Cell cycle regulation of human endometrial stromal cells during decidualization

Reproductive Sciences

Volumn 19, Issue 8, 2012, Pages 883-894

  Logan, Philip C ^a   Steiner, Michael ^a   Ponnampalam, Anna P ^a   Mitchell, Murray D ^a,b,c  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

14 3 3 sigma; decidualization; DNA methylation; endometrial stromal cell; p53

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CYCLIC AMP; CYCLIN B1; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; ESTRADIOL; GESTAGEN; MEDROXYPROGESTERONE ACETATE; PROTEIN P53; STRATIFIN;

APOPTOSIS; ARTICLE; CELL COUNT; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DECIDUALIZATION; DNA METHYLATION; ENDOMETRIAL STROMAL CELL; ENDOMETRIUM CELL; FEMALE; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; HORMONE ACTION; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; S PHASE CELL CYCLE CHECKPOINT; STROMA CELL; WESTERN BLOTTING;

AZACITIDINE; CELL CYCLE; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL LINE; CYCLIC AMP; DECIDUA; DNA METHYLATION; ENDOMETRIUM; ESTRADIOL; FEMALE; G0 PHASE; G1 PHASE; GENE EXPRESSION; HUMANS; MEDROXYPROGESTERONE ACETATE; POLYMERASE CHAIN REACTION; PROGESTINS; STROMAL CELLS; UP-REGULATION;

EID: 84864357443     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719112438447     Document Type: Article

References (68)

