KLF11 epigenetically regulates glycodelin-a, a marker of endometrial biology via histone-modifying chromatin mechanisms

Reproductive Sciences

Volumn 21, Issue 3, 2014, Pages 319-328

  Tabbaa, Zaid M ^a   Zheng, Ye ^a   Daftary, Gaurang S ^a  

^a MAYO CLINIC   (United States)

Author keywords

endometrium; glycodelin A; KLF11; repressor; SIN3 HDAC

Indexed keywords

GLYCODELIN A; HISTONE DEACETYLASE; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 11; MESSENGER RNA; PLACENTA PROTEIN 14; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVITY; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENDOMETRIUM; ENDOMETRIUM CELL; EPIGENETICS; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPRESSOR GENE; CHROMATIN; DNA VECTOR; ENDOMETRIAL CANCER CELL LINE; EPIGENETIC REPRESSION; FEMALE; PROTEIN SECRETION; WILD TYPE;

ENDOMETRIUM; GLYCODELIN-A; KLF11; REPRESSOR; SIN3/HDAC;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMATIN; ENDOMETRIUM; EPIGENESIS, GENETIC; FEMALE; GLYCOPROTEINS; HISTONES; HUMANS; REPRESSOR PROTEINS;

EID: 84896831002     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719113503407     Document Type: Article

References (57)

1. Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest. 1998; 101 (7). 1379-1384
2. Taylor HS, Igarashi P, Olive DL, Arici A. Sex steroids mediate HOXA11 expression in the human peri-implantation endometrium. J Clin Endocrinol Metab. 1999; 84 (3). 1129-1135
3. Lessey BA. Endometrial integrins and the establishment of uterine receptivity. Hum Reprod. 1998; 13 (suppl 3). 247-258
4. Ding YQ, Zhu LJ, Bagchi MK, Bagchi IC. Progesterone stimulates calcitonin gene expression in the uterus during implantation. Endocrinology. 1994; 135 (5). 2265-2274
5. Martel D, Monier MN, Roche D, Psychoyos A. Hormonal dependence of pinopode formation at the uterine luminal surface. Hum Reprod. 1991; 6 (4). 597-603
6. Kao LC, Germeyer A, Tulac S, et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology. 2003; 144 (7). 2870-2881
7. Daftary GS, Taylor HS. Reproductive tract gene transfer. Fertil Steril. 2003; 80 (3). 475-484
8. Anderson WF. Human gene therapy. Nature. 1998; 392 (6679 suppl). 25-30
9. Crystal RG. Transfer of genes to humans: early lessons and obstacles to success. Science. 1995; 270 (5235). 404-410
10. Bjornsson HT, Fallin MD, Feinberg AP. An integrated epigenetic and genetic approach to common human disease. Trends Genet. 2004; 20 (8). 350-358
11. Berger SL. The complex language of chromatin regulation during transcription. Nature. 2007; 447 (7143). 407-412
12. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000; 403 (6765). 41-45
13. Garcia-Ramirez M, Rocchini C, Ausio J. Modulation of chromatin folding by histone acetylation. J Biol Chem. 1995; 270 (30). 17923-17928
14. Wu C. Chromatin remodeling and the control of gene expression. J Biol Chem. 1997; 272 (45). 28171-28174
15. Hildmann C, Riester D, Schwienhorst A. Histone deacetylases-an important class of cellular regulators with a variety of functions. Appl Microbiol Biotechnol. 2007; 75 (3). 487-497
16. Lomberk G, Wallrath L, Urrutia R. The Heterochromatin Protein 1 family. Genome Biol. 2006; 7 (7). 228
17. Chen H, Lin RJ, Xie W, Wilpitz D, Evans RM. Regulation of hormone-induced histone hyperacetylation and gene activation via acetylation of an acetylase. Cell. 1999; 98 (5). 675-686
18. Grimaldi G, Christian M, Quenby S, Brosens JJ. Expression of epigenetic effectors in decidualizing human endometrial stromal cells. Mol Hum Reprod. 2012; 18 (9). 451-458
19. Tamura I, Asada H, Maekawa R, et al. Induction of IGFBP-1 expression by cAMP is associated with histone acetylation status of the promoter region in human endometrial stromal cells. Endocrinology. 2012; 153 (11). 5612-5621
20. Vic P, Garcia M, Humeau C, Rochefort H. Early effect of estrogen on chromatin ultrastructure in endometrial nuclei. Mol Cell Endocrinol. 1980; 19 (1). 79-92
21. Buttar NS, DeMars CJ, Lomberk G, et al. Distinct role of Kruppel-like factor 11 in the regulation of prostaglandin E2 biosynthesis. J Biol Chem. 2010; 285 (15). 11433-11444
22. Fernandez-Zapico ME, van Velkinburgh JC, Gutierrez-Aguilar R, et al. MODY7 gene, KLF11, is a novel p300-dependent regulator of Pdx-1 (MODY4) transcription in pancreatic islet beta cells. J Biol Chem. 2009; 284 (52). 36482-36490
23. Bieker JJ. Kruppel-like factors: three fingers in many pies. J Biol Chem. 2001; 276 (37). 34355-34358
24. Kaczynski J, Cook T, Urrutia R. Sp1-and Kruppel-like transcription factors. Genome Biol. 2003; 4 (2). 206
25. Daftary GS, Zheng Y, Tabbaa ZM, et al. A novel role of the Sp/KLF transcription factor KLF11 in arresting progression of endometriosis. PLoS One. 2013; 8 (3). e60165
26. Yin P, Lin Z, Reierstad S, et al. Transcription factor KLF11 integrates progesterone receptor signaling and proliferation in uterine leiomyoma cells. Cancer Res. 2010; 70 (4). 1722-1730
27. Bonnefond A, Lomberk G, Buttar N, et al. Disruption of a novel Kruppel-like transcription factor p300-regulated pathway for insulin biosynthesis revealed by studies of the c.-331 INS mutation found in neonatal diabetes mellitus. J Biol Chem. 2011; 286 (32). 28414-28424
28. Lomberk G, Mathison AJ, Grzenda A, et al J Biol Chem. 2012:
29. Mueller MD, Vigne JL, Vaisse C, Taylor RN. Glycodelin: a pane in the implantation window. Semin Reprod Med. 2000; 18 (3). 289-298
30. Seppala M, Taylor RN, Koistinen H, Koistinen R, Milgrom E. Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr Rev. 2002; 23 (4). 401-430
31. Clark GF, Oehninger S, Patankar MS, et al. A role for glycoconjugates in human development: the human feto-embryonic defence system hypothesis. Hum Reprod. 1996; 11 (3). 467-473
32. Lessey BA, Ilesanmi AO, Castelbaum AJ, et al. Characterization of the functional progesterone receptor in an endometrial adenocarcinoma cell line (Ishikawa): progesterone-induced expression of the alpha1 integrin [published erratum appears in J Steroid Biochem Mol Biol 1997 Jan;60(1-2):161]. J Steroid Biochem Mol Biol. 1996; 59 (1). 31-39
33. Nishida M, Kasahara K, Kaneko M, Iwasaki H, Hayashi K. [Establishment of a new human endometrial adenocarcinoma cell line, Ishikawa cells, containing estrogen and progesterone receptors]. Nippon Sanka Fujinka Gakkai Zasshi. 1985; 37 (7). 1103-1111
