Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Journal of Hematology & Oncology
Published in: Journal of Hematology & Oncology 1/2020

Open Access 01-12-2020 | Review

Principles and innovative technologies for decrypting noncoding RNAs: from discovery and functional prediction to clinical application

Authors: Yu-Meng Sun, Yue-Qin Chen

Published in: Journal of Hematology & Oncology | Issue 1/2020

Login to get access

Abstract

Noncoding RNAs (ncRNAs) are a large segment of the transcriptome that do not have apparent protein-coding roles, but they have been verified to play important roles in diverse biological processes, including disease pathogenesis. With the development of innovative technologies, an increasing number of novel ncRNAs have been uncovered; information about their prominent tissue-specific expression patterns, various interaction networks, and subcellular locations will undoubtedly enhance our understanding of their potential functions. Here, we summarized the principles and innovative methods for identifications of novel ncRNAs that have potential functional roles in cancer biology. Moreover, this review also provides alternative ncRNA databases based on high-throughput sequencing or experimental validation, and it briefly describes the current strategy for the clinical translation of cancer-associated ncRNAs to be used in diagnosis.
Literature
1.
Warner, Soeiro R, Birnboim HC, Girard M, Darnell JE. Rapidly labeled HeLa cell nuclear RNA. I. Identification by zone sedimentation of a heterogeneous fraction separate from ribosomal precursor RNA. J Mol Biol. 1966;19:349–61.PubMed
2.
Weinberg RA, Penman S. Small molecular weight monodisperse nuclear RNA. J Mol Biol. 1968;38:289–304.PubMed
3.
Zieve G, Penman S. Small RNA species of the HeLa cell: metabolism and subcellular localization. Cell. 1976;8:19–31.PubMed
4.
Eddy SR. Non-coding RNA genes and the modern RNA world. Nat Rev Genet. 2001;2:919–29.PubMed
5.
Pachnis V, Brannan CI, Tilghman SM. The structure and expression of a novel gene activated in early mouse embryogenesis. EMBO J. 1988;7:673–81.PubMedPubMedCentral
6.
Quinn JJ, Chang HY. Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2016;17:47–62.PubMed
7.
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333–8.PubMed
8.
Li X, Yang L, Chen LL. The biogenesis, functions, and challenges of circular RNAs. Mol Cell. 2018;71:428–42.PubMed
9.
Schimmel P. The emerging complexity of the tRNA world: mammalian tRNAs beyond protein synthesis. Nat Rev Mol Cell Biol. 2018;19:45–58.PubMed
10.
Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, et al. A human snoRNA with microRNA-like functions. Mol Cell. 2008;32:519–28.PubMed
11.
Lambert M, Benmoussa A, Provost P. Small non-coding RNAs derived from eukaryotic ribosomal RNA. Noncoding RNA. 2019;5:16.PubMedCentral
12.
13.
Huarte M. The emerging role of lncRNAs in cancer. Nat Med. 2015;21:1253–61.PubMed
14.
Dong Y, He D, Peng Z, Peng W, Shi W, Wang J, et al. Circular RNAs in cancer: an emerging key player. J Hematol Oncol. 2017;10:2.PubMedPubMedCentral
15.
Pekarsky Y, Balatti V, Palamarchuk A, Rizzotto L, Veneziano D, Nigita G, et al. Dysregulation of a family of short noncoding RNAs, tsRNAs, in human cancer. Proc Natl Acad Sci U S A. 2016;113:5071–6.PubMedPubMedCentral
16.
Li Y, Zeng C, Hu J, Pan Y, Shan Y, Liu B, et al. Long non-coding RNA-SNHG7 acts as a target of miR-34a to increase GALNT7 level and regulate PI3K/Akt/mTOR pathway in colorectal cancer progression. J Hematol Oncol. 2018;11:89.PubMedPubMedCentral
17.
Fort RS, Matho C, Oliveira-Rizzo C, Garat B, Sotelo-Silveira JR, Duhagon MA. An integrated view of the role of miR-130b/301b miRNA cluster in prostate cancer. Exp Hematol Oncol. 2018;7:10.PubMedPubMedCentral
18.
Basati G, Khaksarian M, Abbaszadeh S, Lashgarian HE, Marzban A. Cancer stem cells and nanotechnological approaches for eradication. Stem Cell Investig. 2019;6:38.PubMedPubMedCentral
19.
Wang WT, Chen TQ, Zeng ZC, Pan Q, Huang W, Han C, et al. The lncRNA LAMP5-AS1 drives leukemia cell stemness by directly modulating DOT1L methyltransferase activity in MLL leukemia. J Hematol Oncol. 2020;13:78.PubMedPubMedCentral
20.
Wang WT, Han C, Sun YM, Chen TQ, Chen YQ. Noncoding RNAs in cancer therapy resistance and targeted drug development. J Hematol Oncol. 2019;12:55.PubMedPubMedCentral
21.
22.
Rastgoo N, Abdi J, Hou J, Chang H. Role of epigenetics-microRNA axis in drug resistance of multiple myeloma. J Hematol Oncol. 2017;10:121.PubMedPubMedCentral
23.
Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, et al. The transcriptional landscape of the mammalian genome. Science. 2005;309:1559–63.PubMed
24.
Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, et al. Landscape of transcription in human cells. Nature. 2012;489:101–8.PubMedPubMedCentral
25.
Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science. 2007;316:1484–8.PubMed
26.
Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705.PubMed
27.
Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129:823–37.PubMed
28.
Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448:553–60.PubMedPubMedCentral
29.
Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009;459:108–12.PubMedPubMedCentral
30.
Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458:223–7.PubMedPubMedCentral
31.
Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009;106:11667–72.PubMedPubMedCentral
32.
Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol. 2010;28:503–10.PubMedPubMedCentral
33.
De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, et al. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. 2010;8:e1000384.PubMedPubMedCentral
34.
Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, Blobel GA, et al. Activating RNAs associate with mediator to enhance chromatin architecture and transcription. Nature. 2013;494:497–501.PubMedPubMedCentral
35.
Jiao W, Chen Y, Song H, Li D, Mei H, Yang F, et al. HPSE enhancer RNA promotes cancer progression through driving chromatin looping and regulating hnRNPU/p300/EGR1/HPSE axis. Oncogene. 2018;37:2728–45.PubMed
36.
Li S, Xu Z, Sheng J. tRNA-derived small RNA: a novel regulatory small non-coding RNA. Genes (Basel). 2018, 9:246.
37.
38.
Danan M, Schwartz S, Edelheit S, Sorek R. Transcriptome-wide discovery of circular RNAs in archaea. Nucleic Acids Res. 2012;40:3131–42.PubMed
39.
Chen LL. The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Biol. 2016;17:205–11.PubMed
40.
41.
42.
Yin QF, Yang L, Zhang Y, Xiang JF, Wu YW, Carmichael GG, et al. Long noncoding RNAs with snoRNA ends. Mol Cell. 2012;48:219–30.PubMed
43.
Dinger ME, Pang KC, Mercer TR, Mattick JS. Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol. 2008;4:e1000176.PubMedPubMedCentral
44.
Anderson DM, Anderson KM, Chang CL, Makarewich CA, Nelson BR, McAnally JR, et al. A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell. 2015;160:595–606.PubMedPubMedCentral
45.
Huang JZ, Chen M, Chen D, Gao XC, Zhu S, Huang H, et al. A peptide encoded by a putative lncRNA HOXB-AS3 suppresses colon cancer growth. Mol Cell. 2017;68:171–84.PubMed
46.
Pamudurti NR, Bartok O, Jens M, Ashwal-Fluss R, Stottmeister C, Ruhe L, et al. Translation of CircRNAs. Mol Cell. 2017;66:9–21.PubMedPubMedCentral
47.
Zhang M, Zhao K, Xu X, Yang Y, Yan S, Wei P, et al. A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma. Nat Commun. 2018;9:4475.PubMedPubMedCentral
48.
Brannan CI, Dees EC, Ingram RS, Tilghman SM. The product of the H19 gene may function as an RNA. Mol Cell Biol. 1990;10:28–36.PubMedPubMedCentral
49.
Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, et al. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell. 1992;71:515–26.PubMed
50.
Novikova IV, Hennelly SP, Sanbonmatsu KY. Structural architecture of the human long non-coding RNA, steroid receptor RNA activator. Nucleic Acids Res. 2012;40:5034–51.PubMedPubMedCentral
51.
Duret L, Chureau C, Samain S, Weissenbach J, Avner P. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science. 2006;312:1653–5.PubMed
52.
Lin MF, Jungreis I, Kellis M. PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics. 2011;27:i275–82.PubMedPubMedCentral
53.
Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013;41:e74.PubMedPubMedCentral
54.
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019;47:D427–32.PubMed
55.
Malone B, Atanassov I, Aeschimann F, Li X, Grosshans H, Dieterich C. Bayesian prediction of RNA translation from ribosome profiling. Nucleic Acids Res. 2017;45:2960–72.PubMedPubMedCentral
56.
Mockler TC, Chan S, Sundaresan A, Chen H, Jacobsen SE, Ecker JR. Applications of DNA tiling arrays for whole-genome analysis. Genomics. 2005;85:1–15.PubMed
57.
Yan B, Wang ZH, Guo JT. The research strategies for probing the function of long noncoding RNAs. Genomics. 2012;99:76–80.PubMed
58.
59.
Mercer TR, Gerhardt DJ, Dinger ME, Crawford J, Trapnell C, Jeddeloh JA, et al. Targeted RNA sequencing reveals the deep complexity of the human transcriptome. Nat Biotechnol. 2011;30:99–104.PubMedPubMedCentral
60.
