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Johnston, Natalie R.; Mitchell, Ryan K.; Haythorne, Elizabeth; Pessoa, Maria Paiva; Semplici, Francesca; Ferrer, Jorge; Piemonti, Lorenzo; Marchetti, Piero; Bugliani, Marco; Bosco, Domenico; Berishvili, Ekaterine; Duncanson, Philip; Watkinson, Michael; Broichhagen, Johannes; Trauner, Dirk; Rutter, Guy A.; Hodson, David J.
Cell metabolism, 09/2016, Letnik: 24, Številka: 3Journal Article
The arrangement of β cells within islets of Langerhans is critical for insulin release through the generation of rhythmic activity. A privileged role for individual β cells in orchestrating these responses has long been suspected, but not directly demonstrated. We show here that the β cell population in situ is operationally heterogeneous. Mapping of islet functional architecture revealed the presence of hub cells with pacemaker properties, which remain stable over recording periods of 2 to 3 hr. Using a dual optogenetic/photopharmacological strategy, silencing of hubs abolished coordinated islet responses to glucose, whereas specific stimulation restored communication patterns. Hubs were metabolically adapted and targeted by both pro-inflammatory and glucolipotoxic insults to induce widespread β cell dysfunction. Thus, the islet is wired by hubs, whose failure may contribute to type 2 diabetes mellitus. Display omitted •Optogenetic targeting reveals a pacemaker-like β cell subpopulation•These cells, termed hubs, are required for normal insulin release•Hubs are highly metabolic and transcriptionally immature•Hubs are targeted by a diabetic milieu to induce islet failure Combining optogenetics and photopharmacology, Johnston et al. show that a few (1%–10%) β cells exert disproportionate control over islet responses to glucose. These specialized cells, called hubs, are transcriptionally immature and highly metabolic. Their failure during type 2 diabetes mellitus may lead to reduced insulin secretion and impaired glucose homeostasis.
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