Progesterone-induced activation of membrane-bound progesterone receptors in murine macrophage cells

Journal of Endocrinology

Volumn 224, Issue 2, 2015, Pages 183-194

  Lu, Jing ^a,b   Reese, Joshua ^a   Zhou, Ying ^a   Hirsch, Emmet ^a,b  

^a NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Inflammatory response; Macrophages; Membrane progesterone receptor; Progesterone

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; BOVINE SERUM ALBUMIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOOXYGENASE 2; HORMONE RECEPTOR; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; OXYTOCIN RECEPTOR; PROGESTERONE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR ALPHA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PTGS2 PROTEIN, MOUSE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIRTH; CELL FUNCTION; CELLS; CONJUGATION; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE TARGETING; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; CELL CULTURE; CELL MEMBRANE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; UPREGULATION;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CYCLOOXYGENASE 2; GENE EXPRESSION; INTERLEUKIN-1BETA; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; PROGESTERONE; RECEPTORS, PROGESTERONE; UP-REGULATION;

EID: 84921341540     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0470     Document Type: Article

References (63)

1. Blackmore PF, Neulen J, Lattanzio F & Beebe SJ 1991 Cell surface-binding sites for progesterone mediate calcium uptake in human sperm. Journal of Biological Chemistry 18655-18659.
2. Care AS, Diener KR, Jasper MJ, Brown HM, Ingman WV & Robertson SA 2013 Macrophages regulate corpus luteum development during embryo implantation in mice. Journal of Clinical Investigation 123 3472-3487. (doi:10.1172/JCI60561)
3. Chandra G, Cogswell JP, Miller LR, Godlevski MM, Stinnett SW, Noel SL, Kadwell SH, Kost TA & Gray JG 1995 Cyclic AMP signaling pathways are important in IL-1b transcriptional regulation. Journal of Immunology 155 4535-4543.
4. Cho H, Aronica SM & Katzenellenbogen BS 1994 Regulation of progesterone receptor gene expression in MCF-7 breast cancer cells: a comparison of the effects of cyclic adenosine 30, 50 -monophosphate, estradiol, insulin-like growth factor-I, and serum factors. Endocrinology 134 658-664. (doi:10.1210/endo.134.2.7507831)
5. Conneely OM, Mulac-Jericevic B & Lydon JP 2003 Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms. Steroids 68 771-778. (doi:10.1016/S0039-128X(03)00126-0)
6. Csapo A 1956 Progesterone block. American Journal of Anatomy 98 273-291. (doi:10.1002/aja.1000980206)
7. Dosiou C & Giudice LC 2005 Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocrine Reviews 26 44-62. (doi:10.1210/er.2003-0021)
8. Dosiou C, Hamilton AE, Pang Y, Overgaard MT, Tulac S, Dong J, Thomas P & Giudice LC 2008 Expression of membrane progesterone receptors on human T lymphocytes and Jurkat cells and activation of G-proteins by progesterone. Journal of Endocrinology 196 67-77. (doi:10.1677/JOE-07-0317)
9. Drake MT, Shenoy SK & Lefkowitz RJ 2006 Trafficking of G protein-coupled receptors. Circulation Research 99 570-582. (doi:10.1161/01.RES. 0000242563.47507.ce)
10. Dressing GE, Goldberg JE, Charles NJ, Schwertfeger KL & Lange CA 2011 Membrane progesterone receptor expression in mammalian tissues: a review of regulation and physiological implications. Steroids 76 11-17. (doi:10.1016/j.steroids.2010.09.006)
11. Druckmann R & Druckmann MA 2005 Progesterone and the immunology of pregnancy. Journal of Steroid Biochemistry and Molecular Biology 97 389-396. (doi:10.1016/j.jsbmb.2005.08.010)
12. Feng L, Antczak BC, Lan L, Grotegut CA, Thompson JL, Allen TK & Murtha AP 2014 Progesterone receptor membrane component 1 (PGRMC1) expression in fetal membranes among women with preterm premature rupture of the membranes (PPROM). Placenta 35 331-333. (doi:10.1016/j.placenta.2014.03.008)
