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The Distribution Profile of Glycoconjugates in the Testis of Brown-Banded Bamboo Shark (Chiloscyllium punctatum) by Using Lectin Histochemistry

Published online by Cambridge University Press:  06 July 2021

Mahmoud S. Gewaily Open the ORCID record for Mahmoud S. Gewaily [Opens in a new window] ,
Ahmed E. Noreldin Open the ORCID record for Ahmed E. Noreldin [Opens in a new window] ,
Mahmoud A.O. Dawood ,
Yamen M. Hegazy  and
Mohamed Kassab
Mahmoud S. Gewaily*
Affiliation:
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516Kafrelsheikh, Egypt
Ahmed E. Noreldin
Affiliation:
Department of Histology and Cytology, Faculty of Veterinary Medicine, the Scientific Campus, Damanhour University, Damanhour, Egypt
Mahmoud A.O. Dawood
Affiliation:
Department of Animal Production, Faculty of Agriculture, Kafrelsheikh University, Kafrelsheikh, Egypt
Yamen M. Hegazy
Affiliation:
Department of Animal Medicine, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516Kafrelsheikh, Egypt
Mohamed Kassab
Affiliation:
Department of Cytology and Histology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33516Kafrelsheikh, Egypt
*
*Author for correspondence: Mahmoud Saad Gewaily, E-mail: [email protected]; [email protected]
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Abstract

The testis of bamboo shark is characterized by diametric development leading to zonation architecture. Here, we investigated the staining pattern of 12 lectins in 6 groups of differential binding specificities within the germ, somatic, and interstitial cells of each zone. The neutral mucopolysaccharides appeared in the interstitial tissue in all the zones and became more significant in the spermatozoal–Sertoli cell junction. The cellular localization of the lectins varies in testicular zones and cell types. There was a gradual increase in glycosylation toward the degenerative zone. The increased intensity of most lectins in the interstitial cells indicates the association of glycoconjugates in their androgen-secreting activity. Statistical analyses showed a significant correlation between the groups of lectins and each lectin used, stronger response to lectins in the interstitial cells (ICs) than other cell types. Moreover, the response to glucosamine (GlcNAc), galactosamine (GalNAc), and fucose tended to be higher than glucose and galactose. Furthermore, the intensity of response was increased toward the degenerative zone. In addition, we can use peanut agglutinin (PNA) as an acrosomal marker in combination with other marker proteins for studying shark spermatogenesis. These findings refer to the crucial role of glycoconjugates in spermatogenesis in the bamboo shark testis.

Keywords

bamboo sharkglycoconjugatesimmunofluorescencelectinstestis
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 5 , October 2021 , pp. 1161 - 1173
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Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Abd-Elmaksoud, A, Sayed-Ahmed, A, Kassab, M & Aly, K (2008). Histochemical mapping of glycoconjugates in the testis of the one humped camel (Camelus dromedarius) during rutting and non-rutting seasons. Acta Histochem 110(2), 124–133.CrossRefGoogle ScholarPubMed
Aire, T, Olowo-Okorun, M & Ayeni, J (1980). The seminiferous epithelium in the guinea fowl (Numida meleagris). Cell Tissue Res 205(2), 319–325.CrossRefGoogle 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 (1984). Distribution of lectin binding in rat testis and epididymis. Andrologia 16(6), 495–508.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
