Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-19T08:40:24.411Z Has data issue: false hasContentIssue false
  • English
  • Français

Melatonin Elicits Stimulatory Action on the Adrenal Gland of Soay Ram: Morphometrical, Immunohistochemical, and Ultrastructural Study

Published online by Cambridge University Press:  04 December 2017

Doaa M. Mokhtar ,
Manal T. Hussein  and
Ahmed H. S. Hassan
Doaa M. Mokhtar*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt
Manal T. Hussein
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt
Ahmed H. S. Hassan
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt
*
*Corresponding author.[email protected]
Get access

Abstract

Endogenous melatonin is a hormone secreted by pineal gland; it has several roles in metabolism, reproduction, and remarkable antioxidant properties. Studies on the melatonin effect on the adrenal glands which are important endocrine organs, controlling essential physiological functions, are still deficient. In this study, we attempted to investigate the effect of exogenous melatonin treatment on the adrenal cortex and medulla using several approaches. Adrenal glands of 15 Soay ram were examined to detect the effect of melatonin treatment. Our results revealed that the cells of adrenal cortex of the treated animals were separated by wide and numerous blood sinusoids and showed signs of increase steroidogenic activity, which are evidenced by functional hypertrophy with increase profiles of mitochondria, smooth endoplasmic reticulum, and lipid droplets. The most striking ultrastructural features in the medulla of the treated group were the engorgement of chromaffin cells with enlarged secretory granules enclosed within a significantly increased diameter of these cells. The cytoplasm of these cells showed numerous mitochondria, rough endoplasmic reticulum (rER), Golgi apparatus, lysosomes, and glycogen granules. Exocytosis of secretory granules to the lumen of blood vessels was evident in the treated group. Piecemeal degranulation mode of secretion was recorded after melatonin treatment. Chromaffin cells in the control group expressed moderate immunoreactivity to Synaptophysin and tyrosine hydroxylase, compared with intensified expression after melatonin treatment. The ganglion cells of the melatonin-treated group showed a significant increase in diameter with numerous rER. The most interesting feature in this study is the presence of small granule chromaffin cells (SGC) and telocytes (TCs) for the first time in the adrenal glands of sheep. Moreover, these SGC cells, Schwann cells, fibroblasts, and progenitor stem cells showed a stimulatory response. The TCs were small branched cells scattered in the adrenal glands around cortical cells, chromaffin cells, nerve fibers, and blood vessels. These cells increased significantly in number, length of their telopodes, and secretory activity after melatonin treatment. In addition, multiple profiles of unmyelinated nerve fibers were demonstrated in all treated specimens. These results indicated that melatonin treatment caused a stimulatory action on all cellular and neuronal elements of the adrenal gland. This study may act as a new direction for treatment of adrenal insufficiency.

Keywords

adrenal cortexchromaffin cellstelocytesnerve fibersSynaptophysin
Type
Biological Science Applications
Information
