Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-18T23:09:52.663Z Has data issue: false hasContentIssue false

Seasonal Variation of the Intraepithelial Gland in Camel Epididymis with Special Reference to Autophagosome

Published online by Cambridge University Press:  18 June 2019

Fatma M. Abdel-Maksoud*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Egypt
Manal T Hussein
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Egypt
Abdelraheim Attaai
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Egypt
*
*Author for correspondence: Fatma M. Abdel-Maksoud, E-mail: fatma.abdelmaksoud@vet.au.edu.eg
Get access

Abstract

The key role of the epididymis is contributing to sperm storage, maturation, and survival. The epididymis of camel has a unique structure called the intraepithelial gland. The present work aimed to investigate the structure of the epididymal intraepithelial gland with special references to the seasonal variation. The samples were collected from the distal part of the corpus epididymes of completely healthy mature camels (Camelus dromedarius) in the breeding and nonbreeding seasons. Tomato lectin-positive material had been demonstrated within the epididymal spermatozoa. Here, we provide the first transmission electron microscopic study for the intraepithelial gland of camel epididymis detecting the autophagy during the nonbreeding season. The autophagosomes originated from the endoplasmic reticulum, surrounding mitochondria, and located mainly next to the basement membrane. This location is probably valuable for subsequent passing of their contents into the interstitium for possible recycling. The histochemical and ultrastructural characteristics of the gland in the breeding season indicated a hyperactive secretory microenvironment enriched with the glycoprotein-producing machinery, which could be controlled by androgens. The present data suggest that the camel intraepithelial gland has a significant impact on the reproductive activity through their secretory microenvironment during the breeding season. Moreover, it recycles the unused organelles or proteins for reuse or to supply energy under stress conditions in the nonbreeding season.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2019 

