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Synaptic connections between endomorphin 2-immunoreactive terminals and μ-opioid receptor-expressing neurons in the sacral parasympathetic nucleus of the rat.

Dou XL, Qin RL, Qu J, Liao YH, Lu Yc, Zhang T, Shao C, Li YQ - PLoS ONE (2013)

Bottom Line: All of the them also expressed MOR.These results provided morphological evidence that EM2-containing axon terminals formed symmetric synapses with MOR-expressing PPNs in the SPN.The present results also show that EM2 and MOR might be involved in both the homeostatic control and information transmission of micturition.

View Article: PubMed Central - PubMed

Affiliation: Department of Urology, Xijing Hospital, The Fourth Military Medical University, Xi'an, China.

ABSTRACT
The urinary bladder is innervated by parasympathetic preganglionic neurons (PPNs) that express μ-opioid receptors (MOR) in the sacral parasympathetic nucleus (SPN) at lumbosacral segments L6-S1. The SPN also contains endomorphin 2 (EM2)-immunoreactive (IR) fibers and terminals. EM2 is the endogenous ligand of MOR. In the present study, retrograde tract-tracing with cholera toxin subunit b (CTb) or wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) via the pelvic nerve combined with immunohistochemical staining for EM2 and MOR to identify PPNs within the SPN as well as synaptic connections between the EM2-IR terminals and MOR-expressing PPNs in the SPN of the rat. After CTb was injected into the pelvic nerve, CTb retrogradely labeled neurons were almost exclusively located in the lateral part of the intermediolateral gray matter at L6-S1 of the lumbosacral spinal cord. All of the them also expressed MOR. EM2-IR terminals formed symmetric synapses with MOR-IR, WGA-HRP-labeled and WGA-HRP/MOR double-labeled neuronal cell bodies and dendrites within the SPN. These results provided morphological evidence that EM2-containing axon terminals formed symmetric synapses with MOR-expressing PPNs in the SPN. The present results also show that EM2 and MOR might be involved in both the homeostatic control and information transmission of micturition.

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A schematic drawing showing the underlying mechanism of micturition inhibition by EM2-containing bladder afferent terminals onto the MOR-expressing PPNs in the SPN.Sensory information from the bladder receptor is directly transmitted to the MOR-expressing PPNs via EM2-containing primary afferent fibers. These EM2-containing fibers exert inhibitory effects onto the MOR-expressing PPNs in the SPN via synaptic connections, resulting in an attenuation of the excitatory effects of the efferent fibers originating from the PPNs onto the parasympathetic postganglionic neurons in the pelvic ganglia. This attenuation affects the micturition reflex and results in urinary retention.
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pone-0062028-g006: A schematic drawing showing the underlying mechanism of micturition inhibition by EM2-containing bladder afferent terminals onto the MOR-expressing PPNs in the SPN.Sensory information from the bladder receptor is directly transmitted to the MOR-expressing PPNs via EM2-containing primary afferent fibers. These EM2-containing fibers exert inhibitory effects onto the MOR-expressing PPNs in the SPN via synaptic connections, resulting in an attenuation of the excitatory effects of the efferent fibers originating from the PPNs onto the parasympathetic postganglionic neurons in the pelvic ganglia. This attenuation affects the micturition reflex and results in urinary retention.

Mentions: Behavioral experiments and cystometry in the bladder have measured the effects of exogenous MOR agonists [55], [56], [57]. These studies have shown that in vitro activation of MOR reduces the contraction of the detrusor [58], [59]. However, the potential local and direct effects of morphine on bladder activity in the spinal cord have been less clear. In the present study, EM2, an endogenous agonist of MOR [60], was used as a substitute for the exogenous MOR agonist to explore the underlying mechanisms of urinary disorders caused by morphine. Our results showed that direct synaptic connections between EM2-containing terminals and MOR-expressing PPNs exist in the SPN. Information of the bladder travels via afferent fibers within the pelvic nerve into the lumbosacral spinal cord. In the SPN, these EM2-containing fibers form symmetric synaptic connections with MOR-expressing PPNs. EM2 is released from the presynaptic bouton and binds with MOR in the postsynaptic membrane, resulting in the inhibition of PPNs activity. Thus, the excitatory information transmitted via the parasympathetic preganglionic efferent fibers to the parasympathetic postganglionic neurons, which innervate the detrusor of bladder in the pelvic ganglion, will be reduced, resulting in a significant attenuation in the contractions in the rat bladder (Figure 6). Finally, the micturition reflex will be affected, which results in urinary retention.


