Therapeutic suppression of premature termination codons: Mechanisms and clinical considerations (Review)
- Authors:
- John Karijolich
- Yi-Tao Yu
-
Affiliations: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA, Department of Biochemistry and Biophysics, University of Rochester School of Medicine and Dentistry, Rochester, NY 14642, USA - Published online on: June 17, 2014 https://doi.org/10.3892/ijmm.2014.1809
- Pages: 355-362
This article is mentioned in:
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|
Brenner S, Barnett L, Katz ER and Crick FH: UGA: a third nonsense triplet in the genetic code. Nature. 213:449–450. 1967. View Article : Google Scholar : PubMed/NCBI | |
|
Brenner S, Stretton AO and Kaplan S: Genetic code: the ‘nonsense’ triplets for chain termination and their suppression. Nature. 206:994–998. 1965. | |
|
Dever TE and Green R: The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harb Perspect Biol. 4:a0137062012. View Article : Google Scholar : PubMed/NCBI | |
|
Bonetti B, Fu L, Moon J and Bedwell DM: The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol. 251:334–345. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Manuvakhova M, Keeling K and Bedwell DM: Aminoglycoside antibiotics mediate context-dependent suppression of termination codons in a mammalian translation system. RNA. 6:1044–1055. 2000. View Article : Google Scholar | |
|
Peltz SW, Morsy M, Welch EM and Jacobson A: Ataluren as an agent for therapeutic nonsense suppression. Annu Rev Med. 64:407–425. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Mort M, Ivanov D, Cooper DN and Chuzhanova NA: A meta-analysis of nonsense mutations causing human genetic disease. Hum Mutat. 29:1037–1047. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Nagy E and Maquat LE: A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci. 23:198–199. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Keeling KM, Xue X, Gunn G and Bedwell DM: Therapeutics based on stop codon readthrough. Annu Rev Genomics Hum Genet. 15:8.1–8.24. 2014. View Article : Google Scholar | |
|
Salas-Marco J and Bedwell DM: GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination. Mol Cell Biol. 24:7769–7778. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Alkalaeva EZ, Pisarev AV, Frolova LY, Kisselev LL and Pestova TV: In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell. 125:1125–1136. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Pisareva VP, Pisarev AV, Hellen CU, Rodnina MV and Pestova TV: Kinetic analysis of interaction of eukaryotic release factor 3 with guanine nucleotides. J Biol Chem. 281:40224–40235. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Mitkevich VA, Kononenko AV, Petrushanko IY, Yanvarev DV, Makarov AA and Kisselev LL: Termination of translation in eukaryotes is mediated by the quaternary eRF1*eRF3*GTP*Mg2+complex. The biological roles of eRF3 and prokaryotic RF3 are profoundly distinct. Nucleic Acids Res. 34:3947–3954. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Kong C, Ito K, Walsh MA, Wada M, Liu Y, Kumar S, Barford D, Nakamura Y and Song H: Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 from S. pombe. Mol Cell. 14:233–245. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Mantsyzov AB, Ivanova EV, Birdsall B, Alkalaeva EZ, Kryuchkova PN, Kelly G, Frolova LY and Polshakov VI: NMR solution structure and function of the C-terminal domain of eukaryotic class 1 polypeptide chain release factor. FEBS J. 277:2611–2627. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Song H, Mugnier P, Das AK, Webb HM, Evans DR, Tuite MF, Hemmings BA and Barford D: The crystal structure of human eukaryotic release factor eRF1 - mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell. 100:311–321. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Bertram G, Bell HA, Ritchie DW, Fullerton G and Stansfield I: Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA. 6:1236–1247. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Chavatte L, Seit-Nebi A, Dubovaya V and Favre A: The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J. 21:5302–5311. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Frolova L, Seit-Nebi A and Kisselev L: Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA. 8:129–136. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Seit-Nebi A, Frolova L and Kisselev L: Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Rep. 3:881–886. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Ito K, Frolova L, Seit-Nebi A, Karamyshev A, Kisselev L and Nakamura Y: Omnipotent decoding potential resides in eukaryotic translation termination factor eRF1 of variant-code organisms and is modulated by the interactions of amino acid sequences within domain 1. Proc Natl Acad Sci USA. 99:8494–8499. 2002. View Article : Google Scholar | |
|
Fan-Minogue H, Du M, Pisarev AV, Kallmeyer AK, Salas-Marco J, Keeling KM, Thompson SR, Pestova TV and Bedwell DM: Distinct eRF3 requirements suggest alternate eRF1 conformations mediate peptide release during eukaryotic translation termination. Mol Cell. 30:599–609. 2008. View Article : Google Scholar | |
|
Cheng Z, Saito K, Pisarev AV, Wada M, Pisareva VP, Pestova TV, Gajda M, Round A, Kong C, Lim M, Nakamura Y, Svergun DI, Ito K and Song H: Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev. 23:1106–1118. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Conard SE, Buckley J, Dang M, Bedwell GJ, Carter RL, Khass M and Bedwell DM: Identification of eRF1 residues that play critical and complementary roles in stop codon recognition. RNA. 18:1210–1221. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kryuchkova P, Grishin A, Eliseev B, Karyagina A, Frolova L and Alkalaeva E: Two-step model of stop codon recognition by eukaryotic release factor eRF1. Nucleic Acids Res. 41:4573–4586. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Merritt GH, Naemi WR, Mugnier P, Webb HM, Tuite MF and von der Haar T: Decoding accuracy in eRF1 mutants and its correlation with pleiotropic quantitative traits in yeast. Nucleic Acids Res. 38:5479–5492. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Frolova LY, Tsivkovskii RY, Sivolobova GF, Oparina NY, Serpinsky OI, Blinov VM, Tatkov SI and Kisselev LL: Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA. 5:1014–1020. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S and Noller HF: Structural basis for translation termination on the 70S ribosome. Nature. 454:852–857. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Weixlbaumer A, Jin H, Neubauer C, Voorhees RM, Petry S, Kelley AC and Ramakrishnan V: Insights into translational termination from the structure of RF2 bound to the ribosome. Science. 322:953–956. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Santos N, Zhu J, Donohue JP, Korostelev AA and Noller HF: Crystal structure of the 70S ribosome bound with the Q253P mutant form of release factor RF2. Structure. 21:1258–1263. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kapp LD and Lorsch JR: The molecular mechanics of eukaryotic translation. Ann Rev Biochem. 73:657–704. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Ter-Avanesyan MD, Kushnirov VV, Dagkesamanskaya AR, Didichenko SA, Chernoff YO, Inge-Vechtomov SG and Smirnov VN: Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol Microbiol. 7:683–692. 1993.PubMed/NCBI | |
|
Kononenko AV, Mitkevich VA, Dubovaya VI, Kolosov PM, Makarov AA and Kisselev LL: Role of the individual domains of translation termination factor eRF1 in GTP binding to eRF3. Proteins. 70:388–393. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Frolova L, Le Goff X, Zhouravleva G, Davydova E, Philippe M and Kisselev L: Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA. 2:334–341. 1996.PubMed/NCBI | |
|
Jones D, Metzger HJ, Schatz A and Waksman SA: Control of gram-negative bacteria in experimental animals by streptomycin. Science. 100:103–105. 1944. View Article : Google Scholar : PubMed/NCBI | |
|
Schatz A, Bugie E and Waksman SA: Streptomycin, a substance exhibiting antibiotic activity against gram-positive and gram-negative bacteria. 1944. Clin Orthop Relat Res. 437:3–6. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Hermann T: Drugs targeting the ribosome. Curr Opin Struct Biol. 15:355–366. 2005. View Article : Google Scholar | |
|
