Activation of the ROS/TXNIP/NLRP3 pathway disrupts insulin-dependent glucose uptake in skeletal muscle of insulin-resistant obese mice
- Russell-Guzmán, Javier 12
- Américo-Da Silva, Luan 1
- Cadagan, Cynthia 1
- Maturana, Martín
- Palomero, Jesús 3
- Estrada, Manuel 1
- Barrientos, Genaro 11
- Buvinic, Sonja 11
- Hidalgo, Cecilia 111
-
Llanos, Paola
11
-
1
Universidad de Chile
info
-
2
Universidad Autónoma de Chile
info
-
3
Universidad de Salamanca
info
ISSN: 0891-5849
Année de publication: 2024
Volumen: 222
Pages: 187-198
Type: Article
D'autres publications dans: Free Radical Biology and Medicine
Résumé
Oxidative stress and the activation of the nucleotide-binding domain, leucine-rich-containing family, pyrin domain containing 3 (NLRP3) inflammasome have been linked to insulin resistance in skeletal muscle. In immune cells, the exacerbated generation of reactive oxygen species (ROS) activates the NLRP3 inflammasome, by facilitating the interaction between thioredoxin interacting protein (TXNIP) and NLRP3. However, the precise role of ROS/TXNIP-dependent NLRP3 inflammasome activation in skeletal muscle during obesity-induced insulin resistance remains undefined. Here, we induced insulin resistance in C57BL/6J mice by feeding them for 8 weeks with a high-fat diet (HFD) and explored whether the ROS/TXNIP/NLRP3 pathway was involved in the induction of insulin resistance in skeletal muscle. Skeletal muscle fibers from insulin-resistant mice exhibited increased oxidative stress, as evidenced by elevated malondialdehyde levels, and altered peroxiredoxin 2 dimerization. Additionally, these fibers displayed augmented activation of the NLRP3 inflammasome, accompanied by heightened ROS-dependent proximity between TXNIP and NLRP3, which was abolished by the antioxidant N-acetylcysteine (NAC). Inhibition of the NLRP3 inflammasome with MCC950 or suppressing the ROS/TXNIP/NLRP3 pathway with NAC restored insulin-dependent glucose uptake in muscle fibers from insulin-resistant mice. These findings provide insights into the mechanistic link between oxidative stress, NLRP3 inflammasome activation, and obesity-induced insulin resistance in skeletal muscle.
Références bibliographiques
- Czech, (2017), Nat. Med., 23, pp. 804, 10.1038/nm.4350
- Zhao, (2023), Front. Endocrinol., 14
- DeFronzo, (2009), Diabetes Care, 32, pp. S157, 10.2337/dc09-S302
- Defronzo, (1981), Diabetes, 30, pp. 1000, 10.2337/diab.30.12.1000
- Abdul-Ghani, (2010), J. Biomed. Biotechnol., 2010, pp. 1, 10.1155/2010/476279
- Americo-Da-Silva, (2021), Int. J. Mol. Sci., 22, 10.3390/ijms221910212
- Sánchez-Aguilera, (2018), Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 1863, pp. 1469, 10.1016/j.bbalip.2018.09.005
- James, (2021), Nat. Rev. Mol. Cell Biol., 22, pp. 751, 10.1038/s41580-021-00390-6
- Avtanski, (2019), Animal Model Exp Med, 2, pp. 252, 10.1002/ame2.12084
- Jorquera, (2021), Diabetologia, 64, pp. 1457, 10.1007/s00125-021-05451-1
- Vandanmagsar, (2011), Nat. Med., 17, pp. 179, 10.1038/nm.2279
- Guo, (2015), Nat. Med., 21, pp. 668, 10.1038/nm.3893
- Paik, (2021), Cell. Mol. Immunol., 18, pp. 1141, 10.1038/s41423-021-00670-3
- Swanson, (2019), Nat. Rev. Immunol., 19, pp. 477, 10.1038/s41577-019-0165-0
- Groslambert, (2018), J. Inflamm. Res., 11, pp. 359, 10.2147/JIR.S141220
