The PRB-dependent FOXO1/IGFBP-1 axis is essential for progestin to inhibit endometrial epithelial growth

Cancer Letters

Volumn 336, Issue 1, 2013, Pages 68-75

  Nakamura, Mitsuhiro ^a   Takakura, Masahiro ^a   Fujii, Reina ^a   Maida, Yoshiko ^a   Bono, Yukiko ^a   Mizumoto, Yasunari ^a   Zhang, Xian ^a   Kiyono, Tohru ^b   Kyo, Satoru ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

Endometrial epithelial cell; FOXO1; Growth inhibition; IGFBP 1; Progestin

Indexed keywords

COMPLEMENTARY DNA; GESTAGEN; LUCIFERASE; MEDROXYPROGESTERONE ACETATE; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; SMALL INTERFERING RNA; SOMATOMEDIN BINDING PROTEIN 1; TRANSCRIPTION FACTOR FKHR;

ARTICLE; BINDING SITE; CELL GROWTH; CELL IMMORTALIZATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MICROARRAY; DRUG EFFECT; DRUG MECHANISM; ENDOMETRIUM CELL; FOXO1 GENE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN LIKE GROWTH FACTOR BINDING PROTEIN 1 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

BINDING SITES; CELL LINE; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; MEDROXYPROGESTERONE ACETATE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGESTINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, PROGESTERONE; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84878986599     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.04.010     Document Type: Article

References (36)

