Specific lectin biomarkers for isolation of human pluripotent stem cells identified through array-based glycomic analysis

Cell Research

Volumn 21, Issue 11, 2011, Pages 1551-1563

  Wang, Yu Chieh ^a   Nakagawa, Masato ^b   Garitaonandia, Ibon ^a   Slavin, Ileana ^a   Altun, Gulsah ^a   Lacharite, Robert M ^a   Nazor, Kristopher L ^a   Tran, Ha T ^a   Lynch, Candace L ^a   Leonardo, Trevor R ^a   Liu, Ying ^a,f   Peterson, Suzanne E ^a   Laurent, Louise C ^a,f   Yamanaka, Shinya ^b,c,d,e   Loring, Jeanne F ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

embryonic stem cells; glycosylation; human pluripotent stem cell; induced pluripotent stem cells; lectins; pluripotency biomarkers

Indexed keywords

BIOLOGICAL MARKER; BIOTIN; FUCOSYLTRANSFERASE; LECTIN; SIALYLTRANSFERASE;

ARTICLE; CELL CULTURE; CELL SEPARATION; CHEMISTRY; CYTOLOGY; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GLYCOBIOLOGY; GLYCOSYLATION; HUMAN; METABOLISM; PLURIPOTENT STEM CELL; PROTEIN BINDING; PROTEIN MICROARRAY;

BIOLOGICAL MARKERS; BIOTIN; CELL SEPARATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; FUCOSYLTRANSFERASES; GENE EXPRESSION PROFILING; GLYCOMICS; GLYCOSYLATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LECTINS; PLURIPOTENT STEM CELLS; PROTEIN ARRAY ANALYSIS; PROTEIN BINDING; SIALYLTRANSFERASES;

EID: 80555122989     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2011.148     Document Type: Article

References (42)

