High Dietary Sugar Reshapes Sweet Taste to Promote Feeding Behavior in Drosophila melanogaster
Christina E. May,
Anoumid Vaziri,
Yong Qi Lin,
Olga Grushko,
Morteza Khabiri,
Qiao-Ping Wang,
Kristina J. Holme,
Scott D. Pletcher,
Peter L. Freddolino,
G. Gregory Neely,
Monica Dus
Affiliations
Christina E. May
Neuroscience Graduate Program, The University of Michigan, Ann Arbor, MI 48109, USA
Anoumid Vaziri
Molecular, Cellular, and Developmental Biology Graduate Program, The University of Michigan, Ann Arbor, MI 48109, USA
Yong Qi Lin
The Dr. John and Anne Chong Lab for Functional Genomics, Charles Perkins Centre and School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia
Olga Grushko
Department of Molecular, Cellular, and Developmental Biology, The University of Michigan, Ann Arbor, MI 48109, USA
Morteza Khabiri
Department of Biological Chemistry, The University of Michigan, Ann Arbor, MI 48109, USA
Qiao-Ping Wang
The Dr. John and Anne Chong Lab for Functional Genomics, Charles Perkins Centre and School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia; School of Pharmaceutical Sciences (Shenzhen), Sun Yat-sen University, Guangzhou, 510275, PR China
Kristina J. Holme
Physiology Graduate Program, Department of Molecular & Integrative Physiology, The University of Michigan Medical School, Ann Arbor, MI 48109, USA
Scott D. Pletcher
Physiology Graduate Program, Department of Molecular & Integrative Physiology, The University of Michigan Medical School, Ann Arbor, MI 48109, USA
Peter L. Freddolino
Department of Biological Chemistry, The University of Michigan, Ann Arbor, MI 48109, USA; Department of Computational Medicine and Bioinformatics, The University of Michigan, Ann Arbor, MI 48109, USA
G. Gregory Neely
The Dr. John and Anne Chong Lab for Functional Genomics, Charles Perkins Centre and School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia
Monica Dus
Neuroscience Graduate Program, The University of Michigan, Ann Arbor, MI 48109, USA; Molecular, Cellular, and Developmental Biology Graduate Program, The University of Michigan, Ann Arbor, MI 48109, USA; Department of Molecular, Cellular, and Developmental Biology, The University of Michigan, Ann Arbor, MI 48109, USA; Corresponding author
Summary: Recent studies find that sugar tastes less intense to humans with obesity, but whether this sensory change is a cause or a consequence of obesity is unclear. To tackle this question, we study the effects of a high sugar diet on sweet taste sensation and feeding behavior in Drosophila melanogaster. On this diet, fruit flies have lower taste responses to sweet stimuli, overconsume food, and develop obesity. Excess dietary sugar, but not obesity or dietary sweetness alone, caused taste deficits and overeating via the cell-autonomous action of the sugar sensor O-linked N-Acetylglucosamine (O-GlcNAc) transferase (OGT) in the sweet-sensing neurons. Correcting taste deficits by manipulating the excitability of the sweet gustatory neurons or the levels of OGT protected animals from diet-induced obesity. Our work demonstrates that the reshaping of sweet taste sensation by excess dietary sugar drives obesity and highlights the role of glucose metabolism in neural activity and behavior. : May et al. discover that excess dietary sugar promotes overfeeding by dulling sweet taste sensation in Drosophila melanogaster. Deficits in taste function occur independently of obesity and, instead, develop because of higher glucose utilization inside the gustatory neurons. Correcting sweet taste function prevents overconsumption and obesity in animals fed a high sugar diet.