Highly individual methylation patterns of alternative glucocorticoid receptor promoters suggest individualized epigenetic regulatory mechanisms
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The transcription start sites (TSS) and promoters of many genes are located in upstream CpG islands. Methylation within such islands is known for both imprinted and oncogenes, although poorly studied for other genes, especially those with complex CpG islands containing multiple first exons and promoters. The glucocorticoid receptor (GR) CpG island contains seven alternative first exons and their promoters. Here we show for the five GR promoters activated in PBMCs that methylation patterns are highly variable between individuals. The majority of positions were methylated at levels >25% in at least one donor affecting each promoter and TSS. We also examined the evolutionarily conserved transcription factor binding sites (TFBS) using an improved in silico phylogenetic footprinting technique. The majority of these contain methylatable CpG sites, suggesting that methylation may orchestrates alternative first exon usage, silencing and controlling tissue-specific expression. The heterogeneity observed may reflect epigenetic mechanisms of GR fine tuning, programmed by early life environment and events. With 78% of evolutionarily conserved alternative first exons falling into such complex CpG islands, their internal structure and epigenetic modifications are bound to be biologically important, and may be a common transcriptional control mechanism used throughout many phyla.
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Stress or trauma was correlated with higher methylation of exon 1F of NR3C1, the homolog of exon 17 in the rat.
“The results of these studies consistently demonstrated that stress or trauma was correlated with higher methylation of exon 1F of NR3C1, which is the homolog of exon 17 in the rat (Turner, Pelascini, Macedo, & Muller, 2008).”
From Associations Between Early Life Stress and Gene Methylation in Children (2015) · cites this paper as Turner et al., 2008
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Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Epigenetic differences arise during the lifetime of monozygotic twins
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500398102 · Cited by 3,602 · 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
Bird, A. (2007) · Nature · doi:10.1038/nature05913 · Cited by 3,011 · see citing works
Genome-scale DNA methylation maps of pluripotent and differentiated cells
Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., et al. (2008) · Nature · doi:10.1038/nature07107 · Cited by 2,536 · see citing works
International Journal of Molecular Medicine
(2026) · International Journal of Molecular Medicine · doi:10.3892/ijmm · Cited by 2,247 · see citing works
A gene hypermethylation profile of human cancer.
Esteller, M., Corn, P. G., Baylin, S. B., & Herman, J. G. (2001) · PubMed · Cited by 2,032 · see citing works
DNA Modification Mechanisms and Gene Activity During Development
Holliday, R., & Pugh, J. E. (1975) · Science · doi:10.1126/science.187.4173.226 · Cited by 1,973 · see citing works
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432 · see citing works
Aberrant CpG-island methylation has non-random and tumour-type–specific patterns
Costello, J., Frühwald, M. C., Smiraglia, D. J., Rush, L. J., Robertson, G. P., Gao, X. Y., Wright, F. A., Feramisco, J. D., Peltomäki, P., Lang, J. C., et al. (2000) · Nature Genetics · doi:10.1038/72785 · Cited by 1,359 · see citing works
X inactivation, differentiation, and DNA methylation
Riggs, A. D. (2008) · Cytogenetics and Cell Genetics · doi:10.1159/000130315 · Cited by 1,343 · see citing works
Bunz, U. H. F. (2005) · Science · doi:10.1126/science.1111098 · Cited by 1,252 · see citing works
MATCHTM: a tool for searching transcription factor binding sites in DNA sequences
Kel, A. E. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg585 · Cited by 1,095 · see citing works
Demmel, R. (1999) · Zeitschrift für Klinische Psychologie und Psychotherapie · doi:10.1026//0084-5345.28.1.68 · Cited by 1,010 · see citing works
Esteller, M., Sánchez‐Céspedes, M., Rosell, R., Sidransky, D., Baylin, S. B., & Herman, J. G. (1999) · PubMed · Cited by 921 · see citing works
