The effects of RNA editing in cancer tissue at different stages in carcinogenesis

. 2021 Nov ; 18 (11) : 1524-1539. [epub] 20210217

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33593231

RNA editing is one of the most prevalent and abundant forms of post-transcriptional RNA modification observed in normal physiological processes and often aberrant in diseases including cancer. RNA editing changes the sequences of mRNAs, making them different from the source DNA sequence. Edited mRNAs can produce editing-recoded protein isoforms that are functionally different from the corresponding genome-encoded protein isoforms. The major type of RNA editing in mammals occurs by enzymatic deamination of adenosine to inosine (A-to-I) within double-stranded RNAs (dsRNAs) or hairpins in pre-mRNA transcripts. Enzymes that catalyse these processes belong to the adenosine deaminase acting on RNA (ADAR) family. The vast majority of knowledge on the RNA editing landscape relevant to human disease has been acquired using in vitro cancer cell culture models. The limitation of such in vitro models, however, is that the physiological or disease relevance of results obtained is not necessarily obvious. In this review we focus on discussing in vivo occurring RNA editing events that have been identified in human cancer tissue using samples surgically resected or clinically retrieved from patients. We discuss how RNA editing events occurring in tumours in vivo can identify pathological signalling mechanisms relevant to human cancer physiology which is linked to the different stages of cancer progression including initiation, promotion, survival, proliferation, immune escape and metastasis.

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Boccaletto P, Machnicka MA, Purta E, et al. MODOMICS: A database of RNA modification pathways. 2017 update. Nucleic Acids Res. 2018;46(D1):D303–D307. PubMed PMC

Gallo A, Vukic D, Michalík D, et al. ADAR RNA editing in human disease; more to it than meets the I. Hum Genet. 2017;136(9):1265–1278. PubMed

Riedmann EM, Schopoff S, Hartner JC, et al. Specificity of ADAR-mediated RNA editing in newly identified targets. Rna. 2008;14(6):1110–1118. PubMed PMC

Blow MJ, Grocock RJ, van Dongen S, et al. RNA editing of human microRNAs. Genome Biol. 2006;7(4):R27. PubMed PMC

Kawahara Y, Zinshteyn B, Sethupathy P, et al. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science. 2007;315(5815):1137–1140. PubMed PMC

Nishikura K. Functions and Regulation of RNA editing by ADAR deaminases. Annu Rev Biochem. 2010;79(1):321–349. PubMed PMC

Bazak L, Haviv A, Barak M, et al. A-to-I RNA editing occurs at over a hundred million genomic sites, located in a majority of human genes. Genome Res. 2014;24(3):365–376. PubMed PMC

Mannion NM, Greenwood SM, Young R, et al. The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep. 2014;9(4):1482–1494. PubMed PMC

Heale BSE, Keegan LP, McGurk L, et al. Editing independent effects of ADARs on the miRNA/siRNA pathways. Embo J. 2009;28(20):3145–3156. PubMed PMC

Oakes E, Anderson A, Cohen-Gadol A, et al. Adenosine deaminase that acts on RNA 3 (adar3) binding to glutamate receptor subunit B Pre-mRNA Inhibits RNA editing in glioblastoma. Journal of Biological Chemistry. 2017;292(10):4326–4335. PubMed PMC

Chen CX, Cho DSC, Wang Q, et al. A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains. Rna. 2000;6(5):755–767. PubMed PMC

Fritz J, Strehblow A, Taschner A, et al. RNA-regulated interaction of transportin-1 and exportin-5 with the double-stranded RNA-binding domain regulates nucleocytoplasmic shuttling of ADAR1. Mol Cell Biol. 2009;29(6):1487–1497. PubMed PMC

Strehblow A, Hallegger M, Jantsch MF. Nucleocytoplasmic distribution of human RNA-editing enzyme ADAR1 is modulated by double-stranded RNA-binding domains, a leucine-rich export signal, and a putative dimerization domain. Mol Biol Cell. 2002;13(11):3822–3835. PubMed PMC

Nishikura K. A-to-I editing of coding and non-coding RNAs by ADARs. Nat Rev Mol Cell Biol. 2016;17(2):83–96. PubMed PMC

