Gliomas Interact with Non-glioma Brain Cells via Extracellular Vesicles

Xiaofei Gao; Zhaohuan Zhang; Tomoyuki Mashimo; Bo Shen; James Nyagilo; Hao Wang; Yihui Wang; Zhida Liu; Aditi Mulgaonkar; Xiao-Ling Hu; Sara G.M. Piccirillo; Ugur Eskiocak; Digant P. Davé; Song Qin; Yongjie Yang; Xiankai Sun; Yang-Xin Fu; Hui Zong; Wenzhi Sun; Robert M. Bachoo; Woo-ping Ge

Cell Reports (Feb 2020)

Gliomas Interact with Non-glioma Brain Cells via Extracellular Vesicles

Xiaofei Gao,
Zhaohuan Zhang,
Tomoyuki Mashimo,
Bo Shen,
James Nyagilo,
Hao Wang,
Yihui Wang,
Zhida Liu,
Aditi Mulgaonkar,
Xiao-Ling Hu,
Sara G.M. Piccirillo,
Ugur Eskiocak,
Digant P. Davé,
Song Qin,
Yongjie Yang,
Xiankai Sun,
Yang-Xin Fu,
Hui Zong,
Wenzhi Sun,
Robert M. Bachoo,
Woo-ping Ge

Affiliations

Xiaofei Gao: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Zhaohuan Zhang: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Neurology, Changzheng Hospital, Second Military Medical University, Shanghai 200003, China
Tomoyuki Mashimo: Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Bo Shen: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
James Nyagilo: Department of Neurology and Neurotherapeutics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Hao Wang: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Yihui Wang: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Tongji Hospital Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 4300030, China
Zhida Liu: Department of Pathology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Aditi Mulgaonkar: Department of Radiology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Xiao-Ling Hu: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Sara G.M. Piccirillo: Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Ugur Eskiocak: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Digant P. Davé: Department of Neurology and Neurotherapeutics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Bioengineering, University of Texas, Arlington, TX 76010, USA
Song Qin: Department of Anatomy, Histology and Embryology, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China
Yongjie Yang: Department of Neuroscience, Graduate School of Biomedical Sciences, Tufts University School of Medicine, Tufts University, Boston, MA 02111, USA
Xiankai Sun: Department of Radiology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Yang-Xin Fu: Department of Pathology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Hui Zong: Department of Microbiology, Immunology, and Cancer Biology, University of Virginia, Charlottesville, VA 22908, USA
Wenzhi Sun: Chinese Institute for Brain Research, Beijing 102206, China; School of Basic Medical Sciences, Capital Medical University, Beijing 100069, China
Robert M. Bachoo: Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Neurology and Neurotherapeutics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Harold C. Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
Woo-ping Ge: Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Neurology and Neurotherapeutics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Harold C. Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Neuroscience, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Corresponding author

Journal volume & issue: Vol. 30, no. 8
pp. 2489 – 2500.e5

Abstract

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Summary: Emerging evidence suggests that crosstalk between glioma cells and the brain microenvironment may influence brain tumor growth. To date, known reciprocal interactions among these cells have been limited to the release of paracrine factors. Combining a genetic strategy with longitudinal live imaging, we find that individual gliomas communicate with distinct sets of non-glioma cells, including glial cells, neurons, and vascular cells. Transfer of genetic material is achieved mainly through extracellular vesicles (EVs), although cell fusion also plays a minor role. We further demonstrate that EV-mediated communication leads to the increase of synaptic activity in neurons. Blocking EV release causes a reduction of glioma growth in vivo. Our findings indicate that EV-mediated interaction between glioma cells and non-glioma brain cells alters the tumor microenvironment and contributes to glioma development. : Non-glioma cells form a unique tumor microenvironment and are critical for glioma progression. Gao et al. find that individual gliomas communicate with distinct sets of non-glioma cells, including glial cells, neurons, and vascular cells. Transfer of genetic material is achieved mainly through extracellular vesicles (EVs). Keywords: glioma, glia, astrocyte, interaction, extracellular vesicle, tumor microenvironment, cell fusion, neuron, exosome

Published in Cell Reports

ISSN: 2211-1247 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General)
Website: http://www.cell.com/cell-reports/home

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