Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients

P P Lee ¹, C Yee , P A Savage , L Fong , D Brockstedt , J S Weber , D Johnson , S Swetter , J Thompson , P D Greenberg , M Roederer , M M Davis

Affiliations

¹ Howard Hughes Medical Institute/Department of Microbiology and Immunology, Stanford University, California 94305, USA.

PMID: 10371507
286 citations

Abstract

We identified circulating CD8+ T-cell populations specific for the tumor-associated antigens (TAAs) MART-1 (27-35) or tyrosinase (368-376) in six of eleven patients with metastatic melanoma using peptide/HLA-A*0201 tetramers. These TAA-specific populations were of two phenotypically distinct types: one, typical for memory/effector T cells; the other, a previously undescribed phenotype expressing both naive and effector cell markers. This latter type represented more than 2% of the total CD8+ T cells in one patient, permitting detailed phenotypic and functional analysis. Although these cells have many of the hallmarks of effector T cells, they were functionally unresponsive, unable to directly lyse melanoma target cells or produce cytokines in response to mitogens. In contrast, CD8+ T cells from the same patient were able to lyse EBV-pulsed target cells and showed robust allogeneic responses. Thus, the clonally expanded TAA-specific population seems to have been selectively rendered anergic in vivo. Peptide stimulation of the TAA-specific T-cell populations in other patients failed to induce substantial upregulation of CD69 expression, indicating that these cells may also have functional defects, leading to blunted activation responses. These data demonstrate that systemic TAA-specific T-cell responses can develop de novo in cancer patients, but that antigen-specific unresponsiveness may explain why such cells are unable to control tumor growth.

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Detection of low avidity CD8(+) T cell populations with coreceptor-enhanced peptide-major histocompatibility complex class I tetramers. J Joseph Melenhorst, Phillip Scheinberg, +12 authors, David A Price. less J Immunol Methods, 2008 Aug 05; 338(1-2). PMID: 18675271 Free PMC article.
Rapid tolerization of virus-activated tumor-specific CD8+ T cells in prostate tumors of TRAMP mice. Ailin Bai, Eileen Higham, +2 authors, Herman N Eisen, K Dane Wittrup, Jianzhu Chen. less Proc Natl Acad Sci U S A, 2008 Aug 30; 105(35). PMID: 18723683 Free PMC article.
Label-free electronic detection of the antigen-specific T-cell immune response. Eric Stern, Erin R Steenblock, Mark A Reed, Tarek M Fahmy. Nano Lett, 2008 Sep 04; 8(10). PMID: 18763834 Free PMC article.
Post-transplant adoptive T-cell immunotherapy. Nicole A Aqui, Carl H June. Best Pract Res Clin Haematol, 2008 Sep 16; 21(3). PMID: 18790452 Free PMC article. Review.
Techniques to improve the direct ex vivo detection of low frequency antigen-specific CD8+ T cells with peptide-major histocompatibility complex class I tetramers. Pratip K Chattopadhyay, J Joseph Melenhorst, +7 authors, David A Price. less Cytometry A, 2008 Oct 07; 73(11). PMID: 18836993 Free PMC article. Review.
Targeting minor histocompatibility antigens in graft versus tumor or graft versus leukemia responses. Xin Feng, Kwok Min Hui, Hashem M Younes, Anthony G Brickner. Trends Immunol, 2008 Oct 28; 29(12). PMID: 18952501 Free PMC article. Review.
Ex vivo characterization of polyclonal memory CD8+ T-cell responses to PRAME-specific peptides in patients with acute lymphoblastic leukemia and acute and chronic myeloid leukemia. Katayoun Rezvani, Agnes S M Yong, +8 authors, A John Barrett. less Blood, 2008 Nov 08; 113(10). PMID: 18988867 Free PMC article.
Behavior of immune players in the tumor microenvironment. Mikael J Pittet. Curr Opin Oncol, 2009 Jan 07; 21(1). PMID: 19125019 Free PMC article. Review.
Impact of epitope escape on PD-1 expression and CD8 T-cell exhaustion during chronic infection. Joseph N Blattman, E John Wherry, +2 authors, Sang-Jun Ha, Robbert G van der Most, Rafi Ahmed. less J Virol, 2009 Feb 13; 83(9). PMID: 19211743 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.
