CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells

Paul A Antony ¹, Ciriaco A Piccirillo , Akgül Akpinarli , Steven E Finkelstein , Paul J Speiss , Deborah R Surman , Douglas C Palmer , Chi-Chao Chan , Christopher A Klebanoff , Willem W Overwijk , Steven A Rosenberg , Nicholas P Restifo

Affiliations

¹ Division of Surgery, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA. Paul.Antony@nih.gov

PMID: 15728465
61 References
312 citations

Abstract

CD4(+) T cells control the effector function, memory, and maintenance of CD8(+) T cells. Paradoxically, we found that absence of CD4(+) T cells enhanced adoptive immunotherapy of cancer when using CD8(+) T cells directed against a persisting tumor/self-Ag. However, adoptive transfer of CD4(+)CD25(-) Th cells (Th cells) with tumor/self-reactive CD8(+) T cells and vaccination into CD4(+) T cell-deficient hosts induced autoimmunity and regression of established melanoma. Transfer of CD4(+) T cells that contained a mixture of Th and CD4(+)CD25(+) T regulatory cells (T(reg) cells) or T(reg) cells alone prevented effective adoptive immunotherapy. Maintenance of CD8(+) T cell numbers and function was dependent on Th cells that were capable of IL-2 production because therapy failed when Th cells were derived from IL-2(-/-) mice. These findings reveal that Th cells can help break tolerance to a persisting self-Ag and treat established tumors through an IL-2-dependent mechanism, but requires simultaneous absence of naturally occurring T(reg) cells to be effective.

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Tumor-specific Th17-polarized cells eradicate large established melanoma. Pawel Muranski, Andrea Boni, +14 authors, Nicholas P Restifo. less Blood, 2008 Mar 21; 112(2). PMID: 18354038 Free PMC article. Highly Cited.
Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Steven A Rosenberg, Nicholas P Restifo, +2 authors, James C Yang, Richard A Morgan, Mark E Dudley. less Nat Rev Cancer, 2008 Mar 21; 8(4). PMID: 18354418 Free PMC article. Highly Cited. Review.
The allogeneic effect revisited: exogenous help for endogenous, tumor-specific T cells. Heather J Symons, Moshe Y Levy, +6 authors, Ephraim J Fuchs. less Biol Blood Marrow Transplant, 2008 Apr 16; 14(5). PMID: 18410892 Free PMC article.
Epigenetics in human autoimmunity. Epigenetics in autoimmunity - DNA methylation in systemic lupus erythematosus and beyond. Faith M Strickland, Bruce C Richardson. Autoimmunity, 2008 Apr 25; 41(4). PMID: 18432408 Free PMC article. Review.
Adoptive cell therapy for patients with melanoma, using tumor-infiltrating lymphocytes genetically engineered to secrete interleukin-2. Bianca Heemskerk, Ke Liu, +9 authors, Steven A Rosenberg. less Hum Gene Ther, 2008 May 01; 19(5). PMID: 18444786 Free PMC article.
Partial reduction of human FOXP3+ CD4 T cells in vivo after CD25-directed recombinant immunotoxin administration. Daniel J Powell, Peter Attia, +3 authors, Steven A Rosenberg. less J Immunother, 2008 May 16; 31(2). PMID: 18481388 Free PMC article.
Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Brian G Till, Michael C Jensen, +13 authors, Oliver W Press. less Blood, 2008 May 30; 112(6). PMID: 18509084 Free PMC article. Highly Cited.
CTL-promoting effects of CD40 stimulation outweigh B cell-stimulatory effects resulting in B cell elimination and disease improvement in a murine model of lupus. Roman Puliaev, Irina Puliaeva, +4 authors, Charles S Via. less J Immunol, 2008 Jun 21; 181(1). PMID: 18566369 Free PMC article.
Defective MHC class II presentation by dendritic cells limits CD4 T cell help for antitumor CD8 T cell responses. Michael Y Gerner, Kerry A Casey, Matthew F Mescher. J Immunol, 2008 Jun 21; 181(1). PMID: 18566380 Free PMC article.
Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. Sergio A Quezada, Karl S Peggs, +3 authors, James P Allison. less J Exp Med, 2008 Aug 30; 205(9). PMID: 18725522 Free PMC article. Highly Cited.
Potent tumor-specific protection ignited by adoptively transferred CD4+ T cells. Zuqiang Liu, Hae S Noh, +3 authors, Janet Chen, Jin H Kim, Louis D Falo, Zhaoyang You. less J Immunol, 2008 Sep 05; 181(6). PMID: 18768895 Free PMC article.
Characterizing and optimizing immune responses to leukaemia antigens after allogeneic stem cell transplantation. Katayoun Rezvani, A John Barrett. Best Pract Res Clin Haematol, 2008 Sep 16; 21(3). PMID: 18790448 Free PMC article. Review.
Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. Mark E Dudley, James C Yang, +17 authors, Steven A Rosenberg. less J Clin Oncol, 2008 Sep 24; 26(32). PMID: 18809613 Free PMC article. Highly Cited.
FOXP3 expression accurately defines the population of intratumoral regulatory T cells that selectively accumulate in metastatic melanoma lesions. Mojgan Ahmadzadeh, Aloisio Felipe-Silva, +4 authors, Steven A Rosenberg. less Blood, 2008 Sep 30; 112(13). PMID: 18820132 Free PMC article.
Adoptive immunotherapy: good habits instilled at youth have long-term benefits. Chrystal M Paulos, Megan M Suhoski, +10 authors, Carl H June. less Immunol Res, 2008 Oct 25; 42(1-3). PMID: 18949448 Free PMC article. Review.
Imatinib mesylate inhibits CD4+ CD25+ regulatory T cell activity and enhances active immunotherapy against BCR-ABL- tumors. Nicolas Larmonier, Nona Janikashvili, +6 authors, Emmanuel Katsanis. less J Immunol, 2008 Nov 05; 181(10). PMID: 18981115 Free PMC article.
In vitro induction of T cells that are resistant to A2 adenosine receptor-mediated immunosuppression. Akio Ohta, J Kjaergaard, +6 authors, M Sitkovsky. less Br J Pharmacol, 2008 Dec 17; 156(2). PMID: 19076726 Free PMC article.
Regulatory T cells in renal disease. Yuan Min Wang, Min Hu, +6 authors, Stephen I Alexander. less Int J Clin Exp Med, 2008 Dec 17; 1(4). PMID: 19079673 Free PMC article.
Quantitative PET reporter gene imaging of CD8+ T cells specific for a melanoma-expressed self-antigen. Chengyi J Shu, Caius G Radu, +5 authors, Owen N Witte. less Int Immunol, 2008 Dec 25; 21(2). PMID: 19106231 Free PMC article.
Characterization of genetically modified T-cell receptors that recognize the CEA:691-699 peptide in the context of HLA-A2.1 on human colorectal cancer cells. Maria R Parkhurst, Jayne Joo, +4 authors, Steven A Rosenberg. less Clin Cancer Res, 2009 Jan 02; 15(1). PMID: 19118044 Free PMC article.
Depletion of CD4 T cells enhances immunotherapy for neuroblastoma after syngeneic HSCT but compromises development of antitumor immune memory. Weiqing Jing, Jill A Gershan, Bryon D Johnson. Blood, 2009 Feb 03; 113(18). PMID: 19182203 Free PMC article.
Use of tumour-responsive T cells as cancer treatment. Mary L Disis, Helga Bernhard, Elizabeth M Jaffee. Lancet, 2009 Feb 24; 373(9664). PMID: 19231634 Free PMC article. Review.
Antigen processing and MHC-II presentation by dermal and tumor-infiltrating dendritic cells. Michael Y Gerner, Matthew F Mescher. J Immunol, 2009 Feb 24; 182(5). PMID: 19234167 Free PMC article.
Adoptive immunotherapy of cancer using CD4(+) T cells. Pawel Muranski, Nicholas P Restifo. Curr Opin Immunol, 2009 Mar 17; 21(2). PMID: 19285848 Free PMC article. Highly Cited. Review.
Adoptive cell therapy for the treatment of patients with metastatic melanoma. Steven A Rosenberg, Mark E Dudley. Curr Opin Immunol, 2009 Mar 24; 21(2). PMID: 19304471 Free PMC article. Highly Cited. Review.
Tumor regulatory T cells potently abrogate antitumor immunity. Zuqiang Liu, Jin H Kim, Louis D Falo, Zhaoyang You. J Immunol, 2009 May 06; 182(10). PMID: 19414769 Free PMC article.
