Nervous system proteoglycans as modulators of neurite outgrowth

Bovolenta, Paola; Fernaud-Espinosa, Isabel

doi:10.1016/s0301-0082(99)00044-1

Cited by 162 publications

(89 citation statements)

References 179 publications

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“…Using in vitro assays, we have shown in the present study that intervertebral disc aggrecan, which forms a major component of the discal ECM, inhibits neurite initiation and neurite outgrowth and induces sensory nerve growth cone turning in a concentration-dependent manner. Although these inhibitory effects compare with the results of previous studies using nonhuman proteoglycans derived from cartilage (9) and neural tissue (10), the effects of different types of proteoglycan vary, and some may even promote nerve growth (14). Thus, this study represents an important initial step in determining factors that may influence new nerve growth into degenerated intervertebral discs.…”

Section: Discussionsupporting

confidence: 66%

Human intervertebral disc aggrecan inhibits nerve growth in vitro

Johnson¹,

Caterson²,

Eisenstein³

et al. 2002

Arthritis & Rheumatism

164

136

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Objective. To assess the effects of human intervertebral disc aggrecan on nerve growth and guidance, using in vitro techniques.Methods. Aggrecan extracted from human lumbar intervertebral discs was incorporated into tissue culture substrata for the culture of the human neuronal cell line, SH-SY5Y, or explants of chick dorsal root ganglia. The effects on nerve growth of different concentrations of aggrecan extracted from the anulus fibrosus and nucleus pulposus, and of these aggrecan preparations following enzymic deglycosylation, were compared.Results. Disc aggrecan inhibited the growth of neurites from SH-SY5Y cells and induced growth cone turning of chick sensory neurites in a concentrationdependent manner. Aggrecan isolated from the anulus fibrosus was more inhibitory than that isolated from the nucleus pulposus, but enzymic pretreatments to reduce the glycosylation of both types of disc aggrecan partially abrogated their inhibitory effects.Conclusion. Nerve growth into degenerate intervertebral discs has been linked with the development of low back pain, but little is known about factors affecting disc innervation. The finding that disc aggrecan inhibits nerve growth in vitro, and that this inhibitory activity depends on aggrecan glycosylation, has important implications for our understanding of mechanisms that may regulate disc innervation in health and disease.

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Section: Discussionsupporting

confidence: 66%

Human intervertebral disc aggrecan inhibits nerve growth in vitro

Johnson¹,

Caterson²,

Eisenstein³

et al. 2002

Arthritis & Rheumatism

164

136

View full text Add to dashboard Cite

show abstract

“…The ECM and several guidance cues that are associated with the ECM have been shown to be important regulators of axon extension and guidance at all stages of differentiation (Letourneau et al, 1992;Bovolenta and Fernaud-Espinosa, 2000). ECM components, such as proteoglycans (PGs) not only trap guidance cues and enhance binding with their receptors, but also modulate adhesive interactions directly both by favoring or inhibiting axon outgrowth (Margolis and Margolis, 1997;Bovolenta and Fernaud-Espinosa, 2000).…”

Section: Extracellular Matrix Components On Immature Granule Cells Armentioning

confidence: 99%

“…ECM components, such as proteoglycans (PGs) not only trap guidance cues and enhance binding with their receptors, but also modulate adhesive interactions directly both by favoring or inhibiting axon outgrowth (Margolis and Margolis, 1997;Bovolenta and Fernaud-Espinosa, 2000).…”

Section: Extracellular Matrix Components On Immature Granule Cells Armentioning

confidence: 99%

The Stop Signal Revised: Immature Cerebellar Granule Neurons in the External Germinal Layer Arrest Pontine Mossy Fiber Growth

Manzini¹,

Ward²,

Zhang³

et al. 2006

J. Neurosci.

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During the formation of neuronal circuits, afferent axons often enter target regions before their target cells are mature and then make temporary contacts with nonspecific targets before forming synapses on specific target cells. The regulation of these different steps of afferent-target interactions is poorly understood.The cerebellum is a good model for addressing these aspects, because cerebellar development is well defined and identified neurons in the circuitry can be purified and combined in vitro. Previous reports from our laboratory showed that cultured granule neurons specifically arrest the extension of their pontine mossy fiber afferents, leading us to propose that granule cells arrested growth of their afferents as a prelude to synaptogenesis. However, we knew little about the differentiation state of the cultured granule cells that mediate afferent arrest.In this study, we better define the purified granule cell fraction by marker expression and morphology, and demonstrate that only freshly plated granule cells in the precursor and premigratory state arrest mossy fiber outgrowth. Mature granule cells, in contrast, support extension, defasciculation, and synapse formation, as in vivo. In addition, axonal tracing in vivo during the first postnatal week indicates that immature mossy fibers extend into the Purkinje cell layer but never into the external germinal layer (EGL), where precursors of granule cell targets reside. We found that the stop-growing signals are dependent on heparin-binding factors, and we propose that such signals in the EGL restrict the extension of mossy fiber afferents and prevent invasion of proliferative regions.

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“…regrowing axons (for review, see Fawcett and Asher, 1999;Bovolenta and Fernaud-Espinosa, 2000). CSs contribute to this inhibition, because treatment of lesion sites with chondroitinase renders these more supportive to axon growth in vitro (McKeon et al, 1995;Zuo et al, 1998) and in vivo (Yick et al, 2000;Moon et al, 2001).…”

mentioning

confidence: 99%

Repellent Guidance of Regenerating Optic Axons by Chondroitin Sulfate Glycosaminoglycans in Zebrafish

Becker

2002

J. Neurosci.

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We analyzed the role of chondroitin sulfate (CS) glycosaminoglycans, putative inhibitors of axonal regeneration in mammals, in the regenerating visual pathway of adult zebrafish. In the adult, CS immunoreactivity was not detectable before or after an optic nerve crush in the optic nerve and tract but was constitutively present in developing and adult nonretinorecipient pretectal brain nuclei, where CSs may form a boundary preventing regenerating optic fibers from growing into these inappropriate locations. Enzymatic removal of CSs by chondroitinase ABC after optic nerve crush significantly increased the number of animals showing erroneous growth of optic axons into the nonretinorecipient magnocellular superficial/ posterior pretectal nucleus (83% vs 42% in controls). In vitro, a substrate border of CSs, but not heparan sulfates, strongly repelled regenerating retinal axons from adult zebrafish. We conclude that CSs contribute to repellent axon guidance during regeneration of the optic projection in zebrafish.

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Nervous system proteoglycans as modulators of neurite outgrowth

Cited by 162 publications

References 179 publications

Human intervertebral disc aggrecan inhibits nerve growth in vitro

Human intervertebral disc aggrecan inhibits nerve growth in vitro

The Stop Signal Revised: Immature Cerebellar Granule Neurons in the External Germinal Layer Arrest Pontine Mossy Fiber Growth

Repellent Guidance of Regenerating Optic Axons by Chondroitin Sulfate Glycosaminoglycans in Zebrafish

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