Trophoblast Differentiation Defect in Human Embryonic Stem Cells Lacking PIG-A and GPI-Anchored Cell-Surface Proteins

Cell Stem Cell

Volumn 2, Issue 4, 2008, Pages 345-355

  Chen, Guibin ^a   Ye, Zhaohui ^a   Yu, Xiaobing ^a   Zou, Jizhong ^a   Mali, Prashant ^a   Brodsky, Robert A ^a   Cheng, Linzhao ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

STEMCELL

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOLGLYCAN CLASS A PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CELL CLONING; CELL DIFFERENTIATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE EXPRESSION; GERM LAYER; HUMAN; HUMAN CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TROPHOBLAST;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; FIBROBLASTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSYLPHOSPHATIDYLINOSITOLS; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC STEM CELLS; HUMANS; KARYOTYPING; MEMBRANE PROTEINS; MICE; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFECTION; TROPHOBLASTS;

EID: 41449118508     PISSN: 19345909     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stem.2008.02.004     Document Type: Article

References (46)

1. Adjaye J., Huntriss J., Herwig R., BenKahla A., Brink T.C., Wierling C., Hultschig C., Groth D., Yaspo M.L., Picton H.M., et al. Primary differentiation in the human blastocyst: Comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells 23 (2005) 1514-1525
2. Babitt J.L., Zhang Y., Samad T.A., Xia Y., Tang J., Campagna J.A., Schneyer A.L., Woolf C.J., and Lin H.Y. Repulsive guidance molecule (RGMa), a DRAGON homologue, is a bone morphogenetic protein co-receptor. J. Biol. Chem. 280 (2005) 29820-29827
3. Babitt J.L., Huang F.W., Wrighting D.M., Xia Y., Sidis Y., Samad T.A., Campagna J.A., Chung R.T., Schneyer A.L., Woolf C.J., et al. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat. Genet. 38 (2006) 531-539
4. Besser D. Expression of nodal, lefty-a, and lefty-B in undifferentiated human embryonic stem cells requires activation of Smad2/3. J. Biol. Chem. 279 (2004) 45076-45084
5. Brodsky R.A., Mukhina G.L., Nelson K.L., Lawrence T.S., Jones R.J., and Buckley J.T. Resistance of Paroxysmal Nocturnal Hemoglobinuria Cells to the Glycosylphosphatidylinositol-Binding Toxin Aerolysin. Blood 93 (1999) 1749-1756
6. Brulet P., and Jacob F. Molecular cloning of a cDNA sequence encoding a trophectoderm-specific marker during mouse blastocyst formation. Proc. Natl. Acad. Sci. USA 79 (1982) 2328-2332
7. Chen D., Ji X., Harris M.A., Feng J.Q., Karsenty G., Celeste A.J., Rosen V., Mundy G.R., and Harris S.E. Differential roles for BMP receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. J. Cell Biol. 142 (1998) 295-305
8. Chesebro B., Trifilo M., Race R., Meade-White K., Teng C., LaCasse R., Raymond L., Favara C., Baron G., Priola S., et al. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308 (2005) 1435-1439
9. Draper J.S., Smith K., Gokhale P., Moore H.D., Maltby E., Johnson J., Meisner L., Zwaka T.P., Thomson J.A., and Andrews P.W. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol. 22 (2004) 53-54
10. Dravid G., Ye Z., Hammond H., Chen G., Pyle A., Donovan P.J., Yu X., and Cheng L. Defining the role of Wnt/beta-catenin signaling in the survival, proliferation and self-renewal of human embryonic stem cells. Stem Cells 23 (2005) 1489-1498
11. Dunn D.E., Tanawattanacharoen P., Boccuni P., Nagakura S., Green S.W., Kirby M.R., Kumar M.S., Rosenfeld S., and Young N.S. Paroxysmal Nocturnal Hemoglobinuria Cells in Patients with Bone Marrow Failure Syndromes. Ann. Intern. Med. 131 (1999) 401-408
12. Dunn D.E., Yu J., Nagarajan S., Devetten M., Weichold F.F., Medof M.E., Young N.S., and Liu J.M. A knock-out model of paroxysmal nocturnal hemoglobinuria: Pig-a(-) hematopoiesis is reconstituted following intercellular transfer of GPI-anchored proteins. Proc. Natl. Acad. Sci. USA 93 (1996) 7938-7943
13. Gerami-Naini B., Dovzhenko O.V., Durning M., Wegner F.H., Thomson J.A., and Golos T.G. Trophoblast differentiation in embryoid bodies derived from human embryonic stem cells. Endocrinology 145 (2004) 1517-1524
14. Ginis I., Luo Y., Miura T., Thies S., Brandenberger R., Gerecht-Nir S., Amit M., Hoke A., Carpenter M.K., Itskovitz-Eldor J., et al. Differences between human and mouse embryonic stem cells. Dev. Biol. 269 (2004) 360-380
15. Hogan B.L. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev. 10 (1996) 1580-1594
16. Hollnagel A., Oehlmann V., Heymer J., Ruther U., and Nordheim A. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J. Biol. Chem. 274 (1999) 19838-19845
17. Hu R., Mukhina G.L., Piantadosi S., Barber J.P., Jones R.J., and Brodsky R.A. PIG-A mutations in normal hematopoiesis. Blood 105 (2005) 3848-3854
18. James D., Levine A.J., Besser D., and Hemmati-Brivanlou A. TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132 (2005) 1273-1282
19. Kaufman D.S., Hanson E.T., Lewis R.L., Auerbach R., and Thomson J.A. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 98 (2001) 10716-10721
