Undersulfation of heparan sulfate restricts differentiation potential of mouse embryonic stem cells

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 10853-10862

  Forsberg, Maud ^a,b   Holmborn, Katarina ^a   Kundu, Soumi ^a   Dagälv, Anders ^a   Kjellén, Lena ^a   Forsberg Nilsson, Karin ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTES; CELL SURFACES; DIFFERENTIATION MARKERS; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRICES; GENE EXPRESSION ANALYSIS; GOLGI COMPARTMENTS; GROWTH FACTOR; HEPARAN SULFATES; IN-VITRO; INTERACTION POTENTIALS; MORPHOGENS; MOUSE EMBRYONIC STEM CELLS; NEURAL CELLS; PROTEOGLYCANS;

BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; CYTOLOGY; GENE EXPRESSION; MAMMALS; PEPTIDES;

OSTEOBLASTS;

CELL ENZYME; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; GLUCOSAMINYL N DEACETYLASE N SULFOTRANSFERASE 1; GLUCOSAMINYL N DEACETYLASE N SULFOTRANSFERASE 2; HEPARAN SULFATE; MORPHOGEN; PROTEOGLYCAN; TRANSCRIPTION FACTOR GATA 4; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ADIPOCYTE; ANIMAL CELL; ARTICLE; BRAIN CELL; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ASSAY; ENZYME SYNTHESIS; EXTRACELLULAR MATRIX; GOLGI COMPLEX; IN VITRO STUDY; INTRACELLULAR SIGNALING; MESODERM; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SULFATION;

ADIPOCYTES; AMIDOHYDROLASES; ANIMALS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL DIFFERENTIATION; ECTODERM; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTORS; GENE KNOCKOUT TECHNIQUES; HEPARIN; HEPARITIN SULFATE; MESODERM; MICE; MUTATION; OSTEOBLASTS; SIGNAL TRANSDUCTION; SULFOTRANSFERASES;

EID: 84859481405     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.337030     Document Type: Article

References (58)