Microscopy and Microanalysis , Volume 23 , Issue 6 , December 2017 , pp. 1173 - 1188
Copyright
© Microscopy Society of America 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abd-Elhafeez, A.A., Mokhtar, D.M. & Hassan, A.H.S. (2017). Effect of melatonin on telocytes in the seminal vesicle of the Soay ram: An immunohistochemical, ultrastructural and morphometrical study. Cell Tissue Org 203(1), 29–54.CrossRefGoogle Scholar
Aunis, D. (1998). Exocytosis in chromaffin cells of the adrenal medulla. Int Rev Cytol 181, 213–320.CrossRefGoogle ScholarPubMed
Bancroft, J.D., Layton, C. & Suvarna, S.K. (2013). Bancroft’s Theory and Practice of Histological Techniques, 7th ed. London: Churchill Livingstone.Google Scholar
Bandyopadhyay, R., DasGupta, M., Chattopadhyay, R. & Chakraborty, S. (2011). Exogenous melatonin induces simultaneous stimulation of pineal and adrenocortical function in relation to karyomorphology, cell proliferation and corticosterone content in male mice (Mus musculus). Proc Zool Soc 64(2), 78–86.CrossRefGoogle Scholar
Benítez-King, G. (2006). Melatonin as a cytoskeletal modulator: Implications for cell physiology and disease. J Pineal Res 40(1), 1–9.CrossRefGoogle ScholarPubMed
Burgoyne, R.D. (1991). Control of exocytosis in adrenal chromaffin cells. Acta Biochim Biophys 1071, 174–202.CrossRefGoogle ScholarPubMed
Carmona, C., Luesma-Bartolome, M.J. & Escribano, C. (2011). Identification of telocytes in the lamina propria of rat duodenum: Transmission electron microscopy. Cell Mol Med 15, 26–30.CrossRefGoogle Scholar
Carrasco-Serrano, C. & Criado, M. (2004). Glucocorticoid activation of neuronal nicotinic acetylcholine receptor A 7 subunit gene: Involvement of transcription factor Egr-1. FEBS Lett 566, 247–250.CrossRefGoogle Scholar
Chen, C.Q., Fichna, J., Bashashati, M., Li, Y.Y. & Storr, M. (2011). Distribution, function and physiological role of melatonin in the lower gut. World J Gastroenterol 17, 3888–3898.CrossRefGoogle ScholarPubMed
Choi, S., Dadakhujaev, S., Ryu, H. & Kim, E.K. (2011). Melatonin protects against oxidative stress in granular corneal dystrophy type 2 corneal fibroblasts by mechanisms that involve membrane melatonin receptors. Pineal Res 51(1), 94–103.CrossRefGoogle ScholarPubMed
Coupland, R.E. (1989). The natural history of the chromaffin cell—Twenty-five years on the beginning. Arch Histol Cytol 52(Suppl), 331–341.CrossRefGoogle ScholarPubMed
Cretoiu, S.M., Cretoiu, D., Suciu, L. & Popescu, L.M. (2009). Interstitial Cajal-like cells of human Fallopian tube express estrogen and progesterone receptors. Mol Hist 40, 387–394.CrossRefGoogle ScholarPubMed
Crivellato, E., Belloni, A., Nico, B., Nussdorfer, G.G. & Ribatti, D. (2004). Chromaffin granules in the rat adrenal medulla release their secretory content in a particulate fashion. Anat Rec A Discov Mol Cell Evol Biol 277, 204–208.CrossRefGoogle Scholar
Crivellato, E., Nico, B., Perissin, L. & Ribatti, D. (2003). Ultrastructural morphology of adrenal chromaffin cells indicative of a process of piecemeal degranulation. Anat Rec 270, 103–108.CrossRefGoogle ScholarPubMed
Decker, J.F. & Quay, W.B. (1982). Stimulatory effect of melatonin on ependymal epithelium of choroid plexuses in golden hamsters. J Neural Transm 55, 53–67.CrossRefGoogle ScholarPubMed
Duquette, R.A., Shmygol, A., aillant, C., Mobasheri, A., Pope, M., Burdyga, T. & Wray, S. (2005). Vimentin-positive, c-kit-negative interstitial cells in human and rat uterus: A role in pacemaking? Biol Reprod 72, 276–283.CrossRefGoogle ScholarPubMed
