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1. Amyloid and Tau Pathology Associations With Personality Traits, Neuropsychiatric Symptoms, and Cognitive Lifestyle in the Preclinical Phases of Sporadic and Autosomal Dominant Alzheimer’s Disease

Author

Alexa Pichet Binette, Étienne Vachon-Presseau, John Morris, Randall Bateman, Tammie Benzinger, D. Louis Collins, Judes Poirier, John C.S. Breitner, Sylvia Villeneuve, Ricardo Allegri, Fatima Amtashar, Randy Bateman, Sarah Berman, Courtney Bodge, Susan Brandon, William (Bill) Brooks, Jill Buck, Virginia Buckles, Sochenda Chea, Jasmeer Chhatwal, Patricio Chrem, Helena Chui, Jake Cinco, Jack Clifford, Carlos Cruchaga, Mirelle D‘Mello, Tamara Donahue, Jane Douglas, Noelia Edigo, Nilufer Erekin-Taner, Anne Fagan, Marty Farlow, Angela Farrar, Howard Feldman, Gigi Flynn, Nick Fox, Erin Franklin, Hisako Fujii, Cortaiga Gant, Samantha Gardener, Bernardino Ghetti, Alison Goate, Jill Goldman, Brian Gordon, Neill Graff-Radford, Julia Gray, Jenny Gurney, Jason Hassenstab, Mie Hirohara, David Holtzman, Russ Hornbeck, Siri Houeland DiBari, Takeshi Ikeuchi, Snezana Ikonomovic, Gina Jerome, Mathias Jucker, Celeste Karch, Kensaku Kasuga, Takeshi Kawarabayashi, William (Bill) Klunk, Robert Koeppe, Elke Kuder-Buletta, Christoph Laske, Jae-Hong Lee, Johannes Levin, Daniel Marcus, Ralph Martins, Neal Scott Mason, Colin Masters, Denise Maue-Dreyfus, Eric McDade, Lucy Montoya, Hiroshi Mori, Akem Nagamatsu, Katie Neimeyer, James Noble, Joanne Norton, Richard Perrin, Marc Raichle, John Ringman, Jee Hoon Roh, Stephen Salloway, Peter Schofield, Hiroyuki Shimada, Tomoyo Shiroto, Mikio Shoji, Wendy Sigurdson, Hamid Sohrabi, Paige Sparks, Kazushi Suzuki, Laura Swisher, Kevin Taddei, Jen Wang, Peter Wang, Mike Weiner, Mary Wolfsberger, Chengjie Xiong, Xiong Xu, Angela Tam, Anne Labonté, Anne-Marie Faubert, Axel Mathieu, Cécile Madjar, Charles Edouard Carrier, Christian Dansereau, Christina Kazazian, Claude Lepage, Cynthia Picard, David Maillet, Diane Michaud, Doris Couture, Doris Dea, Claudio Cuello, Alan Barkun, Alan Evans, Blandine Courcot, Christine Tardif, Clément Debacker, Clifford R. Jack, David Fontaine, David S. Knopman, Gerhard Maultaup, Jamie Near, Jeannie-Marie Leoutsakos, Jean-Robert Maltais, Jason Brandt, Jens Pruessner, John C. Morris, Laksanun Cheewakriengkrai, Lisa-Marie Münter, Louis Collins, Mallar Chakravarty, Mark A. Sager, Marina Dauar-Tedeschi, Mark Eisenberg, Natasha Rajah, Paul Aisen, Joanne Toussaint, Pedro Rosa-Neto, Pierre Bellec, Penelope Kostopoulos, Pierre Etienne, Pierre N. Tariot, Pierre Orban, Reisa A. Sperling, Rick Hoge, Ronald G. Thomas, Serge Gauthier, Suzanne Craft, Thomas J. Montine, Vasavan Nair, Véronique Bohbot, Vinod Venugopalan, Vladimir Fonov, Yasser Ituria-Medina, Zaven S. Khachaturian, Eduard Teigner, Elena Anthal, Elsa Yu, Fabiola Ferdinand, Galina Pogossova, Ginette Mayrand, Guerda Duclair, Guylaine Gagné, Holly Newbold-Fox, Illana Leppert, Isabelle Vallée, Jacob W. Vogel, Jennifer Tremblay-Mercier, Joanne Frenette, Josée Frappier, Justin Kat, Justin Miron, Karen Wan, Laura Mahar, Leopoldina Carmo, Louise Théroux, Mahsa Dadar, Marianne Dufour, Marie-Elyse Lafaille-Magnan, Melissa Appleby, Mélissa Savard, Miranda Tuwaig, Mirela Petkova, Pierre Rioux, Pierre-François Meyer, Rana El-Khoury, Renee Gordon, Renuka Giles, Samir Das, Seqian Wang, Shirin Tabrizi, Sulantha Mathotaarachchi, Sylvie Dubuc, Tanya Lee, Thomas Beaudry, Valérie Gervais, Véronique Pagé, Julie Gonneaud, Gülebru Ayranci, Tharick A. Pascoal, René Desautels, Fatiha Benbouhoud, Eunice Farah Saint-Fort, Sander C.J. Verfaillie, Sarah Farzin, Alyssa Salaciak, Stephanie Tullo, Etienne Vachon-Presseau, Leslie-Ann Daoust, Theresa Köbe, Nathan Spreng, Melissa McSweeney, Nathalie Nilsson, Morteza Pishnamazi, and Christophe Bedetti

