Effects of glial cell line-derived neurotrophic factor on axonal growth and apoptosis in adult mammalian sensory neurons in vitro

Leclere, Pascal; Ekström, Per; Edström, Anders; Priestley, John V.; Averill, Sharon; Tonge, David

doi:10.1016/s0306-4522(97)00307-2

Cited by 50 publications

(43 citation statements)

References 51 publications

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“…Scale bar, 200 m. (8) n ϭ 178 (16) n ϭ 78 (7) mine directly whether nerve segments released physiologically detectable GDNF-like activity, PN-DRGs were incubated in CM or RPMI medium containing concentrations of GDNF varying between 10 pg/ml and 50 ng/ml for 3 d and then labeled using IB4 and Cy3-or TRITC-conjugated avidin. As in our previous study (Leclere et al, 1998), we found that 50 ng/ml GDNF increased the numbers of outgrowing IB4-labeled axons and also observed significant increases at levels as low as 2 ng/ml but not at 100 or 10 pg/ml (Table 4). However, in preparations cultured in LNCM, although overall axonal outgrowth was clearly increased (Fig.…”

Section: Neurite Outgrowth In Media Conditioned By Cultured Peripherasupporting

confidence: 88%

“…10 A) but relatively few short IB4-labeled axons (Fig. 10 B) as observed in a previous study (Leclere et al, 1998). In three conditioned preparations in which the intercostals nerve was cut proximal to the initial crush site, before culture in the collagen gels, marked increase in outgrowth of GAP 43-positive axons (Fig.…”

Section: Neurite Outgrowth In Media Conditioned By Cultured Peripherasupporting

confidence: 77%

“…Because mAb 21/27 selectively blocks activity of NGF but not BDNF or NT-3 (Nanduri et al, 1994), it appears that most of the axonal growth-stimulating activity in both types of CM is attributable to NGF rather than other neurotrophins or GDNF. However, although recombinant GDNF stimulates axonal outgrowth from adult PN-DRGs in collagen gels, axons labeled by IB4 in such cultures were much shorter than those of other classes (Leclere et al, 1998). It is therefore possible that effects of GDNF present in the conditioned media samples might not be detected by sole measurement of axonal lengths.…”

Section: Neurite Outgrowth In Media Conditioned By Cultured Peripheramentioning

confidence: 97%

“…NGF, NT-3, and GDNF also promote axonal regeneration of adult neurons (Mohiuddin et al, 1995;Edström et al, 1996;Naveilhan et al, 1997;Leclere et al, 1998;Gavazzi et al, 1999;Ramer et al, 2000;Fine et al, 2002). BDNF does not stimulate growth of DRG axons in adult rodents (Malgrange et al, 1994;Edström et al, 1996;Kimpinski et al, 1997;Gavazzi et al, 1999), but BDNF and NT-4 both stimulate axonal growth from nodose ganglia (Wiklund and Ekström, 2000).…”

Section: Introductionmentioning

confidence: 97%

“…After peripheral nerve (PN) lesions, synthesis of NGF, BDNF, NT-4, and GDNF increases (Meyer et al, 1992;Funakoshi et al, 1993;Trupp et al, 1995;Naveilhan et al, 1997;Bar et al, 1998;Hoke et al, 2000Hoke et al, , 2002Dethleffsen et al, 2002). Because NGF and GDNF stimulate axonal growth from DRG neurons in vitro and in vivo (Edström et al, 1996;Naveilhan et al, 1997;Leclere et al, 1998;Gavazzi et al, 1999;Ramer et al, 2000;Fine et al, 2002), their upregulation in lesioned peripheral nerves might be expected to promote axonal regeneration.…”

Section: Introductionmentioning

confidence: 99%

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Impaired Axonal Regeneration by Isolectin B4-Binding Dorsal Root Ganglion NeuronsIn Vitro

Leclere¹,

Norman²,

Groutsi³

et al. 2007

J. Neurosci.

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The subpopulation of dorsal root ganglion (DRG) neurons recognized by Griffonia simplicifolia isolectin B4 (IB4) differ from other neurons by expressing receptors for glial cell line-derived neurotrophic factor (GDNF) rather than neurotrophins. Additionally, IB4-labeled neurons do not express the laminin receptor, ␣7-integrin (Gardiner et al., 2005), necessary for optimal axonal regeneration in the peripheral nervous system. In cultures of dissociated DRG neurons of adult mice on laminin, robust spontaneous neurite outgrowth from IB4-negative neurons occurs and is strongly enhanced by previous axotomy. In contrast, IB4-labeled neurons show little neurite outgrowth and do not express GAP 43, even after axotomy or culture with GDNF. Moreover, growth of their axons through collagen gels is impaired compared with other DRG neurons. To determine whether the sparse neurite outgrowth of IB4-labeled neurons is attributable to lack of integrin expression, DRG cultures were infected with a herpes simplex 1 vector encoding ␣7-integrin, but its forced expression failed to promote neurite outgrowth in either IB4-labeled or other DRG neurons or in cultured adult retinal ganglion cells. Forced coexpression of both ␣7-integrin and GAP 43 also failed to promote neurite outgrowth in IB4-labeled neurons. In addition, cultured sciatic nerve segments were found to release much lower levels of GDNF, demonstrated by ELISA, than nerve growth factor. These findings together with their impaired intrinsic axonal regeneration capacity may contribute to the known vulnerability of the IB4-labeled population of DRG neurons to peripheral nerve injury.

