Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T07:57:15.014Z Has data issue: false hasContentIssue false
  • English
  • Français

Histological, histochemical, immunohistochemical and ultrastructural characterization of the testes of the dove

Published online by Cambridge University Press:  03 September 2020

Fatma El-Zahraa A. Mustafa Open the ORCID record for Fatma El-Zahraa A. Mustafa [Opens in a new window]  and
Ruwaida Elhanbaly
Fatma El-Zahraa A. Mustafa*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Egypt
Ruwaida Elhanbaly
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Egypt
*
Author for correspondence: Fatma El-Zahraa A. Mustafa, Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Egypt. E-mail: [email protected]; [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Avian testes have been used in the study of germ cell transfer, importantly for understanding the preservation and control of birds. For this purpose, we use light microscopy, electron microscopy and immunohistochemistry to understand the reproductive efficiency of dove testes. The tunica albuginea was thin and septula testes were not observed. The testicular parenchyma was formed mainly of closely packed convoluted seminiferous tubules with little interstitial area. Three types of spermatogonia were distinguished. The primary spermatocyte appeared as the largest spermatogenic cell and was identified at different stages of meiosis. Different morphological stages of the spermatid were categorized. Various cellular associations were described within the seminiferous epithelium. The cytoplasm of Sertoli cells was pale and ill defined due to its close relationship to the germinal epithelium. The spermatid attached to the luminal border of Sertoli cells and germ cells were closely associated. A single layer of myoid cells surrounded the seminiferous tubule. Testicular telocytes of doves were located in the peritubular region and near the blood vessels. Telopods appeared as long cytoplasmic processes arising from the cell body. Leydig cells were distributed singly or in small groups and cords. The intensity of androgen receptor (AR) immunostaining in the testes of the dove was established for the first time and is described in this paper.

Keywords

AndrogenGerm cellsLeydig cellMyoid cellSertoli cellsTelocyte
Type
Research Article
Information
Zygote , Volume 29 , Issue 1 , February 2021 , pp. 33 - 41
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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

