Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models
Summary: We present a consensus atlas of the human brain transcriptome in Alzheimer’s disease (AD), based on meta-analysis of differential gene expression in 2,114 postmortem samples. We discover 30 brain coexpression modules from seven regions as the major source of AD transcriptional perturbations...
| Published in: | Cell Reports |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Article |
| Language: | English |
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Elsevier
2020-07-01
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124720308895 |
| _version_ | 1852785074752192512 |
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| author | Ying-Wooi Wan Rami Al-Ouran Carl G. Mangleburg Thanneer M. Perumal Tom V. Lee Katherine Allison Vivek Swarup Cory C. Funk Chris Gaiteri Mariet Allen Minghui Wang Sarah M. Neuner Catherine C. Kaczorowski Vivek M. Philip Gareth R. Howell Heidi Martini-Stoica Hui Zheng Hongkang Mei Xiaoyan Zhong Jungwoo Wren Kim Valina L. Dawson Ted M. Dawson Ping-Chieh Pao Li-Huei Tsai Jean-Vianney Haure-Mirande Michelle E. Ehrlich Paramita Chakrabarty Yona Levites Xue Wang Eric B. Dammer Gyan Srivastava Sumit Mukherjee Solveig K. Sieberts Larsson Omberg Kristen D. Dang James A. Eddy Phil Snyder Yooree Chae Sandeep Amberkar Wenbin Wei Winston Hide Christoph Preuss Ayla Ergun Phillip J. Ebert David C. Airey Sara Mostafavi Lei Yu Hans-Ulrich Klein Gregory W. Carter David A. Collier Todd E. Golde Allan I. Levey David A. Bennett Karol Estrada T. Matthew Townsend Bin Zhang Eric Schadt Philip L. De Jager Nathan D. Price Nilüfer Ertekin-Taner Zhandong Liu Joshua M. Shulman Lara M. Mangravite Benjamin A. Logsdon |
| author_facet | Ying-Wooi Wan Rami Al-Ouran Carl G. Mangleburg Thanneer M. Perumal Tom V. Lee Katherine Allison Vivek Swarup Cory C. Funk Chris Gaiteri Mariet Allen Minghui Wang Sarah M. Neuner Catherine C. Kaczorowski Vivek M. Philip Gareth R. Howell Heidi Martini-Stoica Hui Zheng Hongkang Mei Xiaoyan Zhong Jungwoo Wren Kim Valina L. Dawson Ted M. Dawson Ping-Chieh Pao Li-Huei Tsai Jean-Vianney Haure-Mirande Michelle E. Ehrlich Paramita Chakrabarty Yona Levites Xue Wang Eric B. Dammer Gyan Srivastava Sumit Mukherjee Solveig K. Sieberts Larsson Omberg Kristen D. Dang James A. Eddy Phil Snyder Yooree Chae Sandeep Amberkar Wenbin Wei Winston Hide Christoph Preuss Ayla Ergun Phillip J. Ebert David C. Airey Sara Mostafavi Lei Yu Hans-Ulrich Klein Gregory W. Carter David A. Collier Todd E. Golde Allan I. Levey David A. Bennett Karol Estrada T. Matthew Townsend Bin Zhang Eric Schadt Philip L. De Jager Nathan D. Price Nilüfer Ertekin-Taner Zhandong Liu Joshua M. Shulman Lara M. Mangravite Benjamin A. Logsdon |
| author_sort | Ying-Wooi Wan |
| collection | DOAJ |
| container_title | Cell Reports |
| description | Summary: We present a consensus atlas of the human brain transcriptome in Alzheimer’s disease (AD), based on meta-analysis of differential gene expression in 2,114 postmortem samples. We discover 30 brain coexpression modules from seven regions as the major source of AD transcriptional perturbations. We next examine overlap with 251 brain differentially expressed gene sets from mouse models of AD and other neurodegenerative disorders. Human-mouse overlaps highlight responses to amyloid versus tau pathology and reveal age- and sex-dependent expression signatures for disease progression. Human coexpression modules enriched for neuronal and/or microglial genes broadly overlap with mouse models of AD, Huntington’s disease, amyotrophic lateral sclerosis, and aging. Other human coexpression modules, including those implicated in proteostasis, are not activated in AD models but rather following other, unexpected genetic manipulations. Our results comprise a cross-species resource, highlighting transcriptional networks altered by human brain pathophysiology and identifying correspondences with mouse models for AD preclinical studies. |