Increased frequency and suppression by regulatory T cells in patients with acute myelogenous leukemia. Miroslaw J Szczepanski, Marta Szajnik, +6 authors, Michael Boyiadzis. less Clin Cancer Res, 2009 May 07; 15(10). PMID: 19417016 Free PMC article.
Therapeutic immunity by adoptive tumor-primed CD4(+) T-cell transfer in combination with in vivo GITR ligation. Zuqiang Liu, Shenghe Tian, +2 authors, Louis D Falo, Shimon Sakaguchi, Zhaoyang You. less Mol Ther, 2009 May 07; 17(7). PMID: 19417739 Free PMC article.
Radiotherapy combined with intratumoral dendritic cell vaccination enhances the therapeutic efficacy of adoptive T-cell transfer. Seagal Teitz-Tennenbaum, Qiao Li, +4 authors, Alfred E Chang. less J Immunother, 2009 Jun 02; 32(6). PMID: 19483649 Free PMC article.
High-avidity autoreactive CD4+ T cells induce host CTL, overcome T(regs) and mediate tumor destruction. Andrew G Brandmaier, Wolfgang W Leitner, +3 authors, Christopher E Touloukian. less J Immunother, 2009 Jun 30; 32(7). PMID: 19561540 Free PMC article.
The PEPvIII-KLH (CDX-110) vaccine in glioblastoma multiforme patients. Amy B Heimberger, John H Sampson. Expert Opin Biol Ther, 2009 Jul 14; 9(8). PMID: 19591631 Free PMC article. Review.
Immunity to murine prostatic tumors: continuous provision of T-cell help prevents CD8 T-cell tolerance and activates tumor-infiltrating dendritic cells. Kimberly A Shafer-Weaver, Stephanie K Watkins, +5 authors, Arthur A Hurwitz. less Cancer Res, 2009 Jul 23; 69(15). PMID: 19622771 Free PMC article.
Treatment of lymphoma with adoptively transferred T cells. Brian G Till, Oliver W Press. Expert Opin Biol Ther, 2009 Sep 03; 9(11). PMID: 19723016 Free PMC article. Review.
IL-4 suppresses very late antigen-4 expression which is required for therapeutic Th1 T-cell trafficking into tumors. Kotaro Sasaki, Angela D Pardee, +10 authors, Walter J Storkus. less J Immunother, 2009 Sep 16; 32(8). PMID: 19752754 Free PMC article.
Regulatory T cells and immune tolerance to tumors. Xuefang Cao. Immunol Res, 2009 Sep 19; 46(1-3). PMID: 19763889 Review.
Antitumor immunity and cancer stem cells. Tobias Schatton, Markus H Frank. Ann N Y Acad Sci, 2009 Oct 03; 1176. PMID: 19796244 Free PMC article.
Suppressors of cytokine signaling (SOCS) in T cell differentiation, maturation, and function. Douglas C Palmer, Nicholas P Restifo. Trends Immunol, 2009 Nov 03; 30(12). PMID: 19879803 Free PMC article. Review.
Dendritic cell recovery post-lymphodepletion: a potential mechanism for anti-cancer adoptive T cell therapy and vaccination. Mohamed Labib Salem, David J Cole. Cancer Immunol Immunother, 2009 Nov 19; 59(3). PMID: 19921513 Free PMC article. Review.
The role of tregs in glioma-mediated immunosuppression: potential target for intervention. William Humphries, Jun Wei, John H Sampson, Amy B Heimberger. Neurosurg Clin N Am, 2009 Dec 01; 21(1). PMID: 19944972 Free PMC article. Review.
Antitumor effect of mSurvivinThr34→Ala in murine colon carcinoma when administered intravenously. Hong-xia Li, Xin-yu Zhao, +16 authors, Xia Zhao. less Med Oncol, 2009 Dec 02; 27(4). PMID: 19949901
Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. Claudia Wrzesinski, Chrystal M Paulos, +6 authors, Nicholas P Restifo. less J Immunother, 2009 Dec 03; 33(1). PMID: 19952961 Free PMC article. Highly Cited.
Cyclophosphamide induces bone marrow to yield higher numbers of precursor dendritic cells in vitro capable of functional antigen presentation to T cells in vivo. Mohamed L Salem, Sabry A El-Naggar, David J Cole. Cell Immunol, 2009 Dec 29; 261(2). PMID: 20036354 Free PMC article.
