Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma

Ying Xie ¹, Akgül Akpinarli , Charles Maris , Edward L Hipkiss , Malcolm Lane , Eun-Kyung M Kwon , Pawel Muranski , Nicholas P Restifo , Paul Andrew Antony

Affiliations

¹ Program in Molecular Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.

PMID: 20156973
86 References
216 citations

Abstract

In vitro differentiated CD8(+) T cells have been the primary focus of immunotherapy of cancer with little focus on CD4(+) T cells. Immunotherapy involving in vitro differentiated T cells given after lymphodepleting regimens significantly augments antitumor immunity in animals and human patients with cancer. However, the mechanisms by which lymphopenia augments adoptive cell therapy and the means of properly differentiating T cells in vitro are still emerging. We demonstrate that naive tumor/self-specific CD4(+) T cells naturally differentiated into T helper type 1 cytotoxic T cells in vivo and caused the regression of established tumors and depigmentation in lymphopenic hosts. Therapy was independent of vaccination, exogenous cytokine support, CD8(+), B, natural killer (NK), and NKT cells. Proper activation of CD4(+) T cells in vivo was important for tumor clearance, as naive tumor-specific CD4(+) T cells could not completely treat tumor in lymphopenic common gamma chain (gamma(c))-deficient hosts. gamma(c) signaling in the tumor-bearing host was important for survival and proper differentiation of adoptively transferred tumor-specific CD4(+) T cells. Thus, these data provide a platform for designing immunotherapies that incorporate tumor/self-reactive CD4(+) T cells.

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Cytotoxic CD4 T cells in antiviral immunity. Nikki B Marshall, Susan L Swain. J Biomed Biotechnol, 2011 Dec 17; 2011. PMID: 22174559 Free PMC article. Review.
Th17 cells are long lived and retain a stem cell-like molecular signature. Pawel Muranski, Zachary A Borman, +19 authors, Nicholas P Restifo. less Immunity, 2011 Dec 20; 35(6). PMID: 22177921 Free PMC article. Highly Cited.
Development of a DNA vaccine targeting Merkel cell polyomavirus. Qi Zeng, Bianca P Gomez, +5 authors, Chien-Fu Hung. less Vaccine, 2012 Jan 03; 30(7). PMID: 22210138 Free PMC article.
Adoptive cell therapy for lymphoma with CD4 T cells depleted of CD137-expressing regulatory T cells. Matthew J Goldstein, Holbrook E Kohrt, +4 authors, Ronald Levy. less Cancer Res, 2012 Jan 11; 72(5). PMID: 22232735 Free PMC article.
Treatment with targeted vesicular stomatitis virus generates therapeutic multifunctional anti-tumor memory CD4 T cells. Y Gao, P Whitaker-Dowling, J A Griffin, I Bergman. Cancer Gene Ther, 2012 Jan 14; 19(4). PMID: 22240921 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.
Induction of MAGE-A3 and HPV-16 immunity by Trojan vaccines in patients with head and neck carcinoma. Caroline J Voskens, Duane Sewell, +15 authors, Scott E Strome. less Head Neck, 2012 Jan 31; 34(12). PMID: 22287423 Free PMC article.
Complementary costimulation of human T-cell subpopulations by cluster of differentiation 28 (CD28) and CD81. Yael Sagi, Angela Landrigan, Ronald Levy, Shoshana Levy. Proc Natl Acad Sci U S A, 2012 Feb 07; 109(5). PMID: 22307619 Free PMC article.
Cellular and molecular requirements for rejection of B16 melanoma in the setting of regulatory T cell depletion and homeostatic proliferation. Justin Kline, Long Zhang, +2 authors, Lauren Battaglia, Kenneth S Cohen, Thomas F Gajewski. less J Immunol, 2012 Feb 09; 188(6). PMID: 22312128 Free PMC article.
