CoChat
Sign Up
Cited by 59RNA and protein synthesis mechanismsRNA Research and SplicingGenomics and Phylogenetic Studies

The functional readthrough extension of malate dehydrogenase reveals a modification of the genetic code

Open access
Hofhuis, Julia, Schueren, Fabian, Nötzel, Christopher, Lingner, Thomas, Gärtner, Jutta, Jahn, Olaf, Thoms, Sven·2016·Open Biology
DOI 10.1098/rsob.160246PMC PMC5133446
Open this paper in CoChat — free account

Abstract

Translational readthrough gives rise to C-terminally extended proteins, thereby providing the cell with new protein isoforms. These may have different properties from the parental proteins if the extensions contain functional domains. While for most genes amino acid incorporation at the stop codon is far lower than 0.1%, about 4% of malate dehydrogenase (MDH1) is physiologically extended by translational readthrough and the actual ratio of MDH1x (e x tended protein) to ‘normal' MDH1 is dependent on the cell type. In human cells, arginine and tryptophan are co-encoded by the MDH1x UGA stop codon. Readthrough is controlled by the 7-nucleotide high-readthrough stop codon context without contribution of the subsequent 50 nucleotides encoding the extension. All vertebrate MDH1x is directed to peroxisomes via a hidden peroxisomal targeting signal (PTS) in the readthrough extension, which is more highly conserved than the extension of lactate dehydrogenase B. The hidden PTS of non-mammalian MDH1x evolved to be more efficient than the PTS of mammalian MDH1x. These results provide insight into the genetic and functional co-evolution of these dually localized dehydrogenases.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1098/rsob.160246

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 79

  1. [1]Hofstetter H, Monstein HJ, Weissmann C 1974 The readthrough protein A1 is essential for the formation of viable Q beta particles. Biochim. Biophys. Acta 374, 238– 251. (doi:10.1016/0005-2787(74)90366-9) 4611493 · DOI
  2. [2]Pelham HR 1978 Leaky UAG termination codon in tobacco mosaic virus RNA. Nature 272, 469– 471. (doi:10.1038/272469a0) 634374 · DOI
  3. [3]Weiner AM, Weber K 1971 Natural readthrough at the UGA termination signal of Q-beta coat protein cistron. Nat. New Biol. 234, 206– 209. (doi:10.1038/newbio234206a0) 5288807 · DOI
  4. [4]Engelberg-Kulka H, Dekel L, Israeli-Reches M, Belfort M 1979 The requirement of nonsense suppression for the development of several phages. Mol. Gen. Genet. 170, 155– 159. (doi:10.1007/BF00337791) 372760 · DOI
  5. [5]Geller AI, Rich A 1980 A UGA termination suppression tRNATrp active in rabbit reticulocytes. Nature 283, 41– 46. (doi:10.1038/283041a0) 7350525 · DOI
  6. [6]Yamaguchi Y, Hayashi A, Campagnoni CW, Kimura A, Inuzuka T, Baba H 2012 L-MPZ, a novel isoform of myelin P0, is produced by stop codon readthrough. J. Biol. Chem. 287, 17 765– 17 776. (doi:10.1074/jbc.M111.314468) PMC3366853 22457349 · DOI
  7. [7]Yates JL, Gette WR, Furth ME, Nomura M 1977 Effects of ribosomal mutations on the read-through of a chain termination signal: studies on the synthesis of bacteriophage lambda O gene protein in vitro. Proc. Natl Acad. Sci. USA 74, 689– 693. (doi:10.1073/pnas.74.2.689) 322139 PMC392358 · DOI
  8. [8]Dunn JG, Foo CK, Belletier NG, Gavis ER, Weissman JS 2013 Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster. Elife 2, e01179 (doi:10.7554/eLife.01179) 24302569 PMC3840789 · DOI
