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Heparan sulfate proteoglycans as key regulators of the mesenchymal niche of hematopoietic stem cells

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Abstract

The complex microenvironment that surrounds hematopoietic stem cells (HSCs) in the bone marrow niche involves different coordinated signaling pathways. The stem cells establish permanent interactions with distinct cell types such as mesenchymal stromal cells, osteoblasts, osteoclasts or endothelial cells and with secreted regulators such as growth factors, cytokines, chemokines and their receptors. These interactions are mediated through adhesion to extracellular matrix compounds also. All these signaling pathways are important for stem cell fates such as self-renewal, proliferation or differentiation, homing and mobilization, as well as for remodeling of the niche. Among these complex molecular cues, this review focuses on heparan sulfate (HS) structures and functions and on the role of enzymes involved in their biosynthesis and turnover. HS associated to core protein, constitute the superfamily of heparan sulfate proteoglycans (HSPGs) present on the cell surface and in the extracellular matrix of all tissues. The key regulatory effects of major medullar HSPGs are described, focusing on their roles in the interactions between hematopoietic stem cells and their endosteal niche, and on their ability to interact with Heparin Binding Proteins (HBPs). Finally, according to the relevance of HS moieties effects on this complex medullar niche, we describe recent data that identify HS mimetics or sulfated HS signatures as new glycanic tools and targets, respectively, for hematopoietic and mesenchymal stem cell based therapeutic applications.

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References

  1. Couchman, J.: Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 26, 89–114 (2010)

    Article  CAS  PubMed  Google Scholar 

  2. Kjellen, L., Lindahl, U.: Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60, 443–475 (1991)

    Article  CAS  PubMed  Google Scholar 

  3. Kreuger, J., et al.: 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 

  4. Gallagher, J.T.: Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Invest. 108(3), 357–361 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kreuger, J., et al.: Fibroblast growth factors share binding sites in heparan sulphate. Biochem. J. 389(Pt 1), 145–150 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lindahl, U., Kusche-Gullberg, M., Kjellen, L.: Regulated diversity of heparan sulfate. J. Biol. Chem. 273(39), 24979–24982 (1998)

    Article  CAS  PubMed  Google Scholar 

  7. Lindahl, U., Li, J.P.: Interactions between heparan sulfate and proteins-design and functional implications. Int. Rev. Cell Mol. Biol. 276, 105–159 (2009)

    Article  PubMed  CAS  Google Scholar 

  8. Kreuger, J., et al.: Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J. Biol. Chem. 276(33), 30744–30752 (2001)

    Article  CAS  PubMed  Google Scholar 

  9. Huynh, M.B., et al.: Glycosaminoglycans from aged human hippocampus have altered capacities to regulate trophic factors activities but not Abeta42 peptide toxicity. Neurobiol. Aging. 33(5), 1005 e11–1005 e22 (2012)

    Article  CAS  Google Scholar 

  10. Huynh, M.B., et al.: Age-related changes in rat myocardium involve altered capacities of glycosaminoglycans to potentiate growth factor functions and heparan sulfate-altered sulfation. J. Biol. Chem. 287(14), 11363–11373 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Negroni, E., et al.: Glycosaminoglycan modifications in Duchenne muscular dystrophy: specific remodeling of chondroitin sulfate/dermatan sulfate. J. Neuropathol. Exp. Neurol. 73(8), 789–797 (2014)

    Article  CAS  PubMed  Google Scholar 

  12. Chevalier, F., et al.: A fine structural modification of glycosaminoglycans is correlated with the progression of muscle regeneration after ischaemia: towards a matrix-based therapy? Eur. Cell. Mater. 30, 51–68 (2015)

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  14. Berninsone, P., Hirschberg, C.B.: Nucleotide sugars, nucleotide sulfate, and ATP transporters of the endoplasmic reticulum and Golgi apparatus. Ann. N. Y. Acad. Sci. 842, 91–99 (1998)

    Article  CAS  PubMed  Google Scholar 

  15. Fuller, M., et al.: A defect in exodegradative pathways provides insight into endodegradation of heparan and dermatan sulfates. Glycobiology. 16(4), 318–325 (2006)

    Article  CAS  PubMed  Google Scholar 

  16. Esko, J.D., Selleck, S.B.: Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435–471 (2002)

    Article  CAS  PubMed  Google Scholar 

  17. 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 

  18. Iozzo, R.V.: Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67, 609–652 (1998)

    Article  CAS  PubMed  Google Scholar 

  19. Bix, G., Iozzo, R.V.: Novel interactions of perlecan: unraveling perlecan's role in angiogenesis. Microsc. Res. Tech. 71(5), 339–348 (2008)

    Article  CAS  PubMed  Google Scholar 

  20. Hohenester, E., et al.: The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol. Cell. 4(5), 783–792 (1999)

    Article  CAS  PubMed  Google Scholar 

  21. Halfter, W., et al.: Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J. Biol. Chem. 273(39), 25404–25412 (1998)

    Article  CAS  PubMed  Google Scholar 

  22. Afratis, N.A., et al.: Syndecans - key regulators of cell signaling and biological functions. FEBS J. 284(1), 14 (2017)