Weaver, I. C. G., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3652-05.2005 · Cited by 905 · see citing works
Weaver, I. C. G., Meaney, M. J., & Szyf, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507526103 · Cited by 771 · see citing works
Park, J. H., Stoffers, D. A., Nicholls, R. D., & Simmons, R. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33655 · Cited by 640 · see citing works
Lillycrop, K. A., Slater-Jefferies, J. L., Hanson, M. A., Godfrey, K. M., Jackson, A. A., & Burdge, G. C. (2007) · British Journal Of Nutrition · doi:10.1017/s000711450769196x · Cited by 563 · see citing works
Kimura, K., Wakamatsu, A., Suzuki, Y., Ota, T., Nishikawa, T., Yamashita, R., Yamamoto, J.-I., Sekine, M., Tsuritani, K., Wakaguri, H., et al. (2006) · Genome Research · doi:10.1101/gr.4039406 · Cited by 506 · see citing works
Lillycrop, K. A., Phillips, E. S., Torrens, C., Hanson, M. A., Jackson, A. A., & Burdge, G. C. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114507894438 · Cited by 461 · see citing works
DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling
Fan, G., Martinowich, K., Chin, M. H., He, F., Fouse, S. D., Hutnick, L. K., Hattori, D., Ge, W., Shen, Y., Wu, H., et al. (2005) · Development · doi:10.1242/dev.01912 · Cited by 420 · see citing works
Song, F., Smith, J. F., Kimura, M., Morrow, A. D., Matsuyama, T., Nagase, H., & Held, W. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408436102 · Cited by 335 · see citing works
DNA-Binding Specificity of NGFI-A and Related Zinc Finger Transcription Factors
Swirnoff, A. H., & Milbrandt, J. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.4.2275 · Cited by 310 · see citing works
Methylation of CpG sequences in eukaryotic DNA
Gruenbaum, Y., Stein, R., Cedar, H., & Razin, A. (1981) · FEBS Letters · doi:10.1016/0014-5793(81)80055-5 · Cited by 301 · see citing works
Expression of various genes is controlled by DNA methylation during mammalian development
Ehrlich, M. (2003) · Journal of Cellular Biochemistry · doi:10.1002/jcb.10464 · Cited by 287 · see citing works
Kiefer, J. C. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21094 · Cited by 284 · see citing works
Lewin, J., Schmitt, A. O., Adorján, P., Hildmann, T., & Piepenbrock, C. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth346 · Cited by 260 · see citing works
McCormick, J. A., Lyons, V., Jacobson, M. D., Noble, J., Diorio, J. C., Nyirenda, M., Weaver, S., Ester, W. A., Yau, J. L. W., Meaney, M. J., et al. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.4.0438 · Cited by 258 · see citing works
Turner, J. D., & Muller, C. P. (2005) · Journal of Molecular Endocrinology · doi:10.1677/jme.1.01822 · Cited by 256 · see citing works
The journal of clinical investigation
(1993) · Journal of the American Dietetic Association · doi:10.1016/0002-8223(93)92071-5 · Cited by 253 · see citing works
Hoque, M. O., Topaloglu, Ö., Begum, S., Henrique, R., Rosenbaum, E., Criekinge, W. V., Westra, W. H., & Sidransky, D. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.07.009 · Cited by 240 · see citing works
Weaver, I. C. G. (2007) · Epigenetics · doi:10.4161/epi.2.1.3881 · Cited by 239 · see citing works
Kim, J. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg028 · Cited by 206 · see citing works
Variations in DNA methylation during mouse cell differentiation in vivo and in vitro.
Razin, A., Webb, C., Moshe Szyf, A., Yisraeli, J. K., Rosenthal, A., Naveh‐Many, T., Sciaky-Gallili, N., & Cedar, H. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.8.2275 · Cited by 191 · see citing works
Diverse transcriptional initiation revealed by fine, large‐scale mapping of mRNA start sites
Suzuki, Y., Taira, H., Tsunoda, T., Mizushima‐Sugano, J., Sese, J., Hata, H., Ota, T., Isogai, T., Tanaka, T., Morishita, S., et al. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve085 · Cited by 159 · see citing works
Allegrucci, C., Wu, Y.-Z., Thurston, A., Denning, C. N., Priddle, H., Mummery, C. L., Oostwaard, D. W., Andrews, P. W., Stojković, M., Smith, N. M., et al. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm074 · Cited by 159 · see citing works
Imamura, T., Ohgane, J., Ito, S., Ogawa, T., Hattori, N., Tanaka, S., & Shiota, K. (2001) · Genomics · doi:10.1006/geno.2001.6607 · Cited by 117 · see citing works
Tissue specific glucocorticoid receptor expression, a role for alternative first exon usage?
