Abstract
Detecting danger is key to the survival and success of all species. Animal nervous and immune systems cooperate to optimize danger detection. Preceding studies have highlighted the benefits of bringing neurons into the defense game, including regulation of immune responses, wound healing, pathogen control, and survival. Here, we summarize the body of knowledge in neuroimmune communication and assert that neuronal participation in the immune response is deeply beneficial in each step of combating infection, from inception to resolution. Despite the documented tight association between the immune and nervous systems in mammals or invertebrate model organisms, interdependence of these two systems is largely unexplored across metazoans. This review brings a phylogenetic perspective of the nervous and immune systems in the context of danger detection and advocates for the use of non-model organisms to diversify the field of neuroimmunology. We identify key taxa that are ripe for investigation due to the emergence of key evolutionary innovations in their immune and nervous systems. This novel perspective will help define the primordial principles that govern neuroimmune communication across taxa.
Highlights
Which appeared first in eukaryotes: immune cells or neurons? Here we propose that a cell with antimicrobial or phagocytic capabilities, whether it was an immune cell or a sensory neuron, predates the emergence of the first in sensu stricto neuronal cell type
The concept of neuronal speed in the context of the immune response has not been widely discussed in the mammalian literature, we propose that neuronal innervation of lymphoid tissues as well as the wide presence of Neuroimmune cell units (NICUs) at mammalian tissue barriers may have been evolutionary driven to optimize the speed of the immune response at the organismal level
The nervous system is an invaluable ally for the immune system to fight infection from the early detection of danger to the shutdown of the immune response
Summary
TLRs are prototypic PRRs with fundamental roles in animal innate immune responses. The protein Toll was originally described as a regulator of dorsoventral patterning in early Drosophila embryogenesis. TLRs localize to either the cell surface, where they recognize PAMPs (e.g., LPS, flagellin) or endosomes where they largely detect nucleic acids (Kawai and Akira, 2010). Ligand binding to the TLR ectodomain, composed of LRRs, initiates a signaling pathway that culminates in NF-kB activation. This highly conserved pathway is present throughout Metazoa, including poriferans (Figure 2). While nucleic acid sensing TLRs are typically restricted to endosomes in the nervous system, these TLRs are expressed on cell surfaces, where they detect selfantigens. This conserved detection and signaling pathway represents a fundamental aspect of neuroimmune communication
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