Let’s talk about sexes: sex-related N-glycosylation in ecologically important invertebrates

  • Freja Scheys
  • Els J. M. Van Damme
  • Guy SmaggheEmail author
Original Article


Parasitic helminths and pest insects are organisms with great ecological importance, having direct or indirect detrimental effects on people’s lives worldwide. Several reports in literature indicate that the glycan repertoire of parasites plays important roles in host-parasite interactions and modulation and evasion of the host immune system, while insect glycans are essential for their survival, growth and development. Although glycosylation is the result of a highly conserved machinery, differences between species and between different stages of one organism’s life cycle occur. This review provides insight into recent glycomics studies both for helminths and insects, focussing on sex differences and the role of carbohydrate structures in reproduction. Information on the differential N-glycosylation process between males and females can generate a better understanding of the biology and physiology of these economic important organisms, and can contribute to the discovery of novel anti-fecundity vaccine candidates and drug targets, as well as in the elaboration of innovative pest management strategies.


N-glycosylation Helminth Parasite Pest insect 


Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. 1.
    van Die, I., Cummings, R.D.: Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response? Glycobiology. 20, 2–12 (2010)CrossRefGoogle Scholar
  2. 2.
    Jiménez-Castells, C., Vanbeselaere, J., Kohlhuber, S., Ruttkowski, B., Joachim, A., Paschinger, K.: Gender and developmental specific N-glycomes of the porcine parasite Oesophagostomum dentatum. Biochim. Biophys. Acta Gen. Subj. (2016).
  3. 3.
    Ghosh, S.: Sialylation and sialyltransferase in insects. Glycoconj. J. 35, 433–441 (2018)CrossRefGoogle Scholar
  4. 4.
    Hokke, C.H., van Diepen, A.: Helminth glycomics – glycan repertoires and host-parasite interactions. Mol. Biochem. Parasitol. 215, 47–57 (2016)CrossRefGoogle Scholar
  5. 5.
    Walski, T., De Schutter, K., Van Damme, E.J.M., Smagghe, G.: Diversity and functions of protein glycosylation in insects. Insect Biochem. Mol. Biol. (2017).
  6. 6.
    Prasanphanich, N.S., Mickum, M.L., Heimburg-Molinaro, J., Cummings, R.D.: Glycoconjugates in host-helminth interactions. Front. Immunol. (2013).
  7. 7.
    Schiller, B., Hykollari, A., Yan, S., Paschinger, K., Wilson, I.B.H.: Complicated N-linked glycans in simple organisms. Biol. Chem. 393, 661–673 (2012)CrossRefGoogle Scholar
  8. 8.
    Walski, T., Van Damme, E.J.M., Smargiasso, N., Christiaens, O., De Pauw, E., Smagghe, G.: Protein N-glycosylation and N-glycan trimming are required for postembryonic development of the pest beetle Tribolium castaneum. Sci. Rep. (2016).
  9. 9.
    Katoh, T., Tiemeyer, M.: The N’s and O’s of Drosophila glycoprotein glycobiology. Glycoconj. J. 30, 57–66 (2013)CrossRefGoogle Scholar
  10. 10.
    North, S.J., Koles, K., Hembd, C., Morris, H.R., Dell, A., Panin, V.M., Haslam, S.M.: Glycomic studies of Drosophila melanogaster embryos. Glycoconj. J. 23, 345–354 (2006)CrossRefGoogle Scholar
  11. 11.
    Fabini, G., Freilinger, A., Altmann, F., Wilson, I.B.: Identification of core α1,3-fucosylated glycans and cloning of the requisite fucosyltransferase cDNA from Drosophila melanogaster. J. Biol. Chem. 276, 28058–28067 (2001)CrossRefGoogle Scholar
  12. 12.
