Secretin activates brown fat and induces satiation.


Journal

Nature metabolism
ISSN: 2522-5812
Titre abrégé: Nat Metab
Pays: Germany
ID NLM: 101736592

Informations de publication

Date de publication:
06 2021
Historique:
received: 19 10 2020
accepted: 07 05 2021
entrez: 23 6 2021
pubmed: 24 6 2021
medline: 4 9 2021
Statut: ppublish

Résumé

Brown adipose tissue (BAT) thermogenesis is activated by feeding. Recently, we revealed a secretin-mediated gut-BAT-brain axis, which stimulates satiation in mice, but the purpose of meal-induced BAT activation in humans has been unclear. In this placebo-controlled, randomized crossover study, we investigated the effects of intravenous secretin on BAT metabolism (measured with [

Identifiants

pubmed: 34158656
doi: 10.1038/s42255-021-00409-4
pii: 10.1038/s42255-021-00409-4
doi:

Substances chimiques

Secretin 1393-25-5
Glucose IY9XDZ35W2

Banques de données

ClinicalTrials.gov
['NCT03290846']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

798-809

Commentaires et corrections

Type : CommentIn

Références

Virtanen, K. A. et al. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518–1525 (2009).
pubmed: 19357407 doi: 10.1056/NEJMoa0808949
Cypess, A. M. et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509–1517 (2009).
pubmed: 19357406 pmcid: 2859951 doi: 10.1056/NEJMoa0810780
van Marken Lichtenbelt, W. D. et al. Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500–1508 (2009).
pubmed: 19357405 doi: 10.1056/NEJMoa0808718
Blondin, D. P. et al. Contributions of white and brown adipose tissues and skeletal muscles to acute cold-induced metabolic responses in healthy men. J. Physiol. 593, 701–714 (2015).
pubmed: 25384777 doi: 10.1113/jphysiol.2014.283598
Villarroya, F., Cereijo, R., Villarroya, J. & Giralt, M. Brown adipose tissue as a secretory organ. Nat. Rev. Endocrinol. 13, 26–35 (2017).
pubmed: 27616452 doi: 10.1038/nrendo.2016.136
Kajimura, S., Spiegelman, B. M. & Seale, P. Brown and beige fat: physiological roles beyond heat generation. Cell Metab. 22, 546–559 (2015).
pubmed: 26445512 pmcid: 4613812 doi: 10.1016/j.cmet.2015.09.007
Rothwell, N. J. & Stock, M. J. A role for brown adipose tissue in diet-induced thermogenesis. Nature 281, 31–35 (1979).
pubmed: 551265 doi: 10.1038/281031a0
Glick, Z., Teague, R. J. & Bray, G. A. Brown adipose tissue: thermic response increased by a single low protein, high carbohydrate meal. Science 213, 1125–1127 (1981).
pubmed: 7268419 doi: 10.1126/science.7268419
U Din, M. et al. Postprandial oxidative metabolism of human brown fat indicates thermogenesis. Cell Metab. 28, 207–216.e3 (2018).
pubmed: 29909972 doi: 10.1016/j.cmet.2018.05.020
Chondronikola, M., Porter, C., Malagaris, I., Nella, A. A. & Sidossis, L. S. Brown adipose tissue is associated with systemic concentrations of peptides secreted from the gastrointestinal system and involved in appetite regulation. Eur. J. Endocrinol. 177, 33–40 (2017).
pubmed: 28566533 pmcid: 6438623 doi: 10.1530/EJE-16-0958
Crovetti, R., Porrini, M., Santangelo, A. & Testolin, G. The influence of thermic effect of food on satiety. Eur. J. Clin. Nutr. 52, 482–488 (1998).
pubmed: 9683329 doi: 10.1038/sj.ejcn.1600578
Li, Y. et al. Secretin-activated brown fat mediates prandial thermogenesis to induce satiation. Cell 175, 1561–1574.e12 (2018).
pubmed: 30449620 doi: 10.1016/j.cell.2018.10.016
Blondin, D. et al. Inhibition of intracellular triglyceride lipolysis suppresses cold-induced brown adipose tissue metabolism and increases shivering in humans. Cell Metab. 25, 438–447 (2017).
pubmed: 28089568 doi: 10.1016/j.cmet.2016.12.005
Wu, C., Jin, X., Tsueng, G., Afrasiabi, C. & Su, A. I. BioGPS: building your own mash-up of gene annotations and expression profiles. Nucleic Acids Res. 44, D313–D316 (2016).
pubmed: 26578587 doi: 10.1093/nar/gkv1104
