Integrative analysis of tissue-specific methylation and alternative splicing identifies conserved transcription factor binding motifs
Open accessAbstract
The exact role of intragenic DNA methylation in regulating tissue-specific gene regulation is unclear. Recently, the DNA-binding protein CTCF has been shown to participate in the regulation of alternative splicing in a DNA methylation-dependent manner. To globally evaluate the relationship between DNA methylation and tissue-specific alternative splicing, we performed genome-wide DNA methylation profiling of mouse retina and brain. In protein-coding genes, tissue-specific differentially methylated regions (T-DMRs) were preferentially located in exons and introns. Gene ontology and evolutionary conservation analysis suggest that these T-DMRs are likely to be biologically relevant. More than 14% of alternatively spliced genes were associated with a T-DMR. T-DMR-associated genes were enriched for developmental genes, suggesting that a specific set of alternatively spliced genes may be regulated through DNA methylation. Novel DNA sequences motifs overrepresented in T-DMRs were identified as being associated with positive and/or negative regulation of alternative splicing in a position-dependent context. The majority of these evolutionarily conserved motifs contain a CpG dinucleotide. Some transcription factors, which recognize these motifs, are known to be involved in splicing. Our results suggest that DNA methylation-dependent alternative splicing is widespread and lay the foundation for further mechanistic studies of the role of DNA methylation in tissue-specific splicing regulation.
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.
Integrity signals
Registry
Cites
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.
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?
Additional mCpG-binding proteins take part in splicing control.
“indicating that other mCpG-binding proteins are involved in regulating the splicing process.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [115]
The honeybee observation is consistent with a global correlation analysis of DNA methylation and differential splicing between brain and retina.
“This observation is consistent with a global correlation analysis of DNA methylation and differential splicing events between the brain and the retina115.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [115]
Other transcription factors might also participate in splicing regulation.
“suggesting that other TFs might also participate in splicing regulation.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [115]
Methylation levels in some regions were positively associated with the inclusion level of spliced exons.
“Interestingly, the methylation levels in some of the regions were positively associated with the inclusion level of the spliced exons”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [115]
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
Clustal W and Clustal X version 2.0
Larkin, M., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., López, R., et al. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm404 · Cited by 28,221 · see citing works
CpG islands in vertebrate genomes.
Gardiner-Garden, M., & Frommer, M. (1987) · Journal of Molecular Biology · doi:10.1016/0022-2836(87)90689-9 · Cited by 3,462 · see citing works
Irizarry, R. A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., et al. (2009) · Nature Genetics · doi:10.1038/ng.298 · Cited by 2,177 · see citing works
Quantifying similarity between motifs
Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L., & Noble, W. S. (2007) · Genome Biology · doi:10.1186/gb-2007-8-2-r24 · Cited by 2,058 · see citing works
TRANSFAC(R): transcriptional regulation, from patterns to profiles
Matys, V. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg108 · Cited by 1,985 · see citing works
A new bioinformatics analysis tools framework at EMBL-EBI
Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., & Lopez, R. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq313 · Cited by 1,846 · see citing works
Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation
Zemach, A., McDaniel, I. E., Silva, P., & Zilberman, D. (2010) · Science · doi:10.1126/science.1186366 · Cited by 1,796 · see citing works
Conserved role of intragenic DNA methylation in regulating alternative promoters
Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D’Souza, C., Fouse, S. D., Johnson, B. E., Hong, C., Nielsen, C., Zhao, Y., et al. (2010) · Nature · doi:10.1038/nature09165 · Cited by 1,743 · see citing works
CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus
Hark, A. T., Schoenherr, C. J., Katz, D. J., Ingram, R. S., Levorse, J. M., & Tilghman, S. M. (2000) · Nature · doi:10.1038/35013106 · Cited by 1,547 · see citing works
Conservation and divergence of methylation patterning in plants and animals
Feng, S., Cokus, S. J., Zhang, X., Chen, P.-Y., Bostick, M., Goll, M. G., Hetzel, J., Jain, J., Strauss, S. H., Halpern, M. E., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002720107 · Cited by 1,285 · see citing works
Doi, A., Park, I., Wen, B., Murakami, P. N., Aryee, M. J., Irizarry, R. A., Herb, B. R., Ladd‐Acosta, C., Rho, J., Loewer, S., et al. (2009) · Nature Genetics · doi:10.1038/ng.471 · Cited by 1,173 · see citing works
CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing
Shukla, S., Kavak, E., Gregory, M., Imashimizu, M., Shutinoski, B., Kashlev, M., Oberdoerffer, P., Sandberg, R., & Oberdoerffer, S. (2011) · Nature · doi:10.1038/nature10442 · Cited by 973 · see citing works
Dynamic Readers for 5-(Hydroxy)Methylcytosine and Its Oxidized Derivatives
Spruijt, C. G., Gnerlich, F., Smits, A. H., Pfaffeneder, T., Jansen, P. W. T. C., Bauer, C., Münzel, M., Wagner, M., Müller, M., Khan, F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.02.004 · Cited by 973 · see citing works
The UCSC Genome Browser database: extensions and updates 2013
Meyer, L. R., Zweig, A. S., Hinrichs, A. S., Karolchik, D., Kuhn, R. M., Wong, M., Sloan, C. A., Rosenbloom, K. R., Roe, G. R., Rhead, B. L., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1048 · Cited by 901 · see citing works
Relationship between nucleosome positioning and DNA methylation
Chodavarapu, R. K., Feng, S., Bernatavichute, Y. V., Chen, P., Stroud, H., Yu, Y., Hetzel, J., Kuo, F., Kim, J., Cokus, S. J., et al. (2010) · Nature · doi:10.1038/nature09147 · Cited by 696 · see citing works
Berger, M. F., Philippakis, A., Qureshi, A. M., He, F. S., Estep, P. W., & Bulyk, M. L. (2006) · Nature Biotechnology · doi:10.1038/nbt1246 · Cited by 685 · see citing works
Differential chromatin marking of introns and expressed exons by H3K36me3
Kolasinska-Zwierz, P., Down, T. A., Latorre, I. J., Liu, T., Liu, X. S., & Ahringer, J. (2009) · Nature Genetics · doi:10.1038/ng.322 · Cited by 671 · see citing works
Chromatin organization marks exon-intron structure
Schwartz, S., Meshorer, E., & Ast, G. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1659 · Cited by 638 · see citing works
Comprehensive methylome map of lineage commitment from haematopoietic progenitors
Ji, H., Ehrlich, L. I. R., Seita, J., Murakami, P. N., Doi, A., Lindau, P., Lee, H.-J., Aryee, M. J., Irizarry, R. A., Kim, K., et al. (2010) · Nature · doi:10.1038/nature09367 · Cited by 636 · see citing works
Davies, M. N., Volta, M., Pidsley, R., Lunnon, K., Dixit, A., Lovestone, S., Coarfa, C., Harris, R. A., Milosavljevic, A., Troakes, C., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-6-r43 · Cited by 630 · see citing works
Orphan CpG Islands Identify Numerous Conserved Promoters in the Mammalian Genome
Illingworth, R. S., Gruenewald-Schneider, U., Webb, S., Kerr, A. R. W., James, K. D., Turner, D. J., Smith, C., Harrison, D. J., Andrews, R., & Bird, A. P. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001134 · Cited by 550 · see citing works
Comprehensive high-throughput arrays for relative methylation (CHARM)Preprint
Irizarry, R. A., Ladd‐Acosta, C., Carvalho, B. S., Wu, H., Brandenburg, S. A., Jeddeloh, J. A., Wen, B., & Feinberg, A. P. (2008) · Genome Research · doi:10.1101/gr.7301508 · Cited by 433 · see citing works