Activation of a helper and not regulatory human CD4+ T cell response by oncolytic H-1 parvovirus. Olivier Moralès, Audrey Richard, +8 authors, Nadira Delhem. less PLoS One, 2012 Feb 24; 7(2). PMID: 22359669 Free PMC article.
Targeting of the non-mutated tumor antigen HER2/neu to mature dendritic cells induces an integrated immune response that protects against breast cancer in mice. Bei Wang, Neeha Zaidi, +4 authors, Ralph M Steinman. less Breast Cancer Res, 2012 Mar 09; 14(2). PMID: 22397502 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.
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.
Immunoglobulin Fc fragment tagging allows strong activation of endogenous CD4 T cells to reshape the tumor milieu and enhance the antitumor effect of lentivector immunization. Yuan Hong, Yibing Peng, +3 authors, Haiyan Xiao, Michael Mi, David Munn, Yukai He. less J Immunol, 2012 Apr 17; 188(10). PMID: 22504640 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.
A systematic analysis of experimental immunotherapies on tumors differing in size and duration of growth. Frank T Wen, Ronald A Thisted, Donald A Rowley, Hans Schreiber. Oncoimmunology, 2012 Jun 22; 1(2). PMID: 22720238 Free PMC article.
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.
Robust tumor immunity to melanoma mediated by interleukin-9-producing T cells. Rahul Purwar, Christoph Schlapbach, +9 authors, Thomas S Kupper. less Nat Med, 2012 Jul 10; 18(8). PMID: 22772464 Free PMC article. Highly Cited.
A coreceptor-independent transgenic human TCR mediates anti-tumor and anti-self immunity in mice. Shikhar Mehrotra, Amir A Al-Khami, +15 authors, Michael I Nishimura. less J Immunol, 2012 Jul 17; 189(4). PMID: 22798675 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.
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.
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.
Widespread CD4+ T-cell reactivity to novel hTERT epitopes following vaccination of cancer patients with a single hTERT peptide GV1001. Else-Marit Inderberg-Suso, Sissel Trachsel, +2 authors, Kari Lislerud, Anne-Marie Rasmussen, Gustav Gaudernack. less Oncoimmunology, 2012 Aug 31; 1(5). PMID: 22934259 Free PMC article.
Induction of tumoricidal function in CD4+ T cells is associated with concomitant memory and terminally differentiated phenotype. Daniel Hirschhorn-Cymerman, Sadna Budhu, +10 authors, Jedd D Wolchok. less J Exp Med, 2012 Sep 26; 209(11). PMID: 23008334 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.
Anti-tumor immunity: myeloid leukocytes control the immune landscape. Melanie R Rutkowski, Tom L Stephen, Jose R Conejo-Garcia. Cell Immunol, 2012 Nov 06; 278(1-2). PMID: 23121972 Free PMC article. Review.
A20 controls macrophage to elicit potent cytotoxic CD4(+) T cell response. Lifeng Wang, Bangxing Hong, +3 authors, Xue F Huang. less PLoS One, 2012 Nov 13; 7(11). PMID: 23145026 Free PMC article.
Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. Jing Ni, Matthias Miller, +2 authors, Ana Stojanovic, Natalio Garbi, Adelheid Cerwenka. less J Exp Med, 2012 Dec 05; 209(13). PMID: 23209317 Free PMC article. Highly Cited.
CD134/CD137 dual costimulation-elicited IFN-γ maximizes effector T-cell function but limits Treg expansion. Marie-Clare St Rose, Roslyn A Taylor, +4 authors, Adam J Adler. less Immunol Cell Biol, 2013 Jan 09; 91(2). PMID: 23295363 Free PMC article.
ATM-dependent spontaneous regression of early Eμ-myc-induced murine B-cell leukemia depends on natural killer and T cells. J Ludovic Croxford, Melissa Li Fang Tang, +7 authors, Stephan Gasser. less Blood, 2013 Jan 26; 121(13). PMID: 23349395 Free PMC article.
Aire deficiency promotes TRP-1-specific immune rejection of melanoma. Meng-Lei Zhu, Anil Nagavalli, Maureen A Su. Cancer Res, 2013 Feb 02; 73(7). PMID: 23370329 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.
