The timing of TGF-β inhibition affects the generation of antigen-specific CD8+ T Cells

BMC Immunology

Volumn 14, Issue 1, 2013, Pages

  Quatromoni, Jon G ^a   Suzuki, Eiji ^a,b   Okusanya, Olugbenga ^a   Judy, Brendan F ^a   Bhojnagarwala, Pratik ^a   Venegas, Ollin ^a   Eruslanov, Evgeniy ^a   Predina, Jarrod D ^a   Albelda, Steven M ^a,b   Singhal, Sunil ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CD8+ Cytotoxic T cell; Immune suppression; Malignant mesothelioma; TGF ; Tumor immunology

Indexed keywords

ADENOVIRUS VECTOR; CD8 ANTIGEN; PROTEIN E7; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SIZE; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CONTROL GROUP; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOSUPPRESSIVE TREATMENT; MALIGNANT MESOTHELIOMA; MOUSE; NONHUMAN; SEVERE COMBINED IMMUNODEFICIENCY; TUMOR GROWTH;

ANIMALS; ANTIGENS, CD86; CD8-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EPITOPES; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN G; LYMPH NODES; LYMPHOCYTE DEPLETION; MICE; NEOPLASM METASTASIS; NEOPLASMS; PAPILLOMAVIRUS E7 PROTEINS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SOLUBILITY; T-LYMPHOCYTES, CYTOTOXIC; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84880182145     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-14-30     Document Type: Article

References (50)

1. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol 1998, 16:137-161. 10.1146/annurev.immunol.16.1.137, 9597127.
2. Achyut BR, Yang L. Transforming growth factor-beta in the gastrointestinal and hepatic tumor microenvironment. Gastroenterology 2011, 141:1167-1178. 10.1053/j.gastro.2011.07.048, 21839702.
3. Kubiczkova L, Sedlarikova L, Hajek R, Sevcikova S. TGF-beta - an excellent servant but a bad master. J Transl Med 2012, 10:183-5876. 10-183, 10.1186/1479-5876-10-183, 3494542, 22943793.
4. de Visser KE, Kast WM. Effects of TGF-beta on the immune system: implications for cancer immunotherapy. Leukemia 1999, 13:1188-1199. 10.1038/sj.leu.2401477, 10450746.
5. Yang L. TGFbeta, a potent regulator of tumor microenvironment and host immune response, implication for therapy. Curr Mol Med 2010, 10:374-380. 10.2174/156652410791317039, 20455854.
6. Wrzesinski SH, Wan YY, Flavell RA. Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin Cancer Res 2007, 13:5262-5270. 10.1158/1078-0432.CCR-07-1157, 17875754.
7. Yang L, Pang Y, Moses HL. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 2010, 31:220-227. 10.1016/j.it.2010.04.002, 2891151, 20538542.
8. Gorelik L, Flavell RA. Transforming growth factor-beta in T-cell biology. Nat Rev Immunol 2002, 2:46-53. 10.1038/nri704, 11905837.
9. Somasundaram R, Jacob L, Swoboda R, Caputo L, Song H, Basak S, Monos D, Peritt D, Marincola F, Cai D, Birebent B, Bloome E, Kim J, Berencsi K, Mastrangelo M, Herlyn D. Inhibition of cytolytic T lymphocyte proliferation by autologous CD4+/CD25+ regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor-beta. Cancer Res 2002, 62:5267-5272.
10. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 2001, 194:629-644. 10.1084/jem.194.5.629, 2195935, 11535631.
11. Carrier Y, Yuan J, Kuchroo VK, Weiner HL. Th3 cells in peripheral tolerance. II. TGF-beta-transgenic Th3 cells rescue IL-2-deficient mice from autoimmunity. J Immunol 2007, 178:172-178.
12. Fahlen L, Read S, Gorelik L, Hurst SD, Coffman RL, Flavell RA, Powrie F. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J Exp Med 2005, 201:737-746. 10.1084/jem.20040685, 2212836, 15753207.
13. Rook AH, Kehrl JH, Wakefield LM, Roberts AB, Sporn MB, Burlington DB, Lane HC, Fauci AS. Effects of transforming growth factor beta on the functions of natural killer cells: depressed cytolytic activity and blunting of interferon responsiveness. J Immunol 1986, 136:3916-3920.
14. Tian F, Wang L, Qin W, Wang F, Song B, Li Y, Wen W, Zhang Z, Zhu K, Zhang Q, Lee C, Zhong W, Guo Y, Wang H. Vaccination with transforming growth factor-beta insensitive dendritic cells suppresses pulmonary metastases of renal carcinoma in mice. Cancer Lett 2008, 271:333-341. 10.1016/j.canlet.2008.06.025, 18675506.
15. Ito M, Minamiya Y, Kawai H, Saito S, Saito H, Nakagawa T, Imai K, Hirokawa M, Ogawa J. Tumor-derived TGFbeta-1 induces dendritic cell apoptosis in the sentinel lymph node. J Immunol 2006, 176:5637-5643.
16. Kobie JJ, Wu RS, Kurt RA, Lou S, Adelman MK, Whitesell LJ, Ramanathapuram LV, Arteaga CL, Akporiaye ET. Transforming growth factor beta inhibits the antigen-presenting functions and antitumor activity of dendritic cell vaccines. Cancer Res 2003, 63:1860-1864.
17. Dumont N, Arteaga CL. Targeting the TGF beta signaling network in human neoplasia. Cancer Cell 2003, 3:531-536. 10.1016/S1535-6108(03)00135-1, 12842082.
18. Wang L, Wen W, Yuan J, Helfand B, Li Y, Shi C, Tian F, Zheng J, Wang F, Chen L, Liang L, Zhou L, Lee C, Chen Z, Guo Y, Wang H, Zhang Q, Qin W. Immunotherapy for human renal cell carcinoma by adoptive transfer of autologous transforming growth factor beta-insensitive CD8+ T cells. Clin Cancer Res 2010, 16:164-173. 10.1158/1078-0432.CCR-09-1758, 20028741.
