ST8SIA4-Dependent Polysialylation is Part of a Developmental Program Required for Germ Layer Formation from Human Pluripotent Stem Cells

Stem Cells

Volumn 34, Issue 7, 2016, Pages 1742-1752

  Berger, Ryan P ^a   Sun, Yu Hua ^a   Kulik, Michael ^a   Lee, Jin Kyu ^a   Nairn, Alison V ^a   Moremen, Kelley W ^a   Pierce, Michael ^a   Dalton, Stephen ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Glycosylation; Neural cell adhesion molecule; Pluripotent stem cells; Polysialic acid

Indexed keywords

ALPHA MANNOSIDASE; GOOSECOID PROTEIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; NERVE CELL ADHESION MOLECULE; SHORT HAIRPIN RNA; SIALYLTRANSFERASE; ST8SIA4 PROTEIN; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL SPECIFICITY; CONTROLLED STUDY; CRISPR CAS SYSTEM; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; EPIGENETICS; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GERM LAYER; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; IMMUNOHISTOCHEMISTRY; MESODERM; PLURIPOTENT STEM CELL; POLYSIALYLATION; POLYSIALYLTRANSFERASE GENE; PROTEIN DOMAIN; SIALYLATION; VERTEBRATE;

EID: 84978975347     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2379     Document Type: Article

References (49)

