Neurite elongation on chondroitin sulfate proteoglycans is characterized by axonal fasciculation

Experimental Neurology

Volumn 182, Issue 2, 2003, Pages 310-321

  Snow, Diane M ^a,b   Smith, Jeffrey D ^a   Cunningham, Andrew T ^a   McFarlin, Jessica ^a   Goshorn, Eric C ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Axon outgrowth; Development; Dorsal root ganglia neurons; Extracellular matrix; Laminin; Proteoglycans (PGs); Retina

Indexed keywords

GROWTH PROMOTOR; LAMININ 1; PROTEOCHONDROITIN SULFATE;

ANIMAL TISSUE; ARTICLE; CELL ELONGATION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; FASCICULATION; GROWTH CONE; NERVE CELL; NERVE FIBER; NEURITE; NONHUMAN; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SPINAL GANGLION;

EID: 0042697061     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00034-7     Document Type: Article

References (97)

1. Acheson A., Sunshine J.L., Rutishauser U. NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol. 114:1991;143-153.
2. Agresti C., Aloisi F., Levi G. Heterotypic and homotypic cellular interactions influencing the growth and differentiation of bipotential oligodendrocyte-type-2 astrocyte progenitors in culture. Dev. Biol. 144:1991;16-29.
3. Aquino D.A., Margolis R.U., Margolis R.K. Immunocytochemical localization of a chondroitin sulfate proteoglycan in nervous tissue. II. Studies in developing brain. J. Cell Biol. 99:1984;1130-1139.
4. Asher R.A., Morgenstern D.A., Moon L.D., Fawcett J.W. Chondroitin sulfate proteoglycans inhibitory components of the glial scar . Prog. Brain Res. 132:2001;611-619.
5. Asher R., Morgenstern D., Shearer M., Adcock K., Pesehva P., Fawcett J. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J. Neurosci. 22:2002;2225-2236.
6. Bagnard D., Lohrum M., Uziel D., Puschel A., Bolz J. Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development. 125:1998;5043-5053.
7. Bastiani M.J., Harrelson A.L., Snow P.M., Goodman C.S. Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell. 48:1987;745-755.
8. Bastmeyer M., Ott H., Leppert C.A., Steurmer C. Fish E587 glycoprotein, a member of the L1 family of cell adhesion molecules, participates in axonal fasciculation and the age-related order of ganglion cell axons in the goldfish retina. J. Cell Biol. 130:1995;969-976.
9. Becker C.G., Becker T. Repellant guidence of regenerating optic axons by chondroitin sulfate glycosaminoglycans in zebrafish. J. Neurosci. 22:2002;842-853.
10. Behar O., Mizuno K., Badminton M., Woolf C. Semaphorin 3A growth cone collapse requires a sequence homologous to tarantula hanatoxin. Proc. Natl. Acad. Sci. USA. 96:1999;13501-13505.
11. Berardi M., Hindelang C., Felix J.M., Stoeckel M.E. L1 and laminin their expression during rat hypophysis ontogenesis and in adult neurohemal areas . Int. J. Dev. Neurosci. 17:1999;121-130.
12. Bicknese A.R., Sheppard A.M., O'Leary D.D.M., Pearlman A.L. Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J. Neurosci. 14:1994;3500-3510.
13. Bignami A., Perides G., Rahemtulla F. Versican, a hyaluronate-binding proteoglycan of embryonal precartilaginous mesenchyma, is mainly expressed postnatally in rat brain. J. Neurosci. Res. 34:1993;97-106.
14. Birgbauer E., Oster S.F., Severin C.G., Sretavan D.W. Retinal axon growth cones respond to EphB extracellular domains as inhibitory axon guidance cues. Develop. 128:2001;3041-3048.
15. Bradbury E.J., Moon L.D.F., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 416:2002;636-640.
16. Brittis P.A., Canning D.R., Silver J. Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science. 255:1992;733-736.
