REVIEW

Sialylation is involved in cell fate decision during development, reprogramming and cancer progression

  • Fenjie Li 1,2 ,
  • Junjun Ding , 1,2
Expand
  • 1. Program in Stem Cell and Regenerative Medicine, The Third Affiliated Hospital of Sun Yat-Sen University, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, China
  • 2. Key Laboratory for Stem Cells and Tissue Engineering, Ministry of Education, Department of Cell Biology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, China

Received date: 06 Oct 2018

Accepted date: 31 Oct 2018

Published date: 15 Aug 2019

Copyright

2018 The Author(s) 2018

Abstract

Sialylation, or the covalent addition of sialic acid to the terminal end of glycoproteins, is a biologically important modification that is involved in embryonic development, neurodevelopment, reprogramming, oncogenesis and immune responses. In this review, we have given a comprehensive overview of the current literature on the involvement of sialylation in cell fate decision during development, reprogramming and cancer progression. Sialylation is essential for early embryonic development and the deletion of UDP-GlcNAc 2-epimerase, a rate-limiting enzyme in sialic acid biosynthesis, is embryonically lethal. Furthermore, the sialyltransferase ST6GAL1 is required for somatic cell reprogramming, and its downregulation is associated with decreased reprogramming efficiency. In addition, sialylation levels and patterns are altered during cancer progression, indicating the potential of sialylated molecules as cancer biomarkers. Taken together, the current evidences demonstrate that sialylation is involved in crucial cell fate decision.

Cite this article

Fenjie Li , Junjun Ding . Sialylation is involved in cell fate decision during development, reprogramming and cancer progression[J]. Protein & Cell, 2019 , 10(8) : 550 -565 . DOI: 10.1007/s13238-018-0597-5

1
Abeln M, Borst KM, Cajic S, Thiesler H, Kats E, Albers I, Kuhn M, Kaever V, Erdmann RB, Munster-Kuhnel A (2017) Sialylation is dispensable for early murine embryonic development in vitro. ChemBioChem 18(13):1305–1316

DOI

2
Angata T, Varki A (2002) Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102(2):439–469

DOI

3
Angata T, Kerr SC, Greaves DR, Varki NM, Crocker PR, Varki A (2002) Cloning and characterization of human Siglec-11. A recently evolved signaling molecule that can interact with SHP-1 and SHP-2 and is expressed by tissue macrophages, including brain microglia. J Biol Chem 277(27):24466–24474

DOI

4
Badr HA, Alsadek DM, Darwish AA, Elsayed AI, Bekmanov BO, Khussainova EM, Zhang X, Cho WC, Djansugurova LB, Li CZ (2014) Lectin approaches for glycoproteomics in FDA-approved cancer biomarkers. Expert Rev Proteomics 11(2):227–236

DOI

5
Baldus SE, Zirbes TK, Monig SP, Engel S, Monaca E, Rafiqpoor K, Hanisch FG, Hanski C, Thiele J, Pichlmaier H (1998) Histopathological subtypes and prognosis of gastric cancer are correlated with the expression of mucin-associated sialylated antigens: Sialosyl-Lewis(a), Sialosyl-Lewis(x) and sialosyl-Tn. Tumour Biol 19(6):445–453

DOI

6
Ballehaninna UK, Chamberlain RS (2012) The clinical utility of serum CA 19-9 in the diagnosis, prognosis and management of pancreatic adenocarcinoma: An evidence based appraisal. J Gastrointest Oncol 3(2):105–119

7
Bhide GP, Colley KJ (2017) Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Histochem Cell Biol 147(2):149–174

DOI

8
Bianconi E, Piovesan A, Facchin F, Beraudi A, Casadei R, Frabetti F, Vitale L, Pelleri MC, Tassani S, Piva F (2013) An estimation of the number of cells in the human body. Ann Human Biol 40(6):463–471

DOI

9
Blix G (1936) Über die Kohlenhydratgruppen des Submaxillarismucins. Hoppe-Seyler's Zeitschrift für physiologische Chemie 240(1–2):43–54