Turner, J. D., Schote, A. B., Macedo, J. A., Pelascini, L. P. L., & Muller, C. P. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.07.005 · Cited by 99 · see citing works
In Silico Detection of Sequence Variations Modifying Transcriptional Regulation
Andersen, M., Engström, P. G., Lithwick, S., Arenillas, D. J., Eriksson, P. O., Lenhard, B., Wasserman, W. W., & Odeberg, J. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0040005 · Cited by 96 · see citing works
Presul, E., Schmidt, S. U., Kofler, R., & Helmberg, A. (2007) · Journal of Molecular Endocrinology · doi:10.1677/jme.1.02183 · Cited by 93 · see citing works
Genomic imprinting and reproduction
Swales, A. K. E., & Spears, N. (2005) · Reproduction · doi:10.1530/rep.1.00395 · Cited by 82 · see citing works
Characterization of the Human Glucocorticoid Receptor Promoter
Nobukuni, Y., Smith, C. L., Hager, G. L., & Detera‐Wadleigh, S. D. (1995) · Biochemistry · doi:10.1021/bi00025a028 · Cited by 78 · see citing works
Impaired methionine synthesis and hypomethylation in rats exposed to valproate during gestation
Alonso-Aperte, E., Úbeda, N., Achón, M., Pérez‐Miguelsanz, J., & Varela‐Moreiras, G. (1999) · Neurology · doi:10.1212/wnl.52.4.750 · Cited by 74 · see citing works
Breslin, M. B., & Vedeckis, W. V. (1998) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00138-1 · Cited by 65 · see citing works
Shimabukuro, M., Jinno, Y., Fuke, C., & Okazaki, Y. (2006) · Behavioral and Brain Functions · doi:10.1186/1744-9081-2-37 · Cited by 64 · see citing works
Characterization of promoter 1B in the human glucocorticoid receptor gene
Nunez, B. S., & Vedeckis, W. V. (2002) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00676-1 · Cited by 56 · see citing works
Moser, D., Molitor, A. M., Kumsta, R., Tatschner, T., Riederer, P. F., & Meyer, J. (2007) · The World Journal of Biological Psychiatry · doi:10.1080/15622970701429862 · Cited by 50 · see citing works
Alternative transcripts and evidence of imprinting of GNAL on 18p11.2
Corradi, J., RAVYN, V., Robbins, A. K., Hagan, K. W., Peters, M. F., Bostwick, R. J., Buono, R. J., Berrettini, W. H., & Furlong, S. T. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001713 · Cited by 40 · see citing works
Transcriptional regulation of neuronal differentiation: The epigenetic layer of complexity
Hamby, M. E., Coskun, V., & Sun, Y. E. (2008) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2008.07.006 · Cited by 36 · see citing works
Hypermethylation of the 5′CpG island of the FHIT gene in clear cell renal carcinomas
Kvasha, S. M., Gordiyuk, V. V., Kondratov, O., Ugryn, D., Zgonnyk, Y. M., Rynditch, A. V., & Vozianov, A. F. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.02.036 · Cited by 32 · see citing works
Tsuritani, K., Irie, T., Yamashita, R., Sakakibara, Y., Wakaguri, H., Kanai, A., Mizushima‐Sugano, J., Sugano, S., Nakai, K., & Suzuki, Y. (2007) · Genome Research · doi:10.1101/gr.6030107 · Cited by 31 · see citing works
Manev, H., & Uz, T. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)01711-9 · Cited by 23 · see citing works
Human embryonic stem cells as a model for nutritional programming: An evaluation
Allegrucci, C., Denning, C. N., Burridge, P. W., Steele, W., Sinclair, K. D., & Young, L. E. (2005) · Reproductive Toxicology · doi:10.1016/j.reprotox.2005.04.010 · Cited by 23 · see citing works
Region-specific DNA methylation in the preimplantation embryo as a target for genomic plasticity
Thurston, A., Lucas, E. S., Allegrucci, C., Steele, W., & Young, L. E. (2007) · Theriogenology · doi:10.1016/j.theriogenology.2007.03.020 · Cited by 15 · see citing works