17. Brittis P.A., Lemmon V., Rutishauser U., Silver J. Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations a time-lapse study of the living retina . Mol. Cell. Neurosci. 6:1995;433-449.
18. Brittis P.A., Silver J. Multiple factors govern intraretinal axon guidance a time-lapse study . Mol. Cell. Neurosci. 6:1995;413-432.
19. Burden-Gulley S.M., Lemmon V. L1, N-cadherin, and laminin induce distinct distribution patterns of cytoskeletal elements in growth cones. Cell Motil. Cytoskeleton. 35:1996;1-23.
20. Cervello M., Lemmon V., Landreth G., Rutishauser U. Phosphorylation-dependent regulation of axon fasciculation. Proc. Natl. Acad. Sci. USA. 88:1991;10548-10552.
21. 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. 273:1998;28444-28453.
22. Cohen N.R., Taylor J.S., Scott L.B., Guillery R.W., Soriano P., Furley A.J. Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol. 8:1998;26-33.
23. Condic M.L., Snow D.M., Letourneau P.C. Embryonic neurons adapt to the inhibitory proteoglycan aggrecan by increasing integrin expression. J. Neurosci. 19:1999;10036-10043.
24. David S., Braun P.E., Jackson D.L., Kottis A., McKerracher L. Laminin overrides the inhibitory effects of peripheral nervous system and central nervous system myelin-derived inhibitors of neurite growth. J. Neurosci. Res. 42:1995;594-602.
25. Davis G.E., Klier F.G., Engvall E., Cornbrooks C., Varon S., Manthorpe M. Association of laminin with heparan and chondroitin sulfate-bearing proteoglycans in neurite-promoting factor complexes from rat Schwannoma cells. Neurochem. Res. 12:1987;909-921.
26. Dillon G.P., Yu X., Bellamkonda R.V. The polarity and magnitude of ambient charge influences three-dimensional neurite extension from DRGs. J. Biomed. Mater. Res. 51:2000;510-519.
27. Dou C., Levine J. Identification of a neuronal cell surface receptor for a growth inhibitory chondroitin sulfate proteoglycan (NG2). J. Neurochem. 68:1997;1021-1030.
28. Dou C.L., Levine J.M. Differential effects of glycosaminoglcyans on neurite growth on laminin and L1 substrates. J. Neurosci. 15:1995;8053-8066.
29. Emerling D.E., Lander A.D. Inhibitors and promoters of thalamic neuron adhesion and outgrowth in embryonic neocortex functional association with chondroitin sulfate . Neuron. 17:1996;1089-1100.
30. Ernst H., Zanin M.K.B., Everman D., Hoffman S. Receptor-mediated adhesive and anti-adhesive functions of chondroitin sulfate proteoglycan preparations from embryonic chick brain. J. Cell Sci. 108:1995;3807-3816.
31. Faissner A., Clement A., Lochter A., Streit A., Mandl C., Schachner M. Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J. Cell Biol. 126:1994;783-799.
32. Faissner A., Steindler D. Boundaries and inhibitory molecules in developing neural tissues. Glia. 13:1995;233-254.
33. Fitch M.T., Silver J. Beyond the glial scar cellular and molecular mechanisms by which glial cells contribute to CNS regenerative failure . Tuszynski M.H., Kordower J.H. CNS Regeneration Basic Science and Clinical Advances . 1999;55-88 Academic Press, New York.
34. Flanders K.C., Ludecke G., Engels S., Cissel D.S., Roberts A.B., Kondaiah P., Lafyatis R., Sporn M.B., Unsicker K. Localization and actions of transforming growth factor-βs in the embryonic nervous system. Development. 113:1991;183-191.
35. Fransen E., D'Hooge R., Van Camp G., Verhoye M., Sijbers J., Reyniers E., Soriano P., Kamiguchi H., Willemsen R., Koekkoek S.K., DeZeeuw C.I., De Deyn P.P., Van der Linden A., Lemmon V., Kooy R.F., Willems P.J. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum. Mol. Genet. 7:1998;999-1009.
36. Friedlander D.R., Milev P., Karthikeyan L., Margolis R.K., Margolis R.U., Grumet M. The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J. Cell Biol. 125:1994;669-680.
