Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Spatial and temporal regulation of glycosylation during Drosophila eye development

  • 255 Accesses

  • 5 Citations

Abstract

Glycosylation plays an essential role during development, in processes such as morphogen distribution, cell-to-cell communication, and extracellular matrix formation. Glycosylation is regulated during development in both a spatial and temporal manner. This study presents a detailed description of glycan distribution from late pupal to adult stages in Drosophila ommatidia by using nine different lectins. The lectins ConA, LCA, and DSA, which recognize high-mannose or complex types of N-linked glycans stain both apical and basolateral membranes of photoreceptor cells, whereas SBA, DBA, and ABA lectins, which bind to mucin-type O-glycans, label the inter-rhabdomeral space. The O-linked GlcNAc moiety is strongly labeled by WGA on the nuclear membrane. The localization of these glycans does not change throughout late pupal development. In contrast, the abundance of O-linked glycans, bisected oligosaccharides, and GlcNAc-containing glycans detected by PNA, PHA-E4, and WGA, respectively, is reduced in rhabdomeres and other subcellular domains during late pupal development. Some of these glycans have also been detected in the Golgi and/or putative secretory vesicles, suggesting their dynamic transport during development. These glycans, whose expression is dynamically regulated in a spatial and temporal manner, may therefore play critical roles in ommatidial development.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Baeg GH, Selva EM, Goodman RM, Dasgupta R, Perrimon N (2004) The Wingless morphogen gradient is established by the cooperative action of Frizzled and heparan sulfate proteoglycan receptors. Dev Biol 276(1):89–100

  2. Bainbridge SP, Bownes M (1981) Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66:57–80

  3. Callaerts P, Vulsteke V, Peumans W, De Loof A (1995) Lectin binding sites during Drosophila embryogenesis. Roux’s Arch Dev Biol 204:229–243

  4. D’Amico P, Jacobs JR (1995) Lectin histochemistry of the Drosophila embryo. Tissue Cell 27:23–30

  5. Fleming RJ, Gu Y, Hukriede NA (1997) Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc. Development 124:2973–2981

  6. Fredieu JR, Mahowald AP (1994) Glycoconjugate expression during Drosophila embryogenesis. Acta Anat 149:89–99

  7. Fristrom DK, Fristrom JW (1982) Cell surface binding sites for peanut agglutinin in the differentiating eye disc of Drosophila. Dev Biol 92:418–427

  8. Haltiwanger RS (2002) Regulation of signal transduction pathways in development by glycosylation. Curr Opin Struct Biol 12:593–598

  9. Husain N, Pellikka M, Hong H, Klimentova T, Choe K-M, Clandinin TR, Tepass U (2006) The agrin/Perlecan-related protein Eyes shut is essential for epithelial lumen formation in the Drosophila retina. Dev Cell 11:483–493

  10. Kramerov AA, Mikhaleva EA, Rozovsky YM, Pochechueva TV, Baikova NA, Arsenjeva EL, Gvozdev VA (1997) Insect mucin-type glycoprotein: immunodetection of the O-glycosylated epitope in Drosophila melanogaster cells and tissues. Insect Biochem Mol Biol 27:513–521

  11. Kumar JP, Ready DF (1995) Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development 121:4359–4370

  12. Liwosz A, Lei T, Kukuruzinska MA (2006) N-Glycosylation affects the molecular organization and stability of E-cadherin junctions. J Biol Chem 281:23138–23149

  13. Longley RL Jr, Ready DF (1995) Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev Biol 171:415–433

  14. Panin VM, Papayannopoulos V, Wilson R, Irvine KD (1997) Fringe modulates Notch-ligand interactions. Nature 387:908–912

  15. Paulsen R, Schwemer J (1979) Vitamin A deficiency reduces the concentration of visual pigment protein within blowfly photoreceptor membranes. Biochim Biophys Acta 557:385–390

  16. Pelham RJ Jr, Chang F (2001) Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nat Cell Biol 3:235–244

  17. Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, Ready DF, Tepass U (2002) Crumbs, the Drosophila homologue of human CRB1/PR12, is essential for photoreceptor morphogenesis. Nature 416:143–149

  18. Perotti ME, Pasini ME (1995) Glycoconjugates of the surface of the spermatozoa of Drosophila melanogaster: a qualitative and quantitative study. J Exp Zool 271:311–318

  19. Perotti ME, Riva A (1988) Concanavalin A binding sites on the surface of Drosophila melanogaster sperm: a fluorescence and ultrastructural study. J Ultrastruct Mol Struct Res 100:173–182

  20. Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240

  21. Rozelle AL, Machesky LM, Yamamoto M, Driessens MH, Insall RH, Roth MG, Luby-Phelps K, Marriott G, Hall A, Yin HL (2000) Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr Biol 10:311–320

  22. Spicer SS, Schulte BA (1992) Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochem Cytochem 40:1–38

  23. Tepass U, Harris KP (2007) Adherence junctions in Drosophila retinal morphogenesis. Trends Cell Biol 17:26–35

  24. Tian E, Ten Hagen KG (2007a) O-linked glycan expression during Drosophila development. Glycobiology 17:820–827

  25. Tian E, Ten Hagen KG (2007b) A UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase is required for epithelial tube formation. J Biol Chem 282:606–614

  26. Tonning A, Helms S, Schwarz H, Uv AE, Moussian B (2006) Hormonal regulation of Mummy is needed for apical extracellular matrix formation and epithelial morphogenesis in Drosophila. Development 133:331–341

  27. Wu AM, Wu JH, Herp A, Liu JH (2003) Effect of polyvalencies of glycotopes on the binding of a lectin from the edible mushroom, Agraricus bisporus. Biochem J 371:311–320

  28. Yamamoto K, Ito S, Yasukawa F, Konami Y, Matsumoto N (2005) Measurement of the carbohydrate-binding specificity of lectins by a multiplexed bead-based flow cytometric assay. Anal Biochem 336:28–38

  29. Yano H, Yamamoto-Hino M, Abe M, Kuwahara R, Haraguchi S, Kusaka I, Awano W, Kinoshita-Toyoda A, Toyoda H, Goto S (2005) Distinct functional units of Golgi complex in Drosophila cells. Proc Natl Acad Sci USA 102:13467–13472

Download references

Acknowledgements

We thank members of the Bio-molecular Structure Analysis Laboratory, Mutant Flies Laboratory, and Goto Laboratory in MITILS for technical support and helpful discussions.

Author information

Correspondence to Satoshi Goto.

Additional information

This work was supported by grants from the Ministry of Education, Culture Sports, Science, and Technology of Japan (to H.Y. and S.G.) and the Japan Science and Technology Agency (to S.G.).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yano, H., Yamamoto-Hino, M. & Goto, S. Spatial and temporal regulation of glycosylation during Drosophila eye development. Cell Tissue Res 336, 137–147 (2009). https://doi.org/10.1007/s00441-009-0753-6

Download citation

Keywords

  • Glycosylation
  • Development
  • Eye
  • Golgi
  • Lectins
  • Drosophila melanogaster (Insecta)