Hostname: page-component-7c8c6479df-ph5wq Total loading time: 0 Render date: 2024-03-28T00:11:06.731Z Has data issue: false hasContentIssue false

Cell contact-inhibition signaling as part of wound-healing processes in brain

Published online by Cambridge University Press:  13 November 2008

Ximena A. Lanosa
Affiliation:
Unidad de Neurobiología Aplicada (UNA), CEMIC, Av. Galván 4102 (C1431FWO), Buenos Aires, Argentina
Jorge A. Colombo*
Affiliation:
Unidad de Neurobiología Aplicada (UNA), CEMIC, Av. Galván 4102 (C1431FWO), Buenos Aires, Argentina
*
Correspondence should be addressed to: Jorge A. Colombo, U.N.A. (CEMIC) Av. Galván 4102 (C1431FWO), Buenos Aires, Argentina, phone: 54 11 4545 6589 ext. 8712 fax: 54 11 4546 8200 email: drjacolombo@yahoo.com

Abstract

Cell contact-dependent signaling is a major regulatory mechanism in the organization of developing tissues and in the reorganization (post-injury responses) of specialized tissues in multicellular organisms. In this review we contribute to the further understanding of post-injury recovery processes in adult nervous tissue. We emphasize evidence that supports the involvement of cell contact-inhibition signaling in the cell proliferation, growth and differentiation that occurs during healing and neural reorganization after brain damage.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abercrombie, M. and Heaysman, J.E. (1954) Observations on the social behavior of cells in tissue culture. II. Monolayering of fibroblasts. Experimental Cell Research 6, 293306.Google Scholar
Allen, B.G., Durussel, I., Walsh, M.P. and Cox, J.A. (1996) Characterization of the Ca2+-binding properties of calgizzarin (S100C) isolated from chicken gizzard smooth muscle. Biochemistry and Cell Biology 74, 687694.Google Scholar
Artavanis-Tsakonas, S., Rand, M.D. and Lake, R.J. (1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770776.Google Scholar
Balasingam, V., Dickson, K., Brade, A. and Yong, V.W. (1996) Astrocyte reactivity in neonatal mice: apparent dependence on the presence of reactive microglia/macrophages. Glia 18, 1126.Google Scholar
Bandtlow, C., Zachleder, T. and Schwab, M.E. (1990) Oligodendrocytes arrest neurite growth by contact inhibition. Journal of Neuroscience 10, 38373848.Google Scholar
Barger, S.W. and Van Eldik, L.J. (1992) S100 beta stimulates calcium fluxes in glial and neuronal cells. Journal of Biological Chemistry 267, 96899694.Google Scholar
Benson, M.D., Romero, M.I., Luz, M.E., Lu, Q.R., Henkemeyer, M. and Parada, L.F. (2005) Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proceedings of the National Academy of Sciences of the U.S.A. 102, 1069410699.Google Scholar
Bovolenta, P., Fernaud-Espinosa, I., Méndez-Otero, R. and Nieto-Sampedro, M. (1997) Neurite outgrowth inhibitor of gliotic brain tissue. Mode of action and cellular localization, studied with specific monoclonal antibodies. European Journal of Neuroscience 9, 977989.Google Scholar
Bregman, B.S., Kunkel-Bagden, E., Schnell, L., Dai, H.N., Gao, D. and Schwab, M.E. (1995) Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378, 498501.Google Scholar
Brock, J.H., Elste, A. and Huntley, G.W. (2004) Distribution and injury-induced plasticity of cadherins in relationship to identified synaptic circuitry in adult rat spinal cord. Journal of Neuroscience 24, 88068817.Google Scholar
Bundesen, L.Q., Scheel, T.A., Bregman, B.S. and Kromer, L.F. (2003) Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. Journal of Neuroscience 23, 77897800.Google Scholar
