Dumbbell-PCR: A method to quantify specific small RNA variants with a single nucleotide resolution at terminal sequences

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages e77-

  Honda, Shozo ^a   Kirino, Yohei ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 16; RNA; RNA LIGASE; SMALL RNA; T4 RNA LIGASE 2; UNCLASSIFIED DRUG; MIRN16 MICRORNA, HUMAN; SMALL UNTRANSLATED RNA;

3' DUMBBELL PCR; 3' TERMINAL SEQUENCE; 5' DUMBBELL PCR; 5' TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; HUMAN; HUMAN CELL; HYBRIDIZATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA TRANSPORT; TAQMAN RT PCR; TERMINAL SEQUENCE; CELL LINE; CHEMISTRY; CONFORMATION; GENETIC VARIABILITY; NUCLEOTIDE SEQUENCE; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

BASE SEQUENCE; CELL LINE; CELL LINE, TUMOR; GENETIC VARIATION; HUMANS; MICRORNAS; NUCLEIC ACID CONFORMATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL UNTRANSLATED;

EID: 84938105530     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv218     Document Type: Article

References (52)

1. Esteller,M. (2011) Non-coding RNAs in human disease. Nat. Rev. Genet., 12, 861-874.
2. Bartel,D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
3. Siomi,M.C., Sato,K., Pezic,D. and Aravin,A.A. (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell. Biol., 12, 246-258.
4. Okamura,K. and Lai,E.C. (2008) Endogenous small interfering RNAs in animals. Nat. Rev. Mol. Cell. Biol., 9, 673-678.
5. Ghildiyal,M. and Zamore,P.D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet., 10, 94-108.
6. Farazi,T.A., Juranek,S.A. and Tuschl,T. (2008) The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development, 135, 1201-1214.
7. Liu,X., Fortin,K. and Mourelatos,Z. (2008) MicroRNAs: biogenesis and molecular functions. Brain Pathol., 18, 113-121.
8. Pillai,R.S., Bhattacharyya,S.N. and Filipowicz,W. (2007) Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol., 17, 118-126.
9. Kozomara,A. and Griffiths-Jones,S. (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res., 42, D68-D73.
10. Friedman,R.C., Farh,K.K., Burge,C.B. and Bartel,D.P. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res., 19, 92-105.
11. Neilsen,C.T., Goodall,G.J. and Bracken,C.P. (2012) IsomiRs-the overlooked repertoire in the dynamic microRNAome. Trends Genet., 28, 544-549.
12. Morin,R.D., O'Connor,M.D., Griffith,M., Kuchenbauer,F., Delaney,A., Prabhu,A.L., Zhao,Y., McDonald,H., Zeng,T., Hirst,M. et al. (2008) Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res., 18, 610-621.
13. Newman,M.A., Mani,V. and Hammond,S.M. (2011) Deep sequencing of microRNA precursors reveals extensive 3′ end modification. RNA, 17, 1795-1803.
14. Starega-Roslan,J., Krol,J., Koscianska,E., Kozlowski,P., Szlachcic,W.J., Sobczak,K. and Krzyzosiak,W.J. (2011) Structural basis of microRNA length variety. Nucleic Acids Res., 39, 257-268.
15. Liu,N., Abe,M., Sabin,L.R., Hendriks,G.J., Naqvi,A.S., Yu,Z., Cherry,S. and Bonini,N.M. (2011) The exoribonuclease Nibbler controls 3′ end processing of microRNAs in Drosophila. Curr. Biol., 21, 1888-1893.
16. Han,B.W., Hung,J.H., Weng,Z., Zamore,P.D. and Ameres,S.L. (2011) The 3′-to-5′ exoribonuclease Nibbler shapes the 3′ ends of microRNAs bound to Drosophila Argonaute1. Curr. Biol., 21, 1878-1887.
