Listeriolysin O as a strong immunogenic molecule for the development of new anti-tumor vaccines

Human Vaccines and Immunotherapeutics

Volumn 9, Issue 5, 2013, Pages 1058-1068

  Sun, Rui ^a   Liu, Yuqin ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

Anti tumor vaccine; Cancer immunotherapy; Cytotoxicity; Immunogenicity; Listeria; LLO; Pore forming toxin

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CANCER ANTIBODY; EPITOPE; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 6; LISTERIOLYSIN O; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR ANTIGEN;

CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TYPE; CYTOTOXICITY; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; LISTERIA MONOCYTOGENES; NONHUMAN; PHAGOSOME; REVIEW;

ANTI-TUMOR VACCINE; CANCER IMMUNOTHERAPY; CYTOTOXICITY; IMMUNOGENICITY; LISTERIA; LLO; PORE-FORMING TOXIN;

ADJUVANTS, IMMUNOLOGIC; ANTIGENS, NEOPLASM; BACTERIAL TOXINS; CANCER VACCINES; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; HUMANS; IMMUNE TOLERANCE; NEOPLASMS;

EID: 84878787539     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.23871     Document Type: Review

References (137)

1. Yaddanapudi K, Mitchell RA, Putty K, Willer S, Sharma RK, Yan J, et al. Vaccination with embryonic stem cells protects against lung cancer: is a broad-spectrum prophylactic vaccine against cancer possible? PLoS One 2012; 7:e42289; PMID:22860107; http://dx.doi.org/10.1371/journal.pone.0042289.
2. Paterson Y, Maciag PC. Listeria-based vaccines for cancer treatment. Curr Opin Mol Ther 2005; 7:454-60; PMID:16248280.
3. Nauts HC, McLaren JR. Coley toxins - the first century. Adv Exp Med Biol 1990; 267:483-500; PMID:2088067; http://dx.doi.org/10.1007/978-1-4684-5766-7-52.
4. Alexandroff AB, Jackson AM, O'Donnell MA, James K. BCG immunotherapy of bladder cancer: 20 years on. Lancet 1999; 353:1689-94; PMID:10335805; http://dx.doi.org/10.1016/S0140-6736(98)07422-4.
5. Shelley MD, Kynaston H, Court J, Wilt TJ, Coles B, Burgon K, et al. A systematic review of intravesical bacillus Calmette-Guérin plus transurethral resection vs transurethral resection alone in Ta and T1 bladder cancer. BJU Int 2001; 88:209-16; PMID:11488731; http://dx.doi.org/10.1046/j. 1464-410x.2001.02306.x.
6. Farber JM, Peterkin PI. Listeria monocytogenes, a foodborne pathogen. Microbiol Rev 1991; 55:476-511; PMID:1943998.
7. Vázquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Domínguez-Bernal G, Goebel W, et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14:584-640; PMID:11432815; http://dx.doi.org/10.1128/CMR.14.3.584-640.2001.
8. Gaillard JL, Finlay BB. Effect of cell polarization and differentiation on entry of Listeria monocytogenes into the enterocyte-like Caco-2 cell line. Infect Immun 1996; 64:1299-308; PMID:8606093.
9. Kuhn M, Goebel W. Identification of an extracellular protein of Listeria monocytogenes possibly involved in intracellular uptake by mammalian cells. Infect Immun 1989; 57:55-61; PMID:2491841.
10. Dramsi S, Biswas I, Maguin E, Braun L, Mastroeni P, Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 1995; 16:251-61; PMID:7565087; http://dx.doi.org/10.1111/j.1365-2958.1995.tb02297.x.
11. MacKaness GB. Cellular resistance to infection. J Exp Med 1962; 116:381-406; PMID:14467923; http://dx.doi.org/10.1084/jem.116.3.381.
12. Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 1991; 65:1127-41; PMID:1905979; http://dx.doi.org/10.1016/0092-8674(91)90009-N.
13. Drevets DA, Sawyer RT, Potter TA, Campbell PA. Listeria monocytogenes infects human endothelial cells by two distinct mechanisms. Infect Immun 1995; 63:4268-76; PMID:7591057.
14. Cossart P, Toledo-Arana A. Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 2008; 10:1041-50; PMID:18775788; http://dx.doi.org/10.1016/j.micinf.2008.07.043.
15. Bruhn KW, Craft N, Miller JF. Listeria as a vaccine vector. Microbes Infect 2007; 9:1226-35; PMID:17719258; http://dx.doi.org/10.1016/j.micinf.2007. 05.010.
