Toward the Existence of a Sympathetic Neuroplasticity Adaptive Mechanism Influencing the Immune Response. A Hypothetical View-Part I

Emanuel Bottasso, Emanuel Bottasso

Abstract

The nervous system exerts a profound influence on the function of the immune system (IS), mainly through the sympathetic arm of the autonomic nervous system. In fact, the sympathetic nervous system richly innervates secondary lymphoid organs (SLOs) such as the spleen and lymph nodes. For decades, different research groups working in the field have consistently reported changes in the sympathetic innervation of the SLOs during the activation of the IS, which are characterized by a decreased noradrenergic activity and retraction of these fibers. Most of these groups interpreted these changes as a pathological phenomenon, referred to as "damage" or "injury" of the noradrenergic fibers. Some of them postulated that this "injury" was probably due to toxic effects of released endogenous mediators. Others, working on animal models of chronic stimulation of the IS, linked it to the very chronic nature of processes. Unlike these views, this first part of the present work reviews evidence which supports the hypothesis of a specific adaptive mechanism of neural plasticity from sympathetic fibers innervating SLOs, encompassing structural and functional changes of noradrenergic nerves. This plasticity mechanism would involve segmental retraction and degeneration of these fibers during the activation of the IS with subsequent regeneration once the steady state is recovered. The candidate molecules likely to mediate this phenomenon are also here introduced. The second part will extend this view as to the potential changes in sympathetic innervation likely to occur in inflamed non-lymphoid peripheral tissues and its possible immunological implications.

Keywords: neural plasticity; neuro-immune interaction; neurotrophins; secondary lymphoid organs; semaphorins; sympathetic fibers.

Copyright © 2019 Bottasso.

Figures

Figure 1
Figure 1
Proposed adaptive mechanism of neural plasticity from STs innervating secondary lymphoid organs such as the spleen. The activation of the IS may be accompanied by retraction and axonal degeneration of STs (red arrows). The activated immune cells are able to produce semaphorins and pro-neurotrophins/neurotrophins, binding to their receptors -plexins/neuropilins and Trk/p75NTR, respectively- probably expressed on STs. In particular, p75NTR may be re-expressed in a pro-inflammatory milieu. The action of these molecules may lead to an inhibition of STs integrin-mediated adhesion to ECM and depolymerization of their actin cytoskeleton, thus favoring their retraction and axonal degeneration (dotted line). In addition, semaphorins and neurotrophins/pro-neurotrophins may be produced by other non-lymphoid cell types as well (i.e., stromal cells), under cytokine influence. A direct action of cytokines as playing a role on STs retraction cannot be disregarded. Once the immune response ceases, the IS returns to the steady state and STs may regenerate, recovering the usual splenic innervation pattern (blue arrows). Neural and immunological phenomena are summarized on the left and right sides, respectively. STs, sympathetic terminals; IS, immune system; Trk, tropomyosin-related kinase; p75NTR, p75 neurotrophin receptor; ECM, extracellular matrix.

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