DOI

10
Blix FG, Gottschalk A, Klenk E (1957) Proposed nomenclature in the field of neuraminic and sialic acids. Nature 179(4569):1088

DOI

11
Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330(6004):612–616

DOI

12
Born GV, Palinski W (1985) Unusually high concentrations of sialic acids on the surface of vascular endothelia. Br J Exp Pathol 66(5):543–549

13
Cazet A, Julien S, Bobowski M, Krzewinski-Recchi MA, Harduin-Lepers A, Groux-Degroote S, Delannoy P (2010) Consequences of the expression of sialylated antigens in breast cancer. Carbohydr Res 345(10):1377–1383

DOI

14
Chen X, Varki A (2010) Advances in the biology and chemistry of sialic acids. ACS Chem Biol 5(2):163–176

DOI

15
Chu CS, Lo PW, Yeh YH, Hsu PH, Peng SH, Teng YC, Kang ML, Wong CH, Juan LJ (2014) O-GlcNAcylation regulates EZH2 protein stability and function. Proc Natl Acad Sci USA 111 (4):1355–1360

DOI

16
Close BE, Colley KJ (1998) In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J Biol Chem 273(51):34586–34593

DOI

17
Coates SW, Gurney T Jr, Sommers LW, Yeh M, Hirschberg CB (1980) Subcellular localization of sugar nucleotide synthetases. J Biol Chem 255(19):9225–9229

18
Comb DG, Roseman S (1958) Enzymic synthesis of N-acetyl-Dmannosamine. Biochim Biophys Acta 29(3):653–654

DOI

19
Corfield AP (2015) Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta 1850(1):236–252

DOI

20
Corfield AP, Myerscough N, Warren BF, Durdey P, Paraskeva C, Schauer R (1999) Reduction of sialic acid O-acetylation in human colonic mucins in the adenoma-carcinoma sequence. Glycoconj J 16(6):307–317

DOI

21
Cui HX, Wang H, Wang Y, Song J, Tian H, Xia C, Shen Y (2016) ST3Gal III modulates breast cancer cell adhesion and invasion by altering the expression of invasion-related molecules. Oncol Rep 36(6):3317–3324

DOI

22
Dalziel M, Whitehouse C, McFarlane I, Brockhausen I, Gschmeissner S, Schwientek T, Clausen H, Burchell JM, Taylor-Papadimitriou J (2001) The relative activities of the C2GnT1 and ST3Gal-I glycosyltransferases determine O-glycan structure and expression of a tumor-associated epitope on MUC1. J Biol Chem 276(14):11007–11015

DOI

23
Dao TL, Ip C, Patel J (1980) Serum sialyltransferase and 5’-nucleotidase as reliable biomarkers in women with breast cancer. J Natl Cancer Inst 65(3):529–534

24
Deng LQ, Chen X, Varki A (2013) Exploration of sialic acid diversity and biology using sialoglycan microarrays. Biopolymers 99 (10):650–665

DOI

25
Dickson JJ, Messer M (1978) Intestinal neuraminidase activity of suckling rats and other mammals. Relationship to the sialic acid content of milk. Biochem J 170(2):407–413

DOI

26
Du J, Meledeo MA, Wang Z, Khanna HS, Paruchuri VD, Yarema KJ (2009) Metabolic glycoengineering: sialic acid and beyond. Glycobiology 19(12):1382–1401

DOI

27
Du J, Hong S, Dong L, Cheng B, Lin L, Zhao B, Chen YG, Chen X (2015) Dynamic sialylation in transforming growth factor-beta (TGF-beta)-induced epithelial to mesenchymal transition. J Biol Chem 290(19):12000–12013

DOI

28
Duraker N, Hot S, Polat Y, Hobek A, Gencler N, Urhan N (2007) CEA, CA 19-9, and CA 125 in the differential diagnosis of benign and malignant pancreatic diseases with or without jaundice. J Surg Oncol 95(2):142–147

DOI

29
Eckhardt M, Gerardy-Schahn R (1998) Genomic organization of the murine polysialyltransferase gene ST8SiaIV (PST-1). Glycobiology 8(12):1165–1172

