SMURF1 activates the cGAS/STING/IFN-1 signal axis by mediating YY1 ubiquitination to accelerate the progression of lupus nephritis

References

• Nascimento DQ, da Silva I, Lima CAD, et al. Expression of the miR-9-5p, miR-125b-5p and its target gene NFKB1 and TRAF6 in childhood-onset systemic lupus erythematosus (cSLE). Autoimmunity. 2022;55(8):1–12.
   PubMed Web of Science ®Google Scholar
• Almaani S, Meara A, Rovin BH. Update on lupus nephritis. Clin J Am Soc Nephrol. 2017;12(5):825–835.
   PubMed Web of Science ®Google Scholar
• Davidson A, Aranow C, Mackay M. Lupus nephritis: challenges and progress. Curr Opin Rheumatol. 2019;31(6):682–688.
   PubMed Web of Science ®Google Scholar
• Li Y, Chen J, Xie M, et al. Identification of a circRNA-miRNA-mRNA network to explore the effects of circRNAs on renal injury in systemic lupus erythematosus. Autoimmunity. 2023;56(1):2193361.
   PubMed Web of Science ®Google Scholar
• Wei J, Ferron M, Clarke CJ, et al. Bone-specific insulin resistance disrupts whole-body glucose homeostasis via decreased osteocalcin activation. J Clin Invest. 2014;124(4):1–13.
   PubMed Web of Science ®Google Scholar
• Shimazu J, Wei J, Karsenty G. Smurf1 inhibits osteoblast differentiation, bone formation, and glucose homeostasis through serine 148. Cell Rep. 2016;15(1):27–35.
   PubMed Web of Science ®Google Scholar
• Gong W, Chen Z, Zou Y, et al. CKIP-1 affects the polyubiquitination of Nrf2 and Keap1 via mediating Smurf1 to resist HG-induced renal fibrosis in GMCs and diabetic mice kidneys. Free Radic Biol Med. 2018;115:338–350.
   PubMed Web of Science ®Google Scholar
• Fukasawa H, Yamamoto T, Togawa A, et al. Down-regulation of Smad7 expression by ubiquitin-dependent degradation contributes to renal fibrosis in obstructive nephropathy in mice. Proc Natl Acad Sci U S A. 2004;101(23):8687–8692.
   PubMed Web of Science ®Google Scholar
• Tian Y, Xiao YH, Geng T, et al. Clusterin suppresses spermatogenic cell apoptosis to alleviate diabetes-induced testicular damage by inhibiting autophagy via the PI3K/AKT/mTOR axis. Biol Cell. 2021;113(1):14–27.
   PubMed Web of Science ®Google Scholar
• Pan YY, Yang JX, Xu YF, et al. Yin yang-1 suppresses CD40 ligand-CD40 signaling-mediated anti-inflammatory cytokine interleukin-10 expression in pulmonary adventitial fibroblasts by promoting histone H3 tri-methylation at lysine 27 modification on interleukin-10 promoter. Cell Biol Int. 2020;44(7):1544–1555.
   PubMed Web of Science ®Google Scholar
• Gao P, Li L, Yang L, et al. Yin yang 1 protein ameliorates diabetic nephropathy pathology through transcriptional repression of TGFβ1. Sci Transl Med. 2019;11(510):eaaw2050
   Web of Science ®Google Scholar
• Wang B, Jiang X, Li Y, et al. YY1 alleviates lupus nephritis-induced renal injury by reducing the Th17/treg cell ratio via the IFN-γ/Fra2 axis. Lab Invest. 2022;102(8):872–884.
   PubMed Web of Science ®Google Scholar
• Ding L, Dong G, Zhang D, et al. The regional function of cGAS/STING signal in multiple organs: one of culprit behind systemic lupus erythematosus? Med Hypotheses. 2015;85(6):846–849.
   PubMed Web of Science ®Google Scholar
• An J, Durcan L, Karr RM, et al. Expression of cyclic GMP-AMP synthase in patients with systemic lupus erythematosus. Arthritis Rheumatol. 2017;69(4):800–807.
   PubMed Web of Science ®Google Scholar
• Zheng L, Zhang H, Tang Y. In lupus nephritis, how do extracellular DNAs trigger type I interferon secretion: under the assistance of HMGB1-cGAS? Med Hypotheses. 2018;121:51–53.
   PubMed Web of Science ®Google Scholar
• Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature. 2009;461(7265):788–792.
   PubMed Web of Science ®Google Scholar
• Guzmán J, Cardiel MH, Arce-Salinas A, et al. Measurement of disease activity in systemic lupus erythematosus. Prospective validation of 3 clinical indices. J Rheumatol. 1992;19:1551–1558.
   PubMed Web of Science ®Google Scholar
• Gladman D, Ginzler E, Goldsmith C, et al. The development and initial validation of the systemic lupus international collaborating clinics/American college of rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum. 1996;39(3):363–369.
   PubMed Web of Science ®Google Scholar
• Castro-Mondragon JA, Riudavets-Puig R, Rauluseviciute I, et al. JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 2022;50(D1):D165–d173.
