Cited by 407Reproductive System and PregnancyPregnancy and preeclampsia studiesReproductive Biology and Fertility

Decidualization of the human endometrium

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Okada, Hidetaka, Tsuzuki, Tomoko, Murata, Hiromi·2018·Reproductive Medicine and Biology

Abstract

Background: Decidualization of the human endometrium, which involves a dramatic morphological and functional differentiation of human endometrial stromal cells (ESC s), is essential for the establishment of a successful pregnancy. Decidualization results from a complex interplay of transcription factors, morphogens, cytokines, cell cycle regulators, and signaling pathways. Methods: Based on a literature review, the regulation of, and the molecular mechanisms involved in, the decidualization of the endometrium are described. Main findings: Progesterone, together with proteins that are regulated by progesterone and/or cyclic adenosine monophosphate, including homeobox A10, forkhead box O1, signal transducers and activators of transcription, and heart and neural crest derivatives expressed transcript 2, forms a critical network for ESC decidualization and is a prerequisite to successful implantation. Decidualized ESC s contribute to the microenvironment at the feto–maternal interface and its direct or indirect influence on extracellular matrix remodeling, regulation of the local immune response, anti‐oxidative stress, and angiogenesis (vascular maturation). Impairment of this process is associated with a variety of pregnancy disorders, including infertility, recurrent miscarriages, and uteroplacental disorders. Conclusion: A deeper understanding of the process of decidualization is expected to provide new insights into the fields of reproductive biology and reproductive medicine.

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  • Decidualization is dysregulated in both endometriosis and PCOS.

    “Decidualization, the collective biochemical and morphological changes to the endometrium that prepare it for implantation (Okada et al., 2018), is dysregulated in both endometriosis and PCOS.”

    From Endometriosis and polycystic ovary syndrome are diametric disorders (2021) · cites this paper as Okada et al., 2018

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  1. [1]Henriet P, Gaide Chevronnay HP, Marbaix E. The endocrine and paracrine control of menstruation. Mol Cell Endocrinol. 2012; 358: 197‐ 207. 21820486
  2. [2]Petracco RG, Kong A, Grechukhina O, Krikun G, Taylor HS. Global gene expression profiling of proliferative phase endometrium reveals distinct functional subdivisions. Reprod Sci. 2012; 19: 1138‐ 1145. 22623515 PMC4052207
  3. [3]Plaisier M. Decidualisation and angiogenesis. Best Pract Res Clin Obstet Gynaecol. 2011; 25: 259‐ 271. 21144801
  4. [4]Okada H, Tsuzuki T, Shindoh H, Nishigaki A, Yasuda K, Kanzaki H. Regulation of decidualization and angiogenesis in the human endometrium: mini review. J Obstet Gynaecol Res. 2014; 40: 1180‐ 1187. 24754847
  5. [5]Singh M, Chaudhry P, Asselin E. Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors. J Endocrinol. 2011; 210: 5‐ 14. 21372150
  6. [6]Lessey BA, Young SL. Homeostasis imbalance in the endometrium of women with implantation defects: the role of estrogen and progesterone. Semin Reprod Med. 2014; 32: 365‐ 375. 24959818
  7. [7]Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet. 2006; 7: 185‐ 199. 16485018
  8. [8]Dimitriadis E, Nie G, Hannan NJ, Paiva P, Salamonsen LA. Local regulation of implantation at the human fetal–maternal interface. Int J Dev Biol. 2010; 54: 313‐ 322. 19757390
  9. [9]Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK. Endometrial decidualization: of mice and men. Semin Reprod Med. 2010; 28: 17‐ 26. 20104425 PMC3095443
