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Sulfated glycosaminoglycans: their distinct roles in stem cell biology

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Abstract

Sulfated glycosaminoglycan (GAG) chains are a class of long linear polysaccharides that are covalently attached to multiple core proteins to form proteoglycans (PGs). PGs are major pericellular and extracellular matrix components that surround virtually all mammalian cell surfaces, and create conducive microenvironments for a number of essential cellular events, such as cell adhesion, cell proliferation, differentiation, and cell fate decisions. The multifunctional properties of PGs are mostly mediated by their respective GAG moieties, including chondroitin sulfate (CS), heparan sulfate (HS), and keratan sulfate (KS) chains. Structural divergence of GAG chains is enzymatically generated and strictly regulated by the corresponding biosynthetic machineries, and is the major driving force for PG functions. Recent studies have revealed indispensable roles of GAG chains in stem cell biology and technology. In this review, we summarize the current understanding of GAG chain-mediated stem cell niches, focusing primarily on structural characteristics of GAG chains and their distinct regulatory functions in stem cell maintenance and fate decisions.

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Abbreviations

ß3GnT7:

β1,3–GlcNAc transferase-7

β4GalT4:

β1,4–galactosyltransferase-4

AP:

alkaline phosphatase

BMP:

bone morphogenetic protein

C4ST:

chondroitin 4-O-sulfotransferase

C6ST:

chondroitin 6-O-sulfotransferase

ChABC:

chondroitinase ABC

ChGn:

chondroitin GalNAc transferase

Chn:

chondroitin

ChPF:

chondroitin polymerizing factor

ChSy:

chondroitin synthase

CS:

chondroitin sulfate

EB:

embryoid body

ESC:

embryonic stem cell

EXT:

exostosin

EXTL:

EXT-like

FAM:

family with sequence similarity

FGF:

fibroblast growth factor

Fuc:

fucose

GAG:

glycosaminoglycan

Gal:

galactose

GalNAc:

N-acetylgalactosamine

GalNAc4S-6ST:

GalNAc 4-sulfate 6-O-sulfotransferase

GalT-I:

β1,4–galactosyltransferase-I

GalT-II:

β1,3–galactosyltransferase-II

GlcA:

glucuronic acid

GlcAT-I:

β1,3–glucuronyltransferase-I

GLCE:

GlcA C5-epimerase

GlcNAc:

N-acetylglucosamine

GlcNAc6ST:

GlcNAc 6-O-sulfotransferase

HS:

heparan sulfate

HS2ST:

HS-specific uronyl 2-O-sulfotransferase

HS3ST:

glucosaminyl 3-O-sulfotransferase

HS6ST:

glucosaminyl 6-O-sulfotransferase

IdoA:

iduronic acid

iPS:

induced pluripotent stem

KS:

keratan sulfate

KSGal6ST:

KS Gal 6-O-sulfotransferase

LIF:

leukemia inhibitory factor

Man:

mannose

NDST:

GlcNAc N-deacetylase/N-sulfotransferase

NeuAc:

N-acetylneuraminic acid

PDGF:

platelet-derived growth factor

PE:

primitive endoderm

PG:

proteoglycan

PXYLP1:

2-O-phosphoxylose phosphatase

RNAi:

RNA interference

Ser:

serine

shRNA:

short hairpin RNA

UST:

CS-specific uronyl 2-O-sulfotransferase

VEGF:

vascular endothelial growth factor

Xyl:

xylose

XYLK:

xylose 2-O-kinase

XylT:

xylosyltransferase

References

  1. Evans M.J., Kaufman M.H.: Establishment in culture of pluripotential cells from mouse embryos. Nature. 292(5819), 154–156 (1981)

    Article  CAS  PubMed  Google Scholar 

  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(12), 7634–7638 (1981)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M.: Embryonic stem cell lines derived from human blastocysts. Science. 282(5391), 1145–1147 (1998)Erratum in: Science. 282(5395), 1827 (1998)

    Article  CAS  PubMed  Google Scholar 

  4. Keller G.: Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 19(10), 1129–1155 (2005)

    Article  CAS  PubMed  Google Scholar 

  5. Takahashi K., Yamanaka S.: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 126(4), 663–676 (2006)

    Article  CAS  PubMed  Google Scholar 

  6. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S.: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 131(5), 861–872 (2007)

    Article  CAS  PubMed  Google Scholar 

  7. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., Slukvin I.I., Thomson J.A.: Induced pluripotent stem cell lines derived from human somatic cells. Science. 318(5858), 1917–1920 (2007)

