Structural and functional analysis of chondroitin sulfate proteoglycans in the neural stem cell niche

Methods in Enzymology

Volumn 479, Issue C, 2010, Pages 37-71

  Sirko, Swetlana ^a   Akita, Kaoru ^b   Von Holst, Alexander ^c   Faissner, Andreas ^c  

^a UNIVERSITY OF MUNICH   (Germany)

^b KYOTO SANGYO UNIVERSITY   (Japan)

^c RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; TENASCIN;

ANIMAL TISSUE; BOOK; CELL DENSITY; CELL PROLIFERATION; EMBRYO; EXTRACELLULAR MATRIX; IN SITU HYBRIDIZATION; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN FUNCTION; STRUCTURE ACTIVITY RELATION; SULFATION;

EID: 77956220669     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0076-6879(10)79003-0     Document Type: Chapter

References (83)

1. Akita K., von Holst A., Furukawa Y., Mikami T., Sugahara K., Faissner A. Expression of multiple chondroitin/dermatan sulfotransferases in the neurogenic regions of the embryonic and adult central nervous system implies that complex chondroitin sulfates have a role in neural stem cell maintenance. Stem Cells 2008, 26:798-809.
2. Alvarez-Buylla A., Lim D.A. For the long run: Maintaining germinal niches in the adult brain. Neuron 2004, 41:683-686.
3. Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2001, 2:287-293.
4. Anthony T.E., Klein C., Fishell G., Heintz N. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 2004, 41:881-890.
5. Bandtlow C.E., Zimmermann D.R. Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol. Rev. 2000, 80:1267-1290.
6. Bao X., Mikami T., Yamada S., Faissner A., Muramatsu T., Sugahara K. Heparin-binding growth factor, pleiotrophin, mediates neuritogenic activity of embryonic pig brain-derived chondroitin sulfate/dermatan sulfate hybrid chains. J. Biol. Chem. 2005, 280:9180-9191.
7. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., Gallo V. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 2003, 161:169-186.
8. Bernreuther C., Dihne M., Johann V., Schiefer J., Cui Y., Hargus G., Schmid J.S., Xu J., Kosinski C.M., Schachner M. Neural cell adhesion molecule L1-transfected embryonic stem cells promote functional recovery after excitotoxic lesion of the mouse striatum. J. Neurosci. 2006, 26:11532-11539.
9. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
10. Busch S.A., Silver J. The role of extracellular matrix in CNS regeneration. Curr. Opin. Neurobiol. 2007, 17:120-127.
11. Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002, 35:865-875.
12. Carulli D., Laabs T., Geller H.M., Fawcett J.W. Chondroitin sulfate proteoglycans in neural development and regeneration. Curr. Opin. Neurobiol. 2005, 15:116-120.
13. Chanas-Sacre G., Thiry M., Pirard S., Rogister B., Moonen G., Mbebi C., Verdiere-Sahuque M., Leprince P. A 295-kDA intermediate filament-associated protein in radial glia and developing muscle cells in vivo and in vitro. Dev. Dyn. 2000, 219:514-525.
14. Chen J., Bernreuther C., Dihne M., Schachner M. Cell adhesion molecule l1-transfected embryonic stem cells with enhanced survival support regrowth of corticospinal tract axons in mice after spinal cord injury. J. Neurotrauma 2005, 22:896-906.
15. Clement A.M., Nadanaka S., Masayama K., Mandl C., Sugahara K., Faissner A. The DSD-1 carbohydrate epitope depends on sulfation, correlates with chondroitin sulfate D motifs, and is sufficient to promote neurite outgrowth. J. Biol. Chem. 1998, 273:28444-28453.
16. Colognato H., ffrench-Constant C., Feltri M.L. Human diseases reveal novel roles for neural laminins. Trends Neurosci. 2005, 28:480-486.
17. Czopka T., Von Holst A., Schmidt G., Ffrench-Constant C., Faissner A. Tenascin C and tenascin R similarly prevent the formation of myelin membranes in a RhoA-dependent manner, but antagonistically regulate the expression of myelin basic protein via a separate pathway. Glia 2009, 57:1790-1801.
18. Dobbertin A., Rhodes K.E., Garwood J., Properzi F., Heck N., Rogers J.H., Fawcett J.W., Faissner A. Regulation of RPTPbeta/phosphacan expression and glycosaminoglycan epitopes in injured brain and cytokine-treated glia. Mol. Cell. Neurosci. 2003, 24:951-971.
19. Doetsch F. The glial identity of neural stem cells. Nat. Neurosci. 2003, 6:1127-1134.
20. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716.
21. Evers M.R., Xia G., Kang H.G., Schachner M., Baenziger J.U. Molecular cloning and characterization of a dermatan-specific N-acetylgalactosamine 4-O-sulfotransferase. J. Biol. Chem. 2001, 276:36344-36353.
22. Faissner A., Clement A., Lochter A., Streit A., Mandl C., Schachner M. Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J. Cell Biol. 1994, 126:783-799.
23. Feng L., Hatten M.E., Heintz N. Brain lipid-binding protein (BLBP): A novel signaling system in the developing mammalian CNS. Neuron 1994, 12:895-908.
24. Fitch M.T., Silver J. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 2008, 209:294-301.
25. Fukuta M., Uchimura K., Nakashima K., Kato M., Kimata K., Shinomura T., Habuchi O. Molecular cloning and expression of chick chondrocyte chondroitin 6-sulfotransferase. J. Biol. Chem. 1995, 270:18575-18580.
26. Garcion E., Faissner A., ffrench-Constant C. Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 2001, 128:2485-2496.
27. Garcion E., Halilagic A., Faissner A., ffrench-Constant C. Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development 2004, 131:3423-3432.
28. Garwood J., Schnadelbach O., Clement A., Schutte K., Bach A., Faissner A. DSD-1-proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J. Neurosci. 1999, 19:3888-3899.
29. Garwood J., Rigato F., Heck N., Faissner A. Tenascin glycoproteins and the complementary ligand DSD-1-PG/ phosphacan-structuring the neural extracellular matrix during development and repair. Restor. Neurol. Neurosci. 2001, 19:51-64.
30. Garwood J., Garcion E., Dobbertin A., Heck N., Calco V., ffrench-Constant C., Faissner A. The extracellular matrix glycoprotein Tenascin-C is expressed by oligodendrocyte precursor cells and required for the regulation of maturation rate, survival and responsiveness to platelet-derived growth factor. Eur. J. Neurosci. 2004, 20:2524-2540.
31. Gates M.A., Thomas L.B., Howard E.M., Laywell E.D., Sajin B., Faissner A., Gotz B., Silver J., Steindler D.A. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J. Comp. Neurol. 1995, 361:249-266.
32. Gotz M., Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:777-788.
33. Habuchi H., Tanaka M., Habuchi O., Yoshida K., Suzuki H., Ban K., Kimata K. The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J. Biol. Chem. 2000, 275:2859-2868.
34. Hartfuss E., Galli R., Heins N., Gotz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 2001, 229:15-30.
35. Hikino M., Mikami T., Faissner A., Vilela-Silva A.C., Pavao M.S., Sugahara K. Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: Implications of dermatan sulfate in neuritogenesis in the brain. J. Biol. Chem. 2003, 278:43744-43754.
36. Hiraoka N., Nakagawa H., Ong E., Akama T.O., Fukuda M.N., Fukuda M. Molecular cloning and expression of two distinct human chondroitin 4-O-sulfotransferases that belong to the HNK-1 sulfotransferase gene family. J. Biol. Chem. 2000, 275:20188-20196.
37. Houle J.D., Tom V.J., Mayes D., Wagoner G., Phillips N., Silver J. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 2006, 26:7405-7415.
38. Ida M., Shuo T., Hirano K., Tokita Y., Nakanishi K., Matsui F., Aono S., Fujita H., Fujiwara Y., Kaji T., Oohira A. Identification and functions of chondroitin sulfate in the milieu of neural stem cells. J. Biol. Chem. 2006, 281:5982-5991.
39. Ito Y., Hikino M., Yajima Y., Mikami T., Sirko S., von Holst A., Faissner A., Fukui S., Sugahara K. Structural characterization of the epitopes of the monoclonal antibodies 473HD, CS-56, and MO-225 specific for chondroitin sulfate d-type using the oligosaccharide library. Glycobiology 2005, 15:593-603.
40. Kabos P., Matundan H., Zandian M., Bertolotto C., Robinson M.L., Davy B.E., Yu J.S., Krueger R.C. Neural precursors express multiple chondroitin sulfate proteoglycans, including the lectican family. Biochem. Biophys. Res. Commun. 2004, 318:955-963.
41. Kang H.G., Evers M.R., Xia G., Baenziger J.U., Schachner M. Molecular cloning and characterization of chondroitin-4-O-sulfotransferase-3. A novel member of the HNK-1 family of sulfotransferases. J. Biol. Chem. 2002, 277:34766-34772.
42. Kim M., Morshead C.M. Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J. Neurosci. 2003, 23:10703-10709.
43. Kitagawa H., Tsutsumi K., Tone Y., Sugahara K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 1997, 272:31377-31381.
44. Kitagawa H., Fujita M., Ito N., Sugahara K. Molecular cloning and expression of a novel chondroitin 6-O-sulfotransferase. J. Biol. Chem. 2000, 275:21075-21080.
45. Kobayashi M., Sugumaran G., Liu J., Shworak N.W., Silbert J.E., Rosenberg R.D. Molecular cloning and characterization of a human uronyl 2-sulfotransferase that sulfates iduronyl and glucuronyl residues in dermatan/chondroitin sulfate. J. Biol. Chem. 1999, 274:10474-10480.
46. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
47. Kusche-Gullberg M., Kjellen L. Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 2003, 13:605-611.
48. Leone D.P., Relvas J.B., Campos L.S., Hemmi S., Brakebusch C., Fassler R., ffrench-Constant C., Suter U. Regulation of neural progenitor proliferation and survival by beta1 integrins. J. Cell Sci. 2005, 118:2589-2599.
49. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 2000, 28:713-726.
50. Louis S.A., Rietze R.L., Deleyrolle L., Wagey R.E., Thomas T.E., Eaves A.C., Reynolds B.A. Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 2008, 26:988-996.
51. Malatesta P., Hartfuss E., Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000, 127:5253-5263.
52. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., Gotz M. Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 2003, 37:751-764.
53. Marshall G.P., Reynolds B.A., Laywell E.D. Using the neurosphere assay to quantify neural stem cells in vivo. Curr. Pharm. Biotechnol. 2007, 8:141-145. 2nd.
54. Massey J.M., Amps J., Viapiano M.S., Matthews R.T., Wagoner M.R., Whitaker C.M., Alilain W., Yonkof A.L., Khalyfa A., Cooper N.G., Silver J., Onifer S.M. Increased chondroitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3. Exp. Neurol. 2008, 209:426-445.
55. Mikami T., Mizumoto S., Kago N., Kitagawa H., Sugahara K. Specificities of three distinct human chondroitin/dermatan N-acetylgalactosamine 4-O-sulfotransferases demonstrated using partially desulfated dermatan sulfate as an acceptor: Implication of differential roles in dermatan sulfate biosynthesis. J. Biol. Chem. 2003, 278:36115-36127.
56. Miyata T., Kawaguchi A., Okano H., Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001, 31:727-741.
57. Moritz S., Lehmann S., Faissner A., von Holst A. An induction gene trap screen in neural stem cells reveals an instructive function of the niche and identifies the splicing regulator sam68 as a tenascin-C-regulated target gene. Stem Cells 2008, 26:2321-2331.
58. Nadanaka S., Clement A., Masayama K., Faissner A., Sugahara K. Characteristic hexasaccharide sequences in octasaccharides derived from shark cartilage chondroitin sulfate D with a neurite outgrowth promoting activity. J. Biol. Chem. 1998, 273:3296-3307.
59. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409:714-720.
60. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 2002, 22:3161-3173.