  9. [9]Jungreis I, Lin MF, Spokony R, Chan CS, Negre N, Victorsen A, White KP, Kellis M 2011 Evidence of abundant stop codon readthrough in Drosophila and other metazoa. Genome Res. 21, 2096– 2113. (doi:10.1101/gr.119974.110) 21994247 PMC3227100 · DOI
  10. [10]Lin MF et al. 2007 Revisiting the protein-coding gene catalog of Drosophila melanogaster using 12 fly genomes. Genome Res. 17, 1823– 1836. (doi:10.1101/gr.6679507) 17989253 PMC2099591 · DOI
  11. [11]Chittum HS, Lane WS, Carlson BA, Roller PP, Lung F-DT, Lee BJ, Hatfield DL 1998 Rabbit β-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps. Biochemistry 37, 10 866– 10 870. (doi:10.1021/bi981042r) 9692979 · DOI
  12. [12]Eswarappa SM et al. 2014 Programmed translational readthrough generates antiangiogenic VEGF-Ax. Cell 157, 1605– 1618. (doi:10.1016/j.cell.2014.04.033) 24949972 PMC4113015 · DOI
  13. [13]Hatfield D, Thorgeirsson SS, Copeland TD, Oroszlan S, Bustin M 1988 Immunopurification of the suppressor tRNA dependent rabbit beta-globin readthrough protein. Biochemistry 27, 1179– 1183. (doi:10.1021/bi00404a017) 3365379 · DOI
  14. [14]Loughran G, Chou M-Y, Ivanov IP, Jungreis I, Kellis M, Kiran AM, Baranov PV, Atkins JF 2014 Evidence of efficient stop codon readthrough in four mammalian genes. Nucleic Acids Res. 42, 8928– 8938. (doi:10.1093/nar/gku608) 25013167 PMC4132726 · DOI
  15. [15]Schueren F, Lingner T, George R, Hofhuis J, Dickel C, Gärtner J, Thoms S 2014 Peroxisomal lactate dehydrogenase is generated by translational readthrough in mammals. Elife 3, e03640 (doi:10.7554/eLife.03640) 25247702 PMC4359377 · DOI · Paper page
  16. [16]Stiebler AC, Freitag J, Schink KO, Stehlik T, Tillmann BAM, Ast J, Bölker M 2014 Ribosomal readthrough at a short UGA stop codon context triggers dual localization of metabolic enzymes in fungi and animals. PLoS Genet. 10, e1004685 (doi:10.1371/journal.pgen.1004685) 25340584 PMC4207609 · DOI
  17. [17]Schueren F, Thoms S 2016 Functional translational readthrough: a systems biology perspective. PLOS Genet 12, e1006196 (doi:10.1371/journal.pgen.1006196) 27490485 PMC4973966 · DOI
  18. [18]Beznosková P, Cuchalová L, Wagner S, Shoemaker CJ, Gunišová S, von der Haar T, Valášek LS 2013 Translation initiation factors eIF3 and HCR1 control translation termination and stop codon readthrough in yeast cells. PLoS Genet. 9, e1003962 (doi:10.1371/journal.pgen.1003962) 24278036 PMC3836723 · DOI
  19. [19]Beznosková P, Wagner S, Jansen ME, von der Haar T, Valášek LS 2015 Translation initiation factor eIF3 promotes programmed stop codon readthrough. Nucleic Acids Res. 43, 5099– 5111. (doi:10.1093/nar/gkv421) 25925566 PMC4446449 · DOI
  20. [20]Baranov PV, Gesteland RF, Atkins JF 2002 Recoding: translational bifurcations in gene expression. Gene 286, 187– 201. (doi:10.1016/S0378-1119(02)00423-7) 11943474 · DOI
  21. [21]Beier H, Grimm M 2001 Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res. 29, 4767– 4782. (doi:10.1093/nar/29.23.4767) 11726686 PMC96686 · DOI
  22. [22]Firth AE, Wills NM, Gesteland RF, Atkins JF 2011 Stimulation of stop codon readthrough: frequent presence of an extended 3′ RNA structural element. Nucleic Acids Res. 39, 6679– 6691. (doi:10.1093/nar/gkr224) 21525127 PMC3159437 · DOI
  23. [23]Harrell L, Melcher U, Atkins JF 2002 Predominance of six different hexanucleotide recoding signals 3′ of readthrough stop codons. Nucleic Acids Res. 30, 2011– 2017. (doi:10.1093/nar/30.9.2011) 11972340 PMC113845 · DOI
