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Article ; Online: Rethinking succinate: an unexpected hormone-like metabolite in energy homeostasis.

Fernández-Veledo, Sonia / Ceperuelo-Mallafré, Victòria / Vendrell, Joan

Trends in endocrinology and metabolism: TEM

2021 Volume 32, Issue 9, Page(s) 680–692

Abstract: There has been an explosion of interest in the signaling capacity of energy metabolites. A prime example is the Krebs cycle substrate succinate, an archetypal respiratory substrate with functions beyond energy production as an intracellular and ... ...

Abstract	There has been an explosion of interest in the signaling capacity of energy metabolites. A prime example is the Krebs cycle substrate succinate, an archetypal respiratory substrate with functions beyond energy production as an intracellular and extracellular signaling molecule. Long associated with inflammation, emerging evidence supports a key role for succinate in metabolic processes relating to energy management. As the natural ligand for SUCNR1, a G protein-coupled receptor, succinate is akin to hormones and likely functions as a reporter of metabolism and stress. In this review, we reconcile new and old observations to outline a regulatory role for succinate in metabolic homeostasis. We highlight the importance of the succinate-SUCNR1 axis in metabolic diseases as an integrator of macrophage immune response, and we discuss new metabolic functions recently ascribed to succinate in specific tissues. Because circulating succinate has emerged as a promising biomarker in chronic metabolic diseases, a better understanding of the physiopathological role of the succinate-SUCNR1 axis in metabolism might open new avenues for clinical use in patients with obesity or diabetes.
MeSH term(s)	Animals ; Energy Metabolism ; Homeostasis ; Humans ; Receptors, G-Protein-Coupled ; Succinic Acid
Chemical Substances	Receptors, G-Protein-Coupled ; Succinic Acid (AB6MNQ6J6L)
Language	English
Publishing date	2021-07-20
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1042384-9
ISSN	1879-3061 ; 1043-2760
ISSN (online)	1879-3061
ISSN	1043-2760
DOI	10.1016/j.tem.2021.06.003
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Zs.A 2999: Show issues

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Article ; Online: Survivin/BIRC5 as a novel molecular effector at the crossroads of glucose metabolism and radioresistance in head and neck squamous cell carcinoma.

Benaiges, Ester / Ceperuelo-Mallafré, Victòria / Guaita, Sandra / Maymó-Masip, Elsa / Madeira, Ana / Gómez, David / Hernández, Victor / Vilaseca, Isabel / Merma, Carla / León, Xavier / Terra, Ximena / Vendrell, Joan / Avilés-Jurado, Francesc Xavier / Fernández-Veledo, Sonia

Head & neck

2024

Abstract: Background: Metabolic reprogramming and abnormal glucose metabolism are hallmarks of head and neck squamous cell carcinoma (HNSCC). Certain oncogenes can promote cancer-related metabolic changes, but understanding their crosstalk in HNSCC biology and ... ...

Abstract	Background: Metabolic reprogramming and abnormal glucose metabolism are hallmarks of head and neck squamous cell carcinoma (HNSCC). Certain oncogenes can promote cancer-related metabolic changes, but understanding their crosstalk in HNSCC biology and treatment is essential for identifying predictive biomarkers and developing target therapies. Methods: We assessed the value of survivin/BIRC5 as a radioresistance factor potentially modulated by glucose for predicting therapeutic sensitivity and prognosis of HNSCC in a cohort of 32 patients. Additionally, we conducted in vitro experiments to explore the role of survivin/BIRC5 in glucose metabolism concerning radiation response. Results: Tumoral BIRC5 expression is associated with serum glucose and predicts locoregional disease-free survival and lower BIRC5 mRNA levels are associated with better outcomes. Upregulation of BIRC5 by radiation depends on glucose levels and provokes a pro-tumoral and radioresistant phenotype in surviving cells. Conclusions: Survivin/BIRC5 might be independently associated with the risk of recurrence in patients with HNSCC.
Language	English
Publishing date	2024-02-02
Publishing country	United States
Document type	Journal Article
ZDB-ID	645165-2
ISSN	1097-0347 ; 0148-6403 ; 1043-3074
ISSN (online)	1097-0347
ISSN	0148-6403 ; 1043-3074
DOI	10.1002/hed.27651
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Zs.A 1493: Show issues

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Article ; Online: Circulating pyruvate is a potent prognostic marker for critical COVID-19 outcomes.