Genetic Control of Individual Differences in Gene-Specific Methylation in Human Brain
Zhang, D., Cheng, L., Badner, J. A., Chen, C., Chen, Q., Luo, W., Craig, D. W., Redman, M., Gershon, E. S., & Liu, C. (2010) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2010.02.005 · Cited by 388 · see citing works
Nucleosomes are well positioned in exons and carry characteristic histone modifications
Andersson, R., Enroth, S., Rada-Iglesias, A., Wadelius, C., & Komorowski, J. (2009) · Genome Research · doi:10.1101/gr.092353.109 · Cited by 325 · see citing works
Co-transcriptional splicing of constitutive and alternative exons
Pandya‐Jones, A., & Black, D. L. (2009) · RNA · doi:10.1261/rna.1714509 · Cited by 300 · see citing works
Cell type–specific DNA methylation at intragenic CpG islands in the immune systemPreprint
Deaton, A. M., Webb, S., Kerr, A. R. W., Illingworth, R. S., Guy, J., Andrews, R., & Bird, A. P. (2011) · Genome Research · doi:10.1101/gr.118703.110 · Cited by 285 · see citing works
Discovery of tissue-specific exons using comprehensive human exon microarrays
Clark, T. A., Schweitzer, A. C., Chen, T. X., Staples, M. K., Lu, G., Wang, H., Williams, A., & Blume, J. E. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-r64 · Cited by 280 · see citing works
Davies, R. C., Calvio, C., Bratt, E., Larsson, S., Lamond, A. I., & Hastie, N. D. (1998) · Genes & Development · doi:10.1101/gad.12.20.3217 · Cited by 246 · see citing works
Long, H. K., Sims, D., Heger, A., Blackledge, N. P., Kutter, C., Wright, M. L., Grützner, F., Odom, D. T., Patient, R. K., Ponting, C. P., et al. (2013) · eLife · doi:10.7554/elife.00348 · Cited by 223 · see citing works
Gelfman, S., Cohen, N., Yearim, A., & Ast, G. (2013) · Genome Research · doi:10.1101/gr.143503.112 · Cited by 222 · see citing works
Genome-wide association between DNA methylation and alternative splicing in an invertebrate
Flores, K., Wolschin, F., Corneveaux, J. J., Allen, A. N., Huentelman, M. J., & Amdam, G. V. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-480 · Cited by 169 · see citing works
Liang, P., Song, F., Ghosh, S., Morien, E., Qin, M., Mahmood, S., Fujiwara, K., Igarashi, J., Nagase, H., & Held, W. A. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-231 · Cited by 140 · see citing works
CpG island shore methylation regulates caveolin-1 expression in breast cancer
Rao, X., Evans, J. M., Chae, H., Pilrose, J. M., Kim, S., Yan, P. S., Huang, R.-L., Lai, H.-C., Lin, H.-J. L., Liu, Y., et al. (2012) · Oncogene · doi:10.1038/onc.2012.474 · Cited by 117 · see citing works
Comparative methylome analysis of benign and malignant peripheral nerve sheath tumorsPreprint
Feber, A., Wilson, G. A., Zhang, L., Presneau, N., Idowu, B. D., Down, T. A., Rakyan, V. K., Noon, L. A., Lloyd, A. C., Stupka, E., et al. (2011) · Genome Research · doi:10.1101/gr.109678.110 · Cited by 115 · see citing works
Dudziec, E., Miah, S., Choudhry, H., Owen, H. C., Blizard, S., Glover, M., Hamdy, F. C., & Catto, J. W. F. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2017 · Cited by 104 · see citing works
Sati, S., Tanwar, V. S., Kumar, K. A., Patowary, A., Jain, V. K., Ghosh, S., Ahmad, S., Singh, M., Reddy, S., Chandak, G. R., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031621 · Cited by 88 · see citing works
Nucleosome deposition and DNA methylation at coding region boundaries
Choi, J. K., Bae, J., Lyu, J., Kim, T., & Kim, Y.-J. (2009) · Genome biology · doi:10.1186/gb-2009-10-9-r89 · Cited by 78 · see citing works
Accurate genome-scale percentage DNA methylation estimates from microarray data
Aryee, M. J., Wu, Z. J., Ladd‐Acosta, C., Herb, B. R., Feinberg, A. P., Yegnasubramanian, S., & Irizarry, R. A. (2010) · Biostatistics · doi:10.1093/biostatistics/kxq055 · Cited by 71 · see citing works
Anastasiadou, C., Malousi, A., Maglaveras, N., & Kouidou, S. (2011) · DNA and Cell Biology · doi:10.1089/dna.2010.1094 · Cited by 70 · see citing works
Cell-Specific DNA Methylation Patterns of Retina-Specific Genes
