The critical role of basement membrane-independent laminin γ1 chain during axon regeneration in the CNS

Journal of Neuroscience

Volumn 22, Issue 8, 2002, Pages 3144-3160

  Grimpe, Barbara ^a   Dong, Sucai ^b   Doller, Catherine ^a   Temple, Katherine ^a   Malouf, Alfred T ^a   Silver, Jerry ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Antisense ODN; Axon guidance; Dendritic spines; DNA enzyme; Extracellular matrix; Glial scar; Hippocampus; Organotypic slice cultures; Reactive astrocytes

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; ENZYME; LAMININ 1; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BRAIN SLICE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENDRITE; GLIA CELL; HIPPOCAMPUS; IMMUNOREACTIVITY; MACROGLIA; MOSSY FIBER; NERVE FIBER REGENERATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PYRAMIDAL NERVE CELL; RAT;

EID: 0037092427     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-08-03144.2002     Document Type: Article

References (136)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
2. Altschul SF, Madden TL, Schaeffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
3. Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
4. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438.
5. Bonner J, O'Connor TP (2001) The permissive cue laminin is essential for growth cone turning in vivo. J Neurosci 21:9782-9791.
6. Buchs P-A, Stoppini L, Muller D (1993) Structural modifications associated with synaptic development in area CA1 of rat hippocampal organotypic cultures. Brain Res Dev Brain Res 71:81-91.
7. Burg MA, Tillet E, Timpl R, Stallcup WB (1996) Binding of the NG2 proteoglycan to type VI collagen and other extracellular matrix molecules. J Biol Chem 271:26110-26116.
8. Burgeson RE, Chiquer M, Deutzmann R, Ekblom P, Engel J, Kleinmann H, Martin GR, Meneguzzi G, Paulson M, Sanes J, Timpl R, Tryggvason K, Yamada Y, Yurchenco PD (1994) A new nomenclature for the laminins. Matrix Biol 14:209-211.
9. Calof AL, Campanero MR, O'Rear JJ, Yurchenco PD, Lander AD (1994) Domain-specific activation of neuronal migration and neurite outgrowth-promoting activities of laminin. Neuron 13:117-130.
10. Canning DR, Hoke A, Malemud CJ, Silver J (1996) A potent inhibitor of neurite outgrowth that predominates in the extracellular matrix of reactive astrocytes. Int J Dev Neurosci 14:153-175.
11. Chauvet N, Parmentier ML, Alonso G (1995) Transected axons of adult hypothalamo-neurohypophysial neurons regenerate along tanycytic processes. J Neurosci Res 41:129-144.
12. Chicurel ME, Harris KM (1992) Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 325:169-182.
13. Cohen J, Johnson AR (1991) Differential effects of laminin and merosin on neurite outgrowth by retinal ganglion cells. J Cell Sci Suppl 15:1-7.
14. Cornbrooks CJ, Carey DJ, McDonald JA, Timpl R, Bunge RP (1983) In vivo and in vitro observation on laminin production by Schwann cells. Proc Natl Acad Sci USA 80:3850-3854.
15. Cremer H, Chazal G, Lledo PM, Rougon G, Montaron MF, Mayo W, Le Moal M, Abrous DN (2000) PSA-NCAM: An important regulator of hippocampal plasticity. Int J Dev Neurosci 18:213-220.
16. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683.
17. Davies SJ, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
18. Doucette R (1995) Olfactory ensheathing cells: Potential for glial cell transplantation into areas of CNS injury. Histol Histopathol 10:502-507.
19. Dow KE, Ethell DW, Steeves JD, Riopelle RJ (1994) Molecular correlates of spinal cord repair in the embryonic chick: Heparan sulfate and chondroitin sulfate proteoglycans. Exp Neurol 128:223-228.
20. Eckenhoff MF, Rakic P (1988) Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8:2729-2747.
21. Eddleston M, Mucke L (1993) Molecular profile of reactive astrocytes implications for their role in neurologic disease. Neuroscience 54:15-36.
