Disruption of gap junctions reduces biomarkers of decidualization and angiogenesis and increases inflammatory mediators in human endometrial stromal cell cultures

Molecular and Cellular Endocrinology

Volumn 344, Issue 1-2, 2011, Pages 25-34

  Yu, Jie ^a   Wu, Juanjuan ^a   Bagchi, Indrani C ^b   Bagchi, Milan K ^c   Sidell, Neil ^a   Taylor, Robert N ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Connexin; Gap junction intercellular communication; Interleukin 6; Prolactin; VEGF

Indexed keywords

CONNEXIN 43; CYCLIC AMP; ESTRADIOL; GAP JUNCTION PROTEIN; INTERLEUKIN 6; PROGESTERONE; PROLACTIN; SHORT HAIRPIN RNA; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DECIDUALIZATION; ENDOMETRIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIOID CELL; FEMALE; GAP JUNCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LAPAROSCOPY; MENSTRUAL CYCLE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA CELL; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL MARKERS; BUCLADESINE; CELL DIFFERENTIATION; CELLS, CULTURED; CONNEXIN 43; DECIDUA; ESTRADIOL; FEMALE; GAP JUNCTIONS; GLYCYRRHETINIC ACID; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; NEOVASCULARIZATION, PHYSIOLOGIC; OCTANOLS; PROGESTERONE; RNA INTERFERENCE; STROMAL CELLS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84860390273     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.04.011     Document Type: Article

References (39)

