Zebrafish rbm8a and magoh mutants reveal EJC developmental functions and new 3′UTR intron-containing NMD targets
Autoři:
Pooja Gangras aff001; Thomas L. Gallagher aff001; Michael A. Parthun aff001; Zhongxia Yi aff001; Robert D. Patton aff002; Kiel T. Tietz aff001; Natalie C. Deans aff001; Ralf Bundschuh aff002; Sharon L. Amacher aff001; Guramrit Singh aff001
Působiště autorů:
Department of Molecular Genetics, The Ohio State University, Ohio, United States of America
aff001; Center for RNA Biology, The Ohio State University, Ohio, United States of America
aff002; Department of Physics, The Ohio State University, Ohio, United States of America
aff003; Department of Chemistry and Biochemistry, The Ohio State University, Ohio, United States of America
aff004; Division of Hematology, Department of Internal Medicine, The Ohio State University, Ohio, United States of America
aff005; Department of Biological Chemistry and Pharmacology, The Ohio State University, Ohio, United States of America
aff006; Center for Muscle Health and Neuromuscular Disorders, The Ohio State University and Nationwide Children’s Hospital, Ohio, United States of America
aff007
Vyšlo v časopise:
Zebrafish rbm8a and magoh mutants reveal EJC developmental functions and new 3′UTR intron-containing NMD targets. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008830
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008830
Souhrn
Many post-transcriptional mechanisms operate via mRNA 3′UTRs to regulate protein expression, and such controls are crucial for development. We show that homozygous mutations in two zebrafish exon junction complex (EJC) core genes rbm8a and magoh leads to muscle disorganization, neural cell death, and motor neuron outgrowth defects, as well as dysregulation of mRNAs subjected to nonsense-mediated mRNA decay (NMD) due to translation termination ≥ 50 nts upstream of the last exon-exon junction. Intriguingly, we find that EJC-dependent NMD also regulates a subset of transcripts that contain 3′UTR introns (3′UI) < 50 nts downstream of a stop codon. Some transcripts containing such stop codon-proximal 3′UI are also NMD-sensitive in cultured human cells and mouse embryonic stem cells. We identify 167 genes that contain a conserved proximal 3′UI in zebrafish, mouse and humans. foxo3b is one such proximal 3′UI-containing gene that is upregulated in zebrafish EJC mutant embryos, at both mRNA and protein levels, and loss of foxo3b function in EJC mutant embryos significantly rescues motor axon growth defects. These data are consistent with EJC-dependent NMD regulating foxo3b mRNA to control protein expression during zebrafish development. Our work shows that the EJC is critical for normal zebrafish development and suggests that proximal 3′UIs may serve gene regulatory function in vertebrates.
Klíčová slova:
Axons – Embryos – Gene expression – Gene regulation – Introns – Messenger RNA – Motor neurons – Zebrafish
Zdroje
1. Mayr C. Regulation by 3′-Untranslated Regions. Annu Rev Genet. 2017;51(1):171–94.
2. Bartel DP. MicroRNAs: Target Recognition and Regulatory Functions. Cell. 2009 Jan 23;136(2):215–33. doi: 10.1016/j.cell.2009.01.002 19167326
3. Matoulkova E, Michalova E, Vojtesek B, Hrstka R. The role of the 3’ untranslated region in post-transcriptional regulation of protein expression in mammalian cells. RNA Biol. 2012 May;9(5):563–76. doi: 10.4161/rna.20231 22614827
4. Mayr C. Evolution and Biological Roles of Alternative 3’UTRs. Trends Cell Biol. 2016 Mar;26(3):227–37. doi: 10.1016/j.tcb.2015.10.012 26597575
5. Tian B, Manley JL. Alternative polyadenylation of mRNA precursors. Nat Rev Mol Cell Biol. 2017;18(1):18–30. doi: 10.1038/nrm.2016.116 27677860
6. Brinegar AE, Cooper TA. Roles for RNA-binding proteins in development and disease. Brain Res. 2016 15;1647:1–8. doi: 10.1016/j.brainres.2016.02.050 26972534
7. Lennox AL, Mao H, Silver DL. RNA on the brain: emerging layers of post-transcriptional regulation in cerebral cortex development. Wiley Interdiscip Rev Dev Biol. 2018;7(1).
