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Nucleic acid and protein methylation modification in renal diseases

Abstract

Although great efforts have been made to elucidate the pathological mechanisms of renal diseases and potential prevention and treatment targets that would allow us to retard kidney disease progression, we still lack specific and effective management methods. Epigenetic mechanisms are able to alter gene expression without requiring DNA mutations. Accumulating evidence suggests the critical roles of epigenetic events and processes in a variety of renal diseases, involving functionally relevant alterations in DNA methylation, histone methylation, RNA methylation, and expression of various non-coding RNAs. In this review, we highlight recent advances in the impact of methylation events (especially RNA m6A methylation, DNA methylation, and histone methylation) on renal disease progression, and their impact on treatments of renal diseases. We believe that a better understanding of methylation modification changes in kidneys may contribute to the development of novel strategies for the prevention and management of renal diseases.

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Fig. 1: The roles of epigenetic methylation modification in kidney diseases.
Fig. 2: Schematic diagram of RNA methylation modification.
Fig. 3: Roles of m6A modification in ccRCC.
Fig. 4: The process of DNA methylation modification.
Fig. 5: The process of histone methylation modification.

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References

  1. Jager KJ, Kovesdy C, Langham R, Rosenberg M, Jha V, Zoccali C. A single number for advocacy and communication-worldwide more than 850 million individuals have kidney diseases. Kidney Int. 2019;96:1048–50.

    Article  PubMed  Google Scholar 

  2. Mehta RL, Cerda J, Burdmann EA, Tonelli M, Garcia-Garcia G, Jha V, et al. International society of nephrology’s 0by25 initiative for acute kidney injury (zero preventable deaths by 2025): a human rights case for nephrology. Lancet. 2015;385:2616–43.

    Article  PubMed  Google Scholar 

  3. Huang R, Fu P, Ma L. Kidney fibrosis: from mechanisms to therapeutic medicines. Signal Transduct Target Ther. 2023;8:129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Borg R, Carlson N, Sondergaard J, Persson F. The growing challenge of chronic kidney disease: an overview of current knowledge. Int J Nephrol. 2023;2023:9609266.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Luyckx VA, Tonelli M, Stanifer JW. The global burden of kidney disease and the sustainable development goals. Bull World Health Organ. 2018;96:414–22D.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Li X, Lu L, Hou W, Huang T, Chen X, Qi J, et al. Epigenetics in the pathogenesis of diabetic nephropathy. Acta Biochim Biophys Sin. 2022;54:163–72.

    Article  CAS  PubMed  Google Scholar 

  7. Wang X, Zhu W, Long Q, Chen E, Sun H, Li X, et al. The prognostic value and immune correlation of IL18 expression and promoter methylation in renal cell carcinoma. Clin Epigenet. 2023;15:14.

    Article  CAS  Google Scholar 

  8. Chen J, Xu C, Yang K, Gao R, Cao Y, Liang L, et al. Inhibition of ALKBH5 attenuates I/R-induced renal injury in male mice by promoting Ccl28 m6A modification and increasing Treg recruitment. Nat Commun. 2023;14:1161.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  9. Jiang L, Liu X, Hu X, Gao L, Zeng H, Wang X, et al. METTL3-mediated m6A modification of TIMP2 mRNA promotes podocyte injury in diabetic nephropathy. Mol Ther. 2022;30:1721–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wang S, Li H, Lian Z, Deng S. The role of RNA modification in HIV-1 Infection. Int J Mol Sci. 2022;23:7571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Nombela P, Miguel-López B, Blanco S. The role of m6A, m5C and Ψ RNA modifications in cancer: novel therapeutic opportunities. Mol Cancer. 2021;20:18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Roundtree IA, Evans ME, Pan T, He C. Dynamic RNA modifications in gene expression regulation. Cell. 2017;169:1187–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Liu T, Sun L, Li ZZ, Yang K, Chen JM, Han XY, et al. The m6A/m5C/m1A regulator genes signature reveals the prognosis and is related with immune microenvironment for hepatocellular carcinoma. BMC Gastroenterol. 2023;23:147.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  15. Yang X, Bai Q, Chen W, Liang J, Wang F, Gu W, et al. m6 A-Dependent modulation via IGF2BP3/MCM5/Notch axis promotes partial EMT and LUAD metastasis. Adv Sci. 2023;10:e2206744.

