CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Reproduction, Fertility and Development   
Reproduction, Fertility and Development
Journal Banner
  Vertebrate Reproductive Science & Technology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Board
Contacts
Content
All Issues
Special Issues
Research Fronts
Sample Issue
For Authors
General Information
Instructions to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review an Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our email Early Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow Connect with SRB
blank image
facebook TwitterIcon

Affiliated Societies

RFD is the official journal of the International Embryo Transfer Society and the Society for Reproductive Biology.


 

Article << Previous     |     Next >>        Online Early    

N-Glycans in Xenopus laevis testis characterised by lectin histochemistry

Galder Valbuena A , Juan Francisco Madrid B , María Martínez de Ubago A C , Laura Gómez-Santos A , Edurne Alonso A C , Lucio Díaz-Flores D and Francisco J. Sáez A C E

A Department of Cell Biology and Histology, School of Medicine and Dentistry, University of the Basque Country UPV/EHU, B° Sarriena s/n, E-48940 Leioa, Vizcaya, Spain.
B Department of Cell Biology and Histology, School of Medicine, Regional Campus of International Excellence ‘Campus Mare Nostrum’, University of Murcia, E-30100 Espinardo, Murcia, Spain.
C Training and Research Unit: Reproduction, Development, Aging and Cancer TRU/UFI 11/44, School of Medicine and Dentistry, University of the Basque Country UPV/EHU, B° Sarriena s/n, E-48940 Leioa, Vizcaya, Spain.
D Department of Anatomy, Pathology, Histology and Radiology, University of La Laguna, Ofra-La Cuesta s/n, La Laguna, E-38071 Tenerife, Spain.
E Corresponding author. Email: francisco.saez@ehu.es

Reproduction, Fertility and Development - http://dx.doi.org/10.1071/RD14077
Submitted: 26 February 2014  Accepted: 3 June 2014   Published online: 22 July 2014


 
PDF (2.3 MB) $25
 Export Citation
 Print
  
Abstract

Analysis of glycan chains of glycoconjugates is difficult because of their considerable variety. Despite this, several functional roles for these glycans have been reported. N-Glycans are oligosaccharides linked to asparagine residues of proteins. They are synthesised in the endoplasmic reticulum (ER) in a unique way, and later modified in both the ER and Golgi apparatus, developing different oligosaccharide chains. An essential role for complex N-glycans in mammalian spermatogenesis has been reported. The aim of the present study was to analyse the N-glycans of the Xenopus laevis testis by means of lectin histochemistry. Five lectins were used that specifically recognise mannose-containing and complex glycans, namely Galanthus nivalis agglutinin (GNA) from snowdrops, concanavalin A (Con A) from the Jack bean, Lens culinaris agglutinin (LCA) from lentils and Phaseolus vulgaris erythroagglutinin (PHA-E) and P. vulgaris leukoagglutinin (PHA-L) from the common bean. GNA and Con A labelled the interstitium and most of the germ cell types, whereas LCA and PHA-E showed affinity only for the interstitium. A granular cytoplasmic region was labelled in spermatogonia and spermatocytes by GNA and PHA-L, whereas GNA and LCA labelled a spermatid region that is probably associated with the centriolar basal body of the nascent flagellum. There was no specific labelling in the acrosome. Some unexpected results were found when deglycosylative pretreatments were used: pre-incubation of tissue sections with peptide N glycosidase F, which removes N-linked glycans, reduced or removed labelling with most lectins, as expected. However, after this pretreatment, the intensity of labelling remained or increased for Con A in the follicle (Sertoli) and post-meiotic germ cells. The β-elimination procedure, which removes O-linked glycans, revealed new labelling patterns with GNA, LCA and PHA-L, suggesting that some N-glycans were masked by O-glycans, and thus they became accessible to these lectins only after removal of the O-linked oligosaccharides. The functional role of the glycan chains identified could be related to the role of N-glycans involved in mammalian spermatogenesis reported previously.