37. Fukudu T., Kawano H., Ohyama K., Li H.P., Takeda Y., Oohira A., Kawamura K. Immunohistochemical localization of neurocan and L1 in the formation of the thalamocortical pathway of developing rats. J. Comp. Neurol. 382:1997;141-152.
38. Garwood J., Schnädelbach O., Clement A., Schütte K., Bach A., Feissner A. DSD-1-proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J. Neurosci. 19:1999;3888-3899.
39. Gates M.A., Fillmore H., Steindler D.A. Chondroition sulfate proteoglycan and tenascin in the wounded adult mouse neostriatum in vitro dopamine neuron attachment and process outgrowth . J. Neurosci. 16:1996;8005-8018.
40. Halfter W. Antisera to basal lamina and glial endfeet disturb the normal extension of axons on retina and pigment epithelium basal laminae. Development. 107:(2):1989;281-297.
41. Hoffman-Kim D., Lander A., Jhaveri S. Patterns of chondroitin sulfate immunoreactivity in the developing tectum reflect regional differences in glycosaminoglycan biosynthesis. J. Neurosci. 18:1998;5881-5890.
42. Hoke, A., Silver, J., 1996. Proteoglycans and other repulsive molecules in glial boundaries during development and regeneration of the nervous system, in: Mize, R., Erzurumlu, R. (Eds.), Progress in Brain Research, Vol. 108, Elsevier Science B.V., pp. 149-163.
43. Honig M., Petersen G., Rutishauser U., Camilli J. In vitro studies of growth cone behavior support a role for fasciculation mediated by cell adhesion molecules in sensory axon guidance during development. Dev. Biol. 204:1998;317-326.
44. Honig M.G., Rutishauser U. Changes in the segmental pattern of sensory neuron projections in the chick hindlimb under conditions of altered cell adhesion molecule function. Dev. Biol. 175:1996;325-337.
45. Hynds D.L., Snow D.M. Neurite outgrowth inhibition by chondroitin sulfate proteoglycan stopping/stalling exceed turning in human neuroblastoma growth cones . Exp. Neurol. 160:1999;244-255.
46. Inatani M., Honjo M., Otori Y., Oohira A., Kldo N., Tano Y., Honda Y., Tanihara H. Inhibitory effect of neurocan and phosphacan on neurite outgrowth from retinal ganglion cells in culture. Invest. Ophthalmol. Vis. Sci. 42:2001;1930-1938.
47. Jacobs J.R., Goodman C.S. Embryonic development of axon pathways in the Drosophila CNS. II. Behavior of pioneer growth cones. J. Neurosci. 9:1989;2412-2422.
48. Jaworski D.M., Kelly G.M., Hockfield S. BEHAB, a new member of the proteoglycan tandem repeat family of hyaluronan-binding proteins that is restricted to the brain. J. Cell Biol. 125:1994;495-509.
49. Jhaveri S., Erzurumlu R.S., Schneider G.E. The optic tract in embryonic hamsters fasciculation, defasciculation, and other rearrangements of retinal axons . Vis. Neurosci. 13:1996;359-374.
50. Kamiguchi H., Lemmon V. Neural cell adhesion molecule L1 signaling pathways and growth cone motility . J. Neurosci. Res. 49:1997;1-8.
51. Lagenaur C., Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc. Natl. Acad. Sci. USA. 84:1987;7753-7757.
52. Laywell E.D., Dorries U., Bartsch U., Faissner A., Schachner M., Steindler D.A. Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc. Natl. Acad. Sci. USA. 89:1992;2634-2638.
53. Lemmon V., Farr K.L., Lagenaur C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron. 2:1989;1597-1603.
54. Lemons M.L., Sandy J.D., Anderson D.K., Howland D.R. Intact aggrecan and fragments generated by both aggrecanse and metalloproteinase-like activites are present in the developing and adult rat spinal cord and their relative abundance is altered by injury. J. Neurosci. 21:2001;4772-4781.
55. Leppert C.A., Diekmann H., Paul C., Laessing U., Marx M., Bastmeyer M., Stuermer C. Neurolin Ig domain 2 participates in retinal axon guidance and Ig domains 1 and 3 in fasciculation. J. Cell Biol. 144:1999;339-349.