DOI

30
Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819):154–156

DOI

31
Eylar EH, Madoff MA, Brody OV, Oncley JL (1962) The contribution of sialic acid to the surface charge of the erythrocyte. J Biol Chem 237:1992–2000

32
Fleming SC, Smith S, Knowles D, Skillen A, Self CH (1998) Increased sialylation of oligosaccharides on IgG paraproteins–a potential new tumour marker in multiple myeloma. J Clin Pathol 51(11):825–830

DOI

33
Fuster MM, Esko JD (2005) The sweet and sour of cancer: Glycans as novel therapeutic targets. Nat Rev Cancer 5(7):526–542

DOI

34
Gal B, Ruano MJ, Puente R, Garcia-Pardo LA, Rueda R, Gil A, Hueso P (1997) Developmental changes in UDP-N-acetylglucosamine 2-epimerase activity of rat and guinea-pig liver. Comp Biochem Physiol B: Biochem Mol Biol 118(1):13–15

DOI

35
Gerardy-Schahn R, Delannoy P, von Itzstein M (2015) SialoGlyco chemistry and biology II tools and techniques to identify and capture sialoglycans preface. Sialoglyco Chemistry and Biology Ii 367:V–Vii

DOI

36
Ghosh S, Roseman S (1961) Enzymatic phosphorylation of N-acetyl-D-mannosamine. Proc Natl Acad Sci USA 47:955–958

DOI

37
Hakomori S (1985) Aberrant glycosylation in cancer cell membranes as focused on glycolipids: overview and perspectives. Cancer Res 45(6):2405–2414

38
Hamamoto T, Kawasaki M, Kurosawa N, Nakaoka T, Lee YC, Tsuji S (1993) Two step single primer mediated polymerase chain reaction. Application to cloning of putative mouse, beta-galactoside alpha 2,6-sialyltransferase cDNA. Bioorg Med Chem 1(2):141–145

DOI

39
Hanover JA (2001) Glycan-dependent signaling: O-linked N-acetylglucosamine. FASEB J 15(11):1865–1876

DOI

40
Hasehira K, Tateno H, Onuma Y, Ito Y, Asashima M, Hirabayashi J (2012) Structural and quantitative evidence for dynamic glycome shift on production of induced pluripotent stem cells. Mol Cell Proteomics 11(12):1913–1923

DOI

41
Hata K, Tochigi T, Sato I, Kawamura S, Shiozaki K, Wada T, Takahashi K, Moriya S, Yamaguchi K, Hosono M (2015) Increased sialidase activity in serum of cancer patients: Identification of sialidase and inhibitor activities in human serum. Cancer Sci 106(4):383–389

DOI

42
Hatano K, Miyamoto Y, Mori M, Nimura K, Nakai Y, Nonomura N, Kaneda Y (2012) Androgen-regulated transcriptional control of sialyltransferases in prostate cancer cells. PLoS ONE 7(2): e31234

DOI

43
Henderson M, Kessel D (1977) Alterations in plasma sialyltransferase levels in patients with neoplastic disease. Cancer 39(3):1129–1134

DOI

44
Hudak JE, Canham SM, Bertozzi CR (2014) Glycocalyx engineering reveals a Siglec-based mechanism for NK cell immunoevasion. Nat Chem Biol 10(1):69–75

DOI

45
Ikehara Y, Shimizu N, Kono M, Nishihara S, Nakanishi H, Kitamura T, Narimatsu H, Tsuji S, Tatematsu M (1999) A novel glycosyltransferase with a polyglutamine repeat; a new candidate for GD1alpha synthase (ST6GalNAc V)(1). FEBS Lett 463(1–2):92–96

DOI

46
James WM, Agnew WS (1987) Multiple oligosaccharide chains in the voltage-sensitive Na channel from electrophorus electricus: evidence for alpha-2,8-linked polysialic acid. Biochem Biophys Res Commun 148(2):817–826

DOI

47
Jandus C, Boligan KF, Chijioke O, Liu H, Dahlhaus M, Demoulins T, Schneider C, Wehrli M, Hunger RE, Baerlocher GM (2014) Interactions between Siglec-7/9 receptors and ligands influence NK cell-dependent tumor immunosurveillance. J Clin Investig 124(4):1810–1820

