TY - JOUR

T1 - Atrial natriuretic peptide orchestrates a coordinated physiological response to fuel non-shivering thermogenesis

AU - Carper, Deborah

AU - Coué, 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 - Déjean, Sébastien

AU - Tavernier, Geneviève

AU - Viguerie, Nathalie

AU - Bourlier, Virginie

AU - Lezoualc'h, Frank

AU - Carrière, Audrey

AU - Saris, Wim H M

AU - Astrup, Arne

AU - Casteilla, Louis

AU - Mithieux, Gilles

AU - van Marken Lichtenbelt, Wouter

AU - Langin, Dominique

AU - Schrauwen, Patrick

AU - Moro, Cedric

N1 - CURIS 2020 NEXS 286

PY - 2020

Y1 - 2020

N2 - The classical view is that brown adipose tissue (BAT) is mainly activated by the sympathetic nervous system. Carper et al. here demonstrate that the cardiac hormone atrial natriuretic peptide is released upon cold exposure and required to activate BAT thermogenesis and white fat browning in mice and humans.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 - The classical view is that brown adipose tissue (BAT) is mainly activated by the sympathetic nervous system. Carper et al. here demonstrate that the cardiac hormone atrial natriuretic peptide is released upon cold exposure and required to activate BAT thermogenesis and white fat browning in mice and humans.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 - Adipocyte

KW - Brown adipose tissue

KW - Lipolysis

KW - Thermogenesis

KW - Uncoupling protein 1

UR - http://www.scopus.com/inward/record.url?scp=85089802256&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2020.108075

DO - 10.1016/j.celrep.2020.108075

M3 - Journal article

C2 - 32846132

AN - SCOPUS:85089802256

VL - 32

JO - Cell Reports

JF - Cell Reports

SN - 2211-1247

IS - 8

M1 - 108075

ER -