Harnessing Listeria monocytogenes to target tumors

Cancer Biology and Therapy

Volumn 9, Issue 4, 2010, Pages 257-265

  Gravekamp, Claudia ^a   Paterson, Yvonne ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Angiogenesis; Cancer vaccine; Immune suppression; Immunotherapy; Listeria monocytogenes; Lysteriolysin O; Metastases; NADPH oxidase; ROS

Indexed keywords

CANCER VACCINE; E7 ACTA FUSION PROTEIN VACCINE; E7 LISTERIOLYSIN O FUSION PROTEIN VACCINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 2 LISTERIOLYSIN O FUSION PROTEIN VACCINE; HIGH MOLECULAR WEIGHT MELANOMA ASSOCIATED ANTIGEN LISTERIOLYSIN O FUSION PROTEIN VACCINE; HYBRID PROTEIN; LISTERIA MONOCYTOGENES VACCINE; LISTERIOLYSIN O; LISTERIOLYSIN O MELANOMA ANTIGEN MAGE B[311-660] FUSION PROTEIN VACCINE; MELANOMA ANTIGEN; NUCLEOPROTEIN LISTERIOLYSIN O FUSION PROTEIN VACCINE; PROSTATE SPECIFIC ANTIGEN; PROTEIN E7; REACTIVE OXYGEN METABOLITE; TUMOR ANTIGEN; TYROSINASE RELATED PROTEIN 2; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANTIGEN PRESENTING CELL; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BREAST TUMOR; CANCER IMMUNOTHERAPY; CANCER MODEL; CLINICAL TRIAL; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; FLU LIKE SYNDROME; HUMAN; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MACROPHAGE; MELANOMA; METASTASIS; MONOCYTE; NEOPLASM; NONHUMAN; PROSTATE CANCER; REVIEW; SIDE EFFECT; SINGLE DRUG DOSE; TUMOR; TUMOR CELL DESTRUCTION; UTERINE CERVIX CARCINOMA; ANIMAL; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; METABOLISM; NEOPLASMS; PATHOLOGY; TUMOR MICROENVIRONMENT; VASCULARIZATION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, NEOPLASM; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNITY, INNATE; LISTERIA MONOCYTOGENES; NEOPLASMS; REACTIVE OXYGEN SPECIES; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT;

EID: 77953607030     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.9.4.11216     Document Type: Review

References (84)