8. Le Hir H, Moore MJ, Maquat LE. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 2000 May 1;14(9):1098–108. 10809668
9. Le Hir H, Izaurralde E, Maquat LE, Moore MJ. The spliceosome deposits multiple proteins 20–24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 2000 Dec 15;19(24):6860–9. doi: 10.1093/emboj/19.24.6860 11118221
10. Merz C, Urlaub H, Will CL, Lührmann R. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA. 2007 Jan;13(1):116–28. doi: 10.1261/rna.336807 17095540
11. Woodward LA, Mabin JW, Gangras P, Singh G. The exon junction complex: a lifelong guardian of mRNA fate. Wiley Interdiscip Rev RNA. 2016 Dec 23;
12. Le Hir H, Saulière J, Wang Z. The exon junction complex as a node of post-transcriptional networks. Nat Rev Mol Cell Biol. 2016 Jan;17(1):41–54. doi: 10.1038/nrm.2015.7 26670016
13. Boehm V, Gehring NH. Exon Junction Complexes: Supervising the Gene Expression Assembly Line. Trends Genet. 2016;32(11):724–35. doi: 10.1016/j.tig.2016.09.003 27667727
14. Singh G, Pratt G, Yeo GW, Moore MJ. The Clothes Make the mRNA: Past and Present Trends in mRNP Fashion. Annu Rev Biochem. 2015;84:325–54. doi: 10.1146/annurev-biochem-080111-092106 25784054
15. Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW. Disassembly of exon junction complexes by PYM. Cell. 2009 May 1;137(3):536–48. doi: 10.1016/j.cell.2009.02.042 19410547
16. Dostie J, Dreyfuss G. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr Biol CB. 2002 Jul 9;12(13):1060–7. doi: 10.1016/s0960-9822(02)00902-8 12121612
17. Maquat LE. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol. 2004 Feb;5(2):89–99. doi: 10.1038/nrm1310 15040442
18. Karousis ED, Nasif S, Mühlemann O. Nonsense-mediated mRNA decay: novel mechanistic insights and biological impact. Wiley Interdiscip Rev RNA. 2016;7(5):661–82. doi: 10.1002/wrna.1357 27173476
19. McGlincy NJ, Smith CWJ. Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem Sci. 2008 Aug;33(8):385–93. doi: 10.1016/j.tibs.2008.06.001 18621535
20. Colak D, Ji S-J, Porse BT, Jaffrey SR. Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell. 2013 Jun 6;153(6):1252–65. doi: 10.1016/j.cell.2013.04.056 23746841
21. Zheng S, Gray EE, Chawla G, Porse BT, O’Dell TJ, Black DL. PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2. Nat Neurosci. 2012 Jan 15;15(3):381–8, S1. doi: 10.1038/nn.3026 22246437
22. Schweingruber C, Rufener SC, Zünd D, Yamashita A, Mühlemann O. Nonsense-mediated mRNA decay—mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta. 2013 Jul;1829(6–7):612–23. doi: 10.1016/j.bbagrm.2013.02.005 23435113
23. Lykke-Andersen S, Jensen TH. Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol. 2015 Nov;16(11):665–77. doi: 10.1038/nrm4063 26397022
24. Bicknell AA, Cenik C, Chua HN, Roth FP, Moore MJ. Introns in UTRs: why we should stop ignoring them. BioEssays News Rev Mol Cell Dev Biol. 2012 Dec;34(12):1025–34.
25. Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, et al. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell. 2007 Jul 13;130(1):179–91. doi: 10.1016/j.cell.2007.05.028 17632064
26. Newmark PA, Boswell RE. The mago nashi locus encodes an essential product required for germ plasm assembly in Drosophila. Dev. 1994 May;120(5):1303–13.
