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Article

Pro-Inflammatory Cytokines Induce Insulin and Glucagon Double Positive Human Islet Cells That Are Resistant to Apoptosis

by
Marta Tesi
1,†,
Marco Bugliani
1,†,
Gianmarco Ferri
2,
Mara Suleiman
1,
Carmela De Luca
1,
Emanuele Bosi
1,
Matilde Masini
3,
Vincenzo De Tata
3,
Conny Gysemans
4,
Francesco Cardarelli
2,
Miriam Cnop
5,6,
Decio L. Eizirik
5,7,
Piero Marchetti
1 and
Lorella Marselli
1,*
1
Pancreatic Islet Laboratory, Department of Clinical and Experimental Medicine, University of Pisa, 56126 Pisa, Italy
2
NEST—Scuola Normale Superiore, Istituto Nanoscienze—CNR (CNR-NANO), 56127 Pisa, Italy
3
Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, 56126 Pisa, Italy
4
Clinical and Experimental Endocrinology (CEE), Katholieke Universiteit Leuven (KU LEUVEN), 3000 Leuven, Belgium
5
ULB Center for Diabetes Research, Medical Faculty, Université Libre de Bruxelles (ULB), 1070 Brussels, Belgium
6
Division of Endocrinology, Erasmus Hospital, Université Libre de Bruxelles, 1070 Brussels, Belgium
7
Indiana Biosciences Research Institute (IBRI), Indianapolis, IN 46202, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Biomolecules 2021, 11(2), 320; https://doi.org/10.3390/biom11020320
Submission received: 20 January 2021 / Revised: 10 February 2021 / Accepted: 15 February 2021 / Published: 19 February 2021
(This article belongs to the Special Issue Pancreatic Islets of Langerhans: Not Only Beta-Cells)
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Abstract

The presence of islet cells double positive for insulin and glucagon (Ins+/Glu+) has been described in the pancreas from both type 2 (T2D) and type 1 (T1D) diabetic subjects. We studied the role of pro-inflammatory cytokines on the occurrence, trajectory, and characteristics of Ins+/Glu+ cells in human pancreatic islets. Pancreas samples, isolated islets, and dispersed islet cells from 3 T1D and 11 non-diabetic (ND) multi-organ donors were studied by immunofluorescence, confocal microscopy, and/or electron microscopy. ND islet cells were exposed to interleukin-1β and interferon-γ for up to 120 h. In T1D islets, we confirmed an increased prevalence of Ins+/Glu+ cells. Cytokine-exposed islets showed a progressive increase of Ins+/Glu+ cells that represented around 50% of endocrine cells after 120h. Concomitantly, cells expressing insulin granules only decreased significantly over time, whereas those containing only glucagon granules remained stable. Interestingly, Ins+/Glu+ cells were less prone to cytokine-induced apoptosis than cells containing only insulin. Cytokine-exposed islets showed down-regulation of β-cell identity genes. In conclusion, pro-inflammatory cytokines induce Ins+/Glu+ cells in human islets, possibly due to a switch from a β- to a β-/α-cell phenotype. These Ins+/Glu+ cells appear to be resistant to cytokine-induced apoptosis.
Keywords: human islets; α-cells; β-cells; insulin; glucagon; diabetes; cytokines; apoptosis human islets; α-cells; β-cells; insulin; glucagon; diabetes; cytokines; apoptosis

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MDPI and ACS Style

Tesi, M.; Bugliani, M.; Ferri, G.; Suleiman, M.; De Luca, C.; Bosi, E.; Masini, M.; De Tata, V.; Gysemans, C.; Cardarelli, F.; et al. Pro-Inflammatory Cytokines Induce Insulin and Glucagon Double Positive Human Islet Cells That Are Resistant to Apoptosis. Biomolecules 2021, 11, 320. https://doi.org/10.3390/biom11020320

AMA Style

Tesi M, Bugliani M, Ferri G, Suleiman M, De Luca C, Bosi E, Masini M, De Tata V, Gysemans C, Cardarelli F, et al. Pro-Inflammatory Cytokines Induce Insulin and Glucagon Double Positive Human Islet Cells That Are Resistant to Apoptosis. Biomolecules. 2021; 11(2):320. https://doi.org/10.3390/biom11020320

Chicago/Turabian Style

Tesi, Marta, Marco Bugliani, Gianmarco Ferri, Mara Suleiman, Carmela De Luca, Emanuele Bosi, Matilde Masini, Vincenzo De Tata, Conny Gysemans, Francesco Cardarelli, and et al. 2021. "Pro-Inflammatory Cytokines Induce Insulin and Glucagon Double Positive Human Islet Cells That Are Resistant to Apoptosis" Biomolecules 11, no. 2: 320. https://doi.org/10.3390/biom11020320

APA Style

Tesi, M., Bugliani, M., Ferri, G., Suleiman, M., De Luca, C., Bosi, E., Masini, M., De Tata, V., Gysemans, C., Cardarelli, F., Cnop, M., Eizirik, D. L., Marchetti, P., & Marselli, L. (2021). Pro-Inflammatory Cytokines Induce Insulin and Glucagon Double Positive Human Islet Cells That Are Resistant to Apoptosis. Biomolecules, 11(2), 320. https://doi.org/10.3390/biom11020320

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