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Immunohistochemical and Ultrastructural Features of the Seasonal Changes in the Epididymal Epithelium of Camel (Camelus dromedarius)

Published online by Cambridge University Press:  23 September 2019

Dalia Ibrahim
Affiliation:
Department of Histology, Faculty of Veterinary Medicine, South Valley University, Qena 83523, Egypt
Fatma M. Abdel-Maksoud*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assuit University, Assuit, Egypt
*
*Author for correspondence: Fatma M. Abdel-Maksoud, E-mail: [email protected]
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Abstract

In order to evaluate the influence of reproductive activity on the functional role of the epididymal epithelium in the Egyptian dromedary camel, Connexin-43 (Cx-43), vascular endothelial growth factor (VEGF), and androgen receptor (AR) immunoreactivity in the epididymal epithelium and the fine structure of the principal, dark, basal, apical, and halo cells were investigated. The secretory activity of the principal cells was amplified in the breeding season, while its endocytotic function became more active in the nonbreeding season. This was evidenced by punctate strong immunoreactive signals for Cx-43, which appeared to be more intense in the apical region of these epithelial cells, and the extremely long slender stereocilia (microvilli) with multiple junctional complexes. The nonbreeding principal cells revealed granular immunoreactive signals for VEGF scattered in the apical and basal cytoplasm. Ultrastructurally, both extreme vacuolation and several multivesicular inclusion bodies were observed in their cytoplasm. Dark cell size greatly diminished in the nonbreeding season and their nuclear morphology greatly changed from oval to lobulated shape. The plasma membrane of the apical cells expressed several infoldings (microvilli) in the breeding season. However, it was almost smooth in the nonbreeding season except for a small microvillus that appeared as a bleb-like projection. In some regions, a strong dense immunoreactivity for VEGF could be recognized in the cytoplasm of the apical cells and some basal ones. Halo cells with numerous multivesicular inclusions occupying most of the cytoplasm and a lobulated eccentric nucleus were detected in the nonbreeding season. In conclusion, these findings indicate that the reproductive activity has a significant impact on the immunohistochemical and ultrastructural profiles of the epithelial cells lining the Egyptian dromedary camel epididymis.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2019 