Dvorak, A.M. (1998). A role for vesicles in human basophil secretion. Cell Tissue Res 293, 1–22.CrossRefGoogle ScholarPubMed
Dvorak, A.M., MacGlashan, D.W. Jr, Morgan, E.S. & Lichtenstein, L.M. (1996). Vesicular transport of histamine in stimulated human basophils. Blood 88, 4090–4101.CrossRefGoogle ScholarPubMed
Eranko, O. & Eranko, L. (1971). Small, intensely fluorescent granule-containing cells in the sympathetic ganglion of the rat. Progr Brain Res 34, 39–50.CrossRefGoogle Scholar
Feng, C., Li, H.Z., Yan, W.G., Luo, Y.F. & Cao, J.L. (2005). The expression and significance of chromogranin A and synaptophysin in adrenal gland tumors. Zhonghua Zhong Liu Za Zhi 27(8), 486–488.Google ScholarPubMed
Goldstein, D.S., Eisenhofer, G. & Kopin, I.J. (2003). Sources and significance of plasma levels of catechols and their metabolites in humans. J Pharmacol Exp Therap 305, 800–811.CrossRefGoogle ScholarPubMed
Greco, D.S. & Stabenfeld, G.H. (2007). Endocrine glands and their function. In Textbook of Veterinary Physiology, Cunningham, J.G. & Klein, B.G. (Eds.), pp. 428–464, 4th ed. St. Louis: Saunders.Google Scholar
Hardeland, R. (2009). Melatonin: Signaling mechanisms of a pleiotropic agent. Biofactors 35, 183–192.CrossRefGoogle ScholarPubMed
Hart, K.A. & Barton, M.H. (2011). Adrenocortical insufficiency in horses and foals. J Vet Clin North Am Equine Pract 27(1), 19–34.CrossRefGoogle ScholarPubMed
Hiremagalur, B. & Sabban, E.L. (1995). Nicotine elicits changes in expression of adrenal catecholamine biosynthetic enzymes, neuropeptide Y and immediate early genes by injection but not continuous administration. Mol Brain Res 32, 109–115.CrossRefGoogle Scholar
Jahng, J.W., Houpt, T.A., Joh, T.H. & Wessel, T.C. (1997). Expression of catecholamine-synthesizing enzymes, peptidylglycine alpha-a mediating monooxygenase, and neu-ropeptide Y mRNA in the rat adrenal medulla after acute systemic nicotine. J Mol Neurosci 8, 45–52.CrossRefGoogle Scholar
Jahn, R., Schiebler, W., Ouimet, C. & Greengard, P.A. (1985). 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A 82, 4137–4141.CrossRefGoogle ScholarPubMed
Jin, J.X., Lee, S., Taweechaipaisankul, A., Kim, G.A. & Lee, B.C. (2017). Melatonin regulates lipid metabolism in porcine oocytes. J Pineal Res 62(2), 1–10.CrossRefGoogle ScholarPubMed
Junqueira, L.C. & Carneiro, J. (2003). Basic Histology: Text and Atlas, pp. 413–418, 10th ed. New York/Chicago/San Francisco/London: McGraw-Hill Companies.Google Scholar
Karnovsky, M.J. (1965). A formaldehyde-glutraldehyde fixative of high osmolarity for use in electron microscopy. Cell Biol 27, 137A.Google Scholar
Kesse, W.K., Parker, T.L. & Coupland, R.E. (1988). The innervation of the adrenal gland. I. The source of pre- and postganglionic nerve fibers to the rat adrenal gland. J Anat 157, 33–41.Google Scholar
Kobayashi, S. & Coupland, R.E. (1993). Morphological aspects of chromaffin tissue: The differential fixation of adrenaline and noradrenaline. J Anat 183, 223–235.Google ScholarPubMed
Kobayashi, S. & Coupland, R.F. (1977). Two populations of microvesicles in the SGC (small granule chromaffin) cells of the mouse adrenal medulla. Arch Histol Jpn 40(3), 251–259.CrossRefGoogle ScholarPubMed
