ADAR1 regulates vascular remodeling in hypoxic pulmonary hypertension through N1-methyladenosine modification of circCDK17

Acta Pharmaceutica Sinica B - Tập 13 - Trang 4840-4855 - 2023
Junting Zhang1, Yiying Li1, Jianchao Zhang1, Lu Liu2, Yuan Chen3, Xusheng Yang3, Xueyi Liao1, Muhua He2, Zihui Jia3, Jun Fan4, Jin-Song Bian2, Xiaowei Nie1
1Shenzhen Institute of Respiratory Disease, Shenzhen Key Laboratory of Respiratory Disease, Shenzhen People's Hospital (the Second Clinical Medical College, Jinan University; the First Affiliated Hospital, Southern University of Science and Technology), Shenzhen 518020, China; Post-Doctoral Scientific Research Station of Basic Medicine, Jinan University, Guangzhou 510632, China
2Department of Pharmacology, School of Medicine, Southern University of Science and Technology, Shenzhen 518055, China
3Lung Transplant Group, Wuxi People's Hospital Affiliated to Nanjing Medical University, Wuxi 211103, China
4Department of Medical Biochemistry and Molecular Biology, School of Medicine, Jinan University, Guangzhou 510632, China

Tài liệu tham khảo

Hoeper, 2021, Switching to riociguat versus maintenance therapy with phosphodiesterase-5 inhibitors in patients with pulmonary arterial hypertension (REPLACE): a multicentre, open-label, randomised controlled trial, Lancet Respir Med, 9, 573, 10.1016/S2213-2600(20)30532-4 Southgate, 2020, Molecular genetic framework underlying pulmonary arterial hypertension, Nat Rev Cardiol, 17, 85, 10.1038/s41569-019-0242-x Badesch, 2009, Longterm survival among patients with scleroderma-associated pulmonary arterial hypertension treated with intravenous epoprostenol, J Rheumatol, 36, 2244, 10.3899/jrheum.081277 Hoffmann, 2020, Evolution of pulmonary hypertension during severe sustained hypoxia, Circulation, 141, 1504, 10.1161/CIRCULATIONAHA.119.045192 Ghofrani, 2006, Hypoxia- and non-hypoxia-related pulmonary hypertension—established and new therapies, Cardiovasc Res, 72, 30, 10.1016/j.cardiores.2006.07.025 Hassoun, 2021, Pulmonary arterial hypertension, N Engl J Med, 385, 2361, 10.1056/NEJMra2000348 Penaloza, 2007, The heart and pulmonary circulation at high altitudes: healthy highlanders and chronic mountain sickness, Circulation, 115, 1132, 10.1161/CIRCULATIONAHA.106.624544 Song, 2018, STIM2 (stromal interaction molecule 2)-mediated increase in resting cytosolic free Ca2 concentration stimulates PASMC proliferation in pulmonary arterial hypertension, Hypertension, 71, 518, 10.1161/HYPERTENSIONAHA.117.10503 Montani, 2014, Targeted therapies in pulmonary arterial hypertension, Pharmacol Ther, 141, 172, 10.1016/j.pharmthera.2013.10.002 Nishikura, 2016, A-to-I editing of coding and non-coding RNAs by ADARs, Nat Rev Mol Cell Biol, 17, 83, 10.1038/nrm.2015.4 Athanasiadis, 2004, Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome, PLoS Biol, 2, e391, 10.1371/journal.pbio.0020391 Orlandi, 2012, Activity regulation of adenosine deaminases acting on RNA (ADARs), Mol Neurobiol, 45, 61, 10.1007/s12035-011-8220-2 Nishikura, 2010, Functions and regulation of RNA editing by ADAR deaminases, Annu Rev Biochem, 79, 321, 10.1146/annurev-biochem-060208-105251 Nie, 2004, Subcellular distribution of ADAR1 isoforms is synergistically determined by three nuclear discrimination signals and a regulatory motif, J Biol Chem, 279, 13249, 10.1074/jbc.M312753200 Fritz, 2009, RNA-regulated interaction of transportin-1 and exportin-5 with the double-stranded RNA-binding domain regulates nucleocytoplasmic shuttling of ADAR1, Mol Cell Biol, 29, 1487, 10.1128/MCB.01519-08 Strehblow, 2002, Nucleocytoplasmic distribution of human RNA-editing enzyme ADAR1 is modulated by double-stranded RNA-binding domains, a leucine-rich export signal, and a putative dimerization domain, Mol Biol Cell, 13, 3822, 10.1091/mbc.e02-03-0161 Ishizuka, 2019, Loss of ADAR1 in tumours overcomes resistance to immune checkpoint blockade, Nature, 565, 43, 10.1038/s41586-018-0768-9 Fei, 2016, ADAR1-mediated RNA editing, a novel mechanism controlling phenotypic modulation of vascular smooth muscle cells, Circ Res, 119, 463, 10.1161/CIRCRESAHA.116.309003 Jiang, 2018, ADAR1 silencing-induced HUVEC apoptosis is mediated by FGFR2 under hypoxia stress, Drug Des Dev Ther, 12, 4181, 10.2147/DDDT.S181312 Ben-Zvi, 2013, F11R expression upon hypoxia is regulated by RNA editing, PLoS One, 8, 10.1371/journal.pone.0077702 Ma, 2019, ADAR1 promotes robust hypoxia signaling via distinct regulation of multiple HIF-1α-inhibiting factors, EMBO Rep, 20, 