16. Barry RA, Bouwer HG, Portnoy DA, Hinrichs DJ. Pathogenicity and immunogenicity of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect Immun 1992; 60:1625-32; PMID:1548084.
17. Bielecki J, Youngman P, Connelly P, Portnoy DA. Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature 1990; 345:175-6; PMID:2110628; http://dx.doi.org/10.1038/345175a0.
18. Portnoy DA, Tweten RK, Kehoe M, Bielecki J. Capacity of listeriolysin O, streptolysin O, and perfringolysin O to mediate growth of Bacillus subtilis within mammalian cells. Infect Immun 1992; 60:2710-7; PMID:1612739.
19. Goldfine H, Wadsworth SJ. Macrophage intracellular signaling induced by Listeria monocytogenes. Microbes Infect 2002; 4:1335-43; PMID:12443898; http://dx.doi.org/10.1016/S1286-4579(02)00011-4.
20. Smith GA, Marquis H, Jones S, Johnston NC, Portnoy DA, Goldfine H. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect Immun 1995; 63:4231-7; PMID:7591052.
21. Tilney LG, Portnoy DA. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 1989; 109:1597-608; PMID:2507553; http://dx.doi.org/10.1083/jcb.109.4.1597.
22. Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev Immunol 2004; 4:812-23; PMID:15459672; http://dx.doi.org/10.1038/nri1461.
23. Singh R, Paterson Y. Listeria monocytogenes as a vector for tumor-associated antigens for cancer immunotherapy. Expert Rev Vaccines 2006; 5:541-52; PMID:16989634; http://dx.doi.org/10.1586/14760584.5.4.541.
24. Wood LM, Guirnalda PD, Seavey MM, Paterson Y. Cancer immunotherapy using Listeria monocytogenes and listerial virulence factors. Immunol Res 2008; 42:233-45; PMID:19018479; http://dx.doi.org/10.1007/s12026-008-8087-0.
25. Witte CE, Archer KA, Rae CS, Sauer JD, Woodward JJ, Portnoy DA. Innate immune pathways triggered by Listeria monocytogenes and their role in the induction of cell-mediated immunity. Adv Immunol 2012; 113:135-56; PMID:22244582; http://dx.doi.org/10.1016/B978-0-12-394590-7.00002-6.
26. Woodward JJ, Iavarone AT, Portnoy DA. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 2010; 328:1703-5; PMID:20508090; http://dx.doi.org/10.1126/science.1189801.
27. Jensen ER, Selvakumar R, Shen H, Ahmed R, Wettstein FO, Miller JF. Recombinant Listeria monocytogenes vaccination eliminates papillomavirus-induced tumors and prevents papilloma formation from viral DNA. J Virol 1997; 71:8467-74; PMID:9343203.
28. Yoshimura K, Jain A, Allen HE, Laird LS, Chia CY, Ravi S, et al. Selective targeting of antitumor immune responses with engineered live-attenuated Listeria monocytogenes. Cancer Res 2006; 66:1096-104; PMID:16424046; http://dx.doi.org/10.1158/0008-5472.CAN-05-2307.
29. Pan ZK, 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 1995; 1:471-7; PMID:7585097; http://dx.doi.org/10.1038/nm0595- 471.
30. Craft N, Bruhn KW, Nguyen BD, Prins R, Lin JW, Liau LM, et al. The TLR7 agonist imiquimod enhances the anti-melanoma effects of a recombinant Listeria monocytogenes vaccine. J Immunol 2005; 175:1983-90; PMID:16034143.
31. Maciag PC, Radulovic S, Rothman J. The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a Phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine 2009; 27:3975-83; PMID:19389451; http://dx.doi.org/10.1016/j.vaccine.2009.04.041.
32. Wallecha A, French C, Petit R, Singh R, Amin A, Rothman J. Lm-LLO-Based Immunotherapies and HPV-Associated Disease. J Oncol 2012; 2012:542851; PMID:22481930; http://dx.doi.org/10.1155/2012/542851.
33. Singh R, Wallecha A. Cancer immunotherapy using recombinant Listeria monocytogenes: transition from bench to clinic. Hum Vaccin 2011; 7:497-505; PMID:21422819; http://dx.doi.org/10.4161/hv.7.5.15132.
34. Berche P, Gaillard JL, Geoffroy C, Alouf JE. T cell recognition of listeriolysin O is induced during infection with Listeria monocytogenes. J Immunol 1987; 139:3813-21; PMID:3119720.
35. Beattie IA, Swaminathan B, Ziegler HK. Cloning and characterization of T-cell-reactive protein antigens from Listeria monocytogenes. Infect Immun 1990; 58:2792-803; PMID:2117570.
