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Molecular Networks and Key Regulators of the Dysregulated Neuronal System in Alzheimer’s Disease

Minghui Wang, Aiqun Li, Michiko Sekiya, Noam D. Beckmann, Xiuming Quan, Nadine Schrode, Michael B. Fernando, Alex Yu, Li Zhu, Jiqing Cao, Liwei Lyu, Emrin Horgusluoglu, Qian Wang, Lei Guo, Yuan-shuo Wang, Ryan Neff, Won-min Song, Erming Wang, Qi Shen, Xianxiao Zhou, Chen Ming, Seok-Man Ho, Sezen Vatansever, H. Umit Kaniskan, Jian Jin, Ming-Ming Zhou, Kanae Ando, Lap Ho, Paul A. Slesinger, Zhenyu Yue, Jun Zhu, Sam Gandy, Michelle E. Ehrlich, Dongming Cai, Vahram Haroutunian, Koichi M. Iijima, Eric Schadt, Kristen J. Brennand, Bin Zhang
doi: https://doi.org/10.1101/788323
Minghui Wang
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Aiqun Li
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Michiko Sekiya
Department of Alzheimer’s Disease Research, Center for Development of Advanced Medicine for Dementia, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan 474-8511Department of Experimental Gerontology, Graduate School of Pharmaceutical Sciences, Nagoya City University, Nagoya, Japan 467-8603
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Noam D. Beckmann
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Xiuming Quan
Department of Alzheimer’s Disease Research, Center for Development of Advanced Medicine for Dementia, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan 474-8511
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Nadine Schrode
Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Michael B. Fernando
Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Alex Yu
Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Li Zhu
Department of Neurology, Icahn School of Medicine at Mount Sinai, New York NY 10029Alzheimer’s Disease Research Center, Icahn School of Medicine at Mount Sinai, New York NY 10029Neurology and Psychiatry, JJ Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
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Jiqing Cao
Department of Neurology, Icahn School of Medicine at Mount Sinai, New York NY 10029Alzheimer’s Disease Research Center, Icahn School of Medicine at Mount Sinai, New York NY 10029Neurology and Psychiatry, JJ Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
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Liwei Lyu
Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Emrin Horgusluoglu
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Qian Wang
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Lei Guo
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Yuan-shuo Wang
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Ryan Neff
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Won-min Song
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Erming Wang
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Qi Shen
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Xianxiao Zhou
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Chen Ming
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Seok-Man Ho
Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Sezen Vatansever
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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H. Umit Kaniskan
Department of Pharmacological Sciences and Oncological Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAMount Sinai Center for Therapeutics Discovery, Icahn School of Medicine at Mount Sinai, New York, NY10029, United States
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Jian Jin
Department of Pharmacological Sciences and Oncological Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAMount Sinai Center for Therapeutics Discovery, Icahn School of Medicine at Mount Sinai, New York, NY10029, United StatesTisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY10029, United States
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Ming-Ming Zhou
Department of Pharmacological Sciences and Oncological Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Kanae Ando
Department of Biological Sciences, Graduate School of Science, Tokyo Metropolitan University, Tokyo, Japan 192-0397
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Lap Ho
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Paul A. Slesinger
Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Zhenyu Yue
Department of Neurology, Icahn School of Medicine at Mount Sinai, New York NY 10029
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Jun Zhu
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Sam Gandy
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Neurology, Icahn School of Medicine at Mount Sinai, New York NY 10029Alzheimer’s Disease Research Center, Icahn School of Medicine at Mount Sinai, New York NY 10029
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Michelle E. Ehrlich
Department of Neurology, Icahn School of Medicine at Mount Sinai, New York NY 10029Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York NY 10029
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Dongming Cai
Department of Neurology, Icahn School of Medicine at Mount Sinai, New York NY 10029Alzheimer’s Disease Research Center, Icahn School of Medicine at Mount Sinai, New York NY 10029Neurology and Psychiatry, JJ Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
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Vahram Haroutunian
Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAAlzheimer’s Disease Research Center, Icahn School of Medicine at Mount Sinai, New York NY 10029Neurology and Psychiatry, JJ Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
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Koichi M. Iijima
Department of Alzheimer’s Disease Research, Center for Development of Advanced Medicine for Dementia, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan 474-8511Department of Experimental Gerontology, Graduate School of Pharmaceutical Sciences, Nagoya City University, Nagoya, Japan 467-8603
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Eric Schadt
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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Kristen J. Brennand
Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USANash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USAFriedman Brain Institute, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USADepartment of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA
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Bin Zhang
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAMount Sinai Center for Transformative Disease Modeling, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USAIcahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA
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  • For correspondence: bin.zhang@mssm.edu
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SUMMARY

