473
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Silibinin protects GLUTag cells from PA-induced injury via suppressing endoplasmic reticulum stress

, , , , , , , , & show all
Pages 442-450 | Received 26 Jan 2023, Accepted 02 Jun 2023, Published online: 22 Jun 2023

References

  • Al Lawati, J. A. (2017). Diabetes mellitus: A local and global public health emergency! Oman Medical Journal, 32(3), 177–179. https://doi.org/10.5001/omj.2017.34
  • Aslani, M. R., Amani, M., Masrori, N., Boskabady, M. H., Ebrahimi, H. A., & Chodari, L. (2022). Crocin attenuates inflammation of lung tissue in ovalbumin-sensitized mice by altering the expression of endoplasmic reticulum stress markers. Biofactors, 48(1), 204–215. https://doi.org/10.1002/biof.1809
  • Barlow, J., Jensen, V. H., Jastroch, M., & Affourtit, C. (2016a). Palmitate-induced impairment of glucose-stimulated insulin secretion precedes mitochondrial dysfunction in mouse pancreatic islets. Biochemical Journal, 473(4), 487–496. https://doi.org/10.1042/bj20151080
  • Barlow, J., Jensen, V. H., Jastroch, M., & Affourtit, C. (2016b). Palmitate-induced impairment of glucose-stimulated insulin secretion precedes mitochondrial dysfunction in mouse pancreatic islets. Biochemical Journal, 473(4), 487–496. https://doi.org/10.1042/BJ20151080
  • Bell, G. I., Sanchez-Pescador, R., Laybourn, P. J., & Najarian, R. C. (1983). Exon duplication and divergence in the human preproglucagon gene. Nature, 304(5924), 368–371. https://doi.org/10.1038/304368a0
  • Chu, C., Li, D., Zhang, S., Ikejima, T., Jia, Y., Wang, D., & Xu, F. (2018). Role of silibinin in the management of diabetes mellitus and its complications. Archives of Pharmacal Research, 41(8), 785–796. https://doi.org/10.1007/s12272-018-1047-x
  • Cui, Y. Y., Zhao, D. M., Sreevatsan, S., Liu, C. F., Yang, W., Song, Z. Q., Yang, L. F., Barrow, P., & Zhou, X. M. (2016). Mycobacterium bovis induces endoplasmic reticulum stress mediated-apoptosis by activating IRF3 in a Murine macrophage cell line. Frontiers in Cellular and Infection Microbiology, 6, Article 182. https://doi.org/10.3389/fcimb.2016.00182
  • Enjalbert, F., Rapior, S., Nouguier-Soulé, J., Guillon, S., Amouroux, N., & Cabot, C. (2002). Treatment of amatoxin poisoning: 20-year retrospective analysis. Journal of Toxicology: Clinical Toxicology, 40(6), 715–757. https://doi.org/10.1081/clt-120014646
  • Gutniak, M., Orskov, C., Holst, J. J., Ahren, B., & Efendic, S. (1992). Antidiabetogenic effect of glucagon-like peptide-1 (7–36)amide in normal subjects and patients with diabetes mellitus. The New England Journal of Medicine, 326(20), 1316–1322. https://doi.org/10.1056/nejm199205143262003
  • Hoyer-Hansen, M., & Jaattela, M. (2007). Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death and Differentiation, 14(9), 1576–1582. https://doi.org/10.1038/sj.cdd.4402200
  • Hu, M. L., Yang, S. L., Yang, L., Cheng, Y. Z., Zhang, H., & Pizzo, S. V. (2016). Interleukin-22 alleviated palmitate-induced endoplasmic reticulum stress in INS-1 cells through activation of autophagy. PLoS One, 11(1), e0146818. https://doi.org/10.1371/journal.pone.0146818
  • Kamarehei, M., Ardestani, S. K., Firouzi, M., Zahednasab, H., Keyvani, H., & Harirchian, M. H. (2019). Increased expression of endoplasmic reticulum stress-related caspase-12 and CHOP in the hippocampus of EAE mice. Brain Research Bulletin, 147, 174–182. https://doi.org/10.1016/j.brainresbull.2019.01.020
  • Khalid, A., & Naseem, I. (2023). Increased therapeutic effect of nanotized silibinin against glycation and diabetes: An in vitro and in silico-based approach. Biochimica et Biophysica Acta (BBA) - General Subjects, 1867(7), 130364. https://doi.org/10.1016/j.bbagen.2023.130364
  • Kondo, Y. (2013). A fundamental framework to organize the curriculum of technology education in senior high school. Seminars in Immunopathology, 35(3), 351–373. https://doi.org/10.1007/s00281-013-0370-z
