Vascular endothelial growth factor-D-mediated blockade of regulatory T cells within tumors is induced by hematopoietic stem cell transplantation

Journal of Immunology

Volumn 191, Issue 6, 2013, Pages 3440-3452

  Udagawa, Takeshi ^a,b   Narumi, Kenta ^a   Suzuki, Koji ^a,c   Aida, Kouichirou ^a,b   Miyakawa, Reina ^a   Ikarashi, Yoshinori ^a   Makimoto, Atsushi ^c   Chikaraishi, Tatsuya ^b   Yoshida, Teruhiko ^a   Aoki, Kazunori ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c NATIONAL CANCER CENTER HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VASCULOTROPIN ANTIBODY; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3 NEUTRALIZING ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL DENSITY; CELL EXPANSION; CELL KINETICS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE TRANSFER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; SPLEEN; UPREGULATION;

ANIMALS; FEMALE; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS, EXPERIMENTAL; T-LYMPHOCYTES, REGULATORY; VASCULAR ENDOTHELIAL GROWTH FACTOR D;

EID: 84884264288     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201454     Document Type: Article

References (45)

1. Halter, J., J. Passweg, and P. Häusermann. 2012. Future trends in hematopoietic stem cell transplantation. Curr. Probl. Dermatol. 43: 165-170.
2. Bregni, M., W. Herr, and D. Blaise; Solid Tumor Working Party of EBMT. 2011. Allogeneic stem cell transplantation for renal cell carcinoma. Expert Rev. Anticancer Ther. 11: 901-911.
3. Demirer, T., L. Barkholt, D. Blaise, P. Pedrazzoli, M. Aglietta, A. M. Carella, J. O. Bay, F. Arpaci, G. Rosti, G. Gurman, et al; EBMT Solid Tumors Working Party. 2008. Transplantation of allogeneic hematopoietic stem cells: an emerging treatment modality for solid tumors. Nat. Clin. Pract. Oncol. 5: 256-267.
4. Barrett, D., J. D. Fish, and S. A. Grupp. 2010. Autologous and allogeneic cellular therapies for high-risk pediatric solid tumors. Pediatr. Clin. North Am. 57: 47-66.
5. Pidala, J. 2011. Graft-vs-host disease following allogeneic hematopoietic cell transplantation. Cancer Contr. 18: 268-276.
6. Borrello, I., E. M. Sotomayor, F. M. Rattis, S. K. Cooke, L. Gu, and H. I. Levitsky. 2000. Sustaining the graft-versus-tumor effect through posttransplant immunization with granulocyte-macrophage colony-stimulating factor (GM-CSF)-producing tumor vaccines. Blood 95: 3011-3019.
7. Hu, H. M., C. H. Poehlein, W. J. Urba, and B. A. Fox. 2002. Development of antitumor immune responses in reconstituted lymphopenic hosts. Cancer Res. 62: 3914-3919.
8. Dummer, W., A. G. Niethammer, R. Baccala, B. R. Lawson, N. Wagner, R. A. Reisfeld, and A. N. Theofilopoulos. 2002. T cell homeostatic proliferation elicits effective antitumor autoimmunity. J. Clin. Invest. 110: 185-192.
9. Wrzesinski, C., and N. P. Restifo. 2005. Less is more: lymphodepletion followed by hematopoietic stem cell transplant augments adoptive T-cell-based anti-tumor immunotherapy. Curr. Opin. Immunol. 17: 195-201.
10. Baccala, R., R. Gonzalez-Quintial, W. Dummer, and A. N. Theofilopoulos. 2005. Tumor immunity via homeostatic T cell proliferation: mechanistic aspects and clinical perspectives. Springer Semin. Immunopathol. 27: 75-85.
11. Antony, P. A., C. A. Piccirillo, A. Akpinarli, S. E. Finkelstein, P. J. Speiss, D. R. Surman, D. C. Palmer, C. C. Chan, C. A. Klebanoff, W. W. Overwijk, et al. 2005. CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174: 2591-2601.
