Chondroitin sulfate is indispensable for pluripotency and differentiation of mouse embryonic stem cells

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Izumikawa, Tomomi ^a   Sato, Ban ^a   Kitagawa, Hiroshi ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CHONDROITIN SULFATE; GALACTOSYLGALACTOYLXYLOSYLPROTEIN 3-BETA-GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE; HEPARAN SULFATE; POLYSACCHARIDE;

ANIMAL; CELL DIFFERENTIATION; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; CADHERINS; CELL DIFFERENTIATION; CHONDROITIN SULFATES; EMBRYONIC STEM CELLS; EXTRACELLULAR MATRIX; GLUCURONOSYLTRANSFERASE; HEPARITIN SULFATE; MICE; POLYSACCHARIDES;

EID: 84892758322     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03701     Document Type: Article

References (47)

1. Evans, M. J. & Kaufman, M. H. Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 (1981). (Pubitemid 11050741)
2. Martin, G. R. 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 (1981). (Pubitemid 12186197)
3. Keller, G. Embryonic stem cell differentiation. Emergence of a new era in biology and medicine. Genes Dev. 19, 1129-1155 (2005). (Pubitemid 40696181)
4. Bissell, M. J., Kenny, P. A. & Radisky, D. C. Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb. Symp. Quant. Biol. 70, 343-356 (2005). (Pubitemid 44124889)
5. Daley, W. P., Peters, S. B. & Larsen, M. Extracellular matrix dynamics in development and regenerative medicine. J. Cell Sci. 121, 255-264 (2008). (Pubitemid 351356696)
6. Chou, Y. F. et al. The growth factor environment defines distinct pluripotent ground states in novel blastocyst-derived stem cells. Cell 135, 449-461 (2008).
7. Soncin, F. et al. Abrogation of E-cadherin-mediated cell-cell contact in mouse embryonic stem cells results in reversible LIF-independent self-renewal. Stem Cells 27, 2069-2080 (2009).
8. Chen, T. et al. E-cadherin-mediated cell-cell contact is critical for induced pluripotent stem cell generation. Stem Cells 28, 1315-1325 (2010).
9. Li, R. et al. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7, 51-63 (2010).
10. Redmer, T. et al. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Reports 12, 720-726 (2011).
11. Kitagawa, H. et al. Molecular Cloning and Expression of Glucuronyltransferase I Involved in the Biosynthesis of the Glycosaminoglycan- Protein Linkage Region of Proteoglycans. J. Biol. Chem. 273, 6615-16618 (1998).
12. Tone, Y., Kitagawa, H., Oka, S., Kawasaki, T. & Sugahara, K. Characterization of recombinant human glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. FEBS Lett. 459, 415-420 (1999). (Pubitemid 29467379)
13. McCormick, C. et al. The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat. Genet. 19, 158-161 (1998). (Pubitemid 28248797)
14. Lind, T., Tufaro, F., McCormick, C., Lindahl, U. & Lidholt, K. The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate. J. Biol. Chem. 273, 26265-26268 (1998). (Pubitemid 28471622)
15. Kitagawa, H., Uyama, T. & Sugahara, K. Molecular Cloning and Expression of a Human Chondroitin Synthase. J. Biol. Chem. 276, 38721-38726 (2001).
16. Izumikawa, T., Uyama, T., Okuura, Y., Sugahara, K. & Kitagawa, H. Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor. Biochem. J. 403, 545-552 (2007). (Pubitemid 46706983)
17. Izumikawa, T. et al. Identification of Chondroitin Sulfate Glucuronyltransferase as Chondroitin Synthase-3 Involved in Chondroitin Polymerization: CHONDROITIN POLYMERIZATION IS ACHIEVED BY MULTIPLE ENZYME COMPLEXES CONSISTING OF CHONDROITIN SYNTHASE FAMILY MEMBERS. J. Biol. Chem. 283, 11396-11406 (2008).
18. Kitagawa, H., Izumikawa, T., Uyama, T. & Sugahara, K. Molecular Cloning of a Chondroitin Polymerizing Factor That Cooperates with Chondroitin Synthase for Chondroitin Polymerization. J. Biol. Chem. 278, 23666-23671 (2003). (Pubitemid 36833253)
19. Sugahara, K. & Kitagawa, H. Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10, 518-527 (2000).
20. Kitagawa, H., Tsutsumi, K., Tone, Y. & Sugahara, K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 272, 31377-31381 (1997). (Pubitemid 28013273)
21. Thiele, H. et al. Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc. Natl. Acad. Sci. U. S. A. 101, 10155-10160 (2004). (Pubitemid 38891211)
