The Enigmatic Helicase DHX9 and Its Association With the Hallmarks of Cancer

References

• Fuller-PaceFV. DExD/H box RNA helicases: multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Res.34(15), 4206–4215 (2006).
   PubMed Web of Science ®Google Scholar
• JainA , BacollaA , DelMundo IM , ZhaoJ , WangG , VasquezKM. DHX9 helicase is involved in preventing genomic instability induced by alternatively structured DNA in human cells. Nucleic Acids Res.41(22), 10345–10357 (2013).
   PubMed Web of Science ®Google Scholar
• CristiniA , GrohM , KristiansenMS , GromakN. RNA/DNA hybrid interactome identifies DXH9 as a molecular player in transcriptional termination and R-loop-associated DNA damage. Cell Rep.23(6), 1891–1905 (2018).
   PubMed Web of Science ®Google Scholar
• CaoS , SunR , WangWet al.RNA helicase DHX9 may be a therapeutic target in lung cancer and inhibited by enoxacin. Am. J. Transl. Res.9(2), 674–682 (2017).
   PubMed Web of Science ®Google Scholar
• YanX , ChangJ , SunRet al.DHX9 inhibits epithelial-mesenchymal transition in human lung adenocarcinoma cells by regulating STAT3. Am. J. Transl. Res.11(8), 4881–4894 (2019).
   PubMed Web of Science ®Google Scholar
• MiJ , RayP , LiuJet al.In vivo selection against human colorectal cancer xenografts identifies an aptamer that targets RNA helicase protein DHX9. Mol. Ther. - Nucleic Acids5, e315 (2016).
   Google Scholar
• LeeT , PelletierJ. The biology of DHX9 and its potential as a therapeutic target. Oncotarget7(27), 42716–42739 (2016).
   PubMedGoogle Scholar
• UmateP , TutejaN , TutejaR. Genome-wide comprehensive analysis of human helicases. Commun. Integr. Biol.4(1), 118 (2011).
   PubMedGoogle Scholar
• GilmanB , TijerinaP , RussellR. Distinct RNA-unwinding mechanisms of DEAD-box and DEAH-box RNA helicase proteins in remodeling structured RNAs and RNPs. Biochem. Soc. Trans.45(6), 1313–1321 (2017).
   PubMedGoogle Scholar
• PyleAM. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys.37(1), 317–336 (2008).
   PubMedGoogle Scholar
• SchützP , KarlbergT , vanden Berg Set al.Comparative structural analysis of human DEAD-Box RNA helicases. PLoS ONE5(9), e12791 (2010).
   PubMed Web of Science ®Google Scholar
• BourgeoisCF , MortreuxF , AuboeufD. The multiple functions of RNA helicases as drivers and regulators of gene expression. Nat. Rev. Mol. Cell Biol.17(7), 426–438 (2016).
   PubMed Web of Science ®Google Scholar
• LeeC-G , EkiT , OkumuraKet al.The human RNA Helicase A (DDX9) gene maps to the prostate cancer susceptibility locus at chromosome band 1q25 and its pseudogene (DDX9P) to 13q22, respectively.Somat Cell Mol Genet25(1), 33–39 (1999).
   PubMedGoogle Scholar
• ZhangS , GrosseF. Domain structure of human nuclear DNA helicase II (RNA helicase A). J. Biol. Chem.272(17), 11487–11494 (1997).
   PubMed Web of Science ®Google Scholar
• FidaleoM , SvetoniF , VolpeE , MiñanaB , CaporossiD , ParonettoMP. Genotoxic stress inhibits ewing sarcoma cell growth by modulating alternative pre-mRNA processing of the RNA helicase DHX9. Oncotarget6(31), 31740–31757 (2015).
   PubMedGoogle Scholar
• ChakrabortyP , GrosseF. Human DHX9 helicase preferentially unwinds RNA-containing displacement loops (R-loops) and G-quadruplexes. DNA Repair (Amst).10(6), 654–665 (2011).
   PubMed Web of Science ®Google Scholar
• MikolaskovaB , JurcikM , CipakovaI , KretovaM , ChovanecM , CipakL. Maintenance of genome stability: the unifying role of interconnections between the DNA damage response and RNA-processing pathways. Curr. Genet.64(5), 971–983 (2018).
