The Influence of Arginine Methylation in Immunity and Inflammation

References

• Blanc RS, Richard S. Arginine methylation: the coming of age. Mol Cell. 2017;65(1):8–24. doi:10.1016/j.molcel.2016.11.003
   PubMed Web of Science ®Google Scholar
• Bedford MT, Clarke SG. Protein arginine methylation in mammals: who, what, and why. Mol Cell. 2009;33(1):1–13. doi:10.1016/j.molcel.2008.12.013
   PubMed Web of Science ®Google Scholar
• Xu J, Richard S. Cellular pathways influenced by protein arginine methylation: implications for cancer. Mol Cell. 2021;81(21):4357–4368. doi:10.1016/j.molcel.2021.09.011
   PubMed Web of Science ®Google Scholar
• Jambhekar A, Anastas JN, Shi Y. Histone lysine demethylase inhibitors. Cold Spring Harb Perspect Med. 2017;7(1):a026484. doi:10.1101/cshperspect.a026484
   PubMed Web of Science ®Google Scholar
• Webby CJ, Wolf A, Gromak N, et al. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science. 2009;325(5936):90–93. doi:10.1126/science.1175865
   PubMed Web of Science ®Google Scholar
• Walport LJ, Hopkinson RJ, Chowdhury R, et al. Arginine demethylation is catalysed by a subset of JmjC histone lysine demethylases. Nat Commun. 2016;7:11974. doi:10.1038/ncomms11974
   PubMed Web of Science ®Google Scholar
• Mondal S, Thompson PR. Chemical biology of protein citrullination by the protein A arginine deiminases. Curr Opin Chem Biol. 2021;63:19–27. doi:10.1016/j.cbpa.2021.01.010
   PubMed Web of Science ®Google Scholar
• Gayatri S, Bedford MT. Readers of histone methylarginine marks. Biochim Biophys Acta. 2014;1839(8):702–710. doi:10.1016/j.bbagrm.2014.02.015
   PubMed Web of Science ®Google Scholar
• Guccione E, Richard S. The regulation, functions and clinical relevance of arginine methylation. Nat Rev Mol Cell Biol. 2019;20(10):642–657. doi:10.1038/s41580-019-0155-x
   PubMed Web of Science ®Google Scholar
• Zhang X, Bai XC, Chen ZJ. Structures and mechanisms in the cGAS-STING innate immunity pathway. Immunity. 2020;53(1):43–53. doi:10.1016/j.immuni.2020.05.013
   PubMed Web of Science ®Google Scholar
• Liu T, Zhang L, Joo D, Sun SC. NF-kappaB signaling in inflammation. Signal Transduct Target Ther. 2017;2. doi:10.1038/sigtrans.2017.23
   Web of Science ®Google Scholar
• Bjorkstrom NK, Strunz B, Ljunggren HG. Natural killer cells in antiviral immunity. Nat Rev Immunol. 2021;22:112–123. doi:10.1038/s41577-021-00558-3
   PubMed Web of Science ®Google Scholar
• Ghasemi N, Razavi S, Nikzad E. Multiple sclerosis: pathogenesis, symptoms, diagnoses and cell-based therapy. Cell J. 2017;19(1):1–10. doi:10.22074/cellj.2016.4867
   PubMed Web of Science ®Google Scholar
• Guo Q, Wang Y, Xu D, Nossent J, Pavlos NJ, Xu J. Rheumatoid arthritis: pathological mechanisms and modern pharmacologic therapies. Bone Res. 2018;6:15. doi:10.1038/s41413-018-0016-9
   PubMed Web of Science ®Google Scholar
• Kudo M, Ishigatsubo Y, Aoki I. Pathology of asthma. Front Microbiol. 2013;4:263. doi:10.3389/fmicb.2013.00263
   PubMed Web of Science ®Google Scholar
• Pawlak MR, Scherer CA, Chen J, Roshon MJ, Ruley HE. Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol Cell Biol. 2000;20(13):4859–4869. doi:10.1128/mcb.20.13.4859-4869.2000
   PubMed Web of Science ®Google Scholar
• Wang H, Huang ZQ, Xia L, et al. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science. 2001;293(5531):853–857. doi:10.1126/science.1060781
   PubMed Web of Science ®Google Scholar
• Kim JH, Yoo BC, Yang WS, Kim E, Hong S, Cho JY. The role of protein arginine methyltransferases in inflammatory responses. Mediators Inflamm. 2016;2016:4028353. doi:10.1155/2016/4028353
   PubMed Web of Science ®Google Scholar
• Fan Z, Li J, Li P, et al. Protein arginine methyltransferase 1 (PRMT1) represses MHC II transcription in macrophages by methylating CIITA. Sci Rep. 2017;7:40531. doi:10.1038/srep40531
   PubMed Web of Science ®Google Scholar
• Reintjes A, Fuchs JE, Kremser L, et al. Asymmetric arginine dimethylation of RelA provides a repressive mark to modulate TNFalpha/NF-kappaB response. Proc Natl Acad Sci U S A. 2016;113(16):4326–4331. doi:10.1073/pnas.1522372113
   PubMed Web of Science ®Google Scholar
• Kleinschmidt MA, Streubel G, Samans B, Krause M, Bauer UM. The protein arginine methyltransferases CARM1 and PRMT1 cooperate in gene regulation. Nucleic Acids Res. 2008;36(10):3202–3213. doi:10.1093/nar/gkn166
