Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism

Human brain metabolism is susceptible to temperature changes. It has been suggested that the supraclavicular brown adipose tissue (BAT) protects the brain from these fluctuations by regulating heat production through the presence of uncoupling protein 1 (UCP-1). It remains unsolved whether inter-ind...

Full description

Bibliographic Details
Main Authors: Mueez U-Din, Eleni Rebelos, Teemu Saari, Tarja Niemi, Katharina Kuellmer, Olli Eskola, Tobias Fromme, Johan Rajander, Markku Taittonen, Martin Klingenspor, Pirjo Nuutila, Lauri Nummenmaa, Kirsi A. Virtanen
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/13/3/387
_version_ 1797610111298961408
author Mueez U-Din
Eleni Rebelos
Teemu Saari
Tarja Niemi
Katharina Kuellmer
Olli Eskola
Tobias Fromme
Johan Rajander
Markku Taittonen
Martin Klingenspor
Pirjo Nuutila
Lauri Nummenmaa
Kirsi A. Virtanen
author_facet Mueez U-Din
Eleni Rebelos
Teemu Saari
Tarja Niemi
Katharina Kuellmer
Olli Eskola
Tobias Fromme
Johan Rajander
Markku Taittonen
Martin Klingenspor
Pirjo Nuutila
Lauri Nummenmaa
Kirsi A. Virtanen
author_sort Mueez U-Din
collection DOAJ
description Human brain metabolism is susceptible to temperature changes. It has been suggested that the supraclavicular brown adipose tissue (BAT) protects the brain from these fluctuations by regulating heat production through the presence of uncoupling protein 1 (UCP-1). It remains unsolved whether inter-individual variation in the expression of <i>UCP-1</i>, which represents the thermogenic capacity of the supraclavicular BAT, is linked with brain metabolism during cold stress. Ten healthy human participants underwent <sup>18</sup>F-FDG PET scanning of the brain under cold stimulus to determine brain glucose uptake (BGU). On a separate day, an excision biopsy of the supraclavicular fat—the fat proximal to the carotid arteries supplying the brain with warm blood—was performed to determine the mRNA expression of the thermogenic protein <i>UCP-1</i>. Expression of <i>UCP-1</i> in supraclavicular BAT was directly related to the whole brain glucose uptake rate determined under cold stimulation (<i>rho</i> = 0.71, <i>p</i> = 0.03). In sub-compartmental brain analysis, <i>UCP-1</i> expression in supraclavicular BAT was directly related to cold-stimulated glucose uptake rates in the hypothalamus, medulla, midbrain, limbic system, frontal lobe, occipital lobe, and parietal lobe (all <i>rho</i> ≥ 0.67, <i>p</i> < 0.05). These relationships were independent of body mass index and age. When analysing gene expressions of BAT secretome, we found a positive correlation between cold-stimulated BGU and <i>DIO2</i>. These findings provide evidence of functional links between brain metabolism under cold stimulation and <i>UCP-1</i> and <i>DIO2</i> expressions in BAT in humans. More research is needed to evaluate the importance of these findings in clinical outcomes, for instance, in examining the supporting role of BAT in cognitive functions under cold stress.
first_indexed 2024-03-11T06:10:57Z
format Article
id doaj.art-082d0503447f4feeb726d4e3fc5d3e17
institution Directory Open Access Journal
issn 2218-1989
language English
last_indexed 2024-03-11T06:10:57Z
publishDate 2023-03-01
publisher MDPI AG
record_format Article
series Metabolites
spelling doaj.art-082d0503447f4feeb726d4e3fc5d3e172023-11-17T12:36:46ZengMDPI AGMetabolites2218-19892023-03-0113338710.3390/metabo13030387Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose MetabolismMueez U-Din0Eleni Rebelos1Teemu Saari2Tarja Niemi3Katharina Kuellmer4Olli Eskola5Tobias Fromme6Johan Rajander7Markku Taittonen8Martin Klingenspor9Pirjo Nuutila10Lauri Nummenmaa11Kirsi A. Virtanen12Turku PET Centre, Turku University Hospital, 20520 Turku, FinlandTurku PET Centre, Turku University Hospital, 20520 Turku, FinlandTurku PET Centre, Turku University Hospital, 20520 Turku, FinlandDepartment of Plastic and General Surgery, Turku University Hospital, 20520 Turku, FinlandChair for Molecular Nutritional Medicine, Technical University Munich, 85354 Freising, GermanyRadiopharmaceutical Chemistry Laboratory, Turku PET Centre, University of Turku, 20520 Turku, FinlandChair for Molecular Nutritional Medicine, Technical University Munich, 85354 Freising, GermanyAccelerator Laboratory, Turku PET Centre, Åbo Akademi