36. Bouwer HG, Nelson CS, Gibbins BL, Portnoy DA, Hinrichs DJ. Listeriolysin O is a target of the immune response to Listeria monocytogenes. J Exp Med 1992; 175:1467-71; PMID:1588276; http://dx.doi.org/10.1084/jem.175.6.1467.
37. Meyer-Morse N, Robbins JR, Rae CS, Mochegova SN, Swanson MS, Zhao Z, et al. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS One 2010; 5:e8610; PMID:20062534; http://dx.doi.org/10.1371/journal.pone.0008610.
38. Lam GY, Fattouh R, Muise AM, Grinstein S, Higgins DE, Brumell JH. Listeriolysin O suppresses phospholipase C-mediated activation of the microbicidal NADPH oxidase to promote Listeria monocytogenes infection. Cell Host Microbe 2011; 10:627-34; PMID:22177565; http://dx.doi.org/10.1016/j. chom.2011.11.005.
39. Kayal S, Lilienbaum A, Poyart C, Memet S, Israel A, Berche P. Listeriolysin O-dependent activation of endothelial cells during infection with Listeria monocytogenes: activation of NF-kappa B and upregulation of adhesion molecules and chemokines. Mol Microbiol 1999; 31:1709-22; PMID:10209744; http://dx.doi.org/10.1046/j.1365-2958.1999.01305.x.
40. Tang P, Rosenshine I, Cossart P, Finlay BB. Listeriolysin O activates mitogen-activated protein kinase in eucaryotic cells. Infect Immun 1996; 64:2359-61; PMID:8675352.
41. Weiglein I, Goebel W, Troppmair J, Rapp UR, Demuth A, Kuhn M. Listeria monocytogenes infection of HeLa cells results in listeriolysin O-mediated transient activation of the Raf-MEK-MAP kinase pathway. FEMS Microbiol Lett 1997; 148:189-95; PMID:9084147; http://dx.doi.org/10.1111/j.1574-6968.1997. tb10287.x.
42. Dramsi S, Cossart P. Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect Immun 2003; 71:3614-8; PMID:12761148; http://dx.doi.org/10.1128/IAI.71.6. 3614-3618.2003.
43. Ribet D, Hamon M, Gouin E, Nahori MA, Impens F, Neyret-Kahn H, et al. Listeria monocytogenes impairs SUMOylation for efficient infection. Nature 2010; 464:1192-5; PMID:20414307; http://dx.doi.org/10.1038/nature08963.
44. Vadia S, Arnett E, Haghighat AC, Wilson-Kubalek EM, Tweten RK, Seveau S. The pore-forming toxin listeriolysin O mediates a novel entry pathway of L. monocytogenes into human hepatocytes. PLoS Pathog 2011; 7:e1002356; PMID:22072970; http://dx.doi.org/10.1371/journal.ppat.1002356.
45. Pamer EG, Harty JT, Bevan MJ. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes. Nature 1991; 353:852-5; PMID:1719425; http://dx.doi.org/10.1038/353852a0.
46. Safley SA, Cluff CW, Marshall NE, Ziegler HK. Role of listeriolysin-O (LLO) in the T lymphocyte response to infection with Listeria monocytogenes. Identification of T cell epitopes of LLO. J Immunol 1991; 146:3604-16; PMID:1709197.
47. Wipke BT, Jameson SC, Bevan MJ, Pamer EG. Variable binding affinities of listeriolysin O peptides for the H-2Kd class I molecule. Eur J Immunol 1993; 23:2005-10; PMID:8344365; http://dx.doi.org/10.1002/eji.1830230842.
48. Pamer EG. Direct sequence identification and kinetic analysis of an MHC class I-restricted Listeria monocytogenes CTL epitope. J Immunol 1994; 152:686-94; PMID:7506732.
49. Villanueva MS, Sijts AJ, Pamer EG. Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells. J Immunol 1995; 155:5227-33; PMID:7594534.
50. Verma NK, Ziegler HK, Wilson M, Khan M, Safley S, Stocker BA, et al. Delivery of class I and class II MHC-restricted T-cell epitopes of listeriolysin of Listeria monocytogenes by attenuated Salmonella. Vaccine 1995; 13:142-50; PMID:7625107; http://dx.doi.org/10.1016/0264-410X(95)93127-U.
51. Vijh S, Pamer EG. Immunodominant and subdominant CTL responses to Listeria monocytogenes infection. J Immunol 1997; 158:3366-71; PMID:9120295.
52. Busch DH, Pamer EG. MHC class I/peptide stability: implications for immunodominance, in vitro proliferation, and diversity of responding CTL. J Immunol 1998; 160:4441-8; PMID:9574549.
