Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors

Duhen, Thomas; Duhen, Rebekka; Montler, Ryan; Moses, Jake; Moudgil, Tarsem; de Miranda, Noel F.; Goodall, Cheri P.; Blair, Tiffany C.; Fox, Bernard A.; McDermott, Jason E.; Chang, Shu -Ching; Grunkemeier, Gary; Leidner, Rom; Bell, Richard Bryan; Weinberg, Andrew D.

doi:10.1038/S41467-018-05072-0

Title: Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors

Abstract

Identifying tumor antigen-specific T cells from cancer patients has important implications for immunotherapy diagnostics and therapeutics. Here, we show that CD103⁺CD39⁺ tumor-infiltrating CD8 T cells (CD8 TIL) are enriched for tumor-reactive cells both in primary and metastatic tumors. This CD8 TIL subset is found across six different malignancies and displays an exhausted tissue-resident memory phenotype. CD103⁺CD39⁺ CD8 TILs have a distinct T-cell receptor (TCR) repertoire, with T-cell clones expanded in the tumor but present at low frequencies in the periphery. CD103⁺CD39⁺ CD8 TILs also efficiently kill autologous tumor cells in a MHC-class I-dependent manner. Finally, higher frequencies of CD103⁺CD39⁺ CD8 TILs in patients with head and neck cancer are associated with better overall survival. Furthermore, our data thus describe an approach for detecting tumor-reactive CD8 TILs that will help define mechanisms of existing immunotherapy treatments, and may lead to future adoptive T-cell cancer therapies.

Authors:

Duhen, Thomas ^[1]; Duhen, Rebekka ^[2]; Montler, Ryan ^[1]; Moses, Jake ^[1]; Moudgil, Tarsem ^[2]; de Miranda, Noel F. ^[3]; Goodall, Cheri P. ^[2]; Blair, Tiffany C. ^[1]; Fox, Bernard A. ^[2];

^[4]; Chang, Shu -Ching ^[5]; Grunkemeier, Gary ^[5]; Leidner, Rom ^[2]; Bell, Richard Bryan ^[2]; Weinberg, Andrew D. ^[6]

AgonOx, Inc., Portland, OR (United States)
Providence Cancer Institute, Portland, OR (United States)
Leiden Univ. Medical Center, Leiden (The Netherlands)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Providence Saint Joseph's Health, Portland, OR (United States)
AgonOx, Inc., Portland, OR (United States); Providence Cancer Institute, Portland, OR (United States)

Publication Date:: 2018-07-13

Research Org.:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1463347

Report Number(s):: PNNL-SA135245
Journal ID: ISSN 2041-1723; PII: 5072

Grant/Contract Number:: AC05-76RL01830

Resource Type:: Accepted Manuscript

Journal Name:: Nature Communications

Additional Journal Information:: Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Duhen, Thomas, Duhen, Rebekka, Montler, Ryan, Moses, Jake, Moudgil, Tarsem, de Miranda, Noel F., Goodall, Cheri P., Blair, Tiffany C., Fox, Bernard A., McDermott, Jason E., Chang, Shu -Ching, Grunkemeier, Gary, Leidner, Rom, Bell, Richard Bryan, and Weinberg, Andrew D. Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors.  United States: N. p., 2018. 
Web.  doi:10.1038/S41467-018-05072-0.

Copy to clipboard


                    Duhen, Thomas, Duhen, Rebekka, Montler, Ryan, Moses, Jake, Moudgil, Tarsem, de Miranda, Noel F., Goodall, Cheri P., Blair, Tiffany C., Fox, Bernard A., McDermott, Jason E., Chang, Shu -Ching, Grunkemeier, Gary, Leidner, Rom, Bell, Richard Bryan, & Weinberg, Andrew D. Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors.  United States.  https://doi.org/10.1038/S41467-018-05072-0

Copy to clipboard


                    Duhen, Thomas, Duhen, Rebekka, Montler, Ryan, Moses, Jake, Moudgil, Tarsem, de Miranda, Noel F., Goodall, Cheri P., Blair, Tiffany C., Fox, Bernard A., McDermott, Jason E., Chang, Shu -Ching, Grunkemeier, Gary, Leidner, Rom, Bell, Richard Bryan, and Weinberg, Andrew D. Fri .  
"Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors".  United States.  https://doi.org/10.1038/S41467-018-05072-0.  https://www.osti.gov/servlets/purl/1463347.

Copy to clipboard


                    
@article{osti_1463347,

  title        = {Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors},

  author       = {Duhen, Thomas and Duhen, Rebekka and Montler, Ryan and Moses, Jake and Moudgil, Tarsem and de Miranda, Noel F. and Goodall, Cheri P. and Blair, Tiffany C. and Fox, Bernard A. and McDermott, Jason E. and Chang, Shu -Ching and Grunkemeier, Gary and Leidner, Rom and Bell, Richard Bryan and Weinberg, Andrew D.},

  abstractNote = {Identifying tumor antigen-specific T cells from cancer patients has important implications for immunotherapy diagnostics and therapeutics. Here, we show that CD103+CD39+ tumor-infiltrating CD8 T cells (CD8 TIL) are enriched for tumor-reactive cells both in primary and metastatic tumors. This CD8 TIL subset is found across six different malignancies and displays an exhausted tissue-resident memory phenotype. CD103+CD39+ CD8 TILs have a distinct T-cell receptor (TCR) repertoire, with T-cell clones expanded in the tumor but present at low frequencies in the periphery. CD103+CD39+ CD8 TILs also efficiently kill autologous tumor cells in a MHC-class I-dependent manner. Finally, higher frequencies of CD103+CD39+ CD8 TILs in patients with head and neck cancer are associated with better overall survival. Furthermore, our data thus describe an approach for detecting tumor-reactive CD8 TILs that will help define mechanisms of existing immunotherapy treatments, and may lead to future adoptive T-cell cancer therapies.},

  doi          = {10.1038/S41467-018-05072-0},

  journal      = {Nature Communications},

  number       = 1,

  volume       = 9,

  place        = {United States},

  year         = {2018},

  month        = {7}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1038/S41467-018-05072-0

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 23 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referenced in this record:

Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients
journal, February 2016

Gros, Alena; Parkhurst, Maria R.; Tran, Eric
Nature Medicine, Vol. 22, Issue 4
DOI: 10.1038/nm.4051

Overcoming T cell exhaustion in infection and cancer
journal, April 2015

Pauken, Kristen E.; Wherry, E. John
Trends in Immunology, Vol. 36, Issue 4
DOI: 10.1016/j.it.2015.02.008

Tumor- and Neoantigen-Reactive T-cell Receptors Can Be Identified Based on Their Frequency in Fresh Tumor
journal, June 2016

Pasetto, A.; Gros, A.; Robbins, P. F.
Cancer Immunology Research, Vol. 4, Issue 9
DOI: 10.1158/2326-6066.CIR-16-0001

CD137 Accurately Identifies and Enriches for Naturally Occurring Tumor-Reactive T Cells in Tumor
journal, September 2013

Ye, Q.; Song, D. -G.; Poussin, M.
Clinical Cancer Research, Vol. 20, Issue 1
DOI: 10.1158/1078-0432.CCR-13-0945

Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer
journal, June 2017

Ganesan, Anusha-Preethi; Clarke, James; Wood, Oliver
Nature Immunology, Vol. 18, Issue 8
DOI: 10.1038/ni.3775

Cancer Regression in Patients After Transfer of Genetically Engineered Lymphocytes
journal, October 2006

Morgan, R. A.; Dudley, M. E.; Wunderlich, J. R.
Science, Vol. 314, Issue 5796
DOI: 10.1126/science.1129003

Tissue-resident memory T cells: local specialists in immune defence
journal, December 2015

Mueller, Scott N.; Mackay, Laura K.
Nature Reviews Immunology, Vol. 16, Issue 2
DOI: 10.1038/nri.2015.3

Tissue-Resident Memory T Cells
journal, December 2014

Schenkel, Jason M.; Masopust, David
Immunity, Vol. 41, Issue 6
DOI: 10.1016/j.immuni.2014.12.007

Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications
journal, July 2009

Lynch, Ht; Lynch, Pm; Lanspa, Sj
Clinical Genetics, Vol. 76, Issue 1
DOI: 10.1111/j.1399-0004.2009.01230.x

Method for assessing the similarity between subsets of the T cell receptor repertoire
journal, January 2008

Venturi, Vanessa; Kedzierska, Katherine; Tanaka, Mark M.
Journal of Immunological Methods, Vol. 329, Issue 1-2
DOI: 10.1016/j.jim.2007.09.016

PD-1 and CD103 Are Widely Coexpressed on Prognostically Favorable Intraepithelial CD8 T Cells in Human Ovarian Cancer
journal, May 2015

Webb, J. R.; Milne, K.; Nelson, B. H.
Cancer Immunology Research, Vol. 3, Issue 8
DOI: 10.1158/2326-6066.CIR-14-0239

PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors
journal, March 2014

Gros, Alena; Robbins, Paul F.; Yao, Xin
Journal of Clinical Investigation, Vol. 124, Issue 5
DOI: 10.1172/JCI73639

Tumor-Infiltrating Lymphocytes Expressing the Tissue Resident Memory Marker CD103 Are Associated with Increased Survival in High-Grade Serous Ovarian Cancer
journal, November 2013

Webb, J. R.; Milne, K.; Watson, P.
Clinical Cancer Research, Vol. 20, Issue 2
DOI: 10.1158/1078-0432.CCR-13-1877

Tumor antigen–specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired
journal, August 2009

Ahmadzadeh, Mojgan; Johnson, Laura A.; Heemskerk, Bianca
Blood, Vol. 114, Issue 8
DOI: 10.1182/blood-2008-12-195792

Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients
journal, June 2011

Baitsch, Lukas; Baumgaertner, Petra; Devêvre, Estelle
Journal of Clinical Investigation, Vol. 121, Issue 6
DOI: 10.1172/JCI46102

TGF-β–dependent CD103 expression by CD8 ⁺ T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease
journal, May 2005

El-Asady, Riham; Yuan, Rongwen; Liu, Kechang
The Journal of Experimental Medicine, Vol. 201, Issue 10
DOI: 10.1084/jem.20041044

Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
journal, September 2005

Subramanian, A.; Tamayo, P.; Mootha, V. K.
Proceedings of the National Academy of Sciences, Vol. 102, Issue 43, p. 15545-15550
DOI: 10.1073/pnas.0506580102

Cancer Regression and Autoimmunity in Patients After Clonal Repopulation with Antitumor Lymphocytes
journal, September 2002

Dudley, M. E.
Science, Vol. 298, Issue 5594
DOI: 10.1126/science.1076514

Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells
journal, October 2016

Hombrink, Pleun; Helbig, Christina; Backer, Ronald A.
Nature Immunology, Vol. 17, Issue 12
DOI: 10.1038/ni.3589

Adoptive T cell therapy using antigen-specific CD8⁺ T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells
journal, November 2002

Yee, C.; Thompson, J. A.; Byrd, D.
Proceedings of the National Academy of Sciences, Vol. 99, Issue 25, p. 16168-16173
DOI: 10.1073/pnas.242600099

Resident memory CD8 T cells trigger protective innate and adaptive immune responses
journal, August 2014

Schenkel, Jason M.; Fraser, Kathryn A.; Beura, Lalit K.
Science, Vol. 346, Issue 6205
DOI: 10.1126/science.1254536

CD39 Expression Defines Cell Exhaustion in Tumor-Infiltrating CD8 ⁺ T Cells
journal, October 2017

Canale, Fernando P.; Ramello, María C.; Núñez, Nicolás
Cancer Research, Vol. 78, Issue 1
DOI: 10.1158/0008-5472.CAN-16-2684

Cutting Edge: CD69 Interference with Sphingosine-1-Phosphate Receptor Function Regulates Peripheral T Cell Retention
journal, January 2015

Mackay, Laura K.; Braun, Asolina; Macleod, Bethany L.
The Journal of Immunology, Vol. 194, Issue 5
DOI: 10.4049/jimmunol.1402256

