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Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions

Brain tumors are dynamic complex ecosystems with multiple cell types. To model the brain tumor microenvironment in a reproducible and scalable system, we developed a rapid three-dimensional (3D) bioprinting method to construct clinically relevant biomimetic tissue models. In recurrent glioblastoma,...

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Autores principales: Tang, Min, Xie, Qi, Gimple, Ryan C., Zhong, Zheng, Tam, Trevor, Tian, Jing, Kidwell, Reilly L., Wu, Qiulian, Prager, Briana C., Qiu, Zhixin, Yu, Aaron, Zhu, Zhe, Mesci, Pinar, Jing, Hui, Schimelman, Jacob, Wang, Pengrui, Lee, Derrick, Lorenzini, Michael H., Dixit, Deobrat, Zhao, Linjie, Bhargava, Shruti, Miller, Tyler E., Wan, Xueyi, Tang, Jing, Sun, Bingjie, Cravatt, Benjamin F., Muotri, Alysson R., Chen, Shaochen, Rich, Jeremy N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Singapore 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7608409/
https://www.ncbi.nlm.nih.gov/pubmed/32499560
http://dx.doi.org/10.1038/s41422-020-0338-1
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author Tang, Min
Xie, Qi
Gimple, Ryan C.
Zhong, Zheng
Tam, Trevor
Tian, Jing
Kidwell, Reilly L.
Wu, Qiulian
Prager, Briana C.
Qiu, Zhixin
Yu, Aaron
Zhu, Zhe
Mesci, Pinar
Jing, Hui
Schimelman, Jacob
Wang, Pengrui
Lee, Derrick
Lorenzini, Michael H.
Dixit, Deobrat
Zhao, Linjie
Bhargava, Shruti
Miller, Tyler E.
Wan, Xueyi
Tang, Jing
Sun, Bingjie
Cravatt, Benjamin F.
Muotri, Alysson R.
Chen, Shaochen
Rich, Jeremy N.
author_facet Tang, Min
Xie, Qi
Gimple, Ryan C.
Zhong, Zheng
Tam, Trevor
Tian, Jing
Kidwell, Reilly L.
Wu, Qiulian
Prager, Briana C.
Qiu, Zhixin
Yu, Aaron
Zhu, Zhe
Mesci, Pinar
Jing, Hui
Schimelman, Jacob
Wang, Pengrui
Lee, Derrick
Lorenzini, Michael H.
Dixit, Deobrat
Zhao, Linjie
Bhargava, Shruti
Miller, Tyler E.
Wan, Xueyi
Tang, Jing
Sun, Bingjie
Cravatt, Benjamin F.
Muotri, Alysson R.
Chen, Shaochen
Rich, Jeremy N.
author_sort Tang, Min
collection PubMed
description Brain tumors are dynamic complex ecosystems with multiple cell types. To model the brain tumor microenvironment in a reproducible and scalable system, we developed a rapid three-dimensional (3D) bioprinting method to construct clinically relevant biomimetic tissue models. In recurrent glioblastoma, macrophages/microglia prominently contribute to the tumor mass. To parse the function of macrophages in 3D, we compared the growth of glioblastoma stem cells (GSCs) alone or with astrocytes and neural precursor cells in a hyaluronic acid-rich hydrogel, with or without macrophage. Bioprinted constructs integrating macrophage recapitulate patient-derived transcriptional profiles predictive of patient survival, maintenance of stemness, invasion, and drug resistance. Whole-genome CRISPR screening with bioprinted complex systems identified unique molecular dependencies in GSCs, relative to sphere culture. Multicellular bioprinted models serve as a scalable and physiologic platform to interrogate drug sensitivity, cellular crosstalk, invasion, context-specific functional dependencies, as well as immunologic interactions in a species-matched neural environment.
