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Cancer Immunology Research
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Hyperglycemia Enhances Cancer Immune Evasion by Inducing Alternative Macrophage Polarization through Increased O-GlcNAcylation

Natália Rodrigues Mantuano, Michal A. Stanczak, Isadora de Araújo Oliveira, Nicole Kirchhammer, Alessandra A. Filardy, Gianni Monaco, Ronan Christian Santos, Agatha Carlos Fonseca, Miguel Fontes, César de Souza Bastos Jr, Wagner B. Dias, Alfred Zippelius, Adriane R. Todeschini and Heinz Läubli
Natália Rodrigues Mantuano
1Cancer Immunology Laboratory, Department of Biomedicine, University of Basel, Basel, Switzerland.
2Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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Michal A. Stanczak
1Cancer Immunology Laboratory, Department of Biomedicine, University of Basel, Basel, Switzerland.
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Isadora de Araújo Oliveira
2Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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  • ORCID record for Isadora de Araújo Oliveira
Nicole Kirchhammer
1Cancer Immunology Laboratory, Department of Biomedicine, University of Basel, Basel, Switzerland.
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Alessandra A. Filardy
2Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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Gianni Monaco
1Cancer Immunology Laboratory, Department of Biomedicine, University of Basel, Basel, Switzerland.
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Ronan Christian Santos
2Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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Agatha Carlos Fonseca
3Hospital Naval Marcílio Dias, Rio de Janeiro, Brazil.
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Miguel Fontes
3Hospital Naval Marcílio Dias, Rio de Janeiro, Brazil.
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César de Souza Bastos Jr
3Hospital Naval Marcílio Dias, Rio de Janeiro, Brazil.
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Wagner B. Dias
2Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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Alfred Zippelius
1Cancer Immunology Laboratory, Department of Biomedicine, University of Basel, Basel, Switzerland.
4Division of Oncology, Department of Internal Medicine, University Hospital Basel, Basel, Switzerland.
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Adriane R. Todeschini
2Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
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  • ORCID record for Adriane R. Todeschini
  • For correspondence: heinz.laeubli@unibas.ch adrianet@biof.ufrj.br
Heinz Läubli
1Cancer Immunology Laboratory, Department of Biomedicine, University of Basel, Basel, Switzerland.
4Division of Oncology, Department of Internal Medicine, University Hospital Basel, Basel, Switzerland.
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  • For correspondence: heinz.laeubli@unibas.ch adrianet@biof.ufrj.br
DOI: 10.1158/2326-6066.CIR-19-0904 Published October 2020
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Abstract

Diabetes mellitus (DM) significantly increases the risk for cancer and cancer progression. Hyperglycemia is the defining characteristic of DM and tightly correlates with a poor prognosis in patients with cancer. The hexosamine biosynthetic pathway (HBP) is emerging as a pivotal cascade linking high glucose, tumor progression, and impaired immune function. Here we show that enhanced glucose flow through the HBP drives cancer progression and immune evasion by increasing O-GlcNAcylation in tumor-associated macrophages (TAM). Increased O-GlcNAc skewed macrophage polarization to a M2-like phenotype supporting tumor progression. Finally, we found an upregulation of M2 markers on TAMs in DM2 patients with colorectal cancer compared with nondiabetic normoglycemic patients. Our results provide evidence for a new and targetable mechanism of cancer immune evasion in patients with hyperglycemia, advocating for strict control of hyperglycemia in patients with cancer.

Footnotes

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

  • Cancer Immunol Res 2020;8:1262–72

  • Received November 14, 2019.
  • Revision received April 25, 2020.
  • Accepted July 21, 2020.
  • Published first July 27, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Immunology Research: 8 (10)
October 2020
Volume 8, Issue 10
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Hyperglycemia Enhances Cancer Immune Evasion by Inducing Alternative Macrophage Polarization through Increased O-GlcNAcylation
Natália Rodrigues Mantuano, Michal A. Stanczak, Isadora de Araújo Oliveira, Nicole Kirchhammer, Alessandra A. Filardy, Gianni Monaco, Ronan Christian Santos, Agatha Carlos Fonseca, Miguel Fontes, César de Souza Bastos Jr, Wagner B. Dias, Alfred Zippelius, Adriane R. Todeschini and Heinz Läubli
Cancer Immunol Res October 1 2020 (8) (10) 1262-1272; DOI: 10.1158/2326-6066.CIR-19-0904

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Hyperglycemia Enhances Cancer Immune Evasion by Inducing Alternative Macrophage Polarization through Increased O-GlcNAcylation
Natália Rodrigues Mantuano, Michal A. Stanczak, Isadora de Araújo Oliveira, Nicole Kirchhammer, Alessandra A. Filardy, Gianni Monaco, Ronan Christian Santos, Agatha Carlos Fonseca, Miguel Fontes, César de Souza Bastos Jr, Wagner B. Dias, Alfred Zippelius, Adriane R. Todeschini and Heinz Läubli
Cancer Immunol Res October 1 2020 (8) (10) 1262-1272; DOI: 10.1158/2326-6066.CIR-19-0904
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