Runt-related transcription factor 1 regulates luteinized hormone-induced prostaglandin-endoperoxide synthase 2 expression in rat periovulatory granulosa cells

Endocrinology

Volumn 150, Issue 7, 2009, Pages 3291-3300

  Liu, Jing ^a   Park, Eun Sil ^a   Jo, Misung ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHORIONIC GONADOTROPIN; LUTEINIZING HORMONE; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 2; PROSTAGLANDIN SYNTHASE; SERIC GONADOTROPIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL CULTURE; CELL ISOLATION; CELL STIMULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE MUTATION; GENE REPRESSION; GRANULOSA CELL; IN VIVO STUDY; KNOCKOUT GENE; NONHUMAN; OVARY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; RAT;

ANIMALS; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 2 SUBUNIT; CYCLOOXYGENASE 2; FEMALE; GRANULOSA CELLS; LUTEINIZING HORMONE; OVULATION; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; TRANSFECTION;

EID: 67649662607     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1527     Document Type: Article

References (63)

1. Hernandez-Gonzalez I, Gonzalez-Robayna I, Shimada M, Wayne CM, Ochsner SA, White L, Richards JS 2006 Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process? Mol Endocrinol 20:1300-1321
2. Jo M, Gieske MC, Payne CE, Wheeler-Price SE, Gieske JB, Ignatius IV, Curry Jr TE, Ko C 2004 Development and application of a rat ovarian gene expression database. Endocrinology 145:5384-5396 (Pubitemid 39551160)
3. Leo CP, Pisarska MD, Hsueh AJ 2001 DNA array analysis of changes in preovulatory gene expression in the rat ovary. Biol Reprod 65:269-276 (Pubitemid 32574809)
4. Espey LL, Richards JS 2002 Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biol Reprod 67:1662-1670 (Pubitemid 35387994)
5. Richards JS 2007 Genetics of ovulation. Semin Reprod Med 25:235-242 (Pubitemid 47047907)
6. Richards JS, Russell DL, Robker RL, Dajee M, Alliston TN 1998 Molecular mechanisms of ovulation and luteinization. Mol Cell Endocrinol 145:47-54 (Pubitemid 29003176)
7. Natraj U, Richards JS 1993 Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology 133:761-769 (Pubitemid 23238890)
8. Russell DL, Doyle KM, Gonzales-Robayna I, Pipaon C, Richards JS 2003 Egr-1 induction in rat granulosa cells by follicle-stimulating hormone and luteinizing hormone: combinatorial regulation by transcription factors cyclic adenosine 3′, 5′-monophosphate regulatory element binding protein, serum response factor, sp1, and early growth response factor-1. Mol Endocrinol 17:520-533 (Pubitemid 36403568)
9. Sirois J, Richards JS 1993 Transcriptional regulation of the rat prostaglandin endoperoxide synthase 2 gene in granulosa cells. Evidence for the role of a cis-acting C/EBPβ promoter element. J Biol Chem 268:21931-21938
10. Jo M, Curry Jr TE 2006 Luteinizing hormone-induced RUNX1 regulates the expression of genes in granulosa cells of rat periovulatory follicles. Mol Endocrinol 20:2156-2172 (Pubitemid 44286711)
11. Park ES, Choi S, Muse KN, Curry Jr TE, Jo M 2008 Response gene to complement 32 expression is induced by the luteinizing hormone (LH) surge and regulated by LH-induced mediators in the rodent ovary. Endocrinology 149:3025-3036 (Pubitemid 351724536)
12. Westendorf JJ, Hiebert SW 1999 Mammalian runt-domain proteins and their roles in hematopoiesis, osteogenesis, and leukemia. J Cell Biochem Suppl 32-33:51-58 (Pubitemid 30041810)
