Skip to main content
Log in

Sialylation and sialyltransferase in insects

  • Mini-Review
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Sialic acids are negatively charged nine carbon monosaccharides located terminally on glycoproteins and glycolipids that control cellular physiological processes. Sialylation is a post translational modification (ptm) regulated by enzymes and has been studied in prokaryotes including bacteria, dueterostomes including vertebrates, Cephalochordates, Ascidians, Echinoderms and protostomes including Molluscs and Arthropods and Plant. Although diverse structures of sialylated molecules have been reported in different organisms, unravelling sialylation in insect biology is a completely new domain. Within protostomes, the study of sialylation in members of Phylum Arthropoda and Class Insecta finds importance. Reports on sialylation in some insects exist. Genetically engineered components of sialylation pathway in Spodoptera frugiperda (Sf9) cell lines have enabled our understanding of sialylation and expression of mammalian proteins in insects. In this study we have summarised the finding on (i) sialylated molecules (ii) processes and enzymes involved (iii) function of sialylation (iv) genetic engineering approaches and generation of mammalian protein expression systems (v) a comparison of sialylation machinery in insects with that of mammals (vi) genes and transcriptional regulation in insects. At present no information on structural studies of insect sialyltransferase (STs) exist. We report minor differences in ST structure in insects on complete protein sequences recorded in Genbank through in silico approaches. An indepth study of all the components of the sialylation pathway in different insect species across different families and their evolutionary significance finds importance as the future scope of this review.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Ruppert, Edward E, Richard S. Fox, and Robert D. Barnes. 2004 Invertebrate Zoology: A Functional Evolutionary Approach. Belmont, CA: Thomson-Brooks/Cole

  2. Ramamurthy VV and Gaur A, Adaptive radiation and insects, Sharma V.P. (eds) Nature at Work: Ongoing Saga of Evolution. Springer, New Delhi, 2010

    Chapter  Google Scholar 

  3. Aslan, C.E., Liang, C.T., Galindo, B., Hill, K., Topete, W.: The role of honey bees as pollinators in natural areas. Nat. Areas J. 36(4), 478–488 (2016)

    Article  Google Scholar 

  4. Hung, K.J., Kingston, J.M., Albrecht, M., Holway, D.A., Kohn, J.R.: The worldwide importance of honey bees as pollinators in natural habitats. Proc. Biol. Sci. 285(1870), 20172140 (2018 Jan 10)

    Article  PubMed  PubMed Central  Google Scholar 

  5. Castillo, J.C., Reynolds, S.E.: Eleftherianos ITrends Parasitol. Insect immune responses to nematode parasites. Trends Parasitol. 27(12), 537–547 (2011 Dec)

    Article  CAS  PubMed  Google Scholar 

  6. Tobias, N.J.: Insect vectors of disease: untapped reservoirs for new antimicrobials? Front. Microbiol. 7, 2085 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chakraborty, A., Banerjee, D., Ghosh, S., Ansar, W.: Thermophilic pupal endoparasitoids: Brachymeria minuta (Hymenoptera: Chalicididae) on forensic indicator Sarcophaga (Parasarcophaga) albiceps. Prommalia. 3, (2015)

  8. Joseph, I., Mathew, D.G., Sathyan, P., Vargheese, G.: The use of insects in forensic investigations: an overview on the scope of forensic entomology. J. Forensic Dent. Sci. 3(2), 89–91 (2011 Jul-Dec)

    Article  PubMed  PubMed Central  Google Scholar 

  9. Lounibos, L.P.: Invasions by insect vectors of human disease. Annu. Rev. Entomol. 47, 233–266 (2002)

    Article  CAS  PubMed  Google Scholar 

  10. Blanke, A., Rühr, P.T., Mokso, R., Villanueva, P., Wilde, F., Stampanoni, M., Uesugi, K., Machida, R., Misof, B.: Structural mouthpart interaction evolved already in the earliest lineages of insects. Proc. Biol. Sci. 282(1812), 20151033 (2015 Aug 7)

    Article  PubMed  PubMed Central  Google Scholar 

  11. Nel, P., Bertrand, S., André, N.: Diversification of insects since the Devonian: a new approach based on morphological disparity of mouthparts, 2018, scientific reports volume 8. Article number. 3516 (2018)

  12. Hore, G., Maity, A., Naskar, A., Ansar, W., Ghosh, S., Saha, G.K., Banerjee, D.: Scanning electron microscopic studies on antenna of Hemipyrellia ligurriens (Wiedemann, 1830) (Diptera: Calliphoridae)-a blow fly species of forensic importance. Acta Trop. 172, 20–28 (2017)