Synaptic connections between endomorphin 2-immunoreactive terminals and μ-opioid receptor-expressing neurons in the sacral parasympathetic nucleus of the rat.

Dou XL, Qin RL, Qu J, Liao YH, Lu Yc, Zhang T, Shao C, Li YQ - PLoS ONE (2013)

A schematic drawing showing the underlying mechanism of micturition inhibition by EM2-containing bladder afferent terminals onto the MOR-expressing PPNs in the SPN.Sensory information from the bladder receptor is directly transmitted to the MOR-expressing PPNs via EM2-containing primary afferent fibers. These EM2-containing fibers exert inhibitory effects onto the MOR-expressing PPNs in the SPN via synaptic connections, resulting in an attenuation of the excitatory effects of the efferent fibers originating from the PPNs onto the parasympathetic postganglionic neurons in the pelvic ganglia. This attenuation affects the micturition reflex and results in urinary retention.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3643968&req=5

pone-0062028-g006: A schematic drawing showing the underlying mechanism of micturition inhibition by EM2-containing bladder afferent terminals onto the MOR-expressing PPNs in the SPN.Sensory information from the bladder receptor is directly transmitted to the MOR-expressing PPNs via EM2-containing primary afferent fibers. These EM2-containing fibers exert inhibitory effects onto the MOR-expressing PPNs in the SPN via synaptic connections, resulting in an attenuation of the excitatory effects of the efferent fibers originating from the PPNs onto the parasympathetic postganglionic neurons in the pelvic ganglia. This attenuation affects the micturition reflex and results in urinary retention.
Mentions: Behavioral experiments and cystometry in the bladder have measured the effects of exogenous MOR agonists [55], [56], [57]. These studies have shown that in vitro activation of MOR reduces the contraction of the detrusor [58], [59]. However, the potential local and direct effects of morphine on bladder activity in the spinal cord have been less clear. In the present study, EM2, an endogenous agonist of MOR [60], was used as a substitute for the exogenous MOR agonist to explore the underlying mechanisms of urinary disorders caused by morphine. Our results showed that direct synaptic connections between EM2-containing terminals and MOR-expressing PPNs exist in the SPN. Information of the bladder travels via afferent fibers within the pelvic nerve into the lumbosacral spinal cord. In the SPN, these EM2-containing fibers form symmetric synaptic connections with MOR-expressing PPNs. EM2 is released from the presynaptic bouton and binds with MOR in the postsynaptic membrane, resulting in the inhibition of PPNs activity. Thus, the excitatory information transmitted via the parasympathetic preganglionic efferent fibers to the parasympathetic postganglionic neurons, which innervate the detrusor of bladder in the pelvic ganglion, will be reduced, resulting in a significant attenuation in the contractions in the rat bladder (Figure 6). Finally, the micturition reflex will be affected, which results in urinary retention.

Bottom Line: All of the them also expressed MOR.These results provided morphological evidence that EM2-containing axon terminals formed symmetric synapses with MOR-expressing PPNs in the SPN.The present results also show that EM2 and MOR might be involved in both the homeostatic control and information transmission of micturition.

View Article: PubMed Central - PubMed

Affiliation: Department of Urology, Xijing Hospital, The Fourth Military Medical University, Xi'an, China.

ABSTRACT
The urinary bladder is innervated by parasympathetic preganglionic neurons (PPNs) that express μ-opioid receptors (MOR) in the sacral parasympathetic nucleus (SPN) at lumbosacral segments L6-S1. The SPN also contains endomorphin 2 (EM2)-immunoreactive (IR) fibers and terminals. EM2 is the endogenous ligand of MOR. In the present study, retrograde tract-tracing with cholera toxin subunit b (CTb) or wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) via the pelvic nerve combined with immunohistochemical staining for EM2 and MOR to identify PPNs within the SPN as well as synaptic connections between the EM2-IR terminals and MOR-expressing PPNs in the SPN of the rat. After CTb was injected into the pelvic nerve, CTb retrogradely labeled neurons were almost exclusively located in the lateral part of the intermediolateral gray matter at L6-S1 of the lumbosacral spinal cord. All of the them also expressed MOR. EM2-IR terminals formed symmetric synapses with MOR-IR, WGA-HRP-labeled and WGA-HRP/MOR double-labeled neuronal cell bodies and dendrites within the SPN. These results provided morphological evidence that EM2-containing axon terminals formed symmetric synapses with MOR-expressing PPNs in the SPN. The present results also show that EM2 and MOR might be involved in both the homeostatic control and information transmission of micturition.

Show MeSH
Related in: MedlinePlus