Predicting and controlling the reactivity of immune cell populations against cancer. Kfir Oved, Eran Eden, +11 authors, Yoram Reiter. less Mol Syst Biol, 2009 Apr 30; 5. PMID: 19401677 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.
Impaired interferon signaling is a common immune defect in human cancer. Rebecca J Critchley-Thorne, Diana L Simons, +9 authors, Peter P Lee. less Proc Natl Acad Sci U S A, 2009 May 20; 106(22). PMID: 19451644 Free PMC article. Highly Cited.
Emerging concepts in biomarker discovery; the US-Japan Workshop on Immunological Molecular Markers in Oncology. Hideaki Tahara, Marimo Sato, +53 authors, Francesco M Marincola. less J Transl Med, 2009 Jun 19; 7. PMID: 19534815 Free PMC article.
PD1 blockade reverses the suppression of melanoma antigen-specific CTL by CD4+ CD25(Hi) regulatory T cells. Wenshi Wang, Roy Lau, +3 authors, Daohai Yu, Weiwei Zhu, Alan Korman, Jeffrey Weber. less Int Immunol, 2009 Aug 05; 21(9). PMID: 19651643 Free PMC article. Highly Cited.
Betting on immunotherapy for melanoma. Mario Sznol. Curr Oncol Rep, 2009 Aug 15; 11(5). PMID: 19679015 Review.
Dendritic cell vaccination combined with CTLA4 blockade in patients with metastatic melanoma. Antoni Ribas, Begoña Comin-Anduix, +15 authors, Jesus Gomez-Navarro. less Clin Cancer Res, 2009 Oct 01; 15(19). PMID: 19789309 Free PMC article.
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.
Targeting lymphotoxin-mediated negative selection to prevent prostate cancer in mice with genetic predisposition. Penghui Zhou, Xianfeng Fang, +6 authors, Pan Zheng. less Proc Natl Acad Sci U S A, 2009 Oct 07; 106(40). PMID: 19805094 Free PMC article.
Immune responses to malignancies. Theresa L Whiteside. J Allergy Clin Immunol, 2010 Jan 12; 125(2 Suppl 2). PMID: 20061007 Free PMC article. Review.
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.
T-cell exhaustion: characteristics, causes and conversion. John S Yi, Maureen A Cox, Allan J Zajac. Immunology, 2010 Mar 06; 129(4). PMID: 20201977 Free PMC article. Highly Cited. Review.
Enhanced CD8 T cell cross-presentation by macrophages with targeted disruption of STAT3. Jason Brayer, Fengdong Cheng, +4 authors, Eduardo M Sotomayor. less Immunol Lett, 2010 Mar 30; 131(2). PMID: 20346983 Free PMC article.
Shaping successful and unsuccessful CD8 T cell responses following infection. Maureen A Cox, Allan J Zajac. J Biomed Biotechnol, 2010 Apr 10; 2010. PMID: 20379363 Free PMC article. Review.
Inhibiting the inhibitors: evaluating agents targeting cancer immunosuppression. Theresa L Whiteside. Expert Opin Biol Ther, 2010 Apr 27; 10(7). PMID: 20415597 Free PMC article. Review.
Dendritic cell subsets as vectors and targets for improved cancer therapy. Karolina Palucka, Hideki Ueno, +2 authors, Lee Roberts, Joseph Fay, Jacques Banchereau. less Curr Top Microbiol Immunol, 2010 May 22; 344. PMID: 20490776 Free PMC article. Review.
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.
IFN-γ upregulates survivin and Ifi202 expression to induce survival and proliferation of tumor-specific T cells. Mary Zimmerman, Dafeng Yang, +8 authors, Kebin Liu. less PLoS One, 2010 Dec 03; 5(11). PMID: 21124930 Free PMC article.
Mechanisms of T-cell protection from death by IRX-2: a new immunotherapeutic. Malgorzata Czystowska, Miroslaw J Szczepanski, +4 authors, Theresa L Whiteside. less Cancer Immunol Immunother, 2010 Dec 25; 60(4). PMID: 21181158 Free PMC article.