   PubMed Web of Science ®Google Scholar
• Wang X, Li Y, He M, et al. UbiBrowser 2.0: a comprehensive resource for proteome-wide known and predicted ubiquitin ligase/deubiquitinase-substrate interactions in eukaryotic species. Nucleic Acids Res. 2022;50(D1):D719–d728.
   PubMed Web of Science ®Google Scholar
• Jin J, Zhao L, Zou W, et al. Activation of cyclooxygenase-2 by ATF4 during endoplasmic reticulum stress regulates kidney podocyte autophagy induced by lupus nephritis. Cell Physiol Biochem. 2018;48(2):753–764.
   PubMedGoogle Scholar
• Feng X, Jia Y, Zhang Y, et al. Ubiquitination of UVRAG by SMURF1 promotes autophagosome maturation and inhibits hepatocellular carcinoma growth. Autophagy. 2019;15(7):1130–1149.
   PubMed Web of Science ®Google Scholar
• Lech M, Anders HJ. The pathogenesis of lupus nephritis. J Am Soc Nephrol. 2013;24(9):1357–1366.
   PubMed Web of Science ®Google Scholar
• Cui JH, Xie X. UCH-L1 expressed by podocytes: a potentially therapeutic target for lupus nephritis? Inflammation. 2017;40(2):657–665.
   PubMed Web of Science ®Google Scholar
• Zhang F, Zhang B, Tang R, et al. The occurrence of lupus nephritis is regulated by USP7-mediated JMJD3 stabilization. Immunol Lett. 2021;235:41–50.
   PubMed Web of Science ®Google Scholar
• Cockram PE, Kist M, Prakash S, et al. Ubiquitination in the regulation of inflammatory cell death and cancer. Cell Death Differ. 2021;28(2):591–605.
   PubMed Web of Science ®Google Scholar
• Song MK, Lee JH, Ryoo IG, et al. Bardoxolone ameliorates TGF-β1-associated renal fibrosis through Nrf2/Smad7 elevation. Free Radic Biol Med. 2019;138:33–42.
   PubMed Web of Science ®Google Scholar
• Wei X, Wang X, Zhan J, et al. Smurf1 inhibits integrin activation by controlling kindlin-2 ubiquitination and degradation. J Cell Biol. 2017;216(5):1455–1471.
   PubMed Web of Science ®Google Scholar
• Lin W, Zhang X, Zhang C, et al. Deletion of Smurf1 attenuates liver steatosis via stabilization of p53. Lab Invest. 2022;102(10):1075–1087.
   PubMed Web of Science ®Google Scholar
• Bian C, Luan Z, Zhang H, et al. miR-154-5p affects the TGFβ1/Smad3 pathway on the fibrosis of diabetic kidney disease via binding E3 ubiquitin ligase Smurf1. Oxid Med Cell Longevity. 2022;2022:1–17.
   Web of Science ®Google Scholar
• Gordon S, Akopyan G, Garban H, et al. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene. 2006;25(8):1125–1142.
   PubMed Web of Science ®Google Scholar
• Du L, Qian X, Li Y, et al. Sirt1 inhibits renal tubular cell epithelial-mesenchymal transition through YY1 deacetylation in diabetic nephropathy. Acta Pharmacol Sin. 2021;42(2):242–251.
   PubMed Web of Science ®Google Scholar
• Liang S, Cuevas G, Tizani S, et al. Novel mechanism of regulation of fibrosis in kidney tumor with tuberous sclerosis. Mol Cancer. 2013;12(1):49.
   PubMedGoogle Scholar
• Khalil MI, Sommer M, Arvin A, et al. Cellular transcription factor YY1 mediates the varicella-zoster virus (VZV) IE62 transcriptional activation. Virology. 2014;449:244–253.
   PubMed Web of Science ®Google Scholar
• Yang T, Hu Y, Chen S, et al. YY1 inactivated transcription co-regulator PGC-1α to promote mitochondrial dysfunction of early diabetic nephropathy-associated tubulointerstitial fibrosis. Cell Biol Toxicol. 2023;39(2):391–413.
   PubMed Web of Science ®Google Scholar
• Davis SE, Khatua AK, Popik W. Nucleosomal dsDNA stimulates APOL1 expression in human cultured podocytes by activating the cGAS/IFI16-STING signaling pathway. Sci Rep. 2019;9(1):15485.
   PubMedGoogle Scholar
• Oduro PK, Zheng X, Wei J, et al. The cGAS-STING signaling in cardiovascular and metabolic diseases: future novel target option for pharmacotherapy. Acta Pharm Sin B. 2022;12(1):50–75.
   PubMed Web of Science ®Google Scholar
• Huang R, Shi Q, Zhang S, et al. Inhibition of the cGAS-STING pathway attenuates lung ischemia/reperfusion injury via regulating endoplasmic reticulum stress in alveolar epithelial type II cells of rats. J Inflamm Res. 2022;15:5103–5119.
   PubMed Web of Science ®Google Scholar
• Kang YQ, Yuan XH, Li ZZ, et al. Antishock characteristics of erythrocyte-mediated endoplasmic reticulum stress in macrophages in severe hemorrhagic shock environment based on TLR9-cGAS-STING-IFN signal axis. Cell Transplant. 2020;29:963689720950218.
   PubMed Web of Science ®Google Scholar