   PubMed Web of Science ®Google Scholar
• Lou X, Sun S, Chen W, et al. Negative feedback regulation of NF-kappaB action by CITED2 in the nucleus. J Immunol. 2011;186(1):539–548. doi:10.4049/jimmunol.1001650
   PubMed Web of Science ®Google Scholar
• Kryukov GV, Wilson FH, Ruth JR, et al. MTAP deletion confers enhanced dependency on the PRMT5 arginine methyltransferase in cancer cells. Science. 2016;351(6278):1214–1218. doi:10.1126/science.aad5214
   PubMed Web of Science ®Google Scholar
• Mavrakis KJ, McDonald ER, Schlabach MR, et al. Disordered methionine metabolism in MTAP/CDKN2A-deleted cancers leads to dependence on PRMT5. Science. 2016;351(6278):1208–1213. doi:10.1126/science.aad5944
   PubMed Web of Science ®Google Scholar
• Marjon K, Cameron MJ, Quang P, et al. MTAP deletions in cancer create vulnerability to targeting of the MAT2A/PRMT5/RIOK1 axis. Cell Rep. 2016;15(3):574–587. doi:10.1016/j.celrep.2016.03.043
   PubMed Web of Science ®Google Scholar
• Browne SK, Roesser JR, Zhu SZ, Ginder GD. Differential IFN-gamma stimulation of HLA-A gene expression through CRM-1-dependent nuclear RNA export. J Immunol. 2006;177(12):8612–8619. doi:10.4049/jimmunol.177.12.8612
   PubMed Web of Science ®Google Scholar
• Lafleur VN, Richard S, Richard DE. Transcriptional repression of hypoxia-inducible factor-1 (HIF-1) by the protein arginine methyltransferase PRMT1. Mol Biol Cell. 2014;25(6):925–935. doi:10.1091/mbc.E13-07-0423
   PubMed Web of Science ®Google Scholar
• Gupta P, Singh A, Gowda P, Ghosh S, Chatterjee A, Sen E. Lactate induced HIF-1alpha-PRMT1 cross talk affects MHC I expression in monocytes. Exp Cell Res. 2016;347(2):293–300. doi:10.1016/j.yexcr.2016.08.008
   PubMed Web of Science ®Google Scholar
• Mowen KA, Schurter BT, Fathman JW, David M, Glimcher LH. Arginine methylation of NIP45 modulates cytokine gene expression in effector T lymphocytes. Mol Cell. 2004;15(4):559–571. doi:10.1016/j.molcel.2004.06.042
   PubMed Web of Science ®Google Scholar
• Fathman JW, Gurish MF, Hemmers S, et al. NIP45 controls the magnitude of the type 2 T helper cell response. Proc Natl Acad Sci U S A. 2010;107(8):3663–3668. doi:10.1073/pnas.0914700107
   PubMed Web of Science ®Google Scholar
• Koch S, Knipfer L, Kolle J, et al. Targeted deletion of NFAT-interacting-protein-(NIP) 45 resolves experimental asthma by inhibiting innate lymphoid cells group 2 (ILC2). Sci Rep. 2019;9(1):15695. doi:10.1038/s41598-019-51690-z
   PubMed Web of Science ®Google Scholar
• Stopa N, Krebs JE, Shechter D. The PRMT5 arginine methyltransferase: many roles in development, cancer and beyond. Cell Mol Life Sci. 2015;72(11):2041–2059. doi:10.1007/s00018-015-1847-9
   PubMed Web of Science ®Google Scholar
• Pollack BP, Kotenko SV, He W, Izotova LS, Barnoski BL, Pestka S. The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem. 1999;274(44):31531–31542. doi:10.1074/jbc.274.44.31531
   PubMed Web of Science ®Google Scholar
• Friesen WJ, Paushkin S, Wyce A, et al. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol Cell Biol. 2001;21(24):8289–8300. doi:10.1128/MCB.21.24.8289-8300.2001
   PubMed Web of Science ®Google Scholar
• Tanaka H, Hoshikawa Y, Oh-hara T, et al. PRMT5, a novel TRAIL receptor-binding protein, inhibits TRAIL-induced apoptosis via nuclear factor-kappaB activation. Mol Cancer Res. 2009;7(4):557–569. doi:10.1158/1541-7786.Mcr-08-0197
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Nagai Y, Okumura M, Greene MI, Kambayashi T. PRMT5 is required for T cell survival and proliferation by maintaining cytokine signaling. Front Immunol. 2020;11:621. doi:10.3389/fimmu.2020.00621
   PubMed Web of Science ®Google Scholar
• Bandyopadhyay S, Harris DP, Adams GN, et al. HOXA9 methylation by PRMT5 is essential for endothelial cell expression of leukocyte adhesion molecules. Mol Cell Biol. 2012;32(7):1202–1213. doi:10.1128/mcb.05977-11
   PubMed Web of Science ®Google Scholar
• Harris DP, Bandyopadhyay S, Maxwell TJ, Willard B, DiCorleto PE. Tumor necrosis factor (TNF)-alpha induction of CXCL10 in endothelial cells requires protein arginine methyltransferase 5 (PRMT5)-mediated nuclear factor (NF)-kappaB p65 methylation. J Biol Chem. 2014;289(22):15328–15339. doi:10.1074/jbc.M114.547349
   PubMed Web of Science ®Google Scholar
