Rac1 Regulates Endometrial Secretory Function to Control Placental Development

PLoS Genetics

Volumn 11, Issue 8, 2015, Pages

  Davila, Juanmahel ^a   Laws, Mary J ^b   Kannan, Athilakshmi ^a   Li, Quanxi ^a   Taylor, Robert N ^c   Bagchi, Milan K ^b   Bagchi, Indrani C ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROGESTERONE; RAB PROTEIN; RAB27B PROTEIN; RAC1 PROTEIN; SOMATOMEDIN BINDING PROTEIN 4; UNCLASSIFIED DRUG; VASCULOTROPIN A; RAC1 PROTEIN, HUMAN; VEGFA PROTEIN, HUMAN;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DECIDUALIZATION; DOWN REGULATION; EMBRYO; ENDOMETRIUM; FEMALE; FEMALE INFERTILITY; FETUS WASTAGE; GENE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MOUSE; NIDATION; NONHUMAN; PLACENTA DEVELOPMENT; POLYMERASE CHAIN REACTION; PREGNANCY DISORDER; PROGESTERONE BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RAB27B GENE; RAC1 GENE; TROPHOBLAST; UPREGULATION; UTERUS BLEEDING; ANIMAL; DECIDUA; MALE; METABOLISM; PHYSIOLOGY; PREGNANCY; REPRODUCTION; SECRETION (PROCESS); TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; DECIDUA; FEMALE; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; MALE; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; PLACENTATION; PREGNANCY; RAC1 GTP-BINDING PROTEIN; TRANSCRIPTIONAL ACTIVATION; TROPHOBLASTS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84940760047     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005458     Document Type: Article

References (69)

1. Cross JC, Werb Z, Fisher SJ, Implantation and the placenta: key pieces of the development puzzle. Science. 1994;266(5190):1508–18. Epub 1994/12/02. 7985020
2. Wang H, Dey SK, Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet. 2006;7(3):185–99. Epub 2006/02/18. 16485018
3. Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK, Endometrial decidualization: of mice and men. Semin Reprod Med. 2010;28(1):17–26. Epub 2010/01/28. doi: 10.1055/s-0029-1242989 20104425
4. Cha J, Sun X, Dey SK, Mechanisms of implantation: strategies for successful pregnancy. Nat Med. 2012;18(12):1754–67. doi: 10.1038/nm.3012 23223073
5. Zhang S, Lin H, Kong S, Wang S, Wang H, Wang H, et al. Physiological and molecular determinants of embryo implantation. Molecular aspects of medicine. 2013;34(5):939–80. Epub 2013/01/08. doi: 10.1016/j.mam.2012.12.011 23290997
6. Irwin JC, Giudice LC, Knobil E, Neill JD, Decidua. In: Encyclopedia of Reproduction. San Diego: Academic Press; 1998. p. 822–35.
7. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest. 2004;114(6):744–54. Epub 2004/09/17. 15372095
8. Chang K, Lubo Z, Review article: steroid hormones and uterine vascular adaptation to pregnancy. Reprod Sci. 2008;15(4):336–48. doi: 10.1177/1933719108317975 18497342
9. Osol G, Mandala M, Maternal uterine vascular remodeling during pregnancy. Physiology (Bethesda). 2009;24:58–71.
10. Sharkey AM, Smith SK, The endometrium as a cause of implantation failure. Best Pract Res Clin Obstet Gynaecol. 2003;17(2):289–307. Epub 2003/05/22. 12758101
11. Norwitz ER, Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod Biomed Online. 2006;13(4):591–9. 17007686
12. Jauniaux E, Van Oppenraaij RH, Burton GJ, Obstetric outcome after early placental complications. Curr Opin Obstet Gynecol. 2010;22(6):452–7. doi: 10.1097/GCO.0b013e3283404e44 20930630
13. Bustelo XR, Sauzeau V, Berenjeno IM, GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. BioEssays: news and reviews in molecular, cellular and developmental biology. 2007;29(4):356–70.