| format | Article |
| id | doaj-art-c0a8fce1711e4e8caa8aeb71e0b9458a |
| institution | Directory of Open Access Journals |
| issn | 2211-1247 |
| language | English |
| publishDate | 2020-07-01 |
| publisher | Elsevier |
| record_format | Article |
| spelling | doaj-art-c0a8fce1711e4e8caa8aeb71e0b9458a2025-08-19T20:46:19ZengElsevierCell Reports2211-12472020-07-0132210790810.1016/j.celrep.2020.107908Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse ModelsYing-Wooi Wan0Rami Al-Ouran1Carl G. Mangleburg2Thanneer M. Perumal3Tom V. Lee4Katherine Allison5Vivek Swarup6Cory C. Funk7Chris Gaiteri8Mariet Allen9Minghui Wang10Sarah M. Neuner11Catherine C. Kaczorowski12Vivek M. Philip13Gareth R. Howell14Heidi Martini-Stoica15Hui Zheng16Hongkang Mei17Xiaoyan Zhong18Jungwoo Wren Kim19Valina L. Dawson20Ted M. Dawson21Ping-Chieh Pao22Li-Huei Tsai23Jean-Vianney Haure-Mirande24Michelle E. Ehrlich25Paramita Chakrabarty26Yona Levites27Xue Wang28Eric B. Dammer29Gyan Srivastava30Sumit Mukherjee31Solveig K. Sieberts32Larsson Omberg33Kristen D. Dang34James A. Eddy35Phil Snyder36Yooree Chae37Sandeep Amberkar38Wenbin Wei39Winston Hide40Christoph Preuss41Ayla Ergun42Phillip J. Ebert43David C. Airey44Sara Mostafavi45Lei Yu46Hans-Ulrich Klein47Gregory W. Carter48David A. Collier49Todd E. Golde50Allan I. Levey51David A. Bennett52Karol Estrada53T. Matthew Townsend54Bin Zhang55Eric Schadt56Philip L. De Jager57Nathan D. Price58Nilüfer Ertekin-Taner59Zhandong Liu60Joshua M. Shulman61Lara M. Mangravite62Benjamin A. Logsdon63Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Jan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USAJan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USA; Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, USADepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Jan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USASage Bionetworks, Seattle, WA 98121, USAJan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USA; Department of Neurology, Baylor College of Medicine, Houston, TX 77030, USAJan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USA; Department of Neurology, Baylor College of Medicine, Houston, TX 77030, USADepartment of Neurobiology and Behavior, University of California, Irvine, CA 92697, USAInstitute for Systems Biology, Seattle, WA 98109, USARush Alzheimer’s Disease Center, Rush University Medical Center, Chicago, IL, USAMayo Clinic, Department of Neuroscience, Jacksonville, FL 32224, USADepartment of Genetics and Genomic Sciences, Mount Sinai Center for Transformative Disease Modeling, Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAThe Jackson Laboratory, Bar Harbor, ME 04609, USAThe Jackson Laboratory, Bar Harbor, ME 04609, USAThe Jackson Laboratory, Bar Harbor, ME 04609, USAThe Jackson Laboratory, Bar Harbor, ME 04609, USAHuffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USADepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USANeuroscience DPU, Shanghai R&D, GlaxoSmithKline, Shanghai, ChinaNeuroscience DPU, Shanghai R&D, GlaxoSmithKline, Shanghai, ChinaNeuroregeneration and Stem Cell Programs, Institute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Physiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USANeuroregeneration and Stem Cell Programs, Institute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Physiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Adrienne Helis Malvin & Diana Helis Henry Medical Research Foundations, New Orleans, LA 70130, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USANeuroregeneration and Stem Cell Programs, Institute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Adrienne Helis Malvin & Diana Helis Henry Medical Research Foundations, New Orleans, LA 70130, USA; Department of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USAThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA; Broad Institute of Harvard University and the Massachusetts Institute of Technology, Cambridge, MA 