Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

DC:

dendritic cell

TCs:

telocytes

TEM:

transmission electron microscopy

Tps:

telopodes

References

  • Abd-Elhafeez HH, Mokhtar DM, Hassan AH (2017) Effect of melatonin on telocytes in the seminal vesicle of the Soay ram: an immunohistochemical, ultrastructural and morphometrical study. Cells Tissues Organs 203:29–54

    CAS  PubMed  Google Scholar 

  • Acuña-Castroviejo D, Escames G, Venegas C, Díaz-Casado ME, Lima-Cabello E, López LC, Rosales-Corral S, Tan DX, Reiter RJ (2014) Extrapineal melatonin: sources, regulation, and potential functions. Cell Mol Life Sci 71(16):2997–3025

    PubMed  Google Scholar 

  • Baba K, Benleulmi-Chaachoua A, Journe A-S, Kamal M, Guillaume J-L, Dussaud S et al (2013) Heteromeric MT1/MT2 melatonin receptors modulate photoreceptor function. Sci Signal 6(296):ra89–ra89

    PubMed  Google Scholar 

  • Bancroft JD, Layton C, Suvarna SK (2013) Bancroft’s theory and practice of histological techniques, 7th edn. Churchill Livingstone, London

    Google Scholar 

  • Bandiera R, Vidal VPI, Motamedi FJ, Clarkson M, Sahut-Barnola I, von Gise A, Pu WT, Hohenstein P, Martinez A, Schedl A (2013) WT1 maintains adrenal-gonadal primordium identity and marks a population of AGP-like progenitors within the adrenal gland. Dev Cell 27(1):5–18

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benitez-King G (2006) Melatonin as a cytoskeletal modulator: implications for cell physiology and disease. J Pineal Res 40(1):1–9

    CAS  PubMed  Google Scholar 

  • Bittman EL, Dempsey RJ, Karsch FJ (1983) Pineal melatonin secretion drives the reproductive response to day length in the ewe. Endocrionology 113:2276–2283

    CAS  Google Scholar 

  • Cantarero I, Luesma MJ, Alvarez-Dotu JM, Muñoz E, Junquera C (2016) Transmission electron microscopy as key technique for the characterization of telocytes. Curr Stem Cell Res Ther 11(5):410–414

    CAS  PubMed  Google Scholar 

  • Ceafalan L, Gherghiceanu M, Popescu LM, Simionescu O (2012) Telocytes in human skin - are they involved in skin regeneration? J Cell Mol Med 16(7):1405–1420

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cismasiu VB, Radu E, Popescu LM (2011) miR-193 expression differentiates telocytes from other stromal cells. J Cell Mol Med 15(5):1071–1074

    CAS  PubMed  PubMed Central  Google Scholar 

  • Compeer EB, Boes M (2014) MICAL-L1-related and unrelated mechanisms underlying elongated tubular endosomal network (ETEN) in human dendritic cells. Commun Integr Biol 7:949–969

    Google Scholar 

  • Díaz-Flores L, Gutiérrez R, Varela H, Valladares F, Alvarez-Argüelles H, Borges R (2008) Histogenesis and morphofunctional characteristics of chromaffin cells. Acta Physiol (Oxford) 192(2):145–163

    Google Scholar 

  • Decker JF, Quay WB (1982) Stimulatory effects of melatonin on ependymal epithelium of choroid plexuses in golden hamsters. J Neural Transm 55(1):53–67

    CAS  PubMed  Google Scholar 

  • Del Rio ML, Bernhardt G, Rodriguez-Barbosa JI, Forster R (2010) Development and functional specialization of CD103+ dendritic cells. Immunol Rev 234:268–281

    PubMed  Google Scholar 

  • Dubocovich ML, Yun K, Al-Ghoul WM, Benloucif S, Masana MI (1998) Selective MT2 melatonin receptor antagonists block melatonin-mediated phase advances of circadian rhythms. FASEB J 12(12):1211–1220

    CAS  PubMed  Google Scholar 

  • ElHafez E, Abouelhamd A, Hassan A (2014) Effects of administration of melatonin on the Harderian gland of sheep. J Interdiscip Hist 2(1):19