Development of an attenuated interleukin-2 fusion protein that can be activated by tumour-expressed proteases. John Puskas, Denise Skrombolas, +3 authors, John Frelinger. less Immunology, 2011 Mar 24; 133(2). PMID: 21426339 Free PMC article.
Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Arne N Akbar, Sian M Henson. Nat Rev Immunol, 2011 Mar 26; 11(4). PMID: 21436838 Highly Cited.
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.
Monitoring the systemic human memory B cell compartment of melanoma patients for anti-tumor IgG antibodies. Amy E Gilbert, Panagiotis Karagiannis, +16 authors, Sophia N Karagiannis. less PLoS One, 2011 May 12; 6(4). PMID: 21559411 Free PMC article.
A clinical microchip for evaluation of single immune cells reveals high functional heterogeneity in phenotypically similar T cells. Chao Ma, Rong Fan, +9 authors, James R Heath. less Nat Med, 2011 May 24; 17(6). PMID: 21602800 Free PMC article. Highly Cited.
T cell surveillance of oncogene-induced prostate cancer is impeded by T cell-derived TGF-β1 cytokine. Moses K Donkor, Abira Sarkar, +5 authors, Ming O Li. less Immunity, 2011 Jul 16; 35(1). PMID: 21757379 Free PMC article.
Interrogating the repertoire: broadening the scope of peptide-MHC multimer analysis. Mark M Davis, John D Altman, Evan W Newell. Nat Rev Immunol, 2011 Jul 16; 11(8). PMID: 21760610 Free PMC article. Review.
Why Do CD8+ T Cells become Indifferent to Tumors: A Dynamic Modeling Approach. Colin Campbell, Ranran Zhang, +5 authors, Juilee Thakar. less Front Physiol, 2011 Aug 03; 2. PMID: 21808621 Free PMC article.
A broadly applicable approach to T cell epitope identification: application to improving tumor associated epitopes and identifying epitopes in complex pathogens. Michael D Valentino, C Siddiq Abdul-Alim, +7 authors, John G Frelinger. less J Immunol Methods, 2011 Aug 30; 373(1-2). PMID: 21872603 Free PMC article.
Elevated tumor-associated antigen expression suppresses variant peptide vaccine responses. Charles B Kemmler, Eric T Clambey, Ross M Kedl, Jill E Slansky. J Immunol, 2011 Sep 24; 187(9). PMID: 21940675 Free PMC article.
Direct activation of antigen-presenting cells is required for CD8+ T-cell priming and tumor vaccination. Wolfgang Kratky, Caetano Reis e Sousa, Annette Oxenius, Roman Spörri. Proc Natl Acad Sci U S A, 2011 Oct 12; 108(42). PMID: 21987815 Free PMC article.
Function but not phenotype of melanoma peptide-specific CD8(+) T cells correlate with survival in a multiepitope peptide vaccine trial (ECOG 1696). Carsten Schaefer, Lisa H Butterfield, +5 authors, Theresa L Whiteside. less Int J Cancer, 2011 Oct 25; 131(4). PMID: 22021080 Free PMC article.
Deconvolving heterogeneity in the CD8+ T-cell response to HIV. W Nicholas Haining, R Anthony Barnitz. Curr Opin HIV AIDS, 2011 Dec 14; 7(1). PMID: 22156844 Free PMC article. Review.
Phase I trial of "bi-shRNAi(furin)/GMCSF DNA/autologous tumor cell" vaccine (FANG) in advanced cancer. Neil Senzer, Minal Barve, +23 authors, John Nemunaitis. less Mol Ther, 2011 Dec 22; 20(3). PMID: 22186789 Free PMC article.
Melanoma: new insights and new therapies. Vasiliki A Nikolaou, Alexander J Stratigos, Keith T Flaherty, Hensin Tsao. J Invest Dermatol, 2012 Jan 06; 132(3 Pt 2). PMID: 22217739 Free PMC article. Review.
T cell- but not tumor cell-produced TGF-β1 promotes the development of spontaneous mammary cancer. Abira Sarkar, Moses K Donkor, Ming O Li. Oncotarget, 2012 Jan 18; 2(12). PMID: 22248703 Free PMC article.