56. Letourneau P.C., Condic M.L., Snow D.M. Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14:1994;915-928.
57. Li M., Shibata A., Li C., Braun P.E., McKerracher L., Roder J., Kater S.B., David S. Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J. Neurosci. Res. 46:1996;404-414.
58. Luo Y., Raper J.A. Inhibitory factors controlling growth cone motility and guidance. Curr. Opin. Neurobiol. 4:1994;648-654.
59. Lyckman A.W., Moya K.L., Confaloni A., Jhaveri S. Early postnatal expression of L1 by retinal fibers in the optic tract and synaptic targets of the Syrian hamster. J. Comp. Neurol. 423:2000;40-51.
60. Margolis R.K., Rauch U., Maurel P., Margolis R.U. Neurocan and phosphacan two major nervous tissue-specific chondroitin sulfate proteoglycans . Perspect. Dev. Neurobiol. 3:1996;273-290.
61. Maurel P., Rauch U., Flad M., Margolis R.K., Margolis R.U. Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. Proc. Natl. Acad. Sci. USA. 91:1994;2512-2516.
62. Miranda J.D., White L., Marcillo A., Willson C., Jagid J., Whittemore S. Induction of Eph B3 after spinal cord injury. Exp. Neurol. 156:1999;218-222.
63. Morris J.E. Steric exclusion of cells a mechanism of glycosaminoglycan-induced cell aggregation . Exp. Cell Res. 120:1979;141-153.
64. Muir D., Engvall E., Varon S., Manthorpe M. Schwannoma cell-derived inhibitor of the neurite promoting activity of laminin. J. Cell Biol. 109:1989;2353-2362.
65. Nishiyama A., Dahlin K.J., Prince J.T., Johnstone S.R., Stallcup W.B. The primary structure of NG2, a novel membrane-spanning proteoglycan. J. Cell Biol. 114:1991;359-371.
66. Ohyama K., Kawano H., Asou H., Fukuda T.A.O., Uyemura K., Kawamura K. Coordinate expression of L1 and 6B4 proteoglycan/phosphacan is correlated with the migration of mesencephalic dopaminergic neurons in mice. Brain Res. Dev. Brain Res. 107:1998;219-226.
67. Payne H.R., Burden S.M., Lemmon V. Modulation of growth cone morphology by substrate-bound adhesion molecules. Cell Motil. Cytoskeleton. 21:1992;65-73.
68. Perris R., Lofberg J., Fallstrom C., Boxberg Y.v., Olsson L., Newgreen D.F. Structural and compositional divergencies in the extracellular matrix encountered by neural crest cells in the white mutant axolotl embryo. Development. 109:1990;533-551.
69. Pettigrew D., Crutcher K. White matter of the CNS supports or inhibits neurite outgrowth in vivo depending on geometry. J. Neurosci. 19:1999;8358-8366.
70. Rathjen F., Schachner M. Immunocytochemical and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 3:1984;1-10.
71. Ring C., Lemmon V., Halfter W. Two chondroitin sulfate proteoglycans diferentially expressed in the developing chick visual system. Dev. Biol. 168:1995;11-27.
72. Ringstedt T., Braisted J.E., Brose K., Kidd T., Goodman C., Tessier-Lavigne M., O'Leary D.D.M. Slit inhibition of retinal axon growth and its role in retinal axon pathfinding and innervation patterns in the diencephalon. J. Neurosci. 20:2000;4983-4991.
73. Schwab M.E. Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci. 13:1990;452-456.
74. Schwartz N.B., Domowicz M., Krueger R.C.J., Li H., Mangoura D. Brain aggrecan. Perspect. Dev. Neurobiol. 3:1996;291-306.
75. Sheppard A.M., Hamilton S.K., Pearlman A.L. Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci. 11:1991;3928-3942.
76. Snow D., Watanabe M., Letourneau P.C., Silver J. A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development. 113:1991;1473-1485.
77. Snow D.M., Atkinson P.B., Hassinger T.D., Letourneau P.C., Kater S.B. Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev. Biol. 166:1994;87-100.