   PubMed Web of Science ®Google Scholar
• RoyD , ZhangZ , LuZ , HsiehC-L , LieberMR. Competition between the RNA transcript and the nontemplate DNA strand during R-loop formation in vitro: a nick can serve as a strong R-loop initiation site. Mol. Cell. Biol.30(1), 146–159 (2010).
   PubMed Web of Science ®Google Scholar
• AllisonDF , WangGG. R-loops: formation, function, and relevance to cell stress. Cell Stress.3(2), 38–46 (2019).
   PubMedGoogle Scholar
• HamperlS , BocekMJ , SaldivarJC , SwigutT , CimprichKA. Transcription-replication conflict orientation modulates R-loop levels and activates distinct DNA damage responses. Cell170(4), 774 (2017).
   PubMed Web of Science ®Google Scholar
• GanW , GuanZ , LiuJet al.R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev.25(19), 2041–2056 (2011).
   PubMed Web of Science ®Google Scholar
• FidaleoM , DePaola E , ParonettoMP. The RNA helicase A in malignant transformation. Oncotarget7(19), 28711–28723 (2016).
   PubMedGoogle Scholar
• ChakrabortyP , HuangJTJ , HiomK. DHX9 helicase promotes R-loop formation in cells with impaired RNA splicing. Nat. Commun.9(1), 4346–4359 (2018).
   PubMedGoogle Scholar
• AndersonSF , SchlegelBP , NakajimaT , WolpinES , ParvinJD. BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat. Genet.19(3), 254–256 (1998).
   PubMed Web of Science ®Google Scholar
• HatchiE , Skourti-StathakiK , VentzSet al.BRCA1 recruitment to transcriptional pause sites is required for R-loop-driven DNA damage repair. Mol. Cell.57(4), 636–647 (2015).
   PubMed Web of Science ®Google Scholar
• Skourti-StathakiK , ProudfootNJ , GromakN. Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol. Cell.42(6), 794–805 (2011).
   PubMed Web of Science ®Google Scholar
• SchlacherK , WuH , JasinM. A distinct replication fork protection pathway connects fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell22(1), 106 (2012).
   PubMed Web of Science ®Google Scholar
• OhleC , TesoreroR , SchermannG , DobrevN , SinningI , FischerT. Transient RNA-DNA hybrids are required for efficient double-strand break repair. Cell167(4), 1001–1013.e7 (2016).
   PubMed Web of Science ®Google Scholar
• YasuharaT , KatoR , HagiwaraYet al.Human Rad52 promotes XPG-mediated R-loop processing to initiate transcription-associated homologous recombination repair. Cell175(2), 558–570.e11 (2018).
   PubMed Web of Science ®Google Scholar
• ChakrabortyP , HiomK. DHX9-dependent recruitment of BRCA1 to RNA is required to promote DNA end resection in homologous recombination. bioRxiv. Doi: https://doi.org/10.1101/2019.12.20.884593 (2019).
   Google Scholar
• Skourti-StathakiK , ProudfootNJ. A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev.28(13), 1384–1396 (2014).
   PubMed Web of Science ®Google Scholar
• FriedemannJ , GrosseF , ZhangS. Nuclear DNA helicase II (RNA helicase A) interacts with Werner syndrome helicase and stimulates its exonuclease activity. J. Biol. Chem.280(35), 31303–31313 (2005).
   PubMed Web of Science ®Google Scholar
• ChakrabortyP , GrosseF. WRN helicase unwinds Okazaki fragment-like hybrids in a reaction stimulated by the human DHX9 helicase. Nucleic Acids Res.38(14), 4722–4730 (2010).
   PubMed Web of Science ®Google Scholar
• LeeT , DiPaola D , MalinaAet al.Suppression of the DHX9 helicase induces premature senescence in human diploid fibroblasts in a p53-dependent manner. J. Biol. Chem.289(33), 22798–22814 (2014).
   PubMed Web of Science ®Google Scholar
• DuquetteML , HandaP , VincentJA , TaylorAF , MaizelsN. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev.18(13), 1618 (2004).