Aviles, M, Castells, M, Martinez-Menarguez, J, Abascal, I & Ballesta, J (1997). Localization of penultimate carbohydrate residues in zona pellucida and acrosomes by means of lectin cytochemistry and enzymatic treatments. Histochem J 29(8), 583–592.CrossRefGoogle ScholarPubMed
Ballesta, J, Martinez-Menarguez, J, Pastor, L, Avilés, M, Madrid, J & Castells, M (1991). Lectin binding pattern in the testes of several tetrapode vertebrates. Eur J Basic Appl Histochem 35(2), 107–117.Google ScholarPubMed
Benton, L, Shan, L-X & Hardy, MP (1995). Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 53(1–6), 61–68.CrossRefGoogle ScholarPubMed
Bernfield, M, Götte, M, Park, PW, Reizes, O, Fitzgerald, ML, Lincecum, J & Zako, M (1999). Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68(1), 729–777.CrossRefGoogle ScholarPubMed
Carreau, S (1996). Paracrine control of human Leydig cell and Sertoli cell functions. Folia Histochem Cytobiol 34(3–4), 111–119.Google ScholarPubMed
Chatchavalvanich, K, Thongpan, A & Nakai, M (2005). Structure of the testis and genital duct of freshwater stingray, Himantura signifer (Elasmobranchii: Myliobatiformes: Dasyatidae). Ichthyol Res 52(2), 123–131.CrossRefGoogle Scholar
Danguy, A, Decaestecker, C, Genten, F, Salmon, I & Kiss, R (1998). Applications of lectins and neoglycoconjugates in histology and pathology. Cells Tissues Organs 161(1–4), 206–218.CrossRefGoogle ScholarPubMed
Desantis, S, Zizza, S, García-López, Á, Sciscioli, V, Mananos, E, De Metrio, V & Sarasquete, C (2010). Lectin-binding pattern of Senegalese sole Solea senegalensis (Kaup) testis. Histol Histopathol 25, 205–216.Google ScholarPubMed
Dingerkus, G & DeFino, TC (1983). A revision of the orectolobiform shark family Hemiscyllidae (Chondrichthyes, Selachii).Bull AMNH 176, 30–35.Google Scholar
Dini, L, Autuori, F, Lentini, A, Oliverio, S & Piacentini, M (1992). The clearance of apoptotic cells in the liver is mediated by the asialoglycoprotein receptor. FEBS Lett 296(2), 174–178.CrossRefGoogle ScholarPubMed
Dobson, S & Dodd, J (1977). Endocrine control of the testis in the dogfish Scyliorhinus canicula L. II. Histological and ultrastructural changes in the testis after partial hypophysectomy (ventral lobectomy). Gen Comp Endocrinol 32(1), 53–71.CrossRefGoogle Scholar
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
Farrag, FA, Lashein, SA, Almadaly, EA, Gewaily, MS, Atta, MS, Abo-Zaid, TK & Kassab, MA (2018). Morphological and immunohistochemical study on the testis of brown-banded bamboo shark (Chiloscyllium punctatum). Alex J Vet Sci 57(1), 126–134.Google Scholar
Fraile, B, Paniagua, R, Rodríguez, MC, Sáez, FJ & Jimenez, A (1989). Annual changes in the number, testosterone content and ultrastructure of glandular tissue cells of the testis in the marbled newt Triturus marmoratus. J Anat 167, 85.Google ScholarPubMed
Gallagher, JT, Morris, A & Dexter, TM (1985). Identification of two binding sites for wheat-germ agglutinin on polylactosamine-type oligosaccharides. Biochem J 231(1), 115–122.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
Girard, M, Rivalan, P & Sinquin, G (2000). Testis and sperm morphology in two deep-water squaloid sharks, Centroscymnus coelolepis and Centrophorus squamosus. J Fish Biol 57(6), 1575–1589.CrossRefGoogle Scholar
Goldstein, I & Poretz, R (1986). Isolation, physicochemical characterization and carbohydrate-binding specificity of lectins. In The Lectins, Liener, IE, Sharon, N & Goldstein, IJ (Eds.), London: Academic Press Inc., Harcourt Bruce Jovanovich, Publishers.Google Scholar
