Caloric restriction preserves memory and reduces anxiety of aging mice with early enhancement of neurovascular functions

Ishita Parikh; Janet Guo; Kai Hsiang Chuang; Yu Zhong; Ralf G. Rempe; Jared D. Hoffman; Rachel Armstrong; Björn Bauer; Anika M.S. Hartz; Ai Ling Lin

doi:10.18632/aging.101094

Caloric restriction preserves memory and reduces anxiety of aging mice with early enhancement of neurovascular functions

Ishita Parikh
, Janet Guo
, Kai Hsiang Chuang
, Yu Zhong
, Ralf G. Rempe
, Jared D. Hoffman
, Rachel Armstrong
, Björn Bauer
, Anika M.S. Hartz
, Ai Ling Lin

Producción científica: Article › revisión exhaustiva

73 Citas (Scopus)

Resumen

Neurovascular integrity plays an important role in protecting cognitive and mental health in aging. Lifestyle interventions that sustain neurovascular integrity may thus be critical on preserving brain functions in aging and reducing the risk for age-related neurodegenerative disorders. Here we show that caloric restriction (CR) had an early effect on neurovascular enhancements, and played a critical role in preserving vascular, cognitive and mental health in aging. In particular, we found that CR significantly enhanced cerebral blood flow (CBF) and blood-brain barrier function in young mice at 5-6 months of age. The neurovascular enhancements were associated with reduced mammalian target of rapamycin expression, elevated endothelial nitric oxide synthase signaling, and increased ketone bodies utilization. With age, CR decelerated the rate of decline in CBF. The preserved CBF in hippocampus and frontal cortex were highly correlated with preserved memory and learning, and reduced anxiety, of the aging mice treated with CR (18-20 months of age). Our results suggest that dietary intervention started in the early stage (e.g., young adults) may benefit cognitive and mental reserve in aging. Understanding nutritional effects on neurovascular functions may have profound implications in human brain aging and age-related neurodegenerative disorders.

Idioma original	English
Páginas (desde-hasta)	2814-2826
Número de páginas	13
Publicación	Aging
Volumen	8
N.º	11
DOI	https://doi.org/10.18632/aging.101094
Estado	Published - 2016

Nota bibliográfica

Funding Information:
We thank Vikas Bakshi, David Powell, Stephanie Edelmann, Shin-ichi Akanuma, and Harrison Tam for their technical assistance. We also thank Dr. Adam Bachstetter for his advice on behavioral assessments. The MRI imaging and data were processed using MANGO software developed by the Research Imaging Institute of the University of Texas Health Science Center at San Antonio. This research was supported by National Institute of Health (NIH) Grant K01AG040164 and American Federation for Aging Research Grant #A12474 to ALL, and NIH R01AG039621 to AMSH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The 7T ClinScan small animal MRI scanner of the University of Kentucky was funded by the S10 NIH Shared Instrumentation Program Grant (1S10RR029541-01).

Financiación

We thank Vikas Bakshi, David Powell, Stephanie Edelmann, Shin-ichi Akanuma, and Harrison Tam for their technical assistance. We also thank Dr. Adam Bachstetter for his advice on behavioral assessments. The MRI imaging and data were processed using MANGO software developed by the Research Imaging Institute of the University of Texas Health Science Center at San Antonio. This research was supported by National Institute of Health (NIH) Grant K01AG040164 and American Federation for Aging Research Grant #A12474 to ALL, and NIH R01AG039621 to AMSH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The 7T ClinScan small animal MRI scanner of the University of Kentucky was funded by the S10 NIH Shared Instrumentation Program Grant (1S10RR029541-01).

Financiadores	Número del financiador
Hartford Foundation/American Federation	R01AG039621, 12474
National Institute of Health National Institute of Minority and Health Disparities Loan Repayment Program	K01AG040164
National Institutes of Health (NIH)	1S10RR029541-01
National Institute of Diabetes and Digestive and Kidney Diseases	T32DK007778
The University of Texas Health Science Center at San Antonio

ODS de las Naciones Unidas

Este resultado contribuye a los siguientes Objetivos de Desarrollo Sostenible

Good health and well being

ASJC Scopus subject areas

Aging
Cell Biology

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10.18632/aging.101094

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title = "Caloric restriction preserves memory and reduces anxiety of aging mice with early enhancement of neurovascular functions",

abstract = "Neurovascular integrity plays an important role in protecting cognitive and mental health in aging. Lifestyle interventions that sustain neurovascular integrity may thus be critical on preserving brain functions in aging and reducing the risk for age-related neurodegenerative disorders. Here we show that caloric restriction (CR) had an early effect on neurovascular enhancements, and played a critical role in preserving vascular, cognitive and mental health in aging. In particular, we found that CR significantly enhanced cerebral blood flow (CBF) and blood-brain barrier function in young mice at 5-6 months of age. The neurovascular enhancements were associated with reduced mammalian target of rapamycin expression, elevated endothelial nitric oxide synthase signaling, and increased ketone bodies utilization. With age, CR decelerated the rate of decline in CBF. The preserved CBF in hippocampus and frontal cortex were highly correlated with preserved memory and learning, and reduced anxiety, of the aging mice treated with CR (18-20 months of age). Our results suggest that dietary intervention started in the early stage (e.g., young adults) may benefit cognitive and mental reserve in aging. Understanding nutritional effects on neurovascular functions may have profound implications in human brain aging and age-related neurodegenerative disorders.",

