Site-specfic anti-tumor immunity: Differences in DC function, TGF-β production and numbers of intratumoral Foxp3+Treg

European Journal of Immunology

Volumn 39, Issue 5, 2009, Pages 1323-1333

  Biollaz, Gregoire ^a   Bernasconi, Luca ^a   Cretton, Christine ^a   Püntener, Ursula ^a   Frei, Karl ^a   Fontana, Adriano ^a   Suter, Tobias ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

DC; Immune privilege; Treg; Tumor immunity

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CANCER; CANCER GROWTH; CANCER LOCALIZATION; CELL FUNCTION; CELL INFILTRATION; CONTROLLED STUDY; DENDRITIC CELL; GLIOMA; GLIOMA CELL; IMMUNE RESPONSE; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SKIN CANCER; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CENTRAL NERVOUS SYSTEM TUMOR; CYTOCHEMISTRY; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; KAPLAN MEIER METHOD; LYMPHOCYTE ACTIVATION; MOUSE MUTANT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN TUMOR; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CENTRAL NERVOUS SYSTEM NEOPLASMS; DENDRITIC CELLS; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; GLIOMA; HISTOCYTOCHEMISTRY; KAPLAN-MEIERS ESTIMATE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SKIN NEOPLASMS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 67649966553     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838921     Document Type: Article

References (50)