Abate-Shen, C and Shen, MM (2000). Molecular genetics of prostate cancer. Genes Dev 14, 2410–34.CrossRefGoogle ScholarPubMed
Abdul-Rahman, II, Obese, FY and Robinson, JE (2017). Spermatogenesis and cellular associations in the seminiferous epithelium of Guinea cock (Numida meleagris). Canadian J Anim Sci 97, 241–9.Google Scholar
Aire, TA (2007). Spermatogenesis and testicular cycles. In Reproductive Biology and Phylogeny of Birds (ed. Jamieson, Barrie GM), CRC Press, pp. 279–348.Google Scholar
Aire, TA and Ozegbe, PC (2007). The testicular capsule and peritubular tissue of birds: morphometry, histology, ultrastructure and immunohistochemistry. J Anat 210, 731–40.CrossRefGoogle ScholarPubMed
Aire, TA, Olowo-Okorun, MO and Ayeni, JS (1980). The seminiferous epithelium in the guinea fowl (Numida meleagris). Cell Tissue Res 205, 319–25.CrossRefGoogle Scholar
Awad, M and Ghanem, ME (2018). Localization of telocytes in rabbits testis: histological and immunohistochemical approach. Microsc Res Tech 81, 1268–74.CrossRefGoogle ScholarPubMed
Bakst, MR, Akuffo, V, Trefil, P and Brillard, JP (2007). Morphological and histochemical characterization of the seminiferous epithelial and Leydig cells of the turkey. Anim Reprod Sci 97, 303–13.CrossRefGoogle ScholarPubMed
Bancroft, JD, Layton, C and Suvarna, SK (2013). Bancroft’s Theory and Practice of Histological Techniques. Churchill Livingstone, 7th edn.Google Scholar
Clermont, Y and Bustos-Obregon, E (1968). Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted ‘in toto’. Am J Anat 122, 237–47.CrossRefGoogle Scholar
Cooksey, EJ and Rothwell, B (1973). The ultrastructure of the Sertoli cell and its differentiation in the domestic fowl (Gallus domesticus). J Anat 114, 329.Google Scholar
De Reviers, M, Richetin, C and Brillard, JP (1971). Le développement testiculaire chez le coq. ii. – morphologie de l’épithélium séminifère et établissement de la spermatogenèse. Annal Biol Anim Biochim Biophys 11, 531–46.CrossRefGoogle Scholar
Deviche, P, Hurley, LL and Fokidis, HB (2011). Avian testicular structure, function, and regulation. In Hormones and Reproduction of Vertebrates. Academic Press, pp. 27–70.Google Scholar
Dharani, P, Kumary, SU, Venkatesan, S, Joseph, C and Geetha, R (2017). Morphometry and histology of the testicular capsule and peritubular tissue of testis of guinea fowl (Numida meleagris). Indian J Vet Anat 29, 67–9.Google Scholar
Earlé, RA and Dean, WRJ (1981). Features of spermatogenesis in the laughing dove Streptopelia senegalensis . African Zool 16, 109–12.CrossRefGoogle Scholar
Gerzilov, V, Bochukov, A, Penchev, G and Petrov, P (2016). Testicular development in the Muscovy duck (Cairina moschata). Bulg J Vet Med 19, 8–18.CrossRefGoogle Scholar
Harrisson, F and Callebaut, M (1993). Smooth muscle cells in the peritubular tissue of the quail testis. Eur J Morphol 31, 60–4.Google Scholar
Hasirci, E, Turunc, T, Bal, N, Goren, MR, Celik, H, Kervancioglu, E, Dirim, A, Tekindal, MA and Ozkardes, H (2017). Distribution and number of Cajal-like cells in testis tissue with azoospermia. Kaohsiung J Med Sci 33, 181–6.CrossRefGoogle ScholarPubMed
Holdcraft, RW and Braun, RE (2004). Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development 131, 459–67.CrossRefGoogle ScholarPubMed
Hsu, SM, Raine, L and Fanger, HX (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29, 577–80.CrossRefGoogle ScholarPubMed
Kannan, TA, Venkatesan, S and Geetha, R (2008). Histochemical studies on the testis of the Japanese quail. Indian Vet J 85, 1129–30.Google Scholar
Karnovsky, MJ (1965). A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. Cell Biol 27, 137–8A.Google Scholar
Kimura, N, Mizokami, A, Oonuma, T, Sasano, H and Nagura, H (1993). Immunocytochemical localization of androgen receptor with polyclonal antibody in paraffin-embedded human tissues. J Histochem Cytochem 41, 671–8.CrossRefGoogle ScholarPubMed
Kirby, JD and Froman, DP (2000). Reproduction in male birds. In Sturkie’s Avian physiology, 5th edn. (ed. Whittow, CG). Academic Press, New York, pp. 597–615.CrossRefGoogle Scholar
Kormano, M and Hovatta, O (1972). Contractility and histochemistry of the myoid cell layer of the rat seminiferous tubules during postnatal development. Z Anat Entwicklungs 137, 239–48.CrossRefGoogle ScholarPubMed
Lan, WEI, Peng, KM, Liu, H, Song, H, Wang, Y and Tang, L (2011). Histological examination of testicular cell development and apoptosis in the ostrich chick. Turk J Vet Anim Sci 35, 7–14.Google Scholar
Li, X, Wang, Z, Jiang, Z, Guo, J, Zhang, Y, Li, C, Chung, J, Folmer, J, Liu, J, Lian, Q, Ge, R, Barry, RZ and Ge, R (2016). Regulation of seminiferous tubule-associated stem Leydig cells in adult rat testes. Proc Natl Acid Sci USA 113, 2666–71.CrossRefGoogle ScholarPubMed
Lin, M and Jones, RC (1992). Renewal and proliferation of spermatogonia during spermatogenesis in the Japanese quail, Coturnix coturnix japonica . Cell Tissue Res 267, 591–601.CrossRefGoogle ScholarPubMed
Lin, M and Jones, RC (1993). Spermiogenesis and spermiation in the Japanese quail (Coturnix coturnix japonica). J Anat 183, 525.Google Scholar
Madkour, FA and Mohamed, AA (2019). Comparative anatomical studies on the glandular stomach of the rock pigeon (Columba livia targia) and the Egyptian laughing dove (Streptopelia senegalensis aegyptiaca). Anat Histol Embryol 48, 53–63.CrossRefGoogle Scholar
