Proteomic analysis identifies immunophilin FK506 binding protein 4 (FKBP52) as a downstream target of Hoxa10 in the periimplantation mouse uterus

Molecular Endocrinology

Volumn 19, Issue 3, 2005, Pages 683-697

  Daikoku, Takiko ^a   Tranguch, Susanne ^a   Friedman, David B ^b   Das, Sanjoy K ^a   Smith, David F ^c   Dey, Sudhansu K ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; ESTROGEN; FK 506 BINDING PROTEIN 4; HORMONE RECEPTOR; IMMUNOPHILIN; INITIATION FACTOR 4E BINDING PROTEIN; PROGESTERONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA10; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL SPECIFICITY; CONTROLLED STUDY; FEMALE; FEMALE INFERTILITY; GEL ELECTROPHORESIS; GENETIC ANALYSIS; HUMAN; IMPLANTATION; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; STROMA CELL; UTERUS; UTERUS CAVITY;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DATABASES; DESMIN; DOWN-REGULATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ESTROGENS; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INFERTILITY, FEMALE; MASS SPECTROMETRY; MICE; MICE, TRANSGENIC; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; PROGESTERONE; PROTEIN BINDING; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STROMAL CELLS; TACROLIMUS BINDING PROTEINS; TIME FACTORS; UP-REGULATION; UTERUS; VIMENTIN;

EID: 14844299827     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2004-0332     Document Type: Article

References (45)

