796
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Downregulation of Glis3 in INS1 cells exposed to chronically elevated glucose contributes to glucotoxicity-associated β cell dysfunction

, & ORCID Icon
Article: 2344622 | Received 06 Dec 2023, Accepted 15 Apr 2024, Published online: 23 Apr 2024

References

  • 2. Classification and diagnosis of diabetes: standards of medical care in diabetes—2021. Diabetes Care. 2021;44(Supplement_1):S15–16. doi:10.2337/dc21-S002.
  • Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and β-cell dysfunction. Endocr Rev. 2008;29(3):351–366. doi:10.1210/er.2007-0023.
  • Swisa A, Glaser B, Dor Y. Metabolic stress and compromised identity of pancreatic beta cells. Front Genet. 2017;8:21. doi:10.3389/fgene.2017.00021.
  • LeRoith D. Beta-cell dysfunction and insulin resistance in type 2 diabetes: role of metabolic and genetic abnormalities. Am J Med. 2002;113(Suppl 6A):3s–11s. doi:10.1016/s0002-9343(02)01276-7.
  • Kawahito S, Kitahata H, Oshita S. Problems associated with glucose toxicity: role of hyperglycemia-induced oxidative stress. World J Gastroenterol. 2009;15(33):4137–4142. doi:10.3748/wjg.15.4137.
  • Andrali SS, Sampley ML, Vanderford NL, Ozcan S. Glucose regulation of insulin gene expression in pancreatic β-cells. Biochem J. 2008;415(1):1–10. doi:10.1042/BJ20081029.
  • Melloul D, Marshak S, Cerasi E. Regulation of insulin gene transcription. Diabetologia. 2002;45(3):309–326. doi:10.1007/s00125-001-0728-y.
  • Ohneda K, Hooi E, German M. Regulation of insulin gene transcription. Semin Cell Dev Biol. 2000;11(4):227–233. doi:10.1006/scdb.2000.0171.
  • Kang HS, Kim Y-S, ZeRuth G, Beak JY, Gerrish K, Kilic G, Sosa-Pineda B, Jensen J, Foley J, Jetten AM. et al. Transcription factor Glis3, a novel critical player in the regulation of pancreatic β-cell development and insulin gene expression. Mol Cell biol. 2009;29(24):6366–6379. doi:10.1128/MCB.01259-09.
  • Yang Y, Chang BH, Samson SL, Li MV, Chan L. The Krüppel-like zinc finger protein Glis3 directly and indirectly activates insulin gene transcription. Nucleic Acids Res. 2009;37(8):2529–2538. doi:10.1093/nar/gkp122.
  • Senee V, Chelala C, Duchatelet S, Feng D, Blanc H, Cossec J-C, Charon C, Nicolino M, Boileau P, Cavener DR. et al. Mutations in GLIS3 are responsible for a rare syndrome with neonatal diabetes mellitus and congenital hypothyroidism. Nat Genet. 2006;38(6):682–687. doi:10.1038/ng1802.
  • Dimitri P, Warner JT, Minton JAL, Patch AM, Ellard S, Hattersley AT, Barr S, Hawkes D, Wales JK, Gregory JW. et al. Novel GLIS3 mutations demonstrate an extended multisystem phenotype. Eur J Endocrinol. 2011;164(3):437–443. doi:10.1530/EJE-10-0893.
  • Sarıkaya E, Kendirci M, Demir M, Dündar M. Neonatal diabetes, congenital hypothyroidism, and congenital glaucoma coexistence: a case of GLIS3 mutation. J Clin Res Pediatr Endocrinol. 2022;15(4):426–430. doi:10.4274/jcrpe.galenos.2022.2021-12-19.
  • Inshaw JRJ, Sidore C, Cucca F, Stefana MI, Crouch DJM, McCarthy MI, Mahajan A, Todd JA. Analysis of overlapping genetic association in type 1 and type 2 diabetes. Diabetologia. 2021;64(6):1342–1347. doi:10.1007/s00125-021-05428-0.
  • Inshaw JRJ, Cutler AJ, Crouch DJM, Wicker LS, Todd JA. Genetic variants predisposing most strongly to type 1 diabetes diagnosed under age 7 years lie near candidate genes that function in the immune system and in pancreatic β-cells. Diabetes Care. 2020;43(1):169–177. doi:10.2337/dc19-0803.
