Progesterone receptor in the vascular endothelium triggers physiological uterine permeability preimplantation

Cell

Volumn 156, Issue 3, 2014, Pages 549-562

  Goddard, Lauren M ^a   Murphy, Thomas J ^a   Org, Tönis ^a   Enciso, Josephine M ^a   Hashimoto Partyka, Minako K ^a   Warren, Carmen M ^a   Domigan, Courtney K ^a   McDonald, Austin I ^a   He, Huanhuan ^b   Sanchez, Lauren A ^a   Allen, Nancy C ^a   Orsenigo, Fabrizio ^c   Chao, Lily C ^a   Dejana, Elisabetta ^c   Tontonoz, Peter ^a   Mikkola, Hanna K A ^a   Iruela Arispe, M Luisa ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR RECEPTOR NUR77; PROGESTERONE; PROGESTERONE RECEPTOR; VASCULOTROPIN; AGGLUTININ; CD31 ANTIGEN; COLLAGEN ANTIBODY; COLLAGEN TYPE 4; LECTIN; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; FEMALE; GENE DELETION; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPH VESSEL; MOUSE; NIDATION; NONHUMAN; OVARY; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; UTERUS; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASCULARIZATION; VEIN; ANIMAL TISSUE; BINDING SITE; CELL JUNCTION; FLUORESCENCE ACTIVATED CELL SORTING; HYPERPLASIA; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RNA SEQUENCE; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; UTERUS WEIGHT; WEIGHT GAIN;

ANIMALS; CAPILLARY PERMEABILITY; ENDOMETRIUM; ENDOTHELIUM, VASCULAR; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MICE; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; UTERUS;

EID: 84893469062     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.12.025     Document Type: Article

References (58)

