Establishing Cerebral Organoids as Models of Human-Specific Brain Evolution
Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features...
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| Published in | Cell Vol. 176; no. 4; pp. 743 - 756.e17 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
07.02.2019
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0092-8674 1097-4172 1097-4172 |
| DOI | 10.1016/j.cell.2019.01.017 |
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| Abstract | Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K-AKT-mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors upregulated specifically in human: INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution.
•Brain organoids preserve gene expression networks despite elevated metabolic stress•Chimpanzee organoids enable studies of the evolution of human brain development•Primary and organoid samples reveal 261 human-specific gene expression changes•Human radial glia exhibit increased mTOR activation compared to non-human primates
Comparisons of cerebral organoids between chimpanzees, macaques, and humans reveal gene duplications and cell-signaling alterations that explain developmental evolutionary differences that are unique to us as a species. |
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| AbstractList | Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially-expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K/AKT/mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors up-regulated specifically in human, INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution. Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K-AKT-mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors upregulated specifically in human: INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution. Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K-AKT-mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors upregulated specifically in human: INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution.Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K-AKT-mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors upregulated specifically in human: INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution. Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K-AKT-mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors upregulated specifically in human: INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution. •Brain organoids preserve gene expression networks despite elevated metabolic stress•Chimpanzee organoids enable studies of the evolution of human brain development•Primary and organoid samples reveal 261 human-specific gene expression changes•Human radial glia exhibit increased mTOR activation compared to non-human primates Comparisons of cerebral organoids between chimpanzees, macaques, and humans reveal gene duplications and cell-signaling alterations that explain developmental evolutionary differences that are unique to us as a species. Direct comparisons of human and non-human primate brains can reveal molecular pathways underlying remarkable specializations of the human brain. However, chimpanzee tissue is inaccessible during neocortical neurogenesis when differences in brain size first appear. To identify human-specific features of cortical development, we leveraged recent innovations that permit generating pluripotent stem cell-derived cerebral organoids from chimpanzee. Despite metabolic differences, organoid models preserve gene regulatory networks related to primary cell types and developmental processes. We further identified 261 differentially expressed genes in human compared to both chimpanzee organoids and macaque cortex, enriched for recent gene duplications, and including multiple regulators of PI3K-AKT-mTOR signaling. We observed increased activation of this pathway in human radial glia, dependent on two receptors upregulated specifically in human: INSR and ITGB8. Our findings establish a platform for systematic analysis of molecular changes contributing to human brain development and evolution. |
| Author | Bedolli, Melanie Fiddes, Ian T. Haussler, David West, Jay A. Pavlovic, Bryan J. Andrews, Madeline G. Mostajo-Radji, Mohammed A. Eichler, Evan E. Alvarado, Beatriz Bershteyn, Marina Kronenberg, Zev N. Kriegstein, Arnold R. Lowe, Craig B. Bhaduri, Aparna Di Lullo, Elizabeth Dougherty, Max L. Salama, Sofie R. Meyerson, Olivia S. Shuga, Joe Nowakowski, Tomasz J. Leyrat, Anne A. Pollen, Alex A. |
| AuthorAffiliation | 4. Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA 5. Genomics Institute, University of California, Santa Cruz, CA, USA 1. Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA 7. Department of Developmental Biology, Stanford University, Stanford CA, USA 3. Department of Anatomy, UCSF, San Francisco, CA, USA 6. New Technologies, Fluidigm, South San Francisco, CA, USA 2. The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, UCSF, San Francisco, CA, USA 8. Howard Hughes Medical Institute |
