Glucocorticoid-induced reversal of interleukin-1β-stimulated inflammatory gene expression in human oviductal cells

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Backman, Stéphanie ^a   Kollara, Alexandra ^a,b   Haw, Robin ^c   Stein, Lincoln ^c   Brown, Theodore J ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 23P19; INTERLEUKIN 8; PROSTAGLANDIN SYNTHASE; PROTEIN PTGS2; UNCLASSIFIED DRUG; GLUCOCORTICOID;

ARTICLE; CANCER RISK; CELL CYCLE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIGH GRADE SEROUS OVARIAN CARCINOMA; HUMAN; HUMAN CELL; IL23A GENE; IL8 GENE; INFLAMMATION; INTRACELLULAR SIGNALING; NUCLEOTIDE SEQUENCE; OVARY CARCINOMA; PI3 GENE; TACC2 GENE; UTERINE TUBE MUCOSA; CARCINOGENESIS; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; UTERINE TUBE;

CARCINOGENESIS; CELL LINE; FALLOPIAN TUBES; FEMALE; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA;

EID: 84901330568     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097997     Document Type: Article

References (80)

1. Soslow RA (2008) Histologic subtypes of ovarian carcinoma: an overview. Int J Gynecol Pathol 27: 161-174.
2. Crum CP, Drapkin R, Miron A, Ince TA, Muto M, et al. (2007) The distal fallopian tube: a new model for pelvic serous carcinogenesis. Curr Opin Obstet Gynecol 19: 3-9. (Pubitemid 46095865)
3. Lee Y, Miron A, Drapkin R, Nucci MR, Medeiros F, et al. (2007) A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 211: 26-35. (Pubitemid 46092026)
4. Sogaard M, Kjaer SK, Gayther S (2006) Ovarian cancer and genetic susceptibility in relation to the BRCA1 and BRCA2 genes. Occurrence, clinical importance and intervention. Acta Obstet Gynecol Scand 85: 93-105. (Pubitemid 43879130)
5. Piek JM, van Diest PJ, Zweemer RP, Jansen JW, Poort-Keesom RJ, et al. (2001) Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J Pathol 195: 451-456. (Pubitemid 33069670)
6. Finch A, Shaw P, Rosen B, Murphy J, Narod SA, et al. (2006) Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol Oncol 100: 58-64. (Pubitemid 41815050)
7. Kindelberger DW, Lee Y, Miron A, Hirsch MS, Feltmate C, et al. (2007) Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. Am J Surg Pathol 31: 161-169. (Pubitemid 46175016)
8. Kuhn E, Kurman RJ, Vang R, Sehdev AS, Han G, et al. (2012) TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma - evidence supporting the clonal relationship of the two lesions. J Pathol 226: 421-426.
9. Carlson JW, Miron A, Jarboe EA, Parast MM, Hirsch MS, et al. (2008) Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention. J Clin Oncol 26: 4160-4165.
10. Seidman JD, Zhao P, Yemelyanova A (2011) "Primary peritoneal" high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer. Gynecol Oncol 120: 470-473.
11. Tang S, Onuma K, Deb P, Wang E, Lytwyn A, et al. (2012) Frequency of serous tubal intraepithelial carcinoma in various gynecologic malignancies: a study of 300 consecutive cases. Int J Gynecol Pathol 31: 103-110.
12. Hunn J, Rodriguez GC (2012) Ovarian cancer: etiology, risk factors, and epidemiology. Clin Obstet Gynecol 55: 3-23.
13. McGuire V, Felberg A, Mills M, Ostrow KL, DiCioccio R, et al. (2004) Relation of contraceptive and reproductive history to ovarian cancer risk in carriers and noncarriers of BRCA1 gene mutations. Am J Epidemiol 160: 613-618. (Pubitemid 39281840)
14. McLaughlin JR, Risch HA, Lubinski J, Moller P, Ghadirian P, et al. (2007) Reproductive risk factors for ovarian cancer in carriers of BRCA1 or BRCA2 mutations: a case-control study. Lancet Oncol 8: 26-34. (Pubitemid 46001033)
15. Tung KH, Wilkens LR, Wu AH, McDuffie K, Nomura AM, et al. (2005) Effect of anovulation factors on pre- and postmenopausal ovarian cancer risk: revisiting the incessant ovulation hypothesis. Am J Epidemiol 161: 321-329. (Pubitemid 40256203)
16. Buscher U, Chen FC, Kentenich H, Schmiady H (1999) Cytokines in the follicular fluid of stimulated and non-stimulated human ovaries; is ovulation a suppressed inflammatory reaction? Hum Reprod 14: 162-166. (Pubitemid 29046332)
17. Karihtala P, Soini Y, Vaskivuo L, Bloigu R, Puistola U (2009) DNA adduct 8-hydroxydeoxyguanosine, a novel putative marker of prognostic significance in ovarian carcinoma. Int J Gynecol Cancer 19: 1047-1051.