  • Kopp, M. C., Larburu, N., Durairaj, V., Adams, C. J., & Ali, M. M. U. (2019). UPR proteins IRE1 and PERK switch BiP from chaperone to ER stress sensor. Nature Structural & Molecular Biology, 26(11), 1053–1062. https://doi.org/10.1038/s41594-019-0324-9
  • Kumar Singh, N., & Bhushan, B. (2023). Preclinical evidence-based neuroprotective potential of silibinin. Current Drug Research Reviews, 15. https://doi.org/10.2174/2589977515666230327154800
  • Larabi, A., Barnich, N., & Nguyen, H. T. T. (2020). New insights into the interplay between autophagy, gut microbiota and inflammatory responses in IBD. Autophagy, 16(1), 38–51. https://doi.org/10.1080/15548627.2019.1635384
  • Lingling, S., Jianing, F., Liu, W., Toshihiko, H., & Yuheng, N. (2020). Silibinin inhibits migration and invasion of breast cancer MDA-MB-231 cells through induction of mitochondrial fusion. Molecular and Cellular Biochemistry, 463(1), 189–201. https://doi.org/10.1007/s11010-019-03640-6
  • Lytrivi, M., Castell, A. L., Poitout, V., & Cnop, M. (2020). Recent insights into mechanisms of beta-cell Lipo- and glucolipotoxicity in type 2 diabetes. Journal of Molecular Biology, 432(5), 1514–1534. https://doi.org/10.1016/j.jmb.2019.09.016
  • Ly, L. D., Xu, S. H., Choi, S. K., Ha, C. M., Thoudam, T., Cha, S. K., Wiederkehr, A., Wollheim, C. B., Lee, I. K., & Park, K. S. (2017). Oxidative stress and calcium dysregulation by palmitate in type 2 diabetes. Experimental and Molecular Medicine, 49(2), e291. https://doi.org/10.1038/emm.2016.157
  • Maiuri, M. C., Zalckvar, E., Kimchi, A., & Kroemer, G. (2007). Self-eating and self-killing: Crosstalk between autophagy and apoptosis. Nature Reviews Molecular Cell Biology, 8(9), 741–752. https://doi.org/10.1038/nrm2239
  • Martchenko, A., & Brubaker, P. L. (2021). Effects of obesogenic feeding and free fatty acids on circadian secretion of metabolic hormones: Implications for the Development of type 2 diabetes. Cells, 10(9), 2297. https://doi.org/10.3390/cells10092297
  • Mauvais-Jarvis, F. (2011). Estrogen and androgen receptors: Regulators of fuel homeostasis and emerging targets for diabetes and obesity. Trends in Endocrinology and Metabolism, 22(1), 24–33. https://doi.org/10.1016/j.tem.2010.10.002
  • Mazraesefidi, M., Mahmoodi, M., & Hajizadeh, M. (2023). Effects of silibinin on apoptosis and insulin secretion in rat RINm5F pancreatic β-cells. Biotechnic & Histochemistry, 98(3), 201–209. https://doi.org/10.1080/10520295.2022.2154840
  • McAlister, E., Kirkby, M., Dominguez-Robles, J., Paredes, A. J., Anjani, Q. K., Moffatt, K., Vora, L. K., Hutton, A. R. J., McKenna, P. E., Larraneta, E., & Donnelly, R. F. (2021). The role of microneedle arrays in drug delivery and patient monitoring to prevent diabetes induced fibrosis. Advanced Drug Delivery Reviews, 175, 113825. https://doi.org/10.1016/j.addr.2021.06.002
  • Meier, J. J. (2012). GLP-1 receptor agonists for individualized treatment of type 2 diabetes mellitus. Nature Reviews Endocrinology, 8(12), 728–742. https://doi.org/10.1038/nrendo.2012.140
  • Nita, I., Hostettler, K., Tamo, L., Medova, M., Bombaci, G., Zhong, J., Allam, R., Zimmer, Y., Roth, M., Geiser, T., & Gazdhar, A. (2017). Hepatocyte growth factor secreted by bone marrow stem cell reduce ER stress and improves repair in alveolar epithelial II cells. Scientific Reports, 7(1), Article 41901. https://doi.org/10.1038/srep41901
  • Opazo-Rios, L., Mas, S., Marin-Royo, G., Mezzano, S., Gomez-Guerrero, C., Moreno, J. A., & Egido, J. (2020). Lipotoxicity and diabetic nephropathy: Novel mechanistic insights and therapeutic opportunities. International Journal of Molecular Sciences, 21(7), 2632. https://doi.org/10.3390/ijms21072632
  • Paglin, S., Hollister, T., Delohery, T., Hackett, N., McMahill, M., Sphicas, E., Domingo, D., & Yahalom, J. (2001). A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Research, 61(2), 439–444.
