785
Views
0
CrossRef citations to date
0
Altmetric
Review

Multiple roles for AU-rich RNA binding proteins in the development of haematologic malignancies and their resistance to chemotherapy

&
Pages 1-17 | Accepted 08 Apr 2024, Published online: 27 May 2024

References

  • Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discov. 2022;12(1):31–46. doi: 10.1158/2159-8290.CD-21-1059
  • Pakos-Zebrucka K, Koryga I, Mnich K, et al. The integrated stress response. EMBO Rep. 2016;17(10):1374–1395. doi: 10.15252/embr.201642195
  • Costa-Mattioli M, Walter P. The integrated stress response: from mechanism to disease. Science. 2020;368(6489). doi: 10.1126/science.aat5314
  • Hetz C, Zhang K, Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol Cell Biol. 2020;21(8):421–438. doi: 10.1038/s41580-020-0250-z
  • Heberle AM, Prentzell MT, van Eunen K, et al. Molecular mechanisms of mTOR regulation by stress. Mol Cell Oncol. 2015;2(2):e970489. doi: 10.4161/23723548.2014.970489
  • Li X, He S, Ma B. Autophagy and autophagy-related proteins in cancer. Mol Cancer. 2020;19(1):12. doi: 10.1186/s12943-020-1138-4
  • Zhu J, Thompson CB. Metabolic regulation of cell growth and proliferation. Nat Rev Mol Cell Biol. 2019;20(7):436–450. doi: 10.1038/s41580-019-0123-5
  • Folmes CD, Dzeja PP, Nelson TJ, et al. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell. 2012;11(5):596–606. doi: 10.1016/j.stem.2012.10.002
  • Tarazona OA, Pourquie O. Exploring the influence of cell metabolism on cell fate through protein post-translational modifications. Dev Cell. 2020;54(2):282–292. doi: 10.1016/j.devcel.2020.06.035
  • Matsumura T, Nakamura-Ishizu A, Muddineni S, et al. Hematopoietic stem cells acquire survival advantage by loss of RUNX1 methylation identified in familial leukemia. Blood. 2020;136(17):1919–1932. doi: 10.1182/blood.2019004292
  • Wortel IMN, van der Meer LT, Kilberg MS, et al. Surviving stress: modulation of ATF4-mediated stress responses in normal and malignant cells. Trends Endocrinol Metab. 2017;28(11):794–806. doi: 10.1016/j.tem.2017.07.003
  • Wolczyk M, Serwa R, Kominek A, et al. TIAR and FMRP shape pro-survival nascent proteome of leukemia cells in the bone marrow microenvironment. iScience. 2023;26(4):106543. doi: 10.1016/j.isci.2023.106543
  • Lee S, Micalizzi D, Truesdell SS, et al. A post-transcriptional program of chemoresistance by AU-rich elements and TTP in quiescent leukemic cells. Genome Biol. 2020;21(1):33. doi: 10.1186/s13059-020-1936-4
  • Kilchert C, Strasser K, Kunetsky V, et al. From parts lists to functional significance-RNA-protein interactions in gene regulation. Wiley Interdiscip Rev RNA. 2020;11(3):e1582. doi: 10.1002/wrna.1582
  • Hentze MW, Castello A, Schwarzl T, et al. A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol. 2018;19(5):327–341. doi: 10.1038/nrm.2017.130
  • Muller-McNicoll M, Rossbach O, Hui J, et al. Auto-regulatory feedback by RNA-binding proteins. J Mol Cell Biol. 2019;11(10):930–939. doi: 10.1093/jmcb/mjz043
  • Quattrone A, Dassi E. The architecture of the human RNA-Binding protein regulatory network. iScience. 2019;21:706–719. doi: 10.1016/j.isci.2019.10.058
  • Wang E, Zhou H, Nadorp B, et al. Surface antigen-guided CRISPR screens identify regulators of myeloid leukemia differentiation. Cell Stem Cell. 2021;28(4):718–31 e6. doi: 10.1016/j.stem.2020.12.005
  • Izquierdo JM, Valcarcel J. Two isoforms of the T-cell intracellular antigen 1 (TIA-1) splicing factor display distinct splicing regulation activities. Control of TIA-1 isoform ratio by TIA-1-related protein. J Biol Chem. 2007;282(27):19410–19417. doi: 10.1074/jbc.M700688200
  • Lee FCY, Ule J. Advances in CLIP technologies for studies of protein-RNA interactions. Mol Cell. 2018;69(3):354–369. doi: 10.1016/j.molcel.2018.01.005
