Reduced connexin 43 in eutopic endometrium and cultured endometrial stromal cells from subjects with endometriosis

Molecular Human Reproduction

Volumn 20, Issue 3, 2014, Pages 260-270

  Yu, Jie ^a,b   Boicea, Anisoara ^c   Barrett, Kara L ^b   James, Christopher O ^b   Bagchi, Indrani C ^d   Bagchi, Milan K ^e   Nezhat, Ceana ^c   Sidell, Neil ^b   Taylor, Robert N ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Nezhat Medical Center   (United States)

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

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

Author keywords

Endometriosis; Gap junctions; Gene expression; Immunohistochemistry; Western blot

Indexed keywords

ENDOMETRIOSIS; GAP JUNCTIONS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; WESTERN BLOT;

ACTINS; CELL COMMUNICATION; CELL DIFFERENTIATION; CONNEXIN 43; CONNEXINS; ENDOMETRIOSIS; ENDOMETRIUM; ESTRADIOL; FEMALE; GAP JUNCTIONS; GENE EXPRESSION; HUMANS; PRIMARY CELL CULTURE; PROGESTERONE; RNA, MESSENGER; STROMAL CELLS;

EID: 84894356581     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat087     Document Type: Article

References (51)

1. Adamson GD, Kennedy S, Hummelshoj L. Creating solutions in endometriosis: global collaboration through the World Endometriosis Foundation. J Endometr 2010;2:3-6.
2. Aghajanova L, Hamilton A, Kwintkiewicz J, VoKC, Giudice LC. Steroidogenic enzyme and key decidualization marker dysregulation in endometrial stromal cells from women with versus without endometriosis. Biol Reprod 2009a;80:105-114.
3. Aghajanova L, Velarde MC, Giudice LC. The progesterone receptor coactivator Hic-5 is involved in the pathophysiology of endometriosis. Endocrinology 2009b;150:3863-3870.
4. American Society for Reproductive Medicine. Revised ASRM classification for endometriosis: 1996. Fertil Steril 1997;67:817-821.
5. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril 2002;77:1148-1155.
6. Brosens JJ, Gellersen B. Death or survival-progesterone-dependent cell fate decisions in the human endometrial stroma. J Mol Endocrinol 2006; 36:389-398.
7. Buck Louis GM, Hediger ML, Peterson CM, Croughan M, Sundaram R, Stanford J, Chen Z, Fujimoto VY, Varner MW, Trumble A et al. Incidence of endometriosis by study population and diagnostic method: the ENDO study. Fertil Steril 2011;96:360-365.
8. Bulun SE, Cheng YH, Pavone ME, Xue Q, Attar E, Trukhacheva E, Tokunaga H, Utsunomiya H, Yin P, Luo X et al. Estrogen receptor-beta, estrogen receptor-alpha, and progesterone resistance in endometriosis. Semin Reprod Med 2010;28:36-43.
9. Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, Nezhat CR, Lessey BA, Giudice LC. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007;148:3814-3826.
10. Cheesman KL, Cheesman SD, Chatterton RT Jr, Cohen MR. Alterations in progesterone metabolism and luteal function in infertile women with endometriosis. Fertil Steril 1983;40:590-595.
11. Darr EA, PatelAD, YuG, Komorowski Z, McCormick S, Tiwari R, Schantz SP, Geliebter J. Reduced Cx43 gap junction plaque expression differentiates thyroid carcinomas from benign disease. Arch Otolaryngol Head Neck Surg 2011;137:1161-1165.
12. de Ziegler D, Borghese B, Chapron C. Endometriosis and infertility: pathophysiology and management. Lancet 2010;376:730-738.
13. D'HoogheTM, Debrock S, Hill JA, MeulemanC. Endometriosis and subfertility: is the relationship resolved? Semin Reprod Med 2003;21:243-254.
14. Donaghay M, Lessey BA. Uterine receptivity: alterations associated with benign gynecological disease. Semin Reprod Med 2007;25:461-475.
15. Eyster KM, Klinkova O, Kennedy V, Hansen KA. Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium. Fertil Steril 2007;88:1505-1533.
16. Fakih H, Marshall J. Subtle tubal abnormalities adversely affect gamete intrafallopian transfer outcome in women with endometriosis. Fertil Steril 1994;62:799-801.
17. Firestone GL, Kapadia BJ. Minireview: regulation of gap junction dynamics by nuclear hormone receptors and their ligands. Mol Endocrinol 2012; 26:1798-1807.
18. Gellersen B, Brosens IA, Brosens JJ. Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin Reprod Med 2007;25:445-453.
19. Giudice LC. Microarray expression profiling reveals candidate genes for human uterine receptivity. Am J Pharmacogenomics 2004;4:299-312.
20. Granot I, DekelN, 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.
21. 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.
22. Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril 2008; 90:247-257.
23. Hannan NJ, Nie G, Rainzcuk A, Rombauts LJ, Salamonsen LA. Uterine lavage or aspirate: which view of the intrauterine environment? Reprod Sci 2012; 19:1125-1132.
