A Positive Feedback Loop Involving Gcm1 and Fzd5 Directs Chorionic Branching Morphogenesis in the Placenta

PLoS Biology

Volumn 11, Issue 4, 2013, Pages

  Lu, Jinhua ^a,b   Zhang, Shuang ^a,b   Nakano, Haruo ^c,f   Simmons, David G ^c,g   Wang, Shumin ^a   Kong, Shuangbo ^a,b   Wang, Qiang ^a,b   Shen, Lianju ^a   Tu, Zhaowei ^a,b   Wang, Weixiang ^a   Wang, Bingyan ^a   Wang, Hongmei ^a   Wang, Yanling ^a   van Es, Johan H ^d   Clevers, Hans ^d   Leone, Gustavo ^e   Cross, James C ^c   Wang, Haibin ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF CALGARY   (Canada)

^d HUBRECHT INSTITUTE   (Netherlands)

^e OHIO STATE UNIVERSITY   (United States)

^f KYOWA HAKKO KOGYO CO LTD   (Japan)

^g UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CLAUDIN 4; CLAUDIN 7; FRIZZLED PROTEIN; FRIZZLED5 PROTEIN; GLIAL CELLS MISSING 1 PROTEIN; PROTEIN ZO1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL JUNCTION; CHORIOALLANTOIC BRANCHING MORPHOGENESIS; CHORION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; MORPHOGENESIS; MOUSE; NONHUMAN; PLACENTA DEVELOPMENT; POSITIVE FEEDBACK; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TROPHOBLAST; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CHORIOALLANTOIC MEMBRANE; CHORIONIC VILLI; FEEDBACK, PHYSIOLOGICAL; FEMALE; FRIZZLED RECEPTORS; GENE EXPRESSION REGULATION; GIANT CELLS; HEK293 CELLS; HUMANS; MALE; MICE; MICE, TRANSGENIC; MORPHOGENESIS; NUCLEAR PROTEINS; PLACENTA; PREGNANCY; TRANSCRIPTION FACTORS; TROPHOBLASTS; WNT SIGNALING PATHWAY;

EID: 84876976574     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001536     Document Type: Article

References (45)

