Atrial Natriuretic Peptide Orchestrates a Coordinated Physiological Response to Fuel Non-shivering Thermogenesis

Deborah Carper; Marine Coue; Emmani B. M. Nascimento; Valentin Barquissau; Damien Lagarde; Carine Pestourie; Claire Laurens; Justine Vily Petit; Maud Soty; Laurent Monbrun; Marie-Adeline Marques; Yannick Jeanson; Yannis Sainte-Marie; Aline Mairal; Sebastien Dejean; Genevieve Tavernier; Nathalie Viguerie; Virginie Bourlier; Frank Lezoualc'h; Audrey Carriere; Wim H. M. Saris; Arne Astrup; Louis Casteilla; Gilles Mithieux; W. D.  van Marken Lichtenbelt; Dominique Langin; Patrick Schrauwen; Cedric Moro

doi:10.1016/j.celrep.2020.108075

Atrial Natriuretic Peptide Orchestrates a Coordinated Physiological Response to Fuel Non-shivering Thermogenesis

Deborah Carper, Marine Coue, Emmani B. M. Nascimento, Valentin Barquissau, Damien Lagarde, Carine Pestourie, Claire Laurens, Justine Vily Petit, Maud Soty, Laurent Monbrun, Marie-Adeline Marques, Yannick Jeanson, Yannis Sainte-Marie, Aline Mairal, Sebastien Dejean, Genevieve Tavernier, Nathalie Viguerie, Virginie Bourlier, Frank Lezoualc'h, Audrey CarriereWim H. M. Saris, Arne Astrup, Louis Casteilla, Gilles Mithieux, W. D. van Marken Lichtenbelt, Dominique Langin, Patrick Schrauwen, Cedric Moro^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Atrial natriuretic peptide (ANP) is a cardiac hormone controlling blood volume and pressure in mammals. It is still unclear whether ANP controls cold-induced thermogenesis in vivo. Here, we show that acute cold exposure induces cardiac ANP secretion in mice and humans. Genetic inactivation of ANP promotes cold intolerance and suppresses half of cold-induced brown adipose tissue (BAT) activation in mice. While white adipocytes are resistant to ANP-mediated lipolysis at thermoneutral temperature in mice, cold exposure renders white adipocytes fully responsive to ANP to activate lipolysis and a thermogenic program, a physiological response that is dramatically suppressed in ANP null mice. ANP deficiency also blunts liver triglycerides and glycogen metabolism, thus impairing fuel availability for BAT thermogenesis. ANP directly increases mitochondrial uncoupling and thermogenic gene expression in human white and brown adipocytes. Together, these results indicate that ANP is a major physiological trigger of BAT thermogenesis upon cold exposure in mammals.

Original language	English
Article number	108075
Number of pages	19
Journal	Cell Reports
Volume	32
Issue number	8
DOIs	https://doi.org/10.1016/j.celrep.2020.108075
Publication status	Published - 25 Aug 2020

Keywords

BROWN ADIPOSE-TISSUE
COLD-INDUCED THERMOGENESIS
ACTIVATED PROTEIN-KINASE
INSULIN-RESISTANCE
BEIGE ADIPOCYTES
WEIGHT-LOSS
RECEPTOR
OBESITY
INDUCE
IDENTIFICATION

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Cite this

Carper, D., Coue, M., Nascimento, E. B. M., Barquissau, V., Lagarde, D., Pestourie, C., Laurens, C., Petit, J. V., Soty, M., Monbrun, L., Marques, M.-A., Jeanson, Y., Sainte-Marie, Y., Mairal, A., Dejean, S., Tavernier, G., Viguerie, N., Bourlier, V., Lezoualc'h, F., ... Moro, C. (2020). Atrial Natriuretic Peptide Orchestrates a Coordinated Physiological Response to Fuel Non-shivering Thermogenesis. Cell Reports, 32(8), Article 108075. https://doi.org/10.1016/j.celrep.2020.108075