17. Landgraf,P., Rusu,M., Sheridan,R., Sewer,A., Iovino,N., Aravin,A., Pfeffer,S., Rice,A., Kamphorst,A.O., Landthaler,M. et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell, 129, 1401-1414.
18. Blow,M.J., Grocock,R.J., van Dongen,S., Enright,A.J., Dicks,E., Futreal,P.A., Wooster,R. and Stratton,M.R. (2006) RNA editing of human microRNAs. Genome Biol., 7, R27.
19. Kawahara,Y., Zinshteyn,B., Sethupathy,P., Iizasa,H., Hatzigeorgiou,A.G. and Nishikura,K. (2007) Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science, 315, 1137-1140.
20. Burroughs,A.M., Ando,Y., de Hoon,M.J., Tomaru,Y., Suzuki,H., Hayashizaki,Y. and Daub,C.O. (2011) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol., 8, 158-177.
21. Azuma-Mukai,A., Oguri,H., Mituyama,T., Qian,Z.R., Asai,K., Siomi,H. and Siomi,M.C. (2008) Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc. Natl. Acad. Sci. U.S.A., 105, 7964-7969.
22. Cloonan,N., Wani,S., Xu,Q., Gu,J., Lea,K., Heater,S., Barbacioru,C., Steptoe,A.L., Martin,H.C., Nourbakhsh,E. et al. (2011) MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol., 12, R126.
23. Loher,P., Londin,E.R. and Rigoutsos,I. (2014) IsomiR expression profiles in human lymphoblastoid cell lines exhibit population and gender dependencies. Oncotarget, 5, 8790-8802.
24. Takeda,A., Iwasaki,S., Watanabe,T., Utsumi,M. and Watanabe,Y. (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol., 49, 493-500.
25. Montgomery,T.A., Howell,M.D., Cuperus,J.T., Li,D., Hansen,J.E., Alexander,A.L., Chapman,E.J., Fahlgren,N., Allen,E. and Carrington,J.C. (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell, 133, 128-141.
26. Mi,S., Cai,T., Hu,Y., Chen,Y., Hodges,E., Ni,F., Wu,L., Li,S., Zhou,H., Long,C. et al. (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell, 133, 116-127.
27. Czech,B., Zhou,R., Erlich,Y., Brennecke,J., Binari,R., Villalta,C., Gordon,A., Perrimon,N. and Hannon,G.J. (2009) Hierarchical rules for Argonaute loading in Drosophila. Mol. Cell, 36, 445-456.
28. Meijer,H.A., Smith,E.M. and Bushell,M. (2014) Regulation of miRNA strand selection: follow the leader? Biochem. Soc. Trans., 42, 1135-1140.
29. Lu,S., Sun,Y.H. and Chiang,V.L. (2009) Adenylation of plant miRNAs. Nucleic Acids Res., 37, 1878-1885.
30. Katoh,T., Sakaguchi,Y., Miyauchi,K., Suzuki,T., Kashiwabara,S., Baba,T. and Suzuki,T. (2009) Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev., 23, 433-438.
31. Boele,J., Persson,H., Shin,J.W., Ishizu,Y., Newie,I.S., Sokilde,R., Hawkins,S.M., Coarfa,C., Ikeda,K., Takayama,K. et al. (2014) PAPD5-mediated 3′ adenylation and subsequent degradation of miR-21 is disrupted in proliferative disease. Proc. Natl. Acad. Sci. U.S.A., 111, 11467-11472.
32. Tan,G.C., Chan,E., Molnar,A., Sarkar,R., Alexieva,D., Isa,I.M., Robinson,S., Zhang,S., Ellis,P., Langford,C.F. et al. (2014) 5′ isomiR variation is of functional and evolutionary importance. Nucleic Acids Res., 42, 9424-9435.
33. Kozubek,J., Ma,Z., Fleming,E., Duggan,T., Wu,R., Shin,D.G. and Dadras,S.S. (2005) In-depth characterization of microRNA transcriptome in melanoma. PLoS One, 8, e72699.
34. Somel,M., Guo,S., Fu,N., Yan,Z., Hu,H.Y., Xu,Y., Yuan,Y., Ning,Z., Hu,Y., Menzel,C. et al. (2010) MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res., 20, 1207-1218.