  16. Han X, Guo J, Fan Z. Interactions between m6A modification and miRNAs in malignant tumors. Cell Death Dis. 2021;12:598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wang T, Kong S, Tao M, Ju S. The potential role of RNA N6-methyladenosine in cancer progression. Mol Cancer. 2020;19:88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wang X, Zhao BS, Roundtree IA, Lu Z, Han D, Ma H, et al. N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell. 2015;161:1388–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jiang X, Liu B, Nie Z, Duan L, Xiong Q, Jin Z, et al. The role of m6A modification in the biological functions and diseases. Signal Transduct Target Ther. 2021;6:74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nielsen J, Christiansen J, Lykke-Andersen J, Johnsen AH, Wewer UM, Nielsen FC. A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol Cell Biol. 1999;19:1262–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Jiang Z, Zhang W, Zeng Z, Tang D, Li C, Cai W, et al. A comprehensive investigation discovered the novel methyltransferase Mettl24 as one presumably prognostic gene for kidney renal clear cell carcinoma potentially modulating tumor immune microenvironment. Front Immunol. 2022;13:926461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liu B, Ao S, Tan F, Ma W, Liu H, Liang H, et al. Transcriptomic analysis and laboratory experiments reveal potential critical genes and regulatory mechanisms in sepsis-associated acute kidney injury. Ann Transl Med. 2022;10:737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pan J, Xie Y, Li H, Li X, Chen J, Liu X, et al. mmu-lncRNA 121686/hsa-lncRNA 520657 induced by METTL3 drive the progression of AKI by targeting miR-328-5p/HtrA3 signaling axis. Mol Ther. 2022;30:3694–713.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li CM, Li M, Zhao WB, Ye ZC, Peng H. Alteration of N6-methyladenosine RNA profiles in cisplatin-induced acute kidney injury in mice. Front Mol Biosci. 2021;8:654465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wang JN, Wang F, Ke J, Li Z, Xu CH, Yang Q, et al. Inhibition of METTL3 attenuates renal injury and inflammation by alleviating TAB3 m6A modifications via IGF2BP2-dependent mechanisms. Sci Transl Med. 2022;14:eabk2709.

    Article  CAS  PubMed  Google Scholar 

  26. Mao Y, Jiang F, Xu XJ, Zhou LB, Jin R, Zhuang LL, et al. Inhibition of IGF2BP1 attenuates renal injury and inflammation by alleviating m6A modifications and E2F1/MIF pathway. Int J Biol Sci. 2023;19:593–609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shen J, Wang W, Shao X, Wu J, Li S, Che X, et al. Integrated analysis of m6A methylome in cisplatin-induced acute kidney injury and berberine alleviation in mouse. Front Genet. 2020;11:584460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zhou P, Wu M, Ye C, Xu Q, Wang L. Meclofenamic acid promotes cisplatin-induced acute kidney injury by inhibiting fat mass and obesity-associated protein-mediated m(6)A abrogation in RNA. J Biol Chem. 2019;294:16908–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Li M, Deng L, Xu G. METTL14 promotes glomerular endothelial cell injury and diabetic nephropathy via m6A modification of alpha-klotho. Mol Med. 2021;27:106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tang W, Zhao Y, Zhang H, Peng Y, Rui Z. METTL3 enhances NSD2 mRNA stability to reduce renal impairment and interstitial fibrosis in mice with diabetic nephropathy. BMC Nephrol. 2022;23:124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lu Z, Liu H, Song N, Liang Y, Zhu J, Chen J, et al. METTL14 aggravates podocyte injury and glomerulopathy progression through N(6)-methyladenosine-dependent downregulating of Sirt1. Cell Death Dis. 2021;12:881.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Xu Z, Jia K, Wang H, Gao F, Zhao S, Li F, et al. METTL14-regulated PI3K/Akt signaling pathway via PTEN affects HDAC5-mediated epithelial-mesenchymal transition of renal tubular cells in diabetic kidney disease. Cell Death Dis. 2021;12:32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lan J, Xu B, Shi X, Pan Q, Tao Q. WTAP-mediated N(6)-methyladenosine modification of NLRP3 mRNA in kidney injury of diabetic nephropathy. Cell Mol Biol Lett. 2022;27:51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sun Q, Geng H, Zhao M, Li Y, Chen X, Sha Q, et al. FTO-mediated m6A modification of SOCS1 mRNA promotes the progression of diabetic kidney disease. Clin Transl Med. 2022;12:e942.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhang W, Zhang S, Dong C, Guo S, Jia W, Jiang Y, et al. A bibliometric analysis of RNA methylation in diabetes mellitus and its complications from 2002 to 2022. Front Endocrinol. 2022;13:997034.

    Article  Google Scholar 

  36. Zhang C, Chen L, Lou W, Su J, Huang J, Liu A, et al. Aberrant activation of m6A demethylase FTO renders HIF2alpha(low/-) clear cell renal cell carcinoma sensitive to BRD9 inhibitors. Sci Transl Med. 2021;13:eabf6045.

    Article  CAS  PubMed  Google Scholar 

  37. Yang Y, Hsu PJ, Chen YS, Yang YG. Dynamic transcriptomic m6A decoration: writers, erasers, readers and functions in RNA metabolism. Cell Res. 2018;28:616–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Xu Z, Chen S, Liu R, Chen H, Xu B, Xu W, et al. Circular RNA circPOLR2A promotes clear cell renal cell carcinoma progression by facilitating the UBE3C-induced ubiquitination of PEBP1 and, thereby, activating the ERK signaling pathway. Mol Cancer. 2022;21:146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Shi Y, Dou Y, Zhang J, Qi J, Xin Z, Zhang M, et al. The RNA N6-methyladenosine methyltransferase Mettl3 promotes the progression of kidney cancer via N6-methyladenosine-dependent translational enhancement of ABCD1. Front Cell Dev Biol. 2021;9:737498.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Miao D, Wang Q, Shi J, Lv Q, Tan D, Zhao C, et al. N6-methyladenosine-modified DBT alleviates lipid accumulation and inhibits tumor progression in clear cell renal cell carcinoma through the ANXA2/YAP axis-regulated Hippo pathway. Cancer Commun. 2023;43:480–502.