• Harris DP, Chandrasekharan UM, Bandyopadhyay S, Willard B, DiCorleto PE. PRMT5-mediated methylation of NF-kappaB p65 at Arg174 is required for endothelial CXCL11 gene induction in response to TNF-alpha and IFN-gamma costimulation. PLoS One. 2016;11(2):e0148905. doi:10.1371/journal.pone.0148905
   PubMed Web of Science ®Google Scholar
• Wei H, Wang B, Miyagi M, et al. PRMT5 dimethylates R30 of the p65 subunit to activate NF-kappaB. Proc Natl Acad Sci U S A. 2013;110(33):13516–13521. doi:10.1073/pnas.1311784110
   PubMed Web of Science ®Google Scholar
• Chen D, Zeng S, Huang M, Xu H, Liang L, Yang X. Role of protein arginine methyltransferase 5 in inflammation and migration of fibroblast-like synoviocytes in rheumatoid arthritis. J Cell Mol Med. 2017;21(4):781–790. doi:10.1111/jcmm.13020
   PubMed Web of Science ®Google Scholar
• Liu H, Jia K, Ren Z, Sun J, Pan LL. PRMT5 critically mediates TMAO-induced inflammatory response in vascular smooth muscle cells. Cell Death Dis. 2022;13(4):299. doi:10.1038/s41419-022-04719-7
   PubMed Web of Science ®Google Scholar
• Smil D, Eram MS, Li F, et al. Discovery of a dual PRMT5-PRMT7 inhibitor. ACS Med Chem Lett. 2015;6(4):408–412. doi:10.1021/ml500467h
   PubMed Web of Science ®Google Scholar
• Chan-Penebre E, Kuplast KG, Majer CR, et al. A selective inhibitor of PRMT5 with in vivo and in vitro potency in MCL models. Nat Chem Biol. 2015;11(6):432–437. doi:10.1038/nchembio.1810
   PubMed Web of Science ®Google Scholar
• Gerhart SV, Kellner WA, Thompson C, et al. Activation of the p53-MDM4 regulatory axis defines the anti-tumour response to PRMT5 inhibition through its role in regulating cellular splicing. Sci Rep. 2018;8(1):9711. doi:10.1038/s41598-018-28002-y
   PubMed Web of Science ®Google Scholar
• Smith CR, Aranda R, Bobinski TP, et al. Fragment-based discovery of MRTX1719, a synthetic lethal inhibitor of the PRMT5•MTA complex for the treatment of MTAP -deleted cancers. J Med Chem. 2022;65:1749–1766. doi:10.1021/acs.jmedchem.1c01900
   PubMed Web of Science ®Google Scholar
• Shen Y, Gao G, Yu X, et al. Discovery of first-in-class protein arginine methyltransferase 5 (PRMT5) degraders. J Med Chem. 2020;63(17):9977–9989. doi:10.1021/acs.jmedchem.0c01111
   PubMed Web of Science ®Google Scholar
• Mulvaney KM, Blomquist C, Acharya N, et al. Molecular basis for substrate recruitment to the PRMT5 methylosome. Mol Cell. 2021;81(17):3481–3495e7. doi:10.1016/j.molcel.2021.07.019
   PubMed Web of Science ®Google Scholar
• Di Lorenzo A, Yang Y, Macaluso M, Bedford MT. A gain-of-function mouse model identifies PRMT6 as a NF-kappaB coactivator. Nucleic Acids Res. 2014;42(13):8297–8309. doi:10.1093/nar/gku530
   PubMed Web of Science ®Google Scholar
• Covic M, Hassa PO, Saccani S, et al. Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-kappaB-dependent gene expression. EMBO J. 2005;24(1):85–96. doi:10.1038/sj.emboj.7600500
   PubMed Web of Science ®Google Scholar
• Miao F, Li S, Chavez V, Lanting L, Natarajan R. Coactivator-associated arginine methyltransferase-1 enhances nuclear factor-kappaB-mediated gene transcription through methylation of histone H3 at arginine 17. Mol Endocrinol. 2006;20(7):1562–1573. doi:10.1210/me.2005-0365
   PubMedGoogle Scholar
• Greenblatt SM, Liu F, Nimer SD. Arginine methyltransferases in normal and malignant hematopoiesis. Exp Hematol. 2016;44(6):435–441. doi:10.1016/j.exphem.2016.03.009
   PubMed Web of Science ®Google Scholar
• Sen S, He Z, Ghosh S, et al. PRMT1 plays a critical role in Th17 differentiation by regulating reciprocal recruitment of STAT3 and STAT5. J Immunol. 2018;201(2):440–450. doi:10.4049/jimmunol.1701654
   PubMed Web of Science ®Google Scholar
• Vadnais C, Chen R, Fraszczak J, et al. GFI1 facilitates efficient DNA repair by regulating PRMT1 dependent methylation of MRE11 and 53BP1. Nat Commun. 2018;9(1):1418. doi:10.1038/s41467-018-03817-5
   PubMed Web of Science ®Google Scholar
• Bonham K, Hemmers S, Lim YH, Hill DM, Finn MG, Mowen KA. Effects of a novel arginine methyltransferase inhibitor on T-helper cell cytokine production. FEBS J. 2010;277(9):2096–2108. doi:10.1111/j.1742-4658.2010.07623.x
   PubMed Web of Science ®Google Scholar
• Dolezal E, Infantino S, Drepper F, et al. The BTG2-PRMT1 module limits pre-B cell expansion by regulating the CDK4-Cyclin-D3 complex. Nat Immunol. 2017;18(8):911–920. doi:10.1038/ni.3774
