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High iron and iron household protein contents in perineuronal net-ensheathed neurons ensure energy metabolism with safe iron handling

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Reinert,  Tilo
Paul Flechsig Institute for Brain Research, University of Leipzig, Germany;
Department Neurophysics (Weiskopf), MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Morawski,  Markus
Paul Flechsig Institute for Brain Research, University of Leipzig, Germany;
Department Neurophysics (Weiskopf), MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Citation

Reinert, A., Reinert, T., Arendt, T., & Morawski, M. (2022). High iron and iron household protein contents in perineuronal net-ensheathed neurons ensure energy metabolism with safe iron handling. International Journal of Molecular Sciences, 23(3): 1634. doi:10.3390/ijms23031634.


Cite as: https://hdl.handle.net/21.11116/0000-0009-F344-8
Abstract
A subpopulation of neurons is less vulnerable against iron-induced oxidative stress and neurodegeneration. A key feature of these neurons is a special extracellular matrix composition that forms a perineuronal net (PN). The PN has a high affinity to iron, which suggests an adapted iron sequestration and metabolism of the ensheathed neurons. Highly active, fast-firing neurons—which are often ensheathed by a PN—have a particular high metabolic demand, and therefore may have a higher need in iron. We hypothesize that PN-ensheathed neurons have a higher intracellular iron concentration and increased levels of iron proteins. Thus, analyses of cellular and regional iron and the iron proteins transferrin (Tf), Tf receptor 1 (TfR), ferritin H/L (FtH/FtL), metal transport protein 1 (MTP1 aka ferroportin), and divalent metal transporter 1 (DMT1) were performed on Wistar rats in the parietal cortex (PC), subiculum (SUB), red nucleus (RN), and substantia nigra (SNpr/SNpc). Neurons with a PN (PN+) have higher iron concentrations than neurons without a PN: PC 0.69 mM vs. 0.51 mM, SUB 0.84 mM vs. 0.69 mM, SN 0.71 mM vs. 0.63 mM (SNpr)/0.45 mM (SNpc). Intracellular Tf, TfR and MTP1 contents of PN+ neurons were consistently increased. The iron concentration of the PN itself is not increased. We also determined the percentage of PN+ neurons: PC 4%, SUB 5%, SNpr 45%, RN 86%. We conclude that PN+ neurons constitute a subpopulation of resilient pacemaker neurons characterized by a bustling iron metabolism and outstanding iron handling capabilities. These properties could contribute to the low vulnerability of PN+ neurons against iron-induced oxidative stress and degeneration.