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 Research

Volumn 68, Issue 19, 2008, Pages 8066-8075

  Maciag, Paulo Cesar ^a,c   Seavey, Matthew M ^a   Pan, Zhen Kun ^a   Ferrone, Soldano ^b   Paterson, Yvonne ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c ADVAXIS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HLA A2 ANTIGEN; LISTERIOLYSIN O; PROTEOCHONDROITIN SULFATE; TUMOR VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BACTERIAL GENE; BREAST CANCER; CANCER CELL CULTURE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; LISTERIA MONOCYTOGENES; MELANOMA; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN TARGETING; RECOMBINANT GENE; TUMOR VASCULARIZATION; WOUND HEALING;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; IMMUNITY, CELLULAR; IMMUNOTHERAPY; LISTERIA MONOCYTOGENES; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PERICYTES; RECOMBINANT PROTEINS; TREATMENT OUTCOME; TUMOR CELLS, CULTURED;

EID: 54249117270     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0287     Document Type: Article

References (48)

1. 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.
2. Chang CC, Campoli M, Luo W, Zhao W, Zaenker KS, Ferrone S. Immunotherapy of melanoma targeting human high molecular weight melanoma-associated antigen: potential role of nonimmunological mechanisms. Ann N Y Acad Sci 2004;1028:340-50.
3. Baluk P, Hashizume H, McDonald DM. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 2005;15:102-11.
4. von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res 2006;312:623-9.
5. Schneider S, Bosse F, D'Urso D, et al. The AN2 protein is a novel marker for the Schwann cell lineage expressed by immature and nonmyelinating Schwann cells. J Neurosci 2001;21:920-33.
6. Mittelman A, Chen ZJ, Yang H, Wong GY, Ferrone S. Human high molecular weight melanoma-associated antigen (HMW-MAA) mimicry by mouse anti-idiotypic monoclonal antibody MK2-23: induction of humoral anti-HMW-MAA immunity and prolongation of survival in patients with stage IV melanoma. Proc Natl Acad Sci U S A 1992;89:466-70.
7. Peng L, Ko E, Luo W, Wang X, Shrikant PA, Ferrone S. CD4-dependent potentiation of a high molecular weight-melanoma-associated antigen-specific CTL response elicited in HLA-A2/Kb transgenic mice. J Immunol 2006;176:2307-15.
8. 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.
9. Gunn GR, Zubair A, Peters C, Pan ZK, Wu TC, 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 2001;167:6471-9.
10. 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.
11. Paterson Y, Maciag PC. Listeria-based vaccines for cancer treatment. Curr Opin Mol Ther 2005;7:454-60.
12. Portnoy DA, Auerbuch V, Glomski IJ. The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 2002;158:409-14.
13. Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev 2004;4:812-23.
14. Dietrich G, Hess J, Gentschev I, Knapp B, Kaufmann SH, Goebel W. From evil to good: a cytolysin in vaccine development. Trends Microbiol 2001;9:23-8.
15. Yamamoto K, Kawamura I, Tominaga T, et al. Listeriolysin O, a cytolysin derived from Listeria monocytogenes, inhibits generation of ovalbumin-specific Th2 immune response by skewing maturation of antigen-specific T cells into Th1 cells. Clin Exp Immunol 2005;142:268-74.
16. Kohda C, Kawamura I, Baba H, 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.
17. Kimoto T, Kawamura I, Kohda C, et al. Differences in γ 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.
18. Sewell DA, Shahabi V, Gunn GR, 3rd, Pan ZK, Dominiecki ME, Paterson Y. Recombinant Listeria vaccines containing PEST sequences are potent immune adjuvants for the tumor-associated antigen human papillomavirus-16 E7. Cancer Res 2004;64:8821-5.
19. Hussain SF, Paterson Y. What is needed for effective antitumor immunotherapy? Lessons learned using Listeria monocytogenes as a live vector for HPV-associated tumors. Cancer Immunol Immunother 2005;54:577-86.
20. Muller WJ. Expression of activated oncogenes in the murine mammary gland: transgenic models for human breast cancer. Cancer Metastasis Rev 1991;10:217-27.
21. Chen ZJ, Ferrone S. Comparison of the binding parameters to melanoma cells of antihuman high molecular weight-melanoma associated antigen (HMW-MAA) monoclonal antibodies (mAb) and syngeneic anti-anti-idiotypic (anti-anti-id) mAb. Ann N Y Acad Sci 1993;690:398-401.
