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Article ; Online: The role of autophagy in brown and beige adipose tissue plasticity.

Cairó, Montserrat / Villarroya, Joan

2019 Volume 76, Issue 2, Page(s) 213–226

Abstract: Since the rediscovery of active brown and beige adipose tissues in humans a decade ago, great efforts have been made to identify the mechanisms underlying the activation and inactivation of these tissues, with the hope of designing potential strategies ... ...

Abstract	Since the rediscovery of active brown and beige adipose tissues in humans a decade ago, great efforts have been made to identify the mechanisms underlying the activation and inactivation of these tissues, with the hope of designing potential strategies to fight against obesity and associated metabolic disorders such as type 2 diabetes. Active brown/beige fat increases the energy expenditure and is associated with reduced hyperglycemia and hyperlipidemia, whereas its atrophy and inactivation have been associated with obesity and aging. Autophagy, which is the process by which intracellular components are degraded within the lysosomes, has recently emerged as an important regulatory mechanism of brown/beige fat plasticity. Studies have shown that autophagy participates in the intracellular remodeling events that occur during brown/beige adipogenesis, thermogenic activation, and inactivation. The autophagic degradation of mitochondria appears to be important for the inactivation of brown fat and the transition from beige-to-white adipose tissue. Moreover, autophagic dysregulation in adipose tissues has been associated with obesity. Thus, understanding the regulatory mechanisms that control autophagy in the physiology and pathophysiology of adipose tissues might suggest novel treatments against obesity and its associated metabolic diseases.
MeSH term(s)	Adipogenesis ; Adipose Tissue, Beige/cytology ; Adipose Tissue, Beige/metabolism ; Adipose Tissue, Beige/pathology ; Adipose Tissue, Brown/cytology ; Adipose Tissue, Brown/metabolism ; Adipose Tissue, Brown/pathology ; Animals ; Autophagy ; Humans ; Metabolic Diseases/metabolism ; Mitochondria/metabolism ; Obesity/metabolism ; Thermogenesis
Language	English
Publishing date	2019-12-06
Publishing country	Spain
Document type	Journal Article ; Review
ZDB-ID	1325104-1
ISSN	1877-8755 ; 0034-9402 ; 1138-7548
ISSN (online)	1877-8755
ISSN	0034-9402 ; 1138-7548
DOI	10.1007/s13105-019-00708-1
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Article ; Online: Parkin depletion prevents the age-related alterations in the FGF21 system and the decline in white adipose tissue thermogenic function in mice.

Delgado-Anglés, Alejandro / Blasco-Roset, Albert / Godoy-Nieto, Francisco J / Cairó, Montserrat / Villarroya, Francesc / Giralt, Marta / Villarroya, Joan

Journal of physiology and biochemistry

2023 Volume 80, Issue 1, Page(s) 41–51

Abstract: Parkin is an ubiquitin-E3 ligase that is involved in cellular mitophagy and was recently shown to contribute to controlling adipose tissue thermogenic plasticity. We found that Parkin expression is induced in brown (BAT) and white (WAT) adipose tissues ... ...

Abstract	Parkin is an ubiquitin-E3 ligase that is involved in cellular mitophagy and was recently shown to contribute to controlling adipose tissue thermogenic plasticity. We found that Parkin expression is induced in brown (BAT) and white (WAT) adipose tissues of aged mice. We determined the potential role of Parkin in the aging-associated decline in the thermogenic capacity of adipose tissues by analyzing subcutaneous WAT, interscapular BAT, and systemic metabolic and physiological parameters in young (5 month-old) and aged (16 month-old) mice with targeted invalidation of the Parkin (Park2) gene, and their wild-type littermates. Our data indicate that suppression of Parkin prevented adipose accretion, increased energy expenditure and improved the systemic metabolic derangements, such as insulin resistance, seen in aged mice. This was associated with maintenance of browning and reduction of the age-associated induction of inflammation in subcutaneous WAT. BAT in aged mice was much less affected by Parkin gene invalidation. Such protection was associated with a dramatic prevention of the age-associated induction of fibroblast growth factor-21 (FGF21) levels in aged Parkin-invalidated mice. This was associated with a parallel reduction in FGF21 gene expression in adipose tissues and liver in aged Parkin-invalidated mice. Additionally, Parkin invalidation prevented the protein down-regulation of β-Klotho (a key co-receptor mediating FGF21 responsiveness in tissues) in aged adipose tissues. We conclude that Parkin down-regulation leads to improved systemic metabolism in aged mice, in association with maintenance of adipose tissue browning and FGF21 system functionality.
MeSH term(s)	Animals ; Mice ; Adipose Tissue/metabolism ; Adipose Tissue, Brown/metabolism ; Adipose Tissue, White/metabolism ; Fibroblast Growth Factors/genetics ; Fibroblast Growth Factors/metabolism ; Thermogenesis ; Ubiquitin-Protein Ligases/genetics ; Ubiquitin-Protein Ligases/metabolism
Chemical Substances	fibroblast growth factor 21 ; Fibroblast Growth Factors (62031-54-3) ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; parkin protein (EC 2.3.2.27)
Language	English
Publishing date	2023-11-02
Publishing country	Spain
Document type	Journal Article
ZDB-ID	1325104-1
ISSN	1877-8755 ; 0034-9402 ; 1138-7548
ISSN (online)	1877-8755
ISSN	0034-9402 ; 1138-7548
DOI	10.1007/s13105-023-00977-x
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Article: Secretory Proteome of Brown Adipocytes in Response to cAMP-Mediated Thermogenic Activation.