Caroni, P. and Schwab, M. (1988) Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1, 8596.Google Scholar
Caveda, L., Martin-Padura, I., Navarro, P., Breviario, F., Corada, M., Gulino, D. et al. (1996) Inhibition of cultured cell growth by vascular endothelial cadherin (cadherin-5/VE-cadherin). Journal of Clinical Investigation 98, 886893.Google Scholar
Cheng, G., Youssef, B.B., Markenscoff, P. and Zygourakis, K. (2006) Cell population dynamics modulate the rates of tissue growth processes. Biophysics Journal 90, 713724.Google Scholar
Chou, R.C. and Langan, T.J. (2003) In vitro synchronization of mammalian astrocytic cultures by serum deprivation. Brain Research. Brain Research Protocols 11, 162167.Google Scholar
Crocker, P.R., Clark, E.A., Filbin, M., Gordon, S., Jones, Y., Kehrl, J.H. et al. (1998) Siglecs: a family of sialic-acid binding lectins. Glycobiology 8, v.Google Scholar
Davy, A., Gale, N.W., Murray, E.W., Klinghoffer, R.A., Soriano, P., Feuerstein, C. et al. (1999) Compartmentalized signaling by GPI anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes and Development 13, 31253135.Google Scholar
De Vellis, J., Morrison, R.S., Peng, W.W. and Arenander, A.T. (1983) The use of primary glial cell cultures in developmental studies of the central nervous system. Birth Defects Original Articles Series 19, 6778.Google Scholar
Donato, R. (2001) S-100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. International Journal of Biochemistry and Cell Biology 33, 637668.Google Scholar
Eclancher, F., Kehrli, P., Labourdette, G. and Sensenbrenner, M. (1996) Basic fibroblast growth factor (bFGF) injection activates the glial reaction in the injured adult rat brain. Brain Research 737, 201214.Google Scholar
Faber-Elman, A., Solomon, A., Abraham, J.A., Marikovsky, M. and Schwartz, M. (1996) Involvement of wound-associated factors in rat brain astrocyte migratory response to axonal injury: in vitro simulation. Journal of Clinical Investigation 97, 162171.Google Scholar
Fallon, J.R. (1985) Neurite guidance by non-neuronal cells in culture: preferential outgrowth of peripheral neurites on glial as compared to nonglial cell surfaces. Journal of Neuroscience 5, 31693177.Google Scholar
Fawcett, J.W. and Asher, R.A. (1999) The glial scar and central nervous system repair. Brain Research Bulletin 49, 377391.Google Scholar
Fitch, M.T., Doller, C., Combs, C.K., Landreth, G.E. and Silver, J. (1999) Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. Journal of Neuroscience 19, 81828198.Google Scholar
Gale, N.W. and Yancopoulos, G.D. (1997) Ephrins and their receptors: a repulsive topic? Cell Tissue Res. 290, 227241.Google Scholar
Gao, P.P., Yue, Y., Zhang, J.H., Cerretti, D.P., Levitt, P. and Zhou, R. (1998) Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: implications in the development of thalamocortical projections. Proceedings of the National Academy of Sciences of the U.S.A. 95, 53295334.Google Scholar
Genoud, S., Lappe-Siefke, C., Goebbels, S., Radtke, F., Aguet, M., Scherer, S.S. et al. (2002) Notch1 control of oligodendrocyte differentiation in the spinal cord. Journal of Cell Biology 158, 709718.Google Scholar
Giaume, C. and McCarthy, K.D. (1996) Control of gap-junctional communication in astrocytic networks. Trends in Neurosciences 19, 319325.Google Scholar
Givogri, M.I., Costa, R.M., Schonmann, V., Silva, A.J., Campagnoni, A.T. and Bongarzone, E.R. (2002) Central nervous system myelination in mice with deficient expression of Notch1 receptor. Journal of Neuroscience Research 67, 309320.Google Scholar