   PubMed Web of Science ®Google Scholar
• Hata K, Yanase N, Sudo K, et al. Differential regulation of T-cell dependent and T-cell independent antibody responses through arginine methyltransferase PRMT1 in vivo. FEBS Lett. 2016;590(8):1200–1210. doi:10.1002/1873-3468.12161
   PubMed Web of Science ®Google Scholar
• Infantino S, Benz B, Waldmann T, Jung M, Schneider R, Reth M. Arginine methylation of the B cell antigen receptor promotes differentiation. J Exp Med. 2010;207(4):711–719. doi:10.1084/jem.20091303
   PubMed Web of Science ®Google Scholar
• Infantino S, Light A, O’Donnell K, et al. Arginine methylation catalyzed by PRMT1 is required for B cell activation and differentiation. Nat Commun. 2017;8(1):891. doi:10.1038/s41467-017-01009-1
   PubMed Web of Science ®Google Scholar
• Zhao J, O’Neil M, Vittal A, Weinman SA, Tikhanovich I. PRMT1-dependent macrophage IL-6 production is required for alcohol-induced HCC progression. Gene Expr. 2019;19(2):137–150. doi:10.3727/105221618x15372014086197
   PubMedGoogle Scholar
• Kim J, Lee J, Yadav N, et al. Loss of CARM1 results in hypomethylation of thymocyte cyclic AMP-regulated phosphoprotein and deregulated early T cell development. J Biol Chem. 2004;279(24):25339–25344. doi:10.1074/jbc.M402544200
   PubMed Web of Science ®Google Scholar
• Kim D, Lee J, Cheng D, et al. Enzymatic activity is required for the in vivo functions of CARM1. J Biol Chem. 2010;285(2):1147–1152. doi:10.1074/jbc.M109.035865
   PubMed Web of Science ®Google Scholar
• Kumar S, Zeng Z, Bagati A, et al. CARM1 inhibition enables immunotherapy of resistant tumors by dual action on tumor cells and T cells. Cancer Discov. 2021;11(8):2050–2071. doi:10.1158/2159-8290.Cd-20-1144
   PubMed Web of Science ®Google Scholar
• Raghu D, Xue HH, Mielke LA. Control of lymphocyte fate, infection, and tumor immunity by TCF-1. Trends Immunol. 2019;40(12):1149–1162. doi:10.1016/j.it.2019.10.006
   PubMed Web of Science ®Google Scholar
• Gautam S, Fioravanti J, Zhu W, et al. The transcription factor c-Myb regulates CD8(+) T cell stemness and antitumor immunity. Nat Immunol. 2019;20(3):337–349. doi:10.1038/s41590-018-0311-z
   PubMed Web of Science ®Google Scholar
• Sen S, Wang F, Zhang J, et al. SRC1 promotes Th17 differentiation by overriding Foxp3 suppression to stimulate RORgammat activity in a PKC-theta-dependent manner. Proc Natl Acad Sci U S A. 2018;115(3):E458–E467. doi:10.1073/pnas.1717789115
   PubMed Web of Science ®Google Scholar
• Lai Y, Li X, Li T, et al. Protein arginine N-methyltransferase 4 (PRMT4) contributes to lymphopenia in experimental sepsis. Thorax. 2022;thoraxjnl-2021-217526. doi:10.1136/thoraxjnl-2021-217526
   Web of Science ®Google Scholar
• Vu LP, Perna F, Wang L, et al. PRMT4 blocks myeloid differentiation by assembling a methyl-RUNX1-dependent repressor complex. Cell Rep. 2013;5(6):1625–1638. doi:10.1016/j.celrep.2013.11.025
   PubMed Web of Science ®Google Scholar
• Greenblatt SM, Man N, Hamard PJ, et al. CARM1 is essential for myeloid leukemogenesis but dispensable for normal hematopoiesis. Cancer Cell. 2018;33(6):1111–1127e5. doi:10.1016/j.ccell.2018.05.007
   PubMed Web of Science ®Google Scholar
• Richard S, Morel M, Cleroux P. Arginine methylation regulates IL-2 gene expression: a role for protein arginine methyltransferase 5 (PRMT5). Biochem J. 2005;388(Pt1):379–386. doi:10.1042/bj20040373
   PubMed Web of Science ®Google Scholar
• Metz PJ, Ching KA, Xie T, et al. Symmetric arginine dimethylation is selectively required for mRNA splicing and the initiation of type I and type III interferon signaling. Cell Rep. 2020;30(6):1935–1950 e8. doi:10.1016/j.celrep.2020.01.054
   PubMed Web of Science ®Google Scholar
• Inoue M, Okamoto K, Terashima A, et al. Arginine methylation controls the strength of γc-family cytokine signaling in T cell maintenance. Nat Immunol. 2018;19(11):1265–1276. doi:10.1038/s41590-018-0222-z
   PubMed Web of Science ®Google Scholar
• Webb LM, Sengupta S, Edell C, et al. Protein arginine methyltransferase 5 promotes cholesterol biosynthesis-mediated Th17 responses and autoimmunity. J Clin Invest. 2020;130(4):1683–1698. doi:10.1172/JCI131254
   PubMed Web of Science ®Google Scholar
• Panfil AR, Al-Saleem J, Howard CM, et al. PRMT5 is upregulated in HTLV-1-mediated T-cell transformation and selective inhibition alters viral gene expression and infected cell survival. Viruses. 2015;8(1):7. doi:10.3390/v8010007