27. Micklem DR, Dasgupta R, Elliott H, Gergely F, Davidson C, Brand A, et al. The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila. Curr Biol. 1997 Jul 1;7(7):468–78. doi: 10.1016/s0960-9822(06)00218-1 9210377
28. Favaro FP, Alvizi L, Zechi-Ceide RM, Bertola D, Felix TM, de Souza J, et al. A noncoding expansion in EIF4A3 causes Richieri-Costa-Pereira syndrome, a craniofacial disorder associated with limb defects. Am J Hum Genet. 2014 Jan 2;94(1):120–8. doi: 10.1016/j.ajhg.2013.11.020 24360810
29. Albers CA, Paul DS, Schulze H, Freson K, Stephens JC, Smethurst PA, et al. Compound inheritance of a low-frequency regulatory SNP and a rare null mutation in exon-junction complex subunit RBM8A causes TAR syndrome. Nat Genet. 2012 Apr;44(4):435–9, S1-2. doi: 10.1038/ng.1083 22366785
30. Mao H, Pilaz L-J, McMahon JJ, Golzio C, Wu D, Shi L, et al. Rbm8a haploinsufficiency disrupts embryonic cortical development resulting in microcephaly. J Neurosci. 2015 May 6;35(18):7003–18. doi: 10.1523/JNEUROSCI.0018-15.2015 25948253
31. Mao H, McMahon JJ, Tsai Y-H, Wang Z, Silver DL. Haploinsufficiency for Core Exon Junction Complex Components Disrupts Embryonic Neurogenesis and Causes p53-Mediated Microcephaly. PLoS Genet [Internet]. 2016 Sep 12;12(9).
32. Haremaki T, Sridharan J, Dvora S, Weinstein DC. Regulation of vertebrate embryogenesis by the exon junction complex core component Eif4a3. Dev Dyn. 2010 Jul;239(7):1977–87. doi: 10.1002/dvdy.22330 20549732
33. Haremaki T, Weinstein DC. Eif4a3 is required for accurate splicing of the Xenopus laevis ryanodine receptor pre-mRNA. Dev Biol. 2012 Dec 1;372(1):103–10. doi: 10.1016/j.ydbio.2012.08.013 22944195
34. Zou D, McSweeney C, Sebastian A, Reynolds DJ, Dong F, Zhou Y, et al. A critical role of RBM8a in proliferation and differentiation of embryonic neural progenitors. Neural Develop. 2015;10:18.
35. Silver DL, Leeds KE, Hwang H-W, Miller EE, Pavan WJ. The EJC component Magoh regulates proliferation and expansion of neural crest-derived melanocytes. Dev Biol. 2013 Mar 15;375(2):172–81. doi: 10.1016/j.ydbio.2013.01.004 23333945
36. McMahon JJ, Miller EE, Silver DL. The exon junction complex in neural development and neurodevelopmental disease. Int J Dev Neurosci. 2016 Dec;55:117–23. doi: 10.1016/j.ijdevneu.2016.03.006 27071691
37. Pilaz L-J, McMahon JJ, Miller EE, Lennox AL, Suzuki A, Salmon E, et al. Prolonged Mitosis of Neural Progenitors Alters Cell Fate in the Developing Brain. Neuron. 2016 Jan 6;89(1):83–99. doi: 10.1016/j.neuron.2015.12.007 26748089
38. Shibuya T, Tange TØ, Sonenberg N, Moore MJ. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat Struct Mol Biol. 2004 Apr;11(4):346–51. doi: 10.1038/nsmb750 15034551
39. Palacios IM, Gatfield D, St Johnston D, Izaurralde E. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature. 2004 Feb 19;427(6976):753–7. doi: 10.1038/nature02351 14973490
40. Ballut L, Marchadier B, Baguet A, Tomasetto C, Séraphin B, Le Hir H. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat Struct Mol Biol. 2005 Oct;12(10):861–9. doi: 10.1038/nsmb990 16170325
41. Ghosh S, Marchand V, Gáspár I, Ephrussi A. Control of RNP motility and localization by a splicing-dependent structure in oskar mRNA. Nat Struct Mol Biol. 2012 Mar 18;19(4):441–9. doi: 10.1038/nsmb.2257 22426546
42. Singh G, Kucukural A, Cenik C, Leszyk JD, Shaffer SA, Weng Z, et al. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell. 2012 Nov 9;151(4):750–64. doi: 10.1016/j.cell.2012.10.007 23084401
