Specific glycosaminoglycans modulate neural specification of mouse embryonic stem cells

Stem Cells

Volumn 29, Issue 4, 2011, Pages 629-640

  Pickford, Claire E ^a   Holley, Rebecca J ^a   Rushton, Graham ^b   Stavridis, Marios P ^c   Ward, Christopher M ^d   Merry, Catherine L R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Differentiation; Embryonic stem cell; Fibroblast growth factors; Heparan sulfate; Pluripotency; Sox1

Indexed keywords

CARBOHYDRATE; GLYCOSAMINOGLYCAN; GLYCOSAMINOGLYCAN POLYSULFATE; HEPARAN SULFATE; HEPARIN; POLYSACCHARIDE; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR SOX1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL PROTECTION; ECTODERM; EMBRYO; EMBRYONIC STEM CELL; MOUSE; NERVE CELL DIFFERENTIATION; NEUROECTODERM; NONHUMAN; PLURIPOTENT STEM CELL; SIGNAL TRANSDUCTION; STEM CELL; SULFATION;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTORS; FLOW CYTOMETRY; GENE KNOCKOUT TECHNIQUES; GLYCOSAMINOGLYCANS; HEPARAN SULFATE PROTEOGLYCANS; MICE; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEURAL PLATE; NEURAL STEM CELLS; RECEPTOR PROTEIN-TYROSINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS;

EID: 79953774591     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.610     Document Type: Article

References (47)

1. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981;292:154-156. (Pubitemid 11050741)
2. Smith AG. Embryo-derived stem cells: Of mice and men. Annu Rev Cell Dev Biol 2001;17:435-462. (Pubitemid 33096183)
3. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest 2001;108:169-173. (Pubitemid 32656238)
4. Ai X, Do AT, Kusche-Gullberg M et al. Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2. J Biol Chem 2006;281:4969-4676.
5. Murphy KJ, Merry CL, Lyon M et al. A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase. J Biol Chem 2004;279:27239-27245. (Pubitemid 38812562)
6. Ford-Perriss M, Guimond SE, Greferath U et al. Variant heparan sulfates synthesized in developing mouse brain differentially regulate FGF signaling. Glycobiology 2002;12:721-727. (Pubitemid 36041476)
7. Habuchi H, Tanaka M, Habuchi O et al. The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J Biol Chem 2000;275:2859-2868. (Pubitemid 30082060)
8. Lanner F, Lee KL, Sohl M et al. Heparan sulfation dependent FGF signalling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells 2009;28:191-200.
9. Sugaya N, Habuchi H, Nagai N et al. 6-O-sulfation of heparan sulfate differentially regulates various fibroblast growth factor-dependent signalings in culture. J Biol Chem 2008;283:10366-10376.
10. Forsberg E, Pejler G, Ringvall M et al. Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 1999;400:773-776. (Pubitemid 29399539)
11. Ringvall M, Ledin J, Holmborn K et al. Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-deacetylase/N- sulfotransferase-1. J Biol Chem 2000;275:25926-25930.
12. Bullock SL, Fletcher JM, Beddington RS et al. Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev 1998;12:1894-1906. (Pubitemid 28304341)
13. Habuchi H, Nagai N, Sugaya N et al. Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J Biol Chem 2007;282:15578-15588.
14. Lin X, Wei G, Shi Z et al. Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev Biol 2000;224:299-311. (Pubitemid 30661012)
15. Stickens D, Zak BM, Rougier N et al. Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 2005;132: 5055-5068. (Pubitemid 41764016)
16. Rapraeger AC, Krufka A, Olwin BB. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991;252:1705-1708. (Pubitemid 21917092)
17. Yayon A, Klagsbrun M, Esko JD et al. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 1991;64:841-848. (Pubitemid 121001170)
18. Nurcombe V, Ford MD, Wildschut JA et al. Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 1993;260:103-106. (Pubitemid 23122755)
19. Brickman YG, Ford MD, Gallagher JT et al. Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J Biol Chem 1998;273:4350-4359. (Pubitemid 28103170)
20. Jiang R, Kato M, Bernfield M et al. Expression of syndecan-1 changes during the differentiation of visceral and parietal endoderm from murine F9 teratocarcinoma cells. Differentiation 1995;59:225-233. (Pubitemid 26004220)
21. Gallagher JT. The interaction and regulation of basic and acidic fibroblast growth factors by heparan sulphate. Trends Glycosci Glycotechnol 1998;10:137-144.
22. Allen BL, Rapraeger AC. Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J Cell Biol 2003;163:637-648. (Pubitemid 37429875)
23. Koziel L, Kunath M, Kelly OG et al. Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev Cell 2004;6:801-813. (Pubitemid 38745415)
24. Baldwin RJ, ten Dam GB, van Kuppevelt TH et al. A developmentally regulated heparan sulfate epitope defines a subpopulation with increased blood potential during mesodermal differentiation. Stem Cells 2008;26:3108-3118.
25. Johnson CE, Crawford BE, Stavridis M et al. Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells 2007;25:1913-1923. (Pubitemid 47258169)
26. Kunath T, Saba-El-Leil MK, Almousailleakh M et al. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007;134:2895-2902. (Pubitemid 47386902)
27. Stavridis MP, Collins BJ, Storey KG. Retinoic acid orchestrates fibroblast growth factor signalling to drive embryonic stem cell differentiation. Development 2010;137:881-890.
28. Stavridis MP, Lunn JS, Collins BJ et al. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 2007;134:2889-2894. (Pubitemid 47386901)
29. Liu R, Xu Y, Chen M et al. Chemoenzymatic design of heparan sulfate oligosaccharides. J Biol Chem 2010;285:34240-34249.
30. 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)
31. Aubert J, Stavridis MP, Tweedie S et al. Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc Natl Acad Sci 2003;100(suppl 1):11836-11841. (Pubitemid 37205892)
32. Wasteson A. A method for the determination of the molecular weight and molecular-weight distribution of chondroitin sulphate. J Chromatogr 1971;59:87-97.
33. Ying QL, Wray J, Nichols J et al. The ground state of embryonic stem cell self-renewal. Nature 2008;453:519-523. (Pubitemid 351733324)
34. Holley RJ, Pickford CE, Rushton G et al. Influencing hematopoietic differentiation of mouse embryonic stem cells using soluble heparin and heparan sulfate saccharides. J Biol Chem 2010 (in press).
35. Sasaki N, Okishio K, Ui-Tei K et al. Heparan sulfate regulates self-renewal and pluripotency of embryonic stem cells. J Biol Chem 2008; 283:3594-3606.
36. Presto J, Thuveson M, Carlsson P et al. Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc Natl Acad Sci USA 2008;105:4751-4756. (Pubitemid 351753818)
37. Pinhal MA, Smith B, Olson S et al. Enzyme interactions in heparan sulfate biosynthesis: Uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc Natl Acad Sci USA 2001;98:12984-12989.
38. Kraushaar DC, Yamaguchi Y, Wang L. Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J Biol Chem 2010; 285:5907-5916.
39. Holmborn K, Ledin J, Smeds E et al. Heparan sulfate synthesized by mouse embryonic stem cells deficient in NDST1 and NDST2 is 6-O-sulfated but contains no N-sulfate groups. J Biol Chem 2004;279: 42355-42358. (Pubitemid 39372115)
40. Sterneckert J, Stehling M, Bernemann C et al. Neural induction intermediates exhibit distinct roles of FGF signaling. Stem Cells 2010;28: 1772-1781.
41. Conlon FL, Lyons KM, Takaesu N et al. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 1994;120:1919-1928.
42. Gadue P, Huber TL, Paddison PJ et al. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci USA 2006; 103:16806-16811. (Pubitemid 44737334)
43. Yamada S, Busse M, Ueno M et al. Embryonic fibroblasts with a gene trap mutation in Ext1 produce short heparan sulfate chains. J Biol Chem 2004;279:32134-32141. (Pubitemid 39014660)
44. Ball SG, Shuttleworth CA, Kielty CM. Platelet-derived growth factor receptors regulate mesenchymal stem cell fate: Implications for neovascularization. Expert Opin Biol Ther 2010;10:57-71.
45. Heldin CH, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 1999;79:1283-1316. (Pubitemid 29473317)
46. Yarden Y. Biology of HER2 and its importance in breast cancer. Oncology 2001;61(suppl 2):1-13. (Pubitemid 33033419)
47. Barros FF, Powe DG, Ellis IO et al. Understanding the HER family in breast cancer: interaction with ligands, dimerization and treatments. Histopathology. 2010;56:560-572.