Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias

Hussein N. Yassine; Wade Self; Bilal E. Kerman; Giulia Santoni; Nanda Kumar Navalpur Shanmugam; Laila Abdullah; Lesley R. Golden; Alfred N. Fonteh; Michael G. Harrington; Johannes Gräff; Gary E. Gibson; Raj Kalaria; Jose A. Luchsinger; Howard H. Feldman; Russell H. Swerdlow; Lance A. Johnson; Benedict C. Albensi; Berislav V. Zlokovic; Rudolph Tanzi; Stephen Cunnane; Cécilia Samieri; Nikolaos Scarmeas; Gene L. Bowman

doi:10.1002/alz.12845

Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias

Hussein N. Yassine
, Wade Self
, Bilal E. Kerman
, Giulia Santoni
, Nanda Kumar Navalpur Shanmugam
, Laila Abdullah
, Lesley R. Golden
, Alfred N. Fonteh
, Michael G. Harrington
, Johannes Gräff
, Gary E. Gibson
, Raj Kalaria
, Jose A. Luchsinger
, Howard H. Feldman
, Russell H. Swerdlow
, Lance A. Johnson
, Benedict C. Albensi
, Berislav V. Zlokovic
, Rudolph Tanzi
, Stephen Cunnane

Cécilia Samieri, Nikolaos Scarmeas, Gene L. Bowman

Research output: Contribution to journal › Review article › peer-review

Abstract

Disturbances in the brain's capacity to meet its energy demand increase the risk of synaptic loss, neurodegeneration, and cognitive decline. Nutritional and metabolic interventions that target metabolic pathways combined with diagnostics to identify deficits in cerebral bioenergetics may therefore offer novel therapeutic potential for Alzheimer's disease (AD) prevention and management. Many diet-derived natural bioactive components can govern cellular energy metabolism but their effects on brain aging are not clear. This review examines how nutritional metabolism can regulate brain bioenergetics and mitigate AD risk. We focus on leading mechanisms of cerebral bioenergetic breakdown in the aging brain at the cellular level, as well as the putative causes and consequences of disturbed bioenergetics, particularly at the blood-brain barrier with implications for nutrient brain delivery and nutritional interventions. Novel therapeutic nutrition approaches including diet patterns are provided, integrating studies of the gut microbiome, neuroimaging, and other biomarkers to guide future personalized nutritional interventions.

Original language	English
Pages (from-to)	1041-1066
Number of pages	26
Journal	Alzheimer's and Dementia
Volume	19
Issue number	3
DOIs	https://doi.org/10.1002/alz.12845
State	Published - Mar 2023

Bibliographical note

Publisher Copyright:
© 2022 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.

Funding

Funders	Funder number
National Institute on Aging	R13AG069386, R21AG056518, R01AG055770, R01AG054434, R01AG067063, RF1AG076124, RF1AG078362, 2P01AG014930-15A1, R01AG043679
L.K. Whittier Foundation
W.M. Keck Foundation	R01NS072497, P30072973
ERC Starting	StG 678832, R01 AG062550, R01 AG060056, R01AG043398
National Institutes of Health	NCCIHR90AT008924

ASJC Scopus Subject Areas

Epidemiology
Health Policy
Developmental Neuroscience
Clinical Neurology
Geriatrics and Gerontology
Cellular and Molecular Neuroscience
Psychiatry and Mental health

Disciplines

Pharmacy and Pharmaceutical Sciences

Access to Document

10.1002/alz.12845License: CC BY-NC

Cite this

Yassine, H. N., Self, W., Kerman, B. E., Santoni, G., Navalpur Shanmugam, N. K., Abdullah, L., Golden, L. R., Fonteh, A. N., Harrington, M. G., Gräff, J., Gibson, G. E., Kalaria, R., Luchsinger, J. A., Feldman, H. H., Swerdlow, R. H., Johnson, L. A., Albensi, B. C., Zlokovic, B. V., Tanzi, R., ... Bowman, G. L. (2023). Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias. Alzheimer's and Dementia, 19(3), 1041-1066. https://doi.org/10.1002/alz.12845