CD103+ intraepithelial T cells in high-grade serous ovarian cancer are phenotypically diverse TCRαβ+ CD8αβ+ T cells that can be targeted for cancer immunotherapy
journal, September 2016

Komdeur, Fenne L.; Wouters, Maartje C. A.; Workel, Hagma H.
Oncotarget, Vol. 7, Issue 46
DOI: 10.18632/oncotarget.12077

Phase I Study of Adoptive T-Cell Therapy Using Antigen-Specific CD8 ⁺ T Cells for the Treatment of Patients With Metastatic Melanoma
journal, November 2006

Mackensen, Andreas; Meidenbauer, Norbert; Vogl, Sandra
Journal of Clinical Oncology, Vol. 24, Issue 31
DOI: 10.1200/JCO.2006.07.1100

Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes
journal, April 2016

Mackay, L. K.; Minnich, M.; Kragten, N. A. M.
Science, Vol. 352, Issue 6284
DOI: 10.1126/science.aad2035

Selection of CD8+PD-1+ Lymphocytes in Fresh Human Melanomas Enriches for Tumor-reactive T Cells
journal, January 2010

Inozume, Takashi; Hanada, Ken-ichi; Wang, Qiong J.
Journal of Immunotherapy, Vol. 33, Issue 9
DOI: 10.1097/CJI.0b013e3181fad2b0

A Solution to the Problem of Monotone Likelihood in Cox Regression
journal, March 2001

Heinze, Georg; Schemper, Michael
Biometrics, Vol. 57, Issue 1
DOI: 10.1111/j.0006-341X.2001.00114.x

TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance
journal, November 2005

Thomas, Dori A.; Massagué, Joan
Cancer Cell, Vol. 8, Issue 5
DOI: 10.1016/j.ccr.2005.10.012

Chromatin states define tumour-specific T cell dysfunction and reprogramming
journal, May 2017

Philip, Mary; Fairchild, Lauren; Sun, Liping
Nature, Vol. 545, Issue 7655
DOI: 10.1038/nature22367

Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes
journal, September 2015

Cohen, Cyrille J.; Gartner, Jared J.; Horovitz-Fried, Miryam
Journal of Clinical Investigation, Vol. 125, Issue 10
DOI: 10.1172/JCI82416

Molecular Signatures Distinguish Human Central Memory from Effector Memory CD8 T Cell Subsets
journal, October 2005

Willinger, Tim; Freeman, Tom; Hasegawa, Hitoshi
The Journal of Immunology, Vol. 175, Issue 9
DOI: 10.4049/jimmunol.175.9.5895

Targeting Cancer-Derived Adenosine:New Therapeutic Approaches
journal, July 2014

Young, A.; Mittal, D.; Stagg, J.
Cancer Discovery, Vol. 4, Issue 8
DOI: 10.1158/2159-8290.CD-14-0341

Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen–specific CD8 ⁺ T cell dysfunction in melanoma patients
journal, September 2010

Fourcade, Julien; Sun, Zhaojun; Benallaoua, Mourad
The Journal of Experimental Medicine, Vol. 207, Issue 10
DOI: 10.1084/jem.20100637

Microsatellite Instability as a Biomarker for PD-1 Blockade
journal, February 2016

Dudley, J. C.; Lin, M. -T.; Le, D. T.
Clinical Cancer Research, Vol. 22, Issue 4
DOI: 10.1158/1078-0432.CCR-15-1678

Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression
journal, May 2007

Deaglio, Silvia; Dwyer, Karen M.; Gao, Wenda
The Journal of Experimental Medicine, Vol. 204, Issue 6
DOI: 10.1084/jem.20062512

limma powers differential expression analyses for RNA-sequencing and microarray studies
journal, January 2015

Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
Nucleic Acids Research, Vol. 43, Issue 7
DOI: 10.1093/nar/gkv007

Exploiting the curative potential of adoptive T-cell therapy for cancer
journal, December 2013

Hinrichs, Christian S.; Rosenberg, Steven A.
Immunological Reviews, Vol. 257, Issue 1
DOI: 10.1111/imr.12132

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
journal, September 2017

Kumar, Brahma V.; Ma, Wenji; Miron, Michelle
Cell Reports, Vol. 20, Issue 12
DOI: 10.1016/j.celrep.2017.08.078

Human Tumor Antigens Yesterday, Today, and Tomorrow
journal, May 2017

Finn, Olivera J.
Cancer Immunology Research, Vol. 5, Issue 5
DOI: 10.1158/2326-6066.CIR-17-0112

PD-1 Blockade in Tumors with Mismatch-Repair Deficiency
journal, June 2015

Le, Dung T.; Uram, Jennifer N.; Wang, Hao
New England Journal of Medicine, Vol. 372, Issue 26
DOI: 10.1056/NEJMoa1500596

CD103 defines intraepithelial CD8+ PD1+ tumour-infiltrating lymphocytes of prognostic significance in endometrial adenocarcinoma
journal, June 2016

Workel, Hagma H.; Komdeur, Fenne L.; Wouters, Maartje C. A.
European Journal of Cancer, Vol. 60
DOI: 10.1016/j.ejca.2016.02.026

Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities
journal, July 2007

Wolfl, Matthias; Kuball, Jürgen; Ho, William Y.
Blood, Vol. 110, Issue 1
DOI: 10.1182/blood-2006-11-056168

Therapeutic T cell engineering
journal, May 2017

Sadelain, Michel; Rivière, Isabelle; Riddell, Stanley
Nature, Vol. 545, Issue 7655
DOI: 10.1038/nature22395

CD39 and CD73 in immunity and inflammation
journal, June 2013

Antonioli, Luca; Pacher, Pál; Vizi, E. Sylvester
Trends in Molecular Medicine, Vol. 19, Issue 6
DOI: 10.1016/j.molmed.2013.03.005

Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade
journal, June 2017

Le, Dung T.; Durham, Jennifer N.; Smith, Kellie N.
Science, Vol. 357, Issue 6349
DOI: 10.1126/science.aan6733

CD39 Expression Identifies Terminally Exhausted CD8+ T Cells
journal, October 2015