1. Lawrenz B, Schiller H, Willbold E, Ruediger M, Muhs A, Esser S. Highly sensitive biosafety model for stem-cell-derived grafts. Cytotherapy 2004; 6:212-222.
2. Andrews PW, Banting G, Damjanov I, Arnaud D, Avner P. Three monoclonal antibodies defining distinct differentiation antigens associated with different high molecular weight polypeptides on the surface of human embryonal carcinoma cells. Hybridoma 1984; 3:347-361.
3. Kannagi R, Cochran NA, Ishigami F, et al. Stage-specific embryonic antigens (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J 1983; 2:2355-2361.
4. Kannagi R, Levery SB, Ishigami F, et al. New globoseries glycosphingolipids in human teratocarcinoma reactive with the monoclonal antibody directed to a developmentally regulated antigen, stage-specific embryonic antigen 3. J Biol Chem 1983; 258:8934-8942.
5. Kolle G, Ho M, Zhou Q, et al. Identification of human embryonic stem cell surface markers by combined membranepolysome translation state array analysis and immunotranscriptional profiling. Stem Cells 2009; 27:2446-2456.
6. Lin SA, Kolle G, Grimmond SM, et al. Subfractionation of differentiating human embryonic stem cell populations allows the isolation of a mesodermal population enriched for intermediate mesoderm and putative renal progenitors. Stem Cells Dev 2010; 19:1637-1648.
7. Pera MF, Blasco-Lafita MJ, Cooper S, Mason M, Mills J, Monaghan P. Analysis of cell-differentiation lineage in human teratomas using new monoclonal antibodies to cytostructural antigens of embryonal carcinoma cells. Differentiation 1988; 39:139-149.
8. Apweiler R, Hermjakob H, Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISSPROT database. Biochim Biophys Acta 1999; 1473:4-8.
9. Reis CA, Osorio H, Silva L, Gomes C, David L. Alterations in glycosylation as biomarkers for cancer detection. J Clin Pathol 2010; 63:322-329.
10. Kakugawa Y, Wada T, Yamaguchi K, et al. Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression. Proc Natl Acad Sci USA 2002; 99:10718-10723.
11. Moody AM, Chui D, Reche PA, Priatel JJ, Marth JD, Reinherz EL. Developmentally regulated glycosylation of the CD8 alpha beta coreceptor stalk modulates ligand binding. Cell 2001; 107:501-512.
12. Fogel AI, Li Y, Giza J, et al. N-glycosylation at the SynCAM (synaptic cell adhesion molecule) immunoglobulin interface modulates synaptic adhesion. J Biol Chem 2010; 285:34864-34874.
13. Reid CW, Fulton KM, Twine SM. Never take candy from a stranger: The role of the bacterial glycome in host-pathogen interactions. Future Microbiol 2010; 5:267-288.
14. Balog CI, Mayboroda OA, Wuhrer M, Hokke CH, Deelder AM, Hensbergen PJ. Mass spectrometric identification of aberrantly glycosylated human apolipoprotein C-III peptides in urine from Schistosoma mansoni-infected individuals. Mol Cell Proteomics 2010; 9:667-681.
15. Haltiwanger RS. Regulation of signal transduction pathways in development by glycosylation. Curr Opin Struct Biol 2002; 12:593-598.
16. Xia L, McDaniel JM, Yago T, Doeden A, McEver RP. Surface fucosylation of human cord blood cells augments binding to P-selectin and E-selectin and enhances engraftment in bone marrow. Blood 2004; 104:3091-3096.
17. Satomaa T, Heiskanen A, Mikkola M, et al. The N-glycome of human embryonic stem cells. BMC Cell Biol 2009; 10:42.
18. Venable A, Mitalipova M, Lyons I, et al. Lectin binding profiles of SSEA-4 enriched, pluripotent human embryonic stem cell surfaces. BMC Dev Biol 2005; 5:15.
19. Kuno A, Uchiyama N, Koseki-Kuno S, et al. Evanescent-field fluorescence-assisted lectin microarray: A new strategy for glycan profiling. Nat Methods 2005; 2:851-856.
20. Pilobello KT, Krishnamoorthy L, Slawek D, Mahal LK. Development of a lectin microarray for the rapid analysis of protein glycopatterns. Chembiochem 2005; 6:985-989.
21. 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.
22. Toyoda M, Yamazaki-Inoue M, Itakura Y, et al. Lectin microarray analysis of pluripotent and multipotent stem cells. Genes Cells 2011; 16:1-11.
23. Honore C, Rorvig S, Hummelshoj T, Skjoedt MO, Borregaard N, Garred P. Tethering of Ficolin-1 to cell surfaces through recognition of sialic acid by the fibrinogen-like domain. J Leukoc Biol 2010; 88:145-158.
24. Marquardt T, Brune T, Luhn K, et al. Leukocyte adhesion deficiency II syndrome, a generalized defect in fucose metabolism. J Pediatr 1999; 134:681-688.
25. Rossi SL, Nistor G, Wyatt T, et al. Histological and functional benefit following transplantation of motor neuron progenitors to the injured rat spinal cord. PLoS One 2010; 5:e11852.
26. Becker DJ, Lowe JB. Fucose: Biosynthesis and biological function in mammals. Glycobiology 2003; 13:41R-53R.
27. Harduin-Lepers A. Comprehensive analysis of sialyltransferases in vertebrate genomes. Glycobiol Insights 2010; 2010:29-61.
28. Draber P, Stanley P. Cytotoxicity of plant lectins for mouse embryonal carcinoma cells. Somat Cell Mol Genet 1984; 10:435-443.
29. Kosmehl H, Langbein L, Katenkamp D. Lectin histochemistry of human testicular germ cell tumors. Neoplasma 1989; 36:29-39.
30. Lee MC, Talerman A, Oosterhuis JW, Damjanov I. Lectin histochemistry of classic and spermatocytic seminoma. Arch Pathol Lab Med 1985; 109:938-942.
31. Muramatsu T, Gachelin G, Damonneville M, Delarbre C, Jacob F. Cell surface carbohydrates of embryonal carcinoma cells: Polysaccharidic side chains of F9 antigens and of receptors to two lectins, FBP and PNA. Cell 1979; 18:183-191.
32. Teshima S, Hirohashi S, Shimosato Y, et al. Histochemically demonstrable changes in cell surface carbohydrates of human germ cell tumors. Lab Invest 1984; 50:271-277.
33. Traving C, Schauer R. Structure, function and metabolism of sialic acids. Cell Mol Life Sci 1998; 54:1330-1349.
34. Landmesser L, Dahm L, Tang JC, Rutishauser U. Polysialic acid as a regulator of intramuscular nerve branching during embryonic-development. Neuron 1990; 4:655-667.
35. Shi SL, Stanley P. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc Natl Acad Sci USA 2003; 100:5234-5239.
36. Schwarzkopf M, Knobeloch KP, Rohde E, et al. Sialylation is essential for early development in mice. Proc Natl Acad Sci USA 2002; 99:5267-5270.
37. Spiro RG. Protein glycosylation: Nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 2002; 12:43R-56R.
38. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872.
39. Xue H, Wu S, Papadeas ST, et al. A targeted neuroglial reporter line generated by homologous recombination in human embryonic stem cells. Stem Cells 2009; 27:1836-1846.
40. Swistowski A, Peng J, Han Y, Swistowska AM, Rao MS, Zeng X. Xeno-free defined conditions for culture of human embryonic stem cells, neural stem cells and dopaminergic neurons derived from them. PLoS One 2009; 4:e6233.
41. Gertow K, Przyborski S, Loring JF, et al. Isolation of human embryonic stem cell-derived teratomas for the assessment of pluripotency. Curr Protoc Stem Cell Biol 2007; Chapter 1:Unit1B.4.
42. Ku S, Soragni E, Campau E, et al. Friedreich's ataxia induced pluripotent stem cells model intergenerational GAATTC triplet repeat instability. Cell Stem Cell 2010; 7:631-637.