17β-Estradiol modulates the macrophage migration inhibitory factor secretory pathway by regulating ABCA1 expression in human first-trimester placenta

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 3, 2010, Pages

  Ietta, Francesca ^a   Bechi, Nicoletta ^a   Romagnoli, Roberta ^a   Bhattacharjee, Jayonta ^a   Realacci, Massimo ^b   Di Vito, Maura ^b   Ferretti, Cristina ^c   Paulesu, Luana ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c Hospital Campostaggia   (Italy)

Author keywords

ATP binding cassette transporter protein A1; Chorionic villous explants; Placental cytokines; Steroid hormones

Indexed keywords

ABC TRANSPORTER A1; CYTOKINE; ESTRADIOL; HORMONE; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA;

ARTICLE; CHORION VILLUS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; EXPLANT; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MODULATION; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ATP-BINDING CASSETTE TRANSPORTERS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; PLACENTA; PREGNANCY; PREGNANCY TRIMESTER, FIRST; SIGNAL TRANSDUCTION;

EID: 77349090178     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00522.2009     Document Type: Article

References (60)

1. Albrecht C, Soumian S, Tetlow N, Patel P, Sullivan MH, Lakasing L, Nicolaides K, Williamson C. Placental ABCA1 expression is reduced in primary antiphospholipid syndrome compared to pre-eclampsia and controls. Placenta 28: 701-708, 2007.
2. Aloisi AM, Pari G, Ceccarelli I, Vecchi I, Ietta F, Lodi L, Paulesu L. Gender-related effects of chronic non-malignant pain and opioid therapy on plasma levels of macrophage migration inhibitory factor (MIF). Pain 115: 142-151, 2005.
3. Arcuri F, Cintorino M, Carducci A, Papa S, Riparbelli MG, Mangioni S, Di Blasio AM, Tosi P, Viganò P. Human decidual natural killer cells as a source and target of macrophage migration inhibitory factor. Reproduction 131: 175-182, 2006.
4. Arcuri F, Cintorino M, Vatti R, Carducci A, Liberatori S, Paulesu L. Expression of macrophage migration inhibitory factor transcript and protein by first-trimester human trophoblasts. Biol Reprod 60: 1299-1303, 1999.
5. Arcuri F, Ricci C, Ietta F, Cintorino M, Tripodi SA, Cetin I, Garcia E, Schatz F, Klemi P, Santopietro R, Paulesu L. Macrophage migration inhibitory factor in the human endometrium: expression and localization during the menstrual cycle and early pregnancy. Biol Reprod 64: 1200-1205, 2001.
6. Ashcroft GS, Mills SJ, Lei K, Gibbons L, Jeong MJ, Taniguchi M, Burow M, Horan MA, Wahl SM, Nakayama T. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 111: 1309-1318, 2003.
7. Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, Gemsa D, Donnelly T, Bucala R. An essential role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA 93: 7849-7854, 1996.
8. Batra S, Bengtsson LP. 17 beta-Estradiol and progesterone concentrations in myometrium of pregnancy and their relationships to concentrations in peripheral plasma. J Clin Endocrinol Metab 46: 622-626, 1978.
9. Baumann R, Casaulta C, Simon D, Conus S, Yousefi S, Simon HU. Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J 17: 2221-2230, 2003.
10. Bechi N, Ietta F, Romagnoli R, Focardi S, Corsi I, Buffi C, Paulesu L. Estrogen-like response to p-nonylphenol in human first trimester placenta and BeWo choriocarcinoma cells. Toxicol Sci 93: 75-81, 2006.
11. Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R. MIF is a pituitaryderived cytokine that potentiates lethal endotoxaemia. Nature 365: 756-759, 1993.
12. Bouman A, Heineman MJ, Faas MM. Sex hormones and the immune response in humans. Hum Reprod Update 11: 411-423, 2005.
13. Bukovsky A, Cekanova M, Caudle MR, Wimalasena J, Foster JS, Henley DC, Elder RF. Expression and localization of estrogen receptoralpha protein in normal and abnormal term placentae and stimulation of trophoblast differentiation by estradiol. Reprod Biol Endocrinol 6: 1-13, 2003.
14. Calandra T, Bucala R. Macrophage migration inhibitory factor: a counter-regulator of glucocorticoid action and critical mediator of septic shock. J Inflamm 47: 39-51, 1996.