Hamlett, WC, Jezior, M & Spieler, R (1999). Ultrastructural analysis of folliculogenesis in the ovary of the yellow spotted stingray, Urolophus jamaicensis. Ann Anat 181(2), 159–172.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
Hedger, MP & de Kretser, DM (2000). Leydig cell function and its regulation. In The Genetic Basis of Male Infertility, McElreavey, K (Ed.), pp. 69–110. Berlin, Heidelberg, New York: Springer.CrossRefGoogle Scholar
Henningsen, AD, Smale, M, Garner, R & Kinnunen, N (2004). Reproduction, embryonic development, and reproductive physiology of elasmobranchs. In The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and Their Relatives, Smith M, Warmolts D, Thoney D & Hueter R (Eds.), pp. 227–236. Ohio: Biological Survey.Google Scholar
Hess, RA & De Franca, LR (2009). Spermatogenesis and cycle of the seminiferous epithelium. In Molecular Mechanisms in Spermatogenesis, Yan Cheng, C (Ed.), pp. 1–15. Springer.Google Scholar
Huhtaniemi, I & Toppari, J (1995). Endocrine, paracrine and autocrine regulation of testicular steroidogenesis. In Tissue Renin-Angiotensin Systems, Mukhopadhyay, AK & Raizada, MK (Eds.), pp. 33–54. Berlin, Heidelberg, New York: Springer.CrossRefGoogle Scholar
Iozzo, RV (1998). Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67(1), 609–652.CrossRefGoogle ScholarPubMed
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
Kassab, M & Yanai, T (2010). Localization of transforming growth factor ß1 (TGF ß1) on the testis of brown banded-bamboo shark (Chiloscyllium punctatum). J Vet Anat 3(1), 71–80.CrossRefGoogle Scholar
Kassab, M, Yanai, T, Ito, K, Sakai, H, Mesegi, T & Yanagisawa, M (2009). Morphology and lectin histochemistry of the testes of brown-banded bamboo shark (Chiloscyllium punctatum). J Vet Anat 2(1), 49–66.CrossRefGoogle Scholar
Kimura, A, Wigzell, H, Holmquist, G, Ersson, B & Carlsson, P (1979). Selective affinity fractionation of murine cytotoxic T lymphocytes (CTL). Unique lectin specific binding of the CTL associated surface glycoprotein, T 145. J Exp Med 149(2), 473–484.CrossRefGoogle ScholarPubMed
Kristiansen, T (1974). [31] group-specific separation of glycoproteins. In Methods in Enzymology, Kaplan, NP, Colowick, NP, Jakoby, WB & Wilchek, M (Eds.), pp. 331–341. Cambridge, MA: Elsevier.CrossRefGoogle Scholar
Labate, M & Desantis, S (1995). Histochemical analysis of lizard testicular glycoconjugates during the annual spermatogenetic cycle. Eur J Histochem 39(3), 201–212.Google ScholarPubMed
Lander, AD & Selleck, SB (2000). The elusive functions of proteoglycans: In vivo veritas. J Cell Biol 148(2), 227–232.CrossRefGoogle ScholarPubMed
Le Roy, C, Lejeune, H, Chuzel, F, Saez, JM & Langlois, D (1999). Autocrine regulation of Leydig cell differentiated functions by insulin-like growth factor I and transforming growth factor beta. J Steroid Biochem Mol Biol 69(1–6), 379–384.CrossRefGoogle ScholarPubMed
Liguoro, A, Prisco, M, Mennella, C, Ricchiari, L, Angelini, F & Andreuccetti, P (2004). Distribution of terminal sugar residues in the testis of the spotted ray Torpedo marmorata. Mol Reprod Dev 68(4), 524–530.CrossRefGoogle ScholarPubMed
Lis, H & Sharon, N (1986). Biological properties of lectins. In The Lectins: Properties, Functions and Applications in Biology and Medicine, Liener I (Ed.), pp. 265–291. Cambridge, MA: Academic Press.CrossRefGoogle Scholar
