Evidence that some preganglionic sympathetic neurons in the rat contain vasoactive intestinal peptide- or peptide histidine isoleucine amide-like immunoreactivities

Baldwin, C.; Sasek, Cathrine A.; Zigmond, Richard E.

doi:10.1016/0306-4522(91)90183-o

Cited by 43 publications

(21 citation statements)

References 45 publications

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“…Probably, the VIP-/GAL-ir fibers derive from postganglionic neurons that exhibit coincidence of both peptides (Klimaschewski et al, 1994). Other sources of VIP-fibres, such as preganglionic sympathetic (Baldwin et al, 1991) or sensory neurons (Dalsgaard et al, 19841, are less likely because they do not colocalize GAL.…”

Section: Nerve Fibresmentioning

confidence: 99%

Immunohistochemistry of small intensely fluorescent (SIF) cells and of sif cell‐associated nerve fibers in the rat superior cervical ganglion

Heym

Klimaschewski

Borghini

et al. 1994

Microscopy Res & Technique

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Double-labelling immunofluorescence was applied on single sections of the rat superior cervical ganglion to evaluate neurochemistry and connectivity of intraganglionic SIF cells. The synaptic vesicle membrane protein synaptophysin and secretoneurin, a newly discovered neuropeptide derived from secretogranin II, proved reliable molecular markers of this cell type, whereas serotonin and tyrosine hydroxylase immunoreactivities were observed in slightly incongruent SIF cell subpopulations. Immunolabelling for vasoactive intestinal polypeptide and neuropeptide Y occurred in few SIF cells. None of the above immunoreactivities were visibly altered by preganglionic or postganglionic denervation, while some SIF cells were immunolabelled for galanin or for the neuronal microtubule-associated protein MAP2 after postganglionic denervation. SIF cells were nonreactive for the pan-neuronal marker protein gene product (PGP) 9.5 or neurofilament 160 kD. Intense staining of NADPH-diaphorase in some SIF cells, suggesting catalytic activity of nitric oxide synthase, could not be substantiated by immunoreactivity for this enzyme. SIF cells were approached by nonidentical fiber populations immunoreactive for PGP 9.5, neurofilament, or neuropeptide Y, whereas immunoreactivities for galanin and vasoactive intestinal polypeptide were colocalized in fiber meshes around SIF cells. The findings indicate (1) neurochemical SIF cell heterogeneity, (2) SIF cell plasticity in response to ganglionic perturbation, and (3) a differentiated innervation of SIF cells in the rat superior cervical ganglion.

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Section: Nerve Fibresmentioning

confidence: 99%

Immunohistochemistry of small intensely fluorescent (SIF) cells and of sif cell‐associated nerve fibers in the rat superior cervical ganglion

Heym

Klimaschewski

Borghini

et al. 1994

Microscopy Res & Technique

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“…Cotransmission has been described in synaptic junctions of sympathetic ganglia (Benarroch, 1994;Burnstock, 1976;Elfvin et al, 1993;Morales et al, 2004;Morris and Gibbins, 1992). Sympathetic preganglionic neurons (SPN) that establish synapses with postganglionic neurons use acetylcholine (ACh; detected by the immunoreactivity of its rate-limiting enzyme, choline acetyl transferase; ChAT) as a classical transmitter and coexpress several neuropeptides (Baldwin et al, 1991;Colombo-Benkmann et al, assumed, although rarely demonstrated, that SPN expressing neuropeptides are also cholinergic. The cooccurrence of ChAT and enkephalin (ENK) has been described in the cell bodies of SPN (Colombo-Benkmann et al, 1995;Kondo et al, 1985); however, it is not clear whether ChAT and neuropeptides also co-occur in the axon fibers, including the boutons and terminals of these neurons.…”

Section: Introductionmentioning

confidence: 99%

Choline acetyl transferase and neuropeptide immunoreactivities are colocalized in somata, but preferentially localized in distinct axon fibers and boutons of cat sympathetic preganglionic neurons

Sámano¹,

Zetina²,

Marin³

et al. 2006

Synapse

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Cholinergic sympathetic preganglionic neurons (SPN) coexpress the biosynthetic enzyme for acetylcholine, choline acetyl-transferase (ChAT), and neuropeptides such as enkephalin (ENK) in their cell bodies. However, it is not clear whether they also coexpress ChAT and neuropeptides in axon fibers and boutons. To explore coexpression of ChAT and neuropeptides in somata and axon processes of SPN, we investigated, using immunohistochemistry, retrograde labeling, confocal analysis, and tridimensional reconstruction, whether ChAT and the peptides neurotensin, methionine-ENK, somatostatin, calcitonin gene-related peptide, and vasoactive intestinal peptide colocalize in somata, axons fibers, and boutons of cat SPN. Practically, complete colocalization for these peptides and ChAT was observed in SPN somata. Conversely, in most instances we observed independent localization of immunoreactivity (IR) for ChAT and the peptides in axon fibers and boutons. The minor colocalization between ChAT- and peptide-IR in preganglionic fibers could correspond to a sequential axonal transport of ChAT and peptides, since we observed coexistence of these transmitters after blocking axonal transport. Contrary to Dale's principle, our results suggest that SPN can synthesize ChAT and peptides in their cell bodies and route them to distinct axon boutons or terminals in sympathetic ganglia. Presence of axon boutons containing either ChAT or neuropeptides lead us to suggest a new neurochemical pattern of cotransmission in sympathetic ganglia based on the concurrent release of transmitters and cotransmitters from distinct presynaptic boutons, rather than in the corelease of these mediators from the same axon process. The possibility that cellular segregation could be transient and depend on functional requirements is considered.

