Persulfidation of transcription factor FOXO1 at cysteine 457: A novel mechanism by which H2S inhibits vascular smooth muscle cell proliferation

Journal of Advanced Research - Tập 27 - Trang 155-164 - 2021
Xiaoyu Tian1,2, Dan Zhou3, Yong Zhang3, Yunjia Song1, Qingyou Zhang1, Dingfang Bu1, Yan Sun1, Liling Wu4,5, Yuan Long3, Chaoshu Tang4,5, Junbao Du1,4, Yaqian Huang1, Hongfang Jin1,2
1Department of Pediatrics, Peking University First Hospital, Beijing, 100034, China
2Research Unit of Clinical Diagnosis and Treatment of Pediatric Syncope and Cardiovascular Diseases, Chinese Academy of Medical Sciences, Beijing, China
3Department of Cardiology, Wuhan Children's Hospital, Wuhan, China
4Key Laboratory of Molecular Cardiology, Ministry of Education, Beijing, China
5Department of Physiology and Pathophysiology, Peking University Health Science Centre, Beijing 100091, China

Tài liệu tham khảo

Gibbons, 1994, The emerging concept of vascular remodeling, N Engl J Med, 330, 1431, 10.1056/NEJM199405193302008 Tang, 2006, Hydrogen sulfide as a new endogenous gaseous transmitter in the cardiovascular system, Curr Vasc Pharmacol, 4, 17, 10.2174/157016106775203144 Jha, 2008, Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: role of antioxidant and antiapoptotic signaling, Am J Physiol Heart Circ Physiol, 295, H801, 10.1152/ajpheart.00377.2008 Yang, 2010, Cystathionine gamma-lyase deficiency and overproliferation of smooth muscle cells, Cardiovasc Res, 86, 487, 10.1093/cvr/cvp420 Liu, 2018, Hydrogen sulfide attenuates myocardial fibrosis in diabetic rats through the JAK/STAT signaling pathway, Int J Mol Med, 41, 1867 Yang, 2008, H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase, Science, 322, 587, 10.1126/science.1162667 Du, 2004, The possible role of hydrogen sulfide as a smooth muscle cell proliferation inhibitor in rat cultured cells, Heart Vessels, 19, 75, 10.1007/s00380-003-0743-7 Li, 2014, H2S inhibition of chemical hypoxia-induced proliferation of HPASMCs is mediated by the upregulation of COX-2/PGI2, Int J Mol Med, 33, 359, 10.3892/ijmm.2013.1579 Tran, 2002, DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein, Science, 296, 530, 10.1126/science.1068712 Seoane, 2004, Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation, Cell, 117, 211, 10.1016/S0092-8674(04)00298-3 Dijkers, 2000, Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1, Curr Biol, 10, 1201, 10.1016/S0960-9822(00)00728-4 Nemoto, 2002, Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway, Science, 295, 2450, 10.1126/science.1069004 Wilhelm, 2016, FOXO1 couples metabolic activity and growth state in the vascular endothelium, Nature, 529, 216, 10.1038/nature16498 Sun, 2015, Hydrogen sulfide upregulates KATP channel expression in vascular smooth muscle cells of spontaneously hypertensive rats, J Mol Med (Berl), 93, 439, 10.1007/s00109-014-1227-1 Majumder, 2019, Hydrogen sulphide mitigates homocysteine-induced apoptosis and matrix remodelling in mesangial cells through Akt/FOXO1 signalling cascade, Cell Signal, 61, 66, 10.1016/j.cellsig.2019.05.003 Savai, 2014, Pro-proliferative and inflammatory signaling converge on FoxO1 transcription factor in pulmonary hypertension, Nat Med, 20, 1289, 10.1038/nm.3695 Siqueira, 2011, FOXO1 modulates osteoblast differentiation, Bone, 48, 1043, 10.1016/j.bone.2011.01.019 Zhang, 2018, The increased endogenous sulfur dioxide acts as a compensatory mechanism for the downregulated endogenous hydrogen sulfide pathway in the endothelial cell inflammation, Front Immunol, 9, 882, 10.3389/fimmu.2018.00882 Du, 2014, Hydrogen sulfide suppresses oxidized low-density lipoprotein (ox-LDL)-stimulated monocyte chemoattractant protein 1 generation from macrophages via the nuclear factor κB (NF-κB) pathway, J Biol Chem, 289, 9741, 10.1074/jbc.M113.517995 Saline, 2019, Lau R, Gunnarsson A, Jacso T, et al, AMPK and AKT protein kinases hierarchically phosphorylate the N-terminus of the FOXO1 transcription factor, modulating interactions with 14–3-3 proteins, J Biol Chem, 294, 13106, 10.1074/jbc.RA119.008649 Elsey, 2010, Regulation of cardiovascular cell function by hydrogen sulfide (H(2)S), Cell Biochem Funct, 28, 95, 10.1002/cbf.1618 Sun, 2016, Exogenous H2S modulates mitochondrial fusion-fission to inhibit vascular smooth muscle cell proliferation in a hyperglycemic state, Cell Biosci, 6, 36, 10.1186/s13578-016-0102-x Wu, 2019, H2S attenuates endoplasmic reticulum stress in hypoxia-induced pulmonary artery hypertension, Biosci Rep, 39, 10.1042/BSR20190304 Jeong, 2016, Long noncoding RNA linc00598 regulates CCND2 transcription and modulates the G1 checkpoint, Sci Rep, 6, 32172, 10.1038/srep32172 Chang, 2013, Liver X receptor α inhibits osteosarcoma cell proliferation through up-regulation of FoxO1, Cell Physiol Biochem, 32, 180, 10.1159/000350134 Link, 2019, Introduction to FOXO biology, Methods Mol Biol, 1890, 1, 10.1007/978-1-4939-8900-3_1 Ye, 2018, Exogenous hydrogen sulfide attenuates the development of diabetic cardiomyopathy via the FoxO1pathway, J Cell Physiol, 233, 9786, 10.1002/jcp.26946 Zhang, 2002, Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms: direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding, J Biol Chem, 277, 45276, 10.1074/jbc.M208063200 Zhang, 2019, Endogenous hydrogen sulfide sulfhydrates IKKβ at cysteine 179 to control pulmonary artery endothelial cell inflammation, Clin Sci (Lond), 133, 2045, 10.1042/CS20190514 Xie, 2014, Sulfhydration of p66Shc at cysteine59 mediates the antioxidant effect of hydrogen sulfide, Antioxid Redox Signal, 21, 2531, 10.1089/ars.2013.5604 Wu, 2018, Amelioration of mitochondrial dysfunction in heart failure through S-sulfhydration of Ca2+/calmodulin-dependent protein kinase II, Redox Biol, 19, 250, 10.1016/j.redox.2018.08.008 Kim, 2010, Regulation of FOXO1 by TAK1-Nemo-like kinase pathway, J Biol Chem, 285, 8122, 10.1074/jbc.M110.101824 Biggs, 1999, Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1, Proc Natl Acad Sci U S A, 96, 7421, 10.1073/pnas.96.13.7421 Gerst, 2015, Anita M Hennige, Protein kinase Cδ regulates nuclear export of FOXO1 through phosphorylation of the chaperone 14–3-3ζ, Diabetologia, 58, 2819, 10.1007/s00125-015-3744-z