10.15252/embr.201847107 Li, 2018, The biogenesis, functions, and challenges of circular RNAs, Mol Cell, 71, 428, 10.1016/j.molcel.2018.06.034 Chen, 2021, The bioinformatics toolbox for circRNA discovery and analysis, Briefings Bioinf, 22, 1706, 10.1093/bib/bbaa001 Kristensen, 2019, The biogenesis, biology and characterization of circular RNAs, Nat Rev Genet, 20, 675, 10.1038/s41576-019-0158-7 Zhou, 2020, Circular RNA: metabolism, functions and interactions with proteins, Mol Cancer, 19, 172, 10.1186/s12943-020-01286-3 Ivanov, 2015, Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals, Cell Rep, 10, 170, 10.1016/j.celrep.2014.12.019 Abe, 2010, Formation of plexiform lesions in experimental severe pulmonary arterial hypertension, Circulation, 121, 2747, 10.1161/CIRCULATIONAHA.109.927681 Halbert, 2007, High-efficiency promoter-dependent transduction by adeno-associated virus type 6 vectors in mouse lung, Hum Gene Ther, 18, 344, 10.1089/hum.2006.182 Wang, 2021, Hepatitis B virus evades immune recognition via RNA adenosine deaminase ADAR1-mediated viral RNA editing in hepatocytes, Cell Mol Immunol, 18, 1871, 10.1038/s41423-021-00729-1 Nie, 2020, Periostin: a potential therapeutic target for pulmonary hypertension?, Circ Res, 127, 1138, 10.1161/CIRCRESAHA.120.316943 Poliseno, 2010, A coding-independent function of gene and pseudogene mRNAs regulates tumour biology, Nature, 465, 1033, 10.1038/nature09144 Chen, 2020, Comprehensive review and assessment of computational methods for predicting RNA post-transcriptional modification sites from RNA sequences, Briefings Bioinf, 21, 1676, 10.1093/bib/bbz112 Dai, 2018, Identification of YTH domain-containing proteins as the readers for N1-methyladenosine in RNA, Anal Chem, 90, 6380, 10.1021/acs.analchem.8b01703 Liu, 2022, tRNA-m(1)A modification promotes T cell expansion via efficient MYC protein synthesis, Nat Immunol, 23, 1433, 10.1038/s41590-022-01301-3 Mathews, 2004, Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure, Proc Natl Acad Sci U S A, 101, 7287, 10.1073/pnas.0401799101 Armaos, 2021, catRAPID omics v2.0: going deeper and wider in the prediction of protein–RNA interactions, Nucleic Acids Res, 49, W72, 10.1093/nar/gkab393 Nevo-Caspi, 2011, A-to-I RNA editing is induced upon hypoxia, Shock, 35, 585, 10.1097/SHK.0b013e31820fe4b7 Vlachogiannis, 2021, Adenosine-to-inosine Alu RNA editing controls the stability of the pro-inflammatory long noncoding RNA NEAT1 in atherosclerotic cardiovascular disease, J Mol Cell Cardiol, 160, 111, 10.1016/j.yjmcc.2021.07.005 Yang, 2015, PTBP1 induces ADAR1 p110 isoform expression through IRES-like dependent translation control and influences cell proliferation in gliomas, Cell Mol Life Sci, 72, 4383, 10.1007/s00018-015-1938-7 Chung, 2018, Human ADAR1 prevents endogenous RNA from triggering translational shutdown, Cell, 172, 811, 10.1016/j.cell.2017.12.038 Nie, 2005, ADAR1 interacts with NF90 through double-stranded RNA and regulates NF90-mediated gene expression independently of RNA editing, Mol Cell Biol, 25, 6956, 10.1128/MCB.25.16.6956-6963.2005 Shi, 2017, Circular RNA expression is suppressed by androgen receptor (AR)-regulated adenosine deaminase that acts on RNA (ADAR1) in human hepatocellular carcinoma, Cell Death Dis, 8, 10.1038/cddis.2017.556 Zhang, 2020, Circ-calm4 serves as an miR-337-3p sponge to regulate Myo10 (Myosin 10) and promote pulmonary artery smooth muscle proliferation, Hypertension, 75, 668, 10.1161/HYPERTENSIONAHA.119.13715 Jiang, 2021, Circular RNA Calm4 regulates hypoxia-induced pulmonary arterial smooth muscle cells pyroptosis via the Circ-Calm4/miR-124-3p/PDCD6 axis, Arterioscler Thromb Vasc Biol, 41, 1675, 10.1161/ATVBAHA.120.315525 Ma, 2020, circRNA CDR1as promotes pulmonary artery smooth muscle cell calcification by upregulating CAMK2D and CNN3 via sponging miR-7-5p, Mol Ther Nucleic Acids, 22, 530, 10.1016/j.omtn.2020.09.018 Yuan, 2021, Impact of circGSAP in peripheral blood mononuclear cells on idiopathic pulmonary arterial hypertension, Am J Respir Crit Care Med, 203, 1579, 10.1164/rccm.202005-2052LE González-Magaña, 2020, Human PCNA structure, function and interactions, Biomolecules, 10, 570, 10.3390/biom10040570 Xiong, 2018, N(1)-Methyladenosine methylome in messenger RNA and non-coding RNA, Curr Opin Chem Biol, 45, 179, 10.1016/j.cbpa.2018.06.017 Zhang, 2019, Elevated serum circ_0068481 levels as a potential diagnostic and prognostic indicator in idiopathic pulmonary arterial hypertension, Pulm Circ, 9, 10.1177/2045894019888416