Hermann T: Aminoglycoside antibiotics: old drugs and new therapeutic approaches. Cell Mol Life Sci. 64:1841–1852. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Moazed D and Noller HF: Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature. 327:389–394. 1987. View Article : Google Scholar : PubMed/NCBI | |
|
Moazed D and Noller HF: Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16 S rRNA. J Mol Biol. 211:135–145. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Yoshizawa S, Fourmy D and Puglisi JD: Recognition of the codon-anticodon helix by ribosomal RNA. Science. 285:1722–1725. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
François B, Russell RJ, Murray JB, Aboul-ela F, Masquida B, Vicens Q and Westhof E: Crystal structures of complexes between aminoglycosides and decoding A site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res. 33:5677–5690. 2005. | |
|
Fan-Minogue H and Bedwell DM: Eukaryotic ribosomal RNA determinants of aminoglycoside resistance and their role in translational fidelity. RNA. 14:148–157. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Gorini L and Kataja E: Phenotypic repair by streptomycin of defective genotypes in E. coli. Proc Natl Acad Sci USA. 51:487–493. 1964. View Article : Google Scholar : PubMed/NCBI | |
|
Lai CH, Chun HH, Nahas SA, Mitui M, Gamo KM, Du L and Gatti RA: Correction of ATM gene function by aminoglycoside-induced read-through of premature termination codons. Proc Natl Acad Sci USA. 101:15676–15681. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Keeling KM and Bedwell DM: Clinically relevant aminoglycosides can suppress disease-associated premature stop mutations in the IDUA and P53 cDNAs in a mammalian translation system. J Mol Med (Berl). 80:367–376. 2002. View Article : Google Scholar | |
|
Sleat DE, Sohar I, Gin RM and Lobel P: Aminoglycoside-mediated suppression of nonsense mutations in late infantile neuronal ceroid lipofuscinosis. Eur J Paediatr Neurol. 5(Suppl A): 57–62. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Howard M, Frizzell RA and Bedwell DM: Aminoglycoside antibiotics restore CFTR function by overcoming premature stop mutations. Nat Med. 2:467–469. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Bedwell DM, Kaenjak A, Benos DJ, Bebok Z, Bubien JK, Hong J, Tousson A, Clancy JP and Sorscher EJ: Suppression of a CFTR premature stop mutation in a bronchial epithelial cell line. Nat Med. 3:1280–1284. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Bidou L, Hatin I, Perez N, Allamand V, Panthier JJ and Rousset JP: Premature stop codons involved in muscular dystrophies show a broad spectrum of readthrough efficiencies in response to gentamicin treatment. Gene Ther. 11:619–627. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Wilschanski M, Yahav Y, Yaacov Y, Blau H, Bentur L, Rivlin J, Aviram M, Bdolah-Abram T, Bebok Z, Shushi L, Kerem B and Kerem E: Gentamicin-induced correction of CFTR function in patients with cystic fibrosis and CFTR stop mutations. N Engl J Med. 349:1433–1441. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Politano L, Nigro G, Nigro V, Piluso G, Papparella S, Paciello O and Comi LI: Gentamicin administration in Duchenne patients with premature stop codon. Preliminary results. Acta Myol. 22:15–21. 2003.PubMed/NCBI | |
|
James PD, Raut S, Rivard GE, Poon MC, Warner M, McKenna S, Leggo J and Lillicrap D: Aminoglycoside suppression of nonsense mutations in severe hemophilia. Blood. 106:3043–3048. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Kellermayer R, Szigeti R, Keeling KM, Bedekovics T and Bedwell DM: Aminoglycosides as potential pharmacogenetic agents in the treatment of Hailey-Hailey disease. J Invest Dermatol. 126:229–231. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Floquet C, Hatin I, Rousset JP and Bidou L: Statistical analysis of readthrough levels for nonsense mutations in mammalian cells reveals a major determinant of response to gentamicin. PLoS Genet. 8:e10026082012. View Article : Google Scholar : PubMed/NCBI | |
|
Turnidge J: Pharmacodynamics and dosing of aminoglycosides. Infect Dis Clin North Am. 17:503–528. 2003. View Article : Google Scholar | |
|
