IL-1β-mediated proinflammatory responses are inhibited by estradiol via down-regulation of IL-1 receptor type I in uterine epithelial cells

Journal of Immunology

Volumn 175, Issue 10, 2005, Pages 6509-6516

  Schaefer, Todd M ^a,b   Wright, Jacqueline A ^a   Pioli, Patricia A ^a   Wira, Charles R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b Department of Physiology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIESTROGEN; BETA DEFENSIN 2; ESTRADIOL; ESTROGEN RECEPTOR; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1BETA; INTERLEUKIN 8; MESSENGER RNA; PROGESTERONE; SEX HORMONE; UNCLASSIFIED DRUG; ALPHA CHEMOKINE; BETA DEFENSIN; DEFB4 PROTEIN, HUMAN; INTERLEUKIN 1;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ENDOCRINE SYSTEM; ENDOMETRIUM; ENDOMETRIUM CELL; ESTROGEN ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOSTIMULATION; INFLAMMATION; OVULATION; PREGNANCY; PRIORITY JOURNAL; PROTEIN SECRETION; RECEPTOR DOWN REGULATION; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DOWN REGULATION; DRUG EFFECT; EPITHELIUM CELL; FEMALE; GENETICS; IMMUNOLOGY; METABOLISM; UTERUS;

BETA-DEFENSINS; CELLS, CULTURED; CHEMOKINES, CXC; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; EPITHELIAL CELLS; ESTRADIOL; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-1; RECEPTORS, ESTROGEN; RECEPTORS, INTERLEUKIN-1; RECEPTORS, INTERLEUKIN-1 TYPE I; RNA, MESSENGER; UTERUS;

EID: 27744536477     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.10.6509     Document Type: Article

References (76)

1. Quayle, A. J. 2002. The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J. Reprod. Immunol. 57: 61-79.
2. King, A. E., H. O. Critchley, and R. W. Kelly. 2000. Presence of secretory leukocyte protease inhibitor in human endometrium and first trimester decidua suggests an antibacterial protective role. Mol. Hum. Reprod. 6: 191-196.
3. King, A. E., D. C. Fleming, H. O. Critchley, and R. W. Kelly. 2003. Differential expression of the natural antimicrobials, β-defensins 3 and 4, in human endometrium. J. Reprod. Immunol. 59: 1-16.
4. Fleming, D. C., A. E. King, A. R. Williams, H. O. Critchley, and R. W. Kelly. 2003. Hormonal contraception can suppress natural antimicrobial gene transcription in human endometrium. Fertil. Steril. 79: 856-863.
5. Fahey, J. V., and C. R. Wira. 2002. Effect of menstrual status on antibacterial activity and secretory leukocyte protease inhibitor production by human uterine -epithelial cells in culture. J. Infect. Dis. 185: 1606-1613.
6. Arici, A., P. C. MacDonald, and M. L. Casey. 1995. Regulation of monocyte chemotactic protein-1 gene expression in human endometrial cells in cultures. 107: 189.
7. Hornung, D., I. P. Ryan, V. A. Chao, J. L. Vigne, E. D. Schriock, and R. N. Taylor. 1997. Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J. Clin. Endocrinol. Metab. 82; 1621-1628.
8. Arid, A., J. R. Head, P. C. MacDonald, and M. L. Casey. 1993. Regulation of interleukin-8 gene expression in human endometrial cells in culture. Mol. Cell. Endocrinol. 94: 195-204.
9. Schaefer, T. M., J. V. Fahey, J. A. Wright, and C. R. Wira. 2005. Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J. Immunol. 174: 992-1002.
10. Simon, C., A. Frances, G. N. Piquette, I. el Danasouri, G. Zurawski, W. Dang, and M. L. Polan. 1994. Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology 134: 521-528.
11. Simon, C., D. Valbuena, J. Krussel, A. Bernal, C. R. Murphy, T. Shaw, A. Pellicer, and M. L. Polan. 1998. Interleukin-1 receptor antagonist prevents embryonic implantation by a direct effect on the endometrial epithelium. Fertil. Steril. 70: 896-906.
