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1. Neuropathological and transcriptomic characteristics of the aged brain

Author

Jeremy A Miller, Angela Guillozet-Bongaarts, Laura E Gibbons, Nadia Postupna, Anne Renz, Allison E Beller, Susan M Sunkin, Lydia Ng, Shannon E Rose, Kimberly A Smith, Aaron Szafer, Chris Barber, Darren Bertagnolli, Kristopher Bickley, Krissy Brouner, Shiella Caldejon, Mike Chapin, Mindy L Chua, Natalie M Coleman, Eiron Cudaback, Christine Cuhaciyan, Rachel A Dalley, Nick Dee, Tsega Desta, Tim A Dolbeare, Nadezhda I Dotson, Michael Fisher, Nathalie Gaudreault, Garrett Gee, Terri L Gilbert, Jeff Goldy, Fiona Griffin, Caroline Habel, Zeb Haradon, Nika Hejazinia, Leanne L Hellstern, Steve Horvath, Kim Howard, Robert Howard, Justin Johal, Nikolas L Jorstad, Samuel R Josephsen, Chihchau L Kuan, Florence Lai, Eric Lee, Felix Lee, Tracy Lemon, Xianwu Li, Desiree A Marshall, Jose Melchor, Shubhabrata Mukherjee, Julie Nyhus, Julie Pendergraft, Lydia Potekhina, Elizabeth Y Rha, Samantha Rice, David Rosen, Abharika Sapru, Aimee Schantz, Elaine Shen, Emily Sherfield, Shu Shi, Andy J Sodt, Nivretta Thatra, Michael Tieu, Angela M Wilson, Thomas J Montine, Eric B Larson, Amy Bernard, Paul K Crane, Richard G Ellenbogen, C Dirk Keene, and Ed Lein

Subjects
Alzheimer's disease, aging, dementia, gene expression, Medicine, Science, Biology (General), QH301-705.5
Abstract

As more people live longer, age-related neurodegenerative diseases are an increasingly important societal health issue. Treatments targeting specific pathologies such as amyloid beta in Alzheimer’s disease (AD) have not led to effective treatments, and there is increasing evidence of a disconnect between traditional pathology and cognitive abilities with advancing age, indicative of individual variation in resilience to pathology. Here, we generated a comprehensive neuropathological, molecular, and transcriptomic characterization of hippocampus and two regions cortex in 107 aged donors (median = 90) from the Adult Changes in Thought (ACT) study as a freely-available resource (http://aging.brain-map.org/). We confirm established associations between AD pathology and dementia, albeit with increased, presumably aging-related variability, and identify sets of co-expressed genes correlated with pathological tau and inflammation markers. Finally, we demonstrate a relationship between dementia and RNA quality, and find common gene signatures, highlighting the importance of properly controlling for RNA quality when studying dementia.

Published
2017
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2. Neuropathological and transcriptomic characteristics of the aged brain

Author

Terri L. Gilbert, Thomas J. Montine, Aaron Szafer, Eiron Cudaback, Nick Dee, Christine Cuhaciyan, Xianwu Li, Kimberly A. Smith, Samuel R Josephsen, Tim A. Dolbeare, Paul K. Crane, Amy Bernard, Nadezhda Dotson, Michael Tieu, Fiona Griffin, Shannon E. Rose, Ed S. Lein, Jeff Goldy, Laura E. Gibbons, Julie Pendergraft, Felix Lee, Nivretta Thatra, Elaine Shen, Elizabeth Rha, Susan M. Sunkin, Garrett Gee, Lydia Potekhina, Nadia Postupna, Darren Bertagnolli, Andy J. Sodt, Nikolas L. Jorstad, Angela L. Guillozet-Bongaarts, Samantha Rice, Jeremy A. Miller, Natalie M Coleman, Zeb Haradon, Tsega Desta, David Rosen, Angela M. Wilson, Justin Johal, Shubhabrata Mukherjee, Kristopher Bickley, Anne Renz, Abharika Sapru, Robert Howard, Desiree A. Marshall, Tracy Lemon, Nika Hejazinia, Rachel A. Dalley, Shu Shi, Steve Horvath, Mindy L Chua, Aimee Schantz, Eric B. Larson, Allison Beller, Michael S. Fisher, Julie Nyhus, C. Dirk Keene, Lydia Ng, Kim Howard, Caroline Habel, Nathalie Gaudreault, Krissy Brouner, Leanne L Hellstern, Shiella Caldejon, Jose Melchor, Emily Sherfield, Chihchau L. Kuan, Mike Chapin, Richard G. Ellenbogen, Chris Barber, Florence Lai, and Eric Lee

