Decidualization induces a secretome switch in perivascular niche cells of the human endometrium

Endocrinology (United States)

Volumn 155, Issue 11, 2014, Pages 4542-4553

  Murakami, Keisuke ^a,b   Lee, Yie Hou ^c   Lucas, Emma S ^a   Chan, Yi Wah ^d   Durairaj, Ruban Peter ^a   Takeda, Satoru ^b   Moore, Jonathan D ^d   Tan, Bee K ^a   Quenby, Siobhan ^a   Chan, Jerry K Y ^e,f   Gargett, Caroline E ^g,h   Brosens, Jan J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^d UNIVERSITY OF WARWICK   (United Kingdom)

^e KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^f DUKE NUS MEDICAL SCHOOL   (Singapore)

^g HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^h MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

KI 67 ANTIGEN; LEUKEMIA INHIBITORY FACTOR; MEMBRANE PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 3; SUSHI DOMAIN CONTAINING 2; UNCLASSIFIED DRUG; NOTCH RECEPTOR; PROTEOME; SUSD2 PROTEIN, HUMAN; TRANSCRIPTOME;

ADULT; ARTICLE; CELL CONTACT; CELL CULTURE; CELL CYCLE; CELL DENSITY; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL FUNCTION; CELL ISOLATION; CELL POPULATION; CELL SELECTION; CELL SUSPENSION; CONTACT INHIBITION; DECIDUALIZATION; DOWN REGULATION; ENDOMETRIUM; ENDOMETRIUM BIOPSY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INNATE IMMUNITY; PERIVASCULAR NICHE CELL; PHENOTYPE; PROTEIN EXPRESSION; RNA SEQUENCE; SECRETOME SWITCH; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL NICHE; STROMA CELL; TISSUE DISTRIBUTION; TROPHOBLAST; UPREGULATION; WESTERN BLOTTING; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; NIDATION; PERICYTE; PHYSIOLOGY; PREGNANCY; SECRETION (PROCESS);

ADULT; CELLS, CULTURED; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE GLYCOPROTEINS; MESENCHYMAL STROMAL CELLS; PERICYTES; PREGNANCY; PROTEOME; RECEPTORS, NOTCH; STEM CELL NICHE; TRANSCRIPTOME;

EID: 84908032073     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1370     Document Type: Article

References (65)

1. Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: A review of the literature. Am J Obstet Gynecol. 2002;187:1416-1423.
2. Emera D, Romero R, Wagner G. The evolution of menstruation: a new model for genetic assimilation: explaining molecular origins of maternal responses to fetal invasiveness. Bioessays. 2012;34:26-35.
3. Brosens JJ, Hayashi N, White JO. Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology. 1999;140:4809-4820.
4. Gellersen B, Brosens J. Cyclic AMP and progesterone receptor crosstalk in human endometrium: A decidualizing affair. J Endocrinol. 2003;178:357-372.
5. Jones MC, Fusi L, Higham JH, et al. Regulation of the SUMO pathway sensitizes differentiating human endometrial stromal cells to progesterone. Proc Natl Acad Sci USA. 2006;103:16272-16277.
6. Brosens JJ, Salker MS, Teklenburg G, et al. Uterine selection of human embryos at implantation. Sci Rep. 2014;4:3894.
7. Teklenburg G, Salker M, Molokhia M, et al. Natural selection of human embryos: Decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation. PLoS One. 2010;5:e10258.
8. Weimar CH, Kavelaars A, Brosens JJ, et al. Endometrial stromal cells of women with recurrent miscarriage fail to discriminate between high- and low-quality human embryos. PLoS One. 2012;7:e41424.
9. Kajihara T, Jones M, Fusi L, et al. Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization. Mol Endocrinol. 2006;20:2444-2455.
10. Leitao B, Jones MC, Fusi L, et al. Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals. Faseb J. 2010;24:1541-1551.
11. Nancy P, Tagliani E, Tay CS, Asp P, Levy DE, Erlebacher A. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science. 2012;336:1317-1321.
12. Zhang S, Lin H, Kong S, et al. Physiological and molecular determinants of embryo implantation. Mol Aspects Med. 2013;34:939-980.
13. Gonzalez M, Neufeld J, Reimann K, et al. Expansion of human trophoblastic spheroids is promoted by decidualized endometrial stromal cells and enhanced by heparin-binding epidermal growth factor-like growth factor and interleukin-1 β. Mol Hum Reprod. 2011;17:421-433.
14. Grewal S, Carver JG, Ridley AJ, Mardon HJ. Implantation of the human embryo requires Rac1-dependent endometrial stromal cell migration. Proc Natl Acad Sci USA. 2008;105:16189-16194.
15. Lockwood CJ, Krikun G, Rahman M, Caze R, Buchwalder L, Schatz F. The role of decidualization in regulating endometrial hemostasis during the menstrual cycle, gestation, and in pathological states. Semin Thromb Hemost. 2007;33:111-117.
16. Lockwood CJ, Paidas M, Murk WK, et al. Involvement of human decidual cell-expressed tissue factor in uterine hemostasis and abruption. Thromb Res. 2009;124:516-520.
17. Evans J, Salamonsen LA. Decidualized human endometrial stromal cells are sensors of hormone withdrawal in the menstrual inflammatory cascade. Biol Reprod. 2014;90:14.
18. Finn CA, Pope M. Vascular and cellular changes in the decidualized endometrium of the ovariectomized mouse following cessation of hormone treatment: A possible model for menstruation. J Endocrinol. 1984;100:295-300.
19. Henriet P, Gaide Chevronnay HP, Marbaix E. The endocrine and paracrine control of menstruation. Mol Cell Endocrinol. 2012;358:197-207.
20. Labied S, Kajihara T, Madureira PA, et al. Progestins regulate the expression and activity of the Forkhead transcription factor FOXO1 in differentiating human endometrium. Mol Endocrinol. 2006;20:35-44.
21. Brosens JJ, Parker MG, McIndoe A, Pijnenborg R, Brosens IA. A role for menstruation in preconditioning the uterus for successful pregnancy. Am J Obstet Gynecol. 2009;200:615 e611-616.
22. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738-1750.
23. Schwab KE, Chan RW, Gargett CE. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil Steril. 2005;84 Suppl 2:1124-1130.
24. Gargett CE, Ye L. Endometrial reconstruction from stem cells. Fertil Steril. 2012;98:11-20.
25. Miyazaki K, Maruyama T, Masuda H, et al. Stem cell-like differentiation potentials of endometrial side population cells as revealed by a newly developed in vivo endometrial stem cell assay. PLoS One. 2012;7:e50749.
26. Masuda H, Maruyama T, Hiratsu E, et al. Noninvasive and realtime assessment of reconstructed functional human endometrium in NOD/SCID/gamma c(null) immunodeficient mice. Proc Natl Acad Sci USA. 2007;104:1925-1930.
27. Wolff EF, Wolff AB, Hongling Du, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci. 2007;14:524-533.
28. Wolff EF, Gao XB, Yao KV, et al. Endometrial stem cell transplantation restores dopamine production in a Parkinson's disease model. J Cell Mol Med. 2011;15:747-755.
29. Schwab KE, Gargett CE. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod. 2007;22:2903-2911.
30. Spitzer TL, Rojas A, Zelenko Z, et al. Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod. 2012;86:58.
31. Bühring HJ, Battula VL, Treml S, Schewe B, Kanz L, Vogel W. Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci. 2007;1106:262-271.
