Integrated Systems Approach Identifies Genetic Nodes and Networks in Late-Onset Alzheimer’s Disease

The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer’s disease (LOAD), we construct...

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Published in	Cell Vol. 153; no. 3; pp. 707 - 720
Main Authors	Zhang, Bin, Gaiteri, Chris, Bodea, Liviu-Gabriel, Wang, Zhi, McElwee, Joshua, Podtelezhnikov, Alexei A., Zhang, Chunsheng, Xie, Tao, Tran, Linh, Dobrin, Radu, Fluder, Eugene, Clurman, Bruce, Melquist, Stacey, Narayanan, Manikandan, Suver, Christine, Shah, Hardik, Mahajan, Milind, Gillis, Tammy, Mysore, Jayalakshmi, MacDonald, Marcy E., Lamb, John R., Bennett, David A., Molony, Cliona, Stone, David J., Gudnason, Vilmundur, Myers, Amanda J., Schadt, Eric E., Neumann, Harald, Zhu, Jun, Emilsson, Valur
Format	Journal Article
Language	English
Published	United States Elsevier Inc 25.04.2013
Subjects	Adaptor Proteins, Signal Transducing - metabolism Alzheimer disease Alzheimer Disease - genetics Alzheimer Disease - metabolism Animals Bayes Theorem brain Brain - metabolism Brain - pathology chemical structure disease models gene expression regulation Gene Regulatory Networks genes Humans Membrane Proteins - metabolism Mice Microglia - metabolism neuroglia pathogens patients phagocytosis tissues
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Abstract	The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer’s disease (LOAD), we constructed gene-regulatory networks in 1,647 postmortem brain tissues from LOAD patients and nondemented subjects, and we demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune- and microglia-specific module that is dominated by genes involved in pathogen phagocytosis, contains TYROBP as a key regulator, and is upregulated in LOAD. Mouse microglia cells overexpressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a framework to test models of disease mechanisms underlying LOAD. [Display omitted] •Systems approach to LOAD based on large-scale human brain-tissue sampling•Molecular networks show strong remodeling effect in LOAD brains•Integrative network-based analysis implicates the immune/microglia network in LOAD•TYROBP implicated as key causal regulator within the immune/microglia module An integrated systems approach leverages transcriptome data from postmortem brains of late-onset Alzheimer’s disease patients to identify key nodes that drive dysregulated or rewired networks in the disease state.
AbstractList	The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer’s disease (LOAD), we constructed gene regulatory networks in 1647 post-mortem brain tissues from LOAD patients and non-demented subjects, and demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune and microglia-specific module dominated by genes involved in pathogen phagocytosis, containing TYROBP as a key regulator and up-regulated in LOAD. Mouse microglia cells over-expressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a novel framework to test models of disease mechanisms underlying LOAD. The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer’s disease (LOAD), we constructed gene-regulatory networks in 1,647 postmortem brain tissues from LOAD patients and nondemented subjects, and we demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune- and microglia-specific module that is dominated by genes involved in pathogen phagocytosis, contains TYROBP as a key regulator, and is upregulated in LOAD. Mouse microglia cells overexpressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a framework to test models of disease mechanisms underlying LOAD. The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer’s disease (LOAD), we constructed gene-regulatory networks in 1,647 postmortem brain tissues from LOAD patients and nondemented subjects, and we demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune- and microglia-specific module that is dominated by genes involved in pathogen phagocytosis, contains TYROBP as a key regulator, and is upregulated in LOAD. Mouse microglia cells overexpressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a framework to test models of disease mechanisms underlying LOAD. The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer's disease (LOAD), we constructed gene-regulatory networks in 1,647 postmortem brain tissues from LOAD patients and nondemented subjects, and we demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune- and microglia-specific module that is dominated by genes involved in pathogen phagocytosis, contains TYROBP as a key regulator, and is upregulated in LOAD. Mouse microglia cells overexpressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a framework to test models of disease mechanisms underlying LOAD.The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer's disease (LOAD), we constructed gene-regulatory networks in 1,647 postmortem brain tissues from LOAD patients and nondemented subjects, and we demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune- and microglia-specific module that is dominated by genes involved in pathogen phagocytosis, contains TYROBP as a key regulator, and is upregulated in LOAD. Mouse microglia cells overexpressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a framework to test models of disease mechanisms underlying LOAD. The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the organized structure of molecular networks. To characterize molecular systems associated with late-onset Alzheimer’s disease (LOAD), we constructed gene-regulatory networks in 1,647 postmortem brain tissues from LOAD patients and nondemented subjects, and we demonstrate that LOAD reconfigures specific portions of the molecular interaction structure. Through an integrative network-based approach, we rank-ordered these network structures for relevance to LOAD pathology, highlighting an immune- and microglia-specific module that is dominated by genes involved in pathogen phagocytosis, contains TYROBP as a key regulator, and is upregulated in LOAD. Mouse microglia cells overexpressing intact or truncated TYROBP revealed expression changes that significantly overlapped the human brain TYROBP network. Thus the causal network structure is a useful predictor of response to gene perturbations and presents a framework to test models of disease mechanisms underlying LOAD. [Display omitted] •Systems approach to LOAD based on large-scale human brain-tissue sampling•Molecular networks show strong remodeling effect in LOAD brains•Integrative network-based analysis implicates the immune/microglia network in LOAD•TYROBP implicated as key causal regulator within the immune/microglia module An integrated systems approach leverages transcriptome data from postmortem brains of late-onset Alzheimer’s disease patients to identify key nodes that drive dysregulated or rewired networks in the disease state.
