Drosophila TDP-43 RNA-Binding Protein Facilitates Association of Sister Chromatid Cohesion Proteins with Genes, Enhancers and Polycomb Response Elements

PLoS Genetics

Volumn 12, Issue 9, 2016, Pages

  Swain, Amanda ^a   Misulovin, Ziva ^a   Pherson, Michelle ^a   Gause, Maria ^a   Mihindukulasuriya, Kathie ^a   Rickels, Ryan A ^b   Shilatifard, Ali ^b   Dorsett, Dale ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; INSECT PROTEIN; LARK RNA BINDING PROTEIN; NIPPED B PROTEIN; RNA BINDING PROTEIN; TAR DNA BINDING PROTEIN HOMOLOG; TDP 43 RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME; CONTROLLED STUDY; DROSOPHILA; ENHANCER REGION; GENE INTERACTION; GENETIC TRANSCRIPTION; IN VITRO STUDY; NONHUMAN; POLYCOMB RESPONSE ELEMENT; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATOR GENE; REGULATORY SEQUENCE; RNA BINDING; RNA SEQUENCE; RNA STRUCTURE; SEQUENCE ANALYSIS; SISTER CHROMATID; SISTER CHROMATID COHESION;

EID: 84990201713     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006331     Document Type: Article

References (51)

