Selective suppression of endothelial cytokine production by progesterone receptor

Vascular Pharmacology

Volumn 59, Issue 1-2, 2013, Pages 36-43

  Goddard, Lauren M ^a   Ton, Amy N ^a   Org, Tõnis ^a   Mikkola, Hanna K A ^a   Iruela Arispe, M Luisa ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Immune cell; Inflammation; Reproduction; Steroid hormone

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYTOKINE; INTERLEUKIN 6; INTERLEUKIN 8; LENTIVIRUS VECTOR; LIPOPOLYSACCHARIDE; PROGESTERONE; PROGESTERONE RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; ENDOTHELIUM; HUMAN; HUMAN CELL; IMMUNOREGULATION; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA SEQUENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UMBILICAL VEIN ENDOTHELIAL CELL;

4′,6-DIAMIDINO-2-PHENYLINDOLE; DAPI; HPR; HUMAN PROGESTERONE RECEPTOR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELL; HUVEC; IMMUNE CELL; INFLAMMATION; LIPOPOLYSACCHARIDE; LPS; PR; PRKO; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR KNOCKOUT; REPRODUCTION; STEROID HORMONE;

CELLS, CULTURED; CHEMOKINES, CXC; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; PROGESTERONE; RECEPTORS, PROGESTERONE; TRANSCRIPTION, GENETIC;

EID: 84880703929     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2013.06.001     Document Type: Article

References (60)

