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Molecular Cancer Research
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Tumor Microenvironment and Immunobiology

Multiorgan Signaling Mobilizes Tumor-Associated Erythroid Cells Expressing Immune Checkpoint Molecules

Yasuyo Sano, Toshimi Yoshida, Min-Kyung Choo, Yanek Jiménez-Andrade, Kathryn R. Hill, Katia Georgopoulos and Jin Mo Park
Yasuyo Sano
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
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Toshimi Yoshida
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
2International Research Center for Medical Sciences, Kumamoto University, Kumamoto, Japan.
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Min-Kyung Choo
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
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Yanek Jiménez-Andrade
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
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  • ORCID record for Yanek Jiménez-Andrade
Kathryn R. Hill
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
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  • ORCID record for Kathryn R. Hill
Katia Georgopoulos
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
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Jin Mo Park
1Cutaneous Biology Research Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts.
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  • For correspondence: jmpark@cbrc2.mgh.harvard.edu
DOI: 10.1158/1541-7786.MCR-20-0746 Published March 2021
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Abstract

Hematopoietic-derived cells are integral components of the tumor microenvironment and serve as critical mediators of tumor–host interactions. Host cells derived from myeloid and lymphoid lineages perform well-established functions linked to cancer development, progression, and response to therapy. It is unclear whether host erythroid cells also contribute to shaping the path that cancer can take, but emerging evidence points to this possibility. Here, we show that tumor-promoting environmental stress and tumor-induced hemodynamic changes trigger renal erythropoietin production and erythropoietin-dependent expansion of splenic erythroid cell populations in mice. These erythroid cells display molecular features indicative of an immature erythroid phenotype, such as the expression of both CD71 and TER119 and the retention of intact nuclei, and express genes encoding immune checkpoint molecules. Nucleated erythroid cells with similar properties are present in mouse and human tumor tissues. Antibody-mediated erythropoietin blockade reduces tumor-responsive erythroid cell induction and tumor growth. These findings reveal the potential of tumor-induced erythropoietin and erythroid cells as targets for cancer treatment.

Implications : Our study identifies erythropoietin and erythroid cells as novel players in tumor–host interactions and highlights the involvement of multiorgan signaling events in their induction in response to environmental stress and tumor growth.

This article is featured in Highlights of This Issue, p. 359

Footnotes

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

  • Mol Cancer Res 2021;19:507–15

  • Received August 26, 2020.
  • Revision received October 7, 2020.
  • Accepted November 20, 2020.
  • Published first November 24, 2020.
  • ©2020 American Association for Cancer Research.
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Molecular Cancer Research: 19 (3)
March 2021
Volume 19, Issue 3
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Multiorgan Signaling Mobilizes Tumor-Associated Erythroid Cells Expressing Immune Checkpoint Molecules
Yasuyo Sano, Toshimi Yoshida, Min-Kyung Choo, Yanek Jiménez-Andrade, Kathryn R. Hill, Katia Georgopoulos and Jin Mo Park
Mol Cancer Res March 1 2021 (19) (3) 507-515; DOI: 10.1158/1541-7786.MCR-20-0746

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Multiorgan Signaling Mobilizes Tumor-Associated Erythroid Cells Expressing Immune Checkpoint Molecules
Yasuyo Sano, Toshimi Yoshida, Min-Kyung Choo, Yanek Jiménez-Andrade, Kathryn R. Hill, Katia Georgopoulos and Jin Mo Park
Mol Cancer Res March 1 2021 (19) (3) 507-515; DOI: 10.1158/1541-7786.MCR-20-0746
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