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1

Grafted serotonergic neurons can reverse changes in gene expression in motoneurons produced by spinal cord injury in rats

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Miazga K., Joachimiak E., Fabczak H., Slawinska U.
Acta Neurobiologiae Experimentalis
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2015
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tom 75
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nr Supl.
BACKGROUND AND AIMS: Serotonin, which is supplied to the spinal cord by serotoninergic cells localized in the raphe nuclei and parapiramidal areas of the medulla, plays a very important role in control of the spinal locomotor central pattern generator (CPG). In our previous study we showed that intraperitoneal application of: 8-OH-DPAT (5-HT1A and 5-HT7 serotonin receptor agonist) and quipazine (mainly 5-HT2A serotonin receptor agonist), or intraspinal transplantation of serotonergic cells isolated from 14-day old rat embryo brain stem, facilitates locomotor-like hindlimb movements in spinal rats (spinal cord total transection between Th9 and Th10). 5-HT7 and 5-HT2 serotonin receptor antagonists blocked the locomotor-like hindlimb movements that had been restored in spinal rats grafted with embryonic serotoninergic cells. The aim of the present study was to examine the influence of spinal cord total transection and transplantation of serotonin neurons isolated from the 14-day old rat embryo brain stem on changes in expression of genes encoding 5-HT2A, 5-HT2C and 5-HT7 serotonin receptors in populations of motoneurons innervating tibialis anterior, gastrocnemius lateralis, and extensor caudae medialis muscles. METHODS: For motoneurons labeling a method of retrograde staining using intra muscle injection with cholera toxin B subunit conjugated with Alexa Fluor 555 was used. Motoneurons were then collected by using the laser capture micro-dissection method, and changes in expression of genes encoding serotonin receptors were analyzed by Real-time PCR. RESULTS: The results show that total spinal cord transection changed expression of genes encoding 5-HT2A, 5-HT2C and 5-HT7 serotonin receptors in ankle flexor and ankle and tail extensor muscles. Grafting of serotonin neurons reverses the effects of spinal cord injury on expression of these genes. CONCLUSION: This is the first demonstration that grafts of serotonergic neurons can reverse changes in gene expression in motoneurons produced by spinal cord injury.
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Komórki macierzyste w naprawie urazów rdzenia kręgowego - aktualny stan wiedzy

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Zawadzka M., Kwasniewska A., Miazga K., Slawinska U.
Wszechświat
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2020
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tom 121
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nr 01-03
3

The role of serotonin in the control of locomotor movements and strategies for restoring locomotion after spinal cord injury

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Slawinska U., Miazga K., Jordan L. M.
Acta Neurobiologiae Experimentalis
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2014
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tom 74
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nr 2
In this review we will discuss different ways for re-establishing serotonergic activity that can enhance recovery of coordinated plantar stepping after spinal cord injury in adult rats. It is well known that serotoninergic neurons located in the medulla are able to initiate locomotor activity. This effect is exerted by actions on motoneurons and on neurons of the locomotor CPG (Central Pattern Generator). Motoneuron and interneuron excitability is increased, and putative CPG interneurons display oscillatory behaviour in response to serotonin receptor activation. The medullary serotonergic nuclei play multiple roles in the control of locomotion, and they terminate on specific target neurons with different types of serotonergic receptors in the spinal cord. Activation of these serotonergic receptors can restore locomotor movements after spinal cord injury. Specifically, using defined serotonergic agonists the 5-HT2 receptors can be stimulated to control CPG activation as well as motoneuron output, while 5-HT7 receptors to control activity of the locomotor CPG. These results are consistent with the roles for these receptors during locomotion in intact rodents and in rodent brainstem-spinal cord in vitro preparations. The other possibility to encourage the remaining spinal cord circuitry below the total transection to control recovery of plantar hindlimb stepping is restoration of serotonergic innervation by intraspinal grafting of embryonic 5-HT neurons. Our data show that grafting of different populations of 5-HT neurons dissected from embryonic brainstem provides differential control over multiple components of the spinal locomotor circuitry through specific serotonin receptors. Moreover, we demonstrated that the best effect of motor recovery is obtained after grafting of neurons destined to form the B1, B2 and B3 descending 5-HT systems. Using only one of the subpopulations for intraspinal grafting, for example, B3 or the lateral group of 5-HT neurons, induces only partial recovery of plantar stepping with a clear lack of proper interlimb coordination. This confirms the hypothesis that transplantation of 5-HT neurons from specific embryonic sources is necessary to obtain optimal recovery of locomotor hindlimb movement.
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Differential effects on locomotor-like movements of paraplegic rats produced by activation of 5-HT2 or 5-HT7 receptors

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Slawinska U., Miazga K., Majczynski H., Cabaj A. M., Jordan L. M.
Acta Neurobiologiae Experimentalis
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2011
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tom 71
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nr S
There is considerable evidence from research in neonatal and adult rat and mouse preparations to warrant the conclusion that activation of 5-HT2 and 5-HT7 receptors leads to activation of the spinal cord circuitry for locomotion. Both types of receptors are involved in control of locomotor movements, but it is not clear how they are implicated in the responses to 5-HT agonists observed after spinal cord injury. Here we used different agonists that are known to be efficient in promoting locomotor recovery in paraplegic rats: 8-OHDPAT (acting on 5-HT7) and quipazine (acting on 5-HT2 receptors). Motor performance was tested before and 15 – 30 min after i.p. drug application in spinal rats placed with the forequarters on a platform above a treadmill while the hindlimbs were touching the moving treadmill belt. Tail pinching was used to induce hindlimb movements that were monitored using video recordings synchronized with simultaneous EMG recordings from the soleus and tibialis anterior muscles of both legs. The application of either 5-HT receptor agonist improved hindlimb plantar walking. Analysis of intra- and interlimb coordination confirmed that the motor performance was significantly better, but in slightly different ways, after application of either drug. Interlimb coordination (left-right coordination) was significantly better after 8-OHDPAT, and the activity of antigravity soleus muscle was significantly longer during locomotor-like movement enhanced by quipazine (an improvement in intralimb coordination). Our results suggest that 5-HT2 and 5-HT7 receptors both facilitate activity in the spinal circuitry controlling locomotion, but their effects are likely exerted on different populations of spinal neurons. These agonists also have affinity to other types of receptors (e.g., 8-OHDPAT acts also on 5-HT1a receptors and quipazine also has affinity for 5-HT3 receptors), so further experiments are needed to substantiate the roles of 5-HT2a and 5-HT7 receptors.
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The potent role of catecholaminergic innervation in locomotor recovery induced by intraspinal grafting of embryonic brainstem tissue in adult paraplegic rats

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Bejrowska A., Miazga K., Majczynski H., Zawadzka M., Slawinska U.
Acta Neurobiologiae Experimentalis
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2019
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tom 79
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nr Suppl.1
INTRODUCTION: In mammals, spinal cord transection results in permanent loss of locomotor function. Our previous investigations demonstrated that intraspinal grafting of an embryonic (E14) brainstem raphe area enhances hindlimb locomotor recovery in adult paraplegic rats. This process is mediated mainly through serotonergic (5‑HT) neurons. AIM(S): The aim of the present investigation was to determine the role of catecholaminergic (CA) neurons that are present in the grafted tissue in this recovery. METHOD(S): The experiments were performed on the inbred strain WAG rats after spinal cord total transection. Grafts were placed in the spinal cord below the total transection and included 5-HT neurons derived from the embryonic (E14) brainstem. Two months later, locomotor performance was tested with chronic EMG recordings from Soleus (Sol) and Tibialis Anterior (TA) muscles, allowing quantification of limb movement recovery. After completing the functional testing, the spinal cords were harvested for morphological investigations. RESULTS: In the graft area, besides 5-HT neurons, we found a number of CA neurons of graft origin. The CA innervation, however, was weaker than that of 5-HT and limited to specific areas of the spinal cord. We showed that the 5-HT and CA neurons were fully differentiated at the time of tissue dissection for grafting and that the host environment did not stimulate their proliferation and differentiation. The locomotor abilities of the spinal grafted rats were facilitated by application of Yohimbine and suppressed by Clonidine, likely through their actions on noradrenergic autoreceptors. CONCLUSIONS: Our results indicate a potent role of the CA innervation in locomotor recovery in paraplegic rats. In addition to the important role of 5‑HT neurons in this process, our findings provide new insights into the mechanisms underlying the locomotor recovery in rats. FINANCIAL SUPPORT: This work was supported by ERA-NET NEURON CoFund Consortium NEURONICHE (ERA‑NET‑Neuron/16/17).
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