FOXO Transcription Factors: From Cell Fate Decisions to Regulation of Human Female Reproduction

  • Jan J. Brosens
  • Miranda S. C. Wilson
  • Eric W. -F. Lam
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 665)

Abstract

All key reproductive events in the human ovary and uterus, including follicle activation, ovulation, implantation, decidualization, luteolysis and menstruation, are dependent upon profound tissue remodelling, characterised by cyclical waves of cell proliferation, differentiation, apoptosis, tissue breakdown and regeneration. FOXO transcription factors, an evolutionarily conserved subfamily of the forkhead transcription factors, have emerged as master regulators ofcell fate decision capable ofintegrating avariety ofstress, growth factor and cytokine signaling pathways with the transcription machinery. The ability of FOXOs to regulate seemingly opposing cellular responses, ranging from cell cycle arrest and oxidative stress responses to differentiation and apoptosis, renders these transcription factors indispensable for cyclic tissue remodelling in female reproduction. Conversely, perturbations in the expression or activity of FOXO transcription factors are increasingly linked to common reproductive disorders, such as pregnancy loss, endometriosis, endometrial cancer and primary ovarian insufficiency.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Weigel D, Jurgens G, Kuttner F et al. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 1989; 57(4):645–658.PubMedCrossRefGoogle Scholar
  2. 2.
    Jiirgens G, Wieschaus E, Niisslein-Volhard C et al. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster II. Zygotic loci on the third chromosome. Rouxs Arch Dev Biol 1984; 193(5):283–295.CrossRefGoogle Scholar
  3. 3.
    Myatt SS, Lam EW The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer 2007; 7(11):847–859.PubMedCrossRefGoogle Scholar
  4. 4.
    Wijchers PJ, Burbach JP, Smidt MP. In control of biology: of mice, men and Foxes. Biochem J 2006; 397(2):233–246.PubMedCrossRefGoogle Scholar
  5. 5.
    Gajiwala KS, Burley SK. Winged helix proteins. Curr Opin Struct Biol 2000; 10(1):110–116.PubMedCrossRefGoogle Scholar
  6. 6.
    Kaestner KH, Knochel W, Martinez DE. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 2000; 14(2):142–146.PubMedGoogle Scholar
  7. 7.
    Lee EJ, Kim JM, Lee MK et al. Splice variants of the forkhead box protein AFX exhibit dominant negative activity and inhibit AFXalpha-mediated tumor cell apoptosis. PLoS ONE 2008; 3(7):e2743.PubMedCrossRefGoogle Scholar
  8. 8.
    Jacobs FM, van der Heide LP, Wijchers PJ et al. Fox06, a novel member of the FoxO classof transcription factors with distinct shuttling dynamics. J Biol Chem 2003; 278(38):35959–35967.PubMedCrossRefGoogle Scholar
  9. 9.
    Maiese K, Chong ZZ, Shang YC et al. A “FOXO” in sight: Targeting Foxo proteins from conception to cancer. Med Res Rev 2009 May;29(3):395–418.PubMedCrossRefGoogle Scholar
  10. 10.
    Sunters A, Fernandez de Mattos S, Stahl M et al. Fox03a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 2003; 278(50):49795–49805.PubMedCrossRefGoogle Scholar
  11. 11.
    Goto T, Takano M, Albergaria A et al. Mechanism and functional consequences of loss of FOXO1 expression in endometrioid endometrial cancer cells. Oncogene 2008; 27(1):9–19.PubMedCrossRefGoogle Scholar
  12. 12.
    Christian M, Zhang X, Schneider-Merck T et al. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/ enhancer-binding protein beta in differentiating human endometrial stromal cells. J Biol Chem 2002; 277(23):20825–20832.PubMedCrossRefGoogle Scholar
  13. 13.
    Kajihara T, Jones M, Fusi L et al. Differential expression of FOX01 and FOX03a confers resistance to oxidative cell death upon endometrial decidualization. Mol Endocrinol 2006; 20(10):2444–2455.PubMedCrossRefGoogle Scholar
  14. 14.