1. Rossant J, Cross JC, (2001) Placental development: lessons from mouse mutants. Nat Rev Genet 2: 538-548.
2. Watson ED, Cross JC, (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20: 180-193.
3. Maltepe E, Bakardjiev AI, Fisher SJ, (2010) The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 120: 1016-1025.
4. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, et al. (2000) The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25: 311-314.
5. Hunter PJ, Swanson BJ, Haendel MA, Lyons GE, Cross JC, (1999) Mrj encodes a DnaJ-related co-chaperone that is essential for murine placental development. Development 126: 1247-1258.
6. Sonderegger S, Pollheimer J, Knofler M, (2010) Wnt signalling in implantation, decidualisation and placental differentiation-review. Placenta 31: 839-847.
7. Parr BA, Cornish VA, Cybulsky MI, McMahon AP, (2001) Wnt7b regulates placental development in mice. Dev Biol 237: 324-332.
8. Aoki M, Mieda M, Ikeda T, Hamada Y, Nakamura H, et al. (2007) R-spondin3 is required for mouse placental development. Dev Biol 301: 218-226.
9. Matsuura K, Jigami T, Taniue K, Morishita Y, Adachi S, et al. (2011) Identification of a link between Wnt/beta-catenin signalling and the cell fusion pathway. Nat Commun 2: 548.
10. Monkley SJ, Delaney SJ, Pennisi DJ, Christiansen JH, Wainwright BJ, (1996) Targeted disruption of the Wnt2 gene results in placentation defects. Development 122: 3343-3353.
11. Ishikawa T, Tamai Y, Zorn AM, Yoshida H, Seldin MF, et al. (2001) Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128: 25-33.
12. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, et al. (2005) Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7: 381-386.
13. Gurtner GC, Davis V, Li H, McCoy MJ, Sharpe A, et al. (1995) Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev 9: 1-14.
14. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, et al. (1995) Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121: 489-503.
15. Yang JT, Rayburn H, Hynes RO, (1995) Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121: 549-560.
16. Cross JC, Nakano H, Natale DR, Simmons DG, Watson ED, (2006) Branching morphogenesis during development of placental villi. Differentiation 74: 393-401.
17. Wenzel PL, Leone G, (2007) Expression of Cre recombinase in early diploid trophoblast cells of the mouse placenta. Genesis 45: 129-134.
18. Wenzel PL, Wu L, de Bruin A, Chong JL, Chen WY, et al. (2007) Rb is critical in a mammalian tissue stem cell population. Genes Dev 21: 85-97.
19. Basyuk E, Cross JC, Corbin J, Nakayama H, Hunter P, et al. (1999) Murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev Dyn 214: 303-311.
20. Stecca B, Nait-Oumesmar B, Kelley KA, Voss AK, Thomas T, et al. (2002) Gcm1 expression defines three stages of chorio-allantoic interaction during placental development. Mech Dev 115: 27-34.
21. Simmons DG, Natale DR, Begay V, Hughes M, Leutz A, et al. (2008) Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 135: 2083-2091.
22. Dupressoir A, Vernochet C, Harper F, Guegan J, Dessen P, et al. (2011) A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc Natl Acad Sci U S A 108: E1164-E1173.
23. Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, et al. (2009) Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc Natl Acad Sci U S A 106: 12127-12132.
24. Thiery JP, Sleeman JP, (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
25. Horowitz A, Simons M, (2009) Branching morphogenesis. Circ Res 104: e21.
26. Mann B, Gelos M, Siedow A, Hanski ML, Gratchev A, et al. (1999) Target genes of beta-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc Natl Acad Sci U S A 96: 1603-1608.
27. Zhang X, Gaspard JP, Chung DC, (2001) Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res 61: 6050-6054.
28. Ring DB, Johnson KW, Henriksen EJ, Nuss JM, Goff D, et al. (2003) Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52: 588-595.
29. Chen B, Dodge ME, Tang W, Lu J, Ma Z, et al. (2009) Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 5: 100-107.
30. ten Berge D, Kurek D, Blauwkamp T, Koole W, Maas A, et al. (2011) Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 13: 1070-1075.
31. Blauwkamp TA, Nigam S, Ardehali R, Weissman IL, Nusse R, (2012) Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 3: 1070.
32. Maiti G, Naskar D, Sen M, (2012) The Wingless homolog Wnt5a stimulates phagocytosis but not bacterial killing. Proc Natl Acad Sci U S A 109: 16600-16605.
33. Baczyk D, Drewlo S, Proctor L, Dunk C, Lye S, (2009) Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 16: 719-727.
34. Mi S, Lee X, Li X, Veldman GM, Finnerty H, et al. (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403: 785-789.
35. Yu C, Shen K, Lin M, Chen P, Lin C, et al. (2002) GCMa regulates the syncytin-mediated trophoblastic fusion. J Biol Chem 277: 50062-50068.
36. Steingrimsson E, Tessarollo L, Reid SW, Jenkins NA, Copeland NG, (1998) The bHLH-Zip transcription factor Tfeb is essential for placental vascularization. Development 125: 4607-4616.
37. Ylikorkala A, Rossi DJ, Korsisaari N, Luukko K, Alitalo K, et al. (2001) Vascular abnormalities and deregulation of VEGF in Lkb1-deficient mice. Science 293: 1323-1326.
38. Chen CP, Chen CY, Yang YC, Su TH, Chen H, (2004) Decreased placental GCM1 (glial cells missing) gene expression in pre-eclampsia. Placenta 25: 413-421.
39. Knerr I, Beinder E, Rascher W, (2002) Syncytin, a novel human endogenous retroviral gene in human placenta: evidence for its dysregulation in preeclampsia and HELLP syndrome. Am J Obstet Gynecol 186: 210-213.
40. Meng T, Chen H, Sun M, Wang H, Zhao G, et al. (2012) Identification of differential gene expression profiles in placentas from preeclamptic pregnancies versus normal pregnancies by DNA microarrays. Omics 16: 301-311.
41. Hogan B, Beddington R, Costantini F, Lacy E (1994) Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press. pp.220-236.
42. Natale DRC, Starovic M, Cross JC, (2006) Phenotypic analysis of the mouse placenta. Methods Mol Med 121: 275-293.
43. Das SK, Wang XN, Paria BC, Damm D, Abraham JA, et al. (1994) Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120: 1071-1083.
44. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC, (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 90: 8424-8428.
45. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J, (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282: 2072-2075.