Identification of the RSX interactome in a marsupial shows functional coherence with the Xist interactome during X inactivation.
RSX protein interactome
Convergent evolution
X chromosome inactivation
Journal
Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660
Informations de publication
Date de publication:
23 May 2024
23 May 2024
Historique:
received:
02
11
2023
accepted:
14
05
2024
medline:
24
5
2024
pubmed:
24
5
2024
entrez:
23
5
2024
Statut:
epublish
Résumé
The marsupial specific RSX lncRNA is the functional analogue of the eutherian specific XIST, which coordinates X chromosome inactivation. We characterized the RSX interactome in a marsupial representative (the opossum Monodelphis domestica), identifying 135 proteins, of which 54 had orthologues in the XIST interactome. Both interactomes were enriched for biological pathways related to RNA processing, regulation of translation, and epigenetic transcriptional silencing. This represents a remarkable example showcasing the functional coherence of independently evolved lncRNAs in distantly related mammalian lineages.
Identifiants
pubmed: 38783307
doi: 10.1186/s13059-024-03280-0
pii: 10.1186/s13059-024-03280-0
doi:
Substances chimiques
RNA, Long Noncoding
0
XIST non-coding RNA
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
134Subventions
Organisme : Australian Research Council Discovery Projects
ID : DP170101147
Organisme : Australian Research Council Discovery Projects
ID : DP180100931
Organisme : Australian Research Council Discovery Projects
ID : DP210103512
Organisme : Australian Research Council Discovery Projects
ID : DP220101429
Organisme : Australian Research Council Discovery Projects
ID : DP170101147
Organisme : Australian Research Council Discovery Projects
ID : DP180100931
Organisme : Australian Research Council Discovery Projects
ID : DP210103512
Organisme : Australian Research Council Discovery Projects
ID : DP220101429
Organisme : NHMRC Ideas Grant
ID : 2021172
Organisme : NHMRC Ideas Grant
ID : 2027730
Organisme : Australian National Health and Medical Research Council Ideas Grant
ID : 1188987
Organisme : National Health and Medical Research Council
ID : 2021172
Informations de copyright
© 2024. The Author(s).
Références
Graves JAM. The evolution of mammalian sex chromosomes and the origin of sex determining genes. Philos Trans R Soc Lond B Biol Sci. 1995;350:305–11.
pubmed: 8570696
doi: 10.1098/rstb.1995.0166
Ohno S. Sex chromosome and sex-linked genes. Heidelberg, Berlin: Springer-Verlag, Berlin; 1967.
doi: 10.1007/978-3-642-88178-7
Zhou Y, Shearwin-Whyatt L, Li J, Song Z, Hayakawa T, Stevens D, et al. Platypus and echidna genomes reveal mammalian biology and evolution. Nature. 2021;592:756–62.
pubmed: 33408411
pmcid: 8081666
doi: 10.1038/s41586-020-03039-0
Graves JAM, Gartler SM. Mammalian X chromosome inactivation: testing the hypothesis of transcriptional control. Somat Cell Mol Genet. 1986;12:275–80.
pubmed: 3459256
doi: 10.1007/BF01570786
Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature. 1991;349:38–44.
pubmed: 1985261
doi: 10.1038/349038a0
Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, et al. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell. 1992;71:515–26.
pubmed: 1423610
doi: 10.1016/0092-8674(92)90519-I
Dixon-McDougall T, Brown CJ. Independent domains for recruitment of PRC1 and PRC2 by human XIST. PLoS Genet. 2021;17:1–28.
doi: 10.1371/journal.pgen.1009123
Chu C, Zhang QC, da Rocha ST, Flynn RA, Bharadwaj M, Calabrese JM, et al. Systematic discovery of Xist RNA binding proteins. Cell. 2015;161:404–16.
pubmed: 25843628
pmcid: 4425988
doi: 10.1016/j.cell.2015.03.025
Minajigi A, Froberg JE, Wei C, Sunwoo H, Kesner B, Colognori D, et al. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation. Science. 1979;2015:349.