   PubMed Web of Science ®Google Scholar
• Igarashi H, Kuwahara K, Yoshida M, et al. GANP suppresses the arginine methyltransferase PRMT5 regulating IL-4-mediated STAT6-signaling to IgE production in B cells. Mol Immunol. 2009;46(6):1031–1041. doi:10.1016/j.molimm.2008.08.272
   PubMed Web of Science ®Google Scholar
• Alinari L, Mahasenan KV, Yan F, et al. Selective inhibition of protein arginine methyltransferase 5 blocks initiation and maintenance of B-cell transformation PRMT5 promotes Cyclin E1 and cell cycle progression in CD4 Th1 cells and correlates with EAE severity. Blood. 2015;125(16):2530–2543. doi:10.1182/blood-2014-12-619783
   PubMed Web of Science ®Google Scholar
• Pal S, Vishwanath SN, Erdjument-Bromage H, Tempst P, Sif S. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol Cell Biol. 2004;24(21):9630–9645. doi:10.1128/MCB.24.21.9630-9645.2004
   PubMed Web of Science ®Google Scholar
• Majumder S, Alinari L, Roy S, et al. Methylation of histone H3 and H4 by PRMT5 regulates ribosomal RNA gene transcription. J Cell Biochem. 2010;109(3):553–563. doi:10.1002/jcb.22432
   PubMed Web of Science ®Google Scholar
• Liu F, Cheng G, Hamard PJ, et al. Arginine methyltransferase PRMT5 is essential for sustaining normal adult hematopoiesis. J Clin Invest. 2015;125(9):3532–3544. doi:10.1172/jci81749
   PubMed Web of Science ®Google Scholar
• Litzler LC, Zahn A, Meli AP, et al. PRMT5 is essential for B cell development and germinal center dynamics. Nat Commun. 2019;10(1):22. doi:10.1038/s41467-018-07884-6
   PubMed Web of Science ®Google Scholar
• Ying Z, Mei M, Zhang P, et al. Histone arginine methylation by PRMT7 controls germinal center formation via regulating Bcl6 transcription. J Immunol. 2015;195(4):1538–1547. doi:10.4049/jimmunol.1500224
   PubMed Web of Science ®Google Scholar
• Jain K, Jin CY, Clarke SG. Epigenetic control via allosteric regulation of mammalian protein arginine methyltransferases. Proc Natl Acad Sci U S A. 2017;114(38):10101–10106. doi:10.1073/pnas.1706978114
   PubMed Web of Science ®Google Scholar
• Sun Q, Liu L, Roth M, et al. PRMT1 upregulated by epithelial proinflammatory cytokines participates in COX2 expression in fibroblasts and chronic antigen-induced pulmonary inflammation. J Immunol. 2015;195(1):298–306. doi:10.4049/jimmunol.1402465
   PubMed Web of Science ®Google Scholar
• Sun Q, Yang X, Zhong B, et al. Upregulated protein arginine methyltransferase 1 by IL-4 increases eotaxin-1 expression in airway epithelial cells and participates in antigen-induced pulmonary inflammation in rats. J Immunol. 2012;188(7):3506–3512. doi:10.4049/jimmunol.1102635
   PubMed Web of Science ®Google Scholar
• Liu L, Sun Q, Bao R, et al. Specific regulation of PRMT1 expression by PIAS1 and RKIP in BEAS-2B epithelia cells and HFL-1 fibroblasts in lung inflammation. Sci Rep. 2016;6:21810. doi:10.1038/srep21810
   PubMed Web of Science ®Google Scholar
• Zhai W, Sun H, Li Z, et al. PRMT1 modulates processing of asthma-related primary MicroRNAs (Pri-miRNAs) into mature miRNAs in lung epithelial cells. J Immunol. 2021;206(1):11–22. doi:10.4049/jimmunol.2000887
   PubMed Web of Science ®Google Scholar
• Bultink IE, Teerlink T, Heijst JA, Dijkmans BA, Voskuyl AE. Raised plasma levels of asymmetric dimethylarginine are associated with cardiovascular events, disease activity, and organ damage in patients with systemic lupus erythematosus. Ann Rheum Dis. 2005;64(9):1362–1365. doi:10.1136/ard.2005.036137
   PubMed Web of Science ®Google Scholar
• Arbuckle MR, McClain MT, Rubertone MV, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349(16):1526–1533. doi:10.1056/NEJMoa021933
   PubMed Web of Science ®Google Scholar
• Chang HH, Hu HH, Lee YJ, et al. Proteomic analyses and identification of arginine methylated proteins differentially recognized by autosera from anti-Sm positive SLE patients. J Biomed Sci. 2013;20:27. doi:10.1186/1423-0127-20-27
   PubMed Web of Science ®Google Scholar
• Beniac DR, Wood DD, Palaniyar N, Ottensmeyer FP, Moscarello MA, Harauz G. Cryoelectron microscopy of protein-lipid complexes of human myelin basic protein charge isomers differing in degree of citrullination. J Struct Biol. 2000;129(1):80–95. doi:10.1006/jsbi.1999.4200
   PubMed Web of Science ®Google Scholar