keywords = "Anxiety, Blood-brain barrier, Caloric restriction, Cerebral blood flow, Cognition, Magnetic resonance imaging (MRI), Mammalian target of rapamcyin (mTOR)",

author = "Ishita Parikh and Janet Guo and Chuang, \{Kai Hsiang\} and Yu Zhong and Rempe, \{Ralf G.\} and Hoffman, \{Jared D.\} and Rachel Armstrong and Bj{\"o}rn Bauer and Hartz, \{Anika M.S.\} and Lin, \{Ai Ling\}",

note = "Funding Information: We thank Vikas Bakshi, David Powell, Stephanie Edelmann, Shin-ichi Akanuma, and Harrison Tam for their technical assistance. We also thank Dr. Adam Bachstetter for his advice on behavioral assessments. The MRI imaging and data were processed using MANGO software developed by the Research Imaging Institute of the University of Texas Health Science Center at San Antonio. This research was supported by National Institute of Health (NIH) Grant K01AG040164 and American Federation for Aging Research Grant \#A12474 to ALL, and NIH R01AG039621 to AMSH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The 7T ClinScan small animal MRI scanner of the University of Kentucky was funded by the S10 NIH Shared Instrumentation Program Grant (1S10RR029541-01).",

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AU - Parikh, Ishita

AU - Guo, Janet

AU - Chuang, Kai Hsiang

AU - Zhong, Yu

AU - Rempe, Ralf G.

AU - Hoffman, Jared D.

AU - Armstrong, Rachel

AU - Bauer, Björn

AU - Hartz, Anika M.S.

AU - Lin, Ai Ling

N1 - Funding Information: We thank Vikas Bakshi, David Powell, Stephanie Edelmann, Shin-ichi Akanuma, and Harrison Tam for their technical assistance. We also thank Dr. Adam Bachstetter for his advice on behavioral assessments. The MRI imaging and data were processed using MANGO software developed by the Research Imaging Institute of the University of Texas Health Science Center at San Antonio. This research was supported by National Institute of Health (NIH) Grant K01AG040164 and American Federation for Aging Research Grant #A12474 to ALL, and NIH R01AG039621 to AMSH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The 7T ClinScan small animal MRI scanner of the University of Kentucky was funded by the S10 NIH Shared Instrumentation Program Grant (1S10RR029541-01).

PY - 2016

Y1 - 2016

N2 - Neurovascular integrity plays an important role in protecting cognitive and mental health in aging. Lifestyle interventions that sustain neurovascular integrity may thus be critical on preserving brain functions in aging and reducing the risk for age-related neurodegenerative disorders. Here we show that caloric restriction (CR) had an early effect on neurovascular enhancements, and played a critical role in preserving vascular, cognitive and mental health in aging. In particular, we found that CR significantly enhanced cerebral blood flow (CBF) and blood-brain barrier function in young mice at 5-6 months of age. The neurovascular enhancements were associated with reduced mammalian target of rapamycin expression, elevated endothelial nitric oxide synthase signaling, and increased ketone bodies utilization. With age, CR decelerated the rate of decline in CBF. The preserved CBF in hippocampus and frontal cortex were highly correlated with preserved memory and learning, and reduced anxiety, of the aging mice treated with CR (18-20 months of age). Our results suggest that dietary intervention started in the early stage (e.g., young adults) may benefit cognitive and mental reserve in aging. Understanding nutritional effects on neurovascular functions may have profound implications in human brain aging and age-related neurodegenerative disorders.

AB - Neurovascular integrity plays an important role in protecting cognitive and mental health in aging. Lifestyle interventions that sustain neurovascular integrity may thus be critical on preserving brain functions in aging and reducing the risk for age-related neurodegenerative disorders. Here we show that caloric restriction (CR) had an early effect on neurovascular enhancements, and played a critical role in preserving vascular, cognitive and mental health in aging. In particular, we found that CR significantly enhanced cerebral blood flow (CBF) and blood-brain barrier function in young mice at 5-6 months of age. The neurovascular enhancements were associated with reduced mammalian target of rapamycin expression, elevated endothelial nitric oxide synthase signaling, and increased ketone bodies utilization. With age, CR decelerated the rate of decline in CBF. The preserved CBF in hippocampus and frontal cortex were highly correlated with preserved memory and learning, and reduced anxiety, of the aging mice treated with CR (18-20 months of age). Our results suggest that dietary intervention started in the early stage (e.g., young adults) may benefit cognitive and mental reserve in aging. Understanding nutritional effects on neurovascular functions may have profound implications in human brain aging and age-related neurodegenerative disorders.

KW - Anxiety

KW - Blood-brain barrier

KW - Caloric restriction

KW - Cerebral blood flow

KW - Cognition

KW - Magnetic resonance imaging (MRI)

KW - Mammalian target of rapamcyin (mTOR)

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UR - https://www.scopus.com/pages/publications/85002158057#tab=citedBy

U2 - 10.18632/aging.101094

DO - 10.18632/aging.101094

M3 - Article

C2 - 27829242

AN - SCOPUS:85002158057

SN - 1945-4589

VL - 8

SP - 2814

EP - 2826

JO - Aging

JF - Aging

IS - 11

ER -

Caloric restriction preserves memory and reduces anxiety of aging mice with early enhancement of neurovascular functions

Resumen

Nota bibliográfica

Financiación

ODS de las Naciones Unidas

ASJC Scopus subject areas

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