University, 20520 Turku, FinlandDepartment of Anesthesiology, Turku University Hospital, 20520 Turku, FinlandChair for Molecular Nutritional Medicine, Technical University Munich, 85354 Freising, GermanyTurku PET Centre, Turku University Hospital, 20520 Turku, FinlandTurku PET Centre, Turku University Hospital, 20520 Turku, FinlandTurku PET Centre, University of Turku, 20520 Turku, FinlandHuman brain metabolism is susceptible to temperature changes. It has been suggested that the supraclavicular brown adipose tissue (BAT) protects the brain from these fluctuations by regulating heat production through the presence of uncoupling protein 1 (UCP-1). It remains unsolved whether inter-individual variation in the expression of <i>UCP-1</i>, which represents the thermogenic capacity of the supraclavicular BAT, is linked with brain metabolism during cold stress. Ten healthy human participants underwent <sup>18</sup>F-FDG PET scanning of the brain under cold stimulus to determine brain glucose uptake (BGU). On a separate day, an excision biopsy of the supraclavicular fat—the fat proximal to the carotid arteries supplying the brain with warm blood—was performed to determine the mRNA expression of the thermogenic protein <i>UCP-1</i>. Expression of <i>UCP-1</i> in supraclavicular BAT was directly related to the whole brain glucose uptake rate determined under cold stimulation (<i>rho</i> = 0.71, <i>p</i> = 0.03). In sub-compartmental brain analysis, <i>UCP-1</i> expression in supraclavicular BAT was directly related to cold-stimulated glucose uptake rates in the hypothalamus, medulla, midbrain, limbic system, frontal lobe, occipital lobe, and parietal lobe (all <i>rho</i> ≥ 0.67, <i>p</i> < 0.05). These relationships were independent of body mass index and age. When analysing gene expressions of BAT secretome, we found a positive correlation between cold-stimulated BGU and <i>DIO2</i>. These findings provide evidence of functional links between brain metabolism under cold stimulation and <i>UCP-1</i> and <i>DIO2</i> expressions in BAT in humans. More research is needed to evaluate the importance of these findings in clinical outcomes, for instance, in examining the supporting role of BAT in cognitive functions under cold stress.https://www.mdpi.com/2218-1989/13/3/387human brown adipose tissueBATcold stimulationbrain metabolismthermogenesisUCP-1
spellingShingle Mueez U-Din
Eleni Rebelos
Teemu Saari
Tarja Niemi
Katharina Kuellmer
Olli Eskola
Tobias Fromme
Johan Rajander
Markku Taittonen
Martin Klingenspor
Pirjo Nuutila
Lauri Nummenmaa
Kirsi A. Virtanen
Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism
Metabolites
human brown adipose tissue
BAT
cold stimulation
brain metabolism
thermogenesis
UCP-1
title Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism
title_full Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism
title_fullStr Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism
title_full_unstemmed Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism
title_short Thermogenic Capacity of Human Supraclavicular Brown Fat and Cold-Stimulated Brain Glucose Metabolism
title_sort thermogenic capacity of human supraclavicular brown fat and cold stimulated brain glucose metabolism
topic human brown adipose tissue
BAT
cold stimulation
brain metabolism
thermogenesis
UCP-1
url https://www.mdpi.com/2218-1989/13/3/387
work_keys_str_mv AT mueezudin thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT elenirebelos thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT teemusaari thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT tarjaniemi thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT katharinakuellmer thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT ollieskola thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT tobiasfromme thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT johanrajander thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT markkutaittonen thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT martinklingenspor thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT pirjonuutila thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT laurinummenmaa thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism
AT kirsiavirtanen thermogeniccapacityofhumansupraclavicularbrownfatandcoldstimulatedbrainglucosemetabolism