• Baldwin GS, Carnegie PR. Specific enzymic methylation of an arginine in the experimental allergic encephalomyelitis protein from human myelin. Science. 1971;171(3971):579–581. doi:10.1126/science.171.3971.579
   PubMed Web of Science ®Google Scholar
• Rho J, Choi S, Seong YR, Cho WK, Kim SH, Im DS. Prmt5, which forms distinct homo-oligomers, is a member of the protein-arginine methyltransferase family. J Biol Chem. 2001;276(14):11393–11401. doi:10.1074/jbc.M008660200
   PubMed Web of Science ®Google Scholar
• Amur SG, Shanker G, Cochran JM, Ved HS, Pieringer RA. Correlation between inhibition of myelin basic protein (arginine) methyltransferase by sinefungin and lack of compact myelin formation in cultures of cerebral cells from embryonic mice. J Neurosci Res. 1986;16(2):367–376. doi:10.1002/jnr.490160204
   PubMed Web of Science ®Google Scholar
• Crang AJ, Jacobson W. The relationship of myelin basic protein (arginine) methyltransferase to myelination in mouse spinal cord. J Neurochem. 1982;39(1):244–247. doi:10.1111/j.1471-4159.1982.tb04726.x
   PubMed Web of Science ®Google Scholar
• Kim S, Lim IK, Park GH, Paik WK. Biological methylation of myelin basic protein: enzymology and biological significance. Int J Biochem Cell Biol. 1997;29(5):743–751. doi:10.1016/s1357-2725(97)00009-5
   PubMed Web of Science ®Google Scholar
• Webb LM, Amici SA, Jablonski KA, et al. PRMT5-selective inhibitors suppress inflammatory T cell responses and experimental autoimmune encephalomyelitis. J Immunol. 2017;198(4):1439–1451. doi:10.4049/jimmunol.1601702
   PubMed Web of Science ®Google Scholar
• Amici SA, Osman W, Guerau-de-Arellano M. PRMT5 promotes cyclin E1 and cell cycle progression in CD4 Th1 cells and correlates with EAE severity. Front Immunol. 2021;12:695947. doi:10.3389/fimmu.2021.695947
   PubMed Web of Science ®Google Scholar
• Snyder KJ, Zitzer NC, Gao Y, et al. PRMT5 regulates T cell interferon response and is a target for acute graft-versus-host disease. JCI Insight. 2020;5(8). doi:10.1172/jci.insight.131099
   Web of Science ®Google Scholar
• Fedoriw A, Rajapurkar SR, O’Brien S, et al. Anti-tumor activity of the type I PRMT inhibitor, GSK3368715, synergizes with PRMT5 inhibition through MTAP loss. Cancer Cell. 2019;36(1):100–114e25. doi:10.1016/j.ccell.2019.05.014
   PubMed Web of Science ®Google Scholar
• Fong JY, Pignata L, Goy PA, et al. Therapeutic targeting of RNA splicing catalysis through inhibition of protein arginine methylation. Cancer Cell. 2019;36(2):194–209 e9. doi:10.1016/j.ccell.2019.07.003
   PubMed Web of Science ®Google Scholar
• Zheng Y, Huang L, Ge W, et al. Protein arginine methyltransferase 5 inhibition upregulates Foxp3(+) regulatory T cells frequency and function during the ulcerative colitis. Front Immunol. 2017;8:596. doi:10.3389/fimmu.2017.00596
   PubMed Web of Science ®Google Scholar
• Liu F, Xu Y, Lu X, et al. PRMT5-mediated histone arginine methylation antagonizes transcriptional repression by polycomb complex PRC2. Nucleic Acids Res. 2020;48(6):2956–2968. doi:10.1093/nar/gkaa065
   PubMed Web of Science ®Google Scholar
• Dong Y, Wang P, Yang Y, et al. PRMT5 inhibition attenuates cartilage degradation by reducing MAPK and NF-kappaB signaling. Arthritis Res Ther. 2020;22(1):201. doi:10.1186/s13075-020-02304-x
   PubMed Web of Science ®Google Scholar
• Burska AN, Hunt L, Boissinot M, et al. Autoantibodies to posttranslational modifications in rheumatoid arthritis. Mediators Inflamm. 2014;2014:492873. doi:10.1155/2014/492873
   PubMed Web of Science ®Google Scholar
• Snir O, Widhe M, von Spee C, et al. Multiple antibody reactivities to citrullinated antigens in sera from patients with rheumatoid arthritis: association with HLA-DRB1 alleles. Ann Rheum Dis. 2009;68(5):736–743. doi:10.1136/ard.2008.091355
   PubMed Web of Science ®Google Scholar
• Chandrasekharan UM, Wang Z, Wu Y, et al. Elevated levels of plasma symmetric dimethylarginine and increased arginase activity as potential indicators of cardiovascular comorbidity in rheumatoid arthritis. Arthritis Res Ther. 2018;20(1):123. doi:10.1186/s13075-018-1616-x
   PubMed Web of Science ®Google Scholar
• Hou J, Wang Y, Shi L, et al. Integrating genome-wide CRISPR immune screen with multi-omic clinical data reveals distinct classes of tumor intrinsic immune regulators. J Immunother Cancer. 2021;9(2). doi:10.1136/jitc-2020-001819