    Chen D, Guarente L. SIR2: a potential target for calorie restriction mimetics. Trends Mol Med 2007; 13(2):64–71.PubMedCrossRefGoogle Scholar
  15. 15.
    Liu L, Rajareddy S, Reddy P et al. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Fox03a. Development 2007; 134(1):199–209.PubMedCrossRefGoogle Scholar
  16. 16.
    Reddy P, Shen L, Ren C et al. Activation ofAkt (PKB) and suppression ofFKHRLl in mouse and rat oocytes by stem cell factor during follicular activation and development. Dev Biol 2005; 281(2):160–170.PubMedCrossRefGoogle Scholar
  17. 17.
    Hosaka T, Biggs WH 3rd, Tieu D et al. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 2004; 101(9):2975–2980.PubMedCrossRefGoogle Scholar
  18. 18.
    Castrillon DH, Miao L, Kollipara R et al. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003; 301(5630):215–218.PubMedCrossRefGoogle Scholar
  19. 19.
    Richards JS, Sharma SC, Falender AE et al. Expression of FKHR, FKHRL1 and AFX genes in the rodent ovary: evidence for regulation by IGF-I, estrogen and the gonadotropins. Mol Endocrinol 2002; 16(3):580–599.PubMedCrossRefGoogle Scholar
  20. 20.
    Pisarska MD, Kuo FT, Tang D et al. Expression of forkhead transcription factors in human granulosa cells. 2009 Apr;91(4 Suppl):1392–4.Google Scholar
  21. 21.
    Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007; 120(Pt 15):2479–2487.PubMedCrossRefGoogle Scholar
  22. 22.
    Pohl BS, Schon C, Rossner A et al. The FoxO-subclassin Xenopus laevisdevelopment. Gene Expr Patterns 2004; 5(2):187–192.PubMedCrossRefGoogle Scholar
  23. 23.
    Kramer JM, Davidge JT, Lockyer JM et al. Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 2003; 3:5.PubMedCrossRefGoogle Scholar
  24. 24.
    Calnan DR, Brunet A. The FoxO code. Oncogene 2008; 27(16):2276–2288.PubMedCrossRefGoogle Scholar
  25. 25.
    Vogt PK, Jiang H, Aoki M. Triple layer control: phosphorylation, acetylation and ubiquitination of FOXO proteins. Cell Cycle 2005; 4(7):908–913.PubMedGoogle Scholar
  26. 26.
    van der Heide LP, Ramakers GM, Smidt MP. Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol 2006; 79(4):205–221.PubMedCrossRefGoogle Scholar
  27. 27.
    Hui RC, Gomes AR, Constantinidou D et al. The forkhead transcription factor FOX03a increases phosphoinositide-3 kinase/Akt activity in drug-resistant leukemic cells through induction of PIK3CA expression. Mol Cell Biol 2008; 28(19):5886–5898.PubMedCrossRefGoogle Scholar
  28. 28.
    Matsumoto M, Han S, Kitamura T et al. Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism. J Clin Invest 2006; 116(9):2464–2472.PubMedGoogle Scholar
  29. 29.
    Huang H, Regan KM, Wang F et al. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci USA 2005; 102(5):1649–1654.PubMedCrossRefGoogle Scholar
  30. 30.
    Lehtinen MK, Yuan Z, Boag PR et al. A conserved MST-FOXO signalingpathway mediates oxidative-stress responses and extends life span. Cell 2006; 125(5):987–1001.PubMedCrossRefGoogle Scholar
  31. 31.
    Essers MA, Weijzen S, de Vries-Smits AM et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 2004; 23(24):4802–4812.PubMedCrossRefGoogle Scholar
  32. 32.
    Brent MM, Anand R, Marmorstein R. Structural basis for DNA recognition by FoxOl and its regulation by posttranslational modification. Structure 2008; 16(9):1407–1416.PubMedCrossRefGoogle Scholar
  33. 33.