  • Garcia-Maurino SM, Rivero-Rodriguez F, Velazquez-Cruz A, et al. RNA binding protein regulation and cross-talk in the control of AU-rich mRNA fate. Front Mol Biosci. 2017;4:71. doi: 10.3389/fmolb.2017.00071
  • Otsuka H, Fukao A, Funakami Y, et al. Emerging evidence of translational control by AU-Rich element-binding proteins. Front Genet. 2019;10:332. doi: 10.3389/fgene.2019.00332
  • Bakheet T, Williams BR, Khabar KS. ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res. 2006;34(Database issue):D111–4. doi: 10.1093/nar/gkj052
  • Gruber AR, Fallmann J, Kratochvill F, et al. Aresite: a database for the comprehensive investigation of AU-rich elements. Nucleic Acids Res. 2011;39(Database issue):D66–9. doi: 10.1093/nar/gkq990
  • Lebedeva S, Jens M, Theil K, et al. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell. 2011;43(3):340–352. doi: 10.1016/j.molcel.2011.06.008
  • Binas O, Tants JN, Peter SA, et al. Structural basis for the recognition of transiently structured AU-rich elements by Roquin. Nucleic Acids Res. 2020;48(13):7385–7403. doi: 10.1093/nar/gkaa465
  • Tan D, Zhou M, Kiledjian M, et al. The ROQ domain of Roquin recognizes mRNA constitutive-decay element and double-stranded RNA. Nat Struct Mol Biol. 2014;21(8):679–685. doi: 10.1038/nsmb.2857
  • Podszywalow-Bartnicka P, Wolczyk M, Kusio-Kobialka M, et al. Downregulation of BRCA1 protein in BCR-ABL1 leukemia cells depends on stress-triggered TIAR-mediated suppression of translation. Cell Cycle. 2014;13(23):3727–3741. doi: 10.4161/15384101.2014.965013
  • Vujovic A, de Rooij L, Chahi AK, et al. In vivo screening unveils pervasive RNA-Binding protein dependencies in leukemic stem cells and identifies ELAVL1 as a therapeutic target. Blood Cancer Discov. 2023;4(3):180–207. doi: 10.1158/2643-3230.BCD-22-0086
  • Tang YJ, Wu W, Chen QQ, et al. miR-29b-3p suppresses the malignant biological behaviors of AML cells via inhibiting NF-kappaB and JAK/STAT signaling pathways by targeting HuR. BMC Cancer. 2022;22(1):909. doi: 10.1186/s12885-022-09996-1
  • Bergalet J, Fawal M, Lopez C, et al. HuR-mediated control of C/EBPbeta mRNA stability and translation in ALK-positive anaplastic large cell lymphomas. Mol Cancer Res. 2011;9(4):485–496. doi: 10.1158/1541-7786.MCR-10-0351
  • Wang LJ, Lee YC, Chiou JT, et al. Effects of SIDT2 on the miR-25/NOX4/HuR axis and SIRT3 mRNA stability lead to ROS-mediated TNF-α expression in hydroquinone-treated leukemia cells. Cell Biol Toxicol. 2022;39(5):2207–2225. doi: 10.1007/s10565-022-09705-5
  • Young DJ, Stoddart A, Nakitandwe J, et al. Knockdown of Hnrnpa0, a del(5q) gene, alters myeloid cell fate in murine cells through regulation of AU-rich transcripts. Haematologica. 2014;99(6):1032–1040. doi: 10.3324/haematol.2013.098657
  • Cannell IG, Merrick KA, Morandell S, et al. A pleiotropic RNA-Binding protein controls distinct cell cycle checkpoints to drive resistance of p53-defective tumors to chemotherapy. Cancer Cell. 2015;28(5):623–637. doi: 10.1016/j.ccell.2015.09.009
  • Wilson GM, Lu J, Sutphen K, et al. Phosphorylation of p40AUF1 regulates binding to a + U-rich mRNA-destabilizing elements and protein-induced changes in ribonucleoprotein structure. J Biol Chem. 2003;278(35):33039–33048. doi: 10.1074/jbc.M305775200
  • Wilson GM, Lu J, Sutphen K, et al. Regulation of a + U-rich element-directed mRNA turnover involving reversible phosphorylation of AUF1. J Biol Chem. 2003;278(35):33029–33038. doi: 10.1074/jbc.M305772200
  • Fawal M, Armstrong F, Ollier S, et al. A “liaison dangereuse” between AUF1/hnRNPD and the oncogenic tyrosine kinase NPM-ALK. Blood. 2006;108(8):2780–2788. doi: 10.1182/blood-2006-04-014902
  • Zhang R, Lin P, Yang X, et al. Survival associated alternative splicing events in diffuse large B-cell lymphoma. Am J Transl Res. 2018;10(8):2636–2647.