  24. [24]Skuzeski JM, Nichols LM, Gesteland RF, Atkins JF 1991 The signal for a leaky UAG stop codon in several plant viruses includes the two downstream codons. J. Mol. Biol. 218, 365– 373. (doi:10.1016/0022-2836(91)90718-L) 2010914 · DOI
  25. [25]Beier H, Barciszewska M, Krupp G, Mitnacht R, Gross HJ 1984 UAG readthrough during TMV RNA translation: isolation and sequence of two tRNAs with suppressor activity from tobacco plants. EMBO J. 3, 351– 356. 16453503 PMC557348
  26. [26]Goelet P, Lomonossoff GP, Butler PJ, Akam ME, Gait MJ, Karn J 1982 Nucleotide sequence of tobacco mosaic virus RNA. Proc. Natl Acad. Sci. USA 79, 5818– 5822. (doi:10.1073/pnas.79.19.5818) 6964389 PMC347001 · DOI
  27. [27]McCaughan KK, Brown CM, Dalphin ME, Berry MJ, Tate WP 1995 Translational termination efficiency in mammals is influenced by the base following the stop codon. Proc. Natl Acad. Sci. USA 92, 5431– 5435. (doi:10.1073/pnas.92.12.5431) 7777525 PMC41708 · DOI · Paper page
  28. [28]Namy O, Hatin I, Rousset JP 2001 Impact of the six nucleotides downstream of the stop codon on translation termination. EMBO Rep. 2, 787– 793. (doi:10.1093/embo-reports/kve176) 11520858 PMC1084031 · DOI
  29. [29]Yoshinaka Y, Katoh I, Copeland TD, Oroszlan S 1985 Translational readthrough of an amber termination codon during synthesis of feline leukemia virus protease. J. Virol. 55, 870– 873. 2991607 PMC255078
  30. [30]Bidou L, Allamand V, Rousset J-P, Namy O 2012 Sense from nonsense: therapies for premature stop codon diseases. Trends Mol. Med. 18, 679– 688. (doi:10.1016/j.molmed.2012.09.008) 23083810 · DOI
  31. [31]Keeling KM, Xue X, Gunn G, Bedwell DM 2014 Therapeutics based on stop codon readthrough. Annu. Rev. Genomics Hum. Genet. 15, 371– 394. (doi:10.1146/annurev-genom-091212-153527) 24773318 PMC5304456 · DOI · Paper page
  32. [32]François B, Russell RJM, Murray JB, Aboul-ela F, Masquida B, Vicens Q, Westhof E 2005 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. (doi:10.1093/nar/gki862) 16214802 PMC1251667 · DOI
  33. [33]Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK 2006 Peroxisomal beta-oxidation---a metabolic pathway with multiple functions. Biochim. Biophys. Acta 1763, 1413– 1426. (doi:10.1016/j.bbamcr.2006.08.034) 17028011 · DOI
  34. [34]Lodhi IJ, Semenkovich CF 2014 Peroxisomes: a nexus for lipid metabolism and cellular signaling. Cell Metab. 19, 380– 392. (doi:10.1016/j.cmet.2014.01.002) 24508507 PMC3951609 · DOI · Paper page
  35. [35]Gould SJ, Keller GA, Hosken N, Wilkinson J, Subramani S 1989 A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108, 1657– 1664. (doi:10.1083/jcb.108.5.1657) 2654139 PMC2115556 · DOI
  36. [36]Brocard C, Hartig A 2006 Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim. Biophys. Acta 1763, 1565– 1573. (doi:10.1016/j.bbamcr.2006.08.022) 17007944 · DOI
  37. [37]Freitas MO, Francisco T, Rodrigues TA, Lismont C, Domingues P, Pinto MP, Grou CP, Fransen M, Azevedo JE 2015 The peroxisomal protein import machinery displays a preference for monomeric substrates. Open Biol. 5, 140236 (doi:10.1098/rsob.140236) 25854684 PMC4422123 · DOI
  38. [38]Thoms S 2015 Import of proteins into peroxisomes: piggybacking to a new home away from home. Open Biol. 5, 150148 (doi:10.1098/rsob.150148) 26581572 PMC4680570 · DOI
  39. [39]Freitag J, Ast J, Bölker M 2012 Cryptic peroxisomal targeting via alternative splicing and stop codon readthrough in fungi. Nature 485, 522– 525. (doi:10.1038/nature11051) 22622582 · DOI
