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

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 highl...

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Published in:	Cancer research (Chicago, Ill.) Vol. 76; no. 23; pp. 6816 - 6827
Main Authors:	Wen, Shu Wen, Sceneay, Jaclyn, Lima, Luize Goncalves, Wong, Christina S F, Becker, Melanie, Krumeich, Sophie, Lobb, Richard J, Castillo, Vanessa, Wong, Ke Ni, Ellis, Sarah, Parker, Belinda S, Möller, Andreas
Format:	Journal Article
Language:	English
Published:	United States 01-12-2016
Subjects:	Animals Breast Neoplasms - immunology Breast Neoplasms - pathology Cell Proliferation Exosomes - metabolism Female Humans Immunosuppression - methods Mice Mice, Inbred BALB C Mice, Inbred C57BL
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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); 6816-27. ©2016 AACR.
AbstractList	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); 6816–27. ©2016 AACR. 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); 6816-27. ©2016 AACR. 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); 6816-27. ©2016 AACR. This study shows how breast cancer-derived exosomes accumulate in premetastatic organs, impact immune cell character and activity, and promote metastatic spread. 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 naive 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); 6816-27. [copy2016 AACR.
Author	Sceneay, Jaclyn Parker, Belinda S Wong, Christina S F Krumeich, Sophie Wen, Shu Wen Lobb, Richard J Wong, Ke Ni Ellis, Sarah Castillo, Vanessa Lima, Luize Goncalves Möller, Andreas Becker, Melanie
Author_xml	– sequence: 1 givenname: Shu Wen surname: Wen fullname: Wen, Shu Wen organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 2 givenname: Jaclyn surname: Sceneay fullname: Sceneay, Jaclyn organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 3 givenname: Luize Goncalves surname: Lima fullname: Lima, Luize Goncalves organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 4 givenname: Christina S F surname: Wong fullname: Wong, Christina S F organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 5 givenname: Melanie surname: Becker fullname: Becker, Melanie organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 6 givenname: Sophie surname: Krumeich fullname: Krumeich, Sophie organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 7 givenname: Richard J surname: Lobb fullname: Lobb, Richard J organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 8 givenname: Vanessa surname: Castillo fullname: Castillo, Vanessa organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 9 givenname: Ke Ni surname: Wong fullname: Wong, Ke Ni organization: Tumor Microenvironment Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia – sequence: 10 givenname: Sarah surname: Ellis fullname: Ellis, Sarah organization: Peter MacCallum Cancer Centre, East Melbourne, and Sir Peter MacCallum Department of Histology, University of Melbourne, Parkville, Australia – sequence: 11 givenname: Belinda S surname: Parker fullname: Parker, Belinda S organization: Department of Biochemistry and Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria, Australia – sequence: 12 givenname: Andreas surname: Möller fullname: Möller, Andreas email: andreas.moller@qimrberghofer.edu.au organization: School of Medicine, University of Queensland, Brisbane, Queensland, Australia
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Snippet	Small membranous secretions from tumor cells, termed exosomes, contribute significantly to intercellular communication and subsequent reprogramming of the... Abstract Small membranous secretions from tumor cells, termed exosomes, contribute significantly to intercellular communication and subsequent reprogramming of... This study shows how breast cancer-derived exosomes accumulate in premetastatic organs, impact immune cell character and activity, and promote metastatic...
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StartPage	6816
SubjectTerms	Animals Breast Neoplasms - immunology Breast Neoplasms - pathology Cell Proliferation Exosomes - metabolism Female Humans Immunosuppression - methods Mice Mice, Inbred BALB C Mice, Inbred C57BL
Title	The Biodistribution and Immune Suppressive Effects of Breast Cancer-Derived Exosomes
URI	https://www.ncbi.nlm.nih.gov/pubmed/27760789 https://search.proquest.com/docview/1835504352 https://search.proquest.com/docview/1872824496
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