Signaling Pathways in Endometriosis (Eutopic/Ectopic)

Endometriosis: Science and Practice

Volumn , Issue , 2012, Pages 164-172

  Kim, J Julie ^a   Yin, Xunqin ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

AKT; Endometriosis; MAPK; Mitogen activated protein kinase; PI3K; PKA; Protein kinase A; Signaling

Indexed keywords

EID: 84886954852     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781444398519.ch16     Document Type: Chapter

References (82)

1. Giudice LC, Kao LC. Endometriosis. Lancet 2004; 364(9447): 1789-1799.
2. Bulun SE. Endometriosis. N Engl J Med 2009; 360(3):268-279.
3. Swiersz LM. Role of endometriosis in cancer and tumor development. Ann N Y Acad Sci 2002; 955:281-292; discussion 93-95, 396-406.
4. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298(5600):1912-1934.
5. Chiaradonna F, Balestrieri C, Gaglio D, Vanoni M. RAS and PKA pathways in cancer: new insight from transcriptional analysis. Front Biosci 2008; 13:5257-5278.
6. Gerits N, Kostenko S, Shiryaev A, Johannessen M, Moens U. Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell Signal 2008; 20(9):1592-1607.
7. Moelling K, Schad K, Bosse M, Zimmermann S, Schweneker M. Regulation of Raf-Akt Cross-talk. J Biol Chem 2002; 277(34): 31099-1106.
8. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 2008; 9(7):517-531.
9. Altomare DA, Testa JR. Perturbations of the AKT signaling pathway in human cancer. Oncogene 2005; 24(50):7455-7464.
10. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB. Exploiting the PI3K/ AKT pathway for cancer drug discovery. Nat Rev Drug Discov 2005; 4(12):988-1004.
11. Steelman LS, Stadelman KM, Chappell WH et al. Akt as a therapeutic target in cancer. Expert Opin Ther Targets 2008; 12(9):1139-1165.
12. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999; 13(22):2905-2927.
13. Bhaskar PT, Hay N. The two TORCs and Akt. Dev Cell 2007; 12(4):487-502.
14. Brazil DP, Yang ZZ, Hemmings BA. Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 2004; 29(5): 233-242.
15. Hay N. The Akt-mTOR tango and its relevance to cancer. Cancer Cell 2005; 8(3):179-183.
16. Lawlor MA, Alessi DR. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J Cell Sci 2001; 114(Pt 16): 2903-2910.
17. Yagyu T, Tsuji Y, Haruta S et al. Activation of mammalian target of rapamycin in postmenopausal ovarian endometriosis. Int J Gynecol Cancer 2006; 16(4):1545-1551.
18. Laudanski P, Szamatowicz J, Kowalczuk O, Kuzmicki M, Grabowicz M, Chyczewski L. Expression of selected tumor suppressor and oncogenes in endometrium of women with endometriosis. Hum Reprod 2009; 24(8):1880-1890.
19. Honda H, Barrueto FF, Gogusev J, Im DD, Morin PJ. Serial analysis of gene expression reveals differential expression between endometriosis and normal endometrium. Possible roles for AXL and SHC1 in the pathogenesis of endometriosis. Reprod Biol Endocrinol 2008; 6:59.
20. Cinar O, Seval Y, Uz YH et al. Differential regulation of Akt phosphorylation in endometriosis. Reprod Biomed Online 2009; 19(6): 864-871.
21. Risinger JI, Hayes AK, Berchuck A, Barrett JC. PTEN/MMAC1 mutations in endometrial cancers. Cancer Res 1997; 57(21):4736-4738.
22. Hecht JL, Mutter GL. Molecular and pathologic aspects of endometrial carcinogenesis. J Clin Oncol 2006; 24(29):4783-4791.
23. Treloar SA, Zhao ZZ, Le L et al. Variants in EMX2 and PTEN do not contribute to risk of endometriosis. Mol Hum Reprod 2007; 13(8): 587-594.
