Bisphenol-A induces expression of HOXC6, an estrogen-regulated homeobox-containing gene associated with breast cancer

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 6, 2015, Pages 697-708

  Hussain, Imran ^a   Bhan, Arunoday ^a   Ansari, Khairul I ^a   Deb, Paromita ^a   Bobzean, Samara A M ^a   Perrotti, Linda I ^a   Mandal, Subhrangsu S ^a  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

Author keywords

Bisphenol A; Endocrine disruption; Epigenetics; Estrogen receptors; HOXC6 expression; Mixed lineage leukemia (MLL)

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA, HUMAN; HOMEODOMAIN PROTEIN; HOXC6 PROTEIN, HUMAN; PHENOL DERIVATIVE;

ANIMAL; BIOSYNTHESIS; BREAST NEOPLASMS; DRUG EFFECTS; EPIGENETICS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; PATHOLOGY; RAT;

ANIMALS; BENZHYDRYL COMPOUNDS; BREAST NEOPLASMS; ENDOCRINE DISRUPTORS; EPIGENOMICS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MCF-7 CELLS; PHENOLS; RATS;

EID: 84938325330     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.02.003     Document Type: Article

References (104)

1. Lappin T.R., Grier D.G., Thompson A., Halliday H.L. HOX genes: seductive science, mysterious mechanisms. Ulster Med. J. 2006, 75:23-31.
2. Yu B.D., Hess J.L., Horning S.E., Brown G.A., Korsmeyer S.J. Altered Hox expression and segmental identity in Mll-mutant mice. Nature 1995, 378:505-508.
3. Alexander T., Nolte C., Krumlauf R. Hox genes and segmentation of the hindbrain and axial skeleton. Annu. Rev. Cell Dev. Biol. 2009, 25:431-456.
4. Takahashi Y., Hamada J.I., Murakawa K., Takada M., Tada M., Nogami I., Hayashi N., Nakamori S., Monden M., Miyamoto M., Katoh H., Moriuchi T. Expression profiles of 39 HOX genes in normal human adult organs and anaplastic thyroid cancer cell lines by quantitative real-time RT-PCR system. Exp. Cell Res. 2004, 293:144-153.
5. Mallo M., Alonso C.R. The regulation of Hox gene expression during animal development. Development 2013, 140:3951-3963.
6. Bhan A., Mandal S.S. Long noncoding RNAs: emerging stars in gene regulation, epigenetics and human disease. ChemMedChem 2014, 9:1932-1956.
7. Hueber S.D., Lohmann I. Shaping segments: Hox gene function in the genomic age. Bioessays 2008, 30:965-979.
8. Chen H., Sukumar S. HOX genes: emerging stars in cancer. Cancer Biol. Ther. 2003, 2:524-525.
9. Friedmann Y., Daniel C.A., Strickland P., Daniel C.W. Hox genes in normal and neoplastic mouse mammary gland. Cancer Res. 1994, 54:5981-5985.
10. Makiyama K., Hamada J., Takada M., Murakawa K., Takahashi Y., Tada M., Tamoto E., Shindo G., Matsunaga A., Teramoto K., Komuro K., Kondo S., Katoh H., Koike T., Moriuchi T. Aberrant expression of HOX genes in human invasive breast carcinoma. Oncol. Rep. 2005, 13:673-679.
11. Maroulakou I.G., Spyropoulos D.D. The study of HOX gene function in hematopoietic, breast and lung carcinogenesis. Anticancer Res. 2003, 23:2101-2110.
12. Nunes F.D., Almeida F.C.S.d., Tucci R., Sousa S.C.O.M.d. Homeobox genes: a molecular link between development and cancer. Pesqui. Odontol. Bras. 2003, 17:94-98.
13. Rhoads K., Arderiu G., Charboneau A., Hansen S.L., Hoffman W., Boudreau N. A role for Hox A5 in regulating angiogenesis and vascular patterning. Lymphat. Res. Biol. 2005, 3:240-252.
14. Ansari K.I., Hussain I., Kasiri S., Mandal S.S. HOXC10 is overexpressed in breast cancer and transcriptionally regulated by estrogen via involvement of histone methylases MLL3 and MLL4. J. Mol. Endocrinol. 2012, 48:61-75.