13. Cameron ER, Neil JC 2004 The Runx genes: lineage-specific oncogenes and tumor suppressors. Oncogene 23:4308-4314 (Pubitemid 38758596)
14. Kagoshima H, Shigesada K, Satake M, Ito Y, Miyoshi H, Ohki M, Pepling M, Gergen P 1993 The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet 9:338-341 (Pubitemid 23296286)
15. Meyers S, Downing JR, Hiebert SW 1993 Identification of AML-1 and the (8;21) translocation protein (AML-1/ETO) as sequence-specific DNA-binding proteins: the runt homology domain is required for DNA binding and protein-protein interactions. Mol Cell Biol 13:6336-6345
16. Wang S, Wang Q, Crute BE, Melnikova IN, Keller SR, Speck NA 1993 Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol Cell Biol 13:3324-3339
17. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR 1996 AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321-330 (Pubitemid 26042836)
18. Lian JB, Balint E, Javed A, Drissi H, Vitti R, Quinlan EJ, Zhang L, Van Wijnen AJ, Stein JL, Speck N, Stein GS 2003 Runx1/AML1 hematopoietic transcription factor contributes to skeletal development in vivo. J Cell Physiol 196:301-311 (Pubitemid 36775877)
19. Theriault FM, Nuthall HN, Dong Z, Lo R, Barnabe-Heider F, Miller FD, Stifani S 2005 Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J Neurosci 25:2050-2061 (Pubitemid 40289410)
20. Espey LL 1994 Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol Reprod 50:233-238 (Pubitemid 24058476)
21. Richards JS, Liu Z, Shimada M 2008 Immune-like mechanisms in ovulation. Trends Endocrinol Metab 19:191-196 (Pubitemid 351993011)
22. Tsafriri A, Lindner HR, Zor U, Lamprecht SA 1972 Physiological role of prostaglandins in the induction of ovulation. Prostaglandins 2:1-10
23. Boerboom D, Sirois J 1998 Molecular characterization of equine prostaglandin G/H synthase-2 and regulation of its messenger ribonucleic acid in preovulatory follicles. Endocrinology 139:1662-1670 (Pubitemid 28513822)
24. Sirois J, Richards JS 1992 Purification and characterization of a novel, distinct isoform of prostaglandin endoperoxide synthase induced by human chorionic gonadotropin in granulosa cells of rat preovulatory follicles. J Biol Chem 267:6382-6388
25. Sirois J 1994 Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology 135:841-848 (Pubitemid 24271169)
26. Duffy DM, Stouffer RL 2001 The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. Mol Hum Reprod 7:731-739 (Pubitemid 32734296)
27. Tokuyama O, Nakamura Y, Muso A, Honda K, Ishiko O, Ogita S 2001 Expression and distribution of cyclooxygenase-2 in human periovulatory ovary. Int J Mol Med 8:603-606
28. Sirois J, Simmons DL, Richards JS 1992 Hormonal regulation of messenger ribonucleic acid encoding a novel isoform of prostaglandin endoperoxide H synthase in rat preovulatory follicles. Induction in vivo and in vitro. J Biol Chem 267:11586-11592
29. Davis BJ, Lennard DE, Lee CA, Tiano HF, Morham SG, Wetsel WC, Langenbach R 1999 Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1′. Endocrinology 140:2685-2695 (Pubitemid 32245148)
30. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK 1997Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91:197-208 (Pubitemid 27456387)
31. Liu J, Antaya M, Boerboom D, Lussier JG, Silversides DW, Sirois J 1999 The delayed activation of the prostaglandin G/H synthase-2 promoter in bovine granulosa cells is associated with down-regulation of truncated upstream stimulatory factor-2. J Biol Chem 274:35037-35045 (Pubitemid 129509555)
