All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination

Cancer Research

Volumn 63, Issue 15, 2003, Pages 4441-4449

  Kusmartsev, Sergei ^a   Cheng, Fengdong ^a   Yu, Bin ^a   Nefedova, Yulia ^a   Sotomayor, Eduardo ^a   Lush, Richard ^a   Gabrilovich, Dmitry ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; PLACEBO; RETINOIC ACID;

ADENOCARCINOMA; ADENOVIRUS; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMATURE MYELOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR IMMUNOLOGY; TUMOR MODEL; TUMOR SUPPRESSOR GENE; VACCINATION; VIRUS INFECTION;

ADENOCARCINOMA; ADOPTIVE TRANSFER; ANIMALS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DRUG SYNERGISM; FEMALE; FIBROSARCOMA; IMMUNE TOLERANCE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS; TRETINOIN;

EID: 0042591427     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (36)

1. Young, M., Newby, M., and Wepsic, T. Hematopoiesis and suppressor bone marrow cells in mice bearing large metastatic Lewis lung carcinoma tumors. Cancer Res., 47: 100-105, 1987.
2. Jaffe, M., Arai, H., and Nabel, G. Mechanisms of tumor-induced immunosuppression: evidence for contact-dependent T-cell suppression by monocytes. Mol. Med., 2: 692-701, 1996.
3. Almand, B., Clark, J. I., Nikitina, E., English, N. R., Knight, S. C., Carbone, D. P., and Gabrilovich, D. I. Increased production of immature myeloid cells in cancer patients. A mechanism of immunosuppression in cancer. J. Immunol., 166: 678-689, 2001.
4. Subiza, J., Vinuela, J., Rodriguez, R., and De la Concha, E. Development of splenic natural suppressor (NS) cells in Ehrlich tumor-bearing mice. Int. J. Cancer, 44: 307-311, 1989.
5. Watson, G., Fu, Y., and Lopez, D. Splenic macrophages from tumor-bearing mice co-expressing Mac-1 and Mac-2 antigens exert immunoregulatory functions via two distinct mechanisms. J. Leukoc. Biol., 49: 126-138, 1991.
6. Almand, B., Resser, J., Lindman, B., Nadaf, S., Clark, J., Kwon, E., Carbone, D., and Gabrilovich, D. Clinical significance of defective dendritic cell differentiation in cancer. Clin. Cancer Res., 6: 1755-1766, 2000.
7. Bronte, V., Chappell, D. B., Apolloni, E., Cabrelle, A., Wang, M., Hwu, P., and Restifo, N. P. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T-cell responses by dysregulating antigen-presenting cell maturation. J. Immunol., 162: 5728-5737, 1999.
8. Kusmartsev, S., Li, Y., and Chen, S. Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T-cell activation induced through CD3/CD28 costimulation. J. Immunol., 165: 779-785, 2000.
9. Otsui, M., Kimura, Y., Aoe, T., Okamoto, Y., and Saito, T. Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 chain of T-cell receptor complex and antigen-specific T-cell responses. Proc. Natl. Acad. Sci. USA, 93: 13119-13124, 1996.
10. Bronte, V., Wang, M., Overwijk, W., Surman, D., Pericle, F., Rosenberg, S. A., and Restifo, N. P. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J. Immunol., 161: 5313-5320, 1998.
11. Gabrilovich, D. I., Velders, M., Sotomayor, E., and Kast, W. M. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J. Immunol., 166: 5398-5406, 2001.
12. Staveley-O'Corrol, K., Sotomayor, E., Mongomery, J., Borrelo, I., Hwang, L., Fein, S., Pardoll, D., and Levitsky, H. Induction of antigen-specific T-cell anergy: an early event in the course of tumor progression. Proc. Natl. Acad. Sci. USA, 95: 1178-1183, 1998.
13. Sotomayor, E. M., Borrello, I., Tubb, E., Rattis, F. M., Bien, H., Lu, Z., Fein, S., Schoenberger, S., and Levitsky, H. I. Conversion of tumor-specific CD4+ T-cell tolerance to T-cell priming through in vivo ligation of CD40. Nat. Med., 5: 780-787, 1999.
14. Breitman, T. R., Collins, S. J., and Keene, B. R. Terminal differentiation of human promyelocytic leukemic cells in primary culture in response to retinoic acid. Blood, 57: 1000-1004, 1981.
15. Hittelman, W. N., Agbor, P., Petkovic, I., Anderson, B., Kantarjian, H., Walters, R., Koller, C., and Beran, M. Detection of leukemic clone maturation in vivo by premature chromosome condensation. Blood, 72: 1950-1960, 1988.
16. Castaigne, S., Chomienne, C., Daniel, M. T., Ballerini, P., Berger, R., Fenaux, P., and Degos, L. All-trans-retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results. Blood, 76: 1704-1709, 1990.
17. Warrell, R. P., Frankel, S. R., Miller, W. H., Scheinberg, D. A., Itri, L. M., Hittelman, W. N., Vyas, R., Andreeff, M., Tafuri, A., and Jakubowski, A. E. A. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid). N. Engl. J. Med., 324: 1385-1393, 1991.