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“…Ganglia taken immediately after removal from animals or after 48 hr in organ culture were immersed in Zamboni's fixative for 16-24 hr at 40C (four to six ganglia for each experimental group for both antisera studied). The tissue was processed for the detection of VIP-IR as described by (9,10). The VIP antiserum (from J. Allen, University of Cambridge; used at a 1:1000 dilution) and the peptide histidine isoleucine amide (PHI) antiserum (from J. Fahrenkrug, Bispebjerg Hospital, Copenhagen; used at a 1:2000 dilution) have been characterized (11,12).…”

mentioning

confidence: 99%

Phenotypic plasticity in adult sympathetic neurons: changes in neuropeptide expression in organ culture.

Zigmond

Hyatt-Sachs

Baldwin

et al. 1992

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

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Vasoactive intestinal peptide (VEP)-like immunoreactivity is present at low levels in the superior cervical ganglion of the adult rat, where immunostained neural processes, but only an occasional immunostained cell body, are found. However, when ganglia are maintained for 24 or 48 hr in organ culture, their content of VIP-like immunoreactivity increases 6-or 31-fold, respectively. When examined at 24 hr, the increase in VIP-like immunoreactivity is totally blocked by an inhibitor of RNA or protein synthesis. Many neuronal cell bodies and processes with immunoreactivity for VIP and the related peptide histidine isoleucine amide (PHI) are seen in cultured ganglia. In addition, VIP/PHI mRNA is abundant in cultured ganglia but only barely detectable in ganglia prior to culture. Under the same culture conditions, neuropeptide Y-like immunoreactivity increases to a small extent, and tyrosine hydroxylase activity and total ganglion protein remain unchanged. These results support the idea that adult sympathetic neurons exhibit plasticity in neuropeptide expression and that this plasticity, in the case of VIP, depends on changes in gene expression.Specific neurons can synthesize and release more than one neurotransmitter. For example, many adult sympathetic neurons synthesize and release both norepinephrine and neuropeptide Y (NPY), a small number synthesize and release acetylcholine and vasoactive intestinal peptide (VIP), and some use other combinations of amines and peptides (1). In addition, during-development, neurons can change the neurotransmitters they utilize. The best studied example is the ability of neonatal sympathetic neurons to start making acetylcholine and to reduce their synthesis of norepinephrine. Initially identified in cell culture, this phenomenon was subsequently shown to occur in vivo, during the development of the cholinergic sympathetic neurons that innervate the rat foot pad (2).In addition to changes in biogenic amine synthesis, the expression of colocalized neuropeptides in neonatal sympathetic neurons can also be regulated during development. Medium conditioned by cultured heart cells contains a factor that, in addition to producing a cholinergic "switch" in neonatal sympathetic neurons from the superior cervical ganglion (SCG), also increases their immunoreactivity for several peptides [i.e., VIP, substance P, somatostatin, but not NPY (3)]. Also, when sympathetic neurons innervating the foot pads in neonatal rats change from a noradrenergic to a cholinergic phenotype, they acquire immunoreactivity for VIP and calcitonin gene-related peptide (2). Finally, placing neonatal SCG in explant culture for 48 hr produces a large (50-fold) increase in the expression of substance P-like immunoreactivity (IR) (4).Much less attention has been paid to the possibility that alterations in transmitter phenotype occur in adult sympathetic neurons. With electrophysiological techniques, only a small percentage of adult sympathetic neurons were found to acquire cholinergic properties in cell culture (...

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Evidence that some preganglionic sympathetic neurons in the rat contain vasoactive intestinal peptide- or peptide histidine isoleucine amide-like immunoreactivities

Cited by 43 publications

References 45 publications

Immunohistochemistry of small intensely fluorescent (SIF) cells and of sif cell‐associated nerve fibers in the rat superior cervical ganglion

Immunohistochemistry of small intensely fluorescent (SIF) cells and of sif cell‐associated nerve fibers in the rat superior cervical ganglion

Choline acetyl transferase and neuropeptide immunoreactivities are colocalized in somata, but preferentially localized in distinct axon fibers and boutons of cat sympathetic preganglionic neurons

Phenotypic plasticity in adult sympathetic neurons: changes in neuropeptide expression in organ culture.

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