  • Peng, G., Li, L. H., Liu, Y. B., Pu, J., Zhang, S. Y., Yu, J. H., Zhao, J. J., & Liu, P. S. (2011). Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology, 152(6), 2206–2218. https://doi.org/10.1210/en.2010-1369
  • Qin, H. R., Zhang, H., Zhang, X. P., Zhang, S. W., Zhu, S. W., & Wang, H. (2021). Resveratrol protects intestinal epithelial cells against radiation-induced damage by promoting autophagy and inhibiting apoptosis through SIRT1 activation. Journal of Radiation Research, 62(4), 574–581. https://doi.org/10.1093/jrr/rrab035
  • Qureshi, F. M., Dejene, E. A., Corbin, K. L., & Nunemaker, C. S. (2015). Stress-induced dissociations between intracellular calcium signaling and insulin secretion in pancreatic islets. Cell Calcium, 57(5–6), 366–375. https://doi.org/10.1016/j.ceca.2015.03.002
  • Reggiori, F., & Molinari, M. (2022). ER-phagy: Mechanisms, regulation, and diseases connected to the lysosomal clearance of the endoplasmic reticulum. Physiological Reviews, 102(3), 1393–1448. https://doi.org/10.1152/physrev.00038.2021
  • Shah, A., Vaidya, N. K., Bhat, H. K., & Kumar, A. (2016). HIV-1 gp120 induces type-1 programmed cell death through ER stress employing IRE1α, JNK and AP-1 pathway. Scientific Reports, 6(1), 18929. https://doi.org/10.1038/srep18929
  • Somm, E., Montandon, S. A., Loizides-Mangold, U., Gaia, N., Lazarevic, V., De Vito, C., Perroud, E., Bochaton-Piallat, M. L., Dibner, C., Schrenzel, J., & Jornayvaz, F. R. (2021). The GLP-1R agonist liraglutide limits hepatic lipotoxicity and inflammatory response in mice fed a methionine-choline deficient diet. Translational Research, 227, 75–88. https://doi.org/10.1016/j.trsl.2020.07.008
  • Song, S. L., Tan, J., Miao, Y. Y., Li, M. M., & Zhang, Q. (2017). Crosstalk of autophagy and apoptosis: Involvement of the dual role of autophagy under ER stress. Journal of Cellular Physiology, 232(11), 2977–2984. https://doi.org/10.1002/jcp.25785
  • Song, S., Tan, J., Miao, Y., Sun, Z., & Zhang, Q. (2018). Intermittent-hypoxia-induced autophagy activation through the ER-Stress-related PERK/eIf2α/ATF4 pathway is a protective response to pancreatic β-cell apoptosis. Cellular Physiology & Biochemistry, 51(6), 2955–2971. https://doi.org/10.1159/000496047
  • Sonnenburg, J. L., & Bäckhed, F. (2016). Diet–microbiota interactions as moderators of human metabolism. Nature, 535(7610), 56–64. https://doi.org/10.1038/nature18846
  • Sozen, E., Karademir, B., & Ozer, N. K. (2015). Basic mechanisms in endoplasmic reticulum stress and relation to cardiovascular diseases. Free Radical Biology and Medicine, 78, 30–41. https://doi.org/10.1016/j.freeradbiomed.2014.09.031
  • Sun, W.-L., Hua, S., Li, X.-Y., Shen, L., Wu, H., & Ji, H.-F. (2023). Microbially produced vitamin B12 contributes to the lipid-lowering effect of silymarin. Nature Communications, 14(1). https://doi.org/10.1038/s41467-023-36079-x
  • Sun, E. W. L., Martin, A. M., Young, R. L., & Keating, D. J. (2018). The regulation of peripheral metabolism by gut-derived hormones. Frontiers in Endocrinology (Lausanne), 9, 754. https://doi.org/10.3389/fendo.2018.00754
