DDX41 regulates the expression and alternative splicing of genes involved in tumorigenesis and immune response
- Authors:
- Kai Qin
- Danni Jian
- Yaqiang Xue
- Yi Cheng
- Peng Zhang
- Yaxun Wei
- Jing Zhang
- Huihua Xiong
- Yi Zhang
- Xianglin Yuan
-
Affiliations: Department of Oncology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, P.R. China, Department of Otolaryngology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China, Laboratory for Genome Regulation and Human Health, ABLife Inc., Optics Valley International Biomedical Park, Wuhan, Hubei 430075, P.R. China, Center for Genome Analysis, ABLife Inc., Optics Valley International Biomedical Park, Wuhan, Hubei 430075, P.R. China - Published online on: January 25, 2021 https://doi.org/10.3892/or.2021.7951
- Pages: 1213-1225
-
Copyright: © Qin et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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|
Jankowsky E: RNA helicases. 511. 1st edition. Academic Press; 2012 | |
|
Tanner NK and Linder P: DExD/H Box RNA helicases: From generic motors to specific dissociation functions. Mol Cell. 8:251–262. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Bourgeois CF, Mortreux F and Auboeuf D: The multiple functions of RNA helicases as drivers and regulators of gene expression. Nat Rev Mol Cell Biol. 17:426–438. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Rocak S and Linder P: DEAD-Box proteins: The driving forces behind RNA metabolism. Nat Rev Mol Cell Biol. 5:232–241. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Jankowsky E: RNA helicases at work: Binding and rearranging. Trends Biochem Sci. 36:19–29. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Fuller-Pace FV: DExD/H box RNA helicases: Multifunctional proteins with important roles in transcriptional regulation. Nucleic Acids Res. 34:4206–4215. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Cruciat CM, Dolde C, de Groot RE, Ohkawara B, Reinhard C, Korswagen HC and Niehrs C: RNA helicase DDX3 is a regulatory subunit of casein kinase 1 in wnt-β-catenin signaling. Science. 339:1436–1441. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Bleichert F and Baserga SJ: The long unwinding road of RNA helicases. Mol Cell. 27:339–352. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Mosallanejad K, Sekine Y, Ishikura-Kinoshita S, Kumagai K, Nagano T, Matsuzawa A, Takeda K, Naguro I and Ichijo H: The DEAH-Box RNA helicase DHX15 activates NF-κB and MAPK signaling downstream of MAVS during antiviral responses. Sci Signal. 7:ra402014. View Article : Google Scholar : PubMed/NCBI | |
|
Fuller-Pace FV: DEAD box RNA helicase functions in cancer. RNA Biol. 10:121–132. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Francis R and Jerry P: Perturbations of RNA helicases in cancer. Wiley Interdiscip Rev RNA. 4:333–349. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Abdelhaleem M: Do human RNA helicases have a role in cancer? Biochim Biophys Acta. 1704:37–46. 2004.PubMed/NCBI | |
|
Cai W, Chen ZX, Rane G, Singh SS, Choo Z, Wang C, Yuan Y, Tan TZ, Arfuso F, Yap CT, et al: Wanted DEAD/H or alive: Helicases winding up in cancers. J Natl Cancer Inst. 25:1092017. | |
|
Chlon TM, Stepanchick E, Choi K, Zheng Y, Hueneman K, Davis A and Starczynowski DT: The inherited MDS gene DDX41 is required for ribosome biogenesis and cell viability. Blood. 134 (Suppl 1):S7732019. View Article : Google Scholar | |
|
Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, et al: Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature. 481:506–510. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Polprasert C, Schulze I, Sekeres MA, Makishima H, Przychodzen B, Hosono N, Singh J, Padgett RA, Gu X, Phillips JG, et al: Inherited and somatic defects in DDX41 in myeloid neoplasms. Cancer Cell. 27:658–670. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Venugopal P, Cheah JJC, Eshraghi L, Shahrin NH, Homan C, Feng J, Schreiber AW, Fine M, Phillips K, Poplawski N, et al: An integrative genomic approach to examine mutations and biological pathways associated with hematological malignancy development in DDX41 mutated families. Blood. 134 (Suppl 1):S26862019. View Article : Google Scholar | |
|