1. J.F. Arnal, C. Fontaine, A. Billon-Galés, J. Favre, H. Laurell, F. Lenfant, and P. Gourdy Estrogen receptors and endothelium Arterioscler. Thromb. Vasc. Biol. 30 2010 1506 1512
2. G.B. Atkins, M.K. Jain, and A. Hamik Endothelial differentiation: molecular mechanisms of specification and heterogeneity Arterioscler. Thromb. Vasc. Biol. 31 2011 1476 1484
3. I. Behrmann, T. Smyczek, P.C. Heinrich, H. Schmitz-Van de Leur, W. Komyod, B. Giese, G. Müller-Newen, S. Haan, and C. Haan Janus kinase (Jak) subcellular localization revisited: the exclusive membrane localization of endogenous Janus kinase 1 by cytokine receptor interaction uncovers the Jak.receptor complex to be equivalent to a receptor tyrosine kinase J. Biol. Chem. 279 2004 35486 35493
4. S.J. Bernelot Moens, G.R. Schnitzler, M. Nickerson, H. Guo, K. Ueda, Q. Lu, M.J. Aronovitz, H. Nickerson, W.E. Baur, and U. Hansen et al. Rapid estrogen receptor signaling is essential for the protective effects of estrogen against vascular injury Circulation 126 2012 1993 2004
5. J.C. Chappell, and V.L. Bautch Vascular development: genetic mechanisms and links to vascular disease Curr. Top. Dev. Biol. 90 2010 43 72
6. A. Das, S.R. Mantena, A. Kannan, D.B. Evans, M.K. Bagchi, and I.C. Bagchi De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis Proc. Natl. Acad. Sci. USA 106 2009 12542 12547
7. E. Dejana, F. Orsenigo, and M.G. Lampugnani The role of adherens junctions and VE-cadherin in the control of vascular permeability J. Cell Sci. 121 2008 2115 2122
8. H.F. Dvorak Vascular permeability to plasma, plasma proteins, and cells: an update Curr. Opin. Hematol. 17 2010 225 229
9. D.P. Edwards, M. Altmann, A. DeMarzo, Y. Zhang, N.L. Weigel, and C.A. Beck Progesterone receptor and the mechanism of action of progesterone antagonists J. Steroid Biochem. Mol. Biol. 53 1995 449 458
10. X. Fan, S. Krieg, C.J. Kuo, S.J. Wiegand, M. Rabinovitch, M.L. Druzin, R.M. Brenner, L.C. Giudice, and N.R. Nayak VEGF blockade inhibits angiogenesis and reepithelialization of endometrium FASEB J. 22 2008 3571 3580
11. H.L. Franco, C.A. Rubel, M.J. Large, M. Wetendorf, R. Fernandez-Valdivia, J.-W. Jeong, T.E. Spencer, R.R. Behringer, J.P. Lydon, and F.J. Demayo Epithelial progesterone receptor exhibits pleiotropic roles in uterine development and function FASEB J. 26 2012 1218 1227
12. B. Gellersen, I.A. Brosens, and J.J. Brosens Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives Semin. Reprod. Med. 25 2007 445 453
13. M. Hickey, and I.S. Fraser Surface vascularization and endometrial appearance in women with menorrhagia or using levonorgestrel contraceptive implants. Implications for the mechanisms of breakthrough bleeding Hum. Reprod. 17 2002 2428 2434
14. W. Huang, B.T. Sherman, and R.A. Lempicki Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 37 2009 1 13
15. S.M. Hyder, G.M. Stancel, C. Chiappetta, L. Murthy, H.L. Boettger-Tong, and S. Makela Uterine expression of vascular endothelial growth factor is increased by estradiol and tamoxifen Cancer Res. 56 1996 3954 3960
16. M.D. Iafrati, R.H. Karas, M. Aronovitz, S. Kim, T.R. Sullivan Jr.; D.B. Lubahn, T.F. O'Donnell Jr.; K.S. Korach, and M.E. Mendelsohn Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice Nat. Med. 3 1997 545 548
17. P.M. Ismail, J. Li, F.J. DeMayo, B.W. O'Malley, and J.P. Lydon A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development Mol. Endocrinol. 16 2002 2475 2489
18. J.F. Strauss, and R.L. Barbieri Yen and Jaffe's Reproductive Endocrinology 2009 Elsevier Health Sciences Amsterdam
19. K.H. Kim, and J.R. Bender Membrane-initiated actions of estrogen on the endothelium Mol. Cell. Endocrinol. 308 2009 3 8
20. Y. Komarova, and A.B. Malik Regulation of endothelial permeability via paracellular and transcellular transport pathways Annu. Rev. Physiol. 72 2010 463 493
21. G. Kovacs Progestogen-only pills and bleeding disturbances Hum. Reprod. 11 Suppl 2 1996 20 23
22. G. Krikun, F. Schatz, R. Taylor, H.O.D. Critchley, P.A.W. Rogers, J. Huang, and C.J. Lockwood Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression J. Clin. Endocrinol. Metab. 90 2005 1812 1818
23. M.J. Large, and F.J. DeMayo The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling Mol. Cell. Endocrinol. 358 2012 155 165
24. J.P. Lydon, F.J. DeMayo, C.R. Funk, S.K. Mani, A.R. Hughes, C.A. Montgomery Jr.; G. Shyamala, O.M. Conneely, and B.W. O'Malley Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities Genes Dev. 9 1995 2266 2278
25. J.P. Lydon, F.J. DeMayo, O.M. Conneely, and B.W. O'Malley Reproductive phenotpes of the progesterone receptor null mutant mouse J. Steroid Biochem. Mol. Biol. 56 1-6 Spec No 1996 67 77
26. J.A. Maybin, and W.C. Duncan The human corpus luteum: which cells have progesterone receptors? Reproduction 128 2004 423 431
27. N.J. McKenna, and B.W. O'Malley From ligand to response: generating diversity in nuclear receptor coregulator function J. Steroid Biochem. Mol. Biol. 74 2000 351 356