Merbs, S. L., Khan, M. A., Hackler, L., Oliver, V. F., Wan, J., Qian, J. X., & Zack, D. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032602 · Cited by 66 · see citing works
Self-citationEpigenetic features are significantly associated with alternative splicing
Zhou, Y., Lu, Y., & Tian, W. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-123 · Cited by 62 · see citing works
Epigenetic control of alternative mRNA processing at the imprinted Herc3/Nap1l5 locus
Cowley, M., Wood, A. J., Böhm, S., Schulz, R., & Oakey, R. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks654 · Cited by 52 · see citing works
Dynamic usage of alternative splicing exons during mouse retina development
Wan, J., Masuda, T., Hackler, L., Torres, K. M., Merbs, S. L., Zack, D. J., & Qian, J. X. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr545 · Cited by 39 · see citing works
Self-citationDNA hypermethylation of alternatively spliced and repeat sequences in humans
Malousi, A., & Kouidou, S. (2012) · Molecular Genetics and Genomics · doi:10.1007/s00438-012-0703-y · Cited by 26 · see citing works
Hackler, L., Masuda, T., Oliver, V. F., Merbs, S. L., & Zack, D. J. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-848-1_21 · Cited by 24 · see citing works
Self-citationLee, R. S., Tamashiro, K. L., Aryee, M. J., Murakami, P. N., Seifuddin, F., Herb, B. R., Huo, Y., Rongione, M. A., Feinberg, A. P., Moran, T. H., et al. (2011) · Epigenetics · doi:10.4161/epi.6.11.18072 · Cited by 21 · see citing works
Oliver, V. F., Wan, J., Agarwal, S., Zack, D. J., Qian, J. X., & Merbs, S. L. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-17 · Cited by 20 · see citing works
Self-citationAlberstein, M., Amit, M., Vaknin, K., O’Donnell, A., Farhy, C., Lerenthal, Y., Shomron, N., Shaham, O., Sharrocks, A. D., Ashery‐Padan, R., et al. (2007) · RNA · doi:10.1261/rna.492907 · Cited by 14 · see citing works
Diniz, S. N., Pendeloski, K. P. T., Morgun, A., Chepelev, I., Gerbase‐DeLima, M., & Shulzhenko, N. (2010) · PubMed · doi:10.1684/ecn.2010.0218 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Transcription factors as readers and effectors of DNA methylation
Zhu, H., Wang, G., & Qian, J. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.83 · Cited by 649 · see citing works
Self-citationThe alternative role of DNA methylation in splicing regulation
Lev-Maor, G., Yearim, A., & Ast, G. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.03.002 · Cited by 566 · see citing works
Astrocytic abnormalities and global DNA methylation patterns in depression and suicide
Nagy, C., Suderman, M., Yang, J., Szyf, M., Mechawar, N., Ernst, C., & Turecki, G. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.21 · Cited by 301 · see citing works
Dyson, M. T., Roqueiro, D., Monsivais, D., Ercan, C. M., Pavone, M. E., Brooks, D. C., Kakinuma, T., Ono, M., Jafari, N., Dai, Y., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004158 · Cited by 211 · see citing works
Wan, J., Oliver, V. F., Wang, G., Zhu, H., Zack, D. J., Merbs, S. L., & Qian, J. (2015) · BMC Genomics · doi:10.1186/s12864-015-1271-4 · Cited by 165 · see citing works
Self-citationWhole genome DNA methylation: beyond genes silencing
Tirado-Magallanes, R., Rebbani, K., Lim, R., Pradhan, S., & Benoukraf, T. (2016) · Oncotarget · doi:10.18632/oncotarget.13562 · Cited by 146 · see citing works
Ai, R., Hammaker, D. R., Boyle, D. L., Morgan, R. L., Walsh, A. M., Fan, S., Firestein, G. S., & Wang, W. (2016) · Nature Communications · doi:10.1038/ncomms11849 · Cited by 135 · see citing works
Epigenetic control of gene regulation during development and disease: A view from the retina
Corso‐Díaz, X., Jaeger, C., Chaitankar, V., & Swaroop, A. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.03.002 · Cited by 129 · see citing works
Limbach, M., Saare, M., Tserel, L., Kisand, K. E., Eglit, T., Sauer, S., Axelsson, T., Syvänen, A., Metspalu, A., Milani, L. A., et al. (2015) · Journal of Autoimmunity · doi:10.1016/j.jaut.2015.09.006 · Cited by 116 · see citing works
Does co-transcriptional regulation of alternative splicing mediate plant stress responses?