    Graves JD, Gotch Y, Draves KE et al. Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J 1998; 17(8):2224–2234.PubMedCrossRefGoogle Scholar
  34. 34.
    Yamagata K, Daitoku H, Takahashi Y et al. Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol Cell 2008; 32(2):221–231.PubMedCrossRefGoogle Scholar
  35. 35.
    Brunet A, Sweeney LB, Sturgill JF et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004; 303(5666):2011–2015.PubMedCrossRefGoogle Scholar
  36. 36.
    Kobayashi Y, Furukawa-Hibi Y, Chen C et al. SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress. Int J Mol Med 2005; 16(2):237–243.PubMedGoogle Scholar
  37. 37.
    Arden KC. FOXO animal models reveala variety of diverseroles for FOXO transcription factors. Oncogene 2008; 27(16):2345–2350.PubMedCrossRefGoogle Scholar
  38. 38.
    Ho KK, Myatt SS, Lam EW. Many forks in the path: cycling with FOXO. Oncogene 2008; 27(16):2300–2311.PubMedCrossRefGoogle Scholar
  39. 39.
    Polager S, Ginsberg D. E2F-at the crossroadsof life and death. Trends Cell Biol 2008; 18(11):528–535.PubMedCrossRefGoogle Scholar
  40. 40.
    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.PubMedCrossRefGoogle Scholar
  41. 41.
    Fernandez de Mattos S, Essafi A, Soeiro I et al. Fox03a and BCR-ABL regulate cyclin D2 transcription through a STAT5/BCL6-dependent mechanism. Mol Cell Biol 2004; 24(22):10058–10071.PubMedCrossRefGoogle Scholar
  42. 42.
    Kops GJ, Medema RH, Glassford J et al. Control of cell cycle exit and entry by protein kinase B-regulated forkhead transcription factors. Mol Cell Biol 2002; 22(7):2025–2036.PubMedCrossRefGoogle Scholar
  43. 43.
    Takano M, Lu Z, Goto T et al. Transcriptional cross talk between the forkhead transcription factor forkhead box 01A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells. Mol Endocrinol 2007; 21(10):2334–2349.PubMedCrossRefGoogle Scholar
  44. 44.
    Martinez-Gac L, Marques M, Garcia Z et al. Control of cyclin G2 mRNA expression by forkhead transcription factors: novel mechanism for cell cycle control by phosphoinositide 3-kinase and forkhead. Mol Cell Biol 2004; 24(5):2181–2189.PubMedCrossRefGoogle Scholar
  45. 45.
    Liu P, Kao TP, Huang H. CDKI promotes cell proliferation and survival via phosphorylation and inhibition of FOXOI transcription factor. Oncogene 2008; 27(34):4733–4744.PubMedCrossRefGoogle Scholar
  46. 46.
    Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9(8):616–627.PubMedCrossRefGoogle Scholar
  47. 47.
    Matsuoka S, Ballif BA, Smogorzewska A et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007; 316(5828):1160–1166.PubMedCrossRefGoogle Scholar
  48. 48.
    Mattila J, Kallijarvi J, Puig O. RNAi screening for kinases and phosphatases identifies FoxO regulators. Proc Natl Acad Sci USA 2008; 105(39):14873–14878.PubMedCrossRefGoogle Scholar
  49. 49.
    Tsai WB, Chung YM, Takahashi Y et al. Functional interaction between FOX03a and ATM regulates DNA damage response. Nat Cell Biol 2008; 10(4):460–467.PubMedCrossRefGoogle Scholar
  50. 50.
    Yalcin S, Zhang X, Luciano JP et al. Fox03 is essential for the regulation of ataxia telangiectasia mutated and oxidative stress-mediated homeostasis of hematopoietic stem cells. J Biol Chem 2008; 283(37): 25692–25705.PubMedCrossRefGoogle Scholar
  51. 51.
    Delpuech O, Griffiths B, East P et al. Induction of Mxil-SR alpha by FOX03a contributes to repression of Myc-dependent gene expression. Mol Cell Biol 2007; 27(13):4917–4930.PubMedCrossRefGoogle Scholar
  52. 52.