Huehne, K., & Rautenstrauß, B. (2001) · International Journal of Molecular Medicine · doi:10.3892/ijmm.7.6.669 · Cited by 12 · see citing works
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Labonte, B., Yerko, V., Gross, J., Mechawar, N., Meaney, M. J., Szyf, M., & Turecki, G. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.034 · Cited by 345 · see citing works
Beck, I. M. E., Vanden Berghe, W., Vermeulen, L., Yamamoto, K. R., Haegeman, G., & De Bosscher, K. (2009) · Endocrine Reviews · doi:10.1210/er.2009-0013 · Cited by 298 · see citing works
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Romens, S. E., McDonald, J., Svaren, J., & Pollak, S. D. (2015) · Child Development · doi:10.1111/cdev.12270 · Cited by 299 · see citing works
Alt, S. R., Turner, J. D., Klok, M. D., Meijer, O. C., Lakke, E. A. J. F., DeRijk, R. H., & Muller, C. P. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.09.001 · Cited by 184 · see citing works
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Leenen, F. A. D., Muller, C. P., & Turner, J. D. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0256-8 · Cited by 186 · see citing works
Role of the hypothalamic–pituitary–adrenal axis in developmental programming of health and disease
Xiong, F., & Zhang, L. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.11.002 · Cited by 177 · see citing works
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Buchheit, T. E., de Ven, T. V., & Shaw, A. (2012) · Pain Medicine · doi:10.1111/j.1526-4637.2012.01488.x · Cited by 175 · see citing works
van der Knaap, L. J., Riese, H., Hudziak, J. J., Verbiest, M. M. P. J., Verhulst, F. C., Oldehinkel, A. J., & van Oort, F. V. A. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.22 · Cited by 165 · see citing works
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Turner, J. D., Alt, S. R., Cao, L., Vernocchi, S., Trifonova, S. T., Battello, N., & Muller, C. P. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.06.037 · Cited by 145 · see citing works
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Wright, R. J. (2010) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2010.09.011 · Cited by 145 · see citing works
Drake, A. J., McPherson, R. C., Godfrey, K. M., Cooper, C. C., Lillycrop, K. A., Hanson, M. A., Meehan, R. R., Seckl, J. R., & Reynolds, R. M. (2012) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2012.04453.x · Cited by 133 · see citing works
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Pal, S., Gupta, R., & Davuluri, R. V. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.08.005 · Cited by 122 · see citing works
Tyrka, A. R., Ridout, K. K., & Parade, S. H. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000870 · Cited by 119 · see citing works
Epigenetic effects of glucocorticoids
Weaver, I. C. G. (2009) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2008.12.002 · Cited by 120 · see citing works
Luo, J., Li, Y., Wang, F., Zhang, W.-M., & Geng, X. (2010) · International Journal of Biological Sciences · doi:10.7150/ijbs.6.784 · Cited by 117 · see citing works
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Weaver, I. C. G. (2009) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20164 · Cited by 116 · see citing works
Hogg, K., Blair, J. D., McFadden, D. E., von Dadelszen, P., & Robinson, W. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062969 · Cited by 113 · see citing works
Perinatal stress and early life programming of lung structure and function
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Traumatic stress and human DNA methylation: A critical review