1. Strowitzki T, Germeyer A, Popovici R, von Wolff M. The human endometrium as a fertility-determining factor. Hum Reprod Update. 2006 ; 12 (5). 617-630 (Pubitemid 44307836)
2. Rider V, Potapova T, Dai G, Soares MJ. Stimulation of a rat uterine stromal cell line in culture reveals a molecular switch for endocrine-dependent differentiation. J Endocrinol. 2005 ; 184 (1). 119-127 (Pubitemid 40207567)
3. Loercher AE, Tank EMH, Delston RB, Harbour JW. MITF links differentiation with cell cycle arrest in melanocytes by transcriptional activation of INK4A. J Cell Biol. 2005 ; 168 (1). 35-40 (Pubitemid 40111055)
4. Derynck R, Wagner EF. Cell differentiation. Curr Opin Cell Biol. 1995 ; 7 (6). 843-844
5. Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol. 2003 ; 178 (3). 357-372 (Pubitemid 37220163)
6. Tierney EP, Tulac S, Huang STJ, Giudice LC. Activation of the protein kinase A pathway in human endometrial stromal cells reveals sequential categorical gene regulation. Physiol. Genomics. 2003 ; 16 (1). 47-66
7. Telgmann R, Maronde E, Tasken K, Gellersen B. Activated protein kinase A is required for differentiation-dependent transcription of the decidual prolactin gene in human endometrial stromal cells. Endocrinology. 1997 ; 138 (3). 929-937 (Pubitemid 27089743)
8. Zarrilli R, Pignata S, Apicella A, et al. Cell cycle block at G1-S or G2-M phase correlates with differentiation of Caco-2 cells: effect of constitutive insulin-like growth factor II expression. Gastroenterology. 1999 ; 116 (6). 1358-1366 (Pubitemid 29258884)
9. Devlin AM, Solban N, Tremblay S, et al. HCaRG is a novel regulator of renal epithelial cell growth and differentiation causing G2 M arrest. Am J Physiol Renal Physiol. 2003 ; 284 (4). F753 - F762
10. Hattori N, Davies TC, Anson-Cartwright L, Cross JC. Periodic expression of the cyclin-dependent kinase inhibitor p57Kip2 in trophoblast giant cells defines a G2-like gap phase of the endocycle. Mol Biol Cell. 2000 ; 11 (3). 1037-1045 (Pubitemid 30159320)
11. Yoshino T, Sakaguchi M, Masuda T, Kawakita M, Takatsuki K. Two regulation points for differentiation in the cell cycle of human megakaryocytes. Br J Haematol. 1996 ; 92 (4). 780-787 (Pubitemid 26111155)
12. Qian K, Chen H, Wei Y, Hu J, Zhu G. Differentiation of endometrial stromal cells in vitro: down-regulation of suppression of the cell cycle inhibitor p57 by HOXA10?. Mol Hum Reprod. 2005 ; 11 (4). 245-251 (Pubitemid 40662809)
13. Schmidt M, Fernandez de Mattos S, van der Horst A, et al. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol. 2002 ; 22 (22). 7842-7852 (Pubitemid 35217295)
14. Takano M, Lu Z, Goto T, et al. Transcriptional cross talk between the forkhead transcription factor forkhead box O1A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells. Mol Endocrinol. 2007 ; 21: 2334-2349 (Pubitemid 47529349)
15. Cobrinik D. Pocket proteins and cell cycle control. Oncogene. 2005 ; 24 (17). 2796-2809 (Pubitemid 40638091)
16. Cloke B, Huhtinen K, Fusi L, et al. The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium. Endocrinology. 2008 ; 149 (9). 4462-4474
17. Aghajanova L, Tatsumi K, Horcajadas JA, et al. Unique transcriptome, pathways, and networks in the human endometrial fibroblast response to progesterone in endometriosis. Biol Reprod. 2011 ; 84 (4). 801-815
18. Tulac S, Overgaard MT, Hamilton AE, Jumbe NL, Suchanek E, Giudice LC. Dickkopf-1, an inhibitor of Wnt signaling, is regulated by progesterone in human endometrial stromal cells. J Clin Endocrinol Metab. 2006 ; 91 (4). 1453-1461
19. Levine AJ, Hu W, Feng Z. The p53 pathway: what questions remain to be explored?. Cell Death Differ. 2006 ; 13 (6). 1027-1036
20. Taylor WR, GR Stark. Regulation of the G2/M transition by p53. Oncogene. 2001 ; 20 (15). 1803-1815 (Pubitemid 32458690)
21. Tang L, Zhang Y, Pan H, et al. Involvement of cyclin B1 in progesterone-mediated cell growth inhibition, G2/M cell cycle arrest, and apoptosis in human endometrial cell. Reprod Biol Endocrinol.. 2009 ; 7 (1). 144
22. Sakai N, Maruyama T, Sakurai R, et al. Involvement of histone acetylation in ovarian steroid-induced decidualization of human endometrial stromal cells. J Biol Chem. 2003 ; 278 (19). 16675-16682 (Pubitemid 36799531)
