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Division of Reproductive Endocrinology and Infertility, Department of Gynecology and Obstetrics, Stanford University Medical Center, Stanford, California 94305
Address all correspondence and requests for reprints to: Linda Giudice, M.D., Stanford University Medical Center, Department of Gynecology and Obstetrics, Division of Reproductive Endocrinology and Fertility, Boswell A370, 300 Pasteur Drive, Stanford, California 94305.
A prerequisite for implantation in humans is differentiation
(decidualization) of stromal cells in the endometrium, believed to be
stimulated by progesterone (P) and/or cAMP. In the current study,
advances in microarray technology have allowed us to investigate genes
differentially expressed in human endometrial stromal cells
decidualized in vitro in response to P or cAMP, compared to
non-decidualized cells. Endometrial stromal cells were isolated from
endometrial biopsy tissue and cultured without steroid hormones, with 1
µM P (after E2 priming), or 1 mM 8-bromo-cAMP. Total RNA
was isolated and reverse transcribed to synthesize
32P-labeled cDNA probes using primers corresponding to
genes represented on the Clontech Human Atlas cDNA Expression Array.
After hybridization, signals were quantified by phosphor imaging
densitometry and were normalized to GAPDH and ubiquitin. Of the 588
genes screened, marked upregulation was observed of cytokines, growth
factors, nuclear transcription factors, members of the cyclin family,
and mediators of the cAMP signal transduction pathway. Additional mRNAs
expressed unexpectedly and regulated by P and cAMP, include the insulin
receptor, some neurotransmitter receptors, neuromodulators, the FSH
receptor, inhibin/activin ßA subunit, inhibin 
, and
TNF-related apoptosis-inducing ligand (TRAIL). Expression of previously
unrecognized genes regulated in decidualized human endometrial stromal
cells suggests mechanisms not yet appreciated in the endometrium during
decidualization. In addition, marked upregulation of cytokines,
chemokines, growth factors, apoptosis modulators, and their receptors
in decidualized stromal cells supports a major role for paracrine
interactions between the stroma and other endogenous and transient cell
populations within the endometrium and during early pregnancy.
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K. Chobotova, N. Karpovich, J. Carver, S. Manek, W. J. Gullick, D. H. Barlow, and H. J. Mardon Heparin-Binding Epidermal Growth Factor and Its Receptors Mediate Decidualization and Potentiate Survival of Human Endometrial Stromal Cells J. Clin. Endocrinol. Metab., February 1, 2005; 90(2): 913 - 919. [Abstract] [Full Text] [PDF]
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E.S. Hayes, E.C. Curnow, A.O. Trounson, L.A. Danielson, and E.N. Unemori Implantation and Pregnancy Following In Vitro Fertilization and the Effect of Recombinant Human Relaxin Administration in Macaca fascicularis Biol Reprod, November 1, 2004; 71(5): 1591 - 1597. [Abstract] [Full Text] [PDF]
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S. K. Dey, H. Lim, S. K. Das, J. Reese, B. C. Paria, T. Daikoku, and H. Wang Molecular Cues to Implantation Endocr. Rev., June 1, 2004; 25(3): 341 - 373. [Abstract] [Full Text] [PDF]
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 E. P. Tierney, S. Tulac, S.-T. J. Huang, and L. C. Giudice Activation of the protein kinase A pathway in human endometrial stromal cells reveals sequential categorical gene regulation Physiol Genomics, December 16, 2003; 16(1): 47 - 66. [Abstract] [Full Text] [PDF]
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G. A. Johnson, R. C. Burghardt, F. W. Bazer, and T. E. Spencer Osteopontin: Roles in Implantation and Placentation Biol Reprod, November 1, 2003; 69(5): 1458 - 1471. [Abstract] [Full Text] [PDF]