24. Ali-Fehmi R, Khalifeh I, Bandyopadhyay S et al. Patterns of loss of heterozygosity at 10q23.3 and microsatellite instability in endometriosis, atypical endometriosis, and ovarian carcinoma arising in association with endometriosis. Int J Gynecol Pathol 2006; 25(3): 223-229.
25. Zhang H, Zhao X, Liu S, Li J, Wen Z, Li M. 17betaE2 promotes cell proliferation in endometriosis by decreasing PTEN via NFkappaBdependent pathway. Mol Cell Endocrinol 2010; 317(1-2):31-43.
26. Podsypanina K, Ellenson LH, Nemes A et al. Mutation of Pten/ Mmac1 in mice causes neoplasia in multiple organ systems. Proc Natl Acad Sci USA 1999; 96(4):1563-1568.
27. Daikoku T, Hirota Y, Tranguch S et al. Conditional loss of uterine Pten unfailingly and rapidly induces endometrial cancer in mice. Cancer Res 2008; 68(14):5619-5627.
28. Dinulescu DM, Ince TA, Quade BJ, Shafer SA, Crowley D, Jacks T. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 2005; 11(1): 63-70.
29. Cheng YH, Imir A, Fenkci V, Yilmaz MB, Bulun SE. Stromal cells of endometriosis fail to produce paracrine factors that induce epithelial 17beta-hydroxysteroid dehydrogenase type 2 gene and its transcriptional regulator Sp1: a mechanism for defective estradiol metabolism. Am J Obstet Gynecol 2007; 196(4):391.
30. Cheng YH, Imir A, Suzuki T et al. SP1 and SP3 mediate progesteronedependent induction of the 17beta hydroxysteroid dehydrogenase type 2 gene in human endometrium. Biol Reprod 2006; 75(4):605-614.
31. Florio P, Rossi M, Sigurdardottir M et al. Paracrine regulation of endometrial function: interaction between progesterone and corticotropin- releasing factor (CRF) and activin A. Steroids 2003; 68(10-13): 801-807.
32. Yang S, Fang Z, Gurates B et al. Stromal PRs mediate induction of 17beta-hydroxysteroid dehydrogenase type 2 expression in human endometrial epithelium: a paracrine mechanism for inactivation of E2. Mol Endocrinol 2001; 15(12):2093-2105.
33. Franco HL, Jeong JW, Tsai SY, Lydon JP, DeMayo FJ. In vivo analysis of progesterone receptor action in the uterus during embryo implantation. Semin Cell Dev Biol 2008; 19(2):178-186.
34. Kurihara I, Lee DK, Petit FG et al. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet 2007; 3(6):e102.
35. Rubel CA, Jeong JW, Tsai SY, Lydon JP, DeMayo FJ. Epithelial-stromal interaction and progesterone receptors in the mouse uterus. Semin Reprod Med 2010; 28(1):27-35.
36. Simon L, Spiewak KA, Ekman GC et al. Stromal progesterone receptors mediate induction of Indian Hedgehog (IHH) in uterine epithelium and its downstream targets in uterine stroma. Endocrinology 2009; 150(8):3871-3876.
37. Cunha GR, Cooke PS, Kurita T. Role of stromal-epithelial interactions in hormonal responses. Arch Histol Cytol 2004; 67(5):417-434.
38. Kurita T, Cooke PS, Cunha GR. Epithelial-stromal tissue interaction in paramesonephric (Mullerian) epithelial differentiation. Dev Biol 2001; 240(1):194-211.
39. Kurita T, Medina R, Schabel AB et al. The activation function-1 domain of estrogen receptor alpha in uterine stromal cells is required for mouse but not human uterine epithelial response to estrogen. Differentiation 2005; 73(6):313-322.
40. Kurita T, Wang YZ, Donjacour AA et al. Paracrine regulation of apoptosis by steroid hormones in the male and female reproductive system. Cell Death Differ 2001; 8(2):192-200.
41. Bulun SE, Cheng YH, Pavone ME et al. 17Beta-hydroxysteroid dehydrogenase- 2 deficiency and progesterone resistance in endometriosis. Semin Reprod Med 2010; 28(1):44-50.