  • Dolatshad H, Pellagatti A, Fernandez-Mercado M, et al. Disruption of SF3B1 results in deregulated expression and splicing of key genes and pathways in myelodysplastic syndrome hematopoietic stem and progenitor cells. Leukemia. 2015;29(5):1092–1103. doi: 10.1038/leu.2014.331
  • Lima M. Aggressive mature natural killer cell neoplasms: from epidemiology to diagnosis. Orphanet J Rare Dis. 2013;8(1):95. doi: 10.1186/1750-1172-8-95
  • Wolczyk M, Podszywalow-Bartnicka P, Bugajski L, et al. Stress granules assembly affects detection of mRNA in living cells by the NanoFlares; an important aspect of the technology. Biochim Biophys Acta Gen Subj. 2017;1861(5 Pt A):1024–1035. doi: 10.1016/j.bbagen.2017.02.010
  • Karmakar S, Ramirez O, Paul KV, et al. Integrative genome-wide analysis reveals EIF3A as a key downstream regulator of translational repressor protein Musashi 2 (MSI2). NAR Cancer. 2022;4(2):zcac015. doi: 10.1093/narcan/zcac015
  • Ito T, Kwon HY, Zimdahl B, et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature. 2010;466(7307):765–768. doi: 10.1038/nature09171
  • Kharas MG, Lengner CJ, Al-Shahrour F, et al. Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nat Med. 2010;16(8):903–908. doi: 10.1038/nm.2187
  • Griner LN, Reuther GW. Aggressive myeloid leukemia formation is directed by the Musashi 2/Numb pathway. Cancer Biol Ther. 2010;10(10):979–982. doi: 10.4161/cbt.10.10.14010
  • Han Y, Ye A, Zhang Y, et al. Musashi-2 silencing exerts potent activity against acute myeloid leukemia and enhances chemosensitivity to Daunorubicin. PLOS ONE. 2015;10(8):e0136484. doi: 10.1371/journal.pone.0136484
  • Kwon HY, Bajaj J, Ito T, et al. Tetraspanin 3 is required for the development and propagation of acute myelogenous leukemia. Cell Stem Cell. 2015;17(2):152–164. doi: 10.1016/j.stem.2015.06.006
  • Vu LP, Prieto C, Amin EM, et al. Functional screen of MSI2 interactors identifies an essential role for SYNCRIP in myeloid leukemia stem cells. Nat Genet. 2017;49(6):866–875. doi: 10.1038/ng.3854
  • Rounbehler RJ, Fallahi M, Yang C, et al. Tristetraprolin impairs myc-induced lymphoma and abolishes the malignant state. Cell. 2012;150(3):563–574. doi: 10.1016/j.cell.2012.06.033
  • Kagoya Y, Nakatsugawa M, Ochi T, et al. Transient stimulation expands superior antitumor T cells for adoptive therapy. JCI Insight. 2017;2(2):e89580. doi: 10.1172/jci.insight.89580
  • Kaehler M, Dworschak M, Rodin JP, et al. ZFP36L1 plays an ambiguous role in the regulation of cell expansion and negatively regulates CDKN1A in chronic myeloid leukemia cells. Exp Hematol. 2021;99:54–64 e7. doi: 10.1016/j.exphem.2021.05.006
  • Jeltsch KM, Hu D, Brenner S, et al. Cleavage of roquin and regnase-1 by the paracaspase MALT1 releases their cooperatively repressed targets to promote T(H)17 differentiation. Nat Immunol. 2014;15(11):1079–1089. doi: 10.1038/ni.3008
  • Wimberger N, Ober F, Avar G, et al. Oncogene-induced MALT1 protease activity drives post-transcriptional gene expression in malignant lymphomas. Blood. 2023;142(23):1985–2001. doi: 10.1182/blood.2023021299
  • Kidoya H, Muramatsu F, Shimamura T, et al. Regnase-1-mediated post-transcriptional regulation is essential for hematopoietic stem and progenitor cell homeostasis. Nat Commun. 2019;10(1):1072. doi: 10.1038/s41467-019-09028-w
  • Okuda H, Miyamoto R, Takahashi S, et al. RNA-binding proteins of KHDRBS and IGF2BP families control the oncogenic activity of MLL-AF4. Nat Commun. 2022;13(1):6688. doi: 10.1038/s41467-022-34558-1
  • Sumithra B, Saxena U, Das AB. A comprehensive study on genome-wide coexpression network of KHDRBS1/Sam68 reveals its cancer and patient-specific association. Sci Rep. 2019;9(1):11083. doi: 10.1038/s41598-019-47558-x
  • Wang Q, Li Y, Cheng J, et al. Sam68 affects cell proliferation and apoptosis of human adult T-acute lymphoblastic leukemia cells via AKT/mTOR signal pathway. Leuk Res. 2016;46:1–9.