Neoplastic "Black Ops": cancer's subversive tactics in overcoming host defenses. Arya Biragyn, Dan L Longo. Semin Cancer Biol, 2012 Jan 20; 22(1). PMID: 22257681 Free PMC article. Review.
Agonistic antibody to CD40 boosts the antitumor activity of adoptively transferred T cells in vivo. Chengwen Liu, Carol M Lewis, +8 authors, Patrick Hwu. less J Immunother, 2012 Mar 17; 35(3). PMID: 22421945 Free PMC article.
Marginating dendritic cells of the tumor microenvironment cross-present tumor antigens and stably engage tumor-specific T cells. John J Engelhardt, Bijan Boldajipour, +5 authors, Matthew F Krummel. less Cancer Cell, 2012 Mar 24; 21(3). PMID: 22439936 Free PMC article. Highly Cited.
Positive and negative regulation of cellular immune responses in physiologic conditions and diseases. S Viganò, M Perreau, G Pantaleo, A Harari. Clin Dev Immunol, 2012 May 02; 2012. PMID: 22548114 Free PMC article. Review.
Reflections upon human cancer immune responsiveness to T cell-based therapy. Ena Wang, Sara Tomei, Francesco M Marincola. Cancer Immunol Immunother, 2012 May 12; 61(6). PMID: 22576055 Free PMC article. Review.
Intracellular signal transduction and modification of the tumor microenvironment induced by RET/PTCs in papillary thyroid carcinoma. Elisa Menicali, Sonia Moretti, +3 authors, Efisio Puxeddu. less Front Endocrinol (Lausanne), 2012 Jun 05; 3. PMID: 22661970 Free PMC article.
Tgf-β1 produced by activated CD4(+) T Cells Antagonizes T Cell Surveillance of Tumor Development. Moses K Donkor, Abira Sarkar, Ming O Li. Oncoimmunology, 2012 Jun 22; 1(2). PMID: 22720237 Free PMC article.
NFAT1 supports tumor-induced anergy of CD4(+) T cells. Brian T Abe, Daniel S Shin, Enric Mocholi, Fernando Macian. Cancer Res, 2012 Aug 07; 72(18). PMID: 22865456 Free PMC article.
CD160 and PD-1 co-expression on HIV-specific CD8 T cells defines a subset with advanced dysfunction. Yoav Peretz, Zhong He, +14 authors, Rafick-Pierre Sékaly. less PLoS Pathog, 2012 Aug 24; 8(8). PMID: 22916009 Free PMC article.
Improving T cell responses to modified peptides in tumor vaccines. Jonathan D Buhrman, Jill E Slansky. Immunol Res, 2012 Sep 01; 55(1-3). PMID: 22936035 Free PMC article. Review.
Augmenting antitumor T-cell responses to mimotope vaccination by boosting with native tumor antigens. Jonathan D Buhrman, Kimberly R Jordan, +3 authors, Jill E Slansky. less Cancer Res, 2012 Nov 20; 73(1). PMID: 23161490 Free PMC article.
Inefficient boosting of antitumor CD8(+) T cells by dendritic-cell vaccines is rescued by restricting T-cell cytotoxic functions. Joel Zhi-Iong Ma, Jianping Yang, +5 authors, Franca Ronchese. less Oncoimmunology, 2012 Dec 25; 1(9). PMID: 23264897 Free PMC article.
Enhanced function of cytotoxic T lymphocytes induced by dendritic cells modified with truncated PSMA and 4-1BBL. Kuang Youlin, Zhang Li, +3 authors, Gou Xin, Xiao Mingchao, Liu Xiuheng, Weng Xiaodong. less Hum Vaccin Immunother, 2013 Jan 09; 9(4). PMID: 23295983 Free PMC article.
KIR gene variability in cutaneous malignant melanoma: influence of KIR2D/HLA-C pairings on disease susceptibility and prognosis. José A Campillo, Isabel Legaz, +10 authors, Jorge A Martínez-Escribano. less Immunogenetics, 2013 Feb 02; 65(5). PMID: 23370861
Targeted therapy and immunotherapy in advanced melanoma: an evolving paradigm. Muhammad Khattak, Rosalie Fisher, Samra Turajlic, James Larkin. Ther Adv Med Oncol, 2013 Mar 02; 5(2). PMID: 23450149 Free PMC article.