- Haneklaus, (2015), Immunol. Rev., 265, pp. 53, 10.1111/imr.12285
- Boucher, (2018), J. Exp. Med., 215, pp. 827, 10.1084/jem.20172222
- Tschopp, (2010), Nat. Rev. Immunol., 10, pp. 210, 10.1038/nri2725
- Zhou, (2010), Nat. Immunol., 11, pp. 136, 10.1038/ni.1831
- Hwang, (2014), Nat. Commun., 5, pp. 2958, 10.1038/ncomms3958
- Yoshihara, (2014), Front. Immunol., 4, pp. 514, 10.3389/fimmu.2013.00514
- Cheng, (2022), Front. Aging Neurosci., 0, pp. 570
- Anderson, (2009), J. Clin. Invest., 119, pp. 573, 10.1172/JCI37048
- Espinosa, (2013), Int. J. Mol. Sci., 14, pp. 15740, 10.3390/ijms140815740
- Henriquez-Olguin, (2023), Redox Biol., 65, 10.1016/j.redox.2023.102842
- Souto Padron de Figueiredo, (2015), J. Biol. Chem., 290, pp. 13427, 10.1074/jbc.M114.626077
- Putti, (2016), Front. Physiol., 6, 10.3389/fphys.2015.00426
- Yao, (2022), Int. J. Mol. Sci., 23, 10.3390/ijms231911384
- Ma, (2017), Pharm. Res. (N. Y.), 176, pp. 139
- Pereira, (2015), J. Endocrinol., 225, pp. 1, 10.1530/JOE-14-0676
- Hui, (2008), Proc Natl Acad Sci U S A, 105, pp. 3921, 10.1073/pnas.0800293105
- Mandala, (2016), Biochem. Biophys. Res. Commun., 479, pp. 933, 10.1016/j.bbrc.2016.09.168
- Muoio, (2007), Cell Metabol., 5, pp. 412, 10.1016/j.cmet.2007.05.011
- Ran, (2020), Diabetes Metab. J, 44
- Yoshihara, (2010), Nat. Commun., 1, pp. 127, 10.1038/ncomms1127
- Chen, (2017), Inflamm. Res., 66, pp. 157, 10.1007/s00011-016-1002-6
- Ismael, (2020), Mol. Neurobiol., 10.1007/s12035-020-01893-7
- Li, (2019), J. Alzheim. Dis., 68, pp. 255, 10.3233/JAD-180814
- Henry, (1956), Proc Soc Exp Biol Med, 92, pp. 748, 10.3181/00379727-92-22601
- Kumar, (2015), J. Vis. Exp., 2015
- Fazakerley, (2018), J. Biol. Chem., 293, pp. 7315, 10.1074/jbc.RA117.001254
- Söderberg, (2006), Nat. Methods, 3, pp. 995, 10.1038/nmeth947
- Ahn, (2016), J. Clin. Invest., 126, pp. 3567, 10.1172/JCI87382
- Devi
- Shah, (2013)
- Tseng, (2016), Sci. Rep., 6, 10.1038/srep35016
- Yu, (2010), J. Biol. Chem., 285, pp. 25822, 10.1074/jbc.M110.108290
- Wojtovich, (2019), Antioxidants Redox Signal., 31, pp. 591, 10.1089/ars.2019.7804
- Fiorenza, (2023), Human Skeletal Muscle, pp. 1
- Hoy, (2007), Am. J. Physiol. Endocrinol. Metab., 293, pp. 1358, 10.1152/ajpendo.00133.2007
- Lee, (2021), J Cachexia Sarcopenia Muscle, 12, pp. 1925, 10.1002/jcsm.12794
- Contreras-Ferrat, (2014), J. Cell Sci., 127, pp. 1911
- Hull, (2020), Neuropharmacology, 180, 10.1016/j.neuropharm.2020.108305
- Cho, (2015), Int. J. Mol. Med., 36, pp. 839, 10.3892/ijmm.2015.2276
- Ismael, (2018), J. Neurotrauma, 35, pp. 1294, 10.1089/neu.2017.5344
- Evavold, (2018), Immunity, 48, pp. 35, 10.1016/j.immuni.2017.11.013
- Heilig, (2018), Eur. J. Immunol., 48, pp. 584, 10.1002/eji.201747404
- Devant, (2023), Cell Rep., 42, 10.1016/j.celrep.2023.112008
- Shen, (2021), J. Inflamm. Res., 14, pp. 711, 10.2147/JIR.S299163
- Finucane, (2019), Sci. Rep., 9, pp. 1, 10.1038/s41598-019-40619-1
- Van Der Heijden, (2017), Arterioscler. Thromb. Vasc. Biol., 37, pp. 1457, 10.1161/ATVBAHA.117.309575
- Llanos, (2015), Am. J. Physiol. Endocrinol. Metab., 308, pp. E294, 10.1152/ajpendo.00189.2014
- Madsen, (2018), Am. J. Physiol. Endocrinol. Metab., 315, pp. E110, 10.1152/ajpendo.00392.2017
- Zhao, (2021), Sci. Rep., 11