Ramskold D, Luo S, Wang YC, Li R, Deng Q, Faridani OR, et al. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat Biotechnol. 2012;30:777–82.PubMedPubMedCentral
61.
Bhargava V, Ko P, Willems E, Mercola M, Subramaniam S. Quantitative transcriptomics using designed primer-based amplification. Sci Rep. 2013;3:1740.PubMedPubMedCentral
62.
Sasagawa Y, Nikaido I, Hayashi T, Danno H, Uno KD, Imai T, et al. Quartz-Seq: a highly reproducible and sensitive single-cell RNA sequencing method, reveals non-genetic gene-expression heterogeneity. Genome Biol. 2013;14:R31.PubMedPubMedCentral
63.
Fan X, Zhang X, Wu X, Guo H, Hu Y, Tang F, et al. Single-cell RNA-seq transcriptome analysis of linear and circular RNAs in mouse preimplantation embryos. Genome Biol. 2015;16:148.PubMedPubMedCentral
64.
Hayashi T, Ozaki H, Sasagawa Y, Umeda M, Danno H, Nikaido I. Single-cell full-length total RNA sequencing uncovers dynamics of recursive splicing and enhancer RNAs. Nat Commun. 2018;9:619.PubMedPubMedCentral
65.
Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401–14.PubMedPubMedCentral
66.
Hagemann-Jensen M, Abdullayev I, Sandberg R, Faridani OR. Small-seq for single-cell small-RNA sequencing. Nat Protoc. 2018;13:2407–24.PubMed
67.
Core LJ, Waterfall JJ, Lis JT. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science. 2008;322:1845–8.PubMedPubMedCentral
68.
Herzog VA, Reichholf B, Neumann T, Rescheneder P, Bhat P, Burkard TR, et al. Thiol-linked alkylation of RNA to assess expression dynamics. Nat Methods. 2017;14:1198–204.PubMedPubMedCentral
69.
Schofield JA, Duffy EE, Kiefer L, Sullivan MC, Simon MD. TimeLapse-seq: adding a temporal dimension to RNA sequencing through nucleoside recoding. Nat Methods. 2018;15:221–5.PubMedPubMedCentral
70.
Chen Y, Wu F, Chen Z, He Z, Wei Q, Zeng W, et al. Acrylonitrile-mediated nascent RNA sequencing for transcriptome-wide profiling of cellular RNA dynamics. Adv Sci (Weinh). 2020;7:1900997.PubMedCentral
71.
Li X, Zhou B, Chen L, Gou LT, Li H, Fu XD. GRID-seq reveals the global RNA-chromatin interactome. Nat Biotechnol. 2017;35:940–50.PubMedPubMedCentral
72.
Yan Z, Huang N, Wu W, Chen W, Jiang Y, Chen J, et al. Genome-wide colocalization of RNA-DNA interactions and fusion RNA pairs. Proc Natl Acad Sci U S A. 2019;116:3328–37.PubMedPubMedCentral
73.
Bell JC, Jukam D, Teran NA, Risca VI, Smith OK, Johnson WL, et al. Chromatin-associated RNA sequencing (ChAR-seq) maps genome-wide RNA-to-DNA contacts. Elife. 2018;7:e27024.PubMedPubMedCentral
74.
Kudla G, Granneman S, Hahn D, Beggs JD, Tollervey D. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc Natl Acad Sci U S A. 2011;108:10010–5.PubMedPubMedCentral
75.
Metkar M, Ozadam H, Lajoie BR, Imakaev M, Mirny LA, Dekker J, et al. Higher-order organization principles of pre-translational mRNPs. Mol Cell. 2018;72:715–26.PubMedPubMedCentral
76.
Nguyen TC, Cao X, Yu P, Xiao S, Lu J, Biase FH, et al. Mapping RNA-RNA interactome and RNA structure in vivo by MARIO. Nat Commun. 2016;7:12023.PubMedPubMedCentral
77.
Lu Z, Zhang QC, Lee B, Flynn RA, Smith MA, Robinson JT, et al. RNA duplex map in living cells reveals higher-order transcriptome structure. Cell. 2016;165:1267–79.PubMedPubMedCentral
78.
Sharma E, Sterne-Weiler T, O’Hanlon D, Blencowe BJ. Global mapping of human RNA-RNA interactions. Mol Cell. 2016;62:618–26.PubMed
79.
Aw JG, Shen Y, Wilm A, Sun M, Lim XN, Boon KL, et al. In vivo mapping of eukaryotic RNA interactomes reveals principles of higher-order organization and regulation. Mol Cell. 2016;62:603–17.PubMed
80.
Cai Z, Cao C, Ji L, Ye R, Wang D, Xia C, et al. RIC-seq for global in situ profiling of RNA–RNA spatial interactions. Nature. 2020;582:432–7.PubMed
81.
Morf J, Wingett SW, Farabella I, Cairns J, Furlan-Magaril M, Jimenez-Garcia LF, et al. RNA proximity sequencing reveals the spatial organization of the transcriptome in the nucleus. Nat Biotechnol. 2019;37:793–802.PubMed
82.
Lee JH, Daugharthy ER, Scheiman J, Kalhor R, Ferrante TC, Terry R, et al. Fluorescent in situ sequencing (FISSEQ) of RNA for gene expression profiling in intact cells and tissues. Nat Protoc. 2015;10:442–58.PubMedPubMedCentral
83.
84.
Kaewsapsak P, Shechner DM, Mallard W, Rinn JL, Ting AY. Live-cell mapping of organelle-associated RNAs via proximity biotinylation combined with protein-RNA crosslinking. Elife. 2017;6:e29224.PubMedPubMedCentral
85.
Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell. 2017;66:22–37.PubMedPubMedCentral
86.
Diallo LH, Tatin F, David F, Godet AC, Zamora A, Prats AC, et al. How are circRNAs translated by non-canonical initiation mechanisms? Biochimie. 2019;164:45–52.PubMed
