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

Journal Article · Fri Jul 13 00:00:00 EDT 2018 · Nature Communications

DOI:https://doi.org/10.1038/S41467-018-05072-0· OSTI ID:1463347

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)

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.

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

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1463347

Report Number(s):: PNNL-SA135245; PII: 5072

Journal Information:: Nature Communications, Vol. 9, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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References (57)

Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients Gros, Alena; Parkhurst, Maria R.; Tran, Eric Nature Medicine, Vol. 22, Issue 4 https://doi.org/10.1038/nm.4051	journal	February 2016
Overcoming T cell exhaustion in infection and cancer Pauken, Kristen E.; Wherry, E. John Trends in Immunology, Vol. 36, Issue 4 https://doi.org/10.1016/j.it.2015.02.008	journal	April 2015
Tumor- and Neoantigen-Reactive T-cell Receptors Can Be Identified Based on Their Frequency in Fresh Tumor Pasetto, A.; Gros, A.; Robbins, P. F. Cancer Immunology Research, Vol. 4, Issue 9 https://doi.org/10.1158/2326-6066.CIR-16-0001	journal	June 2016
CD137 Accurately Identifies and Enriches for Naturally Occurring Tumor-Reactive T Cells in Tumor Ye, Q.; Song, D. -G.; Poussin, M. Clinical Cancer Research, Vol. 20, Issue 1 https://doi.org/10.1158/1078-0432.CCR-13-0945	journal	September 2013
Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer Ganesan, Anusha-Preethi; Clarke, James; Wood, Oliver Nature Immunology, Vol. 18, Issue 8 https://doi.org/10.1038/ni.3775	journal	June 2017
Cancer Regression in Patients After Transfer of Genetically Engineered Lymphocytes Morgan, R. A.; Dudley, M. E.; Wunderlich, J. R. Science, Vol. 314, Issue 5796 https://doi.org/10.1126/science.1129003	journal	October 2006
Tissue-resident memory T cells: local specialists in immune defence Mueller, Scott N.; Mackay, Laura K. Nature Reviews Immunology, Vol. 16, Issue 2 https://doi.org/10.1038/nri.2015.3	journal	December 2015
Tissue-Resident Memory T Cells Schenkel, Jason M.; Masopust, David Immunity, Vol. 41, Issue 6 https://doi.org/10.1016/j.immuni.2014.12.007	journal	December 2014
Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications Lynch, Ht; Lynch, Pm; Lanspa, Sj Clinical Genetics, Vol. 76, Issue 1 https://doi.org/10.1111/j.1399-0004.2009.01230.x	journal	July 2009
Method for assessing the similarity between subsets of the T cell receptor repertoire Venturi, Vanessa; Kedzierska, Katherine; Tanaka, Mark M. Journal of Immunological Methods, Vol. 329, Issue 1-2 https://doi.org/10.1016/j.jim.2007.09.016	journal	January 2008
PD-1 and CD103 Are Widely Coexpressed on Prognostically Favorable Intraepithelial CD8 T Cells in Human Ovarian Cancer Webb, J. R.; Milne, K.; Nelson, B. H. Cancer Immunology Research, Vol. 3, Issue 8 https://doi.org/10.1158/2326-6066.CIR-14-0239	journal	May 2015
PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors Gros, Alena; Robbins, Paul F.; Yao, Xin Journal of Clinical Investigation, Vol. 124, Issue 5 https://doi.org/10.1172/JCI73639	journal	March 2014
Tumor-Infiltrating Lymphocytes Expressing the Tissue Resident Memory Marker CD103 Are Associated with Increased Survival in High-Grade Serous Ovarian Cancer Webb, J. R.; Milne, K.; Watson, P. Clinical Cancer Research, Vol. 20, Issue 2 https://doi.org/10.1158/1078-0432.CCR-13-1877	journal	November 2013
Tumor antigen–specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired Ahmadzadeh, Mojgan; Johnson, Laura A.; Heemskerk, Bianca Blood, Vol. 114, Issue 8 https://doi.org/10.1182/blood-2008-12-195792	journal	August 2009
Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients Baitsch, Lukas; Baumgaertner, Petra; Devêvre, Estelle Journal of Clinical Investigation, Vol. 121, Issue 6 https://doi.org/10.1172/JCI46102	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 El-Asady, Riham; Yuan, Rongwen; Liu, Kechang The Journal of Experimental Medicine, Vol. 201, Issue 10 https://doi.org/10.1084/jem.20041044	journal	May 2005
