Fertility and Sterility
Volume 91, Issue 4 , Pages 1042-1049.e9 , April 2009

Endometrial biopsy-induced gene modulation: first evidence for the expression of bladder-transmembranal uroplakin Ib in human endometrium

  • Yael Kalma, Ph.D.

      Affiliations

    • Department of Biological Regulation, Weizmann Institute of Science, Rehovot, Israel
    • ,
  • Irit Granot, Ph.D.

      Affiliations

    • IVF Unit, Department of Obstetrics and Gynecology, Kaplan Medical Center (Affiliated with the Medical School of the Hebrew University and Hadassah, Jerusalem), Rehovot, Israel
    • Corresponding Author InformationReprint requests: Irit Granot, Ph.D., IVF Unit, Department of Obstetrics and Gynecology, Kaplan Medical Center, Rehovot, 76100, Israel (FAX: 972-8-9441-217).
    • ,
  • Yulia Gnainsky, Ph.D.

      Affiliations

    • Department of Biological Regulation, Weizmann Institute of Science, Rehovot, Israel
    • ,
  • Yuval Or, M.D.

      Affiliations

    • IVF Unit, Department of Obstetrics and Gynecology, Kaplan Medical Center (Affiliated with the Medical School of the Hebrew University and Hadassah, Jerusalem), Rehovot, Israel
    • ,
  • Bernard Czernobilsky, M.D.

      Affiliations

    • Patho-Lab Diagnostics, Ness-Ziona, Israel
    • ,
  • Nava Dekel, Ph.D.

      Affiliations

    • Department of Biological Regulation, Weizmann Institute of Science, Rehovot, Israel
    • ,
  • Amihai Barash, M.D.

      Affiliations

    • IVF Unit, Department of Obstetrics and Gynecology, Kaplan Medical Center (Affiliated with the Medical School of the Hebrew University and Hadassah, Jerusalem), Rehovot, Israel

Received 26 August 2007 ,Revised 11 January 2008 ,Accepted 11 January 2008.