  10. [10]Evans J, Salamonsen LA, Winship A, et al. Fertile ground: human endometrial programming and lessons in health and disease. Nat Rev Endocrinol. 2016; 12: 654‐ 667. 27448058
  11. [11]Wu D, Kimura F, Zheng L, et al. Chronic endometritis modifies decidualization in human endometrial stromal cells. Reprod Biol Endocrinol. 2017; 15: 16. 28259137 PMC5336610
  12. [12]Cha J, Sun X, Dey SK. Mechanisms of implantation: strategies for successful pregnancy. Nat Med. 2012; 18: 1754‐ 1767. 23223073 PMC6322836
  13. [13]Garrido‐Gomez T, Dominguez F, Quinonero A, et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. Proc Natl Acad Sci USA. 2017; 114: E8468‐ E8477. 28923940 PMC5635883
  14. [14]Coulam C. What about superfertility, decidualization, and natural selection? J Assist Reprod Genet. 2016; 33: 577‐ 580. 26843392 PMC4870434
  15. [15]Gellersen B, Brosens JJ. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr Rev. 2014; 35: 851‐ 905. 25141152
  16. [16]Schatz F, Guzeloglu‐Kayisli O, Arlier S, Kayisli UA, Lockwood CJ. The role of decidual cells in uterine hemostasis, menstruation, inflammation, adverse pregnancy outcomes and abnormal uterine bleeding. Hum Reprod Update. 2016; 22: 497‐ 515. 26912000 PMC4917742
  17. [17]Su RW, Fazleabas AT. Implantation and establishment of pregnancy in human and nonhuman primates. Adv Anat Embryol Cell Biol. 2015; 216: 189‐ 213. 26450500 PMC5098399
  18. [18]Kajihara T, Tanaka K, Oguro T, et al. Androgens modulate the morphological characteristics of human endometrial stromal cells decidualized in vitro. Reprod Sci. 2014; 21: 372‐ 380. 23885104
  19. [19]Wetendorf M, DeMayo FJ. The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network. Mol Cell Endocrinol. 2012; 357: 108‐ 118. 22115959 PMC3443857
  20. [20]Maruyama T, Yoshimura Y. Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium. Endocr J. 2008; 55: 795‐ 810. 18580040
  21. [21]Hamilton KJ, Arao Y, Korach KS. Estrogen hormone physiology: reproductive findings from estrogen receptor mutant mice. Reprod Biol. 2014; 14: 3‐ 8. 24607249 PMC4777324
  22. [22]Koos RD. Minireview: putting physiology back into estrogens’ mechanism of action. Endocrinology. 2011; 152: 4481‐ 4488. 21952239
  23. [23]Bhurke AS, Bagchi IC, Bagchi MK. Progesterone‐regulated endometrial factors controlling implantation. Am J Reprod Immunol. 2016; 75: 237‐ 245. 26804062 PMC4754106
  24. [24]Conneely OM, Mulac‐Jericevic B, DeMayo F, Lydon JP, O'Malley BW. Reproductive functions of progesterone receptors. Recent Prog Horm Res. 2002; 57: 339‐ 355. 12017551
  25. [25]Conneely OM, Lydon JP. Progesterone receptors in reproduction: functional impact of the A and B isoforms. Steroids. 2000; 65: 571‐ 577. 11108861
  26. [26]Okada H, Sanezumi M, Nakajima T, Okada S, Yasuda K, Kanzaki H. Rapid down‐regulation of CD63 transcription by progesterone in human endometrial stromal cells. Mol Hum Reprod. 1999; 5: 554‐ 558. 10341003
  27. [27]Okada H, Nakajima T, Yoshimura T, Yasuda K, Kanzaki H. The inhibitory effect of dienogest, a synthetic steroid, on the growth of human endometrial stromal cells in vitro. Mol Hum Reprod. 2001; 7: 341‐ 347. 11279296
  28. [28]Okada H, Nie G, Salamonsen LA. Requirement for proprotein convertase 5/6 during decidualization of human endometrial stromal cells in vitro. J Clin Endocrinol Metab. 2005; 90: 1028‐ 1034. 15522936
  29. [29]Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross‐talk in human endometrium: a decidualizing affair. J Endocrinol. 2003; 178: 357‐ 372. 12967329
  30. [30]Kajihara T, Brosens JJ, Ishihara O. The role of FOXO1 in the decidual transformation of the endometrium and early pregnancy. Med Mol Morphol. 2013; 46: 61‐ 68. 23381604