Jabre, I., Reddy, A. S. N., Kalyna, M., Chaudhary, S., Khokhar, W., Byrne, L. J., Wilson, C. M., & Syed, N. H. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz121 · Cited by 103 · see citing works
Grunert, M., Dorn, C., Cui, H., Dunkel, I., Schulz, K., Schoenhals, S., Sun, W., Berger, F. F., Chen, W., & Sperling, S. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw195 · Cited by 76 · see citing works
Splicing alterations in healthy aging and disease
Angarola, B. L., & Anczuków, O. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1643 · Cited by 69 · see citing works
New themes in the biological functions of 5‐methylcytosine and 5‐hydroxymethylcytosine
Moen, E. L., Mariani, C. J., Zullow, H. J., Jeff‐Eke, M., Litwin, E., Nikitas, J. N., & Godley, L. A. (2014) · Immunological Reviews · doi:10.1111/imr.12242 · Cited by 66 · see citing works
CTCF as a regulator of alternative splicing: new tricks for an old player
Alharbi, A. B., Schmitz, U., Bailey, C. G., & Rasko, J. E. J. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab520 · Cited by 66 · see citing works
The effect of maternal care on gene expression and DNA methylation in a subsocial bee
Arsenault, S. V., Hunt, B. G., & Rehan, S. M. (2018) · Nature Communications · doi:10.1038/s41467-018-05903-0 · Cited by 66 · see citing works
Yang, H., Ratnapriya, R., Cogliati, T., Kim, J.-W., & Swaroop, A. (2015) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2015.01.005 · Cited by 51 · see citing works
Oliver, V. F., Franchina, M., Jaffe, A. E., Branham, K. E. H., Othman, M., Heckenlively, J. R., Swaroop, A., Campochiaro, B., Vote, B. J. T., Craig, J. E., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.11.042 · Cited by 50 · see citing works
Self-citationLien, Y., Condon, D. E., Georgieff, M., Simmons, R. A., & Tran, P. V. (2019) · Nutrients · doi:10.3390/nu11051191 · Cited by 50 · see citing works
Epigenetic Mechanisms of the Aging Human Retina
Pennington, K. L., & DeAngelis, M. M. (2015) · Journal of Experimental Neuroscience · doi:10.4137/jen.s25513 · Cited by 41 · see citing works
Genome Wide Methylome Alterations in Lung Cancer
Mullapudi, N., Ye, B., Suzuki, M., Fazzari, M. J., Han, W., Shi, M. K., Marquardt, G., Lin, J., Wang, T., Keller, S. M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143826 · Cited by 36 · see citing works
Conserved and Divergent Patterns of DNA Methylation in Higher Vertebrates
Jiang, N., Wang, L., Chen, J., Wang, L., Leach, L. J., & Luo, Z. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu238 · Cited by 34 · see citing works
Cross-tissue comparisons of leptin and adiponectin
Houde, A.-A., Légaré, C., Hould, F., Lebel, S., Marceau, P., Tchernof, A., Vohl, M., Hivert, M., & Bouchard, L. (2014) · Adipocyte · doi:10.4161/adip.28308 · Cited by 31 · see citing works
Xing, K., Liu, Z., Liu, L., Zhang, J., Qanmber, G., Wang, Y., Liu, L., Gu, Y., Zhang, C., Li, S., et al. (2023) · The Plant Journal · doi:10.1111/tpj.16274 · Cited by 29 · see citing works
Smith, A. A., Huang, Y., Eliot, M., Houseman, E. A., Marsit, C. J., Wiencke, J. K., & Kelsey, K. T. (2014) · Epigenetics · doi:10.4161/epi.28571 · Cited by 29 · see citing works
