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Review

RNA-Binding Proteins as a Molecular Link between COPD and Lung Cancer

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Pages 18-30 | Received 31 May 2022, Accepted 08 Jul 2022, Published online: 19 Jan 2023

References

  • Barnes PJ, Adcock IM. Chronic obstructive pulmonary disease and lung cancer: a lethal association. Am J Respir Crit Care Med. 2011;184(8):866–867. DOI:10.1164/rccm.201108-1436ED
  • Barreiro E, Fermoselle C, Mateu-Jimenez M, et al. Oxidative stress and inflammation in the normal airways and blood of patients with lung cancer and COPD. Free Radic Biol Med. 2013;65:859–871. DOI:10.1016/j.freeradbiomed.2013.08.006
  • Durham AL, Adcock IM. The relationship between COPD and lung cancer. Lung Cancer. 2015;90(2):121–127. DOI:10.1016/j.lungcan.2015.08.017
  • Nucera F, Mumby S, Paudel KR, Dharwal V, Di Stefano A, Casolaro V, Hansbro PM, Adcock IM, Caramori G. Role of oxidative stress in the pathogenesis of COPD. Minerva Med. 2022;113(3):370–404. DOI:10.23736/S0026-4806.22.07972-1
  • Lu JY, Sadri N, Schneider RJ. Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev. 2006;20(22):3174–3184. DOI:10.1101/gad.1467606
  • Hitti E, Bakheet T, Al-Souhibani N, et al. Systematic analysis of AU-Rich element expression in cancer reveals common functional clusters regulated by key RNA-Binding proteins. Cancer Res. 2016;76(14):4068–4080. DOI:10.1158/0008-5472.CAN-15-3110
  • Anderson P. Post-transcriptional regulons coordinate the initiation and resolution of inflammation. Nat Rev Immunol. 2010;10(1):24–35. DOI:10.1038/nri2685
  • Gerstberger S, Hafner M, Tuschl T. A census of human RNA-binding proteins. Nat Rev Genet. 2014;15(12):829–845. DOI:10.1038/nrg3813
  • Keller A, Fehlmann T, Ludwig N, et al. Genome-wide MicroRNA expression profiles in COPD: Early predictors for cancer development. Genomics Proteomics Bioinformatics. 2018;16(3):162–171. DOI:10.1016/j.gpb.2018.06.001
  • Zhuang Y, Hobbs BD, Hersh CP, et al. Identifying miRNA-mRNA networks associated with COPD phenotypes. Front Genet. 2021;12:748356.
  • Abdelmohsen K, Kuwano Y, Kim HH, et al. Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol Chem. 2008;389(3):243–255. DOI:10.1515/BC.2008.022
  • Wang Z, Bhattacharya A, Ivanov DN. Identification of Small-Molecule inhibitors of the HuR/RNA interaction using a fluorescence polarization screening assay followed by NMR validation. PLoS One. 2015;10(9):e0138780.
  • Patial S, Blackshear PJ. Tristetraprolin as a therapeutic target in inflammatory disease. Trends Pharmacol Sci. 2016;37(10):811–821. DOI:10.1016/j.tips.2016.07.002
  • Hong S. RNA binding protein as an emerging therapeutic target for cancer prevention and treatment. J Cancer Prev. 2017;22(4):203–210. DOI:10.15430/JCP.2017.22.4.203
  • Caramori G, Ruggeri P, Mumby S, et al. Molecular links between COPD and lung cancer: new targets for drug discovery? Expert Opin Ther Targets. 2019;23(6):539–553. DOI:10.1080/14728222.2019.1615884
  • Hung RJ, McKay JD, Gaborieau V, et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature. 2008;452(7187):633–637. DOI:10.1038/nature06885
  • Pillai SG, Ge D, Zhu G, ICGN Investigators, et al. A genome-wide association study in chronic obstructive pulmonary disease (COPD): identification of two major susceptibility loci. PLoS Genet. 2009;5(3):e1000421.
  • Young RP, Hopkins RJ, Whittington CF, et al. Individual and cumulative effects of GWAS susceptibility loci in lung cancer: associations after Sub-phenotyping for COPD. PLoS One. 2011;6(2):e16476.
  • Karimian A, Ahmadi Y, Yousefi B. Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Repair (Amst). 2016;42:63–71. DOI:10.1016/j.dnarep.2016.04.008
  • Choi YY, Kang HK, Choi JE, et al. Comprehensive assessment of P21 polymorphisms and lung cancer risk. J Hum Genet. 2008;53(1):87–95. DOI:10.1007/s10038-007-0222-6
  • Lee YL, Chen W, Tsai WK, et al. Polymorphisms of p53 and p21 genes in chronic obstructive pulmonary disease. J Lab Clin Med. 2006;147(5):228–233. DOI:10.1016/j.lab.2005.12.008
  • Caramori G, Adcock IM, Casolari P, et al. Unbalanced oxidant-induced DNA damage and repair in COPD: a link towards lung cancer. Thorax. 2011;66(6):521–527. DOI:10.1136/thx.2010.156448
  • Meek K, Gupta S, Ramsden DA, et al. The DNA-dependent protein kinase: the director at the end. Immunol Rev. 2004;200:132–141. DOI:10.1111/j.0105-2896.2004.00162.x
  • Pramanik S, Roychoudhury S, Bhakat KK. Oxidized DNA base damage repair and transcription. In Chakraborti S., Ray B.K., Roychoudhury S. (eds) Handbook of oxidative stress in cancer: Mechanistic aspects. Springer, Singapore. 2022. 1621–1637.