Desterro JMP, Keegan LP, Lafarga M, et al. Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci. 2003;116(9):1805–1818. PubMed

Eckmann CR, Neunteufl A, Pfaffstetter L, et al. The human but not the Xenopus RNA-editing enzyme ADAR1 has an atypical nuclear localization signal and displays the characteristics of a shuttling protein. Mol Biol Cell. 2001;12(7):1911–1924. PubMed PMC

George CX, Samuel CE. Human RNA-specific adenosine deaminase ADAR1 transcripts possess alternative exon 1 structures that initiate from different promoters, one constitutively active and the other interferon inducible. Proc Natl Acad Sci U S A. 1999;96(8):4621–4626. PubMed PMC

O’Connell MA,  Krause S, Higuchi M, et al. Cloning of cDNAs encoding mammalian double-stranded RNA-specific adenosine deaminase. Mol Cell Biol. 1995;15(3):1389–1397. PubMed PMC

Hartner JC, Schmittwolf C, Kispert A, et al. Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing Enzyme ADAR1. J Biol Chem. 2004;279(6):4894–4902. PubMed

Wang G, Wang H, Singh S, et al. ADAR1 prevents liver injury from inflammation and suppresses interferon production in hepatocytes. Am J Pathol. 2015;185(12):3224–3237. PubMed PMC

Ben-Shoshan SO, Kagan P, Sultan M, et al. ADAR1 deletion induces NF κ B and interferon signaling dependent liver inflammation and fibrosis. RNA Biol. 2017;14(5):587–602. PubMed PMC

Chalk AM, Taylor S, Heraud-Farlow JE, et al. The majority of A-to-I RNA editing is not required for mammalian homeostasis. Genome Biol. 2019;20(1):268. PubMed PMC

Marek-Trzonkowska N, Piekarska K, Filipowicz N, et al. Mild hypothermia provides Treg stability. Sci Rep. 2017;7(1):11915. PubMed PMC

Sinigaglia K, Wiatrek D, Khan A, et al. ADAR RNA editing in innate immune response phasing, in circadian clocks and in sleep. Biochim Biophys Acta - Genet Regul Mech. 2019;1862(3):356–369. PubMed

Hartner JC, Walkley CR, Lu J, et al. ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling. Nat Immunol. 2009;10(1):109–115. PubMed PMC

Gannon HS, Zou T, Kiessling MK, et al. Identification of ADAR1 adenosine deaminase dependency in a subset of cancer cells. Nat Commun. 2018;9(1):5450. PubMed PMC

Rice GI, Kasher PR, Forte GMA, et al. Mutations in ADAR1 cause Aicardi-Goutières syndrome associated with a type I interferon signature. Nat Genet. 2012;44(11):1243–1248. PubMed PMC

Uggenti C, Lepelley A, Crow YJ. Self-Awareness: nucleic Acid–Driven Inflammation and the Type I Interferonopathies. Annu Rev Immunol. 2019;37(1):247–267. PubMed

Liddicoat BJ, Hartner JC, Piskol R, et al. Adenosine-to-inosine RNA editing by ADAR1 is essential for normal murine erythropoiesis. Exp. Hematol. 2016;44(10):947–963. PubMed PMC

Zipeto MA, Court AC, Sadarangani A, et al. ADAR1 activation drives leukemia stem cell self-renewal by impairing let-7 biogenesis. Cell Stem Cell. 2016;19(2):177–191. PubMed PMC

Higuchi M, Single FN, Köhler M, et al. RNA editing of AMPA receptor subunit GluR-B: A base-paired intron-exon structure determines position and efficiency. Cell. 1993;75(7):1361–1370. PubMed

Higuchi M, Maas S, Single FN, et al. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature. 2000;406(6791):78–81. PubMed

Sommer B, Köhler M, Sprengel R, et al. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell. 1991;67(1):11–19. PubMed

Lomeli H, Mosbacher J, Melcher T, et al. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science. 1994;266(5191):1709–1713. PubMed

Eisenberg E, Levanon EY. A-to-I RNA editing - Immune protector and transcriptome diversifier. Nat Rev Genet. 2018;19(8):473–490. PubMed