    Google Scholar 

  • Esposito E, Cuzzocrea S (2010) Antiinflammatory activity of melatonin in central nervous system. Curr Neuropharmacol 8(3):228–242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Faussone-Pellegrini MS, Thuneberg L (1999) Guide to the identification of interstitial cells of Cajal. Microsc Res Tech 47(4):248–266

    CAS  PubMed  Google Scholar 

  • Hardeland R (2009) Melatonin: signaling mechanisms of a pleiotropic agent. BioFactors (Oxford, England) 35(2):183–192

    CAS  Google Scholar 

  • Harrison FA, McDonald IR (1966) The arterial supply to the adrenal gland of the sheep. J Anat 100(Pt 1):189–202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hodel A (2001) Effects of glucocorticoids on adrenal chromaffin cells. J Neuroendocrinol 13(2):216–220

    CAS  PubMed  Google Scholar 

  • Hoyo GM, Martın P, Fernandez Arias C, Marın AR, Ardavın C (2002) CD8α dendritic cells originate from the CD8α dendritic cell subset by a maturation process involving CD8α, DEC-205, and CD24 up-regulation. Blood 99:999–1004

    Google Scholar 

  • Hussein MM, Mokhtar DM (2018) The roles of telocytes in lung development and angiogenesis: an immunohistochemical, ultrastructural, scanning electron microscopy and morphometrical study. Dev Biol 443(2):137–152

    CAS  PubMed  Google Scholar 

  • Jaensson E, Uronen-Hansson H, Pabst O, Eksteen B, Tian J, Coombes JL, Berg PL, Davidsson T, Powrie F, Johansson-Lindbom B, Agace WW (2008) Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med 205:2139–2149

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jánossy A, Orsó E, Szalay KS, Jurányi Z, Beck M, Vizi ES (1998) Cholinergic regulation of the rat adrenal zona glomerulosa. J Endocrinol 157(2):305–315

    PubMed  Google Scholar 

  • Kameda Y (1996) Differential distribution of S-100 protein and vimentin in the hypophyseal pars tuberalis of the guinea pig. J Histochem Cytochem 44(5):501–510

    CAS  PubMed  Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A

    Google Scholar 

  • Kim J-B, Jung JY, Ahn J-C, Rhee CK, Hwang H-J (2009) Antioxidant and anti-apoptotic effect of melatonin on the vestibular hair cells of rat utricles. Clin Exp Otorhinolaryngol 2(1):6–12

    PubMed  PubMed Central  Google Scholar 

  • Kobayashi S, Coupland RE (1993) Morphological aspects of chromaffin tissue: the differential fixation of adrenaline and noradrenaline. J Anat 183 ( Pt 2:223–235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laming PR, Kimelberg H, Robinson S, Salm A, Hawrylak N, Müller C, Ng K (2000) Neuronal-glial interactions and behavior. Neurosci Biobehav Rev 24(3):295–340

    CAS  PubMed  Google Scholar 

  • Li H, Oehrlein SA, Wallerath T, Ihrig-Biedert I, Wohlfart P, Ulshöfer T, Kleinert H (1998) Activation of protein kinase C alpha and/or epsilon enhances transcription of the human endothelial nitric oxide synthase gene. Mol Pharmacol 53(4):630–637

    CAS  PubMed  Google Scholar 

  • Li H, Zhang H, Yang L, Lu S, Ge J (2014) Telocytes in mice bone marrow: electron microscope evidence. J Cell Mol Med 18(6):975–978

    PubMed  PubMed Central  Google Scholar 

  • Lincoln GA, Short RV (1980) Seasonal breeding: nature’s contraceptive. Recent Prog Horm Res 36:1–52

    CAS  PubMed  Google Scholar 

  • Luesma MJ, Gherghiceanu M, Popescu LM (2013) Telocytes and stem cells in limbus and uvea of mouse eye. J Cell Mol Med 17(8):1016–1024

    CAS  PubMed  PubMed Central  Google Scholar 

  • Magro G, Grasso S (1997) Immunohistochemical identification and comparison of glial cell lineage in fetal, neonatal, adult and neoplastic human adrenal medulla. Histochem J 29(4):293–299

    CAS  PubMed  Google Scholar 

  • Masana MI, Doolen S, Ersahin C, Al-Ghoul WM, Duckles SP, Dubocovich ML, Krause DN (2002) MT(2) melatonin receptors are present and functional in rat caudal artery. J Pharmacol Exp Ther 302(3):1295–1302