Subjects
0301 basic medicine, Male, Amyloid beta, QH301-705.5, Science, Hippocampus, Disease, General Biochemistry, Genetics and Molecular Biology, Transcriptome, 03 medical and health sciences, 0302 clinical medicine, Alzheimer Disease, medicine, Dementia, Humans, Biology (General), Gene, Pathological, Aged, Aged, 80 and over, Cerebral Cortex, General Immunology and Microbiology, biology, business.industry, General Neuroscience, Gene Expression Profiling, aging, Cognition, General Medicine, Alzheimer's disease, medicine.disease, 3. Good health, Tools and Resources, 030104 developmental biology, biology.protein, gene expression, Medicine, Female, business, Neuroscience, 030217 neurology & neurosurgery, Human, dementia
Abstract

As more people live longer, age-related neurodegenerative diseases are an increasingly important societal health issue. Treatments targeting specific pathologies such as amyloid beta in Alzheimer’s disease (AD) have not led to effective treatments, and there is increasing evidence of a disconnect between traditional pathology and cognitive abilities with advancing age, indicative of individual variation in resilience to pathology. Here, we generated a comprehensive neuropathological, molecular, and transcriptomic characterization of hippocampus and two regions cortex in 107 aged donors (median = 90) from the Adult Changes in Thought (ACT) study as a freely-available resource (http://aging.brain-map.org/). We confirm established associations between AD pathology and dementia, albeit with increased, presumably aging-related variability, and identify sets of co-expressed genes correlated with pathological tau and inflammation markers. Finally, we demonstrate a relationship between dementia and RNA quality, and find common gene signatures, highlighting the importance of properly controlling for RNA quality when studying dementia.

Published
2017

3. Author response: Neuropathological and transcriptomic characteristics of the aged brain

Author

Lydia Ng, Shubhabrata Mukherjee, Amy Bernard, Mindy L Chua, Jeff Goldy, Fiona Griffin, Darren Bertagnolli, Shu Shi, Ed S. Lein, Susan M. Sunkin, Nika Hejazinia, Justin Johal, Krissy Brouner, Jeremy A. Miller, Steve Horvath, Zeb Haradon, Natalie M Coleman, Jose Melchor, Desiree A. Marshall, Samuel R Josephsen, Paul K. Crane, Kristopher Bickley, Tim A. Dolbeare, Kim Howard, Michael S. Fisher, C. Dirk Keene, Angela M. Wilson, Tracy Lemon, Aaron Szafer, Eiron Cudaback, Nick Dee, Eric B. Larson, Elizabeth Rha, Chris Barber, Julie Nyhus, Michael Tieu, Lydia Potekhina, Caroline Habel, Nathalie Gaudreault, Kimberly A. Smith, Shannon E. Rose, Nikolas L. Jorstad, Angela L. Guillozet-Bongaarts, Terri L. Gilbert, Felix Lee, Nivretta Thatra, Florence Lai, Julie Pendergraft, Elaine Shen, Eric Lee, Christine Cuhaciyan, Chihchau L. Kuan, Mike Chapin, Richard G. Ellenbogen, Andy J. Sodt, Leanne L Hellstern, Shiella Caldejon, Nadia Postupna, David Rosen, Emily Sherfield, Tsega Desta, Anne Renz, Xianwu Li, Abharika Sapru, Robert Howard, Rachel A. Dalley, Aimee Schantz, Allison Beller, Samantha Rice, Nadezhda Dotson, Laura E. Gibbons, Garrett Gee, and Thomas J. Montine