Cao, W., Xu, Y., Luo, D., Saeed, M., & Sun, C. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000487343 · Cited by 29 · see citing works
Estimating the prevalence of functional exonic splice regulatory information
Savisaar, R., & Hurst, L. D. (2017) · Human Genetics · doi:10.1007/s00439-017-1798-3 · Cited by 25 · see citing works
DNA methylation in oligodendroglial cells during developmental myelination and in disease
Moyon, S., & Casaccia, P. (2017) · Neurogenesis · doi:10.1080/23262133.2016.1270381 · Cited by 24 · see citing works
Methylation-specific PCR: four steps in primer design
Davidović, R. S., Božović, A., Mandušić, V., & Krajnović, M. (2014) · Open Life Sciences · doi:10.2478/s11535-014-0324-z · Cited by 23 · see citing works
Ctcf haploinsufficiency mediates intron retention in a tissue-specific manner
Alharbi, A. B., Schmitz, U., Marshall, A. D., Vanichkina, D., Nagarajah, R., Vellozzi, M., Wong, J. J. L., Bailey, C. G., & Rasko, J. E. J. (2020) · RNA Biology · doi:10.1080/15476286.2020.1796052 · Cited by 21 · see citing works
Ullah, F., Jabeen, S., Salton, M., Reddy, A. S. N., & Ben‐Hur, A. (2023) · Genome biology · doi:10.1186/s13059-023-02885-1 · Cited by 21 · see citing works
Prediction of promoters and enhancers using multiple DNA methylation-associated features
Hwang, W., Oliver, V. F., Merbs, S. L., Zhu, H., & Qian, J. X. (2015) · BMC Genomics · doi:10.1186/1471-2164-16-s7-s11 · Cited by 19 · see citing works
Self-citationPrioritizing protein complexes implicated in human diseases by network optimization
Chen, Y., Jacquemin, T., Zhang, S., & Jiang, R. (2014) · BMC Systems Biology · doi:10.1186/1752-0509-8-s1-s2 · Cited by 18 · see citing works
Dechow, C. D., & Liu, W. (2018) · BMC Genomics · doi:10.1186/s12864-018-5124-9 · Cited by 18 · see citing works
DNA methylation in Schwann cells and in oligodendrocytes
Arthur‐Farraj, P., & Moyon, S. (2020) · Glia · doi:10.1002/glia.23784 · Cited by 17 · see citing works
Epigenetic Regulation of Alternative mRNA Splicing in Dilated Cardiomyopathy
Gi, W., Haas, J., Sedaghat‐Hamedani, F., Kayvanpour, E., Tappu, R., Lehmann, D. H., Samani, O. S., Wisdom, M., Keller, A., Katus, H. A., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9051499 · Cited by 18 · see citing works
Erdem, G. Ç., Erdemir, S., Abacı, İ., Aydın, A. K., Everest, E., & Turanlı, E. T. (2017) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2016-0234 · Cited by 12 · see citing works
Fang, S.-Y., Liu, S., Yang, D., Yang, L., Hu, C.-D., & Wan, J. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.957023 · Cited by 10 · see citing works
Self-citationEpigenetics in Ocular Medicine
Oliver, V. F., van Bysterveldt, K. A., & Merbs, S. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803239-8.00022-3 · Cited by 11 · see citing works
Self-citationYang, Y., Kumar, H., Xie, Y., Zhao, L., Li, R., Chen, W., Diala, C. S., Ali, M. A., Xu, Y., Wu, A., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae1018 · Cited by 9 · see citing works
Alternative splicing in aging and aging-related diseases: From pathogenesis to therapy
Han, M., Han, P., Wang, Z., Kong, L., Xu, Q., Liu, Q., & Sun, Y. (2025) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2025.108887 · Cited by 9 · see citing works