18. Lu H, Ouyang W, Huang C (2006) Inflammation, a key event in cancer development. Mol Cancer Res 4: 221-233.
19. Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′- deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27: 120-139.
20. Singh N, Rieder MJ, Tucker MJ (2004) Mechanisms of glucocorticoid- mediated anti-inflammatory and immunosuppressive action. Paediatric and Perinatal Drug Therapy 6: 107-115. (Pubitemid 40430753)
21. Tone AA, Virtanen C, Shaw P, Brown TJ (2012) Prolonged postovulatory proinflammatory signaling in the fallopian tube epithelium may be mediated through a BRCA1/DAB2 axis. Clin Cancer Res 18: 4334-4344.
22. Zhu XO, Yang Z, Guo CM, Ni XT, Li JN, et al. (2009) Paradoxical stimulation of cyclooxygenase-2 expression by glucocorticoids via a cyclic AMP response element in human amnion fibroblasts. Mol Endocrinol 23: 1839-1849.
23. Wang B, Palomares K, Parobchak N, Cece J, Rosen M, et al. (2012) Glucocorticoid Receptor Signaling Contributes to Constitutive Activation of the Noncanonical NF-kappaB Pathway in Term Human Placenta. Mol Endocrinol 27: 203-211.
24. Sun H, Sheveleva E, Xu B, Inoue H, Bowden TG, et al. (2008) Corticosteroids induce COX-2 expression in cardiomyocytes: role of glucocorticoid receptor and C/EBP-beta. Am J Physiol Cell Physiol 295: C915-922.
25. Pujols L, Benitez P, Alobid I, Martinez-Anton A, Roca-Ferrer J, et al. (2009) Glucocorticoid therapy increases COX-2 gene expression in nasal polyps in vivo. Eur Respir J 33: 502-508.
26. Mulayim N, Palter SF, Selam B, Arici A (2003) Expression and regulation of interleukin-8 in human fallopian tubal cells. American journal of obstetrics and gynecology 188: 651-656. (Pubitemid 36332429)
27. Gerard N, Caillaud M, Martoriati A, Goudet G, Lalmanach AC (2004) The interleukin-1 system and female reproduction. J Endocrinol 180: 203-212.
28. Lee YL, Lee KF, Xu JS, Wang YL, Tsao SW, et al. (2001) Establishment and characterization of an immortalized human oviductal cell line. Mol Reprod Dev 59: 400-409.
29. Monkkonen KS, Aflatoonian R, Lee KF, Yeung WS, Tsao SW, et al. (2007) Hormonal regulation of Galphai2 and mPRalpha in immortalized human oviductal cell line OE-E6/E7. Mol Hum Reprod 13: 845-851.
30. Ling L, Lee YL, Lee KF, Tsao SW, Yeung WS, et al. (2005) Expression of human oviductin in an immortalized human oviductal cell line. Fertil Steril 84 Suppl 2: 1095-1103. (Pubitemid 41396533)
31. Fotheringham S, Levanon K, Drapkin R (2011) Ex vivo culture of primary human fallopian tube epithelial cells. J Vis Exp 51. Available: http://www.jove.com/details.php?id=2728, doi:10.3791/2728.
32. Kollara A, Brown TJ (2006) Functional interaction of nuclear receptor coactivator 4 with aryl hydrocarbon receptor. Biochem Biophys Res Commun 346: 526-534. (Pubitemid 43902715)
33. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
34. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, et al. (2006) GenePattern 2.0. Nat Genet 38: 500-501.
35. Wettenhall JM, Smyth GK (2004) limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706. (Pubitemid 40136823)
36. Wu G, Feng X, Stein L (2010) A human functional protein interaction network and its application to cancer data analysis. Genome Biol 11: R53.
37. Mikosz CA, Brickley DR, Sharkey MS, Moran TW, Conzen SD (2001) Glucocorticoid receptor-mediated protection from apoptosis is associated with induction of the serine/threonine survival kinase gene, sgk-1. J Biol Chem 276: 16649-16654.