87.
Jiao Y, Meyerowitz EM. Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol Syst Biol. 2010;6:419.PubMedPubMedCentral
88.
Ingolia NT, Lareau LF, Weissman JS. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell. 2011;147:789–802.PubMedPubMedCentral
89.
Sun YM, Wang WT, Zeng ZC, Chen TQ, Han C, Pan Q, et al. circMYBL2, a circRNA from MYBL2, regulates FLT3 translation by recruiting PTBP1 to promote FLT3-ITD AML progression. Blood. 2019;134:1533–46.PubMedPubMedCentral
90.
Struhl K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol. 2007;14:103–5.PubMed
91.
Giambruno R, Mihailovich M, Bonaldi T. Mass spectrometry-based proteomics to unveil the non-coding RNA world. Front Mol Biosci. 2018;5:90.PubMedPubMedCentral
92.
Esteller M. Non-coding RNAs in human disease. Nat Rev Genet. 2011;12:861–74.PubMed
93.
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97.PubMed
94.
Elbashir SM, Lendeckel W, Tuschl T. RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev. 2001;15:188–200.PubMedPubMedCentral
95.
Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007;316:744–7.PubMed
96.
Taft RJ, Glazov EA, Cloonan N, Simons C, Stephen S, Faulkner GJ, et al. Tiny RNAs associated with transcription start sites in animals. Nat Genet. 2009;41:572–8.PubMed
97.
98.
99.
100.
Bachellerie JP, Cavaille J, Huttenhofer A. The expanding snoRNA world. Biochimie. 2002;84:775–90.PubMed
101.
Hamm J, Darzynkiewicz E, Tahara SM, Mattaj IW. The trimethylguanosine cap structure of U1 snRNA is a component of a bipartite nuclear targeting signal. Cell. 1990;62:569–77.PubMed
102.
103.
Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 2014;15:409.PubMedPubMedCentral
104.
Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-type specific features of circular RNA expression. PLoS Genet. 2013;9:e1003777.PubMedPubMedCentral
105.
Xing YH, Yao RW, Zhang Y, Guo CJ, Jiang S, Xu G, et al. SLERT regulates DDX21 rings associated with pol I transcription. Cell. 2017;169:664–78.PubMed
106.
Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, et al. An atlas of active enhancers across human cell types and tissues. Nature. 2014;507:455–61.PubMedPubMedCentral
107.
Selenko P, Sprangers R, Stier G, Buhler D, Fischer U, Sattler M. SMN tudor domain structure and its interaction with the Sm proteins. Nat Struct Biol. 2001;8:27–31.PubMed
108.
Dupuis-Sandoval F, Poirier M, Scott MS. The emerging landscape of small nucleolar RNAs in cell biology. Wiley Interdiscip Rev RNA. 2015;6:381–97.PubMedPubMedCentral
109.
Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P. Fast folding and comparison of RNA secondary structures. Monatshefte für Chemie/Chemical Monthly. 1994;125:167–88.
110.
Xu L, Sun L, Guan G, Huang Q, Lv J, Yan L, et al. The effects of pH and salts on nucleic acid partitioning during phenol extraction. Nucleosides Nucleotides Nucleic Acids. 2019;38:305–20.PubMed
111.
Nicosia A, Tagliavia M, Costa S. Regeneration of total RNA purification silica-based columns. Biomed Chromatogr. 2010;24:1263–4.PubMed
112.
Fromm B, Harris PD, Bachmann L. MicroRNA preparations from individual monogenean Gyrodactylus salaris-a comparison of six commercially available totalRNA extraction kits. BMC Res Notes. 2011;4:217.PubMedPubMedCentral
113.
Chen EA, Souaiaia T, Herstein JS, Evgrafov OV, Spitsyna VN, Rebolini DF, et al. Effect of RNA integrity on uniquely mapped reads in RNA-Seq. BMC Res Notes. 2014;7:753.PubMedPubMedCentral
114.
Veneziano D, Di Bella S, Nigita G, Lagana A, Ferro A, Croce CM. Noncoding RNA: current deep sequencing data analysis approaches and challenges. Hum Mutat. 2016;37:1283–98.PubMed
115.
Modrek B, Lee C. A genomic view of alternative splicing. Nat Genet. 2002;30:13–9.PubMed
116.
Zhang XO, Dong R, Zhang Y, Zhang JL, Luo Z, Zhang J, et al. Diverse alternative back-splicing and alternative splicing landscape of circular RNAs. Genome Res. 2016;26:1277–87.PubMedPubMedCentral
117.
Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L. Complementary sequence-mediated exon circularization. Cell. 2014;159:134–47.PubMed
118.
Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 2015;22:256–64.PubMed
119.
Vo JN, Cieslik M, Zhang Y, Shukla S, Xiao L, Zhang Y, et al. The landscape of circular RNA in cancer. Cell. 2019;176:869–81.PubMedPubMedCentral
120.
Guarnerio J, Bezzi M, Jeong JC, Paffenholz SV, Berry K, Naldini MM, et al. Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations. Cell. 2016;166:1055–6.PubMed
121.
Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol. 2005;15:331–41.PubMed