   PubMed Web of Science ®Google Scholar
• MyöhänenS , BaylinSB. Sequence-specific DNA binding activity of RNA helicase A to the p16INK4a promoter. J. Biol. Chem.276(2), 1634–1642 (2001).
   PubMed Web of Science ®Google Scholar
• ZhongX , SafaAR. Phosphorylation of RNA helicase a by DNA-dependent protein kinase is indispensable for expression of the MDR1 gene product P-glycoprotein in multidrag-resistant human leukemia cells. Biochemistry46(19), 5766–5775 (2007).
   PubMed Web of Science ®Google Scholar
• HuoL , WangYN , XiaWet al.RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc. Natl Acad. Sci. USA107(37), 16125–16130 (2010).
   PubMed Web of Science ®Google Scholar
• MonteiroAN. BRCA1: exploring the links to transcription. Trends Biochem. Sci.25(10), 469–474 (2000).
   PubMed Web of Science ®Google Scholar
• NakajimaT , UchidaC , AndersonSFet al.RNA helicase A mediates association of CBP with RNA polymerase II. Cell90(6), 1107–1112 (1997).
   PubMed Web of Science ®Google Scholar
• TetsukaT , UranishiH , SandaTet al.RNA helicase A interacts with nuclear factor κB p65 and functions as a transcriptional coactivator. Eur. J. Biochem.271(18), 3741–3751 (2004).
   PubMedGoogle Scholar
• MukherjeeSP , BeharM , BirnbaumHA , HoffmannA , WrightPE , GhoshG. Analysis of the RelA:CBP/p300 interaction reveals its involvement in NF-κB-driven transcription. PLoS Biol.11(9), e1001647 (2013).
   PubMed Web of Science ®Google Scholar
• ParsyanA , SvitkinY , ShahbazianDet al.mRNA helicases: the tacticians of translational control. Nat. Rev. Mol. Cell Biol.12(4), 235–245 (2011).
   PubMed Web of Science ®Google Scholar
• MuratP , MarsicoG , HerdyB , GhanbarianA , PortellaG , BalasubramanianS. RNA G-quadruplexes at upstream open reading frames cause DHX36- and DHX9-dependent translation of human mRNAs. Genome Biol.19(1), 229 (2018).
   PubMedGoogle Scholar
• HartmanTR , QianS , BolingerC , FernandezS , SchoenbergDR , Boris-LawrieK. RNA helicase A is necessary for translation of selected messenger RNAs. Nat. Struct. Mol. Biol.13(6), 509–516 (2006).
   PubMed Web of Science ®Google Scholar
• RobbGB , RanaTM. RNA helicase A interacts with RISC in human cells and functions in RISC loading. Mol. Cell26(4), 523–537 (2007).
   PubMed Web of Science ®Google Scholar
• FuQ , YuanYA. Structural insights into RISC assembly facilitated by dsRNA-binding domains of human RNA helicase A (DHX9). Nucleic Acids Res.41(5), 3457 (2013).
   PubMed Web of Science ®Google Scholar
• KawaiS , AmanoA. BRCA1 regulates microRNA biogenesis via the DROSHA microprocessor complex. J. Cell Biol.197(2), 201–208 (2012).
   PubMed Web of Science ®Google Scholar
• BoerasI , SongZ , MoranAet al.DHX9/RHA binding to the PBS-segment of the genomic RNA during HIV-1 assembly bolsters virion infectivity. J. Mol. Biol.428(11), 2418–2429 (2016).
   PubMed Web of Science ®Google Scholar
• NgYC , ChungWC , KangHRet al.A DNA-sensing–independent role of a nuclear RNA helicase, DHX9, in stimulation of NF-B–mediated innate immunity against DNA virus infection. Nucleic Acids Res.46(17), 9011–9026 (2018).
   PubMed Web of Science ®Google Scholar
• KimT , PazhoorS , BaoMet al.Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc. Natl Acad. Sci. USA107(34), 15181–15186 (2010).
   PubMed Web of Science ®Google Scholar
• ZhangZ , YuanB , LuN , FacchinettiV , LiuY-J. DHX9 pairs with IPS-1 to sense double-stranded RNA in myeloid dendritic cells. J. Immunol.187(9), 4501 (2011).