Pilot study of sentinel-node-based adoptive immunotherapy in advanced colorectal cancer. Mona Karlsson, Per Marits, +4 authors, Ola Winqvist. less Ann Surg Oncol, 2010 Feb 02; 17(7). PMID: 20119674 Free PMC article.
Cytokine working group study of lymphodepleting chemotherapy, interleukin-2, and granulocyte-macrophage colony-stimulating factor in patients with metastatic melanoma: clinical outcomes and peripheral-blood cell recovery. Krishna S Gunturu, Kenneth R Meehan, +13 authors, Marc S Ernstoff. less J Clin Oncol, 2010 Feb 04; 28(7). PMID: 20124177 Free PMC article.
Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. Sergio A Quezada, Tyler R Simpson, +9 authors, James P Allison. less J Exp Med, 2010 Feb 17; 207(3). PMID: 20156971 Free PMC article. Highly Cited.
Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. Ying Xie, Akgül Akpinarli, +6 authors, Paul Andrew Antony. less J Exp Med, 2010 Feb 17; 207(3). PMID: 20156973 Free PMC article. Highly Cited.
The role of regulatory T cells in cancer. Tai-You Ha. Immune Netw, 2010 Feb 17; 9(6). PMID: 20157609 Free PMC article.
Redirecting the immune response: role of adoptive T cell therapy. Anna Mondino, Valérie Dardalhon, +2 authors, Naomi Taylor. less Hum Gene Ther, 2010 Mar 06; 21(5). PMID: 20201627 Free PMC article. Review.
T(H)17 cells in tumour immunity and immunotherapy. Weiping Zou, Nicholas P Restifo. Nat Rev Immunol, 2010 Mar 26; 10(4). PMID: 20336152 Free PMC article. Highly Cited. Review.
Self-specific CD8+ T cells maintain a semi-naive state following lymphopenia-induced proliferation. Lisa D S Johnson, Stephen C Jameson. J Immunol, 2010 Apr 16; 184(10). PMID: 20393139 Free PMC article.
Both CD4 and CD8 T cells mediate equally effective in vivo tumor treatment when engineered with a highly avid TCR targeting tyrosinase. Timothy L Frankel, William R Burns, +7 authors, Richard A Morgan. less J Immunol, 2010 Apr 30; 184(11). PMID: 20427771 Free PMC article.
Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. James N Kochenderfer, Zhiya Yu, +2 authors, Dorina Frasheri, Nicholas P Restifo, Steven A Rosenberg. less Blood, 2010 Jul 16; 116(19). PMID: 20631379 Free PMC article. Highly Cited.
Comparison of OX40 ligand and CD70 in the promotion of CD4+ T cell responses. Jonathan S Kurche, Matthew A Burchill, +2 authors, Ross M Kedl. less J Immunol, 2010 Jul 20; 185(4). PMID: 20639485 Free PMC article.
Tumor-specific CD8+ T cells expressing interleukin-12 eradicate established cancers in lymphodepleted hosts. Sid P Kerkar, Pawel Muranski, +12 authors, Nicholas P Restifo. less Cancer Res, 2010 Jul 22; 70(17). PMID: 20647327 Free PMC article. Highly Cited.
CD8+ enriched "young" tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Mark E Dudley, Colin A Gross, +17 authors, Steven A Rosenberg. less Clin Cancer Res, 2010 Jul 30; 16(24). PMID: 20668005 Free PMC article.
Early expression of stem cell-associated genes within the CD8 compartment after treatment with a tumor vaccine. M Eric Kohler, William H D Hallett, +3 authors, Rimas J Orentas. less Cell Immunol, 2010 Aug 10; 265(1). PMID: 20692654 Free PMC article.
Dendritic cells: are they clinically relevant? Karolina Palucka, Hideki Ueno, +2 authors, Lee Roberts, Joseph Fay, Jacques Banchereau. less Cancer J, 2010 Aug 10; 16(4). PMID: 20693842 Free PMC article. Review.
A CpG-loaded tumor cell vaccine induces antitumor CD4+ T cells that are effective in adoptive therapy for large and established tumors. Matthew J Goldstein, Bindu Varghese, +5 authors, Ronald Levy. less Blood, 2010 Sep 30; 117(1). PMID: 20876455 Free PMC article.
Designing vaccines based on biology of human dendritic cell subsets. Karolina Palucka, Jacques Banchereau, Ira Mellman. Immunity, 2010 Oct 30; 33(4). PMID: 21029958 Free PMC article. Highly Cited. Review.