15. Ansari K.I., Hussain I., Shrestha B., Kasiri S., Mandal S.S. HOXC6 Is transcriptionally regulated via coordination of MLL histone methylase and estrogen receptor in an estrogen environment. J. Mol. Biol. 2011, 411:334-349.
16. Shrestha B., Ansari K.I., Bhan A., Kasiri S., Hussain I., Mandal S.S. Homeodomain-containing protein HOXB9 regulates expression of growth and angiogenic factors, facilitates tumor growth in vitro and is overexpressed in breast cancer tissue. FEBS J. 2012, 279:3715-3726.
17. Kasiri S., Ansari K.I., Hussain I., Bhan A., Mandal S.S. Antisense oligonucleotide mediated knockdown of HOXC13 affects cell growth and induces apoptosis in tumor cells and over expression of HOXC13 induces 3D-colony formation. RSC Adv. 2013, 3:3260-3269.
18. Chen H., Sukumar S. Role of homeobox genes in normal mammary gland development and breast tumorigenesis. J. Mammary Gland Biol. Neoplasia 2003, 8:159-175.
19. Kelly Z.L., Michael A., Butler-Manuel S., Pandha H.S., Morgan R.G. HOX genes in ovarian cancer. J Ovarian Res 2011, 4:16.
20. Yamashita T., Tazawa S., Yawei Z., Katayama H., Kato Y., Nishiwaki K., Yokohama Y., Ishikawa M. Suppression of invasive characteristics by antisense introduction of overexpressed HOX genes in ovarian cancer cells. Int. J. Oncol. 2006, 28:931-938.
21. Bodey B., Bodey B., Siegel S.E., Kaiser H.E. Immunocytochemical detection of the homeobox B3, B4, and C6 gene products in breast carcinomas. Anticancer Res. 2000, 20:3281-3286.
22. Castronovo V., Kusaka M., Chariot A., Gielen J., Sobel M. Homeobox genes: potential candidates for the transcriptional control of the transformed and invasive phenotype. Biochem. Pharmacol. 1994, 47:137-143.
23. Garcia-Gasca A., Spyropoulos D.D. Differential mammary morphogenesis along the anteroposterior axis in Hoxc6 gene targeted mice. Dev. Dyn. 2000, 219:261-276.
24. Ramachandran S., Liu P.B., Young A.N., Yin-Goen Q.Q., Lim S.D., Laycock N., Amin M., Carney J.K., Marshall F.F., Petros J.A., Moreno C.S. Loss of HOXC6 expression induces apoptosis in prostate cancer cells. Oncogene 2005, 24:188-198.
25. Bodey B., Bodey B., Groger A.M., Siegel S.E., Kaiser H.E. Immunocytochemical detection of homeobox B3, B4, and C6 gene product expression in lung carcinomas. Anticancer Res. 2000, 20:2711-2716.
26. Vinarskaja A., Yamanaka M., Ingenwerth M., Schulz W.A. DNA methylation and the HOXC6 paradox in prostate cancer. Cancers (Basel) 2011, 3:3714-3725.
27. Bijl J., van Oostveen J.W., Kreike M., Rieger E., van der Raaij-Helmer L.M., Walboomers J.M., Corte G., Boncinelli E., van den Brule A.J., Meijer C.J. Expression of HOXC4, HOXC5, and HOXC6 in human lymphoid cell lines, leukemias, and benign and malignant lymphoid tissue. Blood 1996, 87:1737-1745.
28. Bodey B., Bodey B., Siegel S.E., Luck J.V., Kaiser H.E. Homeobox B3, B4, and C6 gene product expression in osteosarcomas as detected by immunocytochemistry. Anticancer Res. 2000, 20:2717-2721.
29. Bodey B., Bodey B., Siegel S.E., Kaiser H.E. Immunocytochemical detection of the homeobox B3, B4, and C6 gene products in childhood medulloblastomas/primitive neuroectodermal tumors. Anticancer Res. 2000, 20:1769-1780.
30. McCabe C.D., Spyropoulos D.D., Martin D., Moreno C.S. Genome-wide analysis of the homeobox C6 transcriptional network in prostate cancer. Cancer Res. 2008, 68:1988-1996.
