Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses

R P Sutmuller ¹, L M van Duivenvoorde , A van Elsas , T N Schumacher , M E Wildenberg , J P Allison , R E Toes , R Offringa , C J Melief

Affiliations

¹ Department of Immunohematology and Blood Transfusion, Tumor Immunology Lab, E3-Q, Leiden University Medical Center, 2300 RC Leiden, the Netherlands.

PMID: 11560997
40 References
303 citations

Abstract

Therapeutic efficacy of a tumor cell-based vaccine against experimental B16 melanoma requires the disruption of either of two immunoregulatory mechanisms that control autoreactive T cell responses: the cytotoxic T lymphocyte-associated antigen (CTLA)-4 pathway or the CD25(+) regulatory T (Treg) cells. Combination of CTLA-4 blockade and depletion of CD25(+) Treg cells results in maximal tumor rejection. Efficacy of the antitumor therapy correlates with the extent of autoimmune skin depigmentation as well as with the frequency of tyrosinase-related protein 2(180-188)-specific CTLs detected in the periphery. Furthermore, tumor rejection is dependent on the CD8(+) T cell subset. Our data demonstrate that the CTL response against melanoma antigens is an important component of the therapeutic antitumor response and that the reactivity of these CTLs can be augmented through interference with immunoregulatory mechanisms. The synergism in the effects of CTLA-4 blockade and depletion of CD25(+) Treg cells indicates that CD25(+) Treg cells and CTLA-4 signaling represent two alternative pathways for suppression of autoreactive T cell immunity. Simultaneous intervention with both regulatory mechanisms is therefore a promising concept for the induction of therapeutic antitumor immunity.

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Adoptive T cell therapy for cancer in the clinic. Carl H June. J Clin Invest, 2007 Jun 06; 117(6). PMID: 17549249 Free PMC article. Highly Cited. Review.
The impact of regulatory T cells on carcinogen-induced sarcogenesis. G Betts, J Twohig, +3 authors, M Van den Broek, S Sierro, A Godkin, A Gallimore. less Br J Cancer, 2007 Jun 15; 96(12). PMID: 17565340 Free PMC article.
Induction of postsurgical tumor immunity and T-cell memory by a poorly immunogenic tumor. Peisheng Zhang, Anik L Côté, +2 authors, Mary Jo Turk. less Cancer Res, 2007 Jul 10; 67(13). PMID: 17616708 Free PMC article.
Steady state dendritic cells present parenchymal self-antigen and contribute to, but are not essential for, tolerization of naive and Th1 effector CD4 cells. Adam T Hagymasi, Aaron M Slaiby, +4 authors, Adam J Adler. less J Immunol, 2007 Jul 21; 179(3). PMID: 17641018 Free PMC article.
CTLA-4 blockade during dendritic cell based booster vaccination influences dendritic cell survival and CTL expansion. Anders E Pedersen, Franca Ronchese. J Immune Based Ther Vaccines, 2007 Jul 31; 5. PMID: 17662155 Free PMC article.
Inhibitory costimulation and anti-tumor immunity. Natalia Martin-Orozco, Chen Dong. Semin Cancer Biol, 2007 Aug 09; 17(4). PMID: 17683946 Free PMC article. Review.
Transplantation tolerance: lessons from experimental rodent models. Cherry I Kingsley, Satish N Nadig, Kathryn J Wood. Transpl Int, 2007 Aug 23; 20(10). PMID: 17711408 Free PMC article. Review.
Induction of the CTLA-4 gene in human lymphocytes is dependent on NFAT binding the proximal promoter. Heather M Gibson, Carrie J Hedgcock, +4 authors, Henry K Wong. less J Immunol, 2007 Sep 06; 179(6). PMID: 17785820 Free PMC article.
Regulatory T cells and toll-like receptors: regulating the regulators. Roger Sutmuller, Anja Garritsen, Gosse J Adema. Ann Rheum Dis, 2007 Nov 21; 66 Suppl 3. PMID: 17934105 Free PMC article. Review.
Resistance to apoptosis and expansion of regulatory T cells in relation to the detection of circulating tumor cells in patients with metastatic epithelial cancer. Stefanie Stanzer, Nadia Dandachi, +3 authors, Thomas Bauernhofer. less J Clin Immunol, 2007 Oct 17; 28(2). PMID: 17939021
Increase of CD4+ CD25+ regulatory T cells in the peripheral blood of patients with metastatic carcinoma: a Phase I clinical trial using cyclophosphamide and immunotherapy to eliminate CD4+ CD25+ T lymphocytes. S Audia, A Nicolas, +12 authors, B Bonnotte. less Clin Exp Immunol, 2007 Oct 25; 150(3). PMID: 17956583 Free PMC article.
