Hectd1 is required for development of the junctional zone of the placenta

Developmental Biology

Volumn 392, Issue 2, 2014, Pages 368-380

  Sarkar, Anjali A ^a   Nuwayhid, Samer J ^a   Maynard, Thomas ^b   Ghandchi, Frederick ^a   Hill, Jonathon T ^c   Lamantia, Anthony S ^b   Zohn, Irene E ^a,b  

^a CHILDREN S RESEARCH INSTITUTE   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

HECT E3 ligase; Placenta; Trophoblast

Indexed keywords

GLYCOGEN; PROTEIN HECTD1; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ADULT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DECIDUA; ENRICHMENT CULTURE; FEMALE; GENE DISRUPTION; HECTD1 GENE; HOMOZYGOSITY; IMMUNOBLOTTING; IMMUNOREACTIVITY; INTRAUTERINE GROWTH RETARDATION; LETHALITY; MESODERM; MOUSE; NATURAL KILLER CELL; NONHUMAN; PLACENTA DEVELOPMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REPRODUCTION; TROPHOBLAST;

HECT E3 LIGASE; PLACENTA; TROPHOBLAST;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; FEMALE; GIANT CELLS; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; MICE; PLACENTA; PLACENTAL LACTOGEN; PREGNANCY; TROPHOBLASTS; UBIQUITIN-PROTEIN LIGASES;

EID: 84904385113     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.05.007     Document Type: Article

References (58)

