Regulation of the neural stem cell compartment by extracellular matrix constituents

Progress in Brain Research

Volumn 214, Issue , 2014, Pages 3-28

  Theocharidis, Ursula ^a   Long, Katherine ^b   ffrench Constant, Charles ^b   Faissner, Andreas ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Asymmetrical division; Extracellular matrix; Glial progenitors; Integrins; Laminin; Neural stem cell niche; Phosphacan; Proteoglycans; Radial glial cells; Subventricular zone; Tenascin

Indexed keywords

LAMININ; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; TENASCIN;

ARTICLE; ASTROCYTE; ASYMMETRIC CELL DIVISION; CELL COMPARTMENTALIZATION; EXTRACELLULAR MATRIX; GENE CONTROL; GLIA; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 84922333935     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-63486-3.00001-3     Document Type: Chapter

References (157)

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. Alam N., Goel H.L., Zarif M.J., Butterfield J.E., Perkins H.M., Sansoucy B.G., Sawyer T.K., Languino L.R. The integrin-growth factor receptor duet. J. Cell. Physiol. 2007, 213:649-653.
3. Alpy F., Jivkov I., Sorokin L., Klein A., Arnold C., Huss Y., Kedinger M., Simon-Assmann P., Lefebvre O. Generation of a conditionally null allele of the laminin alpha1 gene. Genesis 2005, 43:59-70.
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. Arora N., Mainali D., Smith E.A. Unraveling the role of membrane proteins Notch, Pvr, and EGFR in altering integrin diffusion and clustering. Anal. Bioanal. Chem. 2012, 404:2339-2348.
6. Aumailley M., Bruckner-Tuderman L., Carter W.G., Deutzmann R., Edgar D., Ekblom P., Engel J., Engvall E., Hohenester E., Jones J.C., Kleinman H.K., Marinkovich M.P., Martin G.R., Mayer U., Meneguzzi G., Miner J.H., Miyazaki K., Patarroyo M., Paulsson M., Quaranta V., Sanes J.R., Sasaki T., Sekiguchi K., Sorokin L.M., Talts J.F., Tryggvason K., Uitto J., Virtanen I., von der Mark K., Wewer U.M., Yamada Y., Yurchenco P.D. A simplified laminin nomenclature. Matrix Biol. 2005, 24:326-332.
7. Bandtlow C.E., Zimmermann D.R. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 2000, 80:1267-1290.
8. Barros C.S., Franco S.J., Muller U. Extracellular matrix: functions in the nervous system. Cold Spring Harb. Persp. Biol. 2011, 3. a005108.
9. Baumgartner S., Martin D., Hagios C., Chiquet-Ehrismann R. Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene. EMBO J. 1994, 13:3728-3740.
10. Blaschuk K.L., Frost E.E., ffrench-Constant C. The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins. Development 2000, 127:1961-1969.
11. Briata P., Ilengo C., Bobola N., Corte G. Binding properties of the human homeodomain protein OTX2 to a DNA target sequence. FEBS Lett. 1999, 445:160-164.
12. Brizzi M.F., Tarone G., Defilippi P. Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr. Opin. Cell Biol. 2012, 24:645-651.
13. Buttery P.C., ffrench-Constant C. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol. Cell. Neurosci. 1999, 14:199-212.
14. Camara J., Wang Z., Nunes-Fonseca C., Friedman H.C., Grove M., Sherman D.L., Komiyama N.H., Grant S.G., Brophy P.J., Peterson A., ffrench-Constant C. Integrin-mediated axoglial interactions initiate myelination in the central nervous system. J. Cell Biol. 2009, 185:699-712.
15. Campos L.S., Leone D.P., Relvas J.B., Brakebusch C., Fassler R., Suter U., ffrench-Constant C. Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 2004, 131:3433-3444.