  40. [40]Beeckmans S, Kanarek L 1981 Demonstration of physical interactions between consecutive enzymes of the citric acid cycle and of the aspartate-malate shuttle. Eur. J. Biochem. 117, 527– 535. (doi:10.1111/j.1432-1033.1981.tb06369.x) 7285903 · DOI
  41. [41]Gronemeyer T et al. 2013 The proteome of human liver peroxisomes: identification of five new peroxisomal constituents by a label-free quantitative proteomics survey. PLoS ONE 8, e57395 (doi:10.1371/journal.pone.0057395) 23460848 PMC3583843 · DOI
  42. [43]Zaher HS, Green R 2009 Fidelity at the molecular level: lessons from protein synthesis. Cell 136, 746– 762. (doi:10.1016/j.cell.2009.01.036) 19239893 PMC3691815 · DOI
  43. [44]Westhof E, Yusupov M, Yusupova G 2014 Recognition of Watson-Crick base pairs: constraints and limits due to geometric selection and tautomerism. F1000Prime Rep. 6, 19 (doi:10.12703/P6-19) 24765524 PMC3974571 · DOI
  44. [45]Demeshkina N, Jenner L, Westhof E, Yusupov M, Yusupova G 2013 New structural insights into the decoding mechanism: translation infidelity via a G·U pair with Watson-Crick geometry. FEBS Lett. 587, 1848– 1857. (doi:10.1016/j.febslet.2013.05.009) 23707250 · DOI
  45. [46]Blanchet S, Cornu D, Argentini M, Namy O 2014 New insights into the incorporation of natural suppressor tRNAs at stop codons in Saccharomyces cerevisiae. Nucleic Acids Res. 42, 10 061– 10 072. (doi:10.1093/nar/gku663) PMC4150775 25056309 · DOI
  46. [47]Roy B, Leszyk JD, Mangus DA, Jacobson A 2015 Nonsense suppression by near-cognate tRNAs employs alternative base pairing at codon positions 1 and 3. Proc. Natl Acad. Sci. USA 112, 3038– 3043. (doi:10.1073/pnas.1424127112) 25733896 PMC4364220 · DOI
  47. [48]Hirsh D 1971 Tryptophan transfer RNA as the UGA suppressor. J. Mol. Biol. 58, 439– 458. (doi:10.1016/0022-2836(71)90362-7) 4933412 · DOI
  48. [49]Urban C, Beier H 1995 Cysteine tRNAs of plant origin as novel UGA suppressors. Nucleic Acids Res. 23, 4591– 4597. (doi:10.1093/nar/23.22.4591) 8524647 PMC307430 · DOI
  49. [50]Zerfass K, Beier H 1992 The leaky UGA termination codon of tobacco rattle virus RNA is suppressed by tobacco chloroplast and cytoplasmic tRNAs(Trp) with CmCA anticodon. EMBO J. 11, 4167– 4173. 1396598 PMC556927
  50. [51]Feng YX, Copeland TD, Oroszlan S, Rein A, Levin JG 1990 Identification of amino acids inserted during suppression of UAA and UGA termination codons at the gag-pol junction of Moloney murine leukemia virus. Proc. Natl Acad. Sci. USA 87, 8860– 8863. (doi:10.1073/pnas.87.22.8860) 2247457 PMC55059 · DOI
  51. [52]Beznosková P, Gunišová S, Valášek LS 2016 Rules of UGA-N decoding by near-cognate tRNAs and analysis of readthrough on short uORFs in yeast. RNA 22, 456– 466. (doi:10.1261/rna.054452.115) 26759455 PMC4748822 · DOI
  52. [53]Eubel H et al. 2008 Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol. 148, 1809– 1829. (doi:10.1104/pp.108.129999) 18931141 PMC2593673 · DOI
  53. [54]Fukao Y, Hayashi M, Nishimura M 2002 Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol. 43, 689– 696. (doi:10.1093/pcp/pcf101) 12154131 · DOI
  54. [55]Pracharoenwattana I, Cornah JE, Smith SM 2007 Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle. Plant J. 50, 381– 390. (doi:10.1111/j.1365-313X.2007.03055.x) 17376163 · DOI
  55. [56]Reumann S et al. 2007 Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19, 3170– 3193. (doi:10.1105/tpc.107.050989) 17951448 PMC2174697 · DOI
