Glycomics of bone marrow-derived mesenchymal stem cells can be used to evaluate their cellular differentiation stage

Glycoconjugate Journal

Volumn 26, Issue 3, 2009, Pages 367-384

  Heiskanen, Annamari ^b   Hirvonen, Tia ^a   Salo, Hanna ^b   Impola, Ulla ^a   Olonen, Anne ^b   Laitinen, Anita ^a   Tiitinen, Sari ^a   Natunen, Suvi ^a   Aitio, Olli ^d   Miller Podraza, Halina ^f   Wuhrer, Manfred ^e   Deelder, André M ^e   Natunen, Jari ^b   Laine, Jarmo ^a   Lehenkari, Petri ^c   Saarinen, Juhani ^b   Satomaa, Tero ^b   Valmu, Leena ^a  

^a FINNISH RED CROSS BLOOD SERVICE   (Finland)

^b GLYKOS FINLAND LTD   (Finland)

^c UNIVERSITY OF OULU   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Differentiation; Exoglycosidase; Glycomics; Mass spectrometry; Mesenchymal stem cells

Indexed keywords

BLOOD GROUP ANTIGEN; EPITOPE; GLYCAN DERIVATIVE; LEWIS X ANTIGEN; MANNOSE; POLY N ACETYLLACTOSAMINE; STAGE SPECIFIC EMBRYO ANTIGEN 4; SULFATE; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MEMBRANE; CONFERENCE PAPER; GLYCOBIOLOGY; GLYCOSYLATION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; SIALYLATION;

BONE MARROW CELLS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; FLOW CYTOMETRY; GLYCOMICS; HUMANS; MASS SPECTROMETRY; MESENCHYMAL STEM CELLS; MOLECULAR SEQUENCE DATA; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS;

EID: 62449124523     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-008-9217-6     Document Type: Conference Paper

References (75)