13. Fernandes MS, Brosens JJ & Gellersen B 2008 Honey, we need to talk about the membrane progestin receptors. Steroids 73 942-952. (doi:10.1016/j.steroids.2007.12.004)
14. Flock GB, Cao X, Maziarz M & Drucker DJ 2013 Activation of entero-endocrine membrane progesterone receptors promotes incretin secretion and improves glucose tolerance in mice. Diabetes 62 283-290. (doi:10.2337/db12-0601)
15. Fuchs AR, Fuchs F, Husslein P & Soloff MS 1984 Oxytocin receptors in the human uterus during pregnancy and parturition. American Journal of Obstetrics and Gynecology 734-741. (doi:10.1016/0002-9378(84)90677-X)
16. Gaetjens E & Pertschuk LP 1980 Synthesis of fluorescein labelled steroid hormone-albumin conjugates for the fluorescent histochemical detection of hormone receptors. Journal of Steroid Biochemistry 13 1001-1003. (doi:10.1016/0022-4731(80)90177-6)
17. Gellersen B, Fernandes MS & Brosens JJ 2009 Non-genomic progesterone actions in female reproduction. Human Reproduction Update 15 119-138. (doi:10.1093/humupd/dmn044)
18. Ghosh R, Garcia GE, Crosby K, Inoue H, Thompson IM, Troyer DA & Kumar AP 2007 Regulation of Cox-2 by cyclic AMP response element binding protein in prostate cancer: potential role for nexrutine. Neoplasia 893-899. (doi:10.1593/neo.07502)
19. Gonzalez GA & Montminy MR 1989 Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59 675-680. (doi:10.1016/0092-8674(89)90013-5)
20. Hadcock JR & Malbon CC 1988 Down-regulation of b-adrenergic receptors: agonist-induced reduction in receptor mRNA levels. PNAS 85 5021-5025. (doi:10.1073/pnas.85.14.5021)
21. Hamilton S, Oomomian Y, Stephen G, Shynlova O, Tower CL, Garrod A, Lye SJ & Jones RL 2012 Macrophages infiltrate the human and rat decidua during term and preterm labor: evidence that decidual inflammation precedes labor. Biology of Reproduction 86 39. (doi:10.1095/biolreprod.111.095505)
22. Horwitz KB, Mockus MB & Lessey BA 1982 Variant T47D human breast cancer cells with high progesterone-receptor levels despite estrogen and antiestrogen resistance. Cell 28 633-642. (doi:10.1016/0092-8674(82)90218-5)
23. Kammerer U, Schoppet M, McLellan AD, Kapp M, Huppertz HI, Kampgen E & Dietl J 2000 Human decidua contains potent immunostimulatory CD83C dendritic cells. American Journal of Pathology 157 159-169. (doi:10.1016/S0002-9440(10)64527-0)
24. Karteris E, Zervou S, Pang Y, Dong J, Hillhouse EW, Randeva HS & Thomas P 2006 Progesterone signaling in human myometrium through two novel membrane G protein-coupled receptors: potential role in functional progesterone withdrawal at term. Molecular Endocrinology 20 1519-1534. (doi:10.1210/me.2005-0243)
25. Kelder J, Azevedo R, Pang Y, de Vlieg J, Dong J & Thomas P 2010 Comparison between steroid binding to membrane progesterone receptor alpha (mPRa) and to nuclear progesterone receptor: correlation with physicochemical properties assessed by comparative molecular field analysis and identification of mPRa-specific agonists. Steroids 75 314-322. (doi:10.1016/j.steroids.2010.01.010)
26. Kombe A, Sirois J & Goff AK 2003 Prolonged progesterone treatment of endometrial epithelial cells modifies the effect of estradiol on their sensitivity to oxytocin. Steroids 68 651-658. (doi:10.1016/S0039-128X(03)00094-1)
27. Krietsch T, Fernandes MS, Kero J, Losel R, Heyens M, Lam EW, Huhtaniemi I, Brosens JJ & Gellersen B 2006 Human homologs of the putative G protein-coupled membrane progestin receptors (mPRa, b, and g) localize to the endoplasmic reticulum and are not activated by progesterone. Molecular Endocrinology 20 3146-3164. (doi:10.1210/me.2006-0129)
28. Lee Y, Sooranna SR, Terzidou V, Christian M, Brosens J, Huhtinen K, Poutanen M, Barton G, Johnson MR & Bennett PR 2012 Interactions between inflammatory signals and the progesterone receptor in regulating gene expression in pregnant human uterine myocytes. Journal of Cellular and Molecular Medicine 2487-2503. (doi:10.1111/j.1582-4934.2012.01567.x)
