Differential Release of Transmitters and Neuropeptides Co-Stored in Central and Peripheral Neurons

Thureson‐Klein, Åsa; Klein, Richard L.; Zhu, Pei-Chun; Kong, Jae-Yang

doi:10.1007/978-3-642-73172-3_8

Cited by 16 publications

(9 citation statements)

References 46 publications

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“…This idea was mainly fuelled by a number of findings. A first one was that, upon nerve stimulation, the amounts of vesicle proteins released in relation to NA were much smaller than expected on the basis of the corresponding ratio in the LDCV, suggesting that SDCV also were involved (Smith et al, 1970;Thureson-Klein et al, 1988). A second one was the observation that nerve terminals contain predominantly SDCV (ThuresonKlein et al, 1988), which are considered the synaptic vesicles of the adrenergic neurons (Stjä rne et al, 1992;Thureson-Klein et al, 1988).…”

Section: Introductionmentioning

confidence: 95%

“…Adrenergic neurons also contain SSV, often referred to as small dense cored vesicles (SDCV) (Bean et al, 1994;Thureson-Klein and Klein, 1990), and LDCV and were the first neurons which have been shown, at least in part, to release their classical transmitter noradrenaline (NA) by a process of exocytosis from LDCV (Geffen et al, 1970;Gewirtz and Kopin, 1970;Smith et al, 1970). Nevertheless, also for these neurons the idea still prevails that both types vesicles undergo regulated exocytosis and that there is a clear separation of the pathways for LDCV and SDCV (Bartfai et al, 1988;De Camilli and Jahn, 1990;Thureson-Klein et al, 1988). This idea was mainly fuelled by a number of findings.…”

Section: Introductionmentioning

confidence: 97%

“…According to the current concept, both SSV and LDCV undergo regulated exocytosis, and many physiological and pharmacological studies indicate that exocytosis of the two types of vesicles is differentially regulated (Bartfai et al, 1988;De Camilli and Jahn, 1990;Kelly, 1993;Lundberg et al, 1994;Sü dhof and Jahn, 1991;ThuresonKlein et al, 1988). Support for two distinct release patterns comes from (1) the demonstration of a change in the relative proportion of peptide and classical transmitter with the frequency of stimulation (Bartfai et al, 1988;Lundberg and Hökfelt, 1983;Lundberg et al, 1989;Whim and Lloyd, 1989), (2) the observation that a-latrotoxin in motor nerve terminals causes a selective and massive release from SSV but not from the LDCV (Matteoli et al, 1988), (3) the analysis of the role of Ca 11 and Ca 11 channels (Miller, 1987;Rane et al, 1987;Smith and Augustine, 1988;Verhage et al, 1991), and (4) the observation that exocytosis of SSV and LDCV occurs at different sites in the neuron (De Camilli and Jahn, 1990;Thureson-Klein et al, 1988).…”

Section: Introductionmentioning

confidence: 99%

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Noradrenergic neurons release both noradrenaline and neuropeptide Y from a single pool: The large dense cored vesicles

Potter

Partoens

Schoups

et al. 1997

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In peripheral adrenergic nerve endings, noradrenaline is stored in two different types of vesicles, the large and the small dense cored vesicles. A systematic study was undertaken to examine the release of noradrenaline and neuropeptide Y from dog spleen and rat vas deferens under various conditions of stimulation, particularly those which previously have demonstrated a differential regulation of exocytosis of the different types of storage vesicles. Here we present evidence that noradrenaline is released by exocytosis exclusively from the large dense cored vesicles, in which it is stored together with neuropeptide Y. Upon a single stimulation (at frequencies varying from 2-20 Hz), the release of noradrenaline and neuropeptide Y from the dog splenic nerve increased with the frequency of stimulation, but the ratio of noradrenaline to neuropeptide Y remained constant. After repeated stimulation of the splenic nerve, both substances' overflow decreased gradually and in parallel to values of 12.5% and 11.1% of the first stimulation for noradrenaline and neuropeptide Y, respectively. Similarly, repeated stimulation of the rat vas deferens (of which only 2-10% is large dense cored vesicles, whereas in the dog splenic nerve the large dense cored vesicles make up 30-40% of the total vesicle population) with 120 mM K+, in the presence of phentolamine, caused a gradual and parallel decline in the release of noradrenaline and neuropeptide Y (31.6% and 34.0%, respectively). Moreover, omega-conotoxin (10(-8) M to 10(-5) M) had a similar inhibitory effect on the release of both substances, alpha-latrotoxin (10(-9) M) evoked a parallel release of both noradrenaline and neuropeptide Y. The results indicate that noradrenaline in peripheral noradrenergic nerves is released exclusively from large dense cored vesicles by an exocytotic mechanism.