  • Chowdhury A. Glutathione peroxidase and lung cancer: an unravel story. In Chakraborti S., Ray B.K., Roychoudhury S. (eds) Handbook of oxidative stress in cancer: Mechanistic aspects. Springer, Singapore. 2022. 1481–1491.
  • Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559. DOI:10.1186/1471-2105-9-559
  • Li P, Wang Y, Wang X, et al. Identification of susceptible genes for chronic obstructive pulmonary disease with lung adenocarcinoma by weighted gene Co-Expression network analysis. Onco Targets Ther. 2021;14:3625–3634. DOI:10.2147/OTT.S303544
  • Eguren M, Manchado E, Malumbres M. Non-mitotic functions of the Anaphase-Promoting complex. Semin Cell Dev Biol. 2011;22(6):572–578. DOI:10.1016/j.semcdb.2011.03.010
  • Lafranchi L, de Boer HR, de Vries EG, et al. APC/C(Cdh1) controls CtIP stability during the cell cycle and in response to DNA damage. Embo J. 2014;33(23):2860–2879. DOI:10.15252/embj.201489017
  • Crawford LJ, Anderson G, Johnston CK, et al. Identification of the APC/C co-factor FZR1 as a novel therapeutic target for multiple myeloma. Oncotarget. 2016;7(43):70481–70493. DOI:10.18632/oncotarget.12026
  • Wan L, Chen M, Cao J, et al. The APC/C E3 ligase complex activator FZR1 restricts BRAF oncogenic function. Cancer Discov. 2017;7(4):424–441. DOI:10.1158/2159-8290.CD-16-0647
  • Miao TW, Xiao W, Du LY, et al. High expression of SPP1 in patients with chronic obstructive pulmonary disease (COPD) is correlated with increased risk of lung cancer. FEBS Open Bio. 2021;11(4):1237–1249. DOI:10.1002/2211-5463.13127
  • Hu Z, Lin D, Yuan J, et al. Overexpression of osteopontin is associated with more aggressive phenotypes in human non-small cell lung cancer. Clin Cancer Res. 2005;11(13):4646–4652. DOI:10.1158/1078-0432.CCR-04-2013
  • Ali MN, Mori M, Mertens TCJ, et al. Osteopontin expression in small airway epithelium in copd is dependent on differentiation and confined to subsets of cells. Sci Rep. 2019;9(1):15566. DOI:10.1038/s41598-019-52208-3
  • Boelens MC, Gustafson AM, Postma DS, et al. A chronic obstructive pulmonary disease related signature in squamous cell lung cancer. Lung Cancer. 2011;72(2):177–183. DOI:10.1016/j.lungcan.2010.08.014
  • Lamontagne M, Bérubé JC, Obeidat M, International COPD Genetics Consortium, et al. Leveraging lung tissue transcriptome to uncover candidate causal genes in COPD genetic associations. Hum Mol Genet. 2018;27(10):1819–1829. DOI:10.1093/hmg/ddy091
  • Houghton AM. Mechanistic links between COPD and lung cancer. Nat Rev Cancer. 2013;13(4):233–245. DOI:10.1038/nrc3477
  • Berg J, Halvorsen AR, Bengtson MB, et al. Levels and prognostic impact of circulating markers of inflammation, endothelial activation and extracellular matrix remodelling in patients with lung cancer and chronic obstructive pulmonary disease. BMC Cancer. 2018;18(1):739. DOI:10.1186/s12885-018-4659-0
  • Barnes PJ. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2016;138(1):16–27. DOI:10.1016/j.jaci.2016.05.011
  • Barnes PJ. Inflammatory endotypes in COPD. Allergy. 2019;74(7):1249–1256. DOI:10.1111/all.13760
  • Crusz SM, Balkwill FR. Inflammation and cancer: advances and new agents. Nat Rev Clin Oncol. 2015;12(10):584–596. DOI:10.1038/nrclinonc.2015.105
  • Tessema M, Yingling CM, Picchi MA, et al. Epigenetic repression of CCDC37 and MAP1B links chronic obstructive pulmonary disease to lung cancer. J Thorac Oncol. 2015;10(8):1181–1188. DOI:10.1097/JTO.0000000000000592
  • Yamamoto R, Song K, Yanagisawa HA, et al. The MIA complex is a conserved and novel dynein regulator essential for normal ciliary motility. J Cell Biol. 2013;201(2):263–278. DOI:10.1083/jcb.201211048
  • Kwon YJ, Lee SJ, Koh JS, et al. Genome-wide analysis of DNA methylation and the gene expression change in lung cancer. J Thorac Oncol. 2012;7(1):20–33. DOI:10.1097/JTO.0b013e3182307f62
  • Li L, Yan S, Zhang H, et al. Interaction of hnRNP K with MAP 1B-LC1 promotes TGF-β1-mediated epithelial to mesenchymal transition in lung cancer cells. BMC Cancer. 2019;19(1):894. DOI:10.1186/s12885-019-6119-x
  • Wauters E, Janssens W, Vansteenkiste J, et al. DNA methylation profiling of non-small cell lung cancer reveals a COPD-driven immune-related signature. Thorax. 2015;70(12):1113–1122. DOI:10.1136/thoraxjnl-2015-207288