15. Calandra T, Roger T. Macrophage migration inhibitory factor. A regulator of innate immunity. Nat Rev Immunol 3: 791-800, 2003.
16. Caniggia I, Taylor CV, Ritchie JW, Lye SJ, Letarte M. Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 138: 4977-4988, 1997.
17. Carruba G, D'Agostino P, Miele M, Calabrò M, Barbera C, Di Bella G, Milano S, Ferlazzo V, Caruso R, La Rosa M, Cocciadiferro L, Campisi I, Castagnetta L, Cillari E. Estrogen regulates cytokine production and apoptosis in PMA-differentiated, macrophage-like U937 cells. J Cell Biochem 90: 187-196, 2003.
18. Chaouat G, Dubanchet S, Ledée N. Cytokines: Important for implantation? J Assist Reprod Genet 24: 491-505, 2007.
19. Donn RP, Ray DW. Macrophage migration inhibitory factor: molecular, cellular and genetic aspects of a key neuroendocrine molecule. J Endocrinol 182: 1-9, 2004.
20. Enmark E, Gustafsson JA. Oestrogen receptors - an overview. J Intern Med 246: 133-138, 1999.
21. Flieger O, Engling A, Bucala R, Lue H, Nickel W, Bernhagen J. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett 551: 78-86, 2003.
22. Gilliver SC, Ruckshanthi JP, Hardman MJ, Nakayama T, Ashcroft GS. Sex dimorphism in wound healing: the roles of sex steroids and macrophage migration inhibitory factor. Endocrinology 149: 5747-5757, 2008.
23. Glass CK, Rosenfeld MG. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 14: 121-141, 2000.
24. Hirano S, Furutama D, Hanafusa T. Physiologically high concentrations of 17β-estradiol enhance NF-κB activity in human T cells. Am J Physiol Regul Integr Comp Physiol 292: R1465-R1471, 2007.
25. Houdeau E, Moriez R, Leveque M, Salvador-Cartier C, Waget A, Leng L, Bueno L, Bucala R, Fioramonti J. Sex steroid regulation of macrophage migration inhibitory factor in normal and inflamed colon in the female rat. Gastroenterology 132: 982-993, 2007.
26. Hsieh YC, Frink M, Hsieh CH, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH. Downregulation of migration inhibitory factor is critical for estrogen-mediated attenuation of lung tissue damage following traumahemorrhage. Am J Physiol Lung Cell Mol Physiol 292: L1227-L1232, 2007.
27. Ietta F, Todros T, Ticconi C, Piccoli C, Zicari A, Piccione E, Paulesu L. Macrophage migration inhibitory factor in human pregnancy and labor. Am J Reprod Immunol 48: 404-409, 2002.
28. Ietta F, Wu Y, Romagnoli R, Soleymanlou N, Orsini B, Zamudio S, Paulesu L, Caniggia I. Oxygen regulation of macrophage migration inhibitory factor in human placenta. Am J Physiol Endocrinol Metab 292: E272-E280, 2007.
29. Janele D, Lang T, Capellino S, Cutolo M, Da Silva JA, Straub RH. Effects of testosterone, 17beta-estradiol, and downstream estrogens on cytokine secretion from human leukocytes in the presence and absence of cortisol. Ann NY Acad Sci 1069: 168-182, 2006.
30. Jauniaux E, Gulbis B, Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus - a review. Placenta 24, Suppl A: S86-S93, 2003.
31. Kanellopoulos-Langevin C, Caucheteux SM, Verbeke P, Ojcius DM. Tolerance of the fetus by the maternal immune system: role of inflammatory mediators at the feto-maternal interface. Reprod Biol Endocrinol 1: 121, 2003.
32. Kats R, Al-Akoum M, Guay S, Metz C, Akoum A. Cycle-dependent expression of macrophage migration inhibitory factor in the human endometrium. Hum Reprod 20: 3518-3525, 2005.
33. Kayisli UA, Guzeloglu-Kayisli O, Arici A. Endocrine-immune interactions in human endometrium. Ann NY Acad Sci 1034: 50-63, 2004.
34. Kovacs EJ, Messingham K, Gregory MS. Estrogen regulation of immune responses after injury. Mol Cell Endocrinol 193: 129-135, 2002.
35. Lang TJ. Estrogen as an immunomodulator. Clin Immunol 113: 224-230, 2004.
36. Langmann T, Kluchen J, Reil M, Liebisch G, Luciani MF, Chimini G, Kaminski WE, Schmitz G. Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem Biophys Res Commun 257: 29-33, 1999.
37. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R. MIF signal transduction initiated by binding to CD74. J Exp Med 197: 1467-1476, 2003.
38. Liao H, Langmann T, Schmitz G, Zhu Y. Native LDL upregulation of ATP-binding cassette transporter-1 in human vascular endothelial cells. Arterioscler Thromb Vasc Biol 22: 127-132, 2002.
39. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)]. Methods 25: 402-408, 2001.
40. Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect 4: 449-460, 2002.
41. Makrigiannakis A, Minas V, Kalantaridou SN, Nikas G, Chrousos GP. Hormonal and cytokine regulation of early implantation. Trends Endocrinol Metab 17: 178-185, 2006.
42. Martal J, Cédaed L. Endocrine functions of the placenta. In: Reproduction in Mammals and Man, edited by Thibault C, Levasseur MC, and Humter RHF. Paris: Elipses, 1993, p. 435-459.
43. Miller RK, Genbacev O, Turner MA, Aplin JD, Caniggia I, Huppertz B. Human placental explants in culture: approaches and assessments. Placenta 26: 439-448, 2005.
44. Moore NK, Viselli SM. Staining and quantification of proteins transferred to polyvinylidene fluoride membranes. Anal Biochem 279: 241-242, 2000.
45. Nishino T, Bernhagen J, Shiiki H, Calandra T, Dohi K, Bucala R. Localization of macrophage migration inhibitory factor (MIF) to secretory granules within the corticotrophic and thyrotrophic cells of the pituitary gland. Mol Med 1: 781-788, 1995.
46. Onodera S, Kaneda K, Mizue Y, Koyama Y, Fujinaga M, Nishihira J. Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J Biol Chem 275: 444-450, 2000.
47. Oshima S, Onodera S, Amizuka N, Li M, Irie K, Watanabe S, Koyama Y, Nishihira J, Yasuda K, Minami A. Macrophage migration inhibitory factor-deficient mice are resistant to ovariectomy-induced bone loss. FEBS Lett 580: 1251-1256, 2006.
48. Roosbeek S, Peelman F, Verhee A, Labeur C, Caster H, Lensink MF, Cirulli C, Grooten J, Cochet C, Vandekerckhove J, Amoresano A, Chimini G, Tavernier J, Rosseneu M. Phosphorylation by protein kinase CK2 modulates the activity of the ATP binding cassette A1 transporter. J Biol Chem 279: 37779-37788, 2004.
49. Sampey AV, Hall PH, Mitchell RA, Metz CN, Morand EF. Regulation of synoviocyte phospholipase A2 and cyclooxygenase 2 by macrophage migration inhibitory factor. Arthritis Rheum 44: 1273-1280, 2001.
50. Siiteri PK, Stites DP. Immunologic and endocrine interrelationships in pregnancy. Biol Reprod 26: 1-14, 1982.
51. Straub RH. The complex role of estrogens in inflammation. Endocr Rev 28: 521-574, 2007.
52. Todros T, Bontempo S, Piccoli E, Ietta F, Romagnoli R, Biolcati M, Castellucci M, Paulesu L. Increased levels of macrophage migration inhibitory factor (MIF) in preeclampsia. Eur J Obstet Gynecol Reprod Biol 123: 162-166, 2005.
53. Tulchinsky D, Hobel CJ. Plasma human chorionic gonadotropin, estrone, estradiol, estriol, progesterone, and 17-hydroxyprogesterone in human pregnancy. Am J Obstet Gynecol 117: 884-893, 1973.
54. Vegeto E, Belcredito S, Etteri S, Ghisletti S, Brusadelli A, Meda C, Krust A, Dupont S, Ciana P, Chambon P, Maggi A. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J Neurosci 21: 1809-1818, 2001.
55. Verjans E, Noetzel E, Bektas N, Schütz AK, Lue H, Lennartz B, Hartmann A, Dahl E, Bernhagen J. Dual role of macrophage migration inhibitory factor (MIF) in human breast cancer. BMC Cancer 9: 230, 2009.
56. Wada S, Kudo T, Kudo M, Sakuragi N, Hareyama H, Nishihira J, Fujimoto S. Induction of macrophage migration inhibitory factor in human ovary by human chorionic gonadotrophin. Hum Reprod 14: 395-399, 1999.
57. Wellington CL, Walker EK, Suarez A, Kwok A, Bissada N, Singaraja R, Yang YZ, Zhang LH, James E, Wilson JE, Francone O, McManus BM, Hayden MR. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab Invest 82: 273-283, 2002.
58. Yamada H, Kato EH, Morikawa M, Shimada S, Saito H, Watari M, Minakami H, Nishihira J. Decreased serum levels of macrophage migration inhibition factor in miscarriages with normal chromosome karyotype. Hum Reprod 18: 616-620, 2003.
59. Yan X, Orentas RJ, Johnson BD. Tumor-derived macrophage migration inhibitory factor (MIF) inhibits T lymphocyte activation. Cytokine 33: 188-198, 2006.
60. Zeng FY, Weiser WY, Kratzin H, Stahl B, Karas M, Gabius HJ. The major binding protein of the interferon antagonist sarcolectin in human placenta is a macrophage migration inhibitory factor. Arch Biochem Biophys 303: 74-80, 1993.