Tumor-Expressed IDO Recruits and Activates MDSCs in a Treg-Dependent Manner

Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood. Here, we find that expression of IDO by tumor cells results in aggressive tumor growth and resistance to T-cell-targeting immunotherapies. We...

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Vydáno v:Cell reports (Cambridge) Ročník 13; číslo 2; s. 412 - 424
Hlavní autoři: Holmgaard, Rikke B., Zamarin, Dmitriy, Li, Yanyun, Gasmi, Billel, Munn, David H., Allison, James P., Merghoub, Taha, Wolchok, Jedd D.
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Elsevier Inc 13.10.2015
Elsevier
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ISSN:2211-1247, 2211-1247
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Abstract Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood. Here, we find that expression of IDO by tumor cells results in aggressive tumor growth and resistance to T-cell-targeting immunotherapies. We demonstrate that IDO orchestrates local and systemic immunosuppressive effects through recruitment and activation of myeloid-derived suppressor cells (MDSCs), through a mechanism dependent on regulatory T cells (Tregs). Supporting these findings, we find that IDO expression in human melanoma tumors is strongly associated with MDSC infiltration. Treatment with a selective IDO inhibitor in vivo reversed tumor-associated immunosuppression by decreasing numbers of tumor-infiltrating MDSCs and Tregs and abolishing their suppressive function. These findings establish an important link between IDO and multiple immunosuppressive mechanisms active in the tumor microenvironment, providing a strong rationale for therapeutic targeting of IDO as one of the central regulators of immune suppression. [Display omitted] •Tumor IDO mediates local/systemic immunosuppression and resistance to immunotherapy•IDO expression in human and mouse tumors is associated with MDSC infiltration•Tumor IDO induces immunosuppression by expanding, recruiting, and activating MDSCs•Tumor-IDO-mediated recruitment and activation of MDSCs are Treg dependent IDO mediates immune inhibition in tumors, though the mechanisms of this are poorly understood. Holmgaard et al. demonstrate that tumor IDO is a central regulator of both local and systemic immunosuppression and resistance to immunotherapy, which is orchestrated through expansion, recruitment, and activation of MDSCs in a Treg-dependent manner.
AbstractList Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood. Here, we find that expression of IDO by tumor cells results in aggressive tumor growth and resistance to T-cell targeting immunotherapies. We demonstrate that IDO orchestrates local and systemic immunosuppressive effects through recruitment and activation of myeloid-derived suppressor cells (MDSCs), through a mechanism dependent on regulatory T cells (Tregs). Supporting these findings, we find that IDO expression in human melanoma tumors is strongly associated with MDSC infiltration. Treatment with a selective IDO inhibitor in vivo reversed tumor-associated immunosuppression by decreasing numbers of tumor-infiltrating MDSCs and Tregs, and abolishing their suppressive function. These findings establish an important link between IDO and multiple immunosuppressive mechanisms active in the tumor microenvironment, providing a strong rationale for therapeutic targeting IDO as one of the central regulators of immune suppression. IDO mediates immune inhibition in tumors, though the mechanisms of this are poorly understood. Holmgaard et al. demonstrate that tumor IDO is a central regulator of both local and systemic immunosuppression and resistance to immunotherapy, which is orchestrated through expansion, recruitment, and activation of MDSCs in a Treg-dependent manner.
Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood. Here, we find that expression of IDO by tumor cells results in aggressive tumor growth and resistance to T-cell-targeting immunotherapies. We demonstrate that IDO orchestrates local and systemic immunosuppressive effects through recruitment and activation of myeloid-derived suppressor cells (MDSCs), through a mechanism dependent on regulatory T cells (Tregs). Supporting these findings, we find that IDO expression in human melanoma tumors is strongly associated with MDSC infiltration. Treatment with a selective IDO inhibitor in vivo reversed tumor-associated immunosuppression by decreasing numbers of tumor-infiltrating MDSCs and Tregs and abolishing their suppressive function. These findings establish an important link between IDO and multiple immunosuppressive mechanisms active in the tumor microenvironment, providing a strong rationale for therapeutic targeting of IDO as one of the central regulators of immune suppression.
Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood. Here, we find that expression of IDO by tumor cells results in aggressive tumor growth and resistance to T-cell-targeting immunotherapies. We demonstrate that IDO orchestrates local and systemic immunosuppressive effects through recruitment and activation of myeloid-derived suppressor cells (MDSCs), through a mechanism dependent on regulatory T cells (Tregs). Supporting these findings, we find that IDO expression in human melanoma tumors is strongly associated with MDSC infiltration. Treatment with a selective IDO inhibitor in vivo reversed tumor-associated immunosuppression by decreasing numbers of tumor-infiltrating MDSCs and Tregs and abolishing their suppressive function. These findings establish an important link between IDO and multiple immunosuppressive mechanisms active in the tumor microenvironment, providing a strong rationale for therapeutic targeting of IDO as one of the central regulators of immune suppression.
Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood. Here, we find that expression of IDO by tumor cells results in aggressive tumor growth and resistance to T-cell-targeting immunotherapies. We demonstrate that IDO orchestrates local and systemic immunosuppressive effects through recruitment and activation of myeloid-derived suppressor cells (MDSCs), through a mechanism dependent on regulatory T cells (Tregs). Supporting these findings, we find that IDO expression in human melanoma tumors is strongly associated with MDSC infiltration. Treatment with a selective IDO inhibitor in vivo reversed tumor-associated immunosuppression by decreasing numbers of tumor-infiltrating MDSCs and Tregs and abolishing their suppressive function. These findings establish an important link between IDO and multiple immunosuppressive mechanisms active in the tumor microenvironment, providing a strong rationale for therapeutic targeting of IDO as one of the central regulators of immune suppression. [Display omitted] •Tumor IDO mediates local/systemic immunosuppression and resistance to immunotherapy•IDO expression in human and mouse tumors is associated with MDSC infiltration•Tumor IDO induces immunosuppression by expanding, recruiting, and activating MDSCs•Tumor-IDO-mediated recruitment and activation of MDSCs are Treg dependent IDO mediates immune inhibition in tumors, though the mechanisms of this are poorly understood. Holmgaard et al. demonstrate that tumor IDO is a central regulator of both local and systemic immunosuppression and resistance to immunotherapy, which is orchestrated through expansion, recruitment, and activation of MDSCs in a Treg-dependent manner.
Author Munn, David H.
Holmgaard, Rikke B.
Li, Yanyun
Gasmi, Billel
Allison, James P.
Zamarin, Dmitriy
Merghoub, Taha
Wolchok, Jedd D.
AuthorAffiliation 1 Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065
4 The University of Texas, MD Anderson Cancer Center, Department of Immunology, Houston, TX 77030
5 Weill Cornell Medical College and Graduate School of Medical Sciences of Cornell University, New York, NY 10065
3 Cancer Center and Department of Pediatrics, Georgia Regents University, Augusta, GA 30912
2 Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY 10065
AuthorAffiliation_xml – name: 1 Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065
– name: 2 Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY 10065
– name: 3 Cancer Center and Department of Pediatrics, Georgia Regents University, Augusta, GA 30912
– name: 5 Weill Cornell Medical College and Graduate School of Medical Sciences of Cornell University, New York, NY 10065
– name: 4 The University of Texas, MD Anderson Cancer Center, Department of Immunology, Houston, TX 77030
Author_xml – sequence: 1
  givenname: Rikke B.
  surname: Holmgaard
  fullname: Holmgaard, Rikke B.
  organization: Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
– sequence: 2
  givenname: Dmitriy
  surname: Zamarin
  fullname: Zamarin, Dmitriy
  organization: Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
– sequence: 3
  givenname: Yanyun
  surname: Li
  fullname: Li, Yanyun
  organization: Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
– sequence: 4
  givenname: Billel
  surname: Gasmi
  fullname: Gasmi, Billel
  organization: Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
– sequence: 5
  givenname: David H.
  surname: Munn
  fullname: Munn, David H.
  organization: Cancer Center and Department of Pediatrics, Georgia Regents University, Augusta, GA 30912, USA
– sequence: 6
  givenname: James P.
  surname: Allison
  fullname: Allison, James P.
  organization: Department of Immunology, The University of Texas, MD Anderson Cancer Center, Houston, TX 77030, USA
– sequence: 7
  givenname: Taha
  surname: Merghoub
  fullname: Merghoub, Taha
  organization: Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
– sequence: 8
  givenname: Jedd D.
  surname: Wolchok
  fullname: Wolchok, Jedd D.
  email: wolchokj@mskcc.org
  organization: Swim Across America/Ludwig Collaborative Laboratory, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26411680$$D View this record in MEDLINE/PubMed
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Snippet Indoleamine 2,3-dioxygenase (IDO) has been described as a major mechanism of immunosuppression in tumors, though the mechanisms of this are poorly understood....
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StartPage 412
SubjectTerms Animals
Cell Movement
Cells, Cultured
Humans
Immunosuppressive Agents - pharmacology
Indoleamine-Pyrrole 2,3,-Dioxygenase - immunology
Indoleamine-Pyrrole 2,3,-Dioxygenase - pharmacology
Mice
Myeloid Cells - drug effects
Myeloid Cells - immunology
Myeloid Cells - physiology
Neoplasms - immunology
T-Lymphocytes, Regulatory - immunology
Title Tumor-Expressed IDO Recruits and Activates MDSCs in a Treg-Dependent Manner
URI https://dx.doi.org/10.1016/j.celrep.2015.08.077
https://www.ncbi.nlm.nih.gov/pubmed/26411680
https://www.proquest.com/docview/1722924897
https://pubmed.ncbi.nlm.nih.gov/PMC5013825
https://doaj.org/article/9e2b7087f0a648589fb3425be74bd5f1
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