43. Saulière J, Murigneux V, Wang Z, Marquenet E, Barbosa I, Le Tonquèze O, et al. CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat Struct Mol Biol. 2012 Nov;19(11):1124–31. doi: 10.1038/nsmb.2420 23085716
44. Hauer C, Sieber J, Schwarzl T, Hollerer I, Curk T, Alleaume A-M, et al. Exon Junction Complexes Show a Distributional Bias toward Alternatively Spliced mRNAs and against mRNAs Coding for Ribosomal Proteins. Cell Rep. 2016 09;16(6):1588–603. doi: 10.1016/j.celrep.2016.06.096 27475226
45. Obrdlik A, Lin G, Haberman N, Ule J, Ephrussi A. The Transcriptome-wide Landscape and Modalities of EJC Binding in Adult Drosophila. Cell Rep. 2019 Jul 30;28(5):1219–1236.e11. doi: 10.1016/j.celrep.2019.06.088 31365866
46. Mabin JW, Woodward LA, Patton RD, Yi Z, Jia M, Wysocki VH, et al. The Exon Junction Complex Undergoes a Compositional Switch that Alters mRNP Structure and Nonsense-Mediated mRNA Decay Activity. Cell Rep. 2018 Nov 27;25(9):2431–2446.e7. doi: 10.1016/j.celrep.2018.11.046 30466796
47. Talbot JC, Amacher SL. A Streamlined CRISPR Pipeline to Reliably Generate Zebrafish Frameshifting Alleles. Zebrafish. 2014 Dec 1;11(6):583–5. doi: 10.1089/zeb.2014.1047 25470533
48. White RJ, Collins JE, Sealy IM, Wali N, Dooley CM, Digby Z, et al. A high-resolution mRNA expression time course of embryonic development in zebrafish. eLife. 2017 16;6.
49. Ma Q, Tatsuno T, Nakamura Y, Ishigaki Y. The stability of Magoh and Y14 depends on their heterodimer formation and nuclear localization. Biochem Biophys Res Commun. 2019 Apr 9;511(3):631–6. doi: 10.1016/j.bbrc.2019.02.097 30826064
50. Anders S, Reyes A, Huber W. Detecting differential usage of exons from RNA-seq data. Genome Res. 2012 Oct 1;22(10):2008–17. doi: 10.1101/gr.133744.111 22722343
51. Wang Z, Murigneux V, Le Hir H. Transcriptome-wide modulation of splicing by the exon junction complex. Genome Biol. 2014;15(12):551. doi: 10.1186/s13059-014-0551-7 25476502
52. Hayashi R, Handler D, Ish-Horowicz D, Brennecke J. The exon junction complex is required for definition and excision of neighboring introns in Drosophila. Genes Dev. 2014 Aug 15;28(16):1772–85. doi: 10.1101/gad.245738.114 25081352
53. Blazquez L, Emmett W, Faraway R, Pineda JMB, Bajew S, Gohr A, et al. Exon Junction Complex Shapes the Transcriptome by Repressing Recursive Splicing. Mol Cell. 2018 Nov 1;72(3):496–509.e9. doi: 10.1016/j.molcel.2018.09.033 30388411
54. Wittkopp N, Huntzinger E, Weiler C, Saulière J, Schmidt S, Sonawane M, et al. Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol Cell Biol. 2009 Jul;29(13):3517–28. doi: 10.1128/MCB.00177-09 19414594
55. Longman D, Hug N, Keith M, Anastasaki C, Patton EE, Grimes G, et al. DHX34 and NBAS form part of an autoregulatory NMD circuit that regulates endogenous RNA targets in human cells, zebrafish and Caenorhabditis elegans. Nucleic Acids Res. 2013 Sep;41(17):8319–31. doi: 10.1093/nar/gkt585 23828042
56. Rodriguez JM, Maietta P, Ezkurdia I, Pietrelli A, Wesselink J-J, Lopez G, et al. APPRIS: annotation of principal and alternative splice isoforms. Nucleic Acids Res. 2013 Jan;41(Database issue):D110–117. doi: 10.1093/nar/gks1058 23161672
57. Baird TD, Cheng KC-C, Chen Y-C, Buehler E, Martin SE, Inglese J, et al. ICE1 promotes the link between splicing and nonsense-mediated mRNA decay. eLife. 2018 12;7.
