Transforming growth factor-β-mediated signaling in T lymphocytes impacts on prostate-specific immunity and early prostate tumor progression

Laboratory Investigation

Volumn 89, Issue 2, 2009, Pages 142-151

  Diener, Kerrilyn R ^a,b   Woods, Anthony E ^b   Manavis, Jim ^a,c   Brown, Michael P ^a,d,e   Hayball, John D ^a,b,e  

^a HANSON INSTITUTE   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c SA Pathology ^*  (Australia)

^d ROYAL ADELAIDE HOSPITAL   (Australia)

^e UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Adoptive transfer; CD4 dnTGFRII; OT IT cells; Prostate cancer

Indexed keywords

GAMMA INTERFERON; OVALBUMIN; PROSTATE SPECIFIC ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; IMMUNOSURVEILLANCE; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE; PROSTATE TUMOR; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSGENICS; TUMOR GROWTH; TUMOR IMMUNITY;

ADENOCARCINOMA; ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNOENZYME TECHNIQUES; LYMPH NODES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 59049090704     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2008.123     Document Type: Article

References (46)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-130.
2. Basler M, Groettrup M. Advances in prostate cancer immunotherapies. Drugs Aging 2007;24:197-221.
3. Vieweg J, Dannull J. Technology insight: vaccine therapy for prostate cancer. Nat Clin Pract Urol 2005;2:44-51.
4. Patel PH, Kockler DR. Sipuleucel-T: a vaccine for metastatic, asymptomatic, androgen-independent prostate cancer. Ann Pharmacother 2008;42:91-98.
5. Small EJ, Schellhammer PF, Higano CS, et al. Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J Clin Oncol 2006;24:3089-3094.
6. Kiessling R, Wasserman K, Horiguchi S, et al. Tumor-induced immune dysfunction. Cancer Immunol Immunother 1999;48:353-362.
7. Pawelec G. Tumour escape: antitumour effectors too much of a good thing? Cancer Immunol Immunother 2004;53:262-274.
8. Ahmad M, Rees RC, Ali SA. Escape from immunotherapy: possible mechanisms that influence tumor regression/progression. Cancer Immunol Immunother 2004;53:844-854.
9. Lees JR, Charbonneau B, Hayball JD, et al. T-cell recognition of a prostate specific antigen is not sufficient to induce prostate tissue destruction. Prostate 2006;66:578-590.
10. Anderson MJ, Shafer-Weaver K, Greenberg NM, et al. Tolerization of tumor-specific T cells despite efficient initial priming in a primary murine model of prostate cancer. J Immunol 2007;178:1268-1276.
11. Isaacs JT. Antagonistic effect of androgen on prostatic cell death. Prostate 1984;5:545-557.
12. Danielpour D. Transdifferentiation of NRP-152 rat prostatic basal epithelial cells toward a luminal phenotype: regulation by glucocorticoid, insulin-like growth factor-I and transforming growth factor-beta. J Cell Sci 1999;112(Part 2):169-179.
13. Lee C, Sintich SM, Mathews EP, et al. Transforming growth factor-beta in benign and malignant prostate. Prostate 1999;39:285-290.
14. Shull MM, Ormsby I, Kier AB, et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992;359:693-699.
15. Kulkarni AB, Huh CG, Becker D, et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 1993;90:770-774.
16. Li MO, Wan YY, Sanjabi S, et al. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 2006;24:99-146.
17. Derynck R. TGF-beta-receptor-mediated signaling. Trends Biochem Sci 1994;19:548-553.
18. Salm SN, Burger PE, Coetzee S, et al. TGF-beta maintains dormancy of prostatic stem cells in the proximal region of ducts. J Cell Biol 2005;170:81-90.
19. Lee HM, Timme TL, Thompson TC. Resistance to lysis by cytotoxic T cells: a dominant effect in metastatic mouse prostate cancer cells. Cancer Res 2000;60:1927-1933.
20. Cardillo MR, Petrangeli E, Perracchio L, et al. Transforming growth factor-beta expression in prostate neoplasia. Anal Quant Cytol Histol 2000;22:1-10.
21. Stravodimos K, Constantinides C, Manousakas T, et al. Immunohistochemical expression of transforming growth factor beta 1 and nm-23 H1 antioncogene in prostate cancer: divergent correlation with clinicopathological parameters. Anticancer Res 2000;20:3823-3828.