  • Schotten LM, Darwiche K, Seweryn M, et al. DNA methylation of PTGER4 in peripheral blood plasma helps to distinguish between lung cancer, benign pulmonary nodules and chronic obstructive pulmonary disease patients. Eur J Cancer. 2021;147:142–150. DOI:10.1016/j.ejca.2021.01.032
  • Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–867. DOI:10.1038/nature01322
  • Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883–899. DOI:10.1016/j.cell.2010.01.025
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. DOI:10.1016/j.cell.2011.02.013
  • Elinav E, Nowarski R, Thaiss CA, et al. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer. 2013;13(11):759–771. DOI:10.1038/nrc3611
  • Barnes PJ, Baker J, Donnelly LE. Cellular senescence as a mechanism and target in chronic lung diseases. Am J Respir Crit Care Med. 2019;200(5):556–564. DOI:10.1164/rccm.201810-1975TR
  • Kumar M, Seeger W, Voswinckel R. Senescence-associated secretory phenotype and its possible role in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2014;51(3):323–333. DOI:10.1165/rcmb.2013-0382PS
  • Agustí A, Hogg JC. Update on the pathogenesis of chronic obstructive pulmonary disease. N Engl J Med. 2019;381(13):1248–1256. DOI:10.1056/NEJMra1900475
  • Yang J, Liu M, Hong D, et al. The paradoxical role of cellular senescence in cancer. Front Cell Dev Biol. 2021;9:722205.
  • Laberge RM, Awad P, Campisi J, et al. Epithelial-mesenchymal transition induced by senescent fibroblasts. Cancer Microenviron. 2012;5(1):39–44. DOI:10.1007/s12307-011-0069-4
  • Mahmood MQ, Shukla SD, Ward C, et al. The underappreciated role of epithelial mesenchymal transition in chronic obstructive pulmonary disease and its strong link to lung cancer. Biomolecules. 2021;11(9):1394. DOI:10.3390/biom11091394
  • Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature. 2009;458(7237):514–518. DOI:10.1038/nature07725
  • Colarusso C, Terlizzi M, Lamort AS, et al. Caspase-11 and AIM2 inflammasome are involved in smoking-induced COPD and lung adenocarcinoma. Oncotarget. 2021;12(11):1057–1071. DOI:10.18632/oncotarget.27964
  • Bulgakova O, Kausbekova A, Kussainova A, et al. Involvement of circulating Cell-Free mitochondrial DNA and proinflammatory cytokines in pathogenesis of chronic obstructive pulmonary disease and lung cancer. Asian Pac J Cancer Prev. 2021;22(6):1927–1933. DOI:10.31557/APJCP.2021.22.6.1927
  • Nam HS, Izumchenko E, Dasgupta S, et al. Mitochondria in chronic obstructive pulmonary disease and lung cancer: where are we now? Biomark Med. 2017;11(6):475–489. DOI:10.2217/bmm-2016-0373
  • Polverino F, Mirra D, Esposito R, et al. Similar programmed death ligand 1 (PD-L1) expression profile in patients with mild COPD and lung cancer. PREPRINT (Version 1) available at Research Square 2022. DOI:10.21203/rs.3.rs-1375680/v1
  • Liu S, Zhan Y, Luo J, et al. Roles of exosomes in the carcinogenesis and clinical therapy of non-small cell lung cancer. Biomed Pharmacother. 2019;111:338–346. DOI:10.1016/j.biopha.2018.12.088
  • van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228. DOI:10.1038/nrm.2017.125
  • Liu Z, Yan J, Tong L, et al. The role of exosomes from BALF in lung disease. J Cell Physiol. 2022;237(1):161–168. DOI:10.1002/jcp.30553
  • O’Farrell HE, Bowman RV, Fong KM, et al. Plasma extracellular vesicle miRNAs can identify lung cancer, current smoking status, and stable COPD. Int J Mol Sci. 2021;22(11):5803. DOI:10.3390/ijms22115803
  • Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet. 2007;8(7):533–543. DOI:10.1038/nrg2111
  • Lunde BM, Moore C, Varani G. RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol. 2007;8(6):479–490. DOI:10.1038/nrm2178
  • Ray D, Kazan H, Cook KB, et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature. 2013;499(7457):172–177. DOI:10.1038/nature12311
  • 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
  • Coppin L, Leclerc J, Vincent A, et al. Messenger RNA Life-Cycle in cancer cells: Emerging role of conventional and Non-Conventional RNA-Binding proteins? Int J Mol Sci. 2018;19(3):650. DOI:10.3390/ijms19030650
  • Dassi E. Handshakes and fights: the regulatory interplay of RNA-Binding proteins. Front Mol Biosci. 2017;4:67.
  • Benoit Bouvrette LP, Bovaird S, Blanchette M, et al. oRNAment: a database of putative RNA binding protein target sites in the transcriptomes of model species. Nucleic Acids Res. 2020;48(D1):D166–d173.