Goldberg, G.S., Bechberger, J.F., Tajima, Y., Merritt, M., Omori, Y., Gawinowicz, M.A. et al. (2000) Connexin43 suppresses MFG-E8 while inducing contact growth inhibition of glioma cells. Cancer Research 60, 60186026.Google Scholar
Gray, G.E., Mann, R.S., Mitsiadis, E., Henrique, D., Carcangiu, M.L., Banks, A. et al. (1999) Human ligands of the Notch receptor. American Journal of Patholology 154, 785794.Google Scholar
Griffin, W.S., Stanley, L.C., Ling, C., White, L., MacLeod, V., Perrot, L.J. et al. (1989) Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proceedings of the National Academy of Sciences of the U.S.A. 86, 76117615.Google Scholar
Hampton, D.W., Rhodes, K.E., Zhao, C., Franklin, R.J. and Fawcett, J.W. (2004) The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127, 813820.Google Scholar
Hinkle, D.A., Baldwin, S.A., Scheff, S.W. and Wise, P.M. (1997) GFAP and S100beta expression in the cortex and hippocampus in response to mild cortical contusion. Journal of Neurotrauma 14, 729738.Google Scholar
Hodges-Savola, C., Rogers, S.D., Ghilardi, J.R., Timm, D.R. and Mantyh, P.W. (1996) Beta-adrenergic receptors regulate astrogliosis and cell proliferation in the central nervous system in vivo. Glia 17, 5262.Google Scholar
Hu, J., Castets, F., Guevara, J.L. and Van Eldik, L.J. (1996) S100 beta stimulates inducible nitric oxide synthase activity and mRNA levels in rat cortical astrocytes. Journal of Biological Chemistry 271, 25432547.Google Scholar
Huang, Z.Y., Wu, Y., Hedrick, N. and Gutmann, D.H. (2003) T-cadherin-mediated cell growth regulation involves G2 phase arrest and requires p21(CIP1/WAF1) expression. Molecular and Cellular Biology 23, 566578.Google Scholar
Huang, J.K., Phillips, G.R., Roth, A.D., Pedraza, L., Shan, W., Belkaid, W. et al. (2005) Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310, 18131817.Google Scholar
Joy, A., Moffett, J., Neary, K., Mordechai, E., Stachowiak, E.K., Coons, S. et al. (1997) Nuclear accumulation of FGF-2 is associated with proliferation of human astrocytes and glioma cells. Oncogene 14, 171183.Google Scholar
Kelm, S., Pelz, A., Schauer, R., Filbin, M.T., Tang, S., de Bellard, M.E. et al. (1994) Sialoadhesin, myelin-associated glycoprotein and CD22 define a new family of sialic acid-dependent adhesion molecules of the immunoglobulin superfamily. Current Biology 4, 965972.Google Scholar
Kim, J.S., Yoon, S.S., Kim, Y.H. and Ryu, J.S. (1996) Serial measurement of interleukin-6, transforming growth factor-beta, and S-100 protein in patients with acute stroke. Stroke 27, 15531557.Google Scholar
Kullander, K., Croll, S.D., Zimmer, M., Pan, L., McClain, J., Hughes, V. et al. (2001) Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes and Development 15, 877888.Google Scholar
Labourdette, G. and Marks, A. (1975) Synthesis of S-100 protein in monolayer cultures of rat-glial cells. European Journal of Biochemistry 58, 7379.Google Scholar
Lampugnani, M.G., Orsenigo, F., Gagliani, M.C., Tacchetti, C. and Dejana, E. (2006) Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. Journal of Cell Biology 174, 593604.Google Scholar
Landis, D.M. (1994) The early reactions of non-neuronal cells to brain injury. Annual Review of Neuroscience 17, 133151.Google Scholar
Lanosa, X.A. and Colombo, J.A. (2007) Astroglial injury in an ex vivo model: contributions to its analysis in enriched cell cultures. In Vitro Cellular and Developmental Biology. Animal 43, 186195.Google Scholar