24. Jahn E, Classen-Linke I, Kusche M, Beier HM, 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.
25. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-2881.
26. Kissler S, Zangos S, Wiegratz I, Kohl J, RodyA, Gaetje R, Doebert N, Wildt L, Kunz G, Leyendecker G et al. Utero-tubal sperm transport and its impairment in endometriosis and adenomyosis. Ann N Y Acad Sci 2007; 1101:38-48.
27. Kjenseth A, Fykerud TA, Sirnes S, Bruun J, Yohannes Z, Kolberg M, Omori Y, Rivedal E, Leithe E. The gap junction channel protein connexin 43 is covalently modified and regulated by SUMOylation. J Biol Chem 2012; 287:15851-15861.
28. Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006; 85:564-572.
29. KyoN, Yamamoto H, Takeda Y, Ezumi K, Ngan CY, Terayama M, MiyakeM, Takemasa I, Ikeda M, Doki Y et al. Overexpression of connexin 26 in carcinoma of the pancreas. Oncol Rep 2008;19:627-631.
30. Laws MJ, Taylor RN, Sidell N, DeMayo FJ, Lydon JP, Gutstein DE, Bagchi MK, Bagchi IC. Gap junction communication between uterine stromal cells plays a critical role in pregnancy-associated neovascularization and embryo survival. Development 2008;135:2659-2668.
31. Li Q, Kannan A, Das A, DeMayo FJ, Hornsby PJ, Young SL, Taylor RN, Bagchi MK, Bagchi IC. WNT4 acts downstream of BMP2 and functions via b-catenin signaling pathway to regulate human endometrial stromal cell differentiation. Endocrinology 2013;154:446-457.
32. Marquez-Rosado L, Solan JL, Dunn CA, Norris RP, Lampe PD. Connexin43 phosphorylation in brain, cardiac, endothelial and epithelial tissues. Biochim Biophys Acta 2012;1818:1985-1992.
33. Martínez-Román S, Balasch J, Creus M, Fábregues F, Carmona F, Vilella R, Vanrell JA. Immunological factors in endometriosis-associated reproductive failure: studies in fertile and infertile women with and without endometriosis. Hum Reprod 1997;12:1794-1799.
34. Nair RR, Jain M, Singh K. Reduced expression of gap junction gene connexin 43 in recurrent early pregnancy loss patients. Placenta 2011;32:619-621.
35. Nevin RL. Mefloquine blockade of connexin 43 (Cx43) and risk of pregnancy loss. Placenta 2011;32:712.
36. Nezhat C, Silfen S, Nezhat F, Martin D. Surgery for endometriosis. Curr Opin Obstet Gynecol 1991;3:385-393.
37. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Am J Obstet Gynecol 1975;122:262-263.
38. Ory SJ. Pelvic endometriosis. Obstet Gynecol Clin North Am 1987; 14:999-1014.
39. Pauken CM, Lo CW. 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.
40. Pritts EA, Ryan IP, Mueller MD, Lebovic DI, Shifren JL, Zaloudek CJ, Korn AP, Darney PD, Taylor RN. Angiogenic effects of norplant contraception on endometrial histology and uterine bleeding. J Clin Endocrinol Metab 2005; 90:2142-2147.
41. Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK. Endometrial decidualization: of mice and men. Semin Reprod Med 2010;28:17-26.
42. Regidor PA, Regidor M, Schindler AE, Winterhager E. Aberrant expression pattern of gap junction connexins in endometriotic tissues. Mol Hum Reprod 1997;3:375-381.
43. Ryan IP, Schriock ED, Taylor RN. Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro. J Clin Endocrinol Metab 1994;78:642-649.
44. Simoens S, Hummelshoj L, D'Hooghe T. Endometriosis: cost estimates and methodological perspective. Hum Reprod Update 2007;13:395-404.
45. Taylor RN, Lundeen SG, Giudice LC. Emerging role of genomics in endometriosis research. Fertil Steril 2002;78:694-698.
46. WangW, TaylorRN, Bagchi IC, BagchiMK. Regulation of human endometrial stromal proliferation and differentiation by C/EBPb involves cyclin E-cdk2 and STAT3. Mol Endocrinol 2012;26:2016-2030.
47. Weiss G, Goldsmith LT, Taylor RN, Bellet D, Taylor HS. Inflammation in reproductive disorders. Reprod Sci 2009;16:216-229.
48. Winterhager E, Stutenkemper R, TraubO, Beyer E, Willecke K. Expression of different connexin genes in rat uterus during decidualization and at term. Eur J Cell Biol 1991;55:133-142.
49. Winterhager E, Grümmer R, Mavrogianis PA, Jones CJ, Hastings JM, Fazleabas AT. Connexin expression pattern in the endometrium of baboons is influenced by hormonal changes and the presence of endometriotic lesions. Mol Hum Reprod 2009;15:645-652.
50. Wu J, Taylor RN, Sidell N. Retinoic acid regulates gap junction intercellular communication in human endometrial stromal cells through modulation of the phosphorylation status of connexin 43. J Cell Physiol 2012; 228:903-910.
51. Yu J, Wu J, Bagchi IC, Bagchi MK, Sidell N, Taylor RN. Disruption of gap junctions reduces biomarkers of decidualization and angiogenesis and increases inflammatory mediators in human endometrial stromal cell cultures. Mol Cell Endocrinol 2011;344:25-34.