    Article  Google Scholar 

  41. Zhu D, Liu Y, Chen J, Wang Q, Li Y, Zhu Y, et al. The methyltransferase Mettl3 promotes tumorigenesis via mediating HHLA2 mRNA m6A modification in human renal cell carcinoma. J Transl Med. 2022;20:298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Li A, Cao C, Gan Y, Wang X, Wu T, Zhang Q, et al. ZNF677 suppresses renal cell carcinoma progression through N6-methyladenosine and transcriptional repression of CDKN3. Clin Transl Med. 2022;12:e906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zhang L, Luo X, Qiao S. METTL14-mediated N6-methyladenosine modification of PTEN mRNA inhibits tumour progression in clear-cell renal cell carcinoma. Br J Cancer. 2022;127:30–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Xu T, Gao S, Ruan H, Liu J, Liu Y, Liu D, et al. METTL14 Acts as a potential regulator of tumor immune and progression in clear cell renal cell carcinoma. Front Genet. 2021;12:609174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Liu Z, Sun T, Piao C, Zhang Z, Kong C. METTL14-mediated N(6)-methyladenosine modification of ITGB4 mRNA inhibits metastasis of clear cell renal cell carcinoma. Cell Commun Signal. 2022;20:36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Shen D, Ding L, Lu Z, Wang R, Yu C, Wang H, et al. METTL14-mediated Lnc-LSG1 m6A modification inhibits clear cell renal cell carcinoma metastasis via regulating ESRP2 ubiquitination. Mol Ther Nucleic Acids. 2022;27:547–61.

    Article  CAS  PubMed  Google Scholar 

  47. Liu T, Wang H, Fu Z, Wang Z, Wang J, Gan X, et al. Methyltransferase-like 14 suppresses growth and metastasis of renal cell carcinoma by decreasing long noncoding RNA NEAT1. Cancer Sci. 2022;113:446–58.

    Article  CAS  PubMed  Google Scholar 

  48. Zhang C, Chen L, Liu Y, Huang J, Liu A, Xu Y, et al. Downregulated METTL14 accumulates BPTF that reinforces super-enhancers and distal lung metastasis via glycolytic reprogramming in renal cell carcinoma. Theranostics. 2021;11:3676–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Chen Y, Lu Z, Qi C, Yu C, Li Y, Huan W, et al. N(6)-methyladenosine-modified TRAF1 promotes sunitinib resistance by regulating apoptosis and angiogenesis in a mettl14-dependent manner in renal cell carcinoma. Mol Cancer. 2022;21:111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Cheng B, Xie M, Zhou Y, Li T, Liu W, Yu W, et al. Vascular mimicry induced by m6A mediated IGFL2-AS1/AR axis contributes to pazopanib resistance in clear cell renal cell carcinoma. Cell Death Discov. 2023;9:121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ying Y, Ma X, Fang J, Chen S, Wang W, Li J, et al. EGR2-mediated regulation of m6A reader IGF2BP proteins drive RCC tumorigenesis and metastasis via enhancing S1PR3 mRNA stabilization. Cell Death Dis. 2021;12:750.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Gundert L, Strick A, von Hagen F, Schmidt D, Klumper N, Tolkach Y, et al. Systematic expression analysis of m6A RNA methyltransferases in clear cell renal cell carcinoma. BJUI Compass. 2021;2:402–11.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Xu Y, Zhou J, Li L, Yang W, Zhang Z, Zhang K, et al. FTO-mediated autophagy promotes progression of clear cell renal cell carcinoma via regulating SIK2 mRNA stability. Int J Biol Sci. 2022;18:5943–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Yang W, Xie L, Wang P, Zhuang C. MiR-155 regulates m6A level and cell progression by targeting FTO in clear cell renal cell carcinoma. Cell Signal. 2022;91:110217.

    Article  CAS  PubMed  Google Scholar 

  55. Hu W, Klumper N, Schmidt D, Ritter M, Ellinger J, Hauser S. Depletion of the m6A demethylases FTO and ALKBH5 impairs growth and metastatic capacity through EMT phenotype change in clear cell renal cell carcinoma. Am J Transl Res. 2023;15:1744–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Xiao Y, Thakkar KN, Zhao H, Broughton J, Li Y, Seoane JA, et al. The m6A RNA demethylase FTO is a HIF-independent synthetic lethal partner with the VHL tumor suppressor. Proc Natl Acad Sci USA. 2020;117:21441–9.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  57. Shen H, Ying Y, Ma X, Xie H, Chen S, Sun J, et al. FTO promotes clear cell renal cell carcinoma progression via upregulation of PDK1 through an m(6)A dependent pathway. Cell Death Discov. 2022;8:356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zhuang C, Zhuang C, Luo X, Huang X, Yao L, Li J, et al. N6-methyladenosine demethylase FTO suppresses clear cell renal cell carcinoma through a novel FTO-PGC-1alpha signalling axis. J Cell Mol Med. 2019;23:2163–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Guimaraes-Teixeira C, Barros-Silva D, Lobo J, Soares-Fernandes D, Constancio V, Leite-Silva P, et al. Deregulation of N6-methyladenosine RNA modification and its erasers FTO/ALKBH5 among the main renal cell tumor subtypes. J Personal Med. 2021;11:996.