    Rendić, D., Sharrow, M., Katoh, T., Overcarsh, B., Nguyen, K., Kapurch, J., Aoki, K., Wilson, I.B.H., Tiemeyer, M.: Neural-specific α3-fucosylation of N-linked glycans in the Drosophila embryo requires fucosyltransferase A and influences developmental signaling associated with O-glycosylation. Glycobiology. 20, 1353–1365 (2010)CrossRefGoogle Scholar
  13. 13.
    Wuhrer, M., Koeleman, C.A.M., Fitzpatrick, J.M., Hoffman, K.F., Deelder, A.M., Hokke, C.H.: Gender-specific expression of complex-type N-glycans in schistosomes. Glycobiology. 16, 991–1006 (2006)CrossRefGoogle Scholar
  14. 14.
    Kim, B., Suo, B., Emmons, S.W.: Gene function prediction based on developmental transcriptomes of the two sexes in C. elegans. Cell Rep. 17, 917–928 (2016)CrossRefGoogle Scholar
  15. 15.
    Loukas, A., Mullin, N.P., Tetteh, K.K.A., Moens, L., Maizels, R.M.: A novel C-type lectin secreted by a tissue-dwelling parasitic nematode. Curr. Biol. 9, 825–828 (1999)CrossRefGoogle Scholar
  16. 16.
    Loukas, A., Maizels, R.M.: Helminth C-type lectins and host-parasite interactions. Parasitol. Today. 16, 333–339 (2000)CrossRefGoogle Scholar
  17. 17.
    Brown, A.C., Harrison, L.M., Kapulkin, W., Jones, B.F., Sinha, A., Savage, A., Villalon, N., Cappello, M.: Molecular cloning and characterization of a C-type lectin from Ancylostoma ceylanicum: evidence for a role in hookworm reproductive physiology. Mol. Biochem. Parasitol. 151, 141–147 (2007)CrossRefGoogle Scholar
  18. 18.
    Vanbeselaere, J., Yan, S., Joachim, A., Paschinger, K., Wilson, I.B.H.: The parasitic nematode Oesophagostomum dentatum synthesizes unusual glycosaminoglycan-like O-glycans. Glycobiology. 28, 474–481 (2018)CrossRefGoogle Scholar
  19. 19.
    Martini, F., Eckmair, B., Štefanić, S., Jin, C., Garg, M., Yan, S., Jiménez-Castells, C., Hykollari, A., Neupert, C., Venco, L., Silva, D.V., Wilson, I.B.H., Paschinger, K.: Highly modified and immunoactive N-glycans of the canine heartworm. Nat. Commun. (2019).
  20. 20.
    Cai, P., Liu, S., Piao, X., Hou, N., Gobert, G.N., McManus, D.P., Chen, Q.: Comprehensive transcriptome analysis of sex-biased expressed genes reveals discrete biological and physiological features of male and female Schistosoma japonicum. PLoS Negl. Trop. Dis. (2016).
  21. 21.
    Hokke, C.H., Fitzpatrick, J.M., Hoffman, K.F.: Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends Parasitol. (2007).
  22. 22.
    Fitzpatrick, J.M., Johnston, D.A., Williams, G.W., Williams, D.J., Freeman, T.C., Dunne, D.W., Hoffmann, K.F.: An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Mol. Biochem. Parasitol. 141, 1–13 (2005)CrossRefGoogle Scholar
  23. 23.
    Liu, F., Lu, J., Hu, W., Wang, S., Cui, S., Chi, M., Yan, Q., Wang, X., Song, H., Xu, X., Wang, J., Zhang, X., Zhang, X., Wang, Z., Xue, C., Brindley, P.J., McManus, D.P., Yang, P., Feng, Z., Chen, Z., Han, Z.: New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analysis of Schistosoma japonicum. PLoS Pathog. (2006).
  24. 24.
    Zhang, M., Hong, Y., Han, Y., Han, H., Peng, J., Qiu, C., Yang, J., Lu, K., Fu, Z., Lin, J.: Proteomic analysis of tegument-exposed proteins of female and male Schistosoma japonicum worms. J. Proteome Res. 12, 5260–5270 (2013)CrossRefGoogle Scholar
  25. 25.