1. K.E. Moore J.F. Mills M.M. Thornton 2006 Alternative sources of adult stem cells: a possible solution to the embryonic stem cell debate Gend. Med. 3 161 168
2. A. Pessina L. Gribaldo 2006 The key role of adult stem cells: therapeutic perspectives Curr. Med. Res. Opin. 22 2287 2300
3. C.D. Porada E.D. Zanjani G. meida-Porad 2006 Adult mesenchymal stem cells: a pluripotent population with multiple applications Curr. Stem Cell Res. Ther. 1 365 369
4. D.J. Prockop 1997 Marrow stromal cells as stem cells for nonhematopoietic tissues Science 276 71 74
5. G.Y. Rochefort B. Delorme A. Lopez O. Herault P. Bonnet P. Charbord V. Eder J. Domenech 2006 Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia Stem Cells 24 2202 2208
6. K. Bieback S. Kern H. Kluter H. Eichler 2004 Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood Stem Cells 22 625 634
7. A. Erices P. Conget J.J. Minguell 2000 Mesenchymal progenitor cells in human umbilical cord blood Br. J. Haematol. 109 235 242
8. D.G. Katritsis P. Sotiropoulou E. Giazitzoglou E. Karvouni M. Papamichail 2007 Electrophysiological effects of intracoronary transplantation of autologous mesenchymal and endothelial progenitor cells Europace 9 167 171
9. N. Zaidi A.J. Nixon 2007 Stem cell therapy in bone repair and regeneration Ann. N Y Acad.Sci. 1117 62 72
10. E.M. Horwitz P.L. Gordon W.K. Koo J.C. Marx M.D. Neel R.Y. McNall L. Muul T. Hofmann 2002 Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone Proc. Natl. Acad. Sci. U S A 99 8932 8937
11. B.K. Le I. Rasmusson B. Sundberg C. Gotherstrom M. Hassan M. Uzunel O. Ringden 2004 Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells Lancet 363 1439 1441
12. G.A. Moviglia V.R. Fernandez J.A. Brizuela J. Saslavsky F. Vrsalovic G. Varela F. Bastos P. Farina G. Etchegaray M. Barbieri G. Martinez F. Picasso Y. Schmidt P. Brizuela C.A. Gaeta H. Costanzo M.T. Moviglia Brandolino S. Merino M.E. Pes M.J. Veloso C. Rugilo I. Tamer G.S. Shuster 2006 Combined protocol of cell therapy for chronic spinal cord injury. Report on the electrical and functional recovery of two patients Cytotherapy 8 202 209
13. A. Varki 1993 Biological roles of oligosaccharides: all of the theories are correct Glycobiology 3 97 130
14. R.S. Haltiwanger J.B. Lowe 2004 Role of glycosylation in development Annu. Rev. Biochem. 73 491 537
15. K. Ohtsubo J.D. Marth 2006 Glycosylation in cellular mechanisms of health and disease Cell 126 855 867
16. R.K. Yu M. Yanagisawa 2006 Glycobiology of neural stem cells CNS Neurol. Disord. Drug Targets 5 415 423
17. J.D. Marth 1994 Will the transgenic mouse serve as a Rosetta Stone to glycoconjugate function? Glycoconj J. 11 3 8
18. J.B. Lowe J.D. Marth 2003 A genetic approach to mammalian glycan function Annu. Rev. Biochem. 72 643 691
19. P. Gagneux A. Varki 1999 Evolutionary considerations in relating oligosaccharide diversity to biological function Glycobiology 9 747 755
20. P.M. Lanctot F.H. Gage A.P. Varki 2007 The glycans of stem cells Curr. Opin. Chem. Biol. 11 373 380
21. T. Muramatsu H. Muramatsu 2004 Carbohydrate antigens expressed on stem cells and early embryonic cells Glycoconj. J. 21 41 45
22. A. Venable M. Mitalipova I. Lyons K. Jones S. Shin M. Pierce S. Stice 2005 Lectin binding profiles of SSEA-4 enriched, pluripotent human embryonic stem cell surfaces BMC Dev. Biol. 5 15
23. K.A. Wearne H.C. Winter K. O'Shea I.J. Goldstein 2006 Use of lectins for probing differentiated human embryonic stem cells for carbohydrates Glycobiology 16 981 990