  • Xu J, Wang D, Ma H, et al. KHSRP combines transcriptional and posttranscriptional mechanisms to regulate monocytic differentiation. Blood Sci. 2022;4(3):103–115. doi: 10.1097/BS9.0000000000000122
  • Kafer R, Schmidtke L, Schrick K, et al. The RNA-Binding protein KSRP modulates cytokine expression of CD4(+) T cells. J Immunol Res. 2019;2019:4726532.
  • Zhang Y, Peng L, Hu T, et al. La-related protein 4B maintains murine MLL-AF9 leukemia stem cell self-renewal by regulating cell cycle progression. Exp Hematol. 2015;43(4):309–18 e2. doi: 10.1016/j.exphem.2014.12.003
  • Corley M, Burns MC, Yeo GW. How RNA-Binding proteins interact with RNA: molecules and mechanisms. Mol Cell. 2020;78(1):9–29. doi: 10.1016/j.molcel.2020.03.011
  • Meyer C, Garzia A, Mazzola M, et al. The TIA1 RNA-Binding protein family regulates EIF2AK2-mediated stress response and cell cycle progression. Mol Cell. 2018;69(4):622–35 e6. doi: 10.1016/j.molcel.2018.01.011
  • Del Gatto-Konczak F, Bourgeois CF, Le Guiner C, et al. The RNA-binding protein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5’ splice site. Mol Cell Biol. 2000;20(17):6287–6299. doi: 10.1128/MCB.20.17.6287-6299.2000
  • Forch P, Puig O, Martinez C, et al. The splicing regulator TIA-1 interacts with U1-C to promote U1 snRNP recruitment to 5’ splice sites. Embo J. 2002;21(24):6882–6892. doi: 10.1093/emboj/cdf668
  • Gal-Mark N, Schwartz S, Ram O, et al. The pivotal roles of TIA proteins in 5’ splice-site selection of alu exons and across evolution. PLOS Genet. 2009;5(11):e1000717. doi: 10.1371/journal.pgen.1000717
  • Wang Z, Kayikci M, Briese M, et al. iCLIP predicts the dual splicing effects of TIA-RNA interactions. PLOS Biol. 2010;8(10):e1000530. doi: 10.1371/journal.pbio.1000530
  • Mukherjee N, Corcoran DL, Nusbaum JD, et al. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell. 2011;43(3):327–339. doi: 10.1016/j.molcel.2011.06.007
  • Li Y, Estep JA, Karginov FV. Transcriptome-wide identification and validation of interactions between the miRNA machinery and HuR on mRNA targets. J Mol Biol. 2018;430(3):285–296. doi: 10.1016/j.jmb.2017.12.006
  • Yoon JH, De S, Srikantan S, et al. PAR-CLIP analysis uncovers AUF1 impact on target RNA fate and genome integrity. Nat Commun. 2014;5(1):5248. doi: 10.1038/ncomms6248
  • Myer VE, Steitz JA. Isolation and characterization of a novel, low abundance hnRNP protein: A0. RNA. 1995;1(2):171–182.