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 El-maksoud, FM (2010). Morphological studies on the seasonal changes in the epididymis of the one-humped camel (Camelus dromedarius). M.V.Sc. Assiut University. Faculty of Veterinary Medicine.Google Scholar
Abd-Elmaksoud, AS, Ebada, SM & Shoaib, MB (2012). Localisation of cytokeratin and smooth muscle actin in the accessory genital glands of camels (Camelus dromedarius) during rutting and non-rutting seasons. Bulg J Vet Med 15, 213227.Google Scholar
Akama, TO, Nakagawa, H, Sugihara, K, Narisawa, S, Ohyama, C, Nishimura, S-I, O'brien, DA, Moremen, KW, Millán, JL & Fukuda, MN (2002). Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 295, 124127.Google Scholar
Akbarsha, MA, Faisal, K & Radha, A (2015). The Epididymis: Structure and Function. Mammalian Endocrinology and Male Reproductive Biology.Boca Raton: CRC/Taylor & Francis, pp. 119120.Google Scholar
Alkafafy, M (2005). Glycohistochemical, Immunohistochemical and Ultrastructural Studies of the bovine epididymis. Anatomy, faculty of veterinary Medicine, Ludwig- Maximilians-Universität, MÜnchen.Google Scholar
Alkafafy, M, Ebada, S, Rashed, R & Attia, H (2012). Comparative morphometric and glycohistochemical studies on the epididymal duct in the donkey (Equus asinus) and dromedary camel (Camelus dromedarius). Acta Histochem 114, 434447.Google Scholar
Alkafafy, M, Elnasharty, M, Sayed-Ahmed, A & Abdrabou, M (2011). Immunohistochemical studies of the epididymal duct in Egyptian water buffalo (Bubalus bubalis). Acta Histochem 113, 96102.Google Scholar
Arenas, MI, de Miguel, MP, Bethencourt, FR, Fraile, B, Royuela, M & Paniagua, R (1996). Lectin histochemistry in the human epididymis. J Reprod Fertil 106, 313320.Google Scholar
Aureli, G, Arrighi, S & Romanello, MG (1984). Ultrastructural and cytochemical study on the epithelium lining ductuli efferentes in Equus asinus. Basic Appl Histochem 28, 101115.Google Scholar
Axner, E, Linde-Forsberg, C & Einarsson, S (1999). Morphology and motility of spermatozoa from different regions of the epididymal duct in the domestic cat. Theriogenology 52, 767778.Google Scholar
Bancroft, JD & Steven, A (1996). Theory and Practice of Histological Techniques, 4th ed. New York, Edinburgh, London, Madrid, Melbourne, San Francisco, Tokyo: Churchill Livingstone.Google Scholar
Beato, M (1989). Gene regulation by steroid hormones. Cell 56, 335344.Google Scholar
Binato de Souza, AP, Schorr-Lenz, ÂM, Lucca, F, & Bustamante-Filho, IC (2017). The epididymis and its role on sperm quality and male fertility. Anim Reprod 14, 12341244.Google Scholar
Blommaart, EF, Krause, U, Schellens, JP, Vreeling-Sindelárová, H & Meijer, AJ (1997). The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243, 240246.Google Scholar
Bogdanov, AA Jr., Lin, CP, Simonova, M, Matuszewski, L & Weissleder, R (2002). Cellular activation of the self-quenchedfluorescent reporter probe in tumor microenvironment. Neoplasia 4, 228236.Google Scholar
Bragulla, HH & Homberger, DG (2009). Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J Anat 214, 516559.Google Scholar
Calvo, A, Bustos-Obregon, E & Pastor, LM (1997). Morphological and histochemical changes in the epididymis of hamsters (Mesocricetus auratus) subjected to short photoperiod. J Anat 191(Pt 1), 7788.Google Scholar
Dacheux, JL & Dacheux, F (2014). New insights into epididymal function in relation to sperm maturation. Reproduction 147, R27R42.Google Scholar
El-Bahrawy, KA & El Hassanein, EE (2011). Seasonal variations of some blood and seminal plasma biochemical parameters of male dromedary camels. Am-Eurasian J Agric Environ Sci 10, 354360.Google Scholar
Elmore, S (2007). Apoptosis: A review of programmed cell death. Toxicol Pathol 35, 495516.Google Scholar
Feng, Y, He, D, Yao, Z & Klionsky, DJ (2014). The machinery of macroautophagy. Cell Res 24, 2441.Google Scholar
Goldstein, IJ & Poretz, RD (1986). Isolation, physicochemical characterization, and carbohydrate-binding specificity of lectins. In The Lectins, Properties, Functions, and Applications in Biology and Medicine, Liener, IE, Sharon, N & Goldstein, IJ (Eds.), pp. 33247. New York: Academic Press.Google Scholar
González, CR, Muscarsel Isla, ML & Vitullo, AD (2018). The balance between apoptosis and autophagy regulates testis regression and recrudescence in the seasonal-breeding South American plains vizcacha, Lagostomus maximus. PLoS ONE 13, 115.Google Scholar
Guyonnet, B, Marot, G, Dacheux, JL, Mercat, MJ, Schwob, S, Jaffrezic, F & Gatti, JL (2009). The adult boar testicular and epididymal transcriptomes. BMC Genomics 10, 369.Google Scholar
Hess, RA (2015). Small tubules, surprising discoveries: From efferent ductules in the Turkey to the discovery that estrogen receptor alpha is essential for fertility in the male. Anim Reprod 12, 723.Google Scholar
Huang, H-H & Stanley, P (2010). A testis-specific regulator of complex and hybrid N-glycan synthesis. J Cell Biol 190, 893910.Google Scholar
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27, 137A138A.Google Scholar
Knowles, MR, Daniels, LA, Davis, SD, Zariwala, MA & Leigh, MW (2013). Primary ciliary dyskinesia. Recent advances in diagnostics, genetics, and characterization of clinical disease. Am J Respir Crit Care Med 188, 913922.Google Scholar