Advancements in immune tolerance. Ping-Ying Pan, Junko Ozao, Zuping Zhou, Shu-Hsia Chen. Adv Drug Deliv Rev, 2007 Nov 03; 60(2). PMID: 17976856 Free PMC article. Review.
Is IDO a key enzyme bridging the gap between tumor escape and tolerance induction? Stefan Löb, Alfred Königsrainer. Langenbecks Arch Surg, 2007 Dec 08; 393(6). PMID: 18064486 Review.
Regulatory T cells and tumour immunity - observations in mice and men. Awen Gallimore, Andrew Godkin. Immunology, 2007 Dec 11; 123(2). PMID: 18067556 Free PMC article. Review.
Anti-tumor activity of an anti-endoglin monoclonal antibody is enhanced in immunocompetent mice. Masanori Tsujie, Tomoko Tsujie, +4 authors, Ben K Seon. less Int J Cancer, 2008 Jan 29; 122(10). PMID: 18224682 Free PMC article.
Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. F Stephen Hodi, Marcus Butler, +17 authors, Glenn Dranoff. less Proc Natl Acad Sci U S A, 2008 Feb 22; 105(8). PMID: 18287062 Free PMC article. Highly Cited.
Comparative methodologies of regulatory T cell depletion in a murine melanoma model. Norimasa Matsushita, Shari A Pilon-Thomas, Lisa M Martin, Adam I Riker. J Immunol Methods, 2008 Feb 26; 333(1-2). PMID: 18295790 Free PMC article.
A20 is an antigen presentation attenuator, and its inhibition overcomes regulatory T cell-mediated suppression. Xiao-Tong Song, Kevin Evel-Kabler, +3 authors, Lei Shen, Lisa Rollins, Xue F Huang, Si-Yi Chen. less Nat Med, 2008 Mar 04; 14(3). PMID: 18311150 Free PMC article.
Regulatory T cells and human disease. Nathalie Cools, Peter Ponsaerts, Viggo F I Van Tendeloo, Zwi N Berneman. Clin Dev Immunol, 2008 Mar 05; 2007. PMID: 18317534 Free PMC article. Review.
Transient T cell depletion causes regression of melanoma metastases. Mary Ann Rasku, Amy L Clem, +8 authors, Jason Chesney. less J Transl Med, 2008 Mar 13; 6. PMID: 18334033 Free PMC article.
Infiltrating regulatory T cell numbers is not a factor to predict patient's survival in oesophageal squamous cell carcinoma. T Yoshioka, M Miyamoto, +13 authors, S Kondo. less Br J Cancer, 2008 Mar 20; 98(7). PMID: 18349839 Free PMC article.
Immunotherapy of malignant brain tumors. Duane A Mitchell, Peter E Fecci, John H Sampson. Immunol Rev, 2008 Mar 28; 222. PMID: 18363995 Free PMC article. Review.
Photodynamic therapy plus low-dose cyclophosphamide generates antitumor immunity in a mouse model. Ana P Castano, Pawel Mroz, Mei X Wu, Michael R Hamblin. Proc Natl Acad Sci U S A, 2008 Apr 02; 105(14). PMID: 18378905 Free PMC article.
Developing idiotype vaccines for lymphoma: from preclinical studies to phase III clinical trials. Hyun Jun Park, Sattva S Neelapu. Br J Haematol, 2008 Apr 22; 142(2). PMID: 18422783 Free PMC article. Review.
Treg depletion inhibits efficacy of cancer immunotherapy: implications for clinical trials. James F Curtin, Marianela Candolfi, +5 authors, Maria G Castro. less PLoS One, 2008 Apr 24; 3(4). PMID: 18431473 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.
The effects of immunosuppression on regulatory CD4(+)CD25(+) T cells: impact on immunosuppression selection in transplantation. Aqeel Javeed, Yong Zhao. Mol Diagn Ther, 2008 May 31; 12(3). PMID: 18510380 Review.
CTLA4 blockade expands FoxP3+ regulatory and activated effector CD4+ T cells in a dose-dependent fashion. Brian Kavanagh, Shaun O'Brien, +6 authors, Lawrence Fong. less Blood, 2008 Jun 05; 112(4). PMID: 18523152 Free PMC article.
