Multivalent RNA Aptamers That Inhibit CTLA-4 and Enhance Tumor Immunity

Cancer Research

Volumn 63, Issue 21, 2003, Pages 7483-7489

  Santulli Marotto, Sandra ^a   Nair, Smita K ^a   Rusconi, Chris ^a   Sullenger, Bruce ^a   Gilboa, Eli ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; CYTOTOXIC T LYMPHOCYTE 4 ANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DEL 60 APTAMER; M9A 9 APTAMER; RNA APTAMER; T LYMPHOCYTE ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; DRUG ACTIVITY; DRUG PROTEIN BINDING; DRUG SYNTHESIS; FEMALE; IMMUNE SYSTEM; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; BASE SEQUENCE; CRICETINAE; FEMALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; OLIGONUCLEOTIDES; RNA;

EID: 0242610799     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Mueller, D. L., Jenkins, M. K., and Schwartz, R. H. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annu. Rev. Immunol., 7: 445-480, 1989.
2. Lenschow, D. J., Walunas, T. L., and Bluestone, J. A. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol., 14: 233-258, 1996.
3. Chambers, C. A., Kuhns, M. S., Egen, J. G., and Allison, J. P. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu. Rev. Immunol., 19: 565-594, 2001.
4. Salomon, B., and Bluestone, J. A. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu. Rev. Immunol., 19: 225-252, 2001.
5. Alegre, M. L., Frauwirth, K. A., and Thompson, C. B. T-cell regulation by CD28 and CTLA-4. Nat. Rev. Immunol., 1: 220-228, 2001.
6. Waterhouse, P., Penninger, J. M., Timms, E., Wakeham, A., Shahinian, A., Lee, K. P., Thompson, C. B., Griesser, H., and Mak, T. W. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4, Science (Wash. DC), 270: 985-988, 1995.
7. Tivol, E. A., Borriello, F., Schweitzer, A. N., Lynch, W. P., Bluestone, J. A., and Sharpe, A. H. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity, 3: 541-547, 1995.
8. Walunas, T. L., Lenschow, D. J., Bakker, C. Y., Linsley, P. S., Freeman, G. J., Green, J. M., Thompson, C. B., and Bluestone, J. A. CTLA-4 can function as a negative regulator of T cell activation. Immunity, 1: 405-413, 1994.
9. Krummel, M. F., and Allison, J. P. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp. Med., 182: 459-465, 1995.
10. Reid, S., Malmstrom, V., and Powrie, F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med., 192: 295-302, 2000.
11. Takahashi, T., Tagami, T. Yamazaki, S., Uede, T., Shimizu, J., Sakaguchi, N., Mak, T. W., and Sakaguchi, S. Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med., 192: 303-310, 2000.
12. Levings, M. K., Sangregorio, R., and Roncarolo, M. G. Human cd25(+)cd4(+) t regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J. Exp. Med., 193: 1295-1302, 2001.
13. Jonuleit, H., Schmitt, E., Stassen, M., Tuettenberg, A., Knop, J., and Enk, A. H. Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J. Exp. Med., 193: 1285-1294, 2001.
14. Sutmuller, R. P., van Duivenvoorde, L. M., van Elsas, A., Schumacher, T. N., Wildenberg, M. E., Allison, J. P., Toes, R. E., Offringa, R., and Melief, C. J. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J. Exp. Med., 194: 823-832, 2001.
15. Leach, D. R., Krummel, M. F., and Allison, J. P. Enhancement of antitumor immunity by CTLA-4 blockade. Science (Wash. DC), 271: 1734-1736, 1996.
16. Yang, Y. F., Zou, J. P., Mu, J., Wijesuriya, R., Ono, S., Walunas, T., Bluestone, J., Fujiwara, H., and Hamaoka, T. Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyte-associated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages. Cancer Res., 57: 4036-4041, 1997.
17. van Elsas, A., Hurwitz, A. A., and Allison, J. P. Combination immunotherapy of B 16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med., 190: 355-366, 1999.
18. Hurwitz, A. A., Foster, B. A., Kwon, E. D., Truong, T., Choi, E. M., Greenberg, N. M., Burg, M. B., and Allison, J. P. Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cancer Res., 60: 2444-2448, 2000.
19. Hurwitz, A. A., Yu, T. F., Leach, D. R., and Allison, J. P. CTLA-4 blockade synergizes with tumor-derived granulocyte-macrophage colony-stimulating factor for treatment of an experimental mammary carcinoma. Proc. Natl. Acad. Sci. USA. 95: 10067-10071, 1998.
20. Mokyr, M. B., Kalinichenko, T., Gorelik, L., and Bluestone, J. A. Realization of the therapeutic potential of CTLA-4 blockade in low-dose chemotherapy-treated tumor-bearing mice. Cancer Res., 58: 5301-5304, 1998.
21. White, R. R., Sullenger, B. A., and Rusconi, C. P. Developing aptamers into therapeutics. J. Clin. Investig., 106: 929-934, 2000.
22. Gold, L. Oligonucleotides as research, diagnostic, and therapeutic agents. J. Biol. Chem., 270: 13581-13584, 1995.
23. Drolet, D. W., Nelson, J., Tucker, C. E., Zack, P. M., Nixon, K., Bolin, R., Judkins, M. B., Farmer, J. A., Wolf, J. L., Gill, S. C., and Bendele, R. A. Pharmacokinetics and safety of an anti-vascular endothelial growth factor aptamer (NX1838) following injection into the vitreous humor of rhesus monkeys. Pharm. Res. 17: 1503-1510, 2000.
