Natural variation in gene expression and viral susceptibility revealed by neural progenitor cell villages
Human genome variation contributes to diversity in neurodevelopmental outcomes and vulnerabilities; recognizing the underlying molecular and cellular mechanisms will require scalable approaches. Here, we describe a “cell village” experimental platform we used to analyze genetic, molecular, and pheno...
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| Published in | Cell stem cell Vol. 30; no. 3; pp. 312 - 332.e13 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
02.03.2023
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1934-5909 1875-9777 1875-9777 |
| DOI | 10.1016/j.stem.2023.01.010 |
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| Abstract | Human genome variation contributes to diversity in neurodevelopmental outcomes and vulnerabilities; recognizing the underlying molecular and cellular mechanisms will require scalable approaches. Here, we describe a “cell village” experimental platform we used to analyze genetic, molecular, and phenotypic heterogeneity across neural progenitor cells from 44 human donors cultured in a shared in vitro environment using algorithms (Dropulation and Census-seq) to assign cells and phenotypes to individual donors. Through rapid induction of human stem cell-derived neural progenitor cells, measurements of natural genetic variation, and CRISPR-Cas9 genetic perturbations, we identified a common variant that regulates antiviral IFITM3 expression and explains most inter-individual variation in susceptibility to the Zika virus. We also detected expression QTLs corresponding to GWAS loci for brain traits and discovered novel disease-relevant regulators of progenitor proliferation and differentiation such as CACHD1. This approach provides scalable ways to elucidate the effects of genes and genetic variation on cellular phenotypes.
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•Brief overexpression of NGN2 converts human stem cells to functional NPCs•Molecular and cellular phenotypes are measured in hPSC-derived NPC “villages”•An IFITM3 SNP explains most inter-donor variation in NPC viral susceptibility•CACHD1 is a novel regulator of neurogenesis
Wells et al. describe an experimental platform that pools rapidly generated neural progenitor cells from multiple human donors into the same culture flask to detect the genetic factors associated with molecular phenotypes and to identify an IFITM3 single nucleotide polymorphism that explains a sizable proportion of inter-donor variation in Zika virus vulnerability. |
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| AbstractList | Human genome variation contributes to diversity in neurodevelopmental outcomes and vulnerabilities; recognizing the underlying molecular and cellular mechanisms will require scalable approaches. Here, we describe a "cell village" experimental platform we used to analyze genetic, molecular, and phenotypic heterogeneity across neural progenitor cells from 44 human donors cultured in a shared in vitro environment using algorithms (Dropulation and Census-seq) to assign cells and phenotypes to individual donors. Through rapid induction of human stem cell-derived neural progenitor cells, measurements of natural genetic variation, and CRISPR-Cas9 genetic perturbations, we identified a common variant that regulates antiviral IFITM3 expression and explains most inter-individual variation in susceptibility to the Zika virus. We also detected expression QTLs corresponding to GWAS loci for brain traits and discovered novel disease-relevant regulators of progenitor proliferation and differentiation such as CACHD1. This approach provides scalable ways to elucidate the effects of genes and genetic variation on cellular phenotypes.Human genome variation contributes to diversity in neurodevelopmental outcomes and vulnerabilities; recognizing the underlying molecular and cellular mechanisms will require scalable approaches. Here, we describe a "cell village" experimental platform we used to analyze genetic, molecular, and phenotypic heterogeneity across neural progenitor cells from 44 human donors cultured in a shared in vitro environment using algorithms (Dropulation and Census-seq) to assign cells and phenotypes to individual donors. Through rapid induction of human stem cell-derived neural progenitor cells, measurements of natural genetic variation, and CRISPR-Cas9 genetic perturbations, we identified a common variant that regulates antiviral IFITM3 expression and explains most inter-individual