1. Barak Y., Liao D., He W., Ong E.S., Nelson M.C., Olefsky J.M., Boland R., Evans R.M. Effects of peroxisome proliferator-activated receptor delta on placentation, adiposity, and colorectal cancer. Proc. Natl. Acad. Sci. USA 2002, 99:303-308.
2. Barak Y., Sadovsky Y., Shalom-Barak T. PPAR signaling in placental development and function. PPAR Res. 2008, 142082.
3. Bebington C., Doherty F.J., Fleming S.D. Ubiquitin and ubiquitin-protein conjugates are present in human cytotrophoblast throughout gestation. Early Pregnancy 2000, 4:240-252.
4. Bergman A., Siegal M.L. Evolutionary capacitance as a general feature of complex gene networks. Nature 2003, 424:549-552.
5. Bilinski M.J., Thorne J.G., Oh M.J., Leonard S., Murrant C., Tayade C., Croy B.A. Uterine NK cells in murine pregnancy. Reprod. Biomed. Online 2008, 16:218-226.
6. Bouillot S., Rampon C., Tillet E., Huber P. Tracing the glycogen cells with protocadherin 12 during mouse placenta development. Placenta 2006, 27:882-888.
7. Carney E.W., Prideaux V., Lye S.J., Rossant J. Progressive expression of trophoblast-specific genes during formation of mouse trophoblast giant cells in vitro. Mol. Reprod. Dev. 1993, 34:357-368.
8. Caspary T., Cleary M.A., Perlman E.J., Zhang P., Elledge S.J., Tilghman S.M. Oppositely imprinted genes p57(Kip2) and igf2 interact in a mouse model for Beckwith-Wiedemann syndrome. Genes Dev. 1999, 13:3115-3124.
9. Catela C., Bilbao-Cortes D., Slonimsky E., Kratsios P., Rosenthal N., Te Welscher P. Multiple congenital malformations of Wolf-Hirschhorn syndrome are recapitulated in Fgfrl1 null mice. Dis. Models Mech. 2009, 2:283-294.
10. Coan P.M., Conroy N., Burton G.J., Ferguson-Smith A.C. Origin and characteristics of glycogen cells in the developing murine placenta. Dev. Dyn.: Off. Publ. Am. Assoc. Anat. 2006, 235:3280-3294.
11. Coan P.M., Ferguson-Smith A.C., Burton G.J. Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol. Reprod. 2004, 70:1806-1813.
12. Copp A.J., Greene N.D., Murdoch J.N. The genetic basis of mammalian neurulation. Nat. Rev. Genet. 2003, 4:784-793.
13. Cross J.C. How to make a placenta: mechanisms of trophoblast cell differentiation in mice-a review. Placenta 2005, 26(Suppl. A):S3-9.
14. Cross J.C. Placental function in development and disease. Reprod. Fertil. Dev. 2006, 18:71-76.
15. Croy B.A., He H., Esadeg S., Wei Q., McCartney D., Zhang J., Borzychowski A., Ashkar A.A., Black G.P., Evans S.S., et al. Uterine natural killer cells: insights into their cellular and molecular biology from mouse modelling. Reproduction 2003, 126:149-160.
16. Eggenschwiler J., Ludwig T., Fisher P., Leighton P.A., Tilghman S.M., Efstratiadis A. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev. 1997, 11:3128-3142.
17. Faria T.N., Ogren L., Talamantes F., Linzer D.I., Soares M.J. Localization of placental lactogen-I in trophoblast giant cells of the mouse placenta. Biol. Reprod. 1991, 44:327-331.
18. Fowden A.L., Forhead A.J., Coan P.M., Burton G.J. The placenta and intrauterine programming. J. Neuroendocrinol. 2008, 20:439-450.
19. Frank D., Fortino W., Clark L., Musalo R., Wang W., Saxena A., Li C.M., Reik W., Ludwig T., Tycko B. Placental overgrowth in mice lacking the imprinted gene Ipl. Proc. Natl. Acad. Sci. USA 2002, 99:7490-7495.
20. Georgiades P., Ferguson-Smith A.C., Burton G.J. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002, 23:3-19.
21. Guillemot F., Nagy A., Auerbach A., Rossant J., Joyner A.L. Essential role of Mash-2 in extraembryonic development. Nature 1994, 371:333-336.
22. Harris L.K. Review: trophoblast-vascular cell interactions in early pregnancy: how to remodel a vessel. Placenta 2010, 31(Suppl.):S93-S98.
23. Hu D., Cross J.C. Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev. Biol. 2011, 358:231-239.
24. Jackson L.L., Colosi P., Talamantes F., Linzer D.I. Molecular cloning of mouse placental lactogen cDNA. Proc. Natl. Acad. Sci. USA 1986, 83:8496-8500.
25. Jiang B., Zhao W., Yuan J., Qian Y., Sun W., Zou Y., Guo C., Chen B., Shao C., Gong Y. Lack of Cul4b, an E3 ubiquitin ligase component, leads to embryonic lethality and abnormal placental development. PloS One 2012, 7:e37070.
26. Kasarskis A., Manova K., Anderson K.V. A phenotype-based screen for embryonic lethal mutations in the mouse. Proc. Natl. Acad. Sci. USA 1998, 95:7485-7490.
27. Li X., Zhou Q., Sunkara M., Kutys M.L., Wu Z., Rychahou P., Morris A.J., Zhu H., Evers B.M., Huang C. Ubiquitylation of phosphatidylinositol 4-phosphate 5-kinase type I gamma by HECTD1 regulates focal adhesion dynamics and cell migration. J. Cell Sci. 2013, 126:2617-2628.
28. Linzer D.I., Lee S.J., Ogren L., Talamantes F., Nathans D. Identification of proliferin mRNA and protein in mouse placenta. Proc. Natl. Acad. Sci. USA 1985, 82:4356-4359.
