Cellular heterogeneity during embryonic stem cell differentiation to epiblast stem cells is revealed by the ShcD/RaLP adaptor protein

Stem Cells

Volumn 30, Issue 11, 2012, Pages 2423-2436

  Turco, Margherita Y ^a   Furia, Laura ^a   Dietze, Anja ^b   Diaz, Luis Fernandez ^a   Ronzoni, Simona ^a   Sciullo, Anna ^c   Simeone, Antonio ^d,e,f   Constam, Daniel ^b   Faretta, Mario ^a   Lanfrancone, Luisa ^a  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b EPFL   (Switzerland)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^e SEMM European School of Molecular Medicine   (Italy)

^f INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

Cdx2; Differentiation; Embryonic stem cells; Epiblast stem cells; Oct4; ShcD RaLP

Indexed keywords

ADAPTOR PROTEIN; CASPASE 3; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN RALP; PROTEIN SHCD; TRANSCRIPTION FACTOR CDX2; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL DEATH; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL POPULATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENZYME ACTIVATION; EPIBLAST STEM CELL; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOFLUORESCENCE TEST; MOUSE; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL; TIME LAPSE IMAGING;

ANIMALS; ANTIGENS, DIFFERENTIATION; APOPTOSIS; CASPASE 3; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM LAYERS; HOMEODOMAIN PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; OCTAMER TRANSCRIPTION FACTOR-3; PHOSPHOPROTEINS; SHC SIGNALING ADAPTOR PROTEINS; TIME-LAPSE IMAGING; TRANSCRIPTION FACTORS;

EID: 84867917232     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1217     Document Type: Article

References (62)