Expanding roles for CD4 T cells and their subpopulations in tumor immunity and therapy. Mark J Dobrzanski. Front Oncol, 2013 Mar 28; 3. PMID: 23533029 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.
Systemic 4-1BB activation induces a novel T cell phenotype driven by high expression of Eomesodermin. Michael A Curran, Theresa L Geiger, +5 authors, James P Allison. less J Exp Med, 2013 Apr 03; 210(4). PMID: 23547098 Free PMC article. Highly Cited.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada. less J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981 Free PMC article. Highly Cited.
Low immunogenicity of neural progenitor cells differentiated from induced pluripotent stem cells derived from less immunogenic somatic cells. Pengfei Liu, Shubin Chen, +10 authors, Duanqing Pei. less PLoS One, 2013 Aug 08; 8(7). PMID: 23922758 Free PMC article.
Role of T cell receptor affinity in the efficacy and specificity of adoptive T cell therapies. Jennifer D Stone, David M Kranz. Front Immunol, 2013 Aug 24; 4. PMID: 23970885 Free PMC article.
Changing T-cell enigma: cancer killing or cancer control? Thomas Wieder, Heidi Braumüller, +2 authors, Ellen Brenner, Lars Zender, Martin Röcken. less Cell Cycle, 2013 Sep 10; 12(19). PMID: 24013429 Free PMC article.
Tumor-specific CD4+ T cells maintain effector and memory tumor-specific CD8+ T cells. Sarah E Church, Shawn M Jensen, +2 authors, Paul A Antony, Nicholas P Restifo, Bernard A Fox. less Eur J Immunol, 2013 Oct 12; 44(1). PMID: 24114780 Free PMC article.
Exchange of cytosolic content between T cells and tumor cells activates CD4 T cells and impedes cancer growth. Matthias Hardtke-Wolenski, Lilli Kraus, +7 authors, Thorsten Lieke. less PLoS One, 2013 Nov 10; 8(10). PMID: 24205259 Free PMC article.
Human cell-based artificial antigen-presenting cells for cancer immunotherapy. Marcus O Butler, Naoto Hirano. Immunol Rev, 2013 Dec 18; 257(1). PMID: 24329798 Free PMC article. Review.
Establishment of HLA-DR4 transgenic mice for the identification of CD4+ T cell epitopes of tumor-associated antigens. Junji Yatsuda, Atsushi Irie, +14 authors, Yasuharu Nishimura. less PLoS One, 2014 Jan 05; 8(12). PMID: 24386437 Free PMC article.
Enhancement of tumor-reactive cytotoxic CD4+ T cell responses after ipilimumab treatment in four advanced melanoma patients. Shigehisa Kitano, Takemasa Tsuji, +7 authors, Jedd D Wolchok. less Cancer Immunol Res, 2014 Jan 08; 1(4). PMID: 24396833 Free PMC article.
TNF-α-dependent hematopoiesis following Bcl11b deletion in T cells restricts metastatic melanoma. Mohammad N Uddin, Yubin Zhang, +2 authors, Dorina Avram. less J Immunol, 2014 Jan 22; 192(4). PMID: 24446520 Free PMC article.
SA-4-1BBL as a novel adjuvant for the development of therapeutic cancer vaccines. Rajesh K Sharma, Esma S Yolcu, Haval Shirwan. Expert Rev Vaccines, 2014 Feb 14; 13(3). PMID: 24521311 Free PMC article. Review.
Immune-based antitumor effects of BRAF inhibitors rely on signaling by CD40L and IFNγ. Ping-Chih Ho, Katrina M Meeth, +3 authors, Susan M Kaech. less Cancer Res, 2014 Apr 17; 74(12). PMID: 24736544 Free PMC article.