19. Quatromoni JG, Wang Y, Vo DD, Morris LF, Jazirehi AR, McBride W, Chatila T, Koya RC, Economou JS. T cell receptor (TCR)-transgenic CD8 lymphocytes rendered insensitive to transforming growth factor beta (TGFbeta) signaling mediate superior tumor regression in an animal model of adoptive cell therapy. J Transl Med 2012, 10:127-5876. 10-127, 10.1186/1479-5876-10-127, 3507675, 22713761.
20. Maggard M, Meng L, Ke B, Allen R, Devgan L, Imagawa DK. Antisense TGF-beta2 immunotherapy for hepatocellular carcinoma: treatment in a rat tumor model. Ann Surg Oncol 2001, 8:32-37.
21. Witham TF, Villa L, Yang T, Pollack IF, Okada H, Robbins PD, Chambers WH. Expression of a soluble transforming growth factor-beta (TGFbeta) receptor reduces tumorigenicity by regulating natural killer (NK) cell activity against 9L gliosarcoma in vivo. J Neurooncol 2003, 64:63-69.
22. Suzuki E, Kapoor V, Cheung HK, Ling LE, DeLong PA, Kaiser LR, Albelda SM. Soluble type II transforming growth factor-beta receptor inhibits established murine malignant mesothelioma tumor growth by augmenting host antitumor immunity. Clin Cancer Res 2004, 10:5907-5918. 10.1158/1078-0432.CCR-03-0611, 15355924.
23. Davis MR, Manning LS, Whitaker D, Garlepp MJ, Robinson BW. Establishment of a murine model of malignant mesothelioma. Int J Cancer 1992, 52:881-886. 10.1002/ijc.2910520609, 1459729.
24. Odaka M, Sterman DH, Wiewrodt R, Zhang Y, Kiefer M, Amin KM, Gao GP, Wilson JM, Barsoum J, Kaiser LR, Albelda SM. Eradication of intraperitoneal and distant tumor by adenovirus-mediated interferon-beta gene therapy is attributable to induction of systemic immunity. Cancer Res 2001, 61:6201-6212.
25. Fitzpatrick DR, Bielefeldt-Ohmann H, Himbeck RP, Jarnicki AG, Marzo AL, Robinson BW. Transforming growth factor-beta: antisense RNA-mediated inhibition affects anchorage-independent growth, tumorigenicity and tumor-infiltrating T-cells in malignant mesothelioma. Growth Factors 1994, 11:29-44. 10.3109/08977199409015049, 7833058.
26. Lin KY, Guarnieri FG, Staveley-O'Carroll KF, Levitsky HI, August JT, Pardoll DM, Wu TC. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 1996, 56:21-26.
27. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 1994, 216:276-284. 10.1006/abio.1994.1042, 8179182.
28. Zheng H, Wang J, Koteliansky VE, Gotwals PJ, Hauer-Jensen M. Recombinant soluble transforming growth factor beta type II receptor ameliorates radiation enteropathy in mice. Gastroenterology 2000, 119:1286-1296. 10.1053/gast.2000.19282, 11054386.
29. Smith JD, Bryant SR, Couper LL, Vary CP, Gotwals PJ, Koteliansky VE, Lindner V. Soluble transforming growth factor-beta type II receptor inhibits negative remodeling, fibroblast transdifferentiation, and intimal lesion formation but not endothelial growth. Circ Res 1999, 84:1212-1222. 10.1161/01.RES.84.10.1212, 10347096.
30. George J, Roulot D, Koteliansky VE, Bissell DM. In vivo inhibition of rat stellate cell activation by soluble transforming growth factor beta type II receptor: a potential new therapy for hepatic fibrosis. Proc Natl Acad Sci USA 1999, 96:12719-12724. 10.1073/pnas.96.22.12719, 23066, 10535989.
31. Lammerts E, Roswall P, Sundberg C, Gotwals PJ, Koteliansky VE, Reed RK, Heldin NE, Rubin K. Interference with TGF-beta1 and -beta3 in tumor stroma lowers tumor interstitial fluid pressure independently of growth in experimental carcinoma. Int J Cancer 2002, 102:453-462. 10.1002/ijc.10722, 12432546.
32. He Z, Wlazlo AP, Kowalczyk DW, Cheng J, Xiang ZQ, Giles-Davis W, Ertl HC. Viral recombinant vaccines to the E6 and E7 antigens of HPV-16. Virology 2000, 270:146-161. 10.1006/viro.2000.0271, 10772987.
33. Kowalczyk DW, Wlazlo AP, Giles-Davis W, Kammer AR, Mukhopadhyay S, Ertl HC. Vaccine-induced CD8+ T cells eliminate tumors by a two-staged attack. Cancer Gene Ther 2003, 10:870-878. 10.1038/sj.cgt.7700653, 14712313.