Ceperuelo-Mallafré, Victòria / Reverté, Laia / Peraire, Joaquim / Madeira, Ana / Maymó-Masip, Elsa / López-Dupla, Miguel / Gutierrez-Valencia, Alicia / Ruiz-Mateos, Ezequiel / Buzón, Maria José / Jorba, Rosa / Vendrell, Joan / Auguet, Teresa / Olona, Montserrat / Vidal, Francesc / Rull, Anna / Fernández-Veledo, Sonia

Frontiers in immunology

2022 Volume 13, Page(s) 912579

Abstract: Background: Coronavirus-19 (COVID-19) disease is driven by an unchecked immune response to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus which alters host mitochondrial-associated mechanisms. Compromised mitochondrial health ... ...

Abstract	Background: Coronavirus-19 (COVID-19) disease is driven by an unchecked immune response to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus which alters host mitochondrial-associated mechanisms. Compromised mitochondrial health results in abnormal reprogramming of glucose metabolism, which can disrupt extracellular signalling. We hypothesized that examining mitochondrial energy-related signalling metabolites implicated in host immune response to SARS-CoV-2 infection would provide potential biomarkers for predicting the risk of severe COVID-19 illness. Methods: We used a semi-targeted serum metabolomics approach in 273 patients with different severity grades of COVID-19 recruited at the acute phase of the infection to determine the relative abundance of tricarboxylic acid (Krebs) cycle-related metabolites with known extracellular signaling properties (pyruvate, lactate, succinate and α-ketoglutarate). Abundance levels of energy-related metabolites were evaluated in a validation cohort (n=398) using quantitative fluorimetric assays. Results: Increased levels of four energy-related metabolites (pyruvate, lactate, a-ketoglutarate and succinate) were found in critically ill COVID-19 patients using semi-targeted and targeted approaches (p<0.05). The combined strategy proposed herein enabled us to establish that circulating pyruvate levels (p<0.001) together with body mass index (p=0.025), C-reactive protein (p=0.039), D-Dimer (p<0.001) and creatinine (p=0.043) levels, are independent predictors of critical COVID-19. Furthermore, classification and regression tree (CART) analysis provided a cut-off value of pyruvate in serum (24.54 µM; p<0.001) as an early criterion to accurately classify patients with critical outcomes. Conclusion: Our findings support the link between COVID-19 pathogenesis and immunometabolic dysregulation, and show that fluorometric quantification of circulating pyruvate is a cost-effective clinical decision support tool to improve patient stratification and prognosis prediction.
MeSH term(s)	Biomarkers ; C-Reactive Protein ; COVID-19 ; Creatinine ; Glucose ; Humans ; Ketoglutaric Acids ; Lactates ; Prognosis ; Pyruvic Acid ; SARS-CoV-2 ; Succinates ; Tricarboxylic Acids
Chemical Substances	Biomarkers ; Ketoglutaric Acids ; Lactates ; Succinates ; Tricarboxylic Acids ; Pyruvic Acid (8558G7RUTR) ; C-Reactive Protein (9007-41-4) ; Creatinine (AYI8EX34EU) ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2022-09-14
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.912579
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Article ; Online: Impaired Succinate Response to a Mixed Meal in Obesity and Type 2 Diabetes Is Normalized After Metabolic Surgery.

Astiarraga, Brenno / Martínez, Laia / Ceperuelo-Mallafré, Victoria / Llauradó, Gemma / Terrón-Puig, Margarida / Rodríguez, M Mar / Casajoana, Anna / Pellitero, Silvia / Megía, Ana / Vilarrasa, Núria / Vendrell, Joan / Fernández-Veledo, Sonia

Diabetes care

2020 Volume 43, Issue 10, Page(s) 2581–2587

Abstract: Objective: To explore the meal response of circulating succinate in patients with obesity and type 2 diabetes undergoing bariatric surgery and to examine the role of gastrointestinal glucose sensing in succinate dynamics in healthy subjects.: Research ...