Additional keywords: acrosome, mannose, N-linked oligosaccharides, spermatogenesis.


References

Abd-Elmaksoud, A., Sayed-Ahmed, A., Kassab, M., and 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, 124–133.
CrossRef | PubMed |

Agungpriyono, S., Kurohmaru, M., Prasetyaningtyas, W. E., Kaspe, L., Leus, K. Y., Sasaki, M., Kitamura, N., Yamada, J., and Macdonald, A. A. (2007). A lectin histochemical study on the testis of the babirusa, Babyroussa babyrussa (Suidae). Anat. Histol. Embryol. 36, 343–348.
CrossRef | CAS | PubMed |

Agungpriyono, S., Kurohmaru, M., Kimura, J., Wahid, A. H., Sasaki, M., Kitamura, N., Yamada, J., Fukuta, K., and Zuki, A. B. (2009). Distribution of lectin-bindings in the testis of the lesser mouse deer, Tragulus javanicus. Anat. Histol. Embryol. 38, 208–213.
CrossRef | CAS | PubMed |

Akama, T. O., Nakagawa, H., Sugihara, K., Narisawa, S., Ohyama, C., Nishimura, S.-I., O'Brien, D. A., Moremen, K. W., Millán, J. L., and Fukuda, M. N. (2002). Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 295, 124–127.
CrossRef | PubMed |

Alonso, E., Sáez, F. J., Madrid, J. F., and Hernández, F. (2001). Galactosides and sialylgalactosides in O-linked oligosaccharides of the primordial germ cells in Xenopus embryos. Glycoconj. J. 18, 225–230.
CrossRef | CAS | PubMed |

Arya, M., and Vanha-Perttula, T. (1984). Distribution of lectin binding in rat testis and epididymis. Andrologia 16, 495–508.
CrossRef | CAS | PubMed |

Arya, M., and Vanha-Perttula, T. (1985). Lectin binding pattern of bull testis. J. Androl. 6, 230–242.
| CAS | PubMed |

Arya, M., and Vanha-Perttula, T. (1986). Comparison of lectin-staining pattern in testis and epididymis of gerbil, guinea pig, mouse and nutria. Am. J. Anat. 175, 449–469.
CrossRef | CAS | PubMed |

Baenziger, J. U., and Fiete, D. (1979). Structural determinants of Concanavalin A specificity for oligosaccharides. J. Biol. Chem. 254, 2400–2407.
| CAS |

Ballesta, J., Martínez-Menárguez, J. A., Pastor, L. M., Avilés, M., Madrid, J. F., and Castells, M. T. (1991). Lectin binding pattern in the testes of several tetrapode vertebrales. Eur. J. Basic Appl. Histochem. 35, 107–117.
| CAS | PubMed |

Basu, D., Nair, J. V., and Appukuttan, P. S. (1987). Oligosaccharide structure determination of glycoconjugates using lectins. J. Biosci. 11, 41–46.
CrossRef | CAS |

Batista, F., Lu, L., Williams, S. A., and Stanley, P. (2012). Complex N-Glycans Are Essential, but Core 1 and 2 Mucin O-Glycans, O-Fucose Glycans, and NOTCH1 Are Dispensable, for Mammalian Spermatogenesis. Biol. Reprod. 86, 179.
CrossRef | PubMed |

Bertozzi, C. R., and Rabuka, D. (2009). Structural basis of glycan diversity. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 23–36. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Bi, J., Yanfen, L., Fengyun, S., Saalbach, A., Klein, C., Miller, D. J., Hess, R., and Nowak, R. A. (2013). Basigin null mutant male mice are sterile and exhibit impaired interactions between germ cells and Sertoli cells. Dev. Biol. 380, 145–156.
CrossRef | CAS | PubMed |