34. Lamikanra A, Pan ZK, Isaacs SN, Wu TC, Paterson Y. Regression of established human papillomavirus type 16 (HPV-16) immortalized tumors in vivo by vaccinia viruses expressing different forms of HPV-16 E7 correlates with enhanced CD8(+) T-cell responses that home to the tumor site. J Virol 2001, 75:9654-9664. 10.1128/JVI.75.20.9654-9664.2001, 114536, 11559797.
35. Winn HJ. In vivo methods for the assessment of antibody-mediated tumor immunity. Natl Cancer Inst Monogr 1972, 35:13-18.
36. DeLong P, Tanaka T, Kruklitis R, Henry AC, Kapoor V, Kaiser LR, Sterman DH, Albelda SM. Use of cyclooxygenase-2 inhibition to enhance the efficacy of immunotherapy. Cancer Res 2003, 63:7845-7852.
37. Wu SP, Sun LZ, Willson JK, Humphrey L, Kerbel R, Brattain MG. Repression of autocrine transforming growth factor beta 1 and beta 2 in quiescent CBS colon carcinoma cells leads to progression of tumorigenic properties. Cell Growth Differ 1993, 4:115-123.
38. Wu SP, Theodorescu D, Kerbel RS, Willson JK, Mulder KM, Humphrey LE, Brattain MG. TGF-beta 1 is an autocrine-negative growth regulator of human colon carcinoma FET cells in vivo as revealed by transfection of an antisense expression vector. J Cell Biol 1992, 116:187-196. 10.1083/jcb.116.1.187, 2289262, 1730743.
39. Kruklitis RJ, Singhal S, Delong P, Kapoor V, Sterman DH, Kaiser LR, Albelda SM. Immuno-gene therapy with interferon-beta before surgical debulking delays recurrence and improves survival in a murine model of malignant mesothelioma. J Thorac Cardiovasc Surg 2004, 127:123-130. 10.1016/j.jtcvs.2003.08.034, 14752422.
40. Cerwenka A, Swain SL. TGF-beta1: immunosuppressant and viability factor for T lymphocytes. Microbes Infect 1999, 1:1291-1296. 10.1016/S1286-4579(99)00255-5, 10611757.
41. Strobl H, Knapp W. TGF-beta1 regulation of dendritic cells. Microbes Infect 1999, 1:1283-1290. 10.1016/S1286-4579(99)00256-7, 10611756.
42. Cerwenka A, Kovar H, Majdic O, Holter W. Fas- and activation-induced apoptosis are reduced in human T cells preactivated in the presence of TGF-beta 1. J Immunol 1996, 156:459-464.
43. Zhang X, Giangreco L, Broome HE, Dargan CM, Swain SL. Control of CD4 effector fate: transforming growth factor beta 1 and interleukin 2 synergize to prevent apoptosis and promote effector expansion. J Exp Med 1995, 182:699-709. 10.1084/jem.182.3.699, 2192155, 7650478.
44. Ayoub IA, Yang TJ. Growth regulatory effects of transforming growth factor-beta 1 and interleukin-2 on IL-2 dependent CD4+T lymphoblastoid cell line. Immunol Invest 1996, 25:129-151. 10.3109/08820139609059297, 8675229.
45. Lee HM, Rich S. Differential activation of CD8+ T cells by transforming growth factor-beta 1. J Immunol 1993, 151:668-677.
46. Sato K, Kawasaki H, Nagayama H, Enomoto M, Morimoto C, Tadokoro K, Juji T, Takahashi TA. TGF-beta 1 reciprocally controls chemotaxis of human peripheral blood monocyte-derived dendritic cells via chemokine receptors. J Immunol 2000, 164:2285-2295.
47. Tanaka T, Delong PA, Amin K, Henry A, Kruklitis R, Kapoor V, Kaiser LR, Albelda SM. Treatment of lung cancer using clinically relevant oral doses of the cyclooxygenase-2 inhibitor rofecoxib: potential value as adjuvant therapy after surgery. Ann Surg 2005, 241:168-178. 1356860, 15622005.
48. Bottinger EP, Jakubczak JL, Haines DC, Bagnall K, Wakefield LM. Transgenic mice overexpressing a dominant-negative mutant type II transforming growth factor beta receptor show enhanced tumorigenesis in the mammary gland and lung in response to the carcinogen 7,12-dimethylbenz-[a]-anthracene. Cancer Res 1997, 57:5564-5570.
49. Akhurst RJ. TGF-beta antagonists: why suppress a tumor suppressor?. J Clin Invest 2002, 109:1533-1536. 151022, 12070299.
50. Amendt C, Schirmacher P, Weber H, Blessing M. Expression of a dominant negative type II TGF-beta receptor in mouse skin results in an increase in carcinoma incidence and an acceleration of carcinoma development. Oncogene 1998, 17:25-34. 10.1038/sj.onc.1202161, 9671311.