T-bet plays a key role in NK-mediated control of melanoma metastatic disease. Miriam B F Werneck, Geanncarlo Lugo-Villarino, +2 authors, Eun Sook Hwang, Harvey Cantor, Laurie H Glimcher. less J Immunol, 2008 Jun 05; 180(12). PMID: 18523263 Free PMC article.
Phase Ib trial assessing autologous, tumor-pulsed dendritic cells as a vaccine administered with or without IL-2 in patients with metastatic melanoma. Bruce G Redman, Alfred E Chang, +5 authors, James J Mulé. less J Immunother, 2008 Jun 06; 31(6). PMID: 18528294 Free PMC article.
Toll-like receptor signalling on Tregs: to suppress or not to suppress? Wendy W C van Maren, Joannes F M Jacobs, +2 authors, Gosse J Adema. less Immunology, 2008 Jun 11; 124(4). PMID: 18540962 Free PMC article. Review.
In silico identified CCR4 antagonists target regulatory T cells and exert adjuvant activity in vaccination. Jagadeesh Bayry, Elma Z Tchilian, +8 authors, David F Tough. less Proc Natl Acad Sci U S A, 2008 Jul 16; 105(29). PMID: 18621704 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.
Distinct effects of IL-18 on the engraftment and function of human effector CD8 T cells and regulatory T cells. Richard G Carroll, Carmine Carpenito, +9 authors, Carl H June. less PLoS One, 2008 Sep 27; 3(9). PMID: 18818761 Free PMC article.
Depletion of CD4(+)CD25(+) regulatory T cells can promote local immunity to suppress tumor growth in benzo[a]pyrene-induced forestomach carcinoma. Yi-Ling Chen, Jung-Hua Fang, Ming-Derg Lai, Yan-Shen Shan. World J Gastroenterol, 2008 Oct 16; 14(38). PMID: 18855977 Free PMC article.
Localized expression of GITR-L in the tumor microenvironment promotes CD8+ T cell dependent anti-tumor immunity. John S Cho, Jeffrey V Hsu, Sherie L Morrison. Cancer Immunol Immunother, 2008 Nov 20; 58(7). PMID: 19018533 Free PMC article.
The role of NKT cells in tumor immunity. Masaki Terabe, Jay A Berzofsky. Adv Cancer Res, 2008 Dec 06; 101. PMID: 19055947 Free PMC article. Highly Cited. Review.
Enhancing therapeutic HPV DNA vaccine potency through depletion of CD4+CD25+ T regulatory cells. Chi-Mu Chuang, Talia Hoory, +3 authors, Chien-Fu Hung. less Vaccine, 2008 Dec 06; 27(5). PMID: 19056449 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.
Disruption of CCR5-dependent homing of regulatory T cells inhibits tumor growth in a murine model of pancreatic cancer. Marcus C B Tan, Peter S Goedegebuure, +6 authors, David C Linehan. less J Immunol, 2009 Jan 22; 182(3). PMID: 19155524 Free PMC article. Highly Cited.
Lymphocyte recruitment into the tumor site is altered in patients with MSI-H colon cancer. Kristen M Drescher, Poonam Sharma, +3 authors, Henry T Lynch. less Fam Cancer, 2009 Jan 24; 8(3). PMID: 19165625
Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Marcin Kortylewski, Hong Xin, +6 authors, Hua Yu. less Cancer Cell, 2009 Feb 03; 15(2). PMID: 19185846 Free PMC article. Highly Cited.
Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. Herschel Wallen, John A Thompson, +3 authors, Cassian Yee. less PLoS One, 2009 Mar 10; 4(3). PMID: 19270751 Free PMC article.
Induction of type I IFN is required for overcoming tumor-specific T-cell tolerance after stem cell transplantation. Ian Horkheimer, Michael Quigley, +3 authors, Yiping Yang. less Blood, 2009 Mar 13; 113(21). PMID: 19279333 Free PMC article.
Costimulatory and coinhibitory receptors in anti-tumor immunity. Gregory Driessens, Justin Kline, Thomas F Gajewski. Immunol Rev, 2009 May 12; 229(1). PMID: 19426219 Free PMC article. Review.
