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Citations to this article

CD73 has distinct roles in nonhematopoietic and hematopoietic cells to promote tumor growth in mice
Long Wang, … , Tyler J. Curiel, Bin Zhang
Long Wang, … , Tyler J. Curiel, Bin Zhang
Published May 2, 2011
Citation Information: J Clin Invest. 2011;121(6):2371-2382. https://doi.org/10.1172/JCI45559.
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CD73 has distinct roles in nonhematopoietic and hematopoietic cells to promote tumor growth in mice

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Abstract

CD73 is overexpressed in many types of human and mouse cancers and is implicated in the control of tumor progression. However, the specific contribution from tumor or host CD73 expression to tumor growth remains unknown to date. Here, we show that host CD73 promotes tumor growth in a T cell–dependent manner and that the optimal antitumor effect of CD73 blockade requires inhibiting both tumor and host CD73. Notably, enzymatic activity of CD73 on nonhematopoietic cells limited tumor-infiltrating T cells by controlling antitumor T cell homing to tumors in multiple mouse tumor models. In contrast, CD73 on hematopoietic cells (including CD4+CD25+ Tregs) inhibited systemic antitumor T cell expansion and effector functions. Thus, CD73 on hematopoietic and nonhematopoietic cells has distinct adenosinergic effects in regulating systemic and local antitumor T cell responses. Importantly, pharmacological blockade of CD73 using its selective inhibitor or an anti-CD73 mAb inhibited tumor growth and completely restored efficacy of adoptive T cell therapy in mice. These findings suggest that both tumor and host CD73 cooperatively protect tumors from incoming antitumor T cells and show the potential of targeting CD73 as a cancer immunotherapy strategy.

Authors

Long Wang, Jie Fan, Linda F. Thompson, Yi Zhang, Tahiro Shin, Tyler J. Curiel, Bin Zhang