How Do CD4(+) T Cells Detect and Eliminate Tumor Cells That Either Lack or Express MHC Class II Molecules? Ole Audun Werner Haabeth, Anders Aune Tveita, +8 authors, Bjarne Bogen. less Front Immunol, 2014 May 02; 5. PMID: 24782871 Free PMC article. Highly Cited. Review.
Th17 cells in cancer: the ultimate identity crisis. Stefanie R Bailey, Michelle H Nelson, +3 authors, Chrystal M Paulos. less Front Immunol, 2014 Jul 06; 5. PMID: 24987392 Free PMC article. Highly Cited. Review.
A new hope in immunotherapy for malignant gliomas: adoptive T cell transfer therapy. Dong-Sup Chung, Hye-Jin Shin, Yong-Kil Hong. J Immunol Res, 2014 Jul 11; 2014. PMID: 25009822 Free PMC article. Review.
CD4 T cells specific for a latency-associated γ-herpesvirus epitope are polyfunctional and cytotoxic. Michael L Freeman, Claire E Burkum, +11 authors, Marcia A Blackman. less J Immunol, 2014 Nov 08; 193(12). PMID: 25378595 Free PMC article.
Alkylating agent melphalan augments the efficacy of adoptive immunotherapy using tumor-specific CD4+ T cells. Xiaoyun Lu, Zhi-Chun Ding, +8 authors, Gang Zhou. less J Immunol, 2015 Jan 07; 194(4). PMID: 25560408 Free PMC article.
Breaking through the central tolerance ceiling to unleash anticancer immune responses. Maureen A Su, Mark S Anderson. Oncoimmunology, 2015 Jan 23; 3(8). PMID: 25610739 Free PMC article.
Metastatic melanoma cells evade immune detection by silencing STAT1. JoDi Lynn Osborn, Susanna F Greer. Int J Mol Sci, 2015 Feb 19; 16(2). PMID: 25690042 Free PMC article.
Individual Motile CD4(+) T Cells Can Participate in Efficient Multikilling through Conjugation to Multiple Tumor Cells. Ivan Liadi, Harjeet Singh, +9 authors, Navin Varadarajan. less Cancer Immunol Res, 2015 Feb 26; 3(5). PMID: 25711538 Free PMC article.
IL-6-mediated environmental conditioning of defective Th1 differentiation dampens antitumour immune responses in old age. Hirotake Tsukamoto, Satoru Senju, +2 authors, Keiko Matsumura, Susan L Swain, Yasuharu Nishimura. less Nat Commun, 2015 Apr 08; 6. PMID: 25850032 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.
Limitations of bystander killing in Th1/M1 immune responses against a secreted tumor antigen. Anders Aune Tveita, Ole Audun Haabeth, Bjarne Bogen. Oncoimmunology, 2015 May 06; 3(9). PMID: 25941607 Free PMC article.
An immunogenomic stratification of colorectal cancer: Implications for development of targeted immunotherapy. Neeraj Lal, Andrew D Beggs, Benjamin E Willcox, Gary W Middleton. Oncoimmunology, 2015 May 08; 4(3). PMID: 25949894 Free PMC article.
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.
Neutrophil-to-lymphocyte ratio and overall survival in all sites of head and neck squamous cell carcinoma. Saleh Rachidi, Kristin Wallace, +3 authors, Zihai Li. less Head Neck, 2015 Jun 05; 38 Suppl 1. PMID: 26040762 Free PMC article.
EBP1 protein modulates the expression of human MHC class II molecules in non-hematopoietic cancer cells. Laura Pisapia, Pasquale Barba, +3 authors, Giovanna Del Pozzo. less Int J Oncol, 2015 Jun 18; 47(2). PMID: 26081906 Free PMC article.
Rapid generation of NY-ESO-1-specific CD4+ THELPER1 cells for adoptive T-cell therapy. Simone Kayser, Cristina Boβ, +11 authors, Tobias Feuchtinger. less Oncoimmunology, 2015 Jul 15; 4(5). PMID: 26155389 Free PMC article.