Villarroya, Joan / Cereijo, Rubén / Giralt, Marta / Villarroya, Francesc

Frontiers in physiology

2019 Volume 10, Page(s) 67

Abstract: Background: ...

Abstract	Background:
Language	English
Publishing date	2019-02-07
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2019.00067
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Article: A Differential Pattern of Batokine Expression in Perivascular Adipose Tissue Depots From Mice.

Mestres-Arenas, Alberto / Villarroya, Joan / Giralt, Marta / Villarroya, Francesc / Peyrou, Marion

Frontiers in physiology

2021 Volume 12, Page(s) 714530

Abstract: Depending on its anatomical placement, perivascular adipose tissue (PVAT) has been found to possess features more (e.g., aortic thoracic) or less (e.g., aortic abdominal) similar to brown/beige adipose tissue in mice, whereas PVAT surrounding the ... ...

Abstract	Depending on its anatomical placement, perivascular adipose tissue (PVAT) has been found to possess features more (e.g., aortic thoracic) or less (e.g., aortic abdominal) similar to brown/beige adipose tissue in mice, whereas PVAT surrounding the mesenteric arteries and the caudal part of abdominal aorta is similar to white fat. PVAT is thought to influence vascular function through the effects of adipose-secreted molecules on vessels. Brown adipose tissue was recently shown to play differential secretory role
Language	English
Publishing date	2021-08-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2021.714530
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Article ; Online: The endocrine role of brown adipose tissue: An update on actors and actions.

Gavaldà-Navarro, Aleix / Villarroya, Joan / Cereijo, Rubén / Giralt, Marta / Villarroya, Francesc

Reviews in endocrine & metabolic disorders

2021 Volume 23, Issue 1, Page(s) 31–41

Abstract: In recent years, brown adipose tissue (BAT) has been recognized not only as a main site of non-shivering thermogenesis in mammals, but also as an endocrine organ. BAT secretes a myriad of regulatory factors. These so-called batokines exert local ... ...

Abstract	In recent years, brown adipose tissue (BAT) has been recognized not only as a main site of non-shivering thermogenesis in mammals, but also as an endocrine organ. BAT secretes a myriad of regulatory factors. These so-called batokines exert local autocrine and paracrine effects, as well as endocrine actions targeting tissues and organs at a distance. The endocrine batokines include peptide factors, such as fibroblast growth factor-21 (FGF21), neuregulin-4 (NRG4), phospholipid transfer protein (PLTP), interleukin-6, adiponectin and myostatin, and also lipids (lipokines; e.g., 12,13-dihydroxy-9Z-octadecenoic acid [12,13-diHOME]) and miRNAs (e.g., miR-99b). The liver, heart, and skeletal muscle are the most commonly reported targets of batokines. In response to BAT thermogenic activation, batokines such as NRG4 and PLTP are released and act to reduce hepatic steatosis and improve insulin sensitivity. Stress-induced interleukin-6-mediated signaling from BAT to liver favors hepatic glucose production through enhanced gluconeogenesis. Batokines may act on liver to induce the secretion of regulatory hepatokines (e.g. FGF21 and bile acids in response to miR-99b and PLTP, respectively), thereby resulting in a systemic expansion of BAT-originating signals. Batokines also target extrahepatic tissues: FGF21 and 12,13-diHOME are cardioprotective, whereas BAT-secreted myostatin and 12,13-diHOME influence skeletal muscle development and performance. Further research is needed to ascertain in humans the role of batokines, which have been identified mostly in experimental models. The endocrine role of BAT may explain the association between active BAT and a healthy metabolism in the human system, which is characterized by small amounts of BAT and a likely moderate BAT-mediated energy expenditure.
MeSH term(s)	Adipose Tissue, Brown/metabolism ; Animals ; Endocrine System ; Energy Metabolism/physiology ; Humans ; Insulin Resistance ; Thermogenesis/physiology
Language	English
Publishing date	2021-03-12
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2185718-0
ISSN	1573-2606 ; 1389-9155
ISSN (online)	1573-2606
ISSN	1389-9155
DOI	10.1007/s11154-021-09640-6
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Article ; Online: Brown adipose tissue as a secretory organ.