    Article  Google Scholar 

  60. Gu Y, Niu S, Wang Y, Duan L, Pan Y, Tong Z, et al. DMDRMR-mediated regulation of m6A-modified CDK4 by m6A reader IGF2BP3 drives ccRCC progression. Cancer Res. 2021;81:923–34.

    Article  CAS  PubMed  Google Scholar 

  61. Chen J, Yu K, Zhong G, Shen W. Identification of a m6A RNA methylation regulators-based signature for predicting the prognosis of clear cell renal carcinoma. Cancer Cell Int. 2020;20:157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wang Y, Cong R, Liu S, Zhu B, Wang X, Xing Q. Decreased expression of METTL14 predicts poor prognosis and construction of a prognostic signature for clear cell renal cell carcinoma. Cancer Cell Int. 2021;21:46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Yang Z, Peng B, Pan Y, Gu Y. Analysis and verification of N(6)-methyladenosine-modified genes as novel biomarkers for clear cell renal cell carcinoma. Bioengineered. 2021;12:9473–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Strick A, von Hagen F, Gundert L, Klumper N, Tolkach Y, Schmidt D, et al. The N(6) -methyladenosine (m6A) erasers alkylation repair homologue 5 (ALKBH5) and fat mass and obesity-associated protein (FTO) are prognostic biomarkers in patients with clear cell renal carcinoma. BJU Int. 2020;125:617–24.

    Article  CAS  PubMed  Google Scholar 

  65. Wang Q, Chen C, Ding Q, Zhao Y, Wang Z, Chen J, et al. METTL3-mediated m6A modification of HDGF mRNA promotes gastric cancer progression and has prognostic significance. Gut. 2020;69:1193–205.

    Article  CAS  PubMed  Google Scholar 

  66. Du QY, Huo FC, Du WQ, Sun XL, Jiang X, Zhang LS, et al. Mettl3 potentiates progression of cervical cancer by suppressing ER stress via regulating m6A modification of TXNDC5 mRNA. Oncogene. 2022;41:4420–32.

    Article  CAS  PubMed  Google Scholar 

  67. Xu QC, Tien YC, Shi YH, Chen SY, Zhu YQ, Huang XT, et al. METTL3 promotes intrahepatic cholangiocarcinoma progression by regulating IFIT2 expression in an m6A-YTHDF2-dependent manner. Oncogene. 2022;41:1622–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Alriquet M, Calloni G, Martinez-Limon A, Delli Ponti R, Hanspach G, Hengesbach M, et al. The protective role of m1A during stress-induced granulation. J Mol Cell Biol. 2021;12:870–80.

    Article  PubMed  Google Scholar 

  69. Safra M, Sas-Chen A, Nir R, Winkler R, Nachshon A, Bar-Yaacov D, et al. The m1A landscape on cytosolic and mitochondrial mRNA at single-base resolution. Nature. 2017;551:251–55.

    Article  CAS  PubMed  ADS  Google Scholar 

  70. Lee HK, Lee BR, Lee TJ, Lee CM, Li C, O’Connor PM, et al. Differential release of extracellular vesicle tRNA from oxidative stressed renal cells and ischemic kidneys. Sci Rep. 2022;12:1646.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  71. Hotta K, Sho M, Fujimoto K, Shimada K, Yamato I, Anai S, et al. Clinical significance and therapeutic potential of prostate cancer antigen-1/ALKBH3 in human renal cell carcinoma. Oncol Rep. 2015;34:648–54.

    Article  CAS  PubMed  Google Scholar 

  72. Mattioli F, Worpenberg L, Li CT, Ibrahim N, Naz S, Sharif S, et al. Biallelic variants in NSUN6 cause an autosomal recessive neurodevelopmental disorder. Genet Med. 2023;25:100900.

    Article  CAS  PubMed  Google Scholar 

  73. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705.

    Article  CAS  PubMed  Google Scholar 

  74. Yang H, Wang Y, Xiang Y, Yadav T, Ouyang J, Phoon L, et al. FMRP promotes transcription-coupled homologous recombination via facilitating TET1-mediated m5C RNA modification demethylation. Proc Natl Acad Sci USA. 2022;119:e2116251119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Chen C, Chen LY, Zhang JX, Xu HG. 5-Methylcytosine (m5C) modification patterns and tumor immune infiltration characteristics in clear cell renal cell carcinoma. Curr Oncol. 2022;30:559–74.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Pandolfini L, Barbieri I, Bannister AJ, Hendrick A, Andrews B, Webster N, et al. METTL1 promotes -7 microRNA processing via m7G methylation. Mol Cell. 2019;74:1278–90.e9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Alexandrov A, Martzen MR, Phizicky EM. Two proteins that form a complex are required for 7-methylguanosine modification of yeast tRNA. RNA. 2002;8:1253–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Zorbas C, Nicolas E, Wacheul L, Huvelle E, Heurgué-Hamard V, Lafontaine DLJ. The human 18S rRNA base methyltransferases DIMT1L and WBSCR22-TRMT112 but not rRNA modification are required for ribosome biogenesis. Mol Biol Cell. 2015;26:2080–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Xia X, Wang Y, Zheng JC. Internal m7G methylation: a novel epitranscriptomic contributor in brain development and diseases. Mol Ther Nucleic Acids. 2023;31:295–308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Ma J, Han H, Huang Y, Yang C, Zheng S, Cai T, et al. METTL1/WDR4-mediated m7G tRNA modifications and m7G codon usage promote mRNA translation and lung cancer progression. Mol Ther. 2021;29:3422–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Huang M, Long J, Yao Z, Zhao Y, Zhao Y, Liao J, et al. Mettl1-Mediated m7G tRNA modification promotes lenvatinib resistance in hepatocellular carcinoma. Cancer Res. 2023;83:89–102.

