TY - JOUR
T1 - YAP mediates compensatory cardiac hypertrophy through aerobic glycolysis in response to pressure overload
AU - Kashihara, Toshihide
AU - Mukai, Risa
AU - Oka, Shin Ichi
AU - Zhai, Peiyong
AU - Nakada, Yasuki
AU - Yang, Zhi
AU - Mizushima, Wataru
AU - Nakahara, Tsutomu
AU - Warren, Junco S.
AU - Abdellatif, Maha
AU - Sadoshima, Junichi
N1 - Funding Information:
We thank Yimin Tian for technical assistance and Daniela Zabloc-ki for critical reading of the manuscript. Metabolomics analysis was performed at the Metabolomics Core Facilities at the University of Utah. Mass spectrometry equipment was obtained through National Center for Research Resources (NCRR) Shared Instrumentation Grants (1S10OD016232-01, 1S10OD018210-01A1, and 1S10OD021505-01). This work was supported in part by an American Heart Association (AHA) Merit Award (35120374, to JS); the Foundation Leducq Transatlantic Network (15CVD04, to JS); and US Public Health Service grants (HL067724, HL091469, HL112330, HL138720, HL144626, HL150881, and AG23039, to JS).
Publisher Copyright:
© 2022, Kashihara et al.
PY - 2022/3/15
Y1 - 2022/3/15
N2 - The heart utilizes multiple adaptive mechanisms to maintain pump function. Compensatory cardiac hypertrophy reduces wall stress and oxygen consumption, thereby protecting the heart against acute blood pressure elevation. The nuclear effector of the Hippo pathway, Yes-associated protein 1 (YAP), is activated and mediates compensatory cardiac hypertrophy in response to acute pressure overload (PO). In this study, YAP promoted glycolysis by upregulating glucose transporter 1 (GLUT1), which in turn caused accumulation of intermediates and metabolites of the glycolytic, auxiliary, and anaplerotic pathways during acute PO. Cardiac hypertrophy was inhibited and heart failure was exacerbated in mice with YAP haploinsufficiency in the presence of acute PO. However, normalization of GLUT1 rescued the detrimental phenotype. PO induced the accumulation of glycolytic metabolites, including l-serine, l-aspartate, and malate, in a YAP-dependent manner, thereby promoting cardiac hypertrophy. YAP upregulated the GLUT1 gene through interaction with TEA domain family member 1 (TEAD1) and HIF-1α in cardiomyocytes. Thus, YAP induces compensatory cardiac hypertrophy through activation of the Warburg effect.
AB - The heart utilizes multiple adaptive mechanisms to maintain pump function. Compensatory cardiac hypertrophy reduces wall stress and oxygen consumption, thereby protecting the heart against acute blood pressure elevation. The nuclear effector of the Hippo pathway, Yes-associated protein 1 (YAP), is activated and mediates compensatory cardiac hypertrophy in response to acute pressure overload (PO). In this study, YAP promoted glycolysis by upregulating glucose transporter 1 (GLUT1), which in turn caused accumulation of intermediates and metabolites of the glycolytic, auxiliary, and anaplerotic pathways during acute PO. Cardiac hypertrophy was inhibited and heart failure was exacerbated in mice with YAP haploinsufficiency in the presence of acute PO. However, normalization of GLUT1 rescued the detrimental phenotype. PO induced the accumulation of glycolytic metabolites, including l-serine, l-aspartate, and malate, in a YAP-dependent manner, thereby promoting cardiac hypertrophy. YAP upregulated the GLUT1 gene through interaction with TEA domain family member 1 (TEAD1) and HIF-1α in cardiomyocytes. Thus, YAP induces compensatory cardiac hypertrophy through activation of the Warburg effect.
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U2 - 10.1172/JCI150595
DO - 10.1172/JCI150595
M3 - Article
C2 - 35133975
AN - SCOPUS:85126490376
SN - 0021-9738
VL - 132
JO - Journal of Clinical Investigation
JF - Journal of Clinical Investigation
IS - 6
M1 - e150595
ER -