Loir, M, Sourdaine, P, Mendis-Handagama, SM & Jégou, B (1995). Cell-cell interactions in the testis of teleosts and elasmobranchs. Microsc Res Tech 32(6), 533–552.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
Marina, P, Annamaria, L, Do, B, Loredana, R, Piero, A & Francesco, A (2002). Fine structure of Leydig and Sertoli cells in the testis of immature and mature spotted ray Torpedo marmorata. Mol Reprod Dev 63(2), 192–201.CrossRefGoogle 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.Google Scholar
Matthews, LH (1950). Reproduction in the basking shark, Cetorhinus maximus (Gunner). Philos Trans R Soc Lond B, Biol Sci 234(612), 247–316.Google Scholar
McClusky, LM (2006). Stage-dependency of apoptosis and the blood-testis barrier in the dogfish shark (Squalus acanthias): Cadmium-induced changes as assessed by vital fluorescence techniques. Cell Tissue Res 325(3), 541–553.CrossRefGoogle ScholarPubMed
Mendis-Handagama, SM (1997). Luteinizing hormone on Leydig cell structure and function. Histol Histopathol 12(3), 869–882.Google ScholarPubMed
Merkle, RK & Cummings, RD (1987). [18] Lectin affinity chromatography of glycopeptides. In Methods in Enzymology, Ginsburg, V (Ed.), pp. 232–259. Cambridge, MA: Elsevier.Google Scholar
Parsons, GR & Grier, HJ (1992). Seasonal changes in shark testicular structure and spermatogenesis. J Exp Zool 261(2), 173–184.CrossRefGoogle Scholar
Pereira, M & Kabat, EA (1976). Immunochemical studies on blood groups LXII. Fractionation of hog and human A, H, and AH blood group active substance on insoluble immunoadsorbents of Dolichos and Lotus lectins. J Exp Med 143(2), 422–436.CrossRefGoogle Scholar
Pinart, E, Bonet, S, Briz, M, Pastor, L, Sancho, S, Garcia, N, Badia, E & Bassols, J (2001). Lectin affinity of the seminiferous epithelium in healthy and cryptorchid post-pubertal boars. Int J Androl 24(3), 153–164.CrossRefGoogle ScholarPubMed
Pratt, HL Jr. (1988). Elasmobranch gonad structure: A description and survey. Copeia 3, 719–729.CrossRefGoogle Scholar
Pratt, HL Jr. & Tanaka, S (1994). Sperm storage in male elasmobranchs: A description and survey. J Morphol 219(3), 297–308.CrossRefGoogle ScholarPubMed
Prisco, M, Liguoro, A, Comitato, R, Cardone, A, D'Onghia, B, Ricchiari, L, Angelini, F & Andreuccetti, P (2003). Apoptosis during spermatogenesis in the spotted ray Torpedo marmorata. Mol Reprod Dev 64(3), 341–348.CrossRefGoogle ScholarPubMed
Pudney, J (1995). Spermatogenesis in nonmammalian vertebrates. Microsc Res Tech 32(6), 459–497.CrossRefGoogle ScholarPubMed
Pudney, J & Callard, GV (1984 a). Development of agranular reticulum in Sertoli cells of the testis of the dogfish Squalus acanthias during spermatogenesis. Anat Rec 209(3), 311–321.CrossRefGoogle ScholarPubMed
Pudney, J & Callard, GV (1984 b). Identification of Leydig-like cells in the testis of the dogfish Squalus acanthias. Anat Rec 209(3), 323–330.CrossRefGoogle ScholarPubMed
Roth, J (1996). Protein glycosylation in the endoplasmic reticulum and the Golgi apparatus and cell type-specificity of cell surface glycoconjugate expression: Analysis by the protein A-gold and lectin-gold techniques. Histochem Cell Biol 106(1), 79–92.CrossRefGoogle ScholarPubMed
Saez, FJ, Madrid, JF, Alonso, E & Hernandez, F (2001 a). Glycan composition of follicle (Sertoli) cells of the amphibian Pleurodeles waltl. A lectin histochemical study. J Anat 198(6), 673–681.Google ScholarPubMed
Saez, FJ, Madrid, JF, Aparicio, R, Hernandez, F & Alonso, E (2001 b). Carbohydrate moieties of the interstitial and glandular tissues of the amphibian Pleurodeles waltl testis shown by lectin histochemistry. J Anat 198(1), 47–56.CrossRefGoogle ScholarPubMed