1. Stupp, R., Mason, W. P., van den Bent, M. J.,Weller,M., Fisher, B., Taphoorn, M. J., Belanger, K. et al., Rdiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005. 352: 987-996.
2. Chahlavi, A., Rayman, P., Richmond, A. L., Biswas, K., Zhang, R., Vogelbaum, M., Tannenbaum, C. et al., Glioblastomas induce T-lymphocyte death by two distinct pathways involving gangliosides and CD70. Cancer Res. 2005. 65: 5428-5438.
3. Zou, J. P., Morford, L. A., Chougnet, C., Dix, A. R., Brooks, A. G., Torres, N., Shuman, J. D. et al., Human glioma-induced immunosuppression involves soluble factor(s) that alters monocyte cytokine profile and surface markers. J. Immunol. 1999. 162: 4882-4892.
4. Ogden, A.T., Horgan, D., Waziri, A., Anderson, D., Louca, J., McKhann, G.M., Sisti, M. B. et al., Defective receptor expression and dendritic cell differentiation of monocytes in glioblastomas. Neurosurgery 2006. 59: 902-909; discussion 909-910.
5. Wrann, M., Bodmer, S., deMartin, R., Siepl, C., Hofer-Warbinek, R., Frei, K., Hofer, E. and Fontana, A., T cell suppressor factor from human glioblastoma cells is a 12.5-kd protein closely related to transforming growth factor-beta. EMBO J. 1987. 6: 1633-1636.
6. Fontana, A., Hengartner, H., de Tribolet, N. and Weber, E., Glioblastoma cells release interleukin 1 and factors inhibiting interleukin 2-mediated effects. J. Immunol. 1984. 132: 1837-1844.
7. de Martin, R., Haendler, B., Hofer-Warbinek, R., Gaugitsch, H.,Wrann, M., Schlusener, H., Seifert, J. M. et al., Complementary DNA for human glioblastoma-derived T cell suppressor factor, a novel member of the transforming growth factor-beta gene family. EMBO J. 1987. 6: 3673-3677.
8. Naganuma, H., Sasaki, A., Satoh, E., Nagasaka, M., Nakano, S., Isoe, S. and Nukui, H., Down-regulation of transforming growth factor-beta and interleukin-10 secretion from malignant glioma cells by cytokines and anticancer drugs. J. Neurooncol. 1998. 39: 227-236.
9. Gabrilovich, D. I., Chen, H. L., Girgis, K. R., Cunningham, H. T., Meny, G. M., Nadaf, S., Kavanaugh, D. and Carbone, D. P., Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 1996. 2: 1096-1103.
10. Kokoglu, E., Tuter, Y., Sandikci, K. S., Yazici, Z., Ulakoglu, E. Z., Sonmez, H. and Ozyurt, E., Prostaglandin E2 levels in human brain tumor tissues and arachidonic acid levels in the plasma membrane of human brain tumors. Cancer Lett. 1998. 132: 17-21.
11. Frank, S., Muller, J., Bonk, C., Haroske, G., Schackert, H. K. and Schackert, G., Transmission of glioblastoma multiforme through liver transplantation. Lancet 1998. 352: 31.
12. Liu, G., Ying, H., Zeng, G., Wheeler, C. J., Black, K. L. and Yu, J. S., HER-2, gp100, and MAGE-1 are expressed in human glioblastoma and recognized by cytotoxic T cells. Cancer Res. 2004. 64: 4980-4986.
13. Tang, J., Flomenberg, P., Harshyne, L., Kenyon, L. and Andrews, D. W., Glioblastoma patients exhibit circulating tumor-specific CD81T cells. Clin. Cancer Res. 2005. 11: 5292-5299.
14. Yu, J. S., Liu, G., Ying, H., Yong, W. H., Black, K. L. and Wheeler, C. J., Vaccination with tumor lysate-pulsed dendritic cells elicits antigenspecific, cytotoxic T-cells in patients with malignant glioma. Cancer Res. 2004. 64: 4973-4979.
15. Insug, O., Ku, G., Ertl, H. C. and Blaszczyk-Thurin, M., A dendritic cell vaccine induces protective immunity to intracranial growth of glioma. Anticancer Res. 2002. 22: 613-621.
16. Ni, H. T., Spellman, S. R., Jean, W. C., Hall, W. A. and Low, W. C., Immunization with dendritic cells pulsed with tumor extract increases survival of mice bearing intracranial gliomas. J. Neurooncol. 2001. 51: 1-9.
17. Steinman, R. M. and Nussenzweig, M. C., Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 2002. 99: 351-358.
18. Vicari, A. P., Caux, C. and Trinchieri, G., Tumour escape from immune surveillance through dendritic cell inactivation. Semin. Cancer Biol. 2002. 12: 33-42.
19. Tosi, P., Sforza, V., Santopietro, R., Lio, R., Gotti, G., Paladini, P., Cevenini, G. and Barbini, P., Bronchiolo-alveolar carcinoma: An analysis of survival predictors. Eur. J. Cancer. 1992. 28A: 1365-1370.
20. Curiel, T. J., Coukos, G., Zou, L., Alvarez, X., Cheng, P., Mottram, P., Evdemon-Hogan, M. et al., Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 2004. 10: 942-949.
21. Zou, W., Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 2006. 6: 295-307.
22. Grauer, O. M., Nierkens, S., Bennink, E., Toonen, L. W., Boon, L., Wesseling, P., Sutmuller, R. P. and Adema, G. J., CD4+FoxP3+regulatory T cells gradually accumulate in gliomas during tumor growth and efficiently suppress antiglioma immune responses in vivo. Int. J. Cancer 2007. 121: 95-105.
23. El Andaloussi, A., Han, Y. and Lesniak, M. S., Prolongation of survival following depletion of CD4+CD25+regulatory T cells in mice with experimental brain tumors. J. Neurosurg. 2006. 105: 430-437.
24. El Andaloussi, A. and Lesniak, M. S., An increase in CD4+CD25+FOXP3+ regulatory T cells in tumor-infiltrating lymphocytes of human glioblastoma multiforme. Neuro-oncology 2006. 8: 234-243.
25. Chaux, P., Favre, N., Martin, M. and Martin, F., Tumor-infiltrating dendritic cells are defective in their antigen-presenting function and inducible B7 expression in rats. Int. J. Cancer 1997. 72: 619-624.