42. Zhang H, Li M, Zheng X, Sun Y, Wen Z, Zhao X. Endometriotic stromal cells lose the ability to regulate cell-survival signaling in endometrial epithelial cells in vitro. Mol Hum Reprod 2009; 15(10):653-663.
43. Rubinfeld H, Seger R. The ERK cascade: a prototype of MAPK signaling. Mol Biotechnol 2005; 31(2):151-174.
44. Cobb MH. MAP kinase pathways. Prog Biophys Mol Biol 1999; 71(3-4):479-500.
45. Bodart JF. Extracellular-regulated kinase-mitogen-activated protein kinase cascade: unsolved issues. J Cell Biochem 2010; 109(5): 850-857.
46. Matsuzaki S, Canis M, Vaurs-Barriere C, Boespflug-Tanguy O, Dastugue B, Mage G. DNA microarray analysis of gene expression in eutopic endometrium from patients with deep endometriosis using laser capture microdissection. Fertil Steril 2005; 84(Suppl 2): 1180-1190.
47. Matsuzaki S, Canis M, Pouly JL, Botchorishvili R, Dechelotte PJ, Mage G. Differential expression of genes in eutopic and ectopic endometrium from patients with ovarian endometriosis. Fertil Steril 2006; 86(3):548-553.
48. Wu Y, Kajdacsy-Balla A, Strawn E et al. Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology 2006; 147(1):232-246.
49. 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.
50. Velarde MC, Aghajanova L, Nezhat CR, Giudice LC. Increased mitogen- activated protein kinase kinase/extracellularly regulated kinase activity in human endometrial stromal fibroblasts of women with endometriosis reduces 3',5'-cyclic adenosine 5'-monophosphate inhibition of cyclin D1. Endocrinology 2009; 150(10):4701-4712.
51. Gazvani MR, Christmas S, Quenby S, Kirwan J, Johnson PM, Kingsland CR. Peritoneal fluid concentrations of interleukin-8 in women with endometriosis: relationship to stage of disease. Hum Reprod 1998; 13(7):1957-1961.
52. Harada T, Yoshioka H, Yoshida S et al. Increased interleukin-6 levels in peritoneal fluid of infertile patients with active endometriosis. Am J Obstet Gynecol 1997; 176(3):593-597.
53. Pizzo A, Salmeri FM, Ardita FV, Sofo V, Tripepi M, Marsico S. Behaviour of cytokine levels in serum and peritoneal fluid of women with endometriosis. Gynecol Obstet Invest 2002; 54(2):82-87.
54. Ryan IP, Tseng JF, Schriock ED, Khorram O, Landers DV, Taylor RN. Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis. Fertil Steril 1995; 63(4):929-932.
55. Yoshino O, Osuga Y, Hirota Y et al. Possible pathophysiological roles of mitogen-activated protein kinases (MAPKs) in endometriosis. Am J Reprod Immunol 2004; 52(5):306-311.
56. Yamauchi N, Harada T, Taniguchi F, Yoshida S, Iwabe T, Terakawa N. Tumor necrosis factor-alpha induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-kappaB and mitogen-activated protein kinase pathways. Fertil Steril 2004; 82(Suppl 3):1023-1028.
57. Taniguchi F, Harada T, Miyakoda H et al. TAK1 activation for cytokine synthesis and proliferation of endometriotic cells. Mol Cell Endocrinol 2009; 307(1-2):196-204.
58. Srivastava AK, Qin X, Wedhas N et al. Tumor necrosis factor-alpha augments matrix metalloproteinase-9 production in skeletal muscle cells through the activation of transforming growth factor-beta-activated kinase 1 (TAK1)-dependent signaling pathway. J Biol Chem 2007; 282(48):35113-35124.
59. Hirota Y, Osuga Y, Hirata T et al. Activation of protease-activated receptor 2 stimulates proliferation and interleukin (IL)-6 and IL-8 secretion of endometriotic stromal cells. Hum Reprod 2005; 20(12): 3547-3553.
60. Grund EM, Kagan D, Tran CA et al. Tumor necrosis factor-alpha regulates inflammatory and mesenchymal responses via mitogenactivated protein kinase kinase, p38, and nuclear factor kappaB in human endometriotic epithelial cells. Mol Pharmacol 2008; 73(5): 1394-1404.