Larue, L., Antos, C., Butz, S., Huber, O., Delmas, V., Dominis, M. and Kemler, R. (1996) A role for cadherins in tissue formation. Development 122, 31853194.Google Scholar
Li, S., Gerrard, E. and Balkovetz, D. (2004) Evidence for ERK 1/2 phosphorylation controlling contact inhibition of proliferation in Madin-Darby carine kidney epithelial cells. American Journal of Physiology. Cell Physiology 287, 432439.Google Scholar
Maillard, I., He, Y. and Pear, W.S. (2003) From the yolk sac to the spleen: New roles for Notch in regulating hematopoiesis. Immunity 18, 587589.Google Scholar
Mandell, J.W. and VandenBerg, S.R. (1999) ERK/MAP kinase is chronically activated in human reactive astrocytes. Neuroreport 10, 35673572.Google Scholar
Mandell, J.W., Gocan, N.C. and Vandenberg, S.R. (2001) Mechanical trauma induces rapid astroglial activation of ERK/MAP kinase: Evidence for a paracrine signal. Glia 34, 283295.Google Scholar
Marti, T., Erttmann, K.D. and Gallin, M.Y. (1996) Host-parasite interaction in human onchocerciasis: identification and sequence analysis of a novel human calgranulin. Biochemical Biophysical Research Communications 221, 454458.Google Scholar
Matsui, T., Mori, T., Tateishi, N., Kagamiishi, Y., Satoh, S., Katsube, N. et al. (2002) Astrocytic activation and delayed infarct expansion after permanent focal ischemia in rats. Part I: enhanced astrocytic synthesis of s-100beta in the periinfarct area precedes delayed infarct expansion. Journal of Cerebral Blood Flow and Metabolism 22, 711722.Google Scholar
Maxwell, W.L., Follows, R., Ashhurst, D.E. and Berry, M. (1990a) The response of the cerebral hemisphere of the rat to injury. II. The neonatal rat. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 328, 501513.Google Scholar
Maxwell, W.L., Follows, R., Ashhurst, D.E. and Berry, M. (1990b) The response of the cerebral hemisphere of the rat to injury. I. The mature rat. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 328, 479500.Google Scholar
Mimura, F., Yamagishi, S., Arimura, N., Fujitani, M., Kubo, T., Kaibuchi, K. et al. (2006) Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. Journal of Biological Chemistry 281, 1597015979.Google Scholar
Miranda, J.D., White, L.A., Marcillo, A.E., Willson, C.A., Jagid, J. and Whittemore, S.R. (1999) Induction of Eph B3 after spinal cord injury. Experimental Neurology 156, 218222.Google Scholar
Moffett, J., Kratz, E., Florkiewicz, R. and Stachowiak, M.K. (1996) Promoter regions involved in density-dependent regulation of basic fibroblast growth factor gene expression in human astrocytic cells. Proceedings of the National Academy of Sciences of the U.S.A. 93, 24702475.Google Scholar
Monschau, B., Kremoser, C., Ohta, K., Tanaka, H., Kaneko, T., Yamada, T. et al. (1997) Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. EMBO Journal 16, 12581267.Google Scholar
Moreno-Flores, M.T. and Wandosell, F. (1999) Up-regulation of Eph tyrosine kinase receptors after excitotoxic injury in adult hippocampus. Neuroscience 91, 193201.Google Scholar
Nakatsuji, Y. and Miller, R.H. (2001) Density dependent modulation of cell cycle protein expression in astrocytes. Journal of Neuroscience Res. 66, 487496.Google Scholar
Nakatsuji, Y. and Miller, R.H. (1998) Homotypic cell contact-dependent inhibition of astrocyte proliferation. Glia 22, 379389.Google Scholar