McHugh CA, Chen CK, Chow A, Surka CF, Tran C, McDonel P, et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature. 2015;521:232–6.
pubmed: 25915022
pmcid: 4516396
doi: 10.1038/nature14443
Pintacuda G, Wei G, Roustan C, Kirmizitas BA, Solcan N, Cerase A, et al. hnRNPK recruits PCGF3/5-PRC1 to the Xist RNA B-repeat to establish polycomb-mediated chromosomal silencing. Mol Cell. 2017;68:955–969.e10.
pubmed: 29220657
pmcid: 5735038
doi: 10.1016/j.molcel.2017.11.013
Bousard A, Raposo AC, Żylicz JJ, Picard C, Pires VB, Qi Y, et al. The role of Xist -mediated polycomb recruitment in the initiation of X-chromosome inactivation. EMBO Rep. 2019;20:1–18.
doi: 10.15252/embr.201948019
Hendrickson DG, Kelley DR, Tenen D, Bernstein B, Rinn JL. Widespread RNA binding by chromatin-associated proteins. Genome Biol. 2016;17:28.
doi: 10.1186/s13059-016-0878-3
Lu Z, Guo JK, Wei Y, Dou DR, Zarnegar B, Ma Q, et al. Structural modularity of the XIST ribonucleoprotein complex. Nat Commun. 2020;11:1–14.
doi: 10.1038/s41467-020-20040-3
Duret L, Chureau C, Samain S, Weissanbach J, Avner P. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science. 1979;2006(312):1653–5.
Hore TA, Koina E, Wakefield MJ, Graves JAM. The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Res. 2007;15:147–61.
pubmed: 17333539
doi: 10.1007/s10577-007-1119-0
Shevchenko AI, Zakharova IS, Elisaphenko EA, Kolesnikov NN, Whitehead S, Bird C, et al. Genes flanking Xist in mouse and human are separated on the X chromosome in American marsupials. Chromosome Res. 2007;15:127–36.
pubmed: 17333537
pmcid: 2797855
doi: 10.1007/s10577-006-1115-9
Grant J, Mahadevaiah SK, Khil P, Sangrithi MN, Royo H, Duckworth J, et al. Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature. 2012;487:254–8. 2012/06/23.
pubmed: 22722828
pmcid: 3484893
doi: 10.1038/nature11171
Johnson RN, O’Meally D, Chen Z, Etherington GJ, Ho SYW, Nash WJ, et al. Adaptation and conservation insights from the koala genome. Nat Genet. 2018;50:1102–11.
pubmed: 29967444
pmcid: 6197426
doi: 10.1038/s41588-018-0153-5
Brown CJ, Hendrich BD, Rupert JL, Lafrenière RG, Xing Y, Lawrence J, et al. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell. 1992;71:527–42.
pubmed: 1423611
doi: 10.1016/0092-8674(92)90520-M
Sprague D, Waters SA, Kirk JM, Wang JR, Samollow PB, Waters PD, et al. Nonlinear sequence similarity between the Xist and Rsx long noncoding RNAs suggests shared functions of tandem repeat domains. RNA. 2019;25:1004–19.
pubmed: 31097619
pmcid: 6633197
doi: 10.1261/rna.069815.118
Naciri I, Lin B, Webb CH, Jiang S, Carmona S, Liu W, et al. Linking chromosomal silencing with xist expression from autosomal integrated transgenes. Front Cell Dev Biol. 2021;9:1–12.
doi: 10.3389/fcell.2021.693154
Al Nadaf S, Deakin JE, Gilbert C, Robinson TJ, Graves JAM, Waters PD. A cross-species comparison of escape from X inactivation in Eutheria: implications for evolution of X chromosome inactivation. Chromosoma. 2012;121:71–8.
pubmed: 21947602
doi: 10.1007/s00412-011-0343-8
Wang ZY, Leushkin E, Liechti A, Ovchinnikova S, Mößinger K, Brüning T, et al. Transcriptome and translatome co-evolution in mammals. Nature. 2020;588:642–7.
pubmed: 33177713
pmcid: 7116861
doi: 10.1038/s41586-020-2899-z
Yin S, Deng W, Zheng H, Zhang Z, Hu L, Kong X. Evidence that the nonsense-mediated mRNA decay pathway participates in X chromosome dosage compensation in mammals. Biochem Biophys Res Commun. 2009;383:378–82.
pubmed: 19364502
doi: 10.1016/j.bbrc.2009.04.021
Brenes AJ, Yoshikawa H, Bensaddek D, Mirauta B, Seaton D, Hukelmann JL, et al. Erosion of human X chromosome inactivation causes major remodeling of the iPSC proteome. Cell Rep. 2021;35: 109032.
pubmed: 33910018
pmcid: 8097692
doi: 10.1016/j.celrep.2021.109032
Faucillion ML, Larsson J. Increased expression of X-linked genes in mammals is associated with a higher stability of transcripts and an increased ribosome density. Genome Biol Evol. 2015;7:1039–52.