Lee S, Yang G, Yong Y, et al. ADAR2-dependent RNA editing of GluR2 is involved in thiamine deficiency-induced alteration of calcium dynamics. Mol. Neurodegener. 2010;5(1):1–13. PubMed PMC

Danie C, Wahlstedt H, Ohlson J, et al. RNA editing affects trafficking of the γ-aminobutyric acid type A (GABAA) receptor. J Biol Chem. 2011;286(3):2031–2040. PubMed PMC

Hoopengardner B, Bhalla T, Staber C, et al. Nervous system targets of RNA editing identified by comparative genomics. Science. 2003;301(5634):832–836. PubMed

Bhalla T, Rosenthal JJC, Holmgren M, et al. Control of human potassium channel inactivation by editing of a small mRNA hairpin. Nat Struct Mol Biol. 2004;11(10):950–956. PubMed

Ganem NS, Ben-Asher N, Lamm AT. In cancer, A-to-I RNA editing can be the driver, the passenger, or the mechanic. Drug Resist. Updat. 2017;32:16–22. PubMed

Stefl R, Xu M, Skrisovska L, et al. Structure and specific RNA binding of ADAR2 double-stranded RNA binding motifs. Structure. 2006;14(2):345–355. PubMed

Tomaselli S,  Bonamassa B, Alisi A, et al. ADAR enzyme and miRNA story: A nucleotide that can make the difference. Int J Mol Sci. 2013;14(11):22796–22816. PubMed PMC

Ward SV, Markle D, Das S, et al. The promoter-proximal KCS element of the PKR kinase gene enhances transcription irrespective of orientation and position relative to the ISRE element and is functionally distinct from the KCS-like element of the ADAR deaminase promoter. J Interf Cytokine Res. 2002;22(8):891–898. PubMed

Melcher T, Maas S, Herb A, et al. RED2, a Brain-specific Member of the RNA-specific Adenosine Deaminase Family. J Biol Chem. 1996;271(50):31795–31798. PubMed

Brown BA, Lowenhaupt K, Wilbert CM, et al. Zα domain of the editing enzyme dsRNA adenosine deaminase binds left-handed Z-RNA as well as Z-DNA. Proc Natl Acad Sci U S A. 2000;97(25):13532–13536. PubMed PMC

Licht K,  Hartl M, Amman F, et al. Inosine induces context-dependent recoding and translational stalling. Nucleic Acids Res. 2019;47(1):3–14. PubMed PMC

Kim DDY. Widespread RNA editing of embedded Alu elements in the human transcriptome. Genome Res. 2004;14(9):1719–1725. PubMed PMC

Athanasiadis A, Rich A, Maas S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol. 2004;2(12): e391. PubMed PMC

Chung H, Calis JJA, Wu X, et al. Human ADAR1 prevents endogenous RNA from triggering translational shutdown. Cell. 2018;172(4):811–824.e14. PubMed PMC

Hiscott J. Triggering the innate antiviral response through IRF-3 activation. J Biol Chem. 2007;282(21):15325–15329. PubMed

Vitali P, Scadden ADJ. Double-stranded RNAs containing multiple IU pairs are sufficient to suppress interferon induction and apoptosis. Nat Struct Mol Biol. 2010;17(9):1043–1050. PubMed PMC

Sakurai M, Yano T, Kawabata H, et al. Inosine cyanoethylation identifies A-to-I RNA editing sites in the human transcriptome. Nat Chem Biol. 2010;6(10):733–740. PubMed

Lev-Maor G, Sorek R, Levanon EY, et al. RNA-editing-mediated exon evolution. Genome Biol. 2007;8(2):R29. PubMed PMC

Pan B. Crystal structure of an RNA octamer duplex r(CCCIUGGG)2 incorporating tandem I.U wobbles. Nucleic Acids Res. 1998;26(24):5699–5706. PubMed PMC

Morita Y, Shibutani T, Nakanishi N, et al. Human endonuclease V is a ribonuclease specific for inosine-containing RNA. Nat Commun. 2013;4(1):2273. PubMed PMC

Scadden ADJ. The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nat Struct Mol Biol. 2005;12(6):489–496. PubMed