    Liebermann DA, Hoffman B. Gadd45 in stress signaling. J Mol Signal 2008; 3:15.PubMedCrossRefGoogle Scholar
  53. 53.
    Tran H, Brunet A, Grenier JM et al. DNA repair pathway stimulated by the forkhead transcription factor FOX03a through the Gadd45 protein. Science 2002; 296(5567):530–534.PubMedCrossRefGoogle Scholar
  54. 54.
    Fu Z, Tindall DJ. FOXOs, cancer and regulation of apoptosis. Oncogene 2008; 27(16):2312–2319.PubMedCrossRefGoogle Scholar
  55. 55.
    Tang TT, Dowbenko D, Jackson A er al. The forkhead transcription factor AFX activates apoptosis by induction of the BCL-6 transcriptional repressor. J Biol Chem 2002; 277(16):14255–14265.PubMedCrossRefGoogle Scholar
  56. 56.
    You H, Yamamoto K, Mak TW Regulation of transactivation-independent proapoptotic activity of p53 by FOX03a. Proc Natl Acad Sci USA 2006; 103(24):9051–9056.PubMedCrossRefGoogle Scholar
  57. 57.
    Wang F, Marshall CB, Yamamoto K et al. Biochemical and structural characterization of an intramolecular interaction in FOX03a and its binding with p53. J Mol Biol 2008; 384(3):590–603.PubMedCrossRefGoogle Scholar
  58. 58.
    Larsen PL. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci USA 1993; 90(19):8905–8909.PubMedCrossRefGoogle Scholar
  59. 59.
    Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000; 408(6809):239–247.PubMedCrossRefGoogle Scholar
  60. 60.
    Boxem M, van den Heuvel S. C. elegans class B synthetic multivulva genes act in G(1) regulation. Curr Biol 2002; 12(11):906–911.PubMedCrossRefGoogle Scholar
  61. 61.
    Kim Y, Sun H. Functional genomic approach to identify novel genes involved in the regulation of oxidative stress resistance and animaI lifespan. Aging Cell 2007; 6(4):489–503.PubMedCrossRefGoogle Scholar
  62. 62.
    Tohyama D, Yamaguchi A, Yamashita T. Inhibition of a eukaryotic initiation factor (eIF2Bdelta/F lIA3.2) during adulthood extends lifespan in Caenorhabditis elegans. FASEB J 2008; 22(12):4327–4337.PubMedCrossRefGoogle Scholar
  63. 63.
    Mukhopadhyay A, Oh SW, Tissenbaum HA. Worming pathways to and from DAF-16/FOXO. Exp Gerontol 2006; 41(10):928–934.PubMedCrossRefGoogle Scholar
  64. 64.
    Giannakou ME, Goss M, Partridge L. Role of dFOXO in lifespan extension by dietary restriction in Drosophila melanogaster: not required, but its activity modulates the response. Aging Cell 2008; 7(2):187–198.PubMedCrossRefGoogle Scholar
  65. 65.
    Masoro EJ. Overview of caloric restriction and ageing. Mech Ageing Dev 2005; 126(9):913–922.PubMedCrossRefGoogle Scholar
  66. 66.
    Kyoung Kim H, Kyoung Kim Y, Song IH et al. Down-regulation of a forkhead transcription factor, FOX03a, accelerates cellular senescence in human dermal fibroblasts. J Gerontol A Biol Sci Med Sci 2005; 60(1):4–9.Google Scholar
  67. 67.
    Yin Y, Shen WH. PTEN: a new guardian of the genome. Oncogene 2008; 27(41):5443–5453.PubMedCrossRefGoogle Scholar
  68. 68.
    Hu MC, Lee DF, Xia W et al. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOX03a. Cell 2004; 117(2):225–237.PubMedCrossRefGoogle Scholar
  69. 69.
    Yamamura Y, Lee WL, Inoue K er al. RUNX3 cooperates with Fox03a to induce apoptosis in gastric cancer cells. J Biol Chem 2006; 281(8):5267–5276.PubMedCrossRefGoogle Scholar
  70. 70.
