Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T07:39:44.297Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative Cellular Localization of Sugar Residues in Bull (Bos taurus) and Donkey (Equus asinus) Testes Using Lectin Histochemistry

Published online by Cambridge University Press:  12 October 2021

Mahmoud S. Gewaily Open the ORCID record for Mahmoud S. Gewaily [Opens in a new window] ,
Mohamed Kassab ,
Asmaa Aboelnour ,
Essam A. Almadaly  and
Ahmed E. Noreldin Open the ORCID record for Ahmed E. Noreldin [Opens in a new window]
Mahmoud S. Gewaily*
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516Kafrelsheikh, Egypt
Mohamed Kassab
Affiliation:
Department of Cytology and Histology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516Kafrelsheikh, Egypt
Asmaa Aboelnour
Affiliation:
Department of Histology and Cytology, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
Essam A. Almadaly
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Kafrelsheikh University, El-Geish Street, 33516, Kafrelsheikh, Egypt
Ahmed E. Noreldin
Affiliation:
Department of Histology and Cytology, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
*
*Corresponding author: Mahmoud Saad Gewaily, E-mail: [email protected], [email protected]
Get access

Abstract

Lectins are glycoproteins of a non-immune origin often used as histochemical reagents to study the distribution of glycoconjugates in different types of tissues. In this study, we performed a comparative cellular localization of sugar residues in bull and donkey testes using immunofluorescent lectin histochemistry. We inspected the cellular localization of the glycoconjugates within the testes using 11 biotin-labeled lectins (LCA, ConA, PNA, WGA, DBA, SBA, ECA, BPL, PTL-II, UEA-1, and PHA-E4) classified under six groups. Although the basic testicular structure in both species was similar, the cellular components showed different lectin localization patterns. The statistical analysis revealed no significant association between the intensity of labeling and different variables, including group and type of lectin and type of cell examined, at p < 0.05. However, a stronger response tended to occur in the donkey than in the bull testes (odds ratio: 1.3). These findings may be associated with the different cellular compositions of the glycoproteins and modification changes during spermatogenesis. Moreover, glycoconjugate profiling through lectin histochemistry can characterize some cell-type selective markers that will be helpful in studying bull and donkey spermatogenesis.