32. Morris JK, Richards JS 1996 An E-box region within the prostaglandin endoperoxide synthase-2 (PGS-2) promoter is required for transcription in rat ovarian granulosa cells. J Biol Chem 271:16633-16643 (Pubitemid 26239022)
33. Sayasith K, Bouchard N, Sawadogo M, Lussier JG, Sirois J 2004 Molecular characterization and role of bovine upstream stimulatory factor 1 and 2 in the regulation of the prostaglandin G/H synthase-2 promoter in granulosa cells. J Biol Chem 279:6327-6336 (Pubitemid 38248765)
34. Mehrotra M, Saegusa M, Voznesensky O, Pilbeam C 2006 Role of Cbfa1/Runx2 in the fluid shear stress induction of COX-2 in osteoblasts. Biochem Biophys Res Commun 341:1225-1230 (Pubitemid 43221795)
35. Chikazu D, Li X, Kawaguchi H, Sakuma Y, Voznesensky OS, Adams DJ, Xu M, Hoshio K, Katavic V, Herschman HR, Raisz LG, Pilbeam CC 2002 Bone morphogenetic protein 2 induces cyclo-oxygenase 2 in osteoblasts via a Cbfal binding site: role in effects of bone morphogenetic protein 2 in vitro and in vivo. J Bone Miner Res 17:1430-1440 (Pubitemid 34803827)
36. Mann JS, Kindy MS, Edwards DR, Curry Jr TE 1991 Hormonal regulation of matrix metalloproteinase inhibitors in rat granulosa cells and ovaries. Endocrinology 128:1825-1832
37. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2[-ΔΔC(T)] method. Methods 25:402-408 (Pubitemid 34164012)
38. Hsieh M, Mulders SM, Friis RR, Dharmarajan A, Richards JS 2003 Expression and localization of secreted frizzled-related protein-4 in the rodent ovary: evidence for selective up-regulation in luteinized granulosa cells. Endocrinology 144:4597-4606 (Pubitemid 37204859)
39. Hayashi K, Natsume W, Watanabe T, Abe N, Iwai N, Okada H, Ito Y, Asano M, Iwakura Y, Habu S, Takahama Y, Satake M 2000 Diminution of the AML1 transcription factor function causes differential effects on the fates of CD4 and CD8 single-positive T cells. J Immunol 165:6816-6824 (Pubitemid 32001149)
40. Akiyama H, Kanno T, Ito H, Terry A, Neil J, Ito Y, Nakamura T 1999 Positive and negative regulation of chondrogenesis by splice variants of PEBP2αA/CBFα1 in clonal mouse EC cells, ATDC5. J Cell Physiol 181:169-178 (Pubitemid 29400384)
41. Sakakura C, Yamaguchi-Iwai Y, Satake M, Bae SC, Takahashi A, Ogawa E, Hagiwara A, Takahashi T, Murakami A, Makino K 1994 Growth inhibition and induction of differentiation of t(8;21) acute myeloid leukemia cells by the DNA-binding domain of PEBP2 and the AML1/MTG8(ETO)-specific antisense oligonucleotide. Proc Natl Acad Sci USA 91:11723-11727 (Pubitemid 24356417)
42. Sun L, Vitolo M, Passaniti A 2001 Runt-related gene 2 in endothelial cells: inducible expression and specific regulation of cell migration and invasion. Cancer Res 61:4994-5001 (Pubitemid 32681526)
43. Lee YS, Terzidou V, Lindstrom T, Johnson M, Bennett PR 2005 The role of CCAAT/enhancer-binding protein beta in the transcriptional regulation of COX-2 in human amnion. Mol Hum Reprod 11:853-858
44. Zhu Y, Saunders MA, Yeh H, Deng WG, Wu KK 2002 Dynamic regulation of cyclooxygenase-2 promoter activity by isoforms of CCAAT/enhancer-binding proteins. J Biol Chem 277:6923-6928 (Pubitemid 34953077)
45. Wu KK, Liou JY, Cieslik K 2005 Transcriptional control of COX-2 via C/EBPβ. Arterioscler Thromb Vasc Biol 25:679-685 (Pubitemid 40463853)
46. Petrovick MS, Hiebert SW, Friedman AD, Hetherington CJ, Tenen DG, Zhang DE 1998 Multiple functional domains of AML1: PU. 1 and C/EBPα synergize with different regions of AML1. Mol Cell Biol 18:3915-3925 (Pubitemid 28287915)
