Locally released small (non‐protein) ninhydrin‐reacting molecules underlie developmental differences of cultured medullary versus spinal dorsal horn neurons

Xie, Yu; Pflueger, Melissa; Feng, Shi Ting; Lin, Shuang-Xiu; Kwan, Chun L.; Galasko, Gail; Sessle, Barry J.; Yu, Xian‐Min

doi:10.1111/j.1471-4159.2012.07797.x

Cited by 4 publications

(16 citation statements)

References 52 publications

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“…The AMPA and NMDA-mediated components have decay time constants around 5 ms and 90 ms, respectively. These parameters are similar to those in SDH and Hip neurons [14,15,19,20,21] .…”

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronssupporting

confidence: 73%

“…Electrophysiological data demonstrate that all neurons at day 14 in culture from Hip, SDH or Vc show whole-cell responses to glutamate in a concentration-dependent manner. Compared with the current density of SDH or Hip neurons, however, the density recorded in Vc neurons is significantly lower [14,15] . Furthermore, less than 30% of recorded Vc neurons show spontaneous miniature excitatory post-synaptic currents (mEPSCs) which can be found in over 80% of recorded SDH and Hip neurons.…”

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 74%

“…Co-labeling of TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling) with Tuj1, NeuN or GFAP antibody shows that more mature neurons undergo cell death in Vc when compared with that in SDH. However, cell death in young neurons or glial cells appears similar in these two regions [14,15] .…”

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 94%

“…neurobasal medium supplemented with B27, β-FGF2 and L-glutamine (which minimizes the growth of glial cells (<15%) [22] ) or MEM supplemented with 10% fetal bovine serum and insulin were examined. Changing the culture medium or altering the concentration of β-FGF2 or insulin added into the medium does not produce significant effects on the difference in cell survival between Vc and SDH [14,15] . However, co-culture of Vc with SDH tissues significantly enhances the growth of Vc neurons.…”

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 96%

“…Recent studies [14,15] have demonstrated that when compared with cultured neurons from the SDH or hippocampus (Hip) of rat embryos (18 days gestation), Vc neurons grow much slower, there are a fewer number of primary processes and the length of the processes are shorter. Two weeks after the culture plating, the processes of Hip and SDH neurons appear merged and form networks while Vc neurons still remain separated [14,15] . Electrophysiological data demonstrate that all neurons at day 14 in culture from Hip, SDH or Vc show whole-cell responses to glutamate in a concentration-dependent manner.…”

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 99%

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Understanding the Regional Specificity of Neurons in the Trigeminal Subnucleus Caudalis and Spinal Dorsal Horn

Jiang

2016

Itch Pain

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Neurons in the trigeminal subnucleus caudalis (Vc) and spinal cord dorsal horn (SDH) play important roles in modulating and relaying pain signals to the higher centers of the central nervous system (CNS). Morphologically, many aspects including a laminated structure, cytoarchitecture and cellular elements in these two central regions are very similar [1 ,2, 3, 4]. Most nociceptive afferents with a small-diameter terminate in the superficial laminae of Vc and SDH. Functionally, sensory neurons in Vc and SDH respectively receive nociceptive inputs from the orofacial and other somatic regions, and convey the inputs to higher brain centers [1, 2, 3, 4, 5]. According to the mechanoreceptive properties, sensory neurons in both the Vc and SDH are classified into three types. They are low-threshold mechanoreceptive (LTM), wide-dynamic range (WDR) and nociceptive-specific neurons (NS) [1, 2, 3, 4, 5]. Because of these similarities Vc has been considered as analogous to SDH [4, 6]. However, some differences between Vc and SDH have also been reported. For example, the distribution pattern of substance P (SP) and calcitonin gene related peptide (CGRP) in Vc of adult animals is different from that in SDH. In SDH there is no dual representation of peripheral regions, which can be found in rostral and caudal Vc. A transitional zone found between Vc and trigeminal subnucleus interpolaris plays a special role in sensorimotor function. However, no such region is found in the spinal system [5, 7, 8]. CNS neurons are regionalized. They are organized as groups through their circuitry. Although it is known that differences in functions among these groups in the adult CNS are predetermined during the development of the neuroepithelium [9, 10, 11, 12, 13] , understanding how the regional specificity is developed in the CNS is still a big challenge in neuroscience research. It has recently been found that ninhydrin-reacting small molecules released locally are involved in the region-specific regulation of neuronal development in cultured Vc and SDH neurons [14, 15]. In this review we focused on present knowledge about the region-specific regulation of neuronal development in these two CNS regions associated with the transmission of nociceptive signals.