24. Hicke, B. J., and Stephens, A. W. Escort aptamers: a delivery service for diagnosis and therapy. J. Clin. Investig., 106: 923-928, 2000.
25. Porgador, A., Gansbacher, B., Bannerji, R., Tzehoval, E., Gilboa, E., Feldman, M., and Eisenbach, L. Anti-metastatic vaccination of tumor-bearing mice with IL-2-gene-inserted tumor cells. Int. J. Cancer. 53: 471-477, 1993.
26. Boczkowski, D., Nair, S. K., Nam, J. H., Lyerly, H. K., and Gilboa, E. Induction of tumor immunity and cytotoxic T lymphocyte responses using dendritic cells transfected with messenger RNA amplified from tumor cells. Cancer Res., 60: 1028-1034, 2000.
27. Soloway, M. S., de Kemion, J. B., Rose, D., and Persky, L. Effect of chemotherapeutic agents on bladder cancer: a new animal model. Surg. Forum, 24: 542-544, 1973.
28. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S., and Steinman, R. M. 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, 1992.
29. Nair, S. K., Heiser, A., Boczkowski, D., Majumdar, A., Naoe, M., Lebkowski, J. S., Viweg, J., and Gilboa, E. Induction of cytotoxic T cell responses and tumor immunity against unrelated tumors using telomerase reverse transcriptase RNA transfected dendritic cells. Nat. Med., 6: 1011-1017, 2000.
30. Tucker, C. E., Chen, L. S., Judkins, M. B., Farmer, J. A., Gill, S. C., and Drolet, D. W. Detection and plasma pharmacokinetics of an anti-vascular endothelial growth factor oligonucleotide-aptamer (NX1838) in rhesus monkeys. J. Chromatogr. B Biomed. Sci. Appl., 732: 203-212, 1999.
31. Willis, M. C., Collins, B. D., Zhang, T., Green, L. S., Sebesta, D. P., Bell, C., Kellogg, E., Gill, S. C., Magallanez. A., Knauer, S., Bendele, R. A., Gill, P. S., Janjic, N., and Collins, B. Liposome anchored vascular endothelial growth factor aptamers. Bioconjug. Chem., 9: 573-582, 1998.
32. Altman, J. D., Moss, P. A., Goulder, P. J., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J., and Davis, M. M. Phenotypic analysis of antigen-specific T lymphocytes. Science (Wash. DC), 274: 94-96, 1996.
33. Ostrov, D. A., Shi, W., Schwartz, J. C., Almo, S. C., and Nathenson, S. G. Structure of murine CTLA-4 and its role in modulating T cell responsiveness. Science (Wash. DC), 290: 816-819, 2000.
34. Ikemizu, S., Gilbert, R. J., Fennelly, J. A., Collins, A. V., Harlos, K., Jones, E. Y., Stuart, D. I., and Davis, S. J. Structure and dimerization of a soluble form of B7-1. Immunity, 12: 51-60, 2000.
35. Shay, J. W., and Bacchetti, S. A survey of telomerase activity in human cancer. Eur. J. Cancer, 33: 787-791, 1997.
36. Vonderheide, R. H., Hahn, W. C., Schultze, J. L., and Nadler, L. M. The telomerase catalytic subunit is a widely expressed tumor-associated antigen recognized by cytotoxic T lymphocytes. Immunity, 10: 673-679, 1999.
37. van Elsas, A., Sutmuller, R. P., Hurwitz, A. A., Ziskin, J., Villasenor, J., Medema, J. P., Overwijk, W. W., Restifo, N. P., Melief, C. J., Offringa, R., and Allison, J. P. Elucidating the autoimmune and antitumor effector mechanisms of a treatment based on cytotoxic T lymphocyte antigen-4 blockade in combination with a B16 melanoma vaccine: comparison of prophylaxis and therapy. J. Exp. Med., 194: 481-489, 2001.
38. Ringquist, S., and Parma, D. Anti-L-selectin oligonucleotide ligands recognize CD62L-positive leukocytes: binding affinity and specificity of univalent and bivalent ligands. Cytometry, 33: 394-405, 1998.
39. Beier, M., and Hoheisel, J. D. Versatile derivatisation of solid support media for covalent bonding on DNA-microchips. Nucleic Acids Res., 27: 1970-1977, 1999.
40. Doudna, J. A., Cech, T. R., and Sullenger, B. A. Selection of an RNA molecule that mimics a major autoantigenic epitope of human insulin receptor. Proc. Natl. Acad. Sci. USA. 92: 2355-2359, 1995.
41. Lee, S. W., and Sullenger, B. A. Isolation of a nuclease-resistant decoy RNA that selectively blocks autoantibody binding to insulin receptors on human lymphocytes. J. Exp. Med., 184: 315-324, 1996.
42. Ishizaki, J., Nevins, J. R., and Sullenger, B. A. Inhibition of cell proliferation by an RNA ligand that selectively blocks E2F function. Nat. Med., 2: 1386-1389, 1996.
43. Rusconi, C. P., Yeh, A., Lyerly, H. K., Lawsom, J. H., and Sullenger, B. A. Blocking the initiation of coagulation by RNA aptamers to factor VIIa. Thromb. Haemost., 84: 841-848, 2000.
44. White, R., Rusconi, C., Scardino, E., Wolberg, A., Lawson, J., Hoffman, M., and Sullenger, B. Generation of species cross-reactive aptamers using "toggle" SELEX. Mol. Ther., 4: 567-573, 2001.
45. Rusconi, C. P., Scardino, E., Layzer, J., Pitoc, G. A., Ortel, T. L., Monroe, D., and Sullenger, B. A. RNA aptamers as reversible antagonists of coagulation factor IXa. Nature (Lond.), 419: 90-94, 2002.