Activated Notch1 maintains the phenotype of radial glial cells and promotes their adhesion to laminin by upregulating nidogen

GLIA

Volumn 56, Issue 6, 2008, Pages 646-658

  Li, Hedong ^a,b   Chang, Yu Wen ^a,b   Mohan, Kriti ^a,b   Su, Hui Wen ^a,b   Ricupero, Christopher L ^a,b   Baridi, Ajoeb ^a,b,c   Hart, Ronald P ^a,b   Grumet, Martin ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

A2B5; Brain development; Laminin; Neural stem cell; Progenitor

Indexed keywords

CELL MARKER; ENTACTIN; LAMININ; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; NOTCH1 RECEPTOR; FABP7 PROTEIN, RAT; FATTY ACID BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN; NOTCH1 PROTEIN, RAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL ADHESION; CELL CLONING; CELL MIGRATION; CELL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; FOREBRAIN; GLIA CELL; MICROARRAY ANALYSIS; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD; UPREGULATION; WHITE MATTER; ANIMAL; CELL CULTURE; CYTOLOGY; DNA MICROARRAY; EMBRYO (ANATOMY); GENETIC TRANSFECTION; GLIA; METABOLISM; METHODOLOGY; PHYSIOLOGY; STEM CELL; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; CELL ADHESION; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; FATTY ACID-BINDING PROTEINS; GREEN FLUORESCENT PROTEINS; LAMININ; MEMBRANE GLYCOPROTEINS; NERVE TISSUE PROTEINS; NEUROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; RATS; RECEPTOR, NOTCH1; SPINAL CORD; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSFECTION; UP-REGULATION;

EID: 45549098554     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20643     Document Type: Article

References (63)

1. Alvarez-Buylla A, Seri B, Doetsch F. 2002. Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57:751-758.
2. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD. 2006. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823-826.
3. Anthony TE, Klein C, Fishell G, Heintz N. 2004. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41:881-890.
4. Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N. 2005. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19:1028-1033.
5. Bartsch S, Bartsch U, Dorries U, Faissner A, Weller A, Ekblom P, Schachner M. 1992. Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736-749.
6. Bauer S, Kerr BJ, Patterson PH. 2007. The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 8:221-232.
7. Bedford L, Walker R, Kondo T, van Cruchten I, King ER, Sablitzky F. 2005. Id4 is required for the correct timing of neural differentiation. Dev Biol 280:386-395.
8. Cao QL, Howard RM, Dennison JB, Whittemore SR. 2002. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp Neurol 177:349-359.
9. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR. 2001. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167:48-58.
10. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella. G, Sun Y, Sarizone S, Ying QL, Cattaneo E, Smith A. 2005. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283.
11. de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossarit J, Conlon RA. 1997. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124:1139-1148.
12. Fan X, Mikolaenko I, Elhassan I, Ni X, Wang Y, Ball D, Brat DJ, Perry A, Eberhart CG. 2004. Notchl and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 64:7787-7793.
13. Feng L, Hatten ME, Heintz N. 1994. Brain lipid-binding protein (BLBP): A novel signaling system in the developing mammalian CNS. Neuron 12:895-908.
14. Fox JW, Mayer U, Nischt R, Aumailley M, Reinhart D, Wiedemann H, Mann K, Timpl R, Krieg T, Chu M-L. 1991. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10:3137-3146.
15. Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, Sayegh MH, Sadee W, Frank MH. 2005. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320-4333.
16. Gaiano N, Nye JS, Fishell G. 2000. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26:395-404.
17. Gotz M, Stoykova A, Gruss P. 1998. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21:1031-1044.
18. Halfter W, Dong S, Yip YP, Willem M, Mayer U. 2001 A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 22:6029-6040.
19. Hartfuss E, Galli R, Heins N, Gotz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15-30.
20. Hasegawa K, Chang Y-W, Li H, Berlin Y, Ikeda O, Kane-Goldsmith, Grumet M. 2005. Embryonic radial glia bridge spinal cord lesions and promote functional recovery following spinal cord injury. Exp Neurol 193:394-410.
21. Hatten ME. 1999. Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
22. Heffron DS, Golden JA. 2000. DM-GRASP is necessary for nonradial cell migration during chick diencephalic development. J Neurosci 20:2287-2294.
23. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker EL, Hack MA, Chapouton P, Barde YA, Gotz M. 2002. Glial cells generate neurons: The role of the transcription factor Pax6. Nat Neurosci 5:308-315.
24. Hibino S, Shibuya M, Engbring JA, Mochizuki M, Nomizu M, Kleinman HK. 2004. Identification of an active site on the laminin α5 chain globular domain that binds to CD44 and inhibits malignancy. Cancer Res 64:4810-4816.
25. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, van der Kooy D. 2002. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16:846-858.
26. Hormigo A, McCarthy M, Nothias JM, Hasegawa K, Huang W, Friedlander DR, Fischer I, Fishell G, Grumet M. 2001. Radial glial cell line C6-R integrates preferentially in adult white matter and facilitates migration of coimplanted neurons in vivo. Exp Neurol 168:310-322.
27. Kim H, Ha CM, Choi J, Choi EJ, Jeon J, Kim C, Park SK, Kang SS, Kim K, Lee BJ. 2002. Ontogeny and the possible furiction of a novel epidermal growth factor-like repeat domain-containing protein, NELL2, in the rat brain J Neurochem 83:1389-1400.
28. Klassen H, Schwartz MR, Bailey AH, Young MJ. 2001. Surface markers expressed by multipotent human and mouse neural progenitor cells include tetraspanins and non-protein epitopes. Neurosci Lett 312:180-182.
29. Kriegstein AR, Gotz M. 2003. Radial glia diversity: A matter of cell fate. Glia 43:37-43.
30. Lai EC. 2004. Notch signaling: Control of cell communication and cell fate. Development 131:965-973.
31. Lefort K, Dotto GP. 2004. Notch signaling in the integrated control of keratinocyte growth/differentiation and tumor suppression. Semin Cancer Biol 14:374-386.
32. Li H, Babiarz J, Woodbury J, Kane-Goldsmith N, Grumet M. 2004. Spatiotemporal heterogeneity of CNS radial glial cells and their transition to restricted precursors. Dev Biol 271:225--238.