    Article  PubMed  Google Scholar 

  13. Schauer, R.: Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19, 507–514 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Schauer, R.: Sialic acids as link to Japanese scientists. Proc Jpn Acad Ser B Phys Biol Sci. 92, 109–120 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Buschiazzo, A., Alzari, P.M.: Sialic acid metabolism structural insights into sialic acid enzymology. Curr. Opin. Chem. Biol. 12, 565–572 (2008)

    Article  CAS  PubMed  Google Scholar 

  16. Teppa, R.E., Petit, D., Plechakova, O., Cogez, V., Harduin-Lepers, A.: Phylogenetic-derived insights into the evolution of sialylation in eukaryotes: comprehensive analysis of vertebrate β-Galactoside α2,3/6-Sialyltransferases (ST3Gal and ST6Gal). Int. J. Mol. Sci. 17, 1286 (2016)

    Article  CAS  PubMed Central  Google Scholar 

  17. Roth, J., Kempf, A., Reuter, G., Schauer, R., Gehring, W.J.: Occurrence of sialic acids in drosophila melanogaster. Science. 256, 673–675 (1992)

    Article  CAS  PubMed  Google Scholar 

  18. Warren, L.: The distribution of sialic acids in nature. Comp. Biochem. Physiol. 10, 153–171 (1963)

    Article  CAS  PubMed  Google Scholar 

  19. Marchal, I., Jarvis, D.L., Cacan, R., Verbert, A.: Glycoproteins from insect cells: sialylated or not? Biol. Chem. 382, 151–159 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ghosh, S., Bandyopadhyay, S., Bhattacharya, D.K., Mandal, C.: Altered erythrocyte membrane characteristics during anemia in childhood acute lymphoblastic leukemia. Ann. Hematol. 84, 76–84 (2005a)

    Article  CAS  PubMed  Google Scholar 

  21. Ghosh, S., Bandyopadhyay, S., Mallick, A., Pal, S., Vlasak, R., Bhattacharya, D.K., Mandal, C.: Interferon gamma promotes survival of lymphoblasts overexpressing 9-O-acetylated sialoglycoconjugates in childhood acute lymphoblastic leukaemia (ALL). J. Cell. Biochem. 95, 206–216 (2005b)

    Article  CAS  PubMed  Google Scholar 

  22. Ghosh, S., Bandyopadhyay, S., Mukherjee, K., Mallick, A., Pal, S., Mandal, C., Bhattacharya, D.K., Mandal, C.: O-acetylation of sialic acids is required for the survival of lymphoblasts in childhood acute lymphoblastic leukemia (ALL). Glycoconj. J. 24(1), 17–24 (2007 Jan)

    Article  CAS  PubMed  Google Scholar 

  23. Ghosh, S.: Sialic acids: biomarkers in endocrinal cancers. Glycoconj. J. 32(3–4), 79–85 (2015 May)

    Article  CAS  PubMed  Google Scholar 

  24. Ghosh, S., Bandyopadhyay, S., Pal, S., Das, B., Bhattacharya, D.K., Mandal, C.: Increased interferon gamma production by peripheral blood mononuclear cells in response to stimulation of overexpressed disease-specific 9-O-acetylated sialoglycoconjugates in children suffering from acute lymphoblastic leukaemia. Br. J. Haematol. 128, 35–41 (2005c)

    Article  CAS  PubMed  Google Scholar 

  25. Kajiura, 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)

    Article  CAS  PubMed  Google Scholar 

  26. Wang, Z., Park, J.H., Park, H.H., Tan, W., Park, T.H.: Enhancement of recombinahuman EPO production and sialylation in chinese hamster ovary cells through Bombyx mori 30Kc19 gene expression. Biotechnol. Bioeng. 108, 1634–1642 (2011)

    Article  CAS  PubMed  Google Scholar 

  27. Cime-Castillo J, Delannoy P, Mendoza-Hernández G, Monroy-Martínez V, Harduin-Lepers A, Lanz-Mendoza H, Hernández-Hernández Fde L,Zenteno E, Cabello-Gutiérrez C, Ruiz-Ordaz BH. 2015 Sialic acid expression in the mosquito Aedes aegypti and its possible role in dengue virus-vector interactions. Biomed. Res. Int. 2015:504187, 1, 16

  28. Karaçalı, S., Kırmızıgül, S., Deveci, R., Deveci, O., Onat, T., Gürcü, B.: Presence of sialic acid in prothoracic glands of galleria mellonella (Lepidoptera). Tissue Cell. 29, 315–321 (1997)

    Article  PubMed  Google Scholar 

  29. Malykh, Y.N., Krisch, B., Gerardy-Schahn, R., Lapina, E.B., Shaw, L., Schauer, R.: The presence of N-acetylneuraminic acid in Malpighian tubules of larvae of the cicada Philaenus spumarius. Glycoconj. J. 16, 731–739 (1999)