12. 1 in human endometrial epithelial cells in vitro. J. Clin. Endocrinol. Metab. 82: 2607-2616.
13. McMahan, C. J., J. L. Slack, B. Mosley, D. Cosman, S. D. Lupton, L. L. Brunton, C. E. Grubin, J. M. Wignall, N. A. Jenkins, C. I. Brannan, et al. 1991. A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J. 10: 2821-2832.
14. Sims, J. E., M. A. Gayle, J. L. Slack, M. R. Alderson, T. A. Bird, J. G. Giri, F. Colotta, F. Re, A. Mantovani, K. Shanebeck, et al. 1993. Interleukin 1 signaling occurs exclusively via the type I receptor. Proc. Natl. Acad. Sci. USA 90: 6155-6159.
15. Stylianou, E., L. A. O'Neill, L. Rawlinson, M. R. Edbrooke, P. Woo, and J. Saklatvala. 1992. Interleukin 1 induces NF-κB through its type I but not its type II receptor in lymphocytes. J. Biol. Chem. 267: 15836-15841.
16. Dinarello, C. A., J. G. Cannon, J. W. Mier, H. A. Bernheim, G. LoPreste, D. L. Lynn, R. N. Love, A. C. Webb, P. E. Auron, R. C. Reuben, et al. 1986. Multiple biological activities of human recombinant interleukin 1. J. Clin. Invest. 77: 1734-1739.
17. + T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking. Immunology 102: 434-440.
18. + T cell-rich lymphoid aggregates in human uterine endometrium. J. Leukocyte Biol. 61: 427-435.
19. Narayanan, S., A. Glasser, Y. S. Hu, and A. M. McDermott. 2005. The effect of interleukin-1 on cytokine gene expression by human corneal epithelial cells. Exp. Eye Res. 80: 175-183.
20. Sun, B., K. Nasu, J. Fukuda, S. Mine, M. Nishida, and I. Miyakawa. 2002. Expression of macrophage inflammatory protein-3α in an endometrial epithelial cell line, HHUA, and cultured human endometrial stromal cells. Mol. Hum. Reprod. 8: 930-933.
21. Cromwell, O., Q. Hamid, C. J. Corrigan, J. Barkans, Q. Meng, P. D. Collins, and A. B. Kay. 1992. Expression and generation of interleukin-8, IL-6 and granulocyte-macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1β and tumour necrosis factor α. Immunology 77: 330-337.
22. Wickremasinghe, M. I., L. H. Thomas, C. M. O'Kane, J. Uddin, and J. S. Friedland. 2004. Transcriptional mechanisms regulating alveolar epithelial cell-specific CCL5 secretion in pulmonary tuberculosis. J. Biol. Chem. 279: 27199-27210.
23. King, A. E., D. C. Fleming, H. O. Critchley, and R. W. Kelly. 2002. Regulation of natural antibiotic expression by inflammatory mediators and mimics of infection in human endometrial epithelial cells. Mol. Hum. Reprod. 8: 341-349.
24. Baggia, S., M. G. Gravett, S. S. Witkin, G. J. Haluska, and M. J. Novy. 1996. Interleukin-1β intra-amniotic infusion induces tumor necrosis factor α, prostaglandin production, and preterm contractions in pregnant rhesus monkeys. J. Soc. Gynecol. Investig. 3: 121-126.
25. Gene, M. R., S. S. Witkin, M. L. Delaney, L. R. Paraskevas, R. E. Tuomala, E. R. Norwitz, and A. B. Onderdonk. 2004. A disproportionate increase in IL-1β over IL-1ra in the cervicovaginal secretions of pregnant women with altered vaginal microflora correlates with preterm birth. Am. J. Obster. Gynecol. 190: 1191-1197.
26. Rinehart, B. K., D. A. Terrone, S. Lagoo-Deenadayalan, W. H. Barber, E. A. Hale, J. N. Martin, Jr., and W. A. Bennett. 1999. Expression of the placental cytokines tumor necrosis factor a, interleukin 1β, and interleukin 10 is increased in preeclampsia. Am. J. Obstet. Gynecol. 181: 915-920.
