccines containing PEST sequences are potent immune adjuvants for the tumor-associated antigen human papillomavirus-16 E7. Cancer Res 64: 8821-8825.
22. Carrero JA, Calderon B, Unanue ER, (2004) Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J Immunol 172: 4866-4874.
23. Gekara NO, Zietara N, Geffers R, Weiss S, (2010) Listeria monocytogenes induces T cell receptor unresponsiveness through pore-forming toxin listeriolysin O. J Infect Dis 202: 1698-1707.
24. Michel E, Reich KA, Favier R, Berche P, Cossart P, (1990) Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol Microbiol 4: 2167-2178.
25. Heuck AP, Moe PC, Johnson BB, (2010) The cholesterol-dependent cytolysin family of gram-positive bacterial toxins. Subcell Biochem 51: 551-577.
26. Browne KA, Blink E, Sutton VR, Froelich CJ, Jans DA, et al. (1999) Cytosolic delivery of granzyme B by bacterial toxins: evidence that endosomal disruption, in addition to transmembrane pore formation, is an important function of perforin. Mol Cell Biol 19: 8604-8615.
27. Hackam DJ, Rotstein OD, Zhang W, Gruenheid S, Gros P, et al. (1998) Host resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J Exp Med 188: 351-364.
28. Pu Z, Carrero JA, Unanue ER, (2002) Distinct recognition by two subsets of T cells of an MHC class II-peptide complex. Proc Natl Acad Sci U S A 99: 8844-8849.
29. Busch DH, Pilip I, Pamer EG, (1998) Evolution of a complex T cell receptor repertoire during primary and recall bacterial infection. J Exp Med 188: 61-70.
30. Darji A, Stockinger B, Wehland J, Chakraborty T, Weiss S, (1997) Antigen-specific T cell receptor antagonism by antigen-presenting cells treated with the hemolysin of Listeria monocytogenes: a novel type of immune escape. Eur J Immunol 27: 1696-1703.
31. Darji A, Stockinger B, Wehland J, Chakraborty T, Weiss S, (1997) T-cell anergy induced by antigen presenting cells treated with the hemolysin of Listeria monocytogenes. Imm Letters 57: 33-37.
32. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK, (2010) Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci U S A 107: 4341-4346.
33. Soltani CE, Hotze EM, Johnson AE, Tweten RK, (2007) Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions. Proc Natl Acad Sci U S A 104: 20226-20231.
34. Glomski IJ, Gedde MM, Tsang AW, Swanson JA, Portnoy DA, (2002) The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J Cell Biol 156: 1029-1038.
35. Schnupf P, Portnoy DA, Decatur AL, (2006) Phosphorylation, ubiquitination and degradation of listeriolysin O in mammalian cells: role of the PEST-like sequence. Cell Microbiol 8: 353-364.
36. Park JM, Ng VH, Maeda S, Rest RF, Karin M, (2004) Anthrolysin O and other gram-positive cytolysins are toll-like receptor 4 agonists. J Exp Med 200: 1647-1655.
37. Giddings KS, Zhao J, Sims PJ, Tweten RK, (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat Struct Mol Biol 11: 1173-1178.
38. Rosado CJ, Buckle AM, Law RH, Butcher RE, Kan WT, et al. (2007) A common fold mediates vertebrate defense and bacterial attack. Science 317: 1548-1551.
39. Heuck AP, Tweten RK, Johnson AE, (2003) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J Biol Chem 278: 31218-31225.
40. Polekhina G, Giddings KS, Tweten RK, Parker MW, (2005) Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc Natl Acad Sci U S A 102: 600-605.
41. Singh R, Dominiecki ME, Jaffee EM, Paterson Y, (2005) Fusion to Listeriolysin O and delivery by Listeria monocytogenes enhances the immunogenicity of HER-2/neu and reveals subdominant epitopes in the FVB/N mouse. J Immunol 175: 3663-3673.
42. Paterson Y, Guirnalda PD, Wood LM, (2010) Listeria and Salmonella bacterial vectors of tumor-associated antigens for cancer immunotherapy. Semin Immunol 22: 183-189.
43. Neeson P, Pan ZK, Paterson Y, (2008) Listeriolysin O is an improved protein carrier for lymphoma immunoglobulin idiotype and provides systemic protection against 38C13 lymphoma. Cancer Immunol Immunother 57: 493-505.
44. Edelson BT, Cossart P, Unanue ER, (1999) Cutting edge: paradigm revisited: antibody provides resistance to Listeria infection. J Immunol 163: 4087-4090.
45. Edelson BT, Unanue ER, (2001) Intracellular antibody neutralizes Listeria growth. Immunity 14: 503-512.
46. Carrero JA, Calderon B, Vivanco-Cid H, Unanue ER, (2009) Recombinant Listeria monocytogenes expressing a cell wall-associated listeriolysin O is weakly virulent but immunogenic. Infect Immun 77: 4371-4382.
47. Brunt LM, Portnoy DA, Unanue ER, (1990) Presentation of Listeria monocytogenes to CD8+ T cells requires secretion of hemolysin and intracellular bacterial growth. J Immunol 145: 3540-3546.
48. Velazquez C, Vidavsky I, van der Drift K, Gross ML, Unanue ER, (2002) Chemical identification of a low abundance lysozyme peptide family bound to I-Ak histocompatibility molecules. J Biol Chem 277: 42514-42522.
49. Celada A, Gray PW, Rinderknecht E, Schreiber RD, (1984) Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity. J Exp Med 160: 55-74.
50. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, et al. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176: 1693-1702.
51. Greenwood FC, Hunter WM, Glover JS, (1963) The Preparation of I-131-Labelled Human Growth Hormone of High Specific Radioactivity. Biochem J 89: 114-123.
52. Wade WF, Chen ZZ, Maki R, McKercher S, Palmer E, et al. (1989) Altered I-A protein-mediated transmembrane signaling in B cells that express truncated I-Ak protein. Proc Natl Acad Sci U S A 86: 6297-6301.