Vinkers, C. H., Kalafateli, A. L., Rutten, B. P., Kas, M. J., Kaminsky, Z., Turner, J. D., & Boks, M. P. (2015) · Epigenomics · doi:10.2217/epi.15.11 · Cited by 112 · see citing works
Self-citationEpigenetics and depressive disorders: a review of current progress and future directions
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Epigenetic regulation of the<i>glucocorticoid receptor</i>promoter 1<sub>7</sub>in adult rats
Witzmann, S. R., Turner, J. D., Mériaux, S. B., Meijer, O. C., & Muller, C. P. (2012) · Epigenetics · doi:10.4161/epi.22363 · Cited by 90 · see citing works
Wan, E. S., Qiu, W., Baccarelli, A., Carey, V. J., Bacherman, H., Rennard, S. I., Agustí, A. G. N., Anderson, W. H., Lomas, D. A., & DeMeo, D. L. (2012) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201207-1280oc · Cited by 86 · see citing works
Gonzalez‐Rodriguez, P. J., Xiong, F., Li, Y., Zhou, J., & Zhang, L. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.01.020 · Cited by 83 · see citing works
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Begum, G., Davies, A., Stevens, A., Oliver, M. H., Jaquiery, A. L., Challis, J. R. G., Harding, J. E., Bloomfield, F. H., & White, A. E. (2013) · Endocrinology · doi:10.1210/en.2013-1693 · Cited by 71 · see citing works
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Zhong, S., Israel, S., Shalev, I., Xue, H., Ebstein, R. P., & Chew, S. H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013765 · Cited by 67 · see citing works
Castillo, P., Ibanez-Carrasco, F., Guajardo, A., Llanos, M. N., & Ronco, A. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044139 · Cited by 62 · see citing works
Cao-Lei, L., Leija, S. C., Kumsta, R., Wüst, S., Meyer, J., Turner, J. D., & Muller, C. P. (2011) · Human Genetics · doi:10.1007/s00439-011-0949-1 · Cited by 58 · see citing works
Guo, C., Li, C., Myatt, L., Nathanielsz, P. W., & Sun, K. (2012) · Diabetes · doi:10.2337/db12-0561 · Cited by 57 · see citing works
de Rooij, S. R., Costello, P. M., Veenendaal, M. V. E., Lillycrop, K. A., Gluckman, P. D., Hanson, M. A., Painter, R. C., & Roseboom, T. J. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.09.010 · Cited by 52 · see citing works
Kay, P., Schlossmacher, G., Matthews, L. C., Sommer, P., Singh, D., White, A. E., & Ray, D. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024839 · Cited by 52 · see citing works
Huber, E., Notaro, U., Recce, S., Rodriguez, F., Ortega, H. H., Salvetti, N., & Rey, F. (2020) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2020.106348 · Cited by 40 · see citing works
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Sittig, L. J., Shukla, P. K., Herzing, L. B. K., & Redei, E. E. (2011) · The FASEB Journal · doi:10.1096/fj.10-179234 · Cited by 41 · see citing works
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Xiong, F., Lin, T., Song, M., Ma, Q., Martinez, S. R., Lv, J., Mata‐Greenwood, E., Xiao, D., Xu, Z., & Zhang, L. (2016) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2016.01.003 · Cited by 38 · see citing works
Chadwick, A. L., Frazier, A., Khan, T. W., & Young, E. E. (2021) · Journal of Pain Research · doi:10.2147/jpr.s320863 · Cited by 40 · see citing works
Hodyl, N. A., Stark, M. J., Osei-Kumah, A., & Clifton, V. L. (2011) · Expert Review of Clinical Immunology · doi:10.1586/eci.11.51 · Cited by 33 · see citing works
Boyce, W. T., & Hertzman, C. (2017) · Springer eBooks · doi:10.1007/978-3-319-47143-3_4 · Cited by 32 · see citing works
Suicidal function of DNA methylation in age-related genome disintegration
Mazin, A. L. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2009.04.005 · Cited by 32 · see citing works
Generalized and tissue specific glucocorticoid resistance