27. Romero, R., M. Mazor, F. Brandt, W. Sepulveda, C. Avila, D. B. Cotton, and C. A. Dinarello. 1992. Interleukin-1α and interleukin-1β in preterm and term human parturition. Am. J. Reprod. Immunol. 27: 117-123.
28. Romero, R., W. Sepulveda, M. Mazor, F. Brandt, D. B. Cotton, C. A. Dinarello, and M. D. Mitchell. 1992. The natural interleukin-1 receptor antagonist in term and preterm parturition. Am. J. Obstet. Gynecol. 167: 863-872.
29. Gravett, M. G., S. S. Witkin, G. J. Haluska, J. L. Edwards, M. J. Cook, and M. J. Novy. 1994. An experimental model for intraamniotic infection and preterm labor in rhesus monkeys. Am. J. Obstet. Gynecol. 171: 1660-1667.
30. Grosskinsky, C. M., and J. Halme. 1993. Endometriosis: the host response. Baillieres Clin. Obstet. Gynaecol. 7: 701-713.
31. Halme, J., S. Becker, and R. Wing. 1984. Accentuated cyclic activation of peritoneal macrophages in patients with endometriosis. Am. J. Obstet. Gynecol. 148: 85-90.
32. Sahakian, V., J. Anners, S. Haskill, and J. Halme. 1993. Selective localization of interleukin-1 receptor antagonist in eutopic endometrium and endometriotic implants. Fertil. Steril. 60: 276-279.
33. Zeller, J. M., I. Henig, E. Radwanska, and W. P. Dmowski. 1987. Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am. J. Reprod. Immunol. Microbiol. 13: 78-82.
34. Mori, H., M. Sawairi, M. Nakagawa, N. Itoh, K. Wada, and T. Tamaya. 1992. Expression of interleukin-1 (IL-1) β messenger ribonucleic acid (mRNA) and IL-1 receptor antagonist mRNA in peritoneal macrophages from patients with endometriosis. Fertil. Steril. 57: 535-542.
35. Abreu, M. T., E. T. Arnold, L. S. Thomas, R. Gonsky, Y. Zhou, B. Hu, and M. Arditi. 2002. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J. Biol. Chem. 277: 20431-20437.
36. Kharfi, A., A. Boucher, and A. Akoum. 2002. Abnormal interleukin-1 receptor type II gene expression in the endometrium of women with endometriosis. Biol. Reprod. 66: 401-406.
37. Bergeron, R. M., T. B. Thompson, L. S. Leonard, L. Pluta, and K. W. Gaido. 1999. Estrogenicity of bisphenol A in a human endometrial carcinoma cell line. Mol. Cell. Endocrinol. 150: 179-187.
38. Dardes, R. C., J. M. Schafer, S. T. Pearce, C. Osipo, B. Chen, and V. C. Jordan. 2002. Regulation of estrogen target genes and growth by selective estrogen-receptor modulators in endometrial cancer cells. Gynecol. Oncol. 85: 498-506.
39. Farnell, Y. Z., and N. H. Ing. 2003. The effects of estradiol and selective estrogen receptor modulators on gene expression and messenger RNA stability in immortalized sheep endometrial stromal cells and human endometrial adenocarcinoma cells. J. Steroid Biochem. Mol. Biol. 84: 453-461.
40. Nguyen, H. N., B. U. Sevin, H. E. Averette, W. Voigt, J. Perras, R. Angioli, R. Ramos, D. Donate, and M. Penalver. 1992. Determination of hormonal response in uterine cancer cell lines by the ATP bioluminescence assay and flow cytometry. Gynecol. Oncol. 46: 55-61.
41. Richardson, J. M., C. Kaushic, and C. R. Wira. 1995. Polymeric immunoglobin (Ig) receptor production and IgA transcytosis in polarized primary cultures of mature rat uterine epithelial cells. Biol. Reprod. 53: 488-498.
42. Godfrey, T. E., S. H. Kim, M. Chavira, D.W. Ruff, R. S. Warren, J. W. Gray, and R. H. Jensen. 2000. Quantitative mRNA expression analysis from formalin-fixed, paraffin-embedded tissues using 5′ nuclease quantitative reverse transcription-polymerase chain reaction. J. Mol. Diagn. 1: 84-91.