1. Evans, M. J., and Kaufman, M. H. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 (Pubitemid 11050741)
2. Martin, G. R. (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U.S.A. 78, 7634-7638
3. Keller, G. (2005) Embryonic stem cell differentiation. Emergence of a new era in biology and medicine. Genes Dev. 19, 1129-1155
4. Doetschman, T. C., Eistetter, H., Katz, M., Schmidt, W., and Kemler, R. (1985) The in vitro development of blastocyst-derived embryonic stem cell lines. Formation of visceral yolk sac, blood islands, and myocardium. J. Embryol. Exp. Morphol. 87, 27-45 (Pubitemid 15029925)
5. Okabe, S., Forsberg-Nilsson, K., Spiro, A. C., Segal, M., and McKay, R. D. (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59, 89-102 (Pubitemid 26325462)
6. Ying, Q. L., Stavridis, M., Griffiths, D., Li, M., and Smith, A. (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186 (Pubitemid 36188218)
7. Bronner-Fraser, M., and Fraser, S. E. (1997) Differentiation of the vertebrate neural tube. Curr. Opin. Cell Biol. 9, 885-891 (Pubitemid 27517280)
8. De Robertis, E. M., and Kuroda, H. (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308 (Pubitemid 39488640)
9. Moreau, M., and Leclerc, C. (2004) The choice between epidermal and neural fate. A matter of calcium. Int. J. Dev. Biol. 48, 75-84 (Pubitemid 38807921)
10. Bachiller, D., Klingensmith, J., Kemp, C., Belo, J. A., Anderson, R. M., May, S. R., McMahon, J. A., McMahon, A. P., Harland, R. M., Rossant, J., and De Robertis, E. M. (2000) The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403, 658-661 (Pubitemid 30104006)
11. Linker, C., and Stern, C. D. (2004) Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development 131, 5671-5681 (Pubitemid 39625210)
12. Streit, A., Berliner, A. J., Papanayotou, C., Sirulnik, A., and Stern, C. D. (2000) Initiation of neural induction by FGF signaling before gastrulation. Nature 406, 74-78 (Pubitemid 30460213)
13. Wilson, S. I., Graziano, E., Harland, R., Jessell, T. M., and Edlund, T. (2000) An early requirement for FGF signaling in the acquisition of neural cell fate in the chick embryo. Curr. Biol. 10, 421-429 (Pubitemid 30247329)
14. Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S., and Smith, A. (2007) FGF stimulation of the Erk1/2 signaling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895-2902 (Pubitemid 47386902)
15. Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., and Smith, A. (2008) The ground state of embryonic stem cell self-renewal. Nature 453, 519-523 (Pubitemid 351733324)
16. Esko, J. D., and Selleck, S. B. (2002) Order out of chaos. Assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471 (Pubitemid 34800227)
17. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037 (Pubitemid 46676065)
18. Bülow, H. E., and Hobert, O. (2006) The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell Dev. Biol. 22, 375-407
19. Grobe, K., Ledin, J., Ringvall, M., Holmborn, K., Forsberg, E., Esko, J. D., and Kjellén, L. (2002) Heparan sulfate and development. Differential roles of the N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes. Biochim. Biophys. Acta 1573, 209-215 (Pubitemid 35335430)
20. Kreuger, J., Perez, L., Giraldez, A. J., and Cohen, S. M. (2004) Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev. Cell 7, 503-512 (Pubitemid 39341836)
21. Esko, J. D., and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173 (Pubitemid 32656238)
22. Kusche-Gullberg, M., Eriksson, I., Pikas, D. S., and Kjellén, L. (1998) Identification and expression in mouse of two heparan sulfate glucosaminyl N-deacetylase/N-sulfotransferase genes. J. Biol. Chem. 273, 11902-11907 (Pubitemid 28272098)
23. Aikawa, T., Segre, G. V., and Lee, K. (2001) Fibroblast growth factor inhibits chondrocytic growth through induction of p21 and subsequent inactivation of cyclin E-Cdk2. J. Biol. Chem. 276, 29347-29352
24. Ringvall, M., Ledin, J., Holmborn, K., van Kuppevelt, T., Ellin, F., Eriksson, I., Olofsson, A. M., Kjellen, L., and Forsberg, E. (2000) Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-deacetylase/N-sulfotransferase-1. J. Biol. Chem. 275, 25926-25930
25. Fan, G., Xiao, L., Cheng, L., Wang, X., Sun, B., and Hu, G. (2000) Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett. 467, 7-11 (Pubitemid 30069532)
26. Grobe, K., Inatani, M., Pallerla, S. R., Castagnola, J., Yamaguchi, Y., and Esko, J. D. (2005) Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development 132, 3777-3786 (Pubitemid 41301113)
27. Ringvall, M., and Kjellén, L. (2010) Mice deficient in heparan sulfate N-deacetylase/N-sulfotransferase 1. Prog. Mol. Biol. Transl Sci. 93, 35-58
28. Forsberg, E., Pejler, G., Ringvall, M., Lunderius, C., Tomasini-Johansson, B., Kusche-Gullberg, M., Eriksson, I., Ledin, J., Hellman, L., and Kjellén, L. (1999) Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400, 773-776 (Pubitemid 29399539)
29. Humphries, D. E., Wong, G. W., Friend, D. S., Gurish, M. F., Qiu, W. T., Huang, C., Sharpe, A. H., and Stevens, R. L. (1999) Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400, 769-772 (Pubitemid 29399538)
30. Pallerla, S. R., Lawrence, R., Lewejohann, L., Pan, Y., Fischer, T., Schlomann, U., Zhang, X., Esko, J. D., and Grobe, K. (2008) Altered heparan sulfate structure in mice with deleted NDST3 gene function. J. Biol. Chem. 283, 16885-16894
31. Holmborn, K., Ledin, J., Smeds, E., Eriksson, I., Kusche-Gullberg, M., and Kjellén, L. (2004) 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. 279, 42355-42358 (Pubitemid 39372115)