Cheah JJC, Hahn CN, Hiwase DK, Scott HS and Brown AL: Myeloid neoplasms with germline DDX41 mutation. Int J Hematol. 106:163–174. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Peters D, Radine C, Reese A, Budach W, Sohn D and Jänicke RU: The DEAD-box RNA helicase DDX41 is a novel repressor of p21 WAF1/CIP1 mRNA translation. J Biol Chem. 292:8331–8341. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Stavrou S, Aguilera AN, Blouch K and Ross SR: DDX41 recognizes RNA/DNA retroviral reverse transcripts and is critical for in vivo control of murine leukemia virus infection. mBio. 9:e00923–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Duan Y, Zeng J, Fan S, Liao Y, Feng M, Wang L, Zhang Y and Li Q: Herpes simplex virus type 1-encoded miR-H2-3p manipulates cytosolic DNA-stimulated antiviral innate immune response by targeting DDX41. Viruses. 15:7562019. View Article : Google Scholar | |
|
Zhang Z, Yuan B, Bao M, Lu N, Kim T and Liu YJ: The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol. 12:959–965. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Parvatiyar K, Zhang Z, Teles RM, Ouyang S, Jiang Y, Iyer SS, Zaver SA, Schenk M, Zeng S, Zhong W, et al: The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol. 13:1155–1161. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Nakamura T, Miyabe H, Hyodo M, Sato Y, Hayakawa Y and Harashima H: Liposomes loaded with a STING pathway ligand, cyclic di-GMP, enhance cancer immunotherapy against metastatic melanoma. J Control Release. 216:149–157. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Miyabe H, Hyodo M, Nakamura T, Sato Y, Hayakawa Y and Harashima H: A new adjuvant delivery system ‘cyclic di-GMP/YSK05 liposome’ for cancer immunotherapy. J Control Release. 184:20–27. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cordin O and Beggs JD: RNA helicases in splicing. RNA Biol. 10:83–95. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Jurica MS, Licklider LJ, Gygi SR, Grigorieff N and Moore MJ: Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA. 8:426–439. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Bessonov S, Anokhina M, Will CL, Urlaub H and Lührmann R: Isolation of an active step I spliceosome and composition of its RNP core. Nature. 452:846–850. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Nam DK, Lee S, Zhou G, Cao X, Wang C, Clark T, Chen J, Rowley JD and Wang SM: Oligo(dT) primer generates a high frequency of truncated cDNAs through internal poly(A) priming during reverse transcription. Proc Natl Acad Sci USA. 99:6152–6156. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Robinson MD, McCarthy DJ and Smyth GK: EdgeR: A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 26:139–140. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY and Wei L: KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39((Web Server Issue)): W316–W322. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Xia H, Chen D, Wu Q, Wu G, Zhou Y, Zhang Y and Zhang L: CELF1 preferentially binds to exon-intron boundary and regulates alternative splicing in HeLa cells. Biochim Biophys Acta Gene Regul Mech. 1860:911–921. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Pryke A, Mostaghim S and Nazemi A: Heatmap visualization of population based multi objective algorithms. Evolutionary multi-criterion optimization. Obayashi S, Deb K, Poloni C, Hiroyasu T and Murata T: Springer Berlin Heidelberg; Berlin, Heidelberg: pp. 361–375. 2007, View Article : Google Scholar | |
|
Katz Y, Wang ET, Silterra J, Schwartz S, Wong B, Thorvaldsdóttir H, Robinson JT, Mesirov JP, Airoldi EM and Burge CB: Quantitative visualization of alternative exon expression from RNA-seq data. Bioinformatics. 31:2400–2402. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R and Salzberg SL: TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R362013. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao M, Kim P, Mitra R, Zhao J and Zhao Z: TSGene 2.0: An updated literature-based knowledgebase for tumor suppressor genes. Nucleic Acids Res. 44(D1): D1023–D1031. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Adey A, Burton JN, Kitzman JO, Hiatt JB, Lewis AP, Martin BK, Qiu R, Lee C and Shendure J: The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature. 500:207–211. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Landry JJ, Pyl PT, Rausch T, Zichner T, Tekkedil MM, Stütz AM, Jauch A, Aiyar RS, Pau G, Delhomme N, et al: The genomic and transcriptomic landscape of a HeLa cell line. G3 (Bethesda). 7:1213–1224. 2013. View Article : Google Scholar | |
|