Abstract	Objective: To explore the meal response of circulating succinate in patients with obesity and type 2 diabetes undergoing bariatric surgery and to examine the role of gastrointestinal glucose sensing in succinate dynamics in healthy subjects. Research design and methods: Cohort I comprised 45 patients with morbid obesity and type 2 diabetes (BMI 39.4 ± 1.9 kg/m Results: In cohort I, succinate response to MTT at follow-up was greater than before the intervention ( Conclusions: The meal-related response of circulating succinate in patients with obesity and type 2 diabetes is recovered after metabolic surgery.
MeSH term(s)	Adult ; Aged ; Bariatric Surgery ; Blood Glucose/metabolism ; Cohort Studies ; Diabetes Mellitus, Type 2/blood ; Diabetes Mellitus, Type 2/complications ; Diabetes Mellitus, Type 2/surgery ; Diagnostic Techniques, Endocrine/standards ; Eating/physiology ; Female ; Follow-Up Studies ; Glucose Tolerance Test ; Humans ; Insulin/blood ; Male ; Meals ; Middle Aged ; Obesity, Morbid/blood ; Obesity, Morbid/complications ; Obesity, Morbid/surgery ; Reference Values ; Succinic Acid/blood ; Succinic Acid/standards ; Young Adult
Chemical Substances	Blood Glucose ; Insulin ; Succinic Acid (AB6MNQ6J6L)
Language	English
Publishing date	2020-07-31
Publishing country	United States
Document type	Journal Article ; Multicenter Study ; Randomized Controlled Trial ; Research Support, Non-U.S. Gov't
ZDB-ID	441231-x
ISSN	1935-5548 ; 0149-5992
ISSN (online)	1935-5548
ISSN	0149-5992
DOI	10.2337/dc20-0460
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Zs.A 1434: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
Zs.MO 365: Show issues

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Article: Succinate Pathway in Head and Neck Squamous Cell Carcinoma: Potential as a Diagnostic and Prognostic Marker.

Terra, Ximena / Ceperuelo-Mallafré, Victoria / Merma, Carla / Benaiges, Ester / Bosch, Ramon / Castillo, Paola / Flores, Joan Carles / León, Xavier / Valduvieco, Izaskun / Basté, Neus / Cámara, Marina / Lejeune, Marylène / Gumà, Josep / Vendrell, Joan / Vilaseca, Isabel / Fernández-Veledo, Sonia / Avilés-Jurado, Francesc Xavier

Cancers

2021 Volume 13, Issue 7

Abstract: Head and neck squamous cell carcinoma (HNSCC) is characterized by high rates of mortality and treatment-related morbidity, underscoring the urgent need for innovative and safe treatment strategies and diagnosis practices. Mitochondrial dysfunction is a ... ...

Abstract	Head and neck squamous cell carcinoma (HNSCC) is characterized by high rates of mortality and treatment-related morbidity, underscoring the urgent need for innovative and safe treatment strategies and diagnosis practices. Mitochondrial dysfunction is a hallmark of cancer and can lead to the accumulation of tricarboxylic acid cycle intermediates, such as succinate, which function as oncometabolites. In addition to its role in cancer development through epigenetic events, succinate is an extracellular signal transducer that modulates immune response, angiogenesis and cell invasion by activating its cognate receptor SUCNR1. Here, we explored the potential value of the circulating succinate and related genes in HNSCC diagnosis and prognosis. We determined the succinate levels in the serum of 66 pathologically confirmed, untreated patients with HNSCC and 20 healthy controls. We also surveyed the expression of the genes related to succinate metabolism and signaling in tumoral and nontumoral adjacent tissue and in normal mucosa from 50 patients. Finally, we performed immunohistochemical analysis of SUCNR1 in mucosal samples. The results showed that the circulating levels of succinate were higher in patients with HNSCC than in the healthy controls. Additionally, the expression of SUCNR1, HIF-1α, succinate dehydrogenase (SDH) A, and SDHB was higher in the tumor tissue than in the matched normal mucosa. Consistent with this, immunohistochemical analysis revealed an increase in SUCNR1 protein expression in tumoral and nontumoral adjacent tissue. High SUCNR1 and SDHA expression levels were associated with poor locoregional control, and the locoregional recurrence-free survival rate was significantly lower in patients with high SUCNR1 and SDHA expression than in their peers with lower levels (77.1% [95% CI: 48.9-100.0] vs. 16.7% [95% CI: 0.0-44.4],
Language	English
Publishing date	2021-04-01
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers13071653
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Article ; Online: Changes in glucagon-like peptide 1 and 2 levels in people with obesity after a diet-induced weight-loss intervention are related to a specific microbiota signature: A prospective cohort study.