1. Ball AR, JrChen YY, Yokomori K, Mechanisms of cohesin-mediated gene regulation and lessons learned from cohesinopathies. Biochim Biophys Acta. 2014;1839: 191–202. doi: 10.1016/j.bbagrm.2013.11.00224269489
2. Remeseiro S, Cuadrado A, Losada A, Cohesin in development and disease. Development. 2013;140: 3715–8. doi: 10.1242/dev.09060523981654
3. Dorsett D, Ström L, The ancient and evolving roles of cohesin in gene expression and DNA repair. Curr Biol. 2012;22: R240–50. doi: 10.1016/j.cub.2012.02.04622497943
4. Nasmyth K, Haering CH, Cohesin: its roles and mechanisms. Annu Rev Genet. 2009;43: 525–58. doi: 10.1146/annurev-genet-102108-13423319886810
5. Dorsett D, Merkenschlager M, Cohesin at active genes: a unifying theme for cohesin and gene expression from model organisms to humans. Curr Opin Cell Biol. 2013;25: 327–33. doi: 10.1016/j.ceb.2013.02.00323465542
6. Mannini L, Cucco F, Quarantotti V, Krantz ID, Musio A, Mutation spectrum and genotype-phenotype correlation in Cornelia de Lange syndrome. Hum Mutat. 2013;34: 1589–96. doi: 10.1002/humu.2243024038889
7. Wu Y, Gause M, Xu D, Misulovin Z, Schaaf CA, Mosarla RC, et al. Drosophila Nipped-B mutants model Cornelia de Lange syndrome in growth and behavior. PLoS Genet. 2015;11: e1005655. doi: 10.1371/journal.pgen.100565526544867
8. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, Yaeger D, et al. Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet. 2004;36: 631–5. doi: 10.1038/ng136415146186
9. Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T, NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet. 2004;36: 636–41. doi: 10.1038/ng136315146185
10. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, et al. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature. 2012;489: 313–7. doi: 10.1038/nature1131622885700
11. Rollins RA, Korom M, Aulner N, Martens A, Dorsett D, Drosophila Nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol. 2004;24: 3100–11. 15060134
12. Vrouwe MG, Elghalbzouri-Maghrani E, Meijers M, Schouten P, Godthelp BC, Bhuiyan ZA, et al. Increased DNA damage sensitivity of Cornelia de Lange syndrome cells: evidence for impaired recombinational repair. Hum Mol Genet. 2007;16: 1478–87. doi: 10.1093/hmg/ddm09817468178
13. Liu J, Zhang Z, Bando M, Itoh T, Deardorff MA, Clark D, et al. Transcriptional dysregulation in NIPBL and cohesin mutant human cells. PLoS Biol. 2009;7: e1000119. doi: 10.1371/journal.pbio.100011919468298
14. Kawauchi S, Calof AL, Santos R, Lopez-Burks ME, Young CM, Hoang MP, et al. Multiple organ system defects and transcriptional dysregulation in the Nipbl(+/-) mouse, a model of Cornelia de Lange Syndrome. PLoS Genet. 2009;5: e1000650. doi: 10.1371/journal.pgen.100065019763162
15. Dorsett D, Kassis JA, 2014. Checks and balances between cohesin and polycomb in gene silencing and transcription. Curr Biol. 2014;24: R535–9. doi: 10.1016/j.cub.2014.04.03724892918
16. Schaaf CA, Misulovin Z, Sahota G, Siddiqui AM, Schwartz YB, Kahn TG, et al. Regulation of the Drosophila Enhancer of split and invected-engrailed gene complexes by sister chromatid cohesion proteins. PLoS One. 2009;4: e6202. doi: 10.1371/journal.pone.000620219587787
17. Schaaf CA, Kwak H, Koenig A, Misulovin Z, Gohara DW, Watson A, et al. Genome-wide control of RNA polymerase II activity by cohesin. PLoS Genet. 2013;9: e1003382. doi: 10.1371/journal.pgen.100338223555293
18. Schaaf CA, Misulovin Z, Gause M, Koenig A, Gohara DW, Watson A, et al. Cohesin and polycomb proteins functionally interact to control transcription at silenced and active genes. PLoS Genet. 2013;9: e1003560. doi: 10.1371/journal.pgen.100356023818863
19. Fay A, Misulovin Z, Li J, Schaaf CA, Gause M, Gilmour DS, et al. 2011. Cohesin selectively binds and regulates genes with paused RNA polymerase. Curr Biol. 2011;21: 1624–34. doi: 10.1016/j.cub.2011.08.03621962715
20. Ayala YM, Pantano S, D'Ambrogio A, Buratti E, Brindisi A, Marchetti C, et al. Human, Drosophila, and C. elegans TDP43: nucleic acid binding properties and splicing regulatory function. J Mol Biol. 2005;348: 575–88. doi: 10.1016/j.jmb.2005.02.03815826655
21. Buratti E, Baralle FE, 2010. The multiple roles of TDP-43 in pre-mRNA processing and gene expression regulation. RNA Biol. 2010;7: 420–9. 20639693
22. Hazelett DJ, Chang JC, Lakeland DL, Morton DB, Comparison of parallel high-throughput RNA sequencing between knockout of TDP-43 and its overexpression reveals primarily nonreciprocal and nonoverlapping gene expression changes in the central nervous system of Drosophila. G3 (Bethesda). 2012;2: 789–802. doi: 10.1534/g3.112.002998
23. Misulovin Z, Schwartz YB, Li XY, Kahn TG, Gause M, MacArthur S, et al. Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma. 2008;117: 89–102. doi: 10.1007/s00412-007-0129-117965872