To study the molecular mechanisms driving the pathogenesis and identify novel therapeutic targets of late onset Alzheimer’s Disease (LOAD), we performed an integrative network analysis of whole-genome DNA and RNA sequencing profiling of four cortical areas, including the parahippocampal gyrus, across 364 donors spanning the full spectrum of LOAD-related cognitive and neuropathological disease severities. Our analyses revealed thousands of molecular changes and uncovered for the first-time multiple neuron specific gene subnetworks most dysregulated in LOAD. ATP6V1A, a critical subunit of vacuolar-type H+-ATPase (v-ATPase), was predicted to be a key regulator of one neuronal subnetwork and its role in disease-related processes was evaluated through CRISPR-based manipulation of human induced pluripotent stem cell derived neurons and RNAi-based knockdown in transgenic Drosophila models. This study advances our understanding of LOAD pathogenesis by providing the global landscape and detailed circuits of complex molecular interactions and regulations in several key brain regions affected by LOAD and the resulting network models provide a blueprint for developing next generation therapeutics against LOAD.

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Posted October 01, 2019.
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Molecular Networks and Key Regulators of the Dysregulated Neuronal System in Alzheimer’s Disease
Minghui Wang, Aiqun Li, Michiko Sekiya, Noam D. Beckmann, Xiuming Quan, Nadine Schrode, Michael B. Fernando, Alex Yu, Li Zhu, Jiqing Cao, Liwei Lyu, Emrin Horgusluoglu, Qian Wang, Lei Guo, Yuan-shuo Wang, Ryan Neff, Won-min Song, Erming Wang, Qi Shen, Xianxiao Zhou, Chen Ming, Seok-Man Ho, Sezen Vatansever, H. Umit Kaniskan, Jian Jin, Ming-Ming Zhou, Kanae Ando, Lap Ho, Paul A. Slesinger, Zhenyu Yue, Jun Zhu, Sam Gandy, Michelle E. Ehrlich, Dongming Cai, Vahram Haroutunian, Koichi M. Iijima, Eric Schadt, Kristen J. Brennand, Bin Zhang
bioRxiv 788323; doi: https://doi.org/10.1101/788323
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Molecular Networks and Key Regulators of the Dysregulated Neuronal System in Alzheimer’s Disease
Minghui Wang, Aiqun Li, Michiko Sekiya, Noam D. Beckmann, Xiuming Quan, Nadine Schrode, Michael B. Fernando, Alex Yu, Li Zhu, Jiqing Cao, Liwei Lyu, Emrin Horgusluoglu, Qian Wang, Lei Guo, Yuan-shuo Wang, Ryan Neff, Won-min Song, Erming Wang, Qi Shen, Xianxiao Zhou, Chen Ming, Seok-Man Ho, Sezen Vatansever, H. Umit Kaniskan, Jian Jin, Ming-Ming Zhou, Kanae Ando, Lap Ho, Paul A. Slesinger, Zhenyu Yue, Jun Zhu, Sam Gandy, Michelle E. Ehrlich, Dongming Cai, Vahram Haroutunian, Koichi M. Iijima, Eric Schadt, Kristen J. Brennand, Bin Zhang
bioRxiv 788323; doi: https://doi.org/10.1101/788323

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