Subjects
0301 basic medicine, Oncology, medicine.medical_specialty, tau Proteins, Disease, Article, 03 medical and health sciences, Cognition, 0302 clinical medicine, Alzheimer Disease, Internal medicine, mental disorders, medicine, Humans, Dementia, Big Five personality traits, Family history, Life Style, Biological Psychiatry, Aged, Amyloid beta-Peptides, Extraversion and introversion, business.industry, medicine.disease, Neuroticism, 3. Good health, 030104 developmental biology, Positron-Emission Tomography, Cohort, Alzheimer's disease, business, 030217 neurology & neurosurgery
Abstract

Background Major prevention trials for Alzheimer’s disease (AD) are now focusing on multidomain lifestyle interventions. However, the exact combination of behavioral factors related to AD pathology remains unclear. In 2 cohorts of cognitively unimpaired individuals at risk of AD, we examined which combinations of personality traits, neuropsychiatric symptoms, and cognitive lifestyle (years of education or lifetime cognitive activity) related to the pathological hallmarks of AD, amyloid-β, and tau deposits. Methods A total of 115 older adults with a parental or multiple-sibling family history of sporadic AD (PREVENT-AD [PRe-symptomatic EValuation of Experimental or Novel Treatments for AD] cohort) underwent amyloid and tau positron emission tomography and answered several questionnaires related to behavioral attributes. Separately, we studied 117 mutation carriers from the DIAN (Dominant Inherited Alzheimer Network) study group cohort with amyloid positron emission tomography and behavioral data. Using partial least squares analysis, we identified latent variables relating amyloid or tau pathology with combinations of personality traits, neuropsychiatric symptoms, and cognitive lifestyle. Results In PREVENT-AD, lower neuroticism, neuropsychiatric burden, and higher education were associated with less amyloid deposition (p = .014). Lower neuroticism and neuropsychiatric features, along with higher measures of openness and extraversion, were related to less tau deposition (p = .006). In DIAN, lower neuropsychiatric burden and higher education were also associated with less amyloid (p = .005). The combination of these factors accounted for up to 14% of AD pathology. Conclusions In the preclinical phase of both sporadic and autosomal dominant AD, multiple behavioral features were associated with AD pathology. These results may suggest potential pathways by which multidomain interventions might help delay AD onset or progression.