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Section: Introductionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Noradrenergic neurons release both noradrenaline and neuropeptide Y from a single pool: The large dense cored vesicles

Potter

Partoens

Schoups

et al. 1997

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“…In contrast, synaptic vesicle proteins, such as synaptophysin (p38), appear to travel to the plasma membrane via the constitutive secretory pathway and are then endocytosed and sorted in endosomes, from which synaptic vesicles (40 nm) bud. Exocytosis/endocytosis and recycling of cholinergic synaptic vesicles takes place at the presynaptic nerve terminal, while neuropeptide-and monoamine-containing LDCVs, located throughout the cell, may release nonsynaptically (7)(8)(9)(10).…”

mentioning

confidence: 99%

The Cytoplasmic Tail of the Vesicular Acetylcholine Transporter Contains a Synaptic Vesicle Targeting Signal

Varoqui

Erickson

1998

Journal of Biological Chemistry

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The human homologue of the vesicular acetylcholine transporter (hVAChT) and the neuronal isoform of the vesicular monoamine transporter (hVMAT2) are differentially targeted to two populations of regulated secretory organelles when expressed in PC12 cells. Western blot analysis of subcellular fractions from sucrose equilibrium density gradients and glycerol velocity gradients of homogenates from stably transfected cells revealed hVAChT immunoreactivity in fractions that contain synaptophysin, a marker of synaptic vesicles, while hVMAT2 immunoreactivity was confined to heavy fractions containing chromogranin B, a marker of large dense core vesicles. In cells treated with nerve growth factor, hVAChT immunoreactivity alone co-localized with synaptophysin and was abundantly expressed on synaptic vesicle clusters. Chimeras between hVMAT2 and hVAChT were utilized to identify the domain of hVAChT required for its expression on synaptic vesicles and which would shift the expression of hVMAT2 from large dense core vesicles to synaptic vesicles. Biochemical, immunocytochemical, and electron microscopic analyses revealed that a chimera in which the cytoplasmic tail of hVMAT2 was replaced with hVAChT sequences was now preferentially targeted to synaptic vesicles. In addition, hVAChT expression on synaptic vesicles was nearly abolished when the hVMAT2 cytoplasmic tail was present. Thus, structural information resides within the terminal cytoplasmic domain of VAChT, which specifically targets it to synaptic vesicles.The organelles used for regulated biogenic amine and acetylcholine (ACh) 1 secretion in neurons and endocrine cells are the large and small dense core vesicles (DCV) and small synaptic vesicles, respectively. The biogenesis and fate of these organelles and targeting of various proteins to them differ in several ways (1-6). LDCVs (approximately 200 nm) are the product of the trans-Golgi network as they contain soluble glycoproteins, such as the chromogranins, and various neuropeptides. Following maturation and subsequent exocytosis at the plasma membrane, components of the LDCV membrane must recycle to the Golgi complex to replenish their soluble neurohormone content and re-enter the regulated secretory pathway. In contrast, synaptic vesicle proteins, such as synaptophysin (p38), appear to travel to the plasma membrane via the constitutive secretory pathway and are then endocytosed and sorted in endosomes, from which synaptic vesicles (40 nm) bud. Exocytosis/endocytosis and recycling of cholinergic synaptic vesicles takes place at the presynaptic nerve terminal, while neuropeptide-and monoamine-containing LDCVs, located throughout the cell, may release nonsynaptically (7-10).Cloning and characterization of the family of vesicular transporters for biogenic amines and ACh has provided new tools for the study of the biogenesis of these regulated secretory organelles (11, 12). The examination of the subcellular localization of these proteins indicates that they are associated with distinct vesicle populations in neurons...

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“…These vesicles have a volume about 10 times larger than normal synaptic vesicles and contain the calcitonin gene-related peptide (Matteoli, Haimann, Torri-Tarelli, Polak, Ceccarelli & De Camilli, 1988) which is believed to have trophic or modulatory effects on transmission (Fontaine, Klarsfeld, Hokfelt & Changeux, 1986). They release their content spontaneously outside active synaptic zones (see review by Thureson-Klein, Klein, Zhu & Kong, 1988) in a calcium-insensitive way (Matteoli et al 1988). Furthermore, the proximo-distal axoplasmic transport of dense-core vesicles is interrupted at low temperature and by metabolic inhibitors (Edstr6m & Hanson, 1973), as is the release of the ACh which gives rise to slow MEPPs, but not that evoking normal fast MEPPs .…”

Section: Postsynaptic Changesmentioning

confidence: 99%

Botulinal Neurotoxins as Tools in Studies of Synaptic Mechanisms

Thesleff

1989

Exp Physiol

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Differential Release of Transmitters and Neuropeptides Co-Stored in Central and Peripheral Neurons

Cited by 16 publications

References 46 publications

Noradrenergic neurons release both noradrenaline and neuropeptide Y from a single pool: The large dense cored vesicles

Noradrenergic neurons release both noradrenaline and neuropeptide Y from a single pool: The large dense cored vesicles

The Cytoplasmic Tail of the Vesicular Acetylcholine Transporter Contains a Synaptic Vesicle Targeting Signal

Botulinal Neurotoxins as Tools in Studies of Synaptic Mechanisms

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