Su, A. I. et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl Acad. Sci. USA. 101, 6062–6067 (2004).
pubmed: 15075390 pmcid: 395923 doi: 10.1073/pnas.0400782101
Nummenmaa, L. et al. μ-opioid receptor system mediates reward processing in humans. Nat. Commun. 9, 1500 (2018).
pubmed: 29662095 pmcid: 5902580 doi: 10.1038/s41467-018-03848-y
Gilbert, J.-A. et al. The effect of tesofensine on appetite sensations. Obesity 20, 553–561 (2012).
pubmed: 21720440 doi: 10.1038/oby.2011.197
Balaz, M. et al. Inhibition of mevalonate pathway prevents adipocyte browning in mice and men by affecting protein prenylation. Cell Metab. 29, 901–916.e8 (2019).
pubmed: 30581121 doi: 10.1016/j.cmet.2018.11.017
Sekar, R. & Chow, B. K. C. Lipolytic actions of secretin in mouse adipocytes. J. Lipid Res. 55, 190–200 (2014).
pubmed: 24273196 pmcid: 3886658 doi: 10.1194/jlr.M038042
Butcher, R. W. & Carlson, L. A. Effects of secretin on fat mobilizing lipolysis and cyclic AMP levels in rat adipose tissue. Acta Physiol. Scand. 79, 559–563 (1970).
pubmed: 4319535 doi: 10.1111/j.1748-1716.1970.tb04758.x
Raiko, J. et al. Brown adipose tissue triglyceride content is associated with decreased insulin sensitivity, independently of age and obesity. Diabetes, Obes. Metab. 17, 516–519 (2015).
doi: 10.1111/dom.12433
U Din, M. et al. Human brown fat radiodensity indicates underlying tissue composition and systemic metabolic health. J. Clin. Endocrinol. Metab. 102, 2258–2267 (2017).
pubmed: 28368474 doi: 10.1210/jc.2016-2698
Yaney, G. C. & Corkey, B. E. Fatty acid metabolism and insulin secretion in pancreatic beta cells. Diabetologia 46, 1297–1312 (2003).
pubmed: 13680127 doi: 10.1007/s00125-003-1207-4
Stein, D. T. et al. The insulinotropic potency of fatty acids is influenced profoundly by their chain length and degree of saturation. J. Clin. Invest. 100, 398–403 (1997).
pubmed: 9218517 pmcid: 508203 doi: 10.1172/JCI119546
Afroze, S. et al. The physiological roles of secretin and its receptor. Ann. Transl. Med. 1, 29 (2013).
pubmed: 25332973 pmcid: 4200670
Broeders, E. P. M. et al. The bile acid chenodeoxycholic acid increases human brown adipose tissue activity. Cell Metab. 22, 418–426 (2015).
pubmed: 26235421 doi: 10.1016/j.cmet.2015.07.002
Amin, A., Dhillo, W. S. & Murphy, K. G. The central effects of thyroid hormones on appetite. J. Thyroid Res. 2011, 306510 (2011).
pubmed: 21687648 pmcid: 3112506 doi: 10.4061/2011/306510
Bianco, A. C. & Silva, J. E. Intracellular conversion of thyroxine to triiodothyronine is required for the optimal thermogenic function of brown adipose tissue. J. Clin. Invest. 79, 295–300 (1987).
pubmed: 3793928 pmcid: 424048 doi: 10.1172/JCI112798
Lahesmaa, M. et al. Hyperthyroidism increases brown fat metabolism in humans. J. Clin. Endocrinol. Metab. 99, E28–E35 (2014).
pubmed: 24152690 doi: 10.1210/jc.2013-2312
Bessesen, D. H. & Van Gaal, L. F. Progress and challenges in anti-obesity pharmacotherapy. Lancet Diabetes Endocrinol. 6, 237–248 (2018).
pubmed: 28919062 doi: 10.1016/S2213-8587(17)30236-X
van Ooijen, A. M. J., van Marken Lichtenbelt, W. D., van Steenhoven, A. A. & Westerterp, K. R. Seasonal changes in metabolic and temperature responses to cold air in humans. Physiol. Behav. 82, 545–553 (2004).
pubmed: 15276821 doi: 10.1016/j.physbeh.2004.05.001
Yoneshiro, T. et al. Recruited brown adipose tissue as an antiobesity agent in humans. J. Clin. Invest. 123, 3404–3408 (2013).
U.-Din, M. et al. Human brown adipose tissue [15O]O
Orava, J. et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 14, 272–279 (2011).
pubmed: 21803297 doi: 10.1016/j.cmet.2011.06.012
Patlak, C. S. & Blasberg, R. G. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J. Cereb. Blood Flow. Metab. 5, 584–590 (1985).
pubmed: 4055928 doi: 10.1038/jcbfm.1985.87
