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Cancer Immunology Research

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Research Articles

Mirc11 Disrupts Inflammatory but Not Cytotoxic Responses of NK Cells

Arash Nanbakhsh, Anupallavi Srinivasamani, Sandra Holzhauer, Matthew J. Riese, Yongwei Zheng, Demin Wang, Robert Burns, Michael H. Reimer, Sridhar Rao, Angela Lemke, Shirng-Wern Tsaih, Michael J. Flister, Shunhua Lao, Richard Dahl, Monica S. Thakar and Subramaniam Malarkannan
Arash Nanbakhsh
Laboratory of Molecular Immunology and Immunotherapy, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.
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Anupallavi Srinivasamani
Laboratory of Molecular Immunology and Immunotherapy, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.
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Sandra Holzhauer
Laboratory of Lymphocyte Signaling, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.
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Matthew J. Riese
Laboratory of Lymphocyte Signaling, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin.Department of Microbiology and Immunology, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Yongwei Zheng
Laboratory of B Cell Biology, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.
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Demin Wang
Department of Microbiology and Immunology, Medical College of Wisconsin, Milwaukee, Wisconsin.Laboratory of B Cell Biology, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.
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Robert Burns
Bioinformatics Core, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.
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Michael H. Reimer
Laboratory of Stem Cell Biology, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.Department of Cell Biology, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Sridhar Rao
Laboratory of Stem Cell Biology, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.Department of Cell Biology, Medical College of Wisconsin, Milwaukee, Wisconsin.
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  • ORCID record for Sridhar Rao
Angela Lemke
Genome Sciences and Precision Medicine Center, Medical College of Wisconsin, Milwaukee, Wisconsin.Department of Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Shirng-Wern Tsaih
Genome Sciences and Precision Medicine Center, Medical College of Wisconsin, Milwaukee, Wisconsin.Department of Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Michael J. Flister
Genome Sciences and Precision Medicine Center, Medical College of Wisconsin, Milwaukee, Wisconsin.Department of Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Shunhua Lao
Laboratory of Molecular Immunology and Immunotherapy, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.Department of Pediatrics, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Richard Dahl
Indiana University School of Medicine, South Bend, Indiana.
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Monica S. Thakar
Laboratory of Molecular Immunology and Immunotherapy, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.Department of Pediatrics, Medical College of Wisconsin, Milwaukee, Wisconsin.
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Subramaniam Malarkannan
Laboratory of Molecular Immunology and Immunotherapy, Blood Research Institute, BloodCenter of Wisconsin, Milwaukee, Wisconsin.Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin.Department of Microbiology and Immunology, Medical College of Wisconsin, Milwaukee, Wisconsin.Genome Sciences and Precision Medicine Center, Medical College of Wisconsin, Milwaukee, Wisconsin.Department of Pediatrics, Medical College of Wisconsin, Milwaukee, Wisconsin.
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  • For correspondence: Subra.malar@bcw.edu
DOI: 10.1158/2326-6066.CIR-18-0934 Published October 2019
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Abstract

Natural killer (NK) cells generate proinflammatory cytokines that are required to contain infections and tumor growth. However, the posttranscriptional mechanisms that regulate NK cell functions are not fully understood. Here, we define the role of the microRNA cluster known as Mirc11 (which includes miRNA-23a, miRNA-24a, and miRNA-27a) in NK cell–mediated proinflammatory responses. Absence of Mirc11 did not alter the development or the antitumor cytotoxicity of NK cells. However, loss of Mirc11 reduced generation of proinflammatory factors in vitro and interferon-γ–dependent clearance of Listeria monocytogenes or B16F10 melanoma in vivo by NK cells. These functional changes resulted from Mirc11 silencing ubiquitin modifiers A20, Cbl-b, and Itch, allowing TRAF6-dependent activation of NF-κB and AP-1. Lack of Mirc11 caused increased translation of A20, Cbl-b, and Itch proteins, resulting in deubiquitylation of scaffolding K63 and addition of degradative K48 moieties on TRAF6. Collectively, our results describe a function of Mirc11 that regulates generation of proinflammatory cytokines from effector lymphocytes.

Footnotes

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

  • Cancer Immunol Res 2019;7:1647–62

  • Received January 24, 2019.
  • Revision received April 14, 2019.
  • Accepted August 12, 2019.
  • Published first September 12, 2019.
  • ©2019 American Association for Cancer Research.
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Cancer Immunology Research: 7 (10)
October 2019
Volume 7, Issue 10
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Mirc11 Disrupts Inflammatory but Not Cytotoxic Responses of NK Cells
Arash Nanbakhsh, Anupallavi Srinivasamani, Sandra Holzhauer, Matthew J. Riese, Yongwei Zheng, Demin Wang, Robert Burns, Michael H. Reimer, Sridhar Rao, Angela Lemke, Shirng-Wern Tsaih, Michael J. Flister, Shunhua Lao, Richard Dahl, Monica S. Thakar and Subramaniam Malarkannan
Cancer Immunol Res October 1 2019 (7) (10) 1647-1662; DOI: 10.1158/2326-6066.CIR-18-0934

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Mirc11 Disrupts Inflammatory but Not Cytotoxic Responses of NK Cells
Arash Nanbakhsh, Anupallavi Srinivasamani, Sandra Holzhauer, Matthew J. Riese, Yongwei Zheng, Demin Wang, Robert Burns, Michael H. Reimer, Sridhar Rao, Angela Lemke, Shirng-Wern Tsaih, Michael J. Flister, Shunhua Lao, Richard Dahl, Monica S. Thakar and Subramaniam Malarkannan
Cancer Immunol Res October 1 2019 (7) (10) 1647-1662; DOI: 10.1158/2326-6066.CIR-18-0934
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