02139, USAThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA; Broad Institute of Harvard University and the Massachusetts Institute of Technology, Cambridge, MA 02139, USADepartments of Neurology and Pediatrics, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USADepartment of Genetics and Genomic Sciences, Mount Sinai Center for Transformative Disease Modeling, Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA; Departments of Neurology and Pediatrics, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAEvelyn F. and William L. McKnight Brain Institute, Center for Translational Research in Neurodegenerative Disease, Department of Neuroscience, University of Florida, Gainesville, FL 32610, USAEvelyn F. and William L. McKnight Brain Institute, Center for Translational Research in Neurodegenerative Disease, Department of Neuroscience, University of Florida, Gainesville, FL 32610, USAMayo Clinic, Department of Neuroscience, Jacksonville, FL 32224, USA; Mayo Clinic, Department of Health Sciences Research, Jacksonville, FL 32224, USADepartment of Biochemistry, Emory University School of Medicine, Atlanta, GA 30322, USAData & Statistical Sciences, AbbVie, Cambridge, MA, USASage Bionetworks, Seattle, WA 98121, USASage Bionetworks, Seattle, WA 98121, USASage Bionetworks, Seattle, WA 98121, USASage Bionetworks, Seattle, WA 98121, USASage Bionetworks, Seattle, WA 98121, USASage Bionetworks, Seattle, WA 98121, USASage Bionetworks, Seattle, WA 98121, USASheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, S10 2HQ, UK; Molecular Oncology Lab, Cancer Research UK – Manchester Institute, The University of Manchester, Manchester, SK10 4TG, UKSheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, S10 2HQ, UK; Department of Biosciences, Durham University, Durham, DH1 3LE, UKSheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, S10 2HQ, UK; Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, USAThe Jackson Laboratory, Bar Harbor, ME 04609, USATranslational Genome Sciences, Biogen, Cambridge, MA, USAEli Lilly & Company, Lilly Corporate Center, Indianapolis, IN 46285, USAEli Lilly & Company, Lilly Corporate Center, Indianapolis, IN 46285, USAUniversity of British Columbia, Vancouver, BC, CanadaRush Alzheimer’s Disease Center, Rush University Medical Center, Chicago, IL, USACenter for Translational & Computational Neuroimmunology, Department of Neurology and Taub Institute for the Study of Alzheimer’s Disease and the Aging Brain, Columbia University Irving Medical Center, New York, NY 10032, USA; Cell Circuits Program, Broad Institute, Cambridge, MA 02142, USAThe Jackson Laboratory, Bar Harbor, ME 04609, USAEli Lilly & Company, Erl Wood Manor, Sunninghill Road, Windlesham, Surrey, GU20 6PH, UKEvelyn F. and William L. McKnight Brain Institute, Center for Translational Research in Neurodegenerative Disease, Department of Neuroscience, University of Florida, Gainesville, FL 32610, USADepartment of Neurology, Emory University School of Medicine, Atlanta, GA 30322, USARush Alzheimer’s Disease Center, Rush University Medical Center, Chicago, IL, USATranslational Genome Sciences, Biogen, Cambridge, MA, USAFoundation Neuroscience Center, AbbVie, Cambridge, MA, USADepartment of Genetics and Genomic Sciences, Mount Sinai Center for Transformative Disease Modeling, Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USADepartment of Genetics and Genomic Sciences, Mount Sinai Center for Transformative Disease Modeling, Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USACenter for Translational & Computational Neuroimmunology, Department of Neurology and Taub Institute for the Study of Alzheimer’s Disease and the Aging Brain, Columbia University Irving Medical Center, New York, NY 10032, USA; Cell Circuits Program, Broad Institute, Cambridge, MA 02142, USAInstitute for Systems Biology, Seattle, WA 98109, USAMayo Clinic, Department of Neuroscience, Jacksonville, FL 32224, USA; Mayo Clinic, Department of