Heightened potency of human pluripotent stem cell lines created by transient BMP4 exposure

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 18, 2015, Pages E2337-E2346

  Yang, Ying ^a   Adachi, Katsuyuki ^b   Sheridan, Megan A ^b   Alexenko, Andrei P ^a   Schust, Danny J ^b   Schulz, Laura C ^b   Ezashi, Toshihiko ^a   Roberts, R Michael ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

Biological sciences; Developmental biology; Pluripotent stem cells; Totipotent; Trophoblast

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; BONE MORPHOGENETIC PROTEIN 4; CHORIONIC GONADOTROPIN; FIBROBLAST GROWTH FACTOR 2; GROWTH DIFFERENTIATION FACTOR 3; HLA G ANTIGEN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR LEFTY1; TRANSCRIPTION FACTOR LEFTY2; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; BMP4 PROTEIN, HUMAN; COLLAGEN; CULTURE MEDIUM; DRUG COMBINATION; LAMININ; MATRIGEL; PROTEOGLYCAN; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL ISOLATION; CELL LINEAGE; CELL RENEWAL; COMPARATIVE ANATOMY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FIBROBLAST; HORMONE RELEASE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KARYOTYPE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PLURIPOTENT STEM CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL CULTURE; SYNCYTIOTROPHOBLAST; TERATOMA; TOTIPOTENT STEM CELL; TROPHOBLAST; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL LINE; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DNA MICROARRAY; DRUG COMBINATION; FEMALE; GENE EXPRESSION REGULATION; METABOLISM; PLACENTA; PREGNANCY; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; COLLAGEN; CULTURE MEDIA; CULTURE MEDIA, CONDITIONED; DRUG COMBINATIONS; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LAMININ; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PLACENTA; PLURIPOTENT STEM CELLS; PREGNANCY; PROTEOGLYCANS; SIGNAL TRANSDUCTION; TERATOMA; TRANSCRIPTOME; TROPHOBLASTS;

EID: 84928946673     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504778112     Document Type: Article

References (66)