Kobayashi, S., Miyabyashi, T., Uchida, T. & Yanaihara, N. (1985). Met-enkephalin-Arg6-Gly7-Leu8 in large-cored vesicles of splanchnic nerve terminals innervating guinea pig adrenal chromaffin cells. Neurosci Lett 53, 247–252.CrossRefGoogle ScholarPubMed
Langevad, L., Madsen, C.G., Siebner, H. & Garde, E. (2014). MRI of the pineal gland. Ugeskreft Laeger 176(46), 10–18.Google ScholarPubMed
Langley, K. & Grant, N.J. (1999). Molecular markers of sympathoadrenal cells. Cell Tissue Res 298(2), 185–206.CrossRefGoogle ScholarPubMed
Lewis, P.R. & Shute, C.C.D. (1969). An electron-microscopic study of cholinesterase distribution in the rat adrenal medulla. J Microsc 89, 181–193.CrossRefGoogle ScholarPubMed
Li, H.S., Lu, H., Liu, J. & Zhang, H. (2014). Scanning electron microscope evidence of telocytes in vasculature. J Cell Mol Med 18, 1486–1489.CrossRefGoogle ScholarPubMed
Lincoln, G.A., Fraser, H.M. & Fletcher, T.J. (1984). Induction of early rutting in male red deer (Cervus elaphus) by melatonin and its dependence on LHRH. Reprod Fertil 72, 339–343.CrossRefGoogle Scholar
Lincoln, G.A. & Short, R.V. (1980). Seasonal breeding: Nature’s contraceptive. Recent Prog Horm Res 36, 1–52.Google ScholarPubMed
Maxwell, G.D., Forbes, M.E. & Christie, D.S. (1988). Analysis of the development of cellular subsets present in the neural crest using cell sorting and cell culture. Neuron 1, 557–568.CrossRefGoogle ScholarPubMed
Mayo, J.C., Sainz, R.M., Tan, D.X., Antolín, I., Rodríguez, C. & Reiter, R.J. (2005). Melatonin and Parkinson’s disease. Endocrine 27(2), 169–178.CrossRefGoogle ScholarPubMed
Mokhtar, D.M., Abd-Elhafeez, H.H., Abou- Elmagd, A. & Hassan, A.H.S. (2016). Melatonin administration induced reactivation in the seminal gland of the Soay rams during nonbreeding season: An ultrastructural and morphometrical study. J Morphol 277, 231–243.CrossRefGoogle ScholarPubMed
Niles, L.P., Armstrong, K.J., Castro, L.M.R., Dao, C.V., Sharma, R., McMillan, C.R., Doering, L.C. & Kirkham, D.L. (2004). Neural stem cells express melatonin receptors and neurotrophic factors: Colocalization of the MT1 receptor with neuronal and glial markers. BMC Neurosci 5, 41.CrossRefGoogle ScholarPubMed
Nussdorfer, G.G., Mazzocchi, G. & Meneghelli, V. (1978). Cytophysiology of the adrenal zona fasciculata. Int Rev Cytol 55, 291–365.CrossRefGoogle ScholarPubMed
Pandi-Perumal, S.R., Srinivasan, V., Maestroni, G.L.M., Cardinali, D.P., Poeggeler, B. & Hardeland, R. (2006). Melatonin nature’s most versatile biological signal? FEBS J 273, 2813–2838.CrossRefGoogle ScholarPubMed
Pandi-Perumal, S.R., Trakht, I., Srinivasan, V., Spence, D.W., Maestroni, G.J., Zisapel, N. & Cardinali, D.P. (2008). Physiological effects of melatonin: Role of melatonin receptors and signal transduction pathways. Prog Neurobiol 85(3), 335–353.CrossRefGoogle ScholarPubMed
Rebuffat, P., Mazzocchi, G., Stachowiak, A., Belloni, A.S., Coi, A. & Nussdorfer, G.G. (1988). A morphometric study of the effects of melatonin on the rat adrenal zona glomerulosa. Exp Clin Endocrinol Diab 91(1), 59–64.CrossRefGoogle ScholarPubMed
Rendon, N.M., Rudolph, L.M., Sengelaub, D.R. & Demas, G.E. (2015). The agonistic adrenal: Melatonin elicits female aggression via regulation of adrenal androgens. Proc R Soc B 282, 2015–2080.CrossRefGoogle ScholarPubMed
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17, 208–212.CrossRefGoogle ScholarPubMed