  • Thibault PA, Ganesan A, Kalyaanamoorthy S, et al. hnRNP A/B proteins: an encyclopedic assessment of their roles in homeostasis and disease. Biology. 2021;10(8):712. doi: 10.3390/biology10080712
  • Briata P, Bordo D, Puppo M, et al. Diverse roles of the nucleic acid-binding protein KHSRP in cell differentiation and disease. Wiley Interdiscip Rev RNA. 2016;7(2):227–240. doi: 10.1002/wrna.1327
  • Briata P, Chen CY, Ramos A, et al. Functional and molecular insights into KSRP function in mRNA decay. Biochim Biophys Acta. 2013;1829(6–7):689–694. doi: 10.1016/j.bbagrm.2012.11.003
  • Feracci M, Foot JN, Grellscheid SN, et al. Structural basis of RNA recognition and dimerization by the STAR proteins T-STAR and Sam68. Nat Commun. 2016;7(1):10355. doi: 10.1038/ncomms10355
  • Duggimpudi S, Kloetgen A, Maney SK, et al. Transcriptome-wide analysis uncovers the targets of the RNA-binding protein MSI2 and effects of MSI2‘s RNA-binding activity on IL-6 signaling. J Biol Chem. 2018;293(40):15359–15369. doi: 10.1074/jbc.RA118.002243
  • Kuspert M, Murakawa Y, Schaffler K, et al. LARP4B is an AU-rich sequence associated factor that promotes mRNA accumulation and translation. RNA. 2015;21(7):1294–1305. doi: 10.1261/rna.051441.115
  • Maraia RJ, Mattijssen S, Cruz-Gallardo I, et al. The La and related RNA-binding proteins (LARPs): structures, functions, and evolving perspectives. Wiley Interdiscip Rev RNA. 2017;8(6). doi: 10.1002/wrna.1430
  • Mao R, Yang R, Chen X, et al. Regnase-1, a rapid response ribonuclease regulating inflammation and stress responses. Cell Mol Immunol. 2017;14(5):412–422. doi: 10.1038/cmi.2016.70
  • Mino T, Takeuchi O. Regnase-1 and Roquin regulate inflammatory mRNAs. Oncotarget. 2015;6(20):17869–17870. doi: 10.18632/oncotarget.4891
  • Nwosu GO, Powell JA, Pitson SM. Targeting the integrated stress response in hematologic malignancies. Exp Hematol Oncol. 2022;11(1):94. doi: 10.1186/s40164-022-00348-0
  • Sanduja S, Blanco FF, Dixon DA. The roles of TTP and BRF proteins in regulated mRNA decay. Wiley Interdiscip Rev RNA. 2011;2(1):42–57. doi: 10.1002/wrna.28
  • Ma W, Zhen G, Xie W, et al. In vivo reconstitution finds multivalent RNA–RNA interactions as drivers of mesh-like condensates. Elife. 2021;10:10. doi: 10.7554/eLife.64252
  • Ma W, Mayr C. A membraneless organelle associated with the endoplasmic reticulum enables 3‘UTR-Mediated protein-protein interactions. Cell. 2018;175(6):1492–506 e19. doi: 10.1016/j.cell.2018.10.007
  • Newton K, Dixit VM. Signaling in innate immunity and inflammation. Cold Spring Harb Perspect Biol. 2012;4(3):a006049–a006049. doi: 10.1101/cshperspect.a006049
  • Wang J, Erlacher M, Fernandez-Orth J. The role of inflammation in hematopoiesis and bone marrow failure: what can we learn from mouse models? Front Immunol. 2022;13:951937. doi: 10.3389/fimmu.2022.951937
  • Ratajczak MZ, Kucia M. Hematopoiesis and innate immunity: an inseparable couple for good and bad times, bound together by an hormetic relationship. Leukemia. 2022;36(1):23–32. doi: 10.1038/s41375-021-01482-0
  • Goncalves AC, Cortesao E, Oliveiros B, et al. Oxidative stress and mitochondrial dysfunction play a role in myelodysplastic syndrome development, diagnosis, and prognosis: a pilot study. Free Radic Res. 2015;49(9):1081–1094. doi: 10.3109/10715762.2015.1035268
  • van Galen P, Mbong N, Kreso A, et al. Integrated stress response activity marks stem cells in normal hematopoiesis and leukemia. Cell Rep. 2018;25(5):1109–17 e5. doi: 10.1016/j.celrep.2018.10.021
  • Follo MY, Finelli C, Mongiorgi S, et al. PKR is activated in MDS patients and its subcellular localization depends on disease severity. Leukemia. 2008;22(12):2267–2269. doi: 10.1038/leu.2008.122
  • Blalock WL, Grimaldi C, Fala F, et al. PKR activity is required for acute leukemic cell maintenance and growth: a role for PKR-mediated phosphatase activity to regulate GSK-3 phosphorylation. J Cell Physiol. 2009;221(1):232–241. doi: 10.1002/jcp.21848