Gupta, Prakash K.; Godec, Jernej; Wolski, David
PLOS Pathogens, Vol. 11, Issue 10
DOI: 10.1371/journal.ppat.1005177

CD8 ⁺ CD103 ⁺ Tumor–Infiltrating Lymphocytes Are Tumor-Specific Tissue-Resident Memory T Cells and a Prognostic Factor for Survival in Lung Cancer Patients
journal, February 2015

Djenidi, Fayçal; Adam, Julien; Goubar, Aïcha
The Journal of Immunology, Vol. 194, Issue 7
DOI: 10.4049/jimmunol.1402711

CD103 ⁺ Tumor Infiltrating Lymphocytes Predict a Favorable Prognosis in Urothelial Cell Carcinoma of the Bladder
journal, August 2015

Wang, Bo; Wu, Shaoxu; Zeng, Hong
Journal of Urology, Vol. 194, Issue 2
DOI: 10.1016/j.juro.2015.02.2941

CD8+ T-cell memory in tumor immunology and immunotherapy
journal, June 2006

Klebanoff, Christopher A.; Gattinoni, Luca; Restifo, Nicholas P.
Immunological Reviews, Vol. 211, Issue 1
DOI: 10.1111/j.0105-2896.2006.00391.x

TGFβ in Cancer
journal, July 2008

Massagué, Joan
Cell, Vol. 134, Issue 2
DOI: 10.1016/j.cell.2008.07.001

Tissue-resident memory T cells
journal, August 2013

Shin, Haina; Iwasaki, Akiko
Immunological Reviews, Vol. 255, Issue 1
DOI: 10.1111/imr.12087

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
text, January 2017

Kumar, Brahma Vencel; Ma, Wenji; Miron, Michelle
Columbia University
DOI: 10.7916/d89p4d5f

An integrative analysis of the age-associated multi-omic landscape across cancers
journal, April 2021

Chatsirisupachai, Kasit; Lesluyes, Tom; Paraoan, Luminita
Nature Communications, Vol. 12, Issue 1
DOI: 10.1038/s41467-021-22560-y

PD-1 blockade in tumors with mismatch-repair deficiency: Le DT (2015) N Engl J Med May 30
journal, June 2015

Aparicio, T.
Côlon & Rectum, Vol. 9, Issue 3
DOI: 10.1007/s11725-015-0588-4

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
journal, January 2018

Kumar, Brahma V.; Ma, Wenji; Miron, Michelle
SSRN Electronic Journal
DOI: 10.2139/ssrn.3155546

limma powers differential expression analyses for RNA-sequencing and microarray studies
text, January 2015

Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
Oxford University Press
DOI: 10.5167/uzh-155268

Works referencing / citing this record:

Accumulation of CD103 ⁺ CD8 ⁺ T cells in a cutaneous melanoma micrometastasis
journal, January 2019

Hochheiser, Katharina; Aw Yeang, Han Xian; Wagner, Teagan
Clinical & Translational Immunology, Vol. 8, Issue 12
DOI: 10.1002/cti2.1100

4‐1BB Delineates Distinct Activation Status of Exhausted Tumor‐Infiltrating CD8 ⁺ T Cells in Hepatocellular Carcinoma
journal, October 2019

Kim, Hyung‐Don; Park, Seongyeol; Jeong, Seongju
Hepatology, Vol. 71, Issue 3
DOI: 10.1002/hep.30881

A new therapeutic target: the CD69-Myl9 system in immune responses
journal, April 2019

Kimura, Motoko Y.; Koyama-Nasu, Ryo; Yagi, Ryoji
Seminars in Immunopathology, Vol. 41, Issue 3
DOI: 10.1007/s00281-019-00734-7

The activation of bystander CD8+ T cells and their roles in viral infection
journal, December 2019

Kim, Tae-Shin; Shin, Eui-Cheol
Experimental & Molecular Medicine, Vol. 51, Issue 12
DOI: 10.1038/s12276-019-0316-1

Tissue-resident lymphocytes: from adaptive to innate immunity
journal, January 2019

Sun, Haoyu; Sun, Cheng; Xiao, Weihua
Cellular & Molecular Immunology, Vol. 16, Issue 3
DOI: 10.1038/s41423-018-0192-y

Local heroes or villains: tissue-resident memory T cells in human health and disease
journal, January 2020

Sasson, S. C.; Gordon, C. L.; Christo, S. N.
Cellular & Molecular Immunology, Vol. 17, Issue 2
DOI: 10.1038/s41423-019-0359-1

CD8+ T cell states in human cancer: insights from single-cell analysis
journal, February 2020

van der Leun, Anne M.; Thommen, Daniela S.; Schumacher, Ton N.
Nature Reviews Cancer, Vol. 20, Issue 4
DOI: 10.1038/s41568-019-0235-4

Precursor exhausted T cells: key to successful immunotherapy?
journal, October 2019

Kallies, Axel; Zehn, Dietmar; Utzschneider, Daniel T.
Nature Reviews Immunology, Vol. 20, Issue 2
DOI: 10.1038/s41577-019-0223-7

Tissue patrol by resident memory CD8+ T cells in human skin
journal, May 2019

Dijkgraaf, Feline E.; Matos, Tiago R.; Hoogenboezem, Mark
Nature Immunology, Vol. 20, Issue 6
DOI: 10.1038/s41590-019-0404-3

Clonal replacement of tumor-specific T cells following PD-1 blockade
journal, July 2019

Yost, Kathryn E.; Satpathy, Ansuman T.; Wells, Daniel K.
Nature Medicine, Vol. 25, Issue 8
DOI: 10.1038/s41591-019-0522-3

Developing neoantigen-targeted T cell–based treatments for solid tumors
journal, October 2019

Yamamoto, Tori N.; Kishton, Rigel J.; Restifo, Nicholas P.
Nature Medicine, Vol. 25, Issue 10
DOI: 10.1038/s41591-019-0596-y

Sequential adjustment of cytotoxic T lymphocyte densities improves efficacy in controlling tumor growth
journal, August 2019

Khazen, Roxana; Müller, Sabina; Lafouresse, Fanny
Scientific Reports, Vol. 9, Issue 1
DOI: 10.1038/s41598-019-48711-2