   PubMed Web of Science ®Google Scholar
• ShenB , ChenY , HuJet al.Hepatitis B virus X protein modulates upregulation of DHX9 to promote viral DNA replication. Cell. Microbiol.22(3), e13148–57 (2020).
   PubMed Web of Science ®Google Scholar
• ChenY , ShenB , ZhengXet al.DHX9 interacts with APOBEC3B and attenuates the anti-HBV effect of APOBEC3B. Emerg. Microbes Infect.9(1), 366–377 (2020).
   PubMed Web of Science ®Google Scholar
• HeQS , TangH , ZhangJ , TruongK , Wong-StaalF , ZhouD. Comparisons of RNAi approaches for validation of human RNA helicase A as an essential factor in hepatitis C virus replication. J. Virol. Methods154(1–2), 216–219 (2008).
   PubMed Web of Science ®Google Scholar
• BolingerC , SharmaA , SinghD , YuL , Boris-LawrieK. RNA helicase A modulates translation of HIV-1 and infectivity of progeny virions. Nucleic Acids Res.38(5), 1686–1696 (2010).
   PubMed Web of Science ®Google Scholar
• MatkovicR , BernardE , FontanelSet al.The host DHX9 DExH-box helicase is recruited to chikungunya virus replication complexes for optimal genomic RNA translation. J. Virol.93(4), e01764–18 (2019).
   PubMed Web of Science ®Google Scholar
• HanahanD , WeinbergRA. Hallmarks of cancer: the next generation. Cell144(5), 646–674 (2011).
   PubMed Web of Science ®Google Scholar
• WangYL , LiuJY , YangJEet al.Lnc-UCID promotes G1/S transition and hepatoma growth by preventing DHX9-mediated CDK6 down-regulation. Hepatology70(1), 259–275 (2019).
   PubMed Web of Science ®Google Scholar
• LeeEYHP , MullerWJ. Oncogenes and tumor suppressor genes. Cold Spring Harb. Perspect. Biol.2(10), a003236–53 (2010).
   PubMed Web of Science ®Google Scholar
• PearsonPL , Vander Luijt RB. The genetic analysis of cancer. J. Intern. Med.243(6), 413–417 (1998).
   PubMed Web of Science ®Google Scholar
• WellsJP , WhiteJ , StirlingPC. R loops and their composite cancer connections. Trends in Cancer5(10), 619–631 (2019).
   PubMed Web of Science ®Google Scholar
• TuranliB , KaragozK , BidkhoriGet al.Multi-omic data interpretation to repurpose subtype specific drug candidates for breast cancer. Front. Genet.10, 420–32 (2019).
   PubMed Web of Science ®Google Scholar
• ScharerCD , McCabeCD , Ali-SeyedM , BergerMF , BulykML , MorenoCS. Genome-wide promoter analysis of the SOX4 transcriptional network in prostate cancer cells. Cancer Res.69(2), 709 (2009).
   PubMed Web of Science ®Google Scholar
• MehtaGA , ParkerJS , SilvaGO , HoadleyKA , PerouCM , GatzaML. Amplification of SOX4 promotes PI3K/Akt signaling in human breast cancer. Breast Cancer Res. Treat.162(3), 439 (2017).
   PubMed Web of Science ®Google Scholar
• LiuP , RamachandranS , AliSeyed Met al.Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res.66(8), 4011–4019 (2006).
   PubMed Web of Science ®Google Scholar
• MorenoCS. SOX4: the unappreciated oncogene. Semin. Cancer Biol. (18), 30145–7 (2019).
   Google Scholar
• LaiYH , ChengJ , ChengDet al.SOX4 interacts with plakoglobin in a Wnt3a-dependent manner in prostate cancer cells. BMC Cell Biol.12, 50–57 (2011).
   PubMedGoogle Scholar
• ZandiR , LarsenAB , AndersenP , StockhausenM-T , PoulsenHS. Mechanisms for oncogenic activation of the epidermal growth factor receptor. Cell. Signal.19(10), 2013–2023 (2007).
   PubMed Web of Science ®Google Scholar
• LinS-Y , MakinoK , XiaWet al.Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat. Cell Biol.3(9), 802–808 (2001).
   PubMed Web of Science ®Google Scholar
• HarbourJW , DeanDC. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev.14(19), 2393–2409 (2000).