Villarroya, Francesc / Cereijo, Rubén / Villarroya, Joan / Giralt, Marta

Nature reviews. Endocrinology

2017 Volume 13, Issue 1, Page(s) 26–35

Abstract: Brown adipose tissue (BAT) is the main site of adaptive thermogenesis and experimental studies have associated BAT activity with protection against obesity and metabolic diseases, such as type 2 diabetes mellitus and dyslipidaemia. Active BAT is present ... ...

Abstract	Brown adipose tissue (BAT) is the main site of adaptive thermogenesis and experimental studies have associated BAT activity with protection against obesity and metabolic diseases, such as type 2 diabetes mellitus and dyslipidaemia. Active BAT is present in adult humans and its activity is impaired in patients with obesity. The ability of BAT to protect against chronic metabolic disease has traditionally been attributed to its capacity to utilize glucose and lipids for thermogenesis. However, BAT might also have a secretory role, which could contribute to the systemic consequences of BAT activity. Several BAT-derived molecules that act in a paracrine or autocrine manner have been identified. Most of these factors promote hypertrophy and hyperplasia of BAT, vascularization, innervation and blood flow, processes that are all associated with BAT recruitment when thermogenic activity is enhanced. Additionally, BAT can release regulatory molecules that act on other tissues and organs. This secretory capacity of BAT is thought to be involved in the beneficial effects of BAT transplantation in rodents. Fibroblast growth factor 21, IL-6 and neuregulin 4 are among the first BAT-derived endocrine factors to be identified. In this Review, we discuss the current understanding of the regulatory molecules (the so-called brown adipokines or batokines) that are released by BAT that influence systemic metabolism and convey the beneficial metabolic effects of BAT activation. The identification of such adipokines might also direct drug discovery approaches for managing obesity and its associated chronic metabolic diseases.
MeSH term(s)	Adipocytes, Brown/metabolism ; Adipocytes, Brown/secretion ; Adipokines/metabolism ; Adipokines/secretion ; Adipose Tissue, Brown/metabolism ; Adipose Tissue, Brown/secretion ; Animals ; Energy Metabolism/physiology ; Humans ; Obesity/metabolism
Chemical Substances	Adipokines
Language	English
Publishing date	2017-01
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2489381-X
ISSN	1759-5037 ; 1759-5029
ISSN (online)	1759-5037
ISSN	1759-5029
DOI	10.1038/nrendo.2016.136
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Article ; Online: Author Correction: The relative deficit of GDF15 in adolescent girls with PCOS can be changed into an abundance that reduces liver fat.

de Zegher, Francis / Díaz, Marta / Villarroya, Joan / Cairó, Montserrat / López-Bermejo, Abel / Villarroya, Francesc / Ibáñez, Lourdes

Scientific reports

2021 Volume 11, Issue 1, Page(s) 20412

Language	English
Publishing date	2021-10-08
Publishing country	England
Document type	Published Erratum
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-99918-1
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Article ; Online: The relative deficit of GDF15 in adolescent girls with PCOS can be changed into an abundance that reduces liver fat.

de Zegher, Francis / Díaz, Marta / Villarroya, Joan / Cairó, Montserrat / López-Bermejo, Abel / Villarroya, Francesc / Ibáñez, Lourdes

Scientific reports

2021 Volume 11, Issue 1, Page(s) 7018

Abstract: A prime concern of young patients with Polycystic Ovary Syndrome (PCOS) is the control of body adiposity, given their tendency to gain weight and/or their difficulty to lose weight. Circulating growth-and-differentiation factor-15 (GDF15) facilitates the ...