The Adaptive and Innate Immune Cell Landscape of Uterine Leiomyosarcomas
journal, January 2020

Manzoni, Marco; Bolognesi, Maddalena M.; Antoranz, Asier
Scientific Reports, Vol. 10, Issue 1
DOI: 10.1038/s41598-020-57627-1

T cell receptor‐based cancer immunotherapy: Emerging efficacy and pathways of resistance
journal, July 2019

Chandran, Smita S.; Klebanoff, Christopher A.
Immunological Reviews, Vol. 290, Issue 1
DOI: 10.1111/imr.12772

Distinct epigenetic features of tumor-reactive CD8+ T cells in colorectal cancer patients revealed by genome-wide DNA methylation analysis
journal, December 2019

Yang, Rui; Cheng, Sijin; Luo, Nan
Genome Biology, Vol. 21, Issue 1
DOI: 10.1186/s13059-019-1921-y

Neoantigen-specific immunity in low mutation burden colorectal cancers of the consensus molecular subtype 4
journal, December 2019

van den Bulk, Jitske; Verdegaal, Els M. E.; Ruano, Dina
Genome Medicine, Vol. 11, Issue 1
DOI: 10.1186/s13073-019-0697-8

Late-differentiated effector neoantigen-specific CD8+ T cells are enriched in peripheral blood of non-small cell lung carcinoma patients responding to atezolizumab treatment
journal, September 2019

Fehlings, Michael; Jhunjhunwala, Suchit; Kowanetz, Marcin
Journal for ImmunoTherapy of Cancer, Vol. 7, Issue 1
DOI: 10.1186/s40425-019-0695-9

Monitoring and characterizing soluble and membrane-bound ectonucleotidases CD73 and CD39
journal, October 2019

Goueli, Said A.; Hsiao, Kevin
PLOS ONE, Vol. 14, Issue 10
DOI: 10.1371/journal.pone.0220094

Renal Cell Carcinoma (RCC) Tumors Display Large Expansion of Double Positive (DP) CD4+CD8+ T Cells With Expression of Exhaustion Markers
journal, November 2018

Menard, Laurence C.; Fischer, Paul; Kakrecha, Bijal
Frontiers in Immunology, Vol. 9
DOI: 10.3389/fimmu.2018.02728

The Tumor Microenvironment in Colorectal Cancer Therapy
journal, August 2019

Pedrosa, Leire; Esposito, Francis; Thomson, Timothy M.
Cancers, Vol. 11, Issue 8
DOI: 10.3390/cancers11081172

Virus-specific memory T cells populate tumors and can be repurposed for tumor immunotherapy
journal, February 2019

Rosato, Pamela C.; Wijeyesinghe, Sathi; Stolley, J. Michael
Nature Communications, Vol. 10, Issue 1
DOI: 10.1038/s41467-019-08534-1

Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis
journal, June 2018

Savas, Peter; Virassamy, Balaji; Ye, Chengzhong
Nature Medicine, Vol. 24, Issue 7
DOI: 10.1038/s41591-018-0078-7

T cell antigen discovery via trogocytosis
journal, January 2019

Li, Guideng; Bethune, Michael T.; Wong, Stephanie
Nature Methods, Vol. 16, Issue 2
DOI: 10.1038/s41592-018-0305-7

Molecular analysis of primary melanoma T cells identifies patients at risk for metastatic recurrence
journal, January 2020

Pruessmann, Wiebke; Rytlewski, Julie; Wilmott, James
Nature Cancer, Vol. 1, Issue 2
DOI: 10.1038/s43018-019-0019-5

Single-cell transcriptomic analysis of tissue-resident memory T cells in human lung cancer
journal, June 2019

Clarke, James; Panwar, Bharat; Madrigal, Ariel
The Journal of Experimental Medicine, Vol. 216, Issue 9
DOI: 10.1084/jem.20190249

Transforming of the Tumor Microenvironment: Implications for TGF- $β$ Inhibition in the Context of Immune-Checkpoint Therapy
journal, December 2018

Löffek, Stefanie
Journal of Oncology, Vol. 2018
DOI: 10.1155/2018/9732939

Tissue Resident CD8 Memory T Cell Responses in Cancer and Autoimmunity
journal, November 2018

Molodtsov, Aleksey; Turk, Mary Jo
Frontiers in Immunology, Vol. 9
DOI: 10.3389/fimmu.2018.02810

Determinants for Neoantigen Identification
journal, June 2019

Garcia-Garijo, Andrea; Fajardo, Carlos Alberto; Gros, Alena
Frontiers in Immunology, Vol. 10
DOI: 10.3389/fimmu.2019.01392

Possible Biomarkers for Cancer Immunotherapy
journal, July 2019

Otoshi, Takehiro; Nagano, Tatsuya; Tachihara, Motoko
Cancers, Vol. 11, Issue 7
DOI: 10.3390/cancers11070935

Targeting Adenosine Receptor Signaling in Cancer Immunotherapy
journal, December 2018

Sek, Kevin; Mølck, Christina; Stewart, Gregory
International Journal of Molecular Sciences, Vol. 19, Issue 12
DOI: 10.3390/ijms19123837

Similar Records in DOE PAGES and OSTI.GOV collections:

Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors

Journal Article Duhen, Thomas ; Duhen, Rebekka ; Montler, Ryan ; ... - Nature Communications

Identifying tumor antigen-specific T cells from cancer patients has been a goal of tumor immunologists for several decades. Here we show that co-expression of CD103 and CD39 on CD8 TIL highly enriched for tumor-reactive T cells. This cell population, which is only present in TIL from primary and metastatic tumors, exhibited features of exhausted cells and displayed characteristics of tissue-resident memory T cells. CD39+CD103+ CD8 TIL had a distinct TCR repertoire compared to other CD8 TIL subsets and were clonally expanded within the tumor. They were highly enriched for tumor antigen recognition and efficiently killed autologous tumor cells. Finally, patientsmore »« less
https://doi.org/10.1038/s41467-018-05072-0
Preoperative Radiomic Approach to Evaluate Tumor-Infiltrating CD8{sup +} T Cells in Hepatocellular Carcinoma Patients Using Contrast-Enhanced Computed Tomography