pubmed: 25786432
pmcid: 4419800
doi: 10.1093/gbe/evv054
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;47:D607–13.
pubmed: 30476243
doi: 10.1093/nar/gky1131
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models. Genome Res. 2003;13:2498–504.
pubmed: 14597658
pmcid: 403769
doi: 10.1101/gr.1239303
Su G, Kuchinsky A, Morris JH, States DJ, Meng F. GLay: community structure analysis of biological networks. Bioinformatics. 2010;26:3135–7.
pubmed: 21123224
pmcid: 2995124
doi: 10.1093/bioinformatics/btq596
Peterson H, Kolberg L, Raudvere U, Kuzmin I, Vilo J. gprofiler2 – an R package for gene list functional enrichment analysis and namespace conversion toolset g: Profiler. F1000Res. 2020;9:1–27.
Chaumeil J, Waters PD, Koina E, Gilbert C, Robinson TJ, Graves JAM. Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS ONE. 2011;6:e19040.
pubmed: 21541345
pmcid: 3081832
doi: 10.1371/journal.pone.0019040
Rens W, Wallduck MS, Lovell FL, Ferguson-Smith MA, Ferguson-Smith AC. Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc Natl Acad Sci U S A. 2010;107:17657–62.
pubmed: 20861449
pmcid: 2955130
doi: 10.1073/pnas.0910322107
Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, et al. G:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 2019;47:W191–8.
pubmed: 31066453
pmcid: 6602461
doi: 10.1093/nar/gkz369
Colognori D, Sunwoo H, Kriz AJ, Wang CY, Lee JT. Xist deletional analysis reveals an interdependency between Xist RNA and polycomb complexes for spreading along the inactive X. Mol Cell. 2019;74:101–117.e10.
pubmed: 30827740
pmcid: 6469964
doi: 10.1016/j.molcel.2019.01.015
Mier P, Andrade-Navarro MA. Between interactions and aggregates: the PolyQ balance. Genome Biol Evol. 2021;13:1–7.
Markaki Y, Gan Chong J, Wang Y, Jacobson EC, Luong C, Tan SYX, et al. Xist nucleates local protein gradients to propagate silencing across the X chromosome. Cell. 2021;184:6174–6192.e32.
pubmed: 34813726
pmcid: 8671326
doi: 10.1016/j.cell.2021.10.022
Cerase A, Armaos A, Neumayer C, Avner P, Guttman M, Tartaglia GG. Phase separation drives X-chromosome inactivation: a hypothesis. Nat Struct Mol Biol. 2019;26:331–4.
pubmed: 31061525
doi: 10.1038/s41594-019-0223-0
Pandya-Jones A, Markaki Y, Serizay J, Chitiashvili T, Mancia Leon WR, Damianov A, et al. A protein assembly mediates Xist localization and gene silencing. Nature. 2020;587:145–51.
pubmed: 32908311
pmcid: 7644664
doi: 10.1038/s41586-020-2703-0
Jachowicz JW, Strehle M, Banerjee AK, Blanco MR, Thai J, Guttman M. Xist spatially amplifies SHARP/SPEN recruitment to balance chromosome-wide silencing and specificity to the X chromosome. Nat Struct Mol Biol. 2022;29:239–49.
pubmed: 35301492
pmcid: 8969943
doi: 10.1038/s41594-022-00739-1
Mészáros B, Erdös G, Dosztányi Z. IUPred2A: context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Res. 2018;46:W329–37.
pubmed: 29860432
pmcid: 6030935
doi: 10.1093/nar/gky384
Belmont AS. Nuclear compartments: an incomplete primer to nuclear compartments, bodies, and genome organization relative to nuclear architecture. Cold Spring Harb Perspect Biol. 2021;14(7):a041268.