43. Larsen, C. G., A. O. Anderson, E. Appella, J. J. Oppenheim, and K. Matsushima. 1989. The neutrophil-activating protein (NAP-1) is also chemotactic for T lymphocytes. Science 243: 1464-1466.
44. Mukaida, N., M. Shiroo, and K. Matsushima. 1989. Genomic structure of the human monocyte-derived neutrophil chemotactic factor IL-8. J. Immunol 143: 1366-1371.
45. Baggiolini, M., and C. A. Dahinden. 1994. CC chemokines in allergic inflammation. Immunol. Today 15: 127-133.
46. Parker, M. G. 1993. Action of "pure" antiestrogens in inhibiting estrogen receptor action. Breast Cancer Res. Treat. 26: 131-137.
47. 2 production. J. Clin. Endocrinol. Metab. 70: 1000-1006.
48. Tabibzadeh, S., K. L. Kaffka, P. L. Kilian, and P. G. Satyaswaroop. 1990. Human endometrial epithelial cell lines for studying steroid and cytokine actions. In Vitro Cell Dev. Biol. 26: 1173-1179.
49. Kauma, S., D. Matt, S. Strom, D. Eierman, and T. Turner. 1990. Interleukin-1β, human leukocyte antigen HLA-DRα, and transforming growth factor β expression in endometrium, placenta, and placental membranes. Am. J. Obstet. Gynecol. 163: 1430-1437.
50. Kayisli, U. A., N. G. Mahutte, and A. Ariel. 2002. Uterine chemokines in reproductive physiology and pathology. Am. J. Reprod. Immunol. 47: 213-221.
51. Yang, D., O. Chertov, S. N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schröder, J. M. Wang, O. M. Howard, and J. J. Oppenheim. 1999. β-Defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286: 525-528.
52. Biragyn, A., M. Surenhu, D. Yang, P. A. Ruffini, B. A. Haines, E. Klyushnenkova, J. J. Oppenheim, and L. W. Kwak. 2001. Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J. Immunol. 167: 6644-6653.
53. Brooks, G. F., and C. J. Lammel. 1989. Humoral immune response to gonococcal infections. Clin. Microbiol. Rev. 2(Suppl.): S5-S10.
54. Joseph, S. B., K. T. Miner, and M. Croft. 1998. Augmentation of naive, Th1 and Th2 effector CD4 responses by IL-6, IL-1 and TNF. Eur. J. Immunol. 28: 277-289.
55. Dale, D. C., W. C. Liles, W. R. Summer, and S. Nelson. 1995. Review: granulocyte colony-stimulating factor: role and relationships in infectious diseases. J. Infect. Dis. 172: 1061-1075.
56. Hartung, T., S. Von Aulock, C. Schneider, and E. Faist. 2003. How to leverage an endogenous immune defense mechanism: the example of granulocyte colony-stimulating factor. Crit. Care Med. 31: S65-S75.
57. Simon, C., G. N. Piquette, A. Frances, and M. L. Polan. 1993. Localization of interleukin-1 type I receptor and interleukin-1β in human endometrium throughout the menstrual cycle. J. Clin. Endocrinol. Metab. 77: 549-555.
58. Bigonnesse, F., Y. Labelle, and A. Akoum. 2001. Triphasic expression of interleukin-1 receptor type I in human endometrium throughout the menstrual cycle of fertile women and women with unexplained infertility. Fertil. Steril. 75: 79-87.
59. Singer, C. F., N. Kronsteiner, E. Marton, I. Walter, M. Kubista, K. Czerwenka, M. Schreiber, W. Tschugguel, F. Wieser, and E. Kubista. 2002. Interleukin-1 system and sex steroid receptor gene expression in human endometrial cancer. Gynecol. Oncol 85: 423-430.
60. Romero, R., S. T. Parvizi, E. Oyarzun, M. Mazor, Y. K. Wu, C. Avila, A. P. Athanassiadis, and M. D. Mitchell. 1990. Amniotic fluid interleukin-1 in spontaneous labor at term. J. Reprod. Med. 35: 235-238.
