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Bader, E. ; Migliorini, A. ; Gegg, M. ; Moruzzi, N. ; Gerdes, J.M. ; Roscioni, S. ; Bakhti, M. ; Brandl, E. ; Irmler, M. ; Beckers, J. ; Aichler, M. ; Feuchtinger, A. ; Leitzinger, C. ; Zischka, H. ; Wang-Sattler, R. ; Jastroch, M. ; Tschöp, M.H. ; Machicao, F. ; Staiger, H. ; Häring, H.-U. ; Chmelova, H. ; Chouinard, J.A.* ; Oskolkov, N.* ; Korsgren, O.* ; Speier, S. ; Lickert, H.

Identification of proliferative and mature β-cells in the islets of Langerhans.

Nature 535, 430-434 (2016)

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Insulin-dependent diabetes is a complex multifactorial disorder characterized by loss or dysfunction of β-cells. Pancreatic β-cells differ in size, glucose responsiveness, insulin secretion and precursor cell potential; understanding the mechanisms that underlie this functional heterogeneity might make it possible to develop new regenerative approaches. Here we show that Fltp (also known as Flattop and Cfap126), a Wnt/planar cell polarity (PCP) effector and reporter gene, acts as a marker gene that subdivides endocrine cells into two subpopulations and distinguishes proliferation-competent from mature β-cells with distinct molecular, physiological and ultrastructural features. Genetic lineage tracing revealed that endocrine subpopulations from Fltp-negative and -positive lineages react differently to physiological and pathological changes. The expression of Fltp increases when endocrine cells cluster together to form polarized and mature 3D islet mini-organs. We show that 3D architecture and Wnt/PCP ligands are sufficient to trigger β-cell maturation. By contrast, the Wnt/PCP effector Fltp is not necessary for β-cell development, proliferation or maturation. We conclude that 3D architecture and Wnt/PCP signalling underlie functional β-cell heterogeneity and induce β-cell maturation. The identification of Fltp as a marker for endocrine subpopulations sheds light on the molecular underpinnings of islet cell heterogeneity and plasticity and might enable targeting of endocrine subpopulations for the regeneration of functional β-cell mass in diabetic patients.

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