Fischel-Ghodsian N: Genetic factors in aminoglycoside toxicity. Pharmacogenomics. 6:27–36. 2005. View Article : Google Scholar | |
|
Moestrup SK, Cui S, Vorum H, Bregengard C, Bjørn SE, Norris K, Gliemann J and Christensen EI: Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J Clin Invest. 96:1404–1413. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Guthrie OW: Aminoglycoside induced ototoxicity. Toxicology. 249:91–96. 2008. View Article : Google Scholar | |
|
Mingeot-Leclercq MP and Tulkens PM: Aminoglycosides: nephrotoxicity. Antimicrob Agents Chemother. 43:1003–1012. 1999.PubMed/NCBI | |
|
Avent ML, Rogers BA, Cheng AC and Paterson DL: Current use of aminoglycosides: indications, pharmacokinetics and monitoring for toxicity. Intern Med J. 41:441–449. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Laurent G, Carlier MB, Rollman B, Van Hoof F and Tulkens P: Mechanism of aminoglycoside-induced lysosomal phospholipidosis: in vitro and in vivo studies with gentamicin and amikacin. Biochem Pharmacol. 31:3861–3870. 1982. View Article : Google Scholar : PubMed/NCBI | |
|
Sha SH and Schacht J: Stimulation of free radical formation by aminoglycoside antibiotics. Hear Res. 128:112–118. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Hobbie SN, Akshay S, Kalapala SK, Bruell CM, Shcherbakov D and Böttger EC: Genetic analysis of interactions with eukaryotic rRNA identify the mitoribosome as target in aminoglycoside ototoxicity. Proc Natl Acad Sci USA. 105:20888–20893. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Welch EM, Barton ER, Zhuo J, Tomizawa Y, Friesen WJ, Trifillis P, Paushkin S, Patel M, Trotta CR, Hwang S, Wilde RG, Karp G, Takasugi J, Chen G, Jones S, Ren H, Moon YC, Corson D, Turpoff AA, Campbell JA, Conn MM, Khan A, Almstead NG, Hedrick J, Mollin A, Risher N, Weetall M, Yeh S, Branstrom AA, Colacino JM, Babiak J, Ju WD, Hirawat S, Northcutt VJ, Miller LL, Spatrick P, He F, Kawana M, Feng H, Jacobson A, Peltz SW and Sweeney HL: PTC124 targets genetic disorders caused by nonsense mutations. Nature. 447:87–91. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Du M, Liu X, Welch EM, Hirawat S, Peltz SW and Bedwell DM: PTC124 is an orally bioavailable compound that promotes suppression of the human CFTR-G542X nonsense allele in a CF mouse model. Proc Natl Acad Sci USA. 105:2064–2069. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Wang B, Yang Z, Brisson BK, Feng H, Zhang Z, Welch EM, Peltz SW, Barton ER, Brown RH Jr and Sweeney HL: Membrane blebbing as an assessment of functional rescue of dysferlin-deficient human myotubes via nonsense suppression. J Appl Physiol. 1985. 109:901–905. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Tan L, Narayan SB, Chen J, Meyers GD and Bennett MJ: PTC124 improves readthrough and increases enzymatic activity of the CPT1A R160X nonsense mutation. J Inherit Metab Dis. 34:443–447. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Goldmann T, Overlack N, Wolfrum U and Nagel-Wolfrum K: PTC124-mediated translational readthrough of a nonsense mutation causing Usher syndrome type 1C. Hum Gene Ther. 22:537–547. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Sarkar C, Zhang Z and Mukherjee AB: Stop codon read-through with PTC124 induces palmitoyl-protein thioesterase-1 activity, reduces thioester load and suppresses apoptosis in cultured cells from INCL patients. Mol Genet Metab. 104:338–345. 2011. View Article : Google Scholar | |
|
Hirawat S, Welch EM, Elfring GL, Northcutt VJ, Paushkin S, Hwang S, Leonard EM, Almstead NG, Ju W, Peltz SW and Miller LL: Safety, tolerability, and pharmacokinetics of PTC124, a nonaminoglycoside nonsense mutation suppressor, following single- and multiple-dose administration to healthy male and female adult volunteers. J Clin Pharmacol. 47:430–444. 2007. View Article : Google Scholar | |
|
Sermet-Gaudelus I, Boeck KD, Casimir GJ, Vermeulen F, Leal T, Mogenet A, Roussel D, Fritsch J, Hanssens L, Hirawat S, Miller NL, Constantine S, Reha A, Ajayi T, Elfring GL and Miller LL: Ataluren (PTC124) induces cystic fibrosis transmembrane conductance regulator protein expression and activity in children with nonsense mutation cystic fibrosis. Am J Respir Crit Care Med. 182:1262–1272. 2010. View Article : Google Scholar | |