  • Chen CY, Shyu AB. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci. 1995;20(11):465–470. DOI:10.1016/S0968-0004(00)89102-1
  • Zubiaga AM, Belasco JG, Greenberg ME. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol Cell Biol. 1995;15(4):2219–2230. DOI:10.1128/MCB.15.4.2219
  • Barreau C, Paillard L, Osborne HB. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 2005;33(22):7138–7150. DOI:10.1093/nar/gki1012
  • Raineri I, Wegmueller D, Gross B, et al. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res. 2004;32(4):1279–1288. DOI:10.1093/nar/gkh282
  • Srikantan S, Gorospe M. HuR function in disease. Front Biosci (Landmark Ed). 2012;17(1):189–205. DOI:10.2741/3921
  • Tiedje C, Diaz-Muñoz MD, Trulley P, et al. The RNA-binding protein TTP is a global post-transcriptional regulator of feedback control in inflammation. Nucleic Acids Res. 2016;44(15):7418–7440. DOI:10.1093/nar/gkw474
  • Piecyk M, Wax S, Beck AR, et al. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. Embo J. 2000;19(15):4154–4163. DOI:10.1093/emboj/19.15.4154
  • García-Mauriño SM, Rivero-Rodríguez F, Velázquez-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.
  • Moore AE, Chenette DM, Larkin LC, et al. Physiological networks and disease functions of RNA-binding protein AUF1. Wiley Interdiscip Rev RNA. 2014;5(4):549–564. DOI:10.1002/wrna.1230
  • Lee EK. Post-translational modifications of RNA-binding proteins and their roles in RNA granules. Curr Protein Pept Sci. 2012;13(4):331–336.
  • Cao H, Deterding LJ, Blackshear PJ. Identification of a major phosphopeptide in human tristetraprolin by phosphopeptide mapping and mass spectrometry. PLoS One. 2014;9(7):e100977. DOI:10.1371/journal.pone.0100977
  • Coelho MA, de Carné Trécesson S, Rana S, et al. Oncogenic RAS signaling promotes tumor immunoresistance by stabilizing PD-L1 mRNA. Immunity. 2017;47(6):1083–1099.e6.
  • Roignant JY, Soller M. m(6)a in mRNA: an ancient mechanism for Fine-Tuning gene expression. Trends Genet. 2017;33(6):380–390. DOI:10.1016/j.tig.2017.04.003
  • Yang Y, Fan X, Mao M, et al. Extensive translation of circular RNAs driven by N(6)-methyladenosine. Cell Res. 2017;27(5):626–641. DOI:10.1038/cr.2017.31
  • Wei CM, Gershowitz A, Moss B. Methylated nucleotides block 5’ terminus of HeLa cell messenger RNA. Cell. 1975;4(4):379–386. DOI:10.1016/0092-8674(75)90158-0
  • Wang S, Sun C, Li J, et al. Roles of rna methylation by means of N(6)-methyladenosine (m(6)A) in human cancers. Cancer Lett. 2017;408:112–120. DOI:10.1016/j.canlet.2017.08.030
  • Ito K, Barnes PJ. COPD as a disease of accelerated lung aging. Chest. 2009;135(1):173–180. DOI:10.1378/chest.08-1419
  • Fulop T, Larbi A, Dupuis G, et al. Immunosenescence and Inflamm-Aging as two sides of the same coin: Friends or foes? Front Immunol. 2017;8:1960. DOI:10.3389/fimmu.2017.01960
  • Anderson P. Post-transcriptional control of cytokine production. Nat Immunol. 2008;9(4):353–359. DOI:10.1038/ni1584
  • Hamilton T, Novotny M, Pavicic PJ, Jr., et al. Diversity in post-transcriptional control of neutrophil chemoattractant cytokine gene expression. Cytokine. 2010;52(1-2):116–122. DOI:10.1016/j.cyto.2010.04.003
  • Yoon JH, De S, Srikantan S, et al. PAR-CLIP analysis uncovers AUF1 impact on target RNA fate and genome integrity. Nat Commun. 2014;5:5248. DOI:10.1038/ncomms6248
  • Herranz N, Gallage S, Mellone M, et al. mTOR regulates MAPKAPK2 translation to control the senescence-associated secretory phenotype. Nat Cell Biol. 2015;17(9):1205–1217. DOI:10.1038/ncb3225
  • Maitra S, Chou CF, Luber CA, et al. The AU-rich element mRNA decay-promoting activity of BRF1 is regulated by mitogen-activated protein kinase-activated protein kinase 2. RNA. 2008;14(5):950–959. DOI:10.1261/rna.983708
  • White EJ, Brewer G, Wilson GM. Post-transcriptional control of gene expression by AUF1: mechanisms, physiological targets, and regulation. Biochim Biophys Acta. 2013;1829(6-7):680–688. DOI:10.1016/j.bbagrm.2012.12.002
  • Fu D, Collins K. Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation. Mol Cell. 2007;28(5):773–785. DOI:10.1016/j.molcel.2007.09.023
  • Skerrett-Byrne DA, Bromfield EG, Murray HC, et al. Time-resolved proteomic profiling of cigarette smoke-induced experimental chronic obstructive pulmonary disease. Respirology. 2021;26(10):960–973. DOI:10.1111/resp.14111
  • Bhattacharyya SN, Habermacher R, Martine U, et al. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 2006;125(6):1111–1124. DOI:10.1016/j.cell.2006.04.031
  • Iadevaia V, Gerber AP. Combinatorial control of mRNA fates by RNA-Binding proteins and Non-Coding RNAs. Biomolecules. 2015;5(4):2207–2222. DOI:10.3390/biom5042207
  • Guo J, Wang H, Jiang S, et al. The cross-talk between tristetraprolin and cytokines in cancer. Anticancer Agents Med Chem. 2017;17(11):1477–1486.