61. Ohtake S., Ito Y., Fukuta M., Habuchi O. Human N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase cDNA is related to human B cell recombination activating gene-associated gene. J. Biol. Chem. 2001, 276:43894-43900.
62. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298:1248-1251.
63. Properzi F., Carulli D., Asher R.A., Muir E., Camargo L.M., van Kuppevelt T.H., ten Dam G.B., Furukawa Y., Mikami T., Sugahara K., Toida T., Geller H.M., et al. Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia. Eur. J. Neurosci. 2005, 21:378-390.
64. Pruszak J., Ludwig W., Blak A., Alavian K., Isacson O. CD15, CD24, and CD29 define a surface biomarker code for neural lineage differentiation of stem cells. Stem Cells 2009, 27:2928-2940.
65. Rietze R.L., Valcanis H., Brooker G.F., Thomas T., Voss A.K., Bartlett P.F. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 2001, 412:736-739.
66. Rougon G., Dubois C., Buckley N., Magnani J.L., Zollinger W. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol. 1986, 103:2429-2437.
67. Scadden D.T. The stem-cell niche as an entity of action. Nature 2006, 441:1075-1079.
68. Shibata T., Yamada K., Watanabe M., Ikenaka K., Wada K., Tanaka K., Inoue Y. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J. Neurosci. 1997, 17:9212-9219.
69. Shihabuddin L.S., Horner P.J., Ray J., Gage F.H. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci. 2000, 20:8727-8735.
70. Silbert J.E., Sugumaran G. Biosynthesis of chondroitin/dermatan sulfate. IUBMB Life 2002, 54:177-186.
71. Sirko S., von Holst A., Wizenmann A., Gotz M., Faissner A. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 2007, 134:2727-2738.
72. Sirko S., Neitz A., Mittmann T., Horvat-Brocker A., von Holst A., Eysel U.T., Faissner A. Focal laser-lesions activate an endogenous population of neural stem/progenitor cells in the adult visual cortex. Brain 2009, 132:2252-2264.
73. Sirko S., von Holst A., Weber A., Wizenmann A., Theocharidis U., Gotz M., Faissner A. Chondroitin sulfates are required for FGF-2-dependent proliferation and maintenance in neural stem cells and for EGF-dependent migration of their progeny. Stem Cells 2010, 28(4):775-787.
74. Sommer I., Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: An immunocytological study in the central nervous system. Dev. Biol. 1981, 83:311-327.
75. Streit A., Yuen C.T., Loveless R.W., Lawson A.M., Finne J., Schmitz B., Feizi T., Stern C.D. The Le(x) carbohydrate sequence is recognized by antibody to L5, a functional antigen in early neural development. J. Neurochem. 1996, 66:834-844.
76. Temple S. The development of neural stem cells. Nature 2001, 414:112-117.
77. Ueoka C., Kaneda N., Okazaki I., Nadanaka S., Muramatsu T., Sugahara K. Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate E. Structural ans functional implications of the over-sulfated chondroitin sulfate. J. Biol. Chem. 2000, 275:37407-37413.
78. von Holst A., Rohrer H. Culture of avian sympathetic neurons. Curr. Top. Dev. Biol. 1998, 36:161-182.
79. von Holst A., Sirko S., Faissner A. The unique 473HD-chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J. Neurosci. 2006, 26:4082-4094.
80. von Holst A., Egbers U., Prochiantz A., Faissner A. Neural stem/progenitor cells express 20 tenascin C isoforms that are differentially regulated by Pax6. J. Biol. Chem. 2007, 282:9172-9181.
81. Wodarz A., Huttner W.B. Asymmetric cell division during neurogenesis in Drosophila and vertebrates. Mech. Dev. 2003, 120:1297-1309.
82. Yamauchi S., Mita S., Matsubara T., Fukuta M., Habuchi H., Kimata K., Habuchi O. Molecular cloning and expression of chondroitin 4-sulfotransferase. J. Biol. Chem. 2000, 275:8975-8981.
83. Zou P., Zou K., Muramatsu H., Ichihara-Tanaka K., Habuchi O., Ohtake S., Ikematsu S., Sakuma S., Muramatsu T. Glycosaminoglycan structures required for strong binding to midkine, a heparin-binding growth factor. Glycobiology 2003, 13:35-42.