31. Moon S.-M., Kim S.-A., Yoon J.-H., Ahn S.-G. HOXC6 is deregulated in human head and neck squamous cell carcinoma and modulates Bcl-2 expression. J. Biol. Chem. 2012, 287:35678-35688.
32. Grishina I.B., Kim S.Y., Ferrara C., Makarenkova H.P., Walden P.D. BMP7 inhibits branching morphogenesis in the prostate gland and interferes with Notch signaling. Dev. Biol. 2005, 288:334-347.
33. Ricort J.M., Binoux M. Insulin-like growth factor-binding protein-3 activates a phosphotyrosine phosphatase. Effects on the insulin-like growth factor signaling pathway. J. Biol. Chem. 2002, 277:19448-19454.
34. Geer P.V., Hunter T., Lindberg R.A. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 1994, 10:251-337.
35. Lin Y., Liu G., Zhang Y., Hu Y.-P., Yu K., Lin C., McKeehan K., Xuan J.W., Ornitz D.M., Shen M.M., Greenberg N., McKeehan W.L., Wang F. Fibroblast growth factor receptor 2 tyrosine kinase is required for prostatic morphogenesis and the acquisition of strict androgen dependency for adult tissue homeostasis. Development 2007, 134:723-734.
36. Chariot A., Castronovo V., Le P., Gillet C., Sobel M.E., Gielen J. Cloning and expression of a new HOXC6 transcript encoding a repressing protein. Biochem. J. 1996, 319(Pt 1):91-97.
37. Zhang X., Hamada J., Nishimoto A., Takahashi Y., Murai T., Tada M., Moriuchi T. HOXC6 and HOXC11 increase transcription of S100beta gene in BrdU-induced in vitro differentiation of GOTO neuroblastoma cells into Schwannian cells. J. Cell. Mol. Med. 2007, 11:299-306.
38. Jones F.S., Holst B.D., Minowa O., De Robertis E.M., Edelman G.M. Binding and transcriptional activation of the promoter for the neural cell adhesion molecule by HoxC6 (Hox-3.3). Proc. Natl. Acad. Sci. U. S. A. 1993, 90:6557-6561.
39. Vandenberg L.N., Hauser R., Marcus M., Olea N., Welshons W.V. Human exposure to bisphenol A (BPA). Reprod. Toxicol. 2007, 24:139-177.
40. Gertz J., Reddy T.E., Varley K.E., Garabedian M.J., Myers R.M. Genistein and bisphenol A exposure cause estrogen receptor 1 to bind thousands of sites in a cell type-specific manner. Genome Res. 2012, 22:2153-2162.
41. Bhan A., Hussain I., Ansari K.I., Bobzean S.A., Perrotti L.I., Mandal S.S. Bisphenol-A and diethylstilbestrol exposure induces the expression of breast cancer associated long noncoding RNA HOTAIR in vitro and in vivo. J. Steroid Biochem. Mol. Biol. 2014, 141:160-170.
42. Bhan A., Hussain I., Ansari K.I., Bobzean S.A., Perrotti L.I., Mandal S.S. Histone methyltransferase EZH2 is transcriptionally induced by estradiol as well as estrogenic endocrine disruptors bisphenol-a and diethylstilbestrol. J. Mol. Biol. 2014, 426:3426-3441.
43. Schonfelder G., Wittfoht W., Hopp H., Talsness C.E., Paul M., Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ. Health Perspect. 2002, 110:A703-A707.
44. Bhan A., Hussain I., Ansari K.I., Kasiri S., Bashyal A., Mandal S.S. Antisense transcript long noncoding RNA (lncRNA) HOTAIR is transcriptionally induced by estradiol. J. Mol. Biol. 2013, 425:3707-3722.
45. Ansari K.I., Kasiri S., Hussain I., Bobzean S.A., Perrotti L.I., Mandal S.S. MLL histone methylases regulate expression of HDLR-SR-B1 in presence of estrogen and control plasma cholesterol in vivo. Mol. Endocrinol. 2013, 27:92-105.
46. Ansari K.I., Kasiri S., Mandal S.S. Histone methylase MLL1 has critical roles in tumor growth and angiogenesis and its knockdown suppresses tumor growth in vivo. Oncogene 2013, 32:3359-3370.