53. Lety MA, Frehel C, Raynaud C, Dupuis M, Charbit A. Exploring the role of the CTL epitope region of listeriolysin O in the pathogenesis of Listeria monocytogenes. Microbiology 2006; 152:1287-96; PMID:16622046; http://dx.doi.org/10.1099/mic.0.28754-0.
54. Rodriguez-Del Rio E, Frande-Cabanes E, Tobes R, Pareja E, Lecea-Cuello MJ, Ruiz-Sáez M, et al. The intact structural form of LLO in endosomes cannot protect against listeriosis. Int J Biochem Mol Biol 2011; 2:207-18; PMID:22003433.
55. Schnupf P, Zhou J, Varshavsky A, Portnoy DA. Listeriolysin O secreted by Listeria monocytogenes into the host cell cytosol is degraded by the N-end rule pathway. Infect Immun 2007; 75:5135-47; PMID:17682039; http://dx.doi.org/10. 1128/IAI.00164-07.
56. Geoffroy C, Gaillard JL, Alouf JE, Berche P. Production of thiol-dependent haemolysins by Listeria monocytogenes and related species. J Gen Microbiol 1989; 135:481-7; PMID:2516113.
57. Tweten RK, Harris RW, Sims PJ. Isolation of a tryptic fragment from Clostridium perfringens thetatoxin that contains sites for membrane binding and self-aggregation. J Biol Chem 1991; 266:12449-54; PMID:2061320.
58. Harris RW, Sims PJ, Tweten RK. Evidence that Clostridium perfringens theta-toxin induces colloidosmotic lysis of erythrocytes. Infect Immun 1991; 59:2499-501; PMID:2050414.
59. Mitchell TJ, Andrew PW. Biological properties of pneumolysin. Microb Drug Resist 1997; 3:19-26; PMID:9109093; http://dx.doi.org/10.1089/mdr.1997.3.19.
60. Tweten RK. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 2005; 73:6199-209; PMID:16177291; http://dx.doi.org/10.1128/IAI.73.10.6199-6209.2005.
61. Mainou-Fowler T, MacGowan AP, Postlethwaite R. Virulence of Listeria spp.: course of infection in resistant and susceptible mice. J Med Microbiol 1988; 27:131-40; PMID:3139882; http://dx.doi.org/10.1099/00222615-27-2-131.
62. Shepard LA, Shatursky O, Johnson AE, Tweten RK. The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. Biochemistry 2000; 39:10284-93; PMID:10956018; http://dx.doi.org/10.1021/ bi000436r.
63. Hotze EM, Heuck AP, Czajkowsky DM, Shao Z, Johnson AE, Tweten RK. Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J Biol Chem 2002; 277:11597-605; PMID:11799121; http://dx.doi.org/10.1074/jbc.M111039200.
64. Portnoy DA, Tweten RK, Kehoe M, Bielecki J. Capacity of listeriolysin O, streptolysin O, and perfringolysin O to mediate growth of Bacillus subtilis within mammalian cells. Infect Immun 1992; 60:2710-7; PMID:1612739.
65. Glomski IJ, Gedde MM, Tsang AW, Swanson JA, Portnoy DA. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J Cell Biol 2002; 156:1029-38; PMID:11901168; http://dx.doi.org/10.1083/jcb.200201081.
66. Jones S, Portnoy DA. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect Immun 1994; 62:5608-13; PMID:7960143.
67. Rossjohn J, Feil SC, McKinstry WJ, Tweten RK, Parker MW. Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 1997; 89:685-92; PMID:9182756; http://dx.doi.org/10.1016/S0092-8674(00) 80251-2.
68. Polekhina G, Giddings KS, Tweten RK, Parker MW. Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc Natl Acad Sci U S A 2005; 102:600-5; PMID:15637162; http://dx.doi.org/10.1073/pnas.0403229101.
69. Benkert P, Biasini M, Schwede T. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 2011; 27:343-50; PMID:21134891; http://dx.doi.org/10.1093/bioinformatics/btq662.
70. Ramachandran R, Tweten RK, Johnson AE. The domains of a cholesterol-dependent cytolysin undergo a major FRET-detected rearrangement during pore formation. Proc Natl Acad Sci U S A 2005; 102:7139-44; PMID:15878993; http://dx.doi.org/10.1073/pnas.0500556102.
71. Soltani CE, Hotze EM, Johnson AE, Tweten RK. Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions. Proc Natl Acad Sci U S A 2007; 104:20226-31; PMID:18077338; http://dx.doi.org/10.1073/pnas.0708104105.