@article{c413411696ba43f68d7a8c4f5987c36a,

title = "Atrial Natriuretic Peptide Orchestrates a Coordinated Physiological Response to Fuel Non-shivering Thermogenesis",

abstract = "Atrial natriuretic peptide (ANP) is a cardiac hormone controlling blood volume and pressure in mammals. It is still unclear whether ANP controls cold-induced thermogenesis in vivo. Here, we show that acute cold exposure induces cardiac ANP secretion in mice and humans. Genetic inactivation of ANP promotes cold intolerance and suppresses half of cold-induced brown adipose tissue (BAT) activation in mice. While white adipocytes are resistant to ANP-mediated lipolysis at thermoneutral temperature in mice, cold exposure renders white adipocytes fully responsive to ANP to activate lipolysis and a thermogenic program, a physiological response that is dramatically suppressed in ANP null mice. ANP deficiency also blunts liver triglycerides and glycogen metabolism, thus impairing fuel availability for BAT thermogenesis. ANP directly increases mitochondrial uncoupling and thermogenic gene expression in human white and brown adipocytes. Together, these results indicate that ANP is a major physiological trigger of BAT thermogenesis upon cold exposure in mammals.",

keywords = "BROWN ADIPOSE-TISSUE, COLD-INDUCED THERMOGENESIS, ACTIVATED PROTEIN-KINASE, INSULIN-RESISTANCE, BEIGE ADIPOCYTES, WEIGHT-LOSS, RECEPTOR, OBESITY, INDUCE, IDENTIFICATION",

author = "Deborah Carper and Marine Coue and Nascimento, {Emmani B. M.} and Valentin Barquissau and Damien Lagarde and Carine Pestourie and Claire Laurens and Petit, {Justine Vily} and Maud Soty and Laurent Monbrun and Marie-Adeline Marques and Yannick Jeanson and Yannis Sainte-Marie and Aline Mairal and Sebastien Dejean and Genevieve Tavernier and Nathalie Viguerie and Virginie Bourlier and Frank Lezoualc'h and Audrey Carriere and Saris, {Wim H. M.} and Arne Astrup and Louis Casteilla and Gilles Mithieux and {van Marken Lichtenbelt}, {W. D.} and Dominique Langin and Patrick Schrauwen and Cedric Moro",

note = "Funding Information: This work was supported by grants from INSERM , Soci{\'e}t{\'e} Francophone du Diab{\`e}te , and the European Foundation for the Study of Diabetes (C.M.) and the Commission of the European Communities ( FP6-513946 DiOGenes and HEALTH-F2-2011-278373 DIABAT ) (D. Lagarde). D.C. is supported by a PhD fellowship from INSERM/Occitanie Region . We are very grateful to Caroline Nevoit, Sarah Gandarillas, and Candy Escassut (CREFRE) for technical assistance in PET/CT imaging. We also thank Alexandre Lucas (APC core facility), Fr{\'e}d{\'e}ric Martins (GET-TQ core facility), Lucie Fontaine (Histology core facility), and Dr. Jean-Philippe Prad{\`e}re and Enzo Piccolo (Liver ORO staining) for their technical support. D.L. is a member of Institut Universitaire de France. We warmly acknowledge Pr. Max Lafontan for critical reading of the manuscript. Funding Information: This work was supported by grants from INSERM, Soci?t? Francophone du Diab?te, and the European Foundation for the Study of Diabetes (C.M.) and the Commission of the European Communities (FP6-513946 DiOGenes and HEALTH-F2-2011-278373 DIABAT) (D. Lagarde). D.C. is supported by a PhD fellowship from INSERM/Occitanie Region. We are very grateful to Caroline Nevoit, Sarah Gandarillas, and Candy Escassut (CREFRE) for technical assistance in PET/CT imaging. We also thank Alexandre Lucas (APC core facility), Fr?d?ric Martins (GET-TQ core facility), Lucie Fontaine (Histology core facility), and Dr. Jean-Philippe Prad?re and Enzo Piccolo (Liver ORO staining) for their technical support. D.L. is a member of Institut Universitaire de France. We warmly acknowledge Pr. Max Lafontan for critical reading of the manuscript. Conceptualization, D.C. and C.M.; Methodology, D.C. and C.M.; Investigation, D.C. M.C. E.B.M.N. V.B. D.A.L. C.P. C.L. J.V.P. M.S. L.M. M.-A.M. Y.J. Y.S.-M. A.M. S.D. G.T. N.V. V.B. F.L. A.C. W.H.M.S. and A.A.; Resources, G.M. W.v.M.L. P.S. D.L.; Writing ? Original Draft, D.C. and C.M.; Writing ? Review & Editing, D.C. E.B.M.N. A.C. L.C. G.M. W.v.M.L. P.S. D.L. and C.M.; Supervision, D.C. and C.M.; Funding Acquisition, D.L. and C.M. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2020 The Author(s)",