1. Adams Waldorf K.M., Nelson J.L. Autoimmune disease during pregnancy and the microchimerism legacy of pregnancy. Immunol. Invest. 2008, 37:631-644.
2. Angstwurm M.W., Gärtner R., Ziegler-Heitbrock H.W. Cyclic plasma IL-6 levels during normal menstrual cycle. Cytokine 1997, 9:370-374.
3. Butts C., Bowers E., Horn J., Shukair S., Belyavskaya E., Tonelli L., Sternberg E. Inhibitory effects of progesterone differ in dendritic cells from female and male rodents. Gend. Med. 2008, 5:434-447.
4. Challis J.R., Lockwood C.J., Myatt L., Norman J.E., Strauss J.F., Petraglia F. Inflammation and pregnancy. Reprod. Sci. 2009, 16:206-215.
5. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 1987, 7:2745-2752.
6. Critchley H.O., Kelly R.W., Lea R.G., Drudy T.A., Jones R.L., Baird D.T. Sex steroid regulation of leukocyte traffic in human decidua. Hum. Reprod. 1996, 11:2257-2262.
7. Critchley H.O., Jones R.L., Lea R.G., Drudy T.A., Kelly R.W., Williams A.R., Baird D.T. Role of inflammatory mediators in human endometrium during progesterone withdrawal and early pregnancy. J. Clin. Endocrinol. Metab. 1999, 84:240-248.
8. de Hoon M.J.L., Imoto S., Nolan J., Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454.
9. Gilliver S.C. Sex steroids as inflammatory regulators. J. Steroid Biochem. Mol. Biol. 2010, 120:105-115.
10. Gotkin J.L., Celver J., McNutt P., Shields A.D., Howard B.C., Paonessa D.J., Napolitano P.G. Progesterone reduces lipopolysaccharide induced interleukin-6 secretion in fetoplacental chorionic arteries, fractionated cord blood, and maternal mononuclear cells. Am. J. Obstet. Gynecol. 2006, 195:1015-1019.
11. Hamilton S., Oomomian Y., Stephen G., Shynlova O., Tower C.L., Garrod A., Lye S.J., Jones R.L. Macrophages infiltrate the human and rat decidua during term and preterm labor: evidence that decidual inflammation precedes labor. Biol. Reprod. 2012, 86:39.
12. Hamilton S.A., Tower C.L., Jones R.L. Identification of chemokines associated with the recruitment of decidual leukocytes in human labour: potential novel targets for preterm labour. PLoS One 2013, 8:e56946.
13. Hannan N.J., Jones R.L., Critchley H.O.D., Kovacs G.J., Rogers P.A.W., Affandi B., Salamonsen L.A. Coexpression of fractalkine and its receptor in normal human endometrium and in endometrium from users of progestin-only contraception supports a role for fractalkine in leukocyte recruitment and endometrial remodeling. J. Clin. Endocrinol. Metab. 2004, 89:6119-6129.
14. Hardy D.B., Janowski B.A., Corey D.R., Mendelson C.R. Progesterone receptor plays a major antiinflammatory role in human myometrial cells by antagonism of nuclear factor-kappaB activation of cyclooxygenase 2 expression. Mol. Endocrinol. 2006, 20:2724-2733.
15. Henriet P., Gaide Chevronnay H.P., Marbaix E. The endocrine and paracrine control of menstruation. Mol. Cell. Endocrinol. 2012, 358:197-207.
16. Hughes G.C. Progesterone and autoimmune disease. Autoimmun. Rev. 2012, 11:A502-A514.
17. Ingegno M.D., Money S.R., Thelmo W., Greene G.L., Davidian M., Jaffe B.M., Pertschuk L.P. Progesterone receptors in the human heart and great vessels. Lab. Invest. 1988, 59:353-356.
18. Iruela-Arispe M.L., Rodriguez-Manzaneque J.C., Abu-Jawdeh G. Endometrial endothelial cells express estrogen and progesterone receptors and exhibit a tissue specific response to angiogenic growth factors. UMIC 1999, 6:127-140.
19. Jones R.L. Identification of chemokines important for leukocyte recruitment to the human endometrium at the times of embryo implantation and menstruation. J. Clin. Endocrinol. Metab. 2004, 89:6155-6167.
20. Jones R.L., Kelly R.W., Critchley H.O. Chemokine and cyclooxygenase-2 expression in human endometrium coincides with leukocyte accumulation. Hum. Reprod. 1997, 12:1300-1306.
21. Kaushic C., Roth K.L., Anipindi V., Xiu F. Increased prevalence of sexually transmitted viral infections in women: the role of female sex hormones in regulating susceptibility and immune responses. J. Reprod. Immunol. 2011, 88:204-209.
22. Kavandi L., Collier M.A., Nguyen H., Syed V. Progesterone and calcitriol attenuate inflammatory cytokines CXCL1 and CXCL2 in ovarian and endometrial cancer cells. J. Cell. Biochem. 2012, 113:3143-3152.
23. Kelly R.W., Illingworth P., Baldie G., Leask R., Brouwer S., Calder A.A. Progesterone control of interleukin-8 production in endometrium and chorio-decidual cells underlines the role of the neutrophil in menstruation and parturition. Hum. Reprod. 1994, 9:253-258.
24. King A.E., Critchley H.O.D. Oestrogen and progesterone regulation of inflammatory processes in the human endometrium. J. Steroid Biochem. Mol. Biol. 2010, 120:116-126.
25. Krikun G., Schatz F., Taylor R., Critchley H.O.D., Rogers P.A.W., Huang J., Lockwood C.J. Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression. J. Clin. Endocrinol. Metab. 2005, 90:1812-1818.
26. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
27. Ley K., Laudanna C., Cybulsky M.I., Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 2007, 7:678-689.
28. Loudon J.A.Z., Elliott C.L., Hills F., Bennett P.R. Progesterone represses interleukin-8 and cyclo-oxygenase-2 in human lower segment fibroblast cells and amnion epithelial cells. Biol. Reprod. 2003, 69:331-337.
29. Luk J., Seval Y., Ulukus M., Ulukus E.C., Arici A., Kayisli U.A. Regulation of monocyte chemotactic protein-1 expression in human endometrial endothelial cells by sex steroids: a potential mechanism for leukocyte recruitment in endometriosis. Reprod. Sci. 2010, 17:278-287.