122.
Seto AG, Kingston RE, Lau NC. The coming of age for Piwi proteins. Mol Cell. 2007;26:603–9.PubMed
123.
Kedersha NL, Rome LH. Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J Cell Biol. 1986;103:699–709.PubMed
124.
van Zon A, Mossink MH, Schoester M, Scheffer GL, Scheper RJ, Sonneveld P, et al. Multiple human vault RNAs. Expression and association with the vault complex. J Biol Chem. 2001;276:37715–21.PubMed
125.
Kickhoefer VA, Searles RP, Kedersha NL, Garber ME, Johnson DL, Rome LH. Vault ribonucleoprotein particles from rat and bullfrog contain a related small RNA that is transcribed by RNA polymerase III. J Biol Chem. 1993;268:7868–73.PubMed
126.
Kiss-Laszlo Z, Henry Y, Bachellerie JP, Caizergues-Ferrer M, Kiss T. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell. 1996;85:1077–88.PubMed
127.
Mondal T, Rasmussen M, Pandey GK, Isaksson A, Kanduri C. Characterization of the RNA content of chromatin. Genome Res. 2010;20:899–907.PubMedPubMedCentral
128.
Schubert T, Pusch MC, Diermeier S, Benes V, Kremmer E, Imhof A, et al. Df31 protein and snoRNAs maintain accessible higher-order structures of chromatin. Mol Cell. 2012;48:434–44.PubMed
129.
Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007;129:1311–23.PubMedPubMedCentral
130.
Yazaki J, Gregory BD, Ecker JR. Mapping the genome landscape using tiling array technology. Curr Opin Plant Biol. 2007;10:534–42.PubMedPubMedCentral
131.
Quinn EM, Cormican P, Kenny EM, Hill M, Anney R, Gill M, et al. Development of strategies for SNP detection in RNA-seq data: application to lymphoblastoid cell lines and evaluation using 1000 genomes data. PLoS One. 2013;8:e58815.PubMedPubMedCentral
132.
Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, et al. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science. 2008;321:956–60.PubMed
133.
Edgren H, Murumagi A, Kangaspeska S, Nicorici D, Hongisto V, Kleivi K, et al. Identification of fusion genes in breast cancer by paired-end RNA-sequencing. Genome Biol. 2011;12:R6.PubMedPubMedCentral
134.
Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105–11.PubMedPubMedCentral
135.
Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011;25:1915–27.PubMedPubMedCentral
136.
Muller S, Rycak L, Winter P, Kahl G, Koch I, Rotter B. omiRas: a web server for differential expression analysis of miRNAs derived from small RNA-Seq data. Bioinformatics. 2013;29:2651–2.PubMed
137.
Han BW, Wang W, Zamore PD, Weng Z. piPipes: a set of pipelines for piRNA and transposon analysis via small RNA-seq, RNA-seq, degradome- and CAGE-seq, ChIP-seq and genomic DNA sequencing. Bioinformatics. 2015;31:593–5.PubMed
138.
Hoogstrate Y, Jenster G, Martens-Uzunova ES. FlaiMapper: computational annotation of small ncRNA-derived fragments using RNA-seq high-throughput data. Bioinformatics. 2015;31:665–73.PubMed
139.
140.
Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, et al. A survey of best practices for RNA-seq data analysis. Genome Biol. 2016;17:13.PubMedPubMedCentral
141.
Baker M. MicroRNA profiling: separating signal from noise. Nat Methods. 2010;7:687–92.PubMed
142.
Langenberger D, Bermudez-Santana C, Hertel J, Hoffmann S, Khaitovich P, Stadler PF. Evidence for human microRNA-offset RNAs in small RNA sequencing data. Bioinformatics. 2009;25:2298–301.PubMed
143.
Li Z, Ender C, Meister G, Moore PS, Chang Y, John B. Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res. 2012;40:6787–99.PubMedPubMedCentral
144.
Giraldez MD, Spengler RM, Etheridge A, Godoy PM, Barczak AJ, Srinivasan S, et al. Comprehensive multi-center assessment of small RNA-seq methods for quantitative miRNA profiling. Nat Biotechnol. 2018;36:746–57.PubMedPubMedCentral
145.
Wright C, Rajpurohit A, Burke EE, Williams C, Collado-Torres L, Kimos M, et al. Comprehensive assessment of multiple biases in small RNA sequencing reveals significant differences in the performance of widely used methods. BMC Genomics. 2019;20:513.PubMedPubMedCentral
146.
Potter SS. Single-cell RNA sequencing for the study of development, physiology and disease. Nat Rev Nephrol. 2018;14:479–92.PubMedPubMedCentral
147.
Warren L, Bryder D, Weissman IL, Quake SR. Transcription factor profiling in individual hematopoietic progenitors by digital RT-PCR. Proc Natl Acad Sci U S A. 2006;103:17807–12.PubMedPubMedCentral
148.
Serra L, Chang DZ, Macchietto M, Williams K, Murad R, Lu D, et al. Adapting the smart-seq2 protocol for robust single worm RNA-seq. Bio Protoc. 2018;8:e2729.PubMedPubMedCentral
149.