61. Tagashira Y, Taniguchi F, Harada T, Ikeda A, Watanabe A, Terakawa N. Interleukin-10 attenuates TNF-alpha-induced interleukin-6 production in endometriotic stromal cells. Fertil Steril 2009; 91(5 Suppl):2185-2192.
62. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19: 683-765.
63. Bogdan C, Vodovotz Y, Nathan C. Macrophage deactivation by interleukin 10. J Exp Med 1991; 174(6):1549-1555.
64. Gellersen B, Brosens J. Cyclic AMP and progesterone receptor crosstalk in human endometrium: a decidualizing affair. J Endocrinol 2003; 178(3):357-372.
65. Frank GR, Brar AK, Cedars MI, Handwerger S. Prostaglandin E2 enhances human endometrial stromal cell differentiation. Endocrinology 1994; 134(1):258-263.
66. Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A. Up-regulation of cyclooxygenase-2 expression and prostaglandin E2 production in human endometriotic cells by macrophage migration inhibitory factor: involvement of novel kinase signaling pathways. Endocrinology 2009; 150(7):3128-3137.
67. Wu MH, Wang CA, Lin CC, Chen LC, Chang WC, Tsai SJ. Distinct regulation of cyclooxygenase-2 by interleukin-1beta in normal and endometriotic stromal cells. J Clin Endocrinol Metab 2005; 90(1): 286-295.
68. Aghajanova L, Hamilton A, Kwintkiewicz J, Vo KC, Giudice LC. Steroidogenic enzyme and key decidualization marker dysregulation in endometrial stromal cells from women with versus without endometriosis. Biol Reprod 2009; 80(1):105-114.
69. Aghajanova L, Horcajadas JA, Weeks JL et al. The protein kinase a pathway- regulated transcriptome of endometrial stromal fibroblasts reveals compromised differentiation and persistent proliferative potential in endometriosis. Endocrinology 2010; 151(3):1341-1355.
70. Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006; 85(3):564-572.
71. Tian Y, Kong B, Zhu W, Su S, Kan Y. Expression of steroidogenic factor 1 (SF-1) and steroidogenic acute regulatory protein (StAR) in endometriosis is associated with endometriosis severity. J Int Med Res2009; 37(5):1389-1395.
72. Attar E, Tokunaga H, Imir G et al. Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J Clin Endocrinol Metab 2009; 94(2):623-631.
73. Sun HS, Hsiao KY, Hsu CC, Wu MH, Tsai SJ. Transactivation of steroidogenic acute regulatory protein in human endometriotic stromalcells is mediated by the prostaglandin EP2 receptor. Endocrinology 2003; 144(9):3934-3942.
74. Kim LC, Song L, Haura EB. Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 2009; 6(10):587-595.
75. McCubrey JA, Steelman LS, Abrams SL et al. Emerging Raf inhibitors. Expert Opin Emerg Drugs 2009; 14(4):633-648.
76. McCubrey JA, Steelman LS, Franklin RA et al. Targeting the RAF/ MEK/ERK, PI3K/AKT and p53 pathways in hematopoietic drug resistance. Adv Enzyme Regul 2007; 47:64-103.
77. Druker BJ. STI571 (Gleevec) as a paradigm for cancer therapy. Trends Mol Med 2002; 8(4 Suppl):S14-18.
78. Becker J. Signal transduction inhibitors - a work in progress. Nat Biotechnol 2004; 22(1):15-18.
79. Carter CA, Kelly RJ, Giaccone G. Small-molecule inhibitors of the human epidermal receptor family. Expert Opin Invest Drugs 2009; 18(12): 1829-1842.
80. Castaneda CA, Gomez HL. Pazopanib: an antiangiogenic drug in perspective. Future Oncol 2009; 5(9):1335-1348.
81. Lane HA, Breuleux M. Optimal targeting of the mTORC1 kinase in human cancer. Curr Opin Cell Biol 2009; 21(2):219-229.
82. Guo SW. Epigenetics of endometriosis. Mol Hum Reprod 2009; 15(10): 587-607.