16. Campos L.S., Decker L., Taylor V., Skarnes W. Notch, epidermal growth factor receptor, and beta1-integrin pathways are coordinated in neural stem cells. J. Biol. Chem. 2006, 281:5300-5309.
17. Chiquet-Ehrismann R., Tucker R.P. Tenascins and the importance of adhesion modulation. Cold Spring Harb. Persp. Biol. 2011, 3. pii: a004960.
18. Chun S.J., Rasband M.N., Sidman R.L., Habib A.A., Vartanian T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J. Cell Biol. 2003, 163:397-408.
19. 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.
20. Colognato H., Ramachandrappa S., Olsen I.M., ffrench-Constant C. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J. Cell Biol. 2004, 167:365-375.
21. Colognato H., Galvin J., Wang Z., Relucio J., Nguyen T., Harrison D., Yurchenco P.D., ffrench-Constant C. Identification of dystroglycan as a second laminin receptor in oligodendrocytes, with a role in myelination. Development 2007, 134:1723-1736.
22. Copertino D.W., Jenkinson S., Jones F.S., Edelman G.M. Structural and functional similarities between the promoters for mouse tenascin and chicken cytotactin. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:2131-2135.
23. Copertino D.W., Edelman G.M., Jones F.S. Multiple promoter elements differentially regulate the expression of the mouse tenascin gene. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1846-1851.
24. Couturier L., Mazouni K., Schweisguth F. Numb localizes at endosomes and controls the endosomal sorting of notch after asymmetric division in Drosophila. Curr. Biol. 2013, 23:588-593.
25. Craig A.M., Kang Y. Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol. 2007, 17:43-52.
26. 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.
27. Czopka T., von Holst A., ffrench-Constant C., Faissner A. Regulatory mechanisms that mediate tenascin C-dependent inhibition of oligodendrocyte precursor differentiation. J. Neurosci. 2010, 30:12310-12322.
28. Dityatev A., Seidenbecher C.I., Schachner M. Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci. 2010, 33:503-512.
29. Dobbertin A., Czvitkovich S., Theocharidis U., Garwood J., Andrews M.R., Properzi F., Lin R., Fawcett J.W., Faissner A. Analysis of combinatorial variability reveals selective accumulation of the fibronectin type III domains B and D of tenascin-C in injured brain. Exp. Neurol. 2010, 225:60-73.
30. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36:1021-1034.
31. Drago J., Nurcombe V., Bartlett P.F. Laminin through its long arm E8 fragment promotes the proliferation and differentiation of murine neuroepithelial cells in vitro. Exp. Cell Res. 1991, 192:256-265.
32. Eyermann C., Czaplinski K., Colognato H. Dystroglycan promotes filopodial formation and process branching in differentiating oligodendroglia. J. Neurochem. 2012, 120:928-947.
33. Faissner A. Glial derived extracellular matrix components: important roles in axon growth and guidance. Neuroscientist 1997, 3:371-380.
34. Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 1990, 5:627-637.
35. Faissner A., Steindler D. Boundaries and inhibitory molecules in developing neural tissues. Glia 1995, 13:233-254.
36. Faissner A., Heck N., Dobbertin A., Garwood J. DSD-1-proteoglycan/phosphacan and receptor protein tyrosine phosphatase-beta isoforms during development and regeneration of neural tissues. Adv. Exp. Med. Biol. 2006, 557:25-53.
37. Ffrench-Constant C., Raff M.C. Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature 1986, 319:499-502.
38. Fietz S.A., Huttner W.B. Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr. Opin. Neurobiol. 2011, 21:23-35.
39. Fietz S.A., Kelava I., Vogt J., Wilsch-Brauninger M., Stenzel D., Fish J.L., Corbeil D., Riehn A., Distler W., Nitsch R., Huttner W.B. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 2010, 13:690-699.
40. Fietz S.A., Lachmann R., Brandl H., Kircher M., Samusik N., Schroder R., Lakshmanaperumal N., Henry I., Vogt J., Riehn A., Distler W., Nitsch R., Enard W., Paabo S., Huttner W.B. Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:11836-11841.
41. Flanagan L.A., Lu J., Wang L., Marchenko S.A., Jeon N.L., Lee A.P., Monuki E.S. Unique dielectric properties distinguish stem cells and their differentiated progeny. Stem Cells 2008, 26:656-665.
42. Freeman M.R. Specification and morphogenesis of astrocytes. Science 2010, 330:774-778.
43. Galvin J., Eyermann C., Colognato H. Dystroglycan modulates the ability of insulin-like growth factor-1 to promote oligodendrocyte differentiation. J. Neurosci. Res. 2010, 88:3295-3307.
44. 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.
45. 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.
46. Gardiner N.J. Integrins and the extracellular matrix: key mediators of development and regeneration of the sensory nervous system. Dev. Neurobiol. 2011, 71:1054-1072.
47. Garthe A., Kempermann G. An old test for new neurons: refining the Morris water maze to study the functional relevance of adult hippocampal neurogenesis. Front. Neurosci. 2013, 7:63.
48. 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.
49. 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.
50. Garwood J., Theocharidis U., Calco V., Dobbertin A., Faissner A. Existence of tenascin-C isoforms in rat that contain the alternatively spliced AD1 domain are developmentally regulated during hippocampal development. Cell. Mol. Neurobiol. 2012, 32:279-287.
51. 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.
52. Gherzi R., Briata P., Boncinelli E., Ponassi M., Querze G., Viti F., Corte G., Zardi L. The human homeodomain protein OTX2 binds to the human tenascin-C promoter and trans-represses its activity in transfected cells. DNA Cell Biol. 1997, 16:559-567.
53. Gotz M., Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:777-788.
54. Gotz M., Stoykova A., Gruss P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 1998, 21:1031-1044.
55. Graus-Porta D., Blaess S., Senften M., Littlewood-Evans A., Damsky C., Huang Z., Orban P., Klein R., Schittny J.C., Muller U. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 2001, 31:367-379.
56. Halfter W., Dong S., Yip Y.P., Willem M., Mayer U. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 2002, 22:6029-6040.
57. Hall P.E., Lathia J.D., Miller N.G., Caldwell M.A., ffrench-Constant C. Integrins are markers of human neural stem cells. Stem Cells 2006, 24:2078-2084.
58. Hall P.E., Lathia J.D., Caldwell M.A., ffrench-Constant C. Laminin enhances the growth of human neural stem cells in defined culture media. BMC Neurosci. 2008, 9:71.
59. Hansen D.V., Lui J.H., Parker P.R., Kriegstein A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464:554-561.
60. Hartfuss E., Galli R., Heins N., Gotz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 2001, 229:15-30.
61. Hennen E., Faissner A. LewisX: a neural stem cell specific glycan?. Int. J. Biochem. Cell Biol. 2012, 44:830-833.
62. Hennen E., Czopka T., Faissner A. Structurally distinct LewisX glycans distinguish subpopulations of neural stem/progenitor cells. J. Biol. Chem. 2011, 286:16321-16331.
63. Holm P.C., Mader M.T., Haubst N., Wizenmann A., Sigvardsson M., Gotz M. Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Mol. Cell. Neurosci. 2007, 34:99-119.
64. Husmann K., Faissner A., Schachner M. Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J. Cell Biol. 1992, 116:1475-1486.
65. 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.
66. Ihrie R.A., Alvarez-Buylla A. Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 2011, 70:674-686.
67. Imbeault S., Gauvin L.G., Toeg H.D., Pettit A., Sorbara C.D., Migahed L., DesRoches R., Menzies A.S., Nishii K., Paul D.L., Simon A.M., Bennett S.A. The extracellular matrix controls gap junction protein expression and function in postnatal hippocampal neural progenitor cells. BMC Neurosci. 2009, 10:13.
68. 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.
69. Jankovski A., Sotelo C. Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J. Comp. Neurol. 1996, 371:376-396.
70. Joester A., Faissner A. Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. J. Biol. Chem. 1999, 274:17144-17151.
71. Joester A., Faissner A. The structure and function of tenascins in the nervous system. Matrix Biol. 2001, 20:13-22.
72. Jones F.S., Jones P.L. The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev. Dyn. 2000, 218:235-259.
73. Jones F.S., Crossin K.L., Cunningham B.A., Edelman G.M. Identification and characterization of the promoter for the cytotactin gene. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:6497-6501.
74. Jones F.S., Chalepakis G., Gruss P., Edelman G.M. Activation of the cytotactin promoter by the homeobox-containing gene Evx-1. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:2091-2095.
75. Jones F.S., Holst B.D., Minowa O., De Robertis E.M., Edelman G.M. Binding and transcriptional activation of the promoter for the neural cell adhesion molecule by HoxC6 (Hox-3.3). Proc. Natl. Acad. Sci. U. S. A. 1993, 90:6557-6561.
76. Jones F.S., Meech R., Edelman D.B., Oakey R.J., Jones P.L. Prx1 controls vascular smooth muscle cell proliferation and tenascin-C expression and is upregulated with Prx2 in pulmonary vascular disease. Circ. Res. 2001, 89:131-138.
77. 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.
78. Karus M., Denecke B., ffrench-Constant C., Wiese S., Faissner A. The extracellular matrix molecule tenascin C modulates expression levels and territories of key patterning genes during spinal cord astrocyte specification. Development 2011, 138:5321-5331.
79. Karus M., Samtleben S., Busse C., Tsai T., Dietzel I.D., Faissner A., Wiese S. Normal sulfation levels regulate spinal cord neural precursor cell proliferation and differentiation. Neural Dev. 2012, 7:20.
80. Kazanis I., ffrench-Constant C. Extracellular matrix and the neural stem cell niche. Dev. Neurobiol. 2011, 71:1006-1017.
81. Kazanis I., Belhadi A., Faissner A., ffrench-Constant C. The adult mouse subependymal zone regenerates efficiently in the absence of tenascin-C. J. Neurosci. 2007, 27:13991-13996.
82. Kazanis I., Lathia J.D., Vadakkan T.J., Raborn E., Wan R., Mughal M.R., Eckley D.M., Sasaki T., Patton B., Mattson M.P., Hirschi K.K., Dickinson M.E., ffrench-Constant C. Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J. Neurosci. 2010, 30:9771-9781.
83. Kempermann G., Jessberger S., Steiner B., Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004, 27:447-452.
84. Kerever A., Schnack J., Vellinga D., Ichikawa N., Moon C., Arikawa-Hirasawa E., Efird J.T., Mercier F. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 2007, 25:2146-2157.
85. Kiernan B.W., Garcion E., Ferguson J., Frost E.E., Torres E.M., Dunnett S.B., Saga Y., Aizawa S., Faissner A., Kaur R., Franklin R.J., ffrench-Constant C. Myelination and behaviour of tenascin-C null transgenic mice. Eur. J. Neurosci. 1999, 11:3082-3092.
86. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
87. Lamanna W.C., Frese M.A., Balleininger M., Dierks T. Sulf loss influences N-, 2-O-, and 6-O-sulfation of multiple heparan sulfate proteoglycans and modulates fibroblast growth factor signaling. J. Biol. Chem. 2008, 283:27724-27735.
88. Lamprianou S., Harroch S. Receptor protein tyrosine phosphatase from stem cells to mature glial cells of the central nervous system. J. Mol. Neurosci. 2006, 29:241-255.
89. Lancaster M.A., Renner M., Martin C.A., Wenzel D., Bicknell L.S., Hurles M.E., Homfray T., Penninger J.M., Jackson A.P., Knoblich J.A. Cerebral organoids model human brain development and microcephaly. Nature 2013, 501:373-379.
90. Lathia J.D., Patton B., Eckley D.M., Magnus T., Mughal M.R., Sasaki T., Caldwell M.A., Rao M.S., Mattson M.P., ffrench-Constant C. Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J. Comp. Neurol. 2007, 505:630-643.
91. Laursen L.S., Chan C.W., ffrench-Constant C. Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K. J. Cell Biol. 2011, 192:797-811.
92. Lee K.K., de Repentigny Y., Saulnier R., Rippstein P., Macklin W.B., Kothary R. Dominant-negative beta1 integrin mice have region-specific myelin defects accompanied by alterations in MAPK activity. Glia 2006, 53:836-844.
93. 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.
94. Licht T., Goshen I., Avital A., Kreisel T., Zubedat S., Eavri R., Segal M., Yirmiya R., Keshet E. Reversible modulations of neuronal plasticity by VEGF. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5081-5086.
95. Liesi P., Dahl D., Vaheri A. Laminin is produced by early rat astrocytes in primary culture. J. Cell Biol. 1983, 96:920-924.
96. Loulier K., Lathia J.D., Marthiens V., Relucio J., Mughal M.R., Tang S.C., Coksaygan T., Hall P.E., Chigurupati S., Patton B., Colognato H., Rao M.S., Mattson M.P., Haydar T.F., ffrench-Constant C. beta1 integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol. 2009, 7. e1000176.
97. Maeda N., Ishii M., Nishimura K., Kamimura K. Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem. Res. 2011, 36:1228-1240.
98. 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.
99. 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.
100. Meiners S., Marone M., Rittenhouse J.L., Geller H.M. Regulation of astrocytic tenascin by basic fibroblast growth factor. Dev. Biol. 1993, 160:480-493.
101. Mercier F., Kitasako J.T., Hatton G.I. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 2002, 451:170-188.
102. Mercier F., Cho Kwon Y., Kodama R. Meningeal/vascular alterations and loss of extracellular matrix in the neurogenic zone of adult BTBR T+ tf/J mice, animal model for autism. Neurosci. Lett. 2011, 498:173-178.
103. Merkle F.T., Alvarez-Buylla A. Neural stem cells in mammalian development. Curr. Opin. Cell Biol. 2006, 18:704-709.
104. Mettouchi A., Cabon F., Montreau N., Dejong V., Vernier P., Gherzi R., Mercier G., Binetruy B. The c-Jun-induced transformation process involves complex regulation of tenascin-C expression. Mol. Cell. Biol. 1997, 17:3202-3209.
105. Miner J.H., Cunningham J., Sanes J.R. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J. Cell Biol. 1998, 143:1713-1723.
106. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005, 28:223-250.
107. Ming G.L., Song H. Adult neurogenesis in the Mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
108. Mobley A.K., Tchaicha J.H., Shin J., Hossain M.G., McCarty J.H. Beta8 integrin regulates neurogenesis and neurovascular homeostasis in the adult brain. J. Cell Sci. 2009, 122:1842-1851.
109. Mohebiany A.N., Nikolaienko R.M., Bouyain S., Harroch S. Receptor-type tyrosine phosphatase ligands: looking for the needle in the haystack. FEBS J. 2013, 280:388-400.
110. 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.
111. Myshrall T.D., Moore S.A., Ostendorf A.P., Satz J.S., Kowalczyk T., Nguyen H., Daza R.A., Lau C., Campbell K.P., Hevner R.F. Dystroglycan on radial glia end feet is required for pial basement membrane integrity and columnar organization of the developing cerebral cortex. J. Neuropathol. Exp. Neurol. 2012, 71:1047-1063.
112. Nave K.A. Myelination and support of axonal integrity by glia. Nature 2010, 468:244-252.
113. Nishiyama A., Komitova M., Suzuki R., Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 2009, 10:9-22.
114. 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.