  • Panganiban RP, Vonakis BM, Ishmael FT, et al. Coordinated post-transcriptional regulation of the chemokine system: messages from CCL2. J Interferon Cytokine Res. 2014;34(4):255–266. DOI:10.1089/jir.2013.0149
  • Wang H, Ding N, Guo J, et al. Dysregulation of TTP and HuR plays an important role in cancers. Tumour Biol. 2016;37(11):14451–14461. DOI:10.1007/s13277-016-5397-z
  • Wang H, Chen Y, Guo J, et al. Dysregulation of tristetraprolin and human antigen R promotes gastric cancer progressions partly by upregulation of the high-mobility group box 1. Sci Rep. 2018;8(1):7080. DOI:10.1038/s41598-018-25443-3
  • Young LE, Sanduja S, Bemis-Standoli K, et al. The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during Colon carcinogenesis. Gastroenterology. 2009;136(5):1669–1679. DOI:10.1053/j.gastro.2009.01.010
  • Lafzi A, Kazan H. Inferring RBP-Mediated regulation in lung squamous cell carcinoma. PLoS One. 2016;11(5):e0155354.
  • Wang J, Wang B, Bi J, et al. Cytoplasmic HuR expression correlates with angiogenesis, lymphangiogenesis, and poor outcome in lung cancer. Med Oncol. 2011;28 Suppl 1:S577–S85.
  • Dong F, Li C, Wang P, et al. The RNA binding protein tristetraprolin down-regulates autophagy in lung adenocarcinoma cells. Exp Cell Res. 2018;367(1):89–96. DOI:10.1016/j.yexcr.2018.03.028
  • Sandri BJ, Kaplan A, Hodgson SW, et al. Multi-omic molecular profiling of lung cancer in COPD. Eur Respir J. 2018;52(1):1702665. DOI:10.1183/13993003.02665-2017
  • Venigalla RK, Turner M. RNA-binding proteins as a point of convergence of the PI3K and p38 MAPK pathways. Front Immunol. 2012;3:398.
  • Harvey RF, Smith TS, Mulroney T, et al. Trans-acting translational regulatory RNA binding proteins. Wiley Interdiscip Rev RNA. 2018;9(3):e1465.
  • Ho JJD, Balukoff NC, Theodoridis PR, et al. A network of RNA-binding proteins controls translation efficiency to activate anaerobic metabolism. Nat Commun. 2020;11(1):2677. DOI:10.1038/s41467-020-16504-1
  • Schneider-Lunitz V, Ruiz-Orera J, Hubner N, et al. Multifunctional RNA-binding proteins influence mRNA abundance and translational efficiency of distinct sets of target genes. PLoS Comput Biol. 2021;17(12):e1009658.
  • Graham JR, Hendershott MC, Terragni J, et al. mRNA degradation plays a significant role in the program of gene expression regulated by phosphatidylinositol 3-kinase signaling. Mol Cell Biol. 2010;30(22):5295–5305. DOI:10.1128/MCB.00303-10
  • Khabar KS. Hallmarks of cancer and AU-rich elements. Wiley Interdiscip Rev RNA. 2017;8(1):e1368. DOI:10.1002/wrna.1368
  • Sandri BJ, Masvidal L, Murie C, et al. Distinct Cancer-Promoting stromal gene expression depending on lung function. Am J Respir Crit Care Med. 2019;200(3):348–358. DOI:10.1164/rccm.201801-0080OC
  • Blethrow JD, Glavy JS, Morgan DO, et al. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc Natl Acad Sci U S A. 2008;105(5):1442–1447. DOI:10.1073/pnas.0708966105
  • Kim HH, Abdelmohsen K, Lal A, et al. Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev. 2008;22(13):1804–1815. DOI:10.1101/gad.1645808
  • Juan Y, Haiqiao W, Xie W, et al. Cold-inducible RNA-binding protein mediates airway inflammation and mucus hypersecretion through a post-transcriptional regulatory mechanism under cold stress. Int J Biochem Cell Biol. 2016;78:335–348. DOI:10.1016/j.biocel.2016.07.029
  • Navratilova Z, Novosadova E, Hagemann-Jensen M, et al. Expression profile of six RNA-Binding proteins in pulmonary sarcoidosis. PLoS ONE. 2016;11(8):e0161669. DOI:10.1371/journal.pone.0161669
  • Baker JR, Vuppusetty C, Ito K, et al. RNA-binding protein HuR inhibits the expression of sirtuin-1 in patients with COPD. European Respiraory Journal. 2017;50(suppl 61):OA287.