Betting on improved cancer immunotherapy by doubling down on CD134 and CD137 co-stimulation. Adam J Adler, Anthony T Vella. Oncoimmunology, 2013 Mar 14; 2(1). PMID: 23482891 Free PMC article.
PD-1 coinhibitory signals: the link between pathogenesis and protection. Deanna A Kulpa, Mariam Lawani, +3 authors, Rafick-Pierre Sékaly. less Semin Immunol, 2013 Apr 04; 25(3). PMID: 23548749 Free PMC article. Review.
Antitumor effects of chimeric receptor engineered human T cells directed to tumor stroma. Sunitha Kakarla, Kevin K H Chow, +8 authors, Stephen Gottschalk. less Mol Ther, 2013 Jun 05; 21(8). PMID: 23732988 Free PMC article. Highly Cited.
Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Stefani Spranger, Robbert M Spaapen, +4 authors, Thomas F Gajewski. less Sci Transl Med, 2013 Aug 30; 5(200). PMID: 23986400 Free PMC article. Highly Cited.
Sindbis viral vectors transiently deliver tumor-associated antigens to lymph nodes and elicit diversified antitumor CD8+ T-cell immunity. Tomer Granot, Yoshihide Yamanashi, Daniel Meruelo. Mol Ther, 2013 Sep 13; 22(1). PMID: 24025748 Free PMC article.
Allogeneic tumor cell vaccines: the promise and limitations in clinical trials. Sanjay Srivatsan, Jaina M Patel, +4 authors, Periasamy Selvaraj. less Hum Vaccin Immunother, 2013 Sep 26; 10(1). PMID: 24064957 Free PMC article. Review.
Stem cells and targeted approaches to melanoma cure. George F Murphy, Brian J Wilson, +2 authors, Sasha D Girouard, Natasha Y Frank, Markus H Frank. less Mol Aspects Med, 2013 Oct 23; 39. PMID: 24145241 Free PMC article. Review.
Testing for HLA/peptide tetramer-binding to the T cell receptor complex on human T lymphocytes. Pauline Weder, Ton N M Schumacher, Hergen Spits, Rosalie M Luiten. Results Immunol, 2012 Jan 01; 2. PMID: 24371571 Free PMC article.
Monitoring the immune competence of cancer patients to predict outcome. Serena Chang, Holbrook Kohrt, Holden T Maecker. Cancer Immunol Immunother, 2014 Feb 04; 63(7). PMID: 24487923 Free PMC article. Review.
High-dimensional single-cell cancer biology. Jonathan M Irish, Deon B Doxie. Curr Top Microbiol Immunol, 2014 Mar 29; 377. PMID: 24671264 Free PMC article. Review.
Melanoma NOS1 expression promotes dysfunctional IFN signaling. Qiuzhen Liu, Sara Tomei, +19 authors, Francesco M Marincola. less J Clin Invest, 2014 Apr 03; 124(5). PMID: 24691438 Free PMC article.
ELISPOT Assay for Monitoring Cytotoxic T Lymphocytes (CTL) Activity in Cancer Vaccine Clinical Trials. Anatoli M Malyguine, Susan Strobl, +2 authors, Kimberly Dunham, Michael R Shurin, Thomas J Sayers. less Cells, 2012 Jan 01; 1(2). PMID: 24710418 Free PMC article.
Shaping the repertoire of tumor-infiltrating effector and regulatory T cells. Peter A Savage, Daniel S Leventhal, Sven Malchow. Immunol Rev, 2014 Apr 10; 259(1). PMID: 24712470 Free PMC article. Review.
Control of the immune response by pro-angiogenic factors. Thibault Voron, Elie Marcheteau, +4 authors, Magali Terme. less Front Oncol, 2014 Apr 26; 4. PMID: 24765614 Free PMC article. Highly Cited. Review.
Targeting fibroblast activation protein in tumor stroma with chimeric antigen receptor T cells can inhibit tumor growth and augment host immunity without severe toxicity. Liang-Chuan S Wang, Albert Lo, +11 authors, Steven M Albelda. less Cancer Immunol Res, 2014 Apr 30; 2(2). PMID: 24778279 Free PMC article. Highly Cited.