Li Y, Qi H, Li X, Hou X, Lu X and Xiao X: A novel dithiocarbamate derivative induces cell apoptosis through p53-dependent intrinsic pathway and suppresses the expression of the E6 oncogene of human papillomavirus 18 in HeLa cells. Apoptosis. 20:787–795. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Jensen PE: Recent advances in antigen processing and presentation. Nat Immunol. 8:1041–1048. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Murata S, Takahama Y, Kasahara M and Tanaka K: The immunoproteasome and thymoproteasome: Functions, evolution and human disease. Nat Immunol. 19:923–931. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Rock KL, Reits E and Neefjes J: Present yourself! by MHC class I and MHC class II molecules. Trends Immunol. 37:724–737. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Becht E, Giraldo NA, Lacroix L, Buttard B, Elarouci N, Petitprez F, Selves J, Laurent-Puig P, Sautès-Fridman C, Fridman WH and de Reyniès A: Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression. Genome Biol. 17:2182016. View Article : Google Scholar : PubMed/NCBI | |
|
Li T, Fu J, Zeng Z, Cohen D, Li J, Chen Q, Li B and Liu XS: TIMER2.0 for analysis of tumor-infiltrating immune cells. Nucleic Acids Res. 48((W1)): W509–W514. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Flood BA, Higgs EF, Li S, Luke JJ and Gajewski TF: STING pathway agonism as a cancer therapeutic. Immunol Rev. 290:24–38. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Yoneyama-Hirozane M, Kondo M, Matsumoto SI, Morikawa-Oki A, Morishita D, Nakanishi A, Kawamoto T and Nakayama M: High-throughput screening to identify inhibitors of DEAD box helicase DDX41. SLAS Discov. 22:1084–1092. 2017.PubMed/NCBI | |
|
Polprasert C, Schulze I, Sekeres MA, Makishima H, Przychodzen BP, Hosono N, Singh J, Padgett RA, Gu X, Jankowsky E, et al: DDX41 is a tumor suppressor gene associated with inherited and acquired mutations. Blood. 124:1252014. View Article : Google Scholar | |
|
Nekulova M, Holcakova J, Coates P, Vojtesek BJC and Letters MB: The role of P63 in cancer, stem cells and cancer stem cells. Cell Mol Biol Lett. 16:296–327. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Graziano V and De Laurenzi V: Role of p63 in cancer development. Biochim Biophys Acta. 1816:57–66. 2011.PubMed/NCBI | |
|
Wang TY, Chen BF, Yang YC, Chen H, Wang Y, Cviko A, Quade BJ, Sun D, Yang A, McKeon FD and Crum CP: Histologic and immunophenotypic classification of cervical carcinomas by expression of the p53 homologue p63: A study of 250 cases. Hum Pathol. 32:479–486. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
McCluggage WG: Immunohistochemistry as a diagnostic aid in cervical pathology. Pathology. 39:97–111. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Houghton O and McCluggage WG: The expression and diagnostic utility of p63 in the female genital tract. Adv Anat Pathol. 16:316–321. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Saritha VN, Veena VS, Jagathnath KM, Somanathan T and Sujathan K: Significance of DNA replication licensing proteins (MCM2, MCM5 and CDC6), p16 and p63 as markers of premalignant lesions of the uterine cervix: Its usefulness to predict malignant potential. Asian Pac J Cancer Prev. 27:141–148. 2018. | |
|
Pattabiraman D and Gonda T: Role and potential for therapeutic targeting of MYB in leukemia. Leukemia. 27:269–277. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Ramsay RG and Gonda TJ: MYB function in normal and cancer cells. Nat Rev Cancer. 8:523–534. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Drier Y, Cotton MJ, Williamson KE, Gillespie SM, Ryan RJ, Kluk MJ, Carey CD, Rodig SJ, Sholl LM, Afrogheh AH, et al: An oncogenic MYB feedback loop drives alternate cell fates in adenoid cystic carcinoma. Nat Genet. 48:265–272. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Sarvaiya PJ, Schwartz JR, Hernandez CP, Rodriguez PC and Vedeckis WV: Role of c-myb in the survival of pre B-cell acute lymphoblastic leukemia and leukemogenesis. Am J Hematol. 87:969–976. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Biroccio A, Benassi B, D'Agnano I, D'Angelo C, Buglioni S, Mottolese M, Ricciotti A, Citro G, Cosimelli M, Ramsay RG, et al: C-Myb and bcl-x overexpression predicts poor prognosis in colorectal cancer: Clinical and experimental findings. Am J Pathol. 158:1289–1299. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Knopfová L, Biglieri E, Volodko N, Masařík M, Hermanová M, Garzón JF, Dúcka M, Kučírková T, Souček K, Šmarda J, et al: Transcription factor c-myb inhibits breast cancer lung metastasis by suppression of tumor cell seeding. Oncogene. 37:1020–1030. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Ma M, Zhao R, Yang X, Zhao L, Liu L, Zhang C, Wang X and Shan B: Low expression of Mda-7/IL-24 and high expression of C-myb in tumour tissues are predictors of poor prognosis for burkitt lymphoma patients. Hematology. 23:448–455. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Werner S, Duan DS, de Vries C, Peters KG, Johnson DE and Williams LT: Differential splicing in the extracellular region of fibroblast growth factor receptor 1 generates receptor variants with different ligand-binding specificities. Mol Cell Biol. 12:82–88. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Johnson DE, Lu J, Chen H, Werner S and Williams LT: The human fibroblast growth factor receptor genes: A common structural arrangement underlies the mechanisms for generating receptor forms that differ in their third immunoglobulin domain. Mol Cell Biol. 11:4627–4634. 1991. View Article : Google Scholar : PubMed/NCBI | |