Nomura, H., Furuta, A. and Iwaki, T. (2002) Dorsal root rupture injury induces extension of astrocytic processes into the peripheral nervous system and expression of GDNF in astrocytes. Brain Research 950, 2130.Google Scholar
Norenberg, M.D. (1994) Astrocyte responses to CNS injury. Journal of Neuropathology and Experimental Neurology 53, 213220.Google Scholar
Ochalski, P.A., Sawchuk, M.A., Hertzberg, E.L. and Nagy, J.I. (1995) Astrocytic gap junction removal, connexin43 redistribution, and epitope masking at excitatory amino acid lesion sites in rat brain. Glia 14, 279294.Google Scholar
Oh, Y.J., Markelonis, G.J. and Oh, T.H. (1993) Effects of interleukin-1 beta and tumor necrosis factor-alpha on the expression of glial fibrillary acidic protein and transferrin in cultured astrocytes. Glia 8, 7786.Google Scholar
Pece, S. and Gutkind, J.S. (2000) Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. Journal of Biological Chemistry 275, 4122741233.Google Scholar
Pforte, C., Henrich-Noack, P., Baldauf, K. and Reymann, K.G. (2005) Increase in proliferation and gliogenesis but decrease of early neurogenesis in the rat forebrain shortly after transient global ischemia. Neuroscience 136, 11331146.Google Scholar
Qian, X., Karpova, T., Sheppard, A.M., McNally, J. and Lowy, D.R. (2004) E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO Journal 23, 17391748.Google Scholar
Rathbone, M.P., Middlemiss, P., Andrew, C., Caciagli, F., Ciccarelli, R., Di Iorio, P. et al. (1998) The trophic effects of purines and purinergic signaling in pathologic reactions of astrocytes. Alzheimer Disease and Associated Disorders 12, S36S45.Google Scholar
Redfield, A., Nieman, M.T. and Knudsen, K.A. (1997) Cadherins promote skeletal muscle differentiation in three-dimensional cultures. Journal of Cell Biology 138, 13231331.Google Scholar
Richter-Landsberg, C. and Heinrich, M. (1995) S-100 immunoreactivity in rat brain glial cultures is associated with both astrocytes and oligodendrocytes, Journal of Neuroscience Research. 42, 657665.Google Scholar
Ridet, J.L., Malhotra, S.K., Privat, A. and Gage, F.H. (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends in Neurosciences 20, 570577.Google Scholar
Rodger, J., Lindsey, K.A., Leaver, S.G., King, C.E., Dunlop, S.A. and Beazley, L.D. (2001) Expression of ephrin-A2 in the superior colliculus and EphA5 in the retina following optic nerve section in adult rat. European Journal of Neuroscience 14, 19291936.Google Scholar
Roitbak, T. and Syková, E. (1999) Diffusion barriers evoked in the rat cortex by reactive astrogliosis. Glia 28, 4048.Google Scholar
Sakaguchi, M., Miyazaki, M., Inoue, Y., Tsuji, T., Kouchi, H., Tanaka, T. et al. (2000) Relationship between contact inhibition and intranuclear S100C of normal human fibroblasts. Journal of Cell Biology 149, 11931206.Google Scholar
Schönekess, B.O. and Walsh, M.P. (1997) Molecular cloning and expression of avian smooth muscle S100A11 (calgizzarin, S100C). Biochemistry and Cell Biology 75, 771775.Google Scholar
Schwab, M.E. and Caroni, P. (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. Journal of Neuroscience 8, 23812393.Google Scholar
Scotto, C., Deloulme, J.C., Rousseau, D., Chambaz, E. and Baudier, J. (1998) Calcium and S100B regulation of p53-dependent cell growth arrest and apoptosis. Molecular and Cellular Biology 18, 42724281.Google Scholar
Sestan, N., Artavanis-Tsakonas, S. and Rakic, P. (1999) Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 286, 741746.Google Scholar