Immune responses in a mouse model of vitiligo with spontaneous epidermal de- and repigmentation. Jonathan M Eby, Hee-Kap Kang, +8 authors, I Caroline Le Poole. less Pigment Cell Melanoma Res, 2014 Jun 18; 27(6). PMID: 24935676 Free PMC article.
Targeting CD8+ T-cell tolerance for cancer immunotherapy. Stephanie R Jackson, Jinyun Yuan, Ryan M Teague. Immunotherapy, 2014 Oct 08; 6(7). PMID: 25290416 Free PMC article. Review.
Treatment of unresectable stage IV metastatic melanoma with aviscumine after anti-neoplastic treatment failure: a phase II, multi-centre study. Uwe Trefzer, Ralf Gutzmer, +6 authors, Peter Mohr. less J Immunother Cancer, 2014 Oct 18; 2. PMID: 25324973 Free PMC article.
Immune response in thyroid cancer: widening the boundaries. Laura Sterian Ward. Scientifica (Cairo), 2014 Oct 21; 2014. PMID: 25328756 Free PMC article. Review.
To affinity and beyond: harnessing the T cell receptor for cancer immunotherapy. Jessica E Thaxton, Zihai Li. Hum Vaccin Immunother, 2014 Dec 09; 10(11). PMID: 25483644 Free PMC article. Review.
Current advances in T-cell-based cancer immunotherapy. Mingjun Wang, Bingnan Yin, Helen Y Wang, Rong-Fu Wang. Immunotherapy, 2014 Dec 20; 6(12). PMID: 25524383 Free PMC article. Review.
Immune profiling and cancer post transplantation. Christopher Martin Hope, Patrick Toby H Coates, Robert Peter Carroll. World J Nephrol, 2015 Feb 11; 4(1). PMID: 25664246 Free PMC article. Review.
Overcoming T cell exhaustion in infection and cancer. Kristen E Pauken, E John Wherry. Trends Immunol, 2015 Mar 24; 36(4). PMID: 25797516 Free PMC article. Highly Cited. Review.
MHC class I chain-related gene a diversity in patients with cutaneous malignant melanoma from southeastern Spain. José Antonio Campillo, Ruth López-Hernández, +13 authors, Manuel Muro. less Dis Markers, 2015 Apr 04; 2015. PMID: 25838620 Free PMC article.
An exhaustion-like phenotype constrains the activity of CD4+ T cells specific for a self and melanoma antigen. Matthew P Rausch, Karen Taraszka Hastings. PLoS One, 2015 Apr 16; 10(4). PMID: 25875653 Free PMC article.
Melanoma-derived factors alter the maturation and activation of differentiated tissue-resident dendritic cells. Kristian M Hargadon, Johnathan D Bishop, +3 authors, Osric A Forrest. less Immunol Cell Biol, 2015 May 27; 94(1). PMID: 26010746
Prognostic value of neutrophil-to-lymphocyte ratio in breast cancer. Jie Chen, Qiwen Deng, +5 authors, Shukui Wang. less FEBS Open Bio, 2015 Jul 03; 5. PMID: 26137435 Free PMC article.
Blockade of Programmed Death 1 Augments the Ability of Human T Cells Engineered to Target NY-ESO-1 to Control Tumor Growth after Adoptive Transfer. Edmund K Moon, Raghuveer Ranganathan, +7 authors, Steven M Albelda. less Clin Cancer Res, 2015 Sep 02; 22(2). PMID: 26324743 Free PMC article.
Targeting cryptic epitope with modified antigen coupled to the surface of liposomes induces strong antitumor CD8 T-cell immune responses in vivo. Yutaka Horiuchi, Akira Takagi, Tetsuya Uchida, Toshitaka Akatsuka. Oncol Rep, 2015 Sep 24; 34(6). PMID: 26398429 Free PMC article.
Screening and Molecular Analysis of Single Circulating Tumor Cells Using Micromagnet Array. Yu-Yen Huang, Peng Chen, +7 authors, John X J Zhang. less Sci Rep, 2015 Nov 06; 5. PMID: 26538094 Free PMC article.