23. Logan PC, Ponnampalam AP, Rahnama F, Lobie PE, Mitchell MD. The effect of DNA methylation inhibitor 5-Aza-2'-deoxycytidine on human endometrial stromal cells. Hum Reprod. 2010 ; 25 (11). 2859-2869
24. Yamagata Y, Asada H, Tamura I, et al. DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen. Hum Reprod. 2009 ; 24 (5). 1126-1132
25. Munro S, Farquhar C, Mitchell M, Ponnampalam A. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod. 2010 ; 16 (5). 297-310
26. Vincent ZL, Farquhar CM, Mitchell MD, Ponnampalam AP. Expression and regulation of DNA methyltransferases in human endometrium. Fertil Steril. 2011 ; 95 (4). 1522 e1521-1525
27. Lamarche N, Tapon N, Stowers L, et al. Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell. 1996 ; 87 (3). 519-529 (Pubitemid 26374325)
28. Coleman ML, Marshall CJ, Olson MF. RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat Rev Mol Cell Biol. 2004 ; 5 (5). 355-366 (Pubitemid 38579473)
29. Mammoto A, Ingber DE. Cytoskeletal control of growth and cell fate switching. Curr Opin Cell Biol. 2009 ; 21 (6). 864-870
30. Olson MF, Ashworth A, Hall A.. An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science. 1995 ; 269 (5228). 1270-1272
31. Welsh CF. Rho GTPases as key transducers of proliferative signals in G1 cell cycle regulation. Breast Cancer Res Treat. 2004 ; 84 (1). 33-42 (Pubitemid 38388858)
32. Krikun G, Mor G, Alvero A, et al. A novel immortalized human endometrial stromal cell line with normal progestational response. Endocrinology. 2004 ; 145 (5). 2291-2296 (Pubitemid 38535058)
33. Kasahara K, Takakura K, Takebayashi K, Kimura F, Nakanishi K, Noda Y. The role of human chorionic gonadotropin on decidualization of endometrial stromal cells in vitro. J Clin Endocrinol Metab. 2001 ; 86 (3). 1281-1286 (Pubitemid 32323017)
34. Tang B, Guller S, Gurpide E. Cyclic adenosine 3',5'-monophosphate induces prolactin expression in stromal cells isolated from human proliferative endometrium. Endocrinology. 1993 ; 133 (5). 2197-2203 (Pubitemid 23324727)
35. Jiemjit A, Fandy TE, Carraway H, et al. p21WAF1//CIP1 induction by 5-azacytosine nucleosides requires DNA damage. Oncogene. 2008 ; 27 (25). 3615-3623 (Pubitemid 351793797)
36. Ferguson AT, Evron E, Umbricht CB, et al. High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc Natl Acad Sci USA. 2000 ; 97 (11). 6049-6054 (Pubitemid 30367521)
37. Milutinovic S, Knox JD, Szyf M. DNA methyltransferase inhibition induces the transcription of the tumor suppressor p21WAF1/CIP1/sdi1. J Biol Chem. 2000 ; 275 (9). 6353-6359 (Pubitemid 30129929)
38. Horiuchi S, Kato K, Suga S, et al. Expression of progesterone receptor B is associated with G0/G1 arrest of the cell cycle and growth inhibition in NIH3T3 cells. Exp Cell Res. 2005 ; 305 (2). 233-243 (Pubitemid 40467577)
39. Chan TA, Hermeking H, Lengauer C, Kinzler KW, Vogelstein B. 14-3-3 sigma is required to prevent mitotic catastrophe after DNA damage. Nature. 1999 ; 401 (6753). 616-620
40. Schultz J, Ibrahim SM, Vera J, Kunz M. 14-3-3 Gene silencing during melanoma progression and its role in cell cycle control and cellular senescence. Mol Cancer. 2009 ; 8: 53
41. Grewal S, Carver JG, Ridley AJ, Mardon H. Implantation of the human embryo requires Rac1-dependent endometrial stromal cell migration. Proc Natl Acad Sci USA. 2008 ; 105 (42). 16189-16194
42. Pohnke Y, Schneider-Merck T, Fahnenstich J, et al. Wild-type p53 protein is up-regulated upon cyclic adenosine monophosphate-induced differentiation of human endometrial stromal cells. J Clin Endocrinol Metab. 2004 ; 89 (10). 5233-5244 (Pubitemid 39391473)
43. Kaneuchi M, Sasaki M, Tanaka Y, et al. Expression and methylation status of 14-3-3 sigma gene can characterize the different histological features of ovarian cancer. Biochem Biophys Res Commun. 2004 ; 316 (4). 1156-1162 (Pubitemid 38369074)
44. Scott SA, Dong WF, Ichinohasama R, et al. 5-Aza-2'-deoxycytidine (decitabine) can relieve p21WAF1 repression in human acute myeloid leukemia by a mechanism involving release of histone deacetylase 1 (HDAC1) without requiring p21WAF1 promoter demethylation. Leuk Res. 2006 ; 30 (1). 69-76 (Pubitemid 41654707)