    Article  CAS  PubMed  Google Scholar 

  8. Nadanaka S., Kitagawa H.: Heparan sulphate biosynthesis and disease. J. Biochem. 144(1), 7–14 (2008)

    Article  CAS  PubMed  Google Scholar 

  9. Mikami T., Kitagawa H.: Biosynthesis and function of chondroitin sulfate. Biochim. Biophys. Acta. 1830(10), 4719–4733 (2013)

    Article  CAS  PubMed  Google Scholar 

  10. Kitagawa H.: Using sugar remodeling to study chondroitin sulfate function. Biol. Pharm. Bull. 37(11), 1705–1712 (2014)

    Article  CAS  PubMed  Google Scholar 

  11. Sugahara K., Kitagawa H.: Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10(5), 518–527 (2000)

    Article  CAS  PubMed  Google Scholar 

  12. Sugahara K., Kitagawa H.: Heparin and heparan sulfate biosynthesis. IUBMB Life. 54(4), 163–175 (2002)

    Article  CAS  PubMed  Google Scholar 

  13. Silbert J.E., Sugumaran G.: Biosynthesis of chondroitin/dermatan sulfate. IUBMB Life. 54(4), 177–186 (2002)

    Article  CAS  PubMed  Google Scholar 

  14. Kitagawa H., Uyama T., Sugahara K.: Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276(42), 38721–38726 (2001)

    Article  CAS  PubMed  Google Scholar 

  15. Gotoh M., Yada T., Sato T., Akashima T., Iwasaki H., Mochizuki H., Inaba N., Togayachi A., Kudo T., Watanabe H., Kimata K., Narimatsu H.: Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine. J. Biol. Chem. 277(41), 38179–38188 (2002)

    Article  CAS  PubMed  Google Scholar 

  16. 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(26), 23666–23671 (2003)

    Article  CAS  PubMed  Google Scholar 

  17. Yada T., Gotoh M., Sato T., Shionyu M., Go M., Kaseyama H., Iwasaki H., Kikuchi N., Kwon Y.D., Togayachi A., Kudo T., Watanabe H., Narimatsu H., Kimata K.: Chondroitin sulfate synthase-2. Molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. J. Biol. Chem. 278(32), 30235–30247 (2003)

    Article  CAS  PubMed  Google Scholar 

  18. Yada T., Sato T., Kaseyama H., Gotoh M., Iwasaki H., Kikuchi N., Kwon Y.D., Togayachi A., Kudo T., Watanabe H., Narimatsu H., Kimata K.: Chondroitin sulfate synthase-3. Molecular cloning and characterization. J. Biol. Chem. 278(41), 39711–39725 (2003)

    Article  CAS  PubMed  Google Scholar 

  19. 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(3), 545–552 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Izumikawa T., Koike T., Shiozawa S., Sugahara K., Tamura J., Kitagawa H.: 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(17), 11396–11406 (2008)

    Article  CAS  PubMed  Google Scholar 

  21. 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(11), 8841–8846 (2002)

    Article  CAS  PubMed  Google Scholar 

  22. Gotoh M., Sato T., Akashima T., Iwasaki H., Kameyama A., Mochizuki H., Yada T., Inaba N., Zhang Y., Kikuchi N., Kwon Y.D., Togayachi A., Kudo T., Nishihara S., Watanabe H., Kimata K., Narimatsu H.: Enzymatic synthesis of chondroitin with a novel chondroitin sulfate N-acetylgalactosaminyltransferase that transfers N-acetylgalactosamine to glucuronic acid in initiation and elongation of chondroitin sulfate synthesis. J. Biol. Chem. 277(41), 38189–38196 (2002)

    Article  CAS  PubMed  Google Scholar 

  23. Sato T., Gotoh M., Kiyohara K., Akashima T., Iwasaki H., Kameyama A., Mochizuki H., Yada T., Inaba N., Togayachi A., Kudo T., Asada M., Watanabe H., Imamura T., Kimata K., Narimatsu H.: Differential roles of two N-acetylgalactosaminyltransferases, CSGalNAcT-1, and a novel enzyme, CSGalNAcT-2. Initiation and elongation in synthesis of chondroitin sulfate. J. Biol. Chem. 278(5), 3063–3071 (2003)