   PubMed Web of Science ®Google Scholar
• OrmandyCJ , MusgroveEA , HuiR , DalyRJ , SutherlandRL. Cyclin D1, EMS1 and 11q13 amplification in breast cancer. Breast Cancer Res. Treat.78(3), 323–35 (2003).
   PubMed Web of Science ®Google Scholar
• GarceaG , NealC , PattendenC , StewardW , BerryD. Molecular prognostic markers in pancreatic cancer: a systematic review. Eur. J. Cancer41(15), 2213–2236 (2005).
   PubMed Web of Science ®Google Scholar
• GautschiO , RatschillerD , GuggerM , BetticherD , HeighwayJ. Cyclin D1 in non-small cell lung cancer: a key driver of malignant transformation. Lung Cancer55(1), 1–14 (2007).
   PubMed Web of Science ®Google Scholar
• PalomboR , FrisoneP , FidaleoM , MercatelliN , SetteC , ParonettoMP. The promoter-associated noncoding RNA PNCCCND1_B assembles a protein–RNA complex to regulate cyclin D1 transcription in Ewing sarcoma. Cancer Res.79(14), 3570–3582 (2019).
   PubMed Web of Science ®Google Scholar
• LiJ , PoiMJ , TsaiM-D. The regulatory mechanisms of tumor supressor p16INK4 and relevance to cancer. Biochemistry50(25), 5566–5582 (2011).
   PubMed Web of Science ®Google Scholar
• SchlegelBP , StaritaLM , ParvinJD. Overexpression of a protein fragment of rna helicase a causes inhibition of endogenous brca1 function and defects in ploidy and cytokinesis in mammary epithelial cells. Oncogene22(7), 983–991 (2003).
   PubMed Web of Science ®Google Scholar
• DengC-X. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res.34(5), 1416 (2006).
   PubMed Web of Science ®Google Scholar
• AprelikovaON , FangBS , MeissnerEGet al.BRCA1-associated growth arrest is RB-dependent. Proc. Natl Acad. Sci. USA96(21), 11866 (1999).
   PubMed Web of Science ®Google Scholar
• GuénardF , LabrieY , OuelletteGet al.Genetic sequence variations of BRCA1-interacting genes AURKA, BAP1, BARD1 and DHX9 in French Canadian Families with high risk of breast cancer. J. Hum. Genet.54(3), 152–161 (2009).
   PubMed Web of Science ®Google Scholar
• FurutaS , JiangX , GuB , ChengE , ChenP , LeeW. Depletion of BRCA1 impairs differentiation but enhances proliferation of mammary epithelial cells. Proc. Natl Acad. Sci. USA102(26), 9176–9181 (2005).
   PubMed Web of Science ®Google Scholar
• OzakiT , NakagawaraA. Role of p53 in cell death and human cancers. Cancers (Basel)3(1), 994–1013 (2011).
   PubMedGoogle Scholar
• LeeT , PaquetM , LarssonO , PelletierJ. Tumor cell survival dependence on the DHX9 DExH-box helicase. Oncogene35(39), 5093–5105 (2016).
   PubMed Web of Science ®Google Scholar
• LeeT , PelletierJ. Dependence of p53-deficient cells on the DHX9 DExH-box helicase. Oncotarget8(19), 30908–30921 (2017).
   PubMedGoogle Scholar
• ChenZX , WallisK , FellSMet al.RNA helicase a is a downstream mediator of KIF1Bβ tumor-suppressor function in neuroblastoma. Cancer Discov.4(4), 434–451 (2014).
   PubMed Web of Science ®Google Scholar
• DingX , JiaX , WangC , XuJ , GaoS-J , LuC. A DHX9-lncRNA-MDM2 interaction regulates cell invasion and angiogenesis of cervical cancer. Cell Death Differ.26(9), 1750–1765 (2019).
   PubMed Web of Science ®Google Scholar
• HansenT , JensenT , ClausenBet al.Natural RNA circles function as efficient microRNA sponges. Nature495(7441), 384–388 (2013).
   PubMed Web of Science ®Google Scholar
• AktaşT , IlikIA , MaticzkaDet al.DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome. Nature544(7648), 115–119 (2017).