1. Varki A, Cummings RD, Esko JD et al. Essentials of Glycobiology. Cold Spring Harbor Laboratory Press; 2009.
2. Haltiwanger RS, Lowe JB. Role of glycosylation in development. Ann Rev Biochem 2004;73:491–537.
3. Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 2008;9:26–35.
4. Mühlenhoff M, Rollenhagen M, Werneburg S et al. Polysialic acid: Versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem Res 2013;38:1134–1143.
5. Close BE, Colley KJ. In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J Biol Chem 1998;273:34586–34593.
6. Finne J. Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J Biol Chem 1982;257:11966–11970.
7. Phillips GR, Krushel LA, Crossin KL. Developmental expression of two rat sialyltransferases that modify the neural cell adhesion molecule, N-CAM. Dev Brain Res 1997;102:143–155.
8. Hildebrandt H, Becker C, Mürau M et al. Heterogeneous expression of the polysialyltransferases ST8Sia II and ST8Sia IV during postnatal rat brain development. J Neurochem 1998;71:2339–2348.
9. Lackie PM, Zuber C, Roth J. Polysialic acid of the neural cell adhesion molecule (N-CAM) is widely expressed during organogenesis in mesodermal and endodermal derivatives. Differentiation 1994;57:119–131.
10. Curreli S, Arany Z, Gerardy-Schahn R et al. Polysialylated Neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J Biol Chem 2007;282:30346–30356.
11. Galuska SP, Rollenhagen M, Kaup M et al. Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc Natl Acad Sci USA 2010;107:10250–10255.
12. Galuska SP, Geyer R, Gerardy-Schahn R et al. Enzyme-dependent variations in the polysialylation of the neural cell adhesion molecule (NCAM) in vivo. J Biol Chem 2007;283:17–28.
13. Close BE, Mendiratta SS, Geiger KM et al. The minimal structural domains required for neural cell adhesion molecule polysialylation by PST/ST8Sia IV and STX/ST8Sia II. J Biol Chem 2003;278:30796–30805.
14. Johnson CP, Fujimoto I, Rutishauser U et al. Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 2005;280:137–145.
15. Li J, Dai G, Cheng YB et al. Polysialylation promotes neural cell adhesion molecule-mediated cell migration in a fibroblast growth factor receptor-dependent manner, but independent of adhesion capability. Glycobiology 2011;21:1010–1018.
16. Rutishauser U, Watanabe M, Silver J et al. Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol 1985;101:1842–1849.
17. Hu H, Tomasiewicz H, Magnuson T et al. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 1996;16:735–743.
18. Landmesser L, Dahm L, Tang J et al. Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 1990;4:655–667.
19. Ono S, Hane M, Kitajima K et al. Novel regulation of fibroblast growth factor 2 (FGF2)-mediated cell growth by polysialic acid. J Biol Chem 2012;287:3710–3722.
20. Eggers K, Werneburg S, Schertzinger A et al. Polysialic acid controls NCAM signals at cell-cell contacts to regulate focal adhesion independent from FGF receptor activity. J Cell Sci 2011;124:3279–3291.
21. Seidenfaden R, Krauter A, Hildebrandt H. The neural cell adhesion molecule NCAM regulates neuritogenesis by multiple mechanisms of interaction. Neurochem Int 2006;49:1–11.
22. Livingston BD, Jacobs JL, Glick MC et al. Extended polysialic acid chains (n > 55) in glycoproteins from human neuroblastoma cells. J Biol Chem 1988;263:9443–9448.
23. Schreiber SC, Giehl K, Kastilan C et al. Polysialylated NCAM represses E-cadherin-mediated cell-cell adhesion in pancreatic tumor cells. Gastroenterology 2008;134:1555–1566.
24. Tanaka F, Otake Y, Nakagawa T et al. Expression of polysialic acid and STX, a human polysialyltransferase, is correlated with tumor progression in non-small cell lung cancer. Cancer Res 2000;60:3072–3080.
25. Roth J, Zuber C, Wagner P et al. Presence of the long chain form of polysialic acid of the neural cell adhesion molecule in Wilms' tumor. Identification of a cell adhesion molecule as an oncodevelopmental antigen and implications for tumor histogenesis. Am J Pathol 1988;133:227.
26. Amoureux M-C, Coulibaly B, Chinot O et al. Polysialic acid neural cell adhesion molecule (PSA-NCAM) is an adverse prognosis factor in glioblastoma, and regulates olig2 expression in glioma cell lines. BMC Cancer 2010;10:91.
27. Wang L, Schulz TC, Sherrer ES et al. Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling. Blood 2007;110:4111–4119.
28. McLean AB, D'Amour KA, Jones KL et al. Activin A efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 2007;25:29–38.
29. Menendez L, Yatskievych TA, Antin PB et al. Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc Natl Acad Sci USA 2011;108:19240–19245.
30. Ran FA, Hsu PD, Wright J et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 2013;8:2281–2308.
31. Mali P, Yang L, Esvelt KM et al. RNA-guided human genome engineering via Cas9. Science 2013;339:823–826.
32. Bernstein BE, Mikkelsen TS, Xie X et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006;125:315–326.
33. Rosenbloom KR, Sloan CA, Malladi VS et al. ENCODE data in the UCSC genome browser: Year 5 update. Nucleic Acids Res 2012;41(D1):D56–D63.
34. Showell C, Binder O, Conlon FL. T-box genes in early embryogenesis. Dev Dyn 2004;229:201–218.
35. Fernando RI, Litzinger M, Trono P et al. The T-box transcription factor Brachyury promotes epithelial-mesenchymal transition in human tumor cells. J Clin Invest 2010;120:533–544.
36. Hartwell KA, Muir B, Reinhardt F et al. The Spemann organizer gene, Goosecoid, promotes tumor metastasis. Proc Natl Acad Sci USA 2006;103:18969–18974.
37. Carey KL, Richards SA, Lounsbury KM et al. Evidence using a green fluorescent protein-glucocorticoid receptor chimera that the Ran/TC4 GTPase mediates an essential function independent of nuclear protein import. J Cell Biol 1996;133:985–996.
38. Artinger M, Blitz I, Inoue K et al. Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech Dev 1997;65:187–196.
39. Lehembre F, Yilmaz M, Wicki A et al. NCAM-induced focal adhesion assembly: A functional switch upon loss of E-cadherin. EMBO J 2008;27:2603–2615.
40. Weinhold B, Seidenfaden R, Röckle I et al. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 2005;280:42971–42977.
41. Chambers SM, Fasano CA, Papapetrou EP et al. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009;27:275–280.
42. Eckhardt M, Bukalo O, Chazal G et al. Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J Neurosci 2000;20:5234–5244.
43. Angata K, Long JM, Bukalo O et al. Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J Biol Chem 2004;279:32603–32613.
44. Liao B-Y, Zhang J. Null mutations in human and mouse orthologs frequently result in different phenotypes. Proc Natl Acad Sci USA 2008;105:6987–6992.
45. Wang Y-C, Stein JW, Lynch CL et al. Glycosyltransferase ST6GAL1 contributes to the regulation of pluripotency in human pluripotent stem cells. Sci Rep 2015:1–13.
46. Alisson-Silva F, de Carvalho Rodrigues D, Vairo L et al. Evidences for the involvement of cell surface glycans in stem cell pluripotency and differentiation. Glycobiology 2014;24:458–468.
47. Swindall AF, Londono-Joshi AI, Schultz MJ et al. 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 2013;73:2368–2378.
48. Wang Y-C, Nakagawa M, Garitaonandia I et al. Specific lectin biomarkers for isolation of human pluripotent stem cells identified through array-based glycomic analysis. Cell Res 2011;21:1551–1563.
49. Tateno H, Toyota M, Saito S et al. Glycome diagnosis of human induced pluripotent stem cells using lectin microarray. J Biol Chem 2011;286:20345–20353.