24. K.A. Wearne H.C. Winter I.J. Goldstein 2008 Temporal changes in the carbohydrates expressed on BG01 human embryonic stem cells during differentiation as embryoid bodies Glycoconj. J. 25 121 136
25. G. Badcock C. Pigott J. Goepel P.W. Andrews 1999 The human embryonal carcinoma marker antigen TRA-1-60 is a sialylated keratan sulfate proteoglycan Cancer Res. 59 4715 4719
26. R. Kannagi N.A. Cochran F. Ishigami S. Hakomori P.W. Andrews B.B. Knowles D. Solter 1983 Stage-specific embryonic antigens (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells EMBO J. 2 2355 2361
27. O. Adewumi B. Aflatoonian L. hrlund-Richter M. Amit P.W. Andrews G. Beighton P.A. Bello N. Benvenisty L.S. Berry S. Bevan B. Blum J. Brooking K.G. Chen A.B. Choo G.A. Churchill M. Corbel I. Damjanov J.S. Draper P. Dvorak K. Emanuelsson R.A. Fleck A. Ford K. Gertow M. Gertsenstein P.J. Gokhale R.S. Hamilton A. Hampl L.E. Healy O. Hovatta J. Hyllner M.P. Imreh J. Itskovitz-Eldor J. Jackson J.L. Johnson M. Jones K. Kee B.L. King B.B. Knowles M. Lako F. Lebrin B.S. Mallon D. Manning Y. Mayshar R.D. McKay A.E. Michalska M. Mikkola M. Mileikovsky S.L. Minger H.D. Moore C.L. Mummery A. Nagy N. Nakatsuji C.M. O'Brien S.K. Oh C. Olsson T. Otonkoski K.Y. Park R. Passier H. Patel M. Patel R. Pedersen M.F. Pera M.S. Piekarczyk R.A. Pera B.E. Reubinoff A.J. Robins J. Rossant P. Rugg-Gunn T.C. Schulz H. Semb E.S. Sherrer H. Siemen G.N. Stacey M. Stojkovic H. Suemori J. Szatkiewicz T. Turetsky T. Tuuri B.S. van den K. Vintersten S. Vuoristo D. Ward T.A. Weaver L.A. Young W. Zhang 2007 Characterization of human embryonic stem cell lines by the International Stem Cell Initiative Nat. Biotechnol. 25 803 816
28. H. Hemmoranta T. Satomaa M. Blomqvist A. Heiskanen O. Aitio J. Saarinen J. Natunen J. Partanen J. Laine T. Jaatinen 2007 N-glycan structures and associated gene expression reflect the characteristic N-glycosylation pattern of human hematopoietic stem and progenitor cells Exp. Hematol. 35 1279 1292
29. H.V. Leskelä J. Risteli S. Niskanen J. Koivunen K.K. Ivaska P. Lehenkari 2003 Osteoblast recruitment from stem cells does not decrease by age at late adulthood Biochem. Biophys. Res. Commun. 311 1008 1013
30. A. Heiskanen T. Satomaa S. Tiitinen A. Laitinen S. Mannelin U. Impola M. Mikkola C. Olsson H. Miller-Podraza M. Blomqvist A. Olonen H. Salo P. Lehenkari T. Tuuri T. Otonkoski J. Natunen J. Saarinen J. Laine 2007 N-glycolylneuraminic acid xenoantigen contamination of human embryonic and mesenchymal stem cells is substantially reversible Stem Cells 25 197 202
31. Y. Huang Y. Mechref M.V. Novotny 2001 Microscale nonreductive release of O-linked glycans for subsequent analysis through MALDI mass spectrometry and capillary electrophoresis Anal. Chem. 73 6063 6069
32. H. Miller-Podraza B. Lanne J. Angstrom S. Teneberg M.A. Milh P.A. Jovall H. Karlsson K.A. Karlsson 2005 Novel binding epitope for Helicobacter pylori found in neolacto carbohydrate chains: structure and cross-binding properties J. Biol. Chem. 280 19695 19703
33. K. Aoki M. Perlman J.M. Lim R. Cantu L. Wells M. Tiemeyer 2007 Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo J. Biol. Chem. 282 9127 9142
34. P. Kang Y. Mechref I. Klouckova M.V. Novotny 2005 Solid-phase permethylation of glycans for mass spectrometric analysis Rapid Commun. Mass Spectrom. 19 3421 3428
35. M.J. Martin A. Muotri F. Gage A. Varki 2005 Human embryonic stem cells express an immunogenic nonhuman sialic acid Nat. Med. 11 228 232
36. D. Fu L. Chen R.A. O'Neill 1994 A detailed structural characterization of ribonuclease B oligosaccharides by 1H NMR spectroscopy and mass spectrometry Carbohydr. Res. 261 173 186