Bhargava V, Head SR, Ordoukhanian P, Mercola M, Subramaniam S. Technical variations in low-input RNA-seq methodologies. Sci Rep. 2014;4:3678.PubMedPubMedCentral
150.
Friedel CC, Dolken L. Metabolic tagging and purification of nascent RNA: implications for transcriptomics. Mol BioSyst. 2009;5:1271–8.PubMed
151.
Wissink EM, Vihervaara A, Tippens ND, Lis JT. Nascent RNA analyses: tracking transcription and its regulation. Nat Rev Genet. 2019;20:705–23.PubMedPubMedCentral
152.
Min IM, Waterfall JJ, Core LJ, Munroe RJ, Schimenti J, Lis JT. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev. 2011;25:742–54.PubMedPubMedCentral
153.
Baptista MAP, Dolken L. RNA dynamics revealed by metabolic RNA labeling and biochemical nucleoside conversions. Nat Methods. 2018;15:171–2.PubMed
154.
Washietl S, Hofacker IL, Lukasser M, Huttenhofer A, Stadler PF. Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nat Biotechnol. 2005;23:1383–90.PubMed
155.
Fabbri M, Girnita L, Varani G, Calin GA. Decrypting noncoding RNA interactions, structures, and functional networks. Genome Res. 2019;29:1377–88.PubMedPubMedCentral
156.
Fu XD. Non-coding RNA: a new frontier in regulatory biology. Natl Sci Rev. 2014;1:190–204.PubMed
157.
Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145–66.PubMed
158.
West JA, Davis CP, Sunwoo H, Simon MD, Sadreyev RI, Wang PI, et al. The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol Cell. 2014;55:791–802.PubMedPubMedCentral
159.
Sridhar B, Rivas-Astroza M, Nguyen TC, Chen W, Yan Z, Cao X, et al. Systematic mapping of RNA-chromatin interactions in vivo. Curr Biol. 2017;27:610–2.PubMed
160.
Simon MD, Wang CI, Kharchenko PV, West JA, Chapman BA, Alekseyenko AA, et al. The genomic binding sites of a noncoding RNA. Proc Natl Acad Sci U S A. 2011;108:20497–502.PubMedPubMedCentral
161.
Chu C, Qu K, Zhong FL, Artandi SE, Chang HY. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell. 2011;44:667–78.PubMedPubMedCentral
162.
Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science. 2013;341:1237973.PubMedPubMedCentral
163.
Kudla G, Wan Y, Helwak A. RNA conformation capture by proximity ligation. Annu Rev Genomics Hum Genet. 2020;21(1):14.
164.
Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell. 2013;153:654–65.PubMedPubMedCentral
165.
Hearst JE. Psoralen photochemistry and nucleic acid structure. J Invest Dermatol. 1981;77:39–44.PubMed
166.
Huber RG, Lim XN, Ng WC, Sim AYL, Poh HX, Shen Y, et al. Structure mapping of dengue and Zika viruses reveals functional long-range interactions. Nat Commun. 2019;10:1408.PubMedPubMedCentral
167.
Li P, Wei Y, Mei M, Tang L, Sun L, Huang W, et al. Integrative analysis of Zika virus genome RNA structure reveals critical determinants of viral infectivity. Cell Host Microbe. 2018;24:875–86.PubMed
168.
Sahu A, Singhal U, Chinnaiyan AM. Long noncoding RNAs in cancer: from function to translation. Trends Cancer. 2015;1:93–109.PubMedPubMedCentral
169.
Cabili MN, Dunagin MC, McClanahan PD, Biaesch A, Padovan-Merhar O, Regev A, et al. Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. Genome Biol. 2015;16:20.PubMedPubMedCentral
170.
Hougaard DM, Hansen H, Larsson LI. Non-radioactive in situ hybridization for mRNA with emphasis on the use of oligodeoxynucleotide probes. Histochem Cell Biol. 1997;108:335–44.PubMed
171.
Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods. 2008;5:877–9.PubMedPubMedCentral
172.
173.
Lee YH, Tan HT, Chung MC. Subcellular fractionation methods and strategies for proteomics. Proteomics. 2010;10:3935–56.PubMed
174.
Sultan M, Amstislavskiy V, Risch T, Schuette M, Dokel S, Ralser M, et al. Influence of RNA extraction methods and library selection schemes on RNA-seq data. BMC Genomics. 2014;15:675.PubMedPubMedCentral
175.
176.
Rhee HW, Zou P, Udeshi ND, Martell JD, Mootha VK, Carr SA, et al. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science. 2013;339:1328–31.PubMedPubMedCentral
177.
Gilbert C, Kristjuhan A, Winkler GS, Svejstrup JQ. Elongator interactions with nascent mRNA revealed by RNA immunoprecipitation. Mol Cell. 2004;14:457–64.PubMed
178.
Fazal FM, Han S, Parker KR, Kaewsapsak P, Xu J, Boettiger AN, et al. Atlas of subcellular RNA localization revealed by APEX-Seq. Cell. 2019;178:473–90.PubMedPubMedCentral
179.
Li J, Han L, Roebuck P, Diao L, Liu L, Yuan Y, et al. TANRIC: an interactive open platform to explore the function of lncRNAs in cancer. Cancer Res. 2015;75:3728–37.PubMedPubMedCentral
180.
Gao Y, Wang P, Wang Y, Ma X, Zhi H, Zhou D, et al. Lnc2Cancer v2.0: updated database of experimentally supported long non-coding RNAs in human cancers. Nucleic Acids Res. 2019;47:D1028–33.PubMed
181.
Liu Y, Zhao M. lnCaNet: pan-cancer co-expression network for human lncRNA and cancer genes. Bioinformatics. 2016;32:1595–7.PubMed
182.
Bao Z, Yang Z, Huang Z, Zhou Y, Cui Q, Dong D. LncRNADisease 2.0: an updated database of long non-coding RNA-associated diseases. Nucleic Acids Res. 2019;47:D1034–7.PubMed
183.
Xia S, Feng J, Chen K, Ma Y, Gong J, Cai F, et al. CSCD: a database for cancer-specific circular RNAs. Nucleic Acids Res. 2018;46:D925–9.PubMed
184.
Ghosal S, Das S, Sen R, Basak P, Chakrabarti J. Circ2Traits: a comprehensive database for circular RNA potentially associated with disease and traits. Front Genet. 2013;4:283.PubMedPubMedCentral
185.
186.
Xie B, Ding Q, Han H, Wu D. miRCancer: a microRNA-cancer association database constructed by text mining on literature. Bioinformatics. 2013;29:638–44.PubMed
187.
Bhattacharya A, Cui Y. SomamiR 2.0: a database of cancer somatic mutations altering microRNA-ceRNA interactions. Nucleic Acids Res. 2016;44:D1005–10.PubMed
188.
Wong NW, Chen Y, Chen S, Wang X. OncomiR: an online resource for exploring pan-cancer microRNA dysregulation. Bioinformatics. 2018;34:713–5.PubMed
189.
Ahmed M, Nguyen H, Lai T, Kim DR. miRCancerdb: a database for correlation analysis between microRNA and gene expression in cancer. BMC Res Notes. 2018;11:103.PubMedPubMedCentral
190.
Yang Z, Wu L, Wang A, Tang W, Zhao Y, Zhao H, et al. dbDEMC 2.0: updated database of differentially expressed miRNAs in human cancers. Nucleic Acids Res. 2017;45:D812–8.PubMed
191.
Chung IF, Chang SJ, Chen CY, Liu SH, Li CY, Chan CH, et al. YM500v3: a database for small RNA sequencing in human cancer research. Nucleic Acids Res. 2017;45:D925–31.PubMed
192.
Zheng LL, Xu WL, Liu S, Sun WJ, Li JH, Wu J, et al. tRF2Cancer: a web server to detect tRNA-derived small RNA fragments (tRFs) and their expression in multiple cancers. Nucleic Acids Res. 2016;44:W185–93.PubMedPubMedCentral
193.
Pliatsika V, Loher P, Magee R, Telonis AG, Londin E, Shigematsu M, et al. MINTbase v2.0: a comprehensive database for tRNA-derived fragments that includes nuclear and mitochondrial fragments from all the cancer genome atlas projects. Nucleic Acids Res. 2018;46:D152–9.PubMed
194.
Yan X, Hu Z, Feng Y, Hu X, Yuan J, Zhao SD, et al. Comprehensive genomic characterization of long non-coding RNAs across human cancers. Cancer Cell. 2015;28:529–40.PubMedPubMedCentral
195.
196.
Zhao Z, Wang K, Wu F, Wang W, Zhang K, Hu H, et al. circRNA disease: a manually curated database of experimentally supported circRNA-disease associations. Cell Death Dis. 2018;9:475.PubMedPubMedCentral
197.
Ruan H, Xiang Y, Ko J, Li S, Jing Y, Zhu X, et al. Comprehensive characterization of circular RNAs in ~1000 human cancer cell lines. Genome Med. 2019;11:55.PubMedPubMedCentral
198.
Jiang Q, Wang Y, Hao Y, Juan L, Teng M, Zhang X, et al. miR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Res. 2009;37:D98–104.PubMed
199.
Volders PJ, Anckaert J, Verheggen K, Nuytens J, Martens L, Mestdagh P, et al. LNCipedia 5: towards a reference set of human long non-coding RNAs. Nucleic Acids Res. 2019;47:D135–9.PubMed
200.
Gong J, Liu C, Liu W, Xiang Y, Diao L, Guo AY, et al. LNCediting: a database for functional effects of RNA editing in lncRNAs. Nucleic Acids Res. 2017;45:D79–84.PubMed
201.
Quek XC, Thomson DW, Maag JL, Bartonicek N, Signal B, Clark MB, et al. lncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs. Nucleic Acids Res. 2015;43:D168–73.PubMed
202.
Ma L, Li A, Zou D, Xu X, Xia L, Yu J, et al. LncRNAWiki: harnessing community knowledge in collaborative curation of human long non-coding RNAs. Nucleic Acids Res. 2015;43:D187–92.PubMed
203.
Ma L, Cao J, Liu L, Du Q, Li Z, Zou D, et al. LncBook: a curated knowledgebase of human long non-coding RNAs. Nucleic Acids Res. 2019;47:D128–34.PubMed
204.
Josset L, Tchitchek N, Gralinski LE, Ferris MT, Eisfeld AJ, Green RR, et al. Annotation of long non-coding RNAs expressed in collaborative cross founder mice in response to respiratory virus infection reveals a new class of interferon-stimulated transcripts. RNA Biol. 2014;11:875–90.PubMedPubMedCentral
205.
Zhao Y, Li H, Fang S, Kang Y, Wu W, Hao Y, et al. NONCODE 2016: an informative and valuable data source of long non-coding RNAs. Nucleic Acids Res. 2016;44:D203–8.PubMed
206.
Wu W, Ji P, Zhao F. CircAtlas: an integrated resource of one million highly accurate circular RNAs from 1070 vertebrate transcriptomes. Genome Biol. 2020;21:101.PubMedPubMedCentral
207.
208.