    Article  CAS  PubMed  Google Scholar 

  82. Chen M, Nie Z, Gao Y, Cao H, Zheng L, Guo N, et al. m7G regulator-mediated molecular subtypes and tumor microenvironment in kidney renal clear cell carcinoma. Front Pharmacol. 2022;13:900006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hong P, Du H, Tong M, Cao Q, Hu D, Ma J, et al. A novel m7G-related microRNAs risk signature predicts the prognosis and tumor microenvironment of kidney renal clear cell carcinoma. Front Genet. 2022;13:922358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Zhang L, Zhang Q, Liu S, Chen Y, Li R, Lin T, et al. DNA methyltransferase 1 may be a therapy target for attenuating diabetic nephropathy and podocyte injury. Kidney Int. 2017;92:140–53.

    Article  CAS  PubMed  Google Scholar 

  85. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484–92.

    Article  CAS  PubMed  Google Scholar 

  86. Liu H, Doke T, Guo D, Sheng X, Ma Z, Park J, et al. Epigenomic and transcriptomic analyses define core cell types, genes and targetable mechanisms for kidney disease. Nat Genet. 2022;54:950–62.

    Article  CAS  PubMed  Google Scholar 

  87. Schlosser P, Tin A, Matias-Garcia PR, Thio CHL, Joehanes R, Liu H, et al. Meta-analyses identify DNA methylation associated with kidney function and damage. Nat Commun. 2021;12:7174.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  88. Wang D, Wu W, Callen E, Pavani R, Zolnerowich N, Kodali S, et al. Active DNA demethylation promotes cell fate specification and the DNA damage response. Science. 2022;378:983–9.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  89. Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature. 2013;502:472–9.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  90. Wang L, You X, Ruan D, Shao R, Dai HQ, Shen W, et al. TET enzymes regulate skeletal development through increasing chromatin accessibility of RUNX2 target genes. Nat Commun. 2022;13:4709.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  91. Zhang X, Li S, He J, Jin Y, Zhang R, Dong W, et al. TET2 suppresses VHL deficiency-driven clear cell renal cell carcinoma by inhibiting HIF signaling. Cancer Res. 2022;82:2097–109.

    Article  CAS  PubMed  Google Scholar 

  92. Peng D, He A, He S, Ge G, Wang S, Ci WM, et al. Ascorbic acid induced TET2 enzyme activation enhances cancer immunotherapy efficacy in renal cell carcinoma. Int J Biol Sci. 2022;18:995–1007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kim JY, Silvaroli JA, Martinez GV, Bisunke B, Luna Ramirez AV, Jayne LA, et al. Zinc finger protein 24-dependent transcription factor SOX9 up-regulation protects tubular epithelial cells during acute kidney injury. Kidney Int. 2023;103:1093–104.

    Article  CAS  PubMed  Google Scholar 

  94. Xu CH, Wang JN, Suo XG, Ji ML, He XY, Chen X, et al. RIPK3 inhibitor-AZD5423 alleviates acute kidney injury by inhibiting necroptosis and inflammation. Int Immunopharmacol. 2022;112:109262.

    Article  CAS  PubMed  Google Scholar 

  95. Misurac JM, Grinsell MM, Narus JH, Mason S, Kallash M, Andreoli SP. NSAID-associated acute kidney injury in hospitalized children–a prospective pediatric nephrology research consortium study. Pediatr Nephrol. 2023;38:3109–16.

    Article  PubMed  Google Scholar 

  96. Yu JT, Hu XW, Yang Q, Shan RR, Zhang Y, Dong ZH, et al. Insulin-like growth factor binding protein 7 promotes acute kidney injury by alleviating poly ADP ribose polymerase 1 degradation. Kidney Int. 2022;102:828–44.

    Article  CAS  PubMed  Google Scholar 

  97. Zhang K, Li R, Chen X, Yan H, Li H, Zhao X, et al. Renal endothelial cell-targeted extracellular vesicles protect the kidney from ischemic injury. Adv Sci. 2023;10:e2204626.

    Article  Google Scholar 

  98. Guo C, Pei L, Xiao X, Wei Q, Chen JK, Ding HF, et al. DNA methylation protects against cisplatin-induced kidney injury by regulating specific genes, including interferon regulatory factor 8. Kidney Int. 2017;92:1194–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Wang J, Li H, Qiu S, Dong Z, Xiang X, Zhang D. MBD2 upregulates miR-301a-5p to induce kidney cell apoptosis during vancomycin-induced AKI. Cell Death Dis. 2017;8:e3120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Xie Y, Liu B, Pan J, Liu J, Li X, Li H, et al. MBD2 mediates septic AKI through activation of PKCeta/p38MAPK and the ERK1/2 Axis. Mol Ther Nucleic Acids. 2021;23:76–88.