Abstract	A prime concern of young patients with Polycystic Ovary Syndrome (PCOS) is the control of body adiposity, given their tendency to gain weight and/or their difficulty to lose weight. Circulating growth-and-differentiation factor-15 (GDF15) facilitates the control of body weight via receptors in the brainstem. C-reactive protein (CRP) and insulin are endogenous GDF15 secretagogues. We hypothesised that PCOS in non-obese adolescents is characterised by low concentrations of circulating GDF15, when judged by the degree of CRP and insulin drive. GDF15 was added as a post-hoc endpoint of two previously reported, randomised studies in non-obese adolescent girls with PCOS (N = 58; 60% normal weight; 40% overweight) who received either an oral oestroprogestogen contraceptive (OC), or a low-dose combination of spironolactone-pioglitazone-metformin (SPIOMET) for 1 year; subsequently, all girls remained untreated for 1 year. Adolescent girls with regular menses (N = 20) served as healthy controls. Circulating GDF15, CRP and fasting insulin were assessed prior to treatment, and halfway the on- and post-treatment years. Pre-treatment, the absolute GDF15 concentrations were normal in PCOS girls, but their relative levels were markedly low, in view of the augmented CRP and insulin drives. OC treatment was accompanied by a near-doubling of circulating GDF15 (on average, from 296 to 507 pg/mL) and CRP, so that the relative GDF15 levels remained low. SPIOMET treatment was accompanied by a 3.4-fold rise of circulating GDF15 (on average, from 308 to 1045 pg/mL) and by a concomitant lowering of CRP and insulin concentrations towards normal, so that the relative GDF15 levels became markedly abundant. Post-OC, the relatively low GDF15 levels persisted; post-SPIOMET, the circulating concentrations of GDF15, CRP and insulin were all normal. BMI remained stable in both treatment groups. Only SPIOMET was accompanied by a reduction of hepato-visceral fat (by MRI) towards normal. In conclusion, early PCOS was found to be characterised by a relative GDF15 deficit that may partly explain the difficulties that young patients experience to control their body adiposity. This relative GDF15 deficit persisted during and after OC treatment. In contrast, SPIOMET treatment was accompanied by an absolute and a relative abundance of GDF15, and followed by normal GDF15, CRP and insulin concentrations. The present findings strengthen the rationale to raise the concentrations of circulating GDF15 in early PCOS, for example with a SPIOMET-like intervention that attenuates low-grade inflammation, insulin resistance and ectopic adiposity, without necessarily lowering body weight.Clinical trial registries: ISRCTN29234515 and ISRCTN11062950.
MeSH term(s)	Adolescent ; Adult ; Case-Control Studies ; Child ; Fatty Liver/etiology ; Fatty Liver/pathology ; Fatty Liver/prevention & control ; Female ; Growth Differentiation Factor 15/deficiency ; Humans ; Hypoglycemic Agents/therapeutic use ; Male ; Metformin/therapeutic use ; Mineralocorticoid Receptor Antagonists/therapeutic use ; Pioglitazone/therapeutic use ; Polycystic Ovary Syndrome/complications ; Polycystic Ovary Syndrome/drug therapy ; Polycystic Ovary Syndrome/metabolism ; Spironolactone/therapeutic use ; Young Adult
Chemical Substances	GDF15 protein, human ; Growth Differentiation Factor 15 ; Hypoglycemic Agents ; Mineralocorticoid Receptor Antagonists ; Spironolactone (27O7W4T232) ; Metformin (9100L32L2N) ; Pioglitazone (X4OV71U42S)
Language	English
Publishing date	2021-03-29
Publishing country	England
Document type	Journal Article ; Randomized Controlled Trial ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-86317-9
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Article ; Online: Circulating diazepam-binding inhibitor in infancy: Relation to markers of adiposity and metabolic health.

Díaz, Marta / Blasco-Roset, Albert / Villarroya, Joan / López-Bermejo, Abel / de Zegher, Francis / Villarroya, Francesc / Ibáñez, Lourdes

Pediatric obesity

2021 Volume 16, Issue 11, Page(s) e12802

Abstract: Background: Diazepam-binding inhibitor (DBI) controls feeding behaviour and glucose homeostasis. Individuals born small-for-gestational-age (SGA) with excessive postnatal catch-up in weight are at risk for obesity and type 2 diabetes.: Objective: To ... ...