22. Klüppel, M., Wight, T. N., Chan, C., Hinek, A. & Wrana, J. L. Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132, 3989-4003 (2005). (Pubitemid 41410261)
23. Miyata, S., Komatsu, Y., Yoshimura, Y., Taya, C.&Kitagawa, H. Persistent cortical plasticity by upregulation of chondroitin 6-sulfation. Nat. Neurosci. 15, 414-422 (2012).
24. Esko, J. D.&Lindahl, U. Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173 (2001). (Pubitemid 32656238)
25. Izumikawa, T. et al. Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficientmice. J. Biol. Chem. 285, 12190-1219 (2010).
26. Lin, X. et al. Disruption of gastrulation and heparan sulfate biosynthesis in EXT1- deficient mice. Dev. Biol. 224, 299-311 (2000). (Pubitemid 30661012)
27. Stickens, D., Zak, B. M., Rougier, N., Esko, J. D. &Werb, Z. Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development 132, 5055-5068 (2005). (Pubitemid 41764016)
28. Forsberg, M. et al. Undersulfation of heparan sulfate restricts differentiation potential of mouse embryonic stem cells. J. Biol. Chem. 287, 10853-10862 (2012).
29. Lanner, F. & Rossant, J. The role of FGF/Erk signaling in pluripotent cells. Development 137, 3351-3360 (2010).
30. Pickford, C. E. et al. Specific glycosaminoglycans modulate neural specification of mouse embryonic stem cells. Stem Cells 29, 629-640 (2011).
31. Kraushaar, D. C., Yamaguchi, Y. & Wang, L. Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J Biol. Chem. 285, 5907-5916 (2010).
32. Uyama, T., Kitagawa, H., Tamura, J. & Sugahara, K. Molecular Cloning and Expression of Human Chondroitin N-Acetylgalactosaminyltransferase: THE KEY ENZYME FOR CHAIN INITIATION AND ELONGATION OF CHONDROITIN/DERMATAN SULFATE ON THE PROTEIN LINKAGE REGION TETRASACCHARIDE SHARED BY HEPARIN/HEPARAN SULFATE. J. Biol. Chem. 277, 8841-8846 (2002). (Pubitemid 34952951)
33. Uyama, T. et al. Molecular Cloning and Expression of a Second Chondroitin NAcetylgalactosaminyltransferase Involved in the Initiation and Elongation of Chondroitin/Dermatan Sulfate. J. Biol. Chem. 278, 3072-3078 (2003). (Pubitemid 36801216)
34. Mountford, P., Nichols, J., Zevnik, B., O'Brien, C. & Smith, A. Maintenance of pluripotential embryonic stem cells by stem cell selection. Reprod. Fertil. Dev. 10, 527-533 (1998).
35. Koike, T., Izumikawa, T., Tamura, J. & Kitagawa, H. Chondroitin sulfate-E finetunes osteoblast differentiation via ERK1/2, Smad3 and Smad1/5/8 signaling by binding to N-cadherin and cadherin-11. Biochem. Biophys. Res. Commun. 420, 523-529 (2012).
36. Xu, Y. et al. Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc. Natl. Acad. Sci. U. S. A. 107, 8129-8134 (2010).
37. Harb, N., Archer, T. K. & Sato, N. The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells. PLoS One. 3, e3001 (2008).
38. Fukata, M. & Kaibuchi, K. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat. Rev. Mol. Cell Biol. 2, 887-897 (2001). (Pubitemid 33674088)
39. Chambers, I. et al. Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234 (2007).
40. Niwa, H., Ogawa, K., Shimosato, D. & Adachi, K. A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460, 118-122 (2009).
41. Kunath, T. et al. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells self-renewal to lineage commitment. Development 134, 2895-2902 (2007). (Pubitemid 47386902)
42. Nichols, J., Silva, J., Roode, M. & from Smith, A. Suppresssion of Erk signaling promotes ground state pluripotency in the mouse embryos. Cell Stem Cell 8, 318-325 (2009).
43. Kang, M., Piliszek, A., Artus, J. & Hadjantonakis, A. K. FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 140, 267-279 (2013).
44. Spencer, H. L. et al. E-cadherin inhibits cell surface localization of the promigratory 5T4 oncofetal antigen in mouse embryonic stem cells. Mol. Biol. Cell 18, 2838-2851 (2007). (Pubitemid 47235292)
45. Zhang, P., Wu, X., Hu, C., Wang, P. & Li, X. Rho kinase inhibitor Y-27632 and Accutase dramatically increase mouse embryonic stem cell derivation. In Vitro Cell Dev. Biol. Anim. 8, 30-36 (2012).
46. Richard, L. C. et al. Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules. Biomaterials 13, 2507-2515 (2009).
47. Mikami, T., Yasunaga, D. & Kitagawa, H. Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J. Biol. Chem. 284, 4494-4499 (2009).