30. MacIntyre D.A., Sykes L., Teoh T.G., Bennett P.R. Prevention of preterm labour via the modulation of inflammatory pathways. J. Matern. Fetal Neonatal Med. 2012, 25(Suppl. 1):17-20.
31. Martocchia A., Stefanelli M., Cola S., Falaschi P. Sex steroids in autoimmune diseases. Curr. Top. Med. Chem. 2011, 11:1668-1683.
32. Maybin J.A., Duncan W.C. The human corpus luteum: which cells have progesterone receptors?. Reproduction 2004, 128:423-431.
33. McCombe P.A., Greer J.M., Mackay I.R. Sexual dimorphism in autoimmune disease. Curr. Mol. Med. 2009, 9:1058-1079.
34. McLean C.Y., Bristor D., Hiller M., Clarke S.L., Schaar B.T., Lowe C.B., Wenger A.M., Bejerano G. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 2010, 28:495-501.
35. Meyer M.R., Haas E., Barton M. Gender differences of cardiovascular disease: new perspectives for estrogen receptor signaling. Hypertension 2006, 47:1019-1026.
36. Naldini L., Blömer U., Gage F.H., Trono D., Verma I.M. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11382-11388.
37. Norman J.E., Bollapragada S., Yuan M., Nelson S.M. Inflammatory pathways in the mechanism of parturition. BMC Pregnancy Childbirth 2007, 7(Suppl. 1):S7.
38. Oertelt-Prigione S. Immunology and the menstrual cycle. Autoimmun. Rev. 2012, 11:A486-A492.
39. Okada M., Matsumori A., Ono K., Furukawa Y., Shioi T., Iwasaki A., Matsushima K., Sasayama S. Cyclic stretch upregulates production of interleukin-8 and monocyte chemotactic and activating factor/monocyte chemoattractant protein-1 in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 1998, 18:894-901.
40. Otsuki M., Saito H., Xu X., Sumitani S., Kouhara H., Kishimoto T., Kasayama S. Progesterone, but not medroxyprogesterone, inhibits vascular cell adhesion molecule-1 expression in human vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2001, 21:243-248.
41. Perrot-Applanat M., Cohen-Solal K., Milgrom E., Finet M. Progesterone receptor expression in human saphenous veins. Circulation 1995, 92:2975-2983.
42. Pober J.S., Sessa W.C. Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 2007, 7:803-815.
43. Red-Horse K., Drake P.M. Human pregnancy: the role of chemokine networks at the fetalmaternal interface. Expert. Rev. Mol. Med. 2004, 6:1-14.
44. Robertson S.A., Christiaens I., Dorian C.L., Zaragoza D.B., Care A.S., Banks A.M., Olson D.M. Interleukin-6 is an essential determinant of on-time parturition in the mouse. Endocrinology 2010, 151:3996-4006.
45. Rodríguez-Manzaneque J.C., Graubert M., Iruela-Arispe M.L. Endothelial cell dysfunction following prolonged activation of progesterone receptor. Hum. Reprod. 2000, 15(Suppl. 3):39-47.
46. Romano M., Sironi M., Toniatti C., Polentarutti N., Fruscella P., Ghezzi P., Faggioni R., Luini W., van Hinsbergh V., Sozzani S., Bussolino F., Poli V., Ciliberto G., Mantovani A. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 1997, 6:315-325.
47. Sakoda T., Kaibuchi K., Kishi K., Kishida S., Doi K., Hoshino M., Hattori S., Takai Y. smg/rap1/Krev-1 p21s inhibit the signal pathway to the c-fos promoter/enhancer from c-Ki-ras p21 but not from c-raf-1 kinase in NIH3T3 cells. Oncogene 1992, 7:1705-1711.
48. Sakoda T., Kasahara N., Hamamori Y., Kedes L. A high-titer lentiviral production system mediates efficient transduction of differentiated cells including beating cardiac myocytes. J. Mol. Cell. Cardiol. 1999, 31:2037-2047.
49. Shields A.D., Wright J., Paonessa D.J., Gotkin J., Howard B.C., Hoeldtke N.J., Napolitano P.G. Progesterone modulation of inflammatory cytokine production in a fetoplacental artery explant model. Am. J. Obstet. Gynecol. 2005, 193:1144-1148.
50. Shynlova O., Tsui P., Dorogin A., Lye S.J. Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor. J. Immunol. 2008, 181:1470-1479.
51. Simoncini T. Differential signal transduction of progesterone and medroxyprogesterone acetate in human endothelial cells. Endocrinology 2004, 145:5745-5756.
52. Tibbetts T.A., Conneely O.M., O'Malley B.W. Progesterone via its receptor antagonizes the pro-inflammatory activity of estrogen in the mouse uterus. Biol. Reprod. 1999, 60:1158-1165.
53. Tibbetts T.A., DeMayo F., Rich S., Conneely O.M., O'Malley B.W. Progesterone receptors in the thymus are required for thymic involution during pregnancy and for normal fertility. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:12021-12026.
54. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
55. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
56. van Mourik M.S.M., Macklon N.S., Heijnen C.J. Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J. Leukoc. Biol. 2009, 85:4-19.
57. Vázquez F., Rodríguez-Manzaneque J.C., Lydon J.P., Edwards D.P., O'Malley B.W., Iruela-Arispe M.L. Progesterone regulates proliferation of endothelial cells. J. Biol. Chem. 1999, 274:2185-2192.
58. Zhang J., Lathbury L.J., Salamonsen L.A. Expression of the chemokine eotaxin and its receptor, CCR3, in human endometrium. Biol. Reprod. 2000, 62:404-411.
59. Zhang Y., Liu T., Meyer C.A., Eeckhoute J., Johnson D.S., Bernstein B.E., Nusbaum C., Myers R.M., Brown M., Li W., Liu X.S. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008, 9:R137.
60. Zhao Y., Koga K., Osuga Y., Izumi G., Takamura M., Harada M., Hirata T., Hirota Y., Yoshino O., Inoue S., Fujii T., Kozuma S. Cyclic stretch augments production of neutrophil chemokines and matrix metalloproteinases-1 (MMP-1) from human decidual cells, and the production was reduced by progesterone. Am. J. Reprod. Immunol. 2013, 69:454-462.