47. Ansari K.I., Kasiri S., Mishra B.P., Mandal S.S. Mixed lineage leukaemia-4 regulates cell-cycle progression and cell viability and its depletion suppresses growth of xenografted tumour in vivo. Br. J. Cancer 2012, 107:315-324.
48. Ansari K.I., Shrestha B., Hussain I., Kasiri S., Mandal S.S. Histone methylases MLL1 and MLL3 coordinate with estrogen receptors in estrogen-mediated HOXB9 expression. Biochemistry 2011, 50:3517-3527.
49. Ansari K.I., Kasiri S., Hussain I., Mandal S.S. Mixed lineage leukemia histone methylases play critical roles in estrogen-mediated regulation of HOXC13. FEBS J. 2009, 276:7400-7411.
50. Ansari K.I., Grant J.D., Kasiri S., Woldemariam G.W., Manda S.S. Mn(III)-salen induce tumor selective apoptosis in MCF7 cells. J. Inorg. Biochem. 2009, 103:818-826.
51. Ansari K.I., Mishra B.P., Mandal S.S. Human CpG binding protein interacts with MLL1, MLL2 and hSet1 and regulates Hox gene expression. Biochim. Biophys. Acta 2008, 1779:66-73.
52. Betancourt A.M., E.I., Desmont R.A., Russo J., Lamartiniere C.A. In-utero exposure to bisphenol A shifts the window of susceptibility for mammary carcinogenesis in the rat. Environ. Health Perspect. 2010, 118:1614-1619.
53. Maclusky H., Leranth The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect. 2005, 11:675-679.
54. Inagaki T., Frankfurt M., Luine V. Estrogen-induced memory enhancements are blocked by acute bisphenol A in adult female rats: role of dendritic spines. Endocrinology 2012, 153:3357-3367.
55. Eilam-Stock T., Serrano P., Frankfurt M., Luine V. Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats. Behav. Neurosci. 2012, 126:175-185.
56. Bobzean S.A., Dennis T.S., Perrotti L.I. Acute estradiol treatment affects the expression of cocaine-induced condition placed preference in ovariectomized female rats. Bran Res. Bull. 2014, 103:49-53.
57. Casals-Casas C., Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption. Annu. Rev. Physiol. 2011, 73:135-162.
58. MacLusky N.J., Hajszan T., Leranth C. The environmental estrogen bisphenol a inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect. 2005, 113:675-679.
59. Nilsson S., Gustafsson J.A. Estrogen receptor transcription and transactivation: Basic aspects of estrogen action. Breast Cancer Res. 2000, 2:360-366.
60. Nilsson S., Gustafsson J.A. Estrogen receptor action. Crit. Rev. Eukaryot. Gene Expr. 2002, 12:237-257.
61. Mo R., Rao S.M., Zhu Y.J. Identification of the MLL2 complex as a coactivator for estrogen receptor alpha. J. Biol. Chem. 2006, 281:15714-15720.
62. Dreijerink K.M.A., Mulder K.W., Winkler G.S., Hoppener J.W.M., Lips C.J.M., Timmers H.T.M. Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res. 2006, 66:4929-4935.
63. Lee S., Lee D.K., Dou Y.L., Lee J., Lee B., Kwak E., Kong Y.Y., Lee S.K., Roeder R.G., Lee J.W. Coactivator as a target gene specificity determinant for histone H3 lysine 4 methyltransferases. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15392-15397.
64. Barkhem T., Nilsson S., Gustafsson J.A. Molecular mechanisms, physiological consequences and pharmacological implications of estrogen receptor action. Am. J. Pharmacogenomics 2004, 4:19-28.
65. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 2001, 81:1535-1565.
66. Guenther M.G., Jenner R.G., Chevalier B., Nakamura T., Croce C.M., Canaani E., Young R.A. Global and Hox-specific roles for the MLL1 methyltransferase. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:8603-8608.
67. Hess J.L. MLL: a histone methyltransferase disrupted in leukemia. Trends Mol. Med. 2004, 10:500-507.
68. Ernst P., Mabon M., Davidson A.J., Zon L.I., Korsmeyer S.J. An Mll-dependent Hox program drives hematopoietic progenitor expansion. Curr. Biol. 2004, 14:2063-2069.