14. Etienne-Manneville S, Hall A, Rho GTPases in cell biology. Nature. 2002;420(6916):629–35. 12478284
15. Hall A, Rho family GTPases. Biochemical Society transactions. 2012;40(6):1378–82. doi: 10.1042/BST20120103 23176484
16. Heasman SJ, Ridley AJ, Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. 2008;9(9):690–701. doi: 10.1038/nrm2476 18719708
17. Fukuda M, Rab27 effectors, pleiotropic regulators in secretory pathways. Traffic. 2013;14(9):949–63. doi: 10.1111/tra.12083 23678941
18. Gomi H, Mori K, Itohara S, Izumi T, Rab27b is expressed in a wide range of exocytic cells and involved in the delivery of secretory granules near the plasma membrane. Mol Biol Cell. 2007;18(11):4377–86. 17761531
19. Ledford BE, Rankin JC, Markwald RR, Baggett B, Biochemical and morphological changes following artificially stimulated decidualization in the mouse uterus. Biol Reprod. 1976;15(4):529–35. Epub 1976/11/01. 974204
20. Laws MJ, Taylor RN, Sidell N, DeMayo FJ, Lydon JP, Gutstein DE, et al. Gap junction communication between uterine stromal cells plays a critical role in pregnancy-associated neovascularization and embryo survival. Development. 2008;135(15):2659–68. Epub 2008/07/05. doi: 10.1242/dev.019810 18599509
21. Grewal S, Carver JG, Ridley AJ, Mardon HJ, Implantation of the human embryo requires Rac1-dependent endometrial stromal cell migration. Proc Natl Acad Sci U S A. 2008;105(42):16189–94. Epub 2008/10/08. doi: 10.1073/pnas.0806219105 18838676
22. Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, Otani H, et al. Rac1 is required for the formation of three germ layers during gastrulation. Oncogene. 1998;17(26):3427–33. 10030666
23. Glogauer M, Marchal CC, Zhu F, Worku A, Clausen BE, Foerster I, et al. Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J Immunol. 2003;170(11):5652–7. Epub 2003/05/22. 12759446
24. Li Q, Kannan A, DeMayo FJ, Lydon JP, Cooke PS, Yamagishi H, et al. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science. 2011;331(6019):912–6. Epub 2011/02/19. doi: 10.1126/science.1197454 21330545
25. Lee KY, Jeong JW, Wang J, Ma L, Martin JF, Tsai SY, et al. Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol. 2007;27(15):5468–78. 17515606
26. Nallasamy S, Li Q, Bagchi MK, Bagchi IC, Msx homeobox genes critically regulate embryo implantation by controlling paracrine signaling between uterine stroma and epithelium. Plos Genet. 2012;8(2):e1002500. doi: 10.1371/journal.pgen.1002500 22383889
27. Lee K, Jeong J, Kwak I, Yu CT, Lanske B, Soegiarto DW, et al. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nature genetics. 2006;38(10):1204–9. Epub 2006/09/05. 16951680
28. Orwig KE, Dai G, Rasmussen CA, Soares MJ, Decidual/trophoblast prolactin-related protein: characterization of gene structure and cell-specific expression. Endocrinology. 1997;138(6):2491–500. 9165040
29. Soares MJ, Muller H, Orwig KE, Peters TJ, Dai G, The uteroplacental prolactin family and pregnancy. Biol Reprod. 1998;58(2):273–84. 9475377
30. Finn CA, Hinchliffe JR, Reaction of the Mouse Uterus during Implantation and Deciduoma Formation as Demonstrated by Changes in the Distribution of Alkaline Phosphatase. J Reprod Fertil. 1964;8:331–8. Epub 1964/12/01. 14248593
31. Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, Bagchi MK, et al. Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. The Journal of biological chemistry. 2007;282(43):31725–32. Epub 2007/08/23. 17711857
32. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA, Jr.et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes & development. 1995;9(18):2266–78. Epub 1995/09/15.