year = "2020",

month = aug,

day = "25",

doi = "10.1016/j.celrep.2020.108075",

language = "English",

volume = "32",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "8",

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Carper, D, Coue, M, Nascimento, EBM, Barquissau, V, Lagarde, D, Pestourie, C, Laurens, C, Petit, JV, Soty, M, Monbrun, L, Marques, M-A, Jeanson, Y, Sainte-Marie, Y, Mairal, A, Dejean, S, Tavernier, G, Viguerie, N, Bourlier, V, Lezoualc'h, F, Carriere, A, Saris, WHM, Astrup, A, Casteilla, L, Mithieux, G, van Marken Lichtenbelt, WD, Langin, D, Schrauwen, P & Moro, C 2020, 'Atrial Natriuretic Peptide Orchestrates a Coordinated Physiological Response to Fuel Non-shivering Thermogenesis', Cell Reports, vol. 32, no. 8, 108075. https://doi.org/10.1016/j.celrep.2020.108075

TY - JOUR

T1 - Atrial Natriuretic Peptide Orchestrates a Coordinated Physiological Response to Fuel Non-shivering Thermogenesis

AU - Carper, Deborah

AU - Coue, Marine

AU - Nascimento, Emmani B. M.

AU - Barquissau, Valentin

AU - Lagarde, Damien

AU - Pestourie, Carine

AU - Laurens, Claire

AU - Petit, Justine Vily

AU - Soty, Maud

AU - Monbrun, Laurent

AU - Marques, Marie-Adeline

AU - Jeanson, Yannick

AU - Sainte-Marie, Yannis

AU - Mairal, Aline

AU - Dejean, Sebastien

AU - Tavernier, Genevieve

AU - Viguerie, Nathalie

AU - Bourlier, Virginie

AU - Lezoualc'h, Frank

AU - Carriere, Audrey

AU - Saris, Wim H. M.

AU - Astrup, Arne

AU - Casteilla, Louis

AU - Mithieux, Gilles

AU - van Marken Lichtenbelt, W. D.

