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Prolonged expression of Puma in cholinergic amacrine cells during the development of rat retina.

ABSTRACT: During development of the nervous system, large numbers of neurons are overproduced and then eliminated by programmed cell death. Puma is a BH3-only protein that is reported to be involved in the initiation of developmental programmed cell death in rodent retinal neurons. The expression and cellular localization of Puma in retinal tissues during development are not, however, well known. Here the authors report the expression pattern of Puma during retinal development in the rat. During the period of programmed cell death in the retina, Puma was expressed in some members of each retinal neuron, including retinal ganglion cells, amacrine cells, bipolar cells, horizontal cells, and photoreceptor cells. Although the developmental programmed cell death of cholinergic amacrine cells is known to be independent of Puma, this protein was expressed in almost all their dendrites and somata of cholinergic amacrine cells at postnatal age 2 to 3 weeks, and it continued to be detected in cholinergic dendrites in the inner plexiform layer for up to 8 weeks after birth. These results suggest that Puma has some significant roles in retinal neurons after eye opening, especially that of cholinergic amacrine cells, in addition to programmed cell death of retinal neurons before eye opening.

SUBMITTER: Wakabayashi T

PROVIDER: S-EPMC3524561 | biostudies-literature | 2012 Oct

REPOSITORIES: biostudies-literature

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Prolonged expression of Puma in cholinergic amacrine cells during the development of rat retina.

Wakabayashi Taketoshi T Kosaka Jun J Mori Tetsuji T Yamada Hisao H

The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society 20120626 10

During development of the nervous system, large numbers of neurons are overproduced and then eliminated by programmed cell death. Puma is a BH3-only protein that is reported to be involved in the initiation of developmental programmed cell death in rodent retinal neurons. The expression and cellular localization of Puma in retinal tissues during development are not, however, well known. Here the authors report the expression pattern of Puma during retinal development in the rat. During the perio ...[more]

PMID: 22736709

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Project description:BackgroundDeveloping retinas display retinal waves, the patterned spontaneous activity essential for circuit refinement. During the first postnatal week in rodents, retinal waves are mediated by synaptic transmission between starburst amacrine cells (SACs) and retinal ganglion cells (RGCs). The neuromodulator adenosine is essential for the generation of retinal waves. However, the cellular basis underlying adenosine's regulation of retinal waves remains elusive. Here, we investigated whether and how the adenosine A(2A) receptor (A(2A)R) regulates retinal waves and whether A(2A)R regulation of retinal waves acts via presynaptic SACs.Methodology/principal findingsWe showed that A(2A)R was expressed in the inner plexiform layer and ganglion cell layer of the developing rat retina. Knockdown of A(2A)R decreased the frequency of spontaneous Ca²⁺ transients, suggesting that endogenous A(2A)R may up-regulate wave frequency. To investigate whether A(2A)R acts via presynaptic SACs, we targeted gene expression to SACs by the metabotropic glutamate receptor type II promoter. Ca²⁺ transient frequency was increased by expressing wild-type A(2A)R (A2AR-WT) in SACs, suggesting that A(2A)R may up-regulate retinal waves via presynaptic SACs. Subsequent patch-clamp recordings on RGCs revealed that presynaptic A(2A)R-WT increased the frequency of wave-associated postsynaptic currents (PSCs) or depolarizations compared to the control, without changing the RGC's excitability, membrane potentials, or PSC charge. These findings suggest that presynaptic A(2A)R may not affect the membrane properties of postsynaptic RGCs. In contrast, by expressing the C-terminal truncated A(2A)R mutant (A(2A)R-ΔC) in SACs, the wave frequency was reduced compared to the A(2A)R-WT, but was similar to the control, suggesting that the full-length A(2A)R in SACs is required for A(2A)R up-regulation of retinal waves.Conclusions/significanceA(2A)R up-regulates the frequency of retinal waves via presynaptic SACs, requiring its full-length protein structure. Thus, by coupling with the downstream intracellular signaling, A(2A)R may have a great capacity to modulate patterned spontaneous activity during neural circuit refinement.

Project description:PurposeIntracellular free calcium ions (Ca(2+)) are an important element in retinal ganglion cell response. Two major EF-hand (E-helix-loop-F-helix-hand) calcium binding proteins in the retina, calretinin and calbindin-28 kDa, are important buffers of intracellular free Ca(2+) in neurons, and may also serve as Ca(2+)-dependent regulators of enzymes and ion channels.MethodsThis study used immunohistochemistry to investigate the subcellular expression patterns of calretinin and calbindin-28 kDa, in the soma, dendrites, and the axonal compartment of rat retinal ganglion cells.ResultsAntibodies for calretinin and calbindin-28 kDa labeled different cell populations in the retinal ganglion cell layer. In this layer, calretinin labeled a larger number of cells compared to calbindin-28 kDa, many, but not all, of which were displaced amacrine cells. The calbindin-28 kDa immunopositive neurons were distinct in that their somata were peripherally encircled by microtubule associated protein 1 (MAP-1) or neurofilament-200 kDa subunit (NF-200 kDa) immunofluorescence. Although somata of retinal ganglion cells contained these calcium binding proteins, neither protein was found in the dendrites or initial segments of the axons. However, both were expressed in the ganglion cell axons in nerve fiber layer. Calretinin and calbindin-28 kDa staining overlapped in some fibers and not in others. Calretinin immunofluorescence was concentrated in discrete axonal regions, which showed limited staining for calbindin-28 kDa or for NF200 kDa, suggesting its close proximity to the plasma membrane.ConclusionsThere is a clear compartmentalization of calbindin-28 kDa and calretinin distribution in retinal ganglion cells. This suggests that the two calcium binding proteins perform distinct functions in localized calcium signaling. It also indicates that rather than freely diffusing through the cytoplasm to attain a homogeneous distribution, calbindin-28 kDa and calretinin must be bound to cellular structures through interactions that are likely important for their functions.

Dataset Information

Prolonged expression of Puma in cholinergic amacrine cells during the development of rat retina.

Publications

Prolonged expression of Puma in cholinergic amacrine cells during the development of rat retina.

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