Melatonin activates the vascular elements, telocytes, and neuroimmune communication in the adrenal gland of Soay rams during the non-breeding season

Abstract

The adrenal glands of 15 adult Soay rams were used to study the effect of melatonin on their vascular elements and cellular organization. A significant increase in the cross-sectional area of the blood sinusoids was demonstrated after melatonin administration. The vimentin-expressing mesenchymal cells were increased in the melatonin-treated group. Intensive S-100 protein expression was observed in the sustentacular cells and telocytes (TCs) of the treated groups. Moreover, S-100 protein expressed intensively in the dendritic cells that distributed around the blood sinusoids. Dendritic cells showed positive immunoreactivity for CD8 and CD103. Many dendritic cells with well-defined processes were observed close to the nerve fibers after melatonin administration. A significant increase in the number and diameter of dendritic cells after melatonin treatment was demonstrated. Many highly active TCs were observed in the medulla of the treated group, which were characterized by long telopodes (Tps) containing abundant secretory vesicles that released into the extracellular milieu and towards the dendritic cells. In the melatonin-treated groups, the nerve fibers showed a significant increase in their cross-sectional area accompanied by an increase in the activity of Schwann cells and neighboring dendritic cells. In the treated group, TCs and DCs appear to contribute to angiogenesis. A planner contact between Tps and the stem cell was demonstrated in the treated group. Melatonin induced a stimulatory action on the vascular and neuronal elements of the adrenal gland. Moreover, it enhances the activity of a variety of cells including telocytes, dendritic, sustentacular, and Schwann cells.

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Abbreviations

DC:

dendritic cell

TCs:

telocytes

TEM:

transmission electron microscopy

Tps:

telopodes

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Acknowledgments

Prof. Dr. A.H.S. Hassan was on sabbatical leave—from the Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University—at MRC, Reproductive Biology Unit, Edinburgh, UK, and supported by British Council grant (1986). The authors are grateful to Prof. G.A. Lincoln, professor of physiology at MRC, Edinburgh, for his great support in the collection of samples for this experiment. In addition, we thank the Electron Microscopy Unit technicians at Assiut University for their help in processing the imaging of the electron microscopy samples.

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Authors

Contributions

M. T. Hussein* performed the immunohistochemical, morphometrical studies, analyzed the results and contributed to preparing and reviewing the paper. D. M. Mokhtar* performed the light- and electron- microscopical study, analyzed the results, and contributed to preparing and reviewing the paper. A. H. S. Hassan collected the samples and contributed to preparing and reviewing the paper. *These authors contributed equally to this work.

Corresponding author

Correspondence to Doaa M. Mokhtar.

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Competing interests

The authors declare that they have no competing interests.

Ethical approval and consent to participate

Experiment no. S/17353 was conducted in accordance with the U.K. Animals (Scientific Procedures) Act of 1986.

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The relevance of this research

• Our previous study on the adrenal gland demonstrated a great stimulatory action on the parenchymal cells. We hypothesized that melatonin can affect the stromal constituents as well.

• The present study aims to demonstrate the effect of melatonin on the stromal cells of the adrenal gland, focusing mainly on the vascular and cellular levels using the light, electron microscopic analysis, morphometrical, and immunohistochemical studies.

• Melatonin caused a stimulatory action on the adrenal vascular elements and stimulates the activity of a variety of cells including telocytes (TCs), dendritic cells (DCs), sustentacular, and Schwann cells.

• Numerous coated vesicles were observed in DCs after melatonin treatment indicating that melatonin enhances antigen-presentation and phagocytosis.

• Many highly active TCs were observed in the medulla of the treated group, which was characterized by releasing of their abundant secretory vesicles into the extracellular milieu and towards the dendritic cells.

• In the melatonin-treated groups, the nerve fibers showed a significant increase in their cross-sectional area accompanied by an increase in the activity of Schwann cells.

• In the treated group, TCs and DCs appear to contribute to angiogenesis.

Handling Editor: Margit Pavelka

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Hussein, M.T., Mokhtar, D.M. & Hassan, A.H.S. Melatonin activates the vascular elements, telocytes, and neuroimmune communication in the adrenal gland of Soay rams during the non-breeding season. Protoplasma 257, 353–369 (2020). https://doi.org/10.1007/s00709-019-01441-8

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Keywords

  • CD8
  • S100-protein
  • Dendritic cells
  • Telocytes
  • Nerve fibers