Virtanen, K. A. et al. Human adipose tissue glucose uptake determined using [18 F]-fluoro-deoxy-glucose ([18 F]FDG) and PET in combination with microdialysis. Diabetologia 44, 2171–2179 (2001).
pubmed: 11793018 doi: 10.1007/s001250100026
Peltoniemi, P. et al. Lumped constant for [18 F]fluorodeoxyglucose in skeletal muscles of obese and nonobese humans. Am. J. Physiol. Metab. 279, E1122–E1130 (2000).
Weir, J. B. & de, V. New methods for calculating metabolic rate with special reference to protein metabolism. J. Physiol. 109, 1–9 (1949).
pubmed: 15394301 pmcid: 1392602 doi: 10.1113/jphysiol.1949.sp004363
Meriläinen, P. T. Metabolic monitor. Int. J. Clin. Monit. Comput. 4, 167–177 (1987).
pubmed: 3116131 doi: 10.1007/BF02915904
Nummenmaa, L. et al. Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS ONE 7, e31089 (2012).
pubmed: 22319604 pmcid: 3272045 doi: 10.1371/journal.pone.0031089
Esteban, O. et al. fMRIPrep: a robust preprocessing pipeline for functional MRI. Nat. Methods https://doi.org/10.1038/s41592-018-0235-4 (2019).
Gorgolewski, K. et al. Nipype: A flexible, lightweight and extensible neuroimaging data processing framework in Python. Front. Neuroinform. https://doi.org/10.3389/fninf.2011.00013 (2011).
Tustison, N. J. et al. N4ITK: Improved N3 bias correction. IEEE Trans. Med. Imag. https://doi.org/10.1109/TMI.2010.2046908 (2010).
Dale, A. M., Fischl, B. & Sereno, M. I. Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage https://doi.org/10.1006/nimg.1998.0395 (1999).
Klein, A. et al. Mindboggling morphometry of human brains. PLoS Comput. Biol. https://doi.org/10.1371/journal.pcbi.1005350 (2017).
Fonov, V., Evans, A., McKinstry, R., Almli, C. & Collins, D. Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. Neuroimage https://doi.org/10.1016/s1053-8119(09)70884-5 (2009).
Avants, B. B., Epstein, C. L., Grossman, M. & Gee, J. C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. https://doi.org/10.1016/j.media.2007.06.004 (2008).
Zhang, Y., Brady, M. & Smith, S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imag. https://doi.org/10.1109/42.906424 (2001).
Cox, R. W. AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. https://doi.org/10.1006/cbmr.1996.0014 (1996).
Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage https://doi.org/10.1016/S1053-8119(02)91132-8 (2002).
Greve, D. N. & Fischl, B. Accurate and robust brain image alignment using boundary-based registration. Neuroimage https://doi.org/10.1016/j.neuroimage.2009.06.060 (2009).
Behzadi, Y., Restom, K., Liau, J. & Liu, T. T. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage https://doi.org/10.1016/j.neuroimage.2007.04.042 (2007).
Power, J. D. et al. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage https://doi.org/10.1016/j.neuroimage.2013.08.048 (2014).
Pruim, R. H. R. et al. ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage https://doi.org/10.1016/j.neuroimage.2015.02.064 (2015).
Flint, A., Raben, A., Blundell, J. E. & Astrup, A. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int. J. Obes. Relat. Metab. Disord. 24, 38–48 (2000).
pubmed: 10702749 doi: 10.1038/sj.ijo.0801083
Soininen, P. et al. High-throughput serum NMR metabonomics for cost-effective holistic studies on systemic metabolism. Analyst 134, 1781 (2009).
pubmed: 19684899 doi: 10.1039/b910205a
Li, Y., Fromme, T., Schweizer, S., Schöttl, T. & Klingenspor, M. Taking control over intracellular fatty acid levels is essential for the analysis of thermogenic function in cultured primary brown and brite/beige adipocytes. EMBO Rep. 15, 1069–1076 (2014).
pubmed: 25135951 pmcid: 4253847 doi: 10.15252/embr.201438775
Rosenthal, R. in The Handbook of Research Synthesis (eds Cooper, H. et al.) 231–244 (Russell Sage Foundation, 1994).
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B-Methodol. 57, 289–300 (1995).

