Increased proliferation and altered cell cycle regulation in pancreatic stem cells derived from patients with congenital hyperinsulinism
Autoři:
Sophie G. Kellaway aff001; Karolina Mosinska aff001; Zainaba Mohamed aff002; Alexander Ryan aff001; Stephen Richardson aff001; Melanie Newbould aff003; Indraneel Banerjee aff002; Mark J. Dunne aff001; Karen E. Cosgrove aff001
Působiště autorů:
Faculty of Biology Medicine and Health, School of Medicine, Division of Diabetes Endocrinology and Gastroenterology, University of Manchester, Manchester, United Kingdom
aff001; Department of Paediatric Endocrinology, Royal Manchester Children’s Hospital, Manchester, United Kingdom
aff002; Department of Paediatric Histopathology, Royal Manchester Children’s Hospital, Manchester, United Kingdom
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222350
Souhrn
Congenital hyperinsulinism (CHI) is characterised by inappropriate insulin secretion causing profound hypoglycaemia and brain damage if inadequately controlled. Pancreatic tissue isolated from patients with diffuse CHI shows abnormal proliferation rates, the mechanisms of which are not fully resolved. Understanding cell proliferation in CHI may lead to new therapeutic options, alongside opportunities to manipulate β-cell mass in patients with diabetes. We aimed to generate cell-lines from CHI pancreatic tissue to provide in vitro model systems for research. Three pancreatic mesenchymal stem cell-lines (CHIpMSC1-3) were derived from patients with CHI disease variants: focal, atypical and diffuse. All CHIpMSC lines demonstrated increased proliferation compared with control adult-derived pMSCs. Cell cycle alterations including increased CDK1 levels and decreased p27Kip1 nuclear localisation were observed in CHIpMSCs when compared to control pMSCs. In conclusion, CHIpMSCs are a useful in vitro model to further understand the cell cycle alterations leading to increased islet cell proliferation in CHI.
Klíčová slova:
Biology and life sciences – Cell biology – Cell processes – Cell cycle and cell division – Biochemistry – Hormones – Anatomy – Endocrine system – Exocrine glands – Physical sciences – Chemistry – Chemical compounds – Organic compounds – Carbohydrates – Monosaccharides – Glucose – Organic chemistry – Medicine and health sciences – Endocrinology – Diabetic endocrinology – Insulin – Pancreas – Research and analysis methods – Spectrum analysis techniques – Spectrophotometry – Cytophotometry – Flow cytometry – Specimen preparation and treatment – Staining – Cell staining – Group-specific staining – Alizarin staining – Nuclear staining
Zdroje
1. Dunne MJ, Cosgrove KE, Shepherd RM, Aynsley-Green A, Lindley KJ. Hyperinsulinism in Infancy: From Basic Science to Clinical Disease. Physiological Reviews. 2004;84(1):239–75. doi: 10.1152/physrev.00022.2003 14715916
2. Verkarre V, Fournet JC, de Lonlay P, Gross-Morand MS, Devillers M, Rahier J, et al. Paternal mutation of the sulfonylurea receptor (SUR1) gene and maternal loss of 11p15 imprinted genes lead to persistent hyperinsulinism in focal adenomatous hyperplasia. The Journal of Clinical Investigation. 1998;102(7):1286–91. doi: 10.1172/JCI4495 9769320
3. Glaser B, Ryan F, Donath M, Landau H, Stanley CA, Baker L, et al. Hyperinsulinism caused by paternal-specific inheritance of a recessive mutation in the sulfonylurea-receptor gene. Diabetes. 1999;48(8):1652–7. doi: 10.2337/diabetes.48.8.1652 10426386
4. Fournet J-C, Mayaud C, de Lonlay P, Gross-Morand M-S, Verkarre V, Castanet M, et al. Unbalanced Expression of 11p15 Imprinted Genes in Focal Forms of Congenital Hyperinsulinism: Association with a Reduction to Homozygosity of a Mutation in ABCC8 or KCNJ11. The American Journal of Pathology. 2001;158(6):2177–84. doi: 10.1016/S0002-9440(10)64689-5 11395395
5. Kassem SA, Ariel I, Thornton PS, Hussain K, Smith V, Lindley KJ, et al. p57KIP2 Expression in Normal Islet Cells and in Hyperinsulinism of Infancy. Diabetes. 2001;50(12):2763–9. doi: 10.2337/diabetes.50.12.2763 11723059
6. Glaser B, Thornton P, Otonkoski T, Junien C. Genetics of neonatal hyperinsulinism. Archives of Disease in Childhood—Fetal and Neonatal Edition. 2000;82(2):F79–F86. doi: 10.1136/fn.82.2.F79 10685979
7. Dunne MJ, Kane C, Shepherd RM, Sanchez JA, James RFL, Johnson PRV, et al. Familial Persistent Hyperinsulinemic Hypoglycemia of Infancy and Mutations in the Sulfonylurea Receptor. New England Journal of Medicine. 1997;336(10):703–6. doi: 10.1056/NEJM199703063361005 9041101
8. Arnoux J-B, Verkarre V, Saint-Martin C, Montravers F, Brassier A, Valayannopoulos V, et al. Congenital hyperinsulinism: current trends in diagnosis and therapy. Orphanet Journal of Rare Diseases. 2011;6(1):1–14.