   PubMed Web of Science ®Google Scholar
• HsiaoK-Y , LinY-C , GuptaSKet al.Non-coding effects of circular RNA CCDC66 promote colon cancer growth and metastasis. Cancer Res.77(9), 2339 (2017).
   PubMed Web of Science ®Google Scholar
• LinY , YuY , LinH , HsiaoK. Oxaliplatin-induced DHX9 phosphorylation promotes oncogenic circular RNA CCDC66 expression and development of chemoresistance. Cancers (Basel)12(3), 1–14 (2020).
   Web of Science ®Google Scholar
• YuJ , XuQ-G , WangZ-Get al.Circular RNA cSMARCA5 inhibits growth and metastasis in hepatocellular carcinoma. J. Hepatol.68(6), 1214–1227 (2018).
   PubMed Web of Science ®Google Scholar
• ZucchiniC , RocchiA , ManaraMCet al.Apoptotic genes as potential markers of metastatic phenotype in human osteosarcoma cell lines. Int. J. Oncol.32(1), 17–31 (2008).
   PubMed Web of Science ®Google Scholar
• SongZ , ZhuoZ , MaZ , HouC , ChenG , XuG. Hsa_Circ_0001206 is downregulated and inhibits cell proliferation, migration and invasion in prostate cancer. Artif. Cells, Nanomedicine, Biotechnol.47(1), 2449–2464 (2019).
   PubMed Web of Science ®Google Scholar
• KamelgarnM , ChenJ , KuangLet al.Proteomic analysis of FUS interacting proteins provides insights into FUS function and its role in ALS. Biochim. Biophys. Acta1862(10), 2004–2014 (2016).
   PubMed Web of Science ®Google Scholar
• MicalizziDS , FarabaughSM , FordHL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J. Mammary Gland Biol. Neoplasia15(2), 117 (2010).
   PubMed Web of Science ®Google Scholar
• ShangB-Q , LiM-L , QuanHet al.Functional roles of circular RNAs during epithelial-to-mesenchymal transition. Mol. Cancer18, 138–147 (2019).
   PubMed Web of Science ®Google Scholar
• YanD , DongW , HeQet al.Circular RNA circPICALM sponges miR-1265 to inhibit bladder cancer metastasis and influence FAK phosphorylation. EBioMedicine48, 316–331 (2019).
   PubMed Web of Science ®Google Scholar
• JosephNA , ChiouS-H , LungZet al.The role of HGF-MET pathway and CCDC66 cirRNA expression in EGFR resistance and epithelial-to-mesenchymal transition of lung adenocarcinoma cells. J. Hematol. Oncol.11, 557–559 (2018).
   Web of Science ®Google Scholar
• WangW-P , SunY , LuQet al.Gankyrin promotes epithelial-mesenchymal transition and metastasis in NSCLC through forming a closed circle with IL-6/STAT3 and TGF-β/SMAD3 signaling pathway. Oncotarget8(4), 5909–5923 (2017).
   PubMedGoogle Scholar
• WoodsD , TurchiJJ. Chemotherapy induced DNA damage response: convergence of drugs and pathways. Cancer Biol. Ther.14(5), 379–389 (2013).
   PubMed Web of Science ®Google Scholar
• NogalesV , ReinholdWC , VarmaSet al.Epigenetic inactivation of the putative DNA/RNA helicase SLFN11 in human cancer confers resistance to platinum drugs. Oncotarget7(3), 3084–3097 (2016).
   PubMedGoogle Scholar
• ZhongX , SafaAR. RNA helicase A in the MEF1 transcription factor complex up-regulates the MDR1 gene in multidrug-resistant cancer cells. J. Biol. Chem.279(17), 17134–17141 (2004).
   PubMed Web of Science ®Google Scholar
• YiG-Z , XiangW , FengW-Yet al.Identification of key candidate proteins and pathways associated with temozolomide resistance in glioblastoma based on subcellular proteomics and bioinformatical analysis. Biomed Res. Int.2018, 5238760 (2018).
   PubMed Web of Science ®Google Scholar
• Boros-OláhB , DobosN , HornyákLet al.Drugging the R-loop interactome: RNA-DNA hybrid binding proteins as targets for cancer therapy. DNA Repair (Amst).84, 102642–52 (2019).
