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Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex

View ORCID ProfileKristen R. Maynard, View ORCID ProfileLeonardo Collado-Torres, View ORCID ProfileLukas M. Weber, View ORCID ProfileCedric Uytingco, View ORCID ProfileBrianna K. Barry, Stephen R. Williams, View ORCID ProfileJoseph L. Catallini, View ORCID ProfileMatthew N. Tran, View ORCID ProfileZachary Besich, View ORCID ProfileMadhavi Tippani, Jennifer Chew, Yifeng Yin, Joel E. Kleinman, View ORCID ProfileThomas M. Hyde, Nikhil Rao, View ORCID ProfileStephanie C. Hicks, View ORCID ProfileKeri Martinowich, View ORCID ProfileAndrew E. Jaffe
doi: https://doi.org/10.1101/2020.02.28.969931
Kristen R. Maynard
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
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  • ORCID record for Kristen R. Maynard
Leonardo Collado-Torres
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
2Center for Computational Biology, Johns Hopkins University, Baltimore, MD, 21205, USA
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  • ORCID record for Leonardo Collado-Torres
Lukas M. Weber
3Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
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  • ORCID record for Lukas M. Weber
Cedric Uytingco
410x Genomics, Pleasanton, CA, 94588, USA
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Brianna K. Barry
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
5Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
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Stephen R. Williams
410x Genomics, Pleasanton, CA, 94588, USA
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Joseph L. Catallini
3Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
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  • ORCID record for Joseph L. Catallini
Matthew N. Tran
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
6Department of Genetic Medicine, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA
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  • ORCID record for Matthew N. Tran
Zachary Besich
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
6Department of Genetic Medicine, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA
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Madhavi Tippani
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
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  • ORCID record for Madhavi Tippani
Jennifer Chew
410x Genomics, Pleasanton, CA, 94588, USA
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Yifeng Yin
410x Genomics, Pleasanton, CA, 94588, USA
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Joel E. Kleinman
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
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Thomas M. Hyde
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
8Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
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Nikhil Rao
410x Genomics, Pleasanton, CA, 94588, USA
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Stephanie C. Hicks
3Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
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  • ORCID record for Stephanie C. Hicks
Keri Martinowich
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
5Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
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  • For correspondence: andrew.jaffe@libd.org
Andrew E. Jaffe
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
2Center for Computational Biology, Johns Hopkins University, Baltimore, MD, 21205, USA
3Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
5Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
6Department of Genetic Medicine, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
9Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
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  • ORCID record for Andrew E. Jaffe
  • For correspondence: andrew.jaffe@libd.org
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Abstract

We used the 10x Genomics Visium platform to define the spatial topography of gene expression in the six-layered human dorsolateral prefrontal cortex (DLPFC). We identified extensive layer-enriched expression signatures, and refined associations to previous laminar markers. We overlaid our laminar expression signatures onto large-scale single nuclei RNA sequencing data, enhancing spatial annotation of expression-driven clusters. By integrating neuropsychiatric disorder gene sets, we showed differential layer-enriched expression of genes associated with schizophrenia and autism spectrum disorder, highlighting the clinical relevance of spatially-defined expression. We then developed a data-driven framework to define unsupervised clusters in spatial transcriptomics data, which can be applied to other tissues or brain regions where morphological architecture is not as well-defined as cortical laminae. We lastly created a web application for the scientific community to explore these raw and summarized data to augment ongoing neuroscience and spatial transcriptomics research (http://research.libd.org/spatialLIBD).

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  • http://research.libd.org/spatialLIBD

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Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex
Kristen R. Maynard, Leonardo Collado-Torres, Lukas M. Weber, Cedric Uytingco, Brianna K. Barry, Stephen R. Williams, Joseph L. Catallini, Matthew N. Tran, Zachary Besich, Madhavi Tippani, Jennifer Chew, Yifeng Yin, Joel E. Kleinman, Thomas M. Hyde, Nikhil Rao, Stephanie C. Hicks, Keri Martinowich, Andrew E. Jaffe
bioRxiv 2020.02.28.969931; doi: https://doi.org/10.1101/2020.02.28.969931
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Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex
Kristen R. Maynard, Leonardo Collado-Torres, Lukas M. Weber, Cedric Uytingco, Brianna K. Barry, Stephen R. Williams, Joseph L. Catallini, Matthew N. Tran, Zachary Besich, Madhavi Tippani, Jennifer Chew, Yifeng Yin, Joel E. Kleinman, Thomas M. Hyde, Nikhil Rao, Stephanie C. Hicks, Keri Martinowich, Andrew E. Jaffe
bioRxiv 2020.02.28.969931; doi: https://doi.org/10.1101/2020.02.28.969931

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