Neurology, Jacksonville, FL 32224, USAJan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USA; Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, USA; Corresponding authorDepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Jan and Dan Duncan Neurologic Research Institute, Texas Children’s Hospital, Houston, TX 77030, USA; Department of Neurology, Baylor College of Medicine, Houston, TX 77030, USA; Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA; Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA; Corresponding authorSage Bionetworks, Seattle, WA 98121, USA; Corresponding authorSage Bionetworks, Seattle, WA 98121, USA; Corresponding authorSummary: We present a consensus atlas of the human brain transcriptome in Alzheimer’s disease (AD), based on meta-analysis of differential gene expression in 2,114 postmortem samples. We discover 30 brain coexpression modules from seven regions as the major source of AD transcriptional perturbations. We next examine overlap with 251 brain differentially expressed gene sets from mouse models of AD and other neurodegenerative disorders. Human-mouse overlaps highlight responses to amyloid versus tau pathology and reveal age- and sex-dependent expression signatures for disease progression. Human coexpression modules enriched for neuronal and/or microglial genes broadly overlap with mouse models of AD, Huntington’s disease, amyotrophic lateral sclerosis, and aging. Other human coexpression modules, including those implicated in proteostasis, are not activated in AD models but rather following other, unexpected genetic manipulations. Our results comprise a cross-species resource, highlighting transcriptional networks altered by human brain pathophysiology and identifying correspondences with mouse models for AD preclinical studies.http://www.sciencedirect.com/science/article/pii/S2211124720308895Alzheimer's diseasetranscriptomeRNA-seqcoexpression analysisdifferential expression analysismeta-analysis |
| spellingShingle | Ying-Wooi Wan Rami Al-Ouran Carl G. Mangleburg Thanneer M. Perumal Tom V. Lee Katherine Allison Vivek Swarup Cory C. Funk Chris Gaiteri Mariet Allen Minghui Wang Sarah M. Neuner Catherine C. Kaczorowski Vivek M. Philip Gareth R. Howell Heidi Martini-Stoica Hui Zheng Hongkang Mei Xiaoyan Zhong Jungwoo Wren Kim Valina L. Dawson Ted M. Dawson Ping-Chieh Pao Li-Huei Tsai Jean-Vianney Haure-Mirande Michelle E. Ehrlich Paramita Chakrabarty Yona Levites Xue Wang Eric B. Dammer Gyan Srivastava Sumit Mukherjee Solveig K. Sieberts Larsson Omberg Kristen D. Dang James A. Eddy Phil Snyder Yooree Chae Sandeep Amberkar Wenbin Wei Winston Hide Christoph Preuss Ayla Ergun Phillip J. Ebert David C. Airey Sara Mostafavi Lei Yu Hans-Ulrich Klein Gregory W. Carter David A. Collier Todd E. Golde Allan I. Levey David A. Bennett Karol Estrada T. Matthew Townsend Bin Zhang Eric Schadt Philip L. De Jager Nathan D. Price Nilüfer Ertekin-Taner Zhandong Liu Joshua M. Shulman Lara M. Mangravite Benjamin A. Logsdon Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models Alzheimer's disease transcriptome RNA-seq coexpression analysis differential expression analysis meta-analysis |
| title | Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models |
| title_full | Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models |
| title_fullStr | Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models |
| title_full_unstemmed | Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models |
| title_short | Meta-Analysis of the Alzheimer’s Disease Human Brain Transcriptome and Functional Dissection in Mouse Models |
| title_sort | meta analysis of the alzheimer s disease human brain transcriptome and functional dissection in mouse models |
| topic | Alzheimer's disease transcriptome RNA-seq coexpression analysis differential expression analysis meta-analysis |
| url | http://www.sciencedirect.com/science/article/pii/S2211124720308895 |
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