  • Boesgaard TW, Grarup N, Jørgensen T, Borch-Johnsen K, Hansen T, Pedersen O. Variants at DGKB/TMEM195, ADRA2A, GLIS3 and C2CD4B loci are associated with reduced glucose-stimulated beta cell function in middle-aged Danish people. Diabetologia. 2010;53(8):1647–1655. doi:10.1007/s00125-010-1753-5.
  • Cho YS, Chen C-H, Hu C, Long J, Hee Ong RT, Sim X, Takeuchi F, Wu Y, Go MJ, Yamauchi T. et al. Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians. Nat Genet. 2012;44(1):67–72. doi:10.1038/ng.1019.
  • Hu C, Zhang R, Wang C, Wang J, Ma X, Hou X, Lu J, Yu W, Jiang F, Bao Y. et al. Variants from GIPR, TCF7L2, DGKB, MADD, CRY2, GLIS3, PROX1, SLC30A8 and IGF1 are associated with glucose metabolism in the Chinese. PLOS ONE. 2010;5(11):e15542. doi:10.1371/journal.pone.0015542.
  • Liu C, Li H, Qi L, Loos RJF, Qi Q, Lu L, Gan W, Lin X. Variants in GLIS3 and CRY2 are associated with type 2 diabetes and impaired fasting glucose in Chinese Hans. PLOS ONE. 2011;6(6):e21464. doi:10.1371/journal.pone.0021464.
  • Rees SD, Hydrie MZI, O’Hare JP, Kumar S, Shera AS, Basit A, Barnett AH, Kelly MA. Effects of 16 genetic variants on fasting glucose and type 2 diabetes in South Asians: ADCY5 and GLIS3 variants may predispose to type 2 diabetes. PLOS ONE. 2011;6(9):e24710. doi:10.1371/journal.pone.0024710.
  • Santin I, Eizirik DL. Candidate genes for type 1 diabetes modulate pancreatic islet inflammation and beta-cell apoptosis. Diabetes Obes Metab. 2013;15(Suppl 3):71–81. doi:10.1111/dom.12162.
  • Harmon JS, Stein R, Robertson RP. Oxidative stress-mediated, post-translational loss of MafA protein as a contributing mechanism to loss of insulin gene expression in glucotoxic beta cells. J Biol Chem. 2005;280(12):11107–11113. doi:10.1074/jbc.M410345200.
  • Kawamori D, Kajimoto Y, Kaneto H, Umayahara Y, Fujitani Y, Miyatsuka T, Watada H, Leibiger IB, Yamasaki Y, Hori M. et al. Oxidative stress induces nucleo-cytoplasmic translocation of pancreatic transcription factor PDX-1 through activation of c-Jun NH(2)-terminal kinase. Diabetes. 2003;52(12):2896–2904. doi:10.2337/diabetes.52.12.2896.
  • Kaneto H, Matsuoka TA. Involvement of oxidative stress in suppression of insulin biosynthesis under diabetic conditions. Int J Mol Sci. 2012;13(12):13680–13690. doi:10.3390/ijms131013680.
  • Olson LK, Redmon JB, Towle HC, Robertson RP. Chronic exposure of HIT cells to high glucose concentrations paradoxically decreases insulin gene transcription and alters binding of insulin gene regulatory protein. J Clin Invest. 1993;92(1):514–519. doi:10.1172/jci116596.
  • Sharma A, Olson LK, Robertson RP, Stein R. The reduction of insulin gene transcription in HIT-T15 beta cells chronically exposed to high glucose concentration is associated with the loss of RIPE3b1 and STF-1 transcription factor expression. Mol Endocrinol. 1995;9(9):1127–1134. doi:10.1210/mend.9.9.7491105.
  • ZeRuth GT, Takeda Y, Jetten AM. The Krüppel-like protein gli-similar 3 (Glis3) functions as a key regulator of insulin transcription. Mol Endocrinol. 2013;27(10):1692–1705. doi:10.1210/me.2013-1117.
  • Raum JC, Gerrish K, Artner I, Henderson E, Guo M, Sussel L, Schisler JC, Newgard CB, Stein R. FoxA2, Nkx2.2, and PDX-1 regulate Islet β-cell-specific mafA expression through conserved sequences located between base Pairs −8118 and −7750 upstream from the transcription start site. Mol Cell biol. 2006;26(15):5735–5743. doi:10.1128/mcb.00249-06.