Dong R, Ma XK, Li GW, Yang L. CIRCpedia v2: an updated database for comprehensive circular RNA annotation and expression comparison. Genomics Proteomics Bioinformatics. 2018;16:226–33.PubMedPubMedCentral
209.
Xia S, Feng J, Lei L, Hu J, Xia L, Wang J, et al. Comprehensive characterization of tissue-specific circular RNAs in the human and mouse genomes. Brief Bioinform. 2017;18:984–92.PubMed
210.
Li JH, Liu S, Zhou H, Qu LH, Yang JH. starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res. 2014;42:D92–7.PubMed
211.
Chou CH, Shrestha S, Yang CD, Chang NW, Lin YL, Liao KW, et al. miRTarBase update 2018: a resource for experimentally validated microRNA-target interactions. Nucleic Acids Res. 2018;46:D296–302.PubMed
212.
213.
Liu T, Zhang Q, Zhang J, Li C, Miao YR, Lei Q, et al. EVmiRNA: a database of miRNA profiling in extracellular vesicles. Nucleic Acids Res. 2019;47:D89–93.PubMed
214.
215.
Kozomara A, Birgaoanu M, Griffiths-Jones S. miRBase: from microRNA sequences to function. Nucleic Acids Res. 2019;47:D155–62.PubMed
216.
Karagkouni D, Paraskevopoulou MD, Chatzopoulos S, Vlachos IS, Tastsoglou S, Kanellos I, et al. DIANA-TarBase v8: a decade-long collection of experimentally supported miRNA-gene interactions. Nucleic Acids Res. 2018;46:D239–45.PubMed
217.
Kuksa PP, Amlie-Wolf A, Katanic Z, Valladares O, Wang LS, Leung YY. DASHR 2.0: integrated database of human small non-coding RNA genes and mature products. Bioinformatics. 2019;35:1033–9.PubMed
218.
Zhang T, Tan P, Wang L, Jin N, Li Y, Zhang L, et al. RNALocate: a resource for RNA subcellular localizations. Nucleic Acids Res. 2017;45:D135–8.PubMed
219.
Mas-Ponte D, Carlevaro-Fita J, Palumbo E, Hermoso Pulido T, Guigo R, Johnson R. LncATLAS database for subcellular localization of long noncoding RNAs. RNA. 2017;23:1080–7.PubMedPubMedCentral
220.
Wang Z, Tollervey J, Briese M, Turner D, Ule J. CLIP: construction of cDNA libraries for high-throughput sequencing from RNAs cross-linked to proteins in vivo. Methods. 2009;48:287–93.PubMed
221.
222.
Wong NK, Huang CL, Islam R, Yip SP. Long non-coding RNAs in hematological malignancies: translating basic techniques into diagnostic and therapeutic strategies. J Hematol Oncol. 2018;11:131.PubMedPubMedCentral
223.
Amodio N, Raimondi L, Juli G, Stamato MA, Caracciolo D, Tagliaferri P, et al. MALAT1: a druggable long non-coding RNA for targeted anti-cancer approaches. J Hematol Oncol. 2018;11:63.PubMedPubMedCentral
224.
Tie Y, Liu B, Fu H, Zheng X. Circulating miRNA and cancer diagnosis. Sci China C Life Sci. 2009;52:1117–22.PubMed
225.
Rupaimoole R, Calin GA, Lopez-Berestein G, Sood AK. miRNA deregulation in cancer cells and the tumor microenvironment. Cancer Discov. 2016;6:235–46.PubMedPubMedCentral
226.
Tahamtan A, Ardebili A. Real-time RT-PCR in COVID-19 detection: issues affecting the results. Expert Rev Mol Diagn. 2020;20:453–4.PubMed
227.
Holdt LM, Stahringer A, Sass K, Pichler G, Kulak NA, Wilfert W, et al. Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nat Commun. 2016;7:12429.PubMedPubMedCentral
228.
Carlevaro-Fita J, Johnson R. Global positioning system: understanding long noncoding RNAs through subcellular localization. Mol Cell. 2019;73:869–83.PubMed
Metadata
Title
Principles and innovative technologies for decrypting noncoding RNAs: from discovery and functional prediction to clinical application
Authors
Yu-Meng Sun
Yue-Qin Chen
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Journal of Hematology & Oncology / Issue 1/2020
Electronic ISSN: 1756-8722
DOI
https://doi.org/10.1186/s13045-020-00945-8

Other articles of this Issue 1/2020

Journal of Hematology & Oncology 1/2020 Go to the issue

Research

GD2 or HER2 targeting T cell engaging bispecific antibodies to treat osteosarcoma

Review

Current understanding of extrachromosomal circular DNA in cancer pathogenesis and therapeutic resistance

Letter to the Editor

Genetic alteration, RNA expression, and DNA methylation profiling of coronavirus disease 2019 (COVID-19) receptor ACE2 in malignancies: a pan-cancer analysis

Research

Treating non-responders: pitfalls and implications for cancer immunotherapy trial design

Research

The functional epigenetic landscape of aberrant gene expression in molecular subgroups of newly diagnosed multiple myeloma

Short report

Haploidentical versus HLA-matched sibling transplantation for refractory acute leukemia undergoing sequential intensified conditioning followed by DLI: an analysis from two prospective data
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine
Image Credits