Bierhuizen, M. F. A., Tedzes, H., Schiphorst, W. E. C. M., van den Eijnden, D. H., and van Dijk, W. (1988). Effect of α(2–6)-linked sialic acid and α(1–3)-linked fucose on the interaction of N-linked glycopeptides and related oligosaccharides with immobilized Phaseolus vulgaris leukoagglutunating lectin (L-PHA). Glycoconj. J. 5, 85–97.
CrossRef | CAS |

Brewer, C. F., and Bhattacharyya, L. (1988). Concavalin A interactions with asparragine-linked glycopeptides. The mechanism of binding of oligomannose bisected hybrid and complex type carbohydrates. Glycoconj. J. 5, 159–173.
CrossRef | CAS |

Cummings, R. D., and Etzler, M. E. (2009). Antibodies and lectins in glycan analysis. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 633–647. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Cummings, R. D., and Kornfeld, S. (1982). Characterization of the structural determinants required for the high affinity interaction of asparragine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J. Biol. Chem. 257, 11 230–11 234.
| CAS |

Debray, H., Decout, D., Strecker, G., Spik, G., and Montreuil, J. (1981). Specificity of twelve lectins towards oligossacharides and glycopeptides related to N-glycolylproteins. Eur. J. Biochem. 117, 41–51.
CrossRef | CAS | PubMed |

Etzler, M. E., and Esko, J. D. (2009) Free glycans as signalling molecules. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 523–529. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.)

Freeze, H. H., and Haltiwanger, R. S. (2009). Other classes of ER/Golgi-derived glycans. In Essentials of Glycobiology, 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp 163–173. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Fujimoto, H., Tadano-Aritomi, K., Tokumasu, A., Ito, K., Hikita, T., Suzuki, K., and Ishizuka, I. (2000). Requirement of seminolipid in spermatogenesis revealed by UDP-galactose:Ceramide galactosyltransferase-deficien mice. J. Biol. Chem. 275, 22 623–22 626.
CrossRef | CAS |

Fukuda, M. N., and Akama, T. O. (2003). The role of N-glycans in spermatogenesis. Cytogenet. Genome Res. 103, 302–306.
CrossRef | CAS | PubMed |

Ge, R., Chen, G., and Hardy, M. P. (2008) The role of the Leydig cell in spermatogenic function. In ‘Molecular Mechanisms in Spermatogenesis’. Advan Exp Med Biol vol 636. (Ed. Yan Cheng C) pp. 16–41. (Landes Bioscience and Springer: Austin, TX.)

Gheri, G., Vannelli, G. B., Marini, M., Zappoli Thyrio, G. D., Gheri, R. G., and Sgambati, E. (2004). Distribution map of terminal and subterminal sugar residues of the glycoconjugates in the prepubertad and postpubertal testis of a subject affected by complete androgen insensitivity síndrome (Morris’s syndrome): lectin histochemical study. Histol. Histopathol. 19, 1–8.
| CAS | PubMed |

Goldstein, I. J., and Hayes, C. E. (1978). The lectins: carbohydrate-binding proteins of plants and animal. Adv. Carbohydr. Chem. Biochem. 35, 127–340.
CrossRef | CAS | PubMed |

Gómez-Santos, L., Alonso, E., Ferrer, C., Zuasti, A., Sáez, F. J., and Madrid, F. (2007). Histochemical demonstration of two subtypes of O-linked oligosaccharides in the rat gastric glands. Microsc. Res. Tech. 70, 809–815.
CrossRef | PubMed |

Griswold, M. D. (1995). Interactions between germ cells and Sertoli cells in the testis. Biol. Reprod. 52, 211–216.
CrossRef | CAS | PubMed |

Hammarström, S., Hammarströn, M.-L., Dillner, N., Sundbland, G., Arnarp, J., and Lönngren, J. (1982). Mitogenic luekoagglutinin from Phaseolus vulgaris binds to a pentasaccharide unit in N-acetyllactosamine-type glycoprotein glycans. Proc. Natl. Acad. Sci. USA 79, 1611–1615.
CrossRef | PubMed |

Hess, R. A., and de Franca, L. R. (2008) Spermatogenesis and cycle of the seminiferous epithelium. In ‘Molecular Mechanisms in Spermatogenesis’. Advan Exp Med Biol vol 636. (Ed. Yan Cheng C) pp. 16–41. (Landes Bioscience and Springer: Austin, TX.)