    CAS  PubMed  Google Scholar 

  • Mokhtar DM, Abd-Elhafez EA (2016) Morphological studies on the peripheral circulation of the ovary in one-humped camel (Camelus dromedarius). Anat Histol Embryol 45(4):319–328

    PubMed  Google Scholar 

  • Mokhtar DM, Abd-Elhafeez HH, Abou-Elmagd A, Hassan AHS (2016) Melatonin administration induced reactivation in the seminal gland of the Soay rams during non-breeding season: an ultrastructural and morphometrical study. J Morphol 277:231–243

    CAS  PubMed  Google Scholar 

  • Mokhtar DM, Hussein MT, Hassan AHS (2017) Melatonin elicits stimulatory action on the adrenal gland of Soay ram: morphometrical, immunohistochemical, and ultrastructural study. Microsc Microanal 23(06):1173–1188

    CAS  PubMed  Google Scholar 

  • Mokhtar DM, Hussein MM (2019) Morphological characteristic and functional dependencies of dendritic cell in developing rabbit lung during fetal and neonatal life. Dev Biol 454:29–43. https://doi.org/10.1016/j.ydbio.2019.06.013

    Article  CAS  PubMed  Google Scholar 

  • Mor M, Plazzi PV, Spadoni G, Tarzia G (1999) Melatonin. Curr Med Chem 6(6):501–518

    CAS  PubMed  Google Scholar 

  • Popescu LM, Gherghiceanu M, Cretoiu D, Radu E (2005) The connective connection: interstitial cells of Cajal (ICC) and ICC-like cells establish synapses with immunoreactive cells. Electron microscope study in situ. J Cell Mol Med 9(3):714–730

    CAS  PubMed  PubMed Central  Google Scholar 

  • Popescu LM, Gherghiceanu M, Suciu LC, Manole CG, Hinescu ME (2011) Telocytes and putative stem cells in the lungs: electron microscopy, electron tomography and laser scanning microscopy. Cell Tissue Res 345(3):391–403

    PubMed  PubMed Central  Google Scholar 

  • Popescu BO, Gherghiceanu M, Kostin S, Ceafalan L, Popescu LM (2012) Telocytes in meninges and choroid plexus. Neurosci Lett 516(2):265–269

    CAS  PubMed  Google Scholar 

  • Radogna F, Diederich M, Ghibelli L (2010) Melatonin: a pleiotropic molecule regulating inflammation. Biochem Pharmacol 80(12):1844–1852

    CAS  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17:208–212.24

    CAS  Google Scholar 

  • Rodriguez H, Filippa V, Mohamed F, Dominquez S, Scardapane L (2007) Interaction between chromaffin and sustentacular cells in adrenal medulla of viscacha (Lagostomus maximus maximus). Anat Histol Embryol 36(3):182–185

    CAS  PubMed  Google Scholar 

  • Susko I, Mornjaković Z, Alicelebić S, Cosović E, Beganović A (2004) Retinal and pineal melatonin from a circadian signal to therapeutic use. Med Arh 58(1):61–64

    PubMed  Google Scholar 

  • Tamarkin L, Baird CJ, Almeida OFX (1985) Melatonin: a coordinating signs for mammalian reproduction. Science (WashDC) 227:714–720

    CAS  Google Scholar 

  • Uyanikgil Y, Cavusoglu T, Kılıc K, Yigitturk G, Celik S, Tubbs R, Turgut M (2017) Useful effects of melatonin in peripheral nerve injury and development of the nervous system. J Branchial Plex Peripher Nerve Inj 12(01):1–6

    PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Author notes

  1. Manal T. Hussein and Doaa M. Mokhtar contributed equally to this work.

Authors and Affiliations

  1. Department of Anatomy and Histology, Faculty of Vet. Medicine, Assiut University, Assiut, 71526, Egypt

    Manal T. Hussein, Doaa M. Mokhtar & A. H. S Hassan

Authors
  1. Manal T. Hussein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doaa M. Mokhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. H. S Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

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.

Additional information

Handling Editor: Margit Pavelka

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01441-8

Keywords

Search

Navigation