22. Edgar D, Timpl R, Thoenen H (1984) The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J 3:1463-1468.
23. 32P-based hybridization. Anal Biochem 210:235-244.
24. Engvall E, Davis GE, Dickerson K, Ruoslahti E, Varon S, Manthorpe M (1986) Mapping of domains in human laminin using monoclonal antibodies: Localization of the neurite-promoting site. J Cell Biol 103:2457-2465.
25. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
26. Ferguson TA, Muir D (2000) MMP-2 and MMP-9 increase the neuritepromoting potential of Schwann cell basal laminae and are upregulated in degenerated nerve. Mol Cell Neurosci 16:157-167.
27. Fischer D, Heiduschka P, Thanos S (2001) Lens-injury-stimulated axonal regeneration throughout the optic pathway of adult rats. Exp Neurol 172:257-272.
28. Fitch MT, Doller C, Combs CK, Landreth GE, 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. J Neurosci 19:8182-8198.
29. Fouad K, Dietz V, Schwab ME (2001) Improving axonal growth and functional recovery after experimental spinal cord injury by neutralizing myelin-associated inhibitors. Brain Res Brain Res Rev 36:204-212.
30. Fry EJ, Saunders NR (2000) Spinal repair in immature animals: A novel approach using the South American opossum Monodelphis domestica. Clin Exp Pharmacol Physiol 27:542-547.
31. Gaarskjaer FB (1986) The organization and development of the hippocampal mossy fiber system. Brain Res Brain Res Rev 11:355-357.
32. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 92:11879-11883.
33. Garcia-Abreu J, Cavalcante LA, Neto VM (1995) Differential patterns of laminin expression in lateral and medial midbrain glia. NeuroReport 6:761-764.
34. Giger RJ, Pasterkamp RJ, Heijnen S, Holtmaat AJ, Verhaagen J (1998) Anatomical distribution of the chemorepellent semaphorin III/ collapsin-1 in the adult rat and human brain: Predominant expression in structures of the olfactory-hippocampal pathway and the motor system. J Neurosci Res 52:27-42.
35. Gonzales RB, DeLeon Galvan CJ, Rangel YM, Claiborne BJ (2001) Distribution of thorny excrescences on CA3 pyramidal neurons in the rat hippocampus. J Comp Neurol 430:357-368.
36. Gordon-Weeks PR, Giffin N, Weekes CS, Barben C (1989) Transient expression of laminin immunoreactivity in the developing rat hippocampus. J Neurocytol 18:451-463.
37. Grimpe B, Probst JC, Hager G (1999) Suppression of nidogen-1 translation by antisense targeting affects the adhesive properties of cultured astrocytes. Glia 28:138-149.
38. Groves AK, Entwistle A, Jat PS, Noble M (1993) The characterization of astrocyte cell lines that display properties of glial scar tissue. Dev Biol 159:87-104.
39. Gundersen RW (1987) Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Dev Biol 121:423-431.
40. Haas CA, Rauch U, Thon N, Meten T, Deller T (1999) Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19:9953-9963.
41. Hagg T, Muir D, Engvall E, Varon S, Manthorpe M (1989) Laminin-like antigen in rat CNS neurons: Distribution and changes upon brain injury and nerve growth factor treatment. Neuron 3:721-732.
42. Hagg T, Portera-Cailliau C, Jucker M, Engvall E (1997) Laminins of the adult mammalian CNS: Laminin-α2 (merosin M-) chain immunoreactivity is associated with neuronal processes. Brain Res 764:17-27.
43. Halfter W (1996) The behavior of optic axons on substrate gradients of retinal basal lamina proteins and merosin. J Neurosci 16:4389-4401.
44. Harrigan MR, Kunkeel DD, Nguyen LB, Malouf AT (1995) Betaamyloid is neurotoxic in hippocampal slice cultures. Neurobiol Aging 16:779-789.