1. Paterson Y, Maciag P. Listeria-based vaccines for cancer treatment. Curr Opin Mol Ther 2005; 7:454-60.
2. Guzman CA, Rohde M, Chakraborty T, Domann E, Hudel M, Wehland J, et al. Interaction of Listeria monocytogenes with mouse dendritic cells. Infect Immun 1995; 63:3665-73.
3. Kolb-Mauer A, Gentschev I, Fries HW, Fiedler F, Brocker EB, Kampgen E, et al. Listeria monocytogenes-infected human dendritic cells uptake and host cell response. Infect Immun 1998; 68:3680-8.
4. Vazquez-Boland JA, Kuhn M, Berche P, Chakarborty T, Dominguez-Bernal G, Goebel W, et al. Listeria pathogenesis and molecular virulence. Clin Microbiol Rev 2001; 14:584-630.
5. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of Listeria monocytogenes into epithelial cells. Cell 1996; 84:923-32.
6. Portnoy DA, Jacks PS, Hinrichs DJ. Role of hemolysin for intracellular growth of Listeria monocytogenes. J Exp Med 1988; 167:1459-71.
7. Kuhn M, Kathariou S, Goebel W. Hemolysin supports survival but not entry of the intracellular bacterium Listeria monocytogenes. Infect Immun 1988; 56:79-82.
8. Seveau S, Pizarro-Cerda J, Cossart P. Molecular mechanisms exploited by Listeria monocytogenes during host cell invasion. Microbes Infect 2007; 9:1167-75.
9. Dramsi S, Biswas I, Maguin E, Braun L, Mastroeni P, Cossart P. Entry of Listeria monocytogenes into hepatocytes requires the expression of InlB, a surface protein of the internalin multigene family. Mol Microbiol 1995; 16:251-61.
10. Gregory SH, Sagnimeni AJ, Wing EJ. Expression of the InlB operon by Listeria monocytogenes is not required for entry into hepatic cells in vivo. Infect Immun 1996; 64:3983-9.
11. Wood S, Maroushek N, Czuprinski. Multiplication of Listeria monocytogenes in murine hepatocyte cell line. Infect Immun 1993; 61:3068-72.
12. Drevets DA, Sawyer RT, Potter TA, Campbell PA. Listeria monocytogenes infects human endothelial cells by two distinct mechanisms. Infect Immun 1995; 63:4268-76.
13. Greiffenberg L, Goebel W, Kim KS, Daniels J, Kuhn M. Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: an electron microscopic study. Infect Immun 2000; 68:3275-9.
14. Parida SK, Domann E, Rohde M, Muller S, Darji A, Hain T, et al. Internalin B is essential for adhesion and mediates invasion of Listeria monocytogenes into human endothelial cells. Mol Microbiol 1998; 28:81-93.
15. Alvarez-Dominguez C, Carrasco-Marin E, Leyva- Cobian F. Role of complement component C1q in phagocytosis of Listeria monocytogenes by murine macrophage- like cell lines. Infect Immun 1993; 61:3664-72.
16. Croize J, Avieux J, Berche P, Colomb MG. Activation of the human complement alternative pathway by Listeria monocytogenes: evidence for direct binding and proteolysis of the C3 component on bacteria. Infect Immun 1993; 61:5134-9.
17. Drevets DA, Campbell PA. Roles of complement and complement receptor type 3 in phagocytosis of Listeria monocytogenes by inflammatory mouse peritoneal macrophages. Infect Immun 1991; 59:2645-52.
18. Drevets DA, Leenen PJM, Campbell PA. Complement receptor type 3 (CD11b/CD18) involvement is essential for killing of Listeria monocytogenes by mouse macrophages. J Immunol 1995; 151:5431-9.
19. Dunne DW, Resnick D, Greenberg J, Krieger M, Joiner KA. The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci USA 1994; 91:1863-7. (Pubitemid 24080306)
20. Greenberg JW, Fischer W, Joiner KA. Influence of lipoteichoic acid structure on recognition by the macrophage scavenger receptor. Infect Immun 1996; 64:3318-25. (Pubitemid 26256182)
21. Shen Y, Naujokas M, Park M, Ireton K. InlB-dependent internalization of Listeria is mediated by the met receptor tyrosine kinase. Cell 2000; 103:501-10.
22. Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature 2004; 432:332-7.
23. Alvarez-Dominguez C, Vazquez-Boland JA, Carrasco- Marin A, Lopez-Mato E, Leyva-Cobian F. Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun 1997; 65:78-88.
24. Gilot P, Andre P, Content J. Listeria monocytogenes possesses adhesions for fibronectin. Infect Immun 1999; 67:6698-701.
25. Barbareschi M, Maisonneuve P, Aldovini D, Cangi MG, Pecciarini L, Mauri FA, et al. High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 2003; 98:474-83.
26. Ghoussoub RA, Dillon DA, D'Aquilla T, Rimm EB, Fearon ER, Rimm DL. Expression of c-met is a strong independent prognostic factor in breast carcinoma. Cancer 1998; 15:1513-20.
27. Ohnishi T, Hiraga, Izumotot S, Matsumura H, Kanemura Y, Arita N, et al. Role of fibronectin-stimulated tumor cell migration in glioma invasion in vivo: clinical significance and fibronectin receptor expressed in human glioma tissues. Clin Exp Metastasis 1998; 16:729-41. (Pubitemid 29170483)