   Web of Science ®Google Scholar
• Zheng NN, Zhou M, Sun F, et al. Combining protein arginine methyltransferase inhibitor and anti-programmed death-ligand-1 inhibits pancreatic cancer progression. World J Gastroenterol. 2020;26(26):3737–3749. doi:10.3748/wjg.v26.i26.3737
   PubMed Web of Science ®Google Scholar
• Lu SX, De Neef E, Thomas JD, et al. Pharmacologic modulation of RNA splicing enhances anti-tumor immunity. Cell. 2021;184(15):4032–4047 e31. doi:10.1016/j.cell.2021.05.038
   PubMed Web of Science ®Google Scholar
• Schonfeld M, Zhao J, Komatz A, Weinman SA, Tikhanovich I. The polymorphism rs975484 in the protein arginine methyltransferase 1 gene modulates expression of immune checkpoint genes in hepatocellular carcinoma. J Biol Chem. 2020;295(20):7126–7137. doi:10.1074/jbc.RA120.013401
   PubMed Web of Science ®Google Scholar
• Drew AE, Moradei O, Jacques SL, et al. Identification of a CARM1 inhibitor with potent in vitro and in vivo activity in preclinical models of multiple myeloma. Sci Rep. 2017;7(1):17993. doi:10.1038/s41598-017-18446-z
   PubMed Web of Science ®Google Scholar
• Zhang Z, Guo Z, Xu X, et al. Structure-based discovery of potent CARM1 inhibitors for solid tumor and cancer immunology therapy. J Med Chem. 2021;64(22):16650–16674. doi:10.1021/acs.jmedchem.1c01308
   PubMed Web of Science ®Google Scholar
• Fedoriw A, Shi L, O’Brien S, et al. Inhibiting type I arginine methyltransferase activity promotes the T cell mediated antitumor immune response. Cancer Immunol Res. 2022;10:420–436. doi:10.1158/2326-6066.CIR-21-0614
   PubMed Web of Science ®Google Scholar
• Kim H, Kim H, Feng Y, et al. PRMT5 control of cGAS/STING and NLRC5 pathways defines melanoma response to antitumor immunity. Sci Transl Med. 2020;12(551). doi:10.1126/scitranslmed.aaz5683
   Web of Science ®Google Scholar
• Nagai Y, Ji MQ, Zhu F, et al. PRMT5 associates with the FOXP3 homomer and when disabled enhances targeted p185(erbB2/neu) tumor immunotherapy. Front Immunol. 2019;10:174. doi:10.3389/fimmu.2019.00174
   PubMed Web of Science ®Google Scholar
• Srour N, Villarreal OD, Hardikar S, et al. PRMT7 ablation stimulates anti-tumor immunity and sensitizes melanoma to immune checkpoint blockade. Cell Rep. 2022;38(13):110582. doi:10.1016/j.celrep.2022.110582
   PubMed Web of Science ®Google Scholar
• Szewczyk MM, Ishikawa Y, Organ S, et al. Pharmacological inhibition of PRMT7 links arginine monomethylation to the cellular stress response. Nat Commun. 2020;11(1):2396. doi:10.1038/s41467-020-16271-z
   PubMed Web of Science ®Google Scholar
• Yan Z, Wu H, Liu H, et al. The protein arginine methyltransferase PRMT1 promotes TBK1 activation through asymmetric arginine methylation. Cell Rep. 2021;36(12):109731. doi:10.1016/j.celrep.2021.109731
   PubMed Web of Science ®Google Scholar
• Zhu J, Liu X, Cai X, et al. Zebrafish prmt7 negatively regulates antiviral responses by suppressing the retinoic acid-inducible gene-I-like receptor signaling. FASEB J. 2020;34(1):988–1000. doi:10.1096/fj.201902219R
   PubMed Web of Science ®Google Scholar
• Zhu J, Liu X, Cai X, et al. Zebrafish prmt3 negatively regulates antiviral responses. FASEB J. 2020;34(8):10212–10227. doi:10.1096/fj.201902569R
   PubMed Web of Science ®Google Scholar
• Zhu J, Li X, Cai X, et al. Arginine monomethylation by PRMT7 controls MAVS-mediated antiviral innate immunity. Mol Cell. 2021;81(15):3171–3186e8. doi:10.1016/j.molcel.2021.06.004
   PubMed Web of Science ®Google Scholar
• Ma D, Yang M, Wang Q, et al. Arginine methyltransferase PRMT5 negatively regulates cGAS-mediated antiviral immune response. Sci Adv. 2021;7(13). doi:10.1126/sciadv.abc1834
   Web of Science ®Google Scholar
• Cui S, Yu Q, Chu L, et al. Nuclear cGAS functions non-canonically to enhance antiviral immunity via recruiting methyltransferase Prmt5. Cell Rep. 2020;33(10):108490. doi:10.1016/j.celrep.2020.108490
   PubMed Web of Science ®Google Scholar
• Zhang H, Han C, Li T, Li N, Cao X. The methyltransferase PRMT6 attenuates antiviral innate immunity by blocking TBK1-IRF3 signaling. Cell Mol Immunol. 2019;16(10):800–809. doi:10.1038/s41423-018-0057-4
   PubMed Web of Science ®Google Scholar
• Jiang Y, Liu L, Yang S, et al. Black carp PRMT6 inhibits TBK1-IRF3/7 signaling during the antiviral innate immune activation. Fish Shellfish Immunol. 2019;93:108–115. doi:10.1016/j.fsi.2019.07.044