58. Bazzini AA, Johnstone TG, Christiano R, Mackowiak SD, Obermayer B, Fleming ES, et al. Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation. EMBO J. 2014 May 2;33(9):981–93. doi: 10.1002/embj.201488411 24705786
59. Johnstone TG, Bazzini AA, Giraldez AJ. Upstream ORFs are prevalent translational repressors in vertebrates. EMBO J. 2016 Apr 1;35(7):706–23. doi: 10.15252/embj.201592759 26896445
60. Lareau LF, Brenner SE. Regulation of Splicing Factors by Alternative Splicing and NMD Is Conserved between Kingdoms Yet Evolutionarily Flexible. Mol Biol Evol. 2015 Apr;32(4):1072–9. doi: 10.1093/molbev/msv002 25576366
61. Martin L, Grigoryan A, Wang D, Wang J, Breda L, Rivella S, et al. Identification and characterization of small molecules that inhibit nonsense-mediated RNA decay and suppress nonsense p53 mutations. Cancer Res. 2014 Jun 1;74(11):3104–13. doi: 10.1158/0008-5472.CAN-13-2235 24662918
62. Lou CH, Shao A, Shum EY, Espinoza JL, Huang L, Karam R, et al. Posttranscriptional Control of the Stem Cell and Neurogenic Programs by the Nonsense-Mediated RNA Decay Pathway. Cell Rep. 2014 Feb 27;6(4):748–64. doi: 10.1016/j.celrep.2014.01.028 24529710
63. Li T, Shi Y, Wang P, Guachalla LM, Sun B, Joerss T, et al. Smg6/Est1 licenses embryonic stem cell differentiation via nonsense-mediated mRNA decay. EMBO J. 2015 Jun 12;34(12):1630–47. doi: 10.15252/embj.201489947 25770585
64. Morris BJ, Willcox DC, Donlon TA, Willcox BJ. FOXO3: A Major Gene for Human Longevity—A Mini-Review. Gerontology. 2015;61(6):515–25. doi: 10.1159/000375235 25832544
65. Liu X, Cai X, Zhang D, Xu C, Xiao W. Zebrafish foxo3b Negatively Regulates Antiviral Response through Suppressing the Transactivity of irf3 and irf7. J Immunol. 2016 15;197(12):4736–49. doi: 10.4049/jimmunol.1601187 27815423
66. Liu X, Cai X, Hu B, Mei Z, Zhang D, Ouyang G, et al. Forkhead Transcription Factor 3a (FOXO3a) Modulates Hypoxia Signaling via Up-regulation of the von Hippel-Lindau Gene (VHL). J Biol Chem. 2016 Dec 2;291(49):25692–705. doi: 10.1074/jbc.M116.745471 27777301
67. Rauwerda H, Wackers P, Pagano JFB, de Jong M, Ensink W, Dekker R, et al. Mother-Specific Signature in the Maternal Transcriptome Composition of Mature, Unfertilized Zebrafish Eggs. PLoS ONE. 2016 Jan 22;11(1).