47. Gutierrez S, Javed A, Tennant DK, van Rees M, Montecino M, Stein GS, Stein JL, Lian JB 2002 CCAAT/enhancer-binding proteins (C/EBP) β and Δ activate osteocalcin gene transcription and synergize with Runx2 at the C/EBP element to regulate bone-specific expression. J Biol Chem 277:1316-1323 (Pubitemid 34968885)
48. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS 2006 Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 20:1352-1365 (Pubitemid 43801236)
49. Joyce IM, Pendola FL, O'Brien M, Eppig JJ 2001 Regulation of prostaglandinendoperoxide synthase 2 messenger ribonucleic acid expression in mouse granulosa cells during ovulation. Endocrinology 142:3187-3197 (Pubitemid 32575556)
50. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684 (Pubitemid 38141636)
51. Takahashi T, Morrow JD, Wang H, Dey SK 2006 Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem 281:37117-37129 (Pubitemid 46042182)
52. Wotton S, Terry A, Kilbey A, Jenkins A, Herzyk P, Cameron E, Neil JC 2008 Gene array analysis reveals a common Runx transcriptional programme controlling cell adhesion and survival. Oncogene 27:5856-5866
53. Choi S, Park E, Jo M 2007 The expression pattern of core binding factor (CBF) in the rodent ovary. Biol Reprod (Special Issue) 95:97
54. Helms C, Cao L, Krueger JG, Wijsman EM, Chamian F, Gordon D, Heffernan M, Daw JA, Robarge J, Ott J, Kwok PY, Menter A, Bowcock AM 2003 A putative RUNX1 binding site variant between SLC9A3R1 and NAT9 is associated with susceptibility to psoriasis. Nat Genet 35:349-356 (Pubitemid 37486918)
55. Prokunina L, Castillejo-López C, Oberg F, Gunnarsson I, Berg L, Magnusson V, Brookes AJ, Tentler D, Kristjansdóttir H, Gröndal G, Bolstad AI, Svenungsson E, Lundberg I, Sturfelt G, Jönssen A, Truedsson L, Lima G, Alcocer- Varela J, Jonsson R, Gyllensten UB, Harley JB, Alarcón-Segovia D, Steinsson K, Alarcón-Riquelme ME 2002 A regulatory polymorphism in PDCD1 is associated with susceptibility to systemic lupus erythematosus in humans. Nat Genet 32:666-669 (Pubitemid 35435182)
56. Tokuhiro S, Yamada R, Chang X, Suzuki A, Kochi Y, Sawada T, Suzuki M, Nagasaki M, Ohtsuki M, Ono M, Furukawa H, Nagashima M, Yoshino S, Mabuchi A, Sekine A, Saito S, Takahashi A, Tsunoda T, Nakamura Y, Yamamoto K 2003 An intronic SNP in a RUNX1 binding site of SLC22A4, encoding an organic cation transporter, is associated with rheumatoid arthritis. Nat Genet 35:341-348 (Pubitemid 37486917)
57. Egawa T, Tillman RE, Naoe Y, Taniuchi I, Littman DR 2007 The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J Exp Med 204:1945-1957 (Pubitemid 47236329)
58. Ichikawa M, Asai T, Saito T, Seo S, Yamazaki I, Yamagata T, Mitani K, Chiba S, Ogawa S, Kurokawa M, Hirai H 2004 AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat Med 10:299-304 (Pubitemid 38667622)
59. Maier H, Ostraat R, Gao H, Fields S, Shinton SA, Medina KL, Ikawa T, Murre C, Singh H, Hardy RR, Hagman J 2004 Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nat Immunol 5:1069-1077 (Pubitemid 41057727)
60. Yamada R, Ymamoto K 2005 Recent findings on genes associated with inflammatory disease. Mutat Res 573:136-151
61. Alarcón-Riquelme ME 2004 Role of RUNX in autoimmune diseases linking rheumatoid arthritis, psoriasis and lupus. Arthritis Res Ther 6:169-173 (Pubitemid 39162379)
62. Smith WL, DeWitt DL, Garavito RM 2000 Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 69:145-182 (Pubitemid 30792207)
63. Rozen S, Skaletzky HJ 2000 Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press; 365-386