Holly, A. C., Pilling, L. C., Hernandez, D. G., Lee, B. P., Singleton, A., Ferrucci, L., Melzer, D. R., & Harries, L. W. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2014.01.005 · Cited by 9 · see citing works
Landscape of alternative splicing in Capra_hircus
Xu, T., Xu, F., Gu, L., Rong, G., Mao, L., Qiao, F., Shi, L., Wang, D., Xia, W., Xun, W., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-33078-7 · Cited by 8 · see citing works
Identification of Novel Regulatory Regions Induced by Intrauterine Growth Restriction in Rat Islets
Lien, Y., Pinney, S. E., Lu, X. M., & Simmons, R. A. (2021) · Endocrinology · doi:10.1210/endocr/bqab251 · Cited by 6 · see citing works
In silico analysis of regulatory and structural motifs of the ovine HSP90AA1 gene
González, C., Salces-Ortiz, J., Calvo, J. H., & Serrano, M. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0668-6 · Cited by 4 · see citing works
He, X., Zhang, W., Fu, W., Liu, X., Yang, P., Wang, J., Zhu, M., Li, S., Zhang, W., Zhang, X., et al. (2022) · Cancer Biomarkers · doi:10.3233/cbm-210407 · Cited by 1 · see citing works
Epigenetic Regulation of Alternative Splicing in Cancer
Kumar, S., & Kumar, D. S. S. (2014) · D-Scholarship@Pitt (University of Pittsburgh) · Cited by 1 · see citing works
Blood DNA methylation biomarkers for breast cancer risk
Brennan, K. (2013) · Spiral (Imperial College London) · doi:10.25560/23641
Epigenetic Modifications to Cytosine and Alzheimer’s Disease
Ellison, E. M. (2017) · UKnowledge (University of Kentucky) · doi:10.13023/etd.2017.398
Epigenetics in ocular medicine
Liu, J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823928-5.00003-7
- Authors
- Wan, J., Oliver, V. F., Zhu, H., Zack, D. J., Qian, J., & Merbs, S. L.
- Affiliations
- Institut de la Vision (FR)
- Corresponding author
- Merbs, S. L.
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-07-24
- Volume
- 41
- Issue
- 18
- Pages
- 8503-8514
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC3794605
- OpenAlex
- W2139756825
- Cited by
- 49
- References
- 49
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 4 · 2016: 6 · 2015: 7 · 2014: 10 · 2013: 2
- FWCI
- 3.74
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nucleic Acids Research (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- ResearchSpace (University of Auckland) (submittedVersion, cc-by)
- Funders
- Research to Prevent Blindness
- National Eye Institute (R21EY018703, R01EY009769, P30EY001765, R21EY021897)
- National Institute of General Medical Sciences (R01GM076102)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- DNA methylation, alternative splicing, CTCF, transcription factor binding motifs, tissue-specific gene regulation, retina, brain, CpG, splicing regulation, developmental genes, evolutionary conservation
- MeSH terms
- Animals, Base Sequence, Binding Sites, Brain, DNA, Exons, Introns, Mice, Inbred C57BL, Organ Specificity, Proteins, Regulatory Sequences, Nucleic Acid, Retina, Transcription Factors, Conserved Sequence, Alternative Splicing, Evolution, Molecular, DNA Methylation, Mice, Nucleotide Motifs
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