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M. Brasted, C.A. White, T.G. Kennedy, and L.A. Salamonsen Mimicking the Events of Menstruation in the Murine Uterus Biol Reprod, October 1, 2003; 69(4): 1273 - 1280. [Abstract] [Full Text] [PDF]
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R.D. Catalano, A. Yanaihara, A.L. Evans, D. Rocha, A. Prentice, S. Saidi, C.G. Print, D.S. Charnock-Jones, A.M. Sharkey, and S.K. Smith The effect of RU486 on the gene expression profile in an endometrial explant model Mol. Hum. Reprod., August 1, 2003; 9(8): 465 - 473. [Abstract] [Full Text] [PDF]
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G. A. Johnson, R. C. Burghardt, M. M. Joyce, T. E. Spencer, F. W. Bazer, C. Pfarrer, and C. A. Gray Osteopontin Expression in Uterine Stroma Indicates a Decidualization-Like Differentiation During Ovine Pregnancy Biol Reprod, June 1, 2003; 68(6): 1951 - 1958. [Abstract] [Full Text] [PDF]
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 N. Sakai, T. Maruyama, R. Sakurai, H. Masuda, Y. Yamamoto, A. Shimizu, I. Kishi, H. Asada, S. Yamagoe, and Y. Yoshimura Involvement of Histone Acetylation in Ovarian Steroid-induced Decidualization of Human Endometrial Stromal Cells J. Biol. Chem., May 2, 2003; 278(19): 16675 - 16682. [Abstract] [Full Text] [PDF]
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A. Riesewijk, J. Martin, R. van Os, J. A. Horcajadas, J. Polman, A. Pellicer, S. Mosselman, and C. Simon Gene expression profiling of human endometrial receptivity on days LH+2 versus LH+7 by microarray technology Mol. Hum. Reprod., May 1, 2003; 9(5): 253 - 264. [Abstract] [Full Text] [PDF]
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O. Yoshino, Y. Osuga, Y. Hirota, K. Koga, T. Yano, O. Tsutsumi, and Y. Taketani Akt as a possible intracellular mediator for decidualization in human endometrial stromal cells Mol. Hum. Reprod., May 1, 2003; 9(5): 265 - 269. [Abstract] [Full Text] [PDF]
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P. Florio, F. M. Severi, S. Luisi, P. Ciarmela, G. Calonaci, L. Cobellis, and F. Petraglia Endometrial Expression and Secretion of Activin A, But Not Follistatin, Increase in the Secretory Phase of the Menstrual Cycle Reproductive Sciences, May 1, 2003; 10(4): 237 - 243. [Abstract] [PDF]
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F. Dominguez, S. Avila, A. Cervero, J. Martin, A. Pellicer, J. L. Castrillo, and C. Simon A Combined Approach for Gene Discovery Identifies Insulin-Like Growth Factor-Binding Protein-Related Protein 1 as a New Gene Implicated in Human Endometrial Receptivity J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1849 - 1857. [Abstract] [Full Text] [PDF]
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C. Richard, J. Gao, N. Brown, and J. Reese Aquaporin Water Channel Genes Are Differentially Expressed and Regulated by Ovarian Steroids during the Periimplantation Period in the Mouse Endocrinology, April 1, 2003; 144(4): 1533 - 1541. [Abstract] [Full Text] [PDF]
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Y. Yamamoto, T. Maruyama, N. Sakai, R. Sakurai, A. Shimizu, T. Hamatani, H. Masuda, H. Uchida, H. Sabe, and Y. Yoshimura Expression and subcellular distribution of the active form of c-Src tyrosine kinase in differentiating human endometrial stromal cells Mol. Hum. Reprod., December 1, 2002; 8(12): 1117 - 1124. [Abstract] [Full Text] [PDF]
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G.C. Weston, I. Haviv, and P.A.W. Rogers Microarray analysis of VEGF-responsive genes in myometrial endothelial cells Mol. Hum. Reprod., September 1, 2002; 8(9): 855 - 863. [Abstract] [Full Text] [PDF]
