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Research Article

Dynamic regulation of pancreatic β cell function and gene expression by the SND1 coregulator in vitro

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Article: 2267725 | Received 17 Aug 2023, Accepted 03 Oct 2023, Published online: 15 Oct 2023

References

  • Zhang P, Torres K, Liu X, Liu CG, Pollock RE. An overview of chromatin-regulating proteins in cells. Curr Protein Pept Sci. 2016;17(5):401–15. doi:10.2174/1389203717666160122120310.
  • Stallcup MR, Poulard C. Gene-specific actions of transcriptional coregulators facilitate physiological plasticity: evidence for a physiological coregulator code. Trends Biochem Sci. 2020;45(6):497–510. doi:10.1016/j.tibs.2020.02.006.
  • Ramazi S, Allahverdi A, Zahiri J. Evaluation of post-translational modifications in histone proteins: a review on histone modification defects in developmental and neurological disorders. J Biosci. 2020;45(1):45. doi:10.1007/s12038-020-00099-2.
  • Gao T, McKenna B, Li C, Reichert M, Nguyen J, Singh T, Yang C, Pannikar A, Doliba N, Zhang T, et al. Pdx1 maintains β cell identity and function by repressing an α cell program. Cell Metab. 2014;19:259–271. doi:10.1016/j.cmet.2013.12.002.
  • Oliver-Krasinski JM, Kasner MT, Yang J, Crutchlow MF, Rustgi AK, Kaestner KH, Stoffers DA. The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice. J Clin Invest. 2009;119:1888–1898. doi:10.1172/JCI37028.
  • Gannon M, Ables ET, Crawford L, Lowe D, Offield MF, Magnuson MA, Wright CVE. Pdx-1 function is specifically required in embryonic β cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Dev Biol. 2008;314:406–417. doi:10.1016/j.ydbio.2007.10.038.
  • Thomas IH, Saini NK, Adhikari A, Lee JM, Kasa-Vubu JZ, Vazquez DM, Menon RK, Chen M, Fajans SS. Neonatal diabetes mellitus with pancreatic agenesis in an infant with homozygous IPF-1 Pro63fsX60 mutation. Pediatr Diabetes. 2009;10:492–496. doi:10.1111/j.1399-5448.2009.00526.x.
  • Abreu GMM, Tarantino RM, da Fonseca ACP, de Souza RB, Soares C, Cabello PH, Rodacki M, Zajdenverg L, Zembrzuski VM, Campos Junior M, et al. PDX1-MODY: a rare missense mutation as a cause of monogenic diabetes. Eur J Med Genet. 2021;64(5):104194. doi:10.1016/j.ejmg.2021.104194.
  • Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, Habener JF. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet. 1997;15(1):106–110. doi:10.1038/ng0197-106.
  • Wang X, Sterr M, Burtscher I, Böttcher A, Beckenbauer J, Siehler J, Meitinger T, Häring HU, Staiger H, Cernilogar FM, et al. Point mutations in the PDX1 transactivation domain impair human beta-cell development and function. Mol Metab. 2019;24:80–97. doi:10.1016/j.molmet.2019.03.006.
  • Macfarlane WM, Frayling TM, Ellard S, Evans JC, Allen LI, Bulman MP, Ayres S, Shepherd M, Clark P, Millward A, et al. Missense mutations in the insulin promoter factor-1 gene predispose to type 2 diabetes. J Clin Invest. 1999;104(9):R33–9. doi:10.1172/JCI7449.
  • Guo S, Dai C, Guo M, Taylor B, Harmon JS, Sander M, Robertson RP, Powers AC, Stein R. Inactivation of specific β cell transcription factors in type 2 diabetes. J Clin Invest. 2013;123:3305–3316. doi:10.1172/JCI65390.
  • McKenna B, Guo M, Reynolds A, Hara M, Stein R. Dynamic recruitment of functionally distinct Swi/Snf chromatin remodeling complexes modulates Pdx1 activity in islet beta cells. Cell Rep. 2015;10:2032–2042. doi:10.1016/j.celrep.2015.02.054.
  • Spaeth JM, Liu JH, Peters D, Guo M, Osipovich AB, Mohammadi F, Roy N, Bhushan A, Magnuson MA, Hebrok M, et al. The Pdx1-bound Swi/Snf chromatin remodeling complex regulates pancreatic progenitor cell proliferation and mature islet β-cell function. Diabetes. 2019;68:1806–1818. doi:10.2337/db19-0349.
  • Davidson RK, Kanojia S, Wu W, Kono T, Xu J, Osmulski M, Bone RN, Casey N, Evans-Molina C, Sims EK, et al. The Chd4 helicase regulates chromatin accessibility and gene expression critical for β-cell function in vivo. Diabetes. 2023;72:746–757. doi:10.2337/db22-0939.
  • Arretxe E, Armengol S, Mula S, Chico Y, Ochoa B, Martinez MJ. Profiling of promoter occupancy by the SND1 transcriptional coactivator identifies downstream glycerolipid metabolic genes involved in TNFalpha response in human hepatoma cells. Nucleic Acids Res. 2015;43:10673–10688. doi:10.1093/nar/gkv858.
