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Microenvironment and Immunology

The Biodistribution and Immune Suppressive Effects of Breast Cancer–Derived Exosomes

Shu Wen Wen, Jaclyn Sceneay, Luize Goncalves Lima, Christina S.F. Wong, Melanie Becker, Sophie Krumeich, Richard J. Lobb, Vanessa Castillo, Ke Ni Wong, Sarah Ellis, Belinda S. Parker and Andreas Möller
Shu Wen Wen
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Jaclyn Sceneay
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Luize Goncalves Lima
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Christina S.F. Wong
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Melanie Becker
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Sophie Krumeich
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Richard J. Lobb
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Vanessa Castillo
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Ke Ni Wong
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
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Sarah Ellis
Peter MacCallum Cancer Centre, East Melbourne, and Sir Peter MacCallum Department of Histology, University of Melbourne, Parkville, Australia.
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Belinda S. Parker
Department of Biochemistry and Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria, Australia.
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Andreas Möller
Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.School of Medicine, University of Queensland, Brisbane, Queensland, Australia.
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  • For correspondence: andreas.moller@qimrberghofer.edu.au
DOI: 10.1158/0008-5472.CAN-16-0868
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Abstract

Small membranous secretions from tumor cells, termed exosomes, contribute significantly to intercellular communication and subsequent reprogramming of the tumor microenvironment. Here, we use optical imaging to determine that exogenously administered fluorescently labeled exosomes derived from highly metastatic murine breast cancer cells distributed predominantly to the lung of syngeneic mice, a frequent site of breast cancer metastasis. At the sites of accumulation, exosomes were taken up by CD45+ bone marrow–derived cells. Subsequent long-term conditioning of naïve mice with exosomes from highly metastatic breast cancer cells revealed the accumulation of myeloid-derived suppressor cells in the lung and liver. This favorable immune suppressive microenvironment was capable of promoting metastatic colonization in the lung and liver, an effect not observed from exosomes derived from nonmetastatic cells and liposome control vesicles. Furthermore, we determined that breast cancer exosomes directly suppressed T-cell proliferation and inhibited NK cell cytotoxicity, and hence likely suppressed the anticancer immune response in premetastatic organs. Together, our findings provide novel insight into the tissue-specific outcomes of breast cancer–derived exosome accumulation and their contribution to immune suppression and promotion of metastases. Cancer Res; 76(23); 1–12. ©2016 AACR.

Footnotes

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

  • Received March 30, 2016.
  • Revision received September 9, 2016.
  • Accepted September 26, 2016.
  • ©2016 American Association for Cancer Research.
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Published OnlineFirst November 18, 2016
doi: 10.1158/0008-5472.CAN-16-0868

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The Biodistribution and Immune Suppressive Effects of Breast Cancer–Derived Exosomes
Shu Wen Wen, Jaclyn Sceneay, Luize Goncalves Lima, Christina S.F. Wong, Melanie Becker, Sophie Krumeich, Richard J. Lobb, Vanessa Castillo, Ke Ni Wong, Sarah Ellis, Belinda S. Parker and Andreas Möller
Cancer Res November 18 2016 DOI: 10.1158/0008-5472.CAN-16-0868

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The Biodistribution and Immune Suppressive Effects of Breast Cancer–Derived Exosomes
Shu Wen Wen, Jaclyn Sceneay, Luize Goncalves Lima, Christina S.F. Wong, Melanie Becker, Sophie Krumeich, Richard J. Lobb, Vanessa Castillo, Ke Ni Wong, Sarah Ellis, Belinda S. Parker and Andreas Möller
Cancer Res November 18 2016 DOI: 10.1158/0008-5472.CAN-16-0868
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Cancer Research Online ISSN: 1538-7445
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