115. Noctor S.C., Martinez-Cerdeno V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 2004, 7:136-144.
116. Orend G., Chiquet-Ehrismann R. Tenascin-C induced signaling in cancer. Cancer Lett. 2006, 244:143-163.
117. Paridaen J.T., Wilsch-Brauninger M., Huttner W.B. Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 2013, 155:333-344.
118. Patel T., Zhou J., Piepmeier J.M., Saltzman W.M. Polymeric nanoparticles for drug delivery to the central nervous system. Adv. Drug Deliv. Rev. 2012, 64:701-705.
119. Pollard S.M., Conti L., Sun Y., Goffredo D., Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb. Cortex 2006, 16(Suppl 1):i112-i120.
120. Porcheri C., Suter U., Jessberger S. Dissecting integrin-dependent regulation of neural stem cell proliferation in the adult brain. J. Neurosci. 2014, 34:5222-5232.
121. Purushothaman A., Sugahara K., Faissner A. Chondroitin sulfate "wobble motifs" modulate maintenance and differentiation of neural stem cells and their progeny. J. Biol. Chem. 2012, 287:2935-2942.
122. Radakovits R., Barros C.S., Belvindrah R., Patton B., Muller U. Regulation of radial glial survival by signals from the meninges. J. Neurosci. 2009, 29:7694-7705.
123. Radner S., Banos C., Bachay G., Li Y.N., Hunter D.D., Brunken W.J., Yee K.T. beta2 and gamma3 laminins are critical cortical basement membrane components: ablation of Lamb2 and Lamc3 genes disrupts cortical lamination and produces dysplasia. Dev. Neurobiol. 2013, 73:209-229.
124. Rakic P. The radial edifice of cortical architecture: from neuronal silhouettes to genetic engineering. Brain Res. Rev. 2007, 55:204-219.
125. Rallis C., Pinchin S.M., Ish-Horowicz D. Cell-autonomous integrin control of Wnt and Notch signalling during somitogenesis. Development 2010, 137:3591-3601.
126. Relucio J., Menezes M.J., Miyagoe-Suzuki Y., Takeda S., Colognato H. Laminin regulates postnatal oligodendrocyte production by promoting oligodendrocyte progenitor survival in the subventricular zone. Glia 2012, 60:1451-1467.
127. Rigato F., Garwood J., Calco V., Heck N., Faivre-Sarrailh C., Faissner A. Tenascin-C promotes neurite outgrowth of embryonic hippocampal neurons through the alternatively spliced fibronectin type III BD domains via activation of the cell adhesion molecule F3/contactin. J. Neurosci. 2002, 22:6596-6609.
128. Saghatelyan A., de Chevigny A., Schachner M., Lledo P.M. Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat. Neurosci. 2004, 7:347-356.
129. Sarrazin S., Lamanna W.C., Esko J.D. Heparan sulfate proteoglycans. Cold Spring Harb. Persp. Biol. 2011, 3. pii: a004952.
130. Satz J.S., Ostendorf A.P., Hou S., Turner A., Kusano H., Lee J.C., Turk R., Nguyen H., Ross-Barta S.E., Westra S., Hoshi T., Moore S.A., Campbell K.P. Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J. Neurosci. 2010, 30:14560-14572.
131. Scadden D.T. The stem-cell niche as an entity of action. Nature 2006, 441:1075-1079.
132. Schroder J.E., Tegeler M.R., Grosshans U., Porten E., Blank M., Lee J., Esapa C., Blake D.J., Kroger S. Dystroglycan regulates structure, proliferation and differentiation of neuroepithelial cells in the developing vertebrate CNS. Dev. Biol. 2007, 307:62-78.
133. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
134. 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.
135. Sirko S., Akita K., Von Holst A., Faissner A. Structural and functional analysis of chondroitin sulfate proteoglycans in the neural stem cell niche. Methods Enzymol. 2010, 479:37-71.
136. Sirko S., von Holst A., Weber A., Wizenmann A., Theocharidis U., Gotz M., Faissner A. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 2010, 28:775-787.