    Article  CAS  Google Scholar 

  23. Fico, A., Maina, F., Dono, R.: Fine-tuning of cell signaling by glypicans. Cell. Mol. Life Sci. 68(6), 6 (2011)

    Article  CAS  Google Scholar 

  24. Fuster, M.M., Wang, L.: Endothelial heparan sulfate in angiogenesis. Prog. Mol. Biol. Transl. Sci. 93, 179–212 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sarrazin, S., Lamanna, W.C., Esko, J.D.: Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol. 3(7) (2011). doi:10.1101/cshperspect.a004952

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

    Article  CAS  PubMed  Google Scholar 

  27. Schofield, R.: The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 4(1–2), 7–25 (1978)

    CAS  PubMed  Google Scholar 

  28. Asada, N., Katayama, Y.: Regulation of hematopoiesis in endosteal microenvironments. Int. J. Hematol. 99(6), 679–684 (2014)

    Article  CAS  PubMed  Google Scholar 

  29. Kiel, M.J., Morrison, S.J.: Uncertainty in the niches that maintain haematopoietic stem cells. Nat. Rev. Immunol. 8(4), 290–301 (2008)

    Article  CAS  PubMed  Google Scholar 

  30. Stier, S., et al.: Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J. Exp. Med. 201(11), 1781–1791 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Zhang, J., et al.: Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 425(6960), 836–841 (2003)

    Article  CAS  PubMed  Google Scholar 

  32. Arai, F., et al.: Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 118(2), 149–161 (2004)

    Article  CAS  PubMed  Google Scholar 

  33. Yoshihara, H., et al.: Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell. 1(6), 685–697 (2007)

    Article  CAS  PubMed  Google Scholar 

  34. Mendez-Ferrer, S., et al.: Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 466(7308), 829–834 (2012)

    Article  CAS  Google Scholar 

  35. Levesque, J.P., Helwani, F.M., Winkler, I.G.: The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization. Leukemia. 24(12), 1979–1992 (2010)

    Article  PubMed  Google Scholar 

  36. Bonewald, L.F.: The amazing osteocyte. J. Bone Miner. Res. 26(2), 229–238 (2011)

    Article  CAS  PubMed  Google Scholar 

  37. Tatsumi, S., et al.: Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 5(6), 464–475 (2007)

    Article  CAS  PubMed  Google Scholar 

  38. Scadden, D.T.: The stem-cell niche as an entity of action. Nature. 441(7097), 1075–1079 (2006)

    Article  CAS  PubMed  Google Scholar 

  39. Kollet, O., et al.: Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat. Med. 12(6), 657–664 (2006)

    Article  CAS  PubMed  Google Scholar 

  40. Sugiyama, T., et al.: Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 25(6), 977–988 (2006)

    Article  CAS  PubMed  Google Scholar 

  41. Sacchetti, B., et al.: Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 131(2), 324–336 (2007)

    Article  CAS  PubMed  Google Scholar 

  42. Heissig, B., et al.: Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 109(5), 625–637 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Avecilla, S.T., et al.: Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat. Med. 10(1), 64–71 (2004)

    Article  CAS  PubMed  Google Scholar 

  44. Purton, L.E., Scadden, D.T.: The hematopoietic stem cell niche. Harvard Stem Cell Institute, Cambridge (2008)

  45. Adams, G.B., Scadden, D.T.: The hematopoietic stem cell in its place. Nat. Immunol. 7(4), 333–337 (2006)

  46. Friel, J., et al.: Diverse isoforms of colony-stimulating factor-1 have different effects on the development of stroma-dependent hematopoietic cells. J. Cell. Physiol. 204(1), 247–259 (2005)

    Article  CAS  PubMed  Google Scholar 

  47. Zandstra, P.W., Lauffenburger, D.A., Eaves, C.J.: A ligand-receptor signaling threshold model of stem cell differentiation control: a biologically conserved mechanism applicable to hematopoiesis. Blood. 96(4), 1215–1222 (2000)

    CAS  PubMed  Google Scholar 

  48. Doran, M.R., et al.: Surface-bound stem cell factor and the promotion of hematopoietic cell expansion. Biomaterials. 30(25), 4047–4052 (2009)

    Article  CAS  PubMed  Google Scholar 

  49. Bhatia, M., et al.: Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture. J. Exp. Med. 186(4), 619–624 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Miller, C.L., Eaves, C.J.: Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc. Natl. Acad. Sci. U. S. A. 94(25), 13648–13653 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Conneally, E., et al.: Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc. Natl. Acad. Sci. U. S. A. 94(18), 9836–9841 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ueda, T., et al.: Expansion of human NOD/SCID-repopulating cells by stem cell factor, Flk2/Flt3 ligand, thrombopoietin, IL-6, and soluble IL-6 receptor. J. Clin. Invest. 105(7), 1013–1021 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ehninger, A., Trumpp, A.: The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J. Exp. Med. 208(3), 421–428 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Thoren, L.A., et al.: Kit regulates maintenance of quiescent hematopoietic stem cells. J. Immunol. 180(4), 2045–2053 (2008)