Journal Article Liao, Haotian ; Zhang, Zhen ; Chen, Jie ; ... - Annals of Surgical Oncology (Online)

Background: To help identify potential hepatocellular carcinoma (HCC) candidates for immunotherapies, we aimed to develop and validate a radiomics-based biomarker (Rad score) to predict the infiltration of tumor-infiltrating CD8{sup +} T cells in HCC patients, and to evaluate the correlation of Rad score with tumor immune characteristics. Methods: Overall, 142 HCC patients (n = 100 and n = 42 in the training and validation sets, respectively) were subjected to radiomic feature extraction. Imaging features and immunochemistry data of patients in the training set were subjected to elastic-net regularized regression analysis to predict the level of CD8{sup +} T cell infiltration. Results: A Rad scoremore »« less
https://doi.org/10.1245/S10434-019-07815-9
CXCR5+ CD8+ T cells potently infiltrate pancreatic tumors and present high functionality

Journal Article Bai, Minghui ; Zheng, Youwei ; Liu, Haichao ; ... - Experimental Cell Research

Despite continued improvement in conventional therapy, pancreatic cancer continues to be one of the deadliest tumors worldwide with abysmal 5-year survival rate. New immunotherapeutic strategies that aim at improving antitumor cytotoxic CD8{sup +} T cell responses are being developed in solid tumors. To assist the development of immunotherapies, we investigated the CD8{sup +} T cells in pancreatic cancer patients. Compared to healthy individuals, pancreatic cancer patients presented a significant enrichment in the frequency of CD8{sup +}CXCR5{sup +} T cells. In the tumor microenvironment, the frequencies of CD8{sup +}CXCR5{sup +} T cells were further increased. In most cases, over half ofmore »« less
https://doi.org/10.1016/J.YEXCR.2017.09.039
Streptococcus salivarius-mediated CD8+ T cell stimulation required antigen presentation by macrophages in oral squamous cell carcinoma

Journal Article Wang, Jie ; Department of Immunology, Xiangya School of Medicine, Central South University, Changsha 410078, ; Yang, Lina ; ... - Experimental Cell Research

It has been shown that the peripheral blood mononuclear cells (PBMCs) from oral squamous cell carcinoma (OSCC) patients presented cytotoxic CD8 T cell response against Streptococcus salivarius (S. salivarius), of which the frequency was positively associated with recurrence-free survival in OSCC patients. To identify the conditions required for regulating S. salivarius-specific CD8 T cell-mediated cytotoxicity, we selectively depleted individual components of the PBMCs, and observed that the depletion of monocytes/macrophages, but not other immune cell subsets, significantly downregulated the S. salivarius-specific CD8 T cell cytotoxicity. Monocyte/macrophage alone was sufficient to reconstitute optimal granzyme B expression from S. salivarius-specific CD8 Tmore »« less
https://doi.org/10.1016/J.YEXCR.2018.03.007
Characteristics and impact of programmed death-ligand 1 expression, CD8+ tumor-infiltrating lymphocytes, and p16 status in head and neck squamous cell carcinoma

Journal Article Ngamphaiboon, Nuttapong ; Chureemas, Teeranuch ; Siripoon, Teerada ; ... - Medical Oncology (Online)

Background: No predictive biomarker of immune checkpoint inhibitors in head and neck squamous cell carcinoma (HNSCC) has been well established. The impact of programmed death-ligand 1 (PD-L1) expression, CD8+ tumor-infiltrating lymphocytes (TILs), and p16 status in HNSCC is unclear and may vary according to ethnicity. Methods: HNSCC patients treated between 2007 and 2013 were reviewed. Archival tissues were retrieved for PD-L1, CD8+ TILs, and p16 analyses. PD-L1 expression was evaluated by using the validated SP142 assay on the VENTANA platform. CD8+ TILs were defined by using semiquantitative scoring. Results: A total of 203 patients were analyzed. PD-L1 expression was observedmore »« less
https://doi.org/10.1007/S12032-018-1241-1

Similar Records

Title: Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors

Abstract

Citation Formats

Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients journal, February 2016

Overcoming T cell exhaustion in infection and cancer journal, April 2015

Tumor- and Neoantigen-Reactive T-cell Receptors Can Be Identified Based on Their Frequency in Fresh Tumor journal, June 2016

CD137 Accurately Identifies and Enriches for Naturally Occurring Tumor-Reactive T Cells in Tumor journal, September 2013

Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer journal, June 2017

Cancer Regression in Patients After Transfer of Genetically Engineered Lymphocytes journal, October 2006

Tissue-resident memory T cells: local specialists in immune defence journal, December 2015

Tissue-Resident Memory T Cells journal, December 2014

Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications journal, July 2009

Method for assessing the similarity between subsets of the T cell receptor repertoire journal, January 2008

PD-1 and CD103 Are Widely Coexpressed on Prognostically Favorable Intraepithelial CD8 T Cells in Human Ovarian Cancer journal, May 2015

PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors journal, March 2014

Tumor-Infiltrating Lymphocytes Expressing the Tissue Resident Memory Marker CD103 Are Associated with Increased Survival in High-Grade Serous Ovarian Cancer journal, November 2013

Tumor antigen–specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired journal, August 2009

Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients journal, June 2011

TGF-β–dependent CD103 expression by CD8 + T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease journal, May 2005

Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles journal, September 2005

Cancer Regression and Autoimmunity in Patients After Clonal Repopulation with Antitumor Lymphocytes journal, September 2002

Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells journal, October 2016

Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells journal, November 2002

Resident memory CD8 T cells trigger protective innate and adaptive immune responses journal, August 2014

CD39 Expression Defines Cell Exhaustion in Tumor-Infiltrating CD8 + T Cells journal, October 2017

Cutting Edge: CD69 Interference with Sphingosine-1-Phosphate Receptor Function Regulates Peripheral T Cell Retention journal, January 2015

CD103+ intraepithelial T cells in high-grade serous ovarian cancer are phenotypically diverse TCRαβ+ CD8αβ+ T cells that can be targeted for cancer immunotherapy journal, September 2016