  • Raum JC, Hunter CS, Artner I, Henderson E, Guo M, Elghazi L, Sosa-Pineda B, Ogihara T, Mirmira RG, Sussel L. et al. Islet β-cell-specific MafA transcription requires the 5′-flanking conserved region 3 control domain. Mol Cell Biol. 2010;30(17):4234–4244. doi:10.1128/mcb.01396-09.
  • Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JRJ, Joung JK. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol. 2013;31(3):227–229. doi:10.1038/nbt.2501.
  • Lee KM, Seo YJ, Kim M-K, Seo H-A, Jeong J-Y, Choi H-S, Lee I-K, Park K-G. Mediation of glucolipotoxicity in INS-1 rat insulinoma cells by small heterodimer partner interacting leucine zipper protein (SMILE). Biochem Bioph Res Co. 2012;419(4):768–773. doi:10.1016/j.bbrc.2012.02.098.
  • Park KG, Lee K-M, Seo H-Y, Suh J-H, Kim H-S, Wang L, Won K-C, Lee H-W, Park J-Y, Lee K-U. et al. Glucotoxicity in the INS-1 rat insulinoma cell line is mediated by the orphan nuclear receptor small heterodimer partner. Diabetes. 2007;56(2):431–437. doi:10.2337/db06-0753.
  • Dinić S, Arambašić Jovanović J, Uskoković A, Mihailović M, Grdović N, Tolić A, Rajić J, Đorđević M, Vidaković M. Oxidative stress-mediated beta cell death and dysfunction as a target for diabetes management. Front Endocrinol. 2022;13:1006376. doi:10.3389/fendo.2022.1006376.
  • Beak JY, Kang HS, Kim YS, Jetten AM. Functional analysis of the zinc finger and activation domains of Glis3 and mutant Glis3(NDH1). Nucleic Acids Res. 2008;36(5):1690–1702. doi:10.1093/nar/gkn009.
  • Pullen TJ, Rutter GA. When less is more: the forbidden fruits of gene repression in the adult β-cell. Diabetes Obes Metab. 2013;15(6):503–512. doi:10.1111/dom.12029.
  • Pullen TJ, Khan AM, Barton G, Butcher SA, Sun G, Rutter GA. Identification of genes selectively disallowed in the pancreatic islet. Islets. 2010;2(2):89–95. doi:10.4161/isl.2.2.11025.
  • Quintens R, Hendrickx N, Lemaire K, Schuit F. Why expression of some genes is disallowed in β-cells. Biochem Soc Trans. 2008;36(3):300–305. doi:10.1042/bst0360300.
  • Ebrahimi AG, Hollister-Lock J, Sullivan BA, Tsuchida R, Bonner-Weir S, Weir GC. Beta cell identity changes with mild hyperglycemia: implications for function, growth, and vulnerability. Mol Metab. 2020;35:100959. doi:10.1016/j.molmet.2020.02.002.
  • Bensellam M, Jonas JC, Laybutt DR. Mechanisms of β-cell dedifferentiation in diabetes: recent findings and future research directions. J Endocrinol. 2018;236(2):R109–r143. doi:10.1530/joe-17-0516.
  • Remedi MS, Emfinger C. Pancreatic β-cell identity in diabetes. Diabetes Obes Metab. 2016;18(S1):110–116. doi:10.1111/dom.12727.
  • Jonas JC, Sharma A, Hasenkamp W, Ilkova H, Patanè G, Laybutt R, Bonner-Weir S, Weir GC. Chronic hyperglycemia triggers loss of pancreatic β cell differentiation in an animal model of diabetes. J Biol Chem. 1999;274(20):14112–14121. doi:10.1074/jbc.274.20.14112.
  • Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell. 2012;150(6):1223–1234. doi:10.1016/j.cell.2012.07.029.
  • Brereton MF, Iberl M, Shimomura K, Zhang Q, Adriaenssens AE, Proks P, Spiliotis II, Dace W, Mattis KK, Ramracheya R. et al. Reversible changes in pancreatic islet structure and function produced by elevated blood glucose. Nat Commun. 2014;5(1):4639. doi:10.1038/ncomms5639.
