Functional differentiation of uterine stromal cells involves cross-regulation between bone morphogenetic protein 2 and Krüppel-like factor (KLF) family members KLF9 and KLF13

Endocrinology

Volumn 151, Issue 7, 2010, Pages 3396-3406

  Pabona, John Mark P ^a   Zeng, Zhaoyang ^a   Simmen, Frank A ^a   Simmen, Rosalia C M ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; BONE MORPHOGENETIC PROTEIN 2; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 13; KRUPPEL LIKE FACTOR 9; LAMIN A; MESSENGER RNA; PROGESTERONE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BTEB1 PROTEIN, MOUSE; CELL CYCLE PROTEIN; KLF13 PROTEIN, MOUSE; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BMP2 GENE; CELL DIFFERENTIATION; CONTROLLED STUDY; DECIDUA; ENDOMETRIUM; FEMALE; GENE; HUMAN; HUMAN CELL; IGFBP1 GENE; KLF13 GENE; KLF9 GENE; MOUSE; NIDATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SUBFERTILITY; UTERUS; WILD TYPE; ANIMAL; CELL LINE; CYTOLOGY; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PREGNANCY; RNA INTERFERENCE; STROMA CELL; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 2; CELL CYCLE PROTEINS; CELL LINE; ENDOMETRIUM; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; POLYMERASE CHAIN REACTION; PREGNANCY; REPRESSOR PROTEINS; RNA INTERFERENCE; STROMAL CELLS; UTERUS;

EID: 77954606831     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-1370     Document Type: Article

References (49)

