Skip to main content
×
×
Home

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

  • Doaa M. Mokhtar (a1), Manal T. Hussein (a1) and Ahmed H. S. Hassan (a1)
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.

Copyright
Corresponding author
* Corresponding author. doaamokhtar33@yahoo.com
References
Hide All
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), 2954.
Aunis, D. (1998). Exocytosis in chromaffin cells of the adrenal medulla. Int Rev Cytol 181, 213320.
Bancroft, J.D., Layton, C. & Suvarna, S.K. (2013). Bancroft’s Theory and Practice of Histological Techniques, 7th ed. London: Churchill Livingstone.
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), 7886.
Benítez-King, G. (2006). Melatonin as a cytoskeletal modulator: Implications for cell physiology and disease. J Pineal Res 40(1), 19.
Burgoyne, R.D. (1991). Control of exocytosis in adrenal chromaffin cells. Acta Biochim Biophys 1071, 174202.
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, 2630.
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, 247250.
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, 38883898.
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), 94103.
Coupland, R.E. (1989). The natural history of the chromaffin cell—Twenty-five years on the beginning. Arch Histol Cytol 52(Suppl), 331341.
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, 387394.
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, 204208.
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, 103108.
Decker, J.F. & Quay, W.B. (1982). Stimulatory effect of melatonin on ependymal epithelium of choroid plexuses in golden hamsters. J Neural Transm 55, 5367.
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, 276283.
Dvorak, A.M. (1998). A role for vesicles in human basophil secretion. Cell Tissue Res 293, 122.
Dvorak, A.M., MacGlashan, D.W. Jr, Morgan, E.S. & Lichtenstein, L.M. (1996). Vesicular transport of histamine in stimulated human basophils. Blood 88, 40904101.
Eranko, O. & Eranko, L. (1971). Small, intensely fluorescent granule-containing cells in the sympathetic ganglion of the rat. Progr Brain Res 34, 3950.
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), 486488.
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, 800811.
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.
Hardeland, R. (2009). Melatonin: Signaling mechanisms of a pleiotropic agent. Biofactors 35, 183192.
Hart, K.A. & Barton, M.H. (2011). Adrenocortical insufficiency in horses and foals. J Vet Clin North Am Equine Pract 27(1), 1934.
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, 109115.
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, 4552.
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, 41374141.
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), 110.
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.
Karnovsky, M.J. (1965). A formaldehyde-glutraldehyde fixative of high osmolarity for use in electron microscopy. Cell Biol 27, 137A.
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, 3341.
Kobayashi, S. & Coupland, R.E. (1993). Morphological aspects of chromaffin tissue: The differential fixation of adrenaline and noradrenaline. J Anat 183, 223235.
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), 251259.
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, 247252.
Langevad, L., Madsen, C.G., Siebner, H. & Garde, E. (2014). MRI of the pineal gland. Ugeskreft Laeger 176(46), 1018.
Langley, K. & Grant, N.J. (1999). Molecular markers of sympathoadrenal cells. Cell Tissue Res 298(2), 185206.
Lewis, P.R. & Shute, C.C.D. (1969). An electron-microscopic study of cholinesterase distribution in the rat adrenal medulla. J Microsc 89, 181193.
Li, H.S., Lu, H., Liu, J. & Zhang, H. (2014). Scanning electron microscope evidence of telocytes in vasculature. J Cell Mol Med 18, 14861489.
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, 339343.
Lincoln, G.A. & Short, R.V. (1980). Seasonal breeding: Nature’s contraceptive. Recent Prog Horm Res 36, 152.
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, 557568.
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), 169178.
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, 231243.
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.
Nussdorfer, G.G., Mazzocchi, G. & Meneghelli, V. (1978). Cytophysiology of the adrenal zona fasciculata. Int Rev Cytol 55, 291365.
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, 28132838.
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), 335353.
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), 5964.
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, 20152080.
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17, 208212.
Rosol, T.J., Yarrington, J.T., Latendresse, J. & Capen, C.C. (2001). Adrenal gland: Structure, function, and mechanisms of toxicity. Toxicol Pathol 29(1), 4148.
Ross, M.H., Kaye, G.I. & Romrell, L.J. (1995). Histology: A Text and Atlas. Baltimore; London: Williams & Wilkins.
Rumessen, J.J. (1994). Identification of interstitial cells of Cajal: Significance for studies of human small intestine and colon. Dan Med Bull 41, 275293.
Rusu, M.C., Mirancea, N., Mănoiu, V.S., Vălcu, M., Nicolescu, M.I. & Păduraru, D. (2012). Skin telocytes. Ann Anat 194, 359367.
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, 21712173.
Sanders, K.M., Koh, S.D. & Ward, S.M. (2006). Interstitial cells of Cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 68, 307343.
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), 591602.
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), C61C71.
Tank, A.W. & Lee Wong, D. (2015). Peripheral and central effects of circulating catecholamines. Comprehens Physiol 5, 115.
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), 99104.
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, 109130.
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), 16.
Wiedenmann, B. (1991). Synaptophysin A widespread constituent of small neuroendocrine vesicles and a new tool in tumor diagnosis. Acta Oncologica 30(4), 435440.
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, 10171028.
Winkler, H. & Carmichael, S.W. (1982). The chromaffin granule. In The Secretory Granule , Poisner, A.M. & Trifaro, J.M. (Eds.), pp 379. Amsterdam: Elsevier Biomedical Press.
Wurtman, R.J. (2002). Stress and the adrenocortical control of epinephrine synthesis. Metabolism 51, 1114.
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, 331345.
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, 7786.
Zheng, Y., Zhu, T., Lin, M., Wu, D. & Wang, X. (2012). Telocytes in the urinary system. Trans Med 10, 188.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Microscopy and Microanalysis
  • ISSN: 1431-9276
  • EISSN: 1435-8115
  • URL: /core/journals/microscopy-and-microanalysis
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 7
Total number of PDF views: 43 *
Loading metrics...

Abstract views

Total abstract views: 164 *
Loading metrics...

* Views captured on Cambridge Core between 4th December 2017 - 21st April 2018. This data will be updated every 24 hours.