72. Shepard LA, Heuck AP, Hamman BD, Rossjohn J, Parker MW, Ryan KR, et al. Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an α-helical to beta-sheet transition identified by fluorescence spectroscopy. Biochemistry 1998; 37:14563-74; PMID:9772185; http://dx.doi.org/10.1021/bi981452f.
73. Ramachandran R, Tweten RK, Johnson AE. Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit beta-strand alignment. Nat Struct Mol Biol 2004; 11:697-705; PMID:15235590; http://dx.doi.org/10.1038/nsmb793.
74. Idone V, Tam C, Andrews NW. Two-way traffic on the road to plasma membrane repair. Trends Cell Biol 2008; 18:552-9; PMID:18848451; http://dx.doi.org/10.1016/j.tcb.2008.09.001.
75. Los FC, Kao CY, Smitham J, McDonald KL, Ha C, Peixoto CA, et al. RAB-5- and RAB-11-dependent vesicle-trafficking pathways are required for plasma membrane repair after attack by bacterial pore-forming toxin. Cell Host Microbe 2011; 9:147-57; PMID:21320697; http://dx.doi.org/10.1016/j.chom.2011.01.005.
76. Decatur AL, Portnoy DA. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 2000; 290:992-5; PMID:11062133; http://dx.doi.org/10.1126/science.290.5493.992.
77. Lety MA, Frehel C, Dubail I, Beretti JL, Kayal S, Berche P, et al. Identification of a PEST-like motif in listeriolysin O required for phagosomal escape and for virulence in Listeria monocytogenes. Mol Microbiol 2001; 39:1124-39; PMID:11251831; http://dx.doi.org/10.1111/j.1365-2958.2001.02281.x.
78. Lety MA, Frehel C, Berche P, Charbit A. Critical role of the N-terminal residues of listeriolysin O in phagosomal escape and virulence of Listeria monocytogenes. Mol Microbiol 2002; 46:367-79; PMID:12406215; http://dx.doi.org/10.1046/j.1365-2958.2002.03176.x.
79. Schnupf P, Portnoy DA, Decatur AL. Phosphorylation, ubiquitination and degradation of listeriolysin O in mammalian cells: role of the PEST-like sequence. Cell Microbiol 2006; 8:353-64; PMID:16441444; http://dx.doi.org/10. 1111/j.1462-5822.2005.00631.x.
80. Rogers S, Wells R, Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 1986; 234:364-8; PMID:2876518; http://dx.doi.org/10.1126/science.2876518.
81. Rechsteiner M, Rogers SW. PEST sequences and regulation by proteolysis. Trends Biochem Sci 1996; 21:267-71; PMID:8755249.
82. Meraro D, Hashmueli S, Koren B, Azriel A, Oumard A, Kirchhoff S, et al. Protein-protein and DNA-protein interactions affect the activity of lymphoid-specific IFN regulatory factors. J Immunol 1999; 163:6468-78; PMID:10586038.
83. Berche P, Gaillard JL, Geoffroy C, Alouf JE. T cell recognition of listeriolysin O is induced during infection with Listeria monocytogenes. J Immunol 1987; 139:3813-21; PMID:3119720.
84. Beattie IA, Swaminathan B, Ziegler HK. Cloning and characterization of T-cell-reactive protein antigens from Listeria monocytogenes. Infect Immun 1990; 58:2792-803; PMID:2117570.
85. Lety MA, Frehel C, Beretti JL, Berche P, Charbit A. Modification of the signal sequence cleavage site of listeriolysin O does not affect protein secretion but impairs the virulence of Listeria monocytogenes. Microbiology 2003; 149:1249-55; PMID:12724386; http://dx.doi.org/10.1099/mic.0.26072-0.
86. Pamer EG, Sijts AJ, Villanueva MS, Busch DH, Vijh S. MHC class I antigen processing of Listeria monocytogenes proteins: implications for dominant and subdominant CTL responses. Immunol Rev 1997; 158:129-36; PMID:9314081; http://dx.doi.org/10.1111/j.1600-065X.1997.tb00999.x.
87. Vijh S, Pilip IM, Pamer EG. Noncompetitive expansion of cytotoxic T lymphocytes specific for different antigens during bacterial infection. Infect Immun 1999; 67:1303-9; PMID:10024575.
88. Finelli A, Kerksiek KM, Allen SE, Marshall N, Mercado R, Pilip I, et al. MHC class I restricted T cell responses to Listeria monocytogenes, an intracellular bacterial pathogen. Immunol Res 1999; 19:211-23; PMID:10493175; http://dx.doi.org/10.1007/BF02786489.