Flt3-L increases CD4+CD25+Foxp3+ICOS+ cells in the lungs of cockroach-sensitized and -challenged mice. Halvor S McGee, Jehad H Edwan, Devendra K Agrawal. Am J Respir Cell Mol Biol, 2009 May 19; 42(3). PMID: 19448155 Free PMC article.
Anti-CTLA-4 treatment induces IL-10-producing ICOS+ regulatory T cells displaying IDO-dependent anti-inflammatory properties in a mouse model of colitis. C Coquerelle, G Oldenhove, +6 authors, M Moser. less Gut, 2009 Jun 10; 58(10). PMID: 19505881 Free PMC article.
Anti-CTLA4 Antibody Clinical Trials in Melanoma. Antoni Ribas. Update Cancer Ther, 2007 Sep 01; 2(3). PMID: 19543441 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.
Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. Karl S Peggs, Sergio A Quezada, +2 authors, Cynthia A Chambers, Alan J Korman, James P Allison. less J Exp Med, 2009 Jul 08; 206(8). PMID: 19581407 Free PMC article. Highly Cited.
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.
Cancer immunotherapy: co-stimulatory agonists and co-inhibitory antagonists. K S Peggs, S A Quezada, J P Allison. Clin Exp Immunol, 2009 Aug 08; 157(1). PMID: 19659765 Free PMC article. Review.
Association of cytotoxic T lymphocyte-associated antigen-4 gene haplotype with the susceptibility to gastric cancer. Ruiping Hou, Bangwei Cao, +5 authors, Ziping Chen. less Mol Biol Rep, 2009 Aug 19; 37(1). PMID: 19688278
Cancer immunotherapy: the role regulatory T cells play and what can be done to overcome their inhibitory effects. Ulf Petrausch, Christian H Poehlein, +20 authors, Bernard A Fox. less Curr Mol Med, 2009 Aug 20; 9(6). PMID: 19689294 Free PMC article. Review.
An enteric pathogen Salmonella enterica serovar Typhimurium suppresses tumor growth by downregulating CD44high and CD4T regulatory (Treg) cell expression in mice: the critical role of lipopolysaccharide and Braun lipoprotein in modulating tumor growth. T Liu, A K Chopra. Cancer Gene Ther, 2009 Aug 29; 17(2). PMID: 19713997 Free PMC article.
Enhancing the efficacy of cancer vaccines in urologic oncology: new directions. Sergei Kusmartsev, Johannes Vieweg. Nat Rev Urol, 2009 Sep 09; 6(10). PMID: 19736551 Review.
Autologous MUC1-specific Th1 effector cell immunotherapy induces differential levels of systemic TReg cell subpopulations that result in increased ovarian cancer patient survival. Mark J Dobrzanski, Kathleen A Rewers-Felkins, +5 authors, Stephen E Wright. less Clin Immunol, 2009 Sep 19; 133(3). PMID: 19762283 Free PMC article.
CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. Franco R D'Alessio, Kenji Tsushima, +8 authors, Landon S King. less J Clin Invest, 2009 Sep 23; 119(10). PMID: 19770521 Free PMC article. Highly Cited.
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.
Toward the discovery of vaccine adjuvants: coupling in silico screening and in vitro analysis of antagonist binding to human and mouse CCR4 receptors. Matthew N Davies, Jagadeesh Bayry, +7 authors, Darren R Flower. less PLoS One, 2009 Dec 17; 4(11). PMID: 20011659 Free PMC article.
Tumor-mediated liver X receptor-alpha activation inhibits CC chemokine receptor-7 expression on dendritic cells and dampens antitumor responses. Eduardo J Villablanca, Laura Raccosta, +15 authors, Vincenzo Russo. less Nat Med, 2009 Dec 29; 16(1). PMID: 20037595
Antibodies designed as effective cancer vaccines. R L Metheringham, V A Pudney, +3 authors, B Gunn, M Towey, I Spendlove, L G Durrant. less MAbs, 2010 Jan 05; 1(1). PMID: 20046577 Free PMC article.
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.
Reduced skin homing by functional Treg in vitiligo. Jared Klarquist, Cecele J Denman, +7 authors, I Caroline Le Poole. less Pigment Cell Melanoma Res, 2010 Feb 24; 23(2). PMID: 20175879 Free PMC article.
DNA vaccines: developing new strategies against cancer. Daniela Fioretti, Sandra Iurescia, Vito Michele Fazio, Monica Rinaldi. J Biomed Biotechnol, 2010 Apr 07; 2010. PMID: 20368780 Free PMC article. Review.