    Article  CAS  PubMed  Google Scholar 

  101. Sun T, Liu Q, Wang Y, Deng Y, Zhang D. MBD2 mediates renal cell apoptosis via activation of Tox4 during rhabdomyolysis-induced acute kidney injury. J Cell Mol Med. 2021;25:4562–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Fu Y, Xiang Y, Li H, Chen A, Dong Z. Inflammation in kidney repair: mechanism and therapeutic potential. Pharmacol Ther. 2022;237:108240.

    Article  CAS  PubMed  Google Scholar 

  103. Tampe B, Steinle U, Tampe D, Carstens JL, Korsten P, Zeisberg EM, et al. Low-dose hydralazine prevents fibrosis in a murine model of acute kidney injury-to-chronic kidney disease progression. Kidney Int. 2017;91:157–76.

    Article  CAS  PubMed  Google Scholar 

  104. Sanchez-Navarro A, Perez-Villalva R, Murillo-de-Ozores AR, Martinez-Rojas MA, Rodriguez-Aguilera JR, Gonzalez N, et al. Vegfa promoter gene hypermethylation at HIF1alpha binding site is an early contributor to CKD progression after renal ischemia. Sci Rep. 2021;11:8769.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  105. Guo X, Zhu Y, Sun Y, Li X. IL-6 accelerates renal fibrosis after acute kidney injury via DNMT1-dependent FOXO3a methylation and activation of Wnt/beta-catenin pathway. Int Immunopharmacol. 2022;109:108746.

    Article  CAS  PubMed  Google Scholar 

  106. Chou YH, Pan SY, Shao YH, Shih HM, Wei SY, Lai CF, et al. Methylation in pericytes after acute injury promotes chronic kidney disease. J Clin Invest. 2020;130:4845–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Castellano G, Franzin R, Sallustio F, Stasi A, Banelli B, Romani M, et al. Complement component C5a induces aberrant epigenetic modifications in renal tubular epithelial cells accelerating senescence by Wnt4/betacatenin signaling after ischemia/reperfusion injury. Aging. 2019;11:4382–406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Smyth LJ, Kerr KR, Kilner J, McGill AE, Maxwell AP, McKnight AJ. Longitudinal epigenome-wide analysis of kidney transplant recipients pretransplant and posttransplant. Kidney Int Rep. 2023;8:330–40.

    Article  PubMed  Google Scholar 

  109. Ai K, Li X, Zhang P, Pan J, Li H, He Z, et al. Genetic or siRNA inhibition of MBD2 attenuates the UUO- and I/R-induced renal fibrosis via downregulation of EGR1. Mol Ther Nucleic Acids. 2022;28:77–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Chen J, Zhang X, Zhang H, Lin J, Zhang C, Wu Q, et al. Elevated klotho promoter methylation is associated with severity of chronic kidney disease. PLoS One. 2013;8:e79856.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  111. Yoshimoto N, Hayashi K, Hishikawa A, Hashiguchi A, Nakamichi R, Sugita-Nishimura E, et al. Significance of podocyte DNA damage and glomerular DNA methylation in CKD patients with proteinuria. Hypertens Res. 2023;46:1000–8.

    Article  CAS  PubMed  Google Scholar 

  112. Nguyen LT, Larkin BP, Wang R, Faiz A, Pollock CA, Saad S. Blood DNA methylation predicts diabetic kidney disease progression in high fat diet-fed mice. Nutrients. 2022;14:785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Vetter VM, Spieker J, Sommerer Y, Buchmann N, Kalies CH, Regitz-Zagrosek V, et al. DNA methylation age acceleration is associated with risk of diabetes complications. Commun Med. 2023;3:21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Khurana I, Kaipananickal H, Maxwell S, Birkelund S, Syreeni A, Forsblom C, et al. Reduced methylation correlates with diabetic nephropathy risk in type 1 diabetes. J Clin Invest. 2023;133:e160959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. An Z, Liu P, Zheng J, Si C, Li T, Chen Y, et al. Sox2 and Klf4 as the functional core in pluripotency induction without exogenous Oct4. Cell Rep. 2019;29:1986–2000.

    Article  CAS  PubMed  Google Scholar 

  116. Hayashi K, Sasamura H, Nakamura M, Azegami T, Oguchi H, Sakamaki Y, et al. KLF4-dependent epigenetic remodeling modulates podocyte phenotypes and attenuates proteinuria. J Clin Invest. 2014;124:2523–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Hayashi K, Sasamura H, Nakamura M, Sakamaki Y, Azegami T, Oguchi H, et al. Renin-angiotensin blockade resets podocyte epigenome through Kruppel-like Factor 4 and attenuates proteinuria. Kidney Int. 2015;88:745–53.

    Article  CAS  PubMed  Google Scholar 

  118. Zhou X, Zang X, Ponnusamy M, Masucci MV, Tolbert E, Gong R, et al. Enhancer of zeste homolog 2 inhibition attenuates renal fibrosis by maintaining smad7 and phosphatase and tensin homolog expression. J Am Soc Nephrol. 2016;27:2092–108.