A high density of tertiary lymphoid structure B cells in lung tumors is associated with increased CD4+ T cell receptor repertoire clonality. Wei Zhu, Claire Germain, +12 authors, Brandon W Higgs. less Oncoimmunology, 2015 Nov 21; 4(12). PMID: 26587322 Free PMC article.
Tailoring the Treatment of Melanoma: Implications for Personalized Medicine. Linna Duan, Eric M Mukherjee, Deepak Narayan. Yale J Biol Med, 2015 Nov 26; 88(4). PMID: 26604863 Free PMC article. Review.
Obligate anaerobic Salmonella typhimurium strain YB1 treatment on xenograft tumor in immunocompetent mouse model. Bin Yu, Lei Shi, +4 authors, Jun-LE Qu. less Oncol Lett, 2015 Dec 02; 10(2). PMID: 26622627 Free PMC article.
Single-cell analysis tools for drug discovery and development. James R Heath, Antoni Ribas, Paul S Mischel. Nat Rev Drug Discov, 2015 Dec 17; 15(3). PMID: 26669673 Free PMC article. Highly Cited. Review.
Low-Intensity Focused Ultrasound Induces Reversal of Tumor-Induced T Cell Tolerance and Prevents Immune Escape. Sanmay Bandyopadhyay, Thomas J Quinn, +5 authors, Chandan Guha. less J Immunol, 2016 Jan 13; 196(4). PMID: 26755821 Free PMC article.
Rational bases for the use of the Immunoscore in routine clinical settings as a prognostic and predictive biomarker in cancer patients. Amos Kirilovsky, Florence Marliot, +3 authors, Franck Pagès. less Int Immunol, 2016 Apr 29; 28(8). PMID: 27121213 Free PMC article. Highly Cited. Review.
Anticancer DNA vaccine based on human telomerase reverse transcriptase generates a strong and specific T cell immune response. Jessie Thalmensi, Elodie Pliquet, +12 authors, Pierre Langlade-Demoyen. less Oncoimmunology, 2016 May 04; 5(3). PMID: 27141336 Free PMC article.
Mechanistic insights into the oncolytic activity of vesicular stomatitis virus in cancer immunotherapy. Boris Simovic, Scott R Walsh, Yonghong Wan. Oncolytic Virother, 2015 Jan 01; 4. PMID: 27512679 Free PMC article. Review.
Regulatory circuits of T cell function in cancer. Daniel E Speiser, Ping-Chih Ho, Grégory Verdeil. Nat Rev Immunol, 2016 Aug 17; 16(10). PMID: 27526640 Highly Cited. Review.
Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Qian Chen, Ligeng Xu, +3 authors, Chao Liang, Chao Wang, Rui Peng, Zhuang Liu. less Nat Commun, 2016 Oct 22; 7. PMID: 27767031 Free PMC article. Highly Cited.
Cell-Intrinsic Barriers of T Cell-Based Immunotherapy. Hazem E Ghoneim, Anthony E Zamora, Paul G Thomas, Ben A Youngblood. Trends Mol Med, 2016 Nov 09; 22(12). PMID: 27825667 Free PMC article. Review.
Tumor-infiltrating lymphocytes are dynamically desensitized to antigen but are maintained by homeostatic cytokine. Bijan Boldajipour, Amanda Nelson, Matthew F Krummel. JCI Insight, 2016 Dec 13; 1(20). PMID: 27942588 Free PMC article.
The Role of the Tumor Vasculature in the Host Immune Response: Implications for Therapeutic Strategies Targeting the Tumor Microenvironment. Shona A Hendry, Rae H Farnsworth, +3 authors, Stephen B Fox. less Front Immunol, 2017 Jan 10; 7. PMID: 28066431 Free PMC article. Highly Cited. Review.
T cell exhaustion: from pathophysiological basics to tumor immunotherapy. Kemal Catakovic, Eckhard Klieser, Daniel Neureiter, Roland Geisberger. Cell Commun Signal, 2017 Jan 12; 15(1). PMID: 28073373 Free PMC article. Highly Cited. Review.
The Principles of Engineering Immune Cells to Treat Cancer. Wendell A Lim, Carl H June. Cell, 2017 Feb 12; 168(4). PMID: 28187291 Free PMC article. Highly Cited. Review.