Allogeneic effector/memory Th-1 cells impair FoxP3+ regulatory T lymphocytes and synergize with chaperone-rich cell lysate vaccine to treat leukemia. Nona Janikashvili, Collin J LaCasse, +7 authors, Emmanuel Katsanis. less Blood, 2010 Dec 03; 117(5). PMID: 21123824 Free PMC article.
Reprogrammed foxp3(+) regulatory T cells provide essential help to support cross-presentation and CD8(+) T cell priming in naive mice. Madhav D Sharma, De-Yan Hou, +6 authors, David H Munn. less Immunity, 2010 Dec 15; 33(6). PMID: 21145762 Free PMC article. Highly Cited.
Dendritic cells and immunity against cancer. K Palucka, H Ueno, J Fay, J Banchereau. J Intern Med, 2010 Dec 17; 269(1). PMID: 21158979 Free PMC article. Review.
Therapeutic cancer vaccines: are we there yet? Christopher A Klebanoff, Nicolas Acquavella, Zhiya Yu, Nicholas P Restifo. Immunol Rev, 2011 Jan 05; 239(1). PMID: 21198663 Free PMC article. Highly Cited. Review.
Immunization delivered by lentiviral vectors for cancer and infectious diseases. Biliang Hu, April Tai, Pin Wang. Immunol Rev, 2011 Jan 05; 239(1). PMID: 21198664 Free PMC article. Review.
Focus on adoptive T cell transfer trials in melanoma. Liat Hershkovitz, Jacob Schachter, Avraham J Treves, Michal J Besser. Clin Dev Immunol, 2011 Jan 15; 2010. PMID: 21234353 Free PMC article. Review.
Recent developments in cancer vaccines. Karolina Palucka, Hideki Ueno, Jacques Banchereau. J Immunol, 2011 Jan 21; 186(3). PMID: 21248270 Free PMC article. Review.
Cell-to-cell interactions and signals involved in the reconstitution of peripheral CD8 T(CM) and T(EM) cell pools. Bruno Zaragoza, César Evaristo, +5 authors, Afonso R M Almeida. less PLoS One, 2011 Mar 23; 6(3). PMID: 21423804 Free PMC article.
Chimeric antigen receptor (CAR)-engineered lymphocytes for cancer therapy. Carlos A Ramos, Gianpietro Dotti. Expert Opin Biol Ther, 2011 Apr 06; 11(7). PMID: 21463133 Free PMC article. Review.
Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication. Sergio A Quezada, Karl S Peggs, Tyler R Simpson, James P Allison. Immunol Rev, 2011 Apr 15; 241(1). PMID: 21488893 Free PMC article. Highly Cited. Review.
Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Steven A Rosenberg, James C Yang, +12 authors, Mark E Dudley. less Clin Cancer Res, 2011 Apr 19; 17(13). PMID: 21498393 Free PMC article. Highly Cited.
Depletion of CD25⁺ T cells from hematopoietic stem cell grafts increases posttransplantation vaccine-induced immunity to neuroblastoma. Weiqing Jing, Xiaocai Yan, +2 authors, William H D Hallett, Jill A Gershan, Bryon D Johnson. less Blood, 2011 Apr 28; 117(25). PMID: 21521781 Free PMC article.
HLA antigen and NK cell activating ligand expression in malignant cells: a story of loss or acquisition. Michael Campoli, Soldano Ferrone. Semin Immunopathol, 2011 Apr 28; 33(4). PMID: 21523560 Free PMC article. Review.
Establishment of antitumor memory in humans using in vitro-educated CD8+ T cells. Marcus O Butler, Philip Friedlander, +19 authors, Naoto Hirano. less Sci Transl Med, 2011 Apr 29; 3(80). PMID: 21525398 Free PMC article.
Anti-leukemia effect of ex vivo expanded DNT cells from AML patients: a potential novel autologous T-cell adoptive immunotherapy. S Merims, X Li, +7 authors, L Zhang. less Leukemia, 2011 May 14; 25(9). PMID: 21566657 Free PMC article.
Randomized multicenter trial of the effects of melanoma-associated helper peptides and cyclophosphamide on the immunogenicity of a multipeptide melanoma vaccine. Craig L Slingluff, Gina R Petroni, +5 authors, William W Grosh. less J Clin Oncol, 2011 Jun 22; 29(21). PMID: 21690475 Free PMC article.