1. Nichols J, Smith A (2009) Naive and primed pluripotent states. Cell Stem Cell 4(6):487-492.
2. Brons IG, et al. (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448(7150):191-195.
3. Tesar PJ, et al. (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448(7150):196-199.
4. Greber B, et al. (2010) Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 6(3):215-226.
5. Vallier L, et al. (2009) Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signalling pathways. PLoS ONE 4(6):e6082.
6. Vallier L, Alexander M, Pedersen RA (2005) Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 118(Pt 19):4495-4509.
7. Vallier L, et al. (2009) Signaling pathways controlling pluripotency and early cell fate decisions of human induced pluripotent stem cells. Stem Cells 27(11):2655-2666.
8. Xu RH, et al. (2008) NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3(2):196-206.
9. Schenke-Layland K, et al. (2007) Collagen IV induces trophoectoderm differentiation of mouse embryonic stem cells. Stem Cells 25(6):1529-1538.
10. He S, Pant D, Schiffmacher A, Meece A, Keefer CL (2008) Lymphoid enhancer factor 1-mediated Wnt signaling promotes the initiation of trophoblast lineage differentiation in mouse embryonic stem cells. Stem Cells 26(4):842-849.
11. Hayashi Y, et al. (2010) BMP4 induction of trophoblast from mouse embryonic stem cells in defined culture conditions on laminin. In Vitro Cell Dev Biol Anim 46(5):416-430.
12. Harun R, et al. (2006) Cytotrophoblast stem cell lines derived from human embryonic stem cells and their capacity to mimic invasive implantation events. Hum Reprod 21(6):1349-1358.
13. Gerami-Naini B, et al. (2004) Trophoblast differentiation in embryoid bodies derived from human embryonic stem cells. Endocrinology 145(4):1517-1524.
14. Chen G, et al. (2008) Trophoblast differentiation defect in human embryonic stem cells lacking PIG-A and GPI-anchored cell-surface proteins. Cell Stem Cell 2(4):345-355.
15. Douglas GC, VandeVoort CA, Kumar P, Chang TC, Golos TG (2009) Trophoblast stem cells: Models for investigating trophectoderm differentiation and placental development. Endocr Rev 30(3):228-240.
16. Drukker M, et al. (2012) Isolation of primitive endoderm, mesoderm, vascular endothelial and trophoblast progenitors from human pluripotent stem cells. Nat Biotechnol 30(6):531-542.
17. Li Y, et al. (2013) BMP4-directed trophoblast differentiation of human embryonic stem cells is mediated through a ΔNp63+ cytotrophoblast stem cell state. Development 140(19):3965-3976.
18. Marchand M, et al. (2011) Transcriptomic signature of trophoblast differentiation in a human embryonic stem cell model. Biol Reprod 84(6):1258-1271.
19. Schulz LC, et al. (2008) Human embryonic stem cells as models for trophoblast differentiation. Placenta 29(Suppl A):S10-S16.
20. Sudheer S, Bhushan R, Fauler B, Lehrach H, Adjaye J (2012) FGF inhibition directs BMP4-mediated differentiation of human embryonic stem cells to syncytiotrophoblast. Stem Cells Dev 21(16):2987-3000.
21. Das P, et al. (2007) Effects of fgf2 and oxygen in the bmp4-driven differentiation of trophoblast from human embryonic stem cells. Stem Cell Res (Amst) 1(1):61-74.
22. Erb TM, et al. (2011) Paracrine and epigenetic control of trophectoderm differentiation from human embryonic stem cells: The role of bone morphogenic protein 4 and histone deacetylases. Stem Cells Dev 20(9):1601-1614.
23. Xu RH, et al. (2002) BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20(12):1261-1264.
24. Lichtner B, Knaus P, Lehrach H, Adjaye J (2013) BMP10 as a potent inducer of trophoblast differentiation in human embryonic and induced pluripotent stem cells. Biomaterials 34(38):9789-9802.
25. Amita M, et al. (2013) Complete and unidirectional conversion of human embryonic stem cells to trophoblast by BMP4. Proc Natl Acad Sci USA 110(13):E1212-E1221.
26. Telugu BP, et al. (2013) Comparison of extravillous trophoblast cells derived from human embryonic stem cells and from first trimester human placentas. Placenta 34(7): 536-543.
27. Bai Q, et al. (2012) Dissecting the first transcriptional divergence during human embryonic development. Stem Cell Rev 8(1):150-162.
28. Ying QL, Nichols J, Chambers I, Smith A (2003) BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115(3):281-292.
29. Hassani SN, et al. (2014) Inhibition of TGFβ signaling promotes ground state pluripotency. Stem Cell Rev 10(1):16-30.
30. Bernardo AS, et al. (2011) BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 9(2):144-155.
31. Roberts RM, et al. (2014) Differentiation of trophoblast cells from human embryonic stem cells: to be or not to be? Reproduction 147(5):D1-D12.