  56. [57]Reumann S et al. 2009 In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol. 150, 125– 143. (doi:10.1104/pp.109.137703) 19329564 PMC2675712 · DOI
  57. [58]Marelli M et al. 2004 Quantitative mass spectrometry reveals a role for the GTPase Rho1p in actin organization on the peroxisome membrane. J. Cell Biol. 167, 1099– 1112. (doi:10.1083/jcb.200404119) 15596542 PMC2172632 · DOI
  58. [59]van Roermund CW, Elgersma Y, Singh N, Wanders RJ, Tabak HF 1995 The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J. 14, 3480– 3486. 7628449 PMC394415
  59. [60]Schäfer H, Nau K, Sickmann A, Erdmann R, Meyer HE 2001 Identification of peroxisomal membrane proteins of Saccharomyces cerevisiae by mass spectrometry. Electrophoresis 22, 2955– 2968. (doi:10.1002/1522-2683(200108)22:14<2955::AID-ELPS2955>3.0.CO;2-U) 11565790 · DOI
  60. [61]Smith JJ, Sydorskyy Y, Marelli M, Hwang D, Bolouri H, Rachubinski RA, Aitchison JD 2006 Expression and functional profiling reveal distinct gene classes involved in fatty acid metabolism. Mol. Syst. Biol. 2, 20060009 (doi:10.1038/msb4100051) PMC1681483 16738555 · DOI
  61. [62]Steffan JS, McAlister-Henn L 1992 Isolation and characterization of the yeast gene encoding the MDH3 isozyme of malate dehydrogenase. J. Biol. Chem. 267, 24 708– 24 715. 1447211
  62. [63]Yi EC, Marelli M, Lee H, Purvine SO, Aebersold R, Aitchison JD, Goodlett DR 2002 Approaching complete peroxisome characterization by gas-phase fractionation. Electrophoresis 23, 3205– 3216. (doi:10.1002/1522-2683(200209)23:18<3205::AID-ELPS3205>3.0.CO;2-Y) 12298092 · DOI
  63. [64]Kabran P, Rossignol T, Gaillardin C, Nicaud J-M, Neuvéglise C 2012 Alternative splicing regulates targeting of malate dehydrogenase in Yarrowia lipolytica. DNA Res. 19, 231– 244. (doi:10.1093/dnares/dss007) 22368181 PMC3372373 · DOI
  64. [65]Antonenkov VD, Sormunen RT, Hiltunen JK 2004 The rat liver peroxisomal membrane forms a permeability barrier for cofactors but not for small metabolites in vitro. J. Cell. Sci. 117, 5633– 5642. (doi:10.1242/jcs.01485) 15509867 · DOI
  65. [66]Visser WF, van Roermund CWT, Ijlst L, Waterham HR, Wanders RJA 2007 Metabolite transport across the peroxisomal membrane. Biochem. J. 401, 365– 375. (doi:10.1042/BJ20061352) 17173541 PMC1820816 · DOI
  66. [68]Safer B 1975 The metabolic significance of the malate-aspartate cycle in heart. Circ. Res. 37, 527– 533. (doi:10.1161/01.RES.37.5.527) 172258 · DOI
  67. [69]Lehninger AL 1951 Phosphorylation coupled to oxidation of dihydrodiphosphopyridine nucleotide. J. Biol. Chem. 190, 345– 359. 14841183
  68. [70]Wolinski H, Petrovic U, Mattiazzi M, Petschnigg J, Heise B, Natter K, Kohlwein SD 2009 Imaging-based live cell yeast screen identifies novel factors involved in peroxisome assembly. J. Proteome Res. 8, 20– 27. (doi:10.1021/pr800782n) 19118449 · DOI
  69. [71]Gebhardt JS, Wadsworth GJ, Matthews BF 1998 Characterization of a single soybean cDNA encoding cytosolic and glyoxysomal isozymes of aspartate aminotransferase. Plant Mol. Biol. 37, 99– 108. (doi:10.1023/A:1005973019045) 9620268 · DOI
  70. [72]Schultz CJ, Coruzzi GM 1995 The aspartate aminotransferase gene family of Arabidopsis encodes isoenzymes localized to three distinct subcellular compartments. Plant J. 7, 61– 75. (doi:10.1046/j.1365-313X.1995.07010061.x) 7894512 · DOI