Engineered artificial antigen presenting cells facilitate direct and efficient expansion of tumor infiltrating lymphocytes. Qunrui Ye, Maria Loisiou, +5 authors, Daniel J Powell. less J Transl Med, 2011 Aug 11; 9. PMID: 21827675 Free PMC article.
Effective colon cancer prophylaxis in mice using embryonic stem cells and carbon nanotubes. Teodora Mocan, Cornel Iancu. Int J Nanomedicine, 2011 Oct 07; 6. PMID: 21976971 Free PMC article.
Protective CD8 memory T cell responses to mouse melanoma are generated in the absence of CD4 T cell help. Anik L Côté, Katelyn T Byrne, +2 authors, Shannon M Steinberg, Peisheng Zhang, Mary Jo Turk. less PLoS One, 2011 Nov 03; 6(10). PMID: 22046294 Free PMC article.
IL-12 triggers a programmatic change in dysfunctional myeloid-derived cells within mouse tumors. Sid P Kerkar, Romina S Goldszmid, +10 authors, Nicholas P Restifo. less J Clin Invest, 2011 Nov 08; 121(12). PMID: 22056381 Free PMC article. Highly Cited.
T cells and adoptive immunotherapy: recent developments and future prospects in gastrointestinal oncology. Amedeo Amedei, Elena Niccolai, Mario M D'Elios. Clin Dev Immunol, 2011 Nov 24; 2011. PMID: 22110523 Free PMC article. Review.
The dendritic cell-regulatory T lymphocyte crosstalk contributes to tumor-induced tolerance. Nona Janikashvili, Bernard Bonnotte, Emmanuel Katsanis, Nicolas Larmonier. Clin Dev Immunol, 2011 Nov 24; 2011. PMID: 22110524 Free PMC article. Review.
Immunological treatment options for locoregionally advanced head and neck squamous cell carcinoma. Christopher Schutt, Klaus Bumm, +9 authors, Maurizio Chiriva-Internati. less Int Rev Immunol, 2012 Jan 19; 31(1). PMID: 22251006 Free PMC article. Review.
A mouse model of vitiligo with focused epidermal depigmentation requires IFN-γ for autoreactive CD8⁺ T-cell accumulation in the skin. John E Harris, Tajie H Harris, +3 authors, Laurence A Turka. less J Invest Dermatol, 2012 Feb 03; 132(7). PMID: 22297636 Free PMC article.
Trafficking of high avidity HER-2/neu-specific T cells into HER-2/neu-expressing tumors after depletion of effector/memory-like regulatory T cells. Vivian L Weiss, Timothy H Lee, +5 authors, Todd D Armstrong. less PLoS One, 2012 Feb 24; 7(2). PMID: 22359647 Free PMC article.
A pilot study of IL-2Rα blockade during lymphopenia depletes regulatory T-cells and correlates with enhanced immunity in patients with glioblastoma. John H Sampson, Robert J Schmittling, +13 authors, Duane A Mitchell. less PLoS One, 2012 Mar 03; 7(2). PMID: 22383993 Free PMC article.
Cytotoxic chemotherapy and CD4+ effector T cells: an emerging alliance for durable antitumor effects. Zhi-Chun Ding, Gang Zhou. Clin Dev Immunol, 2012 Mar 09; 2012. PMID: 22400040 Free PMC article. Review.
B7-H1 expression is associated with expansion of regulatory T cells in colorectal carcinoma. Dong Hua, Jing Sun, +3 authors, Yong Mao, Lu-Jun Chen, Yu-Yu Wu, Xue-Guang Zhang. less World J Gastroenterol, 2012 Mar 13; 18(9). PMID: 22408358 Free PMC article.
Cancer immunotherapy via dendritic cells. Karolina Palucka, Jacques Banchereau. Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437871 Free PMC article. Highly Cited. Review.
Adoptive immunotherapy for cancer: harnessing the T cell response. Nicholas P Restifo, Mark E Dudley, Steven A Rosenberg. Nat Rev Immunol, 2012 Mar 23; 12(4). PMID: 22437939 Free PMC article. Highly Cited. Review.
Advances in the treatment of metastatic melanoma: adoptive T-cell therapy. Chantale Bernatchez, Laszlo G Radvanyi, Patrick Hwu. Semin Oncol, 2012 Apr 10; 39(2). PMID: 22484193 Free PMC article. Review.
