Thymus-derived rather than tumor-induced regulatory T cells predominate in brain tumors

Neuro-Oncology

Volumn 13, Issue 12, 2011, Pages 1308-1323

  Wainwright, Derek A ^a   Sengupta, Sadhak ^a   Han, Yu ^a   Lesniak, Maciej S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Brain cancer; CD25; CD4; FoxP3; GBM; Glioblastoma; Glioma; RasB8; Regulatory T cells; Tregs.

Indexed keywords

CD103 ANTIGEN; CD45RB ANTIGEN; KI 67 ANTIGEN; L SELECTIN; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GLIOBLASTOMA; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; THYMECTOMY; THYMUS; TRANSGENIC MOUSE; TUMOR MICROENVIRONMENT;

ANIMALS; BRAIN NEOPLASMS; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SURVIVAL RATE; T-LYMPHOCYTES, REGULATORY; THYMECTOMY; THYMUS GLAND; TUMOR MARKERS, BIOLOGICAL;

EID: 84863393191     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nor134     Document Type: Article

References (44)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987-996. (Pubitemid 40349501)
2. Pellegatta S, Poliani PL, Stucchi E, et al. Intra-tumoral dendritic cells increase efficacy of peripheral vaccination by modulation of glioma microenvironment. Neuro Oncol. 2010;12:377-388.
3. Curtin JF, Liu N, Candolfi M, et al. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med. 2009;6:e10.
4. El Andaloussi A, Han Y, Lesniak MS. Prolongation of survival following depletion of CD4+CD25+ regulatory T cells in mice with experimental brain tumors. J Neurosurg. 2006;105:430-437. (Pubitemid 44358755)
5. Yu JS, Burwick JA, Dranoff G, et al. Gene therapy for metastatic brain tumors by vaccination with granulocyte-macrophage colony-stimulating factor-transduced tumor cells. Hum Gene Ther. 1997;8:1065-1072. (Pubitemid 27308204)
6. El Andaloussi A, Lesniak MS. An increase in CD4+CD25+FOXP3+ regulatory T cells in tumor-infiltrating lymphocytes of human glioblastoma multiforme. Neuro Oncol. 2006;8:234-243. (Pubitemid 46542648)
7. El Andaloussi A, Lesniak MS. CD4+ CD25+ FoxP3+ T-cell infiltration and heme oxygenase-1 expression correlate with tumor grade in human gliomas. J Neurooncol. 2007;83:145-152. (Pubitemid 46784987)
8. Heimberger AB, Abou-Ghazal M, Reina-Ortiz C, et al. Incidence and prognostic impact of FoxP3+ regulatory T cells in human gliomas. Clin Cancer Res. 2008;14:5166-5172.
9. Fecci PE, Mitchell DA, Whitesides JF, et al. Increased regulatory T-cell fraction amidst a diminished CD4 compartment explains cellular immune defects in patients with malignant glioma. Cancer Res. 2006;66:3294-3302.
10. Curtin JF, Candolfi M, Fakhouri TM, et al. Treg depletion inhibits efficacy of cancer immunotherapy: Implications for clinical trials. PLoS One. 2008;3:e1983.
11. Shimizu J, Yamazaki S, Takahashi T, et al. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol. 2002;3:135-142. (Pubitemid 34141443)
12. Read S, Malmström V, 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. 2000;192:295-302. (Pubitemid 30470312)
13. Zheng SG, Wang JH, Gray JD, et al. Natural and induced CD4+CD25+ cells educate CD4+CD25- cells to develop suppressive activity: The role of IL-2, TGF-beta, and IL-10. J Immunol. 2004;172:5213-5221. (Pubitemid 38542018)
14. Hsieh CS, Zheng Y, Liang Y, et al. An intersection between the selfreactive regulatory and nonregulatory T cell receptor repertoires. Nat Immunol. 2006;7:401-410.
15. Wong J, Obst R, Correia-Neves M, et al. Adaptation of TCR repertoires to self-peptides in regulatory and nonregulatory CD4+ T cells. J Immunol. 2007;178:7032-7041. (Pubitemid 46847429)
16. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057-1061. (Pubitemid 36222930)
17. Jordan MS, Boesteanu A, Reed AJ, et al. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol. 2001;2:301-306. (Pubitemid 33706340)
18. Liu VC,Wong LY, Jang T, et al. Tumor evasion of the immune system by converting CD4+CD25- T cells into CD4+CD25+ T regulatory cells: Role of tumor-derived TGF-beta. J Immunol. 2007;178:2883-2892. (Pubitemid 46333166)
19. Kretschmer K, Apostolou I, Hawiger D, et al. Inducing and expanding regulatory T cell populations by foreign antigen. Nat Immunol. 2005;6:1219-1227. (Pubitemid 43045633)
