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Metabolic phenotyping reveals a reduction in the bioavailability of serotonin and kynurenine pathway metabolites in both the urine and serum of individuals living with Alzheimer's disease

Metabolic phenotyping reveals a reduction in the bioavailability of serotonin and kynurenine pathway metabolites in both the urine and serum of individuals living with Alzheimer's disease
Metabolic phenotyping reveals a reduction in the bioavailability of serotonin and kynurenine pathway metabolites in both the urine and serum of individuals living with Alzheimer's disease

BACKGROUND: Both serotonergic signalling disruption and systemic inflammation have been associated with the pathogenesis of Alzheimer's disease (AD). The common denominator linking the two is the catabolism of the essential amino acid, tryptophan. Metabolism via tryptophan hydroxylase results in serotonin synthesis, whilst metabolism via indoleamine 2,3-dioxygenase (IDO) results in kynurenine and its downstream derivatives. IDO is reported to be activated in times of host systemic inflammation and therefore is thought to influence both pathways. To investigate metabolic alterations in AD, a large-scale metabolic phenotyping study was conducted on both urine and serum samples collected from a multi-centre clinical cohort, consisting of individuals clinically diagnosed with AD, mild cognitive impairment (MCI) and age-matched controls.

METHODS: Metabolic phenotyping was applied to both urine (n = 560) and serum (n = 354) from the European-wide AddNeuroMed/Dementia Case Register (DCR) biobank repositories. Metabolite data were subsequently interrogated for inter-group differences; influence of gender and age; comparisons between two subgroups of MCI - versus those who remained cognitively stable at follow-up visits (sMCI); and those who underwent further cognitive decline (cMCI); and the impact of selective serotonin reuptake inhibitor (SSRI) medication on metabolite concentrations.

RESULTS: Results revealed significantly lower metabolite concentrations of tryptophan pathway metabolites in the AD group: serotonin (urine, serum), 5-hydroxyindoleacetic acid (urine), kynurenine (serum), kynurenic acid (urine), tryptophan (urine, serum), xanthurenic acid (urine, serum), and kynurenine/tryptophan ratio (urine). For each listed metabolite, a decreasing trend in concentrations was observed in-line with clinical diagnosis: control > MCI > AD. There were no significant differences in the two MCI subgroups whilst SSRI medication status influenced observations in serum, but not urine.

CONCLUSIONS: Urine and serum serotonin concentrations were found to be significantly lower in AD compared with controls, suggesting the bioavailability of the neurotransmitter may be altered in the disease. A significant increase in the kynurenine/tryptophan ratio suggests that this may be a result of a shift to the kynurenine metabolic route due to increased IDO activity, potentially as a result of systemic inflammation. Modulation of the pathways could help improve serotonin bioavailability and signalling in AD patients.

Alzheimer’s disease, Kynurenine, Mass spectrometry, Metabolic phenotyping, Serotonergic signalling, Serotonin, Systemic inflammation, Tryptophan
1758-9193
Whiley, Luke
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Chappell, Katie E
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D'Hondt, Ellie
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Lewis, Matthew R
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Jiménez, Beatriz
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Snowden, Stuart G
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Soininen, Hilkka
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Kłoszewska, Iwona
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Mecocci, Patrizia
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Tsolaki, Magda
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Vellas, Bruno
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Swann, Jonathan R
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Hye, Abdul
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Lovestone, Simon
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Legido-Quigley, Cristina
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Holmes, Elaine
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AddNeuroMed consortium
Whiley, Luke
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Chappell, Katie E
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D'Hondt, Ellie
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Lewis, Matthew R
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Jiménez, Beatriz
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Snowden, Stuart G
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Soininen, Hilkka
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Kłoszewska, Iwona
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Mecocci, Patrizia
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Tsolaki, Magda
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Vellas, Bruno
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Swann, Jonathan R
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Hye, Abdul
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Lovestone, Simon
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Legido-Quigley, Cristina
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Holmes, Elaine
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AddNeuroMed consortium (2021) Metabolic phenotyping reveals a reduction in the bioavailability of serotonin and kynurenine pathway metabolites in both the urine and serum of individuals living with Alzheimer's disease. Alzheimer's Research & Therapy, 13 (1), [20]. (doi:10.1186/s13195-020-00741-z).