Keywords

bulldonkeyglycoconjugateslectin histochemistrytestis
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 6 , December 2021 , pp. 1529 - 1538
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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-Hafeez, HH (2005). Histomorphological Studies on the Testis of Donkey During Postnatal Period. Assiut, Egypt: Assiut University.Google Scholar
Abd-Elmaksoud, A (2005). Morphological, glycohistochemical, and immunohistochemical studies on the embryonic and adult bovine testis. PhD Thesis, Institute of Veterinary Anatomy II, Faculty of Veterinary Medicine, LMU, Munich, Germany.Google Scholar
Ahluwalia, B, Farshori, P, Jamuar, M, Baccetti, B & Anderson, W (1990). Specific localization of lectins in boar and bull spermatozoa. J Submicrosc Cytol Pathol 22(1), 53–62.Google ScholarPubMed
Ahmed, A-E & Sinowatz, F (2005). Morphological, glycohistochemical, and immunohistochemical studies on the embryonic and adult bovine testis. PhD Thesis, Vet. Med. Ludwig-Maximilians-Univ.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(5552), 124–127.CrossRefGoogle ScholarPubMed
Arenas, M, Madrid, J, Bethencourt, F, Fraile, B & Paniagua, R (1998). Lectin histochemistry of the human testis. Int J Androl 21(6), 332–342.CrossRefGoogle ScholarPubMed
Arya, M & Vanha-Perttula, T (1985). Lectin-binding pattern of bull testis and epididymis. J Androl 6(4), 230–242.CrossRefGoogle ScholarPubMed
Arya, M & Vanha-Perttula, T (1986). Comparison of lectin-staining pattern in testis and epididymis of gerbil, Guinea pig, mouse, and nutria. Am J Anat 175(4), 449–469.CrossRefGoogle ScholarPubMed
Bains, H, Bawa, S, Pabst, M & Sehgal, S (1993). Plasma membrane alterations of maturing goat (Capra indicus) spermatozoa: Lectin-binding and freeze-fracture study. Cell Tissue Res 271(1), 159–168.CrossRefGoogle ScholarPubMed
Bains, H, Werner, G, Bansal, M & Bawa, S (1994). Qualitative and quantitative analysis of lectin binding on the epididymal spermatozoa of cat (Felis catus). Acta Microsc 3(2), 51–65.Google Scholar
Bao, SN (1997). Cytochemical localization of carbohydrate in the spermatid of Rhodnius prolixus (Hemiptera, Reduviidae). Acta Microsc 6(1), 14–20.Google Scholar
De Rooij, DG & Russell, LD (2000). All you wanted to know about spermatogonia but were afraid to ask. J Androl 21(6), 776–798.Google Scholar
Dym, M & Fawcett, DW (1970). The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3(3), 308–326.CrossRefGoogle ScholarPubMed
Ertl, C & Wrobel, K-H (1992). Distribution of sugar residues in the bovine testis during postnatal ontogenesis demonstrated with lectin-horseradish peroxidase conjugates. Histochemistry 97(2), 161–171.CrossRefGoogle ScholarPubMed
Faraggiana, T, Malchiodi, F, Prado, A & Churg, J (1982). Lectin-peroxidase conjugate reactivity in normal human kidney. J Histochem Cytochem 30(5), 451–458.CrossRefGoogle ScholarPubMed
Fielding, D (1988). Reproductive characteristics of the jenny donkey—Equus asinus: A review. Trop Anim Health Prod 20(3), 161–166.CrossRefGoogle ScholarPubMed
Gabius, H (1987). Vertebrate lectins and their possible role in fertilization, development and tumor biology. In Vivo (Athens, Greece) 1(2), 75–83.Google ScholarPubMed
Gabius, H-J (2000). Biological information transfer beyond the genetic code: The sugar code. Naturwissenschaften 87(3), 108–121.CrossRefGoogle ScholarPubMed
Gabius, H-J, André, S, Kaltner, H & Siebert, H-C (2002). The sugar code: Functional lectinomics. Biochimica et Biophysica Acta (BBA) – General Subjects 1572(2–3), 165–177.CrossRefGoogle ScholarPubMed
Gabius, HJ, Siebert, HC, André, S, Jiménez-Barbero, J & Rüdiger, H (2004). Chemical biology of the sugar code. ChemBioChem 5(6), 740–764.CrossRefGoogle ScholarPubMed
Gewaily, MS, Kassab, M, Farrag, FA, Almadaly, EA, Atta, MS, Abd-Elmaksoud, A & Wakayama, T (2020). Comparative expression of cell adhesion molecule1 (CADM1) in the testes of experimental mice and some farm animals. Acta Histochem 122(1), 151456.CrossRefGoogle ScholarPubMed