Antigen quality determines the efficiency of antitumor immune responses generated in the absence of regulatory T cells. A-S Bergot, A Durgeau, +3 authors, B Levacher, B M Colombo, J L Cohen, D Klatzmann. less Cancer Gene Ther, 2010 May 15; 17(9). PMID: 20467452 Free PMC article.
RNA vaccines in cancer treatment. Anita Bringmann, Stefanie Andrea Erika Held, Annkristin Heine, Peter Brossart. J Biomed Biotechnol, 2010 Jul 14; 2010. PMID: 20625504 Free PMC article. Review.
B7-H1-dependent sex-related differences in tumor immunity and immunotherapy responses. Pei-Yi Lin, Lishi Sun, +11 authors, Tyler J Curiel. less J Immunol, 2010 Aug 06; 185(5). PMID: 20686128 Free PMC article.
Trends in cancer immunotherapy. Joseph F Murphy. Clin Med Insights Oncol, 2010 Aug 13; 4. PMID: 20703326 Free PMC article.
Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. Jennifer L Gnerlich, Jonathan B Mitchem, +8 authors, David C Linehan. less J Immunol, 2010 Sep 02; 185(7). PMID: 20805420 Free PMC article.
Control of established melanoma by CD27 stimulation is associated with enhanced effector function and persistence, and reduced PD-1 expression of tumor infiltrating CD8(+) T cells. Drew J Roberts, Nathan A Franklin, +4 authors, Timothy N J Bullock. less J Immunother, 2010 Sep 16; 33(8). PMID: 20842060 Free PMC article.
Extended dose ipilimumab with a peptide vaccine: immune correlates associated with clinical benefit in patients with resected high-risk stage IIIc/IV melanoma. Amod A Sarnaik, Bin Yu, +9 authors, Jeffrey S Weber. less Clin Cancer Res, 2010 Nov 26; 17(4). PMID: 21106722 Free PMC article.
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.
CTLA-4 exon 1 +49 polymorphism alone and in a haplotype with -318 promoter polymorphism may confer susceptibility to chronic HBV infection in Chinese Han patients. Shaoqiong Duan, Guoyu Zhang, +11 authors, Fanfan Xing. less Mol Biol Rep, 2010 Dec 17; 38(8). PMID: 21161390
A reversed CD4/CD8 ratio of tumor-infiltrating lymphocytes and a high percentage of CD4(+)FOXP3(+) regulatory T cells are significantly associated with clinical outcome in squamous cell carcinoma of the cervix. Walayat Shah, Xiaofei Yan, +3 authors, Li Jing, Yi Zhou, Hongwei Chen, Yili Wang. less Cell Mol Immunol, 2011 Jan 05; 8(1). PMID: 21200385 Free PMC article.
T cell-tumor interaction directs the development of immunotherapies in head and neck cancer. A E Albers, L Strauss, +2 authors, T Liao, T K Hoffmann, A M Kaufmann. less Clin Dev Immunol, 2011 Jan 15; 2010. PMID: 21234340 Free PMC article. Review.
Enhancement of T-cell-mediated antitumor response: angiostatic adjuvant to immunotherapy against cancer. Ruud P M Dings, Kieng B Vang, +7 authors, Kevin H Mayo. less Clin Cancer Res, 2011 Jan 22; 17(10). PMID: 21252159 Free PMC article.
Whole recombinant yeast vaccine induces antitumor immunity and improves survival in a genetically engineered mouse model of melanoma. A Tanaka, J D Jensen, +6 authors, M Fujita. less Gene Ther, 2011 Mar 11; 18(8). PMID: 21390072 Free PMC article.
Molecular profiling of melanoma and the evolution of patient-specific therapy. Thomas F Gajewski. Semin Oncol, 2011 Mar 23; 38(2). PMID: 21421113 Free PMC article. Review.
Deletion of galectin-3 in the host attenuates metastasis of murine melanoma by modulating tumor adhesion and NK cell activity. Gordana Radosavljevic, Ivan Jovanovic, +5 authors, Miodrag L Lukic. less Clin Exp Metastasis, 2011 Mar 29; 28(5). PMID: 21442355
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.
TLR2-dependent induction of IL-10 and Foxp3+ CD25+ CD4+ regulatory T cells prevents effective anti-tumor immunity induced by Pam2 lipopeptides in vivo. Sayuri Yamazaki, Kohei Okada, +3 authors, Tsukasa Seya. less PLoS One, 2011 May 03; 6(4). PMID: 21533081 Free PMC article.