|
Wilschanski M, Miller LL, Shoseyov D, Blau H, Rivlin J, Aviram M, Cohen M, Armoni S, Yaakov Y, Pugatsch T, Cohen-Cymberknoh M, Miller NL, Reha A, Northcutt VJ, Hirawat S, Donnelly K, Elfring GL, Ajayi T and Kerem E: Chronic ataluren (PTC124) treatment of nonsense mutation cystic fibrosis. Eur Respir J. 38:59–69. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Finkel RS, Flanigan KM, Wong B, Bönnemann C, Sampson J, Sweeney HL, Reha A, Northcutt VJ, Elfring G, Barth J and Peltz SW: Phase 2a study of ataluren-mediated dystrophin production in patients with nonsense mutation Duchenne muscular dystrophy. PLoS One. 8:e813022013. View Article : Google Scholar : PubMed/NCBI | |
|
Kerem E, Konstan MW, De Boeck K, Accurso FJ, Sermet-Gaudelus I, Wilschanski M, Elborn JS, Melotti P, Bronsveld I, Fajac I, Malfroot A, Rosenbluth DB, Walker PA, McColley SA, Knoop C, Quattrucci S, Rietschel E, Zeitlin PL, Barth J, Elfring GL, Welch EM, Branstrom A, Spiegel RJ, Peltz SW, Ajayi T and Rowe SM; for the Cystic Fibrosis Ataluren Study Group. Ataluren for the treatment of nonsense-mutation cystic fibrosis: a randomised, double-blind, placebo-controlled phase 3 trial. Lancet Respir Med. pii: S2213-2600(14)70100-6. View Article : Google Scholar : 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Amrani N, Ganesan R, Kervestin S, Mangus DA, Ghosh S and Jacobson A: A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature. 432:112–118. 2004. | |
|
Auld DS, Thorne N, Maguire WF and Inglese J: Mechanism of PTC124 activity in cell-based luciferase assays of nonsense codon suppression. Proc Natl Acad Sci USA. 106:3585–3590. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Auld DS, Lovell S, Thorne N, Lea WA, Maloney DJ, Shen M, Rai G, Battaile KP, Thomas CJ, Simeonov A, Hanzlik RP and Inglese J: Molecular basis for the high-affinity binding and stabilization of firefly luciferase by PTC124. Proc Natl Acad Sci USA. 107:4878–4883. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Peltz SW, Welch EM, Jacobson A, Trotta CR, Naryshkin N, Sweeney HL and Bedwell DM: Nonsense suppression activity of PTC124 (ataluren). Proc Natl Acad Sci USA. 106:E64author reply E65. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
McElroy SP, Nomura T, Torrie LS, Warbrick E, Gartner U, Wood G and McLean WH: A lack of premature termination codon read-through efficacy of PTC124 (Ataluren) in a diverse array of reporter assays. PLoS Biol. 11:e10015932013. View Article : Google Scholar : PubMed/NCBI | |
|
Karijolich J and Yu YT: Converting nonsense codons into sense codons by targeted pseudouridylation. Nature. 474:395–398. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Karijolich J, Kantartzis A and Yu YT: RNA modifications: a mechanism that modulates gene expression. Methods Mol Biol. 629:1–19. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Karijolich J and Yu YT: Spliceosomal snRNA modifications and their function. RNA Biol. 7:192–204. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Kierzek E, Malgowska M, Lisowiec J, Turner DH, Gdaniec Z and Kierzek R: The contribution of pseudouridine to stabilities and structure of RNAs. Nucleic Acids Res. 42:3492–3501. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Fernández IS, Ng CL, Kelley AC, Wu G, Yu YT and Ramakrishnan V: Unusual base pairing during the decoding of a stop codon by the ribosome. Nature. 500:107–110. 2013.PubMed/NCBI | |
|
Ganot P, Bortolin ML and Kiss T: Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell. 89:799–809. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Huang C, Karijolich J and Yu YT: Post-transcriptional modification of RNAs by artificial Box H/ACA and Box C/D RNPs. Methods Mol Biol. 718:227–244. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Barbalat R, Ewald SE, Mouchess ML and Barton GM: Nucleic acid recognition by the innate immune system. Ann Rev Immunol. 29:185–214. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Frischmeyer PA and Dietz HC: Nonsense-mediated mRNA decay in health and disease. Hum Mol Genet. 8:1893–1900. 1999. View Article : Google Scholar : PubMed/NCBI |