Yassine, HN, Self, W, Kerman, BE, Santoni, G, Navalpur Shanmugam, NK, Abdullah, L, Golden, LR, Fonteh, AN, Harrington, MG, Gräff, J, Gibson, GE, Kalaria, R, Luchsinger, JA, Feldman, HH, Swerdlow, RH, Johnson, LA, Albensi, BC, Zlokovic, BV, Tanzi, R, Cunnane, S, Samieri, C, Scarmeas, N & Bowman, GL 2023, 'Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias', Alzheimer's and Dementia, vol. 19, no. 3, pp. 1041-1066. https://doi.org/10.1002/alz.12845

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title = "Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias",

abstract = "Disturbances in the brain's capacity to meet its energy demand increase the risk of synaptic loss, neurodegeneration, and cognitive decline. Nutritional and metabolic interventions that target metabolic pathways combined with diagnostics to identify deficits in cerebral bioenergetics may therefore offer novel therapeutic potential for Alzheimer's disease (AD) prevention and management. Many diet-derived natural bioactive components can govern cellular energy metabolism but their effects on brain aging are not clear. This review examines how nutritional metabolism can regulate brain bioenergetics and mitigate AD risk. We focus on leading mechanisms of cerebral bioenergetic breakdown in the aging brain at the cellular level, as well as the putative causes and consequences of disturbed bioenergetics, particularly at the blood-brain barrier with implications for nutrient brain delivery and nutritional interventions. Novel therapeutic nutrition approaches including diet patterns are provided, integrating studies of the gut microbiome, neuroimaging, and other biomarkers to guide future personalized nutritional interventions.",

author = "Yassine, \{Hussein N.\} and Wade Self and Kerman, \{Bilal E.\} and Giulia Santoni and \{Navalpur Shanmugam\}, \{Nanda Kumar\} and Laila Abdullah and Golden, \{Lesley R.\} and Fonteh, \{Alfred N.\} and Harrington, \{Michael G.\} and Johannes Gr{\"a}ff and Gibson, \{Gary E.\} and Raj Kalaria and Luchsinger, \{Jose A.\} and Feldman, \{Howard H.\} and Swerdlow, \{Russell H.\} and Johnson, \{Lance A.\} and Albensi, \{Benedict C.\} and Zlokovic, \{Berislav V.\} and Rudolph Tanzi and Stephen Cunnane and C{\'e}cilia Samieri and Nikolaos Scarmeas and Bowman, \{Gene L.\}",

note = "Publisher Copyright: {\textcopyright} 2022 The Authors. Alzheimer's \& Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.",

year = "2023",

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AU - Yassine, Hussein N.

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AU - Navalpur Shanmugam, Nanda Kumar

AU - Abdullah, Laila

AU - Golden, Lesley R.

AU - Fonteh, Alfred N.

AU - Harrington, Michael G.

AU - Gräff, Johannes

AU - Gibson, Gary E.

AU - Kalaria, Raj

AU - Luchsinger, Jose A.

AU - Feldman, Howard H.

AU - Swerdlow, Russell H.

AU - Johnson, Lance A.

AU - Albensi, Benedict C.

AU - Zlokovic, Berislav V.

AU - Tanzi, Rudolph

AU - Cunnane, Stephen

AU - Samieri, Cécilia

AU - Scarmeas, Nikolaos

AU - Bowman, Gene L.

PY - 2023/3

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N2 - Disturbances in the brain's capacity to meet its energy demand increase the risk of synaptic loss, neurodegeneration, and cognitive decline. Nutritional and metabolic interventions that target metabolic pathways combined with diagnostics to identify deficits in cerebral bioenergetics may therefore offer novel therapeutic potential for Alzheimer's disease (AD) prevention and management. Many diet-derived natural bioactive components can govern cellular energy metabolism but their effects on brain aging are not clear. This review examines how nutritional metabolism can regulate brain bioenergetics and mitigate AD risk. We focus on leading mechanisms of cerebral bioenergetic breakdown in the aging brain at the cellular level, as well as the putative causes and consequences of disturbed bioenergetics, particularly at the blood-brain barrier with implications for nutrient brain delivery and nutritional interventions. Novel therapeutic nutrition approaches including diet patterns are provided, integrating studies of the gut microbiome, neuroimaging, and other biomarkers to guide future personalized nutritional interventions.

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Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias

Abstract

Bibliographical note

Funding

ASJC Scopus Subject Areas

Disciplines

Access to Document

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