1. Pelicci G, Lanfrancone L, Grignani F et al. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 1992;70:93-104.
2. Pelicci G, Dente L, De Giuseppe A et al. A family of Shc related proteins with conserved PTB, CH1 and SH2 regions. Oncogene 1996;13:633-641. (Pubitemid 26283860)
3. Lai KM, Pawson T. The ShcA phosphotyrosine docking protein sensitizes cardiovascular signaling in the mouse embryo. Genes Dev 2000;14:1132-1145. (Pubitemid 30324426)
4. Conti L, De Fraja C, Gulisano M et al. Expression and activation of SH2/PTB-containing ShcA adaptor protein reflects the pattern of neurogenesis in the mammalian brain. Proc Natl Acad Sci USA 1997;94:8185-8190. (Pubitemid 27343798)
5. Orsini F, Migliaccio E, Moroni M et al. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem 2004;279:25689-25695. (Pubitemid 38756832)
6. Giorgio M, Migliaccio E, Orsini F et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005;122:221-233. (Pubitemid 41032986)
7. O'Bryan JP, Songyang Z, Cantley L et al. A mammalian adaptor protein with conserved Src homology 2 and phosphotyrosine-binding domains is related to Shc and is specifically expressed in the brain. Proc Natl Acad Sci USA 1996;93:2729-2734. (Pubitemid 26114317)
8. Pelicci G, Troglio F, Bodini A et al. The neuron-specific Rai (ShcC) adaptor protein inhibits apoptosis by coupling Ret to the phosphatidylinositol 3-kinase/Akt signaling pathway. Mol Cell Biol 2002;22:7351-7363.
9. Jones N, Hardy WR, Friese MB et al. Analysis of a Shc family adaptor protein, ShcD/Shc4, that associates with muscle-specific kinase. Mol Cell Biol 2007;27:4759-4773. (Pubitemid 47016129)
10. Fagiani E, Giardina G, Luzi L et al. RaLP, a new member of the Src homology and collagen family, regulates cell migration and tumor growth of metastatic melanomas. Cancer Res 2007;67:3064-3073. (Pubitemid 46724843)
11. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981;292:154-156. (Pubitemid 11050741)
12. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981;78:7634-7638. (Pubitemid 12186197)
13. Tesar PJ. Derivation of germ-line-competent embryonic stem cell lines from preblastocyst mouse embryos. Proc Natl Acad Sci USA 2005;102:8239-8244. (Pubitemid 40800073)
14. Suda Y, Suzuki M, Ikawa Y et al. Mouse embryonic stem cells exhibit indefinite proliferative potential. J Cell Physiol 1987;133:197-201. (Pubitemid 18022466)
15. Beddington RS, Robertson EJ. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 1989;105:733-737. (Pubitemid 19107071)
16. Bradley A, Evans M, Kaufman MH et al. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 1984;309:255-256. (Pubitemid 14139934)
17. Chambers I, Silva J, Colby D et al. Nanog safeguards pluripotency and mediates germline development. Nature 2007;450:1230-1234.
18. Masui S, Nakatake Y, Toyooka Y et al. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 2007;9:625-635. (Pubitemid 47214724)
19. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000;24:372-376. (Pubitemid 30187435)
20. Hay DC, Sutherland L, Clark J et al. Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells 2004;22:225-235. (Pubitemid 38282637)
21. ten Berge D, Koole W, Fuerer C et al. Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 2008;3:508-518.
22. Zhang K, Li L, Huang C et al. Distinct functions of BMP4 during different stages of mouse ES cell neural commitment. Development 2010;137:2095-2105.
23. Abranches E, Silva M, Pradier L et al. Neural differentiation of embryonic stem cells in vitro: A road map to neurogenesis in the embryo. PLoS One 2009;4:e6286.
24. Sterneckert J, Stehling M, Bernemann C et al. Neural induction intermediates exhibit distinct roles of fgf signaling. Stem Cells 2010;28:1772-1781.
25. Hawley SP, Wills MK, Rabalski AJ et al. Expression patterns of ShcD and Shc family adaptor proteins during mouse embryonic development. Dev Dyn 2011;240:221-231.
26. Nichols J, Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009;4:487-492.
27. Tesar PJ, Chenoweth JG, Brook FA et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007;448:196-199. (Pubitemid 47067378)
28. Brons IG, Smithers LE, Trotter MW et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007;448:191-195. (Pubitemid 47067373)
29. Berge DT, Kurek D, Blauwkamp T et al. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 2011;13:1070-1075.
30. Guo G, Yang J, Nichols J et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 2009;136:1063-1069.
31. Burdon T, Chambers I, Stracey C et al. Signaling mechanisms regulating self-renewal and differentiation of pluripotent embryonic stem cells. Cells Tissues Organs 1999;165:131-143.
32. Buehr M, Smith A. Genesis of embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 2003;358:1397-1402; discussion 1402.
33. Ying QL, Stavridis M, Griffiths D et al. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 2003;21:183-186. (Pubitemid 36188218)
34. Ying QL, Nichols J, Evans EP et al. Changing potency by spontaneous fusion. Nature 2002;416:545-548. (Pubitemid 34288857)
35. Ying QL, Wray J, Nichols J et al. The ground state of embryonic stem cell self-renewal. Nature 2008;453:519-523. (Pubitemid 351733324)
36. Ying QL, Smith AG. Defined conditions for neural commitment and differentiation. Methods Enzymol 2003;365:327-341. (Pubitemid 37531558)
37. Conti L, Pollard SM, Gorba T et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005;3:e283.
38. Desbaillets I, Ziegler U, Groscurth P et al. Embryoid bodies: An in vitro model of mouse embryogenesis. Exp Physiol 2000;85:645-651.
39. Lowell S, Benchoua A, Heavey B et al. Notch promotes neural lineage entry by pluripotent embryonic stem cells. PLoS Biol 2006;4:e121.
40. Strumpf D, Mao CA, Yamanaka Y et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005;132:2093-2102. (Pubitemid 40744469)
41. Niwa H, Toyooka Y, Shimosato D et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005;123:917-929. (Pubitemid 41721036)
42. Smith ZD, Nachman I, Regev A et al. Dynamic single-cell imaging of direct reprogramming reveals an early specifying event. Nat Biotechnol 2010;28:521-526.
43. Lu CW, Yabuuchi A, Chen L et al. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet 2008;40:921-926. (Pubitemid 351913657)
44. Singh AM, Hamazaki T, Hankowski KE et al. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 2007;25:2534-2542. (Pubitemid 47582745)
45. Canham MA, Sharov AA, Ko MS et al. Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol 2010;8:e1000379.
46. Nichols J, Zevnik B, Anastassiadis K et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998;95:379-391. (Pubitemid 28507326)
47. Rosner MH, Vigano MA, Ozato K et al. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 1990;345:686-692.
48. Avilion AA, Nicolis SK, Pevny LH et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003;17:126-140. (Pubitemid 36062514)
49. Ng RK, Dean W, Dawson C et al. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 2008;10:1280-1290.
50. Schenke-Layland K, Angelis E, Rhodes KE et al. Collagen IV induces trophoectoderm differentiation of mouse embryonic stem cells. Stem Cells 2007;25:1529-1538. (Pubitemid 47106022)
51. He S, Pant D, Schiffmacher A et al. Lymphoid enhancer factor 1-mediated Wnt signaling promotes the initiation of trophoblast lineage differentiation in mouse embryonic stem cells. Stem Cells 2008;26:842-849.
52. Hemberger M, Nozaki T, Winterhager E et al. Parp1-deficiency induces differentiation of ES cells into trophoblast derivatives. Dev Biol 2003;257:371-381. (Pubitemid 36506851)
53. Macfarlan TS, Gifford WD, Driscoll S et al. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 2012;487:57-63.
54. Chawengsaksophak K, de Graaff W, Rossant J et al. Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 2004;101:7641-7645. (Pubitemid 38658082)
55. Bernardo AS, Faial T, Gardner L et al. BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 2011;9:144-155.
56. Han DW, Greber B, Wu G et al. Direct reprogramming of fibroblasts into epiblast stem cells. Nat Cell Biol 2011;13:66-71.
57. Bernemann C, Greber B, Ko K et al. Distinct developmental ground states of epiblast stem cell lines determine different pluripotency features. Stem Cells 2011;29:1496-1503.
58. Toyooka Y, Shimosato D, Murakami K et al. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 2008;135:909-918. (Pubitemid 351524145)
59. Hayashi K, Lopes SM, Tang F et al. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 2008;3:391-401.
60. Han DW, Tapia N, Joo JY et al. Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell 2010;143:617-627.
61. Chazaud C, Yamanaka Y, Pawson T et al. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 2006;10:615-624.
62. Kelly KF, Ng DY, Jayakumaran G et al. Beta-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 2011;8:214-227.