28. F. Orsenigo, C. Giampietro, A. Ferrari, M. Corada, A. Galaup, S. Sigismund, G. Ristagno, L. Maddaluno, G.Y. Koh, and D. Franco et al. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo Nat. Commun. 3 2012 1208
29. M.A. Pearen, and G.E.O. Muscat Minireview: Nuclear hormone receptor 4A signaling: implications for metabolic disease Mol. Endocrinol. 24 2010 1891 1903
30. L. Pei, A. Castrillo, and P. Tontonoz Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77 Mol. Endocrinol. 20 2006 786 794
31. M. Perrot-Applanat, K. Cohen-Solal, E. Milgrom, and M. Finet Progesterone receptor expression in human saphenous veins Circulation 92 1995 2975 2983
32. E.R. Regan, and W.C. Aird Dynamical systems approach to endothelial heterogeneity Circ. Res. 111 2012 110 130
33. C.A. Rubel, R.B. Lanz, R. Kommagani, H.L. Franco, J.P. Lydon, and F.J. DeMayo Research resource: genome-wide profiling of progesterone receptor binding in the mouse uterus Mol. Endocrinol. 26 2012 1428 1442
34. R. Runic, F. Schatz, L. Wan, R. Demopoulos, G. Krikun, and C.J. Lockwood Effects of norplant on endometrial tissue factor expression and blood vessel structure J. Clin. Endocrinol. Metab. 85 2000 3853 3859
35. J.L. Shifren, J.F. Tseng, C.J. Zaloudek, I.P. Ryan, Y.G. Meng, N. Ferrara, R.B. Jaffe, and R.N. Taylor Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis J. Clin. Endocrinol. Metab. 81 1996 3112 3118
36. D. Shoupe, D.R. Mishell Jr.; B.L. Bopp, and M. Fielding The significance of bleeding patterns in Norplant implant users Obstet. Gynecol. 77 1991 256 260
37. N. Sugino, S. Kashida, A. Karube-Harada, S. Takiguchi, and H. Kato Expression of vascular endothelial growth factor (VEGF) and its receptors in human endometrium throughout the menstrual cycle and in early pregnancy Reproduction 123 2002 379 387
38. F. Vázquez, J.C. Rodríguez-Manzaneque, J.P. Lydon, D.P. Edwards, B.W. O'Malley, and M.L. Iruela-Arispe Progesterone regulates proliferation of endothelial cells J. Biol. Chem. 274 1999 2185 2192
39. M. Wetendorf, and F.J. DeMayo The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network Mol. Cell. Endocrinol. 357 2012 108 118
40. Y. Zhao, and D. Bruemmer NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology Arterioscler. Thromb. Vasc. Biol. 30 2010 1535 1541
41. D. Zhao, L. Qin, P.M. Bourbon, L. James, H.F. Dvorak, and H. Zeng Orphan nuclear transcription factor TR3/Nur77 regulates microvessel permeability by targeting endothelial nitric oxide synthase and destabilizing endothelial junctions Proc. Natl. Acad. Sci. USA 108 2011 12066 12071
42. Y. Zhu, Z. Bian, P. Lu, R.H. Karas, L. Bao, D. Cox, J. Hodgin, P.W. Shaul, P. Thoren, and O. Smithies et al. Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta Science 295 2002 505 508
43. J.A. Alva, A.C. Zovein, A. Monvoisin, T. Murphy, A. Salazar, N.L. Harvey, P. Carmeliet, and M.L. Iruela-Arispe VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells Dev. Dyn. 235 2006 759 767
44. D. Blankenberg, A. Gordon, G. Von Kuster, N. Coraor, J. Taylor, A. Nekrutenko Galaxy Team Manipulation of FASTQ data with Galaxy Bioinformatics 26 2010 1783 1785
45. M.J.L. de Hoon, S. Imoto, J. Nolan, and S. Miyano Open source clustering software Bioinformatics 20 2004 1453 1454
46. L.M. Goddard, A.N. Ton, T. Org, H.K.A. Mikkola, and M.L. Iruela-Arispe Selective suppression of endothelial cytokine production by progesterone receptor Vascul. Pharmacol. 59 2013 36 43
47. M.K. Hashimoto-Partyka, J.P. Lydon, and M.L. Iruela-Arispe Generation of a mouse for conditional excision of progesterone receptor Genesis 44 2006 391 395
48. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
49. W.J. Kent, C.W. Sugnet, T.S. Furey, K.M. Roskin, T.H. Pringle, A.M. Zahler, and D. Haussler The human genome browser at UCSC Genome Res. 12 2002 996 1006
50. M. Lakso, J.G. Pichel, J.R. Gorman, B. Sauer, Y. Okamoto, E. Lee, F.W. Alt, and H. Westphal Efficient in vivo manipulation of mouse genomic sequences at the zygote stage Proc. Natl. Acad. Sci. USA 93 1996 5860 5865
51. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
52. S.L. Lee, R.L. Wesselschmidt, G.P. Linette, O. Kanagawa, J.H. Russell, and J. Milbrandt Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nur77) Science 269 1995 532 535
53. C.Y. McLean, D. Bristor, M. Hiller, S.L. Clarke, B.T. Schaar, C.B. Lowe, A.M. Wenger, and G. Bejerano GREAT improves functional interpretation of cis-regulatory regions Nat. Biotechnol. 28 2010 495 501
54. A.E. Moran, K.L. Holzapfel, Y. Xing, N.R. Cunningham, J.S. Maltzman, J. Punt, and K.A. Hogquist T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse J. Exp. Med. 208 2011 1279 1289
55. P. Soriano Generalized lacZ expression with the ROSA26 Cre reporter strain Nat. Genet. 21 1999 70 71
56. C. Trapnell, L. Pachter, and S.L. Salzberg TopHat: discovering splice junctions with RNA-Seq Bioinformatics 25 2009 1105 1111
57. C. Trapnell, B.A. Williams, G. Pertea, A. Mortazavi, G. Kwan, M.J. van Baren, S.L. Salzberg, B.J. Wold, and L. Pachter Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Nat. Biotechnol. 28 2010 511 515
58. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137