Scadden ADJ. Specific cleavage of hyper-edited dsRNAs. Embo J. 2001;20(15):4243–4252. PubMed PMC

Lehmann KA, Bass BL. The importance of internal loops within RNA substrates of ADAR1. J Mol Biol. 1999;291(1):1–13. PubMed

Thomas JM, Beal PA. How do ADARs bind RNA? New protein-RNA structures illuminate substrate recognition by the RNA editing ADARs. BioEssays. 2017;39(4):1600187. PubMed PMC

Eggington JM, Greene T, Bass BL. Predicting sites of ADAR editing in double-stranded RNA. Nat Commun. 2011;2(1):1–9. PubMed PMC

Wong SK, Sato S, Lazinski DW. Substrate recognition by ADAR1 and ADAR2. Rna. 2001;7(6):846–858. PubMed PMC

Bartel DP. Metazoan MicroRNAs. Cell. 2018;173(1):20–51. PubMed PMC

Kawahara Y, Megraw M, Kreider E, et al. Frequency and fate of microRNA editing in human brain. Nucleic Acids Res. 2008;36(16):5270–5280. PubMed PMC

Shoshan E, Mobley AK, Braeuer RR, et al. Reduced adenosine-to-inosine miR-455-5p editing promotes melanoma growth and metastasis. Nat Cell Bio. 2015;17(3):311–321. PubMed PMC

Kawahara Y, Zinshteyn B, Sethupathy P, et al. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science. 2007;315(5815):1137–1140. PubMed PMC

Navaratnam N, Bhattacharya S, Fujino T, et al. Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA-binding motif at its active site. Cell. 1995;81:(2):187-95. PubMed

Blanc V, Davidson NO. APOBEC-1-mediated RNA editing. Wiley Interdiscip. Rev. Syst. Biol. Med. 2010;2(5):594–602. PubMed PMC

Sharma S, Patnaik SK, Thomas Taggart R, et al. APOBEC3A cytidine deaminase induces RNA editing in monocytes and macrophages. Nat Commun. 2015;6(1):1–15. PubMed PMC

Sharma S, Patnaik SK, Taggart RT, et al. The double-domain cytidine deaminase APOBEC3G is a cellular site-specific RNA editing enzyme. Sci Rep. 2016;6:1–12. PubMed PMC

Patnaik SK, Kannisto E . APOBEC3B is a new RNA editing enzyme . in Proceedings of the RNA 2016, Annual Meeting of RNA Society, Kyoto, Japan. 28 June–2 July 2016 (2016).

Moris A, Murray S, Cardinaud S. AID and APOBECs span the gap between innate and adaptive immunity. Front Microbiol. 2014;5:1–13. PubMed PMC

Roberts SA,  Lawrence MS, Klimczak LJ, et al. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet. 2013;45(9):970–976. PubMed PMC

Swanton C, McGranahan N, Starrett GJ, et al. Mutagenic fuel for cancer evolution and heterogeneity. Cancer Discov. 2015;5(7):704–712. PubMed PMC

Chan K, Roberts SA, Klimczak LJ, et al. An APOBEC3A hypermutation signature is distinguishable from the signature of background mutagenesis by APOBEC3B in human cancers. Nat Genet. 2015;47(9):1067–1072. PubMed PMC

Burns MB,  Lackey L, Carpenter MA, et al. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature. 2013;494(7437):366–370. PubMed PMC

Knisbacher BA, Gerber D, Levanon EYDNA. Editing by APOBECs: A genomic preserver and transformer. Trends Genet. 2016;32(1):16–28. PubMed

Davidson NO, Shelness GS. A POLIPOPROTEIN B: mRNA editing, lipoprotein assembly, and presecretory degradation. Annu Rev Nutr. 2000;20(1):169–193. PubMed

Prohaska KM, Bennett RP, Salter JD, et al. The multifaceted roles of RNA binding in APOBEC cytidine deaminase functions. Wiley Interdiscip Rev RNA. 2014;5(4):493–508. PubMed PMC

Sharma S, Patnaik SK, Kemer Z, et al. Transient overexpression of exogenous APOBEC3A causes C-to-U RNA editing of thousands of genes. RNA Biol. 2017;14(5):603–610. PubMed PMC