Gewaily, MS, Noreldin, AE, Dawood, MA, Hegazy, YM & Kassab, M (2021). The distribution profile of glycoconjugates in the testis of brown-banded bamboo shark (Chiloscyllium punctatum) by using lectin histochemistry. Microsc Microanal 27(5), 1161–1173.CrossRefGoogle Scholar
Gilmont, RR, Senger, PL, Sylvester, SR & Griswold, MD (1990). Seminal transferrin and spermatogenic capability in the bull. Biol Reprod 43(1), 151–157.CrossRefGoogle ScholarPubMed
Goldstein, I & Poretz, RD (2012). 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. 233–247. Cambridge, MA: Academic Press.Google Scholar
Goldstein, IJ (1980). What should be called a lectin? Nature 285, 66.CrossRefGoogle Scholar
Goldstein, IJ & Hayes, CE (1978). The lectins: Carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem 35, 127–340.CrossRefGoogle ScholarPubMed
Hakomori, S-i (1981). Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu Rev Biochem 50(1), 733–764.CrossRefGoogle ScholarPubMed
Harrell, FE (2015). Ordinal logistic regression. In Regression Modeling Strategies: With Applications to Linear Models, Logistic and Ordinal Regression, and Survival Analysis, Harrell, FE (Ed.), pp. 311–325. Cham: Springer International Publishing.CrossRefGoogle Scholar
Jones, CJ, Morrison, CA & Stoddart, RW (1992 a). Histochemical analysis of rat testicular glycoconjugates. 1. Subsets of N-linked saccharides in seminiferous tubules. Histochem J 24(6), 319–326.CrossRefGoogle ScholarPubMed
Jones, CJ, Morrison, CA & Stoddart, RW (1992 b). Histochemical analysis of rat testicular glycoconjugates. 2. β-galactosyl residues in O-and N-linked glycans in seminiferous tubules. Histochem J 24(6), 327–336.CrossRefGoogle ScholarPubMed
Jones, CJ, Morrison, CA & Stoddart, RW (1993). Histochemical analysis of rat testicular glycoconjugates. 3. Non-reducing terminal residues in seminiferous tubules. Histochem J 25(10), 711–718.Google ScholarPubMed
Jutte, NH, Jansen, R, Grootegoed, J, Rommerts, F, Clausen, O & Van der Molen, H (1982). Regulation of survival of rat pachytene spermatocytes by lactate supply from sertoli cells. Reproduction 65(2), 431–438.CrossRefGoogle ScholarPubMed
Jutte, NH, Jansen, R, Grootegoed, J, Rommerts, F & Van der Molen, H (1983). FSH stimulation of the production of pyruvate and lactate by rat Sertoli cells may be involved in hormonal regulation of spermatogenesis. Reproduction 68(1), 219–226.CrossRefGoogle ScholarPubMed
Kocourek, J & Horejsi, V (1983). A note on the recent discussion on definition of the term ‘lectin’. In Lectins: Biology, Biochemistry, Clinical Biochemistry, Van Driessche, E, Fisher, J, Beeckmans, S & Bøg-Hansen, TC (Eds.), vol. 3. pp. 3–6. Hellerup, DK: Textop.Google Scholar
Kurohmaru, M, Kanai, Y & Hayashi, Y (1991). Lectin-binding patterns in the spermatogenic cells of the shiba goat testis. J Vet Med Sci 53(5), 893–897.CrossRefGoogle ScholarPubMed
Lee, MC & Damjanov, I (1985). Lectin binding sites on human sperm and spermatogenic cells. Anat Rec 212(3), 282–287.CrossRefGoogle ScholarPubMed
Malmi, R, Fröjdman, K & Söderström, K-O (1990). Differentiation-related changes in the distribution of glycoconjugates in rat testis. Histochemistry 94(4), 387–395.CrossRefGoogle ScholarPubMed
Malmi, R, Kallajoki, M & Suominen, J (1987). Distribution of glycoconjugates in human testis. A histochemical study using fluorescein- and rhodamine-conjugated lectins. Andrologia 19(3), 322–332.CrossRefGoogle ScholarPubMed
Manning, J, Seyrek, K, Kaltner, H, André, S, Sinowatz, F & Gabius, H (2004). Glycomic profiling of developmental changes in bovine testis by lectin histochemistry and further analysis of the most prominent alteration on the level of the glycoproteome by lectin blotting and lectin affinity chromatography. Histol Histopathol 19, 1043–1060.Google ScholarPubMed
Martínez-Menárguez, JA, Avilés, M, Madrid, JF, Castells, M & Ballesta, J (1993). Glycosylation in Golgi apparatus of early spermatids of rat. A high resolution lectin cytochemical study. Eur J Cell Biol 61, 21–21.Google Scholar