69. Lee S., Kim D.H., Goo Y.H., Lee Y.C., Lee S.K., Lee J.W. Crucial roles for interactions between MLL3/4 and INI1 in nuclear receptor transactivation. Mol. Endocrinol. 2009, 23:610-619.
70. Mandal S.S., Ansari K.I., Hussain I., Kasiri S., Shrestha B. MLL histone methylases in estrogen-mediated regulation of HOX genes involved in hair follicle development and leukemia. FASEB J. 2010, 24.
71. Ansari K.I., Mishra B.P., Mandal S.S. MLL histone methylases in gene expression, hormone signaling and cell cycle. Front. Biosci. 2009, 14:3483-3495.
72. Mandal S.S. Mixed lineage leukemia: versatile player in epigenetics and human disease. FEBS J. 2010, 277:1789-1789.
73. Ansari K.I., Mandal S.S. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS J. 2010, 277:1790-1804.
74. Ansari K.I., Hussain I., Das H.K., Mandal S.S. Overexpression of human histone methylase MLL1 upon exposure to a food contaminant mycotoxin, deoxynivalenol. FEBS J. 2009, 276:3299-3307.
75. Mishra B.P., Ansari K.I., Mandal S.S. Dynamic association of MLL1, H3K4 trimethylation with chromatin and Hox gene expression during the cell cycle. FEBS J. 2009, 276:1629-1640.
76. Jiang S., Meyer R., Kang K., Osborne C.K., Wong J., Oesterreich S. Scaffold attachment factor SAFB1 suppresses estrogen receptor alpha-mediated transcription in part via interaction with nuclear receptor corepressor. Mol. Endocrinol. 2006, 20:311-320.
77. Oesterreich S., Zhang Q., Hopp T., Fuqua S.A., Michaelis M., Zhao H.H., Davie J.R., Osborne C.K., Lee A.V. Tamoxifen-bound estrogen receptor (ER) strongly interacts with the nuclear matrix protein HET/SAF-B, a novel inhibitor of ER-mediated transactivation. Mol. Endocrinol. 2000, 14:369-381.
78. Shibata H., Spencer T.E., Onate S.A., Jenster G., Tsai S.Y., Tsai M.J., O'Malley B.W. Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action. Recent Prog. Horm. Res. 1997, 52:141-164. (discussion 164-145).
79. Velghe A.I., Van Cauwenberghe S., Polyansky A.A., Chand D., Montano-Almendras C.P., Charni S., Hallberg B., Essaghir A., Demoulin J.B. PDGFRA alterations in cancer: characterization of a gain-of-function V536E transmembrane mutant as well as loss-of-function and passenger mutations. Oncogene 2014, 33:2568-2576.
80. Fujiki K., Duerr E.M., Kikuchi H., Ng A., Xavier R.J., Mizukami Y., Imamura T., Kulke M.H., Chung D. HOXC6 is overexpressed in gastrointestinal carcinoids and interacts with JunD to regulate tumor growth. Gastroenterology 2008, 134:907-916.
81. Miller G.J., Miller H.L., van Bokhoven A., Lambert J.R., Werahera P.N., Schirripa O., Lucia M.S., Nordeen S.K. Aberrant HOXC expression accompanies the malignant phenotype in human prostate. Cancer Res. 2003, 63:5879-5888.
82. Frasor J., Danes J.M., Komm B., Chang K.C., Lyttle C.R., Katzenellenbogen B.S. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 2003, 144:4562-4574.
83. Stender J.D., Frasor J., Komm B., Chang K.C., Kraus W.L., Katzenellenbogen B.S. Estrogen-regulated gene networks in human breast cancer cells: involvement of E2F1 in the regulation of cell proliferation. Mol. Endocrinol. 2007, 21:2112-2123.
84. Welboren W.J., van Driel M.A., Janssen-Megens E.M., van Heeringen S.J., Sweep F.C.G.J., Span P.N., Stunnenberg H.G. ChIP-Seq of ER alpha and RNA polymerase II defines genes differentially responding to ligands. EMBO J. 2009, 28:1418-1428.
85. Krishnan A.V., Stathis P., Permuth S.F., Tokes L., Feldman D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 1993, 132:2279-2286.