| AuthorAffiliation_xml | – name: 5. Genomics Institute, University of California, Santa Cruz, CA, USA – name: 7. Department of Developmental Biology, Stanford University, Stanford CA, USA – name: 8. Howard Hughes Medical Institute – name: 1. Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – name: 3. Department of Anatomy, UCSF, San Francisco, CA, USA – name: 4. Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA – name: 2. The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, UCSF, San Francisco, CA, USA – name: 6. New Technologies, Fluidigm, South San Francisco, CA, USA |
| Author_xml | – sequence: 1 givenname: Alex A. surname: Pollen fullname: Pollen, Alex A. email: alex.pollen@ucsf.edu organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 2 givenname: Aparna surname: Bhaduri fullname: Bhaduri, Aparna organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 3 givenname: Madeline G. surname: Andrews fullname: Andrews, Madeline G. organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 4 givenname: Tomasz J. surname: Nowakowski fullname: Nowakowski, Tomasz J. organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 5 givenname: Olivia S. surname: Meyerson fullname: Meyerson, Olivia S. organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 6 givenname: Mohammed A. surname: Mostajo-Radji fullname: Mostajo-Radji, Mohammed A. organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 7 givenname: Elizabeth surname: Di Lullo fullname: Di Lullo, Elizabeth organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 8 givenname: Beatriz surname: Alvarado fullname: Alvarado, Beatriz organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 9 givenname: Melanie surname: Bedolli fullname: Bedolli, Melanie organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 10 givenname: Max L. surname: Dougherty fullname: Dougherty, Max L. organization: Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA – sequence: 11 givenname: Ian T. surname: Fiddes fullname: Fiddes, Ian T. organization: Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA, USA – sequence: 12 givenname: Zev N. surname: Kronenberg fullname: Kronenberg, Zev N. organization: Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA – sequence: 13 givenname: Joe surname: Shuga fullname: Shuga, Joe organization: New Technologies, Fluidigm, South San Francisco, CA, USA – sequence: 14 givenname: Anne A. surname: Leyrat fullname: Leyrat, Anne A. organization: New Technologies, Fluidigm, South San Francisco, CA, USA – sequence: 15 givenname: Jay A. surname: West fullname: West, Jay A. organization: New Technologies, Fluidigm, South San Francisco, CA, USA – sequence: 16 givenname: Marina surname: Bershteyn fullname: Bershteyn, Marina organization: The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, UCSF, San Francisco, CA, USA – sequence: 17 givenname: Craig B. surname: Lowe fullname: Lowe, Craig B. organization: Department of Developmental Biology, Stanford University, Stanford, CA, USA – sequence: 18 givenname: Bryan J. surname: Pavlovic fullname: Pavlovic, Bryan J. organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA – sequence: 19 givenname: Sofie R. surname: Salama fullname: Salama, Sofie R. organization: Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA, USA – sequence: 20 givenname: David surname: Haussler fullname: Haussler, David organization: Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA, USA – sequence: 21 givenname: Evan E. surname: Eichler fullname: Eichler, Evan E. organization: Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA – sequence: 22 givenname: Arnold R. surname: Kriegstein fullname: Kriegstein, Arnold R. email: arnold.kriegstein@ucsf.edu organization: Department of Neurology, University of California, San Francisco (UCSF), San Francisco, CA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30735633$$D View this record in MEDLINE/PubMed |
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| Keywords | single-cell RNA sequencing cerebral organoids macaque radial glia human-specific evolution mTOR chimpanzee cortical development neural progenitor cells |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Methodology: AB, TJN, MGA, JS, AAL, JAW, CL, OSM, AAP. Investigation: AAP, AB, TJN, OSM, EDL, MAMR, BA, MaB, MeB, MGA. Resources: BP, MaB. Software: CBL, ITF. Formal analysis AB, TJN, MGA, ZNK, MLD, CBL, ITF, OSM, AAP. Writing: AAP, AB, with input from all authors. Funding acquisition ARK AAP. Conceptualization AAP. Supervision: ARK, SRS, DH, EEE, AAP. Lead contact: alex.pollen@ucsf.edu AUTHOR CONTRIBUTIONS These authors contributed equally |
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| Title | Establishing Cerebral Organoids as Models of Human-Specific Brain Evolution |
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