  • Sun, Y., Yang, J., Liu, W. W., Yao, G. D., Xu, F. X., Hayashi, T., Onodera, S., & Ikejima, T. (2019). Attenuating effect of silibinin on palmitic acid-induced apoptosis and mitochondrial dysfunction in pancreatic beta-cells is mediated by estrogen receptor alpha. Molecular and Cellular Biochemistry, 460(1–2), 81–92. https://doi.org/10.1007/s11010-019-03572-1
  • Tang, X. M., Wang, L. S., Ye, H., Zhao, H. Q., & Zhao, L. S. (2022). Biological matrix-derived carbon quantum dots: Highly selective detection of tetracyclines. Journal of Photochemistry and Photobiology A-Chemistry, 424, Article 113653. https://doi.org/10.1016/j.jphotochem.2021.113653
  • Thivolet, C., Vial, G., Cassel, R., Rieusset, J., & Madec, A. M. (2017). Reduction of endoplasmic reticulum mitochondria interactions in beta cells from patients with type 2 diabetes. PLoS One, 12(7), Article e0182027. https://doi.org/10.1371/journal.pone.0182027
  • Vasu, S., Moffett, R. C., McClenaghan, N. H., & Flatt, P. R. (2015). Differential molecular and cellular responses of GLP-1 secreting L-cells and pancreatic alpha cells to glucotoxicity and lipotoxicity. Experimental Cell Research, 336(1), 100–108. https://doi.org/10.1016/j.yexcr.2015.05.022
  • Wadhwa, K., Pahwa, R., Kumar, M., Kumar, S., Sharma, P. C., Singh, G., Verma, R., Mittal, V., Singh, I., Kaushik, D., & Jeandet, P. (2022). Mechanistic insights into the pharmacological significance of silymarin. Molecules, 27(16), 5327. https://doi.org/10.3390/molecules27165327
  • Wah Kheong, C., Nik Mustapha, N. R., & Mahadeva, S. (2017). A randomized trial of silymarin for the treatment of nonalcoholic steatohepatitis. Clinical Gastroenterology and Hepatology, 15(12), 1940–1949.e8. https://doi.org/10.1016/j.cgh.2017.04.016
  • Wang, K., Zhang, C., Bao, J. L., Jia, X. J., Liang, Y. E., Wang, X. T., Chen, M. W., Su, H. X., Li, P., Wan, J. B., & He, C. W. (2016). Synergistic chemopreventive effects of curcumin and berberine on human breast cancer cells through induction of apoptosis and autophagic cell death. Scientific Reports, 6(1), Article 26064. https://doi.org/10.1038/srep26064
  • Wang, J. Y., Zhang, L. X., Cao, H., Shi, X. Y., Zhang, X. R., Gao, Z. H., Ikeda, K., Yan, T. X., Jia, Y., & Xu, F. X. (2022). Silibinin improves L-cell mass and function through an estrogen receptor-mediated antioxidative mechanism. Phytomedicine, 99, 154022. https://doi.org/10.1016/j.phymed.2022.154022
  • Wang, J., Zhang, X., Zhang, L., Yan, T., Wu, B., Xu, F., & Jia, Y. (2020). Silychristin a activates Nrf2-HO-1/SOD2 pathway to reduce apoptosis and improve GLP-1 production through upregulation of estrogen receptor alpha in GLUTag cells. European Journal of Pharmacology, 881, 173236. https://doi.org/10.1016/j.ejphar.2020.173236