Published
2021
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2. A soluble phosphorylated tau signature links tau, amyloid and the evolution of stages of dominantly inherited Alzheimer’s disease

Author

Barthélemy, Nicolas R, Li, Yan, Morris, John C, Neimeyer, Katie, Noble, James, Norton, Joanne, Perrin, Richard, Raichle, Marc, Renton, Alan, Ringman, John, Roh, Jee Hoon, Salloway, Stephen, Schofield, Peter, Karch, Celeste M, Shimada, Hiroyuki, Sigurdson, Wendy, Sohrabi, Hamid, Sparks, Paige, Suzuki, Kazushi, Taddei, Kevin, Wang, Peter, Xiong, Chengjie, Xu, Xiong, Allegri, Ricardo, Mendez, Patricio Chrem, Berman, Sarah B, Ikeuchi, Takeshi, Mori, Hiroshi, Shoji, Mikio, Joseph-Mathurin, Nelly, Farlow, Martin, Chhatwal, Jasmeer, Graff-Radford, Neill R, Schofield, Peter R, Masters, Colin L, Martins, Ralph N, O'Connor, Antoinette, Gordon, Brian A, Fox, Nick C, Levin, Johannes, Jucker, Mathias, Gabelle, Audrey, Lehmann, Sylvain, Sato, Chihiro, Bateman, Randall J, McDade, Eric, Network, Dominantly Inherited Alzheimer, Hassenstab, Jason, Bateman, Randy, Bechara, Jacob, Benzinger, Tammie, Berman, Sarah, Bodge, Courtney, Brandon, Susan, Brooks, William Bill, Buck, Jill, Buckles, Virginia, Chea, Sochenda, Benzinger, Tammie L S, Chrem Mendez, Patricio, Chui, Helena, Cinco, Jake, Clifford, Jack, Cruchaga, Carlos, Donahue, Tamara, Douglas, Jane, Edigo, Noelia, Erekin-Taner, Nilufer, Fagan, Anne, Fitzpatrick, Colleen, Flynn, Gigi, Fox, Nick, Franklin, Erin, Fujii, Hisako, Gant, Cortaiga, Gardener, Samantha, Ghetti, Bernardino, Fagan, Anne M, Goate, Alison, Goldman, Jill, Gordon, Brian, Graff-Radford, Neill, Gray, Julia, Groves, Alexander, Hoechst-Swisher, Laura, Holtzman, David, Hornbeck, Russ, Perrin, Richard J, DiBari, Siri Houeland, Ikonomovic, Snezana, Jerome, Gina, Karch, Celeste, Kasuga, Kensaku, Kawarabayashi, Takeshi, Klunk, William Bill, Koeppe, Robert, Kuder-Buletta, Elke, Goate, Alison M, Laske, Christoph, Lee, Jae-Hong, Martins, Ralph, Mason, Neal Scott, Masters, Colin, Maue-Dreyfus, Denise, Morris, John, Nagamatsu, Akem, Washington University School of Medicine in St. Louis, Washington University in Saint Louis (WUSTL), Icahn School of Medicine at Mount Sinai [New York] (MSSM), Fundación para la Lucha contra las Enfermedades Neurológicas de la Infancia [Buenos Aires] (FLENI), FLENI, University of Pittsburgh School of Medicine, Pennsylvania Commonwealth System of Higher Education (PCSHE), Niigata University, Osaka City University (OCU), Hirosaki University, The University of Tokyo (UTokyo), Columbia University [New York], Indiana University - Purdue University Indianapolis (IUPUI), Indiana University System, Harvard Medical School [Boston] (HMS), Mayo Clinic [Jacksonville], Brown University, Neuroscience Research Australia (NeuRA), University of New South Wales [Sydney] (UNSW), The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Edith Cowan University (ECU), Commonwealth Scientific and Industrial Research Organisation [Canberra] (CSIRO)-Planning and Transport Research Centre (PATREC), University College of London [London] (UCL), German Research Center for Neurodegenerative Diseases - Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), Ludwig-Maximilians-Universität München (LMU), Munich Cluster for systems neurology [Munich] (SyNergy), Technische Universität Munchen - Université Technique de Munich [Munich, Allemagne] (TUM)-Ludwig-Maximilians-Universität München (LMU), University of Tübingen, Centre Hospitalier Régional Universitaire [Montpellier] (CHRU Montpellier), BioCampus Montpellier (BCM), Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Dominantly Inherited Alzheimer Network: Ricardo Allegri, Randy Bateman, Jacob Bechara, Tammie Benzinger, Sarah Berman, Courtney Bodge, Susan Brandon, William Bill Brooks, Jill Buck, Virginia Buckles, Sochenda Chea, Jasmeer Chhatwal, Patricio Chrem Mendez, Helena Chui, Jake Cinco, Jack Clifford, Carlos Cruchaga, Tamara Donahue, Jane Douglas, Noelia Edigo, Nilufer Erekin-Taner, Anne Fagan, Martin Farlow, Colleen Fitzpatrick, Gigi Flynn, Nick Fox, Erin Franklin, Hisako Fujii, Cortaiga Gant, Samantha Gardener, Bernardino Ghetti, Alison Goate, Jill Goldman, Brian Gordon, Neill Graff-Radford, Julia Gray, Alexander Groves, Jason Hassenstab, Laura Hoechst-Swisher, David Holtzman, Russ Hornbeck, Siri Houeland DiBari, Takeshi Ikeuchi, Snezana Ikonomovic, Gina Jerome, Mathias Jucker, Celeste Karch, Kensaku Kasuga, Takeshi Kawarabayashi, William Bill Klunk, Robert Koeppe, Elke Kuder-Buletta, Christoph Laske, Jae-Hong Lee, Johannes Levin, Ralph Martins, Neal Scott Mason, Colin Masters, Denise Maue-Dreyfus, Eric McDade, Hiroshi Mori, John Morris, Akem Nagamatsu, Katie Neimeyer, James Noble, Joanne Norton, Richard Perrin, Marc Raichle, Alan Renton, John Ringman, Jee Hoon Roh, Stephen Salloway, Peter Schofield, Hiroyuki Shimada, Wendy Sigurdson, Hamid Sohrabi, Paige Sparks, Kazushi Suzuki, Kevin Taddei, Peter Wang, Chengjie Xiong, Xiong Xu, Technische Universität München [München] (TUM)-Ludwig-Maximilians-Universität München (LMU), BioCampus (BCM), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), and Michel-Avella, Amandine