Subjects
0301 basic medicine, Transcriptome, 03 medical and health sciences, 030104 developmental biology, business.industry, Medicine, business, Neuroscience
Published
2017

4. A comprehensive transcriptional map of primate brain development

Author

Songlin Ding, R.D. Young, Paul Wohnoutka, Anna Hoerder-Suabedissen, Brian L. Youngstrom, Rachel A. Dalley, Terri L. Gilbert, Stephanie Butler, Lydia Potekhina, Jody Parente, Shiella Caldejon, Shu Shi, Kimberly A. Smith, Lon T. Luong, Chinh Dang, Aaron Oldre, Shelby Cate, Emi J. Byrnes, Susan M. Sunkin, Joshua J. Royall, Jefferey Chen, Amanda Ebbert, Jeffrey Rogers, Zeb Haradon, Lindsey Gourley, Ryan May, Naveed Mastan, Aaron Szafer, Chihchau L. Kuan, Kristopher Bickley, Tracy Lemon, Nick Dee, Nerick Mosqueda, Ed S. Lein, David Rosen, Mike Chapin, John W. Phillips, Guangyu Gu, Crissa Bennett, Nadia Dotson, Kate Roll, Ali Kriedberg, Nika Hejazinia, Nadiya V. Shapovalova, Brandon Rogers, Jon Hall, David G. Amaral, Robert Howard, Melaine Sarreal, Sheana Parry, Kaylynn Aiona, Tim A. Dolbeare, Michael Hawrylycz, Allan R. Jones, Robert F. Hevner, Nathan Sjoquist, Tyson Roberts, Marty Kinnunen, Lissette Velasquez, Jay Jochim, Richard A. Gibbs, Anita Carey, Tsega Desta, Jennifer Wu, Kiet Ngo, Julie Nyhus, Julie Pendergraft, Ben W. Gregor, Sheila Shapouri, Amy Bernard, Lydia Ng, Darren Bertagnolli, Eric Olson, Jeff Goldy, Udi Wagley, Changkyu Lee, Christopher Lau, David R. Haynor, Krissy Brouner, Erika Mott, Jeremy A. Miller, Andy J. Sodt, Jeffrey L. Bennett, Jose Melchor, Patrick D. Parker, Cassandra White, Zoltán Molnár, Andrew F. Boe, Zackery L. Riley, Trygve E. Bakken, David Sandman, Garrett Gee, James M. Arnold, Erich Fulfs, Robbie Townsend, Wayne Wakeman, John G. Hohmann, Felix Lee, and Melissa Reding

Subjects
0301 basic medicine, Male, Microcephaly, Aging, Transcription, Genetic, Autism Spectrum Disorder, Neocortex, Molecular neuroscience, Transcriptome, 0302 clinical medicine, Risk Factors, 2.1 Biological and endogenous factors, Primate, Conserved Sequence, Pediatric, Multidisciplinary, biology, Neurogenesis, Brain, Mental Health, medicine.anatomical_structure, Autism spectrum disorder, Neurological, Stem Cell Research - Nonembryonic - Non-Human, Female, Transcription, Biotechnology, General Science & Technology, Intellectual and Developmental Disabilities (IDD), 1.1 Normal biological development and functioning, Article, 03 medical and health sciences, Spatio-Temporal Analysis, Species Specificity, Genetic, biology.animal, Intellectual Disability, Genetics, medicine, Cell Adhesion, Animals, Humans, Cell projection, Human Genome, Neurosciences, Stem Cell Research, medicine.disease, Macaca mulatta, Brain Disorders, 030104 developmental biology, Neurodevelopmental Disorders, Schizophrenia, Neuroscience, 030217 neurology & neurosurgery
Abstract