  • Callebaut I, Mornon JP. The human EBNA-2 coactivator p100: multidomain organization and relationship to the staphylococcal nuclease fold and to the tudor protein involved in drosophila melanogaster development. Biochem J. 1997;321(Pt 1):125–132. doi:10.1042/bj3210125.
  • Paukku K, Yang J, Silvennoinen O. Tudor and nuclease-like domains containing protein p100 function as coactivators for signal transducer and activator of transcription 5. Mol Endocrinol. 2003;17(9):1805–1814. doi:10.1210/me.2002-0256.
  • Yang J, Aittomaki S, Pesu M, Carter K, Saarinen J, Kalkkinen N, Kieff E, Silvennoinen O. Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. EMBO J. 2002;21:4950–4958. doi:10.1093/emboj/cdf463.
  • Duan Z, Zhao X, Fu X, Su C, Xin L, Saarikettu J, Yang X, Yao Z, Silvennoinen O, Wei M, et al. Tudor-SN, a novel coactivator of peroxisome proliferator-activated receptor γ protein, is essential for adipogenesis. J Biol Chem. 2014;289:8364–8374. doi:10.1074/jbc.M113.523456.
  • Yu L, Di Y, Xin L, Ren Y, Liu X, Sun X, Zhang W, Yao Z, Yang J. SND1 acts as a novel gene transcription activator recognizing the conserved Motif domains of smad promoters, inducing TGFβ1 response and breast cancer metastasis. Oncogene. 2017;36:3903–3914. doi:10.1038/onc.2017.30.
  • Shen M, Wei Y, Kim H, Wan L, Jiang YZ, Hang X, Raba M, Remiszewski S, Rowicki M, Wu C-G, et al. Small-molecule inhibitors that disrupt the MTDH–SND1 complex suppress breast cancer progression and metastasis. Nat Cancer. 2022;3:43–59. doi:10.1038/s43018-021-00279-5.
  • Davidson RK, Weaver SA, Casey N, Kanojia S, Hogarth E, Schneider Aguirre R, Sims EK, Evans-Molina C, Spaeth JM. The Chd4 subunit of the NuRD complex regulates Pdx1-controlled genes involved in β-cell function. J Mol Endocrinol. 2022;69:329–341. doi:10.1530/JME-22-0011.
  • Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB. Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes. 2000;49(3):424–430. doi:10.2337/diabetes.49.3.424.
  • Khoo C, Yang J, Weinrott SA, Kaestner KH, Naji A, Schug J, Stoffers DA. Research resource: the pdx1 cistrome of pancreatic islets. Mol Endocrinol. 2012;26:521–533. doi:10.1210/me.2011-1231.
  • Yin J, Ding J, Huang L, Tian X, Shi X, Zhi L, Song J, Zhang Y, Gao X, Yao Z, et al. SND1 affects proliferation of hepatocellular carcinoma cell line SMMC-7721 by regulating IGFBP3 expression. Anat Rec (Hoboken). 2013;296:1568–1575. doi:10.1002/ar.22737.
  • Nauck MA, D’Alessio DA. Tirzepatide, a dual GIP/GLP-1 receptor co-agonist for the treatment of type 2 diabetes with unmatched effectiveness regrading glycaemic control and body weight reduction. Cardiovasc Diabetol. 2022;21:169. doi:10.1186/s12933-022-01604-7.
  • Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology. 2007;132(6):2131–2157. doi:10.1053/j.gastro.2007.03.054.
  • Ast J, Novak AN, Podewin T, Fine NHF, Jones B, Tomas A, Birke R, Roßmann K, Mathes B, Eichhorst J, et al. Expanded LUXendin color palette for GLP1R detection and visualization in vitro and in vivo. JACS Au. 2022;2:1007–1017. doi:10.1021/jacsau.2c00130.
  • Ast J, Arvaniti A, Fine NHF, Nasteska D, Ashford FB, Stamataki Z, Koszegi Z, Bacon A, Jones BJ, Lucey MA, et al. Super-resolution microscopy compatible fluorescent probes reveal endogenous glucagon-like peptide-1 receptor distribution and dynamics. Nat Commun. 2020;11(1):467. doi:10.1038/s41467-020-14309-w.
  • Eng J, Kleinman WA, Singh L, Singh G, Raufman JP. Isolation and characterization of exendin-4, an exendin-3 analogue, from Heloderma suspectum venom. Further evidence for an exendin receptor on dispersed acini from guinea pig pancreas. J Biol Chem. 1992;267(11):7402–7405. doi:10.1016/S0021-9258(18)42531-8.
  • Thorens B, Porret A, Buhler L, Deng SP, Morel P, Widmann C. Cloning and functional expression of the human islet GLP-1 receptor. Demonstration that exendin-4 is an agonist and exendin-(9-39) an antagonist of the receptor. Diabetes. 1993;42:1678–1682. doi:10.2337/diab.42.11.1678.