32. Masuda H, Anwar SS, Bühring HJ, Rao JR, Gargett CE. A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplant. 2012;21:2201-2214.
33. Sivasubramaniyan K, Harichandan A, Schumann S, et al. Prospective isolation of mesenchymal stem cells from human bone marrow using novel antibodies directed against Sushi domain containing 2. Stem Cells Dev. 2013;22:1944-1954.
34. Murakami K, Bhandari H, Lucas ES, et al. Deficiency in clonogenic endometrial mesenchymal stem cells in obese women with reproductive failure - a pilot study. PLoS One. 2013;8:e82582.
35. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
36. Trapnell C, Pachter L, Salzberg SL. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105-1111.
37. Wagner GP, Kin K, Lynch VJ. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 2012;131:281-285.
38. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106.
39. Hardcastle TJ, Kelly KA. baySeq: Empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics. 2010;11:422.
40. Robinson MD, McCarthy DJ, Smyth GK. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139-140.
41. Fukushi J, Makagiansar IT, Stallcup WB. NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrin. Mol Biol Cell. 2004;15:3580-3590.
42. Cattaruzza S, Nicolosi PA, Braghetta P, et al. NG2/CSPG4-collagen type VI interplays putatively involved in the microenvironmental control of tumour engraftment and local expansion. J Mol Cell Biol. 2013;5:176-193.
43. Kuroda K, Venkatakrishnan R, Salker MS, et al. Induction of 11β-HSD 1 and activation of distinct mineralocorticoid receptor- and glucocorticoid receptor-dependent gene networks in decidualizing human endometrial stromal cells. Mol Endocrinol. 2013;27:192-202.
44. Salker MS, Nautiyal J, Steel JH, et al. Disordered IL-33/ST2 Activation in Decidualizing Stromal Cells Prolongs Uterine Receptivity in Women with Recurrent Pregnancy Loss. PLoS One. 2012;7:e52252.
45. Cheung TH, Rando TA. Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol. 2013;14:329-340.
46. Blanks AM, Brosens JJ. Meaningful menstruation: Cyclic renewal of the endometrium is key to reproductive success. Bioessays. 2013;35:412.
47. Finn CA. Menstruation: A nonadaptive consequence of uterine evolution. Q Rev Biol. 1998;73:163-173.
48. Martin RD. The evolution ofhumanreproduction:Aprimatological perspective. Am J Phys Anthropol. 2007;Suppl 45:59-84.
49. Ramsey EM, Houston ML, Harris JW. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am J Obstet Gynecol. 1976;124:647-652.
50. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: Stem cells and their niche. Cell. 2004;116:769-778.
51. Scadden DT. Nice Neighborhood: Emerging Concepts of the Stem Cell Niche. Cell. 2014;157:41-50.
52. Sugahara T, Yamashita Y, Shinomi M, et al. von Willebrand factor type D domain mutant of SVS-1/SUSD2, vWD(m), induces apoptosis in HeLa cells. Cancer Sci. 2007;98:909-915.
53. Sugahara T, Yamashita Y, Shinomi M, et al. Isolation of a novel mouse gene, mSVS-1/SUSD2, reversing tumorigenic phenotypes of cancer cells in vitro. Cancer Sci. 2007;98:900-908.
54. Watson AP, Evans RL, Egland KA. Multiple functions of sushi domain containing 2 (SUSD2) in breast tumorigenesis. Mol Cancer Res. 2013;11:74-85.
55. Bjornson CR, Cheung TH, Liu L, Tripathi PV, Steeper KM, Rando TA. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells. 2012;30:232-242.
56. Lake RJ, Tsai PF, Choi I, Won KJ, Fan HY. RBPJ, the major transcriptional effector of Notch signaling, remains associated with chromatin throughout mitosis, suggesting a role in mitotic bookmarking. PLoS Genet. 2014;10:e1004204.
57. Jalkanen S, Salmi M. VAP-1 and CD73, endothelial cell surface enzymes in leukocyte extravasation. Arterioscler Thromb Vasc Biol. 2008;28:18-26.
58. Rollins BJ. Chemokines. Blood. 1997;90:909-928.
59. Menten P, Wuyts A, Van Damme J. Monocyte chemotactic protein-3. Eur Cytokine Netw. 2001;12:554-560.
60. Shuya LL, Menkhorst EM, Yap J, Li P, Lane N, Dimitriadis E. Leukemia inhibitory factor enhances endometrial stromal cell decidualization in humans and mice. PLoS One. 2011;6:e25288.
61. Stewart CL, Kaspar P, Brunet LJ, et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature. 1992;359:76-79.
62. Gellersen B, Wolf A, Kruse M, Schwenke M, Bamberger AM. Human Endometrial Stromal Cell-Trophoblast Interactions: Mutual Stimulation of Chemotactic Migration and Pro-Migratory Roles of Cell Surface Molecules CD82 and CEACAM1. Biol Reprod. 2013;88:80.
63. Tapia A, Salamonsen LA, Manuelpillai U, Dimitriadis E. Leukemia inhibitory factor promotes human first trimester extravillous trophoblast adhesion to extracellular matrix and secretion of tissue inhibitor of metalloproteinases-1 and -2. Hum Reprod. 2008;23:1724-1732.
64. Brosens I, Pijnenborg R, Vercruysse L, Romero R. The "Great Obstetrical Syndromes" are associated with disorders of deep placentation. Am J Obstet Gynecol. 2011;204:193-201.
65. Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol. 1967;93:569-579.