Sharma S, Wang J, Alqassim E, et al. Mitochondrial hypoxic stress induces widespread RNA editing by APOBEC3G in natural killer cells. Genome Biol. 2019;20(1):1–17. PubMed PMC

Takeda E, Tsuji-Kawahara S, Sakamoto M, et al. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo. J Virol. 2008;82(22):10998–11008. PubMed PMC

Li JB,  Levanon EY, Yoon J-K, et al. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science.2009;324(5931):1210–1213. PubMed

Porath HT, Carmi S, Levanon EY. A genome-wide map of hyper-edited RNA reveals numerous new sites. Nat Commun. 2014;5(1):4726. PubMed PMC

Chieca M, Torrini S, Conticello SG. Live-cell quantification of APOBEC1-mediated RNA editing: a comparison of RNA EDITING Assays. in Encyclopedia of Biological Chemistry: Second Edition. 2021;69–81. DOI:10.1007/978-1-0716-0787-9_5. PubMed DOI

Jalili P, Bowen D, Langenbucher A, et al. Quantification of ongoing APOBEC3A activity in tumor cells by monitoring RNA editing at hotspots. Nat Commun. 2020;11(1):2971. PubMed PMC

Kiran A, Baranov PV. DARNED: a DAtabase of RNa EDiting in humans. Bioinformatics. 2010;26(14):1772–1776. PubMed

Ramaswami G, Li JB. RADAR: A rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res. 2014;42(D1):109–113. PubMed PMC

Picardi E, Regina TMR, Brennicke A, et al. REDIdb: the RNA editing database. Nucleic Acids Res. 2007;35:D173–D177. PubMed PMC

Picardi E, D’Erchia AM, Lo Giudice C, et al. REDIportal: a comprehensive database of A-to-I RNA editing events in humans. Nucleic Acids Res. 2017;45(D1):D750–D757. PubMed PMC

Beghini A, Ripamonti CB, Peterlongo P, et al. RNA hyperediting and alternative splicing of hematopoietic cell phosphatase (PTPN6) gene in acute myeloid leukemia. Hum Mol Genet. 2000;9(15):2297–2304. PubMed

Han L, Diao L, Yu S, et al. The genomic landscape and clinical relevance of A-to-I RNA editing in human cancers. Cancer Cell. 2015;28(4):515–528. PubMed PMC

Zhang L, Yang C-S, Varelas X, et al. RNA editing in 3′ UTR perturbs microRNA-mediated regulation of oncogenes and tumor-suppressors. Sci Rep. 2016;6(1):23226. PubMed PMC

Baysal BE, Sharma S, Hashemikhabir S, et al. Editing in pathogenesis of cancer. Cancer Res. 2017;77(14):3733–3739. PubMed

Paz-Yaacov N, Bazak L, Buchumenski I, et al. Elevated RNA editing activity is a major contributor to transcriptomic diversity in tumors. Cell Rep. 2015;13(2):267–276. PubMed

Anadón C, Guil S, Simó-Riudalbas L, et al. Gene amplification-associated overexpression of the RNA editing enzyme ADAR1 enhances human lung tumorigenesis. Oncogene. 2016;35(33):4407–4413. PubMed PMC

Teoh PJ, An O, Chung TH, et al. Aberrant hyperediting of the myeloma transcriptome by ADAR1 confers oncogenicity and is a marker of poor prognosis. Blood. 2018;132(12):1304–1317. PubMed

Qin Y-R, Qiao J-J, Chan THM, et al. Adenosine-to-Inosine RNA editing mediated by ADARs in esophageal squamous cell carcinoma. Cancer Res. 2014;74(3):840–851. PubMed

Chen W,  He W, Cai H, et al. A-to-I RNA editing of BLCAP lost the inhibition to STAT3 activation in cervical cancer. Oncotarget. 2017;8(24):39417–39429. PubMed PMC

Galeano F, Leroy A, Rossetti C, et al. Human BLCAP transcript: new editing events in normal and cancerous tissues. Int J Cancer. 2010;127(1):127–137. PubMed PMC

Fritzell K, Xu L-D, Lagergren J, et al. ADARs and editing: the role of A-to-I RNA modification in cancer progression. Seminars in Cell & Developmental Biology. 2018;79: 123–130. PubMed

Ishiuchi S,  Tsuzuki K, Yoshida Y, et al. Blockage of Ca2+-permeable AMPA receptors suppresses migration and induces apoptosis in human glioblastoma cells. Nat Med. 2002;8(9):971–978. PubMed

Maas S, Patt S, Schrey M, et al. Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc Natl Acad Sci. 2001;98(25):14687–14692. PubMed PMC

Ishiuchi S, Yoshida Y, Sugawara K, et al. Ca2+-Permeable AMPA receptors regulate growth of human glioblastoma via akt activation. J Neurosci. 2007;27(30):7987–8001. PubMed PMC

Galeano F, Rossetti C, Tomaselli S, et al. ADAR2-editing activity inhibits glioblastoma growth through the modulation of the CDC14B/Skp2/p21/p27 axis. Oncogene. 2013;32(8):998–1009. PubMed PMC

Salameh A,  Lee AK, Cardó-Vila M, et al. PRUNE2 is a human prostate cancer suppressor regulated by the intronic long noncoding RNA PCA3. Proc Natl Acad Sci. 2015;112(27):8403–8408. PubMed PMC

Yamanaka S, Poksay KS, Arnold KS, et al. A novel translational repressor mRNA is edited extensively in livers containing tumors caused by the transgene expression of the apoB mRNA-editing enzyme. Genes Dev. 1997;11(3):321–333. PubMed

Chen L, Li Y, Lin CH, et al. Recoding RNA editing of AZIN1 predisposes to hepatocellular carcinoma. Nat Med. 2013;19(2):209–216. PubMed PMC

Anant S, Davidson NO, An AU, et al. UUUN[A/U]U) downstream of the edited C in apolipoprotein B mRNA is a high-affinity binding site for apobec-1: binding of apobec-1 to this motif in the 3ʹ untranslated region of c-myc increases mRNA stability. Mol Cell Biol. 2000;20(6):1982–1992. PubMed PMC

Mukhopadhyay D,  Anant S, Lee RM, et al. C→U editing of neurofibromatosis 1 mRNA occurs in tumors that express both the type II transcript and apobec-1, the catalytic subunit of the apolipoprotein B mRNA-editing enzyme. Am J Hum Genet. 2002;70(1):38–50. PubMed PMC

Cappione AJ, French BL, Skuse GR. A potential role for NF1 mRNA editing in the pathogenesis of NF1 tumors. Am J Hum Genet. 1997;60(2):305–312. PubMed PMC

Skuse GR, Cappione AJ, Sowden M, et al. The neurofibromatosis type I messenger RNA undergoes base-modification RNA editing. Nucleic Acids Res. 1996;24(3):478–486. PubMed PMC

Chan THM, Lin CH, Qi L, et al. A disrupted RNA editing balance mediated by ADARs (Adenosine DeAminases that act on RNA) in human hepatocellular carcinoma. Gut. 2014;63(5):832–843. PubMed PMC

Han S-W,  Kim H-P, Shin J-Y, et al. RNA editing in RHOQ promotes invasion potential in colorectal cancer. J Exp Med. 2014;211(4):613–621. PubMed PMC

Chen Y-B,  Liao X-Y, Zhang J-B, et al. ADAR2 functions as a tumor suppressor via editing IGFBP7 in esophageal squamous cell carcinoma. Int J Oncol. 2017;50(2):622–630. PubMed PMC

Tomaselli S,  Galeano F, Alon S, et al. Modulation of microRNA editing, expression and processing by ADAR2 deaminase in glioblastoma. Genome Biol. 2015;16(1):5. PubMed PMC

Fumagalli D, Gacquer D, Rothé F, et al. Principles Governing A-to-I RNA Editing in the Breast Cancer Transcriptome. Cell Rep. 2015;13(2):277–289. PubMed PMC

Shigeyasu K, Okugawa Y, Toden S, et al. AZIN1 RNA editing confers cancer stemness and enhances oncogenic potential in colorectal cancer. JCI Insight. 2018;3(12):e99976. PubMed PMC