1. Matzuk MM, Lamb DJ 2002 Genetic dissection of mammalian fertility pathways. Nat Cell Biol 4(Suppl):S41-S49
2. Psychoyos A 1973 Hormonal control of ovoimplantation. Vitam Horm 31:201-256
3. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H 2004 Molecular cues to implantation. Endocr Rev 25:341-373
4. Wang H, Dey SK 2006 Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185-199
5. McKenna NJ, O'Malley BW 2002 Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108:465-474
6. Lonard DM, O'Malley BW 2006 The expanding cosmos of nuclear receptor coactivators. Cell 125:411-414
7. Gellersen B, Brosens IA, Brosens JJ 2007 Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin Reprod Med 25:445-453
8. Tsai MJ, O'Malley BW 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63:451-486
9. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
10. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM 2000 Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289:1751-1754
11. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM 2003 Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci USA 100:9744-9749
12. Arnett-Mansfield RL, DeFazio A, Mote PA, Clarke CL 2004 Subnuclear distribution of progesterone receptors A and B in normal and malignant endometrium. J Clin Endocrinol Metab 89:1429-1442
13. Balleine RL, Earls PJ, Webster LR, Mote PA, deFazio A, Harnett PR, Clarke CL 2004 Expression of progesterone receptors A and B isoforms in low-grade endometrial stromal sarcoma. Int J Gynecol Pathol 23:138-144
14. Mote PA, Bartow S, Tran N, Clarke CL 2002 Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast Cancer Res Treat 72:163-172
15. Imataka H, Sogawa K, Yasumoto K, Kikuchi Y, Sasano K, Kobayashi A, Hayami M, Fujii-Kuriyama Y 1992 Two regulatory proteins that bind to the basic transcription element (BTE), a GC box sequence in the promoter region of the rat P-4501A1 gene. EMBO J 11:3663-3671
16. Zhang D, Zhang XL, Michel FJ, Blum JL, Simmen FA, Simmen RCM 2002 Direct interaction of the Krüppel-like family (KLF) member, BTEB1, and PR mediates progesterone responsive gene expression in endometrial epithelial cells. Endocrinology 143:62-73
17. Zhang XL, Zhang D, Michel FJ, Blum JL, Simmen FA, Simmen RCM 2003 Selective interactions of KLF9/BTEB1 with progesterone receptor isoforms A and B determine transcriptional activity of progesterone-responsive genes in endometrial epithelial cells. J Biol Chem 278:21474-21482
18. Simmen RCM, Eason RR, McQuown JR, Linz AL, Kang TJ, Chatman Jr L, Till SR, Fujii-Kuriyama Y, Simmen FA, Oh SP 2004 Subfertility, uterine hypoplasia, and partial progesterone resistance in mice lacking the Krüppel-like factor 9/basic transcription element binding protein 1 (BTEB1) gene. J Biol Chem 279:29286-29294
19. Velarde MC, Geng Y, Eason RR, Simmen FA, Simmen RCM 2005 Null mutation of Krüppel-like factor 9/basic transcription element binding protein 1 alters peri-implantation uterine development in mice. Biol Reprod 73:472-481
20. Nifuji A, Kellermann O, Kuboki Y, Wozney JM, Noda Masaki 1997 Perturbation of BMP signaling in somatogenesis resulted in vertebral and rib malformations in the axial skeletal formation. J Bone Miner Res 12:332-342
21. Abe E, Yamamoto M, Taguchi Y, Lecka-Czernik B, O'Brien CA, Economides AN, Stahl N, Jilka RL, Manolagas SC 2000 Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin. J Bone Miner Res 15:663-673
22. Canalis E, Economides AN, Gazzerro E 2003 Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24:218-235
23. James RG, Schultheiss TM 2005 BMP signaling promotes intermediate mesoderm gene expression in a dose-dependent, cell autonomous and translation-dependent manner. Dev Biol 288:113-125
24. Schlueter J, Männer J, Brand T 2006 BMPis an important regulator of proepicardial identity in the chick embryo. Dev Biol 295:546-558
25. Zhang H, Bradley A 1996 Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977-2986
26. Lee KY, Jeong JW, Wang J, Ma L, Martin JF, Tsai SY, Lydon JP, DeMayo FJ 2007 BMP2 is critical for the murine uterine decidual response. Mol Cell Biol 27:5468-5478
27. Ying Y, Zhao GQ 2000 Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, smad1, during mouse decidualization. Biol Reprod 63:1781-1786
28. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, Hogan BLM 2001 Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci USA 98:1047-1052
29. Suske G, Bruford E, Philipsen S 2005 Mammalian SP/KLF transcription factors: bring in the family. Genomics 85:551-556
30. Krikun G, Mor G, Alvero A, Guller S, Schatz F, Sapi E, Rahman M, Caze R, Qumsiyeh M, Lockwood CJ 2004 A novel immortalized human endometrial stromal cell line with normal progestational response. Endocrinology 145:2291-2296
31. Pabona JMP, Velarde MC, Zeng Z, Simmen FA, Simmen RCM 2009 Nuclear receptor co-regulator Krüppel-like factor 9 and prohibitin 2 expression in estrogen-induced epithelial cell proliferation in the mouse uterus. J Endocrinol 200:63-73
32. Velarde MC, Iruthayanathan M, Eason RR, Zhang D, Simmen FA, Simmen RCM 2006 Progesterone receptor transactivation of the secretory leukocyte protease inhibitor gene in Ishikawa endometrial epithelial cells involves recruitment of Krüppel-like factor 9/basic transcription element binding protein 1 (BTEB1). Endocrinology 147:1969-1978
33. Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, Bagchi MK, Bagchi IC 2007 Bone morphogenetic 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. J Biol Chem 282:31725-31732
34. 2 regulate interleukin 11 during human endometrial stromal cell decidualization. J Clin Endocrinol Metab 90:3458-3465
35. Glozak MA, Rogers MB 1996 Specific induction of apoptosis in P19 embryonal carcinoma cells by retinoic acid and BMP2 or BMP4. Dev Biol 179:458-470
36. Kawamura C, Kizaki M, Yamato K, Uchida H, Fukuchi Y, Hattori Y, Koseki T, Nishihara T, Ikeda Y 2000 Bone morphogenetic protein-2 induces apoptosis in human myeloma cells with modulation of STAT3. Blood 96:2005-2011
37. Hallahan AR, Pritchard JI, Chandraratna RA, Ellenbogen RG, Geyer JR, Overland RP, Strand AD, Tapscott SJ, Olson JM 2003 BMP-2 mediates retinoid-induced apoptosis in medulloblastoma cells through a paracrine effect. Nat Med 9:1033-1038
38. Zhang S, Fantozzi I, Tigno DD, Yi ES, Platoshyn O, Thistlethwaite PA, Kriett JM, Yung G, Rubin LJ, Yuan JX 2003 Bone morphogenetic proteins induce apoptosis in human pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 285:L740-L754
39. Abrams KL, Xu J, Nativelle-Serpentini C, Dabirshahsahebi S, Rogers MB 2004 An evolutionary and molecular analysis of Bmp2 expression. J Biol Chem 279:15916-15928
40. Xu J, Rogers MB 2007 Modulation of bone morphogenetic (BMP) 2 gene expression by Sp1 transcription factors. Gene 392:221-229
41. Velarde MC, Zeng Z, McQuown JR, Simmen FA, Simmen RCM 2007 Krüppel-like factor 9 is a negative regulator of ligand-dependent estrogen receptor α signaling in Ishikawa endometrial adenocarcinoma cells. Mol Endocrinol 21:2988-3001
42. Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, Nezhat CR, Lessey BA, Giudice LC 2007 Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 148:3814-3826
43. Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE 2000 Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab 85:2897-2902
44. Igarashi TM, Bruner-Tran KL, Yeaman GR, Lessey BA, Edwards DP, Eisenberg E, Osteen KG 2005 Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-ρ-dioxin. Fertil Steril 84:67-74
45. Eaton SA, Funnell AP, Sue N, Nicholas H, Pearson RC, Crossley M 2008 A network of Krüppel-like factors (Klfs). Klf8 is repressed by Klf3 and activated by Klf1 in vivo. J Biol Chem 283:26937-26947
46. Oishi Y, Manabe I, Tobe K, Tsushima K, Shindo T, Fujiu K, Nishimura G, Maemura K, Yamauchi T, Kubota N, Suzuki R, Kitamura T, Akira S, Kadowaki T, Nagai R 2005 Krüppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab 1:27-39
47. Lomberk G, Urrutia R 2005 The family feud: turning off Sp1 by Sp1-like KLF proteins. Biochem J 392:1-11
48. Simmen RCM, Pabona JMP, Velarde MC, Simmons C, Rahal O, Simmen FA 2010 The emerging role of Krüppel-like factors in endocrine-responsive cancers of female reproductive tissues. J Endocrinol 204:223-231
49. Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, Genbecev-Krtolica O, Mavrogianis P, Ferrer K, Kruessel J, Fazleabas AT, Fisher SJ, Giudice LC 2007 Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod 76:102-117