Abstract	Background: Diazepam-binding inhibitor (DBI) controls feeding behaviour and glucose homeostasis. Individuals born small-for-gestational-age (SGA) with excessive postnatal catch-up in weight are at risk for obesity and type 2 diabetes. Objective: To assess serum concentrations of DBI (0-2 years) in appropriate-for-gestational-age (AGA, n = 70) vs SGA infants (n = 33) with spontaneous catch-up and their relationship with endocrine-metabolic and adiposity markers. Methods: Longitudinal assessments included auxology, fasting glucose, insulin, insulin-like growth factor, high-molecular-weight adiponectin, DBI and body composition (absorptiometry). DBI was measured cross-sectionally in pregnant and non-pregnant women and in 2-day-old newborns. DBI mRNA expression levels were assessed in adult and neonatal tissues. Results: Cord blood DBI concentrations were similar in AGA and SGA newborns and about fivefold higher than those in women. Serum DBI levels decreased by age 2 days, were higher in SGA vs AGA infants at age 2 years and associated negatively with markers of adiposity and insulin resistance and positively with high-molecular-weight adiponectin. DBI mRNA expression was lower in placenta than in other tissues. Conclusion: The increased DBI concentrations at birth are unrelated to prenatal growth. The higher DBI levels in SGA subjects at age 2 years may be related to catch-up growth or represent an adaptive mechanism to promote lipogenesis.
MeSH term(s)	Adiposity ; Child, Preschool ; Diabetes Mellitus, Type 2 ; Diazepam ; Diazepam Binding Inhibitor ; Humans ; Infant, Newborn ; Obesity
Chemical Substances	Diazepam Binding Inhibitor ; Diazepam (Q3JTX2Q7TU)
Language	English
Publishing date	2021-05-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2655527-X
ISSN	2047-6310 ; 2047-6302
ISSN (online)	2047-6310
ISSN	2047-6302
DOI	10.1111/ijpo.12802
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Article ; Online: New insights into the secretory functions of brown adipose tissue.

Villarroya, Joan / Cereijo, Rubén / Gavaldà-Navarro, Aleix / Peyrou, Marion / Giralt, Marta / Villarroya, Francesc

The Journal of endocrinology

2019 Volume 243, Issue 2, Page(s) R19–R27

Abstract: In recent years, an important secretory role of brown adipose tissue (BAT) has emerged, which is consistent, to some extent, with the earlier recognition of the important secretory role of white fat. The so-called brown adipokines or 'batokines' may play ...

Abstract	In recent years, an important secretory role of brown adipose tissue (BAT) has emerged, which is consistent, to some extent, with the earlier recognition of the important secretory role of white fat. The so-called brown adipokines or 'batokines' may play an autocrine role, which may either be positive or negative, in the thermogenic function of brown adipocytes. Additionally, there is a growing recognition of the signalling molecules released by brown adipocytes that target sympathetic nerve endings (such as neuregulin-4 and S100b protein), vascular cells (e.g., bone morphogenetic protein-8b), and immune cells (e.g., C-X-C motif chemokine ligand-14) to promote the tissue remodelling associated with the adaptive BAT recruitment in response to thermogenic stimuli. Moreover, existing indications of an endocrine role of BAT are being confirmed through the release of brown adipokines acting on other distant tissues and organs; a recent example is the recognition that BAT-secreted fibroblast growth factor-21 and myostatin target the heart and skeletal muscle, respectively. The application of proteomics technologies is aiding the identification of new members of the brown adipocyte secretome, such as the extracellular matrix or complement system components. In summary, BAT can no longer be considered a mere producer of heat in response to environment or dietary challenges; it is also an active secretory tissue releasing brown adipokines with a relevant local and systemic action. The identification of the major brown adipokines and their roles is highly important for the discovery of novel candidates useful in formulating intervention strategies for metabolic diseases.
MeSH term(s)	Adipocytes, Brown/metabolism ; Adipokines/metabolism ; Adipose Tissue, Brown/cytology ; Adipose Tissue, Brown/metabolism ; Animals ; Autocrine Communication/physiology ; Energy Metabolism/physiology ; Fibroblast Growth Factors/metabolism ; Humans ; Metabolic Diseases/diagnosis ; Metabolic Diseases/physiopathology ; Metabolic Diseases/therapy ; Thermogenesis/physiology
Chemical Substances	Adipokines ; fibroblast growth factor 21 ; Fibroblast Growth Factors (62031-54-3)
Language	English
Publishing date	2019-07-31
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	3028-4
ISSN	1479-6805 ; 0022-0795
ISSN (online)	1479-6805
ISSN	0022-0795
DOI	10.1530/JOE-19-0295
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