  31. [31]Ujvari D, Jakson I, Babayeva S, et al. Dysregulation of in vitro decidualization of human endometrial stromal cells by insulin via transcriptional inhibition of Forkhead box protein O1. PLoS ONE. 2017; 12: e0171004 10.1371/journal.pone.0171004 28135285 PMC5279782 · DOI
  32. [32]Popovici RM, Kao LC, Giudice LC. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology. 2000; 141: 3510‐ 3513. 10965925
  33. [33]Shindoh H, Okada H, Tsuzuki T, Nishigaki A, Kanzaki H. Requirement of heart and neural crest derivatives‐expressed transcript 2 during decidualization of human endometrial stromal cells in vitro. Fertil Steril. 2014; 101: 1781‐ 1790e1‐5. 24745730
  34. [34]Pawar S, Hantak AM, Bagchi IC, Bagchi MK. Minireview: Steroid‐regulated paracrine mechanisms controlling implantation. Mol Endocrinol. 2014; 28: 1408‐ 1422. 25051170 PMC4154240
  35. [35]Huyen DV, Bany BM. Evidence for a conserved function of heart and neural crest derivatives expressed transcript 2 in mouse and human decidualization. Reproduction. 2011; 142: 353‐ 368. 21527398 PMC3141103
  36. [36]Li Q, Kannan A, DeMayo FJ, et al. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science. 2011; 331: 912‐ 916. 21330545 PMC3320855
  37. [37]Cho H, Okada H, Tsuzuki T, Nishigaki A, Yasuda K, Kanzaki H. Progestin‐induced heart and neural crest derivatives expressed transcript 2 is associated with fibulin‐1 expression in human endometrial stromal cells. Fertil Steril. 2013; 99: 248‐ 255. 23036802
  38. [38]Vinketova K, Mourdjeva M, Oreshkova T. Human decidual stromal cells as a component of the implantation niche and a modulator of maternal immunity. J Pregnancy. 2016; 2016: 8689436. 27239344 PMC4864559
  39. [39]Mori M, Bogdan A, Balassa T, Csabai T, Szekeres‐Bartho J. The decidua‐the maternal bed embracing the embryo‐maintains the pregnancy. Semin Immunopathol. 2016; 38: 635‐ 649. 27287066 PMC5065593
  40. [40]Sharma S, Godbole G, Modi D. Decidual control of trophoblast invasion. Am J Reprod Immunol. 2016; 75: 341‐ 350. 26755153
  41. [41]Okada H, Nakajima T, Yoshimura T, Yasuda K, Kanzaki H. Microarray analysis of genes controlled by progesterone in human endometrial stromal cells in vitro. Gynecol Endocrinol. 2003; 17: 271‐ 280. 14503970
  42. [42]Timpl R, Sasaki T, Kostka G, Chu ML. Fibulins: a versatile family of extracellular matrix proteins. Nat Rev Mol Cell Biol. 2003; 4: 479‐ 489. 12778127
  43. [43]de Vega S, Iwamoto T, Yamada Y. Fibulins: multiple roles in matrix structures and tissue functions. Cell Mol Life Sci. 2009; 66: 1890‐ 1902. 19189051 PMC11115505
  44. [44]Haendler B, Yamanouchi H, Lessey BA, Chwalisz K, Hess‐Stumpp H. Cycle‐dependent endometrial expression and hormonal regulation of the fibulin‐1 gene. Mol Reprod Dev. 2004; 68: 279‐ 287. 15112320
  45. [45]Nakamoto T, Okada H, Nakajima T, Ikuta A, Yasuda K, Kanzaki H. Progesterone induces the fibulin‐1 expression in human endometrial stromal cells. Hum Reprod. 2005; 20: 1447‐ 1455. 15774544
  46. [46]Laws MJ, Taylor RN, Sidell N, et al. Gap junction communication between uterine stromal cells plays a critical role in pregnancy‐associated neovascularization and embryo survival. Development. 2008; 135: 2659‐ 2668. 18599509 PMC2692722
  47. [47]Yu J, Wu J, Bagchi IC, Bagchi MK, Sidell N, Taylor RN. Disruption of gap junctions reduces biomarkers of decidualization and angiogenesis and increases inflammatory mediators in human endometrial stromal cell cultures. Mol Cell Endocrinol. 2011; 344: 25‐ 34. 21767601 PMC3162129
  48. [48]Pollheimer J, Fock V, Knofler M. Review: the ADAM metalloproteinases – novel regulators of trophoblast invasion? Placenta. 2014; 35: S57‐ S63. 24231445
  49. [49]Lee SK, Kim CJ, Kim DJ, Kang JH. Immune cells in the female reproductive tract. Immune Netw. 2015; 15: 16‐ 26. 25713505 PMC4338264