Rodríguez-Peña, M-Mar / Astiarraga, Brenno / Seco, Jesus / Ceperuelo-Mallafré, Victoria / Caballé, Adrià / Pérez-Brocal, Vicente / Attolini, Camille Stephan-Otto / Moya, Andrés / Llauradó, Gemma / Megía, Ana / Pellitero, Silvia / Vilarrasa, Núria / Fernández-Veledo, Sonia / Vendrell, Joan

Clinical and translational medicine

2021 Volume 11, Issue 11, Page(s) e575

MeSH term(s)	Adult ; Cohort Studies ; Female ; Glucagon-Like Peptide 1/metabolism ; Glucagon-Like Peptide 1/pharmacology ; Glucagon-Like Peptide 1/therapeutic use ; Glucagon-Like Peptide 2/metabolism ; Glucagon-Like Peptide 2/pharmacology ; Glucagon-Like Peptide 2/therapeutic use ; Humans ; Male ; Microbiota/drug effects ; Microbiota/physiology ; Middle Aged ; Obesity/diet therapy ; Obesity/drug therapy ; Prospective Studies ; Weight Reduction Programs/methods ; Weight Reduction Programs/standards ; Weight Reduction Programs/statistics & numerical data
Chemical Substances	Glucagon-Like Peptide 2 ; Glucagon-Like Peptide 1 (89750-14-1)
Language	English
Publishing date	2021-11-28
Publishing country	United States
Document type	Letter ; Research Support, Non-U.S. Gov't
ZDB-ID	2697013-2
ISSN	2001-1326 ; 2001-1326
ISSN (online)	2001-1326
ISSN	2001-1326
DOI	10.1002/ctm2.575
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Article ; Online: Effects of stem cells from inducible brown adipose tissue on diet-induced obesity in mice.

Calvo, Enrique / Keiran, Noelia / Núñez-Roa, Catalina / Maymó-Masip, Elsa / Ejarque, Miriam / Sabadell-Basallote, Joan / Del Mar Rodríguez-Peña, María / Ceperuelo-Mallafré, Victòria / Seco, Jesús / Benaiges, Ester / Michalopoulou, Theodora / Jorba, Rosa / Vendrell, Joan / Fernández-Veledo, Sonia

Scientific reports

2021 Volume 11, Issue 1, Page(s) 13923

Abstract: Adipose-derived mesenchymal stem cells (ASCs) are a promising option for the treatment of obesity and its metabolic co-morbidities. Despite the recent identification of brown adipose tissue (BAT) as a potential target in the management of obesity, the ... ...

Abstract	Adipose-derived mesenchymal stem cells (ASCs) are a promising option for the treatment of obesity and its metabolic co-morbidities. Despite the recent identification of brown adipose tissue (BAT) as a potential target in the management of obesity, the use of ASCs isolated from BAT as a therapy for patients with obesity has not yet been explored. Metabolic activation of BAT has been shown to have not only thermogenic effects, but it also triggers the secretion of factors that confer protection against obesity. Herein, we isolated and characterized ASCs from the visceral adipose tissue surrounding a pheochromocytoma (IB-hASCs), a model of inducible BAT in humans. We then compared the anti-obesity properties of IB-hASCs and human ASCs isolated from visceral white adipose tissue (W-hASCs) in a murine model of diet-induced obesity. We found that both ASC therapies mitigated the metabolic abnormalities of obesity to a similar extent, including reducing weight gain and improving glucose tolerance. However, infusion of IB-hASCs was superior to W-hASCs in suppressing lipogenic and inflammatory markers, as well as preserving insulin secretion. Our findings provide evidence for the metabolic benefits of visceral ASC infusion and support further studies on IB-hASCs as a therapeutic option for obesity-related comorbidities.
MeSH term(s)	Adipose Tissue, White/pathology ; Adrenal Gland Neoplasms/pathology ; Animals ; Biomarkers/metabolism ; Diet ; Female ; Gene Expression Regulation ; Glucose/metabolism ; Humans ; Inflammation/genetics ; Lipid Metabolism/genetics ; Male ; Mice, Inbred C57BL ; Middle Aged ; Obesity/pathology ; Pheochromocytoma/pathology ; Stem Cells/pathology ; Weight Gain ; Mice
Chemical Substances	Biomarkers ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2021-07-06
Publishing country	England
Document type	Journal Article ; 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/s41598-021-93224-6
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Article ; Online: Orally administered Odoribacter laneus improves glucose control and inflammatory profile in obese mice by depleting circulating succinate.

