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Altered neuronal architecture and plasticity in the visual cortex of adult MMP-3-deficient mice

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Abstract

Matrix metalloproteinases (MMPs) are Zn2+-dependent endopeptidases considered to be essential for normal brain development and neuroplasticity by modulating extracellular matrix proteins, receptors, adhesion molecules, growth factors and cytoskeletal proteins. Specifically, MMP-3 has recently been implicated in synaptic plasticity, hippocampus-dependent learning and neuronal development and migration in the cerebellum. However, the function(s) of this enzyme in the neocortex is understudied. Therefore, we explored the phenotypical characteristics of the neuronal architecture and the capacity for experience-dependent cortical plasticity in the visual cortex of adult MMP-3-deficient (MMP-3−/−) mice. Golgi–Cox stainings revealed a significant reduction in apical dendritic length and an increased number of apical obliques for layer V pyramidal neurons in the visual cortex of adult MMP-3−/− mice compared to wild-type (WT) animals. In addition, a significant upregulation of both phosphorylated and non-phosphorylated neurofilament protein (NF)-high, phosphorylated NF-medium, NF-low and α-internexin was detected in the visual cortex of MMP-3−/− mice. To assess the effect of MMP-3 deficiency on cortical plasticity, we monocularly enucleated adult MMP-3−/− mice and analyzed the reactivation of the contralateral visual cortex 7 weeks post-enucleation. In contrast to previous results in C57Bl/6J adult mice, activity remained confined to the binocular zone and did not expand into the monocular regions indicative for an aberrant open-eye potentiation. Permanent hypoactivity in the monocular cortex lateral and medial to V1 also indicated a lack of cross-modal plasticity. These observations demonstrate that genetic inactivation of MMP-3 has profound effects on the structural integrity and plasticity response of the visual cortex of adult mice.

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Acknowledgments

We gratefully thank Ria Vanlaer and Lieve Geenen for excellent technical assistance. Jeroen Aerts is supported by a Ph.D. fellowship of the Agency for Innovation through Science and Technology Flanders (IWT Vlaanderen). This work is supported by the Fund for Scientific Research-Flanders (FWO Vlaanderen).

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Authors and Affiliations

  1. Laboratory of Neuroplasticity and Neuroproteomics, KU Leuven, Naamsestraat 59, 3000, Leuven, Belgium

    Jeroen Aerts, Julie Nys, Tjing-Tjing Hu & Lutgarde Arckens

  2. Laboratory of Neural Circuit Development and Regeneration, KU Leuven, Naamsestraat 61, 3000, Leuven, Belgium

    Lieve Moons & Tjing-Tjing Hu

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  1. Jeroen Aerts
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  2. Julie Nys
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  3. Lieve Moons
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  4. Tjing-Tjing Hu
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  5. Lutgarde Arckens
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Correspondence to Lutgarde Arckens.

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Aerts, J., Nys, J., Moons, L. et al. Altered neuronal architecture and plasticity in the visual cortex of adult MMP-3-deficient mice. Brain Struct Funct 220, 2675–2689 (2015). https://doi.org/10.1007/s00429-014-0819-4

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  • DOI: https://doi.org/10.1007/s00429-014-0819-4

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