    Article  CAS  PubMed  Google Scholar 

  24. Uyama T., Kitagawa H., Tanaka J., Tamura J., Ogawa T., Sugahara K.: Molecular cloning and expression of a second chondroitin N-acetylgalactosaminyltransferase involved in the initiation and elongation of chondroitin/dermatan sulfate. J. Biol. Chem. 278(5), 3072–3078 (2003)

    Article  CAS  PubMed  Google Scholar 

  25. Izumikawa T., Okuura Y., Koike T., Sakoda N., Kitagawa H.: Chondroitin 4-O-sulfotransferase-1 regulates the chain length of chondroitin sulfate in co-operation with chondroitin N-acetylgalactosaminyltransferase-2. Biochem. J. 434(2), 321–331 (2011)

    Article  CAS  PubMed  Google Scholar 

  26. Izumikawa T., Koike T., Kitagawa H.: Chondroitin 4-O-sulfotransferase-2 regulates the number of chondroitin sulfate chains initiated by chondroitin N-acetylgalactosaminyltransferase-1. Biochem. J. 441(2), 697–705 (2012)

    Article  CAS  PubMed  Google Scholar 

  27. McCormick C., Duncan G., Goutsos K.T., Tufaro F.: The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc. Natl. Acad. Sci. U. S. A. 97(2), 668–673 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kim B.T., Kitagawa H., Tanaka J., Tamura J., Sugahara K.: In vitro heparan sulfate polymerization: crucial roles of core protein moieties of primer substrates in addition to the EXT1-EXT2 interaction. J. Biol. Chem. 278(43), 41618–41623 (2003)

    Article  CAS  PubMed  Google Scholar 

  29. Kusche-Gullberg M., Kjellén L.: Sulfotransferases in glycosaminoglycan biosynthesis. Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13(5), 605–611 (2003)

    Article  CAS  PubMed  Google Scholar 

  30. Gulberti S., Lattard V., Fondeur M., Jacquinet J.C., Mulliert G., Netter P., Magdalou J., Ouzzine M., Fournel-Gigleux S.: Phosphorylation and sulfation of oligosaccharide substrates critically influence the activity of human beta1,4-galactosyltransferase 7 (GalT-I) and beta1,3-glucuronosyltransferase I (GlcAT-I) involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem. 280(2), 1417–1425 (2005)

    Article  CAS  PubMed  Google Scholar 

  31. Tone Y., Pedersen L.C., Yamamoto T., Izumikawa T., Kitagawa H., Nishihara J., Tamura J., Negishi M., Sugahara K.: 2-o-phosphorylation of xylose and 6-o-sulfation of galactose in the protein linkage region of glycosaminoglycans influence the glucuronyltransferase-I activity involved in the linkage region synthesis. J. Biol. Chem. 283(24), 16801–16807 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wen J., Xiao J., Rahdar M., Choudhury B.P., Cui J., Taylor G.S., Esko J.D., Dixon J.E.: Xylose phosphorylation functions as a molecular switch to regulate proteoglycan biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 111(44), 15723–15728 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Koike T., Izumikawa T., Tamura J., Kitagawa H.: FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region. Biochem. J. 421(2), 157–162 (2009)

    Article  CAS  PubMed  Google Scholar 

  34. Koike T., Izumikawa T., Sato B., Kitagawa H.: Identification of phosphatase that dephosphorylates xylose in the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem. 289(10), 6695–6708 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Izumikawa T., Sato B., Mikami T., Tamura J., Igarashi M., Kitagawa H.: GlcUAβ1-3Galβ1-3Galβ1-4Xyl(2-O-phosphate) is the preferred substrate for chondroitin N-acetylgalactosaminyltransferase-1. J. Biol. Chem. 290(9), 5438–5448 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Nadanaka S., Zhou S., Kagiyama S., Shoji N., Sugahara K., Sugihara K., Asano M., Kitagawa H.: EXTL2, a member of the EXT family of tumor suppressors, controls glycosaminoglycan biosynthesis in a xylose kinase-dependent manner. J. Biol. Chem. 288(13), 9321–9333 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Funderburgh J.L.: Keratan sulfate: structure, biosynthesis, and function. Glycobiology. 10(10), 951–958 (2000)