Microbiome

2022 Volume 10, Issue 1, Page(s) 135

Abstract: Background: Succinate is produced by both human cells and by gut bacteria and couples metabolism to inflammation as an extracellular signaling transducer. Circulating succinate is elevated in patients with obesity and type 2 diabetes and is linked to ... ...

Abstract	Background: Succinate is produced by both human cells and by gut bacteria and couples metabolism to inflammation as an extracellular signaling transducer. Circulating succinate is elevated in patients with obesity and type 2 diabetes and is linked to numerous complications, yet no studies have specifically addressed the contribution of gut microbiota to systemic succinate or explored the consequences of reducing intestinal succinate levels in this setting. Results: Using germ-free and microbiota-depleted mouse models, we show that the gut microbiota is a significant source of circulating succinate, which is elevated in obesity. We also show in vivo that therapeutic treatments with selected bacteria diminish the levels of circulating succinate in obese mice. Specifically, we demonstrate that Odoribacter laneus is a promising probiotic based on its ability to deplete succinate and improve glucose tolerance and the inflammatory profile in two independent models of obesity (db/db mice and diet-induced obese mice). Mechanistically, this is partly mediated by the succinate receptor 1. Supporting these preclinical findings, we demonstrate an inverse correlation between plasma and fecal levels of succinate in a cohort of patients with severe obesity. We also show that plasma succinate, which is associated with several components of metabolic syndrome including waist circumference, triglycerides, and uric acid, among others, is a primary determinant of insulin sensitivity evaluated by the euglycemic-hyperinsulinemic clamp. Conclusions: Overall, our work uncovers O. laneus as a promising next-generation probiotic to deplete succinate and improve glucose tolerance and obesity-related inflammation. Video Abstract.
MeSH term(s)	Animals ; Bacteroidetes ; Blood Glucose ; Diabetes Mellitus, Type 2/microbiology ; Diet, High-Fat ; Humans ; Inflammation ; Mice ; Mice, Inbred C57BL ; Mice, Obese ; Obesity/etiology ; Succinic Acid
Chemical Substances	Blood Glucose ; Succinic Acid (AB6MNQ6J6L)
Language	English
Publishing date	2022-08-25
Publishing country	England
Document type	Journal Article ; Video-Audio Media ; Research Support, Non-U.S. Gov't
ZDB-ID	2697425-3
ISSN	2049-2618 ; 2049-2618
ISSN (online)	2049-2618
ISSN	2049-2618
DOI	10.1186/s40168-022-01306-y
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Article ; Online: Protective effects of the succinate/SUCNR1 axis on damaged hepatocytes in NAFLD.

Marsal-Beltran, Anna / Rodríguez-Castellano, Adrià / Astiarraga, Brenno / Calvo, Enrique / Rada, Patricia / Madeira, Ana / Rodríguez-Peña, M-Mar / Llauradó, Gemma / Núñez-Roa, Catalina / Gómez-Santos, Beatriz / Maymó-Masip, Elsa / Bosch, Ramon / Frutos, María Dolores / Moreno-Navarrete, José María / Ramos-Molina, Bruno / Aspichueta, Patricia / Joven, Jorge / Fernández-Real, José-Manuel / Quer, Juan Carlos /

Valverde, Ángela M / Pardo, Albert / Vendrell, Joan / Ceperuelo-Mallafré, Victòria / Fernández-Veledo, Sonia

Metabolism: clinical and experimental

2023 Volume 145, Page(s) 155630

Abstract: Objective: Succinate and succinate receptor 1 (SUCNR1) are linked to fibrotic remodeling in models of non-alcoholic fatty liver disease (NAFLD), but whether they have roles beyond the activation of hepatic stellate cells remains unexplored. We ... ...