78. Snow D.M., Brown E.M., Letourneau P.C. Growth cone behavior in the presence of soluble chondroitin sulfate proteoglycan (CSPG), compared to behavior on CSPG bound to laminin or fibronectin. Int. J. Dev. Neurosci. 14:1996;331-349.
79. Snow D.M., Lemmon V., Carrino D.A., Caplan A.I., Silver J. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 109:1990;111-130.
80. Snow D.M., Letourneau P.C. Neurite outgrowth on a step gradient of chondroitin sulfate proteoglycan (CS-PG). J. Neurobiol. 23:1992;322-336.
81. Snow D.M., Smith J.D., Gurwell J.A. Binding characteristics of chondroitin sulfate proteoglycans and laminin-1, and correlative neurite outgrowth behaviors in a standard tissue culture choice assay. J. Neurobiol. 51:2002;285-301.
82. Snow D.M., Steindler D.A., Silver J. Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum a possible role for a proteoglycan in the development of an axon barrier . Dev. Biol. 138:1990;359-376.
83. Steindler D.A., Settles D., Erickson H.P., Laywell E.D., Yoshiki A., Faissner A., Kusakabe M. Tenascin knock-out mice barrels, boundary molecules, and glial scars . J. Neurosci. 15:1995;1973-1983.
84. Streit A., Nolte C., Rasony T., Schachner M. Interactions of astrochondrin with extracellular matrix components and its involvement in astrocyte process formation and cerebellar granule cell migration. J. Cell Biol. 120:1993;799-814.
85. Tang J., Rutishauser U., Landmesser L.T. Polysialic acid regulates growth cone behavior during sorting out of motor axons in the plexus region. Neuron. 13:1994;405-414.
86. Tang S., Qiu J., Nikulina E., Filbin M.T. Soluble myelin-associated glycoprotein released from damaged white matter inhibits axonal regeneration. Mol. Cell. Neurosci. 18:2001;259-269.
87. Tomaselli K.J., Doherty P., Emmett C.J., Damsky C.H., Walsh F.S., Reichardt L.F. Expression of β1 integrins in sensory neurons of the dorsal root ganglion and their function in neurite outgrowth on two laminin isoforms. J.Neurosci. 13:1993;4880-4888.
88. Tuttle R., Braisted J.E., Richards L.J., O'Leary D.M. Retinal axon guidance by region-specific cues in diencephalon. Development. 125:1998;791-801.
89. Tuttle R., Schlaggar B.L., Braisted J.E., O'Leary D.D.M. Maturation-dependent upregulation of growth-promoting molecules in developing cortical plate controls thalamic and cortical neurite growth. J. Neurosci. 15:1995;3039-3052.
90. Van Vactor D. Adhesion and signaling in axonal fasciculation. Curr. Opin. Neurobiol. 8:1998;80-86.
91. Wilson M.T., Snow D.M. Chondroitin sulfate proteoglycan expression pattern in hippocampal development potential regulation of axon tract formation . J. Comp. Neurol. 424:2000;532-546.
92. Winberg M., Mitchell K., Goodman C. Genetic analysis of the mechanisms controlling target selection complementary and combinatorial functions of netrins, semaphorins, and IgCAMs . Cell. 93:1998;581-591.
93. Xiao Z., Revest J., Laeng P., Rougon G., Schachner M., Montag D. Defasciculation of neurites is mediated by tenascin-R and its neuronal receptor F3/11. J. Neurosci. Res. 52:1998;390-404.
94. Yamada H., Watanabe K., Shimonaka M., Yamaguchi Y. Molecular cloning of brevican, a novel brain proteoglycan of the aggrecan/versican family. J. Biol. Chem. 269:1994;10119-10126.
95. Zuo J., Ferguson T., Hernandez Y., Stetler-Stevenson W., Muir D. Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J. Neurosci. 18:1998;5203-5211.
96. Zuo J., Hernandez Y., Muir D. Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury. J. Neurobiol. 34:1997;41-54.
97. Zuo J., Neubauer D., Dyess K., Ferguson T., Muir D. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp. Neurol. 154:1998;654-662.