18. Van Bockstaele, D. R., Lenjou, M., Snoeck, H-W., Lardon, F., Stryckmans, P., and Peetermans, M. E. Direct effects of 13-cis and all-trans retinoic acid on normal bone marrow (BM) progenitors: comparative study on BM mononuclear cells and on isolated CD34+ BM cells. Ann. Hematol., 66: 61-66, 1993.
19. Gratas, C., Menot, M. L., Dresch, C., and Chomienne, C. Retinoic acid supports granulocytic but not erythroid differentiation of myeloid progenitors in normal bone marrow cells. Leukemia (Baltimore), 7: 1156-1162, 1993.
20. Tohda, S., and Minden, M. D. Modulation of growth factor receptors on acute myeloblastic leukemia cells by retinoic acid. Jpn. J. Cancer Res., 85: 378-383, 1994.
21. Nikitina, E. Y., Chada, S., Muro-Cacho, C., Fang, B., Zhang, R., Roth, J. A., and Gabrilovich, D. I. An effective immunization and cancer treatment with activated dendritic cells transduced with full-length wild-type p53. Gene Ther., 9: 345-352, 2002.
22. Feltkamp, M. C. W., Smits, H. L., Vierboom, M. P. M., Minnaar, R. P., de Jongh, B. M., Drijfhout, J. W., ter Schegget, J., Melief, C. J. M., and Kast, W. M. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur. J. Immunol., 23: 2242-2249, 1993.
23. Feltkamp, M. C. W., Vreugdenhil, G. R., Vierboom. M. P. M., Ras, E., van der Burg, S. H., ter Schegget, J., Melief, C. J. M., and Kast, W. M. Cytotoxic T lymphocytes raised against a subdominant epitope offered as a synthetic peptide eradicate human papillomavirus type 16-induced tumors. Eur. J. Immunol., 25: 2638-2642, 1995.
24. Xu, X., Wong, W., Goldberg, L., Baer, S., Wolf, J., Ramsdell, W., Alberts, D., Lippman, S., and Lotan, R. Progressive decreases in nuclear retinoid receptors during skin squamous carcinogenesis. Cancer Res., 61: 4306-4310, 2001.
25. Gabrilovich, D. I., Ishida, T., Nadaf, S., Ohm, J., and Carbone, D. P. Antibodies to vascular endothelial growth factor enhance the efficacy of cancer immunotherapy by improving endogenous dendritic cell function. Clin. Cancer Res., 5: 2963-2970, 1999.
26. Pugh, C. W., MacPherson, G. G., and Steer, H. W. Characterization of non lymphoid cells derived from rat peripheral lymph. J. Exp. Med., 157: 1758-1763, 1983.
27. Salomon, B., Lores, P., Pioche, C., Racz, P., Jami, J., and Klatzmann, D. Conditional ablation of dendritic cells in transgenic mice. J. Immunol., 152: 537-547, 1994.
28. Nikitina, E. Y., and Gabrilovich, D. I. Combination of γ irradiation and dendritic cell administration in treatment of advanced cancer. Int. J. Cancer, 94: 825-833, 2001.
29. Mangelsdorf, D., Umesono, K., and Evans, R. The retinoid receptors. In: M. Sporn, B. Roberts, and D. Goodman (eds.), The Retinoids: Biology, Chemistry, and Medicine, pp. 319-349. New York: Raven, 1994.
30. Nakajima, H., Kizaki, M., Sonoda, A., Mori, S., Harigaya, K., and Ikeda, Y. Retinoids (all-trans- and 9-cis-retinoic acid) stimulate production of macrophage colony-stimulating factor and granulocyte-macrophage colony-stimulating factor by human bone marrow stromal cells. Blood, 84: 4107-4115, 1994.
31. Dubois, C., Schlageter, M. H., de Gentile, A., Balitrand, N., Toubert, M. E., Krawice, I., Fenaux, P., Castaigne, S., Najean, Y., and Degos, L. Modulation of IL-8, IL-1β, and G-CSF secretion by all-trans retinoic acid in acute promyelocytic leukemia. Leukemia (Baltimore), 10: 1750-1757, 1994.
32. Ishida, T., Oyama, T., Carbone, D., and Gabrilovich, D. I. Defective function of Langerhans cells in tumor-bearing animals is the result of defective maturation from hematopoietic progenitors. J. Immunol., 161: 4842-4851, 1998.
33. Kusmartsev, S., Gabrilovich, D. Inhibition of myeloid cell differentiation in cancer: The role of oxygene species. J. Leukoc. Biol., in press, 2003.
34. Bronte, V., Serafini, P., Appoloni, E., and Zanovello, P. Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J. Immunother., 24: 431-446, 2001.
35. Sotomayor, E. M., Borrello, I., Tubb, E., Allison, J. P., and Levitsky, H. I. In vivo blockade of CTLA-4 enhances the priming of responsive T cells but fails to prevent the induction of tumor antigen-specific tolerance. Proc. Natl. Acad. Sci. USA, 96: 11476-11481, 1999.
36. Gabrilovich, D., Ciernik, F., and Carbone, D. P. Dendritic cells in anti-tumor immune responses. I. Defective antigen presentation in tumor-bearing hosts. Cell. Immunol., 170: 101-110, 1996.