The sleep-wake cycle regulates brain interstitial fluid tau in mice and CSF tau in humans
The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer’s disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We...
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| Published in | Science (American Association for the Advancement of Science) Vol. 363; no. 6429; pp. 880 - 884 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Association for the Advancement of Science
22.02.2019
The American Association for the Advancement of Science |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0036-8075 1095-9203 1095-9203 |
| DOI | 10.1126/science.aav2546 |
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| Abstract | The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer’s disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We tested whether ISF/CSF tau and tau seeding and spreading were influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness versus sleep and ~100% during SD. Human CSF tau also increased more than 50% during SD. In a tau seeding-and-spreading model, chronic SD increased tau pathology spreading. Chemogenetically driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau, and SD increases ISF and CSF tau as well as tau pathology spreading. |
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| AbstractList | The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer's disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We tested whether ISF/CSF tau and tau seeding and spreading were influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness versus sleep and ~100% during SD. Human CSF tau also increased more than 50% during SD. In a tau seeding-and-spreading model, chronic SD increased tau pathology spreading. Chemogenetically driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau, and SD increases ISF and CSF tau as well as tau pathology spreading.The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer's disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We tested whether ISF/CSF tau and tau seeding and spreading were influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness versus sleep and ~100% during SD. Human CSF tau also increased more than 50% during SD. In a tau seeding-and-spreading model, chronic SD increased tau pathology spreading. Chemogenetically driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau, and SD increases ISF and CSF tau as well as tau pathology spreading. Sleep may protect the brain from ADTwo main proteins accumulate in the brain in Alzheimer's disease (AD), β-amyloid (Aβ) and tau. Aβ appears to instigate AD, but tau appears to drive brain damage and cognitive decline. Sleep deprivation is known to increase Aβ acutely and chronically. Now, Holth et al. show that chronic sleep deprivation strongly increases tau acutely over hours and also drives tau pathology spreading in the brains of mice and humans (see the Perspective by Noble and Spires-Jones). Thus, sleep appears to have a direct protective effect on a key protein that drives AD pathology.Science, this issue p. 880; see also p. 813The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer’s disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We tested whether ISF/CSF tau and tau seeding and spreading were influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness versus sleep and ~100% during SD. Human CSF tau also increased more than 50% during SD. In a tau seeding-and-spreading model, chronic SD increased tau pathology spreading. Chemogenetically driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau, and SD increases ISF and CSF tau as well as tau pathology spreading. The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer’s disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We tested whether ISF/CSF tau and tau seeding and spreading were influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness versus sleep and ~100% during SD. Human CSF tau also increased more than 50% during SD. In a tau seeding-and-spreading model, chronic SD increased tau pathology spreading. Chemogenetically driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau, and SD increases ISF and CSF tau as well as tau pathology spreading. The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal (CSF) levels of amyloid-β (Aβ) that accumulates in Alzheimer disease (AD) and chronic sleep deprivation (SD) increases Aβ plaques. However, tau not Aβ accumulation appears to drive AD neurodegeneration. Therefore, we tested whether ISF/CSF tau and tau seeding/spreading was influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness vs. sleep and ~100% during SD. Human CSF tau also increased over 50% during SD. In a tau seeding and spreading model, chronic SD increased tau pathology spreading. Chemogenetically-driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau and sleep deprivation increases ISF and CSF tau as well as tau pathology spreading. Brain interstitial fluid tau is increased during wakefulness and with sleep deprivation, which is relevant for Alzheimer disease and other tauopathies. Two main proteins accumulate in the brain in Alzheimer's disease (AD), β-amyloid (Aβ) and tau. Aβ appears to instigate AD, but tau appears to drive brain damage and cognitive decline. Sleep deprivation is known to increase Aβ acutely and chronically. Now, Holth et al. show that chronic sleep deprivation strongly increases tau acutely