45. Harris KM, Kater SB (1994) Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
46. Hunter DD, Shah V, Merlie JP, Sanes JR (1989) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338:229-234.
47. Isacson O, Deacon TW, Pakzaban P, Galpern WR, Dinsmore J, Burns LH (1995) Transplanted xenogeneic neural cells in neurodegenerative disease models exhibit remarkable axonal target specificity and distinct growth patterns of glial and axonal fibres. Nat Med 1:1189-1194.
48. Ivins JK, Colognato H, Kreidberg JA, Yurchenco PD, Lander AD (1998) Neuronal receptors mediating responses to antibody-activated laminin-1. J Neurosci 18:9703-9715.
49. Jontes JD, Smith SJ (2000) Filopodia, spines, and the generation of synaptic diversity. Neuron 27:11-14.
50. Joosten EA, Dijkstra S, Brook GA, Veldman H, Bar PR (2000) Collagen IV deposits do not prevent regrowing axons from penetrating the lesion site in spinal cord injury. J Neurosci Res 62:686-691.
51. Jucker M, Kleinman HK, Hoehmann C, Ordy JM, Ingram DK (1991) Distinct immunoreactivity to 110 kDa laminin-binding protein in adult and lesioned rat forebrain. Brain Res 555:305-312.
52. Kalil K, Reh T (1979) Regrowth of severed axons in the neonatal central nervous system: Establishment of normal connections. Science 205:1158-1161.
53. Kaplan MS, Hinds JW (1977) Neurogenesis in adult rat: Electron microscopic analysis of light radioautographs. Science 197:1092-1094.
54. Kennedy TE, Tessier-Lavigne M (1995) Guidance and induction of branch formation in developing axons by target-derived diffusible factors. Curr Opin Neurobiol 5:83-90.
55. Koch M, Olson PF, Albus A, Jin W, Hunter DD, Brunken WJ, Burgeson RE, Champliaud MF (1999) Characterization and expression of the laminin γ3 chain: A novel, non-basement membrane-associated, laminin chain. J Cell Biol 145:605-618.
56. Korkotian E, Segal M (2001) Regulation of dendritic spine motility in cultured hippocampal neurons. J Neurosci 21:6115-6124.
57. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
58. Kuhn TB, Schmidt MF, Kater SB (1995) Laminin and fibronectin guide-posts signal sustained but opposite effects to passing growth cones. Neuron 14:275-285.
59. Kunkel DD, Nguyen LB, Harrigan MR, Schwartzkroin PA, Malouf AT (1994) Somatostatin-containing neurons in rat organotypic hippocampal slice cultures: Light and electron microscopic immunocytochemistry. Hippocampus 4:157-166.
60. Kunkel-Bagden E, Dai HN, Bregman BS (1992) Recovery of function after spinal cord hemisection in newborn and adult rats: Differential effects on reflex and locomotor function. Exp Neurol 116:40-51.
61. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
62. Laurberg S, Zimmer J (1981) Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats. J Comp Neurol 200:433-459.
63. Lemons ML, Sandy JD, Anderson DK, Howland DR (2001) Intact aggrecan and fragments generated by both aggrecanase and metalloproteinase-like activities are present in the developing and adult rat spinal cord and their relative abundance is altered by injury. J Neurosci 21:4772-4781.
64. Leslie RA, Hunter AJ, Robertson HA (1999) Antisense Technology in the Central Nervous System. New York: Oxford UP.
65. Letourneau PC, Madsen AM, Palm SL, Furcht LT (1988) Immunoreactivity for laminin in the developing ventral longitudinal pathway of the brain. Dev Biol 125:1-8.
66. Li D, Field PM, Yoshioka M, Raisman G (1994) Axons regenerate with correct specificity in horizontal slice culture of the postnatal rat entorhino-hippocampal system. Eur J Neurosci 6:1026-1037.
67. Li Y, Field PM, Raisman G (1999) Death of oligodendrocytes and microglial phagocytosis of myelin precede immigration of Schwann cells into the spinal cord. J Neurocytol 28:417-427.