35. Fernandez-Valverde,S.L., Taft,R.J. and Mattick,J.S. (2010) Dynamic isomiR regulation in Drosophila development. RNA, 16, 1881-1888.
36. Bizuayehu,T.T., Lanes,C.F., Furmanek,T., Karlsen,B.O., Fernandes,J.M., Johansen,S.D. and Babiak,I. (2012) Differential expression patterns of conserved miRNAs and isomiRs during Atlantic halibut development. BMC Genomics, 13, 11.
37. Chen,C., Ridzon,D.A., Broomer,A.J., Zhou,Z., Lee,D.H., Nguyen,J.T., Barbisin,M., Xu,N.L., Mahuvakar,V.R., Andersen,M.R. et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res., 33, e179.
38. Schamberger,A. and Orban,T.I. (2014) 3′ IsomiR species and DNA contamination influence reliable quantification of microRNAs by stem-loop quantitative PCR. PLoS One, 9, e106315.
39. Ho,C.K. and Shuman,S. (2002) Bacteriophage T4 RNA ligase 2 (gp24.1) exemplifies a family of RNA ligases found in all phylogenetic domains. Proc. Natl. Acad. Sci. U.S.A., 99, 12709-12714.
40. Bullard,D.R. and Bowater,R.P. (2006) Direct comparison of nick-joining activity of the nucleic acid ligases from bacteriophage T4. Biochem. J., 398, 135-144.
41. Nandakumar,J., Ho,C.K., Lima,C.D. and Shuman,S. (2004) RNA substrate specificity and structure-guided mutational analysis of bacteriophage T4 RNA ligase 2. J. Biol. Chem., 279, 31337-31347.
42. Nandakumar,J. and Shuman,S. (2005) Dual mechanisms whereby a broken RNA end assists the catalysis of its repair by T4 RNA ligase 2. J. Biol. Chem., 280, 23484-23489.
43. Clepet,C. (2011) RNA captor: a tool for RNA characterization. PLoS One, 6, e18445.
44. Park,K., Choi,B.R., Kim,Y.S., Shin,S., Hah,S.S., Jung,W., Oh,S. and Kim,D.E. (2011) Detection of single-base mutation in RNA using T4 RNA ligase-based nick-joining or DNAzyme-based nick-generation. Anal. Biochem., 414, 303-305.
45. Honda,S., Kirino,Y., Maragkakis,M., Alexiou,P., Ohtaki,A., Murali,R. and Mourelatos,Z. (2013) Mitochondrial protein BmPAPI modulates the length of mature piRNAs. RNA, 19, 1405-1418.
46. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
47. Ranade,K., Chang,M.S., Ting,C.T., Pei,D., Hsiao,C.F., Olivier,M., Pesich,R., Hebert,J., Chen,Y.D., Dzau,V.J. et al. (2001) High-throughput genotyping with single nucleotide polymorphisms. Genome Res., 11, 1262-1268.
48. Lagos-Quintana,M., Rauhut,R., Meyer,J., Borkhardt,A. and Tuschl,T. (2003) New microRNAs from mouse and human. RNA, 9, 175-179.
49. Kawaoka,S., Hayashi,N., Suzuki,Y., Abe,H., Sugano,S., Tomari,Y., Shimada,T. and Katsuma,S. (2009) The Bombyx ovary-derived cell line endogenously expresses PIWI/PIWI-interacting RNA complexes. RNA, 15, 1258-1264.
50. Riaz,M., van Jaarsveld,M.T., Hollestelle,A., Prager-van der Smissen,W.J., Heine,A.A., Boersma,A.W., Liu,J., Helmijr,J., Ozturk,B., Smid,M. et al. (2013) miRNA expression profiling of 51 human breast cancer cell lines reveals subtype and driver mutation-specific miRNAs. Breast Cancer Res., 15, R33.
51. Li,T., Li,D., Sha,J., Sun,P. and Huang,Y. (2009) MicroRNA-21 directly targets MARCKS and promotes apoptosis resistance and invasion in prostate cancer cells. Biochem. Biophys. Res. Commun., 383, 280-285.
52. Shigematsu,M., Honda,S. and Kirino,Y. (2014) Transfer RNA as a source of small functional RNA. J. Mol. Biol. Mol. Imaging, 1, 8.