Neves, ES, Chiarini-Garcia, H & França, LR (2002). Comparative testis morphometry and seminiferous epithelium cycle length in donkeys and mules. Biol Reprod 67(1), 247–255.CrossRefGoogle ScholarPubMed
Nicolson, GL (1974). The interactions of lectins with animal cell surfaces. Int Rev Cytol 39, 89–190.CrossRefGoogle ScholarPubMed
Nipken, C & Wrobel, K (1997). A quantitative morphological study of age-related changes in the donkey testis in the period between puberty and senium. Andrologia 29(3), 149–161.CrossRefGoogle ScholarPubMed
Parillo, F, Verini Supplizi, A, Mancuso, R & Catone, G (2012). Glycomolecule modifications in the seminiferous epithelial cells and in the acrosome of post-testicular spermatozoa in the alpaca. Reprod Domest Anim 47(4), 675–686.CrossRefGoogle ScholarPubMed
Pinart, E, Bonet, S, Briz, M, Pastor, L, Sancho, S, Garcıa, N, Badia, E & Bassols, J (2002). Histochemical study of the interstitial tissue in scrotal and abdominal boar testes. Vet J 163(1), 68–76.CrossRefGoogle ScholarPubMed
Pugh, D (2002). Donkey reproduction. In Proc. Am. Assoc. Equine Pract. pp. 113–114.Google Scholar
Raychoudhury, SS & Millette, CF (1997). Multiple fucosyltransferases and their carbohydrate ligands are involved in spermatogenic cell-Sertoli cell adhesion in vitro in rats. Biol Reprod 56(5), 1268–1273.CrossRefGoogle ScholarPubMed
Renner-Martin, T, Forstenpointner, G, Weissengruber, G & Eberhardt, L (2009). Gross anatomy of the female genital organs of the domestic donkey (Equus asinus Linné, 1758). Anat Histol Embryol 38(2), 133–138.CrossRefGoogle Scholar
Roth, J (1983). Application of lectin–gold complexes for electron microscopic localization of glycoconjugates on thin sections. J Histochem Cytochem 31(8), 987–999.CrossRefGoogle ScholarPubMed
Russell, L & Griswold, M (1993). The Sertoli Cell. Clearwater, FL: Cache River Press.Google Scholar
Russell, LD, Ettlin, RA, Hikim, APS & Clegg, ED (1993). Histological and Histopathological Evaluation of the Testis. The Cache River: Wiley Online Library.CrossRefGoogle Scholar
Setchell, B (1970). Testicular blood supply, lymphatic drainage, and secretion of fluid. The Testis 1, 101–239.Google Scholar
Sharpe, R (1994). Regulation of spermatogenesis. The Physiology of Reproduction 1, 1363–1434.Google Scholar
Solís, D, Jiménez-Barbero, J, Kaltner, H, Romero, A, Siebert, H-C, Von der Lieth, C-W & Gabius, H-J (2001). Towards defining the role of glycans as hardware in information storage and transfer: Basic principles, experimental approaches and recent progress. Cells Tissues Organs 168(1-2), 5–23.CrossRefGoogle ScholarPubMed
Spicer, S, Schulte, B, Thomopoulos, G, Parmley, R & Takagi, M (1983). Cytochemistry of complex carbohydrates by light and electron microscopy: Available methods and their application. Monogr Pathol 24, 163–211.Google ScholarPubMed
Srivastav, A, Singh, B, Chandra, A, Jamal, F, Khan, MY & Chowdhury, SR (2004). Partial characterization, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta). Reproduction 127(3), 343–357.CrossRefGoogle Scholar
Staub, C & Johnson, L (2018). Spermatogenesis in the bull. Animal 12(s1), s27–s35.CrossRefGoogle ScholarPubMed
Tulsiani, DR (2006). Glycan-modifying enzymes in luminal fluid of the mammalian epididymis: An overview of their potential role in sperm maturation. Mol Cell Endocrinol 250(1-2), 58–65.CrossRefGoogle ScholarPubMed
Verini-Supplizi, A, Stradaioli, G, Fagioli, O & Parillo, F (2000). Localisation of the lectin reactive sites in adult and prepubertal horse testes. Res Vet Sci 69(2), 113–118.CrossRefGoogle Scholar
Wollina, U, Schreiber, G, Zollmann, C, Hipler, C & Günther, E (1989). Lectin-binding sites in normal human testis/lektinbindungsstellen normaler humaner hoden. Andrologia 21(2), 127–130.CrossRefGoogle Scholar
Supplementary material: File

Gewaily et al. supplementary material

Gewaily et al. supplementary material

Download Gewaily et al. supplementary material(File)
File 523.8 KB