    Gomes AR, Brosens JJ, Lam EW. Resist or die: FOXO transcription factors determine the cellular response to chemotherapy. Cell Cycle 2008; 7(20):3133–3136.PubMedGoogle Scholar
  71. 71.
    Balk SP, Knudsen KE. AR, the cell cycle and prostate cancer. Nucl Recept Signal 2008; 6:e001.PubMedGoogle Scholar
  72. 72.
    Li P, Lee H, Guo S et ale AKT-independent protection of prostate cancer cells from apoptosis mediated through complex formation between the androgen receptor and FKHR. Mol Cell Biol 2003; 23(1):104–118.PubMedCrossRefGoogle Scholar
  73. 73.
    Li P, Nicosia SV, Bai W. Antagonism between PTEN/MMACl/TEP-l and androgen receptor in growth and apoptosis of prostatic cancer cells. J Biol Chem 2001; 276(23):20444–20450.PubMedCrossRefGoogle Scholar
  74. 74.
    Ma Q, Fu W, Li P et al. FoxO1 mediates PTEN suppression of androgen receptor N-and C-terminal interactions and coactivator recruitment. Mol Endocrinol 2009; 23(2):213–225.PubMedCrossRefGoogle Scholar
  75. 75.
    Yang L, Xie S, Jamaluddin MS et al. Induction of androgen receptor expression by phosphatidylinositol 3-kinase/Akt downstream substrate, FOXO3a and their roles in apoptosis of LNCaP prostate cancer cells. J Biol Chem 2005; 280(39):33558–33565.PubMedCrossRefGoogle Scholar
  76. 76.
    Lynch RL, Konicek BW, McNulty AM et al. The progression of LNCaP human prostate cancer cells to androgen independence involves decreased FOXO3a expression and reduced p27KIPl promoter transactivation. Mol Cancer Res 2005; 3(3):163–169.PubMedCrossRefGoogle Scholar
  77. 77.
    Li J, Wang E, Rinaldo F et al. Upregulation of VEGF-C by androgen depletion: the involvement of IGF-IR-FOXO pathway. Oncogene 2005; 24(35):5510–5520.PubMedCrossRefGoogle Scholar
  78. 78.
    Ward EC, Hoekstra AV, Blok LJ et ale The regulation and function of the forkhead transcription factor, Forkhead box O1, is dependent on the progesterone receptor in endometrial carcinoma. Endocrinology 2008; 149(4):1942–1950.PubMedCrossRefGoogle Scholar
  79. 79.
    Zou Y, Tsai WB, Cheng CJ et al. Forkhead box transcription factor FOXO3a suppresses estrogen-dependent breast cancer cell proliferation and tumorigenesis. Breast Cancer Res 2008; 10(1):R21.PubMedCrossRefGoogle Scholar
  80. 80.
    Fernandez de Mattos S, Villalonga P, Clardy J et al. FOXO3a mediates the cytotoxic effects of cisplatin in colon cancer cells. Mol Cancer Ther 2008; 7(10):3237–3246.PubMedCrossRefGoogle Scholar
  81. 81.
    Arimoto-Ishida E, Ohmichi M, Mabuchi S et al. Inhibition of phosphorylation of a forkhead transcription factor sensitizes human ovarian cancer cells to cisplatin. Endocrinology 2004; 145(4):2014–2022.PubMedCrossRefGoogle Scholar
  82. 82.
    Hui RC, Francis RE, Guest SK et al. Doxorubicin activates FOXO3a to induce the expression of multidrug resistance gene ABCBl (MDR1) in K562 leukemic cells. Mol Cancer Ther 2008; 7(3):670–678.PubMedCrossRefGoogle Scholar
  83. 83.
    Han CY, Cho KB, Choi HS et al. Role of FoxOl activation in MDRI expression in adriamycin-resistant breast cancer cells. Carcinogenesis 2008; 29(9):1837–1844.PubMedCrossRefGoogle Scholar
  84. 84.