33. Hu D, Cross JC, Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol. 2010;54(2–3):341–54. Epub 2009/10/31. doi: 10.1387/ijdb.082768dh 19876834
34. Rossant J, Cross JC, Placental development: lessons from mouse mutants. Nat Rev Genet. 2001;2(7):538–48. 11433360
35. Cross JC, How to make a placenta: mechanisms of trophoblast cell differentiation in mice—a review. Placenta. 2005;26 Suppl A:S3–9. Epub 2005/04/20. 15837063
36. Tolmachova T, Abrink M, Futter CE, Authi KS, Seabra MC, Rab27b regulates number and secretion of platelet dense granules. Proc Natl Acad Sci U S A. 2007;104(14):5872–7. 17384153
37. Singh RK, Mizuno K, Wasmeier C, Wavre-Shapton ST, Recchi C, Catz SD, et al. Distinct and opposing roles for Rab27a/Mlph/MyoVa and Rab27b/Munc13-4 in mast cell secretion. FEBS J. 2013;280(3):892–903. doi: 10.1111/febs.12081 23281710
38. Kanai-Azuma M, Kanai Y, Kurohmaru M, Sakai S, Hayashi Y, Insulin-like growth factor (IGF)-I stimulates proliferation and migration of mouse ectoplacental cone cells, while IGF-II transforms them into trophoblastic giant cells in vitro. Biol Reprod. 1993;48(2):252–61. 8439614
39. Giudice LC, Irwin JC, Roles of the insulinlike growth factor family in nonpregnant human endometrium and at the decidual: trophoblast interface. Seminars in reproductive endocrinology. 1999;17(1):13–21. 10406071
40. Giudice LC, Conover CA, Bale L, Faessen GH, Ilg K, Sun I, et al. Identification and regulation of the IGFBP-4 protease and its physiological inhibitor in human trophoblasts and endometrial stroma: evidence for paracrine regulation of IGF-II bioavailability in the placental bed during human implantation. The Journal of clinical endocrinology and metabolism. 2002;87(5):2359–66. 11994388
41. Henemyre C, Markoff E, Decidualization and expression of insulin-like growth factor-I and insulin-like growth factor binding protein-4 in the periimplantation mouse uterus. Biol Reprod. 1998;58(3):801–6. 9510969
42. Markoff E, Henemyre C, Fellows J, Pennington E, Zeitler PS, Cedars MI, Localization of insulin-like growth factor binding protein-4 expression in the mouse uterus during the peri-implantation period. Biol Reprod. 1995;53(5):1103–9. 8527514
43. Tang B, Guller S, Gurpide E, Cyclic adenosine 3',5'-monophosphate induces prolactin expression in stromal cells isolated from human proliferative endometrium. Endocrinology. 1993;133(5):2197–203. Epub 1993/11/01. 8404671
44. Ryan IP, Schriock ED, Taylor RN, Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro. The Journal of clinical endocrinology and metabolism. 1994;78(3):642–9. Epub 1994/03/01. 8126136
45. Ferri N, Corsini A, Bottino P, Clerici F, Contini A, Virtual screening approach for the identification of new Rac1 inhibitors. J Med Chem. 2009;52(14):4087–90. doi: 10.1021/jm8015987 19527032
46. Mack NA, Whalley HJ, Castillo-Lluva S, Malliri A, The diverse roles of Rac signaling in tumorigenesis. Cell Cycle. 2011;10(10):1571–81. 21478669
47. Pai SY, Kim C, Williams DA, Rac GTPases in human diseases. Disease markers. 2010;29(3–4):177–87. doi: 10.3233/DMA-2010-0738 21178276
48. Moshfegh Y, Bravo-Cordero JJ, Miskolci V, Condeelis J, Hodgson L, A Trio-Rac1-Pak1 signalling axis drives invadopodia disassembly. Nature cell biology. 2014;16(6):574–86. doi: 10.1038/ncb2972 24859002
49. Ridley AJ, Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends in cell biology. 2006;16(10):522–9. Epub 2006/09/05. 16949823
50. Raimondi C, Ruhrberg C, Neuropilin signalling in vessels, neurons and tumours. Seminars in cell & developmental biology. 2013;24(3):172–8. Epub 2013/01/16.
51. Scholz A, Plate KH, Reiss Y, Angiopoietin-2: a multifaceted cytokine that functions in both angiogenesis and inflammation. Annals of the New York Academy of Sciences. 2015. Epub 2015/03/17.