Sheng, J.G., Mrak, R.E., Rovnaghi, C.R., Kozlowska, E., Van Eldik, L.J. and Griffin, W.S. (1996) Human brain S100 beta and S100 beta mRNA expression increases with age: pathogenic implications for Alzheimer's disease. Neurobiology of Aging 17, 359363.Google Scholar
St Croix, B., Sheehan, C., Rak, J.W., Florenes, V.A., Slingerland, J.M. and Kerbel, R.S. (1998) E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). Journal of Cell Biology 142, 557571.Google Scholar
Takeichi, M. (1998) The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102, 639655.Google Scholar
Tang, S., Shen, Y.J., DeBellard, M.E., Mukhopadhyay, G., Salzer, J.L., Crocker, P.R. and Filbin, M.T. (1997) Myelin-associated glycoprotein interacts with neurons via a sialic acid binding site at ARG118 and a distinct neurite inhibition site. Journal of Cell Biology 138, 13551366.Google Scholar
Tian, D.S., Yu, Z.Y., Xie, M.J., Bu, B.T., Witte, O.W. and Wang, W. (2006) Suppression of astroglial scar formation and enhanced axonal regeneration associated with functional recovery in a spinal cord injury rat model by the cell cycle inhibitor olomoucine. Journal of Neuroscience Research 84, 10531063.Google Scholar
Trapp, B.D. (1988) Distribution of the myelin-associated glycoprotein and P0 protein during myelin compaction in quaking mouse peripheral nerve. Journal of Cell Biology 107, 675685.Google Scholar
Trapp, B.D. (1990) Myelin-associated glycoprotein. Location and potential functions. Annals of the New York Academy of Sciences 605, 2943.Google Scholar
Wahl, S., Barth, H., Ciossek, T., Aktories, K. and Mueller, B.K. (2000) Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. Journal of Cell Biology 149, 263270.Google Scholar
Wang, H.U. and Anderson, D.J. (1997) Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18, 383396.Google Scholar
Wang, S., Sdrulla, A.D., DiSibio, G., Bush, G., Nofziger, D., Hicks, C. et al. (1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21, 6375.Google Scholar
Watanabe, M., Ando, Y., Todoroki, H., Minami, H. and Hidaka, H. (1991) Molecular cloning and sequencing of a cDNA clone encoding a new calcium binding protein, named calgizzarin, from rabbit lung. Biochemical Biophysical Research Communications 181, 644649.Google Scholar
Wieser, R.J., Schütz, S., Tschank, G., Thomas, H., Dienes, H.P. and Oesch, F. (1990) Isolation and characterization of a 60-70-kD plasma membrane glycoprotein involved in the contact-dependent inhibition of growth. Journal of Cell Biology 111, 26812692.Google Scholar
Williams, E.J., Williams, G., Howell, F.V., Skaper, S.D., Walsh, F.S. and Doherty, P. (2001) Identification of an N-cadherin motif that can interact with the fibroblast growth factor receptor and is required for axonal growth. Journal of Biological Chemistry 276, 4387943886.Google Scholar
Willson, C.A., Irizarry-Ramírez, M., Gaskins, H.E., Cruz-Orengo, L., Figueroa, J.D., Whittemore, S.R. et al. (2002) Upregulation of EphA receptor expression in the injured adult rat spinal cord. Cell Transplantation 11, 229239.Google Scholar
Yong, V.W., Moumdjian, R., Yong, F.P., Ruijs, T.C., Freedman, M.S., Cashman, N. et al. (1991) Gamma-interferon promotes proliferation of adult human astrocytes in vitro and reactive gliosis in the adult mouse brain in vivo. Proceedings of the National Academy of Sciences of the U.S.A. 88, 70167020.Google Scholar
Yue, Y., Su, J., Cerretti, D.P., Fox, G.M., Jing, S. and Zhou, R. (1999) Selective inhibition of spinal cord neurite outgrowth and cell survival by the Eph family ligand ephrin-A5. Journal of Neuroscience 19, 1002610035.Google Scholar