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spelling pubmed-76084092020-11-05 Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions Tang, Min Xie, Qi Gimple, Ryan C. Zhong, Zheng Tam, Trevor Tian, Jing Kidwell, Reilly L. Wu, Qiulian Prager, Briana C. Qiu, Zhixin Yu, Aaron Zhu, Zhe Mesci, Pinar Jing, Hui Schimelman, Jacob Wang, Pengrui Lee, Derrick Lorenzini, Michael H. Dixit, Deobrat Zhao, Linjie Bhargava, Shruti Miller, Tyler E. Wan, Xueyi Tang, Jing Sun, Bingjie Cravatt, Benjamin F. Muotri, Alysson R. Chen, Shaochen Rich, Jeremy N. Cell Res Article Brain tumors are dynamic complex ecosystems with multiple cell types. To model the brain tumor microenvironment in a reproducible and scalable system, we developed a rapid three-dimensional (3D) bioprinting method to construct clinically relevant biomimetic tissue models. In recurrent glioblastoma, macrophages/microglia prominently contribute to the tumor mass. To parse the function of macrophages in 3D, we compared the growth of glioblastoma stem cells (GSCs) alone or with astrocytes and neural precursor cells in a hyaluronic acid-rich hydrogel, with or without macrophage. Bioprinted constructs integrating macrophage recapitulate patient-derived transcriptional profiles predictive of patient survival, maintenance of stemness, invasion, and drug resistance. Whole-genome CRISPR screening with bioprinted complex systems identified unique molecular dependencies in GSCs, relative to sphere culture. Multicellular bioprinted models serve as a scalable and physiologic platform to interrogate drug sensitivity, cellular crosstalk, invasion, context-specific functional dependencies, as well as immunologic interactions in a species-matched neural environment. Springer Singapore 2020-06-04 2020-10 /pmc/articles/PMC7608409/ /pubmed/32499560 http://dx.doi.org/10.1038/s41422-020-0338-1 Text en © Center for Excellence in Molecular Cell Science, CAS 2020 https://smart.servier.com/This work was supported by grants provided by the National Institutes of Health: CA217065 (R.C.G); CA217066 (B.C.P.); DK099810 and DK114785 (B.F.C); CA197718, CA154130, CA169117, CA171652, CA238662, NS087913, NS089272, NS103434 (J.N.R); CA243296 (D.L.); R01EB021857, R21AR074763, R33HD090662 (S.C.), and the National Science Foundation: 1644967, 1937653 (S.C.). H.J. is a Biogen fellow of the Life Sciences Research Foundation. A.R.M. is supported by the California Institute for Regenerative Medicine (DISC2-09649) and by the National Institutes of Health (MH107367, N5105969). We thank the UCSD School of Medicine Microscopy Core, which is supported by a NINDS P30 grant (NS047101), for use of their confocal microscopes. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE-1650112 (J.S.). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. Portions of individual panels were prepared in part using images from Servier Medical Art by Servier (https://smart.servier.com/), which is licenced under a Creative Commons Attribution 3.0 Unported License (https://creativecommons.org/licenses/by/3.0/).
spellingShingle Article
Tang, Min
Xie, Qi
Gimple, Ryan C.
Zhong, Zheng
Tam, Trevor
Tian, Jing
Kidwell, Reilly L.
Wu, Qiulian
Prager, Briana C.
Qiu, Zhixin
Yu, Aaron
Zhu, Zhe
Mesci, Pinar
Jing, Hui
Schimelman, Jacob
Wang, Pengrui
Lee, Derrick
Lorenzini, Michael H.
Dixit, Deobrat
Zhao, Linjie
Bhargava, Shruti
Miller, Tyler E.
Wan, Xueyi
Tang, Jing
Sun, Bingjie
Cravatt, Benjamin F.
Muotri, Alysson R.
Chen, Shaochen
Rich, Jeremy N.
Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
title Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
title_full Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
title_fullStr Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
title_full_unstemmed Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
title_short Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
title_sort three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7608409/
https://www.ncbi.nlm.nih.gov/pubmed/32499560
http://dx.doi.org/10.1038/s41422-020-0338-1
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