20. Keller P., Payne J.L., Tremml G., Greer P.A., Gaboli M., Pandolfi P.P., and Bessler M. FES-Cre targets phosphatidylinositol glycan class A (PIGA) inactivation to hematopoietic stem cells in the bone marrow. J. Exp. Med. 194 (2001) 581-589
21. Kinoshita T., Ohishi K., and Takeda J. GPI-anchor synthesis in mammalian cells: Genes, their products, and a deficiency. J. Biochem. (Tokyo) 122 (1997) 251-257
22. Lensch M.W., and Daley G.Q. Scientific and clinical opportunities for modeling blood disorders with embryonic stem cells. Blood 107 (2006) 2605-2612
23. Lopez-Rovira T., Chalaux E., Massague J., Rosa J.L., and Ventura F. Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J. Biol. Chem. 277 (2002) 3176-3185
24. Luzzatto L., Bessler M., and Rotoli B. Somatic mutations in paroxysmal nocturnal hemoglobinuria: A blessing in disguise?. Cell 88 (1997) 1-4
25. Minchiotti G., Parisi S., Liguori G., Signore M., Lania G., Adamson E.D., Lago C.T., and Persico M.G. Membrane-anchorage of Cripto protein by glycosylphosphatidylinositol and its distribution during early mouse development. Mech. Dev. 90 (2000) 133-142
26. Niwa H., Miyazaki J., and Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24 (2000) 372-376
27. Niwa H., Toyooka Y., Shimosato D., Strumpf D., Takahashi K., Yagi R., and Rossant J. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123 (2005) 917-929
28. Pera M.F., Andrade J., Houssami S., Reubinoff B., Trounson A., Stanley E.G., Ward-van Oostwaard D., and Mummery C. Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J. Cell Sci. 117 (2004) 1269-1280
29. Qi X., Li T.G., Hao J., Hu J., Wang J., Simmons H., Miura S., Mishina Y., and Zhao G.Q. BMP4 supports self-renewal of embryonic stem cells by inhibiting mitogen-activated protein kinase pathways. Proc. Natl. Acad. Sci. USA 101 (2004) 6027-6032
30. Rosti V., Tremml G., Soares V., Pandolfi P.P., Luzzatto L., and Bessler M. Murine embryonic stem cells without pig-a gene activity are competent for hematopoiesis with the PNH phenotype but not for clonal expansion. J. Clin. Invest. 100 (1997) 1028-1036
31. Samad T.A., Rebbapragada A., Bell E., Zhang Y., Sidis Y., Jeong S.J., Campagna J.A., Perusini S., Fabrizio D.A., Schneyer A.L., et al. DRAGON, a bone morphogenetic protein co-receptor. J. Biol. Chem. 280 (2005) 14122-14129
32. Schenke-Layland K., Angelis E., Rhodes K.E., Heydarkhan-Hagvall S., Mikkola H.K., and Maclellan W.R. Collagen IV induces trophoectoderm differentiation of mouse embryonic stem cells. Stem Cells 25 (2007) 1529-1538
33. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., and Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132 (2005) 2093-2102
34. Takeda J., Miyata T., Kawagoe K., Iida Y., Endo Y., Fujita T., Takahashi M., Kitani T., and Kinoshita T. Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria. Cell 73 (1993) 703-711
35. Tanaka T.S., Kunath T., Kimber W.L., Jaradat S.A., Stagg C.A., Usuda M., Yokota T., Niwa H., Rossant J., and Ko M.S. Gene expression profiling of embryo-derived stem cells reveals candidate genes associated with pluripotency and lineage specificity. Genome Res. 12 (2002) 1921-1928
36. Urbach A., Schuldiner M., and Benvenisty N. Modeling for Lesch-Nyhan disease by gene targeting in human embryonic stem cells. Stem Cells 22 (2004) 635-641
37. Xia Y., Sidis Y., Mukherjee A., Samad T.A., Brenner G., Woolf C.J., Lin H.Y., and Schneyer A. Localization and action of Dragon (repulsive guidance molecule b), a novel bone morphogenetic protein coreceptor, throughout the reproductive axis. Endocrinology 146 (2005) 3614-3621
38. Xia Y., Yu P.B., Sidis Y., Beppu H., Bloch K.D., Schneyer A.L., and Lin H.Y. Repulsive guidance molecule (RGMa) alters utilization of bone morphogenetic protein (BMP) type II receptors by BMP2 and BMP4. J. Biol. Chem. 282 (2007) 18129-18140
39. Xu R.H., Chen X., Li D.S., Li R., Addicks G.C., Glennon C., Zwaka T.P., and Thomson J.A. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat. Biotechnol. 20 (2002) 1261-1264
40. Xu R.H., Peck R.M., Li D.S., Feng X., Ludwig T., and Thomson J.A. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat. Methods 2 (2005) 185-190
41. Ying Q.L., Nichols J., Chambers I., and Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115 (2003) 281-292
42. Zhan X., Dravid G., Ye Z., Hammond H., Shamblott M., Gearhart J., and Cheng L. Functional antigen-presenting leucocytes derived from human embryonic stem cells in vitro. Lancet 364 (2004) 163-171
43. Zhang J., and Li L. BMP signaling and stem cell regulation. Dev. Biol. 284 (2005) 1-11
44. Zhou B.Y., Ye Z., Gao P.Z., Chen G., Zhang Y.A., and Cheng L. Inducible and reversible transgene expression in human stem cells after efficient and stable gene transfer. Stem Cells 25 (2007) 779-789
45. Zhang J., Tam W.L., Tong G.Q., Wu Q., Chan H.Y., Soh B.S., Lou Y., Yang J., Ma Y., Chai L., et al. Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat. Cell Biol. 8 (2006) 1114-1123
46. Zwaka T.P., and Thomson J.A. Homologous recombination in human embryonic stem cells. Nat. Biotechnol. 21 (2003) 319-321