  • Cheng X, Byrne M, Brown KD, et al. PKR inhibits the DNA damage response, and is associated with poor survival in AML and accelerated leukemia in NHD13 mice. Blood. 2015;126(13):1585–1594. doi: 10.1182/blood-2015-03-635227
  • Piwocka K, Vejda S, Cotter TG, et al. Bcr-Abl reduces endoplasmic reticulum releasable calcium levels by a Bcl-2-independent mechanism and inhibits calcium-dependent apoptotic signaling. Blood. 2006;107(10):4003–4010. doi: 10.1182/blood-2005-04-1523
  • Kusio-Kobialka M, Podszywalow-Bartnicka P, Peidis P, et al. The PERK-eIf2alpha phosphorylation arm is a pro-survival pathway of BCR-ABL signaling and confers resistance to imatinib treatment in chronic myeloid leukemia cells. Cell Cycle. 2012;11(21):4069–4078. doi: 10.4161/cc.22387
  • Dudka W, Hoser G, Mondal SS, et al. Targeting integrated stress response with ISRIB combined with imatinib treatment attenuates RAS/RAF/MAPK and STAT5 signaling and eradicates chronic myeloid leukemia cells. BMC Cancer. 2022;22(1):1254. doi: 10.1186/s12885-022-10289-w
  • Biancon G, Joshi P, Zimmer JT, et al. Precision analysis of mutant U2AF1 activity reveals deployment of stress granules in myeloid malignancies. Mol Cell. 2022;82(6):1107–22 e7. doi: 10.1016/j.molcel.2022.02.025
  • Diaz-Munoz MD, Kiselev VY, Le Novere N, et al. Tia1 dependent regulation of mRNA subcellular location and translation controls p53 expression in B cells. Nat Commun. 2017;8(1):530. doi: 10.1038/s41467-017-00454-2
  • Bonomo I, Assoni G, La Pietra V, et al. HuR modulation counteracts lipopolysaccharide response in murine macrophages. Dis Model Mech. 2023;16(3): doi: 10.1242/dmm.050120
  • Hu X, Li J, Fu M, et al. The JAK/STAT signaling pathway: from bench to clinic. Signal Transduct Target Ther. 2021;6(1):402. doi: 10.1038/s41392-021-00791-1
  • Zhang T, Ma C, Zhang Z, et al. NF-kappaB signaling in inflammation and cancer. MedComm. 2021;2(4):618–653. doi: 10.1002/mco2.104
  • Kudinov AE, Karanicolas J, Golemis EA, et al. Musashi RNA-Binding proteins as cancer drivers and novel therapeutic targets. Clin Cancer Res. 2017;23(9):2143–2153. doi: 10.1158/1078-0432.CCR-16-2728
  • Majeti R, Jamieson C, Pang WW, et al. Clonal expansion of Stem/Progenitor cells in cancer, fibrotic diseases, and atherosclerosis, and CD47 protection of pathogenic cells. Annu Rev Med. 2022;73(1):307–320. doi: 10.1146/annurev-med-042420-104436
  • Leppek K, Schott J, Reitter S, et al. Roquin promotes constitutive mRNA decay via a conserved class of stem-loop recognition motifs. Cell. 2013;153(4):869–881. doi: 10.1016/j.cell.2013.04.016
  • Hauer J, Fischer U, Borkhardt A. Toward prevention of childhood ALL by early-life immune training. Blood. 2021;138(16):1412–1428. doi: 10.1182/blood.2020009895
  • Carbone A, Tripodo C, Carlo-Stella C, et al. The role of inflammation in lymphoma. Adv Exp Med Biol. 2014;816:315–333.
  • Popovic B, Nicolet BP, Guislain A, et al. Time-dependent regulation of cytokine production by RNA binding proteins defines T cell effector function. Cell Rep. 2023;42(5):112419. doi: 10.1016/j.celrep.2023.112419
  • Heeren JJ F-V. Post-transcriptional control of T-cell cytokine production: implications for cancer therapy. Immunology. 2021;164(1):57–72. doi: 10.1111/imm.13339
  • Gillis P, Malter JS. The adenosine-uridine binding factor recognizes the AU-rich elements of cytokine, lymphokine, and oncogene mRnas. J Biol Chem. 1991;266(5):3172–3177. doi: 10.1016/S0021-9258(18)49970-X
  • Curdy N, Lanvin O, Cadot S, et al. Stress granules in the post-transcriptional regulation of immune cells. Front Cell Dev Biol. 2020;8:611185. doi: 10.3389/fcell.2020.611185
  • Naz S, Battu S, Khan RA, et al. Activation of integrated stress response pathway regulates IL-1beta production through posttranscriptional and translational reprogramming in macrophages. Eur J Immunol. 2019;49(2):277–289. doi: 10.1002/eji.201847513