Huang, H.-H., and Stanley, P. (2010). A testis-specific regulator of complex and hybrid N-glycan synthesis. J. Cell Biol. 190, 893–910.
CrossRef | CAS | PubMed |

Jones, C. J., Morrison, C. A., and Stoddart, R. W. (1992a). Histochemical analysis of rat testicular glycoconjugates. 1. Subsets of N-linked saccharides in seminiferous tubules. Histochem. J. 24, 319–326.
CrossRef | CAS | PubMed |

Jones, C. J., Morrison, C. A., and Stoddart, R. W. (1992b). Histochemical analysis of rat testicular glycoconjugates. 2. Beta-galactosyl residues in O- and N-linked glycans in seminiferous tubules. Histochem. J. 24, 327–336.
CrossRef | CAS | PubMed |

Kalt, M. R. (1976). Morphology and kinetics of spermatogenesis in Xenopus laevis. J. Exp. Zool. 195, 393–407.
CrossRef | CAS | PubMed |

Kornfeld, R., and Kornfeld, S. (1970). The structure of a Phytohemagglutinin receptor site from human erythrocytes. J. Biol. Chem. 245, 2536–2545.
| CAS | PubMed |

Kornfeld, K., Reitman, M. L., and Kornfeld, R. (1981). The carbohydrate-binding specificity of pea and lentil lectins. J. Biol. Chem. 256, 6633–6640.
| CAS | PubMed |

Kurohmaru, M., Kobayashi, H., Kanai, Y., Hatori, S., Nishida, T., and Hayashi, Y. (1995). Distribution of lectin binding in the testes of the musk shrew, Suncus murinus. J. Anat. 187, 323–329.
| CAS | PubMed |

Kurohmaru, M., Maeda, S., Suda, A., Hondo, E., Ogawa, K., Endo, H., Kimura, J., Yamada, J., Rerkamnuaychoke, W., Chungsamarnyart, N., Hayashi, Y., and Nishida, T. (1996). An ultrastructural and lectin histochemical study on the seminiferous epithelium of the commom tree shrew (Tupaia glis). J. Anat. 189, 87–95.
| PubMed |

Labate, M., and Desantis, S. (1995). Histochemical analysis of lizard testicular glycoconjugates during the annual spermatogenetic cycle. Eur. J. Histochem. 39, 201–212.
| CAS | PubMed |

Lowe, J. B., and Marth, J. D. (2003). A genetic approach to mammalian glycan function. Annu. Rev. Biochem. 72, 643–691.
CrossRef | CAS | PubMed |

Madrid, J. F., Ballesta, J., Castells, M. T., and Hernández, F. (1990). Glycoconjugate distribution in the human fundic mucosa revealed by lectin- and glycoprotein-gold cytochemistry. Histochemistry 95, 179–187.
CrossRef | CAS | PubMed |

Malmi, R., Fröjdman, K., and Söderström, K.-O. (1990). Differentiation-related changes in the distribution of glycoconjugates in rat testis. Histochemistry 94, 387–395.
CrossRef | CAS | PubMed |

Martínez-Menárguez, J. A., Ballesta, J., Avilés, M., Castells, M. T., and Madrid, J. F. (1992). Cytochemical characterization of glycoproteins in the developing acrosome of rats. An ultrastructural study using lectin histochemistry, enzymes and chemical deglycosylation. Histochemistry 97, 439–449.
CrossRef | PubMed |

Martínez-Menárguez, J. A., Avilés, M., Madrid, J. F., Castells, M. T., and Ballesta, J. (1993). Glycosylation in Golgi apparatus of early spermatids of rat. A high resolution lectin cytochemical study. Eur. J. Cell Biol. 61, 21–33.
| PubMed |