The transcriptional underpinnings of brain development remain poorly understood, particularly in humans and closely related non-human primates. We describe a high-resolution transcriptional atlas of rhesus monkey (Macaca mulatta) brain development that combines dense temporal sampling of prenatal and postnatal periods with fine anatomical division of cortical and subcortical regions associated with human neuropsychiatric disease. Gene expression changes more rapidly before birth, both in progenitor cells and maturing neurons. Cortical layers and areas acquire adult-like molecular profiles surprisingly late in postnatal development. Disparate cell populations exhibit distinct developmental timing of gene expression, but also unexpected synchrony of processes underlying neural circuit construction including cell projection and adhesion. Candidate risk genes for neurodevelopmental disorders including primary microcephaly, autism spectrum disorder, intellectual disability, and schizophrenia show disease-specific spatiotemporal enrichment within developing neocortex. Human developmental expression trajectories are more similar to monkey than rodent, although approximately 9% of genes show human-specific regulation with evidence for prolonged maturation or neoteny compared to monkey.

Published
2016

5. An anatomic transcriptional atlas of human glioblastoma

Author

Greg Foltz, Parvinder Hothi, Ali Kriedberg, Krissy Brouner, David Feng, Chantal Murthy, Robert Howard, Robert C. Rostomily, David Sandman, Eric Olson, Nadezhda Dotson, Nameeta Shah, Guangyu Gu, Kris Bickley, Lydia Ng, Nika Hejazinia, John W. Phillips, Leonard Kuan, Charles Cobbs, Garrett Gee, Tim A. Dolbeare, Tsega Desta, Shiella Caldejon, Kiet Ngo, Haley Gittleman, Andrew F. Boe, Hwahyung Lee, Rachel A. Dalley, Steven J. White, Chris Lau, Bart Keogh, Graham Stockdale, Lindsey Gourley, Fuhui Long, Darren Bertagnolli, Andrew Sodt, Michael Hawrylycz, Amanda Ebbert, Jill S. Barnholtz-Sloan, David Rosen, Michael S. Fisher, Antonio Iavarone, Ed S. Lein, Stephanie Butler, Patrick J. Cimino, Tracy Lemon, Zack Riley, Allan R. Jones, Megha S Uppin, Mike Chapin, Naveed Mastan, Kimberly A. Smith, Michael E. Berens, Clifford R. Slaughterbeck, Aaron Szafer, Nick Dee, Wayne Wakeman, John G. Hohmann, Benjamin W. Gregor, Suvro Datta, Felix Lee, Ralph B. Puchalski, Melissa Reding, Nadiya V. Shapovalova, Xu Feng, Amy Bernard, Jae Guen Yoon, Erika Mott, Jeremy A. Miller, Justin D. Lathia, Steve R. Nomura, Steven Rostad, Kevin M. Joines, Paul Wohnoutka, Jeff Goldy, Don Marsh, Farrokh Farrokhi, Michael Lankerovich, C. Dirk Keene, and Chinh Dang

Subjects
0301 basic medicine, Poor prognosis, Multidisciplinary, Extramural, Brain Neoplasms, Gene Expression Profiling, Brain tumor, Computational biology, Biology, medicine.disease, Prognosis, Genomic databases, Data resources, Article, nervous system diseases, Gene expression profiling, 03 medical and health sciences, 030104 developmental biology, Atlases as Topic, Databases, Genetic, medicine, Humans, Glioblastoma, neoplasms
Abstract

Anatomically correct tumor genomics Glioblastoma is the most lethal form of human brain cancer. The genomic alterations and gene expression profiles characterizing this tumor type have been widely studied. Puchalski et al. created the Ivy Glioblastoma Atlas, a freely available online resource for the research community. The atlas, a collaborative effort between bioinformaticians and pathologists, maps molecular features of glioblastomas, such as transcriptional signatures, to histologically defined anatomical regions of the tumors. The relationships identified in this atlas, in conjunction with associated databases of clinical and genomic information, could provide new insights into the pathogenesis, diagnosis, and treatment of glioblastoma. Science , this issue p. 660