Maekawa, M, Kamimura, K and Nagano, T (1996). Peritubular myoid cells in the testis: their structure and function. Arch Histol Cytol 59, 1–13.CrossRefGoogle ScholarPubMed
Marini, M, Rosa, I, Guasti, D, Gacci, M, Sgambati, E, Ibba-Manneschi, L and Manetti, M (2018). Reappraising the microscopic anatomy of human testis: identification of telocyte networks in the peritubular and intertubular stromal space. Sci Rep 8, 14780.CrossRefGoogle ScholarPubMed
Nicholls, TJ and Graham, GP (1972). Observations on the ultrastructure and differentiation of Leydig cells in the testis of the Japanese quail (Coturnix coturnix japonica). Biol Reprod 6, 179–92.CrossRefGoogle Scholar
Niedenberger, BA, Cook, K, Baena, V, Serra, ND, Velte, EK, Agno, JE, Litwa, KA, Terasaki, M, Hermann, BP, Matzuk, MM and Geyer, CB (2018). Dynamic cytoplasmic projections connect mammalian spermatogonia in vivo . Development 145, 161323.CrossRefGoogle ScholarPubMed
Pawlicki, P, Hejmej, A, Milon, A, Lustofin, K, Płachno, BJ, Tworzydlo, W, Gorowska-Wojtowicz, E, Pawlicka, B, Kotula-Balak, M and Bilinska, B (2019). Telocytes in the mouse testicular interstitium: implications of G-protein-coupled estrogen receptor (GPER) and estrogen-related receptor (ERR) in the regulation of mouse testicular interstitial cells. Protoplasma 256, 393–408.CrossRefGoogle ScholarPubMed
Regadera, J, MartÍnez-GarcÍa, F, González-Peramato, P, Serrano, A, Nistal, M and Suárez-Quian, C (2001). Androgen receptor expression in Sertoli cells as a function of seminiferous tubule maturation in the human cryptorchid testis. J Clin Endocrinol Metab 86, 413–21.Google ScholarPubMed
Reynolds, ES (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208.CrossRefGoogle ScholarPubMed
Rothwell, B (1973). The ultrastructure of Leydig cells in the testis of the domestic fowl. J Anat 116, 245.Google ScholarPubMed
Rothwell, B and Tingari, MD (1973). The ultrastructure of the boundary tissue of the seminiferous tubule in the testis of the domestic fowl (Gallus domesticus). J Anat 114, 321.Google Scholar
Ruizeveld de Winter, J, Trapman, J, Vermey, M, Mulder, E, Zegers, N and van der Kwast, T (1991). Androgen receptor expression in human tissues: an immunohistochemical study. J Histochem Cytochem 39, 927–36.CrossRefGoogle ScholarPubMed
Scheltinga, DM and Jamieson, BG (2003). Spermatogenesis and the mature spermatozoon: form, function and phylogenetic implications. In Reproductive Biology and Phylogeny of Anura (ed. Jamieson, BGM). Science Publishers, Inc., pp. 119–251.Google Scholar
Sharpe, RM, McKinnell, C, Kivlin, C and Fisher, JS (2003). Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125, 769–84.CrossRefGoogle ScholarPubMed
Shi, L, Xun, W, Zhou, H, Hou, G, Yue, W, Zhang, C, Ren, Y and Yang, R (2013). Ultrastructure of germ cells, Sertoli cells and mitochondria during spermatogenesis in mature testis of the Chinese Taihang black goats (Capra hircus). Micron 50, 14–9.CrossRefGoogle Scholar
Sutinen, P, Malinen, M and Palvimo, JJ (2017). Androgen receptor. In Endocrinology of the Testis and Male Reproduction (eds Simoni, M and Huhtaniemi, I). Springer, pp. 395–416.CrossRefGoogle Scholar
Trefil, P, Micáková, A, Mucksová, J, Hejnar, J, Poplstein, M, Bakst, MR, Kalina, J and Brillard, JP (2006). Restoration of spermatogenesis and male fertility by transplantation of dispersed testicular cells in the chicken. Biol Reprod 75, 575–81.CrossRefGoogle ScholarPubMed
Ventela, S, Toppari, J and Parvinen, M (2003). Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: mechanisms of haploid gene product sharing. Mol Biol Cell 14, 2768–80.CrossRefGoogle ScholarPubMed
Villagra, LI, Ramos, I, Cisint, S, Crespo, CA and Fernández, SN (2018). Electron microscopy observations on testis and spermatozoa of Leptodactylus chaquensis (Anura, Leptodactylidae). Micron 105, 35–46.CrossRefGoogle Scholar
Vornberger, W, Prins, G, Musto, N and Suarez-Quian, C (1994). Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology 134, 2307–16.CrossRefGoogle ScholarPubMed
Yang, P, Ahmad, N, Hunag, Y, Ullah, S, Zhang, Q, Waqas, Y, Liu, Y, Li, Q, Hu, L and Chen, Q (2015). Telocytes: novel interstitial cells present in the testis parenchyma of the Chinese soft-shelled turtle Pelodiscus sinensis . J Cell Mol Med 19, 2888–99.CrossRefGoogle ScholarPubMed
Wang, RS, Yeh, S, Tzeng, CR and Chang, C (2009). Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocrine Rev 30, 119–32.CrossRefGoogle ScholarPubMed
Welsh, M, Moffat, L, Belling, K, De Franca, L R, Segatelli, TM, Saunders, PTK, Sharpe, RM and Smith, LB (2012). Androgen receptor signalling in peritubular myoid cells is essential for normal differentiation and function of adult Leydig cells. Int J Androl 35, 25–40.CrossRefGoogle ScholarPubMed
Wright, WW and Frankel, AI (1980). An androgen receptor in the nuclei of late spermatids in testes of male rats. Endocrinology 107, 314–8.CrossRefGoogle ScholarPubMed
Zhou, X, Kudo, A, Kawakami, H and Hirano, H (1996). Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development. Anat Rec 245, 509–18.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Zhu, LJ, Hardy, MP, Inigo, IV, Huhtaniemi, I, Bardin, CW and Moo-Young, AJ (2000). Effects of androgen on androgen receptor expression in rat testicular and epididymal cells: a quantitative immunohistochemical study. Biol Reprod 63, 368–76.CrossRefGoogle ScholarPubMed