DNA damage to β cells in culture recapitulates features of senescent β cells that accumulate in type 1 diabetes.
DNA damage to β cells in culture recapitulates features of senescent β cells that accumulate in type 1 diabetes.
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DOI:
10.1016/j.molmet.2022.101524
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发表时间:
2022-08
影响因子:
8.1
通讯作者:
Thompson, Peter J.
中科院分区:
文献类型:
--
作者:
Brawerman, Gabriel;Pipella, Jasmine;Thompson, Peter J.
Type 1 Diabetes (T1D) is characterized by progressive loss of insulin-producing pancreatic β cells as a result of autoimmune destruction. In addition to β cell death, recent work has shown that subpopulations of β cells acquire dysfunction during T1D. We previously reported that β cells undergoing a DNA damage response (DDR) and senescence accumulate during the pathogenesis of T1D. However, the question of how senescence develops in β cells has not been investigated. Here, we tested the hypothesis that unrepaired DNA damage in the context of genetic susceptibility triggers β cell senescence using culture models including the mouse NIT1 β cell line derived from the T1D-susceptible nonobese diabetic (NOD) strain, human donor islets and EndoC β cells. DNA damage was chemically induced using etoposide or bleomycin and cells or islets were analyzed by a combination of molecular assays for senescence phenotypes including Western blotting, qRT-PCR, Luminex assays, flow cytometry and histochemical staining. RNA-seq was carried out to profile global transcriptomic changes in human islets undergoing DDR and senescence. Insulin ELISAs were used to quantify glucose-stimulated insulin secretion from chemically-induced senescent human islets, EndoC β cells and mouse β cell lines in culture. Sub-lethal DNA damage in NIT1 cells led to several classical hallmarks of senescence including sustained DDR activation, growth arrest, enlarged flattened morphology and a senescence-associated secretory phenotype (SASP) resembling what occurs in primary β cells during T1D in NOD mice. These phenotypes differed between NIT1 cells and the MIN6 β cell line derived from a non-T1D susceptible mouse strain. RNA-seq analysis of DNA damage-induced senescence in human islets from two different donors revealed a p53 transcriptional program and upregulation of prosurvival and SASP genes, with inter-donor variability in this response. Inter-donor variability in human islets was also apparent in the extent of persistent DDR activation and SASP at the protein level. Notably, chemically induced DNA damage also led to DDR activation and senescent phenotypes in EndoC-βH5 human β cells, confirming that this response can occur directly in a human β cell line. Finally, DNA damage led to different effects on glucose-stimulated insulin secretion in mouse β cell lines as compared with human islets and EndoC β cells. Taken together, these findings suggest that some of the phenotypes of senescent β cells that accumulate during the development of T1D in the NOD mouse and humans can be modeled by chemically induced DNA damage to mouse β cell lines, human islets and EndoC β cells in culture. The differences between β cells from different mouse strains and different human islet donors and EndoC β cells highlights species differences and the role for genetic background in modifying the β cell response to DNA damage and its effects on insulin secretion. These culture models will be useful tools to understand some of the mechanisms of β cell senescence in T1D. DNA damage elicits senescent phenotypes in mouse β cell lines. DNA damage induces a p53 program and senescent phenotypes in human islets and EndoC-βH5 cells. DNA damage-induced senescence leads to different effects on insulin secretion depending on the culture model.
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影响因子:
30.8
作者:
Dooley J;Tian L;Schonefeldt S;Delghingaro-Augusto V;Garcia-Perez JE;Pasciuto E;Di Marino D;Carr EJ;Oskolkov N;Lyssenko V;Franckaert D;Lagou V;Overbergh L;Vandenbussche J;Allemeersch J;Chabot-Roy G;Dahlstrom JE;Laybutt DR;Petrovsky N;Socha L;Gevaert K;Jetten AM;Lambrechts D;Linterman MA;Goodnow CC;Nolan CJ;Lesage S;Schlenner SM;Liston A
通讯作者:
Liston A
影响因子:
3.3
作者:
Freund A;Laberge RM;Demaria M;Campisi J
通讯作者:
Campisi J
DOI:
10.1016/s2213-8587(21)00139-x
发表时间:
2021-08
期刊:
The lancet. Diabetes & endocrinology
影响因子:
--
作者:
Gitelman SE;Bundy BN;Ferrannini E;Lim N;Blanchfield JL;DiMeglio LA;Felner EI;Gaglia JL;Gottlieb PA;Long SA;Mari A;Mirmira RG;Raskin P;Sanda S;Tsalikian E;Wentworth JM;Willi SM;Krischer JP;Bluestone JA;Gleevec Trial Study Group
通讯作者:
Gleevec Trial Study Group
影响因子:
8
作者:
Fischer M
通讯作者:
Fischer M
影响因子:
8.1
作者:
Benazra, Marion;Lecomte, Marie-Jose;Ravassard, Philippe
通讯作者:
Ravassard, Philippe