Zhao B, Katuwawala A, Oldfield CJ, Hu G, Wu Z, Uversky VN, et al. Intrinsic disorder in human RNA-binding proteins. J Mol Biol. 2021;433:167229.
pubmed: 34487791
doi: 10.1016/j.jmb.2021.167229
Uversky VN. Recent developments in the field of intrinsically disordered proteins: intrinsic disorder-based emergence in cellular biology in light of the physiological and pathological liquid-liquid phase transitions. Annu Rev Biophys. 2021;50:135–56.
pubmed: 33503380
doi: 10.1146/annurev-biophys-062920-063704
Al Nadaf S, Waters PD, Koina E, Deakin JE, Jordan KS, Graves JAM. Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic. Genome Biol. 2010;11:R122.
pubmed: 21182760
pmcid: 3046482
doi: 10.1186/gb-2010-11-12-r122
Rodríguez-Delgado CL, Waters SA, Waters DP. Paternal X inactivation does not correlate with X chromosome evolutionary strata in marsupials. BMC Evol Biol. 2014;14:4–11.
doi: 10.1186/s12862-014-0267-z
Robert-Finestra T, Tan BF, Mira-Bontenbal H, Timmers E, Gontan C, Merzouk S, et al. SPEN is required for Xist upregulation during initiation of X chromosome inactivation. Nat Commun. 2021;12:1–13.
doi: 10.1038/s41467-021-27294-5
Dossin F, Pinheiro I, Żylicz JJ, Roensch J, Collombet S, Le Saux A, et al. SPEN integrates transcriptional and epigenetic control of X-inactivation. Nature. 2020;578:455–60.
pubmed: 32025035
pmcid: 7035112
doi: 10.1038/s41586-020-1974-9
Lister NC, Milton AM, Patel HR, Waters SA, McIntyre KL, Livernois AM, et al. Incomplete transcriptional dosage compensation of vertebrate sex chromosomes is 1 balanced by post-transcriptional compensation. bioRxiv. 2023:312–20.
Stellaris Probe Designer | LGC Biosearch Technologies. https://www.biosearchtech.com/support/tools/design-software/stellaris-probe-designer . Accessed 1 Feb 2015.
Gatlin CL, Kleemann GR, Hays LG, Link AJ, Yates JR. Protein identification at the low femtomole level from silver-stained gels using a new fritless electrospray interface for liquid chromatography- microspray and nanospray mass spectrometry. Anal Biochem. 1998;263:93–101.
pubmed: 9750149
doi: 10.1006/abio.1998.2809
Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26:1367–72.
pubmed: 19029910
doi: 10.1038/nbt.1511
Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794–805.
pubmed: 21254760
doi: 10.1021/pr101065j
Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics. 2014;13:2513–26.
pubmed: 24942700
pmcid: 4159666
doi: 10.1074/mcp.M113.031591
BioSettia shRNA designer. https://biosettia.com/support/shrna-designer/ . Accessed 1 Sept 2015.
Invitrogen RNAi Designer. https://rnaidesigner.thermofisher.com/rnaiexpress/ . Accessed 1 Sept 2015.
IDT RNAi Design Tool. https://sg.idtdna.com/site/account?ReturnURL=/site/order/tool/index/DSIRNA_CUSTOM . Accessed 1 Sept 2015.
Amarzguioui M, Rossi JJ, Kim D. Approaches for chemically synthesized siRNA and vector-mediated RNAi. FEBS Lett. 2005;579:5974–81.
pubmed: 16199038
doi: 10.1016/j.febslet.2005.08.070
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–82.
pubmed: 22743772
doi: 10.1038/nmeth.2019
Ensembl 97 BioMart. [cited]. http://jul2019.archive.ensembl.org/index.html . Accessed 24 Feb 2024.
UniProt protein BLAST. https://www.uniprot.org/blast . Accessed 24 Feb 2024.
g:Profiler. https://biit.cs.ut.ee/gprofiler/gost . Accessed 24 Feb 2024.
NCBI Gene database. https://www.ncbi.nlm.nih.gov/gene/ . Accessed 24 Feb 2024.
Ensembl (v111). https://www.ensembl.org/ . Accessed 30 Jan 2024.
NCBI Multiple Sequence Alignment Viewer. https://www.ncbi.nlm.nih.gov/projects/msaviewer/ . Accessed 26 Feb 2024.
McIntyre KL, Waters SA, Zhong L, Hart-Smith G, Raftery M, Chew ZA, Patel HR, Marshall Graves JA, Waters PD. Identification of the RSX interactome in a marsupial shows functional coherence with the Xist interactome during X inactivation. github.com. https://github.com/kango2/Rsx_prot .
McIntyre KL, Waters SA, Zhong L, Hart-Smith G, Raftery M, Chew ZA, Patel HR, Marshall Graves JA, Waters PD. Identification of the RSX interactome in a marsupial shows functional coherence with the Xist interactome during X inactivation. Figshare. https://doi.org/10.6084/m9.figshare.25807144 .