  50. [50]Hanna J, Goldman‐Wohl D, Hamani Y, et al. Decidual NK cells regulate key developmental processes at the human fetal–maternal interface. Nat Med. 2006; 12: 1065‐ 1074. 16892062
  51. [51]Santoni A, Carlino C, Gismondi A. Uterine NK cell development, migration and function. Reprod Biomed Online. 2008; 16: 202‐ 210. 18284874
  52. [52]Wu X, Jin LP, Yuan MM, Zhu Y, Wang MY, Li DJ. Human first‐trimester trophoblast cells recruit CD56brightCD16‐NK cells into decidua by way of expressing and secreting of CXCL12/stromal cell‐derived factor 1. J Immunol. 2005; 175: 61‐ 68. 15972632
  53. [53]Lobo SC, Huang ST, Germeyer A, et al. The immune environment in human endometrium during the window of implantation. Am J Reprod Immunol. 2004; 52: 244‐ 251. 15494045
  54. [54]Wallace AE, Fraser R, Gurung S, et al. Increased angiogenic factor secretion by decidual natural killer cells from pregnancies with high uterine artery resistance alters trophoblast function. Hum Reprod. 2014; 29: 652‐ 660. 24522839 PMC3949498
  55. [55]Hofmann AP, Gerber SA, Croy BA. Uterine natural killer cells pace early development of mouse decidua basalis. Mol Hum Reprod. 2014; 20: 66‐ 76. 24000237
  56. [56]Lima PD, Zhang J, Dunk C, Lye SJ, Croy BA. Leukocyte driven‐decidual angiogenesis in early pregnancy. Cell Mol Immunol. 2014; 11: 522‐ 537. 25066422 PMC4220841
  57. [57]Wallace AE, Fraser R, Cartwright JE. Extravillous trophoblast and decidual natural killer cells: a remodelling partnership. Hum Reprod Update. 2012; 18: 458‐ 471. 22523109 PMC3373213
  58. [59]Kitaya K, Yamaguchi T, Honjo H. Central role of interleukin‐15 in postovulatory recruitment of peripheral blood CD16(‐) natural killer cells into human endometrium. J Clin Endocrinol Metab. 2005; 90: 2932‐ 2940. 15713701
  59. [60]Okada S, Okada H, Sanezumi M, Nakajima T, Yasuda K, Kanzaki H. Expression of interleukin‐15 in human endometrium and decidua. Mol Hum Reprod. 2000; 6: 75‐ 80. 10611264
  60. [61]Mariee N, Li TC, Laird SM. Expression of leukaemia inhibitory factor and interleukin 15 in endometrium of women with recurrent implantation failure after IVF; correlation with the number of endometrial natural killer cells. Hum Reprod. 2012; 27: 1946‐ 1954. 22537815
  61. [62]Okada H, Nakajima T, Yasuda K, Kanzaki H. Interleukin‐1 inhibits interleukin‐15 production by progesterone during in vitro decidualization in human. J Reprod Immunol. 2004; 61: 3‐ 12. 14967219
  62. [63]Okada H, Nakajima T, Sanezumi M, Ikuta A, Yasuda K, Kanzaki H. Progesterone enhances interleukin‐15 production in human endometrial stromal cells in vitro. J Clin Endocrinol Metab. 2000; 85: 4765‐ 4770. 11134140
  63. [65]Almada M, Fonseca BM, Amaral C, Diniz‐da‐Costa M, Correia‐da‐Silva G, Teixeira N. Anandamide oxidative metabolism‐induced endoplasmic reticulum stress and apoptosis. Apoptosis. 2017; 22: 816‐ 826. 28220271
  64. [66]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. 16709600
  65. [67]Sugino N. The role of oxygen radical‐mediated signaling pathways in endometrial function. Placenta. 2007; 28 Suppl A: S133‐ S136. 17291583
  66. [68]Lou Y, Hu M, Mao L, Zheng Y, Jin F. Involvement of serum glucocorticoid‐regulated kinase 1 in reproductive success. FASEB J. 2017; 31: 447‐ 456. 27871060
  67. [69]Salker MS, Christian M, Steel JH, et al. Deregulation of the serum‐ and glucocorticoid‐inducible kinase SGK1 in the endometrium causes reproductive failure. Nat Med. 2011; 17: 1509‐ 1513. 22001908
  68. [70]Albrecht ED, Pepe GJ. Steroid hormone regulation of angiogenesis in the primate endometrium. Front Biosci. 2003; 8: d416‐ d429. 12456304
  69. [71]Weston G, Rogers PA. Endometrial angiogenesis. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000; 14: 919‐ 936. 11141341
  70. [72]Virdis A, Dell'Agnello U, Taddei S. Impact of inflammation on vascular disease in hypertension. Maturitas. 2014; 78: 179‐ 183. 24846805