Abstract	Objective: Succinate and succinate receptor 1 (SUCNR1) are linked to fibrotic remodeling in models of non-alcoholic fatty liver disease (NAFLD), but whether they have roles beyond the activation of hepatic stellate cells remains unexplored. We investigated the succinate/SUCNR1 axis in the context of NAFLD specifically in hepatocytes. Methods: We studied the phenotype of wild-type and Sucnr1 Results: Sucnr1 was upregulated in murine liver and primary hepatocytes in response to diet-induced NASH. Sucnr1 deficiency provoked both beneficial (reduced fibrosis and endoplasmic reticulum stress) and detrimental (exacerbated steatosis and inflammation and reduced glycogen content) effects in the liver, and disrupted glucose homeostasis. Studies in vitro revealed that hepatocyte injury increased Sucnr1 expression, which when activated improved lipid and glycogen homeostasis in damaged hepatocytes. In humans, SUCNR1 expression was a good determinant of NAFLD progression to advanced stages. In a population at risk of NAFLD, circulating succinate was elevated in patients with a fatty liver index (FLI) ≥60. Indeed, succinate had good predictive value for steatosis diagnosed by FLI, and improved the prediction of moderate/severe steatosis through biopsy when added to an FLI algorithm. Conclusions: We identify hepatocytes as target cells of extracellular succinate during NAFLD progression and uncover a hitherto unknown function for SUCNR1 as a regulator of hepatocyte glucose and lipid metabolism. Our clinical data highlight the potential of succinate and hepatic SUCNR1 expression as markers to diagnose fatty liver and NASH, respectively.
MeSH term(s)	Animals ; Humans ; Mice ; Disease Models, Animal ; Fibrosis ; Glucose/metabolism ; Glycogen/metabolism ; Hepatocytes/metabolism ; Liver/metabolism ; Mice, Inbred C57BL ; Non-alcoholic Fatty Liver Disease/metabolism ; Succinates/metabolism ; Succinates/pharmacology
Chemical Substances	Glucose (IY9XDZ35W2) ; Glycogen (9005-79-2) ; Succinates ; SUCNR1 protein, human ; GPR91 protein, mouse
Language	English
Publishing date	2023-06-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80230-x
ISSN	1532-8600 ; 0026-0495
ISSN (online)	1532-8600
ISSN	0026-0495
DOI	10.1016/j.metabol.2023.155630
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Article ; Online: SUCNR1 signaling in adipocytes controls energy metabolism by modulating circadian clock and leptin expression.

Villanueva-Carmona, Teresa / Cedó, Lídia / Madeira, Ana / Ceperuelo-Mallafré, Victòria / Rodríguez-Peña, M-Mar / Núñez-Roa, Catalina / Maymó-Masip, Elsa / Repollés-de-Dalmau, Maria / Badia, Joan / Keiran, Noelia / Mirasierra, Mercedes / Pimenta-Lopes, Carolina / Sabadell-Basallote, Joan / Bosch, Ramón / Caubet, Laura / Escolà-Gil, Joan Carles / Fernández-Real, José-Manuel / Vilarrasa, Nuria / Ventura, Francesc /

Vallejo, Mario / Vendrell, Joan / Fernández-Veledo, Sonia

Cell metabolism

2023 Volume 35, Issue 4, Page(s) 601–619.e10

Abstract: Adipose tissue modulates energy homeostasis by secreting leptin, but little is known about the factors governing leptin production. We show that succinate, long perceived as a mediator of immune response and lipolysis, controls leptin expression via its ... ...

Abstract	Adipose tissue modulates energy homeostasis by secreting leptin, but little is known about the factors governing leptin production. We show that succinate, long perceived as a mediator of immune response and lipolysis, controls leptin expression via its receptor SUCNR1. Adipocyte-specific deletion of Sucnr1 influences metabolic health according to nutritional status. Adipocyte Sucnr1 deficiency impairs leptin response to feeding, whereas oral succinate mimics nutrient-related leptin dynamics via SUCNR1. SUCNR1 activation controls leptin expression via the circadian clock in an AMPK/JNK-C/EBPα-dependent manner. Although the anti-lipolytic role of SUCNR1 prevails in obesity, its function as a regulator of leptin signaling contributes to the metabolically favorable phenotype in adipocyte-specific Sucnr1 knockout mice under standard dietary conditions. Obesity-associated hyperleptinemia in humans is linked to SUCNR1 overexpression in adipocytes, which emerges as the major predictor of adipose tissue leptin expression. Our study establishes the succinate/SUCNR1 axis as a metabolite-sensing pathway mediating nutrient-related leptin dynamics to control whole-body homeostasis.
MeSH term(s)	Animals ; Humans ; Mice ; Adipocytes/metabolism ; Circadian Clocks ; Energy Metabolism/physiology ; Leptin/metabolism ; Mice, Knockout ; Obesity/metabolism ; Succinates/metabolism
Chemical Substances	Leptin ; Succinates ; GPR91 protein, mouse
Language	English
Publishing date	2023-03-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2176834-1
ISSN	1932-7420 ; 1550-4131
ISSN (online)	1932-7420
ISSN	1550-4131
DOI	10.1016/j.cmet.2023.03.004
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