45. Murakami J, Asaumi JI, Maki Y, et al. Effects of demethylating agent 5-aza-2'-deoxycytidine and histone deacetylase inhibitor FR901228 on maspin gene expression in oral cancer cell lines. Oral Oncology. 2004 ; 40 (6). 597-603 (Pubitemid 38452679)
46. Quelle DE, Ashmun RA, Shurtleff SA, et al. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Gene Dev. 1993 ; 7 (8). 1559-1571 (Pubitemid 23234349)
47. Nheu T, He H, Hirokawa Y, Walker F, Wood J, Maruta H. PAK is essential for RAS-induced upregulation of cyclin D1 during the G1 to S transition. Cell Cycle. 2004 ; 3 (1). 71-74 (Pubitemid 40268591)
48. Patra S, Bettuzzi S. Epigenetic DNA-(cytosine-5-carbon) modifications: 5-aza-2-deoxycytidine and DNA-demethylation. Biochemistry Mos. 2009 ; 74 (6). 613-619
49. Yang AS, Estecio MRH, Doshi K, Kondo Y, Tajara EH, Issa JPJ. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004 ; 32 (3). e38
50. Edgar BA, Orr-Weaver TL. Endoreplication cell cycles: more for less. Cell. 2001 ; 105 (3). 297-306 (Pubitemid 32455339)
51. Ma X, Gao F, Rusie A, et al. Decidual cell polyploidization necessitates mitochondrial activity. PLoS ONE. 2011 ; 6 (10). e26774
52. Tan J, Raja S, Davis MK, Tawfik O, Dey SK, Das SK. Evidence for coordinated interaction of cyclin D3 with p21 and cdk6 in directing the development of uterine stromal cell decidualization and polyploidy during implantation. Mech Dev. 2002 ; 111 (1-2). 99-113 (Pubitemid 34136982)
53. Moulton BC, Koenig BB. Uterine deoxyribonucleic acid synthesis during preimplantation in precursors of stromal cell differentiation during decidualization. Endocrinology. 1984 ; 115 (4). 1302-1307 (Pubitemid 14000289)
54. Heijden FVD, James J. Polyploidy in the human myometrium. Z Mikrosk Anat Forsch. 1975 ; 89 (1). 18-26
55. Lakin ND, Jackson SP. Regulation of p53 in response to DNA damage. Oncogene. 1999 ; 18 (53). 7644-7655 (Pubitemid 30052691)
56. Schneider-Merck T, Pohnke Y, Kempf R, Christian M, Brosens JJ, Gellersen B. Physical interaction and mutual transrepression between CCAAT/Enhancer- binding protein {beta} and the p53 tumor suppressor. J Biol Chem. 2006 ; 281 (1). 269-278 (Pubitemid 43671186)
57. Yang HY, Wen YY, Chen CH, Lozano G, Lee MH. 14-3-3 sigma positively regulates p53 and suppresses tumor growth. Mol Cell Biol. 2003 ; 23 (20). 7096-7107 (Pubitemid 37210993)
58. Hermeking H, Lengauer C, Polyak K, et al. 14-3-3[sigma] is a p53-regulated inhibitor of G2/M progression. Mol Cell. 1997 ; 1 (1). 3-11 (Pubitemid 127376388)
59. Jones MC, Fusi L, Higham JH, et al. Regulation of the SUMO pathway sensitizes differentiating human endometrial stromal cells to progesterone. Proc Natl Acad Sci U S A. 2006 ; 103 (44). 16272-16277 (Pubitemid 44715186)
60. Brosens JJ, Gellersen B. Death or survival-progesterone-dependent cell fate decisions in the human endometrial stroma. J Mol Endocrinol. 2006 ; 36 (3). 389-398 (Pubitemid 43904935)
61. Hirota Y, Daikoku T, Tranguch S, Xie H, Bradshaw HB, Dey SK. Uterine-specific p53 deficiency confers premature uterine senescence and promotes preterm birth in mice. J Clin Invest. 2010 ; 120 (3). 803-815
62. Soddu S, Blandino G, Scardigli R, et al. Interference with p53 protein inhibits hematopoietic and muscle differentiation. J Cell Biol. 1996 ; 134 (1). 193-204 (Pubitemid 26231530)
63. Dellambra E, Golisano O, Bondanza S, et al. Downregulation of 14-3-3 sigma prevents clonal evolution and leads to immortalization of primary human keratinocytes. J Cell Biol. 2000 ; 149 (5). 1117-1130
64. Xin Y, Lu Q, Li Q. 14-3-3[sigma] controls corneal epithelial cell proliferation and differentiation through the Notch signaling pathway. Biochem Biophys Res Commun. 2010 ; 392 (4). 593-598
65. McKinsey TA, Zhang CL, Olson EN. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc Natl Acad Sci USA. 2000 ; 97 (26). 14400-14405
66. Parker SB, Eichele G, Zhang P, et al. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science. 1995 ; 267 (5200). 1024-1027
67. Neupane D. Korc M. 14-3-3 modulates pancreatic cancer cell survival and invasiveness. Clin Cancer Res. 2008 ; 14 (23). 7614-7623
68. Samuel T, Weber HO, Rauch P, et al. The G2/M regulator 14-3-3sigma prevents apoptosis through sequestration of Bax. J Biol Chem. 2001 ; 276 (48). 45201-45206