  • Cinti F, Bouchi R, Kim-Muller JY, Ohmura Y, Sandoval PR, Masini M, Marselli L, Suleiman M, Ratner LE, Marchetti P. et al. Evidence of β-cell dedifferentiation in human type 2 diabetes. J Clin Endocr Metab. 2016;101(3):1044–1054. doi:10.1210/jc.2015-2860.
  • Yang Y, Chang BH, Chan L. Sustained expression of the transcription factor GLIS3 is required for normal beta cell function in adults. EMBO Mol Med. 2013;5(1):92–104. doi:10.1002/emmm.201201398.
  • Akerman I, Maestro MA, De Franco E, Grau V, Flanagan S, García-Hurtado J, Mittler G, Ravassard P, Piemonti L, Ellard S. et al. Neonatal diabetes mutations disrupt a chromatin pioneering function that activates the human insulin gene. Cell Rep. 2021;35(2):108981. doi:10.1016/j.celrep.2021.108981.
  • Dooley J, Tian L, Schonefeldt S, Delghingaro-Augusto V, Garcia-Perez JE, Pasciuto E, Di Marino D, Carr EJ, Oskolkov N, Lyssenko V. et al. Genetic predisposition for beta cell fragility underlies type 1 and type 2 diabetes. Nat Genet. 2016;48(5):519–527. doi:10.1038/ng.3531.
  • Lu Y, Li Y, Li G, Lu H. Identification of potential markers for type 2 diabetes mellitus via bioinformatics analysis. Mol Med Rep. 2020;22(3):1868–1882. doi:10.3892/mmr.2020.11281.
  • Marselli L, Thorne J, Dahiya S, Sgroi DC, Sharma A, Bonner-Weir S, Marchetti P, Weir GC. Gene expression profiles of beta-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes. PLOS ONE. 2010;5(7):e11499. doi:10.1371/journal.pone.0011499.
  • Taneera J, Lang S, Sharma A, Fadista J, Zhou Y, Ahlqvist E, Jonsson A, Lyssenko V, Vikman P, Hansson O. et al. A systems genetics approach identifies genes and pathways for type 2 diabetes in human islets. Cell Metab. 2012;16(1):122–134. doi:10.1016/j.cmet.2012.06.006.
  • Scoville D, Lichti-Kaiser K, Grimm S, Jetten A. GLIS3 binds pancreatic beta cell regulatory regions alongside other islet transcription factors. J Endocrinol. 2019;243(1):1–14. doi:10.1530/joe-19-0182.
  • Nishimura W, Takahashi S, Yasuda K. MafA is critical for maintenance of the mature beta cell phenotype in mice. Diabetologia. 2015;58(3):566–574. doi:10.1007/s00125-014-3464-9.
  • Dai C, Kayton NS, Shostak A, Poffenberger G, Cyphert HA, Aramandla R, Thompson C, Papagiannis IG, Emfinger C, Shiota M. et al. Stress-impaired transcription factor expression and insulin secretion in transplanted human islets. J Clin Invest. 2016;126(5):1857–1870. doi:10.1172/jci83657.
  • Deng Z, Kuno A, Ojima M, Takahashi S. MafB maintains β-cell identity under MafA-deficient conditions. Mol Cell Biol. 2022;42(8):e0054121. doi:10.1128/mcb.00541-21.
  • Boidot R, Végran F, Meulle A, Le Breton A, Dessy C, Sonveaux P, Lizard-Nacol S, Feron O. Regulation of monocarboxylate transporter MCT1 expression by p53 mediates inward and outward lactate fluxes in tumors. Cancer Res. 2012;72(4):939–948. doi:10.1158/0008-5472.can-11-2474.
  • Huang D, Hubbard CJ, Jungmann RA. Lactate dehydrogenase a subunit messenger RNA stability is synergistically regulated via the protein kinase a and C signal transduction pathways. Mol Endocrinol. 1995;9(8):994–1004. doi:10.1210/mend.9.8.7476996.
  • Hoard TM, Yang XP, Jetten AM, ZeRuth GT. PIAS-family proteins negatively regulate Glis3 transactivation function through SUMO modification in pancreatic β cells. Heliyon. 2018;4(7):e00709. doi:10.1016/j.heliyon.2018.e00709.
  • Liang J, Chirikjian M, Pajvani UB, Bartolomé A. MafA regulation in β-cells: from transcriptional to post-translational mechanisms. Biomolecules. 2022;12(4):535. doi:10.3390/biom12040535.