38. Gross JL, Yellen J (1998) Graph Theory and Its Applications. Boca Raton, FL: CRC Press.
39. Girvan M, Newman ME (2002) Community structure in social and biological networks. Proc Natl Acad Sci USA 99: 7821-7826. (Pubitemid 34650963)
40. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504. (Pubitemid 37428274)
41. Trinchieri G (2012) Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu Rev Immunol 30: 677-706.
42. Maccio A, Madeddu C (2012) Inflammation and ovarian cancer. Cytokine 58: 133-147.
43. Johnson ML, Murdoch J, Van Kirk EA, Kaltenbach JE, Murdoch WJ (1999) Tumor necrosis factor alpha regulates collagenolytic activity in preovulatory ovine follicles: relationship to cytokine secretion by the oocyte-cumulus cell complex. Biol Reprod 61: 1581-1585.
44. Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, et al. (2009) Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol 7: 40.
45. Tone AA, Begley H, Sharma M, Murphy J, Rosen B, et al. (2008) Gene expression profiles of luteal phase fallopian tube epithelium from BRCA mutation carriers resemble high-grade serous carcinoma. Clin Cancer Res 14: 4067-4078.
46. Tone AA, Virtanen C, Shaw PA, Brown TJ (2011) Decreased progesterone receptor isoform expression in luteal phase fallopian tube epithelium and high-grade serous carcinoma. Endocr Relat Cancer 18: 221-234.
47. Karin M (2009) NF-kappaB as a critical link between inflammation and cancer. Cold Spring Harb Perspect Biol 1: a000141.
48. Aggarwal BB, Sung B (2011) NF-kappaB in cancer: a matter of life and death. Cancer Discov 1: 469-471.
49. Almawi WY, Beyhum HN, Rahme AA, Rieder MJ (1996) Regulation of cytokine and cytokine receptor expression by glucocorticoids. J Leukoc Biol 60: 563-572. (Pubitemid 26400412)
50. Caldenhoven E, Liden J, Wissink S, Van de Stolpe A, Raaijmakers J, et al. (1995) Negative cross-talk between RelA and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids. Mol Endocrinol 9: 401-412.
51. Necela BM, Cidlowski JA (2004) Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. Proc Am Thorac Soc 1: 239-246.
52. Sen R, Smale ST (2010) Selectivity of the NF-κB response. Cold Spring Harb Perspect Biol 2: a000257.
53. Chaturvedi MM, Sung B, Yadav VR, Kannappan R, Aggarwal BB (2011) NF-kappaB addiction and its role in cancer: 'one size does not fit all'. Oncogene 30: 1615-1630.
54. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, et al. (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91: 197-208. (Pubitemid 27456387)
55. Wanggren K, Stavreus-Evers A, Olsson C, Andersson E, Gemzell-Danielsson K (2008) Regulation of muscular contractions in the human Fallopian tube through prostaglandins and progestagens. Hum Reprod 23: 2359-2368.
56. Menter DG, Schilsky RL, DuBois RN (2010) Cyclooxygenase-2 and cancer treatment: understanding the risk should be worth the reward. Clin Cancer Res 16: 1384-1390.
57. Wang D, Dubois RN (2010) The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene 29: 781-788.
58. Ammundsen HB, Faber MT, Jensen A, Hogdall E, Blaakaer J, et al. (2012) Use of analgesic drugs and risk of ovarian cancer: results from a Danish case-control study. Acta Obstet Gynecol Scand 91: 1094-1102.
59. Baandrup L, Faber MT, Christensen J, Jensen A, Andersen KK, et al. (2013) Nonsteroidal anti-inflammatory drugs and risk of ovarian cancer: systematic review and meta-analysis of observational studies. Acta Obstet Gynecol Scand 92: 245-255.