Preparing Viable Single Cells from Human Tissue and Tumors for Cytomic Analysis. Nalin Leelatian, Deon B Doxie, +3 authors, Jonathan M Irish. less Curr Protoc Mol Biol, 2017 Apr 04; 118. PMID: 28369679 Free PMC article.
Immune surveillance in melanoma: From immune attack to melanoma escape and even counterattack. Fade Mahmoud, Bradley Shields, +5 authors, Alan J Tackett. less Cancer Biol Ther, 2017 May 18; 18(7). PMID: 28513269 Free PMC article. Review.
Expanding Role of T Cells in Human Autoimmune Diseases of the Central Nervous System. Deepti Pilli, Alicia Zou, +2 authors, Fiona Tea, Russell C Dale, Fabienne Brilot. less Front Immunol, 2017 Jun 24; 8. PMID: 28638382 Free PMC article. Review.
The Antitumor Effects of Vaccine-Activated CD8+ T Cells Associate with Weak TCR Signaling and Induction of Stem-Like Memory T Cells. Sha Wu, Wei Zhu, +11 authors, Yukai He. less Cancer Immunol Res, 2017 Aug 31; 5(10). PMID: 28851693 Free PMC article.
Differential Inhibitory Receptor Expression on T Cells Delineates Functional Capacities in Chronic Viral Infection. Jeffrey E Teigler, Gennadiy Zelinskyy, +11 authors, Hendrik Streeck. less J Virol, 2017 Sep 15; 91(23). PMID: 28904197 Free PMC article.
Overcoming resistance to targeted therapy with immunotherapy and combination therapy for metastatic melanoma. Hilary R Keller, Xin Zhang, +2 authors, Li Li, Helmut Schaider, James W Wells. less Oncotarget, 2017 Nov 02; 8(43). PMID: 29088901 Free PMC article. Review.
Management of intracranial melanomas in the era of precision medicine. Grace J Young, Wenya Linda Bi, +3 authors, Ian F Dunn. less Oncotarget, 2017 Nov 29; 8(51). PMID: 29179523 Free PMC article. Review.
T-Cell Exhaustion Signatures Vary with Tumor Type and Are Severe in Glioblastoma. Karolina Woroniecka, Pakawat Chongsathidkiet, +19 authors, Peter E Fecci. less Clin Cancer Res, 2018 Feb 14; 24(17). PMID: 29437767 Free PMC article. Highly Cited.
Exhaustion of the CD8+ T Cell Compartment in Patients with Mutations in Phosphoinositide 3-Kinase Delta. Marjolein W J Wentink, Yvonne M Mueller, +5 authors, Peter D Katsikis. less Front Immunol, 2018 Mar 23; 9. PMID: 29563914 Free PMC article.
Current Strategies to Enhance Anti-Tumour Immunity. Katherine W Cook, Lindy G Durrant, Victoria A Brentville. Biomedicines, 2018 Mar 24; 6(2). PMID: 29570634 Free PMC article. Review.
T-cell Dysfunction in Glioblastoma: Applying a New Framework. Karolina I Woroniecka, Kristen E Rhodin, +2 authors, Peter E Fecci. less Clin Cancer Res, 2018 Mar 30; 24(16). PMID: 29593027 Free PMC article. Highly Cited. Review.
IL-27 gene therapy induces depletion of Tregs and enhances the efficacy of cancer immunotherapy. Jianmin Zhu, Jin-Qing Liu, +11 authors, Xue-Feng Bai. less JCI Insight, 2018 Apr 06; 3(7). PMID: 29618655 Free PMC article.
A cancer vaccine-mediated postoperative immunotherapy for recurrent and metastatic tumors. Tingting Wang, Dangge Wang, +6 authors, Yaping Li. less Nat Commun, 2018 Apr 20; 9(1). PMID: 29670088 Free PMC article.
Human T-cell lymphotropic/leukemia virus type 1 (HTLV-1) Tax-specific T-cell exhaustion in HTLV-1-infected individuals. Ayako Masaki, Takashi Ishida, +9 authors, Shinsuke Iida. less Cancer Sci, 2018 May 31; 109(8). PMID: 29845702 Free PMC article.
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