    Article  CAS  PubMed  Google Scholar 

  30. Geib, S.M., Calla, B., Hall, B., Hou, S., Manoukis, N.C.: Characterizing the developmental transcriptome of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae) through comparative genomic analysis with Drosophila melanogaster utilizing mod ENCODE datasets. BMC Genomics. 15, 942 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Scott, H., Panin, V.M.: The role of protein N-glycosylation in neural transmission. Glycobiology. 24, 407–417 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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)

    Article  CAS  PubMed  Google Scholar 

  33. Koles K, Lim JM, Aoki K, Porterfield M, Tiemeyer M, Wells L, Panin V. 2007, Identification of N-glycosylated proteins from the central nervous system of Drosophila melanogaster

  34. Koles, K., Repnikova, E., Pavlova, G., Korochkin, L.I., Panin, V.M.: Sialylation in protostomes: a perspective from Drosophila genetics and biochemistry. Glycoconj. J. 26, 313–324 (2009)

    Article  CAS  PubMed  Google Scholar 

  35. Koles, K., Irvine, K.D., Panin, V.M.: Functional characterization of Drosophila sialyltransferase. J. Biol. Chem. 279, 4346–4357 (2004)

    Article  CAS  PubMed  Google Scholar 

  36. Repnikova E., Koles K., Nakamura M., Pitts J., Li H., et al. , 2010. Sialyltransferase regulates nervous system function in Drosophila. J. Neurosci. 30: 6466–6476

    Article  CAS  PubMed  Google Scholar 

  37. Haines, N., Irvine, K.D.: Functional analysis of Drosophila beta1,4-N-acetlygalactosaminyltransferases. Glycobiology. 15, 335–346 (2005)

    Article  CAS  PubMed  Google Scholar 

  38. Haines, N., Stewart, B.A.: Functional roles for beta1,4-N-acetlygalactosaminyltransferase-a in Drosophila larval neurons and muscles. Genetics. 175, 671–679 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nakamura M, Pandey D, and Vladislav M. Panin 2012 Genetic Interactions Between Drosophila sialyltransferase and β1,4-N-acetylgalactosaminyltransferase-A Genes Indicate Their Involvement in the Same Pathway. G3 (Bethesda). 2: 653–656

  40. Islam, R., Nakamura, M., Scott, H., Repnikova, E., Carnahan, M., Pandey, D., Caster, C., Khan, S., Zimmermann, T., Zoran, M.J., Panin, V.M.: The role of Drosophila cytidine monophosphate-sialic acid synthetase in the nervous system. J. Neurosci. 33, 12306–12315 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zhang, Y.: I-TASSER server for proteins 3D structure prediction. BMC Bioinformatics. 9, 40 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. März, L., Altmann, F., Staudacher, E., Kubelka, V. Protein glycosylation in insects. In: Montreuil, J., Schachter, H., Vliegenthart, J.F.G. (eds.) Glycoproteins, pp. 543–563. Elsevier, Amsterdam, The Netherlands (1995)

  43. Angata, T., Varki, A.: Cloning, characterization, and phylogenetic analysis of siglec-9, a new member of the CD33-related group of siglecs. Evidence for co-evolution with sialic acid synthesis pathways. J Biol Chem. 275, 22127–22135 (2000)

    CAS  PubMed  Google Scholar 

  44. Hollister, J., Conradt, H., Jarvis, D.L.: Evidence for a sialic acid salvaging pathway in lepidopteran insect cells. Glycobiology. 13, 487–495 (2003)

    Article  CAS  PubMed  Google Scholar 

  45. Kim, K., Lawrence, S.M., Park, J., Pitts, L., Vann, W.F., Betenbaugh, M.J., Palter, K.B.: Expression of a functional Drosophila melanogaster N-acetylneuraminic acid (Neu5Ac) phosphate synthase gene: evidence for endogenous sialic acid biosynthetic ability in insects. Glycobiology. 12, 73–83 (2002)

    Article  CAS  PubMed  Google Scholar 

  46. Hooker, A.D., Green, N.H., Baines, A.J., Bull, A.T., Jenkins, N., Strange, P.G., James, D.C.: Constraints on the transport and glycosylation of recombinant IFN-gamma in Chinese hamster ovary and insect cells. Biotech Bioengr. 63, 559–572 (1999)

    Article  CAS  Google Scholar 

  47. Tomiya, N., Ailor, E., Lawrence, S.M., Betenbaugh, M.J., Lee, Y.C.: Determination of nucleotides and sugar nucleotides involved in protein glycosylation by high-performance anion-exchange chromatography: sugar nucleotide contents in cultured insect cells and mammalian cells. Anal. Biochem. 293, 129–137 (2001)