Martins, C. S., & de Castro, M. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111277 · Cited by 30 · see citing works
Qin, X. Y., Chen, P., Li, X., Zhang, G., Patterson, A. J., & Luo, J. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.115.129916 · Cited by 31 · see citing works
Heinrich, A., Buchmann, A. F., Zohsel, K., Dukal, H., Frank, J., Treutlein, J., Nieratschker, V., Witt, S. H., Brandeis, D., Schmidt, M. H., et al. (2015) · Behavior Genetics · doi:10.1007/s10519-015-9721-y · Cited by 28 · see citing works
Where does transcription start? 5′-RACE adapted to next-generation sequencing
Leenen, F. A. D., Vernocchi, S., Hunewald, O. E., Schmitz, S., Molitor, A. M., Muller, C. P., & Turner, J. D. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1328 · Cited by 28 · see citing works
Chen, H., Fan, J., Shou, Q., Zhang, L., Ma, H., & Fan, Y. (2015) · Rheumatology International · doi:10.1007/s00296-015-3266-5 · Cited by 26 · see citing works
Epigenetic programming of diverse glucocorticoid response and inflammatory/immune-mediated disease
Chen, P., Jiang, T., Ouyang, J., Cui, Y., & Chen, Y. (2009) · Medical Hypotheses · doi:10.1016/j.mehy.2009.08.013 · Cited by 25 · see citing works
Epigenetic studies of suicidal behavior
Bani‐Fatemi, A., Howe, A. S., & Luca, V. D. (2014) · Neurocase · doi:10.1080/13554794.2013.826679 · Cited by 24 · see citing works
Herbeck, Y. E., Gulevich, R. G., Amelkina, O., Plyusnina, I. Z., & Oskina, I. N. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.10.004 · Cited by 23 · see citing works
Endothelial glucocorticoid receptor promoter methylation according to dexamethasone sensitivity
Mata‐Greenwood, E., Jackson, P. N., Pearce, W. J., & Zhang, L. (2015) · Journal of Molecular Endocrinology · doi:10.1530/jme-15-0124 · Cited by 21 · see citing works
Huang, K., Hu, Y., Sun, Y., Yu, Z., Liu, W. Y., Zhu, P., & Tao, F. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.11.014 · Cited by 17 · see citing works
Agba, O. B., Lausser, L. M., Huse, K., Bergmeier, C., Jahn, N., Groth, M., Bens, M., Sahm, A., Gall, M., Witte, O. W., et al. (2017) · Physiological Genomics · doi:10.1152/physiolgenomics.00009.2017 · Cited by 17 · see citing works
Mor, D., & Keay, K. A. (2013) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-013-9962-3 · Cited by 16 · see citing works
Breivik, T., Gundersen, Y., Murison, R., Turner, J. D., Muller, C., Gjermo, P., & Opstad, K. (2015) · Open Dentistry Journal · doi:10.2174/1874210601509010065 · Cited by 17 · see citing works
The Role for Epigenetic Modifications in Pain and Analgesia Response
Lessans, S., & Dorsey, S. G. (2013) · Nursing Research and Practice · doi:10.1155/2013/961493 · Cited by 16 · see citing works
Zou, H., Li, R., Jia, Y., Yang, X., Ni, Y., Cong, R., Soloway, P. D., & Zhao, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040432 · Cited by 15 · see citing works
Epigenetic Effects of Childhood Adversity in the Brain and Suicide Risk
Dwivedi, Y. (2012) · CRC Press eBooks · doi:10.1201/b12215-19 · Cited by 14 · see citing works
Vetrovoy, O. V., Stratilov, V. A., Lomert, E. V., & Tyulkova, E. I. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03837-0 · Cited by 13 · see citing works
Stepanov, Y. K., Speidel, J. D., Herrmann, C., Schmid, N., Behr, R., Köhn, F., Stöckl, J. B., Pickl, U., Trottmann, M., Fröhlich, T., et al. (2022) · Cells · doi:10.3390/cells11193164 · Cited by 12 · see citing works
Epigenetic regulation of glucocorticoid receptor and infantile spasms
Yang, G., Zou, L., Wang, J., & Ding, Y.-X. (2010) · Medical Hypotheses · doi:10.1016/j.mehy.2010.09.014 · Cited by 11 · see citing works