Subjects
0301 basic medicine, Male, [SDV]Life Sciences [q-bio], Inheritance Patterns, genetics [Alzheimer Disease], Plaque, Amyloid, Disease, 0302 clinical medicine, Cerebrospinal fluid, Cognition, pathology [Brain], Phosphorylation, biology, Neurodegeneration, Brain, General Medicine, Middle Aged, Magnetic Resonance Imaging, 3. Good health, [SDV] Life Sciences [q-bio], cerebrospinal fluid [Alzheimer Disease], 030220 oncology & carcinogenesis, Disease Progression, Female, Alzheimer's disease, metabolism [Alzheimer Disease], Adult, Amyloid, genetics [Inheritance Patterns], Tau protein, Neuroimaging, tau Proteins, General Biochemistry, Genetics and Molecular Biology, Article, 03 medical and health sciences, Atrophy, Alzheimer Disease, Fluorodeoxyglucose F18, mental disorders, medicine, Humans, ddc:610, pathology [Plaque, Amyloid], chemistry [Fluorodeoxyglucose F18], metabolism [Amyloid], Aged, medicine.disease, metabolism [tau Proteins], 030104 developmental biology, cerebrospinal fluid [tau Proteins], Solubility, biology.protein, diagnostic imaging [Alzheimer Disease], Neuroscience
Abstract

International audience; Development of tau-based therapies for Alzheimer's disease requires an understanding of the timing of disease-related changes in tau. We quantified the phosphorylation state at multiple sites of the tau protein in cerebrospinal fluid markers across four decades of disease progression in dominantly inherited Alzheimer's disease. We identified a pattern of tau staging where site-specific phosphorylation changes occur at different periods of disease progression and follow distinct trajectories over time. These tau phosphorylation state changes are uniquely associated with structural, metabolic, neurodegenerative and clinical markers of disease, and some (p-tau217 and p-tau181) begin with the initial increases in aggregate amyloid-β as early as two decades before the development of aggregated tau pathology. Others (p-tau205 and t-tau) increase with atrophy and hypometabolism closer to symptom onset. These findings provide insights into the pathways linking tau, amyloid-β and neurodegeneration, and may facilitate clinical trials of tau-based treatments.

Published
2020
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