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Cancer research 2016
Identification of a novel human memory T-cell population with the characteristics of stem-like chemo-resistance
K Murata, T Tsukahara, M Emori, Y Shibayama, E Mizushima, H Matsumiya, K Yamashita, M Kaya, Y Hirohashi, T Kanaseki, T Kubo, T Himi, S Ichimiya, T Yamashita, N Sato, T Torigoe
OncoImmunology 2016
Damage-associated molecular patterns in cancer: a double-edged sword
C Hernandez, P Huebener, RF Schwabe
Oncogene 2016
Anti-CD73 in Cancer Immunotherapy: Awakening New Opportunities
L Antonioli, GG Yegutkin, P Pacher, C Blandizzi, G Haskó
Trends in Cancer 2016
Trial Watch—Small molecules targeting the immunological tumor microenvironment for cancer therapy
A Buqué, N Bloy, F Aranda, I Cremer, A Eggermont, WH Fridman, J Fucikova, J Galon, R Spisek, E Tartour, L Zitvogel, G Kroemer, L Galluzzi
OncoImmunology 2016
Downregulation of CD73 in 4T1 breast cancer cells through siRNA-loaded chitosan-lactate nanoparticles
F Jadidi-Niaragh, F Atyabi, A Rastegari, E Mollarazi, M Kiani, A Razavi, M Yousefi, N Kheshtchin, H Hassannia, J Hadjati, F Shokri
Tumor Biology 2016
CD73 Expressed on γδ T Cells Shapes Their Regulatory Effect in Experimental Autoimmune Uveitis
D Liang, A Zuo, R Zhao, H Shao, WK Born, RL O'Brien, HJ Kaplan, D Sun, X Bai
PloS one 2016
Loss of CD73-mediated actin polymerization promotes endometrial tumor progression
Jessica L. Bowser, Michael R. Blackburn, Gregory L. Shipley, Jose G. Molina, Kenneth Dunner Jr., Russell R. Broaddus
Journal of Clinical Investigation 2015
Combination cancer immunotherapies tailored to the tumour microenvironment
MJ Smyth, SF Ngiow, A Ribas, MW Teng
Nature Reviews Clinical Oncology 2015
Immunological landscape and immunotherapy of hepatocellular carcinoma
J Prieto, I Melero, B Sangro
Nature Reviews Gastroenterology & Hepatology 2015
Big opportunities for small molecules in immuno-oncology
JL Adams, J Smothers, R Srinivasan, A Hoos
Nature Reviews Drug Discovery 2015
Ecto-5′-Nucleotidase (CD73) Deficiency in Mycobacterium tuberculosis-Infected Mice Enhances Neutrophil Recruitment
L Petit-Jentreau, G Jouvion, P Charles, L Majlessi, B Gicquel, L Tailleux, S Ehrt
Infection and immunity 2015
CD73-mediated adenosine production promotes stem cell-like properties in mouse Tc17 cells
F Flores-Santibáñez, D Fernández, D Meza, G Tejón, L Vargas, L Varela-Nallar, S Arredondo, V Guixé, M Rosemblatt, MR Bono, D Sauma
Immunology 2015
Advances in Cancer Research
JD Peske, AB Woods, VH Engelhard
Advances in cancer research 2015
A2aR antagonists: Next generation checkpoint blockade for cancer immunotherapy
RD Leone, YC Lo, JD Powell
Computational and Structural Biotechnology Journal 2015
A2B adenosine receptor activation switches differentiation of bone marrow cells to a CD11c + Gr-1 + dendritic cell subset that promotes the Th17 response: Role of adenosine receptor in DC differentiation
D Liang, A Zuo, H Shao, M Chen, HJ Kaplan, D Sun
Immunity, Inflammation and Disease 2015
Targeting Ornithine Decarboxylase by  -Difluoromethylornithine Inhibits Tumor Growth by Impairing Myeloid-Derived Suppressor Cells
C Ye, Z Geng, D Dominguez, S Chen, J Fan, L Qin, A Long, Y Zhang, TM Kuzel, B Zhang
Journal of immunology (Baltimore, Md. : 1950) 2015
A non-canonical adenosinergic pathway led by CD38 in human melanoma cells induces suppression of T cell proliferation
F Morandi, B Morandi, AL Horenstein, A Chillemi, V Quarona, G Zaccarello, P Carrega, G Ferlazzo, MC Mingari, L Moretta, V Pistoia, F Malavasi
Oncotarget 2015
Alternative splicing of human NT5E in cirrhosis and hepatocellular carcinoma produces a negative regulator of ecto-5'-nucleotidase (CD73)
NT Snider, PJ Altshuler, S Wan, TH Welling, J Cavalcoli, MB Omary
Molecular biology of the cell 2014
Requirement of NK cells for selective A 2A receptor blockade to suppress CD73 + tumor metastasis
L Qin, LF Thompson, TM Kuzel, B Zhang
Immunotherapy 2014
Human CD4 + CD39 + regulatory T cells produce adenosine upon co-expression of surface CD73 or contact with CD73 + exosomes or CD73 + cells: CD73 co-expression in human CD39 + T reg
PJ Schuler, Z Saze, CS Hong, L Muller, DG Gillespie, D Cheng, M Harasymczuk, M Mandapathil, S Lang, EK Jackson, TL Whiteside
Clinical & Experimental Immunology 2014
Roles of the Adenosine Receptor and CD73 in the Regulatory Effect of γδ T Cells
Dongchun Liang, Aijun Zuo, Hui Shao, Mingjiazi Chen, Henry J. Kaplan, Deming Sun
PloS one 2014
Growth and metastasis of B16-F10 melanoma cells is not critically dependent on host CD73 expression in mice
S Burghoff, X Gong, C Viethen, C Jacoby, U Flögel, S Bongardt, A Schorr, A Hippe, B Homey, J Schrader
BMC Cancer 2014
CD73-Generated Adenosine Is Critical for Immune Regulation during Toxoplasma gondii Infection
DA Mahamed, LE Toussaint, MS Bynoe, JA Appleton