Interest of Tumor-Specific CD4 T Helper 1 Cells for Therapeutic Anticancer Vaccine. Jeanne Galaine, Christophe Borg, Yann Godet, Olivier Adotévi. Vaccines (Basel), 2015 Sep 10; 3(3). PMID: 26350591 Free PMC article. Review.
Depletion of B220+NK1.1+ cells enhances the rejection of established melanoma by tumor-specific CD4+ T cells. Kyle A Wilson, Stephen R Goding, +2 authors, Harold R Neely, Kristina M Harris, Paul Andrew Antony. less Oncoimmunology, 2015 Sep 26; 4(8). PMID: 26405570 Free PMC article.
Direct tumor recognition by a human CD4(+) T-cell subset potently mediates tumor growth inhibition and orchestrates anti-tumor immune responses. Junko Matsuzaki, Takemasa Tsuji, +7 authors, Kunle Odunsi. less Sci Rep, 2015 Oct 09; 5. PMID: 26447332 Free PMC article.
New Strategies in Engineering T-cell Receptor Gene-Modified T cells to More Effectively Target Malignancies. Thomas M Schmitt, Ingunn M Stromnes, Aude G Chapuis, Philip D Greenberg. Clin Cancer Res, 2015 Oct 16; 21(23). PMID: 26463711 Free PMC article. Review.
Highly efficient homology-driven genome editing in human T cells by combining zinc-finger nuclease mRNA and AAV6 donor delivery. Jianbin Wang, Joshua J DeClercq, +5 authors, Michael C Holmes. less Nucleic Acids Res, 2015 Nov 04; 44(3). PMID: 26527725 Free PMC article.
T-cell receptor gene therapy--ready to go viral? Terhi Karpanen, Johanna Olweus. Mol Oncol, 2015 Nov 10; 9(10). PMID: 26548533 Free PMC article. Review.
Tumor-Unrelated CD4 T Cell Help Augments CD134 plus CD137 Dual Costimulation Tumor Therapy. Payal Mittal, Marie-Clare St Rose, +4 authors, Adam J Adler. less J Immunol, 2015 Nov 13; 195(12). PMID: 26561553 Free PMC article.
Lineage re-commitment of CD4CD8αα intraepithelial lymphocytes in the gut. Yunji Park, Sook-Jin Moon, Seung-Woo Lee. BMB Rep, 2015 Nov 26; 49(1). PMID: 26592937 Free PMC article. Review.
Identification of Melanoma-reactive CD4+ T-Cell Subsets From Human Melanoma Draining Lymph Nodes. Mei Zhang, Hallie Graor, Lu Yan, Julian Kim. J Immunother, 2015 Dec 08; 39(1). PMID: 26641258 Free PMC article.
CRTAM determines the CD4+ cytotoxic T lymphocyte lineage. Arata Takeuchi, Mohamed El Sherif Gadelhaq Badr, +11 authors, Takashi Saito. less J Exp Med, 2015 Dec 24; 213(1). PMID: 26694968 Free PMC article.
Clonal Abundance of Tumor-Specific CD4(+) T Cells Potentiates Efficacy and Alters Susceptibility to Exhaustion. Nicole Malandro, Sadna Budhu, +9 authors, Jedd D Wolchok. less Immunity, 2016 Jan 21; 44(1). PMID: 26789923 Free PMC article.
Exploiting IL-17-producing CD4+ and CD8+ T cells to improve cancer immunotherapy in the clinic. Kinga Majchrzak, Michelle H Nelson, +5 authors, Chrystal M Paulos. less Cancer Immunol Immunother, 2016 Jan 31; 65(3). PMID: 26825102 Free PMC article. Review.
Tumour-specific CD4 T cells eradicate melanoma via indirect recognition of tumour-derived antigen. Elena Shklovskaya, Alexandra M Terry, +5 authors, Barbara Fazekas de St. Groth. less Immunol Cell Biol, 2016 Feb 04; 94(6). PMID: 26837456
A role for pre-mNK cells in tumor progression. Carolyn Rosinsky, Paul Andrew Antony. J Immunother Cancer, 2016 Mar 17; 4. PMID: 26981246 Free PMC article.