    Article  CAS  PubMed  Google Scholar 

  38. Funderburgh J.L.: Keratan sulfate biosynthesis. IUBMB Life. 54(4), 187–194 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kawabe K., Tateyama D., Toyoda H., Kawasaki N., Hashii N., Nakao H., Matsumoto S., Nonaka M., Matsumura H., Hirose Y., Morita A., Katayama M., Sakuma M., Kawasaki N., Furue M.K., Kawasaki T.: A novel antibody for human induced pluripotent stem cells and embryonic stem cells recognizes a type of keratan sulfate lacking oversulfated structures. Glycobiology. 23(3), 322–336 (2013)

    Article  CAS  PubMed  Google Scholar 

  40. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., Gifford D.K., Melton D.A., Jaenisch R., Young R.A.: Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 122(6), 947–956 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., Wagner E.F., Metcalf D., Nicola N.A., Gough N.M.: Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature. 336(6200), 684–687 (1988)

    Article  CAS  PubMed  Google Scholar 

  42. Smith A.G., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M., Rogers D.: Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature. 336(6200), 688–690 (1988)

    Article  CAS  PubMed  Google Scholar 

  43. Okita K., Yamanaka S.: Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr. Stem Cell Res. Ther. 1(1), 103–111 (2006)

    Article  CAS  PubMed  Google Scholar 

  44. Xu R.H., Peck R.M., Li D.S., Feng X., Ludwig T., Thomson J.A.: Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat. Methods. 2(3), 185–190 (2005)

    Article  CAS  PubMed  Google Scholar 

  45. Levenstein M.E., Ludwig T.E., Xu R.H., Llanas R.A., VanDenHeuvel-Kramer K., Manning D., Thomson J.A.: Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells. 24(3), 568–574 (2006)

    Article  CAS  PubMed  Google Scholar 

  46. Lin X., Wei G., Shi Z., Dryer L., Esko J.D., Wells D.E., Matzuk M.M.: Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev. Biol. 224(2), 299–311 (2000)

    Article  CAS  PubMed  Google Scholar 

  47. Nairn A.V., Kinoshita-Toyoda A., Toyoda H., Xie J., Harris K., Dalton S., Kulik M., Pierce J.M., Toida T., Moremen K.W., Linhardt R.J.: Glycomics of proteoglycan biosynthesis in murine embryonic stem cell differentiation. J. Proteome Res. 6(11), 4374–4387 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Izumikawa T., Sato B., Kitagawa H.: Chondroitin sulfate is indispensable for pluripotency and differentiation of mouse embryonic stem cells. Sci. Rep. 4, 3701 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  49. 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., Merry C.L.: 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(8), 1913–1923 (2007)Erratum in: Stem Cells. 25(9), 2389 (2007)

    Article  CAS  PubMed  Google Scholar 

  50. Gasimli L., Hickey A.M., Yang B., Li G., dela Rosa M., Nairn A.V., Kulik M.J., Dordick J.S., Moremen K.W., Dalton S., Linhardt R.J.: Changes in glycosaminoglycan structure on differentiation of human embryonic stem cells towards mesoderm and endoderm lineages. Biochim. Biophys. Acta. 1840(6), 1993–2003 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kraushaar D.C., Yamaguchi Y., Wang L.: Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J. Biol. Chem. 285(8), 5907–5916 (2010) Erratum in: J. Biol. Chem. 290(38), 23023 (2015)

    Article  Google Scholar 

  52. Holley R.J., Pickford C.E., Rushton G., Lacaud G., Gallagher J.T., Kouskoff V., Merry C.L.: Influencing hematopoietic differentiation of mouse embryonic stem cells using soluble heparin and heparan sulfate saccharides. J. Biol. Chem. 286(8), 6241–6252 (2011)

    Article  CAS  PubMed  Google Scholar 

  53. Holmborn K., Ledin J., Smeds E., Eriksson I., Kusche-Gullberg M., Kjellén L.: 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(41), 42355–42358 (2004)

    Article  CAS  PubMed  Google Scholar 

  54. Izumikawa T., Kanagawa N., Watamoto Y., Okada M., Saeki M., Sakano M., Sugahara K., Sugihara K., Asano M., Kitagawa H.: Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice. J. Biol. Chem. 285(16), 12190–12196 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kitagawa H., Tone Y., Tamura J., Neumann K.W., Ogawa T., Oka S., Kawasaki T., Sugahara K.: Molecular cloning and expression of glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem. 273(12), 6615–6618 (1998)

    Article  CAS  PubMed  Google Scholar 

  56. Wei G., Bai X., Sarkar A.K., Esko J.D.: Formation of HNK-1 determinants and the glycosaminoglycan tetrasaccharide linkage region by UDP-GlcUA:galactose beta1, 3-glucuronosyltransferases. J. Biol. Chem. 274(12), 7857–7864 (1999)