    Cui Y, Parra I, Zhang M et al. Elevated expression of mitogen-activated protein kinase phosphatase 3 in breast tumors: a mechanism of tamoxifen resistance. Cancer Res 2006; 66(11):5950–5959.PubMedCrossRefGoogle Scholar
  85. 85.
    Chan DW, Liu VW, Tsao GS et al. Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 2008; 29(9):1742–1750.PubMedCrossRefGoogle Scholar
  86. 86.
    Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 2002; 187(5):1416–1423.PubMedCrossRefGoogle Scholar
  87. 87.
    Gellersen B, Brosens IA, Brosens JJ. Decidualization of the human endometrium: mechanisms, functions and clinical perspectives. Semin Reprod Med 2007; 25(6):445–453.PubMedCrossRefGoogle Scholar
  88. 88.
    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 USA 2006; 103(44):16272–16277.PubMedCrossRefGoogle Scholar
  89. 89.
    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.PubMedCrossRefGoogle Scholar
  90. 90.
    Mak IY, Brosens JJ, Christian M et al. Regulated expression of signal transducer and activator of transcription, Stat5 and its enhancement of PRL expression in human endometrial stromal cells in vitro. J Clin Endocrinol Metab 2002; 87(6):2581–2588.PubMedCrossRefGoogle Scholar
  91. 91.
    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.PubMedCrossRefGoogle Scholar
  92. 92.
    Sekiya T, Adachi S, Kohu K et al. Identification of BMP and activin membrane-bound inhibitor (BAMBI), an inhibitor of transforming growth factor-beta signaling, as a target of the beta-catenin pathway in colorectal tumor cells. J Biol Chem 2004; 279(8):6840–6846.PubMedCrossRefGoogle Scholar
  93. 93.
    Feroze-Zaidi F, Fusi L, Takano M et al. Role and regulation of the serum-and glucocorticoid-regulated kinase 1 in fertile and infertile human endometrium. Endocrinology 2007; 148(10):5020–5029.PubMedCrossRefGoogle Scholar
  94. 94.
    Labied S, Kajihara T, Madureira PA et al. Progestins regulate the expression and activity of the forkhead transcription factor FOXO1 in differentiating human endometrium. Mol Endocrinol 2006; 20(1):35–44.PubMedCrossRefGoogle Scholar
  95. 95.
    Brosens JJ, Parker MG, McIndoe A et al. A role for menstruation in preconditioning the uterus for successful pregnancy. Am J Obstet Gynecol 2009; [Epub ahead of print]Google Scholar
  96. 96.
    Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004; 11(6):342–352.PubMedCrossRefGoogle Scholar
  97. 97.
    Amant F, Moerman P, Neven P et al. Endometrial cancer. Lancet 2005; 366(9484):491–505.PubMedCrossRefGoogle Scholar
  98. 98.
    Shang Y. Molecular mechanisms of oestrogen and SERMs in endometrial carcinogenesis. Nat Rev Cancer 2006; 6(5):360–368.PubMedCrossRefGoogle Scholar
  99. 99.
    Kong D, Suzuki A, Zou TT et al. PTEN1 is frequently mutated in primary endometrial carcinomas. Nat Genet 1997; 17(2):143–144.PubMedCrossRefGoogle Scholar
  100. 100.
    Lahav-Baratz S, Ben-Izhak O, Sabo E et al. Decreased level of the cell cycle regulator p27 and increased level of its ubiquitin ligase Skp2 in endometrial carcinoma but not in normal secretory or in hyperstimulated endometrium. Mol Hum Reprod 2004; 10(8):567–572.PubMedCrossRefGoogle Scholar
  101. 101.
    Sun M, Paciga JE, Feldman RI et al. Phosphatidylinositol-3-OH Kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor alpha (ERalpha) via interaction between ERalpha and PI3K. Cancer Res 2001; 61(16):5985–5991.PubMedGoogle Scholar
  102. 102.