Sharon, N (1983). Lectin receptors as lymphocyte surface markers. In Advances in Immunology, Dixon, FJ & Kunkel, HG (Eds.), pp. 213–298. Cambridge, MA: Elsevier.Google Scholar
Söderström, K, Malmi, R & Karjalainen, K (1984). Binding of fluorescein isothiocyanate conjugated lectins to rat spermatogenic cells in tissue sections. Histochemistry 80(6), 575–579.CrossRefGoogle ScholarPubMed
Spicer, S & Schulte, B (1992). Diversity of cell glycoconjugates shown histochemically: A perspective. J Histochem Cytochem 40(1), 1–38.CrossRefGoogle ScholarPubMed
Stanley, HP (1966). The structure and development of the seminiferous follicle in Scyliorhinus caniculus and Torpedo marmorata (Elasmobranchii). Z Zellforsch Mikrosk Anat 75(2), 453–468.CrossRefGoogle Scholar
Szasz, F, Sirivaidyapong, S, Cheng, F, Voorhout, W, Marks, A, Colenbrander, B, Solti And, L & Gadella, B (2000). Detection of calcium ionophore induced membrane changes in dog sperm as a simple method to predict the cryopreservability of dog semen. Mol Reprod Dev 55(3), 289–298.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Topic Popovic, N, Strunjak-Perovic, I, Coz-Rakovac, R, Barisic, J, Jadan, M, Persin Berakovic, A & Sauerborn Klobucar, R (2012). Tricaine methane-sulfonate (MS-222) application in fish anaesthesia. J Appl Ichthyol 28(4), 553–564.CrossRefGoogle Scholar
Valbuena, G, Alonso, E, de Ubago, MM, Madrid, JF, Díaz-Flores, L & Sáez, FJ (2012). Histochemical identification of sialylated glycans in Xenopus laevis testis. J Anat 221(4), 318–330.CrossRefGoogle ScholarPubMed
Varki, A & Lowe, JB (2009). Biological roles of glycans. In Essentials of Glycobiology, Varki, A, Cummings, RD & Cummings, JD (Eds.), 2nd edn., pp. 3–49. New York: Cold Spring Harbor Laboratory Press.Google 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
Wakayama, T, Nakata, H, Kumchantuek, T, Gewaily, MS & Iseki, S (2015). Identification of 5-bromo-2’-deoxyuridine-labeled cells during mouse spermatogenesis by heat-induced antigen retrieval in lectin staining and immunohistochemistry. J Histochem Cytochem 63(3), 190–205.CrossRefGoogle ScholarPubMed
Wine, RN & Chapin, RE (1997). Evaluation of the binding patterns of eleven FITC-conjugated lectins in fischer 344 rat testes. J Androl 18(1), 71–79.Google ScholarPubMed
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
Wu, AM (2003). Carbohydrate structural units in glycoproteins and polysaccharides as important ligands for Gal and GalNAc reactive lectins. J Biomed Sci 10(6), 676–688.CrossRefGoogle ScholarPubMed
Wu, AM, Lisowska, E, Duk, M & Yang, Z (2009). Lectins as tools in glycoconjugate research. Glycoconjugate J 26(8), 899.CrossRefGoogle ScholarPubMed
Wu, AM & Sugii, S (1991). Coding and classification of D-galactose, N-acetyl-D-galactosamine, and β-D-galp-[1→ 3 (4)]-β-D-GlcpNAc, specificities of applied lectins. Carbohydr Res 213, 127–143.CrossRefGoogle Scholar
Wu, AM, Sugii, S & Herp, A (1988). A guide for carbohydrate specificities of lectins. Adv Exp Med Biol 228, 819–847.CrossRefGoogle ScholarPubMed
Ziak, M, Qu, B, Zuo, X, Zuber, C, Kanamori, A, Kitajima, K, Inoue, S, Inoue, Y & Roth, J (1996). Occurrence of poly (alpha2, 8-deaminoneuraminic acid) in mammalian tissues: Widespread and developmentally regulated but highly selective expression on glycoproteins. Proc Natl Acad Sci USA 93(7), 2759–2763.CrossRefGoogle ScholarPubMed
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