26. Fischer, H. G., Bonifas, U. and Reichmann, G., Phenotype and functions of brain dendritic cells emerging during chronic infection of mice with Toxoplasma gondii. J. Immunol. 2000. 164: 4826-4834.
27. Ponomarev, E. D., Shriver, L. P., Maresz, K. and Dittel, B. N., Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. J. Neurosci. Res. 2005. 81: 374-389.
28. Enk, A. H., Jonuleit, H., Saloga, J. and Knop, J., Dendritic cells as mediators of tumor-induced tolerance in metastatic melanoma. Int. J. Cancer 1997. 73: 309-316.
29. Chen, W., Jin, W., Hardegen, N., Lei, K. J., Li, L., Marinos, N., McGrady, G. and Wahl, S. M., Conversion of peripheral CD4+CD25- naive T cells to CD41CD251regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 2003. 198: 1875-1886.
30. Scarpino, S., Stoppacciaro, A., Ballerini, F., Marchesi, M., Prat, M., Stella, M. C., Sozzani, S. et al., Papillary carcinoma of the thyroid: Hepatocyte growth factor (HGF) stimulates tumor cells to release chemokines active in recruiting dendritic cells. Am. J. Pathol. 2000. 156: 831-837.
31. Bell, D., Chomarat, P., Broyles, D., Netto, G., Harb, G. M., Lebecque, S., Valladeau, J. et al., In breast carcinoma tissue, immature dendritic cells reside within the tumor, whereas mature dendritic cells are located in peritumoral areas. J. Exp. Med. 1999. 190: 1417-1426.
32. Suter, T., Biollaz, G., Gatto, D., Bernasconi, L., Herren, T., Reith, W. and Fontana, A., The brain as an immune privileged site: Dendritic cells of the central nervous system inhibit T cell activation. Eur. J. Immunol. 2003. 33: 2998-3006.
33. McMahon, E. J., Bailey, S. L., Castenada, C. V., Waldner, H. and Miller, S. D., Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat. Med. 2005. 11: 335-339.
34. Guiducci, C., Vicari, A. P., Sangaletti, S., Trinchieri, G. and Colombo, M. P., Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 2005. 65: 3437-3446.
35. Vicari, A. P., Chiodoni, C., Vaure, C., Ait-Yahia, S., Dercamp, C., Matsos, F., Reynard, O. et al., Reversal of tumor-induced dendritic cell paralysis by CpG immunostimulatory oligonucleotide and anti-interleukin 10 receptor antibody. J. Exp. Med. 2002. 196: 541-549.
36. Preynat-Seauve, O., Schuler, P., Contassot, E., Beermann, F., Huard, B. and French, L. E., Tumor-infiltrating dendritic cells are potent antigenpresenting cells able to activate T cells and mediate tumor rejection. J. Immunol. 2006. 176: 61-67.
37. Facoetti, A., Nano, R., Zelini, P., Morbini, P., Benericetti, E., Ceroni, M., Campoli, M. and Ferrone, S., Human leukocyte antigen and antigen processing machinery component defects in astrocytic tumors. Clin. Cancer Res. 2005. 11: 8304-8311.
38. Frei, K., Siepl, C., Groscurth, P., Bodmer, S., Schwerdel, C. and Fontana, A., Antigen presentation and tumor cytotoxicity by interferon-gammatreated microglial cells. Eur. J. Immunol. 1987. 17: 1271-1278.
39. Flugel, A., Labeur, M. S., Grasbon-Frodl, E. M., Kreutzberg, G. W. and Graeber, M. B., Microglia only weakly present glioma antigen to cytotoxic T cells. Int. J. Dev. Neurosci. 1999. 17: 547-556.
40. Boissonnas, A., Fetler, L., Zeelenberg, I. S., Hugues, S. and Amigorena, S., In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 2007. 19: 345-356.
41. Flugel, A., Berkowicz, T., Ritter, T., Labeur, M., Jenne, D. E., Li, Z., Ellwart, J. W. et al., Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity 2001. 14: 547-560.
42. Bauer, J., Bradl, M., Hickley, W. F., Forss-Petter, S., Breitschopf, H., Linington, C., Wekerle, H. and Lassmann, H., T-cell apoptosis in inflammatory brain lesions: Destruction of T cells does not depend on antigen recognition. Am. J. Pathol. 1998. 153: 715-724.
43. Didenko, V. V., Ngo, H. N., Minchew, C. and Baskin, D. S., Apoptosis of T lymphocytes invading glioblastomas multiforme: A possible tumor defense mechanism. J. Neurosurg. 2002. 96: 580-584.
44. Hollenbaugh, J. A. and Dutton, R. W., IFN-gamma regulates donor CD8 T cell expansion, migration, and leads to apoptosis of cells of a solid tumor. J. Immunol. 2006. 177: 3004-3011.
45. Jonuleit, H., Schmitt, E., Schuler, G., Knop, J. and Enk, A. H., Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 2000. 192: 1213-1222.
46. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K. and Flavell, R. A., Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 2006. 24: 99-146.
47. Fakhrai, H., Dorigo, O., Shawler, D. L., Lin, H., Mercola, D., Black, K. L., Royston, I. and Sobol, R. E., Eradication of established intracranial rat gliomas by transforming growth factor beta antisense gene therapy. Proc. Natl. Acad. Sci. USA 1996. 93: 2909-2914.
48. Fontana, A., Frei, K., Bodmer, S., Hofer, E., Schreier, M. H., Palladino,M. A., Jr. and Zinkernagel, R. M., Transforming growth factor-beta inhibits the generation of cytotoxic T cells in virus-infected mice. J. Immunol. 1989. 143: 3230-3234.
49. Nagashima, G., Suzuki, R., Asai, J. and Fujimoto, T., Immunohistochemical analysis of reactive astrocytes around glioblastoma: an immunohistochemical study of postmortem glioblastoma cases. Clin. Neurol. Neurosurg. 2002. 104: 125-131.
50. Liu, Y., Teige, I., Birnir, B. and Issazadeh-Navikas, S., Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat. Med. 2006. 12: 518-525.