|
Chellaiah AT, McEwen DG, Werner S, Xu J and Ornitz M: Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J Biol Chem. 269:11620–11627. 1994. View Article : Google Scholar : PubMed/NCBI | |
|
Vainikka S, Partanen J, Bellosta P, Coulier F, Birnbaum D, Basilico C, Jaye M and Alitalo K: Fibroblast growth factor receptor-4 shows novel features in genomic structure, ligand binding and signal transduction. EMBO J. 12:4273–4280. 1992. View Article : Google Scholar | |
|
Tomlinson DC and Knowles MA: Altered splicing of FGFR1 is associated with high tumor grade and stage and leads to increased sensitivity to FGF1 in bladder cancer. Am J Pathol. 177:2379–2386. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Tang S, Hao Y, Yuan Y, Liu R and Chen Q: Role of fibroblast growth factor receptor 4 in cancer. Cancer Sci. 109:3024–3031. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Touat M, Ileana E, Postel-Vinay S, André F and Soria JC: Targeting FGFR signaling in cancer. Clin Cancer Res. 21:2684–2694. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Babina IS and Turner NC: Advances and challenges in targeting FGFR signalling in cancer. Nat Rev Cancer. 17:318–332. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Trembleau S, Penna G, Bosi E, Mortara A, Gately MK and Adorini L: Interleukin 12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J Exp Med. 181:817–821. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Poe JC, Fujimoto Y, Hasegawa M, Haas KM, Miller AS, Sanford IG, Bock CB, Fujimoto M and Tedder TF: CD22 regulates B lymphocyte function in vivo through both ligand-dependent and ligand-independent mechanisms. Nat Immunol. 5:1078–1087. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Milani V, Noessner E, Ghose S, Kuppner M, Ahrens B, Scharner A, Gastpar R and Issels RD: Heat shock protein 70: Role in antigen presentation and immune stimulation. Int J Hyperthermia. 18:563–575. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Castelli C, Ciupitu AM, Rini F, Rivoltini L, Mazzocchi A, Kiessling R and Parmiani G: Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res. 61:222–227. 2001.PubMed/NCBI | |
|
Noessner E, Gastpar R, Milani V, Brandl A, Hutzler PJ, Kuppner MC, Roos M, Kremmer E, Asea A, Calderwood SK and Issels RD: Tumor-Derived heat shock protein 70 peptide complexes are cross-presented by human dendritic cells. J Immunol. 169:5424–5432. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Banchereau J and Palucka AK: Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol. 5:296–306. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Noessner E: Thermal stress-related modulation of tumor cell physiology and immune responses. Cancer Immunol Immunother. 55:289–291. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Albakova Z, Armeev GA, Kanevskiy LM, Kovalenko EI and Sapozhnikov AM: HSP70 multi-functionality in cancer. Cells. 9:5872020. View Article : Google Scholar | |
|
Lee KG, Susana SY, Kui L, Chih-Cheng Voon D, Mauduit M, Bist P, Bi X, Pereira NA, Liu C, Sukumaran B, et al: Bruton's tyrosine kinase phosphorylates DDX41 and activates its binding of dsDNA and STING to initiate type 1 interferon response. Cell Rep. 10:1055–1065. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Ma JX, Li JY, Fan DD, Feng W, Lin AF, Xiang LX and Shao JZ: Identification of DEAD-box RNA helicase DDX41 as a trafficking protein that involves in multiple innate immune signaling pathways in a zebrafish model. Front Immunol. 9:13272018. View Article : Google Scholar : PubMed/NCBI | |
|
Woo SR, Corrales L and Gajewski TF: The STING pathway and the T cell-inflamed tumor microenvironment. Trends Immunol. 36:250–256. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Barber GN: STING-Dependent cytosolic DNA sensing pathways. Trends Immunol. 35:88–93. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Barber GN: STING: Infection, inflammation and cancer. Nat Rev Immunol. 15:760–770. 2015. View Article : Google Scholar : PubMed/NCBI |
