Neurotrophin Effects on Survival and Expression of Cholinergic Properties in Cultured Rat Septal Neurons under Normal and Stress Conditions

Nonner, Doris; Barrett, Ellen F.; Barrett, John N.

doi:10.1523/jneurosci.16-21-06665.1996

Cited by 38 publications

(50 citation statements)

References 76 publications

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“…The methods used for single-channel recording from patches of membrane from oocytes obtained from Xenopus laevis have been described (6, 7). The neurons used for recording were cultured from the hippocampal region of embryonic (e15) rat brain as described (20). Patch pipettes were fabricated from borosilicate (hard) glass (equivalent to Corning 7740 glass; Clark Electromedical Instruments, Reading, U.K.), and the tips were heat polished.…”

Section: Methodsmentioning

confidence: 99%

Voltage-induced membrane displacement in patch pipettes activates mechanosensitive channels

Gil

Silberberg

Magleby

1999

Proc. Natl. Acad. Sci. U.S.A.

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The patch-clamp technique allows currents to be recorded through single ion channels in patches of cell membrane in the tips of glass pipettes. When recording, voltage is typically applied across the membrane patch to drive ions through open channels and to probe the voltage-sensitivity of channel activity. In this study, we used video microscopy and single-channel recording to show that prolonged depolarization of a membrane patch in borosilicate pipettes results in delayed slow displacement of the membrane into the pipette and that this displacement is associated with the activation of mechanosensitive (MS) channels in the same patch. The membrane displacement, Ϸ1 m with each prolonged depolarization, occurs after variable delays ranging from tens of milliseconds to many seconds and is correlated in time with activation of MS channels. Increasing the voltage step shortens both the delay to membrane displacement and the delay to activation. Preventing depolarization-induced membrane displacement by applying positive pressure to the shank of the pipette or by coating the tips of the borosilicate pipettes with soft glass prevents the depolarization-induced activation of MS channels. The correlation between depolarization-induced membrane displacement and activation of MS channels indicates that the membrane displacement is associated with sufficient membrane tension to activate MS channels. Because membrane tension can modulate the activity of various ligand and voltage-activated ion channels as well as some transporters, an apparent voltage dependence of a channel or transporter in a membrane patch in a borosilicate pipette may result from voltage-induced tension rather than from direct modulation by voltage. M echanosensitive (MS) ion channels can act as transducers for the senses of touch, hearing, balance, and proprioception and also seem to be involved in the regulation of cell volume (1-3). MS channels in patches of membrane in the tips of patch pipettes are readily activated when the membrane is stretched by the application of negative pressure to the shank of the patch pipette (4). The stretching of the membrane patch by negative pressure is thought to activate the channels by increased tension in the membrane (5). When the pressure is released, the channels then readily deactivate. In addition to stretch activation, some MS channels can also be activated by voltage (1). In this regard, depolarization of membrane patches from Xenopus oocytes activates endogenous MS channels in the patch after prolonged delays of typically 1-20 s (6). After stepping the voltage back to negative potentials, the MS channels then deactivate over several seconds. The delayed activation is observed for both on-cell and excised patches and typically occurs in a cooperative manner, with all channels activating over a short period of time compared with the duration of the delay to activation.We have shown recently that the delayed activation of the MS channels is not observed in outside-out patches, in membrane outside of the patc...

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Section: Methodsmentioning

confidence: 99%

Voltage-induced membrane displacement in patch pipettes activates mechanosensitive channels

Gil

Silberberg

Magleby

1999

Proc. Natl. Acad. Sci. U.S.A.

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“…BDNF supports the survival of many types of neurons, including mesencephalic dopaminergic neurons (Knüsel et al, 1991), septal cholinergic neurons (Nonner et al, 1996), and striatal GABAergic neurons (Ventimiglia et al, 1995). This neurotrophin influences the development of patterned connections (Cabelli et al, 1995) and growth and complexity of dendrites in the cerebral cortex (McAllister et al, 1995).…”

mentioning

confidence: 99%

Involvement of Brain-Derived Neurotrophic Factor in Spatial Memory Formation and Maintenance in a Radial Arm Maze Test in Rats

et al. 2000

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Brain-derived neurotrophic factor (BDNF) regulates both shortterm synaptic functions and activity-dependent synaptic plasticity such as long-term potentiation. In the present study, we investigated the role of BDNF in the spatial reference and working memory in a radial arm maze test. The radial arm maze training resulted in a significant increase in the BDNF mRNA expression in the hippocampus, although the expression in the frontal cortex did not change. When spatial learning was inhibited by treatment with 7-nitroindazole, an inhibitor of brain nitric oxide synthase, the increase in the hippocampal BDNF mRNA did not occur. To clarify the causal relation between BDNF mRNA expression and spatial memory formation, we examined the effects of antisense BDNF treatment on spatial learning and memory. A continuous intracerebroventricular infusion of antisense BDNF oligonucleotide resulted in an impairment of spatial learning, although the sense oligonucleotide had no effect. Treatment with antisense, but not sense, BDNF oligonucleotide was associated with a significant reduction of BDNF mRNA and protein levels in the hippocampus. Furthermore, treatment with antisense BDNF oligonucleotide in rats, which had previously acquired spatial memory by an extensive training, impaired both reference and working memory. There were no differences in locomotor activity, food consumption, and body weight between the antisense and sense oligonucleotide-treated rats. These results suggest that BDNF plays an important role not only in the formation, but also in the retention and/or recall, of spatial memory.