  71. [73]Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003; 9: 653‐ 660. 12778163
  72. [74]Nishigaki A, Okada H, Okamoto R, et al. The concentration of human follicular fluid stromal cell‐derived factor‐1 is correlated with luteinization in follicles. Gynecol Endocrinol. 2013; 29: 230‐ 234. 23193972
  73. [75]Girling JE, Rogers PA. Recent advances in endometrial angiogenesis research. Angiogenesis. 2005; 8: 89‐ 99. 16211359
  74. [76]Smith SK. Regulation of angiogenesis in the endometrium. Trends Endocrinol Metab. 2001; 12: 147‐ 151. 11295569
  75. [77]Gargett CE, Rogers PA. Human endometrial angiogenesis. Reproduction. 2001; 121: 181‐ 186. 11226042
  76. [78]Lockwood CJ. Mechanisms of normal and abnormal endometrial bleeding. Menopause. 2011; 18: 408‐ 411. 21499503 PMC3074585
  77. [79]Tsuzuki T, Okada H, Shindoh H, Shimoi K, Nishigaki A, Kanzaki H. Effects of the hypoxia‐inducible factor‐1 inhibitor echinomycin on vascular endothelial growth factor production and apoptosis in human ectopic endometriotic stromal cells. Gynecol Endocrinol. 2016; 32: 323‐ 328. 26654708
  78. [80]Jabbour HN, Kelly RW, Fraser HM, Critchley HO. Endocrine regulation of menstruation. Endocr Rev. 2006; 27: 17‐ 46. 16160098
  79. [81]Hey‐Cunningham AJ, Peters KM, Zevallos HB, Berbic M, Markham R, Fraser IS. Angiogenesis, lymphangiogenesis and neurogenesis in endometriosis. Front Biosci (Elite Ed). 2013; 5: 1033‐ 1056. 23747918
  80. [82]Bradford LS, Rauh‐Hain JA, Schorge J, Birrer MJ, Dizon DS. Advances in the management of recurrent endometrial cancer. Am J Clin Oncol. 2015; 38: 206‐ 212. 23764681
  81. [83]Albrecht ED, Pepe GJ. Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy. Int J Dev Biol. 2010; 54: 397‐ 408. 19876841 PMC2804030
  82. [84]Tsuzuki T, Okada H, Cho H, et al. Divergent regulation of angiopoietin‐1, angiopoietin‐2, and vascular endothelial growth factor by hypoxia and female sex steroids in human endometrial stromal cells. Eur J Obstet Gynecol Reprod Biol. 2013; 168: 95‐ 101. 23352606
  83. [85]Tsutsumi A, Okada H, Nakamoto T, Okamoto R, Yasuda K, Kanzaki H. Estrogen induces stromal cell‐derived factor 1 (SDF‐1/CXCL12) production in human endometrial stromal cells: a possible role of endometrial epithelial cell growth. Fertil Steril. 2011; 95: 444‐ 447. 20869048
  84. [86]Koga K, Osuga Y, Tsutsumi O, et al. Demonstration of angiogenin in human endometrium and its enhanced expression in endometrial tissues in the secretory phase and the decidua. J Clin Endocrinol Metab. 2001; 86: 5609‐ 5614. 11701742
  85. [87]Soufla G, Sifakis S, Spandidos DA. FGF2 transcript levels are positively correlated with EGF and IGF‐1 in the malignant endometrium. Cancer Lett. 2008; 259: 146‐ 155. 18006148
  86. [88]Dai H, Zhao S, Xu L, Chen A, Dai S. Expression of Efp, VEGF and bFGF in normal, hyperplastic and malignant endometrial tissue. Oncol Rep. 2010; 23: 795‐ 799. 20127022
  87. [89]Evans J, Catalano RD, Brown P, et al. Prokineticin 1 mediates fetal–maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB J. 2009; 23: 2165‐ 2175. 19255255 PMC2704594
  88. [90]Tsuzuki T, Okada H, Cho H, et al. Hypoxic stress simultaneously stimulates vascular endothelial growth factor via hypoxia‐inducible factor‐1 alpha and inhibits stromal cell‐derived factor‐1 in human endometrial stromal cells. Hum Reprod. 2012; 27: 523‐ 530. 22128293
  89. [91]Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004; 25: 581‐ 611. 15294883
  90. [92]Croy BA, Chen Z, Hofmann AP, Lord EM, Sedlacek AL, Gerber SA. Imaging of vascular development in early mouse decidua and its association with leukocytes and trophoblasts. Biol Reprod. 2012; 87: 125. 22954796 PMC3509781