22. Peters C, Paterson Y. Enhancing the immunogenicity of bioengineered Listeria monocytogenes by passaging through live animal hosts. Vaccine 2003;21:1187-94.
23. Niethammer AG, Xiang R, Becker JC, et al. A DNA vaccine against VEGF receptor 2 prevents effective angiogenesis and inhibits tumor growth. Nat Med 2002;8:1369-75.
24. Reilly RT, Gottlieb MB, Ercolini AM, et al. HER-2/neu is a tumor rejection target in tolerized HER-2/neu transgenic mice. Cancer Res 2000;60:3569-76.
25. Geginat G, Schenk S, Skoberne M, Goebel W, Hof H. A novel approach of direct ex vivo epitope mapping identifies dominant and subdominant CD4 and CD8 T cell epitopes from Listeria monocytogenes . J Immunol 2001;166:1877-84.
26. Kamm C, Skoberne M, Geginat G. CD8 T cell immunome analysis of Listeria monocytogenes. FEMS Immunol Med Microbiol 2003;35:235-42.
27. Brzoza KL, Rockel AB, Hiltbold EM. Cytoplasmic entry of Listeria monocytogenes enhances dendritic cell maturation and T cell differentiation and function. J Immunol 2004;173:2641-51.
28. Berche P, Gaillard JL, Sansonetti PJ. Intracellular growth of Listeria monocytogenes as a prerequisite for in vivo induction of T cell-mediated immunity. J Immunol 1987;138:2266-71.
29. +-T-cell potency during bacterial infection. Infect Immun 2006;74:6387-97.
30. Schafer R, Portnoy DA, Brassell SA, Paterson Y. Induction of a cellular immune response to a foreign antigen by a recombinant Listeria monocytogenes vaccine. J Immunol 1992;149:53-9.
31. + T cell response to Listeria monocytogenes infection. J Immunol 2004;173:5679-87.
32. Lamikanra A, Pan ZK, Isaacs SN, Wu TC, Paterson Y. Regression of established human papillomavirus type 16 (HPV-16) immortalized tumors in vivo by vaccinia viruses expressing different forms of HPV-16 E7 correlates with enhanced CD8(+) T-cell responses that home to the tumor site. J Virol 2001;75:9654-64.
33. Shedlock DJ, Whitmire JK, Tan J, MacDonald AS, Ahmed R, Shen H. Role of CD4 T cell help and costimulation in CD8 T cell responses during Listeria monocytogenes infection. J Immunol 2003;170:2053-63.
34. Ossendorp F, Toes RE, Offringa R, van der Burg SH, Melief CJ. Importance of CD4(+) T helper cell responses in tumor immunity. Immunol Lett 2000;74:75-9.
35. Wu TY, Fleischmann WR, Jr. Murine B16 melanoma vaccination-induced tumor immunity: identification of specific immune cells and functions involved. J Interferon Cytokine Res 2001;21:1117-27.
36. + T cell immunity against B16 melanoma. J Immunol 2003;171:5940-7.
37. Knutson KL, Disis ML. Tumor antigen-specific T helper cells in cancer immunity and immunotherapy. Cancer Immunol Immunother 2005;54:721-8.
38. Yamaguchi T, Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin Cancer Biol 2006;16:115-23.
39. high regulatory T cell function in vivo . J Immunol 2007;179:1532-41.
40. + regulatory T cells that secrete TGFh and IL-10 are preferentially induced by a vaccine vector. J Immunother (1997) 2004;27:339-46.
41. Huang B, Zhao J, Shen S, et al. Listeria monocytogenes promotes tumor growth via tumor cell toll-like receptor 2 signaling. Cancer Res 2007;67:4346-52.
42. Thale C, Kiderlen AF. Sources of interferon-γ (IFN-γ) in early immune response to Listeria monocytogenes . Immunobiology 2005;210:673-83.
43. Yao L, Sgadari C, Furuke K, Bloom ET, Teruya-Feldstein J, Tosato G. Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood 1999;93:1612-21.
44. 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. Am J Pathol 1990;136:1393-405.
45. Haanen JB, Baars A, Gomez R, et al. Melanoma-specific tumor-infiltrating lymphocytes but not circulating melanoma-specific T cells may predict survival in resected advanced-stage melanoma patients. Cancer Immunol Immunother 2006;55:451-8.
46. Pietras K, Hanahan D. A multitargeted, metronomic, and maximum-tolerated dose "chemo-switch" regimen is antiangiogenic, producing objective responses and survival benefit in a mouse model of cancer. J Clin Oncol 2005;23:939-52.
47. Starks H, Bruhn KW, Shen H, et al. Listeria monocytogenes as a vaccine vector: virulence attenuation or existing antivector immunity does not diminish therapeutic efficacy. J Immunol 2004;173:420-7.
48. 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.