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Sialyltransferase, Sialylation, and Sulfoylation

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Ganglioside Biochemistry

Abstract

Sialyl-glycoconjugates are associated with various life processes including cellular responses of fertilization, development, differentiation, transformation, tumor metastasis, and inflammation. The sialyl-carbohydrates are key molecules in cellular recognition and cell–pathogen interaction. To synthesize the sialyl-glycoconjugates, sialyltransferases (STs) transfer SA residues from donor substrates to acceptors (Fig. 3.1). The naturally occurring SAs are structurally diverse due to its modification in its carbon position. The carbon no. 2 is the anomeric position. For example, in GD3 O-acetylation, 9-O acetylated GDs are found in most tissues except for thymus, placenta, and certain T cells. 9-O and 7-O acetylated are found in certain cell types of differentiation or leukemic cells (Fig. 3.2).

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References

  1. Lee YC, Kurosawa N, Hamamoto T, Nakaoka T, Tsuji S (1993) Molecular cloning and expression of Gal beta 1,3GalNAc alpha 2,3-sialyltransferase from mouse brain. Eur J Biochem 216:377–385

    CAS  PubMed  Google Scholar 

  2. Lee KY, Kim HG, Hwang MR, Chae JI, Yang JM, Lee YC, Choo YK, Lee YI, Lee SS, Do SI (2002) The Hexapeptide inhibitor of Galbeta 1,3GalNAc-specific alpha 2,3-sialyltransferase as a generic inhibitor of sialyltransferases. J Biol Chem 277(51):49341–49351

    CAS  PubMed  Google Scholar 

  3. Lee YC, Kojima N, Wada E, Kurosawa N, Nakaoka T, Hamamoto T, Tsuji S (1994) Cloning and expression of cDNA for a new type of Gal beta 1,3GalNAc alpha 2,3-sialyltransferase. J Biol Chem 269:10028–10033

    CAS  PubMed  Google Scholar 

  4. Kim YJ, Kim KS, Kim SH, Kim CH, Ko JH, Choe IS, Tsuji S, Lee YC (1996) Molecular cloning and expression of human Gal beta 1,3GalNAc alpha 2,3-sialytransferase (hST3Gal II). Biochem Biophys Res Commun 228(2):324–327

    CAS  PubMed  Google Scholar 

  5. Kim KW, Kim KS, Kim CH, Kim JK, Lee YC (1999) Molecular cloning and sequence analysis of human GM3 synthase (hST3Gal V). J Biochem Mol Biol 32:409–413

    CAS  Google Scholar 

  6. Kim SW, Lee SH, Kim KS, Kim CH, Choo YK, Lee YC (2002) Isolation and characterization of the promoter region of the human GM3 synthase gene. Biochim Biophys Acta 1578:84–89

    CAS  PubMed  Google Scholar 

  7. Lee YC, Kaufmann M, Kitazume-Kawaguchi S, Kono M, Takashima S, Kurosawa N, Liu H, Pircher H, Tsuji S (1999) Molecular cloning and functional expression of two members of mouse NeuAcalpha2,3Galbeta1,3GalNAc GalNAcalpha2,6-sialyltransferase family, ST6GalNAc III and IV. J Biol Chem 274:11958–11967

    CAS  PubMed  Google Scholar 

  8. Ko HK, Song KH, Jin UH, Seong HH, Chang YC, Kim NH, Kim DS, Lee YC, Kim CH (2010) Molecular characterization of pig alpha2,3-Gal-beta1,3-GalNAc-alpha2,6-sialyltransferase (pST6GalNAc IV) gene specific for Neu5Acalpha2-3Galbeta1-3GalNAc trisaccharide structure. Glycoconj J 27(3):367–374

    CAS  PubMed  Google Scholar 

  9. Lee YC, Kim SW, Kim KS, Min KS, Kim CH (2001) Molecular cloning and substrate specificity of human NeuAc 2,3Gal 1,3GalNAc GalNac 2,6-Sialyltransferase (hST6GalNac IV). J Life Sci 11:57–64

    Google Scholar 

  10. Lee YC, Kim YJ, Lee KY, Kim KS, Kim BU, Kim HN, Kim CH, Do SI (1998) Cloning and expression of cDNA for a human Sia alpha 2,3Gal beta 1, 4GlcNA:alpha 2,8-sialyltransferase (hST8Sia III). Arch Biochem Biophys 360:41–46

    CAS  PubMed  Google Scholar 

  11. Kim YJ, Kim KS, Do S, Kim CH, Kim SK, Lee YC (1997) Molecular cloning and expression of human alpha2,8-sialyltransferase (hST8Sia V). Biochem Biophys Res Commun 235:327–330

    CAS  PubMed  Google Scholar 

  12. Jeanneau C, Chazalet V, Augé C, Soumpasis DM, Harduin-Lepers A, Delannoy P, Imberty A, Breton C (2004) Structure-function analysis of the human sialyltransferase ST3Gal I: role of n-glycosylation and a novel conserved sialylmotif. J Biol Chem 279(14):13461–13468

    CAS  PubMed  Google Scholar 

  13. Sjoberg ER, Powell LD, Klein A, Varki A (1994) Natural ligands of the B cell adhesion molecule CD22 beta can be masked by 9-O-acetylation of sialic acids. J Cell Biol 126(2):549–562

    CAS  PubMed  Google Scholar 

  14. Boonsuk P, Payungporn S, Chieochansin T et al (2008) Detection of influenza virus types A and B and type A subtypes (H1, H3, and H5) by multiplex polymerase chain reaction. Tohoku J Exp Med 215(3):247–255

    CAS  PubMed  Google Scholar 

  15. Gnanesh Kumar BS, Surolia A (2016) Site specific N-glycan profiling of NeuAc(α2-6)-Gal/GalNAc-binding bark Sambucus nigra agglutinin using LC-MSn revealed differential glycosylation. Glycoconj J 33(6):907–915

    CAS  PubMed  Google Scholar 

  16. Koles K, Irvine KD, Panin VM (2004) Functional characterization of Drosophila sialyltransferase. J Biol Chem 279(6):4346–4357

    CAS  PubMed  Google Scholar 

  17. Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328(2):307–317

    CAS  PubMed  Google Scholar 

  18. Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P (2001) The human sialyltransferase family. Biochimie 3(8):727–737

    Google Scholar 

  19. Harduin-Lepers A, Mollicone R, Delannoy P, Oriol R (2005) The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 15:805–817

    CAS  PubMed  Google Scholar 

  20. Rohfritsch PF, Joosten JA, Krzewinski-Recchi MA, Harduin-Lepers A, Laporte B, Juliant S, Cerutti M, Delannoy P, Vliegenthart JF, Kamerling JP (2006) Probing the substrate specificity of four different sialyltransferases using synthetic beta-D-Galp-1,4-beta-D-GlcpNAc-1,2-alpha-D-Manp-1,O (CH2)7CH3 analogues general activating effect of replacing N-acetylglucosamine by N-propionylglucosamine. Biochim Biophys Acta 1760(4):685–692

    CAS  PubMed  Google Scholar 

  21. Schultz MJ, Holdbrooks AT, Chakraborty A et al (2016) The tumor-associated glycosyltransferase ST6Gal-I regulates stem cell transcription factors and confers a cancer stem cell phenotype. Cancer Res 76(13):3978–3988

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Hsieh CC et al (2017) Elevation of beta-galactoside alpha2,6-sialyltransferase 1 in a fructose responsive manner promotes pancreatic cancer metastasis. Oncotarget 8:7691–7709

    PubMed  Google Scholar 

  23. Nakano M, Saldanha R, Göbel A, Kavallaris M, Packer NH (2011) Identification of glycan structure alterations on cell membrane proteins in desoxyepothilone B resistant leukemia cells. Mol Cell Proteomics 10(11):M111

    PubMed  PubMed Central  Google Scholar 

  24. Swindall AF, Bellis SL (2011) Sialylation of the Fas death receptor by ST6Gal-I provides protection against Fas-mediated apoptosis in colon carcinoma cells. J Biol Chem 286(26):22982–22990

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Swindall AF, Londoño-Joshi AI, Schultz MJ, Fineberg N, Buchsbaum DJ, Bellis SL (2013) ST6Gal-I protein expression is upregulated in human epithelial tumors and correlates with stem cell markers in normal tissues and colon cancer cell lines. Cancer Res 73(7):2368–2378

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Lu J, Isaji T, Im S, Fukuda T, Hashii N, Takakura D, Kawasaki N, Gu J (2014) beta-Galactoside alpha2,6-sialyltranferase 1 promotes transforming growth factor-beta-mediated epithelial-mesenchymal transition. J Biol Chem 289(50):34627–34641

    PubMed  PubMed Central  Google Scholar 

  27. Yuan Q, Chen X, Han Y et al (2018) Modification of alpha2,6-sialylation mediates the invasiveness and tumorigenicity of non-small cell lung cancer cells in vitro and in vivo via. Notch1/Hes1/MMPs Pathway 143(9):2319–2330

    CAS  Google Scholar 

  28. Venturi G, Ferreira IG, Pucci M, Ferracin M, Malagolini N, Chiricolo M, Dall'Olio F (2019) Impact of sialyltransferase ST6GAL1 overexpression on different colon cancer cell types. Glycobiology 29:684–695

    CAS  PubMed  Google Scholar 

  29. Zhou L, Zhang S, Zou X et al (2019) The beta-galactoside alpha2,6-sialyltranferase 1 (ST6GAL1) inhibits the colorectal cancer metastasis by stabilizing intercellular adhesion molecule-1 via sialylation. Cancer Manag Res 11:6185–6199

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Jun L, Yuanshu W, Yanying X et al (2012) Altered mRNA expressions of sialyltransferases in human gastric cancer tissues. Med Oncol 29(1):84–90

    PubMed  Google Scholar 

  31. Gao X, Wang X (2017) Effects of Taxol on proliferation, apoptosis, and mRNA expression of α2, 6-sialic acid and ST6Gal in cervical carcinoma cell line U14. Chin J Pathophysiol 33(6):1038–1042

    Google Scholar 

  32. Dall’Olio F, Mariani E, Tarozzi A et al (1997) Expression of beta-galactoside alpha 2,6-sialyltransferase does not alter the susceptibility of human colon cancer cells to NK-mediated cell lysis. Glycobiology 7(4):507–513

    PubMed  Google Scholar 

  33. Jones MB, Nasirikenari M, Lugade AA, Thanavala Y, Lau JT (2012) Anti-inflammatory IgG production requires functional P1 promoter in β-galactoside α2,6-sialyltransferase 1 (ST6Gal-1) gene. J Biol Chem 287(19):15365–15370

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Taniguchi A, Hasegawa Y, Higai K, Matsumoto K (2000) Transcriptional regulation of human beta-galactoside alpha2, 6-sialyltransferase (hST6Gal I) gene during differentiation of the HL-60 cell line. Glycobiology 10(6):623–628

    CAS  PubMed  Google Scholar 

  35. Christie DR, Shaikh FM, Lucas JA 4th, Lucas JA 3rd, Bellis SL (2008) ST6Gal-I expression in ovarian cancer cells promotes an invasive phenotype by altering integrin glycosylation and function. J Ovarian Res 1(1):3

    PubMed  PubMed Central  Google Scholar 

  36. Maksimovic J, Sharp JA, Nicholas KR, Cocks BG, Savin K (2011) Conservation of the ST6Gal I gene and its expression in the mammary gland. Glycobiology 21(4):467–481

    CAS  PubMed  Google Scholar 

  37. Vázquez-Martín C, Cuevas E, Gil-Martín E, Fernández-Briera A (2004) Correlation analysis between tumor-associated antigen sialyl-Tn expression and ST6GalNAc I activity in human colon adenocarcinoma. Oncology 67(2):159–165

    PubMed  Google Scholar 

  38. Appenheimer MM, Huang RY, Chandrasekaran EV et al (2003) Biologic contribution of P1 promoter-mediated expression of ST6Gal I sialyltransferase. Glycobiology 13(8):591–600

    CAS  PubMed  Google Scholar 

  39. Milflores-Flores L, Millán-Pérez L, Santos-López G, Reyes-Leyva J, Vallejo-Ruiz V (2012) Characterization of P1 promoter activity of the beta-galactoside alpha2,6-sialyltransferase I gene (siat 1) in cervical and hepatic cancer cell lines. J Biosci 37(2):259–267

    CAS  PubMed  Google Scholar 

  40. Lu J, Isaji T, Im S, Fukuda T, Hashii N, Takakura D, Kawasaki N, Gu J (2014) Beta-galactoside alpha2,6-sialyltranferase 1 promotes transforming growth factor-beta-mediated epithelial-mesenchymal transition. J Biol Chem 289:34627–34641

    PubMed  PubMed Central  Google Scholar 

  41. Maksimovic J, Sharp JA, Nicholas KR, Cocks BG, Savin K (2011) Conservation of the ST6Gal I gene and its expression in the mammary gland. Glycobiology 21(4):467–481

    CAS  PubMed  Google Scholar 

  42. Petit D, Mir A-M, Petit J-M et al (2010) Molecular phylogeny and functional genomics of β-Galactoside α2, 6-Sialyltransferases that explain ubiquitous expression of ST6GAL1 gene in amniotes. J Biol Chem 285(49):38399–38414