  71. [73]Verleur N, Elgersma Y, Van Roermund CW, Tabak HF, Wanders RJ 1997 Cytosolic aspartate aminotransferase encoded by the AAT2 gene is targeted to the peroxisomes in oleate-grown Saccharomyces cerevisiae. Eur. J. Biochem. 247, 972– 980. (doi:10.1111/j.1432-1033.1997.00972.x) 9288922 · DOI
  72. [74]Goward CR, Nicholls DJ 1994 Malate dehydrogenase: a model for structure, evolution, and catalysis. Protein Sci. 3, 1883– 1888. (doi:10.1002/pro.5560031027) 7849603 PMC2142602 · DOI
  73. [75]Cendrin F, Chroboczek J, Zaccai G, Eisenberg H, Mevarech M 1993 Cloning, sequencing, and expression in Escherichia coli of the gene coding for malate dehydrogenase of the extremely halophilic archaebacterium Haloarcula marismortui. Biochemistry 32, 4308– 4313. (doi:10.1021/bi00067a020) 8476859 · DOI
  74. [76]Richard SB, Madern D, Garcin E, Zaccai G 2000 Halophilic adaptation: novel solvent protein interactions observed in the 2.9 and 2.6 A resolution structures of the wild type and a mutant of malate dehydrogenase from Haloarcula marismortui. Biochemistry 39, 992– 1000. (doi:10.1021/bi991001a) 10653643 · DOI
  75. [77]Wilks HM et al. 1988 A specific, highly active malate dehydrogenase by redesign of a lactate dehydrogenase framework. Science 242, 1541– 1544. (doi:10.1126/science.3201242) 3201242 · DOI
  76. [78]Wagner E et al. 2012 Stimulated emission depletion live-cell super-resolution imaging shows proliferative remodeling of T-tubule membrane structures after myocardial infarction. Circ. Res. 111, 402– 414. (doi:10.1161/CIRCRESAHA.112.274530) 22723297 PMC4219578 · DOI
  77. [79]Wagner E, Brandenburg S, Kohl T, Lehnart SE 2014 Analysis of tubular membrane networks in cardiac myocytes from atria and ventricles. J. Vis. Exp. e51823 (doi:10.3791/51823) 25350293 PMC4541455 · DOI
  78. [80]Schmidt C, Hesse D, Raabe M, Urlaub H, Jahn O 2013 An automated in-gel digestion/iTRAQ-labeling workflow for robust quantification of gel-separated proteins. Proteomics 13, 1417– 1422. (doi:10.1002/pmic.201200366) 23456960 · DOI
  79. [81]Ott C et al 2015 Widespread expression of erythropoietin receptor in brain and its induction by injury. Mol. Med. 21, 803–815 (doi:10.2119/molmed.2015.00192) PMC4818269 26349059 · DOI

Cited by

Sorted by citations

Authors
Hofhuis, J., Schueren, F., Nötzel, C., Lingner, T., Gärtner, J., Jahn, O., & Thoms, S.
Affiliations
  • Universitätsmedizin Göttingen (DE)
  • Max Planck Institute of Experimental Medicine (DE)
Corresponding author
Thoms, Sven
ORCID
Venue
Open Biology
Publisher
The Royal Society
Published
2016-11
Volume
6
Issue
11
Pages
160246
ISSN
2046-2441 (ISSN-L)
DOI
10.1098/rsob.160246
PMC
PMC5133446
OpenAlex
W2550546953
Cited by
59
References
2
Citations by year
2026: 5 · 2025: 5 · 2024: 8 · 2023: 3 · 2022: 12 · 2021: 7 · 2020: 2 · 2019: 5 · 2018: 8 · 2017: 4
FWCI
2.42
Type
journal article
Language
en
Open access
Licence
Locations
  • Open Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
  • GRO (submittedVersion, cc-by)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
Deutsche Forschungsgemeinschaft (SFB1002/2 (TP 10A))
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
translational readthrough, malate dehydrogenase, MDH1, stop codon, UGA codon, genetic code, protein isoforms, peroxisomal targeting signal, peroxisome targeting, LDHB, coevolution
MeSH terms
Animals, Arginine, Cell Line, Genetic Code, HeLa Cells, Humans, Malate Dehydrogenase, Protein Biosynthesis, Tryptophan, Codon, Terminator, Peroxisomes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review