Lipotoxicity disrupts incretin-regulated human β cell connectivity
Open accessAbstract
Pancreatic β cell dysfunction is pathognomonic of type 2 diabetes mellitus (T2DM) and is driven by environmental and genetic factors. β cell responses to glucose and to incretins such as glucagon-like peptide-1 (GLP-1) and glucose-dependent insulinotropic polypeptide (GIP) are altered in the disease state. While rodent β cells act as a coordinated syncytium to drive insulin release, this property is unexplored in human islets. In situ imaging approaches were therefore used to monitor in real time the islet dynamics underlying hormone release. We found that GLP-1 and GIP recruit a highly coordinated subnetwork of β cells that are targeted by lipotoxicity to suppress insulin secretion. Donor BMI was negatively correlated with subpopulation responses to GLP-1, suggesting that this action of incretin contributes to functional β cell mass in vivo. Conversely, exposure of mice to a high-fat diet unveiled a role for incretin in maintaining coordinated islet activity, supporting the existence of species-specific strategies to maintain normoglycemia. These findings demonstrate that β cell connectedness is an inherent property of human islets that is likely to influence incretin-potentiated insulin secretion and may be perturbed by diabetogenic insults to disrupt glucose homeostasis in humans.
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Coordinated [Ca2+]i oscillations are observed in human islets in the presence of the incretin hormones GLP-1 and GIP.
“However, although [Ca2+]i oscillations elicited by high glucose appear to be stochastic in human islets, coordinated oscillations are observed in the presence of the incretin hormones GLP-1 and GIP (284).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [284]
The section “GLP-1 activates a coordinated subpopulation of β cells” reports stochastic Ca²⁺ oscillations under elevated glucose and markedly more coordinated Ca²⁺ activity after GLP-1 application in human islets. The copy identifies GIP as an incretin in the Introduction, but the passages found do not show coordinated oscillations in human islets in response to GIP. (LLM, conf=0.88)
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- Authors
- Hodson, D. J., Mitchell, R. K., Bellomo, E. A., Sun, G., Vinet, L., Meda, P., Li, D., Li, W.-H., Bugliani, M., Marchetti, P., Bosco, D., Piemonti, L., Johnson, P., Hughes, S. J., & Rutter, G. A.
- Affiliations
- Imperial College London (GB)
- University of Geneva (CH)
- The University of Texas Southwestern Medical Center (US)
- University of Pisa (IT)
- Vita-Salute San Raffaele University (IT)
- University of Oxford (GB)
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2013-09-09
- Volume
- 123
- Issue
- 10
- Pages
- 4182-4194
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC4382273
- OpenAlex
- W2065285024
- Cited by
- 210
- References
- 12
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 14 · 2023: 14 · 2022: 15 · 2021: 23 · 2020: 19 · 2019: 14 · 2018: 17 · 2017: 22 · 2016: 13 · 2015: 25 · 2014: 24 · 2013: 1
- FWCI
- 19.12
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- National Science Foundation (FP7/2007-2013, 0004431)
- Wellcome Trust (FP7/2007–2013, 098424, WT098424AIA)
- European Federation of Pharmaceutical Industries and Associations (FP7/20072013)
- Diabetes UK (11/0004210, 12/0004431)
- European Commission (289932, EU-FP7, 2007–2013, CR32I3_129987, FP7 2007-2013, FP7/2007, 99-2012-775, 222980)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (FP7/2007-2013, 141162, 99-2012-775, 129987, BETATRAIN 289932, BETAIMAGE 222980, 310030)
- Innovative Medicines Initiative (FP7/2007‐2013, 155005)
- East China Institute of Technology
- National Institutes of Health (FP7/2007-2013)
- Medical Research Council (MR/K001981/1, MR/J0003042/1, EU FP7)
- National Institute of General Medical Sciences (R01GM077593)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
- Keywords
- lipotoxicity, pancreatic beta cells, incretins, glucagon-like peptide-1, glucose-dependent insulinotropic polypeptide, insulin secretion, type 2 diabetes, body mass index, high-fat diet, in situ imaging, glucose homeostasis
- MeSH terms
- Insulin Secretion, Animals, Blood Glucose, Cell Communication, Cells, Cultured, Diabetes Mellitus, Type 2, Fatty Acids, Nonesterified, Glucose, Homeostasis, Humans, Insulin, Mice, Inbred C57BL, Species Specificity, Body Mass Index, Gap Junctions, Calcium Signaling, Insulin-Secreting Cells, Mice, Glucagon-Like Peptide 1, Incretins, Diet, High-Fat
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