DOI

48
Jiang C, Liu S, He W, Zhang B, Xia L (2017) The prognostic and predictive value of carbohydrate antigen 19-9 in metastatic colorectal cancer patients with first line bevacizumab containing chemotherapy. J Cancer 8(8):1410–1416

DOI

49
Jones RB, Dorsett KA, Hjelmeland AB, Bellis SL (2018) The ST6Gal-I sialyltransferase protects tumor cells against hypoxia by enhancing HIF-1α signaling. J Biol Chem 293(15):jbc-RA117

DOI

50
Jourdian GW, Swanson AL, Watson D, Roseman S (1964) Isolation of sialic acid 9-phosphatase from human erythrocytes. J Biol Chem 239:PC2714-6

51
Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi K, Sato I, Miyagi T (2002) Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression. Proc Natl Acad Sci USA 99(16):10718–10723

DOI

52
Kannagi R (2007) Carbohydrate antigen sialyl Lewis a–its pathophysiological significance and induction mechanism in cancer progression. Chang Gung Med J 30(3):189–209

53
Kashef J, Franz CM (2015) Quantitative methods for analyzing cellcell adhesion in development. Dev Biol 401(1):165–174

DOI

54
Kiermaier E, Moussion C, Veldkamp CT, Gerardy-Schahn R, de Vries I, Williams LG, Chaffee GR, Phillips AJ, Freiberger F, Imre R (2016) Polysialylation controls dendritic cell trafficking by regulating chemokine recognition. Science 351(6269):186–190

DOI

55
Klenk E (1941) Neuraminsäure, das Spaltprodukt eines neuen Gehirnlipoids. Hoppe-Seyler's Zeitschrift für physiologische Chemie 268(1–2):50–58

DOI

56
Kochlamazashvili G, Senkov O, Grebenyuk S, Robinson C, Xiao MF, Stummeyer K, Gerardy-Schahn R, Engel AK, Feig L, Semyanov A (2010) Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors. J Neurosci 30(11):4171–4183

DOI

57
Kodar K, Stadlmann J, Klaamas K, Sergeyev B, Kurtenkov O (2012) Immunoglobulin G Fc N-glycan profiling in patients with gastric cancer by LC-ESI-MS: relation to tumor progression and survival. Glycoconj J 29(1):57–66

DOI

58
Kono M, Takashima S, Liu H, Inoue M, Kojima N, Lee YC, Hamamoto T, Tsuji S (1998) Molecular cloning and functional expression of a fifth-type alpha 2,3-sialyltransferase (mST3Gal V: GM3 synthase). Biochem Biophys Res Commun 253(1):170–175

DOI

59
Krzewinski-Recchi MA, Julien S, Juliant S, Teintenier-Lelievre M, Samyn-Petit B, Montiel MD, Mir AM, Cerutti M, Harduin-Lepers A, Delannoy P (2003) Identification and functional expression of a second human beta-galactoside alpha 2,6-sialyltransferase, ST6Gal II. Eur J Biochem 270(5):950–961

DOI

60
Kurosawa N, Inoue M, Yoshida Y, Tsuji S (1996) Molecular cloning and genomic analysis of mouse Galbeta 1, 3GalNAc-specific GalNAc alpha2,6-sialyltransferase. J Biol Chem 271(25):15109–15116

DOI

61
Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, Dennis JW (2007) Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129(1):123–134

DOI

62
Le Marer N, Laudet V, Svensson EC, Cazlaris H, Van Hille B, Lagrou C, Stehelin D, Montreuil J, Verbert A, Delannoy P (1992) The c-Ha-ras oncogene induces increased expression of beta-galactoside alpha-2, 6-sialyltransferase in rat fibroblast (FR3T3) cells. Glycobiology 2(1):49–56

DOI

63
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 (13):10028–10033

64
Li RH, Liang JL, Ni S, Zhou T, Qing XB, Li HP, He WZ, Chen JK, Li F, Zhuang QA (2010) A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7(1):51–63