Zhu, J., Zhu, F., Zhao, N., Mu, X. N., Li, P., Wang, W. T., Liu, J., & Ma, X. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23913 · Cited by 11 · see citing works
Taylor, K., Wheeler, R. J., Singh, N., Vosloo, D., Ray, D. W., & Sommer, P. (2018) · Scientific Reports · doi:10.1038/s41598-018-23309-2 · Cited by 11 · see citing works
What is a functional locus? Understanding the genetic basis of complex phenotypic traits
Ruiz-Narváez, E. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.01.019 · Cited by 10 · see citing works
Prenatal Stress as a Factor of the Development of Addictive States
Stratilov, V. A., Tyulkova, E. I., & Vetrovoy, O. V. (2020) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093020060010 · Cited by 9 · see citing works
Weaver, I. C. G. (2011) · Springer eBooks · doi:10.1007/978-3-642-17426-1_11 · Cited by 6 · see citing works
Vos, S., den Bergh, B. R. H. V., Martens, D. S., Bijnens, E. M., Shkedy, Z., Kindermans, H. P. J., Platzer, M., Schwab, M. G., & Nawrot, T. S. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107088 · Cited by 5 · see citing works
Investigation of Interactions between DNA and Nuclear Receptors: A Review of the Most Used Methods
Fattori, J., Indolfo, N. D. C., Campos, J. C. L. D. O., Videira, N. B., Bridi, A. V., Doratioto, T. R., de Assis, M. A., & Figueira, A. C. M. (2014) · Nuclear Receptor Research · doi:10.11131/2014/101090 · Cited by 5 · see citing works
The Epigenetics of Depression and Suicide
Labonté, B., & Turecki, G. (2011) · Springer eBooks · doi:10.1007/978-3-642-17426-1_4 · Cited by 5 · see citing works
Weaver, I. C. G. (2010) · Advances in neurobiology · doi:10.1007/978-1-4419-7197-5_3 · Cited by 4 · see citing works
Antenatal Steroids and Cord Blood T-cell Glucocorticoid Receptor DNA Methylation and Exon 1 Splicing
Carpenter, J. R., Jablonski, K. A., Koncinsky, J., Varner, M. W., Gyamfi‐Bannerman, C., & Joss‐Moore, L. A. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-00859-5 · Cited by 4 · see citing works
Epigenetics: Integrating Genetic Programs, Brain Development and Emergent Phenotypes
Weaver, I. C. G. (2014) · Cell & Developmental Biology · doi:10.4172/2168-9296.1000132 · Cited by 3 · see citing works
Singh, N., Taylor, K., Mjoli, P. B., Poolman, T. M., Ray, D. W., & Sommer, P. (2014) · Genes Chromosomes and Cancer · doi:10.1002/gcc.22209 · Cited by 3 · see citing works
DNA Methylation Analysis of Steroid Hormone Receptor Genes
Camacho‐Arroyo, I., Hansberg-Pastor, V., & Rodríguez‐Dorantes, M. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-0856-1_8 · Cited by 3 · see citing works
Selective Activation of Alternative MYC Core Promoters by Wnt-Responsive Enhancers
Bardales, J. A., Wieser, E., Kawaji, H., Murakawa, Y., & Darzacq, X. (2018) · Genes · doi:10.3390/genes9060270 · Cited by 3 · see citing works
Turner, J. D., Kirschner, S. A., Molitor, A. M., Evdokimov, K., & Muller, C. P. (2015) · Elsevier eBooks · doi:10.1016/b978-0-08-097086-8.14142-x · Cited by 3 · see citing works
Use of alternative promoters may hide genetic effects on phenotypic traits
Ruiz-Narváez, E. (2012) · Journal of Human Genetics · doi:10.1038/jhg.2012.115 · Cited by 2 · see citing works
Impact of the Early-Life Environment on the Epigenome and Behavioral Development
Labonté, B., & Turecki, G. (2013) · Springer eBooks · doi:10.1007/978-1-4614-8078-5_8 · Cited by 1 · see citing works
Epigenomics: Epigenetic effects of childhood abuse on the human brain
Labonté, B., & Turecki, G. (2012) · Cambridge University Press eBooks · doi:10.1017/cbo9780511777271.040
Stolerman, I. P., & Price, L. H. (2015) · Springer eBooks · doi:10.1007/978-3-642-36172-2_200048 · Cited by 2 · see citing works