Muramatsu, T. (2002). Carbohydrate recognition in spermatogenesis. Science 295, 53–54.
CrossRef | CAS | PubMed |

Nagano, R., Kanai, Y., Kurohmaru, M., Hayashi, Y., and Nishida, T. (1995). Changes in lectin binding patterns of chick primordial germ cells and Sertoli cells during sexual differentiation. J. Vet. Med. Sci. 57, 623–627.
CrossRef | CAS | PubMed |

Nizet, V., and Esko, J. D. (2009). Bacterial and viral infections. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 537–551. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Ono, K., Katsuyama, T., and Hotchi, M. (1983). Histochemical applications of mild alkaline hydrolysis for selective elimination of O-glycosidically linked glycoproteins. Stain Technol. 58, 309–312.
| CAS | PubMed |

Peel, S., and Bulmer, J. N. (1996). Lectin histochemistry of pregnant rat uterine tissues. J. Anat. 188, 197–205.
| CAS | PubMed |

Pudney, J. (1995). Spermatogenesis in nonmammalian vertebrates. Microsc. Res. Tech. 32, 459–497.
CrossRef | CAS | PubMed |

Rabionet, M., van der Spoel, A. C., Chuang, C.-C., von Tümpling-Radosta, B., Litjens, M., Bouwmeester, D., Hellbusch, C. C., Körner, C., Wiegandt, H., Gorgas, K., Platt, F. M., Gröne, H. J., and Sandhoff, R. (2008). Male germ cells require polyenoic sphingolipids with complex glycosylation for completion of meiosis: a link to ceramide synthase-3. J. Biol. Chem. 283, 13 357–13 369.
CrossRef | CAS |

Reed, S. C., and Stanley, H. P. (1972). Fine structure of spermatogenesis in the South African clawed toad Xenopus laevis Daudin. J. Ultrastruct. Res. 41, 277–285.
CrossRef | CAS | PubMed |

Sáez, F. J., Madrid, J. F., Aparicio, R., Leis, O., and Oporto, B. (1999). Lectin histochemical localization of N- and O-linked oligosaccharides during the spermiogenesis of the urodele amphibian Pleurodeles waltl. Glycoconj. J. 16, 639–648.
CrossRef | PubMed |

Sáez, F. J., Madrid, J. F., Alonso, E., and Hernández, F. (2000a). Lectin histochemical identification of the carbohydrate moieties on N- and O-linked oligosaccharides in the duct cells of the testis of an amphibian urodele, the Spanish newt (Pleurodeles waltl). Histochem. J. 32, 717–724.
CrossRef | PubMed |

Sáez, F. J., Madrid, J. F., Aparicio, R., Alonso, E., and Hernández, F. (2000b). Glycan residues of N- and O-linked oligosaccharides in the premeiotic spermatogenetic cells of the urodele amphibian Pleurodeles waltl characterized by means of lectin histochemistry. Tissue Cell 32, 302–311.
CrossRef | PubMed |

Sáez, F. J., Madrid, J. F., Alonso, E., and Hernández, F. (2001). Glycan composition of follicle (Sertoli) cells of the amphibian Pleurodeles waltl. A lectin histochemical study. J. Anat. 198, 673–681.
CrossRef | PubMed |

Sáez, F. J., Madrid, J. F., Cardoso, S., Gómez, L., and Hernández, F. (2004). Glycoconjugates of the urodele amphibian testis shown by lectin cytochemical methods. Microsc. Res. Tech. 64, 63–76.
CrossRef | PubMed |

Sandhoff, R., Geyer, R., Jennemann, R., Paret, C., Kiss, E., Yamashita, T., Gorgas, K., Sijmonsma, T. P., Iwamori, M., Finaz, C., Proia, R. L., Wiegandt, H., and Gröne, H. J. (2005). Novel class of glycosphingolipids involved in male fertility. J. Biol. Chem. 280, 27 310–27 318.
CrossRef | CAS |