33. Li H, Berlin Y, Hart RP, Grumet M. 2003. Microtubules are critical for radial glial morphology: Possible regulation by MAPS and MARKS. Glia 44:37-46.
34. Li H, Grumet M. 2007. BMP and LIF signaling coordinately regulate lineage restriction of radial glia in the developing forebrain. Glia 55:24-35.
35. Liesi P, Silver J. 1988. Is astrocyte laminin involved in axon guidance in the mammalian CNS? Dev Biol 130:774-785.
36. Liu KJ, Harland RM. 2003. Cloning and characterization of Xenopus Id4 reveals differing roles for Id genes. Dev Biol 264:339-351.
37. Liu Y, Han SS, Wu Y, Tuohy TM, Xue H, Cai J, Back SA, Sherman LS, Fischer 1, Rao MS. 2004. CD44 expression identifies astrocyte-restricted precursor cells. Dev Biol 276:31-46.
38. Liu Y, Wu Y, Lee JC, Xue H, Pevny LH, Kaprielian Z, Rao MS. 2002. Oligodendrocyte and astrocyte development in rodents: An in situ and immunohistological analysis during embryonic development. Glia 40:25-43.
39. Lowell S, Benchoua A, Heavey B, Smith AG. 2006. Notch promotes neural lineage entry by pluripotent embryonic stem cells. PLoS Biol 4:e121
40. Marcus RC, Mason CA. 1995. The first retinal axon growth in the mouse optic chiasm: Axon patterning and the cellular environment. J Neurosci 15:6389-6402.
41. Marin-Husstege M, He Y, Li J, Kondo T, Sablitzky F, Casaccia-Bonnefil P. 2006. Multiple roles of Id4 in developmental myelination: Predicted outcomes and unexpected findings. Glia 54:285-296.
42. McKee KK, Harrison D, Capizzi S, Yurchenco PD. 2007. Role of laminin terminal globular domains in basement membrane assembly. J Biol Chem 282:21437-21447.
43. Morgenstern DA, Asher RA, Fawcett JW. 2002. Chondroitin sulphate proteoglycans in the CNS injury response. Prog Brain Res 137:313-332.
44. Mothe AJ, Brown IR. 2002. Effect of hyperthermia on the transport of mRNA encoding the extracellular matrix glycoprotein SC1 into Bergmann glial cell processes. Brain Res 931:146-158.
45. Noble M, Arhin A, Gass D, Mayer-Proschel M. 2003. The cortical ancestry of oligodendrocytes: Common principles and novel features. Dev Neurosci 25:217-233.
46. Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, Jacobsen SE, Nuber UA. 2007. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastorna cells. Cancer Res 67:5727-5736.
47. Purow BW, Haque RM, Noel MW, Su Q, Burdick MJ, Lee J, Sundaresan T, Pastorino S, Park JK, Mikolaenko I, Marie D, Eberhart CG, Fine HA. 2005. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 65:2353-2363.
48. Rakic P. 1990. Principles of neural cell migration. Experientia 46:882-891.
49. Reichardt LF, Tomaselli KJ. 1991. Extracellular matrix molecules and their receptors: Functions in neural development. Annu Rev Neurosci 14:531-570.
50. Sievers J, Pehlemann FW, Gude S, Berry M. 1994. Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 23:135-149.
51. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
52. Smirnov SP, McDearmon EL, Li S, Ervasti JM, Tryggvason K, Yurchenco PD. 2002. Contributions of the LG modules and furin processing to laminin-2 functions. J Biol Chem 277:18928-18937.
53. Smyth GK. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3.
54. Sretavan DW, Feng L, Pure E, Reichardt LF. 1994. Embryonic neurons of the developing optic chiasm express L1 and CD44, cell surface molecules with opposing effects on retinal axon growth. Neuron 12:957-975.
55. Tanigaki K, Nogaki F, Takahashi J, Tashiro K, Kurooka H, Honjo T. 2001. Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29:45-55.
56. Temple S. 2001. Stem cell plasticity - Building the brain of our dreams. Nat Rev Neurosci 2:513-520.
57. Vilimas T, Mascarenhas J, Palomero T, Mandal M, Buonamici S, Meng F, Thompson B, Spaulding C, Macaroun S, Alegre ML, Kee BL, Ferrando A, Miele L, Aifantis I. 2007. Targeting the NF-κB signaling pathway in Notch1-induced T-cell leukemia. Nat Med 13:70-77.
58. Villa A, Snyder EY, Vescovi A, Martinez-Serrano A. 2000. Establishment and properties of a growth factor-dependent, perpetual neural stem cell line from the human CNS. Exp Neurol 161:67-84.
59. Wettenhall JM, Simpson KM, Satterley K, Smyth GK. 2006. affylm-GUI: A graphical user interface for linear modeling of single channel microarray data. Bioinformatics 22:897-899.
60. W ettenhall JM, Smyth GK. 2004. limmaGUI: A graphical user interface for linear modeling of microarray data. Bioinformaties 20: 3705-3706.
61. Yoon K, Gaiano N. 2005. Notch signaling in the mammalian central nervous system: Insights from mouse mutants. Nat Neurosci 8:709-715.
62. Yoon K, Nery S, Rutlin ML, Radtke F, Fishell G, Gaiano N. 2004. Fibroblast growth factor receptor signaling promotes radial glial identity and interacts with Notch1 signaling in telencephalic progenitors. J Neurosci 24:9497-9506.
63. Yurchenco PD, Schittny JC. 1990. Molecular architecture of basement membranes. Faseb J 4:1577-1590.