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Section: Neurite Outgrowth In Media Conditioned By Cultured Peripherasupporting

confidence: 88%

Section: Neurite Outgrowth In Media Conditioned By Cultured Peripherasupporting

confidence: 77%

Section: Neurite Outgrowth In Media Conditioned By Cultured Peripheramentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

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Impaired Axonal Regeneration by Isolectin B4-Binding Dorsal Root Ganglion NeuronsIn Vitro

Leclere¹,

Norman²,

Groutsi³

et al. 2007

J. Neurosci.

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Axonal outgrowth from adult mouse nodose gangliain vitro is stimulated by neurotrophin-4 in a Trk receptor and mitogen-activated protein kinase-dependent way

Wiklund

Ekström

2000

J. Neurobiol.

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The actions of neurotrophic factors on sensory neurons of the adult nodose ganglion were studied in vitro. The ganglia were explanted in an extracellular matrix–based gel that permitted observation of the growing axons. Neurotrophin‐4 (NT‐4) was a very efficient stimulator of outgrowth of axons from the nodose ganglion and had almost doubled the outgrowth length when this was analyzed after 2 days in culture. Brain‐derived neurotrophic factor also stimulated outgrowth, but to a lesser degree, whereas NT‐3 gave only weak stimulatory tendencies. Nerve growth factor and glial cell line–derived neurotrophic factor both lacked stimulatory effects. NT‐4 is known to act via TrkB receptors, and the presence of these on growing nodose neurons was demonstrated immunohistochemically. In line with a Trk‐mediated growth effect, the NT‐4 stimulation was abolished by K252a, a selective inhibitor of neurotrophin receptor–associated tyrosine kinase activity. K252a had no effect on the unstimulated preparation. NT‐4 treatment led to activation of the mitogen‐activated protein kinase and inhibition of the latter pathway by PD98059 significantly reduced the NT‐4 stimulated outgrowth, whereas the drug had no effect on the unstimulated growth. In conclusion, the data suggest that NT‐4 can serve as a powerful growth factor for neurons of adult nodose ganglia and that the growth stimulation involves TrkB‐ and mitogen‐activated protein kinase. © 2000 John Wiley & Sons, Inc. J Neurobiol 45: 142–151, 2000

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Pericellular Griffonia simplicifolia I isolectin B4‐binding ring structures in the dorsal root ganglia following peripheral nerve injury in rats

Zhou

2001

J of Comparative Neurology

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Patients with a peripheral nerve injury often suffer from persistent chronic pain, but the underlying mechanism remains largely unknown. The persistent nature of the pain suggests injury-induced profound structural changes along the sensory pathways. In the present study, using the plant Griffonia simplicifolia I isolectin B4 (IB4) as a marker for nonpeptidergic small sensory neurons, we sought to examine whether these neurons sprout in the dorsal root ganglia (DRG) in response to peripheral nerve injury. The lumbar 5 (L5) spinal nerve was transected, and rats were allowed to survive for varying lengths of time before IB4 histology was performed. We found that a subpopulation of IB4-positive sensory neurons sprouted robustly after spinal nerve injury. Twelve weeks after spinal nerve injury, the IB4-positive ring structures became dramatic and encircled both large and small neurons in the DRG. The aberrant sprouting of small sensory neurons was also demonstrated by retrograde labeling. The processes of satellite cells surrounding large sensory neurons also became IB4 positive, and 87.8% of perineuronal IB4-positive ring structures intermingled and/or coexpressed with glial fibrillary acidic protein-positive satellite cells. Thus, the sprouting axons of IB4-positive neurons were intermingled with IB4-positive satellite cells, forming perineuronal ring structures surrounding large-diameter neurons. Ultrastructural examinations further confirmed that IB4-positive nerve terminals were entangled with satellite cells and IB4-negative unmyelinated sprouting fibers around sensory neurons. These studies have provided the first evidence that a subpopulation of IB4-binding small sensory neurons sprouts and forms perineuronal ring structures together with IB4-positive satellite cells in response to nerve injury. The significance of the sprouting of IB4-positive neurons remains to be determined.

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Effects of glial cell line-derived neurotrophic factor on axonal growth and apoptosis in adult mammalian sensory neurons in vitro

Cited by 50 publications

References 51 publications

Impaired Axonal Regeneration by Isolectin B4-Binding Dorsal Root Ganglion NeuronsIn Vitro

Impaired Axonal Regeneration by Isolectin B4-Binding Dorsal Root Ganglion NeuronsIn Vitro

Axonal outgrowth from adult mouse nodose gangliain vitro is stimulated by neurotrophin-4 in a Trk receptor and mitogen-activated protein kinase-dependent way

Pericellular Griffonia simplicifolia I isolectin B4‐binding ring structures in the dorsal root ganglia following peripheral nerve injury in rats

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