89. Carrero JA, Vivanco-Cid H, Unanue ER. Listeriolysin o is strongly immunogenic independently of its cytotoxic activity. PLoS One 2012; 7:e32310; PMID:22403645; http://dx.doi.org/10.1371/journal.pone.0032310.
90. Rose F, Zeller SA, Chakraborty T, Domann E, Machleidt T, Kronke M, et al. Human endothelial cell activation and mediator release in response to Listeria monocytogenes virulence factors. Infect Immun 2001; 69:897-905; PMID:11159983; http://dx.doi.org/10.1128/IAI.69.2.897-905.2001.
91. Kayal S, Lilienbaum A, Join-Lambert O, Li X, Israël A, Berche P. Listeriolysin O secreted by Listeria monocytogenes induces NF-kappaB signalling by activating the IkappaB kinase complex. Mol Microbiol 2002; 44:1407-19; PMID:12028384; http://dx.doi.org/10.1046/j.1365-2958.2002.02973.x.
92. Yoshikawa H, Kawamura I, Fujita M, Tsukada H, Arakawa M, Mitsuyama M. Membrane damage and interleukin-1 production in murine macrophages exposed to listeriolysin O. Infect Immun 1993; 61:1334-9; PMID:8454336.
93. Nishibori T, Xiong H, Kawamura I, Arakawa M, Mitsuyama M. Induction of cytokine gene expression by listeriolysin O and roles of macrophages and NK cells. Infect Immun 1996; 64:3188-95; PMID:8757852.
94. Nomura T, Kawamura I, Tsuchiya K, Kohda C, Baba H, Ito Y, et al. Essential role of interleukin-12 (IL-12) and IL-18 for gamma interferon production induced by listeriolysin O in mouse spleen cells. Infect Immun 2002; 70:1049-55; PMID:11854182; http://dx.doi.org/10.1128/IAI.70.3.1049-1055.2002.
95. Kohda C, Kawamura I, Baba H, Nomura T, Ito Y, Kimoto T, et al. Dissociated linkage of cytokine-inducing activity and cytotoxicity to different domains of listeriolysin O from Listeria monocytogenes. Infect Immun 2002; 70:1334-41; PMID:11854218; http://dx.doi.org/10.1128/IAI.70.3.1334-1341.2002.
96. Kimoto T, Kawamura I, Kohda C, Nomura T, Tsuchiya K, Ito Y, et al. Differences in gamma interferon production induced by listeriolysin O and ivanolysin O result in different levels of protective immunity in mice infected with Listeria monocytogenes and Listeria ivanovii. Infect Immun 2003; 71:2447-54; PMID:12704115; http://dx.doi.org/10.1128/IAI.71.5.2447-2454.2003.
97. Wallecha A, Wood L, Pan ZK, Maciag PC, Shahabi V, Paterson Y. Listeria monocytogenes-Derived Listeriolysin O Has Pathogen-Associated Molecular Pattern-Like Properties Independent of Its Hemolytic Ability. Clin Vaccine Immunol 2013; 20:77-84; PMID:23136118; http://dx.doi.org/10.1128/CVI.00488-12.
98. Lee KD, Oh YK, Portnoy DA, Swanson JA. Delivery of macromolecules into cytosol using liposomes containing hemolysin from Listeria monocytogenes. J Biol Chem 1996; 271:7249-52; PMID:8631734; http://dx.doi.org/10.1074/jbc.271.13. 7249.
99. Schrama D, Reisfeld RA, Becker JC. Antibody targeted drugs as cancer therapeutics. Nat Rev Drug Discov 2006; 5:147-59; PMID:16424916; http://dx.doi.org/10.1038/nrd1957.
100. Carter P. Improving the efficacy of antibody-based cancer therapies. Nat Rev Cancer 2001; 1:118-29; PMID:11905803; http://dx.doi.org/10.1038/35101072.
101. Pastan I, Kreitman RJ. Immunotoxins for targeted cancer therapy. Adv Drug Deliv Rev 1998; 31:53-88; PMID:10837618; http://dx.doi.org/10.1016/S0169- 409X(97)00094-X.
102. Kerr DE, Wu GY, Wu CH, Senter PD. Listeriolysin O potentiates immunotoxin and bleomycin cytotoxicity. Bioconjug Chem 1997; 8:781-4; PMID:9404648; http://dx.doi.org/10.1021/bc970124+.
103. Bergelt S, Frost S, Lilie H. Listeriolysin O as cytotoxic component of an immunotoxin. Protein Sci 2009; 18:1210-20; PMID:19472336; http://dx.doi.org/10. 1002/pro.130.