68. Chuang T-W, Chang W-L, Lee K-M, Tarn W-Y. The RNA-binding protein Y14 inhibits mRNA decapping and modulates processing body formation. Mol Biol Cell. 2013 Jan;24(1):1–13. doi: 10.1091/mbc.E12-03-0217 23115303
69. Chuang T-W, Lee K-M, Tarn W-Y. Function and pathological implications of exon junction complex factor Y14. Biomolecules. 2015;5(2):343–55. doi: 10.3390/biom5020343 25866920
70. Gudikote JP, Wilkinson MF. T-cell receptor sequences that elicit strong down-regulation of premature termination codon-bearing transcripts. EMBO J. 2002 Jan 15;21(1–2):125–34. doi: 10.1093/emboj/21.1.125 11782432
71. Hoek TA, Khuperkar D, Lindeboom RGH, Sonneveld S, Verhagen BMP, Boersma S, et al. Single-Molecule Imaging Uncovers Rules Governing Nonsense-Mediated mRNA Decay. Mol Cell. 2019 25;75(2):324–339.e11. doi: 10.1016/j.molcel.2019.05.008 31155380
72. Zhang Z, Krainer AR. Involvement of SR proteins in mRNA surveillance. Mol Cell. 2004 Nov 19;16(4):597–607. doi: 10.1016/j.molcel.2004.10.031 15546619
73. Aznarez I, Nomakuchi TT, Tetenbaum-Novatt J, Rahman MA, Fregoso O, Rees H, et al. Mechanism of Nonsense-Mediated mRNA Decay Stimulation by Splicing Factor SRSF1. Cell Rep. 2018 May 15;23(7):2186–98. doi: 10.1016/j.celrep.2018.04.039 29768215
74. Mahowald GK, Mahowald MA, Moon C, Khor B, Sleckman BP. Out-of-Frame T Cell Receptor Beta Transcripts Are Eliminated by Multiple Pathways In Vivo. PLOS ONE. 2011 Jul 13;6(7):e21627. doi: 10.1371/journal.pone.0021627 21765899
75. Kishor A, Ge Z, Hogg JR. hnRNP L-dependent protection of normal mRNAs from NMD subverts quality control in B cell lymphoma. EMBO J. 2019 Feb 1;38(3).
76. Scofield DG, Lynch M. Evolutionary diversification of the Sm family of RNA-associated proteins. Mol Biol Evol. 2008 Nov;25(11):2255–67. doi: 10.1093/molbev/msn175 18687770
77. Hong X, Scofield DG, Lynch M. Intron size, abundance, and distribution within untranslated regions of genes. Mol Biol Evol. 2006 Dec;23(12):2392–404. doi: 10.1093/molbev/msl111 16980575
78. Webb AE, Brunet A. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci. 2014 Apr;39(4):159–69. doi: 10.1016/j.tibs.2014.02.003 24630600
79. Webb AE, Kundaje A, Brunet A. Characterization of the direct targets of FOXO transcription factors throughout evolution. Aging Cell. 2016;15(4):673–85. doi: 10.1111/acel.12479 27061590
80. Xie X, Liu J-X, Hu B, Xiao W. Zebrafish foxo3b negatively regulates canonical Wnt signaling to affect early embryogenesis. PloS One. 2011;6(9):e24469. doi: 10.1371/journal.pone.0024469 21915332
81. Chung YM, Park S-H, Tsai W-B, Wang S-Y, Ikeda M-A, Berek JS, et al. FOXO3 signalling links ATM to the p53 apoptotic pathway following DNA damage. Nat Commun. 2012;3:1000. doi: 10.1038/ncomms2008 22893124
82. You H, Yamamoto K, Mak TW. Regulation of transactivation-independent proapoptotic activity of p53 by FOXO3a. Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9051–6. doi: 10.1073/pnas.0600889103 16757565
83. Gilley J, Coffer PJ, Ham J. FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol. 2003 Aug 18;162(4):613–22. doi: 10.1083/jcb.200303026 12913110
84. He C-W, Liao C-P, Pan C-L. Wnt signalling in the development of axon, dendrites and synapses. Open Biol [Internet]. 2018 Oct 3;8(10).