Sharpe, R. M. (1993). Experimental evidence for Sertoli-germ cell and Sertoli-Leydig cell interactions. In ‘The Sertoli Cell’. (Eds L.D. Russell and M.D. Griswold.) pp. 391–418. (Cache River Press: Clearwater, FL)

Shibuya, N., Goldstein, I. J., Van Damme, E. J. M., and Peumans, W. J. (1988). Binding properties of a mannose-specific lectin from the snowdrop (Galanthus nivalis) bulb. J. Biol. Chem. 263, 728–734.
| CAS | PubMed |

Söderström, K.-O., Malmi, R. Y., and Karjalainen, K. (1984). Binding of fluorescein isothiocyanate conjugated lectins to rat spermatogenic cells in tissue sections. Enhancement of lectin fluorescence obtained by fixation in Bouin’s fluid. Histochemistry 80, 575–579.
CrossRef | PubMed |

Spicer, S. S., and Schulte, B. A. (1992). Diversity of cell glycoconjugates shown histochemically: a perspective. J. Histochem. Cytochem. 40, 1–38.
CrossRef | CAS | PubMed |

Stanley, P., and Cummings, R. D. (2009) Structures common to different glycans. In ‘Essentials of Glycobiology’. 2nd ed. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp 175–198. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.)

Stanley, P., Schachter, H., and Taniguchi, N. (2009) N-glycans. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 101–114. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.)

Strahl-Bolsinger, S., Gentzsch, M., and Tanner, W. (1999). Protein O-mannosylation. Biochim. Biophys. Acta 1426, 297–307.
CrossRef | CAS | PubMed |

Tadano-Aritomi, K., Matsuda, J., Fujimoto, H., Suzuki, K., and Ishizuka, I. (2003). Seminolipid and its precursor/degradative product, galactosylalkylacylglycerol, in the testis of saposin A- and proacrosin-deficient mice. J. Lipid Res. 44, 1737–1743.
CrossRef | CAS | PubMed |

Takamiya, K., Yamamoto, A., Furukawa, K., Zhao, J., Fukumoto, S., Yamashiro, S., Okada, M., Haraguchi, M., Shin, M., Kishikawa, M., Shiku, H., Aizawa, S., and Furukawa, K. (1998). Complex gangliosides are essential in spermatogenesis of mice: possible roles in the transport of testosterone. Proc. Natl. Acad. Sci. USA 95, 12 147–12 152.
CrossRef | CAS |

Valbuena, G., Madrid, J. F., Hernández, F., and Sáez, F. J. (2010). Identification of fucosylated glycoconjugates in Xenopus laevis testis by lectin histochemistry. Histochem. Cell Biol. 134, 215–225.
CrossRef | CAS | PubMed |

Varki, A., and Freeze, H. H. (2009) Glycans in acquired human diseases. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 601–615. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Varki, A., and Sharon, N. (2009) Historical background and overview. In Essentials of Glycobiology, 2nd ed. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 1–22. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.)

Varki, A., Freeze, H. H., and Vacquier, V. D. (2009). Glycans in development and systemic physiology. In ‘Essentials of Glycobiology’. 2nd edn. (Eds Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E) pp. 531–536. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.)

Walker, W. H. (2003). Molecular mechanisms controlling Sertoli cell proliferation and differentiation. Endocrinology 144, 3719–3721.
CrossRef | CAS | PubMed |

Wollina, U., Schereiber, G., Zollmann, C., Hipler, C., and Günther, E. (1989). Lectin-binding sites in normal human testis. Andrologia 21, 127–130.
CrossRef | CAS | PubMed |

Yamamoto, N. (1982). Electron microscopic analysis of sugar residues of glycoproteins in the acrosomes of spermatids using various lectins. Acta Histochem. Cytochem. 15, 139–150.
CrossRef | CAS |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2014