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Ankyrin-B structurally defines terminal microdomains of peripheral somatosensory axons

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Abstract

Axons are subdivided into functionally organized microdomains, which are required for generation and propagation of action potentials (APs). In the central nervous system (CNS), APs are generated near the soma in the axon initial segment (AIS) and propagated by nodes of Ranvier (noR). The crucial role of the membrane adapter proteins ankyrin-B and ankyrin-G as organizers of AIS and noR is now well established. By comparison, little is known on the localization and function of these proteins in sensory axon terminals of the peripheral nervous systems (PNS). Here, we tested the hypothesis that somatosensory PNS terminals are organized by distinct members of the ankyrin protein family. We discovered a specific distribution of ankyrin-B in somatosensory axon terminals of skin and muscle. Specifically, ankyrin-B was localized along the membrane of axons innervating Meissner corpuscles, Pacinian corpuscles and hair follicle receptors. Likewise, proprioceptive terminals of muscle spindles exhibited prominent ankyrin-B expression. Furthermore, ankyrin-B expression extended into nociceptive and thermoceptive intraepidermal nerve fibers. Interestingly, all studied somatosensory terminals were largely devoid of ankyrin-G, indicating that this scaffolding protein does not contribute to organization of mechanoelectric transduction zones in peripheral somatosensory neurons. Instead, we propose that ankyrin-B serves as a major membrane organizer in mechanoreceptive and nociceptive terminals of the PNS.

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Acknowledgments

This study was supported by Deutsche Forschungsgemeinschaft DFG Grant Schu1412/2-1 and a research grant from the Prof. Dr. Karl and Gerhard Schiller-Stiftung. We are grateful to Drs. Martin Schmelz and Otilia Obreja, Mannheim, for valuable discussions and supply of porcine skin samples. We would also like to thank Prof. Dr. Eberhard Buse and Dr. Gunnar Habermann from Covance Laboratories GmbH, Münster, for macaque tissue samples. Furthermore, we thank Richard Trauth for graphic design support.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Center for Biomedicine and Medical Technology Mannheim (CBTM), Research Division Neuroanatomy, Medical Faculty Mannheim, Heidelberg University, Ludolf-Krehl-Str. 13-17, 68167, Mannheim, Germany

    Maren Engelhardt, Silke Vorwald, Jürgen-Markus Sobotzik & Christian Schultz

  2. Interdisciplinary Center for Neurosciences (IZN), Heidelberg University, Heidelberg, Germany

    Maren Engelhardt, Silke Vorwald, Jürgen-Markus Sobotzik & Christian Schultz

  3. Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC, USA

    Vann Bennett

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  1. Maren Engelhardt
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  5. Christian Schultz
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Correspondence to Maren Engelhardt.

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Engelhardt, M., Vorwald, S., Sobotzik, JM. et al. Ankyrin-B structurally defines terminal microdomains of peripheral somatosensory axons. Brain Struct Funct 218, 1005–1016 (2013). https://doi.org/10.1007/s00429-012-0443-0

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  • DOI: https://doi.org/10.1007/s00429-012-0443-0

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