85. Nelson JO, Moore KA, Chapin A, Hollien J, Metzstein MM. Degradation of Gadd45 mRNA by nonsense-mediated decay is essential for viability. eLife. 2016 08;5.
86. Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res. 2019 Jan 8;47(Database issue):D419–26. doi: 10.1093/nar/gky1038 30407594
87. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn Off Publ Am Assoc Anat. 1995 Jul;203(3):253–310.
88. Sander JD, Zaback P, Joung JK, Voytas DF, Dobbs D. Zinc Finger Targeter (ZiFiT): an engineered zinc finger/target site design tool. Nucleic Acids Res. 2007 Jul;35(Web Server issue):W599–605. doi: 10.1093/nar/gkm349 17526515
89. Sander JD, Maeder ML, Reyon D, Voytas DF, Joung JK, Dobbs D. ZiFiT (Zinc Finger Targeter): an updated zinc finger engineering tool. Nucleic Acids Res. 2010 Jul;38(Web Server issue):W462–468. doi: 10.1093/nar/gkq319 20435679
90. Jao L-E, Wente SR, Chen W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A. 2013 Aug 20;110(34):13904–9. doi: 10.1073/pnas.1308335110 23918387
91. Longair MH, Baker DA, Armstrong JD. Simple Neurite Tracer: open source software for reconstruction, visualization and analysis of neuronal processes. Bioinformatics. 2011 Sep 1;27(17):2453–4. doi: 10.1093/bioinformatics/btr390 21727141
92. Gallagher TL, Arribere JA, Geurts PA, Exner CRT, McDonald KL, Dill KK, et al. Rbfox-regulated alternative splicing is critical for zebrafish cardiac and skeletal muscle functions. Dev Biol. 2011 Nov 15;359(2):251–61. doi: 10.1016/j.ydbio.2011.08.025 21925157
93. Gangras P, Dayeh DM, Mabin JW, Nakanishi K, Singh G. Cloning and Identification of Recombinant Argonaute-Bound Small RNAs Using Next-Generation Sequencing. Methods Mol Biol Clifton NJ. 2018;1680:1–28.
94. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013 Apr 25;14(4):R36. doi: 10.1186/gb-2013-14-4-r36 23618408
95. Love MI, Anders S, Kim V, Huber W. RNA-Seq workflow: gene-level exploratory analysis and differential expression. F1000Research. 2015;4:1070. doi: 10.12688/f1000research.7035.1 26674615
96. Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M, Gentleman R, et al. Software for Computing and Annotating Genomic Ranges. PLOS Comput Biol. 2013 Aug 8;9(8):e1003118. doi: 10.1371/journal.pcbi.1003118 23950696
97. Morgan M, Obenchain V, Hester J, Pagès H. SummarizedExperiment: SummarizedExperiment container. 2019. R package version 1.18.1.
98. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014 Dec 5;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281
99. Risso D, Ngai J, Speed TP, Dudoit S. Normalization of RNA-seq data using factor analysis of control genes or samples. Nat Biotechnol. 2014 Sep;32(9):896–902. doi: 10.1038/nbt.2931 25150836
100. Strimmer K. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinform. 2008 Jun 15;24(12):1461–2.
101. Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019 Jan 8;47(D1):D607–13. doi: 10.1093/nar/gky1131 30476243
102. Hu Y, Xie S, Yao J. Identification of Novel Reference Genes Suitable for qRT-PCR Normalization with Respect to the Zebrafish Developmental Stage. PloS One. 2016;11(2):e0149277. doi: 10.1371/journal.pone.0149277 26891128
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PLOS Genetics
2020 Číslo 6
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- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Osteocalcin promotes bone mineralization but is not a hormone
- AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization
- Super-resolution imaging of RAD51 and DMC1 in DNA repair foci reveals dynamic distribution patterns in meiotic prophase
- Steroid hormones regulate genome-wide epigenetic programming and gene transcription in human endometrial cells with marked aberrancies in endometriosis