Hu X, Chen J, Shi X, et al. RNA editing of AZIN1 induces the malignant progression of non-small-cell lung cancers. Tumor Biol. 2017;39(8):1010428317700001. PubMed

Lazzari E, Mondala PK, Santos ND, et al. Alu-dependent RNA editing of GLI1 promotes malignant regeneration in multiple myeloma. Nat Commun. 2017;8(1):1922. PubMed PMC

Shimokawa T,  Rahman MF-U, Tostar U, et al. RNA editing of the GLI1 transcription factor modulates the output of Hedgehog signaling. RNA Biol. 2013;10(2):321–333. PubMed PMC

Yao J, Duan L, Fan M, et al. Overexpression of BLCAP induces S phase arrest and apoptosis independent of p53 and NF-κB in human tongue carcinoma. Mol Cell Biochem. 2007;297(1-2):81–92. PubMed

Hu X,  Wan S, Ou Y, et al. RNA over-editing of BLCAP contributes to hepatocarcinogenesis identified by whole-genome and transcriptome sequencing. Cancer Lett. 2015;357(2):510–519. PubMed

Clutterbuck DR, Leroy A, O’Connell MA, et al. A bioinformatic screen for novel A-I RNA editing sites reveals recoding editing in BC10. Bioinformatics. 2005;21(11):2590–2595. PubMed

Rodier G, Coulombe P, Tanguay P-L, et al. Phosphorylation of Skp2 regulated by CDK2 and Cdc14B protects it from degradation by APCCdh1 in G1 phase. Embo J. 2008;27(4):679–691. PubMed PMC

Zhang F,  Qi Y, Zhou K, et al. The cAMP phosphodiesterase Prune localizes to the mitochondrial matrix and promotes mtDNA replication by stabilizing TFAM. EMBO Rep. 2015;16(4):520–527. PubMed PMC

Upadhyaya M, Cooper DN. Neurofibromatosis Type 1. 1st ed. Heidelberg: Springer-Verlag Berlin Heidelberg; 2012.

Sawyer GM, Clark AR, Robertson SP, et al. Disease-associated substitutions in the filamin B actin binding domain confer enhanced actin binding affinity in the absence of major structural disturbance: insights from the crystal structures of filamin B actin binding domains. J Mol Biol. 2009;390(5):1030–1047. PubMed

Zhang M, Fritsche J, Roszik J, et al. RNA editing derived epitopes function as cancer antigens to elicit immune responses. Nat Commun. 2018;9(1):3919. PubMed PMC

Asaoka M, Ishikawa T, Takabe K, et al. APOBEC3-mediated RNA editing in breast cancer is associated with heightened immune activity and improved survival. Int J Mol Sci. 2019;20(22): 5621. PubMed PMC

Gumireddy K,  Li A, Kossenkov A V, et al. The mRNA-edited form of GABRA3 suppresses GABRA3-mediated Akt activation and breast cancer metastasis. Nat Commun. 2016;7(1):10715. PubMed PMC

Nakano M, Fukami T, Gotoh S, et al. RNA editing up-regulates human dihydrofolate reductase in breast cancer. J Biol Chem. 2017;292(12):4873–4884. PubMed PMC

Fu L, Qin Y-R, Ming X-Y, et al. RNA editing of SLC22A3 drives early tumor invasion and metastasis in familial esophageal cancer. Proc Natl Acad Sci. 2017;114(23):E4631–E4640. PubMed PMC

Shelton PM, Duran A, Nakanishi Y, et al. The Secretion of miR-200s by a PKCζ/ADAR2 signaling axis promotes liver metastasis in colorectal cancer. Cell Rep. 2018;23(4):1178–1191. PubMed PMC

Amin EM, Lin Y, Su D, et al. The RNA-editing enzyme ADAR promotes lung adenocarcinoma migration and invasion by stabilizing FAK. Sci Signal. 2017;10(497): eaah3941. PubMed PMC

Velazquez-Torres G, Shoshan E, Ivan C, et al. A-to-I miR-378a-3p editing can prevent melanoma progression via regulation of PARVA expression. Nat Commun. 2018;9(1):461. PubMed PMC