22. Shariat SF, Kattan MW, Traxel E, et al. Association of pre- and postoperative plasma levels of transforming growth factor beta(1) and interleukin 6 and its soluble receptor with prostate cancer progression. Clin Cancer Res 2004;10:1992-1999.
23. Steiner MS, Barrack ER. Transforming growth factor-beta 1 overproduction in prostate cancer: effects on growth in vivo and in vitro. Mol Endocrinol 1992;6:15-25.
24. Wikstrom P, Stattin P, Franck-Lissbrant I, et al. Transforming growth factor beta1 is associated with angiogenesis, metastasis, and poor clinical outcome in prostate cancer. Prostate 1998;37:19-29.
25. Wikstrom P, Damber J, Bergh A. Role of transforming growth factor-beta1 in prostate cancer. Microsc Res Tech 2001;52:411-419.
26. Kim IY, Ahn HJ, Lang S, et al. Loss of expression of transforming growth factor-beta receptors is associated with poor prognosis in prostate cancer patients. Clin Cancer Res 1998;4:1625-1630.
27. Kim WS, Park C, Jung YS, et al. Reduced transforming growth factor-beta type II receptor (TGF-beta RII) expression in adenocarcinoma of the lung. Anticancer Res 1999;19:301-306.
28. Inge TH, Hoover SK, Susskind BM, et al. Inhibition of tumor-specific cytotoxic T-lymphocyte responses by transforming growth factor beta 1. Cancer Res 1992;52:1386-1392.
29. Matthews E, Yang T, Janulis L, et al. Down-regulation of TGF-beta1 production restores immunogenicity in prostate cancer cells. Br J Cancer 2000;83:519-525.
30. Lees JR, Charbonneau B, Swanson AK, et al. Deletion is neither sufficient nor necessary for the induction of peripheral tolerance in mature CD8+ T cells. Immunology 2006;117:248-261.
31. Hogquist KA, Jameson SC, Heath WR, et al. T cell receptor antagonist peptides induce positive selection. Cell 1994;76:17-27.
32. Greenberg NM, DeMayo F, Finegold MJ, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 1995;92:3439-3443.
33. Gorelik L, Flavell RA. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 2000;12:171-181.
34. Lyons AB, Parish CR. Determination of lymphocyte division by flow cytometry. J Immunol Methods 1994;171:131-137.
35. Diener KR, Moldenhauer LM, Lyons AB, et al. Human Flt-3-ligand-mobilized dendritic cells require additional activation to drive effective immune responses. Exp Hematol 2008;36:51-60.
36. Gingrich JR, Barrios RJ, Foster BA, et al. Pathologic progression of autochthonous prostate cancer in the TRAMP model. Prostate Cancer Prostatic Dis 1999;2:70-75.
37. Hurwitz AA, Foster BA, Kwon ED, et al. Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cancer Res 2000;60:2444-2448.
38. Gojova A, Brun V, Esposito B, et al. Specific abrogation of transforming growth factor-beta signaling in T cells alters atherosclerotic lesion size and composition in mice. Blood 2003;102:4052-4058.
39. Zhang Q, Jang TL, Yang X, et al. Infiltration of tumor-reactive transforming growth factor-beta insensitive CD8+ T cells into the tumor parenchyma is associated with apoptosis and rejection of tumor cells. Prostate 2006;66:235-247.
40. Yaswen L, Kulkarni AB, Fredrickson T, et al. Autoimmune manifestations in the transforming growth factor-beta 1 knockout mouse. Blood 1996;87:1439-1445.
41. Lucas PJ, Kim SJ, Melby SJ, et al. Disruption of T cell homeostasis in mice expressing a T cell-specific dominant negative transforming growth factor beta II receptor. J Exp Med 2000;191:1187-1196.
42. Gorelik L, Flavell RA. Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signaling in T cells. Nat Med 2001;7:1118-1122.
43. Shah AH, Tabayoyong WB, Kundu SD, et al. Suppression of tumor metastasis by blockade of transforming growth factor beta signaling in bone marrow cells through a retroviral-mediated gene therapy in mice. Cancer Res 2002;62:7135-7138.
44. Degl'Innocenti E, Grioni M, Boni A, et al. Peripheral T cell tolerance occurs early during spontaneous prostate cancer development and can be rescued by dendritic cell immunization. Eur J Immunol 2005;35:66-75.
45. Mihalyo MA, Hagymasi AT, Slaiby AM, et al. Dendritic cells program non-immunogenic prostate-specific T cell responses beginning at early stages of prostate tumorigenesis. Prostate 2007;67:536-546.
46. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006;6:836-848.