Gråberg, T., Bergman, E. A., Strömmer, L., Sjöholm, L. K., Wikström, A., Winqvist, O., & Winerdal, M. (2022) · Molecular Medicine Reports · doi:10.3892/mmr.2022.12714 · Cited by 1 · see citing works
Hsu, C. (2012) · NC Digital Online Collection of Knowledge and Scholarship (The University of North Carolina at Greensboro) · Cited by 1 · see citing works
Social Disparities in Lung Growth and Respiratory Health
Brunst, K. J., & Wright, R. J. (2015) · Respiratory medicine · doi:10.1007/978-3-319-23675-9_8 · Cited by 1 · see citing works
Antenatal determinants of child lung development
Holden, K. A., Gibson, M., Sinha, I. P., & Hawcutt, D. B. (2023) · European Respiratory Society eBooks · doi:10.1183/2312508x.10016222 · Cited by 1 · see citing works
Kay, P., Schlossmacher, G., Matthews, L. C., Sommer, P., Singh, D., White, A. E., & Ray, D. W. (2013) · PLoS ONE · doi:10.1371/annotation/4aad3313-abac-404f-85b0-3b95aec89be4 · Cited by 1 · see citing works
George, S. (2011) · InTech eBooks · doi:10.5772/23106
Regional Anesthesia and Valproate Sodium for the Prevention of Chronic Post-Amputation Pain
Buchheit, T. E., Hsia, H.-L. J., Shaw, A., Buckenmaier, C. C., & de Ven, T. V. (2013) · doi:10.21236/ada598745
The effects of a cigarette carcinogen on glucocorticoid receptor methylation.
Wheeler, R. J. (2014)
Modulation of GR transcriptional signalling by HIV-1 Vpr: insights into regulation by progestins
Grantham, N. J. (2012) · Open University of Cape Town (University of Cape Town)
Labonté, B., & Turecki, G. (2014) · Cambridge University Press eBooks · doi:10.1017/cbo9781139519502.034
The Role of Glucocorticoid Receptor in the Racial/Ethnic Disparity of Aggressive Breast Cancer
Al‐Alem, U. (2015) · Figshare
Research: Mediators and Moderators
Koslow, S. H., Ruiz, P., & Nemeroff, C. B. (2014) · Cambridge University Press eBooks · doi:10.1017/cbo9781139519502.033
Characterization of Glucocorticoid Receptor Promoter Methylation in Breast Cancer
Nesset, K. A. (2012) · QSpace (Queen's University Library)
Locus specific DNA methylation in human immunological responses
Bergman, E. A. (2018) · Figshare
Mendieta, B., & Adalberto, J. (2018)
Genetics and Epigenetics of Suicidal Behavior
Bani‐Fatemi, A. (2018) · TSpace (University of Toronto)
- Authors
- Turner, J. D., Pelascini, L. P. L., Macedo, J. A., & Muller, C. P.
- Affiliations
- Laboratoire National de Santé (LU)
- Corresponding author
- Muller, C. P.
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-11-12
- Volume
- 36
- Issue
- 22
- Pages
- 7207-7218
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC2602793
- OpenAlex
- W2169090691
- Cited by
- 104
- References
- 56
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 5 · 2021: 2 · 2020: 2 · 2018: 6 · 2017: 2 · 2016: 5 · 2015: 12 · 2014: 13 · 2013: 10 · 2012: 19
- FWCI
- 3.29
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nucleic Acids Research (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (GRK 1389/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- glucocorticoid receptor, alternative first exons, promoter methylation, CpG islands, transcription start sites, transcription factor binding sites, phylogenetic footprinting, tissue-specific gene expression, epigenetic regulation, peripheral blood mononuclear cells
- MeSH terms
- Adult, Aged, Animals, Binding Sites, Cattle, Female, Humans, Male, Middle Aged, Phylogeny, Promoter Regions, Genetic, Receptors, Glucocorticoid, Transcription Factors, CpG Islands, DNA Methylation, Genomics, Transcription Initiation Site, Epigenesis, Genetic, Mice, Rats
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