Sex bias in CNS autoimmune disease mediated by androgen control of autoimmune regulator. Meng-Lei Zhu, Pearl Bakhru, +6 authors, Maureen A Su. less Nat Commun, 2016 Apr 14; 7. PMID: 27072778 Free PMC article.
Collaboration between tumor-specific CD4+ T cells and B cells in anti-cancer immunity. Thomas V Guy, Alexandra M Terry, +6 authors, Barbara Fazekas de St. Groth. less Oncotarget, 2016 Apr 29; 7(21). PMID: 27121060 Free PMC article.
Overrepresentation of IL-10-Expressing B Cells Suppresses Cytotoxic CD4+ T Cell Activity in HBV-Induced Hepatocellular Carcinoma. Hongwei Xue, Fuhuang Lin, +3 authors, Ludong Zhao. less PLoS One, 2016 May 03; 11(5). PMID: 27136203 Free PMC article.
Isolation and Characterization of an HLA-DPB1*04: 01-restricted MAGE-A3 T-Cell Receptor for Cancer Immunotherapy. Xin Yao, Yong-Chen Lu, +8 authors, Paul F Robbins. less J Immunother, 2016 May 11; 39(5). PMID: 27163739 Free PMC article.
An oncofetal antigen, IMP-3-derived long peptides induce immune responses of both helper T cells and CTLs. Masatoshi Hirayama, Yusuke Tomita, +16 authors, Yasuharu Nishimura. less Oncoimmunology, 2016 Jul 30; 5(6). PMID: 27471607 Free PMC article.
IL-7 signaling imparts polyfunctionality and stemness potential to CD4(+) T cells. Zhi-Chun Ding, Chufeng Liu, +10 authors, Gang Zhou. less Oncoimmunology, 2016 Jul 30; 5(6). PMID: 27471650 Free PMC article.
Tumor-specific CD4+ T cells eradicate myeloma cells genetically deficient in MHC class II display. Anders Tveita, Marte Fauskanger, Bjarne Bogen, Ole Audun Werner Haabeth. Oncotarget, 2016 Sep 15; 7(41). PMID: 27626487 Free PMC article.
CD4+ T cell-mediated cytotoxicity eliminates primary tumor cells in metastatic melanoma through high MHC class II expression and can be enhanced by inhibitory receptor blockade. Hongxia Yan, Xianglian Hou, +4 authors, Ruijie Zhu. less Tumour Biol, 2016 Oct 07;. PMID: 27709550
Exogenous IL-2 Induces FoxP3+ Th17 Cells In Vivo in Melanoma Patients. Maggie L Diller, Ragini R Kudchadkar, +2 authors, Keith A Delman, David H Lawson, Mandy L Ford. less J Immunother, 2016 Oct 16; 39(9). PMID: 27741090 Free PMC article.
Cytokines and metabolic factors regulate tumoricidal T-cell function during cancer immunotherapy. Adam J Adler, Payal Mittal, +3 authors, Anthony T Vella. less Immunotherapy, 2016 Dec 22; 9(1). PMID: 28000531 Free PMC article. Review.
The distribution and function of human memory T cell subsets in lung cancer. Si Yuan Sheng, Yong Gu, +3 authors, RongFu Wang. less Immunol Res, 2017 Jan 20; 65(3). PMID: 28101811 Free PMC article.
Systemic Immunity Is Required for Effective Cancer Immunotherapy. Matthew H Spitzer, Yaron Carmi, +10 authors, Edgar G Engleman. less Cell, 2017 Jan 24; 168(3). PMID: 28111070 Free PMC article. Highly Cited.
CpG oligodeoxynucleotide nanomedicines for the prophylaxis or treatment of cancers, infectious diseases, and allergies. Nobutaka Hanagata. Int J Nanomedicine, 2017 Feb 02; 12. PMID: 28144136 Free PMC article. Review.