    Khoo, K., Chatterjee, D., Caulfield, J.P., Morris, H.R., Dell, A.: Structural mapping of the glycans from the egg glycoproteins of Schistosoma mansoni and Schistosoma japonicum: identification of novel core structures and terminal sequences. Glycobiology. 7, 663–677 (1997)CrossRefGoogle Scholar
  26. 26.
    Smit, C.H., van Diepen, A., Nguyen, D.L., Wuhrer, M., Hoffman, K.F., Deelder, A.M., Hokke, C.H.: Glycomic analysis of life stages of the human parasite Schistosoma mansoni reveals developmental expression profiles of functional and antigenic glycan motifs. Mol. Cell. Proteomics. 14, 1750–1769 (2015)CrossRefGoogle Scholar
  27. 27.
    Sanderson, M.J.: Phylogenetic signal in the eukaryotic tree of life. Science. 321, 121–123 (2008)CrossRefGoogle Scholar
  28. 28.
    Aoki, K., Perlman, M., Lim, J.M., Cantu, R., Wells, L., Tiemeyer, M.: Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J. Biol. Chem. 282, 9127–9142 (2007)CrossRefGoogle Scholar
  29. 29.
    Ten Hagen, K.G., Zhang, L., Tian, E., Zhang, Y.: Glycobiology on the fly: developmental and mechanistic insights from Drosophila. Glycobiology. 19, 102–111 (2009)CrossRefGoogle Scholar
  30. 30.
    Kurz, S., Aoki, K., Jin, C., Karlsson, N.G., Tiemeyer, M., Wilson, I.B.H., Paschinger, K.: Targeted release and fractionation reveal glucoronylated and sulphated N- and O-glycans in larvae of dipteran insects. J. Proteome. 126, 172–188 (2015)CrossRefGoogle Scholar
  31. 31.
    Dönitz, J., Schmitt-Engel, C., Grossmann, D., Gerischer, L., Tech, M., Schoppmeier, M., Klingler, M., Bucher, G.: iBeetle-base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Res. 43, D720–D725 (2014)CrossRefGoogle Scholar
  32. 32.
    Stanton, R., Hykollari, A., Eckmair, B., Malzl, D., Dragosits, M., Palmberger, D., Wang, P., Wilson, I.B.H., Paschinger, K.: The underestimated N-glycomes of lepidopteran species. Biochim. Biophys. Acta. 1861, 699–714 (2017)CrossRefGoogle Scholar
  33. 33.
    Kajihura, H., Hamaguchi, Y., Mizushima, H., Misaki, R., Fujiyama, K.: Sialylation potentials of the silkworm, Bombyx mori; B. mori possesses an active α2,6-sialyltransferase. Glycobiology. 25, 1441–1453 (2015)CrossRefGoogle Scholar
  34. 34.
    Mabashi-Asazuma, H., Sohn, B.H., Kim, Y.S., Kuo, C.W., Khoo, K.H., Kucharski, C.A., Fraser, M.J.J., Jarvis, D.L.: Targeted glycoengineering extends the protein N-glycosylation pathway in the silkworm silk gland. Insect Biochem. Mol. Biol. 65, 20–27 (2015)CrossRefGoogle Scholar
  35. 35.
    Soya, S., Sahar, U., Karaçali, S.: Monosaccharide profiling of silkworm (Bombyx mori L.) nervous system during development and aging. Invertebr. Neurosci. (2016).
  36. 36.
    Kubelka, V., Altmann, F., Staudacher, E., Tretter, V., März, L., Hård, K., Kamerling, J.P., Vliegenthart, J.F.: Primary structures of the N-linked carbohydrate chains from honeybee venom phospholipase A2. Eur. J. Biochem. 213, 1193–1204 (1993)CrossRefGoogle Scholar
  37. 37.
    Kubelka, V., Altmann, F., März, L.: The asparagine-linked carbohydrate of honeybee venom hyaluronidase. Glycoconj. J. 12, 77–83 (1995)CrossRefGoogle Scholar
  38. 38.