   PubMed Web of Science ®Google Scholar
• Boulanger MC, Liang C, Russell RS, et al. Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J Virol. 2005;79(1):124–131. doi:10.1128/jvi.79.1.124-131.2005
   PubMed Web of Science ®Google Scholar
• Fulcher AJ, Sivakumaran H, Jin H, Rawle DJ, Harrich D, Jans DA. The protein arginine methyltransferase PRMT6 inhibits HIV-1 Tat nucleolar retention. Biochim Biophys Acta. 2016;1863(2):254–262. doi:10.1016/j.bbamcr.2015.11.019
   PubMed Web of Science ®Google Scholar
• Sivakumaran H, van der Horst A, Fulcher AJ, et al. Arginine methylation increases the stability of human immunodeficiency virus type 1 Tat. J Virol. 2009;83(22):11694–11703. doi:10.1128/jvi.00499-09
   PubMed Web of Science ®Google Scholar
• Invernizzi CF, Xie B, Frankel FA, et al. Arginine methylation of the HIV-1 nucleocapsid protein results in its diminished function. AIDS. 2007;21(7):795–805. doi:10.1097/QAD.0b013e32803277ae
   PubMed Web of Science ®Google Scholar
• Murakami H, Suzuki T, Tsuchiya K, et al. Protein arginine N-methyltransferases 5 and 7 promote HIV-1 production. Viruses. 2020;12(3):355. doi:10.3390/v12030355
   PubMed Web of Science ®Google Scholar
• Barrera A, Ramos H, Vera-Otarola J, et al. Post-translational modifications of hnRNP A1 differentially modulate retroviral IRES-mediated translation initiation. Nucleic Acids Res. 2020;48(18):10479–10499. doi:10.1093/nar/gkaa765
   PubMed Web of Science ®Google Scholar
• Lubyova B, Hodek J, Zabransky A, et al. PRMT5: a novel regulator of Hepatitis B virus replication and an arginine methylase of HBV core. PLoS One. 2017;12(10):e0186982. doi:10.1371/journal.pone.0186982
   PubMed Web of Science ®Google Scholar
• Cai T, Yu Z, Wang Z, Liang C, Richard S. Arginine methylation of SARS-Cov-2 nucleocapsid protein regulates RNA binding, its ability to suppress stress granule formation, and viral replication. J Biol Chem. 2021;297(1):100821. doi:10.1016/j.jbc.2021.100821
   PubMed Web of Science ®Google Scholar
• Liang Z, Wen C, Jiang H, Ma S, Liu X. Protein arginine methyltransferase 5 functions via interacting proteins. Front Cell Dev Biol. 2021;9:725301. doi:10.3389/fcell.2021.725301
   PubMed Web of Science ®Google Scholar
• McKinney DC, McMillan BJ, Ranaghan MJ, et al. Discovery of a First-in-Class Inhibitor of the PRMT5-Substrate Adaptor Interaction. J Med Chem. 2021;64(15):11148–11168. doi:10.1021/acs.jmedchem.1c00507
   PubMed Web of Science ®Google Scholar
• Hwang JW, Cho Y, Bae GU, Kim SN, Kim YK. Protein arginine methyltransferases: promising targets for cancer therapy. Exp Mol Med. 2021;53(5):788–808. doi:10.1038/s12276-021-00613-y
   PubMed Web of Science ®Google Scholar
• Eram MS, Shen Y, Szewczyk M, et al. A potent, selective, and cell-active inhibitor of human type I protein arginine methyltransferases. ACS Chem Biol. 2016;11(3):772–781. doi:10.1021/acschembio.5b00839
   PubMed Web of Science ®Google Scholar
• Shen Y, Szewczyk MM, Eram MS, et al. Discovery of a potent, selective, and cell-active dual inhibitor of protein arginine methyltransferase 4 and protein arginine methyltransferase 6. J Med Chem. 2016;59(19):9124–9139. doi:10.1021/acs.jmedchem.6b01033
   PubMed Web of Science ®Google Scholar
• Mitchell LH, Drew AE, Ribich SA, et al. Aryl pyrazoles as potent inhibitors of arginine methyltransferases: identification of the first PRMT6 tool compound. ACS Med Chem Lett. 2015;6(6):655–659. doi:10.1021/acsmedchemlett.5b00071
   PubMed Web of Science ®Google Scholar
• Kaushik S, Liu F, Veazey KJ, et al. Genetic deletion or small-molecule inhibition of the arginine methyltransferase PRMT5 exhibit anti-tumoral activity in mouse models of MLL-rearranged AML. Leukemia. 2018;32(2):499–509. doi:10.1038/leu.2017.206
   PubMed Web of Science ®Google Scholar
• Vinet M, Suresh S, Maire V, et al. Protein arginine methyltransferase 5: a novel therapeutic target for triple-negative breast cancers. Cancer Med. 2019;8(5):2414–2428. doi:10.1002/cam4.2114
   PubMed Web of Science ®Google Scholar
• Huang T, Yang Y, Song X, et al. PRMT6 methylation of RCC1 regulates mitosis, tumorigenicity, and radiation response of glioblastoma stem cells. Mol Cell. 2021;81(6):1276–1291e9. doi:10.1016/j.molcel.2021.01.015
   PubMed Web of Science ®Google Scholar