  • Weigt, C., Hertrampf, T., Kluxen, F. M., Flenker, U., Hulsemann, F., Fritzemeier, K. H., & Diel, P. (2013). Molecular effects of ER alpha- and beta-selective agonists on regulation of energy homeostasis in obese female Wistar rats. Molecular and Cellular Endocrinology, 377(1–2), 147–158. https://doi.org/10.1016/j.mce.2013.07.007
  • Wu, H. Y., Gao, Y. A., Li, S. L., Bao, X. Y., Wang, J. Q., & Zheng, N. (2022). Lactoferrin alleviated AFM1-induced apoptosis in intestinal NCM 460 cells through the autophagy pathway. Foods, 11(1), 23. https://doi.org/10.3390/foods11010023
  • Xu, F., Du, W. Q., Zou, Q., Wang, Y. T., Zhang, X., Xing, X. D., Li, Y., Zhang, D. C., Wang, H. M., Zhang, W. H., Hu, X. Y., Liu, X., Liu, X. L., Zhang, S. J., Yu, J. Q., Fang, J. H., Li, F. J., Zhou, Y. … Yu, L. (2021). COPII mitigates ER stress by promoting formation of ER whorls. Cell Research, 31(2), 141–156. https://doi.org/10.1038/s41422-020-00416-2
  • Xue, X. L., Li, F., Cai, M., Hu, J. Y., Wang, Q., Lou, S. J., & Rastegar, M. (2021). Interactions between endoplasmic reticulum stress and autophagy: Implications for apoptosis and neuroplasticity-related proteins in palmitic acid-treated prefrontal cells. Neural Plasticity, 2021, 1–14. Article 8851327. https://doi.org/10.1155/2021/8851327
  • Xu, R., Qiu, S., Zhang, J., Liu, X., Zhang, L., Xing, H., You, M., Wang, M., Lu, Y., Zhang, P., & Zhu, J. (2022). Silibinin Schiff base derivatives counteract CCl4-induced acute liver injury by enhancing anti-inflammatory and antiapoptotic bioactivities. Drug Design, Development and Therapy, 16, 1441–1456. https://doi.org/10.2147/dddt.s356847
  • Yang, L., Liu, Q., Zhang, H., Wang, Y., Li, Y., Chen, S., Song, G., & Ren, L. (2021). Silibinin improves nonalcoholic fatty liver by regulating the expression of miR‑122: An in vitro and in vivo study. Molecular Medicine Reports, 23(5). https://doi.org/10.3892/mmr.2021.11974
  • Yang, J., Sun, Y., Xu, F., Liu, W., Hayashi, T., Onodera, S., Tashiro, S. I., & Ikejima, T. (2018). Involvement of estrogen receptors in silibinin protection of pancreatic beta-cells from TNFalpha- or IL-1beta-induced cytotoxicity. Biomedicine & Pharmacotherapy, 102, 344–353. https://doi.org/10.1016/j.biopha.2018.01.128
  • Yaribeygi, H., Sathyapalan, T., & Sahebkar, A. (2019). Molecular mechanisms by which GLP-1 RA and DPP-4i induce insulin sensitivity. Life Sciences, 234, 116776. https://doi.org/10.1016/j.lfs.2019.116776
  • Ye, R., Onodera, T., & Scherer, P. E. (2019). Lipotoxicity and beta cell maintenance in obesity and type 2 diabetes. Journal of the Endocrine Society, 3(3), 617–631. https://doi.org/10.1210/js.2018-00372
  • Zhou, Z. Q., Ribas, V., Rajbhandari, P., Drew, B. G., Moore, T. M., Fluitt, A. H., Reddish, B. R., Whitney, K. A., Georgia, S., Vergnes, L., Reue, K., Liesa, M., Shirihai, O., van der Bliek, A. M., Chi, N. W., Mahata, S. K., Tiano, J. P., Hewitt, S. C. … Hevener, A. L. (2018). Estrogen receptor alpha protects pancreatic beta-cells from apoptosis by preserving mitochondrial function and suppressing endoplasmic reticulum stress. Journal of Biological Chemistry, 293(13), 4735–4751. https://doi.org/10.1074/jbc.M117.805069