12. Sica, A., and V. Bronte. 2007. Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 117: 1155-1166.
13. Turk, M. J., J. A. Guevara-Patiño, G. A. Rizzuto, M. E. Engelhorn, S. Sakaguchi, and A. N. Houghton. 2004. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J. Exp. Med. 200: 771-782.
14. Mirmonsef, P., G. Tan, G. Zhou, T. Morino, K. Noonan, I. Borrello, and H. I. Levitsky. 2008. Escape from suppression: tumor-specific effector cells outcompete regulatory T cells following stem-cell transplantation. Blood 111: 2112-2121.
15. Nizar, S., J. Copier, B. Meyer, M. Bodman-Smith, C. Galustian, D. Kumar, and A. Dalgleish. 2009. T-regulatory cell modulation: the future of cancer immunotherapy? Br. J. Cancer 100: 1697-1703.
16. Nishikawa, H., and S. Sakaguchi. 2010. Regulatory T cells in tumor immunity. Int. J. Cancer 127: 759-767.
17. Bahram, F., and L. Claesson-Welsh. 2010. VEGF-mediated signal transduction in lymphatic endothelial cells. Pathophysiology 17: 253-261.
18. Kobayashi, A., H. Hara, M. Ohashi, T. Nishimoto, K. Yoshida, N. Ohkohchi, T. Yoshida, and K. Aoki. 2007. Allogeneic MHC gene transfer enhances an effective antitumor immunity in the early period of autologous hematopoietic stem cell transplantation. Clin. Cancer Res. 13: 7469-7479.
19. Narumi, K., T. Udagawa, A. Kondoh, A. Kobayashi, H. Hara, Y. Ikarashi, S. Ohnami, F. Takeshita, T. Ochiya, T. Okada, et al. 2012. In vivo delivery of interferon-a gene enhances tumor immunity and suppresses immunotolerance in reconstituted lymphopenic hosts. Gene Ther. 19: 34-48.
20. Bilate, A. M., and J. J. Lafaille. 2012. Induced CD4(+)Foxp3(+) regulatory T cells in immune tolerance. Annu. Rev. Immunol. 30: 733-758.
21. Hurwitz, A. A., and S. K. Watkins. 2012. Immune suppression in the tumor microenvironment: a role for dendritic cell-mediated tolerization of T cells. Cancer Immunol. Immunother. 61: 289-293.
22. Rabinovich, G. A., D. Gabrilovich, and E. M. Sotomayor. 2007. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 25: 267-296.
23. Onizuka, S., I. Tawara, J. Shimizu, S. Sakaguchi, T. Fujita, and E. Nakayama. 1999. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res. 59: 3128-3133.
24. Steinman, R. M. 2012. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30: 1-22.
25. Garcia, C. A., H. Wang, M. R. Benakanakere, E. Barrett, D. F. Kinane, and M. Martin. 2009. c-jun controls the ability of IL-12 to induce IL-10 production from human memory CD4+ T cells. J. Immunol. 183: 4475-4482.
26. Pasare, C., and R. Medzhitov. 2003. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
27. Hamrah, P., L. Chen, Q. Zhang, and M. R. Dana. 2003. Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells. Am. J. Pathol. 163: 57-68.
28. Nykänen, A. I., H. Sandelin, R. Krebs, M. A. Keränen, R. Tuuminen, T. Kärpänen, Y. Wu, B. Pytowski, P. K. Koskinen, S. Ylä-Herttuala, et al. 2010. Targeting lymphatic vessel activation and CCL21 production by vascular endothelial growth factor receptor-3 inhibition has novel immunomodulatory and antiarteriosclerotic effects in cardiac allografts. Circulation 121: 1413-1422.
29. Tugues, S., S. Koch, L. Gualandi, X. Li, and L. Claesson-Welsh. 2011. Vascular endothelial growth factors and receptors: anti-angiogenic therapy in the treatment of cancer. Mol. Aspects Med. 32: 88-111.
