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Epidermal Growth Factor Suppresses the Development of GABAergic Neurons Via the Modulation of Perineuronal Net Formation in the Neocortex of Developing Rodent Brains

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Abstract

Previously, we reported that epidermal growth factor (EGF) suppresses GABAergic neuronal development in the rodent cortex. Parvalbumin-positive GABAergic neurons (PV neurons) have a unique extracellular structure, perineuronal nets (PNNs). PNNs are formed during the development of PV neurons and are mainly formed from chondroitin sulfate (CS) proteoglycans (CSPGs). We examined the effect of EGF on CSPG production and PNN formation as a potential molecular mechanism for the inhibition of inhibiting GABAergic neuronal development by EGF. In EGF-overexpressing transgenic (EGF-Tg) mice, the number of PNN-positive PV neurons was decreased in the cortex compared with that in wild-type mice, as in our previous report. The amount of CS and neurocan was also lower in the cortex of EGF-Tg mice, with a similar decrease observed in EGF-treated cultured cortical neurons. PD153035, an EGF receptor (ErbB1) kinase inhibitor, prevented those mentioned above excess EGF-induced reduction in PNN. We explored the molecular mechanism underlying the effect of EGF on PNNs using fluorescent substrates for matrix metalloproteinases (MMPs) and a disintegrin and metalloproteinases (ADAMs). EGF increased the enzyme activity of MMPs and ADAMs in cultured neurons. These enzyme activities were also increased in the EGF-Tg mice cortex. GM6001, a broad inhibitor of MMPs and ADAMs, also blocked EGF-induced PNN reductions. Therefore, EGF/EGF receptor signals may regulate PNN formation in the developing cortex.

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Acknowledgements

We thank Ms. Eiko Kitayama and Dr. Meiko Kawamura for their technical assistance with the experiments.

Funding

This study was supported by KAKENHI under Grant Number 18K06460.

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Authors and Affiliations

  1. Department of Brain Tumor Biology, Brain Research Institute, Niigata University, Niigata, 951-8122, Japan

    Yuriko Iwakura & Nobuyuki Takei

  2. Department of Molecular Neurobiology, Brain Research Institute, Niigata University, Niigata, 951-8122, Japan

    Yuriko Iwakura, Yutaro Kobayashi, Hisaaki Namba, Hiroyuki Nawa & Nobuyuki Takei

  3. Department of Biochemistry, Graduate School of Medicine, Faculty of Medicine, University of Yamanashi, Yamanashi, 409-3898, Japan

    Yutaro Kobayashi

  4. Department of Physiological Sciences, School of Pharmaceutical Sciences, Wakayama Medical University, Wakayama, 640-8156, Japan

    Hisaaki Namba & Hiroyuki Nawa

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Contributions

All authors contributed to the study’s conception and design. Y. I., H. N, and N. T. contributed to the study conception and design. Y.I. and Y.K. performed experiments. Materials were prepared or collected by Y. I., Y. K., and H. N. The first draft of the manuscript was written by Y. I. and all authors commented on previous versions of the manuscript. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Yuriko Iwakura.

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Institutional Review Board Statement

The animal study protocol was approved by the Animal Use and Care Committee of Niigata University (protocol code SA00246, 2018 May 7, SA00664, 2021 April 05, SA00835, 2023 January 30.)

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The authors declare no competing interests.

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Iwakura, Y., Kobayashi, Y., Namba, H. et al. Epidermal Growth Factor Suppresses the Development of GABAergic Neurons Via the Modulation of Perineuronal Net Formation in the Neocortex of Developing Rodent Brains. Neurochem Res 49, 1347–1358 (2024). https://doi.org/10.1007/s11064-024-04122-y

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