    Article  CAS  PubMed  Google Scholar 

  48. Lawrence, S.M., Huddleston, K.A., Pitts, L.R., Nguyen, N., Lee, Y.C., Vann, W.F., Coleman, T.A., Betenbaugh, M.J.: Cloning and expression of the human N-acetylneuraminic acid phosphate synthase gene with 2-keto-3-deoxy-D-glycero-D-galactonononic acid biosynthetic ability. J. Biol. Chem. 275, 17869–17877 (2000)

    Article  CAS  PubMed  Google Scholar 

  49. Mabashi-Asazuma, H., Shi, X., Geisler, C., Kuo, C.W., Khoo, K.H., Jarvis, D.L.: Impact of a human CMP-sialic acid transporter on recombinant glycoprotein sialylation in glycoengineered insect cells. Glycobiology. 23, 199–210 (2013)

    Article  CAS  PubMed  Google Scholar 

  50. Park, J.H., Wang, Z., Jeong, H.J., Park, H.H., Kim, B.G., Tan, W.S., Choi, S.S., Park, T.H.: Enhancement of recombinant human EPO production and glycosylation in serum-free suspension culture of CHO cells through expression and supplementation of 30Kc19. Appl. Microbiol. Biotechnol. 96, 671–683 (2012)

    Article  CAS  PubMed  Google Scholar 

  51. Granell, A.E., Palter, K.B., Akan, I., Aich, U., Yarema, K.J., Betenbaugh, M.J., Thornhill, W.B., Recio-Pinto, E.: DmSAS is required for sialic acid biosynthesis in cultured Drosophila third instar larvae CNS neurons. ACS Chem. Biol. 6, 1287–1295 (2011)

    Article  CAS  PubMed  Google Scholar 

  52. Kim, Y.K., Kim, K.R., Kang, D.G., Jang, S.Y., Kim, Y.H., Cha, H.J.: Expression of β-1,4-galactosyltransferase and suppression of β-N-acetylglucosaminidase to aid synthesis of complex N-glycans in insect Drosophila S2 cells. J. Biotechnol. 153, 145–152 (2011)

    Article  CAS  PubMed  Google Scholar 

  53. Petit, D., Mir, A.M., Petit, J.M., Thisse, C., Delannoy, P., Oriol, R., Thisse, B., Harduin-Lepers, A.: Molecular phylogeny and functional genomics of beta-galactoside alpha2,6-sialyltransferases that explain ubiquitous expression of st6gal1 gene in amniotes. J. Biol. Chem. 285, 38399–38414 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Viswanathan, K., Tomiya, N., Park, J., Singh, S., Lee, Y.C., Palter, K., Betenbaugh, M.J.: Expression of a functional Drosophila melanogaster CMP-sialic acid synthetase. Differential localization of the Drosophila and human enzymes. J Biol Chem. 281, 15929–15940 (2006)

    Article  CAS  PubMed  Google Scholar 

  55. Viswanathan, K., Narang, S., Betenbaugh, M.J.: Engineering Sialic Acid Synthesis Ability in Insect Cells. Methods Mol. Biol. 1321, 171–178 (2015)

    Article  PubMed  Google Scholar 

  56. Geisler, C., Jarvis, D.L.: Innovative use of a bacterial enzyme involved in sialic acid degradation to initiate sialic acid biosynthesis in glycoengineered insect cells. Metab. Eng. 14, 642–652 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hillar, A., Jarvis, D.L.: Re-visiting the endogenous capacity for recombinant glycoprotein sialylation by baculovirus-infected Tn-4h and DpN1 cells. Glycobiology. 20, 1323–1330 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tomiya, N., Narang, S., Lee, Y.C., Betenbaugh, M.J.: Comparing N-glycan processing in mammalian cell lines to native and engineered lepidopteran insect cell lines. Glycoconj. J. 21, 343–360 (2004)

    Article  CAS  PubMed  Google Scholar 

  59. Medvedova, L., Knopp, J., Farkas, R.: Steroid regulation of terminal protein glycosyltransferase genes: molecular and functional homologies within sialyltransferase and fucosyltransferase families. Endocr. Regul. 37, 203–210 (2003)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author acknowledges School of Biological Sciences NISER and HBNI, India for the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shyamasree Ghosh.

Ethics declarations

Conflict of interest

None declared.

Ethical approval

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghosh, S. Sialylation and sialyltransferase in insects. Glycoconj J 35, 433–441 (2018). https://doi.org/10.1007/s10719-018-9835-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-018-9835-6

Keywords

Navigation