30. Borrello, I. M., H. I. Levitsky, W. Stock, D. Sher, L. Qin, D. J. DeAngelo, E. P. Alyea, R. M. Stone, L. E. Damon, C. A. Linker, et al. 2009. Granulocyte-macrophage colony-stimulating factor (GM-CSF)-secreting cellular immunotherapy in combination with autologous stem cell transplantation (ASCT) as postremission therapy for acute myeloid leukemia (AML). Blood 114: 1736-1745.
31. Udagawa, T., K. Narumi, N. Goto, K. Aida, K. Suzuki, T. Ochiya, A. Makimoto, T. Yoshida, T. Chikaraishi, and K. Aoki. 2012. Syngeneic hematopoietic stem cell transplantation enhances the antitumor immunity of intratumoral type I interferon gene transfer for sarcoma. Hum. Gene Ther. 23: 173-186.
32. Rocha, B., A. Grandien, and A. A. Freitas. 1995. Anergy and exhaustion are independent mechanisms of peripheral T cell tolerance. J. Exp. Med. 181: 993-1003.
33. Luznik, L., J. E. Slansky, S. Jalla, I. Borrello, H. I. Levitsky, D. M. Pardoll, and E. J. Fuchs. 2003. Successful therapy of metastatic cancer using tumor vaccines in mixed allogeneic bone marrow chimeras. Blood 101: 1645-1652.
34. Jing,W., X. Yan, W. H. Hallett, J. A. Gershan, and B. D. Johnson. 2011. Depletion of CD25+ T cells from hematopoietic stem cell grafts increases posttransplantation vaccine-induced immunity to neuroblastoma. Blood 117: 6952-6962.
35. Lal, G., N. Zhang, W. van der Touw, Y. Ding, W. Ju, E. P. Bottinger, S. P. Reid, D. E. Levy, and J. S. Bromberg. 2009. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J. Immunol. 182: 259-273.
36. Zhou, L., M. M. Chong, and D. R. Littman. 2009. Plasticity of CD4+ T cell lineage differentiation. Immunity 30: 646-655.
37. Paavonen, K., P. Puolakkainen, L. Jussila, T. Jahkola, and K. Alitalo. 2000. Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am. J. Pathol. 156: 1499-1504.
38. Stacker, S. A., C. Caesar, M. E. Baldwin, G. E. Thornton, R. A. Williams, R. Prevo, D. G. Jackson, S. Nishikawa, H. Kubo, and M. G. Achen. 2001. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat. Med. 7: 186-191.
39. Baluk, P., T. Tammela, E. Ator, N. Lyubynska, M. G. Achen, D. J. Hicklin, M. Jeltsch, T. V. Petrova, B. Pytowski, S. A. Stacker, et al. 2005. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Invest. 115: 247-257.
40. Iwata, C., M. R. Kano, A. Komuro, M. Oka, K. Kiyono, E. Johansson, Y. Morishita, M. Yashiro, K. Hirakawa, M. Kaminishi, and K. Miyazono. 2007. Inhibition of cyclooxygenase-2 suppresses lymph node metastasis via reduction of lymphangiogenesis. Cancer Res. 67: 10181-10189.
41. Ristimäki, A., K. Narko, B. Enholm, V. Joukov, and K. Alitalo. 1998. Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J. Biol. Chem. 273: 8413-8418.
42. Chen, L., P. Hamrah, C. Cursiefen, Q. Zhang, B. Pytowski, J. W. Streilein, and M. R. Dana. 2004. Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nat. Med. 10: 813-815.
43. Ohm, J. E., D. I. Gabrilovich, G. D. Sempowski, E. Kisseleva, K. S. Parman, S. Nadaf, and D. P. Carbone. 2003. VEGF inhibits T-cell development and may contribute to tumor-induced immune suppression. Blood 101: 4878-4886.
44. Laakkonen, P., M. Waltari, T. Holopainen, T. Takahashi, B. Pytowski, P. Steiner, D. Hicklin, K. Persaud, J. R. Tonra, L. Witte, and K. Alitalo. 2007. Vascular endothelial growth factor receptor 3 is involved in tumor angiogenesis and growth. Cancer Res. 67: 593-599.
45. Ye, J., R. S. Livergood, and G. Peng. 2013. The role and regulation of human Th17 cells in tumor immunity. Am. J. Pathol. 182: 10-20.