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Cancer Immunology Research
Cancer Immunology Research
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Research Articles

Glycans as Immune Checkpoints: Removal of Branched N-glycans Enhances Immune Recognition Preventing Cancer Progression

Mariana C. Silva, Ângela Fernandes, Maria Oliveira, Carlos Resende, Alexandra Correia, Julio C. de-Freitas-Junior, Aonghus Lavelle, Jéssica Andrade-da-Costa, Magdalena Leander, Helena Xavier-Ferreira, José Bessa, Carina Pereira, Rui M. Henrique, Fátima Carneiro, Mário Dinis-Ribeiro, Ricardo Marcos-Pinto, Margarida Lima, Bernd Lepenies, Harry Sokol, José C. Machado, Manuel Vilanova and Salomé S. Pinho
Mariana C. Silva
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
2Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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Ângela Fernandes
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
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Maria Oliveira
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
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Carlos Resende
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
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Alexandra Correia
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
2Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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Julio C. de-Freitas-Junior
3Cellular and Molecular Oncobiology Program, Brazilian National Cancer Institute (INCA), Rio de Janeiro, Brazil.
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Aonghus Lavelle
4Sorbonne Université, INSERM, Saint-Antoine Research Center (CRSA), Paris, France.
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Jéssica Andrade-da-Costa
3Cellular and Molecular Oncobiology Program, Brazilian National Cancer Institute (INCA), Rio de Janeiro, Brazil.
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Magdalena Leander
5Department of Hematology, Hospital Center of Porto, Porto, Portugal.
6Multidisciplinary Unit for Biomedical Research, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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Helena Xavier-Ferreira
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
2Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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José Bessa
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
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Carina Pereira
7CINTESIS – Centre for Health Technology and Services Research, University of Porto, Porto, Portugal.
8Molecular Oncology and Viral Pathology Group, IPO Porto Research Group (CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto, Portugal.
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  • ORCID record for Carina Pereira
Rui M. Henrique
9Department of Pathology and Cancer Biology and Epigenetics Group, IPO Porto Research Center (CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto, Portugal.
10Department of Pathology and Molecular Immunology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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Fátima Carneiro
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
11Department of Pathology, Hospital Center of São João, Porto, Portugal.
12Faculty of Medicine, University of Porto, Porto, Portugal.
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Mário Dinis-Ribeiro
7CINTESIS – Centre for Health Technology and Services Research, University of Porto, Porto, Portugal.
13Department of Gastroenterology, Portuguese Oncology Institute of Porto (IPO Porto), Porto, Portugal.
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Ricardo Marcos-Pinto
2Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
14Department of Gastroenterology, Hospital Center of Porto, Porto, Portugal.
15Medical Faculty, Centre for Research in Health Technologies and Information Systems, Porto, Portugal.
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Margarida Lima
5Department of Hematology, Hospital Center of Porto, Porto, Portugal.
6Multidisciplinary Unit for Biomedical Research, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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Bernd Lepenies
16Department of Biomolecular Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany.
17Immunology Unit and Research Center for Emerging Infections and Zoonoses, University of Veterinary Medicine Hannover, Hannover, Germany.
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Harry Sokol
4Sorbonne Université, INSERM, Saint-Antoine Research Center (CRSA), Paris, France.
18INRA, UMR1319 Micalis, AgroParisTech, Jouy-en-Josas, France.
19Department of Gastroenterology, Saint Antoine Hospital, Assistance Publique - Hopitaux de Paris, Sorbonne Universités, Paris, France.
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José C. Machado
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
12Faculty of Medicine, University of Porto, Porto, Portugal.
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Manuel Vilanova
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
2Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Porto, Portugal.
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Salomé S. Pinho
1Institute for Research and Innovation in Health (i3S), University of Porto, Porto, Portugal.
12Faculty of Medicine, University of Porto, Porto, Portugal.
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  • For correspondence: salomep@ipatimup.pt
DOI: 10.1158/2326-6066.CIR-20-0264 Published November 2020
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Abstract

Tumor growth is accompanied with dramatic changes in the cellular glycome, such as the aberrant expression of complex branched N-glycans. However, the role of this protumoral N-glycan in immune evasion and whether its removal contributes to enhancement of immune recognition and to unleashing an antitumor immune response remain elusive. We demonstrated that branched N-glycans are used by colorectal cancer cells to escape immune recognition, instructing the creation of immunosuppressive networks through inhibition of IFNγ. The removal of this “glycan-mask” exposed immunogenic mannose glycans that potentiated immune recognition by DC-SIGN–expressing immune cells, resulting in an effective antitumor immune response. We revealed a glycoimmune checkpoint in colorectal cancer, highlighting the therapeutic efficacy of its deglycosylation to potentiate immune recognition and, thus, improving cancer immunotherapy.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • Cancer Immunol Res 2020;8:1407–25

  • Received April 9, 2020.
  • Revision received July 3, 2020.
  • Accepted September 8, 2020.
  • Published first September 15, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Immunology Research: 8 (11)
November 2020
Volume 8, Issue 11
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Glycans as Immune Checkpoints: Removal of Branched N-glycans Enhances Immune Recognition Preventing Cancer Progression
Mariana C. Silva, Ângela Fernandes, Maria Oliveira, Carlos Resende, Alexandra Correia, Julio C. de-Freitas-Junior, Aonghus Lavelle, Jéssica Andrade-da-Costa, Magdalena Leander, Helena Xavier-Ferreira, José Bessa, Carina Pereira, Rui M. Henrique, Fátima Carneiro, Mário Dinis-Ribeiro, Ricardo Marcos-Pinto, Margarida Lima, Bernd Lepenies, Harry Sokol, José C. Machado, Manuel Vilanova and Salomé S. Pinho
Cancer Immunol Res November 1 2020 (8) (11) 1407-1425; DOI: 10.1158/2326-6066.CIR-20-0264

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Glycans as Immune Checkpoints: Removal of Branched N-glycans Enhances Immune Recognition Preventing Cancer Progression
Mariana C. Silva, Ângela Fernandes, Maria Oliveira, Carlos Resende, Alexandra Correia, Julio C. de-Freitas-Junior, Aonghus Lavelle, Jéssica Andrade-da-Costa, Magdalena Leander, Helena Xavier-Ferreira, José Bessa, Carina Pereira, Rui M. Henrique, Fátima Carneiro, Mário Dinis-Ribeiro, Ricardo Marcos-Pinto, Margarida Lima, Bernd Lepenies, Harry Sokol, José C. Machado, Manuel Vilanova and Salomé S. Pinho
Cancer Immunol Res November 1 2020 (8) (11) 1407-1425; DOI: 10.1158/2326-6066.CIR-20-0264
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