Immunological and clinical effects of vaccines targeting p53-overexpressing malignancies. R Vermeij, N Leffers, +3 authors, H W Nijman. less J Biomed Biotechnol, 2011 May 05; 2011. PMID: 21541192 Free PMC article. Review.
Tumor-associated macrophages recruit CCR6+ regulatory T cells and promote the development of colorectal cancer via enhancing CCL20 production in mice. Jinlin Liu, Ning Zhang, +6 authors, Honglin Wang. less PLoS One, 2011 May 12; 6(4). PMID: 21559338 Free PMC article.
Immunomodulatory effects of cyclophosphamide and implementations for vaccine design. Antonella Sistigu, Sophie Viaud, +3 authors, Laurence Zitvogel. less Semin Immunopathol, 2011 May 26; 33(4). PMID: 21611872 Highly Cited. Review.
Immunosuppressive tumor microenvironment in cervical cancer patients. Sytse J Piersma. Cancer Microenviron, 2011 Jun 01; 4(3). PMID: 21626415 Free PMC article.
Targeted toxins for glioblastoma multiforme: pre-clinical studies and clinical implementation. Marianela Candolfi, Kurt M Kroeger, +11 authors, Maria G Castro. less Anticancer Agents Med Chem, 2011 Jun 29; 11(8). PMID: 21707497 Free PMC article. Review.
Therapeutic effectiveness of intratumorally delivered dendritic cells engineered to express the pro-inflammatory cytokine, interleukin (IL)-32. Y Qu, J L Taylor, A Bose, W J Storkus. Cancer Gene Ther, 2011 Jul 16; 18(9). PMID: 21760628 Free PMC article.
Monoclonal antibody blockade of IL-2 receptor α during lymphopenia selectively depletes regulatory T cells in mice and humans. Duane A Mitchell, Xiuyu Cui, +13 authors, John H Sampson. less Blood, 2011 Jul 20; 118(11). PMID: 21768296 Free PMC article.
Regulatory T cell: a protection for tumour cells. Yi Wang, Yushui Ma, +4 authors, Xizhong Shen. less J Cell Mol Med, 2011 Sep 08; 16(3). PMID: 21895966 Free PMC article. Review.
Targeting the immunoregulator SRA/CD204 potentiates specific dendritic cell vaccine-induced T-cell response and antitumor immunity. Huanfa Yi, Chunqing Guo, +7 authors, Xiang-Yang Wang. less Cancer Res, 2011 Sep 15; 71(21). PMID: 21914786 Free PMC article.
Therapeutic options in cutaneous melanoma: latest developments. Rodabe N Amaria, Karl D Lewis, Rene Gonzalez. Ther Adv Med Oncol, 2011 Oct 01; 3(5). PMID: 21957431 Free PMC article.
Enhancement of anti-tumor immunity through local modulation of CTLA-4 and GITR by dendritic cells. Scott K Pruitt, David Boczkowski, +5 authors, Smita Nair. less Eur J Immunol, 2011 Oct 27; 41(12). PMID: 22028176 Free PMC article.
Immune recovery after cyclophosphamide treatment in multiple myeloma: implication for maintenance immunotherapy. Amir Sharabi, Nechama Haran-Ghera. Bone Marrow Res, 2011 Nov 03; 2011. PMID: 22046558 Free PMC article.
Blockade of cytotoxic T-lymphocyte antigen-4 as a new therapeutic approach for advanced melanoma. Xiang-Yang Wang, Daming Zuo, Devanand Sarkar, Paul B Fisher. Expert Opin Pharmacother, 2011 Nov 15; 12(17). PMID: 22077831 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.
Regulatory T cells and IL-10 independently counterregulate cytotoxic T lymphocyte responses induced by transcutaneous immunization. Pamela Stein, Michael Weber, +7 authors, Markus P Radsak. less PLoS One, 2011 Nov 25; 6(11). PMID: 22114725 Free PMC article.
Challenges in immunotherapy presented by the glioblastoma multiforme microenvironment. Christopher Jackson, Jacob Ruzevick, +2 authors, Jillian Phallen, Zineb Belcaid, Michael Lim. less Clin Dev Immunol, 2011 Dec 23; 2011. PMID: 22190972 Free PMC article. Review.