T-regulatory cells: key players in tumor immune escape and angiogenesis. Andrea Facciabene, Gregory T Motz, George Coukos. Cancer Res, 2012 May 03; 72(9). PMID: 22549946 Free PMC article. Highly Cited. Review.
Kinetics of rebounding of lymphoid and myeloid cells in mouse peripheral blood, spleen and bone marrow after treatment with cyclophosphamide. Mohamed L Salem, Amir A Al-Khami, +4 authors, David J Cole. less Cell Immunol, 2012 May 09; 276(1-2). PMID: 22560674 Free PMC article.
Pten loss in CD4 T cells enhances their helper function but does not lead to autoimmunity or lymphoma. Dalya R Soond, Fabien Garçon, +5 authors, Klaus Okkenhaug. less J Immunol, 2012 May 23; 188(12). PMID: 22611241 Free PMC article.
Absence of CD4 T-cell help provides a robust CD8 T-cell response while inducing effective memory in a preclinical model of melanoma. Maria Muccioli, Caitlin Longstaff, Fabian Benencia. Immunotherapy, 2012 May 31; 4(5). PMID: 22642330 Free PMC article.
Quorum-Sensing in CD4(+) T Cell Homeostasis: A Hypothesis and a Model. Afonso R M Almeida, Inês F Amado, +4 authors, Antonio A Freitas. less Front Immunol, 2012 Jun 02; 3. PMID: 22654881 Free PMC article.
T cells in gastric cancer: friends or foes. Amedeo Amedei, Chiara Della Bella, +2 authors, Elena Silvestri, Domenico Prisco, Mario M D'Elios. less Clin Dev Immunol, 2012 Jun 14; 2012. PMID: 22693525 Free PMC article. Review.
Increased frequency of suppressive regulatory T cells and T cell-mediated antigen loss results in murine melanoma recurrence. Shawn M Jensen, Christopher G Twitty, +6 authors, Bernard A Fox. less J Immunol, 2012 Jun 23; 189(2). PMID: 22723522 Free PMC article.
DNA fusion-gene vaccination in patients with prostate cancer induces high-frequency CD8(+) T-cell responses and increases PSA doubling time. Lindsey Chudley, Katy McCann, +13 authors, Christian Ottensmeier. less Cancer Immunol Immunother, 2012 Jun 26; 61(11). PMID: 22729556 Free PMC article.
The development and immunosuppressive functions of CD4(+) CD25(+) FoxP3(+) regulatory T cells are under influence of the adenosine-A2A adenosine receptor pathway. Akio Ohta, Radhika Kini, +3 authors, Michail Sitkovsky. less Front Immunol, 2012 Jul 12; 3. PMID: 22783261 Free PMC article. Highly Cited.
Adoptive immunotherapy of advanced melanoma. Ronnie Shapira-Frommer, Jacob Schachter. Curr Treat Options Oncol, 2012 Aug 07; 13(3). PMID: 22864561 Review.
MHC class II/ESO tetramer-based generation of in vitro primed anti-tumor T-helper lines for adoptive cell therapy of cancer. Caroline Poli, Caroline Raffin, +3 authors, Danila Valmori. less Haematologica, 2012 Aug 10; 98(2). PMID: 22875619 Free PMC article.
Tumor-infiltrating lymphocytes in melanoma. Sylvia Lee, Kim Margolin. Curr Oncol Rep, 2012 Aug 11; 14(5). PMID: 22878966 Free PMC article. Review.
MHC-class I-restricted CD4 T cells: a nanomolar affinity TCR has improved anti-tumor efficacy in vivo compared to the micromolar wild-type TCR. Carolina M Soto, Jennifer D Stone, +4 authors, David M Kranz. less Cancer Immunol Immunother, 2012 Aug 29; 62(2). PMID: 22926060 Free PMC article.
Augmentation of anti-tumor immunity by adoptive T-cell transfer after allogeneic hematopoietic stem cell transplantation. Marie Bleakley, Cameron J Turtle, Stanley R Riddell. Expert Rev Hematol, 2012 Sep 21; 5(4). PMID: 22992235 Free PMC article. Review.
Regulatory T cell infiltration predicts outcome following resection of colorectal cancer liver metastases. Steven C Katz, Zubin M Bamboat, +9 authors, Ronald P DeMatteo. less Ann Surg Oncol, 2012 Sep 27; 20(3). PMID: 23010736 Free PMC article.