variation in susceptibility to the Zika virus. We also detected expression QTLs corresponding to GWAS loci for brain traits and discovered novel disease-relevant regulators of progenitor proliferation and differentiation such as CACHD1. This approach provides scalable ways to elucidate the effects of genes and genetic variation on cellular phenotypes. Human genome variation contributes to diversity in neurodevelopmental outcomes and vulnerabilities; recognizing the underlying molecular and cellular mechanisms will require scalable approaches. Here, we describe a "cell village" experimental platform we used to analyze genetic, molecular, and phenotypic heterogeneity across neural progenitor cells from 44 human donors cultured in a shared in vitro environment using algorithms (Dropulation and Census-seq) to assign cells and phenotypes to individual donors. Through rapid induction of human stem cell-derived neural progenitor cells, measurements of natural genetic variation, and CRISPR-Cas9 genetic perturbations, we identified a common variant that regulates antiviral IFITM3 expression and explains most inter-individual variation in susceptibility to the Zika virus. We also detected expression QTLs corresponding to GWAS loci for brain traits and discovered novel disease-relevant regulators of progenitor proliferation and differentiation such as CACHD1. This approach provides scalable ways to elucidate the effects of genes and genetic variation on cellular phenotypes. Human genome variation contributes to diversity in neurodevelopmental outcomes and vulnerabilities; recognizing the underlying molecular and cellular mechanisms will require scalable approaches. Here, we describe a “cell village” experimental platform we used to analyze genetic, molecular, and phenotypic heterogeneity across neural progenitor cells from 44 human donors cultured in a shared in vitro environment using algorithms (Dropulation and Census-seq) to assign cells and phenotypes to individual donors. Through rapid induction of human stem cell-derived neural progenitor cells, measurements of natural genetic variation, and CRISPR-Cas9 genetic perturbations, we identified a common variant that regulates antiviral IFITM3 expression and explains most inter-individual variation in susceptibility to the Zika virus. We also detected expression QTLs corresponding to GWAS loci for brain traits and discovered novel disease-relevant regulators of progenitor proliferation and differentiation such as CACHD1. This approach provides scalable ways to elucidate the effects of genes and genetic variation on cellular phenotypes. [Display omitted] •Brief overexpression of NGN2 converts human stem cells to functional NPCs•Molecular and cellular phenotypes are measured in hPSC-derived NPC “villages”•An IFITM3 SNP explains most inter-donor variation in NPC viral susceptibility•CACHD1 is a novel regulator of neurogenesis Wells et al. describe an experimental platform that pools rapidly generated neural progenitor cells from multiple human donors into the same culture flask to detect the genetic factors associated with molecular phenotypes and to identify an IFITM3 single nucleotide polymorphism that explains a sizable proportion of inter-donor variation in Zika virus vulnerability. |
| Author | Salick, Max R. Guss, Ellen J. Eggan, Kevin Raymond, Joseph J. Pietilainen, Olli Siekmann, Marco T. Nehme, Ralda Peterson, Brant K. Raghunathan, Kavya Chan, Karrie Mitchell, Jana M. Worringer, Kathleen A. Ghosh, Sulagna Neumann, Anna Mello, Curtis J. Nemesh, James Zuccaro, Emanuela Piccioni, Federica Tegtmeyer, Matthew Gold, John T. McCarroll, Steven A. Hawes, Derek Wells, Michael F. Meyer, Daniel Ho, Daniel Kommineni, Sravya Kaykas, Ajamete |
| Author_xml | – sequence: 1 givenname: Michael F. surname: Wells fullname: Wells, Michael F. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 2 givenname: James surname: Nemesh fullname: Nemesh, James organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 3 givenname: Sulagna surname: Ghosh fullname: Ghosh, Sulagna organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 4 givenname: Jana M. orcidid: 0000-0002-2113-5989 surname: Mitchell fullname: Mitchell, Jana M. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 5 givenname: Max R. surname: Salick fullname: Salick, Max R. organization: Insitro, South San Francisco, CA 94080, USA – sequence: 6 givenname: Curtis J. surname: Mello fullname: Mello, Curtis J. organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 7 givenname: Daniel surname: Meyer fullname: Meyer, Daniel organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 8 givenname: Olli surname: Pietilainen fullname: Pietilainen, Olli organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 9 givenname: Federica surname: Piccioni fullname: Piccioni, Federica organization: Genetic Perturbation Platform, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 10 givenname: Ellen J. orcidid: 0000-0002-2579-8712 surname: Guss fullname: Guss, Ellen J. organization: Department of Stem Cell and Regenerative Biology, and Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA – sequence: 11 givenname: Kavya surname: Raghunathan fullname: Raghunathan, Kavya organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 12 givenname: Matthew surname: Tegtmeyer fullname: Tegtmeyer, Matthew organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 13 givenname: Derek surname: Hawes fullname: Hawes, Derek organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 14 givenname: Anna surname: Neumann fullname: Neumann, Anna organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 15 givenname: Kathleen A. surname: Worringer fullname: Worringer, Kathleen A. organization: Department of Neuroscience, Novartis Institute for BioMedical Research, Cambridge, MA 02139, USA – sequence: 16 givenname: Daniel surname: Ho fullname: Ho, Daniel organization: Department of Neuroscience, Novartis Institute for BioMedical Research, Cambridge, MA 02139, USA – sequence: 17 givenname: Sravya surname: Kommineni fullname: Kommineni, Sravya organization: Department of Neuroscience, Novartis Institute for BioMedical Research, Cambridge, MA 02139, USA – sequence: 18 givenname: Karrie surname: Chan fullname: Chan, Karrie organization: Department of Neuroscience, Novartis Institute for BioMedical Research, Cambridge, MA 02139, USA – sequence: 19 givenname: Brant K. surname: Peterson fullname: Peterson, Brant K. organization: Department of Neuroscience, Novartis Institute for BioMedical Research, Cambridge, MA 02139, USA – sequence: 20 givenname: Joseph J. orcidid: 0000-0003-3880-6694 surname: Raymond fullname: Raymond, Joseph J. organization: Department of Neuroscience, Novartis Institute for BioMedical Research, Cambridge, MA 02139, USA – sequence: 21 givenname: John T. surname: Gold fullname: Gold, John T. organization: Department of Stem Cell and Regenerative Biology, and Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA – sequence: 22 givenname: Marco T. surname: Siekmann fullname: Siekmann, Marco T. organization: Department of Stem Cell and Regenerative Biology, and Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA – sequence: 23 givenname: Emanuela surname: Zuccaro fullname: Zuccaro, Emanuela organization: Department of Stem Cell and Regenerative Biology, and Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA – sequence: 24 givenname: Ralda orcidid: 0000-0001-7215-3311 surname: Nehme fullname: Nehme, Ralda organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 25 givenname: Ajamete surname: Kaykas fullname: Kaykas, Ajamete organization: Insitro, South San Francisco, CA 94080, USA – sequence: 26 givenname: Kevin surname: Eggan fullname: Eggan, Kevin email: kevin.eggan@bmrn.com organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA – sequence: 27 givenname: Steven A. surname: McCarroll fullname: McCarroll, Steven A. email: smccarro@broadinstitute.org organization: Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard University, Cambridge, MA 02142, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36796362$$D View this record in MEDLINE/PubMed |
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| Keywords | proliferation CRISPR-Cas9 screen CACHD1 Zika virus neural progenitor cells Neurogenin-2 neurodevelopmental disorders cell villages |
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| SubjectTerms | Brain - metabolism CACHD1 Cell Differentiation - genetics cell villages CRISPR-Cas9 screen Gene Expression Humans Membrane Proteins - metabolism neural progenitor cells Neural Stem Cells - metabolism neurodevelopmental disorders Neurogenin-2 proliferation RNA-Binding Proteins - metabolism Zika virus Zika Virus - metabolism Zika Virus Infection |
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| Title | Natural variation in gene expression and viral susceptibility revealed by neural progenitor cell villages |
| URI | https://dx.doi.org/10.1016/j.stem.2023.01.010 https://www.ncbi.nlm.nih.gov/pubmed/36796362 https://www.proquest.com/docview/2783492218 https://escholarship.org/uc/item/4r2062rd |
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