    Article  CAS  PubMed  Google Scholar 

  57. Lin X.: Functions of heparan sulfate proteoglycans in cell signaling during development. Development. 131(24), 6009–6021 (2004)

    Article  CAS  PubMed  Google Scholar 

  58. Kreuger J., Spillmann D., Li J.P., Lindahl U.: Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell Biol. 174(3), 323–327 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Bishop J.R., Schuksz M., Esko J.D.: Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature. 446(7139), 1030–1037 (2007)

    Article  CAS  PubMed  Google Scholar 

  60. Ying Q.L., Nichols J., Chambers I., Smith A.: BMP induction of id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell. 115(3), 281–292 (2003)

    Article  CAS  PubMed  Google Scholar 

  61. Hao J., Li T.G., Qi X., Zhao D.F., Zhao G.Q.: WNT/beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Dev. Biol. 290(1), 81–91 (2006)

    Article  CAS  PubMed  Google Scholar 

  62. Cole M.F., Johnstone S.E., Newman J.J., Kagey M.H., Young R.A.: Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev. 22(6), 746–755 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Pickford C.E., Holley R.J., Rushton G., Stavridis M.P., Ward C.M., Merry C.L.: Specific glycosaminoglycans modulate neural specification of mouse embryonic stem cells. Stem Cells. 29(4), 629–640 (2010)

    Article  Google Scholar 

  64. Lanner F., Lee K.L., Sohl M., Holmborn K., Yang H., Wilbertz J., Poellinger L., Rossant J., Farnebo F.: Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells. 28(2), 191–200 (2010)

    CAS  PubMed  Google Scholar 

  65. Sasaki N., Okishio K., Ui-Tei K., Saigo K., Kinoshita-Toyoda A., Toyoda H., Nishimura T., Suda Y., Hayasaka M., Hanaoka K., Hitoshi S., Ikenaka K., Nishihara S.: Heparan sulfate regulates self-renewal and pluripotency of embryonic stem cells. J. Biol. Chem. 2283(6), 3594–3606 (2008)

    Article  Google Scholar 

  66. 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(2), 267–279 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mikami, T., Kitagawa, H. (2014). Glycosaminoglycans: their modes of action for a possible new avenue for therapeutic intervention. In: Taniguchi, N., Endo, T., Hart, G.W., Seeberger, P.H., Wong, C.H., (eds) Glycoscience: Biology and Medicine, pp. 511–517. Springer, Tokyo

  68. Mikami T., Yasunaga D., Kitagawa H.: Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J. Biol. Chem. 284(7), 4494–4499 (2009)

    Article  CAS  PubMed  Google Scholar 

  69. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., He Z., Silver J., Flanagan J.G.: PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science. 326(5952), 592–596 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Coles C.H., Shen Y., Tenney A.P., Siebold C., Sutton G.C., Lu W., Gallagher J.T., Jones E.Y., Flanagan J.G., Aricescu A.R.: Proteoglycan-specific molecular switch for RPTPσ clustering and neuronal extension. Science. 332(6028), 484–488 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Fisher D., Xing B., Dill J., Li H., Hoang H.H., Zhao Z., Yang X.L., Bachoo R., Cannon S., Longo F.M., Sheng M., Silver J., Li S.: Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J. Neurosci. 31(40), 14051–14066 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Dickendesher T.L., Baldwin K.T., Mironova Y.A., Koriyama Y., Raiker S.J., Askew K.L., Wood A., Geoffroy C.G., Zheng B., Liepmann C.D., Katagiri Y., Benowitz L.I., Geller H.M., Giger R.J.: NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 15(5), 703–712 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Koike T., Izumikawa T., Tamura J., Kitagawa H.: Chondroitin sulfate-E fine-tunes osteoblast differentiation via ERK1/2, Smad3 and Smad1/5/8 signaling by binding to N-cadherin and cadherin-11. Biochem. Biophys. Res. Commun. 420(3), 523–529 (2012)

    Article  CAS  PubMed  Google Scholar 

  74. Koike T., Mikami T., Shida M., Habuchi O., Kitagawa H.: Chondroitin sulfate-E mediates estrogen-induced osteoanabolism. Sci. Rep. 5, 8994 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Soncin F., Mohamet L., Eckardt D., Ritson S., Eastham A.M., Bobola N., Russell A., Davies S., Kemler R., Merry C.L., Ward C.M.: Abrogation of E-cadherin-mediated cell-cell contact in mouse embryonic stem cells results in reversible LIF-independent self-renewal. Stem Cells. 27(9), 2069–2080 (2009)