32. Jakobsson, L., Kreuger, J., Holmborn, K., Lundin, L., Eriksson, I., Kjellén, L., and Claesson-Welsh, L. (2006) Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell 10, 625-634
33. Lanner, F., Lee, K. L., Sohl, M., Holmborn, K., Yang, H., Wilbertz, J., Poellinger, L., Rossant, J., and Farnebo, F. (2010) Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells 28, 191-200
34. Rosen, E. D., Sarraf, P., Troy, A. E., Bradwin, G., Moore, K., Milstone, D. S., Spiegelman, B. M., and Mortensen, R. M. (1999) PPAR γ is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell 4, 611-617 (Pubitemid 29531140)
35. Phillips, B. W., Belmonte, N., Vernochet, C., Ailhaud, G., and Dani, C. (2001) Compactin enhances osteogenesis in murine embryonic stem cells. Biochem. Biophys. Res. Commun. 284, 478-484 (Pubitemid 32918002)
36. Lindahl, U., Cifonelli, J. A., Lindahl, B., and Roden, L. (1965) The Role of Serine in the Linkage of Heparin to Protein. J. Biol. Chem. 240, 2817-2820
37. Stavridis, M. P., Lunn, J. S., Collins, B. J., and Storey, K. G. (2007) A discrete period of FGF-induced Erk1/2 signaling is required for vertebrate neural specification. Development 134, 2889-2894 (Pubitemid 47386901)
38. Lin, X., Wei, G., Shi, Z., Dryer, L., Esko, J. D., Wells, D. E., and Matzuk, M. M. (2000) Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev. Biol. 224, 299-311 (Pubitemid 30661012)
39. Stickens, D., Zak, B. M., Rougier, N., Esko, J. D., and Werb, Z. (2005) Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132, 5055-5068 (Pubitemid 41764016)
40. Johnson, C. E., Crawford, B. E., Stavridis, M., Ten Dam, G., Wat, A. L., Rushton, G., Ward, C. M., Wilson, V., van Kuppevelt, T. H., Esko, J. D., Smith, A., Gallagher, J. T., and Merry, C. L. (2007) Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells. Stem Cells 25, 1913-1923 (Pubitemid 47258169)
41. Kraushaar, D. C., Yamaguchi, Y., and Wang, L. (2010) Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J. Biol. Chem. 285, 5907-5916
42. Pickford, C. E., Holley, R. J., Rushton, G., Stavridis, M. P., Ward, C. M., and Merry, C. L. (2011) Specific glycosaminoglycans modulate neural specification of mouse embryonic stem cells. Stem Cells 29, 629-640
43. Hoffmann, A., and Gross, G. (2001) BMP signaling pathways in cartilage and bone formation. Crit. Rev. Eukaryot. Gene Expr. 11, 23-45 (Pubitemid 32994858)
44. Taha, M. F., Valojerdi, M. R., and Mowla, S. J. (2006) Effect of bone morphogenetic protein-4 (BMP-4) on adipocyte differentiation from mouse embryonic stem cells. Anat. Histol. Embryol. 35, 271-278
45. Wilsie, L. C., Chanchani, S., Navaratna, D., and Orlando, R. A. (2005) Cell surface heparan sulfate proteoglycans contribute to intracellular lipid accumulation in adipocytes. Lipids Health Dis. 4, 2
46. Haub, O., and Goldfarb, M. (1991) Expression of the fibroblast growth factor-5 gene in the mouse embryo. Development 112, 397-406
47. Rojas, A., Schachterle, W., Xu, S. M., Martín, F., and Black, B. L. (2010) Direct transcriptional regulation of Gata4 during early endoderm specification is controlled by FoxA2 binding to an intronic enhancer. Dev. Biol. 346, 346-355
48. Levine, A. J., and Brivanlou, A. H. (2007) Proposal of a model of mammalian neural induction. Dev. Biol. 308, 247-256 (Pubitemid 47223107)
49. Irie, A., Habuchi, H., Kimata, K., and Sanai, Y. (2003) Heparan sulfate is required for bone morphogenetic protein-7 signaling. Biochem. Biophys. Res. Commun. 308, 858-865 (Pubitemid 36976539)
50. Jasuja, R., Allen, B. L., Pappano, W. N., Rapraeger, A. C., and Greenspan, D. S. (2004) Cell surface heparan sulfate proteoglycans potentiate chordin antagonism of bone morphogenetic protein signaling and are necessary for cellular uptake of chordin. J. Biol. Chem. 279, 51289-51297 (Pubitemid 40017874)
51. Bornemann, D. J., Park, S., Phin, S., and Warrior, R. (2008) A translational block to HSPG synthesis permits BMP signaling in the early Drosophila embryo. Development 135, 1039-1047 (Pubitemid 351578132)
52. Ma, Y. G., Rosfjord, E., Huebert, C., Wilder, P., Tiesman, J., Kelly, D., and Rizzino, A. (1992) Transcriptional regulation of the murine k-FGF gene in embryonic cell lines. Dev. Biol. 154, 45-54
53. Stavridis, M. P., Collins, B. J., and Storey, K. G. (2010) Retinoic acid orchestrates fibroblast growth factor signalling to drive embryonic stem cell differentiation. Development 137, 881-890
54. Gao, G., and Goldfarb, M. (1995) Heparin can activate a receptor tyrosine kinase. EMBO J. 14, 2183-2190
55. Berry, D., Lynn, D. M., Sasisekharan, R., and Langer, R. (2004) Poly(β-amino ester)s promote cellular uptake of heparin and cancer cell death. Chem. Biol. 11, 487-498 (Pubitemid 38503583)
56. Bae, K. H., Mok, H., and Park, T. G. (2008) Synthesis, characterization, and intracellular delivery of reducible heparin nanogels for apoptotic cell death. Biomaterials 29, 3376-3383
57. Jordan, P. M., Cain, L. D., and Wu, P. (2008) Astrocytes enhance long-term survival of cholinergic neurons differentiated from human fetal neural stem cells. J. Neurosci. Res. 86, 35-47
58. Pettersson, I., Kusche, M., Unger, E., Wlad, H., Nylund, L., Lindahl, U., and Kjellén, L. (1991) Biosynthesis of heparin. Purification of a 110-kDa mouse mastocytoma protein required for both glucosaminyl N-deacetylation and N-sulfation. J. Biol. Chem. 266, 8044-8049 (Pubitemid 21906472)