29. Liang J, Sun L, Wang Q & Hou Y 2006 Progesterone regulates mouse dendritic cells differentiation and maturation. International Immuno-pharmacology 6 830-838. (doi:10.1016/j.intimp.2005.12.002)
30. Lu CC & Tsai SC 2007 The cyclic AMP-dependent protein kinase A pathway is involved in progesterone effects on calcitonin secretion from TT cells. Life Sciences 81 1411-1420. (doi:10.1016/j.lfs.2007.08.046)
31. Mackler AM, Iezza G, Akin MR, McMillan P & Yellon SM 1999 Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. Biology of Reproduction 61 879-883. (doi:10.1095/biolreprod61.4.879)
32. Mansour I, Reznikoff-Etievant MF & Netter A 1994 No evidence for the expression of the progesterone receptor on peripheral blood lympho-cytes during pregnancy. Human Reproduction 9 1546-1549.
33. Meis PJ, Klebanoff M, Thom E, Dombrowski MP, Sibai B, Moawad AH, Spong CY, Hauth JC, Miodovnik M, Varner MW et al. 2003 Prevention of recurrent preterm delivery by 17a-hydroxyprogesterone caproate. New England Journal of Medicine 2379-2385. (doi:10.1056/NEJMoa035140)
34. Merlino AA, Welsh TN, Tan H, Yi LJ, Cannon V, Mercer BM & Mesiano S 2007 Nuclear progesterone receptors in the human pregnancy myometrium: evidence that parturition involves functional progesterone withdrawal mediated by increased expression of progesterone receptor-A. Journal of Clinical Endocrinology and Metabolism 92 1927-1933. (doi:10.1210/jc.2007-0077)
35. Mesiano S, Wang Y & Norwitz ER 2011 Progesterone receptors in the human pregnancy uterus: do they hold the key to birth timing?. Reproductive Sciences 18 6-19. (doi:10.1177/1933719110382922)
36. Miller L & Hunt JS 1996 Sex steroid hormones and macrophage function. Life Sciences 1-14. (doi:10.1016/0024-3205(96)00122-1)
37. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP & Conneely OM 2000 Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289 1751-1754. (doi:10.1126/science.289.5485.1751)
38. Murata T, Murata E, Liu CX, Narita K, Honda K & Higuchi T 2000 Oxytocin receptor gene expression in rat uterus: regulation by ovarian steroids. Journal of Endocrinology 166 45-52. (doi:10.1677/joe.0.1660045)
39. Ndiaye K, Poole DH & Pate JL 2008 Expression and regulation of functional oxytocin receptors in bovine T lymphocytes. Biology of Reproduction 78 786-793. (doi:10.1095/biolreprod.107.065938)
40. Ndiaye K, Poole DH, Walusimbi S, Cannon MJ, Toyokawa K, Maalouf SW, Dong J, Thomas P & Pate JL 2012 Progesterone effects on lymphocytes may be mediated by membrane progesterone receptors. Journal of Reproductive Immunology 95 15-26. (doi:10.1016/j.jri.2012.04.004)
41. Ou CW, Chen ZQ, Qi S & Lye SJ 1998 Increased expression of the rat myometrial oxytocin receptor messenger ribonucleic acid during labor requires both mechanical and hormonal signals. Biology of Reproduction 59 1055-1061. (doi:10.1095/biolreprod59.5.1055)
42. Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sampognaro S, Parronchi P, Manetti R, Annunziato F, Livi C et al. 1995 Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. Journal of Immunology 155 128-133.
43. Pieber D, Allport VC, Hills F, Johnson M & Bennett PR 2001 Interactions between progesterone receptor isoforms in myometrial cells in human labour. Molecular Human Reproduction 7 875-879. (doi:10.1093/molehr/7.9.875)
44. Raghupathy R 1997 Th1-type immunity is incompatible with successful pregnancy. Immunology Today 18 478-482. (doi:10.1016/S0167-5699(97)01127-4)
45. Raghupathy R, Al-Mutawa E, Al-Azemi M, Makhseed M, Azizieh F & Szekeres-Bartho J 2009 Progesterone-induced blocking factor (PIBF) modulates cytokine production by lymphocytes from women with recurrent miscarriage or preterm delivery. Journal of Reproductive Immunology 80 91-99. (doi:10.1016/j.jri.2009.01.004)
46. Renthal NE, Chen CC, Williams KC, Gerard RD, Prange-Kiel J & Mendelson CR 2010 miR-200 family and targets, ZEB1 and ZEB2, modulate uterine quiescence and contractility during pregnancy and labor. PNAS 107 20828-20833. (doi:10.1073/pnas.1008301107)