Fine-tuning the CAR spacer improves T-cell potency. Norihiro Watanabe, Pradip Bajgain, +6 authors, Juan F Vera. less Oncoimmunology, 2017 Feb 10; 5(12). PMID: 28180032 Free PMC article. Highly Cited.
Combination immunotherapy: a road map. Patrick A Ott, F Stephen Hodi, +2 authors, Howard L Kaufman, Jon M Wigginton, Jedd D Wolchok. less J Immunother Cancer, 2017 Feb 28; 5. PMID: 28239469 Free PMC article. Highly Cited. Review.
CD4 CTL, a Cytotoxic Subset of CD4+ T Cells, Their Differentiation and Function. Arata Takeuchi, Takashi Saito. Front Immunol, 2017 Mar 11; 8. PMID: 28280496 Free PMC article. Highly Cited. Review.
Murine Th17 cells utilize IL-2 receptor gamma chain cytokines but are resistant to cytokine withdrawal-induced apoptosis. Daniel J Neitzke, Jacob S Bowers, +7 authors, Mark P Rubinstein. less Cancer Immunol Immunother, 2017 Mar 11; 66(6). PMID: 28280853 Free PMC article.
Th17 cells are refractory to senescence and retain robust antitumor activity after long-term ex vivo expansion. Jacob S Bowers, Michelle H Nelson, +6 authors, Chrystal M Paulos. less JCI Insight, 2017 Mar 16; 2(5). PMID: 28289713 Free PMC article.
Generation of murine tumor cell lines deficient in MHC molecule surface expression using the CRISPR/Cas9 system. Krishna Das, David Eisel, +5 authors, Stefan B Eichmüller. less PLoS One, 2017 Mar 17; 12(3). PMID: 28301575 Free PMC article.
The cryo-thermal therapy eradicated melanoma in mice by eliciting CD4+ T-cell-mediated antitumor memory immune response. Kun He, Ping Liu, Lisa X Xu. Cell Death Dis, 2017 Mar 24; 8(3). PMID: 28333145 Free PMC article.
HLA class II antigen-processing pathway in tumors: Molecular defects and clinical relevance. Barbara Seliger, Matthias Kloor, Soldano Ferrone. Oncoimmunology, 2017 Mar 28; 6(2). PMID: 28344859 Free PMC article. Review.
β-catenin and PI3Kδ inhibition expands precursor Th17 cells with heightened stemness and antitumor activity. Kinga Majchrzak, Michelle H Nelson, +9 authors, Chrystal M Paulos. less JCI Insight, 2017 Apr 20; 2(8). PMID: 28422756 Free PMC article.
B cells and the humoral response in melanoma: The overlooked players of the tumor microenvironment. Giulia Chiaruttini, Silvia Mele, +4 authors, Sophia N Karagiannis. less Oncoimmunology, 2017 May 17; 6(4). PMID: 28507802 Free PMC article. Review.
Polyfunctional response by ImmTAC (IMCgp100) redirected CD8+ and CD4+ T cells. Caroline Boudousquie, Giovanna Bossi, +3 authors, Namir J Hassan. less Immunology, 2017 Jun 24; 152(3). PMID: 28640942 Free PMC article.
Resident memory T cells in the skin mediate durable immunity to melanoma. Brian T Malik, Katelyn T Byrne, +9 authors, Mary Jo Turk. less Sci Immunol, 2017 Jul 25; 2(10). PMID: 28738020 Free PMC article. Highly Cited.
Vaccines targeting helper T cells for cancer immunotherapy. Marit Melssen, Craig L Slingluff. Curr Opin Immunol, 2017 Jul 30; 47. PMID: 28755541 Free PMC article. Review.
Treatment of Patients With Metastatic Cancer Using a Major Histocompatibility Complex Class II-Restricted T-Cell Receptor Targeting the Cancer Germline Antigen MAGE-A3. Yong-Chen Lu, Linda L Parker, +14 authors, Steven A Rosenberg. less J Clin Oncol, 2017 Aug 16; 35(29). PMID: 28809608 Free PMC article. Highly Cited.