1. Boehm K.D., Daimon M., Gorodeski I.G., Sheean L.A., Utian W.H., Ilan J. Expression of the insulin-like and platelet-derived growth factor genes in human uterine tissues. Mol. Reprod. Dev. 1990, 27:93-101.
2. Bulun S.E., Cheng Y.H., Yin P., Imir G., Utsunomiya H., Attar E., Innes J., Julie Kim J. Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol. Cell Endocrinol. 2006, 248:94-103.
3. Falcone T., Lebovic D.I. Clinical management of endometriosis. Obstet. Gynecol. 2011, 118:691-705.
4. Frost R.A., Mazella J., Tseng L. Insulin-like growth factor binding protein-1 inhibits the mitogenic effect of insulin-like growth factors and progestins in human endometrial stromal cells. Biol. Reprod. 1993, 49:104-111.
5. Giudice L.C., Dsupin B.A., Irwin J.C. Steroid and peptide regulation of insulin-like growth factor-binding proteins secreted by human endometrial stromal cells is dependent on stromal differentiation. J. Clin. Endocrinol. Metab. 1992, 75:1235-1241.
6. Giudice L.C., Dsupin B.A., Jin I.H., Vu T.H., Hoffman A.R. Differential expression of messenger ribonucleic acids encoding insulin-like growth factors and their receptors in human uterine endometrium and decidua. J. Clin. Endocrinol. Metab. 1993, 76:1115-1122.
7. Goto T., Takano M., Albergaria A., Briese J., Pomeranz K.M., Cloke B., Fusi L., Feroze-Zaidi F., Maywald N., Sajin M., Dina R.E., Ishihara O., Takeda S., Lam E.W., Bamberger A.M., Ghaem-Maghami S., Brosens J.J. Mechanism and functional consequences of loss of FOXO1 expression in endometrioid endometrial cancer cells. Oncogene 2008, 27:9-19.
8. Horwitz K.B., Alexander P.S. In situ photolinked nuclear progesterone receptors of human breast cancer cells: subunit molecular weights after transformation and translocation. Endocrinology 1983, 113:2195-2201.
9. Jacobsen B.M., Richer J.K., Schittone S.A., Horwitz K.B. New human breast cancer cells to study progesterone receptor isoform ratio effects and ligand-independent gene regulation. J. Biol. Chem. 2002, 277:27793-27800.
10. Kim J.J., Buzzio O.L., Li S., Lu Z. Role of FOXO1A in the regulation of insulin-like growth factor-binding protein-1 in human endometrial cells: interaction with progesterone receptor. Biol. Reprod. 2005, 73:833-839.
11. Kim J.J., Chapman-Davis E. Role of progesterone in endometrial cancer. Semin. Reprod. Med. 2010, 28:81-90.
12. Kleinman D., Karas M., Roberts C.T., LeRoith D., Phillip M., Segev Y., Levy J., Sharoni Y. Modulation of insulin-like growth factor I (IGF-I) receptors and membrane-associated IGF-binding proteins in endometrial cancer cells by estradiol. Endocrinology 1995, 136:2531-2537.
13. Krett N.L., Wei L.L., Francis M.D., Nordeen S.K., Gordon D.F., Wood W.M., Horwitz K.B. Human progesterone A-receptors can be synthesized intracellularly and are biologically functional. Biochem. Biophys. Res. Commun. 1988, 157:278-285.
14. Kumar N.S., Richer J., Owen G., Litman E., Horwitz K.B., Leslie K.K. Selective down-regulation of progesterone receptor isoform B in poorly differentiated human endometrial cancer cells: implications for unopposed estrogen action. Cancer Res. 1998, 58:1860-1865.
15. Kyo S., Nakamura M., Kiyono T., Maida Y., Kanaya T., Tanaka M., Yatabe N., Inoue M. Successful immortalization of endometrial glandular cells with normal structural and functional characteristics. Am. J. Pathol. 2003, 163:2259-2269.
16. Kyo S., Sakaguchi J., Kiyono T., Shimizu Y., Maida Y., Mizumoto Y., Mori N., Nakamura M., Takakura M., Miyake K., Sakamoto M., Inoue M. Forkhead transcription factor FOXO1 is a direct target of progestin to inhibit endometrial epithelial cell growth. Clin. Cancer Res. 2011, 17:525-537.
17. Leslie K.K., Kumar N.S., Richer J., Owen G., Takimoto G., Horwitz K.B., Lange C. Differential expression of the A and B isoforms of progesterone receptor in human endometrial cancer cells. Only progesterone receptor B is induced by estrogen and associated with strong transcriptional activation. Ann. NY Acad. Sci. 1997, 828:17-26.
18. Liu H.C., He Z.Y., Mele C., Damario M., Davis O., Rosenwaks Z. Hormonal regulation of expression of messenger RNA encoding insulin-like growth factor binding proteins in human endometrial stromal cells cultured in vitro. Mol. Hum. Reprod. 1997, 3:21-26.
19. Lydon J.P., DeMayo F.J., Funk C.R., Mani S.K., Hughes A.R., Montgomery C.A., Shyamala G., Conneely O.M., O'Malley B.W. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995, 9:2266-2278.
20. Meyer M.E., Quirin-Stricker C., Lerouge T., Bocquel M.T., Gronemeyer H. A limiting factor mediates the differential activation of promoters by the human progesterone receptor isoforms. J. Biol. Chem. 1992, 267:10882-10887.
21. Momoeda M., Harada T., Terakawa N., Aso T., Fukunaga M., Hagino H., Taketani Y. Long-term use of dienogest for the treatment of endometriosis. J. Obstet. Gynaecol. Res. 2009, 35:1069-1076.
22. Mote P.A., Balleine R.L., McGowan E.M., Clarke C.L. Colocalization of progesterone receptors A and B by dual immunofluorescent histochemistry in human endometrium during the menstrual cycle. J. Clin. Endocrinol. Metab. 1999, 84:2963-2971.
23. Mulac-Jericevic B., Lydon J.P., DeMayo F.J., Conneely O.M. Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc. Natl. Acad. Sci. USA 2003, 100:9744-9749.
24. Mulac-Jericevic B., Mullinax R.A., DeMayo F.J., Lydon J.P., Conneely O.M. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 2000, 289:1751-1754.
25. Murphy L.J., Ghahary A. Uterine insulin-like growth factor-1: regulation of expression and its role in estrogen-induced uterine proliferation. Endocr. Rev. 1990, 11:443-453.
26. Pollak M.N., Schernhammer E.S., Hankinson S.E. Insulin-like growth factors and neoplasia. Nat. Rev. Cancer 2004, 4:505-518.
27. Rutanen E.M. Insulin-like growth factors in endometrial function. Gynecol. Endocrinol. 1998, 12:399-406.
28. Rutanen E.M., Nyman T., Lehtovirta P., Ammälä M., Pekonen F. Suppressed expression of insulin-like growth factor binding protein-1 mRNA in the endometrium: a molecular mechanism associating endometrial cancer with its risk factors. Int. J. Cancer 1994, 59:307-312.
29. Rutanen E.M., Pekonen F., Mäkinen T. Soluble 34K binding protein inhibits the binding of insulin-like growth factor I to its cell receptors in human secretory phase endometrium: evidence for autocrine/paracrine regulation of growth factor action. J. Clin. Endocrinol. Metab. 1988, 66:173-180.
30. Sartorius C.A., Melville M.Y., Hovland A.R., Tung L., Takimoto G.S., Horwitz K.B. A third transactivation function (AF3) of human progesterone receptors located in the unique N-terminal segment of the B-isoform. Mol. Endocrinol. 1994, 8:1347-1360.
31. Schreiber E., Matthias P., Müller M.M., Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucl. Acids Res. 1989, 17:6419.
32. Takano M., Lu Z., Goto T., Fusi L., Higham J., Francis J., Withey A., Hardt J., Cloke B., Stavropoulou A.V., Ishihara O., Lam E.W., Unterman T.G., Brosens J.J., Kim J.J. 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.
33. Vegeto E., Shahbaz M.M., Wen D.X., Goldman M.E., O'Malley B.W., McDonnell D.P. Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Mol. Endocrinol. 1993, 7:1244-1255.
34. Wang H.S., Chard T. IGFs and IGF-binding proteins in the regulation of human ovarian and endometrial function. J. Endocrinol. 1999, 161:1-13.
35. Ward E.C., Hoekstra A.V., Blok L.J., Hanifi-Moghaddam P., Lurain J.R., Singh D.K., Buttin B.M., Schink J.C., Kim J.J. The regulation and function of the forkhead transcription factor, Forkhead box O1, is dependent on the progesterone receptor in endometrial carcinoma. Endocrinology 2008, 149:1942-1950.
36. Zhou J., Dsupin B.A., Giudice L.C., Bondy C.A. Insulin-like growth factor system gene expression in human endometrium during the menstrual cycle. J. Clin. Endocrinol. Metab. 1994, 79:1723-1734.