Phase I Study of Adoptive T-Cell Therapy Using Antigen-Specific CD8 + T Cells for the Treatment of Patients With Metastatic Melanoma journal, November 2006

Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes journal, April 2016

Selection of CD8+PD-1+ Lymphocytes in Fresh Human Melanomas Enriches for Tumor-reactive T Cells journal, January 2010

A Solution to the Problem of Monotone Likelihood in Cox Regression journal, March 2001

TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance journal, November 2005

Chromatin states define tumour-specific T cell dysfunction and reprogramming journal, May 2017

Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes journal, September 2015

Molecular Signatures Distinguish Human Central Memory from Effector Memory CD8 T Cell Subsets journal, October 2005

Targeting Cancer-Derived Adenosine:New Therapeutic Approaches journal, July 2014

Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen–specific CD8 + T cell dysfunction in melanoma patients journal, September 2010

Microsatellite Instability as a Biomarker for PD-1 Blockade journal, February 2016

Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression journal, May 2007

limma powers differential expression analyses for RNA-sequencing and microarray studies journal, January 2015

Exploiting the curative potential of adoptive T-cell therapy for cancer journal, December 2013

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites journal, September 2017

Human Tumor Antigens Yesterday, Today, and Tomorrow journal, May 2017

PD-1 Blockade in Tumors with Mismatch-Repair Deficiency journal, June 2015

CD103 defines intraepithelial CD8+ PD1+ tumour-infiltrating lymphocytes of prognostic significance in endometrial adenocarcinoma journal, June 2016

Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities journal, July 2007

Therapeutic T cell engineering journal, May 2017

CD39 and CD73 in immunity and inflammation journal, June 2013

Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade journal, June 2017

CD39 Expression Identifies Terminally Exhausted CD8+ T Cells journal, October 2015

CD8 + CD103 + Tumor–Infiltrating Lymphocytes Are Tumor-Specific Tissue-Resident Memory T Cells and a Prognostic Factor for Survival in Lung Cancer Patients journal, February 2015

CD103 + Tumor Infiltrating Lymphocytes Predict a Favorable Prognosis in Urothelial Cell Carcinoma of the Bladder journal, August 2015

CD8+ T-cell memory in tumor immunology and immunotherapy journal, June 2006

TGFβ in Cancer journal, July 2008

Tissue-resident memory T cells journal, August 2013

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites text, January 2017

An integrative analysis of the age-associated multi-omic landscape across cancers journal, April 2021

PD-1 blockade in tumors with mismatch-repair deficiency: Le DT (2015) N Engl J Med May 30 journal, June 2015

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites journal, January 2018

limma powers differential expression analyses for RNA-sequencing and microarray studies text, January 2015

Accumulation of CD103 + CD8 + T cells in a cutaneous melanoma micrometastasis journal, January 2019

4‐1BB Delineates Distinct Activation Status of Exhausted Tumor‐Infiltrating CD8 + T Cells in Hepatocellular Carcinoma journal, October 2019

A new therapeutic target: the CD69-Myl9 system in immune responses journal, April 2019

The activation of bystander CD8+ T cells and their roles in viral infection journal, December 2019

Tissue-resident lymphocytes: from adaptive to innate immunity journal, January 2019

Local heroes or villains: tissue-resident memory T cells in human health and disease journal, January 2020

CD8+ T cell states in human cancer: insights from single-cell analysis journal, February 2020

Precursor exhausted T cells: key to successful immunotherapy? journal, October 2019

Tissue patrol by resident memory CD8+ T cells in human skin journal, May 2019

Clonal replacement of tumor-specific T cells following PD-1 blockade journal, July 2019

Developing neoantigen-targeted T cell–based treatments for solid tumors journal, October 2019

Sequential adjustment of cytotoxic T lymphocyte densities improves efficacy in controlling tumor growth journal, August 2019

The Adaptive and Innate Immune Cell Landscape of Uterine Leiomyosarcomas journal, January 2020

T cell receptor‐based cancer immunotherapy: Emerging efficacy and pathways of resistance journal, July 2019

Distinct epigenetic features of tumor-reactive CD8+ T cells in colorectal cancer patients revealed by genome-wide DNA methylation analysis journal, December 2019

Neoantigen-specific immunity in low mutation burden colorectal cancers of the consensus molecular subtype 4 journal, December 2019

Late-differentiated effector neoantigen-specific CD8+ T cells are enriched in peripheral blood of non-small cell lung carcinoma patients responding to atezolizumab treatment journal, September 2019

Monitoring and characterizing soluble and membrane-bound ectonucleotidases CD73 and CD39 journal, October 2019

Renal Cell Carcinoma (RCC) Tumors Display Large Expansion of Double Positive (DP) CD4+CD8+ T Cells With Expression of Exhaustion Markers journal, November 2018

The Tumor Microenvironment in Colorectal Cancer Therapy journal, August 2019

Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients
journal, February 2016

Overcoming T cell exhaustion in infection and cancer
journal, April 2015

Tumor- and Neoantigen-Reactive T-cell Receptors Can Be Identified Based on Their Frequency in Fresh Tumor
journal, June 2016

CD137 Accurately Identifies and Enriches for Naturally Occurring Tumor-Reactive T Cells in Tumor
journal, September 2013

Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer
journal, June 2017

Cancer Regression in Patients After Transfer of Genetically Engineered Lymphocytes
journal, October 2006

Tissue-resident memory T cells: local specialists in immune defence
journal, December 2015

Tissue-Resident Memory T Cells
journal, December 2014

Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications
journal, July 2009

Method for assessing the similarity between subsets of the T cell receptor repertoire
journal, January 2008

PD-1 and CD103 Are Widely Coexpressed on Prognostically Favorable Intraepithelial CD8 T Cells in Human Ovarian Cancer
journal, May 2015

PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors
journal, March 2014

Tumor-Infiltrating Lymphocytes Expressing the Tissue Resident Memory Marker CD103 Are Associated with Increased Survival in High-Grade Serous Ovarian Cancer
journal, November 2013

Tumor antigen–specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired
journal, August 2009

Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients
journal, June 2011

TGF-β–dependent CD103 expression by CD8 ⁺ T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease
journal, May 2005

Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
journal, September 2005

Cancer Regression and Autoimmunity in Patients After Clonal Repopulation with Antitumor Lymphocytes
journal, September 2002

Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells
journal, October 2016

Adoptive T cell therapy using antigen-specific CD8⁺ T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells
journal, November 2002

Resident memory CD8 T cells trigger protective innate and adaptive immune responses
journal, August 2014

CD39 Expression Defines Cell Exhaustion in Tumor-Infiltrating CD8 ⁺ T Cells
journal, October 2017

Cutting Edge: CD69 Interference with Sphingosine-1-Phosphate Receptor Function Regulates Peripheral T Cell Retention
journal, January 2015

CD103+ intraepithelial T cells in high-grade serous ovarian cancer are phenotypically diverse TCRαβ+ CD8αβ+ T cells that can be targeted for cancer immunotherapy
journal, September 2016

Phase I Study of Adoptive T-Cell Therapy Using Antigen-Specific CD8 ⁺ T Cells for the Treatment of Patients With Metastatic Melanoma
journal, November 2006

Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes
journal, April 2016

Selection of CD8+PD-1+ Lymphocytes in Fresh Human Melanomas Enriches for Tumor-reactive T Cells
journal, January 2010

A Solution to the Problem of Monotone Likelihood in Cox Regression
journal, March 2001

TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance
journal, November 2005

Chromatin states define tumour-specific T cell dysfunction and reprogramming
journal, May 2017

Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes
journal, September 2015

Molecular Signatures Distinguish Human Central Memory from Effector Memory CD8 T Cell Subsets
journal, October 2005

Targeting Cancer-Derived Adenosine:New Therapeutic Approaches
journal, July 2014

Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen–specific CD8 ⁺ T cell dysfunction in melanoma patients
journal, September 2010

Microsatellite Instability as a Biomarker for PD-1 Blockade
journal, February 2016

Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression
journal, May 2007

limma powers differential expression analyses for RNA-sequencing and microarray studies
journal, January 2015

Exploiting the curative potential of adoptive T-cell therapy for cancer
journal, December 2013

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
journal, September 2017

Human Tumor Antigens Yesterday, Today, and Tomorrow
journal, May 2017

PD-1 Blockade in Tumors with Mismatch-Repair Deficiency
journal, June 2015

CD103 defines intraepithelial CD8+ PD1+ tumour-infiltrating lymphocytes of prognostic significance in endometrial adenocarcinoma
journal, June 2016

Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities
journal, July 2007

Therapeutic T cell engineering
journal, May 2017

CD39 and CD73 in immunity and inflammation
journal, June 2013

Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade
journal, June 2017

CD39 Expression Identifies Terminally Exhausted CD8+ T Cells
journal, October 2015

CD8 ⁺ CD103 ⁺ Tumor–Infiltrating Lymphocytes Are Tumor-Specific Tissue-Resident Memory T Cells and a Prognostic Factor for Survival in Lung Cancer Patients
journal, February 2015

CD103 ⁺ Tumor Infiltrating Lymphocytes Predict a Favorable Prognosis in Urothelial Cell Carcinoma of the Bladder
journal, August 2015

CD8+ T-cell memory in tumor immunology and immunotherapy
journal, June 2006

TGFβ in Cancer
journal, July 2008

Tissue-resident memory T cells
journal, August 2013

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
text, January 2017

An integrative analysis of the age-associated multi-omic landscape across cancers
journal, April 2021

PD-1 blockade in tumors with mismatch-repair deficiency: Le DT (2015) N Engl J Med May 30
journal, June 2015

Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
journal, January 2018

limma powers differential expression analyses for RNA-sequencing and microarray studies
text, January 2015

Accumulation of CD103 ⁺ CD8 ⁺ T cells in a cutaneous melanoma micrometastasis
journal, January 2019

4‐1BB Delineates Distinct Activation Status of Exhausted Tumor‐Infiltrating CD8 ⁺ T Cells in Hepatocellular Carcinoma
journal, October 2019

A new therapeutic target: the CD69-Myl9 system in immune responses
journal, April 2019

The activation of bystander CD8+ T cells and their roles in viral infection
journal, December 2019

Tissue-resident lymphocytes: from adaptive to innate immunity
journal, January 2019

Local heroes or villains: tissue-resident memory T cells in human health and disease
journal, January 2020

CD8+ T cell states in human cancer: insights from single-cell analysis
journal, February 2020

Precursor exhausted T cells: key to successful immunotherapy?
journal, October 2019

Tissue patrol by resident memory CD8+ T cells in human skin
journal, May 2019

Clonal replacement of tumor-specific T cells following PD-1 blockade
journal, July 2019

Developing neoantigen-targeted T cell–based treatments for solid tumors
journal, October 2019

Sequential adjustment of cytotoxic T lymphocyte densities improves efficacy in controlling tumor growth
journal, August 2019

The Adaptive and Innate Immune Cell Landscape of Uterine Leiomyosarcomas
journal, January 2020

T cell receptor‐based cancer immunotherapy: Emerging efficacy and pathways of resistance
journal, July 2019

Distinct epigenetic features of tumor-reactive CD8+ T cells in colorectal cancer patients revealed by genome-wide DNA methylation analysis
journal, December 2019

Neoantigen-specific immunity in low mutation burden colorectal cancers of the consensus molecular subtype 4
journal, December 2019

Late-differentiated effector neoantigen-specific CD8+ T cells are enriched in peripheral blood of non-small cell lung carcinoma patients responding to atezolizumab treatment
journal, September 2019

Monitoring and characterizing soluble and membrane-bound ectonucleotidases CD73 and CD39
journal, October 2019

Renal Cell Carcinoma (RCC) Tumors Display Large Expansion of Double Positive (DP) CD4+CD8+ T Cells With Expression of Exhaustion Markers
journal, November 2018

The Tumor Microenvironment in Colorectal Cancer Therapy
journal, August 2019

Virus-specific memory T cells populate tumors and can be repurposed for tumor immunotherapy
journal, February 2019

Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis
journal, June 2018

T cell antigen discovery via trogocytosis
journal, January 2019