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D. D. Carson, E. Lagow, A. Thathiah, R. Al-Shami, M. C. Farach-Carson, M. Vernon, L. Yuan, M. A. Fritz, and B. Lessey Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening Mol. Hum. Reprod., September 1, 2002; 8(9): 871 - 879. [Abstract] [Full Text] [PDF]
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N. Sugino, A. Karube-Harada, A. Sakata, S. Takiguchi, and H. Kato Nuclear Factor-{kappa}B Is Required for Tumor Necrosis Factor-{alpha}-Induced Manganese Superoxide Dismutase Expression in Human Endometrial Stromal Cells J. Clin. Endocrinol. Metab., August 1, 2002; 87(8): 3845 - 3850. [Abstract] [Full Text] [PDF]
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E. Dimitriadis, L. Robb, and L.A. Salamonsen Interleukin 11 advances progesterone-induced decidualization of human endometrial stromal cells Mol. Hum. Reprod., July 1, 2002; 8(7): 636 - 643. [Abstract] [Full Text] [PDF]
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T. Liu and T. F. Ogle Signal Transducer and Activator of Transcription 3 Is Expressed in the Decidualized Mesometrium of Pregnancy and Associates with the Progesterone Receptor Through Protein-Protein Interactions Biol Reprod, July 1, 2002; 67(1): 114 - 118. [Abstract] [Full Text] [PDF]
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L. C. Kao, S. Tulac, S. Lobo, B. Imani, J. P. Yang, A. Germeyer, K. Osteen, R. N. Taylor, B. A. Lessey, and L. C. Giudice Global Gene Profiling in Human Endometrium during the Window of Implantation Endocrinology, June 1, 2002; 143(6): 2119 - 2138. [Abstract] [Full Text] [PDF]
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H.-W. Chen, J. J.W. Chen, C.-R. Tzeng, H.-N. Li, S.-J. Chang, Y.-F. Cheng, C.-W. Chang, R.-S. Wang, P.-C. Yang, and Y.-T. Lee Global analysis of differentially expressed genes in early gestational decidua and chorionic villi using a 9600 human cDNA microarray Mol. Hum. Reprod., May 1, 2002; 8(5): 475 - 484. [Abstract] [Full Text] [PDF]
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F. M. Reis, D. D'Antona, and F. Petraglia Predictive Value of Hormone Measurements in Maternal and Fetal Complications of Pregnancy Endocr. Rev., April 1, 2002; 23(2): 230 - 257. [Abstract] [Full Text] [PDF]
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J. Reese, S. K. Das, B. C. Paria, H. Lim, H. Song, H. Matsumoto, K. L. Knudtson, R. N. DuBois, and S. K. Dey Global Gene Expression Analysis to Identify Molecular Markers of Uterine Receptivity and Embryo Implantation J. Biol. Chem., November 16, 2001; 276(47): 44137 - 44145. [Abstract] [Full Text] [PDF]
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M. Hemberger, J. C. Cross, H.-H. Ropers, H. Lehrach, R. Fundele, and H. Himmelbauer UniGene cDNA array-based monitoring of transcriptome changes during mouse placental development PNAS, November 6, 2001; 98(23): 13126 - 13131. [Abstract] [Full Text] [PDF]
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A. Karube-Harada, N. Sugino, S. Kashida, S. Takiguchi, H. Takayama, Y. Yamagata, Y. Nakamura, and H. Kato Induction of manganese superoxide dismutase by tumour necrosis factor-{alpha} in human endometrial stromal cells Mol. Hum. Reprod., November 1, 2001; 7(11): 1065 - 1072. [Abstract] [Full Text] [PDF]
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 S. Shah, L. Nathan, R. Singh, Y. S. Fu, and G. Chaudhuri E2 and not P4 increases NO release from NANC nerves of the gastrointestinal tract: implications in pregnancy Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2001; 280(5): R1546 - R1554. [Abstract] [Full Text] [PDF]
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A. K. BRAR, S. HANDWERGER, C. A. KESSLER, and B. J. ARONOW Gene induction and categorical reprogramming during in vitro human endometrial fibroblast decidualization Physiol Genomics, December 21, 2001; 7(2): 135 - 148. [Abstract] [Full Text] [PDF]
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