Record type: Article

Abstract

BACKGROUND: Both serotonergic signalling disruption and systemic inflammation have been associated with the pathogenesis of Alzheimer's disease (AD). The common denominator linking the two is the catabolism of the essential amino acid, tryptophan. Metabolism via tryptophan hydroxylase results in serotonin synthesis, whilst metabolism via indoleamine 2,3-dioxygenase (IDO) results in kynurenine and its downstream derivatives. IDO is reported to be activated in times of host systemic inflammation and therefore is thought to influence both pathways. To investigate metabolic alterations in AD, a large-scale metabolic phenotyping study was conducted on both urine and serum samples collected from a multi-centre clinical cohort, consisting of individuals clinically diagnosed with AD, mild cognitive impairment (MCI) and age-matched controls.

METHODS: Metabolic phenotyping was applied to both urine (n = 560) and serum (n = 354) from the European-wide AddNeuroMed/Dementia Case Register (DCR) biobank repositories. Metabolite data were subsequently interrogated for inter-group differences; influence of gender and age; comparisons between two subgroups of MCI - versus those who remained cognitively stable at follow-up visits (sMCI); and those who underwent further cognitive decline (cMCI); and the impact of selective serotonin reuptake inhibitor (SSRI) medication on metabolite concentrations.

RESULTS: Results revealed significantly lower metabolite concentrations of tryptophan pathway metabolites in the AD group: serotonin (urine, serum), 5-hydroxyindoleacetic acid (urine), kynurenine (serum), kynurenic acid (urine), tryptophan (urine, serum), xanthurenic acid (urine, serum), and kynurenine/tryptophan ratio (urine). For each listed metabolite, a decreasing trend in concentrations was observed in-line with clinical diagnosis: control > MCI > AD. There were no significant differences in the two MCI subgroups whilst SSRI medication status influenced observations in serum, but not urine.

CONCLUSIONS: Urine and serum serotonin concentrations were found to be significantly lower in AD compared with controls, suggesting the bioavailability of the neurotransmitter may be altered in the disease. A significant increase in the kynurenine/tryptophan ratio suggests that this may be a result of a shift to the kynurenine metabolic route due to increased IDO activity, potentially as a result of systemic inflammation. Modulation of the pathways could help improve serotonin bioavailability and signalling in AD patients.

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Accepted/In Press date: 7 December 2020
e-pub ahead of print date: 9 January 2021
Published date: 9 January 2021
Keywords: Alzheimer’s disease, Kynurenine, Mass spectrometry, Metabolic phenotyping, Serotonergic signalling, Serotonin, Systemic inflammation, Tryptophan

Identifiers

Local EPrints ID: 448358
URI: http://eprints.soton.ac.uk/id/eprint/448358
ISSN: 1758-9193
PURE UUID: 1f81d7e6-2234-42ba-bcc4-aec2f5d16344
ORCID for Jonathan R Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 21 Apr 2021 16:30
Last modified: 17 Mar 2024 04:00

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Contributors

Author: Luke Whiley
Author: Katie E Chappell
Author: Ellie D'Hondt
Author: Matthew R Lewis
Author: Beatriz Jiménez
Author: Stuart G Snowden
Author: Hilkka Soininen
Author: Iwona Kłoszewska
Author: Patrizia Mecocci
Author: Magda Tsolaki
Author: Bruno Vellas
Author: Abdul Hye
Author: Simon Lovestone
Author: Cristina Legido-Quigley
Author: Elaine Holmes
Corporate Author: AddNeuroMed consortium

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