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“…The AMPA and NMDA-mediated components have decay time constants around 5 ms and 90 ms, respectively. These parameters are similar to those in SDH and Hip neurons [14,15,19,20,21] .…”

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronssupporting

confidence: 73%

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 74%

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 94%

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 96%

Section: Developmental Differences Of Cultured Vc Versus Sdh Neuronsmentioning

confidence: 99%

See 3 more Smart Citations

Understanding the Regional Specificity of Neurons in the Trigeminal Subnucleus Caudalis and Spinal Dorsal Horn

Jiang

2016

Itch Pain

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Postnatal development of inner lamina II interneurons of the rat medullary dorsal horn

Mermet-Joret

Alba-Delgado

Descheemaeker

et al. 2021

Pain

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Pain processing in young mammals is immature. Despite the central role of the medullary dorsal horn (MDH) in processing orofacial sensory information, the maturation of the neurons within the MDH has been largely overlooked. Combining in vitro electrophysiological recordings and 3D morphological analysis over the first postnatal month in rats, we investigated the agedependent development of the neurons within the inner lamina II (IIi) of the MDH. We show the lamina IIi neuronal population transition into a more hyperpolarized state, with modification of the action potential waveform, and a shift from single spiking, at early postnatal ages, to tonic firing and initial bursting at later stages. These physiological changes are associated with a strong structural remodelling of the neuronal morphology with most of the modifications occurring after the third postnatal week. Among the lamina IIi neuronal population, the subpopulation of interneurons expressing the g isoform of the protein kinase C (PKCg 1 ) are key elements for the circuits underlying facial mechanical allodynia. How do they develop from the rest of the lamina IIi constitute an important question that remained to be addressed. Here, we show that PKCg 1 interneurons display electrophysiological changes over time comparable with the PKCg 2 population. However, they show a distinctive increase of the soma volume and primary branches length, as opposed to the PKCg 2 population. Together, our data demonstrate a novel pattern of late postnatal maturation of lamina IIi interneurons, with a spotlight on PKCg 1 interneurons, that may be relevant for the development of orofacial sensitivity.

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Regulated internalization of NMDA receptors drives PKD1-mediated suppression of the activity of residual cell-surface NMDA receptors

et al. 2015

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BackgroundConstitutive and regulated internalization of cell surface proteins has been extensively investigated. The regulated internalization has been characterized as a principal mechanism for removing cell-surface receptors from the plasma membrane, and signaling to downstream targets of receptors. However, so far it is still not known whether the functional properties of remaining (non-internalized) receptor/channels may be regulated by internalization of the same class of receptor/channels. The N-methyl-D-aspartate receptor (NMDAR) is a principal subtype of glutamate-gated ion channel and plays key roles in neuronal plasticity and memory functions. NMDARs are well-known to undergo two types of regulated internalization – homologous and heterologous, which can be induced by high NMDA/glycine and DHPG, respectively. In the present work, we investigated effects of regulated NMDAR internalization on the activity of residual cell-surface NMDARs and neuronal functions.ResultsIn electrophysiological experiments we discovered that the regulated internalization of NMDARs not only reduced the number of cell surface NMDARs but also caused an inhibition of the activity of remaining (non-internalized) surface NMDARs. In biochemical experiments we identified that this functional inhibition of remaining surface NMDARs was mediated by increased serine phosphorylation of surface NMDARs, resulting from the activation of protein kinase D1 (PKD1). Knockdown of PKD1 did not affect NMDAR internalization but prevented the phosphorylation and inhibition of remaining surface NMDARs and NMDAR-mediated synaptic functions.ConclusionThese data demonstrate a novel concept that regulated internalization of cell surface NMDARs not only reduces the number of NMDARs on the cell surface but also causes an inhibition of the activity of remaining surface NMDARs through intracellular signaling pathway(s). Furthermore, modulating the activity of remaining surface receptors may be an effective approach for treating receptor internalization-induced changes in neuronal functions of the CNS.Electronic supplementary materialThe online version of this article (doi:10.1186/s13041-015-0167-1) contains supplementary material, which is available to authorized users.

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Locally released small (non‐protein) ninhydrin‐reacting molecules underlie developmental differences of cultured medullary versus spinal dorsal horn neurons

Cited by 4 publications

References 52 publications

Understanding the Regional Specificity of Neurons in the Trigeminal Subnucleus Caudalis and Spinal Dorsal Horn

Understanding the Regional Specificity of Neurons in the Trigeminal Subnucleus Caudalis and Spinal Dorsal Horn

Postnatal development of inner lamina II interneurons of the rat medullary dorsal horn

Regulated internalization of NMDA receptors drives PKD1-mediated suppression of the activity of residual cell-surface NMDA receptors

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