Author	Emilsson, Valur Dobrin, Radu Fluder, Eugene Zhang, Chunsheng MacDonald, Marcy E. Gudnason, Vilmundur Gaiteri, Chris Schadt, Eric E. Gillis, Tammy Mysore, Jayalakshmi Lamb, John R. McElwee, Joshua Suver, Christine Tran, Linh Narayanan, Manikandan Myers, Amanda J. Podtelezhnikov, Alexei A. Molony, Cliona Wang, Zhi Neumann, Harald Bodea, Liviu-Gabriel Bennett, David A. Stone, David J. Clurman, Bruce Xie, Tao Mahajan, Milind Zhang, Bin Shah, Hardik Zhu, Jun Melquist, Stacey
AuthorAffiliation	10 GNF Novartis, 10675 John Jay Hopkins Drive, San Diego, CA 92121, USA 8 Fred Hutch Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109, USA 13 Department of Psychiatry and Behavioral Sciences, Division of Neuroscience, Miller School of Medicine, University of Miami, Miami, FL 33136, USA 3 Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA 11 Rush Alzheimer Disease Center, Rush University Medical Center, Chicago, IL, USA 5 Neural Regeneration Group, Institute of Reconstructive Neurobiology, University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany 1 Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai School, 1425 Madison Avenue, NY 10029, USA 6 Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA 4 Sage Bionetworks, Seattle, 1100 Fairview Avenue North, WA 98109, USA 7 Merck Research Laboratories, Merck & Co. Inc., 770
AuthorAffiliation_xml	– name: 3 Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029, USA – name: 9 Center for Human Genetic Research, Massachusetts General Hospital, 185 Cambridge Street, Boston, MA 02114, USA – name: 2 Icahn Institute of Genomics and Multi-scale Biology, Icahn School of Medicine at Mount Sinai School of Medicine, 1425 Madison Avenue, NY10029-6501, USA – name: 6 Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – name: 7 Merck Research Laboratories, Merck & Co. Inc., 770 Sumneytown Pike, WP53B-120 West Point, PA 19486, USA – name: 12 Icelandic Heart Association, Holtasmari 1, IS-201 Kopavogur, Iceland – name: 5 Neural Regeneration Group, Institute of Reconstructive Neurobiology, University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany – name: 8 Fred Hutch Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109, USA – name: 1 Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai School, 1425 Madison Avenue, NY 10029, USA – name: 4 Sage Bionetworks, Seattle, 1100 Fairview Avenue North, WA 98109, USA – name: 11 Rush Alzheimer Disease Center, Rush University Medical Center, Chicago, IL, USA – name: 10 GNF Novartis, 10675 John Jay Hopkins Drive, San Diego, CA 92121, USA – name: 13 Department of Psychiatry and Behavioral Sciences, Division of Neuroscience, Miller School of Medicine, University of Miami, Miami, FL 33136, USA
Author_xml	– sequence: 1 givenname: Bin surname: Zhang fullname: Zhang, Bin email: bin.zhang@mssm.edu organization: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA – sequence: 2 givenname: Chris surname: Gaiteri fullname: Gaiteri, Chris organization: Sage Bionetworks, 1100 Fairview Avenue North, Seattle, WA 98109, USA – sequence: 3 givenname: Liviu-Gabriel surname: Bodea fullname: Bodea, Liviu-Gabriel organization: Neural Regeneration Group, Institute of Reconstructive Neurobiology, University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany – sequence: 4 givenname: Zhi surname: Wang fullname: Wang, Zhi organization: Sage Bionetworks, 1100 Fairview Avenue North, Seattle, WA 98109, USA – sequence: 5 givenname: Joshua surname: McElwee fullname: McElwee, Joshua organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 6 givenname: Alexei A. surname: Podtelezhnikov fullname: Podtelezhnikov, Alexei A. organization: Merck Research Laboratories, Merck & Co. Inc., 770 Sumneytown Pike, WP53B-120 West Point, PA 19486, USA – sequence: 7 givenname: Chunsheng surname: Zhang fullname: Zhang, Chunsheng organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 8 givenname: Tao surname: Xie fullname: Xie, Tao organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 9 givenname: Linh surname: Tran fullname: Tran, Linh organization: Sage Bionetworks, 1100 Fairview Avenue North, Seattle, WA 98109, USA – sequence: 10 givenname: Radu surname: Dobrin fullname: Dobrin, Radu organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 11 givenname: Eugene surname: Fluder fullname: Fluder, Eugene organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 12 givenname: Bruce surname: Clurman fullname: Clurman, Bruce organization: Fred Hutch Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109, USA – sequence: 13 givenname: Stacey surname: Melquist fullname: Melquist, Stacey organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 14 givenname: Manikandan surname: Narayanan fullname: Narayanan, Manikandan organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 15 givenname: Christine surname: Suver fullname: Suver, Christine organization: Sage Bionetworks, 1100 Fairview Avenue North, Seattle, WA 98109, USA – sequence: 16 givenname: Hardik surname: Shah fullname: Shah, Hardik organization: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA – sequence: 17 givenname: Milind surname: Mahajan fullname: Mahajan, Milind organization: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA – sequence: 18 givenname: Tammy surname: Gillis fullname: Gillis, Tammy organization: Center for Human Genetic Research, Massachusetts General Hospital, 185 Cambridge Street, Boston, MA 02114, USA – sequence: 19 givenname: Jayalakshmi surname: Mysore fullname: Mysore, Jayalakshmi organization: Center for Human Genetic Research, Massachusetts General Hospital, 185 Cambridge Street, Boston, MA 02114, USA – sequence: 20 givenname: Marcy E. surname: MacDonald fullname: MacDonald, Marcy E. organization: Center for Human Genetic Research, Massachusetts General Hospital, 185 Cambridge Street, Boston, MA 02114, USA – sequence: 21 givenname: John R. surname: Lamb fullname: Lamb, John R. organization: GNF Novartis, 10675 John Jay Hopkins Drive, San Diego, CA 92121, USA – sequence: 22 givenname: David A. surname: Bennett fullname: Bennett, David A. organization: Rush Alzheimer Disease Center, Rush University Medical Center, Chicago, IL 60612, USA – sequence: 23 givenname: Cliona surname: Molony fullname: Molony, Cliona organization: Merck Research Laboratories, Merck & Co. Inc., 33 Avenue Louis Pasteur, Boston, MA 02115, USA – sequence: 24 givenname: David J. surname: Stone fullname: Stone, David J. organization: Merck Research Laboratories, Merck & Co. Inc., 770 Sumneytown Pike, WP53B-120 West Point, PA 19486, USA – sequence: 25 givenname: Vilmundur surname: Gudnason fullname: Gudnason, Vilmundur organization: Icelandic Heart Association and University of Iceland, Holtasmari 1, IS-201 Kopavogur, Iceland – sequence: 26 givenname: Amanda J. surname: Myers fullname: Myers, Amanda J. organization: Department of Psychiatry and Behavioral Sciences, Division of Neuroscience, Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 27 givenname: Eric E. surname: Schadt fullname: Schadt, Eric E. organization: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA – sequence: 28 givenname: Harald surname: Neumann fullname: Neumann, Harald organization: Neural Regeneration Group, Institute of Reconstructive Neurobiology, University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany – sequence: 29 givenname: Jun surname: Zhu fullname: Zhu, Jun organization: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA – sequence: 30 givenname: Valur surname: Emilsson fullname: Emilsson, Valur email: valur@hjarta.is organization: Icelandic Heart Association and University of Iceland, Holtasmari 1, IS-201 Kopavogur, Iceland
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23622250$$D View this record in MEDLINE/PubMed
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Snippet	The genetics of complex disease produce alterations in the molecular interactions of cellular pathways whose collective effect may become clear through the...
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SubjectTerms	Adaptor Proteins, Signal Transducing - metabolism Alzheimer disease Alzheimer Disease - genetics Alzheimer Disease - metabolism Animals Bayes Theorem brain Brain - metabolism Brain - pathology chemical structure disease models gene expression regulation Gene Regulatory Networks genes Humans Membrane Proteins - metabolism Mice Microglia - metabolism neuroglia pathogens patients phagocytosis tissues
Title	Integrated Systems Approach Identifies Genetic Nodes and Networks in Late-Onset Alzheimer’s Disease
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