137. Stenzel D., Wilsch-Brauninger M., Wong F.K., Heuer H., Huttner W.B. Integrin alphavbeta3 and thyroid hormones promote expansion of progenitors in embryonic neocortex. Development 2014, 141:795-806.
138. Stoykova A., Gotz M., Gruss P., Price J. Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 1997, 124:3765-3777.
139. Sypecka J., Dragun-Szymczak P., Zalewska T., Domanska-Janik K. Laminin promotes oligogliogenesis and increases MMPs activity in human neural stem cells of HUCB-NSC line. Acta Neurobiol. Exp. (Wars) 2009, 69:37-45.
140. Theocharidis U., Faissner A. Analysis of alternatively spliced domains in multimodular gene products-the extracellular matrix glycoprotein tenascin C. Polymerase Chain Reaction 2012, 487-500. InTech Open Access Publisher, Rijeka, Croatia, (Chapter 23). P. Hernandez-Rodriguez (Ed.).
141. Trotter J., Karram K., Nishiyama A. NG2 cells: properties, progeny and origin. Brain Res. Rev. 2010, 63:72-82.
142. Tsuda S., Kitagawa T., Takashima S., Asakawa S., Shimizu N., Mitani H., Shima A., Tsutsumi M., Hori H., Naruse K., Ishikawa Y., Takeda H. FAK-mediated extracellular signals are essential for interkinetic nuclear migration and planar divisions in the neuroepithelium. J. Cell Sci. 2010, 123:484-496.
143. Tucker R.P., Drabikowski K., Hess J.F., Ferralli J., Chiquet-Ehrismann R., Adams J.C. Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage. BMC Evol. Biol. 2006, 6:60.
144. von Holst A. Tenascin C in stem cell niches: redundant, permissive or instructive?. Cells Tissues Organs 2008, 188:170-177.
145. 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.
146. 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.
147. Wehrle-Haller B., Chiquet M. Dual function of tenascin: simultaneous promotion of neurite growth and inhibition of glial migration. J. Cell Sci. 1993, 106(Pt 2):597-610.
148. Wright K.M., Lyon K.A., Leung H., Leahy D.J., Ma L., Ginty D.D. Dystroglycan organizes axon guidance cue localization and axonal pathfinding. Neuron 2012, 76:931-944.
149. Xu H., Yang Y., Tang X., Zhao M., Liang F., Xu P., Hou B., Xing Y., Bao X., Fan X. Bergmann glia function in granule cell migration during cerebellum development. Mol. Neurobiol. 2013, 47:833-844.
150. Yadlapalli S., Yamashita Y.M. Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 2013, 498:251-254.
151. Yamaguchi Y., Inatani M., Matsumoto Y., Ogawa J., Irie F. Roles of heparan sulfate in mammalian brain development current views based on the findings from Ext1 conditional knockout studies. Prog. Mol. Biol. Transl. Sci. 2010, 93:133-152.
152. Young K.M., Psachoulia K., Tripathi R.B., Dunn S.J., Cossell L., Attwell D., Tohyama K., Richardson W.D. Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 2013, 77:873-885.
153. Yuasa S. Bergmann glial development in the mouse cerebellum as revealed by tenascin expression. Anat. Embryol. (Berl.) 1996, 194:223-234.
154. Zawadzka M., Rivers L.E., Fancy S.P., Zhao C., Tripathi R., Jamen F., Young K., Goncharevich A., Pohl H., Rizzi M., Rowitch D.H., Kessaris N., Suter U., Richardson W.D., Franklin R.J. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 2010, 6:578-590.
155. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
156. Zimmermann D.R., Dours-Zimmermann M.T. Extracellular matrix of the central nervous system: from neglect to challenge. Histochem. Cell Biol. 2008, 130:635-653.
157. Zipursky S.L., Sanes J.R. Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 2010, 143:343-353.