DOI

65
Liang Y, Xu P, Zou Q, Luo H, Yu W (2018) An epigenetic perspective on tumorigenesis: loss of cell identity, enhancer switching, and NamiRNA network. Semin Cancer Biol. https://doi.org/10.1016/j.semcancer.2018.09.004

DOI

66
Liu XP, Sun H, Qi J, Wang LL, He SW, Liu J, Feng CQ, Chen CL, Li W, Guo YQ (2013) Sequential introduction of reprogramming factors reveals a time-sensitive requirement for individual factors and a sequential EMT-MET mechanism for optimal reprogramming. Nat Cell Biol 15(7):829-+

DOI

67
Lowe JB (2 003) Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr Opin Cell Biol 15(5):531–538

DOI

68
Ludwig JA, Weinstein JN (2005) Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer 5(11):845–856

DOI

69
Macauley MS, Crocker PR, Paulson JC (2014) Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol 14(10):653–666

DOI

70
Macbeth RALBJG (1962) Plasma glycoproteins in various disease states including carcinoma. Cancer Res 22(10):1170–1176

71
Margolis RK, Margolis RU (1983) Distribution and characteristics of polysialosyl oligosaccharides in nervous tissue glycoproteins. Biochem Biophys Res Commun 116(3):889–894

DOI

72
Melo-Braga MN, Schulz M, Liu QY, Swistowski A, Palmisano G, Engholm-Keller K, Jakobsen L, Zeng XM, Larsen MR (2014)Comprehensive quantitative comparison of the membrane proteome, phosphoproteome, and sialiome of human embryonic and neural stem cells. Mol Cell Proteomics 13(1):311–328

DOI

73
Mincarelli L, Lister A, Lipscombe J, Macaulay IC (2018) Defining cell identity with single-cell omics. Proteomics 18(18):e1700312

DOI

74
Miyagi T, Takahashi K, Hata K, Shiozaki K, Yamaguchi K (2012) Sialidase significance for cancer progression. Glycoconj J 29(8–9):567–577

DOI

75
Moris N, Pina C, Arias AM (2016) Transition states and cell fate decisions in epigenetic landscapes. Nat Rev Genet 17(11):693–703

DOI

76
Moyer VA, Force USPST (2012) Screening for prostate cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 157(2):120–134

DOI

77
Muhlenhoff M, Rollenhagen M, Werneburg S, Gerardy-Schahn R, Hildebrandt H (2013) Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem Res 38(6):1134–1143

DOI

78
Nakagoe T, Sawai T, Tsuji T, Jibiki M, Nanashima A, Yamaguchi H, Kurosaki N, Yasutake T, Ayabe H (2001) Circulating sialyl Lewis (x), sialyl Lewis(a), and sialyl Tn antigens in colorectal cancer patients: multivariate analysis of predictive factors for serum antigen levels. J Gastroenterol 36(3):166–172

DOI

79
Nicoll G, Avril T, Lock K, Furukawa K, Bovin N, Crocker PR (2003) Ganglioside GD3 expression on target cells can modulate NK cell cytotoxicity via siglec-7-dependent and-independent mechanisms. Eur J Immunol 33(6):1642–1648

DOI

80
Nomura H, Tamada Y, Miyagi T, Suzuki A, Taira M, Suzuki N, Susumu N, Irimura T, Aoki D (2006) Expression of NEU3 (plasma membrane-associated sialidase) in clear cell adenocarcinoma of the ovary: its relationship with T factor of pTNM classification. Oncol Res 16(6):289–297

DOI

81
O’Reilly MK, Paulson JC (2009) Siglecs as targets for therapy in immune-cell-mediated disease. Trends Pharmacol Sci 30(5):240–248

DOI

82
Okajima T, Fukumoto S,Miyazaki H, Ishida H, Kiso M, Furukawa K, Urano T, Furukawa K (1999) Molecular cloning of a novel alpha 2,3-sialyltransferase (ST3Gal VI) that sialylates type II lactosamine structures on glycoproteins and glycolipids. J Biol Chem 274(17):11479–11486

