Control of circadian muscle glucose metabolism through the BMAL1–HIF axis in obesity

C Claire A. Chaikin (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine) A Abhishek V. Thakkar (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine) A Adam W. T. Steffeck (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine) E Eric M. Pfrender (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine) K Kaitlyn Hung (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine) P Pei Zhu (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine) N Nathan J. Waldeck (Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine) R Rino Nozawa (Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine) W Weimin Song (Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine) C Christopher R. Futtner (Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine) M Mattia Quattrocelli (Division of Molecular Cardiovascular Biology, Cincinnati Children’s Hospital) J Joseph Bass (Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine) I Issam Ben-Sahra C Clara B. Peek (Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine)

Abstract

Disruptions of circadian rhythms are widespread in modern society and lead to accelerated and worsened symptoms of metabolic syndrome. In healthy mice, the circadian clock factor BMAL1 is required for skeletal muscle function and metabolism. However, the importance of muscle BMAL1 in the development of metabolic diseases, such as diet-induced obesity (DIO), remains unclear. Here, we demonstrate that skeletal muscle–specific BMAL1-deficient mice exhibit worsened glucose tolerance upon high-fat diet feeding, despite no evidence of increased weight gain. Metabolite profiling from Bmal1 -deficient muscles revealed impaired glucose utilization specifically at early steps in glycolysis that dictate the switch between anabolic and catabolic glucose fate. We provide evidence that this is due to abnormal control of the nutrient stress–responsive hypoxia-inducible factor (HIF) pathway. Genetic HIF1α stabilization in muscle Bmal1 -deficient mice restores glucose tolerance and expression of 217/736 dysregulated genes during DIO, including glycolytic enzymes. Together, these data indicate that during DIO, skeletal muscle BMAL1 is an important regulator of HIF-driven glycolysis and metabolic flexibility, which influences the development of high-fat-diet-induced glucose intolerance.

Article Details

Volume / Issue Vol. 122, Issue 13
Published April 01, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (14)

C

Claire A. Chaikin

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine

A

Abhishek V. Thakkar

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine

A

Adam W. T. Steffeck

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine

E

Eric M. Pfrender

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine

K

Kaitlyn Hung

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine

P

Pei Zhu

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine

N

Nathan J. Waldeck

Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine

R

Rino Nozawa

Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine

W

Weimin Song

Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine

C

Christopher R. Futtner

Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine

M

Mattia Quattrocelli

Division of Molecular Cardiovascular Biology, Cincinnati Children’s Hospital

J

Joseph Bass

Department of Medicine, Division of Endocrinology, Metabolism and Molecular Medicine, Northwestern University Feinberg School of Medicine

I

Issam Ben-Sahra

C

Clara B. Peek

Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine