Determination of sialic acids in the nervous system of silkworm (<i>Bombyx mori</i>L.): effects of aging and development

Authors

  • Seçkin Soya Ege University, Faculty of Science, Department of Biology, Molecular Biology Section
  • Umut Şahar Ege University, Faculty of Science, Department of Biology, Molecular Biology Section
  • Mehmet Salih Yıkılmaz Ege University, Faculty of Science, Department of Biology, Molecular Biology Section
  • Sabire Karaçalı Ege University, Faculty of Science, Department of Biology, Molecular Biology Section

Keywords:

Sialic acids, nervous system, capLC-ESI-MS/MS, lectin immunohistochemistry, development, aging

Abstract

Sialic acids mainly occur as components on cell surface glycoproteins and glycolipids. They play a major role in the chemical and biological diversity of glycoconjugates. Although sialic acids exhibit great structural variability in vertebrates, glycoconjugates with sialic acids have also been determined in small amounts in invertebrates. It has been suggested that sialic acids play important roles in the development and function of the nervous system. Despite Bombyx mori being a model organism for the investigation of many physiological processes, sialic acid changes in its nervous system have not been examined during development and aging. Therefore, in this study we aimed to determine sialic acid changes in the nervous system of Bombyx mori during development and aging processes. Liquid chromatography-mass spectrometry (LC-MS) and lectin immunohistochemistry were carried out in order to find variations among different developmental stages. Developmental stages were selected as 3rd instar (the youngest) and 5th larval instar (young), motionless prepupa (the oldest) and 13-day-old pupa (adult development). At all stages, only Neu5Ac was present, however, it dramatically decreased during the developmental and aging stages. On the other hand, an increase was observed in the amount of Neu5Ac during the pupal stage. In immunohistochemistry experiments with Maackia amurensis agglutinin (MAA) and Sambucus nigra agglutinin (SNA) lectins, the obtained staining was consistent with the obtainedLC-MS results. These findings indicate that sialic acids are abundant at the younger stages but that they decrease in the insect nervous system during development and aging, similarly as in mammals.

https://doi.org/10.2298/ABS160401117S

Received: April 1, 2016; Revised: May 13, 2016; Accepted: June 10, 2016; Published online: November 30, 2016

How to cite this article: Soya S, Şahar U, Yıkılmaz MS, Karaçalı S. Determination of sialic acids in the nervous system of silkworm (Bombyx mori L.): Effects of aging and development. Arch Biol Sci. 2017;69(2):369-78.

Downloads

Download data is not yet available.

References

Varki A. Diversity in the sialic acids. Glycobiology. 1992;2:25-40.

Schauer R, Kamerling JP. Chemistry, biochemistry and biology of sialic acids. In: Montreuil J, Vliegenthart JFG, Schachter H, editors. Glycoproteins II. Amsterdam: Elsevier; 1997. p. 243-402.

Schauer R. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 2009;19:507-14.

Yu RK, Schengrund CL. Glycobiology of the Nervous System. New York: Springer; 2014. 590p.

Schauer R. Sialic acids: fascinating sugars in higher animals and man. Zoology. 2004;107 (1):49-64.

Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. Essentials of Glycobiology. 2nd ed. New York: Cold Spring Harbor Laboratory Press; 2009. 653p.

Schnaar RL, Gerardy-Schahn R, Hildebrandt H. Sialic acids in the brain: Gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev. 2014;94:461-518.

Schauer R. Achievements and challenges in sialic acid research. Glycoconj J. 2000a;17:485-99.

Schauer R. Biochemistry of sialic acid diversity. In: Carbohydrates in Chemistry and Biology 2000b;3:227-43.

Ando S. Glycoconjugate changes in aging and age-related diseases. In: Yu RK, Schengrund CL, editors. Glycobiology of the nervous system. New York: Springer; 2014. p. 415-48.

Murrey HE, Hsieh-Wilson LC. The chemical neurobiology of carbohydrates. Chem Rev. 2008;108:1708-31.

Varki A, Gagneux, P. Multifarious roles of sialic acids in immunity. Ann NY Acad Sci. 2012;1253:16-36.

Park JJ, Lee M. Increasing the α2,6 sialylation of glycoproteins may contribute to metastatic spread and therapeutic resistance in colorectal cancer. Gut Liver. 2013;7(6):629-41.

Büll C, Stoel MA, den Brok MH, Adema GJ. Sialic acids sweeten a tumor's life. Cancer Res. 2014;74(12):3199-204.

Karaçalı S, İzzetoğlu S, Deveci R. Glycosylation changes leading to the increase in size on the common core of N-glycans, required enzymes, and related cancer-associated proteins. Turk J Biol. 2014;38:754-71.

Corfield AP, Williams AJK, Clamp JR, Wagner SA, Mountford RA. Degradation by bacterial enzymes of colonic mucus from normal subjects and patients with inflammatory bowel disease: the role of sialic acid metabolism and the detection of a novel O-acetylsialic acid esterase. Clin Sci. 1988;74:71-8.

Dimitrovy JD, Bayryy J, Siberil S, Kaveri SV. Sialylated therapeutic IgG: a sweet remedy for inflammatory diseases? Nephrol Dial Transplant. 2007;22:1301-4.

Böhm S, Schwab I, Lux A, Nimmerjahn F. The role of sialic acid as a modulator of the anti-inflammatory activity of IgG. Semin Immunopathol. 2012;34:443-53.

Schnaar RL. Glycans and glycan binding proteins in immune regulation: A concise introduction to glycobiology for the allergist. J Allergy Clin Immunol. 2015;135(3):609-15.

Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, Wiley DC. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature. 1988;333(6172):426-31.

Isa P, Arias CF, López S. Role of sialic acids in rotavirus infection. Glycoconj J. 2006;23(1-2):27-37.

Huberman K, Peluso RW, Moscona A. Hemagglutinin-neuraminidase of human parainfluenza 3: role of the neuraminidase in the viral life cycle. Virology. 1995;214:294- 300.

Neu U, Bauer J, Stehle T. Viruses and sialic acids: rules of engagement. Curr Opin Struct Biol. 2011;21(5):610-8.

van Breedam W, Pöhlmann S, Favoreel HW, de Groot RJ, Nauwynck HJ. Bitter-sweet symphony: glycan-lectin interactions in virus biology. FEMS Microbiol Rev. 2014;38(4):598-632.

Stencel-Baerenwald JE, Reiss K, Reiter DM, Stehle T, Dermody TS. The sweet spot: defining virus-sialic acid interactions. Nat Rev Microbiol. 2014;12:739-49.

Wang B, Brand-Miller J. The role and potential of sialic acid in human nutrition. Eur J Clin Nutr. 2003;57(11):1351-69.

Varki A. Uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci USA. 2010;107(2):8939-46.

Inoue S, Kitajima K. KDN (deaminatedneuraminic acid): dreamful past and exciting future of the newest member of the sialic acid family. Glycoconj J. 2006;23(5-6):277-90.

Davies LR, Varki A. Why is N-glycolylneuraminic acid rare in the vertebrate brain? Top Curr Chem. 2015;366:31-54.

Warren L. The distribution of sialic acids in nature. Comp Biochem Physiol. 1963;10:153-71.

Corfield AP, Schauer R. Occurrence of sialic acids. In: Schauer, R, editor. Sialic Acids: Chemistry, Metabolism and Function. Wien, New York: Springer-Verlag; 1982. p 5-50 (Cell Biology Monographs, vol. 10).

Gollub M, Shaw L. Isolation and characterization of cytidine-5'-monophosphate-N-acetylneuraminate hydroxylase from the starfish Asterias rubens. Comp Biochem Physiol B Biochem Mol Biol. 2003;134(1):89-101.

İzzetoğlu S, Şahar U, Şener E, Deveci R. Determination of sialic acids in immune system cells (coelomocytes) of sea urchin, Paracentrotus lividus, using capillary LC-ESI-MS/MS. Fish Shellfish Immunol. 2014;36(1):181-6.

Roth J, Kempf A, Reuter G, Schauer R, Gehring WJ. Occurrence of sialic acids in Drosophila melanogaster. Science. 1992;256(5057):673-75.

Aoki K, Perlman M, Lim J, Cantu R, Wells L, Tiemeyer M. Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J Biol Chem. 2007;282:9127-42.

Koles K, Lim JM, Aoki K, Porterfield M, Tiemeyer M, Wells L and Panin VM. Identification of N-glycosylated proteins from the central nervous system of Drosophila melanogaster. Glycobiology. 2007;17:1388-403.

Koles K, Repnikova E, Pavlova G, Korochkin LLI, Panin VM. Sialylation in protostomes: a perspective from Drosophila genetics and biochemistry. Glycoconj J. 2009;26:313-24.

Repnikova E, Koles K, Nakamura M, Pitts J, Li H, Ambavane A, Zoran MJ, Panin VM. Sialyltransferase regulates nervous system function in Drosophila. J Neurosci. 2010;30(18):6466-76.

Islam R, Nakamura M, Scott H, Repnikova E, Carnahan M, Pandey D, Caster C, Khan S, Zimmermann T, Zoran MJ and Panin VM. The role of Drosophila cytidine monophosphate-sialic acid synthetase in the nervous system. J Neurosci. 2013;33(30):12306-15.

Malykh YN, Schauer R, Shaw L. N-Glycolylneuraminic acid in human tumours. Biochimie. 2001;83:623-634.

Karaçalı S, Kırmızıgül S, Deveci R and Deveci Ö. Presence of sialic acid in the hemolymph of Dociostaurus maroccanus Thun. (Orthoptera: Acrididae). Invertebr Reprod Dev. 2003;43(2):91-4.

Karaçalı S, Deveci Ö, Deveci R, Onat T, Gürcü B. Spectrophotometrical determination of sialic acid in several tissues of isolated and crowded Locusta migrotoria (Orthoptera). İst Üniv Fen Fak Biy Der. 1995a;58:47-57.

Karaçalı S, Deveci R, Deveci Ö, Onat T, Gürcü B. Spectrophotometrical determination of sialic acid in the tissues of Galleria mellonella (Lepidoptera). İst Üniv Fen Fak Biy Der. 1995b;58:59-67.

Karaçalı S, Kırmızıgül S, Deveci R, Deveci Ö, Onat T, Gürcü B. Presence of sialic acid in prothoracic glands of Galleria mellonella (Lepidoptera). Tissue Cell. 1997;29:315-21.

Karaçalı S, Deveci R, Pehlivan S, Özcan A. Adhesion of hemocytes to desialylated prothoracic glands of Galleria mellonella (Lepidoptera) in larval stage. Invertebr Reprod Dev. 2000;37(2):167-70.

Karaçalı S, Kırmızıgül S, Deveci R. Sialic acids in developing testis of Galleria mellonella (Lepidoptera). Invertebr Reprod Dev. 1999;35(3):225-9.

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

Shah MM, Fujiyama K, Flynn CR, Joshi L. Sialylated endogenous glycoconjugates in plant cells. Nat Biotechnol. 2003;21:1470 - 71.

Seveno M, Bardor M, Paccalet T, Gomord V, Lerouge P, Faye L. Glycoprotein sialylation in plants? Nat Biotechnol. 2004;22:5-6.

Kleene R, Schachner M. Glycans and neural cell interactions. Nat Rev Neurosci. 2004;5:195-208.

Murrey HE, Gama CI, Kalovidouris SA, Luo WI, Driggers EM, Porton B, Hsieh-Wilson LC. Protein fucosylation regulates synapsinIa/Ib expression and neuronal morphology in primary hippocampal neurons. Proc Natl Acad Sci USA. 2006;103:21-6.

Scott H, Panin VM. The role of protein N-glycosylation in neural transmission. Glycobiology. 2014;24(5):407-17.

Yoo SW, Motari MG, Susuki K, Prendergast J, Mountney A, Hurtado A, Schnaar RL. Sialylation regulates brain structure and function. FASEB J. 2015;29(7):3040-53.

Sandi C, Rose SPR, Mileusnic R, Lancashire C. Corticosterone facilitates long-term memory formation via enhanced glycoprotein synthesis. Neuroscience. 1995;69:1087-93.

Salinska E, Bourne RC, Rose SPR. Reminder effects: the molecular cascade following a reminder in young chicks does not recapitulate that following training on a passive avoidance task. Eur J Neurosci. 2004;19:3042-47.

Sørensen LK. Determination of sialic acids in infant formula by liquid chromatography tandem mass spectrometry. Biomed Chromatogr. 2010;24,1208-12.

Brunngraber EG, Witting LA, Haberland C, Brown B. Glycoproteins in Tay-sachs disease: isolation and carbohydrate composition of glycopeptides. Brain Res. 1972; 38: 151-62.

McMaster MC. LC/MS: A Practical User’s Guide. 1st ed. New Jersey: Wiley and Sons; 2005. p. 184.

Yuriev E, Ramsland PA. Structural Glycobiology. Boca Raton: Taylor and Francis; 2013. p 347.

Sasaki T, Akimoto Y, Sato Y, Kawakami H, Hirano H, Endo T. Distribution of sialoglycoconjugates in the rat cerebellum and its change with aging. J Histochem Cytochem. 2002;50(9):1179-86.

Gabius HJ, Gabius S. Lectins and Glycobiology. Tokyo: Springer-Verlag; 1993. p 521.

Brooks SA, Leathem A.Expression of N-acetyl galactosaminylated and sialylated glycans by metastases arising from primary breast cancer. Invasion Metastasis. 1998;18(3):115-21.

Vijayan M, Chandra N. Lectins. Curr Opin Struct Biol. 1999;9(6):707-14.

Duverger E, Frison N, Roche AC, Monsigny M. Carbohydrate-lectin interactions assessed by surface plasmon resonance. Biochimie. 2003;85(1-2):167-79.

Hirabayashi J. Lectins: Methods and Protocols. New York: Humana Press; 2014. p 613.

Rossenberg A. Biology of the Sialic Acids. New York: Springer; 1995. p 378.

Grimaldi D, Engel MS. Evolution of the insects. Cambridge: University Press; 2005. p 772.

Goldsmith MR, Marec F. Molecular Biology and Genetics of the Lepidoptera. Boca Raton: CRC Press; 2010. p 368.

Klein A, Diaz S, Ferreira I, Lamblin G, Roussel P, Manzi AE. New sialic acids from biological sources identified by a comprehensive and sensitive approach: liquid chromatography-electrospray ionization-mass spectrometry (LC-ESI/MS) of SIA quinoxalinones. Glycobiology. 1997;7(3):421-32.

Kamerling J, Gerwig GJ. Structural analysis of naturally occurring sialic acids. In: Brockhausen I, editor. Glycobiology Protocols. New York: Humana Press; 2007. p. 69-91.

Izzetoğlu S, Karaçalı S. The determination of N-acetylneuraminic acid (Neu5Ac) and N-glycolyl-neuraminic acid (Neu5Gc) types of sialic acids in hematopoietic organ of the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae). Kafkas Univ Vet Fak Derg. 2012;18(1):147-50.

Lopez LL, Tiller PR, Senko MW, Schwartz JC. Automated strategies for obtaining standardized collisionally induced dissociation spectra on a benchtop ion trap mass spectrometer. Rapid Commun. Mass Spectrom. 1999;13:663-8.

Yesilyurt B, Sahar U, Deveci R. Determination of the type and quantity of sialic acid in the egg jelly coat of the sea urchin Paracentrotus lividus using capillary LC-ESI-MS/MS. Mol Reprod Dev. 2015;82:115-22.

Pipa RL. Studies on the hexapod nervous system.VII. Ventral nerve cord shortening; a metamorphic process in Galleria mellonella (L.). Z. Zellforsch Mikrosk Anat. 1963;63:405-17.

Jakubowska-Solarska J, Solski J. Sialic acids of young and old red blood cells in healthy subjects. Med Sci Monit. 2000;6(5):871-4.

Gheri G, Noci I, Sgambati E, Borri P, Taddei G, Bryk SG. Ageing of the human oviduct: lectin histochemistry. Histol Histopathol. 2001;16:21-8.

Uslu E, KaragözGüzey F, Oguz E, Güzey D. The effects of ageing on brain tissue sialic acid contents following cold trauma. Acta Neurochirurgica. 2004;146(12):1337-40.

Sprenger N, Julita M, Donnicola D, Jann A. Sialic acid feeding aged rats rejuvenates stimulated salivation and colon enteric neuron chemotypes. Glycobiology. 2009;19(12):1492-502.

Huang YX, Wu ZJ, Mehrishi J, Huang BT, Chen XY, Zheng XJ, Liu WJ, Luo M. Human red blood cell aging: correlative changes in surface charge and cell properties. J Cell Mol Med. 2011;15(12):2634-42.

Sprenger N, Duncan PI. Sialic Acid Utilization. Adv Nutr. 2012;3:392S-397S.

Cakatay U, Aydın S, Atukeren P, Yanar K, Sitar ME, Dalo E, Uslu E. Increased protein oxidation and loss of protein-bound sialic acid in hepatic tissues of D-galactose induced aged rats. Curr Aging Sci. 2013;6(2):135-41.

Dall'Olio F, Vanhooren V, Chen CC, Slagboom PE, Wuhrer M, Franceschi C. N-glycomic biomarkers of biological aging and longevity: a link with inflammaging. Ageing Res Rev. 2013;12(2):685-98.

Hanisch F, Weidemann W, Großmann M, Joshi PR, Holzhausen HJ, Stoltenburg G, Weis J, Zierz S, Horstkorte R.. Sialylation and muscle performance: sialic acid is a marker of muscle ageing. PLoS One. 2013;8(12):e80520.

Üstündağ ÜV, Oktay Ş, Emekli-Alturfan E, Alturfan AA, Yanar K, Mengi M, Cebe T, Aydın S, Çakatay U. D-Galaktozile oluşturulmuş yaşlanma modelinde doku faktörü aktivitesinin ve sialik asit miktarının değerlendirilmesi. MÜSBED. 2014;4(1):5-9.

Huang YX, Tuo WW, Wang D, Kang LL, Chen XY, Luo M. Restoring the youth of aged red blood cells and extending their lifespan in circulation by remodelling membrane sialic acid. J Cell Mol Med. 2016;20(2):294-301.

Sato Y, Kimura M, Endo T. Comparison of lectin-binding patterns between young adult and older rat glycoproteins in the brain. Glycoconj J. 1998;15:1133-1140.

Sarıbek B, Erden S, Karaçalı S. Determination of α-2,6 sialic acid in developmental stages of Galleria mellonella (Lepidoptera). Invertebr Reprod Dev. 2009;53:145-52.

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. 2015;25(12):1441-53.

North SJ, Koles K, Hembd C, Morris HR, Dell A, Panin VM, Haslam SM. Glycomics studies of Drosophila melanogaster embryos. Glycoconj J. 2006;23:345-54.

Park YI, Wood HA, Lee YC. Monosaccharide compositions of Danaus plexippus (monarch butterfly) and Trichoplusia ni (cabbage looper) egg glycoproteins. Glycoconj J. 1999;16(10):629-38.

Marini M, Ambrosini S, Sarchielli E, Thyrion GD, Bonaccini L, Vannelli GB, Sgambati E. Expression of sialic acids in human adult skeletal muscle tissue. Acta Histochem. 2014;116(5):926-35.

Downloads

Published

2017-05-25

How to Cite

1.
Soya S, Şahar U, Yıkılmaz MS, Karaçalı S. Determination of sialic acids in the nervous system of silkworm (&lt;i&gt;Bombyx mori&lt;/i&gt;L.): effects of aging and development. Arch Biol Sci [Internet]. 2017May25 [cited 2024Apr.18];69(2):369-78. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/406

Issue

Section

Articles