DOI

83
Okajima T, Chen HH, Ito H, Kiso M, Tai T, Furukawa K, Urano T, Furukawa K (2000) Molecular cloning and expression of mouse GD1alpha/GT1aalpha/GQ1balpha synthase (ST6GalNAc VI) gene. J Biol Chem 275(10):6717–6723

DOI

84
Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, Rademacher TW, Mizuochi T, Taniguchi T, Matsuta K (1985) Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 316(6027):452–457

DOI

85
Pihikova D, Kasak P, Kubanikova P, Sokol R, Tkac J (2016) Aberrant sialylation of a prostate-specific antigen: Electrochemical labelfree glycoprofiling in prostate cancer serum samples. Anal Chim Acta 934:72–79

DOI

86
Pinho SS, Reis CA (2015) Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 15(9):540–555

DOI

87
Pucic M, Knezevic A, Vidic J, Adamczyk B, Novokmet M, Polasek O, Gornik O, Supraha-Goreta S, Wormald MR, Redzic I (2011) High throughput isolation and glycosylation analysis of IgGvariability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics 10(10):M111 010090

DOI

88
Raval GN, Patel DD, Parekh LJ, Patel JB, Shah MH, Patel PS (2003) Evaluation of serum sialic acid, sialyltransferase and sialoproteins in oral cavity cancer. Oral Dis 9(3):119–128

DOI

89
Roseman S, Jourdian GW, Watson D, Rood R (1961) Enzymatic synthesis of sialic acid 9-phosphates. Proc Natl Acad Sci USA 47:958–961

DOI

90
Saito S, Onuma Y, Ito Y, Tateno H, Toyoda M, Hidenori A, Nishino K, Chikazawa E, Fukawatase Y, Miyagawa Y (2011) Possible linkages between the inner and outer cellular states of human induced pluripotent stem cells. BMC Syst Biol 5(Suppl 1):S17

DOI

91
Sakuma K, Aoki M, Kannagi R (2012) Transcription factors c-Myc and CDX2 mediate E-selectin ligand expression in colon cancer cells undergoing EGF/bFGF-induced epithelial-mesenchymal transition. Proc Natl Acad Sci USA 109(20):7776–7781

DOI

92
Saldova R, Wormald MR, Dwek RA, Rudd PM (2008) Glycosylation changes on serum glycoproteins in ovarian cancer may contribute to disease pathogenesis. Dis Markers 25(4–5):219–232

DOI

93
Santos-Silva F, Fonseca A, Caffrey T, Carvalho F, Mesquita P, Reis C, Almeida R, David L, Hollingsworth MA (2005) Thomsen-Friedenreich antigen expression in gastric carcinomas is associated with MUC1 mucin VNTR polymorphism. Glycobiology 15(5):511–517

DOI

94
Sasaki K, Watanabe E, Kawashima K, Sekine S, Dohi T, Oshima M, Hanai N, Nishi T, Hasegawa M (1993) Expression cloning of a novel Gal beta (1-3/1-4) GlcNAc alpha 2,3-sialyltransferase using lectin resistance selection. J Biol Chem 268(30):22782–22787

95
Sato C, Kitajima K (2013) Disialic, oligosialic and polysialic acids: distribution, functions and related disease. J Biochem 154(2):115–136

DOI

96
Sawhney H, Kumar CA (2011) Correlation of serum biomarkers (TSA & LSA) and epithelial dysplasia in early diagnosis of oral precancer and oral cancer. Cancer Biomark 10(1):43–49

DOI

97
Schroeder FH, Hugosson J, Roobol MJ, Tammela TLJ, Ciatto S, Nelen V, Kwiatkowski M, Lujan M, Lilja H, Zappa M (2009) Screening and Prostate-Cancer Mortality in a Randomized European Study. N Engl J Med 360(13):1320–1328

DOI

98
Schultz MJ, Holdbrooks AT, Chakraborty A, Grizzle WE, Landen CN, Buchsbaum DJ, Conner MG, Arend RC, Yoon KJ, Klug CA (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

DOI

99
Schwarzkopf M, Knobeloch KP, Rohde E, Hinderlich S, Wiechens N, Lucka L, Horak I, Reutter W, Horstkorte R (2002) Sialylation is essential for early development in mice. Proc Natl Acad Sci USA 99(8):5267–5270