28. Gagglioli C, Robert G, Bertolotto C, Bailet O, Abbe P, Spadafora A, et al. Tumor-derived fibronectin is involved in melanoma cell invasion and regulated by V600E B-Raf signaling pathway. J Invest Derm 2007; 127:400-10. (Pubitemid 46106920)
29. Braun L, Dramsi S, Dehoux P, Bierne H, Lindahl G, Cossart P. InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol Microb 1997; 25:285-94.
30. McLaughlan AM, Foster SJ. Molecular characterization of an autolytic amidase of Listeria monocytogenes EGD. Microbiology 1998; 144:1359-67.
31. Miller R, Britigan BE. Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 1997; 10:1-18.
32. Santiago NI, Zipf A, Bhunia AK. Influence of temperature and growth phase on expression of a 104-kilodalton Listeria adhesion protein in Listeria monocytogenes. Appl Environ Microbiol 1999; 65:2765-9.
33. Ofek I, Sharon N. Lectinophagocytosis: a molecular mechanism of recognition between cell surface sugars and lectins in the phagocytosis of bacteria. Infect Immun 1988; 56:539-47.
34. Cottin J, Loiseau O, Robert R, Mahaza C, Carbonelle B, Senet JM. Surface Listeria monocytogenes carbohydrate- binding components revealed by agglutination with neoglycoproteins. FEMS Microbiol Lett 1990; 68:301-6.
35. Cowart RE, Lashmet J, McIntosh ME, Adams TJ. Adherence of virulent strains of Listeria monocytogenes to the surface of hepatocarcinoma cell line via lectin-substrate interaction. Arch Microbiol 1990; 153:282-6.
36. Dussurget O, Pizarro-Cerda J, Cossart P. Molecular determinants of Listeria monocytogenes virulence. Ann Rev 2004; 58:587-610.
37. Gedde MM, Higgins DE, Tilney LG, Portnoy DA. Role of Listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 2000; 68:999-1003.
38. Janda J, Schöneberger P, Skoberne M, Messerle M, Rüssmann H, Geginat G. Cross-presentation of Listeria-derived CD8 T cell epitopes requires unstable bacterial translation products. J Immunol 2004; 173:5644-51. (Pubitemid 39392152)
39. Wallecha A, Carroll KD, Maciag PC, Rivera S, Shahabi V, Paterson Y. Multiple effector mechanisms induced by recombinant Listeria monocytogenes anti-cancer immunotherapeutics. Adv Appl Microbiol 2009; 66:1-27.
40. Pamer EG. Immune responses to Listeria monocytogenes. Nature 2004; 4:812-23.
41. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003; 19:59-70.
42. +-T-cell potency during bacterial infection. Infect Immun 2006; 74:6387-97.
43. von Koenig CH, Finger H, Hof H. Failure of killed Listeria monocytogenes vaccine to produce protective immunity. Nature 1982; 297:233-4.
44. Lauvau G, Vijh S, Kong P, Horng T, Kerksiek K, Serbina N, et al. Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science 2001; 294:1735-9. (Pubitemid 33104848)
45. + T cells provide immunity to Listeria monocytogenes by a mechanism that is independent of CD95 and IFNγ but required TNFα. J Immunol 1998; 160:898-905.
46. Pan ZK, Okonomidis G, Lazenby A, Pardoll D, Paterson Y. A recombinant Listeria monocytogenes vaccine expressing a model tumor antigen protects mice against lethal tumor challenge and causes regression of established tumors. Nature Med 1995; 1:471-7.
47. Pan ZK, Weiskkirch LM, Paterson Y. Regression of established B16F10 melanoma with recombinant Listeria monocytogenes vaccine. Cancer Res 1999; 59:5264-9.
48. Gunn GR, Zubair A, Peters C, Pan ZK, Wu TC, Paterson Y. Two Listeria monocytogenes vaccine vectors that express different molecular forms of human papillomavirus- 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 2001; 167:6471-9.
49. Sewell DA, Shahabi V, Gun GR III, Pan ZK, Dominiecki ME, Paterson Y. Recombinant Listeria vaccines containing PEST sequences are potent adjuvants for the tumor-associated antigen human papillomavirus- 16 E7. Cancer Res 2004; 64:8821-5. (Pubitemid 39665484)
50. + T cells capable of killing a solid tumor in a transgenic mouse model of cancer. Cancer Immunity 2007; 7:2.
51. Sewell DA, Pan Z-K, Paterson Y. Listeria-based HPV- 16 E7 vaccines limit autochthonous tumor growth in a transgenic mouse model for HPV-16 transformed tumors. Vaccine 2008; 26:5322-7.
52. Bruhn KW, Craft N, Nguyen BD, Yip J, Miller JF. Characterization of anti-self CD8 T-cell responses stimulated by recombinant Listeria monocytogenes expressing the melanoma antigen TRP-2. Vaccine 2005; 23:4263-72.
53. Kim SH, Castro F, Gonzalez D, Maciag PC, Paterson Y, Gravekamp C. Mage-b vaccine delivered by recombinant Listeria monocytogenes is highly effective against breast cancer metastases. Br J Cancer 2008; 99:741-9.