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles Subramanian, A.; Tamayo, P.; Mootha, V. K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 43, p. 15545-15550 https://doi.org/10.1073/pnas.0506580102	journal	September 2005
Cancer Regression and Autoimmunity in Patients After Clonal Repopulation with Antitumor Lymphocytes Dudley, M. E. Science, Vol. 298, Issue 5594 https://doi.org/10.1126/science.1076514	journal	September 2002
Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells Hombrink, Pleun; Helbig, Christina; Backer, Ronald A. Nature Immunology, Vol. 17, Issue 12 https://doi.org/10.1038/ni.3589	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 Yee, C.; Thompson, J. A.; Byrd, D. Proceedings of the National Academy of Sciences, Vol. 99, Issue 25, p. 16168-16173 https://doi.org/10.1073/pnas.242600099	journal	November 2002
Resident memory CD8 T cells trigger protective innate and adaptive immune responses Schenkel, Jason M.; Fraser, Kathryn A.; Beura, Lalit K. Science, Vol. 346, Issue 6205 https://doi.org/10.1126/science.1254536	journal	August 2014
CD39 Expression Defines Cell Exhaustion in Tumor-Infiltrating CD8 ⁺ T Cells Canale, Fernando P.; Ramello, María C.; Núñez, Nicolás Cancer Research, Vol. 78, Issue 1 https://doi.org/10.1158/0008-5472.CAN-16-2684	journal	October 2017
Cutting Edge: CD69 Interference with Sphingosine-1-Phosphate Receptor Function Regulates Peripheral T Cell Retention Mackay, Laura K.; Braun, Asolina; Macleod, Bethany L. The Journal of Immunology, Vol. 194, Issue 5 https://doi.org/10.4049/jimmunol.1402256	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 Komdeur, Fenne L.; Wouters, Maartje C. A.; Workel, Hagma H. Oncotarget, Vol. 7, Issue 46 https://doi.org/10.18632/oncotarget.12077	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 Mackensen, Andreas; Meidenbauer, Norbert; Vogl, Sandra Journal of Clinical Oncology, Vol. 24, Issue 31 https://doi.org/10.1200/JCO.2006.07.1100	journal	November 2006
Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes Mackay, L. K.; Minnich, M.; Kragten, N. A. M. Science, Vol. 352, Issue 6284 https://doi.org/10.1126/science.aad2035	journal	April 2016
Selection of CD8+PD-1+ Lymphocytes in Fresh Human Melanomas Enriches for Tumor-reactive T Cells Inozume, Takashi; Hanada, Ken-ichi; Wang, Qiong J. Journal of Immunotherapy, Vol. 33, Issue 9 https://doi.org/10.1097/CJI.0b013e3181fad2b0	journal	January 2010
A Solution to the Problem of Monotone Likelihood in Cox Regression Heinze, Georg; Schemper, Michael Biometrics, Vol. 57, Issue 1 https://doi.org/10.1111/j.0006-341X.2001.00114.x	journal	March 2001
TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance Thomas, Dori A.; Massagué, Joan Cancer Cell, Vol. 8, Issue 5 https://doi.org/10.1016/j.ccr.2005.10.012	journal	November 2005
Chromatin states define tumour-specific T cell dysfunction and reprogramming Philip, Mary; Fairchild, Lauren; Sun, Liping Nature, Vol. 545, Issue 7655 https://doi.org/10.1038/nature22367	journal	May 2017
Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes Cohen, Cyrille J.; Gartner, Jared J.; Horovitz-Fried, Miryam Journal of Clinical Investigation, Vol. 125, Issue 10 https://doi.org/10.1172/JCI82416	journal	September 2015
Molecular Signatures Distinguish Human Central Memory from Effector Memory CD8 T Cell Subsets Willinger, Tim; Freeman, Tom; Hasegawa, Hitoshi The Journal of Immunology, Vol. 175, Issue 9 https://doi.org/10.4049/jimmunol.175.9.5895	journal	October 2005
Targeting Cancer-Derived Adenosine:New Therapeutic Approaches Young, A.; Mittal, D.; Stagg, J. Cancer Discovery, Vol. 4, Issue 8 https://doi.org/10.1158/2159-8290.CD-14-0341	journal	July 2014
Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen–specific CD8 ⁺ T cell dysfunction in melanoma patients Fourcade, Julien; Sun, Zhaojun; Benallaoua, Mourad The Journal of Experimental Medicine, Vol. 207, Issue 10 https://doi.org/10.1084/jem.20100637	journal	September 2010
Microsatellite Instability as a Biomarker for PD-1 Blockade Dudley, J. C.; Lin, M. -T.; Le, D. T. Clinical Cancer Research, Vol. 22, Issue 4 https://doi.org/10.1158/1078-0432.CCR-15-1678	journal	February 2016
Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression Deaglio, Silvia; Dwyer, Karen M.; Gao, Wenda The Journal of Experimental Medicine, Vol. 204, Issue 6 https://doi.org/10.1084/jem.20062512	journal	May 2007
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Nucleic Acids Research, Vol. 43, Issue 7 https://doi.org/10.1093/nar/gkv007	journal	January 2015
Exploiting the curative potential of adoptive T-cell therapy for cancer Hinrichs, Christian S.; Rosenberg, Steven A. Immunological Reviews, Vol. 257, Issue 1 https://doi.org/10.1111/imr.12132	journal	December 2013
Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites Kumar, Brahma V.; Ma, Wenji; Miron, Michelle Cell Reports, Vol. 20, Issue 12 https://doi.org/10.1016/j.celrep.2017.08.078	journal	September 2017
Human Tumor Antigens Yesterday, Today, and Tomorrow Finn, Olivera J. Cancer Immunology Research, Vol. 5, Issue 5 https://doi.org/10.1158/2326-6066.CIR-17-0112	journal	May 2017
PD-1 Blockade in Tumors with Mismatch-Repair Deficiency Le, Dung T.; Uram, Jennifer N.; Wang, Hao New England Journal of Medicine, Vol. 372, Issue 26 https://doi.org/10.1056/NEJMoa1500596	journal	June 2015
CD103 defines intraepithelial CD8+ PD1+ tumour-infiltrating lymphocytes of prognostic significance in endometrial adenocarcinoma Workel, Hagma H.; Komdeur, Fenne L.; Wouters, Maartje C. A. European Journal of Cancer, Vol. 60 https://doi.org/10.1016/j.ejca.2016.02.026	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 Wolfl, Matthias; Kuball, Jürgen; Ho, William Y. Blood, Vol. 110, Issue 1 https://doi.org/10.1182/blood-2006-11-056168	journal	July 2007
Therapeutic T cell engineering Sadelain, Michel; Rivière, Isabelle; Riddell, Stanley Nature, Vol. 545, Issue 7655 https://doi.org/10.1038/nature22395	journal	May 2017
CD39 and CD73 in immunity and inflammation Antonioli, Luca; Pacher, Pál; Vizi, E. Sylvester Trends in Molecular Medicine, Vol. 19, Issue 6 https://doi.org/10.1016/j.molmed.2013.03.005	journal	June 2013
Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade Le, Dung T.; Durham, Jennifer N.; Smith, Kellie N. Science, Vol. 357, Issue 6349 https://doi.org/10.1126/science.aan6733	journal	June 2017
CD39 Expression Identifies Terminally Exhausted CD8+ T Cells Gupta, Prakash K.; Godec, Jernej; Wolski, David PLOS Pathogens, Vol. 11, Issue 10 https://doi.org/10.1371/journal.ppat.1005177	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 Djenidi, Fayçal; Adam, Julien; Goubar, Aïcha The Journal of Immunology, Vol. 194, Issue 7 https://doi.org/10.4049/jimmunol.1402711	journal	February 2015
CD103 ⁺ Tumor Infiltrating Lymphocytes Predict a Favorable Prognosis in Urothelial Cell Carcinoma of the Bladder Wang, Bo; Wu, Shaoxu; Zeng, Hong Journal of Urology, Vol. 194, Issue 2 https://doi.org/10.1016/j.juro.2015.02.2941	journal	August 2015
CD8+ T-cell memory in tumor immunology and immunotherapy Klebanoff, Christopher A.; Gattinoni, Luca; Restifo, Nicholas P. Immunological Reviews, Vol. 211, Issue 1 https://doi.org/10.1111/j.0105-2896.2006.00391.x	journal	June 2006
TGFβ in Cancer Massagué, Joan Cell, Vol. 134, Issue 2 https://doi.org/10.1016/j.cell.2008.07.001	journal	July 2008
Tissue-resident memory T cells Shin, Haina; Iwasaki, Akiko Immunological Reviews, Vol. 255, Issue 1 https://doi.org/10.1111/imr.12087	journal	August 2013
Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites Kumar, Brahma Vencel; Ma, Wenji; Miron, Michelle Columbia University https://doi.org/10.7916/d89p4d5f	text	January 2017
An integrative analysis of the age-associated multi-omic landscape across cancers Chatsirisupachai, Kasit; Lesluyes, Tom; Paraoan, Luminita Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22560-y	journal	April 2021
PD-1 blockade in tumors with mismatch-repair deficiency: Le DT (2015) N Engl J Med May 30 Aparicio, T. Côlon & Rectum, Vol. 9, Issue 3 https://doi.org/10.1007/s11725-015-0588-4	journal	June 2015
Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites Kumar, Brahma V.; Ma, Wenji; Miron, Michelle SSRN Electronic Journal https://doi.org/10.2139/ssrn.3155546	journal	January 2018
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Oxford University Press https://doi.org/10.5167/uzh-155268	text	January 2015

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