Cancer immunotherapy. Thomas F Gajewski. Mol Oncol, 2012 Jan 18; 6(2). PMID: 22248437 Free PMC article. Review.
Myeloid suppressor cells and immune modulation in lung cancer. Minu K Srivastava, Åsa Andersson, +4 authors, Sherven Sharma. less Immunotherapy, 2012 Mar 10; 4(3). PMID: 22401635 Free PMC article. Review.
Targeting costimulatory molecules to improve antitumor immunity. Daria Capece, Daniela Verzella, +2 authors, Edoardo Alesse. less J Biomed Biotechnol, 2012 Apr 14; 2012. PMID: 22500111 Free PMC article. Review.
CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Andrew J Rech, Rosemarie Mick, +13 authors, Robert H Vonderheide. less Sci Transl Med, 2012 May 18; 4(134). PMID: 22593175 Free PMC article. Highly Cited.
Ipilimumab pharmacotherapy in patients with metastatic melanoma. Joanne M Jeter, Lee D Cranmer, Evan M Hersh. Clin Med Insights Oncol, 2012 Aug 21; 6. PMID: 22904648 Free PMC article.
Role of immune escape mechanisms in Hodgkin's lymphoma development and progression: a whole new world with therapeutic implications. Luis de la Cruz-Merino, Marylène Lejeune, +6 authors, Tomás Álvaro. less Clin Dev Immunol, 2012 Aug 29; 2012. PMID: 22927872 Free PMC article. Review.
Selective BRAF inhibition decreases tumor-resident lymphocyte frequencies in a mouse model of human melanoma. Anna Hooijkaas, Jules Gadiot, +3 authors, Christian U Blank. less Oncoimmunology, 2012 Aug 31; 1(5). PMID: 22934253 Free PMC article.
T-cell trafficking facilitated by high endothelial venules is required for tumor control after regulatory T-cell depletion. James P Hindley, Emma Jones, +11 authors, Awen M Gallimore. less Cancer Res, 2012 Sep 11; 72(21). PMID: 22962270 Free PMC article.
Regulation of COX2 expression in mouse mammary tumor cells controls bone metastasis and PGE2-induction of regulatory T cell migration. John Karavitis, Laura M Hix, +3 authors, Ming Zhang. less PLoS One, 2012 Oct 03; 7(9). PMID: 23029485 Free PMC article.
Immunology beats cancer: a blueprint for successful translation. Drew M Pardoll. Nat Immunol, 2012 Nov 20; 13(12). PMID: 23160205 Free PMC article.
Immunotherapies: the blockade of inhibitory signals. Yan-Ling Wu, Jing Liang, +2 authors, Wen Zhang, Yoshimasa Tanaka, Hiroshi Sugiyama. less Int J Biol Sci, 2012 Dec 01; 8(10). PMID: 23197939 Free PMC article. Review.
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.
Amphiregulin enhances regulatory T cell-suppressive function via the epidermal growth factor receptor. Dietmar M W Zaiss, Jorg van Loosdregt, +7 authors, Alice J A M Sijts. less Immunity, 2013 Jan 22; 38(2). PMID: 23333074 Free PMC article. Highly Cited.
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.
CTLA-4 blockade in tumor models: an overview of preclinical and translational research. Joseph F Grosso, Maria N Jure-Kunkel. Cancer Immun, 2013 Feb 08; 13. PMID: 23390376 Free PMC article. Highly Cited. Review.
Antigen choice determines vaccine-induced generation of immunogenic versus tolerogenic dendritic cells that are marked by differential expression of pancreatic enzymes. Adam M Farkas, Douglas M Marvel, Olivera J Finn. J Immunol, 2013 Feb 20; 190(7). PMID: 23420890 Free PMC article.
Higher frequencies of GARP(+)CTLA-4(+)Foxp3(+) T regulatory cells and myeloid-derived suppressor cells in hepatocellular carcinoma patients are associated with impaired T-cell functionality. Suresh Kalathil, Amit A Lugade, +2 authors, Austin Miller, Renuka Iyer, Yasmin Thanavala. less Cancer Res, 2013 Feb 21; 73(8). PMID: 23423978 Free PMC article. Highly Cited.
The nature of activatory and tolerogenic dendritic cell-derived signal II. Ghaith Bakdash, Simone P Sittig, +2 authors, Tjeerd van Dijk, Carl G Figdor, I Jolanda M de Vries. less Front Immunol, 2013 Mar 02; 4. PMID: 23450201 Free PMC article.
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