    Article  CAS  PubMed  Google Scholar 

  55. Zhang, C.C., Sadek, H.A.: Hypoxia and metabolic properties of hematopoietic stem cells. Antioxid. Redox Signal. 20(12), 1891–1901 (2012)

    Article  CAS  Google Scholar 

  56. Chen, J., et al.: Erythropoietin-dependent autocrine secretion of tumor necrosis factor-alpha in hematopoietic cells modulates proliferation via MAP kinase--ERK-1/2 and does not require tyrosine docking sites in the EPO receptor. Exp. Cell Res. 298(1), 155–166 (2004)

    Article  CAS  PubMed  Google Scholar 

  57. Sitnicka, E., et al.: Key role of flt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity. 17(4), 463–472 (2002)

    Article  CAS  PubMed  Google Scholar 

  58. Adolfsson, J., et al.: Upregulation of Flt3 expression within the bone marrow Lin(−)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity. 15(4), 659–669 (2001)

    Article  CAS  PubMed  Google Scholar 

  59. Nilsson, S.K., et al.: Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood. 106(4), 1232–1239 (2005)

    Article  CAS  PubMed  Google Scholar 

  60. Coombe, D.R., Kett, W.C.: Heparan sulfate-protein interactions: therapeutic potential through structure-function insights. Cell. Mol. Life Sci. 62(4), 410–424 (2005)

    Article  CAS  PubMed  Google Scholar 

  61. Han, Z.C., et al.: Glycosaminoglycans enhance megakaryocytopoiesis by modifying the activities of hematopoietic growth regulators. J. Cell. Physiol. 168(1), 97–104 (1996)

    Article  CAS  PubMed  Google Scholar 

  62. Gupta, P., McCarthy, J.B., Verfaillie, C.M.: Stromal fibroblast heparan sulfate is required for cytokine-mediated ex vivo maintenance of human long-term culture-initiating cells. Blood. 87(8), 3229–3236 (1996)

    CAS  PubMed  Google Scholar 

  63. Verfaillie, C.M., Miller, J.S.: CD34+/CD33- cells reselected from macrophage inflammatory protein 1 alpha+interleukin-3--supplemented "stroma-noncontact" cultures are highly enriched for long-term bone marrow culture initiating cells. Blood. 84(5), 1442–1449 (1994)

    CAS  PubMed  Google Scholar 

  64. Hoogewerf, A.J., et al.: Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry. 36(44), 13570–13578 (1997)

    Article  CAS  PubMed  Google Scholar 

  65. Xu, Y., Liu, Y.J., Yu, Q.: Angiopoietin-3 is tethered on the cell surface via heparan sulfate proteoglycans. J. Biol. Chem. 279(39), 41179–41188 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Cazes, A., et al.: Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton. Circ. Res. 99(11), 1207–1215 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Netelenbos, T., et al.: Proteoglycans on bone marrow endothelial cells bind and present SDF-1 towards hematopoietic progenitor cells. Leukemia. 17(1), 175–184 (2003)

    Article  CAS  PubMed  Google Scholar 

  68. Dar, A., Kollet, O., Lapidot, T.: Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp. Hematol. 34(8), 967–975 (2006)

    Article  CAS  PubMed  Google Scholar 

  69. Bhardwaj, G., et al.: Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat. Immunol. 2(2), 172–180 (2001)

    Article  CAS  PubMed  Google Scholar 

  70. Bhatia, M., et al.: Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells. J. Exp. Med. 189(7), 1139–1148 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Khan, S.A., et al.: Endogenous heparan sulfate and heparin modulate bone morphogenetic protein-4 signaling and activity. Am. J. Physiol. Cell. Physiol. 294(6), C1387–C1397 (2008)

    Article  CAS  PubMed  Google Scholar 

  72. Jackson, R.A., Nurcombe, V., Cool, S.M.: Coordinated fibroblast growth factor and heparan sulfate regulation of osteogenesis. Gene. 379, 79–91 (2006)

    Article  CAS  PubMed  Google Scholar 

  73. Yeoh, J.S., et al.: Fibroblast growth factor-1 and -2 preserve long-term repopulating ability of hematopoietic stem cells in serum-free cultures. Stem Cells. 24(6), 1564–1572 (2006)

    Article  CAS  PubMed  Google Scholar 

  74. Marie, P.J., Coffin, J.D., Hurley, M.M.: FGF and FGFR signaling in chondrodysplasias and craniosynostosis. J. Cell. Biochem. 96(5), 888–896 (2005)

    Article  CAS  PubMed  Google Scholar 

  75. Bonaventure, J., El Ghouzzi, V.: Molecular and cellular bases of syndromic craniosynostoses. Expert Rev. Mol. Med. 5(4), 1–17 (2003)

    Article  PubMed  Google Scholar 

  76. Marie, P.J.: Fibroblast growth factor signaling controlling osteoblast differentiation. Gene. 316, 23–32 (2003)

    Article  CAS  PubMed  Google Scholar 

  77. Turnbull, J.E., et al.: Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267(15), 10337–10341 (1992)

    CAS  PubMed  Google Scholar 

  78. Pellegrini, L., et al.: Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature. 407(6807), 1029–1034 (2000)

    Article  CAS  PubMed  Google Scholar 

  79. Jackson, R.A., et al.: Heparan sulfate regulates the anabolic activity of MC3T3-E1 preosteoblast cells by induction of Runx2. J. Cell. Physiol. 210(1), 38–50 (2007)

    Article  CAS  PubMed  Google Scholar 

  80. Logan, C.Y., Nusse, R.: The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781–810 (2004)

    Article  CAS  PubMed  Google Scholar 

  81. Bejsovec, A.: Wnt pathway activation: new relations and locations. Cell. 120(1), 11–14 (2005)

    CAS  PubMed  Google Scholar 

  82. Morimoto-Tomita, M., et al.: Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277(51), 49175–49185 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hoppler, S., Kavanagh, C.L.: Wnt signalling: variety at the core. J. Cell Sci. 120(Pt 3), 385–393 (2007)

    Article  CAS  PubMed  Google Scholar 

  84. Anton, R., Kestler, H.A., Kuhl, M.: Beta-catenin signaling contributes to stemness and regulates early differentiation in murine embryonic stem cells. FEBS Lett. 581(27), 5247–5254 (2007)

    Article  CAS  PubMed  Google Scholar 

  85. Duncan, A.W., et al.: Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 6(3), 314–322 (2005)

    Article  CAS  PubMed  Google Scholar 

  86. Lai, X.N., et al.: Sensory neuropeptide SP modulating expression of EGF, FGF-2 and their receptors in fibroblasts of granulation in vivo and in vitro. Zhonghua Yi Xue Za Zhi. 83(16), 1433–1436 (2003)

    CAS  PubMed  Google Scholar 

  87. Schofield, K.P., Gallagher, J.T., David, G.: Expression of proteoglycan core proteins in human bone marrow stroma. Biochem. J. 343(Pt 3), 663–668 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Spooncer, E., et al.: Regulation of haemopoiesis in long-term bone marrow cultures. IV. Glycosaminoglycan synthesis and the stimulation of haemopoiesis by beta-D-xylosides. J. Cell Biol. 96(2), 510–514 (1983)

    Article  CAS  PubMed  Google Scholar 

  89. Spooncer, E., Dexter, T.M.: Transplantation of long-term cultured bone marrow cells. Transplantation. 35(6), 624–627 (1983)

    Article  CAS  PubMed  Google Scholar 

  90. Gallagher, J.T.: E. Spooncer, and T.M. Dexter, Role of the cellular matrix in haemopoiesis. I. Synthesis of glycosaminoglycans by mouse bone marrow cell cultures. J. Cell Sci. 63, 155–171 (1983)

    CAS  PubMed  Google Scholar 

  91. Wight, T.N., et al.: Proteoglycans in human long-term bone marrow cultures: biochemical and ultrastructural analyses. Blood. 67(5), 1333–1343 (1986)

    CAS  PubMed  Google Scholar 

  92. Gallagher, J.T., Lyon, M., Steward, W.P.: Structure and function of heparan sulphate proteoglycans. Biochem. J. 236(2), 313–325 (1986)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Drzeniek, Z., et al.: Proteoglycan synthesis in haematopoietic cells: isolation and characterization of heparan sulphate proteoglycans expressed by the bone-marrow stromal cell line MS-5. Biochem. J. 327(Pt 2), 473–480 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Gupta, P., et al.: Structurally specific heparan sulfates support primitive human hematopoiesis by formation of a multimolecular stem cell niche. Blood. 92(12), 4641–4651 (1998)

    CAS  PubMed  Google Scholar 

  95. Rodgers, K.D., San Antonio, J.D., Jacenko, O.: Heparan sulfate proteoglycans: a GAGgle of skeletal-hematopoietic regulators. Dev. Dyn. 237(10), 2622–2642 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Bruno, E., et al.: Marrow-derived heparan sulfate proteoglycan mediates the adhesion of hematopoietic progenitor cells to cytokines. Exp. Hematol. 23(11), 1212–1217 (1995)

    CAS  PubMed  Google Scholar 

  97. Siczkowski, M., Clarke, D., Gordon, M.Y.: Binding of primitive hematopoietic progenitor cells to marrow stromal cells involves heparan sulfate. Blood. 80(4), 912–919 (1992)

    CAS  PubMed  Google Scholar 

  98. Wight, T.N., Kinsella, M.G., Qwarnstrom, E.E.: The role of proteoglycans in cell adhesion, migration and proliferation. Curr. Opin. Cell Biol. 4(5), 793–801 (1992)

    Article  CAS  PubMed  Google Scholar 

  99. Bernfield, M., et al.: Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8, 365–393 (1992)

    Article  CAS  PubMed  Google Scholar 

  100. Chen, X.D., et al.: Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. J. Bone Miner. Res. 22(12), 1943–1956 (2007)

    Article  CAS  PubMed  Google Scholar 

  101. Tumova, S., Woods, A., Couchman, J.R.: Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int. J. Biochem. Cell Biol. 32(3), 269–288 (2000)

    Article  CAS  PubMed  Google Scholar 

  102. Rapraeger, A.C.: Syndecan-regulated receptor signaling. J. Cell Biol. 149(5), 995–998 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Zaragosi, L.E., et al.: Syndecan-1 regulates adipogenesis: new insights in dedifferentiated liposarcoma tumorigenesis. Carcinogenesis. 36(1), 32–40 (2014)

    Article  PubMed  CAS  Google Scholar 

  104. Gotte, M., et al.: Role of syndecan-1 in leukocyte-endothelial interactions in the ocular vasculature. Invest. Ophthalmol. Vis. Sci. 43(4), 1135–1141 (2002)

    PubMed  Google Scholar 

  105. Andersen, N.F., et al.: Upregulation of Syndecan-1 in the bone marrow microenvironment in multiple myeloma is associated with angiogenesis. Eur. J. Haematol. 95(3), 211–217 (2015)

    Article  CAS  PubMed  Google Scholar 

  106. Mahtouk, K., et al.: Heparanase influences expression and shedding of syndecan-1, and its expression by the bone marrow environment is a bad prognostic factor in multiple myeloma. Blood. 109(11), 4914–4923 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Jung, O., et al.: Heparanase-induced shedding of syndecan-1/CD138 in myeloma and endothelial cells activates VEGFR2 and an invasive phenotype: prevention by novel synstatins. Oncogene. 5, e202 (2016)

    Article  CAS  Google Scholar 

  108. Filmus, J.: Glypicans in growth control and cancer. Glycobiology. 11(3), 19R–23R (2001)

    Article  CAS  PubMed  Google Scholar 

  109. Yanagishita, M., Hascall, V.C.: Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267(14), 9451–9454 (1992)

    CAS  PubMed  Google Scholar 

  110. Viviano, B.L., et al.: Altered hematopoiesis in glypican-3-deficient mice results in decreased osteoclast differentiation and a delay in endochondral ossification. Dev. Biol. 282(1), 152–162 (2005)

    Article  CAS  PubMed  Google Scholar 

  111. Haupt, L.M., et al.: The heparan sulfate proteoglycan (HSPG) glypican-3 mediates commitment of MC3T3-E1 cells toward osteogenesis. J. Cell. Physiol. 220(3), 780–791 (2009)

    Article  CAS  PubMed  Google Scholar 

  112. Teplyuk, N.M., et al.: The osteogenic transcription factor Runx2 regulates components of the fibroblast growth factor/proteoglycan signaling axis in osteoblasts. J. Cell. Biochem. 107(1), 144–154 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Khurana, S., et al.: Glypican-3-mediated inhibition of CD26 by TFPI: a novel mechanism in hematopoietic stem cell homing and maintenance. Blood. 121(14), 2587–2595 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Litwack, E.D., et al.: Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev. Dyn. 211(1), 72–87 (1998)

    Article  CAS  PubMed  Google Scholar 

  115. Siebertz, B., et al.: Expression of glypican-4 in haematopoietic-progenitor and bone-marrow-stromal cells. Biochem. J. 344(Pt 3), 937–943 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Arikawa-Hirasawa, E., et al.: Perlecan is essential for cartilage and cephalic development. Nat. Genet. 23(3), 354–358 (1999)

    Article  CAS  PubMed  Google Scholar 

  117. Thompson, W.R., et al.: Perlecan/Hspg2 deficiency alters the pericellular space of the lacunocanalicular system surrounding osteocytic processes in cortical bone. J. Bone Miner. Res. 26(3), 618–629 (2011)

    Article  CAS  PubMed  Google Scholar 

  118. Wang, B., et al.: Perlecan-containing pericellular matrix regulates solute transport and mechanosensing within the osteocyte lacunar-canalicular system. J. Bone Miner. Res. 29(4), 878–891 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Gustafsson, E., et al.: Role of collagen type II and perlecan in skeletal development. Ann. N. Y. Acad. Sci. 995, 140–150 (2003)

    Article  CAS  PubMed  Google Scholar 

  120. Ishijima, M., et al.: Perlecan modulates VEGF signaling and is essential for vascularization in endochondral bone formation. Matrix Biol. 31(4), 234–245 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Klein, G., et al.: Perlecan in human bone marrow: a growth-factor-presenting, but anti-adhesive, extracellular matrix component for hematopoietic cells. Matrix Biol. 14(6), 457–465 (1995)

    Article  CAS  PubMed  Google Scholar 

  122. Yang, W.D., et al.: Perlecan domain I promotes fibroblast growth factor 2 delivery in collagen I fibril scaffolds. Tissue Eng. 11(1–2), 76–89 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Muthusamy, A., Cooper, C.R., Gomes Jr., R.R.: Soluble perlecan domain I enhances vascular endothelial growth factor-165 activity and receptor phosphorylation in human bone marrow endothelial cells. BMC Biochem. 11, 43 (2010)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Lai, Y., et al.: Reconstitution of marrow-derived extracellular matrix ex vivo: a robust culture system for expanding large-scale highly functional human mesenchymal stem cells. Stem Cells Dev. 19(7), 1095–1107 (2010)

    Article  CAS  PubMed  Google Scholar 

  125. Nigro, J., et al.: The effect of bovine endosteum-derived particles on the proliferation of human mesenchymal stem cells. Biomaterials. 31(21), 5689–5699 (2010)

    Article  CAS  PubMed  Google Scholar 

  126. Nakamura, R., Nakamura, F., Fukunaga, S.: Contrasting effect of perlecan on adipogenic and osteogenic differentiation of mesenchymal stem cells in vitro. Anim. Sci. J. 85(3), 262–270 (2014)

    Article  CAS  PubMed  Google Scholar 

  127. Decarlo, A.A., et al.: Perlecan domain 1 recombinant proteoglycan augments BMP-2 activity and osteogenesis. BMC Biotechnol. 12, 60 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Ruegg, M.A., Bixby, J.L.: Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci. 21(1), 22–27 (1998)

    Article  CAS  PubMed  Google Scholar 

  129. Kim, N., et al.: Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell. 135(2), 334–342 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Hausser, H.J., et al.: Agrin is highly expressed by chondrocytes and is required for normal growth. Histochem. Cell Biol. 127(4), 363–374 (2007)

    Article  CAS  PubMed  Google Scholar 

  131. Mazzon, C., et al.: Agrin is required for survival and function of monocytic cells. Blood. 119(23), 5502–5511 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Zhang, J., et al.: Agrin is involved in lymphocytes activation that is mediated by alpha-dystroglycan. FASEB J. 20(1), 50–58 (2006)

    Article  PubMed  CAS  Google Scholar 

  133. Barresi, R., Campbell, K.P.: Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119(Pt 2), 199–207 (2006)

    Article  CAS  PubMed  Google Scholar 

  134. Yang, B., et al.: SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem. 270(20), 11711–11714 (1995)

    Article  CAS  PubMed  Google Scholar 

  135. Koch, C.A., et al.: SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science. 252(5006), 668–674 (1991)

    Article  CAS  PubMed  Google Scholar 

  136. Steidl, U., et al.: Primary human CD34+ hematopoietic stem and progenitor cells express functionally active receptors of neuromediators. Blood. 104(1), 81–88 (2004)

    Article  CAS  PubMed  Google Scholar 

  137. Mazzon, C., et al.: The critical role of agrin in the hematopoietic stem cell niche. Blood. 118(10), 2733–2742 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Kiel, M.J., et al.: SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 121(7), 1109–1121 (2005)

    Article  CAS  PubMed  Google Scholar 

  139. To, L.B, et al.: The biology and clinical uses of blood stem cells. Blood. 89(7), 2233–2258 (1997)

    Google Scholar 

  140. Weaver, C.H., Schulman, K.A., Buckner, C.D.: Mobilization of peripheral blood stem cells following myelosuppressive chemotherapy: a randomized comparison of filgrastim, sargramostim, or sequential sargramostim and filgrastim. Bone Marrow Transplant. 27(Suppl 2), S23–S29 (2001)

    Article  PubMed  Google Scholar 

  141. Winkler, I.G., Levesque, J.P.: Mechanisms of hematopoietic stem cell mobilization: when innate immunity assails the cells that make blood and bone. Exp. Hematol. 34(8), 996–1009 (2006)

    Article  CAS  PubMed  Google Scholar 

  142. Ma, Q., et al.: Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 95(16), 9448–9453 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Nagasawa, T., et al.: Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 382(6592), 635–638 (1996)

    Article  CAS  PubMed  Google Scholar 

  144. Bleul, C.C., et al.: A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 184(3), 1101–1109 (1996)

    Article  CAS  PubMed  Google Scholar 

  145. Netelenbos, T., et al.: Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells. J. Leukoc. Biol. 72(2), 353–362 (2002)

    CAS  PubMed  Google Scholar 

  146. Avigdor, A., et al.: CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood. 103(8), 2981–2989 (2004)

    Article  CAS  PubMed  Google Scholar 

  147. Amara, A., et al.: Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine. J. Biol. Chem. 274(34), 23916–23925 (1999)

    Article  CAS  PubMed  Google Scholar 

  148. Sadir, R., et al.: Characterization of the stromal cell-derived factor-1alpha-heparin complex. J. Biol. Chem. 276(11), 8288–8296 (2001)

    Article  CAS  PubMed  Google Scholar 

  149. Frenette, P.S., Weiss, L.: Sulfated glycans induce rapid hematopoietic progenitor cell mobilization: evidence for selectin-dependent and independent mechanisms. Blood. 96(7), 2460–2468 (2000)

    CAS  PubMed  Google Scholar 

  150. Sweeney, E.A., et al.: Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells. Blood. 99(1), 44–51 (2002)

    Article  CAS  PubMed  Google Scholar 

  151. Albanese, P., et al.: Glycosaminoglycan mimetics-induced mobilization of hematopoietic progenitors and stem cells into mouse peripheral blood: structure/function insights. Exp. Hematol. 37(9), 1072–1083 (2009)

    Article  CAS  PubMed  Google Scholar 

  152. Papy-Garcia, D., et al.: Nondegradative sulfation of polysaccharides. Synthesis and structure characterization of biologically active heparan sulfate mimetics. Macromolecules. 38, 4647–4654 (2005)

    Article  CAS  Google Scholar 

  153. Saez, B., et al.: Inhibiting stromal cell heparan sulfate synthesis improves stem cell mobilization and enables engraftment without cytotoxic conditioning. Blood. 124(19), 2937–2947 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Pittenger, M.F., et al.: Multilineage potential of adult human mesenchymal stem cells. Science. 284(5411), 143–147 (1999)

    Article  CAS  PubMed  Google Scholar 

  155. Muschler, G.F., Nakamoto, C., Griffith, L.G.: Engineering principles of clinical cell-based tissue engineering. J. Bone Joint Surg. Am. 86-A(7), 1541–1558 (2004)

    Article  PubMed  Google Scholar 

  156. Wexler, S.A., et al.: Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br. J. Haematol. 121(2), 368–374 (2003)

    Article  PubMed  Google Scholar 

  157. Baksh, D., Song, L., Tuan, R.S.: Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J. Cell. Mol. Med. 8(3), 301–316 (2004)

    Article  CAS  PubMed  Google Scholar 

  158. Dombrowski, C., et al.: Heparan sulfate mediates the proliferation and differentiation of rat mesenchymal stem cells. Stem Cells Dev. 18(4), 661–670 (2009)

    Article  CAS  PubMed  Google Scholar 

  159. Manton, K.J., et al.: Disruption of heparan and chondroitin sulfate signaling enhances mesenchymal stem cell-derived osteogenic differentiation via bone morphogenetic protein signaling pathways. Stem Cells. 25(11), 2845–2854 (2007)

    Article  CAS  PubMed  Google Scholar 

  160. Cool, S.M., Nurcombe, V.: The osteoblast-heparan sulfate axis: control of the bone cell lineage. Int. J. Biochem. Cell Biol. 37(9), 1739–1745 (2005)

    Article  CAS  PubMed  Google Scholar 

  161. Nurcombe, V., et al.: Temporal and functional changes in glycosaminoglycan expression during osteogenesis. J. Mol. Histol. 38(5), 469–481 (2007)

    Article  CAS  PubMed  Google Scholar 

  162. Montero, A., et al.: Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J. Clin. Invest. 105(8), 1085–1093 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Muller, B., et al.: Increased levels of xylosyltransferase I correlate with the mineralization of the extracellular matrix during osteogenic differentiation of mesenchymal stem cells. Matrix Biol. 27(2), 139–149 (2008)

    Article  PubMed  CAS  Google Scholar 

  164. Molteni, A., et al.: Alterations of matrix- and cell-associated proteoglycans inhibit osteogenesis and growth response to fibroblast growth factor-2 in cultured rat mandibular condyle and calvaria. Cell Tissue Res. 295(3), 523–536 (1999)

    Article  CAS  PubMed  Google Scholar 

  165. Ostrovsky, O., et al.: Differential effects of heparin saccharides on the formation of specific fibroblast growth factor (FGF) and FGF receptor complexes. J. Biol. Chem. 277(4), 2444–2453 (2002)

    Article  CAS  PubMed  Google Scholar 

  166. Goodger, S.J., et al.: Evidence that heparin saccharides promote FGF2 mitogenesis through two distinct mechanisms. J. Biol. Chem. 283(19), 13001–13008 (2008)

    Article  CAS  PubMed  Google Scholar 

  167. Guimond, S.E., Turnbull, J.E.: Fibroblast growth factor receptor signalling is dictated by specific heparan sulphate saccharides. Curr. Biol. 9(22), 1343–1346 (1999)

    Article  CAS  PubMed  Google Scholar 

  168. Frescaline, G., et al.: Glycosaminoglycans mimetics potentiate the clonogenicity, proliferation, migration and differentiation properties of rat mesenchymal stem cells. Stem Cell Res. 8(2), 180–192 (2012)

    Article  CAS  PubMed  Google Scholar 

  169. Frescaline, G., et al.: Glycosaminoglycan mimetic associated to human mesenchymal stem cell-based scaffolds inhibit ectopic bone formation, but induce angiogenesis in vivo. Tissue Eng. Part A. 19(13–14), 1641–1653 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Grellier, M., Bordenave, L., Amedee, J.: Cell-to-cell communication between osteogenic and endothelial lineages: implications for tissue engineering. Trends Biotechnol. 27(10), 562–571 (2009)

    Article  CAS  PubMed  Google Scholar 

  171. Esko, J.D., Lindahl, U.: Molecular diversity of heparan sulfate. J. Clin. Invest. 108(2), 169–173 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Kusche-Gullberg, M., et al.: Identification and expression in mouse of two heparan sulfate glucosaminyl N-deacetylase/N-sulfotransferase genes. J. Biol. Chem. 273(19), 11902–11907 (1998)

    Article  CAS  PubMed  Google Scholar 

  173. Grobe, K., et al.: Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function. Development. 132(16), 3777–3786 (2005)

    Article  CAS  PubMed  Google Scholar 

  174. Fan, G., et al.: Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett. 467(1), 7–11 (2000)

    Article  CAS  PubMed  Google Scholar 

  175. Ringvall, M., et al.: Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-deacetylase/N-sulfotransferase-1. J. Biol. Chem. 275(34), 25926–25930 (2000)