DOI

100
Seales EC, Jurado GA, Singhal A, Bellis SL (2003) Ras oncogene directs expression of a differentially sialylated, functionally altered beta1 integrin. Oncogene 22(46):7137–7145

DOI

101
Seales EC, Shaikh FM, Woodard-Grice AV, Aggarwal P, McBrayer AC, Hennessy KM, Bellis SL (2005) A protein kinase C/Ras/ERK signaling pathway activates myeloid fibronectin receptors by altering beta1 integrin sialylation. J Biol Chem 280(45):37610–37615

DOI

102
Shah MH, Telang SD, Shah PM, Patel PS (2008) Tissue and serum alpha 2-3- and alpha 2-6-linkage specific sialylation changes in oral carcinogenesis. Glycoconj J 25(3):279–290

DOI

103
Stojkovic Lalosevic M, Stankovic S, Stojkovic M, Markovic V, Dimitrijevic I, Lalosevic J, Petrovic J, Brankovic M, Pavlovic Markovic A, Krivokapic Z (2017) Can preoperative CEA and CA19-9 serum concentrations suggest metastatic disease in colorectal cancer patients? Hell J Nucl Med 20(1):41–45

104
Suzuki O, Abe M, Hashimoto Y (2015) Sialylation by betagalactoside alpha-2,6-sialyltransferase and N-glycans regulate cell adhesion and invasion in human anaplastic large cell lymphoma. Int J Oncol 46(3):973–980

DOI

105
Svennerholm L, Bostrom K, Fredman P, Mansson JE, Rosengren B, Rynmark BM (1989) Human brain gangliosides: developmental changes from early fetal stage to advanced age. Biochim Biophys Acta 1005(2):109–117

DOI

106
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

DOI

107
Tajiri M, Ohyama C, Wada Y (2008) Oligosaccharide profiles of the prostate specific antigen in free and complexed forms from the prostate cancer patient serum and in seminal plasma: a glycopeptide approach. Glycobiology 18(1):2–8

DOI

108
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676

DOI

109
Takashima S, Tachida Y, Nakagawa T, Hamamoto T, Tsuji S (1999) Quantitative analysis of expression of mouse sialyltransferase genes by competitive PCR. Biochem Biophys Res Commun 260(1):23–27

DOI

110
Takashima S, Ishida HK, Inazu T, Ando T, Ishida H, Kiso M, Tsuji S, Tsujimoto M (2002) Molecular cloning and expression of a sixth type of alpha 2,8-sialyltransferase (ST8Sia VI) that sialylates O-glycans. J Biol Chem 277(27):24030–24038

DOI

111
Theodoratou E, Thaci K, Agakov F, Timofeeva MN, Stambuk J, Pucic-Bakovic M, Vuckovic F, Orchard P, Agakova A, Din FV (2016) Glycosylation of plasma IgG in colorectal cancer prognosis. Sci Rep 6:28098

DOI

112
Uckun FM, Goodman P, Ma H, Dibirdik I, Qazi S (2010) CD22 EXON 12 deletion as a pathogenic mechanism of human B-precursor leukemia. Proc Natl Acad Sci USA 107(39):16852–16857

DOI

113
van Karnebeek CDM, Bonafe L, Wen XY, Tarailo-Graovac M, Balzano S, Royer-Bertrand B, Ashikov A, Garavelli L, Mammi I, Turolla L (2017) NANS-mediated synthesis of sialic acid is required for brain and skeletal development (vol 48, pg 777, 2016). Nat Genet 49(6):969

DOI

114
Varki A (2008) Sialic acids in human health and disease. Trends Mol Med 14(8):351–360

DOI

115
Vuckovic F, Theodoratou E, Thaci K, Timofeeva M, Vojta A, Stambuk J, Pucic-Bakovic M, Rudd PM, Derek L, Servis D (2016) IgG glycome in colorectal cancer. Clin Cancer Res 22(12):3078–3086

DOI

116
Wang B (2009) Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr 29:177–222

DOI

117
Wang B (2012) Molecular mechanism underlying sialic acid as an essential nutrient for brain development and cognition. Advances in Nutrition 3(3):465s–472s