52. Mizugishi K, Li C, Olivera A, Bielawski J, Bielawska A, Deng CX, et al. Maternal disturbance in activated sphingolipid metabolism causes pregnancy loss in mice. J Clin Invest. 2007;117(10):2993–3006. Epub 2007/09/22. 17885683
53. Schiera G, Proia P, Alberti C, Mineo M, Savettieri G, Di Liegro I, Neurons produce FGF2 and VEGF and secrete them at least in part by shedding extracellular vesicles. Journal of cellular and molecular medicine. 2007;11(6):1384–94. Epub 2008/01/22. doi: 10.1111/j.1582-4934.2007.00100.x 18205708
54. Guzman-Hernandez ML, Potter G, Egervari K, Kiss JZ, Balla T, Secretion of VEGF-165 has unique characteristics, including shedding from the plasma membrane. Mol Biol Cell. 2014;25(7):1061–72. Epub 2014/02/07. doi: 10.1091/mbc.E13-07-0418 24501421
55. Burgoyne RD, Morgan A, Secretory granule exocytosis. Physiological reviews. 2003;83(2):581–632. Epub 2003/03/29. 12663867
56. Lane B, Oxberry W, Mazella J, Tseng L, Decidualization of human endometrial stromal cells in vitro: effects of progestin and relaxin on the ultrastructure and production of decidual secretory proteins. Hum Reprod. 1994;9(2):259–66. 7517949
57. Giudice LC, Irwin JC, Dsupin BA, Pannier EM, Jin IH, Vu TH, et al. Insulin-like growth factor (IGF), IGF binding protein (IGFBP), and IGF receptor gene expression and IGFBP synthesis in human uterine leiomyomata. Hum Reprod. 1993;8(11):1796–806. 7507128
58. Nagashima T, Li Q, Clementi C, Lydon JP, DeMayo FJ, Matzuk MM, BMPR2 is required for postimplantation uterine function and pregnancy maintenance. J Clin Invest. 2013;123(6):2539–50. doi: 10.1172/JCI65710 23676498
59. Ahmed A, Perkins J, Angiogenesis and intrauterine growth restriction. Bailliere's best practice & research Clinical obstetrics & gynaecology. 2000;14(6):981–98. Epub 2001/01/06.
60. Barut F, Barut A, Gun BD, Kandemir NO, Harma MI, Harma M, et al. Intrauterine growth restriction and placental angiogenesis. Diagnostic pathology. 2010;5:24. Epub 2010/04/24. doi: 10.1186/1746-1596-5-24 20412591
61. Fisher SJ, The placental problem: linking abnormal cytotrophoblast differentiation to the maternal symptoms of preeclampsia. Reproductive biology and endocrinology: RB&E. 2004;2:53. Epub 2004/07/09.
62. Khaliq A, Dunk C, Jiang J, Shams M, Li XF, Acevedo C, et al. Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for "placental hyperoxia" in intrauterine growth restriction. Laboratory investigation; a journal of technical methods and pathology. 1999;79(2):151–70. Epub 1999/03/06. 10068204
63. Plaisier M, Dennert I, Rost E, Koolwijk P, van Hinsbergh VW, Helmerhorst FM, Decidual vascularization and the expression of angiogenic growth factors and proteases in first trimester spontaneous abortions. Hum Reprod. 2009;24(1):185–97. Epub 2008/10/16. doi: 10.1093/humrep/den296 18854409
64. Vuorela P, Carpen O, Tulppala M, Halmesmaki E, VEGF, its receptors and the tie receptors in recurrent miscarriage. Molecular human reproduction. 2000;6(3):276–82. Epub 2000/02/29. 10694277
65. Qiu Q, Bell M, Lu X, Yan X, Rodger M, Walker M, et al. Significance of IGFBP-4 in the development of fetal growth restriction. The Journal of clinical endocrinology and metabolism. 2012;97(8):E1429–39. doi: 10.1210/jc.2011-2511 22689691
66. Irwin JC, Suen LF, Martina NA, Mark SP, Giudice LC, Role of the IGF system in trophoblast invasion and pre-eclampsia. Hum Reprod. 1999;14 Suppl 2:90–6. Epub 2000/02/26. 10690804
67. Mantena SR, Kannan A, Cheon YP, Li Q, Johnson PF, Bagchi IC, et al. C/EBPbeta is a critical mediator of steroid hormone-regulated cell proliferation and differentiation in the uterine epithelium and stroma. Proc Natl Acad Sci U S A. 2006;103(6):1870–5. Epub 2006/01/28. 16439483
68. Huang da W, Sherman BT, Lempicki RA, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009;4(1):44–57. Epub 2009/01/10. doi: 10.1038/nprot.2008.211 19131956
69. Livak KJ, Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. 11846609