    Article  CAS  PubMed  Google Scholar 

  119. Sun GD, Cui WP, Guo QY, Miao LN. Histone lysine methylation in diabetic nephropathy. J Diabetes Res. 2014;2014:654148.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Mushtaq A, Mir US, Hunt CR, Pandita S, Tantray WW, Bhat A, et al. Role of histone methylation in maintenance of genome integrity. Genes. 2021;12:1000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Li B, Xia Y, Mei S, Ye Z, Song B, Yan X, et al. Histone H3K27 methyltransferase EZH2 regulates apoptotic and inflammatory responses in sepsis-induced AKI. Theranostics. 2023;13:1860–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Zhou X, Zang X, Guan Y, Tolbert T, Zhao TC, Bayliss G, et al. Targeting enhancer of zeste homolog 2 protects against acute kidney injury. Cell Death Dis. 2018;9:1067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Liang H, Huang Q, Liao MJ, Xu F, Zhang T, He J, et al. EZH2 plays a crucial role in ischemia/reperfusion-induced acute kidney injury by regulating p38 signaling. Inflamm Res. 2019;68:325–36.

    Article  CAS  PubMed  Google Scholar 

  124. Wen L, Tao SH, Guo F, Li LZ, Yang HL, Liang Y, et al. Selective EZH2 inhibitor zld1039 alleviates inflammation in cisplatin-induced acute kidney injury partially by enhancing RKIP and suppressing NF-kappaB p65 pathway. Acta Pharmacol Sin. 2022;43:2067–80.

    Article  CAS  PubMed  Google Scholar 

  125. Wen L, Ren Q, Guo F, Du X, Yang H, Fu P, et al. Tubular aryl hydratocarbon receptor upregulates EZH2 to promote cellular senescence in cisplatin-induced acute kidney injury. Cell Death Dis. 2023;14:18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Liu Y, Yu Y, Zhang J, Wang C. The therapeutic effect of dexmedetomidine on protection from renal failure via inhibiting KDM5A in lipopolysaccharide-induced sepsis of mice. Life Sci. 2019;239:116868.

    Article  CAS  PubMed  Google Scholar 

  127. Dreval K, de Conti A, Furuya S, Beland FA, Rusyn I, Pogribny IP. miR-1247 blocks SOX9-mediated regeneration in alcohol- and fibrosis-associated acute kidney injury in mice. Toxicology. 2017;384:40–9.

    Article  CAS  PubMed  Google Scholar 

  128. Cui B, Hou X, Liu M, Li Q, Yu C, Zhang S, et al. Pharmacological inhibition of SMYD2 protects against cisplatin-induced acute kidney injury in mice. Front Pharmacol. 2022;13:829630.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zhang L, Chen Q, Chen Z, Wang Y, Gamboa JL, Ikizler TA, et al. Mechanisms regulating muscle protein synthesis in CKD. J Am Soc Nephrol. 2020;31:2573–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Lefevre GM, Patel SR, Kim D, Tessarollo L, Dressler GR. Altering a histone H3K4 methylation pathway in glomerular podocytes promotes a chronic disease phenotype. PLoS Genet. 2010;6:e1001142.

    Article  PubMed  PubMed Central  Google Scholar 

  131. Gomes OV, Guimaraes MP, Barbosa BMB, Marinho CLA, Nicacio JM, Barreira MP, et al. Awareness of stroke among patients with chronic kidney disease on hemodialysis: a cross-sectional study. Sao Paulo Med J. 2024;142:e2022644.

    Article  Google Scholar 

  132. Lin SH, Ho WT, Wang YT, Chuang CT, Chuang LY, Guh JY. Histone methyltransferase Suv39h1 attenuates high glucose-induced fibronectin and p21(WAF1) in mesangial cells. Int J Biochem Cell Biol. 2016;78:96–105.

    Article  CAS  PubMed  Google Scholar 

  133. Wang J, Shen X, Liu J, Chen W, Wu F, Wu W, et al. High glucose mediates NLRP3 inflammasome activation via upregulation of ELF3 expression. Cell Death Dis. 2020;11:383.

    Article  PubMed  PubMed Central  Google Scholar 

  134. Lu L, Li X, Zhong Z, Zhou W, Zhou D, Zhu M, et al. KMT5A downregulation participated in high glucose-mediated EndMT via upregulation of ENO1 expression in diabetic nephropathy. Int J Biol Sci. 2021;17:4093–107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Jia Y, Reddy MA, Das S, Oh HJ, Abdollahi M, Yuan H, et al. Dysregulation of histone H3 lysine 27 trimethylation in transforming growth factor-beta1-induced gene expression in mesangial cells and diabetic kidney. J Biol Chem. 2019;294:12695–707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Hung PH, Hsu YC, Chen TH, Ho C, Lin CL. The histone demethylase inhibitor GSK-J4 is a therapeutic target for the kidney fibrosis of diabetic kidney disease via DKK1 modulation. Int J Mol Sci. 2022;23:9407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Yin SS, Zhang Q, Yang J, Lin WJ, Li YN, Chen F, et al. TGFβ-incurred epigenetic aberrations of miRNA and DNA methyltransferase suppress klotho and potentiate renal fibrosis. Biochim Biophys Acta Mol Cell Res. 2017;1864:1207–16.

    Article  CAS  PubMed  Google Scholar 

  138. Yu JT, Hu XW, Chen HY, Yang Q, Li HD, Dong YH, et al. DNA methylation of FTO promotes renal inflammation by enhancing m6A of PPAR-α in alcohol-induced kidney injury. Pharmacol Res. 2021;163:105286.

