Localization of individual calcium channels at the release face of a presynaptic nerve terminal

Haydon, Philip G.; Henderson, Eric; Stanley, Elise F.

doi:10.1016/0896-6273(94)90414-6

Cited by 116 publications

(90 citation statements)

References 44 publications

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“…On the other hand, calcium channels were never found in patches of the exposed membrane surface of the bouton, in spite of the presence of a macroscopic calcium current (our unpublished observations). This could be explained by assuming that calcium channels are located in the releasing face of the bouton, as in other presynaptic terminals (Haydon et al, 1994). Should this be the case, it would reinforce the idea that type III boutons secrete into the synaptic space toward the muscle membrane.…”

Section: Discussionmentioning

confidence: 92%

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K⁺Currents

Martínez-Padrón

Ferrús

1997

J. Neurosci.

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We have performed direct electrophysiological recordings from Drosophila peptidergic synaptic boutons in situ, taking advantage of a mutation, ecdysone, which causes an increase in size of these terminals. Using patch-clamp techniques, we have analyzed voltage-dependent potassium currents at the macroscopic and single-channel level. The synaptic membrane contained at least two distinct voltage-activated potassium currents with different kinetics and voltage sensitivity: an I A -like current with fast activation and inactivation kinetics and voltage-dependent steady-state inactivation; a complex delayed current that includes a slowly inactivating component, resembling the I K described in other preparations; and a noninactivating component. The I A -like current in these peptidergic boutons is not encoded by the gene Shaker, because it is not affected by null mutations at this locus. Rather, synaptic I A has properties similar to those of the Shal-encoded I A . Singlechannel recordings revealed the presence in synaptic membranes of three different potassium channel types (A 2 , K D , K L ), with biophysical properties that could account for the macroscopic currents and resemble those of the Shal, Shab, and Shaw channels described in heterologous expression systems and Drosophila neuronal somata. A 2 channels (6 -9 pS) have brief open times, and like the macroscopic I A they exhibited voltage-dependent steady-state inactivation and a rapidly inactivating ensemble average current profile. K D channels (13-16 pS) had longer open times, activate and inactivate with much slower kinetics, and may account for the slowly inactivating component of the macroscopic current. K L (44 -54 pS) channels produced a noninactivating ensemble average and may contribute to the delayed macroscopic current observed.

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Section: Discussionmentioning

confidence: 92%

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K⁺Currents

Martínez-Padrón

Ferrús

1997

J. Neurosci.

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“…The validity of such CgTx-based approaches (Jones et al, 1989;Robitaille et al, 1990;Cohen et al, 1991;Komura and Rakic, 1992;Filloux et al, 1994;Haydon et al, 1994;Mills et al, 1994) is substantiated by the similar temporal expression patterns of the 220 kDa ␣ 1B subunit, -CgTx binding sites, and overall Fl--CgTx labeling. Our study also agrees with that of Filloux et al (1994), who used [ 125 I] -CgTx autoradiography to explore N-VDCC ontogeny in the rat brain; however, we did not detect the developmental increase in [ 125 I] -CgTx affinity reported by these authors.…”

Section: Discussionmentioning

confidence: 92%

“…Expression studies indicate that the precise complexion of gene products in the ␣ 1 , ␣ 2 /␦, and ␤-VDCC heteromers defines their pharmacology and biophysical characteristics (Hofmann et al, 1994;Dunlap et al, 1995). However, specific VDCC subtypes also have unique patterns of expression in discrete brain regions and even within individual neurons (Jones et al, 1989;Robitaille et al, 1990;Westenbroek et al, 1990Westenbroek et al, , 1992Westenbroek et al, , 1995Cohen et al, 1991;Hell et al, 1993;Haydon et al, 1994;Mills et al, 1994;Elliott et al, 1995). Thus, neurons may exploit V DCC diversity to tailor voltage-dependent Ca 2ϩ influx in discrete f unctional compartments .…”

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confidence: 99%

“…This V DCC has important roles in neurotransmitter release (Robitaille et al, 1990;Cohen et al, 1991;Haydon et al, 1994;Wheeler et al, 1994;Dunlap et al, 1995;Scholz and Miller, 1995), dendritic f unction (Mills et al, 1994), and neuronal migration (Komura and Rakic, 1992). Via expression Williams et al, 1992b;Brust et al, 1993;Fujita et al, 1993;Stea et al, 1993) and biochemical studies (Wagner et al, 1988;Westenbroek et al, 1992;Witcher et al, 1993;Leveque et al, 1994;Scott et al, 1996), it seems that most N-V DCC s in adult brain are ␣ 1B , ␣ 2 /␦, and ␤ 3 heteromers, although subpopulations containing ␤ 1 or ␤ 4 rather than ␤ 3 subunits also may exist (Scott et al, 1996).…”