    Scheys, F., De Schutter, K., Shen, Y., Yu, N., Smargiasso, N., De Pauw, E., Van Damme, E.J.M., Smagghe, G.: The N-glycome of the hemipteran pest insect Nilaparvata lugens reveals unexpected sex differences. Insect Biochem. Mol. Biol. (2019).
  39. 39.
    Cattaneo, F., Pasini, M.E., Intra, J., Matsumoto, M., Briani, F., Hoshi, M., Perotti, M.E.: Identification and expression analysis of Drosophila melanogaster genes encoding beta-hexosaminidases of the sperm plasma membrane. Glycobiology. 16, 786–800 (2006)CrossRefGoogle Scholar
  40. 40.
    Cattaneo, F., Pasini, M.E., Perotti, M.E.: Glycosidases are present on the surface of Drosophila melanogaster spermatozoa. Mol. Reprod. Dev. 48, 276–281 (1997)CrossRefGoogle Scholar
  41. 41.
    Cattaneo, F., Ogiso, M., Hoshi, M., Perotti, M.E., Pasini, M.E.: Purification and characterization of the plasma membrane glycosidases of Drosophila melanogaster spermatozoa. Insect Biochem. Mol. Biol. 32, 929–941 (2002)CrossRefGoogle Scholar
  42. 42.
    Intra, J., Cenni, F., Perotti, M.E.: An α-L-fucosidase potentially involved in fertilization is present on Drosophila spermatozoa surface. Mol. Reprod. Dev. 73, 1149–1158 (2006)CrossRefGoogle Scholar
  43. 43.
    Intra, J., De Caro, D., Perotti, M.E., Perotti, M.E.: Glycosidases in the plasma membrane of Ceratitis capitata spermatozoa. Insect Biochem. Mol. Biol. 41, 90–100 (2011)CrossRefGoogle Scholar
  44. 44.
    Pasini, M.E., Intra, J., Gomulski, L.M., Calvenzani, V., Petroni, K., Briani, F., Perotti, M.E.: Identification and expression profiling of Ceratitis capitata genes coding for β-hexosaminidases. Gene. 473, 44–56 (2010)CrossRefGoogle Scholar
  45. 45.
    Stephens, K., Thaler, C.D., Cardullo, R.A.: Characterization of plasma membrane associated type II α-D-mannosidase and β-N-acetylglucosaminidase of Aquarius remigis sperm. Insect Biochem. Mol. Biol. 60, 78–85 (2015)CrossRefGoogle Scholar
  46. 46.
    Intra, J., Cenni, F., Pavesi, G., Pasini, M.E., Perotti, M.E.: Interspecific analysis of the glycosidases of the sperm plasma membrane in Drosophila. Mol. Reprod. Dev. 76, 85–100 (2009)CrossRefGoogle Scholar
  47. 47.
    Perotti, M., Cattaneo, F., Pasini, M.E., Vernì, F., Hackstein, J.H.P.: Male sterile mutant casanova gives clues to mechanisms of sperm-egg interactions in Drosophila melanogaster. Mol. Reprod. Dev. 60, 248–259 (2001)CrossRefGoogle Scholar
  48. 48.
    Intra, J., Veltri, C., De Caro, D., Perotti, M.E., Pasini, M.E.: In vitro evidence for the participation of Drosophila melanogaster sperm β-N-acetylglucosaminidases in the interactions with glycans carrying terminal N-acetylglucosamine residues on the egg's envelopes. Arch. Insect Biochem. Physiol. (2017).
  49. 49.
    Intra, J., Concetta, V., De Caro, D., Perotti, M.E., Pasini, M.E.: Drosophila sperm surface alpha-L-fucosidase interacts with the egg coats through its core fucose residues. Insect Biochem. Mol. Biol. 63, 133–143 (2015)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biotechnology, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium
  2. 2.Department of Plants and Crops, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

Personalised recommendations