  • Paget M, Cadena C, Ahmad S, et al. Stress granules are shock absorbers that prevent excessive innate immune responses to dsRNA. Mol Cell. 2023;83(7):1180–96 e8. doi: 10.1016/j.molcel.2023.03.010
  • Kong G, Dou Y, Xiao X, et al. Transgenic expression of a Mutant Ribonuclease Regnase-1 in T cells disturbs T cell development and functions. Front Immunol. 2021;12:682220. doi: 10.3389/fimmu.2021.682220
  • Bhat N, Virgen-Slane R, Ramezani-Rad P, et al. Regnase-1 is essential for B cell homeostasis to prevent immunopathology. J Exp Med. 2021;218(5): doi: 10.1084/jem.20200971
  • Moore MJ, Blachere NE, Fak JJ, et al. ZFP36 RNA-binding proteins restrain T cell activation and anti-viral immunity. Elife. 2018;7. doi: 10.7554/eLife.33057
  • Ott G, Rosenwald A, Campo E. Understanding MYC-driven aggressive B-cell lymphomas: pathogenesis and classification. Blood. 2013;122(24):3884–3891. doi: 10.1182/blood-2013-05-498329
  • Izquierdo JM, Majos N, Bonnal S, et al. Regulation of fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition. Mol Cell. 2005;19(4):475–484. doi: 10.1016/j.molcel.2005.06.015
  • Izquierdo JM. Hu antigen R (HuR) functions as an alternative pre-mRNA splicing regulator of fas apoptosis-promoting receptor on exon definition. J Biol Chem. 2008;283(27):19077–19084. doi: 10.1074/jbc.M800017200
  • Villa-Morales M, Cobos MA, Gonzalez-Gugel E, et al. FAS system deregulation in T-cell lymphoblastic lymphoma. Cell Death Dis. 2014;5(3):e1110. doi: 10.1038/cddis.2014.83
  • Razzaghi R, Agarwal S, Kotlov N, et al. Compromised counterselection by FAS creates an aggressive subtype of germinal center lymphoma. J Exp Med. 2021;218(3): doi: 10.1084/jem.20201173
  • Diaz-Munoz MD, Bell SE, Fairfax K, et al. The RNA-binding protein HuR is essential for the B cell antibody response. Nat Immunol. 2015;16(4):415–425. doi: 10.1038/ni.3115
  • Papadaki O, Milatos S, Grammenoudi S, et al. Control of thymic T cell maturation, deletion and egress by the RNA-binding protein HuR. J Immunol. 2009;182(11):6779–6788. doi: 10.4049/jimmunol.0900377
  • Yu S, Tripod M, Atasoy U, et al. HuR plays a positive role to strengthen the signaling pathways of CD4(+) T cell activation and Th17 cell differentiation. J Immunol Res. 2021;2021:9937243. doi: 10.1155/2021/9937243
  • Vivori C, Papasaikas P, Stadhouders R, et al. Dynamics of alternative splicing during somatic cell reprogramming reveals functions for RNA-binding proteins CPSF3, hnRNP UL1, and TIA1. Genome Biol. 2021;22(1):171. doi: 10.1186/s13059-021-02372-5
  • Kurata M, Onishi I, Takahara T, et al. C/EBPbeta induces B-cell acute lymphoblastic leukemia and cooperates with BLNK mutations. Cancer Sci. 2021;112(12):4920–4930. doi: 10.1111/cas.15164
  • Piva R, Pellegrino E, Mattioli M, et al. Functional validation of the anaplastic lymphoma kinase signature identifies CEBPB and BCL2A1 as critical target genes. J Clin Invest. 2006;116(12):3171–3182. doi: 10.1172/JCI29401
  • Stelmach P, Trumpp A. Leukemic stem cells and therapy resistance in acute myeloid leukemia. Haematologica. 2023;108(2):353–366. doi: 10.3324/haematol.2022.280800
  • Hubstenberger A, Courel M, Benard M, et al. P-Body purification reveals the condensation of repressed mRNA regulons. Mol Cell. 2017;68(1):144–57 e5. doi: 10.1016/j.molcel.2017.09.003
  • Sanchez-Jimenez C, Ludena MD, Izquierdo JM. T-cell intracellular antigens function as tumor suppressor genes. Cell Death Dis. 2015;6(3):e1669. doi: 10.1038/cddis.2015.43
  • Sung HM, Schott J, Boss P, et al. Stress-induced nuclear speckle reorganization is linked to activation of immediate early gene splicing. J Cell Bio. 2023;222(12): doi: 10.1083/jcb.202111151
  • Galloway A, Saveliev A, Lukasiak S, et al. RNA-binding proteins ZFP36L1 and ZFP36L2 promote cell quiescence. Science. 2016;352(6284):453–459. doi: 10.1126/science.aad5978