61. Ammala, M., T. Nyman, A. Salmi, and E. M. Rutanen. 1997. The interleukin-1 system in gestational tissues at term: effect of labour. Placenta 18: 717-723.
62. Dudley, D. J., D. Collmer, M. D. Mitchell, and M. S. Trautman. 1996. Inflammatory cytokine mRNA in human gestational tissues: implications for term and preterm labor. J. Soc. Gynecol Investig. 3: 328-335.
63. Keelan, J. A., K. W. Marvin, T. A. Sato, M. Coleman, L. M. McCowan, and M. D. Mitchell. 1999. Cytokine abundance in placental tissues: evidence of inflammatory activation in gestational membranes with term and preterm parturition. Am. J. Obstet. Gynecol. 181: 1530-1536.
64. Santhanam, U., C. Avila, R. Romero, H. Viguet, N. Ida, S. Sakurai, and P. B. Sehgal. 1991. Cytokines in normal and abnormal parturition: elevated amniotic fluid interleukin-6 levels in women with premature rupture of membranes associated with intrauterine infection. Cytokine 3: 155-163.
65. Gonzalez Bosquet, E., I. Ferrer, C. Valls, M. Borras, and J. M. Lailla. 2005. The value of interleukin-8, interleukin-6 and interleukin-1β in vaginal wash as predictors of preterm delivery. Gynecol. Obstet. Invest. 59: 175-178.
66. Espinoza, J., T. Chaiworapongsa, R. Romero, S. Edwin, C. Rathnasabapathy, R. Gomez, E. Bujold, N. Camacho, Y. M. Kim, S. Hassan, et al. 2003. Antimicrobial peptides in amniotic fluid: defensins, calprotectin and bacterial/permeability-increasing protein in patients with microbial invasion of the amniotic cavity, intra-amniotic inflammation, preterm labor and premature rupture of membranes. J. Matern. Fetal Neonatal Med. 13: 2-21.
67. Tabibzadeh, S. S., U. Santhanam, P. B. Sehgal, and L. T. May. 1989. Cytokine-induced production of IFN-β2/IL-6 by freshly explanted human endometrial stromal cells: modulation by estradiol-17β. J. Immunol. 142: 3134-3139.
68. Boucher, A., W. Mourad, J. Mailloux, A. Lemay, and A. Akoum. 2000. Ovarian hormones modulate monocyte chemotactic protein-1 expression in endometrial cells of women with endometriosis. Mol. Hum. Reprod. 6: 618-626.
69. Wu, M. Y., and H. N. Ho. 2003. The role of cytokines in endometriosis. Am. J. Reprod. Immunol. 49: 285-296.
70. Cato, A. C., A. Nestl, and S. Mink. 2002. Rapid actions of steroid receptors in cellular signaling pathways. Sci. STKE 2002: RE9.
71. Beato, M. 1989. Gene regulation by steroid hormones. Cell 56: 335-344.
72. Paech, K., P. Webb, G. G. Kuiper, S. Nilsson, J. Gustafsson, P. J. Kushner, and T. S. Scanlan. 1997. Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science 277: 1508-1510.
73. Dana, S. L., P. A. Hoener, D. A. Wheeler, C. B. Lawrence, and D. P. McDonnell. 1994. Novel estrogen response elements identified by genetic selection in yeast are differentially responsive to estrogens and antiestrogens in mammalian cells. Mol. Endocrinol. 8: 1193-1207.
74. Krishnan, V., X. Wang, and S. Safe. 1994. Estrogen receptor-Sp1 complexes mediate estrogen-induced cathepsin D gene expression in MCF-7 human breast cancer cells. J. Biol. Chem. 269: 15912-15917.
75. Ye, K., E. Vannier, B. D. Clark, J. E. Sims, and C. A. Dinarello. 1996. Three distinct promoters direct transcription of different 5′ untranslated regions of the human interleukin I type I receptor: a possible mechanism for control of translation. Cytokine 8: 421-429.
76. Sunyer, T., J. Lewis, P. Collin-Osdoby, and P. Osdoby. 1999. Estrogen's bone-protective effects may involve differential IL-1 receptor regulation in human osteoclast-like cells. J. Clin. Invest. 103: 1409-1418.