Isolation of human MHC class II-restricted T cell receptors from the autologous T-cell repertoire with potent anti-leukaemic reactivity. Luise U Weigand, Xiaoling Liang, +8 authors, Angela M Krackhardt. less Immunology, 2012 Oct 03; 137(3). PMID: 23025755 Free PMC article.
Neuropilin 1 deficiency on CD4+Foxp3+ regulatory T cells impairs mouse melanoma growth. Wiebke Hansen, Marina Hutzler, +10 authors, Iris Helfrich. less J Exp Med, 2012 Oct 10; 209(11). PMID: 23045606 Free PMC article. Highly Cited.
Donor bone marrow-derived T cells inhibit GVHD induced by donor lymphocyte infusion in established mixed allogeneic hematopoietic chimeras. Hui Wang, Yanping Yang, +4 authors, Yong-Guang Yang. less PLoS One, 2012 Oct 19; 7(10). PMID: 23077554 Free PMC article.
Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? Christopher A Klebanoff, Luca Gattinoni, Nicholas P Restifo. J Immunother, 2012 Oct 24; 35(9). PMID: 23090074 Free PMC article. Highly Cited. Review.
The past, present, and future of adoptive T cell therapy. Donghoon Choi, Tai-Gyu Kim, Young Chul Sung. Immune Netw, 2012 Oct 24; 12(4). PMID: 23091437 Free PMC article.
Suppression, subversion and escape: the role of regulatory T cells in cancer progression. K Oleinika, R J Nibbs, G J Graham, A R Fraser. Clin Exp Immunol, 2012 Dec 04; 171(1). PMID: 23199321 Free PMC article. Review.
Clinical opportunities in combining immunotherapy with radiation therapy. Steven E Finkelstein, Mayer Fishman. Front Oncol, 2012 Dec 13; 2. PMID: 23233905 Free PMC article.
HDAC inhibition suppresses primary immune responses, enhances secondary immune responses, and abrogates autoimmunity during tumor immunotherapy. Byram W Bridle, Lan Chen, +9 authors, Yonghong Wan. less Mol Ther, 2013 Jan 09; 21(4). PMID: 23295947 Free PMC article.
Effects of tumor irradiation on host T-regulatory cells and systemic immunity in the context of adoptive T-cell therapy in mice. Shuang Wei, Martin U Egenti, +2 authors, Seagal Teitz-Tennenbaum, Weiping Zou, Alfred E Chang. less J Immunother, 2013 Feb 05; 36(2). PMID: 23377667 Free PMC article.
Influence of tumors on protective anti-tumor immunity and the effects of irradiation. Gemma A Foulds, Jürgen Radons, +2 authors, Mira Kreuzer, Gabriele Multhoff, Alan G Pockley. less Front Oncol, 2013 Feb 05; 3. PMID: 23378947 Free PMC article.
Restoring immune function of tumor-specific CD4+ T cells during recurrence of melanoma. Stephen R Goding, Kyle A Wilson, +7 authors, Paul Andrew Antony. less J Immunol, 2013 Mar 29; 190(9). PMID: 23536636 Free PMC article. Highly Cited.
GARP-TGF-β complexes negatively regulate regulatory T cell development and maintenance of peripheral CD4+ T cells in vivo. Angela X Zhou, Lina Kozhaya, Hodaka Fujii, Derya Unutmaz. J Immunol, 2013 Apr 12; 190(10). PMID: 23576681 Free PMC article.
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Chemotherapy in the management of advanced cutaneous malignant melanoma. Jason J Luke, Gary K Schwartz. Clin Dermatol, 2013 Apr 24; 31(3). PMID: 23608448 Free PMC article. Review.
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Dendritic-tumor fusion cells derived heat shock protein70-peptide complex has enhanced immunogenicity. Yunfei Zhang, Yong Zhang, +2 authors, Jun Chen, Yunyan Liu, Wen Luo. less PLoS One, 2015 May 12; 10(5). PMID: 25961716 Free PMC article.
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scRNA-seq of human vitiligo reveals complex networks of subclinical immune activation and a role for CCR5 in Treg function. Kyle J Gellatly, James P Strassner, +13 authors, John E Harris. less Sci Transl Med, 2021 Sep 14; 13(610). PMID: 34516831 Free PMC article.
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