Auteurs

Sanna Laurila (S)

Turku PET Centre, University of Turku, Turku, Finland.
Heart Center, Turku University Hospital, Turku, Finland.
Satakunta Central Hospital, Pori, Finland.

Lihua Sun (L)

Turku PET Centre, University of Turku, Turku, Finland.

Minna Lahesmaa (M)

Turku PET Centre, University of Turku, Turku, Finland.
Department of Internal Medicine, Jorvi Hospital, Helsinki University Hospital, Helsinki, Finland.

Katharina Schnabl (K)

Chair for Molecular Nutritional Medicine, Technical University of Munich, TUM School of Life Sciences, Freising, Germany.
EKFZ - Else Kröner Fresenius Center for Nutritional Medicine, Technical University of Munich, Freising, Germany.
ZIEL - Institute for Food & Health, Technical University of Munich, Freising, Germany.

Kirsi Laitinen (K)

Institute of Biomedicine, University of Turku, Turku, Finland.

Riku Klén (R)

Turku PET Centre, University of Turku, Turku, Finland.

Yongguo Li (Y)

Chair for Molecular Nutritional Medicine, Technical University of Munich, TUM School of Life Sciences, Freising, Germany.
EKFZ - Else Kröner Fresenius Center for Nutritional Medicine, Technical University of Munich, Freising, Germany.
ZIEL - Institute for Food & Health, Technical University of Munich, Freising, Germany.

Miroslav Balaz (M)

Institute of Food, Nutrition and Health, ETH Zürich, Schwerzenbach, Switzerland.

Christian Wolfrum (C)

Institute of Food, Nutrition and Health, ETH Zürich, Schwerzenbach, Switzerland.

Katja Steiger (K)

Institue of Pathology, School of Medicine, Technical University of Munich, Munich, Germany.

Tarja Niemi (T)

Department of Plastic and General Surgery, Turku University Hospital, Turku, Finland.

Markku Taittonen (M)

Department of Anesthesiology, Turku University Hospital, Turku, Finland.

Mueez U-Din (M)

Turku PET Centre, University of Turku, Turku, Finland.
Turku PET Centre, Turku University Hospital, Turku, Finland.

Tommi Välikangas (T)

Turku Bioscience Centre, University of Turku, Turku, Finland.

Laura L Elo (LL)

Institute of Biomedicine, University of Turku, Turku, Finland.
Turku Bioscience Centre, University of Turku, Turku, Finland.
Turku Bioscience Centre, Åbo Akademi University, Turku, Finland.

Olli Eskola (O)

Turku PET Centre, University of Turku, Turku, Finland.

Anna K Kirjavainen (AK)

Turku PET Centre, University of Turku, Turku, Finland.

Lauri Nummenmaa (L)

Turku PET Centre, University of Turku, Turku, Finland.
Department of Psychology, University of Turku, Turku, Finland.

Kirsi A Virtanen (KA)

Turku PET Centre, Turku University Hospital, Turku, Finland.
Institute of Public Health and Clinical Nutrition - University of Eastern Finland (UEF), Kuopio, Finland.
Department of Endocrinology and Clinical Nutrition, Kuopio University Hospital, Kuopio, Finland.

Martin Klingenspor (M)

Chair for Molecular Nutritional Medicine, Technical University of Munich, TUM School of Life Sciences, Freising, Germany.
EKFZ - Else Kröner Fresenius Center for Nutritional Medicine, Technical University of Munich, Freising, Germany.
ZIEL - Institute for Food & Health, Technical University of Munich, Freising, Germany.

Pirjo Nuutila (P)

Turku PET Centre, University of Turku, Turku, Finland. pirjo.nuutila@utu.fi.
Turku PET Centre, Turku University Hospital, Turku, Finland. pirjo.nuutila@utu.fi.
Department of Endocrinology, Turku University Hospital, Turku, Finland. pirjo.nuutila@utu.fi.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH