Cell Adhesion Molecules in Neural Stem Cell and Stem Cell- Based Therapy for Neural Disorders

Neural stem/progenitor cells (NS/PCs), found in both the developing and the adult mamma‐ lian central nervous system (CNS), are a heterogeneous population of multipotent cells with the potential to self-renew by symmetric cell division or to differentiate into neurons, astrocytes and oligodendrocytes through asymmetric cell division (Gage, 2000; Alvarez-Buylla et al., 2001; Temple, 2001; Gotz and Huttner, 2005). NS/PCs have been found in almost all regions of the developing mammalian CNS, including the basal forebrain, cerebral cortex, ganglionic eminence, hippocampus, cerebellum, neural crest and spinal cord (Temple, 2001). Throughout development, NS/PCs give rise to neurons and glial cell populations of the CNS. In the adult CNS, NS/PCs are mainly found in the subventricular zone (SVZ) and subgranular layer (SGL) of hippocampal dentate gyrus (DG) (Goritz and Frisen, 2012). The ependymal cells lining the central canal of spinal cord of the adult mouse could be another potential source of adult NS/ PCs (Meletis et al., 2008). Because neurogenesis and gliogenesis occur during different stages of mammalian brain development, it was long assumed that neurons and glial cells in the CNS were generated from distinct precursor populations, known as early-embryonic, late-embry‐ onic, and adult NS/PCs. However, abundant evidence has since now demonstrated that embryonic and adult NS/PCs are likely lineage-related. Neuroepithelial cells behaving as NS/ PCs during very early developmental stages of the mammalian CNS give rise to radial glial cells around embryonic day 12 (E12). As the progeny of neuroepithelial cells, radial glial cells act as NS/PCs in the fetal and perinatal brain, and develop into astrocyte-like stem cells in the adult brains. Astrocyte-like adult stem cells function as stem cells to generate new nerve cells in the adult mammalian CNS. (Doetsch et al., 1999; Alvarez-Buylla et al., 2001; Merkle et al., 2004; Merkle and Alvarez-Buylla, 2006).

[1]  A. Fournier,et al.  Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration , 2001, Nature.

[2]  A. Irintchev,et al.  Delayed applications of L1 and chondroitinase ABC promote recovery after spinal cord injury. , 2012, Journal of neurotrauma.

[3]  R. Akeson,et al.  At least 27 alternatively spliced forms of the neural cell adhesion molecule mRNA are expressed during rat heart development , 1991, Molecular and cellular biology.

[4]  Kevin Truong,et al.  Cadherins in embryonic and neural morphogenesis , 2000, Nature Reviews Molecular Cell Biology.

[5]  F. Doetsch,et al.  A niche for adult neural stem cells. , 2003, Current opinion in genetics & development.

[6]  M. Schachner,et al.  Analysis of Interactions of the Adhesion Molecule TAG-1 and Its Domains with Other Immunoglobulin Superfamily Members , 2002, Molecular and Cellular Neuroscience.

[7]  T. Shimazaki,et al.  Regulation of adult neural progenitor cells by Galectin‐1/β1 Integrin interaction , 2010, Journal of neurochemistry.

[8]  C. ffrench-Constant,et al.  Neural precursor cell chain migration and division are regulated through different beta1 integrins. , 1998, Development.

[9]  Wei Zheng,et al.  The promotion of neural progenitor cells proliferation by aligned and randomly oriented collagen nanofibers through β1 integrin/MAPK signaling pathway. , 2011, Biomaterials.

[10]  J. Sanes,et al.  γ-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina , 2008, Development.

[11]  A. Irintchev,et al.  Carbohydrate mimics promote functional recovery after peripheral nerve repair , 2006, Annals of neurology.

[12]  W. Young,et al.  Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. , 2003, Journal of neurotrauma.

[13]  Yasuhiko Kizuka,et al.  Expression and function of the HNK-1 carbohydrate. , 2007, Journal of biochemistry.

[14]  Yoshihiro Ito,et al.  A fusion protein N-cadherin-Fc as an artificial extracellular matrix surface for maintenance of stem cell features. , 2010, Biomaterials.

[15]  V. Berezin,et al.  Zippers Make Signals: NCAM-mediated Molecular Interactions and Signal Transduction , 2004, Neurochemical Research.

[16]  D. Häussinger,et al.  Analysis of Heterophilic and Homophilic Interactions of Cadherins Using the c-Jun/c-Fos Dimerization Domains* , 2002, The Journal of Biological Chemistry.

[17]  Y. Itoyama,et al.  Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rat. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Schachner,et al.  Different extracellular domains of the neural cell adhesion molecule (N- CAM) are involved in different functions , 1992, The Journal of cell biology.

[19]  H. T. Ghashghaei,et al.  Neuronal migration in the adult brain: are we there yet? , 2007, Nature Reviews Neuroscience.

[20]  C. ffrench-Constant,et al.  Integrins Are Markers of Human Neural Stem Cells , 2006, Stem cells.

[21]  J. Kiss,et al.  PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival , 2007, Development.

[22]  C. Redies,et al.  δ-Protocadherins: a gene family expressed differentially in the mouse brain , 2005, Cellular and Molecular Life Sciences CMLS.

[23]  G. Landreth,et al.  Activation of the MAPK Signal Cascade by the Neural Cell Adhesion Molecule L1 Requires L1 Internalization* , 1999, The Journal of Biological Chemistry.

[24]  M. Schachner,et al.  Neural Cell Adhesion Molecule Modulates Dopaminergic Signaling and Behavior by Regulating Dopamine D2 Receptor Internalization , 2009, The Journal of Neuroscience.

[25]  M. Glukhova,et al.  Adhesion within the stem cell niches. , 2009, Current opinion in cell biology.

[26]  M. Schachner,et al.  A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis , 2008, Nature Cell Biology.

[27]  J. Schiefer,et al.  Neural Cell Adhesion Molecule L1-Transfected Embryonic Stem Cells Promote Functional Recovery after Excitotoxic Lesion of the Mouse Striatum , 2006, The Journal of Neuroscience.

[28]  R. Brewster,et al.  N-cadherin–mediated cell adhesion restricts cell proliferation in the dorsal neural tube , 2011, Molecular biology of the cell.

[29]  C. Redies,et al.  Expression of N‐cadherin mRNA during development of the mouse brain , 1993, Developmental dynamics : an official publication of the American Association of Anatomists.

[30]  H. Zhang,et al.  A role for the polysialic acid – neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells , 2004, Journal of Cell Science.

[31]  M. Takeichi,et al.  Neural crest emigration from the neural tube depends on regulated cadherin expression. , 1998, Development.

[32]  Sruthi K. Swaminathan,et al.  Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. , 2010, Developmental cell.

[33]  L. Landmesser,et al.  Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions , 1996, Trends in Neurosciences.

[34]  W. Birchmeier,et al.  Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. , 2010, Cold Spring Harbor perspectives in biology.

[35]  A. Artola,et al.  The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long‐term potentiation , 1996, Journal of neuroscience research.

[36]  M. Schachner,et al.  Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration , 2006, Nature Neuroscience.

[37]  Lia S. Campos,et al.  Regulation of neural progenitor proliferation and survival by β1 integrins , 2005, Journal of Cell Science.

[38]  U. Rutishauser,et al.  Polysialic acid regulates cell contact‐dependent neuronal differentiation of progenitor cells from the subventricular zone , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[39]  J. McCarty,et al.  β8 integrin is essential for neuroblast migration in the rostral migratory stream , 2011, Glia.

[40]  F. Miller,et al.  Home at last: neural stem cell niches defined. , 2009, Cell stem cell.

[41]  G. Kusek,et al.  VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. , 2012, Cell stem cell.

[42]  A. Walch,et al.  Cadherin-2 Controls Directional Chain Migration of Cerebellar Granule Neurons , 2009, PLoS biology.

[43]  Y. Takai,et al.  Nectin and afadin: novel organizers of intercellular junctions , 2003, Journal of Cell Science.

[44]  G. Edelman,et al.  Neural Cell Adhesion Molecule (N-CAM) Homophilic Binding Mediated by the Two N-terminal Ig Domains Is Influenced by Intramolecular Domain-Domain Interactions* , 2004, Journal of Biological Chemistry.

[45]  Arturo Alvarez-Buylla,et al.  A unified hypothesis on the lineage of neural stem cells , 2001, Nature Reviews Neuroscience.

[46]  M. Schachner,et al.  β 1 Integrin-mediated Effects of Tenascin-R Domains EGFL and FN6-8 on Neural Stem/Progenitor Cell Proliferation and Differentiation in Vitro* , 2008, Journal of Biological Chemistry.

[47]  M. Ikura,et al.  Structural basis of calcium-induced E-cadherin rigidification and dimerization , 1996, Nature.

[48]  M. Schachner,et al.  Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve , 1986, The Journal of cell biology.

[49]  Mitsuhiko Ikura,et al.  Structural basis of calcium-induced E-cadherin rigidification and dimerization , 1996 .

[50]  M. Hoshino,et al.  Rab GTPases-Dependent Endocytic Pathways Regulate Neuronal Migration and Maturation through N-Cadherin Trafficking , 2010, Neuron.

[51]  Sally Temple,et al.  The development of neural stem cells , 2001, Nature.

[52]  Y. Takai,et al.  Enhancement of Serum- and Platelet-derived Growth Factor-induced Cell Proliferation by Necl-5/Tage4/Poliovirus Receptor/CD155 through the Ras-Raf-MEK-ERK Signaling* , 2004, Journal of Biological Chemistry.

[53]  D. Leckband,et al.  Direct Evidence That Neural Cell Adhesion Molecule (NCAM) Polysialylation Increases Intermembrane Repulsion and Abrogates Adhesion* , 2005, Journal of Biological Chemistry.

[54]  M. Bronner‐Fraser,et al.  N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. , 2000, Science.

[55]  M. Schachner,et al.  Transplanted L1 expressing radial glia and astrocytes enhance recovery after spinal cord injury. , 2011, Journal of neurotrauma.

[56]  U. Rutishauser,et al.  Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus , 2008, Developmental neurobiology.

[57]  M. Schachner,et al.  A New Role for the Cell Adhesion Molecule L1 in Neural Precursor Cell Proliferation, Differentiation, and Transmitter-Specific Subtype Generation , 2003, The Journal of Neuroscience.

[58]  Lia S. Campos,et al.  β1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance , 2004, Development.

[59]  Rong A. Wang,et al.  Vascular Development of the Brain Requires β8 Integrin Expression in the Neuroepithelium , 2005, The Journal of Neuroscience.

[60]  Y. Takai,et al.  Biology and pathology of nectins and nectin-like molecules. , 2004, Current opinion in cell biology.

[61]  K. Moore,et al.  Stem Cells and Their Niches , 2006, Science.

[62]  N. Hogg,et al.  Involvement of the "I" domain of LFA-1 in selective binding to ligands ICAM-1 and ICAM-3 , 1994, The Journal of cell biology.

[63]  B. Gumbiner,et al.  E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. , 2007, Molecular biology of the cell.

[64]  S. Chu,et al.  Resolving cadherin interactions and binding cooperativity at the single-molecule level , 2009, Proceedings of the National Academy of Sciences.

[65]  T. Fahrig,et al.  Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction , 1987, The Journal of cell biology.

[66]  K. Kaibuchi,et al.  Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases. , 2009, Cold Spring Harbor perspectives in biology.

[67]  M. Schachner,et al.  Embryonic Stem Cell-Derived L1 Overexpressing Neural Aggregates Enhance Recovery after Spinal Cord Injury in Mice , 2011, PloS one.

[68]  A. Irintchev,et al.  Polysialic acid glycomimetics promote myelination and functional recovery after peripheral nerve injury in mice. , 2009, Brain : a journal of neurology.

[69]  B. Geiger,et al.  Signaling from adherens-type junctions. , 2005, European journal of cell biology.

[70]  J. Marth,et al.  Polysialic Acid-Directed Migration and Differentiation of Neural Precursors Are Essential for Mouse Brain Development , 2007, Molecular and Cellular Biology.

[71]  W. Weis,et al.  Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. , 2005, Cell.

[72]  Jean-Loup Duband,et al.  Cross Talk between Adhesion Molecules: Control of N-cadherin Activity by Intracellular Signals Elicited by β1 and β3 Integrins in Migrating Neural Crest Cells , 1997, The Journal of cell biology.

[73]  P. Sonderegger,et al.  Cell adhesion molecules NgCAM and axonin-1 form heterodimers in the neuronal membrane and cooperate in neurite outgrowth promotion , 1996, The Journal of cell biology.

[74]  J. Salzer,et al.  The amino acid sequences of the myelin-associated glycoproteins: homology to the immunoglobulin gene superfamily , 1987, The Journal of cell biology.

[75]  L. Bonfanti,et al.  Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb , 1994, Neuroscience.

[76]  B. Angst,et al.  COMMENTARY The cadherin superfamily: diversity in form and function , 2022 .

[77]  V. Berezin,et al.  Structural biology of NCAM homophilic binding and activation of FGFR , 2005, Journal of neurochemistry.

[78]  H. Fukuhara,et al.  Direct association of TSLC1 and DAL-1, two distinct tumor suppressor proteins in lung cancer. , 2002, Cancer research.

[79]  D. Benson,et al.  Functional binding interaction identified between the axonal CAM L1 and members of the ERM family , 2002, The Journal of cell biology.

[80]  S. Willaime-Morawek,et al.  E-Cadherin Regulates Neural Stem Cell Self-Renewal , 2009, The Journal of Neuroscience.

[81]  G. Demyanenko,et al.  Abnormalities in Neuronal Process Extension, Hippocampal Development, and the Ventricular System of L1 Knockout Mice , 1999, The Journal of Neuroscience.

[82]  L. Landmesser,et al.  NCAM 180 Acting via a Conserved C-Terminal Domain and MLCK Is Essential for Effective Transmission with Repetitive Stimulation , 2005, Neuron.

[83]  P. Tittmann,et al.  Implications for the domain arrangement of axonin‐1 derived from the mapping of its NgCAM binding site. , 1996, The EMBO journal.

[84]  H. Fukuhara,et al.  Association of a lung tumor suppressor TSLC1 with MPP3, a human homologue of Drosophila tumor suppressor Dlg , 2003, Oncogene.

[85]  S. Kenwrick,et al.  Cis and trans interactions of L1 with neuropilin‐1 control axonal responses to semaphorin 3A , 2002, The EMBO journal.

[86]  T. Magnuson,et al.  The Role of Polysialic Acid in Migration of Olfactory Bulb Interneuron Precursors in the Subventricular Zone , 1996, Neuron.

[87]  M. Schachner,et al.  Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth , 2005, The Journal of cell biology.

[88]  T. Jessell,et al.  Developmental expression of the axonal glycoprotein TAG-1: differential regulation by central and peripheral neurons in vitro. , 1991, Development.

[89]  T. Jessell,et al.  The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity , 1990, Cell.

[90]  V. Berezin,et al.  Neural Cell Adhesion Molecule-Stimulated Neurite Outgrowth Depends on Activation of Protein Kinase C and the Ras–Mitogen-Activated Protein Kinase Pathway , 2000, The Journal of Neuroscience.

[91]  C. Portera-Cailliau,et al.  Foxp-Mediated Suppression of N-Cadherin Regulates Neuroepithelial Character and Progenitor Maintenance in the CNS , 2012, Neuron.