  • Ricciardi L, Col JD, Casolari P, et al. Differential expression of RNA-binding proteins in bronchial epithelium of stable COPD patients. Int J Chron Obstruct Pulmon Dis. 2018;13:3173–3190. DOI:10.2147/COPD.S166284
  • Ricciardi L, Giurato G, Memoli D, et al. Posttranscriptional gene regulatory networks in chronic airway inflammatory diseases: in silico mapping of RNA-Binding protein expression in airway epithelium. Front Immunol. 2020;11:579889.
  • O’Brien K, Breyne K, Ughetto S, et al. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020;21(10):585–606. DOI:10.1038/s41580-020-0251-y
  • Cianferoni A, Schroeder JT, Kim J, et al. Selective inhibition of interleukin-4 gene expression in human T cells by aspirin. Blood. 2001;97(6):1742–1749. DOI:10.1182/blood.v97.6.1742
  • Yu SY, Ip MS, Li X, et al. Low-dose aspirin and incidence of lung carcinoma in patients with chronic obstructive pulmonary disease in Hong Kong: a cohort study. PLoS Med. 2022;19(1):e1003880. DOI:10.1371/journal.pmed.1003880
  • Sengupta S, Jang BC, Wu MT, et al. The RNA-binding protein HuR regulates the expression of cyclooxygenase-2. J Biol Chem. 2003;278(27):25227–25233. DOI:10.1074/jbc.M301813200
  • Blanco FF, Preet R, Aguado A, et al. Impact of HuR inhibition by the small molecule MS-444 on colorectal cancer cell tumorigenesis. Oncotarget. 2016;7(45):74043–74058. DOI:10.18632/oncotarget.12189
  • Zhou L, Gu W, Kui F, et al. The mechanism and candidate compounds of aged citrus peel (chenpi) preventing chronic obstructive pulmonary disease and its progression to lung cancer. Food Nutr Res. 2021;65. DOI:10.29219/fnr.v65.7526
  • Ishmael FT, Fang X, Galdiero MR, et al. Role of the RNA-binding protein tristetraprolin in glucocorticoid-mediated gene regulation. J Immunol. 2008;180(12):8342–8353. DOI:10.4049/jimmunol.180.12.8342
  • Patel B, Priefer R. Impact of chronic obstructive pulmonary disease, lung infection, and/or inhaled corticosteroids use on potential risk of lung cancer. Life Sci. 2022;294:120374. DOI:10.1016/j.lfs.2022.120374
  • Voura M, Sflakidou E, Sarli V. Modulators of ROS/NF-κB signaling in cancer therapy. In Chakraborti S., Ray B.K., Roychoudhury S. (eds) Handbook of oxidative stress in cancer: Mechanistic aspects. Springer, Singapore. 2022. 2165–2184.
  • Youn H, Jeong JC, Jeong YS, et al. Quercetin potentiates apoptosis by inhibiting nuclear factor-kappaB signaling in H460 lung cancer cells. Biol Pharm Bull. 2013;36(6):944–951. DOI:10.1248/bpb.b12-01004
  • Li X, Qu Z, Jing S, et al. Dioscin-60-O-acetate inhibits lung cancer cell proliferation via inducing cell cycle arrest and caspase-dependent apoptosis. Phytomedicine. 2019;53:124–133. DOI:10.1016/j.phymed.2018.09.033
  • Schichl YM, Resch U, Hofer-Warbinek R, et al. Tristetraprolin impairs NF-kappaB/p65 nuclear translocation. J Biol Chem. 2009;284(43):29571–29581. DOI:10.1074/jbc.M109.031237
  • Mohibi S, Chen X, Zhang J. Cancer the’RBP’eutics-RNA-binding proteins as therapeutic targets for cancer. Pharmacol Ther. 2019;203:107390. DOI:10.1016/j.pharmthera.2019.07.001
  • Meisner NC, Hintersteiner M, Mueller K, et al. Identification and mechanistic characterization of low-molecular-weight inhibitors for HuR. Nat Chem Biol. 2007;3(8):508–515. DOI:10.1038/nchembio.2007.14
  • Kondaskar A, Kondaskar S, Kumar R, et al. Novel, broad spectrum anti-Cancer agents containing the tricyclic 5:7:5-Fused diimidazodiazepine ring system. ACS Med Chem Lett. 2010;2(3):252–256. DOI:10.1021/ml100281b
  • Clingman CC, Deveau LM, Hay SA, et al. Allosteric inhibition of a stem cell RNA-binding protein by an intermediary metabolite. Elife. 2014;3:e02848. DOI:10.7554/eLife.02848
  • Amreddy N, Babu A, Panneerselvam J, et al. Chemo-biologic combinatorial drug delivery using folate receptor-targeted dendrimer nanoparticles for lung cancer treatment. Nanomedicine. 2018;14(2):373–384. DOI:10.1016/j.nano.2017.11.010
  • Muralidharan R, Babu A, Amreddy N, et al. Tumor-targeted nanoparticle delivery of HuR siRNA inhibits lung tumor growth in vitro and in vivo by disrupting the oncogenic activity of the RNA-binding protein HuR. Mol Cancer Ther. 2017;16(8):1470–1486. DOI:10.1158/1535-7163.MCT-17-0134