over hours and also drives tau pathology spreading in the brains of mice and humans (see the Perspective by Noble and Spires-Jones). Thus, sleep appears to have a direct protective effect on a key protein that drives AD pathology. Science , this issue p. 880 ; see also p. 813 Extracellular tau is increased during wakefulness and with sleep deprivation, with potential relevance for Alzheimer’s disease. The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer’s disease (AD). Furthermore, chronic sleep deprivation (SD) increases Aβ plaques. However, tau, not Aβ, accumulation appears to drive AD neurodegeneration. We tested whether ISF/CSF tau and tau seeding and spreading were influenced by the sleep-wake cycle and SD. Mouse ISF tau was increased ~90% during normal wakefulness versus sleep and ~100% during SD. Human CSF tau also increased more than 50% during SD. In a tau seeding-and-spreading model, chronic SD increased tau pathology spreading. Chemogenetically driven wakefulness in mice also significantly increased both ISF Aβ and tau. Thus, the sleep-wake cycle regulates ISF tau, and SD increases ISF and CSF tau as well as tau pathology spreading. |
| Author | Wang, Chanung Holtzman, David M. Holth, Jerrah K. Mahan, Thomas E. Lucey, Brendan P. Pedersen, Nigel P. Manis, Melissa Cirrito, John R. Finn, Mary Beth Fuller, Patrick M. Geerling, Joel C. Fritschi, Sarah K. |
| AuthorAffiliation | 2 Department of Neurology, Emory Epilepsy Center and Program in Neuroscience, Emory University, Atlanta, GA 30322, USA 3 Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, IA 52242, USA 1 Department of Neurology, Hope Center for Neurological Disorders, and Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110, USA 4 Department of Neurology, Beth Israel Deaconess Medical Center, Division of Sleep Medicine, Harvard Medical School, Boston, MA 02215, USA |
| AuthorAffiliation_xml | – name: 1 Department of Neurology, Hope Center for Neurological Disorders, and Charles F. and Joanne Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO 63110, USA – name: 4 Department of Neurology, Beth Israel Deaconess Medical Center, Division of Sleep Medicine, Harvard Medical School, Boston, MA 02215, USA – name: 2 Department of Neurology, Emory Epilepsy Center and Program in Neuroscience, Emory University, Atlanta, GA 30322, USA – name: 3 Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, IA 52242, USA |
| Author_xml | – sequence: 1 givenname: Jerrah K. surname: Holth fullname: Holth, Jerrah K. – sequence: 2 givenname: Sarah K. surname: Fritschi fullname: Fritschi, Sarah K. – sequence: 3 givenname: Chanung surname: Wang fullname: Wang, Chanung – sequence: 4 givenname: Nigel P. surname: Pedersen fullname: Pedersen, Nigel P. – sequence: 5 givenname: John R. surname: Cirrito fullname: Cirrito, John R. – sequence: 6 givenname: Thomas E. surname: Mahan fullname: Mahan, Thomas E. – sequence: 7 givenname: Mary Beth surname: Finn fullname: Finn, Mary Beth – sequence: 8 givenname: Melissa surname: Manis fullname: Manis, Melissa – sequence: 9 givenname: Joel C. surname: Geerling fullname: Geerling, Joel C. – sequence: 10 givenname: Patrick M. surname: Fuller fullname: Fuller, Patrick M. – sequence: 11 givenname: Brendan P. surname: Lucey fullname: Lucey, Brendan P. – sequence: 12 givenname: David M. surname: Holtzman fullname: Holtzman, David M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30679382$$D View this record in MEDLINE/PubMed |
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| Snippet | The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer’s disease (AD).... Two main proteins accumulate in the brain in Alzheimer's disease (AD), β-amyloid (Aβ) and tau. Aβ appears to instigate AD, but tau appears to drive brain... The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal fluid (CSF) levels of β-amyloid (Aβ) that accumulates in Alzheimer's disease (AD).... Sleep may protect the brain from ADTwo main proteins accumulate in the brain in Alzheimer's disease (AD), β-amyloid (Aβ) and tau. Aβ appears to instigate AD,... The sleep-wake cycle regulates interstitial fluid (ISF) and cerebrospinal (CSF) levels of amyloid-β (Aβ) that accumulates in Alzheimer disease (AD) and chronic... |
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| SubjectTerms | Alzheimer's disease Amyloid beta-Peptides - analysis Amyloid beta-Peptides - cerebrospinal fluid Amyloid beta-Peptides - metabolism Animals Brain Brain - metabolism Brain damage Brain injury Cerebrospinal fluid Circadian Rhythm Cognitive ability Extracellular Fluid - chemistry Extracellular Fluid - metabolism Female Male Mice Mice, Transgenic Neurodegeneration Neurodegenerative diseases Neurological Impairments Pathology Proteins Senile plaques Sleep Sleep - physiology Sleep and wakefulness Sleep deprivation Sleep Deprivation - cerebrospinal fluid Sleep Deprivation - metabolism Spires Spreading Tau protein tau Proteins - analysis tau Proteins - cerebrospinal fluid tau Proteins - metabolism Wakefulness Wakefulness - genetics Wakefulness - physiology β-Amyloid |
| Title | The sleep-wake cycle regulates brain interstitial fluid tau in mice and CSF tau in humans |
| URI | https://www.jstor.org/stable/26762241 https://www.ncbi.nlm.nih.gov/pubmed/30679382 https://www.proquest.com/docview/2184544557 https://www.proquest.com/docview/2179473424 https://pubmed.ncbi.nlm.nih.gov/PMC6410369 |
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