[92]  W. Stallcup,et al.  Mutational Analysis of the L1 Neuronal Cell Adhesion Molecule Identifies Membrane-Proximal Amino Acids of the Cytoplasmic Domain That Are Required for Cytoskeletal Anchorage , 1997, Molecular and Cellular Neuroscience.

[93]  T. Kirchhausen,et al.  The Neural Cell Adhesion Molecule L1 Interacts with the AP-2 Adaptor and Is Endocytosed via the Clathrin-Mediated Pathway , 1998, The Journal of Neuroscience.

[94]  F. Zipp,et al.  Neural Cell Adhesion Molecule Polysialylation Enhances the Sensitivity of Embryonic Stem Cell‐Derived Neural Precursors to Migration Guidance Cues , 2007, Stem cells.

[95]  J. Sanes,et al.  Gamma Protocadherins Are Required for Survival of Spinal Interneurons , 2002, Neuron.

[96]  J. Haspel,et al.  L1 mediated homophilic binding and neurite outgrowth are modulated by alternative splicing of exon 2. , 2002, Journal of neurobiology.

[97]  M. Schachner,et al.  In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid , 2006, The European journal of neuroscience.

[98]  A. Ludwig,et al.  Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination , 2006, Development.

[99]  S. Barthel,et al.  Targeting selectins and selectin ligands in inflammation and cancer , 2007, Expert opinion on therapeutic targets.

[100]  R. Geisler,et al.  parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. , 2002, Development.

[101]  H. Yagi,et al.  Involvement of β1-Integrin Up-regulation in Basic Fibroblast Growth Factor- and Epidermal Growth Factor-induced Proliferation of Mouse Neuroepithelial Cells* , 2010, The Journal of Biological Chemistry.

[102]  M. Marín‐Padilla,et al.  Neocortical Development , 1992, Journal of Cognitive Neuroscience.

[103]  G. Paratcha,et al.  The Neural Cell Adhesion Molecule NCAM Is an Alternative Signaling Receptor for GDNF Family Ligands , 2003, Cell.

[104]  M. Mattson,et al.  β1 Integrin Maintains Integrity of the Embryonic Neocortical Stem Cell Niche , 2009, PLoS biology.

[105]  C. Ryu,et al.  Brief Report: L1 Cell Adhesion Molecule, a Novel Surface Molecule of Human Embryonic Stem cells, Is Essential for Self‐Renewal and Pluripotency , 2011, Stem cells.

[106]  Daniel A. Lim,et al.  Subventricular Zone Astrocytes Are Neural Stem Cells in the Adult Mammalian Brain , 1999, Cell.

[107]  M. Hortsch,et al.  The L1 Family of Neural Cell Adhesion Molecules: Old Proteins Performing New Tricks , 1996, Neuron.

[108]  G. Edelman,et al.  Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[109]  K. Irie,et al.  Nectins and nectin‐like molecules: Roles in cell adhesion, migration, and polarization , 2003, Cancer science.

[110]  P. Maness,et al.  A MAP Kinase-Signaling Pathway Mediates Neurite Outgrowth on L1 and Requires Src-Dependent Endocytosis , 2000, The Journal of Neuroscience.

[111]  Cécile Boscher,et al.  N-Cadherin Mediates Neuronal Cell Survival through Bim Down-Regulation , 2012, PloS one.

[112]  R. Quarles Myelin-associated glycoprotein in development and disease. , 1983, Developmental neuroscience.

[113]  G. Edelman,et al.  Distinct calcium-independent and calcium-dependent adhesion systems of chicken embryo cells. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[114]  G. Alonso,et al.  Neuronal progenitor‐like cells expressing polysialylated neural cell adhesion molecule are present on the ventricular surface of the adult rat brain and spinal cord , 1999, The Journal of comparative neurology.

[115]  Jiping Xu,et al.  Neural stem cell differentiation is mediated by integrin beta4 in vitro. , 2009, The international journal of biochemistry & cell biology.

[116]  M. Schachner,et al.  Polysialylated Neural Cell Adhesion Molecule Is Involved in Induction of Long-Term Potentiation and Memory Acquisition and Consolidation in a Fear-Conditioning Paradigm , 2006, The Journal of Neuroscience.

[117]  H. Zhang,et al.  PSA‐NCAM modulates BDNF‐dependent survival and differentiation of cortical neurons , 2001, The European journal of neuroscience.

[118]  M. Schachner,et al.  Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice. , 2010, Brain : a journal of neurology.

[119]  Marco Domeniconi,et al.  Myelin-Associated Glycoprotein Interacts with the Nogo66 Receptor to Inhibit Neurite Outgrowth , 2002, Neuron.

[120]  P. Richardson,et al.  Induced expression of polysialic acid in the spinal cord promotes regeneration of sensory axons , 2007, Molecular and Cellular Neuroscience.

[121]  William I. Weis,et al.  α-Catenin Is a Molecular Switch that Binds E-Cadherin-β-Catenin and Regulates Actin-Filament Assembly , 2005, Cell.

[122]  Andrés J. García,et al.  Specific β1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum , 2004, Molecular and Cellular Neuroscience.

[123]  V. Vasioukhin,et al.  Adhesive and signaling functions of cadherins and catenins in vertebrate development. , 2009, Cold Spring Harbor perspectives in biology.

[124]  J. Papamatheakis,et al.  The Fibronectin Domains of the Neural Adhesion Molecule TAX-1 Are Necessary and Sufficient for Homophilic Binding* , 1996, The Journal of Biological Chemistry.

[125]  Lia S. Campos,et al.  Notch, Epidermal Growth Factor Receptor, and β1-Integrin Pathways Are Coordinated in Neural Stem Cells* , 2006, Journal of Biological Chemistry.

[126]  A. Álvarez-Buylla,et al.  Network of tangential pathways for neuronal migration in adult mammalian brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[127]  J. García-Verdugo,et al.  Radial glia give rise to adult neural stem cells in the subventricular zone. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[128]  M. Monden,et al.  Direct Binding of Cell Polarity Protein PAR-3 to Cell-Cell Adhesion Molecule Nectin at Neuroepithelial Cells of Developing Mouse* , 2003, The Journal of Biological Chemistry.

[129]  Melitta Schachner,et al.  Signal transduction pathways implicated in neural recognition molecule L1 triggered neuroprotection and neuritogenesis , 2005, Journal of neurochemistry.

[130]  A. Baines,et al.  Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. , 2001, Physiological reviews.

[131]  T. Hisatsune,et al.  Decrease in expression of α5β1 integrin during neuronal differentiation of cortical progenitor cells , 2003 .

[132]  Emmanuel Dias-Neto,et al.  Discovery of a functional protein complex of netrin-4, laminin γ1 chain, and integrin α6β1 in mouse neural stem cells , 2009, Proceedings of the National Academy of Sciences.

[133]  Gareth Williams,et al.  A dimeric version of the short N-cadherin binding motif HAVDI promotes neuronal cell survival by activating an N-cadherin/fibroblast growth factor receptor signalling cascade , 2004, Molecular and Cellular Neuroscience.

[134]  S. Krauss,et al.  N-cadherin mediates cortical organization in the mouse brain. , 2007, Developmental biology.

[135]  R. Heimark,et al.  Protocadherins: a large family of cadherin‐related molecules in central nervous system. , 1993, The EMBO journal.

[136]  M. Schachner,et al.  Promotion of Spinal Cord Regeneration by Neural Stem Cell-Secreted Trimerized Cell Adhesion Molecule L1 , 2012, PloS one.

[137]  C Chothia,et al.  The molecular structure of cell adhesion molecules. , 1997, Annual review of biochemistry.

[138]  T. Seki,et al.  Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system , 1993, Neuroscience Research.

[139]  C. Betzel,et al.  CHL1 Is a Selective Organizer of the Presynaptic Machinery Chaperoning the SNARE Complex , 2010, PloS one.