29. Longtine M.S., Nelson D.M. Placental dysfunction and fetal programming: the importance of placental size, shape, histopathology, and molecular composition. Semin. Reprod. Med. 2011, 29:187-196.
30. Malassine A., Frendo J.L., Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum. Reprod. Update 2003, 9:531-539.
31. Maynard T.M., Gopalakrishna D., Meechan D.W., Paronett E.M., Newbern J.M., LaMantia A.S. 22q11 Gene dosage establishes an adaptive range for sonic hedgehog and retinoic acid signaling during early development. Hum. Mol. Genet. 2013, 22:300-312.
32. Nagy A. Manipulating the Mouse Embryo: A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 3rd ed.
33. Parast M.M., Yu H., Ciric A., Salata M.W., Davis V., Milstone D.S. PPARgamma regulates trophoblast proliferation and promotes labyrinthine trilineage differentiation. PloS One 2009, 4:e8055.
34. Queitsch C., Sangster T.A., Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624.
35. Riley P., Anson-Cartwright L., Cross J.C. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat. Genet. 1998, 18:271-275.
36. Rohner N., Jarosz D.F., Kowalko J.E., Yoshizawa M., Jeffery W.R., Borowsky R.L., Lindquist S., Tabin C.J. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 2013, 342:1372-1375.
37. Rossant J., Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2001, 2:538-548.
38. Ruden D.M., Garfinkel M.D., Sollars V.E., Lu X. Waddington's widget: Hsp90 and the inheritance of acquired characters. Semin. Cell Dev. Biol. 2003, 14:301-310.
39. Rutherford S.L., Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998, 396:336-342.
40. Sarkar A.A., Zohn I.E. Hectd1 regulates intracellular localization and secretion of Hsp90 to control cellular behavior of the cranial mesenchyme. J. Cell Biol. 2012, 196:789-800.
41. Sarkar, A.A., Zohn, I.E., Hectd1 is required for development of the placental labyrinth, in preparation.
42. Scott I.C., Anson-Cartwright L., Riley P., Reda D., Cross J.C. The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol. Cell. Biol. 2000, 20:530-541.
43. Simmons D.G., Fortier A.L., Cross J.C. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 2007, 304:567-578.
44. Sollars V., Lu X., Xiao L., Wang X., Garfinkel M.D., Ruden D.M. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat. Genet. 2003, 33:70-74.
45. Sonderegger S., Pollheimer J., Knofler M. Wnt signalling in implantation, decidualisation and placental differentiation-review. Placenta 2010, 31:839-847.
46. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
47. Tanaka M., Gertsenstein M., Rossant J., Nagy A. Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev. Biol. 1997, 190:55-65.
48. Tesser R.B., Scherholz P.L., do Nascimento L., Katz S.G. Trophoblast glycogen cells differentiate early in the mouse ectoplacental cone: putative role during placentation. Histochem. Cell Biol. 2010, 134:83-92.
49. Tran H., Bustos D., Yeh R., Rubinfeld B., Lam C., Shriver S., Zilberleyb I., Lee M.W., Phu L., Sarkar A.A., et al. HectD1 E3 ligase modifies adenomatous polyposis coli (APC) with polyubiquitin to promote the APC-axin interaction. J. Biol. Chem. 2013, 288:3753-3767.
50. van Nes J., de Graaff W., Lebrin F., Gerhard M., Beck F., Deschamps J. The Cdx4 mutation affects axial development and reveals an essential role of Cdx genes in the ontogenesis of the placental labyrinth in mice. Development 2006, 133:419-428.
51. Voss A.K., Thomas T., Gruss P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development 2000, 127:1-11.
52. Wallace A.E., Fraser R., Cartwright J.E. Extravillous trophoblast and decidual natural killer cells: a remodelling partnership. Hum. Reprod. Update 2012, 18:458-471.
53. Withington S.L., Scott A.N., Saunders D.N., Lopes Floro K., Preis J.I., Michalicek J., Maclean K., Sparrow D.B., Barbera J.P., Dunwoodie S.L. Loss of Cited2 affects trophoblast formation and vascularization of the mouse placenta. Dev. Biol. 2006, 294:67-82.
54. Yang Z.Z., Tschopp O., Hemmings-Mieszczak M., Feng J., Brodbeck D., Perentes E., Hemmings B.A. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J. Biol. Chem. 2003, 278:32124-32131.
55. Yeyati P.L., van Heyningen V. Incapacitating the evolutionary capacitor: Hsp90 modulation of disease. Curr. Opin. Genet. Dev. 2008, 18:264-272.
56. Yuen R.K., Robinson W.P. Review: a high capacity of the human placenta for genetic and epigenetic variation: implications for assessing pregnancy outcome. Placenta 2011, 32(Suppl. 2):S136-141.
57. Zohn I.E., Anderson K.V., Niswander L. The Hectd1 ubiquitin ligase is required for development of the head mesenchyme and neural tube closure. Dev. Biol. 2007, 306:208-221.
58. Zohn I.E., Li Y., Skolnik E.Y., Anderson K.V., Han J., Niswander L. p38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 2006, 125:957-969.