86. Smith C.C., Taylor H.S. Xenoestrogen exposure imprints expression of genes (Hoxa10) required for normal uterine development. FASEB J. 2007, 21:239-246.
87. Vandenberg L.N., Maffini M.V., Wadia P.R., Sonnenschein C., Rubin B.S., Soto A.M. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 2007, 148:116-127.
88. Munoz-de-Toro M., Markey C.M., Wadia P.R., Luque E.H., Rubin B.S., Sonnenschein C., Soto A.M. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146:4138-4147.
89. Washington W., Hubert L., Jones D., Gray W.G. Bisphenol a binds to the low-affinity estrogen binding site. In Vitr. Mol. Toxicol. 2001, 14:43-51.
90. Blair R.M., Fang H., Branham W.S., Hass B.S., Dial S.L., Moland C.L., Tong W., Shi L., Perkins R., Sheehan D.M. The estrogen receptor relative binding affinities of 188 natural and xenochemicals: structural diversity of ligands. Toxicol. Sci. 2000, 54:138-153.
91. Akbas G.E., Song J., Taylor H.S. A HOXA10 estrogen response element (ERE) is differentially regulated by 17 beta-estradiol and diethylstilbestrol (DES). J. Mol. Biol. 2004, 340:1013-1023.
92. Anderson I., Gorski J. Estrogen receptor alpha interaction with estrogen response element half-sites from the rat prolactin gene. Biochemistry 2000, 39:3842-3847.
93. Klinge C.M. Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res. 2001, 29:2905-2919.
94. Klinge C.M., Studinski-Jones A.L., Kulakosky P.C., Bambara R.A., Hilf R. Comparison of tamoxifen ligands on estrogen receptor interaction with estrogen response elements. Mol. Cell. Endocrinol. 1998, 143:79-90.
95. Lopez D., Sanchez M.D., Shea-Eaton W., McLean M.P. Estrogen activates the high-density lipoprotein receptor gene via binding to estrogen response elements and interaction with sterol regulatory element binding protein-1A. Endocrinology 2002, 143:2155-2168.
96. Shu F.J., Sidell N., Yang D.Z., Kallen C.B. The tri-nucleotide spacer sequence between estrogen response element half-sites is conserved and modulates ER alpha-mediated transcriptional responses. J. Steroid Biochem. 2010, 120:172-179.
97. Sidell N., Mathad R.I., Shu F.J., Zhang Z.J., Kallen C.B., Yang D.Z. Intercalation of XR5944 with the estrogen response element is modulated by the tri-nucleotide spacer sequence between half-sites. J. Steroid Biochem. 2011, 124:121-127.
98. Ansari A.Z., Peterson-Kaufman K.J. A partner evokes latent differences between Hox proteins. Cell 2011, 147:1220-1221.
99. Fullwood M.J., Liu M.H., Pan Y.F., Liu J., Xu H., Mohamed Y.B., Orlov Y.L., Velkov S., Ho A., Mei P.H., Chew E.G., Huang P.Y., Welboren W.J., Han Y., Ooi H.S., Ariyaratne P.N., Vega V.B., Luo Y., Tan P.Y., Choy P.Y., Wansa K.D., Zhao B., Lim K.S., Leow S.C., Yow J.S., Joseph R., Li H., Desai K.V., Thomsen J.S., Lee Y.K., Karuturi R.K., Herve T., Bourque G., Stunnenberg H.G., Ruan X., Cacheux-Rataboul V., Sung W.K., Liu E.T., Wei C.L., Cheung E., Ruan Y. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 2009, 462:58-64.
100. Fullwood M.J., Ruan Y. ChIP-based methods for the identification of long-range chromatin interactions. J. Cell. Biochem. 2009, 107:30-39.
101. Fullwood M.J., Wei C.L., Liu E.T., Ruan Y. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res. 2009, 19:521-532.
102. Holwerda S., de Laat W. Chromatin loops, gene positioning, and gene expression. Front. Genet. 2012, 3:217.
103. Theodorou V., Carroll J.S. Estrogen receptor action in three dimensions - looping the loop. Breast Cancer Res. 2010, 12:303.
104. Liu M.H., Cheung E. Estrogen receptor-mediated long-range chromatin interactions and transcription in breast cancer. Mol. Cell. Endocrinol. 2014, 382:624-632.