References 

  1. Wang H, Dey SK. Road map to embryo implantation: clues from mouse models. Nat Rev Gen. 2006;7:185–199
  2. Dunn CL, Kelly RW, Critchley HO. Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod Biomed Online. 2003;7:151–161
  3. Paria BC, Reese J, Das SK, Dey SK. Deciphering the cross-talk of implantation: advances and challenges. Science. 2002;296:2185–2188
  4. Dimitriadis E, Salmonsen LA, Robb L. Expression of interleukin-11 during the human menstrual cycle: coincidence with stromal cell decidualization and relationship to leukemia inhibitory factor and prolactin. Mol Hum Reprod. 2000;6:907–914
  5. Cork BA, Li TC, Warren MA, Laird SM. Interleukin-11 (IL-11) in human endometrium: expression throughout the menstrual cycle and the effects of cytokines on endometrial IL-11 production in vitro. J Reprod Immunol. 2001;50:3–17
  6. Dimitriadis E, Stoikos C, Baca M, Fairlie WD, McCoubrie JE, Salmonsen LA. Relaxin and prostaglandin E(2) regulate interleukin 11 during human endometrial stromal cell decidualization. J Clin Endocrinol Metab. 2005;90:3458–3465
  7. Akbas GE, Taylor HS. HOXC and HOXD gene expression in human endometrium: lack of redundancy with HOXA paralogs. Biol Reprod. 2004;70:39–45
  8. Popovici RM, Kao LC, Giudice LC. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology. 2000;141:3510–3513
  9. Carson DD, Lagow E, Thathiah A, Al-Shami R, Farach-Carson MC, Vernon M, et al. 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. 2002;8:871–879
  10. Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, et al. Global gene profiling in human endometrium during the window of implantation. Endocrinology. 2002;143:2119–2138
  11. Dominguez F, Remohi J, Pellocer A, Simon C. Human endometrial receptivity: a genomic approach. Reprod Biomed Online. 2003;6:332–338
  12. Giudice LC. Microarray expression profiling reveals candidate genes for human uterine receptivity. Am J Pharmacogenomics. 2004;4:299–312
  13. Riesewijk A, Martin J, van Os R, Horcajadas JA, Polman J, Pellicer A, et al. Gene expression profiling of human endometrial receptivity on days LH+2 versus LH+7 by microarray technology. Mol Hum Reprod. 2003;9:253–264
  14. Stewart CL, Kasper P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, et al. Blastocyst implantation depends on maternal expression of leukemia inhibitory factor. Nature. 1992;3(359):76–79
  15. Satokata I, Benson G, Maas R. Sexually dimorphic sterility phenotypes in Hoxa10 deficient mice. Nature. 1995;37:460–463
  16. Benson GV, Lim H, Paria BC, Satokata I, Dey SK, Maas RL. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development. 1996;122:2687–2696
  17. Nie G, Li Y, Wang M, Liu YX, Findlay JK, Salmonsen LA. Inhibiting uterine PC6 blocks embryo implantation: an obligatory role for a proprotein convertase in fertility. Biol Reprod. 2005;72:1029–1036
  18. Dimitriadis E, Stoikos C, Stafford-Bell M, Clark I, Pavia P, Kovacs , et al. Interleukin-11, IL-11 receptor alpha and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J Reprod Immunol. 2006;69:53–64
  19. Mikolajczyk M, Wirstlein P, Skrzypczak J. Leukemia inhibitory factor and interleukin 11 levels in uterine flushings of infertile patients with endometriosis. Hum Reprod. 2006;21:3054–3058
  20. Barash A, Dekel N, Fieldust S, Segal I, Schechtman E, Granot I. Local injury of the endometrium doubles the incidence of successful pregnancies in patients undergoing in-vitro fertilization. Fertil Steril. 2003;79:1317–1322
  21. Raziel A, Schachter M, Strassburger D, Berno O, Ron-El R, Friedler S. Favorable influence of local injury to the endometrium in intracytoplasmic sperm injection patients with high-order implantation failure. Fertil Steril. 2007;87:198–201
  22. Zhou L, Li R, Wang R, Huang HX, Zhong K. Local injury to the endometrium in controlled ovarian hyperstimulation cycles improves implantation rates. Fertil Steril. Published online 6 August 2007. doi: 10.1016/j.fertnstert.2007.05.064. [E-pub ahead of print].
  23. Wu XR, Manabe M, Yu J, Sun TT. Large scale purification and immunolocalization of bovine uroplakins I, II, and III. Molecular markers of urothelial differentiation. J Biol Chem. 1990;265:19170–19179
  24. Yu J, Lin JH, Wu XR, Sun TT. Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J Cell Biol. 1994;125:171–182
  25. Granot I, Dekel N, Bechor E, Segal I, Fieldust S, Barash A. Temporal analysis of connexin43, protein and gene expression, throughout the menstrual cycle in human endometrium. Fertil Steril. 2000;73:381–386
  26. Horne AW, Lalani EN, Margara RA, Ryder TA, Mobberley MA, White JO. The expression pattern of MUC1 glycoforms and other biomarkers of endometrial receptivity in fertile and infertile women. Mol Reprod Dev. 2005;72:216–229
  27. Dey SK. Fatty link to fertility. Nature. 2005;435:34–35
  28. Hicks RM, Ketterer B. Hexagonal lattice of subunits in the thick luminal membrane of the rat urinary bladder. Nature. 1969;224:1304–1305
  29. Vergara JA, Longley W, Robertson JD. A hexagonal arrangement of subunits in membrane of mouse urinary bladder. J Mol Biol. 1969;46:593–596
  30. Brisson A, Wade RH. Three-dimensional structure of luminal plasma membrane protein from urinary bladder. J Mol Biol. 1983;166:21–36
  31. Negrete HO, Rivers RL, Goughs AH, Colombini M, Zeidel ML. Individual leaflets of a membrane bilayer can independently regulate permeability. J Biol Chem. 1996;271:11627–11630
  32. Lewis SA. Everything you wanted to know about the bladder epithelium but were afraid to ask. Am J Physiol. 2000;278:F867–F874
  33. Apodaca G. The uroepithelium: not just a passive barrier. Traffic. 2004;5:117–128
  34. Helmer ME. Transpanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Ann Rev Cell Dev Biol. 2003;19:397–422
  35. Wu XR, Medina JJ, Sun TT. Selective interactions of UPIa and UPIb, Two members of the transmembrane 4 superfamily, with distinct single transmembrane-domained proteins in differentiated urothelial cells. J Biol Chem. 1995;270:29752–29759
  36. Mahbub Hasan AKM, Sato K, Sakakibara K, Ou Z, Iwasaki T, Ueda Y, et al. Uroplakin III, a novel Src subutrate in Xenopus egg rafts, is a target for sperm protease essential for fertilization. Dev Biol. 2005;286:483–492
  37. Sakakibara K, Sato K, Yoshino K, Oshiro N, Hirahara S, Mahbub Hasan AKM, et al. Molecular identification and characterization of Xenopus egg uroplakin III, an egg raft-associated transmembrane protein that is tyrosine-phosphorylated upon fertilization. J Biol Chem. 2005;280:15029–15037
  38. Mahbub Hasan AKM, Ou Z, Sakakibara K, Hirahara S, Iwasaki T, Sato K, et al. Characterization of Xenopus egg membrane microdomains containing uroplakin Ib/III complex: roles of their molecular interactions for subcellular localization and signal transduction. Genes to Cells. 2007;12:251–267
  39. Tu L, Sun TT, Kreibich G. Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol Biol Cell. 2002;13:4221–4230
  40. Horne AW, Lalani EN, Margara RA, White JO. The effect of sex steroids hormones and interleuklin-1-beta on MUC1 expression in endometrial epithelial cell lines. Reproduction. 2006;131:733–742
  41. Aplin JD. Adhesion molecules in implantation. Reproduction. 1997;2:84–93
  42. Carson DD, Julian J, Lessey BA, Prakobphol A, Fisher SJ. MUC1 is a scaffold for selectin ligands in the human uterus. Front Biosci. 2006;11:2903–2908
  43. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniax E. Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab. 2002;87:2954–2959

 Yael Kalma and Irit Granot contributed equally to this paper.

 This work was supported by the Dwek Fund for Biomedical Research.

 All authors have nothing to disclose.

PII: S0015-0282(08)00138-6

doi: 10.1016/j.fertnstert.2008.01.043

Fertility and Sterility
Volume 91, Issue 4 , Pages 1042-1049.e9 , April 2009

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