   PubMed Web of Science ®Google Scholar
• CheslerL , GoldenbergDD , CollinsRet al.Chemotherapy-induced apoptosis in a transgenic model of neuroblastoma proceeds through p53 induction. Neoplasia10(11), 1268–1274 (2008).
   PubMed Web of Science ®Google Scholar
• MillsJR , MalinaA , LeeTet al.RNAi screening uncovers DHX9 as a modifier of ABT-737 resistance in an Em-myc/BCL-2 mouse model. Blood121(17), 3402–3412 (2013).
   PubMed Web of Science ®Google Scholar
• ToretskyJA , ErkizanV , LevensonAet al.Oncoprotein EWS-FLI1 activity is enhanced by RNA helicase A. Cancer Res.66(11), 5574–5581 (2006).
   PubMed Web of Science ®Google Scholar
• PalomboR , VerdileV , ParonettoMP. Poison-exon inclusion in DHX9 reduces its expression and sensitizes Ewing sarcoma cells to chemotherapeutic treatment. Cells9(2), 328 (2020).
   PubMed Web of Science ®Google Scholar
• SchirrmacherV. From chemotherapy to biological therapy: a review of novel concepts to reduce the side effects of systemic cancer treatment (Review). Int. J. Oncol.54(2), 407–419 (2019).
   PubMed Web of Science ®Google Scholar
• LeeCG , DaCosta Soares V , NewbergerC , ManovaK , LacyE , HurwitzJ. RNA helicase A is essential for normal gastrulation. Proc. Natl Acad. Sci. USA95(23), 13709–13713 (1998).
   PubMed Web of Science ®Google Scholar
• RivlinN , BroshR , OrenM , RotterV. Mutations in the p53 tumor suppressor gene: important milestones at the various steps of tumorigenesis. Genes Cancer2(4), 466 (2011).
   PubMedGoogle Scholar
• GuoZS. The 2018 Nobel Prize in medicine goes to cancer immunotherapy (editorial for BMC cancer). BMC Cancer18, 1086–1088 (2018).
   PubMed Web of Science ®Google Scholar
• RajaJ , LudwigJM , GettingerSN , SchalperKA , KimHS. Oncolytic virus immunotherapy: future prospects for oncology. J. Immunother. Cancer6(1), 140 (2018).
   PubMedGoogle Scholar
• ChesneyJ , PuzanovI , CollichioFet al.Randomized, open-label Phase II study evaluating the efficacy and safety of talimogene laherparepvec in combination with ipilimumab versus ipilimumab alone in patients with advanced, unresectable melanoma. J. Clin. Oncol.36(17), 1658–1667 (2018).
   PubMed Web of Science ®Google Scholar
• RibasA , DummerR , PuzanovIet al.Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell170(6), 1109–1119.e10 (2017).
   PubMed Web of Science ®Google Scholar
• ChanWM , RahmanMM , McFaddenG. Oncolytic myxoma virus: the path to clinic. Vaccine31(39), 4252–4258 (2013).
   PubMed Web of Science ®Google Scholar
• RahmanMM , MadlambayanGJ , CogleCR , McFaddenG. Oncolytic viral purging of leukemic hematopoietic stem and progenitor cells with Myxoma virus. Cytokine Growth Factor Rev.21(2–3), 169–175 (2010).
   PubMed Web of Science ®Google Scholar
• RahmanMM , BagdassarianE , AliMAM , McFaddenG. Identification of host DEAD-box RNA helicases that regulate cellular tropism of oncolytic Myxoma virus in human cancer cells. Sci. Rep.7(1), 1–14 (2017).
   PubMedGoogle Scholar
• RahmanMM , LiuJ , ChanWM , RothenburgS , McFaddenG. Myxoma virus protein M029 is a dual function immunomodulator that inhibits PKR and also conscripts RHA/DHX9 to promote expanded host tropism and viral replication. PLoS Pathog.9(7), e1003465 (2013).
   PubMed Web of Science ®Google Scholar
• SadlerAJ , LatchoumaninO , HawkesD , MakJ , WilliamsBRG. An antiviral response directed by PKR phosphorylation of the RNA helicase A. PLoS Pathog.5(2), e1000311 (2009).
   PubMed Web of Science ®Google Scholar