9. Henquin J-C, Sempoux C, Marchandise J, Godecharles S, Guiot Y, Nenquin M, et al. Congenital Hyperinsulinism Caused by Hexokinase I Expression or Glucokinase-Activating Mutation in a Subset of β-Cells. Diabetes. 2013;62(5):1689–96. doi: 10.2337/db12-1414 23274908
10. Han B, Mohamed Z, Estebanez MS, Craigie RJ, Newbould M, Cheesman E, et al. Atypical Forms of Congenital Hyperinsulinism in Infancy Are Associated With Mosaic Patterns of Immature Islet Cells. The Journal of Clinical Endocrinology & Metabolism. 2017;102(9):3261–7.
11. Alexandrescu S, Tatevian N, Olutoye O, Brown RE. Persistent hyperinsulinemic hypoglycemia of infancy: constitutive activation of the mTOR pathway with associated exocrine-islet transdifferentiation and therapeutic implications. International Journal of Clinical and Experimental Pathology. 2010;3(7):691–705. 20830240
12. Salisbury RJ, Han B, Jennings RE, Berry AA, Stevens A, Mohamed Z, et al. Altered Phenotype of β-Cells and Other Pancreatic Cell Lineages in Patients With Diffuse Congenital Hyperinsulinism in Infancy Caused by Mutations in the ATP-Sensitive K-Channel. Diabetes. 2015;64(9):3182–8. doi: 10.2337/db14-1202 25931474
13. Bertoli C, Skotheim JM, de Bruin RAM. Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol. 2013;14(8):518–28. doi: 10.1038/nrm3629 23877564
14. Morgan DO. Principles of CDK regulation. Nature. 1995;374(6518):131–4. doi: 10.1038/374131a0 7877684
15. Satyanarayana A, Kaldis P. Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene. 2009;28(33):2925–39. doi: 10.1038/onc.2009.170 19561645
16. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature. 2004;429(6987):41–6 doi: 10.1038/nature02520 15129273
17. Shimomura K, Tusa M, Iberl M, Brereton MF, Kaizik S, Proks P, et al. A Mouse Model of Human Hyperinsulinism Produced by the E1506K Mutation in the Sulphonylurea Receptor SUR1. Diabetes. 2013;62(11):3797–806. doi: 10.2337/db12-1611 23903354
18. Kulkarni RN, Mizrachi E-B, Ocana AG, Stewart AF. Human β-Cell Proliferation and Intracellular Signaling. Driving in the Dark Without a Road Map. 2012;61(9):2205–13.
19. Fiaschi-Taesch NM, Kleinberger JW, Salim FG, Troxell R, Wills R, Tanwir M, et al. Human Pancreatic β-Cell G1/S Molecule Cell Cycle Atlas. Diabetes. 2013;62(7):2450–9. doi: 10.2337/db12-0777 23493570
20. Burrow KL, Hoyland JA, Richardson SM. Human Adipose-Derived Stem Cells Exhibit Enhanced Proliferative Capacity and Retain Multipotency Longer than Donor-Matched Bone Marrow Mesenchymal Stem Cells during Expansion In Vitro. Stem Cells International. 2017;2017:15.
21. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause DS, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7. doi: 10.1080/14653240600855905 16923606
22. Russ HA, Ravassard P, Kerr-Conte J, Pattou F, Efrat S. Epithelial-Mesenchymal Transition in Cells Expanded In Vitro from Lineage-Traced Adult Human Pancreatic Beta Cells. PLoS ONE. 2009;4(7):e6417. doi: 10.1371/journal.pone.0006417 19641613
23. Malumbres M, Sotillo Ro, Santamaría D, Galán J, Cerezo A, Ortega S, et al. Mammalian Cells Cycle without the D-Type Cyclin-Dependent Kinases Cdk4 and Cdk6. Cell. 2004;118(4):493–504. doi: 10.1016/j.cell.2004.08.002 15315761
24. Eberhardt M, Salmon P, von Mach M-A, Hengstler JG, Brulport M, Linscheid P, et al. Multipotential nestin and Isl-1 positive mesenchymal stem cells isolated from human pancreatic islets. Biochemical and Biophysical Research Communications. 2006;345(3):1167–76. doi: 10.1016/j.bbrc.2006.05.016 16713999
25. Gallo R, Gambelli F, Gava B, Sasdelli F, Tellone V, Masini M, et al. Generation and expansion of multipotent mesenchymal progenitor cells from cultured human pancreatic islets. Cell Death Differ. 2007;14(11):1860–71. doi: 10.1038/sj.cdd.4402199 17612586
26. Lima MJ, Muir KR, Docherty HM, Drummond R, McGowan NWA, Forbes S, et al. Suppression of Epithelial-to-Mesenchymal Transitioning Enhances Ex Vivo Reprogramming of Human Exocrine Pancreatic Tissue Toward Functional Insulin-Producing β-Like Cells. Diabetes. 2013;62(8):2821–33. doi: 10.2337/db12-1256 23610058
27. Joglekar MV, Joglekar VM, Joglekar SV, Hardikar AA. Human fetal pancreatic insulin-producing cells proliferate in vitro. Journal of Endocrinology. 2009;201(1):27–36. doi: 10.1677/JOE-08-0497 19171567
28. LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, Chou HS, et al. New functional activities for the p21 family of CDK inhibitors. Genes & Development. 1997;11(7):847–62.
29. Zhang Li, Jiang Yang, Lei Cai, et al. GLP-1 ameliorates the proliferation activity of INS-1 cells inhibited by intermittent high glucose concentrations through the regulation of cyclins. Molecular Medicine Reports. 2014;10(2):683–8. doi: 10.3892/mmr.2014.2265 24859892
30. Hershko A. Mechanisms and regulation of the degradation of cyclin B. Philosophical Transactions of the Royal Society B: Biological Sciences. 1999;354(1389):1571–6.
31. Hall E, Nitert MD, Volkov P, Malmgren S, Mulder H, Bacos K, et al. The effects of high glucose exposure on global gene expression and DNA methylation in human pancreatic islets. Molecular and Cellular Endocrinology. 2017.
32. Chen X, Niu H, Yu Y, Wang J, Zhu S, Zhou J, et al. Enrichment of Cdk1-cyclins at DNA double-strand breaks stimulates Fun30 phosphorylation and DNA end resection. Nucleic Acids Research. 2016;44(6):2742–53. doi: 10.1093/nar/gkv1544 26801641
33. Tornovsky-Babeay S, Dadon D, Ziv O, Tzipilevich E, Kadosh T, Schyr-Ben Haroush R, et al. Type 2 Diabetes and Congenital Hyperinsulinism Cause DNA Double-Strand Breaks and p53 Activity in β Cells. Cell Metabolism. 2014;19(1):109–21. doi: 10.1016/j.cmet.2013.11.007 24332968
34. Paris M, Bernard-Kargar C, Berthault M-F, Bouwens L, Ktorza A. Specific and Combined Effects of Insulin and Glucose on Functional Pancreatic β-Cell Mass in Vivo in Adult Rats. Endocrinology. 2003;144(6):2717–27. doi: 10.1210/en.2002-221112 12746336
35. Annicotte J-S, Blanchet E, Chavey C, Iankova I, Costes S, Assou S, et al. The CDK4-pRB-E2F1 pathway controls insulin secretion. Nat Cell Biol. 2009;11(8):1017–23. doi: 10.1038/ncb1915 19597485
Článek vyšel v časopise
PLOS One
2019 Číslo 9
- Případ Bulovka: Jak postupují jiné nemocnice, aby podobným tragédiím zabránily?
- Jak často se u masových střelců vyskytují duševní choroby?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Klinický význam menších rozestupů mezi silami přípravků s levothyroxinem v léčbě hypotyreózy
Nejčtenější v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy