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Fractones: Home and Conductors of the Neural Stem Cell Niche

  • Frederic Mercier
  • Jason Schnack
  • Maureen Saint Georges Chaumet

Abstract

Throughout life, neural stem cells proliferate and differentiate in restricted zones of the brain, termed niches, to produce new neurons and glial cells. In these niches, growth factors and extracellular matrix (ECM) molecules determine the fate of neural stem and progenitor cells (NSPC). However, the precise compounds and the mechanisms that regulate growth factors and other signaling molecules in the niches are unknown. Based on the evidence that NSPCs proliferate next to blood vessels in the dentate gyrus, the concept of a vascular niche for neurogenesis has been initially proposed. In the subventricular zone of the lateral ventricle, the most neurogenic zone in adulthood, we have found that NSPC directly contact a novel type of ECM structure that we have named fractones. Fractones contain heparan sulfate proteoglycans (HSPG) that collect and concentrate the neurogenic growth factor FGF2 at the NSPC surface and likely direct its signaling via tyrosine kinase receptors. Our preliminary results indicate that FGF2 binding to fractone-HSPG is essential for activating FGF2 at the NSPC surface. Moreover, we have found fractones express diverse HSPG at the surface of proliferating NSPC during development, even before the brain vasculature emerges. Therefore, fractones hold considerable promise for promoting growth factors at the stem cell surface to ultimately regulate neurogenesis during development and adulthood.

Keywords

Olfactory Bulb Dentate Gyrus Neural Stem Cell Lateral Ventricle Rostral Migratory Stream 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Altman, J. (1963). Autoradiographic investigation of cell proliferation in the brain of cats and rats. Anat. Rec. 145, 573–591.PubMedCrossRefGoogle Scholar
  2. Altman, J. (1969). Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137, 433–458.PubMedCrossRefGoogle Scholar
  3. Altman, J., Das, G.D. (1966). Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special references to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 126, 337–390.PubMedCrossRefGoogle Scholar
  4. Alvarez-Buylla, A., Nottebohm, F. (1988). Migration of young neurons in adult avian brain. Nature 335, 353–354.CrossRefGoogle Scholar
  5. Aviezer, D., Hecht, D., Safran, M., Elsinger, M. David, G., Yayon, A. (1994). Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell 79, 1005–1013.PubMedCrossRefGoogle Scholar
  6. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M.T., Spring, J., Gallo, R.L. (1992). Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8, 365–93.PubMedCrossRefGoogle Scholar
  7. Bernfield, M., Banerjee, S.D., Koda, J.E., Rapraeger, A.C. (1994). Remodelling of basement membranes as a mechanism of morphogenetic tissue interactions. In: Trelstadt, R.L. (ed) The role of extracellular matrix in development. New York, Liss, A.R.Google Scholar
  8. Bernfield, M., Gotte, M., Park, P., Reizes, O., Fitzgerald, M., Lincecum, J., Zako, M. (1999). Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729–777.PubMedCrossRefGoogle Scholar
  9. Blanpain, C., Lowry, W., Georghegan, A., Polak, L., Fuchs, E. (2004). Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118, 635–648.PubMedCrossRefGoogle Scholar
  10. Brickman, Y.G., Ford, M.D., Small, D.H., Bartlett, P.F., Nurcombe, V. (1995). Heparan sulfates mediate the binding of basic fibroblast growth factor to a specific receptor on neural precursor cells. J. Biol. Chem. 270, 24941–24948.PubMedCrossRefGoogle Scholar
  11. Brickman, Y., Ford, M., Gallagher, J., Nurcombe, V., Bartlett, P., Turnbull, J. (1998). Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 8:5, 4350–4359.Google Scholar
  12. Brightman, M.W. (1965). The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. J. Cell Biol. 26, 99–123.PubMedCrossRefGoogle Scholar
  13. Brightman, M.W. (2002). The brain’s interstitial clefts and their glial walls. J. Neurocytol. 31, 595–603.PubMedCrossRefGoogle Scholar
  14. Chadashvili, T., Peterson, D. (2006). Cytoarchitecture of fibroblast growth factor receptor 2 (FGFR-2) immunoreactivity in astrocytes of neurogenic and non-neurogenic regions of the young adult and aged rat brain. J. Comp. Neurol. 498:1, 1–15.Google Scholar
  15. Chang, Z., Meyer, K., Rapraeger, A.C., Friedl, A. (2000). Differential ability of heparan sulfate proteoglycans to assemble the fibroblast growth factor receptor complex in situ. FASEB J. 14, 137–144.PubMedGoogle Scholar
  16. Craig, CG, Tropepe, V, Morshead, CM, Reynolds, BA, Weiss, S, van der Kooy, D. (1996). In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16, 2649–2658.Google Scholar
  17. Doetsch, F., Alvarez-Buylla, A. (1996). Network of tangential pathways for neuronal migration in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 93, 14895–14900.PubMedCrossRefGoogle Scholar
  18. Doetsch, F., Garcia-Verdugo, J.M., Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization in the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046–5061.PubMedGoogle Scholar
  19. Falk, A., Frisen, J. (2002). Amphiregulin is a mitogen for adult neural stem cells. J. Neurosci. Res. 69, 757–762.PubMedCrossRefGoogle Scholar
  20. Fitzgerald, M., Hayward, I.P., Thomas, A.C., Campbell, G.R., Campbell, J.H. (1999). Matrix metalloproteinase can facilitate the heparanase-induced promotion of phenotype change in vascular smooth muscle cells. Atherosclerosis 145:1, 97–106.PubMedCrossRefGoogle Scholar
  21. Gallagher, J.T. (2001). Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Invest. 108:3, 357–361PubMedGoogle Scholar
  22. Goodger, S., Robinson, C., Murphy, K., Gasiunas, N., Harmer, N., Blundell, T., Pye, D., Gallagher, J. (2008). Evidence that heparin saccharides promote FGF2 mitogenesis through two distinct mechanisms. J. Biol. Chem. 283, 13001–13008.PubMedCrossRefGoogle Scholar
  23. Gordon, M.Y., Riley, G.P., Watt, S.M., Greaves, M.F. (1987). Compartmentalization of a haematopoeitic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment. Nature 326, 403–405.CrossRefGoogle Scholar
  24. Grobe, K., Ledin, J., Ringvall, M., Holmborn, K., Forsberg, E., Esko, J.D., Kjellén, L. (2002). Heparan sulfate and development: differential roles of the N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes. Biochim. Biophys. Acta 1573:3, 209–215.PubMedCrossRefGoogle Scholar
  25. Guimond, S., Maccarana, M., Olwin, B., Lindahl, U., Rapraeger, A. (1993). Activating and inhibitory heparin sequences for FGF-2 (basic FGF) distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 268, 23906–23914.PubMedGoogle Scholar
  26. Halfter, W. (1998). Disruption of the retinal basal lamina during early embryonic development leads to a retraction of vitral endfeet, an increase number of ganglion cells, and aberrant axonal outgrowth. J. Comp. Neurol. 397, 99–104.Google Scholar
  27. Hayamizu, T.F., Chan, P.T., Johanson, C.E. (2001). FGF-2 immunoreactivity in adult rat ependyma and choroid plexus: responses to global forebrain ischemia and intraventricular FGF-2. Neurol. Res. 23, 353–358.PubMedCrossRefGoogle Scholar
  28. Hienola, A., Pekkanen, M., Raulo, E., (2004). HB-GAM inhibits proliferation and enhances differentiation of neural stem cells. Mol. Cell. Neurosci. 26, 75–88.PubMedCrossRefGoogle Scholar
  29. Hienola, A., Tumova, S., Kulesskiy, E., Rauvala, H. (2006). N-syndecan deficiency impairs neural migration in the brain. J. Cell Biol. 174, 569–580.PubMedCrossRefGoogle Scholar
  30. Iozzo, R.V. (2005). Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell. Biol. 6, 646–656.PubMedCrossRefGoogle Scholar
  31. Jasuja, R., Allen, B., Pappano, W., Rapraeger, A., Greenspan, D. (2004). Cell-surface heparen sulfate proteoglycans chordin antagonism of bone morphogenetic protein signaling and are necessary for cellular uptake of chordin. J. Biol. Chem. 279, 51289–51297.PubMedCrossRefGoogle Scholar
  32. Jayson, G.C., Lyon, M., Paraskeva, C., Turnbull, J.E., Deakin, J.A., Gallagher, J.T. (1998). Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 273:1, 51–57.PubMedCrossRefGoogle Scholar
  33. Kaji, T., Yamamoto, C., Oh-i, M., Fujiwara, Y., Yamazaki, Y., Morita, T., Plaas, A.H., Wight, T.N. (2006). The vascular endothelial growth factor VEGF165 induces perlecan synthesis via VEGF receptor-2 in cultured human brain microvascular endothelial cells. Biochim. Biophys. Acta 1760:9, 1465–1474.PubMedCrossRefGoogle Scholar
  34. Kerever, A., Schnack, J., Vellinga, D., Ichikawa, N., Moon, C., Arikawa-Hirasawa, E., Efird, J.T., Mercier, F. (2007). Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor FGF-2 from the extracellular milieu. Stem Cells 25, 2146–2157.PubMedCrossRefGoogle Scholar
  35. Kim, C.W., Goldberger, O.A., Gallo, R.L., Bernfield, M. (1994). Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-,tissue-, and development-specific patterns. Mol. Biol. Cell 5, 797–805.PubMedGoogle Scholar
  36. Kim, S.J., Son, T.G., Kim, K., Park, H.R., Mattson, M.P., Lee, J. (2007). Interferon-gamma promotes differentiation of neural progenitor cells via the JNK pathway. Neurochem. Res. 32, 1399–1406.PubMedCrossRefGoogle Scholar
  37. Klein, G., Conzelmann, S., Beck, S., Timpl, R., Müller, C.A. (1995). Perlecan in human bone marrow: a growth-factor-presenting, but anti-adhesive, extracellular matrix component for hematopoietic cells. Matrix Biol. 14, 457–465.PubMedCrossRefGoogle Scholar
  38. Knox, S., Merry, C., Stringer, S., Melrose, J., Whitelock, J. (2002). Not all perlecans are created equal. J. Biol. Chem. 277, 14657–14665.PubMedGoogle Scholar
  39. Kobayashi, M., Shimada, K., Ozawa, T. (1992). Human platelet-derived transforming growth factor-beta stimulates synthesis of glycosaminoglycans in cultured porcine aortic endothelial cells. Gerontology 38, 36–42.PubMedCrossRefGoogle Scholar
  40. Kuhn, H.G., Winkler, J., Kempermann, G. Thal, L.J., Gage, F.H. (1997). Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17, 5820–5827.PubMedGoogle Scholar
  41. Lamanna, W.C., Baldwin, R.J., Padva, M., Kalus, I., Ten Dam, G., van Kuppevelt, T.H., Gallagher, J.T., von Figura, K., Dierks, T., Merry, C.L. (2006). Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity. Biochem. J. 400, 63–73.PubMedCrossRefGoogle Scholar
  42. Langsdorf, A., Do, A.T., Kusche-Gullberg, M., Emerson, C.P. Jr, Ai, X. (2007). Sulfs are regulators of growth factor signaling for satellite cell differentiation and muscle regeneration. Dev. Biol. 311:2, 464–477.Google Scholar
  43. Lim, D., Tramontin, A., Trevejo, J., Herrera, D., Garcia-Verdugi, J., Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713–726.PubMedCrossRefGoogle Scholar
  44. Lindahl, U., Kusche-Gullberg, M., Kjellen, L. (1998). Regulated diversity of heparan sulfate. J. Biol. Chem. 273:29, 24979–24982.PubMedCrossRefGoogle Scholar
  45. Litwack, E.D., Ivins, J.K., Kumbasor, A., Paine-Saunolers, S., Stipp, C.S., Lanoler, A.D. (1998). Expression of the heparan sulfate proteoglycon glypicon-1 in the developing rodent. Dev. Dyn. 211, 72–87.PubMedCrossRefGoogle Scholar
  46. Lois, C., Alvarez-Buylla, A. (1994). Long distance neuronal migration in the adult mammalian brain. Science 264, 1145–1148.PubMedCrossRefGoogle Scholar
  47. Lortat-Jacob, H., Grimaud, J.A. (1991). Interferon-gamma C-terminal function: networking hypothesis. Heparan sulfate and heparin, new targets for IFNGamma, protect, relax the cytokine and regulate its activity. Cell Mol. Biol. 37:3, 253–260.PubMedGoogle Scholar
  48. Mandelbrot, B.B. (ed) (1983). The fractal geometry of nature. Freeman, San FranciscoGoogle Scholar
  49. Martens, D.J., Seaber, R.M., van der Kooy, D. (2002). In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the proliferation of neural progenitors around the fourth ventricle and the central canal of the spinal cord. Eur. J. Neurosci. 16, 1045–1057.PubMedCrossRefGoogle Scholar
  50. Mercier, F. (2004). Astroglia as a modulation interface between meninges and neurons. In: Hatton, G.I., Parpura, V. (eds) Glial/neuronal signaling. Amsterdam, Kluwer Pub, 125–162.Google Scholar
  51. Mercier, F., Hatton, G.I. (2000). Immunocytochemical basis for a meningeo-glial network. J. Comp. Neurol. 420, 445–465.PubMedCrossRefGoogle Scholar
  52. Mercier, F., Hatton, G.I. (2001). Connexin 26 and bFGF are primarily expressed in subpial and subependymal layers in adult brain parenchyma: roles in stem cell proliferation and morphological plasticity? J. Comp. Neurol. 431, 88–104.PubMedCrossRefGoogle Scholar
  53. Mercier, F., Hatton, G.I. (2004). Meninges and perivasculature as mediators of CNS plasticity. In: Bittar, E.E., Hertz, L. (eds.) Non-neuronal cells in the nervous system: function and dysfunction. Elsevier Bioscience, Amsterdam, Adv. Mol. Cell. Biol. 31, 215–253.Google Scholar
  54. Mercier, F., Kitasako, J.T., Hatton, G.I. (2002). Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 451, 170–188.PubMedCrossRefGoogle Scholar
  55. Mercier, F., Kitasako, J.T., Hatton, G.I. (2003). Fractones and other basal laminae in the hypothalamus. J. Comp. Neurol. 455, 324–340.PubMedCrossRefGoogle Scholar
  56. Mohammadi, M., Olsen, S.K., Ibrahimi, O.A. (2005). Structural basis for fibroblast receptor activation. Cyt. Growth Fact. Rev. 16, 107–137.PubMedCrossRefGoogle Scholar
  57. Monje, M.L., Toda, H., Palmer, T.D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Science, 302, 1760–1765.PubMedCrossRefGoogle Scholar
  58. Mulloy, B., Forster, M.J., Jones, C., Drake, A.F., Johnson, E.A., Davies, D.B. (1994). The effect of variation of substitution on the solution conformation of heparin: a spectroscopic and molecular modelling study. Carbohydr. Res. 255, 1–26.PubMedCrossRefGoogle Scholar
  59. Nakato, H., Kimata, K. (2002). Heparan sulfate fine structure and specificity of proteoglycan functions. Biochim. Biophys. Acta 1573:3, 312–318.PubMedCrossRefGoogle Scholar
  60. Narita, K., Chien, J., Mullany, S.A., Staub, J., Qian, X., Lingle, W.L., Shridhar, V. (2007). Loss of HSulf-1 expression enhances autocrine signaling mediated by amphiregulin in breast cancer. J Biol. Chem. 282:19, 14413–14420.PubMedCrossRefGoogle Scholar
  61. Nawroth, R., Zante, A., Cervantes, S., McManus, M., Helbrok, M., Rosen, S. (2007). Extracellular sulfatases, elements of the WNT signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS One 2:4, 1–11.Google Scholar
  62. Ornitz, D.M., Yayon, A., Flanagan, J.G., Svahn, C.M., Levi, E., Leder, P. (1992). Heparin is required for cell-free binding of basic fibroblastic growth factor to a soluble receptor and for mitogenesis in whole cells. Mol. Cell. Biol. 12, 240–247.PubMedGoogle Scholar
  63. Paine-Saunders, S., Vivano, B., Economides, A., Saunders, S. (2002). Heparan sulfate proteoglycans retain noggins at the cell surface: a potential mechanism for shaping bone morphogenic protein gradients. J. Biol. Chem. 277, 2089–2096.PubMedCrossRefGoogle Scholar
  64. Palmer, T.D., Ray, J., Gage, F.H. (1995). FGF-2 responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci. 6, 474–486.PubMedCrossRefGoogle Scholar
  65. Palmer, T.D., Willhoite, A.R., Gage, F.H. (2000). Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479–494.PubMedCrossRefGoogle Scholar
  66. Pencea, V., Bingaman, K.D., Wiegand, S.J., Luskin, M.B. (2001). Infusion of brain derived neurotrophic growth factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J. Neurosci. 21, 6706–6717.PubMedGoogle Scholar
  67. Proia, P., Schiera, G., Mineo, M., Ingrassia, A.M., Santoro, G., Savettieri, G., Di Liegro, I. (2008). Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor. Int. J. Mol. Med. 21, 63–67.PubMedGoogle Scholar
  68. Properzi, F., Lin, R., Kwok, J., Naidu, M., Van Kuppevelt, T., Dam, G., Camargo, L., Raha-Chowdhury, R., Furukawa, Y., Mikami, T., Sugahara, K. (2008). Heparan sulphate proteoglycan in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur. J. Neurosci. 27, 593–604.Google Scholar
  69. Rapraeger, A. (1995). In the clutches of proteoglycans: how does heparan sulfate regulate FGF binding. Chem. Biol. 2, 137–144.CrossRefGoogle Scholar
  70. Reiland, J., Rapraeger, A.C. (1993). Heparan sulfate protoglycan and FGF receptor target basic FGF to different intracellular destinations. J. Cell Sci. 105, 1085–1093.PubMedGoogle Scholar
  71. Rider, C.C. (2006). Heparin/heparan sulphate binding in the TGF-beta cytokine super family. Biochem. Soc. Trans. 34, 458–460.PubMedCrossRefGoogle Scholar
  72. Roberts, R., Gallagher, J., Spooncer, E., Allen, T.D., Bloomfield, F., Dexter, T.M. (1988). Heparan sulfate bond growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature 332, 376–378.CrossRefGoogle Scholar
  73. Sakaguchi, K., Lorenzi, M.V., Bottaro, D.P., Miki, T. (1999). The acidic domain and first immunoglobulin-like loop of fibroblast growth factor receptor 2 modulate downstream signaling through glycosaminoglycan modification. Mol. Cell. Biol. 19, 6754–6764.PubMedGoogle Scholar
  74. Saksela, O., Moscatelli, D., Sommer, A., Rifkin, D.B. (1988). Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell Biol. 107:2, 743–51.PubMedCrossRefGoogle Scholar
  75. Sawamoto, K., Wichterle, H., Gonzalez-Perez, O., Choifin, J.A., Yamada, M., Spassky, N., Murcia, N.S., Garcia-Verdugo, J.M., Marin, O., Rubenstein, J.L.M., Tessier-Lavigne, M., Okano, H., Alvarez-Buylla, A. (2006). New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311, 626–632.CrossRefGoogle Scholar
  76. Seaberg, R.M., van der Kooy, D. (2002). Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22, 1784–1793.PubMedGoogle Scholar
  77. Seki, T., Array, Y. (1993). Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci. 13, 2351–2358.PubMedGoogle Scholar
  78. Seri, B., Herrera, D.G., Gritti, A., Ferron, S., Collado, L., Vescovi, A., Garcia-Verdugo, J.M., Alvarez-Buylla, A. (2006). Composition and organization of the SCZ: a large germinal layer containing neural stem cells in the adult mammalian brain. Cereb. Cortex 16, 103–111.CrossRefGoogle Scholar
  79. Sharma, B., Iozzo, R. (1998). Transcriptional silencing of perlecan gene expression by interferon. J. Biol. Chem. 273, 4642–4646.PubMedCrossRefGoogle Scholar
  80. Smits, N.C., Robbesom, A.A., Versteeg, E.M., van de Westerlo, E.M., Dekhuijzen, P.N., van Kuppevelt, T.H. (2004). Heterogeneity of heparan sulfates in human lung. Am. J. Respir. Cell Mol. Biol. 30, 166–173.PubMedCrossRefGoogle Scholar
  81. Stopa, E.G., Berzin, T.M., Kim, S., Song, P., Kuo-Leblanc, V., Rodriguez-Wolf, M., Baird, A., Johanson, C.E. (2001). Choroid plexus growth factors: what are the implications for CSF dynamics in Alzheimer’s disease? Exp. Neurol. 167, 40–47.PubMedCrossRefGoogle Scholar
  82. Stringer, S., Gallagher, J. (1997). Heparan sulfate. Int. J. Biochem. Cell Biol. 29:5, 709–714.PubMedCrossRefGoogle Scholar
  83. Unger, E., Pettersson, I., Eriksson, U.J., Lindahl, U., Kjellén, L. (1991). Decreased activity of the heparan sulfate-modifying enzyme glucosaminyl N-deacetylase in hepatocytes from streptozotocin-diabetic rats. J. Biol. Chem. 266:14, 43–961.Google Scholar
  84. Venkataraman, G., Sasisekharan, V., Herr, A.B., Ornitz, D.M., Waksman, G., Cooney, C.L., Langer, R., Sasisekharan, R. (1996). Preferential self-association of basic fibroblastic growth factor is stabilized by heparin during receptor dimerization and activation. Proc. Natl. Acad. Sci. USA 93, 845–890.PubMedCrossRefGoogle Scholar
  85. Vlodavsky, I., Korner, G., Ishai-Michaeli, R., Bashkin, P., Bar-Shavit, R., Fuks, Z. (1990). Extracellular matrix-resident growth factors and enzymes: possible involvement in tumor metastasis and angiogenesis. Cancer Metastasis Rev. 32:3, 313–318Google Scholar
  86. Walker, A., Turnbul, J., Gallagher, J. (1994). Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor. J. Biol. Chem. 269:2, 931–935.PubMedGoogle Scholar
  87. Weiss, S., Dunne, C., Hewson, J. (1996). Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16, 7599–7609.PubMedGoogle Scholar
  88. Westling, C., Lindahl, U. (2002). Location of N-unsubstituted glucosamine residues in heparan sulfate. J. Biol. Chem. 277:51, 49247–49255.PubMedCrossRefGoogle Scholar
  89. Wexler, E.M., Geschwind, D.H., Palmer, T.D. (2007). Lithium regulates adult hippocampal progenitor development through canonical wnt pathway activation. Mol. Psychiatr. 13:285–292.CrossRefGoogle Scholar
  90. Whitelock, J., Murdoch, A., Iozzo, R., Underwood, A. (1996). The degradation of human endothelial cell-derived perlecan and release of bound basis fibroblast growth factor by stromelysin collagenase, plasmin, and heparanases. J. Biol. Chem. 271:17, 10079–10086.Google Scholar
  91. Wieseler-Frank, J., Jekich, B.M., Mahoney, J.H., Bland, S.T., Maier, S.F., Watkins, L.R. (2007). A novel immune to CNS communication pathway: cells of the meninges surrounding the spinal cord CSF space produce proinflammatory cytokines in response to an inflammatory cytokine. Brain Behav. Immun. 21, 711–718.PubMedCrossRefGoogle Scholar
  92. Wurmser, H.M, Palmer, T.D., Gage, F.H. (2004). Neuroscience-Cellular interactions in the stem cell niches. Science 304, 1253–1255.CrossRefGoogle Scholar
  93. Yang, W.D., Gomes, R.R. Jr, Alicknavitch, M., Farach-Carson, M.C., Carson, D.D. (2005). Perlecan domain I promotes fibroblast growth factor 2 delivery in collagen I fibril scaffolds. Tissue Eng. 11:1–2, 76–89.PubMedCrossRefGoogle Scholar
  94. Yayon, A., Klagsbrun, M., Esko, J.D., Leder, P., Ornitz, D.P. (1991). Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841–848.PubMedCrossRefGoogle Scholar
  95. Yurchenko, P.D., Schyttny, J.C. (1990). Molecular architecture of basement membranes. FASEB J. 4, 1577–1590.Google Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Frederic Mercier
    • 1
  • Jason Schnack
    • 1
  • Maureen Saint Georges Chaumet
    • 1
  1. 1.Department of Tropical MedicineMedical Microbiology and Pharmacology, John A, Burns School of Medicine, University of HawaiiHonoluluUSA

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