47. Santos SJ, Aupperlee MD, Xie J, Durairaj S, Miksicek R, Conrad SE, Leipprandt JR, Tan YS, Schwartz RC & Haslam SZ 2009 Progesterone receptor A-regulated gene expression in mammary organoid cultures. Journal of Steroid Biochemistry and Molecular Biology 115 161-172. (doi:10.1016/j.jsbmb.2009.04.001)
48. Shynlova O, Nedd-Roderique T, Li Y, Dorogin A & Lye SJ 2013 Myometrial immune cells contribute to term parturition, preterm labour and post-partum involution in mice. Journal of Cellular and Molecular Medicine 17 90-102. (doi:10.1111/j.1582-4934.2012.01650.x)
49. Smith JL, Kupchak BR, Garitaonandia I, Hoang LK, Maina AS, Regalla LM & Lyons TJ 2008 Heterologous expression of human mPRa, mPRb and mPRg in yeast confirms their ability to function as membrane progesterone receptors. Steroids 73 1160-1173. (doi:10.1016/j.steroids.2008.05.003)
50. Sulke AN, Jones DB & Wood PJ 1985 Hormonal modulation of human natural killer cell activity in vitro. Journal of Reproductive Immunology 7 105-110. (doi:10.1016/0165-0378(85)90064-6)
51. Sykes L, MacIntyre DA, Yap XJ, Teoh TG & Bennett PR 2012 The Th1:Th2 dichotomy of pregnancy and preterm labour. Mediators of Inflammation 2012 967629. (doi:10.1155/2012/967629)
52. Szekeres-Bartho J & Chaouat G 1990 Lymphocyte-derived progesterone-induced blocking factor corrects resorption in a murine abortion system. American Journal of Reproductive Immunology 23 26-28. (doi:10.1111/j.1600-0897.1990.tb00664.x)
53. Szekeres-Bartho J, Szekeres G, Debre P, Autran B & Chaouat G 1990 Reactivity of lymphocytes to a progesterone receptor-specific mono-clonal antibody. Cellular Immunology 125 273-283. (doi:10.1016/0008-8749(90)90083-4)
54. Szekeres-Bartho J, Halasz M & Palkovics T 2009 Progesterone in pregnancy; receptor-ligand interaction and signaling pathways. Journal of Reproductive Immunology 83 60-64. (doi:10.1016/j.jri.2009.06.262)
55. Szeto A, Nation DA, Mendez AJ, Dominguez-Bendala J, Brooks LG, Schneiderman N & McCabe PM 2008 Oxytocin attenuates NADPH-dependent superoxide activity and IL-6 secretion in macrophages and vascular cells. American Journal of Physiology Endocrinology and Metabolism E1495-E1501. (doi:10.1152/ajpendo. 90718.2008)
56. Tan H, Yi L, Rote NS, Hurd WW & Mesiano S 2012 Progesterone receptor-A and -B have opposite effects on proinflammatory gene expression in human myometrial cells: implications for progesterone actions in human pregnancy and parturition. Journal of Clinical Endocrinology and Metabolism 97 E719-E730. (doi:10.1210/jc.2011-3251)
57. Thomas P 2008 Characteristics of membrane progestin receptor alpha (mPRa) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Frontiers in Neuroendocrinology 29 292-312. (doi:10.1016/j.yfrne.2008.01.001)
58. Thomas P, Pang Y, Dong J, Groenen P, Kelder J, de Vlieg J, Zhu Y & Tubbs C 2007 Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor a subtypes and their evolution-ary origins. Endocrinology 148 705-718. (doi:10.1210/en.2006-0974)
59. Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJ, Cameron IT, Greer IA & Norman JE 1999 Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Human Reproduction 14 229-236. (doi:10.1093/humrep/14.1.229)
60. Webster JI, Tonelli L & Sternberg EM 2002 Neuroendocrine regulation of immunity. Annual Review of Immunology 20 125-163. (doi:10.1146/annurev.immunol.20.082401.104914)
61. Wortzel I & Seger R 2011 The ERK cascade: distinct functions within various subcellular organelles. Genes & Cancer 2 195-209. (doi:10.1177/1947601911407328)
62. Zakar T & Hertelendy F 2007 Progesterone withdrawal: key to parturition. American Journal of Obstetrics and Gynecology 289-296. (doi:10.1016/j.ajog.2006.09.005)
63. Zhu Y, Rice CD, Pang Y, Pace M & Thomas P 2003 Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. PNAS 100 2231-2236. (doi:10.1073/pnas.0336132100)