Infection and immunity 2014
Adenosine A2A Receptors Intrinsically Regulate CD8+ T Cells in the Tumor Microenvironment
C Cekic, J Linden
Cancer research 2014
Extracellular adenosine metabolism in immune cells in melanoma.
Umansky V, Shevchenko I, Bazhin AV, Utikal J
Cancer Immunology, Immunotherapy 2014
Expression and clinical significance of CD73 and hypoxia-inducible factor-1α in gastric carcinoma
XX Lu, YT Chen, B Feng, XB Mao, B Yu, XY Chu
World journal of gastroenterology : WJG 2013
Graft-versus-Host Disease Is Enhanced by Selective CD73 Blockade in Mice
L Wang, J Fan, S Chen, Y Zhang, TJ Curiel, B Zhang, T Eckle
PloS one 2013
Immunotherapeutic approaches in triple-negative breast cancer: latest research and clinical prospects
J Stagg, B Allard
Therapeutic advances in medical oncology 2013
Immunity, inflammation and cancer: a leading role for adenosine
L Antonioli, C Blandizzi, P Pacher, G Haskó
Nature Reviews Cancer 2013
Immune modulation of the tumor microenvironment for enhancing cancer immunotherapy
C Devaud, LB John, JA Westwood, PK Darcy, MH Kershaw
OncoImmunology 2013
Peripheral tissue homing receptor control of naïve, effector, and memory CD8 T cell localization in lymphoid and non-lymphoid tissues
CC Brinkman, JD Peske, VH Engelhard
Frontiers in immunology 2013
Overexpression of CD73 in Prostate Cancer is Associated with Lymph Node Metastasis
Q Yang, J Du, L Zu
Pathology & Oncology Research 2013
Blockade of A2A receptors potently suppresses the metastasis of CD73+ tumors
PA Beavis, U Divisekera, C Paget, MT Chow, LB John, C Devaud, K Dwyer, J Stagg, MJ Smyth, PK Darcy
Proceedings of the National Academy of Sciences 2013
CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer
S Loi, S Pommey, B Haibe-Kains, PA Beavis, PK Darcy, MJ Smyth, J Stagg
Proceedings of the National Academy of Sciences 2013
CD73 and adenosine generation in the creation of regulatory microenvironments
FS Regateiro, SP Cobbold, H Waldmann
Clinical & Experimental Immunology 2013
A delicate balance
LF Thompson, H Tsukamoto, P Chernogorova, R Zeiser
OncoImmunology 2013
Ectonucleotidases in solid organ and allogeneic hematopoietic cell transplantation
P Chernogorova, R Zeiser
Journal of Biomedicine and Biotechnology 2012
Production of adenosine by ectonucleotidases: a key factor in tumor immunoescape
F Ghiringhelli, M Bruchard, F Chalmin, C Rébé
Journal of Biomedicine and Biotechnology 2012
CD73-generated adenosine: orchestrating the tumor-stroma interplay to promote cancer growth
B Allard, M Turcotte, J Stagg
Journal of Biomedicine and Biotechnology 2012
Ectonucleotidases in tumor cells and tumor-associated immune cells: an overview
LS Bergamin, E Braganhol, RF Zanin, MI Edelweiss, AM Battastini
Journal of Biomedicine and Biotechnology 2012
CD73 promotes tumor growth and metastasis
B Zhang
OncoImmunology 2012
Host CD73 impairs anti-tumor immunity
M Salmi, S Jalkanen
OncoImmunology 2012
The double-edge sword effect of anti-CD73 cancer therapy
J Stagg
OncoImmunology 2012
NT5E (CD73) is epigenetically regulated in malignant melanoma and associated with metastatic site specificity
H Wang, S Lee, CL Nigro, L Lattanzio, M Merlano, M Monteverde, R Matin, K Purdie, N Mladkova, D Bergamaschi, C Harwood, N Syed, P Szlosarek, E Briasoulis, A McHugh, A Thompson, A Evans, I Leigh, C Fleming, GJ Inman, E Hatzimichael, C Proby, T Crook
British Journal of Cancer 2012
Immunomodulation via Chemotherapy and Targeted Therapy: A New Paradigm in Breast Cancer Therapy?
J Stagg, F Andre, S Loi
Breast Care 2012
Inhibition of CD73 improves B cell-mediated anti-tumor immunity in a mouse model of melanoma
G Forte, R Sorrentino, A Montinaro, A Luciano, IM Adcock, P Maiolino, C Arra, C Cicala, A Pinto, S Morello
Journal of immunology (Baltimore, Md. : 1950) 2012
Deficiency of CD73/ecto-5′-nucleotidase in mice enhances acute graft-versus-host disease
H Tsukamoto, P Chernogorova, K Ayata, UV Gerlach, A Rughani, JW Ritchey, J Ganesan, M Follo, R Zeiser, LF Thompson, M Idzko
Blood 2012
Tumor microenvironment and lymphocyte infiltration
G Rahir, M Moser
Cancer Immunology Immunotherapy 2012
CD73-generated extracellular adenosine in chronic lymphocytic leukemia creates local conditions counteracting drug-induced cell death
S Serra, AL Horenstein, T Vaisitti, D Brusa, D Rossi, L Laurenti, G D'Arena, M Coscia, C Tripodo, G Inghirami, SC Robson, G Gaidano, F Malavasi, S Deaglio
Blood 2011
Role of CD73 and extracellular adenosine in disease
SC Robson
Purinergic Signalling 2011
Intrinsic Growth Deficiencies of Mesenchymal Stromal Cells in Myelodysplastic Syndromes
CM Aanei, P Flandrin, FZ Eloae, E Carasevici, D Guyotat, E Wattel, L Campos
Stem Cells and Development 2011
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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