  91. [93]Binder NK, Evans J, Gardner DK, Salamonsen LA, Hannan NJ. Endometrial signals improve embryo outcome: functional role of vascular endothelial growth factor isoforms on embryo development and implantation in mice. Hum Reprod. 2014; 29: 2278‐ 2286. 25124669
  92. [94]Aberdeen GW, Wiegand SJ, Bonagura TW Jr, Pepe GJ, Albrecht ED. Vascular endothelial growth factor mediates the estrogen‐induced breakdown of tight junctions between and increase in proliferation of microvessel endothelial cells in the baboon endometrium. Endocrinology. 2008; 149: 6076‐ 6083. 18687775 PMC2613057
  93. [95]Salamonsen LA. Tissue injury and repair in the female human reproductive tract. Reproduction. 2003; 125: 301‐ 311. 12611594
  94. [96]Fan X, Krieg S, Kuo CJ, et al. VEGF blockade inhibits angiogenesis and reepithelialization of endometrium. FASEB J. 2008; 22: 3571‐ 3580. 18606863 PMC2537439
  95. [97]Shifren JL, Tseng JF, Zaloudek CJ, et al. 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. 1996; 81: 3112‐ 3118. 8768883
  96. [98]Okada H, Tsutsumi A, Imai M, Nakajima T, Yasuda K, Kanzaki H. Estrogen and selective estrogen receptor modulators regulate vascular endothelial growth factor and soluble vascular endothelial growth factor receptor 1 in human endometrial stromal cells. Fertil Steril. 2010; 93: 2680‐ 2686. 19828145
  97. [99]Herve MA, Meduri G, Petit FG, et al. Regulation of the vascular endothelial growth factor (VEGF) receptor Flk‐1/KDR by estradiol through VEGF in uterus. J Endocrinol. 2006; 188: 91‐ 99. 16394178
  98. [100]Thomas M, Augustin HG. The role of the angiopoietins in vascular morphogenesis. Angiogenesis. 2009; 12: 125‐ 137. 19449109
  99. [101]Hewett P, Nijjar S, Shams M, Morgan S, Gupta J, Ahmed A. Down‐regulation of angiopoietin‐1 expression in menorrhagia. Am J Pathol. 2002; 160: 773‐ 780. 11891175 PMC1867155
  100. [102]Nishigaki A, Okada H, Tsuzuki T, Cho H, Yasuda K, Kanzaki H. Angiopoietin 1 and angiopoietin 2 in follicular fluid of women undergoing a long protocol. Fertil Steril. 2011; 96: 1378‐ 1383. 22000910
  101. [103]Maisonpierre PC, Suri C, Jones PF, et al. Angiopoietin‐2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997; 277: 55‐ 60. 9204896
  102. [104]Thurston G, Rudge JS, Ioffe E, et al. Angiopoietin‐1 protects the adult vasculature against plasma leakage. Nat Med. 2000; 6: 460‐ 463. 10742156
  103. [105]Diamond JR, Wu B, Agarwal N, et al. Pharmacokinetic drug–drug interaction study of the angiopoietin‐1/angiopoietin‐2‐inhibiting peptibody trebananib (AMG 386) and paclitaxel in patients with advanced solid tumors. Invest New Drugs. 2015; 33: 691‐ 699. 25895965

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Authors
Okada, H., Tsuzuki, T., & Murata, H.
Affiliations
  • Kansai Medical University (JP)
  • Department of Obstetrics and Gynecology Kansai Medical University Osaka Japan
Corresponding author
Okada, Hidetaka
Venue
Reproductive Medicine and Biology
Publisher
Wiley
Published
2018-02
Volume
17
Issue
3
Pages
220-227
ISSN
  • 1445-5781 (ISSN-L)
  • 1447-0578
OpenAlex
W2793805814
Cited by
407
References
2
Citations by year
2026: 58 · 2025: 64 · 2024: 43 · 2023: 52 · 2022: 77 · 2021: 57 · 2020: 35 · 2019: 18 · 2018: 2
FWCI
2.86
Type
journal article
Language
en
Open access
Locations
  • Reproductive Medicine and Biology (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Japan Society for the Promotion of Science (17K11260, 15K20169)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords
decidualization, endometrium, endometrial stromal cells, progesterone, cyclic AMP, FOXO1, signal transducer and activator of transcription, embryo implantation, maternal-fetal interface, extracellular matrix remodeling, local immune response, oxidative stress, angiogenesis, pregnancy disorders, recurrent pregnancy loss, infertility

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