    Article  CAS  PubMed  Google Scholar 

  139. Larkin BP, Nguyen LT, Hou M, Glastras SJ, Chen H, Faiz A, et al. Low-dose hydralazine reduces albuminuria and glomerulosclerosis in a mouse model of obesity-related chronic kidney disease. Diabetes Obes Metab. 2022;24:1939–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Tampe B, Tampe D, Muller CA, Sugimoto H, LeBleu V, Xu X, et al. Tet3-mediated hydroxymethylation of epigenetically silenced genes contributes to bone morphogenic protein 7-induced reversal of kidney fibrosis. J Am Soc Nephrol. 2014;25:905–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. An CL, Jiao BH, Du H, Tran M, Song B, Wang PH, et al. Jumonji domain-containing protein-3 (JMJD3) promotes myeloid fibroblast activation and macrophage polarization in kidney fibrosis. Br J Pharmacol. 2023;180:2250–65.

    Article  CAS  PubMed  Google Scholar 

  142. Yu C, Xiong C, Tang J, Hou X, Liu N, Bayliss G, et al. Histone demethylase JMJD3 protects against renal fibrosis by suppressing TGFβ and Notch signaling and preserving PTEN expression. Theranostics. 2021;11:2706–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Xu Y, Yuan XD, Wu JJ, Chen RY, Xia L, Zhang M, et al. The N6-methyladenosine mRNA methylase METTL14 promotes renal ischemic reperfusion injury via suppressing YAP1. J Cell Biochem. 2020;121:524–33.

    Article  CAS  PubMed  Google Scholar 

  144. Wang J, Ishfaq M, Xu L, Xia C, Chen C, Li J. Mettl3/m6A/miRNA-873-5p attenuated oxidative stress and apoptosis in colistin-induced kidney injury by modulating Keap1/Nrf2 pathway. Front Pharmacol. 2019;10:517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Li S, Zhou H, Liang Y, Yang Q, Zhang J, Shen W, et al. Integrated analysis of transcriptome-wide m(6)A methylation in a Cd-induced kidney injury rat model. Ecotoxicol Environ Saf. 2023;256:114903.

    Article  CAS  PubMed  Google Scholar 

  146. Li H, Zhang W, Zhong F, Das GC, Xie Y, Li Z, et al. Epigenetic regulation of RCAN1 expression in kidney disease and its role in podocyte injury. Kidney Int. 2018;94:1160–76.

    Article  CAS  PubMed  Google Scholar 

  147. Lin CL, Hsu YC, Huang YT, Shih YH, Wang CJ, Chiang WC, et al. A KDM6A-KLF10 reinforcing feedback mechanism aggravates diabetic podocyte dysfunction. EMBO Mol Med. 2019;11:e9828.

    Article  PubMed  PubMed Central  Google Scholar 

  148. Dai X, Liao R, Liu C, Liu S, Huang H, Liu J, et al. Epigenetic regulation of TXNIP-mediated oxidative stress and NLRP3 inflammasome activation contributes to SAHH inhibition-aggravated diabetic nephropathy. Redox Biol. 2021;45:102033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Cao A, Li J, Asadi M, Basgen JM, Zhu B, Yi Z, et al. DACH1 protects podocytes from experimental diabetic injury and modulates PTIP-H3K4Me3 activity. J Clin Invest. 2021;131:e141279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Liu M, Liang K, Zhen J, Zhou M, Wang X, Wang Z, et al. Sirt6 deficiency exacerbates podocyte injury and proteinuria through targeting Notch signaling. Nat Commun. 2017;8:413.

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  151. Zeng X, Chen K, Li L, Tian J, Ruan W, Hu Z, et al. Epigenetic activation of RBM15 promotes clear cell renal cell carcinoma growth, metastasis and macrophage infiltration by regulating the m6A modification of CXCL11. Free Radic Biol Med. 2022;184:135–47.

    Article  CAS  PubMed  Google Scholar 

  152. Li W, Ye K, Li X, Liu X, Peng M, Chen F, et al. YTHDC1 is downregulated by the YY1/HDAC2 complex and controls the sensitivity of ccRCC to sunitinib by targeting the ANXA1-MAPK pathway. J Exp Clin Cancer Res. 2022;41:250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Yang L, Chen Y, Liu N, Lu Y, Ma W, Yang Z, et al. CircMET promotes tumor proliferation by enhancing CDKN2A mRNA decay and upregulating smad3. Mol Cancer. 2022;21:23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Zhou X, Chen H, Hu Y, Ma X, Li J, Shi Y, et al. Enhancer of zeste homolog 2 promotes renal fibrosis after acute kidney injury by inducing epithelial-mesenchymal transition and activation of M2 macrophage polarization. Cell Death Dis. 2023;14:253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Zhang C, Guan Y, Zou J, Yang X, Bayliss G, Zhuang S. Histone methyltransferase MLL1 drives renal tubular cell apoptosis by p53-dependent repression of E-cadherin during cisplatin-induced acute kidney injury. Cell Death Dis. 2022;13:770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 81970584, No. 82270738 and 82100727), Promotion Plan of Basic and Clinical Cooperative Research in Anhui Medical University (No. 2019xkjT014 and 2020xkjT016).

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Jin, J., Liu, Xm., Shao, W. et al. Nucleic acid and protein methylation modification in renal diseases. Acta Pharmacol Sin 45, 661–673 (2024). https://doi.org/10.1038/s41401-023-01203-6

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