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Liang L, Xu J, Wang M et al (2018) LncRNA HCP5 promotes follicular thyroid carcinoma progression via miRNAs sponge. Cell Death Dis 9(3):372

    PubMed  PubMed Central  Google Scholar 

  44. Castellana B, Escuin D, Peiro G (2012) ASPN and GJB2 are implicated in the mechanisms of invasion of ductal breast carcinomas. J Cancer 3:175

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Laporte B, Gonzalez-Hilarion S, Maftah A, Petit JM (2009) The second bovine beta-galactoside-alpha2,6-sialyltransferase (ST6Gal II): genomic organization and stimulation of its in vitro expression by IL-6 in bovine mammary epithelial cells. Glycobiology 19(10):1082–1093

    CAS  PubMed  Google Scholar 

  46. Harduin-Lepers A, Stokes DC, Steelant WF, Samyn-Petit B (2000) Cloning, expression and gene organization of a human Neu5Acɑ2-3Galβ1-3GalNAcɑ2,6-sialyltransferase: hST6GalNAc IV. Biochem J 352(Pt1):37–48

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Lam KK, Chiu PC, Lee CL et al (2011) Glycodelin-A protein interacts with Siglec-6 protein to suppress trophoblast invasiveness by down-regulating extracellular signal-regulated kinase (ERK)/c-Jun signaling pathway. J Biol Chem 286(43):37118–37127

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Rumer KK, Uyenishi J, Hoffman MC, Fisher BM, Winn VD (2013) Siglec-6 expression is increased in placentas from pregnancies complicated by preterm preeclampsia. Reprod Sci 20:646–653

    PubMed  PubMed Central  Google Scholar 

  49. Khoza T, Hosie M (2008) Clomiphene citrate modulates the expression of endometrial carbohydrates (especially N-acetyl-d-glucosamine and sialic acid) in pseudopregnant rats. Theriogenology 70:612–621

    CAS  PubMed  Google Scholar 

  50. Brown HM, Green ES, Tan TCY et al (2018) Periconception onset diabetes is associated with embryopathy and fetal growth retardation, reproductive tract hyperglycosylation and impaired immune adaptation to pregnancy. Sci Rep 8(1):2114

    PubMed  PubMed Central  Google Scholar 

  51. Munkley J (2016) The role of Sialyl-Tn in cancer. Int J Mol Sci 17:275

    PubMed  PubMed Central  Google Scholar 

  52. Choi HJ, Chung TW, Choi HJ, Han JH, Choi JH, Kim CH, Ha KT (2018) Increased α2-6 sialylation of endometrial cells contributes to the development of endometriosis. Exp Mol Med 50(12):164

    CAS  PubMed Central  Google Scholar 

  53. Stanley P (2016) What have we learned from glycosyltransferase knockouts in mice? J Mol Biol 428:3166–3182

    CAS  PubMed  PubMed Central  Google Scholar 

  54. King SL, Joshi HJ, Schjoldager KT, Halim A, Madsen TD, Dziegiel MH et al (2017) Characterizing the O-glycosylation landscape of human plasma, platelets, and endothelial cells. Blood Adv 1:429–442

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Teintenier-Lelièvre M, Julien S, Juliant S, Guerardel Y, Duonor-Cérutti M, Delannoy P, Harduin-Lepers A (2005) Molecular cloning and expression of a human hST8Sia VI (alpha2,8-sialyltransferase) responsible for the synthesis of the diSia motif on O-glycosylproteins. Biochem J 392:665–374

    PubMed  PubMed Central  Google Scholar 

  56. Harduin-Lepers A, Petit D, Mollicone R, Delannoy P, Petit JM, Oriol R (2008) Evolutionary history of the alpha2,8-sialyltransferase (ST8Sia) gene family: tandem duplications in early deuterostomes explain most of the diversity found in the vertebrate ST8Sia genes. BMC Evol Biol 258:8

    Google Scholar 

  57. Pearce OM, Laubli H (2016) Sialic acids in cancer biology and immunity. Glycobiology 26:111–128

    CAS  PubMed  Google Scholar 

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  1. Molecular and Cellular Glycobiology Lab, SungKyunKwan University, Suwon, Korea (Republic of)

    Cheorl-Ho Kim

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Kim, CH. (2020). Sialyltransferase, Sialylation, and Sulfoylation. In: Ganglioside Biochemistry. Springer, Singapore. https://doi.org/10.1007/978-981-15-5815-3_3

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