104. Slingerland M, Guchelaar HJ, Gelderblom H. Liposomal drug formulations in cancer therapy: 15 years along the road. Drug Discov Today 2012; 17:160-6; PMID:21983329; http://dx.doi.org/10.1016/j.drudis.2011.09.015.
105. Tailor TD, Hanna G, Yarmolenko PS, Dreher MR, Betof AS, Nixon AB, et al. Effect of pazopanib on tumor microenvironment and liposome delivery. Mol Cancer Ther 2010; 9:1798-808; PMID:20515941; http://dx.doi.org/10.1158/1535-7163.MCT- 09-0856.
106. Haley B, Frenkel E. Nanoparticles for drug delivery in cancer treatment. Urol Oncol 2008; 26:57-64; PMID:18190833; http://dx.doi.org/10.1016/j.urolonc. 2007.03.015.
107. Di Legge A, Trivellizzi IN, Moruzzi MC, Pesce A, Scambia G, Lorusso D. Phase 2 trial of nonpegylated doxorubicin (Myocet) as second-line treatment in advanced or recurrent endometrial cancer. Int J Gynecol Cancer 2011; 21:1446-51; PMID:22027749; http://dx.doi.org/10.1097/IGC.0b013e31822d754e.
108. Mir LM, Morsli N, Garbay JR, Billard V, Robert C, Marty M. Electrochemotherapy: a new treatment of solid tumors. J Exp Clin Cancer Res 2003; 22(Suppl):145-8; PMID:16767921.
109. Safaei R, Katano K, Larson BJ, Samimi G, Holzer AK, Naerdemann W, et al. Intracellular localization and trafficking of fluorescein-labeled cisplatin in human ovarian carcinoma cells. Clin Cancer Res 2005; 11:756-67; PMID:15701866.
110. Kullberg M, Mann K, Anchordoquy TJ. Targeting Her-2+ Breast Cancer Cells with Bleomycin Immunoliposomes Linked to LLO. Mol Pharm 2012; 9:2000-8; PMID:22621404; http://dx.doi.org/10.1021/mp300049n.
111. Lee RJ, Huang L. Folate-targeted, anionic liposome-entrapped polylysine-condensed DNA for tumor cell-specific gene transfer. J Biol Chem 1996; 271:8481-7; PMID:8626549; http://dx.doi.org/10.1074/ jbc.271.14.8481.
112. Shi G, Guo W, Stephenson SM, Lee RJ. Efficient intracellular drug and gene delivery using folate receptor-targeted pH-sensitive liposomes composed of cationic/anionic lipid combinations. J Control Release 2002; 80:309-19; PMID:11943407; http://dx.doi.org/10.1016/S0168-3659(02)00017-2.
113. Sun X, Provoda C, Lee KD. Enhanced in vivo gene expression mediated by listeriolysin O incorporated anionic LPDII: Its utility in cytotoxic T lymphocyte-inducing DNA vaccine. J Control Release 2010; 148:219-25; PMID:20620181; http://dx.doi.org/10.1016/j.jconrel.2010.06.017.
114. Rescigno M, Winzler C, Delia D, Mutini C, Lutz M, Ricciardi-Castagnoli P. Dendritic cell maturation is required for initiation of the immune response. J Leukoc Biol 1997; 61:415-21; PMID:9103227.
115. Rescigno M, Citterio S, Thèry C, Rittig M, Medaglini D, Pozzi G, et al. Bacteria-induced neo-biosynthesis, stabilization, and surface expression of functional class I molecules in mouse dendritic cells. Proc Natl Acad Sci U S A 1998; 95:5229-34; PMID:9560258; http://dx.doi.org/10.1073/pnas.95.9.5229.
116. Radford KJ, Higgins DE, Pasquini S, Cheadle EJ, Carta L, Jackson AM, et al. A recombinant E. coli vaccine to promote MHC class I-dependent antigen presentation: application to cancer immunotherapy. Gene Ther 2002; 9:1455-63; PMID:12378408; http://dx.doi.org/10.1038/sj.gt.3301812.
117. + T cells. Int J Cancer 2003; 105:811-9; PMID:12767067; http://dx.doi.org/10.1002/ijc.11149.
118. Dai MS, Nitcheu-Tefit J, Alcock S, Ramirez-Jimenez F, Chao TY, Baril P, et al. Development of an Escherichia coli expressing listeriolysin-O vaccine against Wilms tumor gene 1-expressing tumors. J Immunother 2009; 32:845-55; PMID:19752749; http://dx.doi.org/10.1097/CJI.0b013e3181aee259.
119. Woo EY, Chu CS, Goletz TJ, Schlienger K, Yeh H, Coukos G, et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res 2001; 61:4766-72; PMID:11406550.
120. Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G, et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 2002; 169:2756-61; PMID:12193750.
121. Sasada T, Kimura M, Yoshida Y, Kanai M, Takabayashi A. CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer 2003; 98:1089-99; PMID:12942579; http://dx.doi.org/10.1002/cncr.11618.
122. Dannull J, Su Z, Rizzieri D, Yang BK, Coleman D, Yancey D, et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 2005; 115:3623-33; PMID:16308572; http://dx.doi.org/10.1172/JCI25947.
123. high regulatory T cell function in vivo. J Immunol 2007; 179:1532-41; PMID:17641019.
124. Peng X, Treml J, Paterson Y. Adjuvant properties of listeriolysin O protein in a DNA vaccination strategy. Cancer Immunol Immunother 2007; 56:797-806; PMID:17102978; http://dx.doi.org/10.1007/s00262-006-0240-9.
125. Dégano P, Schneider J, Hannan CM, Gilbert SC, Hill AV. Gene gun intradermal DNA immunization followed by boosting with modified vaccinia virus Ankara: enhanced CD8+ T cell immunogenicity and protective efficacy in the influenza and malaria models. Vaccine 1999; 18:623-32; PMID:10547421; http://dx.doi.org/10.1016/S0264-410X(99)00278-9.
126. Dai MS, Vassaux G, Xu M, You RI, Hsieh YF, Ouisse LH, et al. Early Treg suppression by a listeriolysin-O-expressing E. coli vaccine in heterologous prime-boost vaccination against cancer. Vaccine 2012; 30:6903-11; PMID:22982404; http://dx.doi.org/10.1016/j.vaccine.2012.09.001.
127. Peng X, Hussain SF, Paterson Y. The ability of two Listeria monocytogenes vaccines targeting human papillomavirus-16 E7 to induce an antitumor response correlates with myeloid dendritic cell function. J Immunol 2004; 172:6030-8; PMID:15128786.
128. + T cells capable of eradicating a solid tumor in a transgenic mouse model of cancer. Cancer Immun 2007; 7:2; PMID:17279610.
129. Sewell DA, Pan ZK, Paterson Y. Listeria-based HPV-16 E7 vaccines limit autochthonous tumor growth in a transgenic mouse model for HPV-16 transformed tumors. Vaccine 2008; 26:5315-20; PMID:18680778; http://dx.doi.org/10.1016/j. vaccine.2008.07.036.
130. Rothman J, Wallecha A, Maciag PC, Rivera S, Shahabi V, Paterson Y. The use of a living Listeria monocytogenes as an active immunotherapy for the treatment of cancer. In: Fialho AM, eds. Emerging Cancer Therapy: Microbial Approaches and Biotechnological Tools. New York: John Wiley & Sons publishing, 2010:13-48.
131. + T cells reactivation against intracellular bacteria in the mouse. PLoS One 2010; 5:e11524; PMID:20634957; http://dx.doi.org/10.1371/journal.pone.0011524.
132. Seavey MM, Paterson Y. Anti-Angiogenesis immunotherapy induces epitope spreading to Her-2/neu resulting in breast tumor immunoediting. Breast Cancer (London) 2009; 1:19-30; PMID:21197144.
133. Wood LM, Pan ZK, Guirnalda P, Tsai P, Seavey M, Paterson Y. Targeting tumor vasculature with novel Listeria-based vaccines directed against CD105. Cancer Immunol Immunother 2011; 60:931-42; PMID:21431419; http://dx.doi.org/10. 1007/s00262-011-1002-x.
134. Maciag PC, Seavey MM, Pan ZK, Ferrone S, Paterson Y. Cancer immunotherapy targeting the high molecular weight melanoma-associated antigen protein results in a broad antitumor response and reduction of pericytes in the tumor vasculature. Cancer Res 2008; 68:8066-75; PMID:18829565; http://dx.doi.org/10. 1158/0008-5472.CAN-08-0287.
135. Neeson P, Pan ZK, Paterson Y. Listeriolysin O is an improved protein carrier for lymphoma immunoglobulin idiotype and provides systemic protection against 38C13 lymphoma. Cancer Immunol Immunother 2008; 57:493-505; PMID:17876582; http://dx.doi.org/10.1007/s00262-007-0388-y.
136. Singh R, Dominiecki ME, Jaffee EM, Paterson Y. 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 2005; 175:3663-73; PMID:16148111.
137. Guirnalda P, Wood L, Paterson Y. Listeria monocytogenes and its products as agents for cancer immunotherapy. Adv Immunol 2012; 113:81-118; PMID:22244580; http://dx.doi.org/10.1016/B978-0-12-394590-7.00004-X.