AU - Langin, Dominique

AU - Schrauwen, Patrick

AU - Moro, Cedric

N1 - Funding Information: This work was supported by grants from INSERM , Société Francophone du Diabète , and the European Foundation for the Study of Diabetes (C.M.) and the Commission of the European Communities ( FP6-513946 DiOGenes and HEALTH-F2-2011-278373 DIABAT ) (D. Lagarde). D.C. is supported by a PhD fellowship from INSERM/Occitanie Region . We are very grateful to Caroline Nevoit, Sarah Gandarillas, and Candy Escassut (CREFRE) for technical assistance in PET/CT imaging. We also thank Alexandre Lucas (APC core facility), Frédéric Martins (GET-TQ core facility), Lucie Fontaine (Histology core facility), and Dr. Jean-Philippe Pradère and Enzo Piccolo (Liver ORO staining) for their technical support. D.L. is a member of Institut Universitaire de France. We warmly acknowledge Pr. Max Lafontan for critical reading of the manuscript. Funding Information: This work was supported by grants from INSERM, Soci?t? Francophone du Diab?te, and the European Foundation for the Study of Diabetes (C.M.) and the Commission of the European Communities (FP6-513946 DiOGenes and HEALTH-F2-2011-278373 DIABAT) (D. Lagarde). D.C. is supported by a PhD fellowship from INSERM/Occitanie Region. We are very grateful to Caroline Nevoit, Sarah Gandarillas, and Candy Escassut (CREFRE) for technical assistance in PET/CT imaging. We also thank Alexandre Lucas (APC core facility), Fr?d?ric Martins (GET-TQ core facility), Lucie Fontaine (Histology core facility), and Dr. Jean-Philippe Prad?re and Enzo Piccolo (Liver ORO staining) for their technical support. D.L. is a member of Institut Universitaire de France. We warmly acknowledge Pr. Max Lafontan for critical reading of the manuscript. Conceptualization, D.C. and C.M.; Methodology, D.C. and C.M.; Investigation, D.C. M.C. E.B.M.N. V.B. D.A.L. C.P. C.L. J.V.P. M.S. L.M. M.-A.M. Y.J. Y.S.-M. A.M. S.D. G.T. N.V. V.B. F.L. A.C. W.H.M.S. and A.A.; Resources, G.M. W.v.M.L. P.S. D.L.; Writing ? Original Draft, D.C. and C.M.; Writing ? Review & Editing, D.C. E.B.M.N. A.C. L.C. G.M. W.v.M.L. P.S. D.L. and C.M.; Supervision, D.C. and C.M.; Funding Acquisition, D.L. and C.M. The authors declare no competing interests. Publisher Copyright: © 2020 The Author(s)

PY - 2020/8/25

Y1 - 2020/8/25

N2 - Atrial natriuretic peptide (ANP) is a cardiac hormone controlling blood volume and pressure in mammals. It is still unclear whether ANP controls cold-induced thermogenesis in vivo. Here, we show that acute cold exposure induces cardiac ANP secretion in mice and humans. Genetic inactivation of ANP promotes cold intolerance and suppresses half of cold-induced brown adipose tissue (BAT) activation in mice. While white adipocytes are resistant to ANP-mediated lipolysis at thermoneutral temperature in mice, cold exposure renders white adipocytes fully responsive to ANP to activate lipolysis and a thermogenic program, a physiological response that is dramatically suppressed in ANP null mice. ANP deficiency also blunts liver triglycerides and glycogen metabolism, thus impairing fuel availability for BAT thermogenesis. ANP directly increases mitochondrial uncoupling and thermogenic gene expression in human white and brown adipocytes. Together, these results indicate that ANP is a major physiological trigger of BAT thermogenesis upon cold exposure in mammals.

AB - Atrial natriuretic peptide (ANP) is a cardiac hormone controlling blood volume and pressure in mammals. It is still unclear whether ANP controls cold-induced thermogenesis in vivo. Here, we show that acute cold exposure induces cardiac ANP secretion in mice and humans. Genetic inactivation of ANP promotes cold intolerance and suppresses half of cold-induced brown adipose tissue (BAT) activation in mice. While white adipocytes are resistant to ANP-mediated lipolysis at thermoneutral temperature in mice, cold exposure renders white adipocytes fully responsive to ANP to activate lipolysis and a thermogenic program, a physiological response that is dramatically suppressed in ANP null mice. ANP deficiency also blunts liver triglycerides and glycogen metabolism, thus impairing fuel availability for BAT thermogenesis. ANP directly increases mitochondrial uncoupling and thermogenic gene expression in human white and brown adipocytes. Together, these results indicate that ANP is a major physiological trigger of BAT thermogenesis upon cold exposure in mammals.

KW - BROWN ADIPOSE-TISSUE

KW - COLD-INDUCED THERMOGENESIS

KW - ACTIVATED PROTEIN-KINASE

KW - INSULIN-RESISTANCE

KW - BEIGE ADIPOCYTES

KW - WEIGHT-LOSS

KW - RECEPTOR

KW - OBESITY

KW - INDUCE

KW - IDENTIFICATION

U2 - 10.1016/j.celrep.2020.108075

DO - 10.1016/j.celrep.2020.108075

M3 - Article

C2 - 32846132

SN - 2211-1247

VL - 32

JO - Cell Reports

JF - Cell Reports

IS - 8

M1 - 108075

ER -