    Article  CAS  PubMed  Google Scholar 

  176. Forsberg, E., et al.: Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature. 400(6746), 773–776 (1999)

    Article  CAS  PubMed  Google Scholar 

  177. Humphries, D.E., et al.: Heparin is essential for the storage of specific granule proteases in mast cells. Nature. 400(6746), 769–772 (1999)

    Article  CAS  PubMed  Google Scholar 

  178. Pallerla, S.R., et al.: Altered heparan sulfate structure in mice with deleted NDST3 gene function. J. Biol. Chem. 283(24), 16885–16894 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Jakobsson, L., et al.: Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell. 10(5), 625–634 (2006)

    Article  CAS  PubMed  Google Scholar 

  180. Forsberg, M., et al.: 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 

  181. Zhao, S., et al.: Heparan sulfate 6-O-sulfotransferase 3 is involved in bone marrow mesenchymal stromal cell osteogenic differentiation. Biochemistry (Mosc). 80(3), 379–389 (2015)

    Article  CAS  Google Scholar 

  182. Shukla, D., et al.: A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell. 99(1), 13–22 (1999)

    Article  CAS  PubMed  Google Scholar 

  183. Patel, V.N., et al.: Hs3st3-modified heparan sulfate controls KIT+ progenitor expansion by regulating 3-O-sulfotransferases. Dev. Cell. 29(6), 662–673 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Hirano, K., Van Kuppevelt, T.H., Nishihara, S.: The transition of mouse pluripotent stem cells from the naive to the primed state requires Fas signaling through 3-O sulfated heparan sulfate structures recognized by the HS4C3 antibody. Biochem. Biophys. Res. Commun. 430(3), 1175–1181 (2013)

    Article  CAS  PubMed  Google Scholar 

  185. Hirano, K., et al.: 3-O-sulfated heparan sulfate recognized by the antibody HS4C3 contributes [corrected] to the differentiation of mouse embryonic stem cells via fas signaling. PLoS One. 7(8), e43440 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Martinez, P., et al.: Macrophage polarization alters the expression and sulfation pattern of glycosaminoglycans. Glycobiology. 25(5), 502–513 (2015)

    Article  CAS  PubMed  Google Scholar 

  187. Sikora, A.S., et al.: Regulation of the expression of Heparan sulfate 3-O-sulfotransferase 3B (HS3ST3B) by inflammatory stimuli in human monocytes. J. Cell. Biochem. 117(7), 1529–1542 (2016)

    Article  CAS  PubMed  Google Scholar 

  188. Kram, V., et al.: Heparanase is expressed in osteoblastic cells and stimulates bone formation and bone mass. J. Cell. Physiol. 207(3), 784–792 (2006)

    Article  CAS  PubMed  Google Scholar 

  189. Schmidt, B., et al.: A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell. 82(2), 271–278 (1995)

    Article  CAS  PubMed  Google Scholar 

  190. Cosma, M.P., et al.: The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell. 113(4), 445–456 (2003)

    Article  CAS  PubMed  Google Scholar 

  191. Dierks, T., et al.: Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme. Cell. 113(4), 435–444 (2003)

    Article  CAS  PubMed  Google Scholar 

  192. Sardiello, M., et al.: Sulfatases and sulfatase modifying factors: an exclusive and promiscuous relationship. Hum. Mol. Genet. 14(21), 3203–3217 (2005)

    Article  CAS  PubMed  Google Scholar 

  193. Cosma, M.P., et al.: Molecular and functional analysis of SUMF1 mutations in multiple sulfatase deficiency. Hum. Mutat. 23(6), 576–581 (2004)

    Article  CAS  PubMed  Google Scholar 

  194. Settembre, C., et al.: Systemic inflammation and neurodegeneration in a mouse model of multiple sulfatase deficiency. Proc. Natl. Acad. Sci. U. S. A. 104(11), 4506–4511 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Buono, M., et al.: Sulfatase modifying factor 1-mediated fibroblast growth factor signaling primes hematopoietic multilineage development. J. Exp. Med. 207(8), 1647–1660 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Taichman, R.S.: Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood. 105(7), 2631–2639 (2005)

    Article  CAS  PubMed  Google Scholar 

  197. Morrison, S.J., Spradling, A.C.: Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 132(4), 598–611 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Bianco, P., et al.: Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells. 19(3), 180–192 (2001)

    Article  CAS  PubMed  Google Scholar 

  199. Katayama, Y., et al.: Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell. 124(2), 407–421 (2006)

    Article  CAS  PubMed  Google Scholar 

  200. Gordon, M.Y.: Extracellular matrix of the marrow microenvironment. Br. J. Haematol. 70(1), 1–4 (1988)

    Article  CAS  PubMed  Google Scholar 

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  1. CRRET Laboratory, Université Paris Est, EA 4397 Université Paris Est Créteil, ERL CNRS 9215, F-94010, Créteil, France

    Dulce Papy-Garcia & Patricia Albanese

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Papy-Garcia, D., Albanese, P. Heparan sulfate proteoglycans as key regulators of the mesenchymal niche of hematopoietic stem cells. Glycoconj J 34, 377–391 (2017). https://doi.org/10.1007/s10719-017-9773-8

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