Choudhury Y, Tay FC, Lam DH, et al. Attenuated adenosine-to-inosine editing of microRNA-376a* promotes invasiveness of glioblastoma cells. J Clin Invest. 2012;122(11):4059–4076. PubMed PMC

Cesarini V, Silvestris DA, Tassinari V, et al. ADAR2/miR-589-3p axis controls glioblastoma cell migration/invasion. Nucleic Acids Res. 2018;46(4):2045–2059. PubMed PMC

Ksiazkiewicz M, Markiewicz A, Zaczek AJ. Epithelial-mesenchymal transition: A hallmark in metastasis formation linking circulating tumor cells and cancer stem cells. Pathobiology. 2012;79(4):195–208. PubMed

Wang Y,  Xu X, Yu S, et al. Systematic characterization of A-to-I RNA editing hotspots in microRNAs across human cancers. Genome Res. 2017;27(7):1112–1125. PubMed PMC

Ramírez-Moya J, Baker AR, Slack FJ, et al. ADAR1-mediated RNA editing is a novel oncogenic process in thyroid cancer and regulates miR-200 activity. Oncogene. 2020. DOI:10.1038/s41388-020-1248-x. PubMed DOI PMC

Sagredo EA,  Blanco A, Sagredo AI, et al. ADAR1-mediated RNA-editing of 3′UTRs in breast cancer. Biol. Res. 2018;51(1):36. PubMed PMC

Schaller MD. Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci. 2010;123(7):1007–1013. PubMed

Sizemore S, Cicek M, Sizemore N, et al. Podocalyxin increases the aggressive phenotype of breast and prostate cancer cells in vitro through its interaction with ezrin. Cancer Res. 2007;67(13):6183–6191. PubMed

Chan THM, Qamra A, Tan KT, et al. ADAR-Mediated RNA editing predicts progression and prognosis of gastric cancer. Gastroenterology. 2016;151(4):637–650.e10. PubMed PMC

Song Y, An O, Ren X, et al. RNA editing mediates the functional switch of COPA in a novel mechanism of hepatocarcinogenesis. J Hepatol. 2020. DOI:10.1016/j.jhep.2020.07.021. PubMed DOI

Watkin LB, Jessen B, Wiszniewski W, et al. COPA mutations impair ER-Golgi transport and cause hereditary autoimmune-mediated lung disease and arthritis. Nat Genet. 2015;47(6):654–660. PubMed PMC

Chen S, Habib G, Yang C, et al. Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science. 1987;238(4825):363–366. PubMed

Powell LM, Wallis SC, Pease RJ, et al. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell. 1987;50(6):831–840. PubMed

Paz N, Levanon EY, Amariglio N, et al. Altered adenosine-to-inosine RNA editing in human cancer. Genome Res. 2007;17(11):1586–1595. PubMed PMC

Paul D, Sinha AN, Ray A, et al. A-to-I editing in human miRNAs is enriched in seed sequence, influenced by sequence contexts and significantly hypoedited in glioblastoma multiforme. Sci Rep. 2017;7(1):2466. PubMed PMC

Ishizuka JJ, Manguso RT, Cheruiyot CK, et al. Loss of ADAR1 in tumours overcomes resistance to immune checkpoint blockade. Nature. 2019;565(7737):43–48. PubMed PMC

Liu H, Golji J, Brodeur LK, et al. Tumor-derived IFN triggers chronic pathway agonism and sensitivity to ADAR loss. Nat Med. 2019;25(1):95–102. PubMed

Mehdipour P, Marhon SA, Ettayebi I, et al. Epigenetic therapy induces transcription of inverted SINEs and ADAR1 dependency. Nature. 2020. DOI:10.1038/s41586-020-2844-1. PubMed DOI

Wo Tsui H, Siminovitch KA, de Souza L, et al. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat Genet. 1993;4(2):124–129. PubMed

Yi T, Ihle JN. Association of hematopoietic cell phosphatase with c-Kit after stimulation with c-Kit ligand. Mol Cell Biol. 1993;13(6):3350–3358. PubMed PMC

Dong X, Chen G, Cai Z, et al. CDK13 RNA over-editing mediated by ADAR1 associates with poor prognosis of hepatocellular carcinoma patients. Cell Physiol Biochem. 2018;47(6):2602–2612. PubMed

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