Leung, PS, Wong, TP & Sernia, C (1999). Angiotensinogen expression by rat epididymis: evidence for an intrinsic, angiotensin-generating system. Mol. Cell Endocrinol 155, 115122.Google Scholar
Levine, B & Klionsky, DJ (2017). Autophagy wins the 2016 nobel prize in physiology or medicine: Breakthroughs in baker's yeast fuel advances in biomedical research. Proc Natl Acad Sci USA 114, 201205.Google Scholar
Lorin, S, Hamai, A, Mehrpour, M & Codogno, P (2013). Autophagy regulation and its role in cancer. Semin Cancer Biol 23, 361379.Google Scholar
Matsumoto, A & Prins, GS (2002). Androgenic regulation of expression of androgen receptor protein in the perineal motoneurons of aged male rats. J Comp Neurol 443, 383387.Google Scholar
Merkle, R & Cummings, R (1987). Relationship of the terminal sequences to the length of poly-N-acetyllactosamine chains in asparagine-linked oligosaccharides from the mouse lymphoma cell line BW5147. Immobilized tomato lectin interacts with high affinity with glycopeptides containing long poly-N-acetyllactosamine chains. J Biol Chem 262, 81798189.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, 11731188.Google Scholar
Molin, SO, Rosengren, L, Baudier, J, Hamberger, A & Haglid, K (1985). S-100 alphalike immunoreactivity in tubules of rat kidney. A clue to the function of a “brain-specific” protein. J. Histochem. Cytochem 33, 367374.Google Scholar
Nagata, Y & Burger, MM (1974). Wheat germ agglutinin. Molecular characteristics and specificity for sugar binding. J Biol Chem 249, 31163122.Google Scholar
Naito, Y, Minamihara, T, Ando, A, Marutani, T, Oguri, S & Nagata, Y (2001). Domain construction of cherry-tomato lectin: Relation to newly found 42-kDa protein. Biosci Biotechnol Biochem 65, 8693.Google Scholar
Nixon, RA, Wegiel, J, Kumar, A, Yu, WH, Peterhoff, C, Cataldo, A & Cuervo, AM (2005). Extensive involvement of autophagy in Alzheimer disease: An immuno-electron microscopy study. J Neuropathol Exp Neurol 64, 113122.Google Scholar
O’Mahony, OA, Djahanbahkch, O, Mahmood, T, Puddefoot, JR & Vinson, GP (2000). Angiotensin II in human seminal fluid. Hum. Reprod 15, 13451349.Google Scholar
Pearse, AGE (1960). Histochemistry: Theoretical and Applied. Brown, Boston: Little.Google Scholar
Reynolds, ES (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208212.Google Scholar
Richardson, KC, Jarett, L & Finke, EM (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35, 313323.Google Scholar
Roberts, KP, Ensrud, KM & Hamilton, DW (2002). A comparative analysis of expression and processing of the rat epididymal fluid and sperm-bound forms of proteins D and E. Biol Reprod 67, 525533.Google Scholar
Singh, UB & Bharadwaj, MB (1980). Histological studies on the testicular seminal pathway and changes in the epididymis of the camel (Camelus dromedarius). Part IV. Acta Anat (Basel) 108, 481489.Google Scholar
Sostaric, E, Aalberts, M, Gadella, BM & Stout, TA (2008). The roles of the epididymis and prostasomes in the attainment of fertilizing capacity by stallion sperm. Anim Reprod Sci 107, 237248.Google Scholar
Su, M, Mei, Y & Sinha, S (2013). Role of the crosstalk between autophagy and apoptosis in cancer. J Oncol 2013, 102735.Google Scholar
Sullivan, R & Saez, F (2013). Epididymosomes, prostasomes, and liposomes: Their roles in mammalian male reproductive physiology. Reproduction 146, R21R35.Google Scholar
Suzuki, F & Racey, PA (1976). Fine structural changes in the epididymal epithelium of moles (Talpa europaea) throughout the year. J Reprod Fertil 47, 4754.Google Scholar
Tingari, MD & Moniem, KA (1979). On the regional histology and histochemistry of the epididymis of the camel (Camelus dromedarius). J Reprod Fertil 57, 1120.Google Scholar
Toivola, DM, Tao, GZ, Habtezion, A, Liao, J & Omary, MB (2005). Cellular integrity plus: Organelle-related and protein-targeting functions of intermediate filaments. Trends Cell Biol 15, 608617.Google Scholar
Ueda, T, Fujimori, O, Tsukise, A & Yamada, K (1998). Histochemical analysis of sialic acids in the epididymis of the rat. Histochem Cell Biol 109, 399407.Google Scholar
Vaidya, MM & Kanojia, D (2007). Keratins: Markers of cell differentiation or regulators of cell differentiation? J Biosci 32, 629634.Google Scholar
Zayed, AE, Aly, K, Ibrahim, IA & Abd El-Maksoud, FM (2012 a). Morphological studies on the epididymal duct of the one-humped camel (Camelus dromedaries). J Vet Med 2, 245254.Google Scholar
Zayed, AE-Z, Aly, KH, Ibrahim, IA-A & El-maksoud, FMA (2012 b). Morphological studies on the seasonal changes in the epididymal duct of the one-humped camel (Camelus dromedarius). Vet Sci Dev 2, 3.Google Scholar
Zayed, AE, Hifny, A, Abou-Elmagd, A & Wrobel, KH (1995). Seasonal changes in the intertubular tissue of the camel testis (Camelus dromedarius). Ann Anat 177, 199212.Google Scholar
Zhou, Y, Sun, Z, Means, AR, Sassone-Corsi, P & Bernstein, KE (1996). cAMP-response element modulator tau is a positive regulator of testis angiotensin converting enzyme trans-cripttion. Proc Natl Acad Sci USA 93(22), 1226212266.Google Scholar