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confidence: 99%

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N-Type Calcium Channels in the Developing Rat Hippocampus: Subunit, Complex, and Regional Expression

et al. 1997

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The expression of multiple classes of voltage-dependent calcium channels (VDCCs) allows neurons to tailor calcium signaling to functionally discrete cellular regions. In the developing hippocampus a central issue is whether the expression of VDCC subtypes plays a role in key phases such as migration and synaptogenesis. Using radioligand binding and immunoblotting, we show that some N-type VDCCs exist before birth, consistent with a role in migration; however, most N-VDCC subunit expression is postnatal, coinciding with synaptogenesis. Immunoprecipitation studies indicate that the increased expression of N-VDCCs in early development occurs without subunit switching because there is no change in the fraction of ␤ 3 subunits in the N-VDCC ␣ 1B -␤ 3 heteromers. Fluorescence imaging of cell surface N-VDCCs during this period reveals that N-VDCCs are expressed on somata before dendrites and that this expression is asynchronous between different subfields of the hippocampus (CA3-CA4 before CA1-CA2 and dentate gyrus). Our data argue that N-VDCC expression is an important cue in the genesis of synaptic transmission in discrete hippocampal subfields.

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“…Morphological studies have provided significant insights about the possible existence of presynaptic slots for VGCCs at transmitter release sites (Heuser et al, 1979;Robitaille et al, 1990;Haydon et al, 1994;Harlow et al, 2001). Biochemical studies have identified numerous molecular interactions between VGCCs and their binding partners that play a crucial role in coupling presynaptic VGCC to the release machinery (Sheng et al, 1998;Maximov et al, 1999;Missler et al, 2003;Spafford et al, 2003;Nishimune et al, 2004;Leenders et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Different Relationship of N- and P/Q-Type Ca²⁺Channels to Channel-Interacting Slots in Controlling Neurotransmission at Cultured Hippocampal Synapses

Cao¹,

Tsien²

2010

J. Neurosci.

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Synaptic transmission at CNS synapses is often mediated by joint actions of multiple Ca2ϩ channel subtypes, most prominently, P/Q-and N-type. We have proposed that P/Q-type Ca 2ϩ channels saturate type-preferring slots at presynaptic terminals, which impose a ceiling on the synaptic efficacy of the channels. To test for analogous interactions for presynaptic N-type Ca 2ϩ channels, we overexpressed their pore-forming Ca V 2.2 subunit in cultured mouse hippocampal neurons, recorded excitatory synaptic transmission from transfected cells, and dissected the contributions of N-, P/Q-, and R-type channels with subtype-specific blockers. Overexpression of Ca V 2.2 did not increase the absolute size of the EPSC even though somatic N-type current was augmented by severalfold. Thus, the strength of neurotransmission is saturated with regard to levels of Ca 2ϩ channel expression for both N-type and P/Q-type channels. Overexpression of Ca 2ϩ -impermeable Ca V 2.2 subunits decreased EPSC size, corroborating competition for channel slots. Striking asymmetries between Nand P/Q-type channels emerged when their relative contributions were compared with channel overexpression. Overexpressed N-type channels could competitively displace P/Q-type channels from P/Q-preferring slots and take over the role of supporting transmission. The converse was not found with overexpression of P/Q-type channels, regardless of their C-terminal domain. We interpret these findings in terms of two different kinds of presynaptic slots at excitatory synapses, one accepting N-type channels but rejecting P/Q-type (N specific ) and the other preferring P/Q-type but also accepting N-type (PQ preferring ). The interaction between channels and slots governs the respective contributions of multiple channel types to neurotransmission and, in turn, the ability of transmission to respond to various stimulus patterns and neuromodulators.

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Localization of individual calcium channels at the release face of a presynaptic nerve terminal

Cited by 116 publications

References 44 publications

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K⁺Currents

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K⁺Currents

N-Type Calcium Channels in the Developing Rat Hippocampus: Subunit, Complex, and Regional Expression

Different Relationship of N- and P/Q-Type Ca²⁺Channels to Channel-Interacting Slots in Controlling Neurotransmission at Cultured Hippocampal Synapses

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Localization of individual calcium channels at the release face of a presynaptic nerve terminal

Cited by 116 publications

References 44 publications

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K+Currents

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K+Currents

N-Type Calcium Channels in the Developing Rat Hippocampus: Subunit, Complex, and Regional Expression

Different Relationship of N- and P/Q-Type Ca2+Channels to Channel-Interacting Slots in Controlling Neurotransmission at Cultured Hippocampal Synapses

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Product

Resources

About

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K⁺Currents

Presynaptic Recordings fromDrosophila: Correlatin of Macroscopic and Single-Channel K⁺Currents

Different Relationship of N- and P/Q-Type Ca²⁺Channels to Channel-Interacting Slots in Controlling Neurotransmission at Cultured Hippocampal Synapses