[140]  X. Lv,et al.  Inhibition of PC-PLC Blocked the Survival of Mouse Neural Cells by Up-Regulating the Expression of Integrin beta4 and Rb , 2006, Developmental Neuroscience.

[141]  β8 integrin regulates neurogenesis and neurovascular homeostasis in the adult brain , 2009, Journal of Cell Science.

[142]  I. Mason Cell Signalling: Do adhesion molecules signal via FGF receptors? , 1994, Current Biology.

[143]  M. Kiso,et al.  MyeliN‐associated Glycoprotein Binding to Gangliosides: Structural Specificity and Functional Implications a , 1998, Annals of the New York Academy of Sciences.

[144]  F. Gage,et al.  Mammalian neural stem cells. , 2000, Science.

[145]  H. Taniguchi,et al.  Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain , 2006, Development.

[146]  Richard O Hynes,et al.  Integrins Bidirectional, Allosteric Signaling Machines , 2002, Cell.

[147]  Hidekazu Tanaka,et al.  N-Cadherin Redistribution during Synaptogenesis in Hippocampal Neurons , 1998, The Journal of Neuroscience.

[148]  M. Götz,et al.  The cell biology of neurogenesis , 2006, International Journal of Developmental Neuroscience.

[149]  L. Shapiro,et al.  Adhesion molecules in the nervous system: structural insights into function and diversity. , 2007, Annual review of neuroscience.

[150]  Keith R. Johnson,et al.  Cadherin-mediated cellular signaling. , 2003, Current opinion in cell biology.

[151]  I. Apostolova,et al.  Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury. , 2007, Brain : a journal of neurology.

[152]  P. Maness,et al.  NCAM140 Interacts with the Focal Adhesion Kinase p125fak and the SRC-related Tyrosine Kinase p59fyn* , 1997, The Journal of Biological Chemistry.

[153]  M. Takeichi,et al.  Cadherins in brain morphogenesis and wiring. , 2012, Physiological reviews.

[154]  T. Hisatsune,et al.  Decrease in expression of alpha 5 beta 1 integrin during neuronal differentiation of cortical progenitor cells. , 2003, Experimental cell research.

[155]  A. Irintchev,et al.  Polysialic acid glycomimetic promotes functional recovery and plasticity after spinal cord injury in mice. , 2010, Molecular therapy : the journal of the American Society of Gene Therapy.

[156]  Y. Takai,et al.  Roles of the intercellular adhesion molecule nectin in intracellular signaling. , 2003, Journal of biochemistry.

[157]  Engineered expression of polysialic acid enhances Purkinje cell axonal regeneration in L1/GAP‐43 double transgenic mice , 2007, The European journal of neuroscience.

[158]  Guoqiang Sun,et al.  Neural stem cell self-renewal. , 2008, Critical reviews in oncology/hematology.

[159]  S. Kaduwal,et al.  Bone morphogenetic protein 4 stimulates attachment of neurospheres and astrogenesis of neural stem cells in neurospheres via phosphatidylinositol 3 kinase-mediated upregulation of N-cadherin , 2010, Neuroscience.

[160]  A. Horwitz,et al.  Deleted in Colorectal Carcinoma and Differentially Expressed Integrins Mediate the Directional Migration of Neural Precursors in the Rostral Migratory Stream , 2002, The Journal of Neuroscience.

[161]  M. Schachner,et al.  The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. , 2001, Development.

[162]  K. Kizhatil,et al.  A New Activity of Doublecortin in Recognition of the Phospho-FIGQY Tyrosine in the Cytoplasmic Domain of Neurofascin , 2002, The Journal of Neuroscience.

[163]  J. Frisén,et al.  Neural stem cells and neurogenesis in the adult. , 2012, Cell stem cell.

[164]  D. Wedlich,et al.  Xenopus cadherin-11 restrains cranial neural crest migration and influences neural crest specification. , 2001, Development.