34. Zhang JS, Moncrieffe MC, Kaczynski J, Ellenrieder V, Prendergast FG, Urrutia R. A conserved alpha-helical motif mediates the interaction of Sp1-like transcriptional repressors with the corepressor mSin3A. Mol Cell Biol. 2001; 21 (15). 5041-5049
35. Daftary GS, Lomberk GA, Buttar NS, et al. Detailed structural-functional analysis of the Kruppel-like factor 16 (KLF16) transcription factor reveals novel mechanisms for silencing Sp/KLF sites involved in metabolism and endocrinology. J Biol Chem. 2012; 287 (10). 7010-7025
36. Truty MJ, Lomberk G, Fernandez-Zapico ME, Urrutia R. Silencing of the transforming growth factor-beta (TGFbeta) receptor II by Kruppel-like factor 14 underscores the importance of a negative feedback mechanism in TGFbeta signaling. J Biol Chem. 2009; 284 (10). 6291-6300
37. Cook T, Gebelein B, Belal M, Mesa K, Urrutia R. Three conserved transcriptional repressor domains are a defining feature of the TIEG subfamily of Sp1-like zinc finger proteins. J Biol Chem. 1999; 274 (41). 29500-29504
38. Gebelein B, Fernandez-Zapico M, Imoto M, Urrutia R. KRAB-independent suppression of neoplastic cell growth by the novel zinc finger transcription factor KS1. J Clin Invest. 1998; 102 (11). 1911-1919
39. Gebelein B, Urrutia R. Sequence-specific transcriptional repression by KS1, a multiple-zinc-finger-Kruppel-associated box protein. Mol Cell Biol. 2001; 21 (3). 928-939
40. Dynan WS, Tjian R. The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell. 1983; 35 (1). 79-87
41. Tjian R, Maniatis T. Transcriptional activation: a complex puzzle with few easy pieces. Cell. 1994; 77 (1). 5-8
42. Gao J, Mazella J, Seppala M, Tseng L. Ligand activated hPR modulates the glycodelin promoter activity through the Sp1 sites in human endometrial adenocarcinoma cells. Mol Cell Endocrinol. 2001; 176 (1-2). 97-102
43. Seo S, Lomberk G, Mathison A, et al. Krüppel-like factor 11 differentially couples to histone acetyltransferase and histone methyltransferase chromatin remodeling pathways to transcriptionally regulate dopamine D2 receptor in neuronal cells. J Biol Chem. 2012; 287 (16). 12723-12735
44. Song CZ, Gavriilidis G, Asano H, Stamatoyannopoulos G. Functional study of transcription factor KLF11 by targeted gene inactivation. Blood Cells Mol Dis. 2005; 34 (1). 53-59
45. Crossley M, Whitelaw E, Perkins A, Williams G, Fujiwara Y, Orkin SH. Isolation and characterization of the cDNA encoding BKLF/TEF-2, a major CACCC-box-binding protein in erythroid cells and selected other cells. Mol Cell Biol. 1996; 16 (4). 1695-1705
46. Joshi SG, Bank JF, Henriques ES, Makarachi A, Matties G. Serum levels of a progestagen-associated endometrial protein during the menstrual cycle and pregnancy. J Clin Endocrinol Metab. 1982; 55 (4). 642-648
47. Waites GT, Wood PL, Walker RA, Bell SC. Immunohistological localization of human endometrial secretory protein, 'pregnancy-associated endometrial alpha 2-globulin' (alpha 2-PEG), during the menstrual cycle. J Reprod Fertil. 1988; 82 (2). 665-672
48. Li TC, Ling E, Dalton C, Bolton AE, Cooke ID. Concentration of endometrial protein PP14 in uterine flushings throughout the menstrual cycle in normal, fertile women. Br J Obstet Gynaecol. 1993; 100 (5). 460-464
49. Bell SC, Hales MW, Patel SR, Kirwan PH, Drife JO, Milford-Ward A. Amniotic fluid concentrations of secreted pregnancy-associated endometrial alpha 1-and alpha 2-globulins (alpha 1-and alpha 2-PEG). Br J Obstet Gynaecol. 1986; 93 (9). 909-915
50. Julkunen M, Koistinen R, Sjöberg J, Rutanen EM, Wahlström T, Seppälä M. Secretory endometrium synthesizes placental protein 14. Endocrinology. 1986; 118 (5). 1782-1786
51. Oehninger S, Coddington CC, Hodgen GD, Seppala M. Factors affecting fertilization: endometrial placental protein 14 reduces the capacity of human spermatozoa to bind to the human zona pellucida. Fertil Steril. 1995; 63 (2). 377-383
52. Mackenna A, Li TC, Dalton C, Bolton A, Cooke I. Placental protein 14 levels in uterine flushing and plasma of women with unexplained infertility. Fertil Steril. 1993; 59 (3). 577-582
53. Taylor RN, Vigne JL, Zhang P, Hoang P, Lebovic DI, Mueller MD. Effects of progestins and relaxin on glycodelin gene expression in human endometrial cells. Am J Obstet Gynecol. 2000; 182 (4). 841-847
54. Taylor RN, Savouret JF, Vaisse C, et al. Promegestone (R5020) and mifepristone (RU486) both function as progestational agonists of human glycodelin gene expression in isolated human epithelial cells. J Clin Endocrinol Metab. 1998; 83 (11). 4006-4012
55. Velarde MC, Zeng Z, McQuown JR, Simmen FA, Simmen RC. Kruppel-like factor 9 is a negative regulator of ligand-dependent estrogen receptor alpha signaling in Ishikawa endometrial adenocarcinoma cells. Mol Endocrinol. 2007; 21 (12). 2988-3001
56. Lomberk G, Urrutia R. The family feud: turning off Sp1 by Sp1-like KLF proteins. Biochem J. 2005; 392 (pt 1). 1-11
57. Uchida H, Maruyama T, Nagashima T, Asada H, Yoshimura Y. Histone deacetylase inhibitors induce differentiation of human endometrial adenocarcinoma cells through up-regulation of glycodelin. Endocrinology. 2005; 146 (12). 5365-5373