20. Zhou G, Levitsky HI. Natural regulatory T cells and de novo-induced regulatory T cells contribute independently to tumor-specific tolerance. J Immunol. 2007;178:2155-2162. (Pubitemid 46233413)
21. Thornton AM, Korty PE, Tran DQ, et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J Immunol. 2010;184:3433-3441.
22. Ding H, Roncari L, Shannon P, et al. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res. 2001;61:3826-3836. (Pubitemid 32695000)
23. Malizia G, Trejdosiewicz LK, Wood GM, et al. The microenvironment of coeliac disease: T cell phenotypes and expression of the T2 'T blast' antigen by small bowel lymphocytes. Clin Exp Immunol. 1985;60:437-446. (Pubitemid 15099895)
24. McHugh RS, Whitters MJ, Piccirillo CA, et al. CD4+CD25+ immunoregulatory T cells: Gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity. 2002;16:311-323. (Pubitemid 34211969)
25. Rao PE, Petrone AL, Ponath PD. Differentiation and expansion of T cells with regulatory function from human peripheral lymphocytes by stimulation in the presence of TGF-b. J Immunol. 2005;174:1446-1455.
26. Chen W, Jin W, Hardegen N, et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875-1886. (Pubitemid 38032120)
27. Valzasina B, Piconese S, Guiducci C, et al. Tumor-induced expansion of regulatory T cells by conversion of CD4+CD25 lymphocytes is thymus and proliferation independent. Cancer Res. 2006;66: 4488-4495.
28. Moo-Young TA, Larson JW, Belt BA, et al. Tumor-derived TGF-beta mediates conversion of CD4+Foxp3+ regulatory T cells in a murine model of pancreas cancer. J Immunother. 2009;32:12-21.
29. Hindley JP, Ferreira C, Jones E, et al. Analysis of the T-cell receptor repertoires of tumor-infiltrating conventional and regulatory T cells reveals no evidence for conversion in carcinogen-induced tumors. Cancer Res. 2011;71:736-746.
30. Weller RO, Djuanda E, Yow HY, et al. Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol. 2009;117:1-14.
31. Prins RM, Graf MR, Merchant RE, et al. Thymic function and output of recent thymic emigrant T cells during intracranial glioma progression. J Neurooncol. 2003;64:45-54. (Pubitemid 36992459)
32. Bulloch K, Moore RY. Innervation of the thymus gland by brain stem and spinal cord in mouse and rat. Am J Anat. 1981;162:157-166. (Pubitemid 12231836)
33. Shannon P, Sabha N, Lau N, et al. Pathological and molecular progression of astrocytomas in a GFAP:12 V-Ha-Ras mouse astrocytoma model. Am J Pathol. 2005;167:859-867. (Pubitemid 41216368)
34. Yamasaki K, Horiguchi S, Kurosaki M, et al. Induction of NKT cellspecific immune responses in cancer tissues after NKT cell-targeted adoptive immunotherapy. Clin Immunol. 2011;138:255-265.
35. Schietinger A, Philip M, Liu RB, et al. Bystander killing of cancer requires the cooperation of CD4(+) and CD8(+) T cells during the effector phase. J Exp Med. 2010;207:2469-2477.
36. Kohm AP, McMahon JS, Podojil JR, et al. Cutting edge: Anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells. J Immunol. 2006;176:3301-3305. (Pubitemid 43363974)
37. Barron L, Dooms H, Hoyer KK, et al. Cutting edge: Mechanisms of IL-2-dependent maintenance of functional regulatory T cells. J Immunol. 2010;185:6426-6430.
38. Jiang Q, Su H, Knudsen G, et al. Delayed functional maturation of natural regulatory T cells in the medulla of postnatal thymus: Role of TSLP. BMC Immunol. 2006;7:6.
39. Mazzucchelli R, Hixon JA, Spolski R, et al. Development of regulatory T cells requires IL-7Ralpha stimulation by IL-7 or TSLP. Blood. 2008;112:3283-3292.
40. Bruinsma M, van Soest PL, Leenen PJ, et al. Keratinocyte growth factor induces expansion of murine peripheral CD4+Foxp3+ regulatory T cells and increases their thymic output. J Immunol. 2007;179:7424-7430.
41. Rubtsov YP, Niec RE, Josefowicz S, et al. Stability of the regulatory T cell lineage in vivo. Science. 2010;329:1667-1671.
42. Gobert M, Treilleux I, Bendriss-Vermare N, et al. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res. 2009;69:2000-2009.
43. Lutsiak ME, Tagaya Y, Adams AJ, et al. Tumor-induced impairment of TCR signaling results in compromised functionality of tumor-infiltrating regulatory T cells. J Immunol. 2008;180:5871-5878.
44. Wainwright DA, Sengupta S, Han Y, et al. The presence of IL-17A and T helper 17 cells in experimental mouse brain tumors and human glioma. PLoS One. 2010;5:e15390.