    Risinger JI, Maxwell GL, Chandramouli GV et al. Microarray analysis reveals distinct gene expression profiles among different histologic types of endometrial cancer. Cancer Res 2003; 63(1):6–11.PubMedGoogle Scholar
  103. 103.
    Burney RO, Talbi S, Hamilton AE et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007; 148(8):3814–3826.PubMedCrossRefGoogle Scholar
  104. 104.
    Shazand K, Baban S, Prive C et al. FOXO1 and c-jun transcription factors mRNA are modulated in endometriosis. Mol Hum Reprod 2004; 10(12):871–877.PubMedCrossRefGoogle Scholar
  105. 105.
    Gebel HM, Braun DP, Tambur A et al. Spontaneous apoptosis of endometrial tissue is impaired in women with endometriosis. Fertil Steril 1998; 69(6):1042–1047.PubMedCrossRefGoogle Scholar
  106. 106.
    Dmowski WP, Ding J, Shen J et al. Apoptosis in endometrial glandular and stromal cells in women with and without endometriosis. Hum Reprod 2001; 16(9):1802–1808.PubMedCrossRefGoogle Scholar
  107. 107.
    Liu L, Rajareddy S, Reddy P et al. Phosphorylation and inactivation of glycogen synthase kinase-3 by soluble kit ligand in mouse oocytes during early follicular development. J Mol Endocrinol 2007; 38(1–2):137–146.PubMedCrossRefGoogle Scholar
  108. 108.
    Halperin J, Devi SY, Elizur S et al. Prolactin signaling through the short form of its receptor represses forkhead transcription factor FOXO3 and its target gene galt causing a severe ovarian defect. Mol Endocrinol 2008; 22(2):513–522.PubMedCrossRefGoogle Scholar
  109. 109.
    Reddy P, Liu L, Ren C et al. Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol Endocrinol 2005; 19(10):2564–2578.PubMedCrossRefGoogle Scholar
  110. 110.
    Wayne CM, Fan HY, Cheng X et al. Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS and the epidermal growth factor receptor are critical for granulosa cell differentiation. Mol Endocrinol 2007; 21(8):1940–1957.PubMedCrossRefGoogle Scholar
  111. 111.
    Nelson LM. Clinical practice. Primary ovarian insufficiency. N Engl J Med 2009; 360(6):606–614.PubMedCrossRefGoogle Scholar
  112. 112.
    Schlessinger D, Herrera L, Crisponi L et al. Genes and translocations involved in POF. Am J Med Genet 2002; 111(3):328–333.PubMedCrossRefGoogle Scholar
  113. 113.
    Aittomaki K, Lucena JL, Pakarinen P et al. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 1995; 82(6):959–968.PubMedCrossRefGoogle Scholar
  114. 114.
    Kaufinan FR, Kogut MD, Donnell GN et al. Hypergonadotropic hypogonadism in female patients with galactosemia. N Engl J Med 1981; 304(17):994–998.Google Scholar
  115. 115.
    Fogli A, Rodriguez D, Eymard-Pierre E et al. Ovarian failure related to eukaryotic initiation factor 2B mutations. Am J Hum Genet 2003; 72(6):1544–1550.PubMedCrossRefGoogle Scholar
  116. 116.
    Crisponi L, Deiana M, Loi A et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet 2001; 27(2):159–166.PubMedCrossRefGoogle Scholar
  117. 117.
    Gallardo TD, John GB, Bradshaw K et al. Sequence variation at the human FOXO3 locus: a study of premature ovarian failure and primary amenorrhea. Hum Reprod 2008; 23(1):216–221.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer+Business Media 2009

Authors and Affiliations

  • Jan J. Brosens
    • 1
  • Miranda S. C. Wilson
    • 2
  • Eric W. -F. Lam
    • 2
  1. 1.Institute of Reproductive and Developmental BiologyImperial College LondonLondonUK
  2. 2.Cancer Research UK Labs and Section of Cancer Cell Biology Department of Oncology Imperial College LondonHammer smith HospitalLondonUK

Personalised recommendations