1. Alam S.M., Konno T., Dai G., Lu L., Wang D., Dunmore J.H., Godwin A.R., Soares M.J. A uterine decidual cell cytokine ensures pregnancy-dependent adaptations to a physiological stressor. Development 2007, 134:407-415.
2. Argraves W.S., Drake C.J. Genes critical to vasculogenesis as defined by systematic analysis of vascular defects in knockout mice. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2005, 286:875-884.
3. Bao L., Tessier C., Prigent-Tessier A., Li F., Buzzio O.L., Callegari E.A., Horseman N.D., Gibori G. Decidual prolactin silences the expression of genes detrimental to pregnancy. Endocrinology 2007, 148:2326-2334.
4. Chaouat G. The Th1/Th2 paradigm: still important in pregnancy?. Semin. Immunopathol. 2007, 29:95-113.
5. Clapp C., López-Gómez F.J., Nava G., Corbacho A., Torner L., Macotela Y., Dueñas Z., Ochoa A., Noris G., Acosta E., Garay E., Martínez de la Escalera G. Expression of prolactin mRNA and of prolactin-like proteins in endothelial cells: evidence for autocrine effects. J. Endocrinol. 1998, 158:137-144.
6. Contreras J.E., Sánchez H.A., Eugenin E.A., Speidel D., Theis M., Willecke K., Bukauskas F.F., Bennett M.V., Sáez J.C. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:495-500.
7. Daly D.C., Maslar I.A., Riddick D.H. Prolactin production during in vitro decidualization of proliferative endometrium. Am. J. Obstet. Gynecol. 1983, 145:672-678.
8. Fazleabas A.T., Kim J.J., Strakova Z. Implantation: embryonic signals and the modulation of the uterine environment - a review. Placenta 2004, 25(Suppl. A):S26-S31.
9. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442.
10. 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.
11. Grümmer R., Reuss B., Winterhager E. Expression pattern of different gap junction connexins is related to embryo implantation. Int. J. Dev. Biol. 1996, 40:361-367.
12. Jahn E., Classen-Linke I., Kusche M., Beier H.M., Traub O., Grümmer R., Winterhager E. Expression of gap junction connexins in the human endometrium throughout the menstrual cycle. Hum. Reprod. 1995, 10:2666-2670.
13. Jauniaux E., Poston L., Burton G.J. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum. Reprod. Update 2006, 12:747-755.
14. Kim J., Sato M., Li Q., Lydon J.P., Demayo F.J., Bagchi I.C., Bagchi M.K. Peroxisome proliferator-activated receptor gamma is a target of progesterone regulation in the preovulatory follicles and controls ovulation in mice. Mol. Cell. Biol. 2008, 28:1770-1782.
15. Koistinen R., Kalkkinen N., Huhtala M.L., Seppälä M., Bohn H., Rutanen E.M. Placental protein 12 is a decidual protein that binds somatomedin and has an identical N-terminal amino acid sequence with somatomedin-binding protein from human amniotic fluid. Endocrinology 1986, 118:1375-1378.
16. Krikun G., Mor G., Alvero A., Guller S., Schatz F., Sapi E., Rahman M., Caze R., Qumsiyeh M., Lockwood C.J. A novel immortalized human endometrial stromal cell line with normal progestational response. Endocrinology 2004, 145:2291-2296.
17. Lawn A.M., Wilson E.W., Finn C.A. The ultrastructure of human decidual and predecidual cells. J. Reprod. Fertil. 1971, 26:85-90.
18. Laws M.J., Taylor R.N., Sidell N., DeMayo F.J., Lydon J.P., Gutstein D.E., Bagchi M.K., Bagchi I.C. Gap junction communication between uterine stromal cells plays a critical role in pregnancy-associated neovascularization and embryo survival. Development 2008, 135:2659-2668.
19. Levine R.J., Maynard S.E., Qian C., Lim K.H., England L.J., Yu K.F., Schisterman E.F., Thadhani R., Sachs B.P., Epstein F.H., Sibai B.M., Sukhatme V.P., Karumanchi S.A. Circulating angiogenic factors and the risk of preeclampsia. New Engl. J. Med. 2004, 350:672-683.
20. Lockwood C.J., Yen C.F., Basar M., Kayisli U.A., Martel M., Buhimschi I., Buhimschi C., Huang S.J., Krikun G., Schatz F. Preeclampsia-related inflammatory cytokines regulate interleukin-6 expression in human decidual cells. Am. J. Pathol. 2008, 172:1571-1579.
21. Mantena S.R., Kannan A., Cheon Y.P., Li Q., Johnson P.F., Bagchi I.C., Bagchi M.K. C/EBP beta is a critical mediator of steroid hormone-regulated cell proliferation and differentiation in the uterine epithelium and stroma. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1870-1875.
22. Mueller M.D., Vigne J.L., Minchenko A., Lebovic D.I., Leitman D.C., Taylor R.N. Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:10972-10977.
23. Orlando-Mathur C.E., Bechberger J.F., Goldberg G.S., Naus C.C., Kidder G.M., Kennedy T.G. Rat endometrial stromal cells express the gap junction genes connexins 26 and 43 and form functional gap junctions during in vitro decidualization. Biol. Reprod. 1996, 54:905-913.
24. Pauken C.M., Lo C.W. Nonoverlapping expression of Cx43 and Cx26 in the mouse placenta and decidua: a pattern of gap junction gene expression differing from that in the rat. Mol. Reprod. Dev. 1995, 41:195-203.
25. Peeters L.L., Vigne J.L., Tee M.K., Zhao D., Waite L.L., Taylor R.N. PPAR gamma represses VEGF expression in human endometrial cells: implications for uterine angiogenesis. Angiogenesis 2005, 8:373-379.
26. Piao M., Mori D., Satoh T., Sugita Y., Tokunaga O. Inhibition of endothelial cell proliferation, in vitro angiogenesis, and the down-regulation of cell adhesion-related genes by genistein. Combined with a cDNA microarray analysis. Endothelium 2006, 13:249-266.
27. Ramathal C.Y., Bagchi I.C., Taylor R.N., Bagchi M.K. Endometrial decidualization: of mice and men. Semin. Reprod. Med. 2010, 28:17-26.
28. Ryan I.P., Schriock E.D., Taylor R.N. Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro. J. Clin. Endocrinol. Metab. 1994, 78:642-649.
29. Saito S. Cytokine network at the feto-maternal interface. J. Reprod. Immunol. 2000, 47:87-103.
30. Salamonsen L.A., Dimitriadis E., Robb L. Cytokines in implantation. Semin. Reprod. Med. 2000, 18:299-310.
31. Schiller P.C., D'Ippolito G., Balkan W., Roos B.A., Howard G.A. Gap-junctional communication is required for the maturation process of osteoblastic cells in culture. Bone 2001, 28:362-369.
32. Sidell N., Feng Y., Hao L., Wu J., Yu J., Kane M.A., Napoli J.L., Taylor R.N. Retinoic acid is a cofactor for translational regulation of vascular endothelial growth factor in human endometrial stromal cells. Mol. Endocrinol. 2010, 24:148-160.
33. Söhl G., Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun. Adhes. 2003, 10:173-180.
34. Struman I., Bentzien F., Lee H., Mainfroid V., D'Angelo G., Goffin V., Weiner R.I., Martial J.A. Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1246-1251.
35. Tabibzadeh S., Kong Q.F., Babaknia A., May L.T. Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum. Reprod. 1995, 10:2793-2799.
36. Tanmahasamut P., Sidell N. Up-regulation of gap junctional intercellular communication and connexin43 expression by retinoic acid in human endometrial stromal cells. J. Clin. Endocrinol. Metab. 2005, 90:4151-4156.
37. Taylor R.N., Grimwood J., Taylor R.S., McMaster M.T., Fisher S.J., North R.A. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am. J. Obstet. Gynecol. 2003, 188:177-182.
38. Yamasaki H., Krutovskikh V., Mesnil M., Tanaka T., Zaidan-Dagli M.L., Omori Y. Role of connexin (gap junction) genes in cell growth control and carcinogenesis. C. R. Acad. Sci. III 1999, 322:151-159.
39. Zenclussen A.C., Blois S., Stumpo R., Olmos S., Arias K., Malan Borel I., Roux M.E., Margni R.A. Murine abortion is associated with enhanced interleukin-6 levels at the feto-maternal interface. Cytokine 2003, 24:150-160.