Abstract
The salivary gland of hard ticks is a highly innervated tissue where multiple intertwined axonal projections enter each individual acini. In the present study, we investigated the ultrastructural architecture of axonal projections within granular salivary gland type II and III acini of Ixodes ricinus female. Using immunogold labeling, we specifically examined the associations of SIFamide neuropeptide, SIFamide receptor (SIFa_R), neuropeptide pigment dispersing factor (PDF), and the invertebrate-specific D1-like dopamine receptor (InvD1L), with acinar cells. In both acini types, SIFamide-positive axons were found to be in direct contact with either basal epithelial cells or a single adlumenal myoepithelial cell in close proximity to the either the acinar duct or its valve, respectively. Accordingly, SIFa_R staining correlated with SIFamide-positive axons in both basal epithelial and myoepithelial cells. Immunoreactivity for both InvD1L and PDF (type II acini exclusively) revealed positive axons radiating along the acinar lumen. These axons were primarily enclosed by the adlumenal myoepithelial cell plasma membrane and interstitial projections of ablumenal epithelial cells. Our study has revealed the detailed ultrastructure of I. ricinus salivary glands, and provides a solid baseline for a comprehensive understanding of the cell-axon interactions and their functions in this essential tick organ.
Highlights
Tick salivary gland (SG) secretions eliminate excess water and ions from tick bodies to maintain homeostasis[1] and simultaneously compromise the host’s defense system to ensure long-term feeding success[2,3]
Using specific antibodies, numerous axonal processes arborizing within type II and III acini have been identified (Fig. 1): (i) neuropeptidergic axon terminals co-expressing myoinhibitory peptide (MIP), SIFamide and elevenin (Elv) terminate at the basal regions in both type II and III acini[18,21]; (ii) neuropeptidergic axon terminals positively immunoreacting to antibodies against both pigment dispersing factor (PDF) and orcokinin only reach the apical parts of type II acini[17,22]; and (iii) axonal projections expressing invertebrate-specific D1-like dopamine receptor (InvD1L) reaching the apical regions of both type II and III acini were identifed[19]
The single adlumenal myoepithelial cell (MC) lines the entire acinar lumen—including the region above the acinar valve—in a web-like fashion[13,19,24]. Combining both morphological and physiological data, we have suggested that the MC is a target for downstream signals of InvD1L-positive axons, whereas basally located MIP/SIFamide/Elv-releasing axon terminals may play a role in the modulation of paracrine/autocrine dopamine actions in the acini and/or control the acinar valve via the MC19,20,25
Summary
Tick salivary gland (SG) secretions eliminate excess water and ions from tick bodies to maintain homeostasis[1] and simultaneously compromise the host’s defense system to ensure long-term feeding success[2,3]. The single adlumenal MC lines the entire acinar lumen—including the region above the acinar valve—in a web-like fashion[13,19,24] Combining both morphological and physiological data, we have suggested that the MC is a target for downstream signals of InvD1L-positive axons, whereas basally located MIP/SIFamide/Elv-releasing axon terminals may play a role in the modulation of paracrine/autocrine dopamine actions in the acini and/or control the acinar valve via the MC19,20,25. It appears that the MC is controlled by different axonal projections[19,20,25], detailed knowledge about the specific cell(s)-axon(s) connections remains enigmatic, mainly due to difficulties in distinguishing clear acinar cell boundaries via wholemount immunohistochemistry (IHC) approaches. The 3D reconstructions of double-immunogold-stained structures identified distinct innervations, revealing their relationship with specific acinar cells for the first time
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