Expression of the MHC class II in triple-negative breast cancer is associated with tumor-infiltrating lymphocytes and interferon signaling. In Ah Park, Seong-Hye Hwang, +7 authors, Hee Jin Lee. less PLoS One, 2017 Aug 18; 12(8). PMID: 28817603 Free PMC article.
The Tumor Microenvironment Regulates Sensitivity of Murine Lung Tumors to PD-1/PD-L1 Antibody Blockade. Howard Y Li, Maria McSharry, +8 authors, Raphael A Nemenoff. less Cancer Immunol Res, 2017 Aug 19; 5(9). PMID: 28819064 Free PMC article.
Most Do, but Some Do Not: CD4⁺CD25- T Cells, but Not CD4⁺CD25⁺ Treg Cells, Are Cytolytic When Redirected by a Chimeric Antigen Receptor (CAR). Andreas A Hombach, Hinrich Abken. Cancers (Basel), 2017 Aug 30; 9(9). PMID: 28850063 Free PMC article.
Transfer of in vitro-expanded naïve T cells after lymphodepletion enhances antitumor immunity through the induction of polyclonal antitumor effector T cells. Tomohiro Tanaka, Satoshi Watanabe, +20 authors, Toshiaki Kikuchi. less PLoS One, 2017 Aug 31; 12(8). PMID: 28854279 Free PMC article.
Timing of PD-1 Blockade Is Critical to Effective Combination Immunotherapy with Anti-OX40. David J Messenheimer, Shawn M Jensen, +6 authors, Bernard A Fox. less Clin Cancer Res, 2017 Sep 01; 23(20). PMID: 28855348 Free PMC article. Highly Cited.
Adjuvant IL-7 potentiates adoptive T cell therapy by amplifying and sustaining polyfunctional antitumor CD4+ T cells. Zhi-Chun Ding, Tsadik Habtetsion, +8 authors, Gang Zhou. less Sci Rep, 2017 Sep 25; 7(1). PMID: 28939858 Free PMC article.
Exploring Synergy in Combinations of Tumor-Derived Vaccines That Harbor 4-1BBL, OX40L, and GM-CSF. Andrea J Manrique-Rincón, Camila M Beraldo, Jessica M Toscaro, Marcio C Bajgelman. Front Immunol, 2017 Oct 05; 8. PMID: 28974950 Free PMC article.
CD4 and CD8 T lymphocyte interplay in controlling tumor growth. Dmitrij Ostroumov, Nora Fekete-Drimusz, +2 authors, Michael Saborowski, Florian Kühnel, Norman Woller. less Cell Mol Life Sci, 2017 Oct 17; 75(4). PMID: 29032503 Free PMC article. Review.
Periodically Pulsed Immunotherapy in a Mathematical Model of Tumor, CD4+ T Cells, and Antitumor Cytokine Interactions. Hsiu-Chuan Wei, Jui-Ling Yu, Chia-Yu Hsu. Comput Math Methods Med, 2017 Dec 19; 2017. PMID: 29250133 Free PMC article.
An Immunotherapeutic CD137 Agonist Releases Eomesodermin from ThPOK Repression in CD4 T Cells. Payal Mittal, Rebecca Abblett, +8 authors, Adam J Adler. less J Immunol, 2018 Jan 07; 200(4). PMID: 29305435 Free PMC article.
Citrullinated α-enolase is an effective target for anti-cancer immunity. Katherine Cook, Ian Daniels, +6 authors, Victoria Brentville. less Oncoimmunology, 2018 Jan 09; 7(2). PMID: 29308319 Free PMC article.
Signaling by the Epstein-Barr virus LMP1 protein induces potent cytotoxic CD4+ and CD8+ T cell responses. Il-Kyu Choi, Zhe Wang, +10 authors, Baochun Zhang. less Proc Natl Acad Sci U S A, 2018 Jan 10; 115(4). PMID: 29311309 Free PMC article.
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