DOI

118
Wang B, Brand-Miller J, McVeagh P, Petocz P (2001) Concentration and distribution of sialic acid in human milk and infant formulas. Am J Clin Nutr 74(4):510–515

DOI

119
Wang B, McVeagh P, Petocz P, Brand-Miller J (2003) Brain ganglioside and glycoprotein sialic acid in breastfed compared with formula-fed infants. Am J Clin Nutr 78(5):1024–1029

DOI

120
Wang YC, Peterson SE, Loring JF (2014) Protein post-translational modifications and regulation of pluripotency in human stem cells. Cell Res 24(2):143–160

DOI

121
Wang YC, Stein JW, Lynch CL, Tran HT, Lee CY, Coleman R, Hatch A, Antontsev VG, Chy HS, O’Brien CM (2015) Glycosyltransferase ST6GAL1 contributes to the regulation of pluripotency in human pluripotent stem cells. Sci Rep 5:13317

DOI

122
Weber KS, Alon R, Klickstein LB (2004) Sialylation of ICAM-2 on platelets impairs adhesion of leukocytes via LFA-1 and DC-SIGN. Inflammation 28(4):177–188

DOI

123
Werneburg S, Buettner FF, Erben L, Mathews M, Neumann H, Muhlenhoff M, Hildebrandt H (2016) Polysialylation and lipopolysaccharide-induced shedding of E-selectin ligand-1 and neuropilin-2 by microglia and THP-1 macrophages. Glia 64(8):1314–1330

DOI

124
Yabe U, Sato C, Matsuda T, Kitajima K (2003) Polysialic acid in human milk—CD36 is a new member of mammalian polysialic acid-containing glycoprotein. J Biol Chem 278(16):13875–13880

DOI

125
Yang X, Qian K (2017) Protein O-GlcNAcylation: emerging mechanisms and functions. Nat Rev Mol Cell Biol 18(7):452–465

DOI

126
Yang PMD, Rutishauser U (1994) Role of charge and hydration in effects of polysialic acid on molecular interactions on and between cell membranes. J Biol Chem 269(37):23039–23044

127
Yoneyama T, Ohyama C, Hatakeyama S, Narita S, Habuchi T, Koie T, Mori K, Hidari KIPJ, Yamaguchi M, Suzuki T (2014) Measurement of aberrant glycosylation of prostate specific antigen can improve specificity in early detection of prostate cancer. Biochem Biophys Res Commun 448(4):390–396

DOI

128
Yoshida Y, Kojima N, Tsuji S (1995) Molecular cloning and characterization of a third type of N-glycan alpha 2,8-sialyltransferase from mouse lung. J Biochem 118(3):658–664

DOI

129
Zhang D, Chen BC, Wang YM, Xia P, He CY, Liu YJ, Zhang RQ, Zhang M, Li ZL (2016) Disease-specific IgG Fc N-glycosylation as personalized biomarkers to differentiate gastric cancer from benign gastric diseases. Sci Rep 6:25957

DOI

130
Zhao J, Simeone DM, Heidt D, Anderson MA, Lubman DM (2006) Comparative serum glycoproteomics using lectin selected sialic acid glycoproteins with mass spectrometric analysis: Application to pancreatic cancer serum. J Proteome Res 5(7):1792–1802

DOI

131
Zhao ZA, Yu Y, Ma HX, Wang XX, Lu X, Zhai Y, Zhang X, Wang H, Li L (2015) The roles of ERAS during cell lineage specification of mouse early embryonic development. Open Biol 5(8):150092

DOI

132
Zhao T, Fu Y, Zhu J, Liu Y, Zhang Q, Yi Z, Chen S, Jiao Z, Xu X, Xu J (2018) Single-cell RNA-Seq reveals dynamic early embryonic-like programs during chemical reprogramming. Cell Stem Cell 23(1):31–45 e7

DOI

133
Zhou Q, Melton DA (2008) Extreme makeover: converting one cell into another. Cell Stem Cell 3(4):382–388

DOI

Outlines

/