32. Ludwig T, A Thompson J (2007) Defined, feeder-independent medium for human embryonic stem cell culture. Curr Protoc Stem Cell Biol Chapter 1:Unit 1C.2.
33. Chan EM, Yates F, Boyer LF, Schlaeger TM, Daley GQ (2008) Enhanced plating efficiency of trypsin-adapted human embryonic stem cells is reversible and independent of trisomy 12/17. Cloning Stem Cells 10(1):107-118.
34. Sánchez L, et al. (2012) Maintenance of human embryonic stem cells in media conditioned by human mesenchymal stem cells obviates the requirement of exogenous basic fibroblast growth factor supplementation. Tissue Eng Part C Methods 18(5):387-396.
35. Tanaka S (2006) Derivation and culture of mouse trophoblast stem cells in vitro. Methods Mol Biol 329:35-44.
36. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282(5396):2072-2075.
37. Müller FJ, et al. (2011) A bioinformatic assay for pluripotency in human cells. Nat Methods 8(4):315-317.
38. Roberts RM, Fisher SJ (2011) Trophoblast stem cells. Biol Reprod 84(3):412-421.
39. Kidder BL, Palmer S (2010) Examination of transcriptional networks reveals an important role for TCFAP2C, SMARCA4, and EOMES in trophoblast stem cell maintenance. Genome Res 20(4):458-472.
40. Ralston A, et al. (2010) Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137(3):395-403.
41. Chen Y, Blair K, Smith A (2013) Robust self-renewal of rat embryonic stem cells requires fine-tuning of glycogen synthase kinase-3 inhibition. Stem Cell Rev 1(3):209-217.
42. Hong J, et al. (2013) A focused microarray for screening rat embryonic stem cell lines. Stem Cells Dev 22(3):431-443.
43. Rajendran G, et al. (2013) Inhibition of protein kinase C signaling maintains rat embryonic stem cell pluripotency. J Biol Chem 288(34):24351-24362.
44. Niakan KK, Eggan K (2013) Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol 375(1):54-64.
45. Berg DK, et al. (2011) Trophectoderm lineage determination in cattle. Dev Cell 20(2): 244-255.
46. Chen L, et al. (2009) Cross-regulation of the Nanog and Cdx2 promoters. Cell Res 19(9):1052-1061.
47. Surani A, Tischler J (2012) Stem cells: A sporadic super state. Nature 487(7405):43-45.
48. Singh AM, Hamazaki T, Hankowski KE, Terada N (2007) A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25(10):2534-2542.
49. Macfarlan TS, et al. (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487(7405):57-63.
50. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445(7124): 214-218.
51. Abad M, et al. (2013) Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502(7471):340-345.
52. Benirschke K (2012) Pathology of the Human Placenta (Springer, New York).
53. Regelson W (1995) Have we found the "definitive cancer biomarker"? The diagnostic and therapeutic implications of human chorionic gonadotropin-beta expression as a key to malignancy. Cancer 76(8):1299-1301.
54. Butler SA, Iles RK (2003) Ectopic human chorionic gonadotropin beta secretion by epithelial tumors and human chorionic gonadotropin beta-induced apoptosis in Kaposi's sarcoma: Is there a connection? Clin Cancer Res 9(13):4666-4673.
55. Stenman UH, Alfthan H, Hotakainen K (2004) Human chorionic gonadotropin in cancer. Clin Biochem 37(7):549-561.
56. Itinteang T, et al. (2011) A placental chorionic villous mesenchymal core cellular origin for infantile haemangioma. J Clin Pathol 64(10):870-874.
57. Clark BZ, Beriwal S, Dabbs DJ, Bhargava R (2014) Semiquantitative GATA-3 immunoreactivity in breast, bladder, gynecologic tract, and other cytokeratin 7-positive carcinomas. Am J Clin Pathol 142(1):64-71.
58. Yang P, et al. (2014) Abnormal oxidative stress responses in fibroblasts from preeclampsia infants. PLoS ONE 9(7):e103110.
59. Graham SJ, et al. (2014) BMP signalling regulates the pre-implantation development of extra-embryonic cell lineages in the mouse embryo. Nat Commun 5:5667.
60. Chu GC, Dunn NR, Anderson DC, Oxburgh L, Robertson EJ (2004) Differential requirements for Smad4 in TGFbeta-dependent patterning of the early mouse embryo. Development 131(15):3501-3512.
61. Okita K, et al. (2011) A more efficient method to generate integration-free human iPS cells. Nat Methods 8(5):409-412.
62. Lee K, et al. (2014) Engraftment of human iPS cells and allogeneic porcine cells into pigs with inactivated RAG2 and accompanying severe combined immunodeficiency. Proc Natl Acad Sci USA 111(20):7260-7265.
63. Ludwig TE, et al. (2006) Feeder-independent culture of human embryonic stem cells. Nat Methods 3(8):637-646.
64. Amit M, et al. (2000) Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227(2):271-278.
65. Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102(13):4783-4788.
66. Xu RH (2006) In vitro induction of trophoblast from human embryonic stem cells. Methods Mol Med 121:189-202.