  • Kristensen LS, Hansen TB, Venø MT, et al. Circular RNAs in cancer: opportunities and challenges in the field. Oncogene. 2018;37(5):555–565. DOI:10.1038/onc.2017.361
  • Abdelmohsen K, Panda AC, Munk R, et al. Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol. 2017;14(3):361–369. DOI:10.1080/15476286.2017.1279788
  • Khabar KS. The AU-rich transcriptome: more than interferons and cytokines, and its role in disease. J Interferon Cytokine Res. 2005;25(1):1–10. DOI:10.1089/jir.2005.25.1
  • Wang W, Furneaux H, Cheng H, et al. HuR regulates p21 mRNA stabilization by UV light. Mol Cell Biol. 2000;20(3):760–769. DOI:10.1128/MCB.20.3.760-769.2000
  • Patino WD, Kang JG, Matoba S, et al. Atherosclerotic plaque macrophage transcriptional regulators are expressed in blood and modulated by tristetraprolin. Circ Res. 2006;98(10):1282–1289. DOI:10.1161/01.RES.0000222284.48288.28
  • Al-Haj L, Blackshear PJ, Khabar KS. Regulation of p21/CIP1/WAF-1 mediated cell-cycle arrest by RNase L and tristetraprolin, and involvement of AU-rich elements. Nucleic Acids Res. 2012;40(16):7739–7752. DOI:10.1093/nar/gks545
  • Pont AR, Sadri N, Hsiao SJ, et al. mRNA decay factor AUF1 maintains normal aging, telomere maintenance, and suppression of senescence by activation of telomerase transcription. Mol Cell. 2012;47(1):5–15. DOI:10.1016/j.molcel.2012.04.019
  • Chang N, Yi J, Guo G, et al. HuR uses AUF1 as a cofactor to promote p16INK4 mRNA decay. Mol Cell Biol. 2010;30(15):3875–3886. DOI:10.1128/MCB.00169-10
  • Pang L, Tian H, Chang N, et al. Loss of CARM1 is linked to reduced HuR function in replicative senescence. BMC Mol Biol. 2013;14(15):15.
  • Wang W, Martindale JL, Yang X, et al. Increased stability of the p16 mRNA with replicative senescence. EMBO Rep. 2005;6(2):158–164. DOI:10.1038/sj.embor.7400346
  • Zhou H, Jarujaron S, Gurley EC, et al. HIV protease inhibitors increase TNF-alpha and IL-6 expression in macrophages: involvement of the RNA-binding protein HuR. Atherosclerosis. 2007;195(1):e134-43–e143. DOI:10.1016/j.atherosclerosis.2007.04.008
  • Spooren A, Mestdagh P, Rondou P, et al. IL-1β potently stabilizes IL-6 mRNA in human astrocytes. Biochem Pharmacol. 2011;81(8):1004–1015. DOI:10.1016/j.bcp.2011.01.019
  • Ouhara K, Munenaga S, Kajiya M, et al. The induced RNA-binding protein, HuR, targets 3’-UTR region of IL-6 mRNA and enhances its stabilization in periodontitis. Clin Exp Immunol. 2018;192(3):325–336. DOI:10.1111/cei.13110
  • Patil CS, Liu M, Zhao W, et al. Targeting mRNA stability arrests inflammatory bone loss. Mol Ther. 2008;16(10):1657–1664. DOI:10.1038/mt.2008.163
  • Van Tubergen E, Vander Broek R, Lee J, et al. Tristetraprolin regulates interleukin-6, which is correlated with tumor progression in patients with head and neck squamous cell carcinoma. Cancer. 2011; Jun117(12):2677–2689. DOI:10.1002/cncr.25859
  • Zhao W, Liu M, D’Silva NJ, et al. Tristetraprolin regulates interleukin-6 expression through p38 MAPK-dependent affinity changes with mRNA 3’ untranslated region. J Interferon Cytokine Res. 2011;31(8):629–637. DOI:10.1089/jir.2010.0154
  • Paschoud S, Dogar AM, Kuntz C, et al. Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNA-binding protein AUF1. Mol Cell Biol. 2006;26(22):8228–8241. DOI:10.1128/MCB.01155-06
  • Dean JL, Wait R, Mahtani KR, et al. The 3’ untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol Cell Biol. 2001;21(3):721–730. DOI:10.1128/MCB.21.3.721-730.2001
  • Deleault KM, Skinner SJ, Brooks SA. Tristetraprolin regulates TNF TNF-alpha mRNA stability via a proteasome dependent mechanism involving the combined action of the ERK and p38 pathways. Mol Immunol. 2008;45(1):13–24. DOI:10.1016/j.molimm.2007.05.017
  • Sadri N, Schneider RJ. Auf1/hnrnpd-deficient mice develop pruritic inflammatory skin disease. J Invest Dermatol. 2009;129(3):657–670. DOI:10.1038/jid.2008.298
  • Li M, Yang J, Liu K, et al. p16 promotes proliferation in cervical carcinoma cells through CDK6-HuR-IL1A axis. J Cancer. 2020;11(6):1457–1467. DOI:10.7150/jca.35479
  • Sneezum L, Eislmayr K, Dworak H, et al. Context-Dependent IL-1 mRNA-Destabilization by TTP prevents dysregulation of immune homeostasis under steady state conditions. Front Immunol. 2020;11:1398.