Published
2016

6. An anatomically comprehensive atlas of the adult human brain transcriptome

Author

Susan M. Sunkin, Preston M. Cartagena, Robert Howard, Christian F. Beckmann, David Feng, Zeb Haradon, Chinh Dang, Angela L. Guillozet-Bongaarts, Derric Williams, Jeff Goldy, Yang Li, Rachel A. Dalley, Tracy Lemon, Darren Bertagnolli, Clifford R. Slaughterbeck, Simon Smith, Steve Horvath, Christof Koch, Amanda Ebbert, Andreas Jeromin, Paul Wohnoutka, Michael Hawrylycz, Andy J. Sodt, Beryl Swanson, H. Ronald Zielke, Zackery L. Riley, John A. Morris, Evan T. Lazarz, Chris Abajian, Allan R. Jones, Mike Chapin, Changkyu Lee, Pedro Adolfo Sequeira, Jay Schulkin, Christopher Lau, Jeremy A. Miller, Tim A. Dolbeare, Ling Li, Nick Dee, Sheana Parry, Barry Daly, Patrick D. Parker, Marty Kinnunen, Amy Bernard, Joshua J. Royall, Vance Faber, John G. Hohmann, Patrick R. Hof, Stephen M. Smith, Suvro Datta, Kimberly A. Smith, Elaine H. Shen, Caroline C. Overly, Ed S. Lein, Jayson M. Jochim, Benjamin W. Gregor, Melissa Reding, M. Mallar Chakravarty, Seth G. N. Grant, Lydia Ng, Jimmy Chong, Marquis P. Vawter, Daniel H. Geschwind, David R. Haynor, Andrew F. Boe, Louie N. van de Lagemaat, David R. Fowler, Magnetic Detection and Imaging, and Faculty of Science and Technology

Subjects
Adult, Male, Cell type, Calbindins, Dopamine, Neocortex, Biology, Hippocampus, Article, Transcriptome, 03 medical and health sciences, Mice, METIS-292322, 0302 clinical medicine, Atlases as Topic, S100 Calcium Binding Protein G, Species Specificity, Databases, Genetic, Transcriptional regulation, medicine, Animals, Humans, RNA, Messenger, Anatomy, Artistic, In Situ Hybridization, 030304 developmental biology, Oligonucleotide Array Sequence Analysis, Genetics, 0303 health sciences, Internet, IR-83002, Multidisciplinary, Anatomical location, Gene Expression Profiling, Brain, Post-Synaptic Density, Human brain, Macaca mulatta, Gene expression profiling, medicine.anatomical_structure, Frontal lobe, Health, Neuroscience, 030217 neurology & neurosurgery
Abstract

Neuroanatomically precise, genome-wide maps of transcript distributions are critical resources to complement genomic sequence data and to correlate functional and genetic brain architecture. Here we describe the generation and analysis of a transcriptional atlas of the adult human brain, comprising extensive histological analysis and comprehensive microarray profiling of ~900 neuroanatomically precise subdivisions in two individuals. Transcriptional regulation varies enormously by anatomical location, with different regions and their constituent cell types displaying robust molecular signatures that are highly conserved between individuals. Analysis of differential gene expression and gene co-expression relationships demonstrates that brain-wide variation strongly reflects the distributions of major cell classes such as neurons, oligodendrocytes, astrocytes and microglia. Local neighbourhood relationships between fine anatomical subdivisions are associated with discrete neuronal subtypes and genes involved with synaptic transmission. The neocortex displays a relatively homogeneous transcriptional pattern, but with distinct features associated selectively with primary sensorimotor cortices and with enriched frontal lobe expression. Notably, the spatial topography of the neocortex is strongly reflected in its molecular topography— the closer two cortical regions, the more similar their transcriptomes. This freely accessible online data resource forms a high-resolution transcriptional baseline for neurogenetic studies of normal and abnormal human brain function.

Published
2012

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