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References

Abdel-Raouf, M & El-Naggar, MA (1964). Studies on reproduction in camels (Camelus dromedarius): 1. Mating technique and collection of semen. J Vet Sci 1, 113119.Google Scholar
Abe, K, Takano, H & Ito, T (1983). Ultrastructure of the mouse epididymal duct with special reference to the regional differences of the principal cells. Arch Histol Jpn 46(1), 5168.Google Scholar
Aguilera-Merlo, C, Fogal, T, Sator, T, Dominguez, S, Sosa, M, Scardapane, L & Piezzi, R (2009). Ultrastructural and biochemical seasonal changes in epididymal corpus and cauda of viscacha (Lagostomus maximus maximus). J Morphol 270(7), 805814.Google Scholar
Akbarsha, MA, Faisal, K & Radha, A (2015). The epididymis: structure and function. In Mammalian Endocrinology and Male Reproductive Biology, pp. 119120. Boca Raton: CRC/Taylor & Francis.Google Scholar
Al Eknah, MM (2000). Reproduction in Old World camels. Anim Reprod Sci 60–61, 583592.Google Scholar
Altay, B, Turna, B, Öktem, G, Aktuğ, H, Semerci, B & Bilir, A (2008). Immunohistochemical expression of connexin 43 and occludin in the rat testis after epididymal and vasal ligation. Fertil Steril 90(1), 141147.Google Scholar
Bates, D, Hillman, N, Pocock, T & Neal, C (2002). Regulation of microvascular permeability by vascular endothelial growth factors. J Anat 200(5), 523534.Google Scholar
Beato, M (1989). Gene regulation by steroid hormones. Cell 56(3), 335344.Google Scholar
Breen, EC (2007). VEGF in biological control. J Cell Biochem 102(6), 13581367.Google Scholar
Brown, BW (2000). A review on reproduction in South American camelids. Anim Reprod Sci 58(3–4), 169195.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
Dufresne, J, Finnson, KW, Gregory, M & Cyr, DG (2003). Expression of multiple connexins in the rat epididymis indicates a complex regulation of gap junctional communication. Am J Physiol Cell Physiol 284(1), C33C43.Google Scholar
Ebisch, IM, Thomas, CM, Wetzels, AM, Willemsen, WN, Sweep, FC & Steegers-Theunissen, RP (2008). Review of the role of the plasminogen activator system and vascular endothelial growth factor in subfertility. Fertil Steril 90(6), 23402350.Google Scholar
Ergün, S, Kilic, N, Fiedler, W & Mukhopadhyay, A (1997). Vascular endothelial growth factor and its receptors in normal human testicular tissue. Mol Cell Endocrinol 131(1), 920.Google Scholar
Ergün, S, Luttmer, W, Fiedler, W & Holstein, A (1998). Functional expression and localization of vascular endothelial growth factor and its receptors in the human epididymis. Biol Reprod 58(1), 160168.Google Scholar
Glover, TD & Nicander, L (1971). Some aspects of structure and function in the mammalian epididymis. J Reprod Fertil Suppl 13(Suppl 13), 3950.Google Scholar
Hejmej, A, Kotula-Balak, M, Sadowska, J & Bilińska, B (2007). Expression of connexin 43 protein in testes, epididymides and prostates of stallions. Equine Vet J 39(2), 122127.Google Scholar
Hermo, L, Korah, N, Gregory, M, Liu, LY, Cyr, DG, D'Azzo, A & Smith, CE (2007). Structural alterations of epididymal epithelial cells in cathepsin A-deficient mice affect the blood-epididymal barrier and lead to altered sperm motility. J Androl 28(5), 784797.Google Scholar
Hoffer, AP, Hamilton, DW & Fawcett, DW (1973). The ultrastructure of the principal cells and intraepithelial leucocytes in the initial segment of the rat epididymis. Anat Rec 175(2), 169201.Google Scholar
Ibrahim, ZH & Singh, SK (2014). Histological and morphometric studies on the dromedary camel epididymis in relation to reproductive activity. Anim Reprod Sci 149(3–4), 212217.Google Scholar
Johnson, L, Amann, RP & Pikett, BW (1978). Scanning electron microscopy of the epithelium and spermatozoa in the equine excurrent duct system. Am J Vet Res 39(9), 14281434.Google Scholar
Jones, RC & Murdoch, RN (1996). Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals. Reprod Fertil Dev 8(4), 553568.Google Scholar
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron-microscopy. J Cell Biol 27, 137138A.Google Scholar
Lincoln, G & Short, R (1980). Seasonal breeding: Nature's contraceptive. In Proceedings of the 1979 Laurentian Hormone Conference. Edinburgh, Scotland: Elsevier.Google Scholar
Martinez-Garcia, F, Regadera, J, Cobo, P, Palacios, J, Paniagua, R & Nistal, M (1995). The apical mitochondria-rich cells of the mammalian epididymis. Andrologia 27(4), 195206.Google Scholar
Mollenhauer, HH (1964). Plastic embedding mixtures for use in electron microscopy. Stain Technol 39, 111114.Google Scholar
Musa, BE & Abusineina, ME (1978). Clinical pregnancy diagnosis in the camel and a comparison with bovine pregnancy. Vet Rec 102(1), 710.Google Scholar
Nicander, L & Malmqvist, M (1977). Ultrastructural observations suggesting merocrine secretion in the initial segment of the mammalian epididymis. Cell Tissue Res 184(4), 487490.Google Scholar
Novoa, C (1970). Reproduction in Camelidae. J Reprod Fertil 22(1), 320.Google Scholar
Osman, AM & el-Azab, EA (1974). Gonadal and epididymal sperm reserves in the camel, Camelus dromedarius. J Reprod Fertil 38(2), 425430.Google Scholar
Ramalho-Santos, J, Varum, S, Amaral, S, Mota, PC, Sousa, AP & Amaral, A (2009). Mitochondrial functionality in reproduction: From gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 15(5), 553572.Google Scholar
Ramos, AS Jr. & Dym, M (1977). Fine structure of the monkey epididymis. Am J Anat 149(4), 501531.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, EH (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35, 313323.Google Scholar
Romeis, B (1989). Mikroskopische Technik. München, Wien, Baltimore: Urban und Schwarzenberg.Google Scholar
Schon, J & Blottner, S (2009). Seasonal variations in the epididymis of the roe deer (Capreolus capreolus). Anim Reprod Sci 111(2–4), 344352.Google Scholar
Sone, H, Deo, BK & Kumagai, AK (2000). Enhancement of glucose transport by vascular endothelial growth factor in retinal endothelial cells. Invest Ophthalmol Vis Sci 41(7), 18761884.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(3–4), 237248.Google Scholar
Tabecka-Lonczynska, A, Mytych, J, Solek, P, Kulpa-Greszta, M, Sowa-Kucma, M & Koziorowski, M (2018). Vascular endothelial growth factor (VEGF-A) and fibroblast growth factor (FGF-2) as potential regulators of seasonal reproductive processes in male European bison (Bison bonasus, Linnaeus 1758). Gen Comp Endocrinol 263, 7279.Google Scholar
Tingari, MD (1989). The fine structure of the epithelial lining of the epididymis of the camel (Camelus dromedarius) with special reference to regional differences. J Anat 165, 201214.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(1), 1120.Google Scholar
Wagener, A, Blottner, S, Göritz, F, Streich, WJ & Fickel, J (2010). Circannual changes in the expression of vascular endothelial growth factor in the testis of roe deer (Capreolus capreolus). Anim Reprod Sci 117(3–4), 275278.Google Scholar
Wang, YF & Holstein, AF (1983). Intraepithelial lymphocytes and macrophages in the human epididymis. Cell Tissue Res 233(3), 517521.Google Scholar
Yeung, CH, Nashan, D, Sorg, C, Oberpenning, F, Schulze, H, Nieschlag, E & Cooper, TG (1994). Basal cells of the human epididymis–antigenic and ultrastructural similarities to tissue-fixed macrophages. Biol Reprod 50(4), 917926.Google Scholar