    Article  CAS  PubMed  Google Scholar 

  76. Chen T., Yuan D., Wei B., Jiang J., Kang J., Ling K., Gu Y., Li J., Xiao L., Pei G.: E-cadherin-mediated cell-cell contact is critical for induced pluripotent stem cell generation. Stem Cells. 28(8), 1315–1325 (2010)

    Article  CAS  PubMed  Google Scholar 

  77. Spencer H.L., Eastham A.M., Merry C.L., Southgate T.D., Perez-Campo F., Soncin F., Ritson S., Kemler R., Stern P.L., Ward C.M.: E-cadherin inhibits cell surface localization of the pro-migratory 5 T4 oncofetal antigen in mouse embryonic stem cells. Mol. Biol. Cell. 18(8), 2838–2851 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Li R., Liang J., Ni S., Zhou T., Qing X., Li H., He W., Chen J., Li F., Zhuang Q., Qin B., Xu J., Li W., Yang J., Gan Y., Qin D., Feng S., Song H., Yang D., Zhang B., Zeng L., Lai L., Esteban M.A., Pei D.: A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell. 7(1), 51–63 (2010)

    Article  CAS  PubMed  Google Scholar 

  79. Redmer T., Diecke S., Grigoryan T., Quiroga-Negreira A., Birchmeier W., Besser D.: E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep. 12(7), 720–726 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kunath T., Saba-El-Leil M.K., Almousailleakh M., Wray J., Meloche S., Smith A.: FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development. 134(16), 2895–2902 (2007)

    Article  CAS  PubMed  Google Scholar 

  81. Kraushaar D.C., Rai S., Condac E., Nairn A., Zhang S., Yamaguchi Y., Moremen K., Dalton S., Wang L.: Heparan sulfate facilitates FGF and BMP signaling to drive mesoderm differentiation of mouse embryonic stem cells. J. Biol. Chem. 287(27), 22691–22700 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Tanaka S.S., Kojima Y., Yamaguchi Y.L., Nishinakamura R., Tam P.P.: Impact of WNT signaling on tissue lineage differentiation in the early mouse embryo. Develop. Growth Differ. 53(7), 843–856 (2011)

    Article  CAS  Google Scholar 

  83. Jakobsson L., Kreuger J., Holmborn K., Lundin L., Eriksson I., Kjellén L., Claesson-Welsh L.: Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell. 10(5), 625–634 (2006)

    Article  CAS  PubMed  Google Scholar 

  84. Le Jan S., Hayashi M., Kasza Z., Eriksson I., Bishop J.R., Weibrecht I., Heldin J., Holmborn K., Jakobsson L., Söderberg O., Spillmann D., Esko J.D., Claesson-Welsh L., Kjellén L., Kreuger J.: Functional overlap between chondroitin and heparan sulfate proteoglycans during VEGF-induced sprouting angiogenesis. Arterioscler. Thromb. Vasc. Biol. 32(5), 1255–1263 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Forsberg M., Holmborn K., Kundu S., Dagälv A., Kjellén L., Forsberg-Nilsson K.: Undersulfation of heparan sulfate restricts differentiation potential of mouse embryonic stem cells. J. Biol. Chem. 287(14), 10853–10862 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported in part by Grants-in-aid for Scientific Research (C) #16K07306 (to T. M.), and for Scientific Research (B) #16H05088 (to H. K.), and the Supported Program for the Strategic Research Foundation at Private Universities, 2012-2016 (to H. K.) from Ministry of Education, Culture, Sports, Science & Technology, Japan.

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  1. Department of Biochemistry, Kobe Pharmaceutical University, Higashinada-ku, Kobe, 658-8558, Japan

    Tadahisa Mikami & Hiroshi Kitagawa

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  1. Tadahisa Mikami
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  2. Hiroshi Kitagawa
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Correspondence to Hiroshi Kitagawa.

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Mikami, T., Kitagawa, H. Sulfated glycosaminoglycans: their distinct roles in stem cell biology. Glycoconj J 34, 725–735 (2017). https://doi.org/10.1007/s10719-016-9732-9

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  • DOI: https://doi.org/10.1007/s10719-016-9732-9

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