60. Palter SF, Mulayim N, Senturk L, Arici A (2001) Interleukin-8 in the human fallopian tube. J Clin Endocrinol Metab 86: 2660-2667. (Pubitemid 32545721)
61. Xu L, Fidler IJ (2000) Interleukin 8: an autocrine growth factor for human ovarian cancer. Oncol Res 12: 97-106.
62. Lokshin AE, Winans M, Landsittel D, Marrangoni AM, Velikokhatnaya L, et al. (2006) Circulating IL-8 and anti-IL-8 autoantibody in patients with ovarian cancer. Gynecol Oncol 102: 244-251. (Pubitemid 44041638)
63. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, et al. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
64. McKenzie BS, Kastelein RA, Cua DJ (2006) Understanding the IL-23-IL-17 immune pathway. Trends Immunol 27: 17-23. (Pubitemid 43083560)
65. Langowski JL, Zhang X, Wu L, Mattson JD, Chen T, et al. (2006) IL-23 promotes tumour incidence and growth. Nature 442: 461-465. (Pubitemid 44264796)
66. Teng MW, Andrews DM, McLaughlin N, von Scheidt B, Ngiow SF, et al. (2010) IL-23 suppresses innate immune response independently of IL-17A during carcinogenesis and metastasis. Proc Natl Acad Sci USA 107: 8328-8333.
67. Still IH, Vettaikkorumakankauv AK, DiMatteo A, Liang P (2004) Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms. BMC Evol Biol 4: 16.
68. Gangisetty O, Lauffart B, Sondarva GV, Chelsea DM, Still IH (2004) The transforming acidic coiled coil proteins interact with nuclear histone acetyltransferases. Oncogene 23: 2559-2563. (Pubitemid 38520753)
69. Lauffart B, Gangisetty O, Still IH (2003) Molecular cloning, genomic structure and interactions of the putative breast tumor suppressor TACC2. Genomics 81: 192-201. (Pubitemid 36298611)
70. Takayama K, Horie-Inoue K, Suzuki T, Urano T, Ikeda K, et al. (2012) TACC2 is an androgen-responsive cell cycle regulator promoting androgen-mediated and castration-resistant growth of prostate cancer. Mol Endocrinol 26: 748-761.
71. Cheng S, Douglas-Jones A, Yang X, Mansel RE, Jiang WG (2010) Transforming acidic coiled-coil-containing protein 2 (TACC2) in human breast cancer, expression pattern and clinical/prognostic relevance. Cancer Genomics Proteomics 7: 67-73.
72. Lauffart B, Vaughan MM, Eddy R, Chervinsky D, DiCioccio RA, et al. (2005) Aberrations of TACC1 and TACC3 are associated with ovarian cancer. BMC Womens Health 5: 8.
73. Lauffart B, Gangisetty O, Still IH (2007) Evolutionary conserved interaction of TACC2/TACC3 with BARD1 and BRCA1: potential implications for DNA damage response in breast and ovarian cancer. Cancer Therapy 5: 409-416.
74. Runnebaum IB, Bruning A (2005) Glucocorticoids inhibit cell death in ovarian cancer and up-regulate caspase inhibitor cIAP2. Clin Cancer Res 11: 6325-6332. (Pubitemid 41262964)
75. Ghosh M, Shen Z, Fahey JV, Cu-Uvin S, Mayer K, et al. (2010) Trappin-2/Elafin: a novel innate anti-human immunodeficiency virus-1 molecule of the human female reproductive tract. Immunology 129: 207-219.
76. Roghanian A, Williams SE, Sheldrake TA, Brown TI, Oberheim K, et al. (2006) The antimicrobial/elastase inhibitor elafin regulates lung dendritic cells and adaptive immunity. Am J Respir Cell Mol Biol 34: 634-642.
77. King AE, Wheelhouse N, Cameron S, McDonald SE, Lee KF, et al. (2009) Expression of secretory leukocyte protease inhibitor and elafin in human fallopian tube and in an in-vitro model of Chlamydia trachomatis infection. Hum Reprod 24: 679-686.
78. Stock SJ, Duthie L, Tremaine T, Calder AA, Kelly RW, et al. (2009) Elafin (SKALP/Trappin-2/proteinase inhibitor-3) is produced by the cervix in pregnancy and cervicovaginal levels are diminished in bacterial vaginosis. Reprod Sci 16: 1125-1134.
79. Bingle L, Tetley TD, Bingle CD (2001) Cytokine-mediated induction of the human elafin gene in pulmonary epithelial cells is regulated by nuclear factor-kappaB. Am J Respir Cell Mol Biol 25: 84-91. (Pubitemid 32682709)
80. Henriksen PA, Hitt M, Xing Z, Wang J, Haslett C, et al. (2004) Adenoviral gene delivery of elafin and secretory leukocyte protease inhibitor attenuates NF-kappa B-dependent inflammatory responses of human endothelial cells and macrophages to atherogenic stimuli. J Immunol 172: 4535-4544. (Pubitemid 38375271)