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“…NGF and TrkA are important for BFCN development, maintenance, and function in vivo (Vantini et al, 1989;Li et al, 1995;Chen et al, 1997;Fagan et al, 1997;Molnar et al, 1998;Debeir et al, 1999;Ruberti et al, 2000), and NGF exposure (days to weeks) enhances cholinergic markers in BF cultures (Hartikka and Hefti, 1988;Takei et al, 1988Takei et al, , 1989Svendsen et al, 1994;Nonner et al, 1996;Pongrac and Rylett, 1998;Oosawa et al, 1999;Auld et al, 2001). The neurotrophins brain-derived neurotrophic factor (BDNF), neurotrophin-3 (NT-3), and neurotrophin-4 (NT-4) also enhance cholinergic markers (Nonomura et al, 1995;Nonner et al, 1996;Auld et al, 2001). Interestingly, even a 30 min exposure to NGF, BDNF, NT-3, or NT-4 increases choline acetyltransferase (ChAT) activity 24 hr later (Nonner et al, 2000).…”

Section: Abstract: Brain-derived Neurotrophic Factor; Choline Acetylmentioning

confidence: 99%

“…6 B). Considering that these neurons respond to NT-3, NT-4, and BDNF with increased ChAT activity (Nonomura et al, 1995;Nonner et al, 1996Nonner et al, , 2000, as well as retrogradely transport them from target regions (DiStefano et al, 1992), we sought to determine whether they acutely induced a persistent increase in ACh release. Under the same conditions as with NGF, a 60 min pretreatment with the other neurotrophins (10 ng/ml) also enhanced ACh release in the hour subsequent to their removal: NT-3, 153 Ϯ 6% of control (n ϭ 4; p Ͻ 0.001 vs control); NT-4, 161 Ϯ 16% (n ϭ 4; p Ͻ 0.01); and BDNF, 177 Ϯ 19% (n ϭ 4; p Ͻ 0.001).…”

Section: Brief Exposure To Neurotrophins Induces Prolonged Ach Releasementioning

confidence: 99%

Nerve Growth Factor Rapidly Induces Prolonged Acetylcholine Release from Cultured Basal Forebrain Neurons: Differentiation between Neuromodulatory and Neurotrophic Influences

2001

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Long-term exposure to nerve growth factor (NGF) is well established to have neurotrophic effects on basal forebrain cholinergic neurons, but its potential actions as a fast-acting neuromodulator are not as well understood. We report that NGF (0.1-100 ng/ml) rapidly (Ͻ60 min) and robustly enhanced constitutive acetylcholine (ACh) release (148-384% of control) from basal forebrain cultures without immediate persistent increases in choline acetyltransferase activity. More ACh was released in response to NGF when exposure was coupled with a higher depolarization level, suggesting activity dependence. In a longterm potentiation-like manner, brief NGF exposure (10 ng/ml; 60 min) induced robust and prolonged increases in ACh release, a capacity that was shared with the other neurotrophins. K252a (10-100 nM), BAPTA-AM (25 M), and Cd 2ϩ (200 M) prevented NGF enhancement of ACh release, suggesting the involvement of TrkA receptors, Ca 2ϩ , and voltage-gated Ca 2ϩ channels, respectively. Forskolin (10 M), a cAMP generator, enhanced constitutive ACh release but did not interact synergistically with NGF. Tetrodotoxin (1 M) and cycloheximide (2 M) did not prevent NGF-induced ACh release, indicative of action at the level of the cholinergic nerve terminal and that new protein synthesis is not required for this neurotransmitter-like effect, respectively. In contrast, after a 24 hr NGF treatment, distinct protein synthesis-dependent and independent effects on choline acetyltransferase activity and ACh release were observed. These results indicate that neuromodulator/neurotransmitter-like (protein synthesis-independent) and neurotrophic (translation-dependent) actions likely make distinct contributions to the enhancement of cholinergic activity by NGF.

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Neurotrophin Effects on Survival and Expression of Cholinergic Properties in Cultured Rat Septal Neurons under Normal and Stress Conditions

Cited by 38 publications

References 76 publications

Voltage-induced membrane displacement in patch pipettes activates mechanosensitive channels

Voltage-induced membrane displacement in patch pipettes activates mechanosensitive channels

Involvement of Brain-Derived Neurotrophic Factor in Spatial Memory Formation and Maintenance in a Radial Arm Maze Test in Rats

Nerve Growth Factor Rapidly Induces Prolonged Acetylcholine Release from Cultured Basal Forebrain Neurons: Differentiation between Neuromodulatory and Neurotrophic Influences

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