Sialylation is involved in cell fate decision during development, reprogramming and cancer progression
Received date: 06 Oct 2018
Accepted date: 31 Oct 2018
Published date: 15 Aug 2019
Copyright
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.
Key words: sialylation; cell fate; development; reprogramming; cancer
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
|
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
|
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
|
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
|
5 |
Baldus SE, Zirbes TK, Monig SP, Engel S, Monaca E, Rafiqpoor K, Hanisch FG, Hanski C, Thiele J, Pichlmaier H
|
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
|
8 |
Bianconi E, Piovesan A, Facchin F, Beraudi A, Casadei R, Frabetti F, Vitale L, Pelleri MC, Tassani S, Piva F
|
9 |
Blix G (1936) Über die Kohlenhydratgruppen des Submaxillarismucins. Hoppe-Seyler's Zeitschrift für physiologische Chemie 240(1–2):43–54
|
10 |
Blix FG, Gottschalk A, Klenk E (1957) Proposed nomenclature in the field of neuraminic and sialic acids. Nature 179(4569):1088
|
11 |
Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330(6004):612–616
|
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
|
14 |
Chen X, Varki A (2010) Advances in the biology and chemistry of sialic acids. ACS Chem Biol 5(2):163–176
|
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
|
16 |
Close BE, Colley KJ (1998) In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J Biol Chem 273(51):34586–34593
|
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
|
19 |
Corfield AP (2015) Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta 1850(1):236–252
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
29 |
Eckhardt M, Gerardy-Schahn R (1998) Genomic organization of the murine polysialyltransferase gene ST8SiaIV (PST-1). Glycobiology 8(12):1165–1172
|
30 |
Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819):154–156
|
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
|
33 |
Fuster MM, Esko JD (2005) The sweet and sour of cancer: Glycans as novel therapeutic targets. Nat Rev Cancer 5(7):526–542
|
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
|
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
|
36 |
Ghosh S, Roseman S (1961) Enzymatic phosphorylation of N-acetyl-D-mannosamine. Proc Natl Acad Sci USA 47:955–958
|
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
|
39 |
Hanover JA (2001) Glycan-dependent signaling: O-linked N-acetylglucosamine. FASEB J 15(11):1865–1876
|
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
|
41 |
Hata K, Tochigi T, Sato I, Kawamura S, Shiozaki K, Wada T, Takahashi K, Moriya S, Yamaguchi K, Hosono M
|
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
|
43 |
Henderson M, Kessel D (1977) Alterations in plasma sialyltransferase levels in patients with neoplastic disease. Cancer 39(3):1129–1134
|
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
|
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
|
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
|
47 |
Jandus C, Boligan KF, Chijioke O, Liu H, Dahlhaus M, Demoulins T, Schneider C, Wehrli M, Hunger RE, Baerlocher GM
|
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
|
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
|
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
|
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
|
54 |
Kiermaier E, Moussion C, Veldkamp CT, Gerardy-Schahn R, de Vries I, Williams LG, Chaffee GR, Phillips AJ, Freiberger F, Imre R
|
55 |
Klenk E (1941) Neuraminsäure, das Spaltprodukt eines neuen Gehirnlipoids. Hoppe-Seyler's Zeitschrift für physiologische Chemie 268(1–2):50–58
|
56 |
Kochlamazashvili G, Senkov O, Grebenyuk S, Robinson C, Xiao MF, Stummeyer K, Gerardy-Schahn R, Engel AK, Feig L, Semyanov A
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
66 |
Liu XP, Sun H, Qi J, Wang LL, He SW, Liu J, Feng CQ, Chen CL, Li W, Guo YQ
|
67 |
Lowe JB (2 003) Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr Opin Cell Biol 15(5):531–538
|
68 |
Ludwig JA, Weinstein JN (2005) Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer 5(11):845–856
|
69 |
Macauley MS, Crocker PR, Paulson JC (2014) Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol 14(10):653–666
|
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
|
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
|
73 |
Mincarelli L, Lister A, Lipscombe J, Macaulay IC (2018) Defining cell identity with single-cell omics. Proteomics 18(18):e1700312
|
74 |
Miyagi T, Takahashi K, Hata K, Shiozaki K, Yamaguchi K (2012) Sialidase significance for cancer progression. Glycoconj J 29(8–9):567–577
|
75 |
Moris N, Pina C, Arias AM (2016) Transition states and cell fate decisions in epigenetic landscapes. Nat Rev Genet 17(11):693–703
|
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
|
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
|
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
|
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
|
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
|
81 |
O’Reilly MK, Paulson JC (2009) Siglecs as targets for therapy in immune-cell-mediated disease. Trends Pharmacol Sci 30(5):240–248
|
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
|
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
|
84 |
Parekh RB, Dwek RA, Sutton BJ, Fernandes DL, Leung A, Stanworth D, Rademacher TW, Mizuochi T, Taniguchi T, Matsuta K
|
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
|
86 |
Pinho SS, Reis CA (2015) Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 15(9):540–555
|
87 |
Pucic M, Knezevic A, Vidic J, Adamczyk B, Novokmet M, Polasek O, Gornik O, Supraha-Goreta S, Wormald MR, Redzic I
|
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
|
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
|
90 |
Saito S, Onuma Y, Ito Y, Tateno H, Toyoda M, Hidenori A, Nishino K, Chikazawa E, Fukawatase Y, Miyagawa Y
|
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
|
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
|
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
|
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
|
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
|
97 |
Schroeder FH, Hugosson J, Roobol MJ, Tammela TLJ, Ciatto S, Nelen V, Kwiatkowski M, Lujan M, Lilja H, Zappa M
|
98 |
Schultz MJ, Holdbrooks AT, Chakraborty A, Grizzle WE, Landen CN, Buchsbaum DJ, Conner MG, Arend RC, Yoon KJ, Klug CA
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
111 |
Theodoratou E, Thaci K, Agakov F, Timofeeva MN, Stambuk J, Pucic-Bakovic M, Vuckovic F, Orchard P, Agakova A, Din FV
|
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
|
113 |
van Karnebeek CDM, Bonafe L, Wen XY, Tarailo-Graovac M, Balzano S, Royer-Bertrand B, Ashikov A, Garavelli L, Mammi I, Turolla L
|
114 |
Varki A (2008) Sialic acids in human health and disease. Trends Mol Med 14(8):351–360
|
115 |
Vuckovic F, Theodoratou E, Thaci K, Timofeeva M, Vojta A, Stambuk J, Pucic-Bakovic M, Rudd PM, Derek L, Servis D
|
116 |
Wang B (2009) Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr 29:177–222
|
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
|
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
|
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
|
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
|
121 |
Wang YC, Stein JW, Lynch CL, Tran HT, Lee CY, Coleman R, Hatch A, Antontsev VG, Chy HS, O’Brien CM
|
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
|
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
|
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
|
125 |
Yang X, Qian K (2017) Protein O-GlcNAcylation: emerging mechanisms and functions. Nat Rev Mol Cell Biol 18(7):452–465
|
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
|
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
|
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
|
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
|
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
|
132 |
Zhao T, Fu Y, Zhu J, Liu Y, Zhang Q, Yi Z, Chen S, Jiao Z, Xu X, Xu J
|
133 |
Zhou Q, Melton DA (2008) Extreme makeover: converting one cell into another. Cell Stem Cell 3(4):382–388
|
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