  • Drucker DJ, Philippe J, Mojsov S, Chick WL, Habener JF. Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line. Proc Natl Acad Sci USA. 1987;84(10):3434–3438. doi:10.1073/pnas.84.10.3434.
  • Pek JW, Anand A, Kai T. Tudor domain proteins in development. Development. 2012;139(13):2255–2266. doi:10.1242/dev.073304.
  • Yoo BK, Santhekadur PK, Gredler R, Chen D, Emdad L, Bhutia S, Pannell L, Fisher PB, Sarkar D. Increased RNA-induced silencing complex (RISC) activity contributes to hepatocellular carcinoma. Hepatology. 2011;53:1538–1548. doi:10.1002/hep.24216.
  • Saarikettu J, Lehmusvaara S, Pesu M, Junttila I, Partanen J, Sipila P, Poutanen M, Yang J, Haikarainen T, Silvennoinen O, et al. The RNA-binding protein Snd1/Tudor-SN regulates hypoxia-responsive gene expression. FASEB Bioadv. 2023;5:183–198. doi:10.1096/fba.2022-00115.
  • Valineva T, Yang J, Palovuori R, Silvennoinen O. The transcriptional co-activator protein p100 recruits histone acetyltransferase activity to STAT6 and mediates interaction between the CREB-binding protein and STAT6. J Biol Chem. 2005;280(15):14989–14996. doi:10.1074/jbc.M410465200.
  • Wang Y, Wang X, Cui X, Zhuo Y, Li H, Ha C, Xin L, Ren Y, Zhang W, Sun X, et al. Oncoprotein SND1 hijacks nascent MHC-I heavy chain to ER-associated degradation, leading to impaired CD8 + T cell response in tumor. Sci Adv. 2020;6:6. doi:10.1126/sciadv.aba5412.
  • Shao J, Gao F, Zhang B, Zhao M, Zhou Y, He J, Ren L, Yao Z, Yang J, Su C, et al. Aggregation of SND1 in stress granules is associated with the microtubule cytoskeleton during heat shock stimulus. Anat Rec (Hoboken). 2017;300:2192–2199. doi:10.1002/ar.23642.
  • Garcia-Arcos I, Rueda Y, Gonzalez-Kother P, Palacios L, Ochoa B, Fresnedo O. Association of SND1 protein to low density lipid droplets in liver steatosis. J Physiol Biochem. 2010;66(1):73–83. doi:10.1007/s13105-010-0011-0.
  • Li CL, Yang WZ, Chen YP, Yuan HS. Structural and functional insights into human Tudor-SN, a key component linking RNA interference and editing. Nucleic Acids Res. 2008;36(11):3579–3589. doi:10.1093/nar/gkn236.
  • Yu L, Liu X, Cui K, Di Y, Xin L, Sun X, Zhang W, Yang X, Wei M, Yao Z, et al. SND1 acts downstream of TGFβ1 and upstream of Smurf1 to promote breast cancer metastasis. Cancer Res. 2015;75:1275–1286. doi:10.1158/0008-5472.CAN-14-2387.
  • Diao C, Guo P, Yang W, Sun Y, Liao Y, Yan Y, Zhao A, Cai X, Hao J, Hu S, et al. SPT6 recruits SND1 to co-activate human telomerase reverse transcriptase to promote colon cancer progression. Mol Oncol. 2021;15(4):1180–1202. doi:10.1002/1878-0261.12878.
  • Kuruma H, Kamata Y, Takahashi H, Igarashi K, Kimura T, Miki K, Miki J, Sasaki H, Hayashi N, Egawa S, et al. Staphylococcal nuclease domain-containing protein 1 as a potential tissue marker for prostate cancer. Am J Pathol. 2009;174(6):2044–2050. doi:10.2353/ajpath.2009.080776.
  • Liang S, Zhu C, Suo C, Wei H, Yu Y, Gu X, Chen L, Yuan M, Shen S, Li S, et al. Mitochondrion-localized SND1 promotes mitophagy and liver cancer progression through PGAM5. Front Oncol. 2022;12:857968. doi:10.3389/fonc.2022.857968.
  • Villasenor A, Wang ZV, Rivera LB, Ocal O, Asterholm IW, Scherer PE, Brekken RA, Cleaver O, Wilkie TM. Rgs16 and Rgs8 in embryonic endocrine pancreas and mouse models of diabetes. Dis Model Mech. 2010;3:567–580. doi:10.1242/dmm.003210.
  • Huang J, Pashkov V, Kurrasch DM, Yu K, Gold SJ, Wilkie TM. Feeding and fasting controls liver expression of a regulator of G protein signaling (Rgs16) in periportal hepatocytes. Comp Hepatol. 2006;5(1):8. doi:10.1186/1476-5926-5-8.
  • Cerf ME. Beta cell dysfunction and insulin resistance. Front Endocrinol (Lausanne). 2013;4:37. doi:10.3389/fendo.2013.00037.