54. Singh R, Domineicki ME, Jaffee EM, Paterson Y. Fusion of 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.
55. Singh R, Paterson Y. In the FVB/N HER-2/neu Transgenic mouse both peripheral and central tolerance limit the immune response targeting HER-2/ neu induced by Listeria monocytogenes-based vaccines. Cancer Immunol Immunother 2007; 56:927-38.
56. Singh R, Paterson Y. Immunoediting sculpts tumor epitopes during immunotherapy. Cancer Res 2007; 67:1887-92. (Pubitemid 46424202)
57. + breast tumors. Clin Cancer Res 2009; 15:924-32.
58. Wallecha A, Maciag PC, Rivera S, Paterson Y, Shahabi V. Construction and characterization of an attenuated Listeria monocytogenes strain for clinical use in cancer immunotherapy. Clin and Vaccine Immunol 2009; 16:96-103.
59. Folkman J. Tumor angiogenesis: therapeutic implications. NJEM 1971; 285:1182-6.
60. Betsholtz C, Lindblom P, Gerhardt H. The role of pericytes in vascular morphogenesis. EXS 2005; 94:115-25.
61. O'Keeffe MB, Devlin AH, Burns AJ, Gardiner TA, Logan ID, Hirst DG, et al. Investigation of pericytes, hypoxia and vascularity in bladder tumors: association with clinical outcomes. Oncol Res 2008; 17:93-101.
62. Folkman J. Tumor angiogenesis and tissue factor. Nat Med 1996; 2:167-8.
63. Shibuya M. Vascular endothelial growth factor (VEGF)- Receptor2: its biological functions, major signaling pathway and specific ligand VEGF-E. Endothelium 2006; 13:63-9. (Pubitemid 44173108)
64. Niethammer AG, Xiang R, Becker JC, Wodrich H, Pertl U, Karsten G, et al. A DNA vaccine against VEGF receptor 2 prevents effective angiogenesis and inhibits tumor growth. Nat Med 2002; 8:1369-75.
65. Luo Y, Markowitz D, Xiang R, Zhou H, Reisfeld RA. FLK-1-based minigene vaccines induce T cell-mediated suppression of angiogenesis and tumor protective immunity in syngeneic BALB/c mice. Vaccine 2007; 25:1409-15.
66. + breast tumors in a mouse model. J Immunol 2009; 182:5537-46.
67. Schlingemann RO, Rietveld FJ, de Waal RM, Ferrone S, Ruiter DJ. Expression of the high molecular weight melanoma-associated antigen by pericytes during angiogenesis in tumors and in healing wounds. The Am J Path 1990; 136:1393-405. (Pubitemid 20210338)
68. Campoli MR, Chang CC, Kageshita T, Wang X, McCarthy JB, Ferrone S. Human high molecular weight-melanoma-associated antigen (HMW-MAA): a melanoma cell surface chondroitin sulfate proteoglycan (MSCP) with biological and clinical significance. Crit Rev Immunol 2004; 24:267-96. (Pubitemid 40052428)
69. 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.
70. Kim SH, Castro F, Paterson Y, Gravekamp C. High efficacy of a Listeria-based vaccine against metastatic breast cancer reveals a dual mode of action. Cancer Res 2009; 69:5860-6.
71. Kowalski PJ, Rubin MA, Kleer R. E-cadherin expression in primary carcinomas of the breast and its distant metastases. Cancer Res 2003; 5:217-22.
72. Velge P, Bottreau E, Kaeffer B, Pardon P. Cell immortalization enhances Listeria monocytogenes invasion. Med Microbiol Immunol 1994; 183:145-58.
73. Yu YA, Shabahang S, Timiryasova TM, Zhang O, Beltz R, Gentschev I, et al. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nature Biotech 2004; 22:313-20. (Pubitemid 38295764)
74. Stritzker J, Pilgrim S, Szalay AA, Goebel W. Prodrug converting enzyme gene delivery by L. monocytogenes. BMC Cancer 2008; 8:94.
75. Lancellotti M, Brocchi M, da Silvedeira WD. Bacteria-induced apoptosis: an approach to bacterial pathogenesis. Braz J Morphol Sci 2006; 23:75-86.
76. North BM. Murine Listeriosis as a model of antimicrobial defense. Immunol Rev 1997; 158:27-36.
77. Rogers HW, Unanue ER. Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes in mice. Infect Immun 1993; 61:5090-6.
78. Unanue ER. Inter-relationships among macrophages, natural killer cells and neutrophils in early stages of Listeria resistance. Curr Opin Immunol 1997; 1:25-43.
79. Wadsworth S, Goldfine H. Mobilization of proteinase C in macrophages induced by Listeria monocytogenes affects its internalization and escape from the phagosome. Infect Immun 2002; 70:4650-60.
80. Gaillard JL, Berche PP, Sansonetti P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun 1986; 52:50-5.
81. 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. (Pubitemid 43356056)
82. Singh R, Jamieson A, Cresswell P. GILT is a critical host factor for Listeria monocytogenes infection. Nature 2008; 455:1244-7.
83. Angelakopoulos H, Loock K, Sisul DM, Jensen ER, Miller JF, Hohman EL. 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 2002; 70:3592-601.
84. 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.