Rosol, T.J., Yarrington, J.T., Latendresse, J. & Capen, C.C. (2001). Adrenal gland: Structure, function, and mechanisms of toxicity. Toxicol Pathol 29(1), 41–48.CrossRefGoogle ScholarPubMed
Ross, M.H., Kaye, G.I. & Romrell, L.J. (1995). Histology: A Text and Atlas. Baltimore; London: Williams & Wilkins.Google Scholar
Rumessen, J.J. (1994). Identification of interstitial cells of Cajal: Significance for studies of human small intestine and colon. Dan Med Bull 41, 275–293.Google ScholarPubMed
Rusu, M.C., Mirancea, N., Mănoiu, V.S., Vălcu, M., Nicolescu, M.I. & Păduraru, D. (2012). Skin telocytes. Ann Anat 194, 359–367.CrossRefGoogle ScholarPubMed
Ryan, T.A. (2003). Kiss-and-run, fuse-pinch-and-linger, fuse-and collapse: The life and times of a neurosecretory granule. Proc Natl Acad Sci USA 100, 2171–2173.CrossRefGoogle ScholarPubMed
Sanders, K.M., Koh, S.D. & Ward, S.M. (2006). Interstitial cells of Cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 68, 307–343.CrossRefGoogle ScholarPubMed
Schneider, J., Lother, A., Hein, L. & Gilsbach, R. (2011). Chronic cardiac pressure overload induces adrenal medulla hypertrophy and increased catecholamine synthesis. Basic Res Cardiol 106(4), 591–602.CrossRefGoogle ScholarPubMed
Shepherd, S.P. & Holzwarth, M.A. (2001). Chromaffin-adrenocortical cell interactions: Effects of chromaffin cell activation in adrenal cell cocultures. Am J Physiol Cell Physiol 280(1), C61–C71.CrossRefGoogle ScholarPubMed
Tank, A.W. & Lee Wong, D. (2015). Peripheral and central effects of circulating catecholamines. Comprehens Physiol 5, 1–15.Google ScholarPubMed
Tomás-Zapico, C. & Coto-Montes, A. (2005). A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J Pineal Res 39(2), 99–104.CrossRefGoogle ScholarPubMed
Unsicker, K., buraHa-Fluh, O. & Zwarg, U. (1978). Different types of small granule-containing cells and neurons in the guinea-pig adrenal medulla. Cell Tissue Res 189, 109–130.CrossRefGoogle ScholarPubMed
Uyanikgil, Y., Cavusoglu, T., Kılıc, K.D., Yigitturk, G., Celik, S., Tubbs, R.S. & Turgut, M. (2017). Useful effects of melatonin in peripheral nerve injury and development of the nervous system. J Brachial Plexus Peripheral Nerve Injury 12(1), 1–6.Google ScholarPubMed
Wiedenmann, B. (1991). Synaptophysin A widespread constituent of small neuroendocrine vesicles and a new tool in tumor diagnosis. Acta Oncologica 30(4), 435–440.CrossRefGoogle Scholar
Wiedenmann, B. & Franke, W.W. (1985). Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41, 1017–1028.CrossRefGoogle Scholar
Winkler, H. & Carmichael, S.W. (1982). The chromaffin granule. In The Secretory Granule , Poisner, A.M. & Trifaro, J.M. (Eds.), pp 3–79. Amsterdam: Elsevier Biomedical Press.Google Scholar
Wurtman, R.J. (2002). Stress and the adrenocortical control of epinephrine synthesis. Metabolism 51, 11–14.CrossRefGoogle ScholarPubMed
Yokota, R. (1973). The granule-containing cell somata in the superior cervical ganglion of the rat, as studied by a serial sampling method for electron microscopy. Z Zellforsch 141, 331–345.CrossRefGoogle ScholarPubMed
Zhang, J., Pho, V., Bonasera, S.J., Holzmann, J., Tang, A.T., Hellmuth, J., Tang, S., Janak, P.H., Tecott, L.H. & Huang, E.J. (2007). Essential function of HIPK2 inTGFbeta-dependent survival of midbrain dopamine neurons. Nat Neurosci 10, 77–86.CrossRefGoogle ScholarPubMed
Zheng, Y., Zhu, T., Lin, M., Wu, D. & Wang, X. (2012). Telocytes in the urinary system. Trans Med 10, 188.CrossRefGoogle ScholarPubMed