  • Chen YL, Huang YL, Lin NY, et al. Differential regulation of ARE-mediated TNFalpha and IL-1beta mRNA stability by lipopolysaccharide in RAW264.7 cells. Biochem Biophys Res Commun. 2006;346(1):160–168. DOI:10.1016/j.bbrc.2006.05.093
  • Fan J, Ishmael FT, Fang X, et al. Chemokine transcripts as targets of the RNA-binding protein HuR in human airway epithelium. J Immunol. 2011;186(4):2482–2494. DOI:10.4049/jimmunol.0903634
  • Hintzen C, Haan C, Tuckermann JP, et al. Oncostatin M-induced and constitutive activation of the JAK2/STAT5/CIS pathway suppresses CCL1, but not CCL7 and CCL8, chemokine expression. J Immunol. 2008;181(10):7341–7349. DOI:10.4049/jimmunol.181.10.7341
  • Datta S, Biswas R, Novotny M, et al. Tristetraprolin regulates CXCL1 (KC) mRNA stability. J Immunol. 2008;180(4):2545–2552. DOI:10.4049/jimmunol.180.4.2545
  • Qiu LQ, Lai WS, Bradbury A, et al. Tristetraprolin (TTP) coordinately regulates primary and secondary cellular responses to proinflammatory stimuli. J Leukoc Biol. 2015;97(4):723–736. DOI:10.1189/jlb.3A0214-106R
  • Kratochvill F, Machacek C, Vogl C, et al. Tristetraprolin-driven regulatory circuit controls quality and timing of mRNA decay in inflammation. Mol Syst Biol. 2011;7:560. DOI:10.1038/msb.2011.93
  • Wang S, Zhang J, Zhang Y, et al. Nitric oxide-p38 MAPK signaling stabilizes mRNA through AU-rich element-dependent and -independent mechanisms. J Leukoc Biol. 2008;83(4):982–990. DOI:10.1189/jlb.0907641
  • Hudy MH, Proud D. Cigarette smoke enhances human rhinovirus-induced CXCL8 production via HuR-mediated mRNA stabilization in human airway epithelial cells. Respir Res. 2013;14(1):88. DOI:10.1186/1465-9921-14-88
  • Suswam E, Li Y, Zhang X, et al. Tristetraprolin down-regulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res. 2008;68(3):674–682. DOI:10.1158/0008-5472.CAN-07-2751
  • Bourcier C, Griseri P, Grépin R, et al. Constitutive ERK activity induces downregulation of tristetraprolin, a major protein controlling interleukin8/CXCL8 mRNA stability in melanoma cells. Am J Physiol Cell Physiol. 2011;301(3):C609–18. DOI:10.1152/ajpcell.00506.2010
  • Jimbo M, Blanco FF, Huang YH, et al. Targeting the mRNA-binding protein HuR impairs malignant characteristics of pancreatic ductal adenocarcinoma cells. Oncotarget. 2015;6(29):27312–27331. DOI:10.18632/oncotarget.4743
  • Liu H, Lan T, Li H, et al. Circular RNA circDLC1 inhibits MMP1-mediated liver cancer progression via interaction with HuR. Theranostics. 2021;11(3):1396–1411. DOI:10.7150/thno.53227
  • Akool el S, Kleinert H, Hamada FM, et al. Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol Cell Biol. 2003;23(14):4901–4916. DOI:10.1128/MCB.23.14.4901-4916.2003
  • Van Tubergen EA, Banerjee R, Liu M, et al. Inactivation or loss of TTP promotes invasion in head and neck cancer via transcript stabilization and secretion of MMP9, MMP2, and IL-6. Clin Cancer Res. 2013;19(5):1169–1179. DOI:10.1158/1078-0432.CCR-12-2927
  • Chenette DM, Cadwallader AB, Antwine TL, et al. Targeted mRNA decay by RNA binding protein AUF1 regulates adult muscle stem cell fate, promoting skeletal muscle integrity. Cell Rep. 2016;16(5):1379–1390. DOI:10.1016/j.celrep.2016.06.095
  • Yiakouvaki A, Dimitriou M, Karakasiliotis I, et al. Myeloid cell expression of the RNA-binding protein HuR protects mice from pathologic inflammation and colorectal carcinogenesis. J Clin Invest. 2012;122(1):48–61. DOI:10.1172/JCI45021
  • Brennan SE, Kuwano Y, Alkharouf N, et al. The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res. 2009;69(12):5168–5176. DOI:10.1158/0008-5472.CAN-08-4238
  • Fellows A, Griffin ME, Petrella BL, et al. AUF1/hnRNP D represses expression of VEGF in macrophages. Mol Biol Cell. 2012;23(8):1414–1422. DOI:10.1091/mbc.E11-06-0545
  • Doller A, Gauer S, Sobkowiak E, et al. Angiotensin II induces renal plasminogen activator inhibitor-1 and cyclooxygenase-2 expression post-transcriptionally via activation of the mRNA-stabilizing factor human-antigen R. Am J Pathol. 2009;174(4):1252–1263. DOI:10.2353/ajpath.2009.080652
  • Yu H, Stasinopoulos S, Leedman P, et al. Inherent instability of plasminogen activator inhibitor type 2 mRNA is regulated by tristetraprolin. J Biol Chem. 2003;278(16):13912–13918. DOI:10.1074/jbc.M213027200