68. Libby RT, Xu Y, Gibbons EP, Hunter DD, Brunken WJ (1997) Identification and localization of laminin chains in human retina. Invest Ophthalmol Vis Sci 38:S30.
69. Libby RT, Lavallee CR, Balkema GW, Brunken WJ, Hunter DD (1999) Disruption of laminin β2 chain production causes alterations in morphology and function in the CNS. J Neurosci 19:9399-9411.
70. Liesi P (1990) Extracellular matrix and neuronal movement. Experientia 46:900-907.
71. Liesi P, Risteli L (1989) Glial cells of mammalian brain produce a variant form of laminin. Exp Neurol 105:86-92.
72. Liesi P, Silver J (1988) Is astrocyte laminin involved in axon guidance in the mammalian CNS? Dev Biol 130:774-785.
73. Liesi P, Seppala I, Trenkne E (1992) Neuronal migration in cerebellar microcultures is inhibited by antibodies against a neurite outgrowth domain of laminin. J Neurosci Res 33:170-176.
74. Luckenbill-Edds L (1997) Laminin and the mechanism of neuronal out-growth. Brain Res Brain Res Rev 23:1-27.
75. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951-955.
76. Manitt C, Colicos MA, Thompson KM, Rousselle E, Peterson AC, Kennedy TE (2001) Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord. J Neurosci 21:3911-3922.
77. Manthorpe M, Engvall E, Ruoslahti E, Longo FM, Davis GE, Varon S (1983) Laminin promotes neuritic regeneration from cultured peripheral and central neurons. J Cell Biol 97:1882-1890.
78. Matsuzawa M, Weight FF, Potember RS, Liesi P (1996) Directional neurite outgrowth and axonal differentiation of embryonic hippocampal neurons are promoted by a neurite outgrowth domain of the B2 chain of laminin. Int J Dev Neurosci 14:283-295.
79. McKeon RJ, Hoke A, Silver J (1995) Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136:32-43.
80. McLoon SC, McLoon LK, Palm SL, Furcht LT (1988) Transient expression of laminin in the optic nerve of the developing rat. J Neurosci 8:1981-1990.
81. McWilliams JR, Lynch G (1983) Rate of synaptic replacement in denervated rat hippocampus declines precipitously from the juvenile period to adulthood. Science 221:572-574.
82. Miller PD, Chung WW, Lagenaur CR, DeKosky ST (1993) Regional distribution of neural cell adhesion molecule (N-CAM) and L1 in human and rodent hippocampus. J Comp Neurol 327:341-349.
83. Mitchell KJ, Doyle JL, Serafini T, Kennedy TE, Tessier-Lavigne M, Goodman CS, Dickson BJ (1996) Genetic analysis of netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17:203-215.
84. Mizuhashi S, Nishiyama N, Matsuki N, Ikegaya Y (2001) Cyclic nucleotide-mediated regulation of hippocampal mossy fiber development: A target-specific guidance. J Neurosci 21:6181-6194.
85. Nakagami Y, Abe K, Nishiyama N, Matsuki N (2000) Laminin degradation by plasmin regulates long-term potentiation. J Neurosci 20:2003-2010.
86. Nguyen LB, Ricciardi TN, Malouf AT (1996) Reinnervation of stratum lucidum by hippocampal mossy fibers is developmentally regulated. Brain Res Dev Brain Res 95:184-193.
87. Niederost BP, Zimmermann DR, Schwab ME, Bandtlow CE (1999) Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J Neurosci 19:8979-8989.
88. Nieto-Sampedro M, Bovolenta P (1990) Growth factors and growth factor receptors in the hippocampus. Role in plasticity and response to injury. Prog Brain Res 83:341-355.
89. Nudel U, Zakut R, Shani M, Neuman S, Levy Z, Yaffa D (1983) The nucleotide sequence of the rat cytoplasmic β-actin gene. Nucleic Acids Res 11:1759-1771.