1. Krumlauf R 1994 Hox genes in vertebrate development. Cell 78:191-201
2. McGinnis W, Krumlauf R 1992 Homeobox genes and axial patterning. Cell 68:283-302
3. Benson GV, Nguyen TH, Maas RL 1995 The expression pattern of the murine Hoxa-10 gene and the sequence recognition of its homeodomain reveal specific properties of abdominal B-like genes. Mol Cell Biol 15: 1591-1601
4. Dolle P, Izpisua-Belmonte JC, Brown JM, Tickle C, Duboule D 1991 HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev 5:1767-7
5. Izpisua-Belmonte JC, Falkenstein H, Dolle P, Renucci A, Duboule D 1991 Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J 10:2279-2289
6. Rijli FM, Matyas R, Pellegrini M, Dierich A, Gruss P, Dolle P, Chambon P 1995 Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc Natl Acad Sci USA 92:8185-8189
7. Satokata I, Benson G, Maas R 1995 Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 374:460-463
8. Benson GV, Lim H, Paria BC, Satokata I, Dey SK, Maas RL 1996 Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 122:2687-2696
9. Lim H, Ma L, Ma WG, Maas RL, Dey SK 1999 Hoxa-10 regulates uterine stromal cell responsiveness to progesterone during implantation and decidualization in the mouse. Mol Endocrinol 13:1005-1017
10. Huet-Hudson YM, Andrews GK, Dey SK 1989 Cell type-specific localization of c-myc protein in the mouse uterus: modulation by steroid hormones and analysis of the periimplantation period. Endocrinology 125: 1683-1690
11. Ma L, Benson GV, Lim H, Dey SK, Maas RL 1998 Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in mullerian duct by the synthetic estrogen diethylstilbestrol (DES). Dev Biol 197:141-154
12. Gade D, Thiermann J, Markowsky D, Rabus R 2003 Evaluation of two-dimensional difference gel electrophoresis for protein profiling. Soluble proteins of the marine bacterium Pirellula sp. strain 1. J Mol Microbiol Biotechnol 5:240-251
13. Alban A, David SO, Bjorkesten L, Andersson C, Sloge E, Lewis S, Currie I 2003 A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3:36-44
14. Tai PK, Maeda Y, Nakao K, Wakim NG, Duhring JL, Faber LE 1986 A 59-kilodalton protein associated with progestin, estrogen, androgen, and glucocorticoid receptors. Biochemistry 25:5269-5275
15. Barent RL, Nair SC, Carr DC, Ruan Y, Rimerman RA, Fulton J, Zhang Y, Smith DF 1998 Analysis of FKBP51/ FKBP52 chimeras and mutants for Hsp90 binding and association with progesterone receptor complexes. Mol Endocrinol 12:342-354
16. Finn CA, Porter DG 1975 The uterus: cells and tissues of the endometrium. Acton, MA: Publishing Sciences Group, Inc.
17. Kover K, Liang L, Andrews GK, Dey SK 1995 Differential expression and regulation of cytokine genes in the mouse uterus. Endocrinology 136:1666-1673
18. Tan Y, Li M, Cox S, Davis MK, Tawfik O, Paria BC, Das SK 2004 HB-EGF directs stromal cell polyploidy and decidualization via cyclin D3 during implantation. Dev Biol 265:181-195
19. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK 1997 Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91: 197-208
20. Glasser SR, Julian J 1986 Intermediate filament protein as a marker of uterine stromal cell decidualization. Biol Reprod 35:463-474
21. Piva M, Flieger O, Rider V 1996 Growth factor control of cultured rat uterine stromal cell proliferation is progesterone dependent. Biol Reprod 55:1333-1342
22. Smith DF, Baggenstoss BA, Marion TN, Rimerman RA 1993 Two FKBP-related proteins are associated with progesterone receptor complexes. J Biol Chem 268: 18365-18371
23. Riggs DL, Roberts PJ, Chirillo SC, Cheung-Flynn J, Prapapanich V, Ratajczak T, Gaber R, Picard D, Smith DF 2003 The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J 22:1158-1167
24. Pratt WB, Galigniana MD, Harrell JM, DeFranco DB 2004 Role of hsp90 and the hsp90-binding immunophilins in signalling protein movement. Cell Signal 16:857-872
25. Quo JZ, Gorski J 1988 Estrogen effects on histone messenger ribonucleic acid levels in the rat uterus. Mol Endocrinol 2:693-700
26. Wang XN, Das SK, Damm D, Klagsbrun M, Abraham JA, Dey SK 1994 Differential regulation of heparin-binding epidermal growth factor-like growth factor in the adult ovariectomized mouse uterus by progesterone and estrogen. Endocrinology 135:1264-1271
27. Das SK, Wang XN, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK 1994 Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120: 1071-1083
28. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H 2004 Molecular cues to implantation. Endocr Rev 25:341-373
29. Pratt WB, Toft DO 2003 Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood) 228:111-133
30. Smith D 2004 Tetratricopeptide repeat cochaperones in steroid receptor complexes. Cell Stress Chap 9:109-121
31. Baughman G, Harrigan MT, Campbell NF, Nurrish SJ, Bourgeois S 1991 Genes newly identified as regulated by glucocorticoids in murine thymocytes. Mol Endocrinol 5:637-644
32. Hubler TR, Denny WB, Valentine DL, Cheung-Flynn J, Smith DF, Scammell JG 2003 The FK506-binding immunophilin FKBP51 is transcriptionally regulated by progestin and attenuates progestin responsiveness. Endocrinology 144:2380-2387
33. Kester HA, van der Leede BM, van der Saag PT, van der Burg B 1997 Novel progesterone target genes identified by an improved differential display technique suggest that progestin-induced growth inhibition of breast cancer cells coincides with enhancement of differentiation. J Biol Chem 272:16637-16643
34. Scammell JG, Denny WB, Valentine DL, Smith DF 2001 Overexpression of the FK506-binding immunophiiin FKBP51 is the common cause of glucocorticoid resistance in three New World primates. Gen Comp Endocrinol 124:152-165
35. Reynolds PD, Ruan Y, Smith DF, Scammell JG 1999 Glucocorticoid resistance in the squirrel monkey is associated with overexpression of the immunophilin FKBP51. J Clin Endocrinol Metab 84:663-669
36. Yao MW, Lim H, Schust DJ, Choe SE, Farago A, Ding Y, Michaud S, Church GM, Maas RL 2003 Gene expression profiling reveals progesterone-mediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. Mol Endocrinol 17:610-627
37. Tan J, Paria BC, Dey SK, Das SK 1999 Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140:5310-5321
38. Kumar P, Mark PJ, Ward BK, Minchin RF, Ratajczak T 2001 Estradiol-regulated expression of the immunophilins cyclophilin 40 and FKBP52 in MCF-7 breast cancer cells. Biochem Biophys Res Commun 284:219-225
39. Daikoku T, Song H, Quo Y, Riesewijk A, Mosselman S, Das SK, Dey SK 2004 Uterine Msx-1 and Wnt4 signaling becomes aberrant in mice with the loss of leukemia inhibitory factor or Hoxa-10: evidence for a novel cytokine-homeobox- Wnt signaling in implantation. Mol Endocrinol 18:1238-1250
40. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O 1993 Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90:11162-11166
41. 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
42. Friedman DB, Hill S, Keller JW, Merchant NB, Levy SE, Coffey RJ, Caprioli RM 2004 Proteome analysis of human colon cancer by two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics 4:793-811
43. Tonge R, Shaw J, Middleton B, Rowlinson r, Rayner S, Young J, Pognan F, Hawkins E, Currie I, Davison M 2001 Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 1:377-396
44. Unlu M, Morgan ME, Minden JS 1997 Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071-2077
45. Gharbi S, Gaffney P, Yang A, Zvelebil MJ, Cramer R, Waterfield MD, Timms JF 2002 Evaluation of two-dimensional differential gel electrophoresis for proteomic expression analysis of a model breast cancer cell system. Mol Cell Proteomics 1:91-98