24. Dorsett D, Misulovin Z, Chromatin immunoprecipitation of sister chromatid cohesion proteins in Drosophila. Meth Mol Biol, 2016;in press.
25. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature. 2011;471: 480–5. doi: 10.1038/nature0972521179089
26. Lehman DA, Patterson B, Johnston LA, Balzer T, Britton JS, Saint R, Edgar BA, Cis-regulatory elements of the mitotic regulator, string/Cdc25. Development. 1999;126: 1793–1803. 10101114
27. Huang Y, Genova G, Roberts M, Jackson FR, The LARK RNA-binding protein selectively regulates the circadian eclosion rhythm by controlling E74 protein expression. PLoS One. 2007;2: e1107. doi: 10.1371/journal.pone.000110717971870
28. Lai MC, Kuo HW, Chang WC, Tarn WY, A novel splicing regulator shares a nuclear import pathway with SR proteins. EMBO J. 2003;22: 1359–69. doi: 10.1093/emboj/cdg12612628928
29. Titov DV, Gilman B, He QL, Bhat S, Low WK, Dang Y, et al. XPB, a subunit of TFIIH, is a target of the natural product triptolide. Nat Chem Biol2011;7: 182–188. doi: 10.1038/nchembio.52221278739
30. Chen F, Gao X, Shilatifard A, Stably paused genes revealed through inhibition of transcription initiation by the TFIIH inhibitor triptolide. Genes Dev. 2015;29: 39–47. doi: 10.1101/gad.246173.11425561494
31. Ray D, Kazan H, Chan ET, Peña Castillo L, Chaudhry S, Talukder S, et al. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol. 2009;27: 667–70. doi: 10.1038/nbt.155019561594
32. Bailey TL, Williams N, Misleh C, Li WW, 2006. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34(Web Server issue): W369–73. doi: 10.1093/nar/gkl19816845028
33. Lin JC, Tarn WY, Exon selection in alpha-tropomyosin mRNA is regulated by the antagonistic action of RBM4 and PTB. Mol Cell Biol. 2005;25: 10111–21. 16260624
34. Lin JC, Hsu M, Tarn WY, Cell stress modulates the function of splicing regulatory protein RBM4 in translation control. Proc Natl Acad Sci U S A. 2007;104: 2235–40. 17284590
35. Buratti E, Baralle FE, Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J Biol Chem. 2001;276: 36337–43. doi: 10.1074/jbc.M10423620011470789
36. Li J, Liu Y, Rhee HS, Ghosh SK, Bai L, Pugh BF, Gilmour DS, Kinetic competition between elongation rate and binding of NELF controls promoter-proximal pausing. Mol Cell. 2013;50: 711–22. doi: 10.1016/j.molcel.2013.05.01623746353
37. Ling SC, Polymenidou M, Cleveland DW, Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron. 2013;79: 416–38. doi: 10.1016/j.neuron.2013.07.03323931993
38. Ratti A, Buratti E, Physiological Functions and Pathobiology of TDP-43 and FUS/TLS proteins. J Neurochem. 2016; Mar26. doi: 10.1111/jnc.13625
39. McNeil GP, Kaur M, Purrier S, Kang R, The Drosophila RNA-binding protein Lark is required for localization of Dmoesin to the oocyte cortex during oogenesis. Dev Genes Evol. 2009;219: 11–9. doi: 10.1007/s00427-008-0260-x18958492
40. Faure AJ, Schmidt D, Watt S, Schwalie PC, Wilson MD, Xu H, et al. Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules. Genome Res. 2012;22: 2163–75. doi: 10.1101/gr.136507.11122780989
41. Wolozin B, Physiological protein aggregation run amuck: stress granules and the genesis of neurodegenerative disease. Discov Med. 2014;17: 47–52. 24411700
42. Bartman CR, Hsu SC, Hsiung CC, Raj A, Blobel GA, Enhancer regulation of transcriptional bursting parameters revealed by forced chromatin looping. Mol Cell. 2016;62: 237–47. doi: 10.1016/j.molcel.2016.03.00727067601
43. Fukaya T, Lim B, Levine M, Enhancer control of transcriptional bursting. Cell. 2016Jun9. pii: S0092-8674(16)30573-6. doi: 10.1016/j.cell.2016.05.025
44. Rollins RA, Morcillo P, Dorsett D, Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics. 1999;152: 577–93. 10353901
45. The Regents of the University of California, Lawrence Berkeley National Laboratory. TiMAT. 2005. Available: http://bdtnp.lbl.gov/Fly-Net/chipchip.jsp?w=timat
46. Johnson WE, Li W, Meyer CA, Gottardo R, Carroll JS, Brown M, et al. Model-based analysis of tiling-arrays for ChIP-chip. Proc Natl Acad Sci U S A. 2006;103: 12457–62. doi: 10.1073/pnas.060118010316895995
47. R Core TeamR: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. 2015. Available: http://www.R-project.org
48. Nicol JW, Helt GA, Blanchard SG, JrRaja A, Loraine AE, The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics. 2009;25: 2730–1. doi: 10.1093/bioinformatics/btp47219654113
49. Mossessova E, Lima CD, Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell. 2000;5: 865–76. 10882122
50. Karsch-Mizrachi I, Haynes SR, The Rb97D gene encodes a potential RNA-binding protein required for spermatogenesis in Drosophila. Nucleic Acids Res. 1993;21: 2229–35. 8502565
51. Newby LM, Jackson FR, A new biological rhythm mutant of Drosophila melanogaster that identifies a gene with an essential embryonic function. Genetics. 1993;135: 1077–90. 8307324