  • Kesarwani M, Kincaid Z, Gomaa A, et al. Targeting c-FOS and DUSP1 abrogates intrinsic resistance to tyrosine-kinase inhibitor therapy in BCR-ABL-induced leukemia. Nat Med. 2017;23(4):472–482. doi: 10.1038/nm.4310
  • Reinhardt HC, Hasskamp P, Schmedding I, et al. DNA damage activates a spatially distinct late cytoplasmic cell-cycle checkpoint network controlled by MK2-mediated RNA stabilization. Mol Cell. 2010;40(1):34–49. doi: 10.1016/j.molcel.2010.09.018
  • Kaloni D, Diepstraten ST, Strasser A, et al. BCL-2 protein family: attractive targets for cancer therapy. Apoptosis. 2023;28(1–2):20–38. doi: 10.1007/s10495-022-01780-7
  • Stella S, Tirro E, Conte E, et al. Suppression of survivin induced by a BCR-ABL/JAK2/STAT3 pathway sensitizes imatinib-resistant CML cells to different cytotoxic drugs. Mol Cancer Ther. 2013;12(6):1085–1098. doi: 10.1158/1535-7163.MCT-12-0550
  • Carter BZ, Mak PY, Mu H, et al. Combined targeting of BCL-2 and BCR-ABL tyrosine kinase eradicates chronic myeloid leukemia stem cells. Sci Transl Med. 2016;8(355):355ra117. doi: 10.1126/scitranslmed.aag1180
  • Roberts AW, Wei AH, Huang DCS. BCL2 and MCL1 inhibitors for hematologic malignancies. Blood. 2021;138(13):1120–1136. doi: 10.1182/blood.2020006785
  • Aichberger KJ, Mayerhofer M, Krauth MT, et al. Identification of mcl-1 as a BCR/ABL-dependent target in chronic myeloid leukemia (CML): evidence for cooperative antileukemic effects of imatinib and mcl-1 antisense oligonucleotides. Blood. 2005;105(8):3303–3311. doi: 10.1182/blood-2004-02-0749
  • Donahue JM, Chang ET, Xiao L, et al. The RNA-binding protein HuR stabilizes survivin mRNA in human oesophageal epithelial cells. Biochem J. 2011;437(1):89–96. doi: 10.1042/BJ20110028
  • Filippova N, Yang X, Wang Y, et al. The RNA-binding protein HuR promotes glioma growth and treatment resistance. Mol Cancer Res. 2011;9(5):648–659. doi: 10.1158/1541-7786.MCR-10-0325
  • Abdelmohsen K, Pullmann R Jr., Lal A, et al. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol Cell. 2007;25(4):543–557. doi: 10.1016/j.molcel.2007.01.011
  • Sasaki Y, Dehnad A, Fish S, et al. NOX4 regulates CCR2 and CCL2 mRNA stability in alcoholic liver disease. Sci Rep. 2017;7(1):46144. doi: 10.1038/srep46144
  • Macanas-Pirard P, Quezada T, Navarrete L, et al. The CCL2/CCR2 axis affects transmigration and proliferation but not resistance to chemotherapy of acute myeloid leukemia cells. PLOS ONE. 2017;12(1):e0168888. doi: 10.1371/journal.pone.0168888
  • Xiao X, Xu Q, Sun Y, et al. 5‑aza‑2‘‑deoxycytidine promotes migration of acute monocytic leukemia cells via activation of CCL2‑CCR2‑ERK signaling pathway. Mol Med Rep. 2017;16(2):1417–1424. doi: 10.3892/mmr.2017.6737
  • Cappell KM, Kochenderfer JN. Long-term outcomes following CAR T cell therapy: what we know so far. Nat Rev Clin Oncol. 2023;20(6):359–371. doi: 10.1038/s41571-023-00754-1
  • Wei J, Long L, Zheng W, et al. Targeting REGNASE-1 programs long-lived effector T cells for cancer therapy. Nature. 2019;576(7787):471–476. doi: 10.1038/s41586-019-1821-z
  • Mai D, Johnson O, Reff J, et al. Combined disruption of T cell inflammatory regulators regnase-1 and roquin-1 enhances antitumor activity of engineered human T cells. Proc Natl Acad Sci U S A. 2023;120(12):e2218632120. doi: 10.1073/pnas.2218632120
  • Zheng W, Wei J, Zebley CC, et al. Regnase-1 suppresses TCF-1+ precursor exhausted T-cell formation to limit CAR-T-cell responses against ALL. Blood. 2021;138(2):122–135. doi: 10.1182/blood.2020009309
  • Liu Y, Li X, Zhang H, et al. HuR up-regulates cell surface PD-L1 via stabilizing CMTM6 transcript in cancer. Oncogene. 2021;40(12):2230–2242. doi: 10.1038/s41388-021-01689-6
  • Cao X, Wang Y, Zhang W, et al. Targeting macrophages for enhancing CD47 blockade-elicited lymphoma clearance and overcoming tumor-induced immunosuppression. Blood. 2022;139(22):3290–3302. doi: 10.1182/blood.2021013901