Advertisement

Glycoconjugate Journal

, Volume 35, Issue 5, pp 433–441 | Cite as

Sialylation and sialyltransferase in insects

  • Shyamasree Ghosh
Mini-Review

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.

Keywords

Sialic acid Neu5Ac Sialyltransferase (ST) Sialylation Insects Drosophila Mosquito 

Notes

Acknowledgements

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

Compliance with ethical standards

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.

References

  1. 1.
    Ruppert, Edward E, Richard S. Fox, and Robert D. Barnes. 2004 Invertebrate Zoology: A Functional Evolutionary Approach. Belmont, CA: Thomson-Brooks/ColeGoogle Scholar
  2. 2.
    Ramamurthy VV and Gaur A, Adaptive radiation and insects, Sharma V.P. (eds) Nature at Work: Ongoing Saga of Evolution. Springer, New Delhi, 2010CrossRefGoogle Scholar
  3. 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)CrossRefGoogle Scholar
  4. 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)CrossRefPubMedGoogle Scholar
  5. 5.
    Castillo, J.C., Reynolds, S.E.: Eleftherianos ITrends Parasitol. Insect immune responses to nematode parasites. Trends Parasitol. 27(12), 537–547 (2011 Dec)CrossRefPubMedGoogle Scholar
  6. 6.
    Tobias, N.J.: Insect vectors of disease: untapped reservoirs for new antimicrobials? Front. Microbiol. 7, 2085 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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)Google Scholar
  8. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Lounibos, L.P.: Invasions by insect vectors of human disease. Annu. Rev. Entomol. 47, 233–266 (2002)CrossRefPubMedGoogle Scholar
  10. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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)Google Scholar
  12. 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)CrossRefPubMedGoogle Scholar
  13. 13.
    Schauer, R.: Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19, 507–514 (2009)CrossRefPubMedGoogle Scholar
  14. 14.
    Schauer, R.: Sialic acids as link to Japanese scientists. Proc Jpn Acad Ser B Phys Biol Sci. 92, 109–120 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Buschiazzo, A., Alzari, P.M.: Sialic acid metabolism structural insights into sialic acid enzymology. Curr. Opin. Chem. Biol. 12, 565–572 (2008)CrossRefPubMedGoogle Scholar
  16. 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)CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Roth, J., Kempf, A., Reuter, G., Schauer, R., Gehring, W.J.: Occurrence of sialic acids in drosophila melanogaster. Science. 256, 673–675 (1992)CrossRefPubMedGoogle Scholar
  18. 18.
    Warren, L.: The distribution of sialic acids in nature. Comp. Biochem. Physiol. 10, 153–171 (1963)CrossRefPubMedGoogle Scholar
  19. 19.
    Marchal, I., Jarvis, D.L., Cacan, R., Verbert, A.: Glycoproteins from insect cells: sialylated or not? Biol. Chem. 382, 151–159 (2001)CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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)CrossRefPubMedGoogle Scholar
  21. 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)CrossRefPubMedGoogle Scholar
  22. 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)CrossRefPubMedGoogle Scholar
  23. 23.
    Ghosh, S.: Sialic acids: biomarkers in endocrinal cancers. Glycoconj. J. 32(3–4), 79–85 (2015 May)CrossRefPubMedGoogle Scholar
  24. 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)CrossRefPubMedGoogle Scholar
  25. 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)CrossRefPubMedGoogle Scholar
  26. 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)CrossRefPubMedGoogle Scholar
  27. 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, 16Google Scholar
  28. 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)CrossRefPubMedGoogle Scholar
  29. 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)CrossRefPubMedGoogle Scholar
  30. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Scott, H., Panin, V.M.: The role of protein N-glycosylation in neural transmission. Glycobiology. 24, 407–417 (2014)CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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)CrossRefPubMedGoogle Scholar
  33. 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 Google Scholar
  34. 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)CrossRefPubMedGoogle Scholar
  35. 35.
    Koles, K., Irvine, K.D., Panin, V.M.: Functional characterization of Drosophila sialyltransferase. J. Biol. Chem. 279, 4346–4357 (2004)CrossRefPubMedGoogle Scholar
  36. 36.
    Repnikova E., Koles K., Nakamura M., Pitts J., Li H., et al. , 2010. Sialyltransferase regulates nervous system function in Drosophila. J. Neurosci. 30: 6466–6476CrossRefPubMedGoogle Scholar
  37. 37.
    Haines, N., Irvine, K.D.: Functional analysis of Drosophila beta1,4-N-acetlygalactosaminyltransferases. Glycobiology. 15, 335–346 (2005)CrossRefPubMedGoogle Scholar
  38. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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: 653–656Google Scholar
  40. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Zhang, Y.: I-TASSER server for proteins 3D structure prediction. BMC Bioinformatics. 9, 40 (2008)CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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)Google Scholar
  43. 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)PubMedGoogle Scholar
  44. 44.
    Hollister, J., Conradt, H., Jarvis, D.L.: Evidence for a sialic acid salvaging pathway in lepidopteran insect cells. Glycobiology. 13, 487–495 (2003)CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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)CrossRefPubMedGoogle Scholar
  46. 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)CrossRefGoogle Scholar
  47. 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)CrossRefPubMedGoogle Scholar
  48. 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)CrossRefPubMedGoogle Scholar
  49. 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)CrossRefPubMedGoogle Scholar
  50. 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)CrossRefPubMedGoogle Scholar
  51. 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)CrossRefPubMedGoogle Scholar
  52. 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)CrossRefPubMedGoogle Scholar
  53. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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)CrossRefPubMedGoogle Scholar
  55. 55.
    Viswanathan, K., Narang, S., Betenbaugh, M.J.: Engineering Sialic Acid Synthesis Ability in Insect Cells. Methods Mol. Biol. 1321, 171–178 (2015)CrossRefPubMedGoogle Scholar
  56. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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)CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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)CrossRefPubMedGoogle Scholar
  59. 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)PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological SciencesNational Institute of Science Education and Research (NISER)BhubaneswarIndia
  2. 2.Homi Bhabha National InstituteAnushakti NagarIndia

Personalised recommendations