90. Obremski VJ, Bunge MB (1995) Addition of purified basal lamina molecules enables Schwann cell ensheathment of sympathetic neurites in culture. Dev Biol 168:124-137.
91. O'Keefe J, Nadel L (1978) The Hippocampus as a Cognitive Map, pp 102-140. New York: Oxford UP.
92. Oleszewski M, Beer S, Katich S, Geiger C, Zeller Y, Rauch U, Altevogt P (1999) Integrin and neurocan binding to L1 involves distinct Ig domains. J Biol Chem 274:24602-24610.
93. Olsen BR (1999) Life without perlecan has its problems. J Cell Biol 147:909-911.
94. Pasterkamp RJ, Giger RJ, Ruitenberg MJ, Holtmaat AJGD, De Wit J, De Winter F, Verhaagen J (1999) Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult, but not neonatal, CNS. Mol Cell Neurosci 13:143-166.
95. Patton BL, Miner JH, Chiu AY, Sanes JR (1997) Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 139:1507-1521.
96. Payne HR, Lemmon V (1993) Glial cells of the O-2A lineage bind preferentially to N-cadherin and develop distinct morphologies. Dev Biol 159:595-607.
97. Peterson DA (2002) Stem cells in brain plasticity and repair [portion of figure on cover]. Curr Opin Pharmacol 2:34-42.
98. Pindzola RR, Doller C, Silver J (1993) Putative inhibition extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesion. Dev Biol 156:34-48.
99. Powell SK, Rao J, Roque E, Nomizu M, Kuratomi Y, Yamada Y, Kleinman HK (2000) Neural cells respond to multiple novel sites on laminin-1. J Neurosci Res 61:302-312.
100. Prange O, Murphy TH (2001) Modular transport of postsynaptic density-95 clusters and association with stable spine precursors during early development of cortical neurons. J Neurosci 21:9325-9333.
101. Probst JC, Skutella T (1996) Elevated messenger RNA levels after antisense oligodeoxynucleotide treatment in vitro and in vivo. Biochem Biophys Res Commun 225:861-868.
102. Raisman G (1985) Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237-254.
103. Ramon-Cueto A, Avila J (1998) Olfactory ensheathing glia: Properties and function. Brain Res Bull 46:175-187.
104. Renaudin A, Lehmann M, Girault JA, McKerracher L (1999) Organization of point contacts in neuronal growth cones. J Neurosci Res 55:458-471.
105. Rudge JS, Silver J (1990) Inhibition of neurite outgrowth on astroglial scars in vitro. J Neurosci 10:3594-3603.
106. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
107. Santoro SW, Joyce GF (1997) A general purpose RNA-cleaving DNA enzyme. Proc Natl Acad Sci USA 94:4262-4266.
108. Sasaki M, Yamada Y (1987) The laminin B2 chain has a multidomain structure homologous to the B1 chain. J Biol Chem 262:17111-17117.
109. Scharff C, Kirn JR, Grossman M, Macklis JD, Nottebohm F (2000) Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25:481-492.
110. Schmidt CE, Dai J, Lauffenburger DA, Sheetz MP, Horwitz AF (1995) Integrin-cytoskeletal interactions in neuronal growth cones. J Neurosci 15:3400-3407.
111. Seil FJ (1998) The extracellular matrix molecule, laminin, induces Purkinje cell dendritic spine proliferation in granule cell-depleted cerebellar cultures. Brain Res 795:112-120.
112. Seki T, Arai Y (1991) The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci Res 12:503-513.
113. Seki T, Rutishauser U (1998) Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J Neurosci 18:3757-3766.
114. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
115. Smith GM, Miller RH, Silver J (1986) Changing role of forebrain astrocytes during development, regenerative failure, and induced regeneration upon transplantation. J Comp Neurol 251:23-43.
116. Smith GM, Rutishauser U, Silver J, Miller RH (1990) Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth. Dev Biol 138:377-390.
117. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulson M, Edgar D (1999) Absence of basement membrane after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144:151-160.
118. Steup A, Lohrum M, Hamscho N, Savaskan NE, Nimmemann O, Nitsch R, Fujisawa H, Pöschel AW, Skutella T (2000) Sema3C and netrin-1 differentially affect axon growth in the hippocampal formation. Mol Cell Neurosci 15:141-155.
119. Steward O (1976) Reinnervation of dentate gyrus by homologous afferents following entorhinal cortical lesions in adult rats. Science 194:426-428.
120. Stichel CC, Muller HW (1994) Relationship between injury-induced astrogliosis, laminin expression, and axonal sprouting in the adult rat brain. J Neurocytol 23:615-630.
121. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
122. Tang S, Qiu J, Nikulina E, Filbin MT (2001) Soluble myelin-associated glycoprotein released from damaged white matter inhibits axonal regeneration. Mol Cell Neurosci 18:259-269.
123. Timpl R, Rodde H, Robey PG, Rennard SI, Foidart J-M, Martin GR (1979) Laminin - A glycoprotein from basement membrane. J Biol Chem 254:9933-9937.
124. Tomaselli KJ, Doherty P, Emmett CJ, Damsky CH, Walsh FS, Reichardt LF (1993) Expression of γ1 integrin in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J Neurosci 13:4880-4888.
125. Tsui HCT, Lankford KL, Klein WL (1985) Differentiation of neuronal growth cones: Specialization of filopodial tips for adhesive interactions. Proc Natl Acad Sci USA 2:8256-8260.
126. Vanden Heuvel GB, Leardkamolkarn V, St. John PL, Abrahamson DR (1996) Carboxy terminal sequence and synthesis of rat kidney laminin γ1 chain. Kidney Int 49:752-760.
127. van Praag H, Christie BR, Palmer TD, Gage FH (2000) Characterization of retrovirally labeled newborn granule cells in the adult mouse dentate gyrus. 30th Annual Meeting Society for Neuroscience, New Orleans, LA.
128. Walsh FS, Doherty P (1997) Neural cell adhesion molecules of the immunoglobulin superfamily: Role in axon growth and guidance. Annu Rev Cell Dev Biol 13:425-456.
129. Willbold E, Rothermel A, Tomlinson S, Layer PG (2000) Mueller glia cells reorganize reaggregating chicken retinal cells into correctly laminated in vitro retinae. Glia 29:45-57.
130. Wilson MT, Snow DM (2000) Chondroitin sulfate proteoglycan expression pattern in hippocampal development: Potential regulation of axon tract formation. J Comp Neurol 424:532-546.
131. Wong EV, Kenwrick S, Willems P, Lemmon V (1995) Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci 18:168-172.
132. Woolhead CL, Zhang Y, Liebermann AR, Schachner M, Emson PC, Anderson PN (1998) Differential effects of autologous peripheral nerve grafts to the corpus striatum of adult rats on the regeneration of axons of striatal and nigral neurons and on the expression of GAP-43 and the cell adhesion molecules N-CAM and L1. J Comp Neurol 391:259-273.
133. Wu GY, Zou DJ, Rajan I, Cline H (1999) Dendritic dynamics in vivo change during neuronal maturation. J Neurosci 19:4472-4483.
134. Wujek JR, Haleem-Smith H, Yamada Y, Lipsky R, Lan YT, Freese E (1990) Evidence that the B2 chain of laminin is responsible for the neurite outgrowth-promoting activity of astrocyte extracellular matrix. Brain Res Dev Brain Res 55:237-247.
135. Zhou FC (1990) Four patterns of laminin-immunoreactive structure in developing rat brain. Brain Res Dev Brain Res 55:191-201.
136. Zimmer J, Gähwiler BH (1987) Growth of hippocampal mossy fibers: A lesion and coculture study of organotypic slice cultures. J Comp Neurol 264:1-13.