37. K. Hard Z.G. Van P. Moonen J.P. Kamerling F.G. Vliegenthart 1992 The Asn-linked carbohydrate chains of human Tamm-Horsfall glycoprotein of one male. Novel sulfated and novel N-acetylgalactosamine-containing N-linked carbohydrate chains Eur. J. Biochem. 209 895 915
38. J. Helin H. Maaheimo A. Seppo A. Keane O. Renkonen 1995 Stepwise transfer of alpha-D-Galp-(1->3)-beta-D-Galp-(1->4)-beta-D-GlcpNAc sequences to 3-OH and 6-OH of distal galactose residues in bi-, tri-, and tetra-antennary asialo-glycans of N-linked complex type Carbohydr. Res. 266 191 209
39. J.S. Draper C. Pigott J.A. Thomson P.W. Andrews 2002 Surface antigens of human embryonic stem cells: changes upon differentiation in culture J. Anat. 200 249 258
40. M. Fukuda M.N. Fukuda S. Hakomori 1979 Developmental change and genetic defect in the carbohydrate structure of band 3 glycoprotein of human erythrocyte membrane J. Biol. Chem. 254 3700 3703
41. H. Leffler S. Carlsson M. Hedlund Y. Qian F. Poirier 2004 Introduction to galectins Glycoconj. J. 19 433 440
42. A. Leppänen S. Stowell O. Blixt R.D. Cummings 2005 Dimeric galectin-1 binds with high affinity to alpha2,3-sialylated and non-sialylated terminal N-acetyllactosamine units on surface-bound extended glycans J. Biol. Chem. 280 5549 5562
43. S.R. Stowell M. as-Baruffi L. Penttila O. Renkonen A.K. Nyame R.D. Cummings 2004 Human galectin-1 recognition of poly-N-acetyllactosamine and chimeric polysaccharides Glycobiology 14 157 167
44. S.R. Stowell C.M. Arthur P. Mehta K.A. Slanina O. Blixt H. Leffler D.F. Smith R.D. Cummings 2008 Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens J. Biol. Chem. 283 10109 10123
45. T. Kadri J.J. Lataillade C. Doucet A. Marie I. Ernou P. Bourin R. Joubert-Caron M. Caron D. Lutomski 2005 Proteomic study of Galectin-1 expression in human mesenchymal stem cells Stem Cells Dev. 14 204 212
46. L.G. Baum D.P. Blackall S. rias-Magallano D. Nanigian S.Y. Uh J.M. Browne D. Hoffmann C.E. Emmanouilides M.C. Territo G.C. Baldwin 2003 Amelioration of graft versus host disease by galectin-1 Clin. Immunol. 109 295 307
47. J. Chan K. O'Donoghue M. Gavina Y. Torrente N. Kennea H. Mehmet H. Stewart D.J. Watt J.E. Morgan N.M. Fisk 2006 Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration Stem Cells 24 1879 1891
48. J.A. Thomson J. Itskovitz-Eldor S.S. Shapiro M.A. Waknitz J.J. Swiergiel V.S. Marshall J.M. Jones 1998 Embryonic stem cell lines derived from human blastocysts Science 282 1145 1147
49. S.N. Brimble E.S. Sherrer E.W. Uhl E. Wang S. Kelly A.H. Merrill Jr. A.J. Robins T.C. Schulz 2007 The cell surface glycosphingolipids SSEA-3 and SSEA-4 are not essential for human ESC pluripotency Stem Cells 25 54 62
50. E.J. Gang D. Bosnakovski C.A. Figueiredo J.W. Visser R.C. Perlingeiro 2007 SSEA-4 identifies mesenchymal stem cells from bone marrow Blood 109 1743 1751
51. V.L. Battula P.M. Bareiss S. Treml S. Conrad I. Albert S. Hojak H. Abele B. Schewe L. Just T. Skutella H.J. Buhring 2007 Human placenta and bone marrow derived MSC cultured in serum-free, b-FGF-containing medium express cell surface frizzled-9 and SSEA-4 and give rise to multilineage differentiation Differentiation 75 279 291
52. I. Peiffer P. Eid R. Barbet M.L. Li R.A. Oostendorp V. Haydont M.N. Monier L. Milon N. Fortunel P. Charbord M. Tovey J. Hatzfeld A. Hatzfeld 2007 A sub-population of high proliferative potential-quiescent human mesenchymal stem cells is under the reversible control of interferon alpha/beta Leukemia 21 714 724
53. M.G. Roubelakis K.I. Pappa V. Bitsika D. Zagoura A. Vlahou H.A. Papadaki A. Antsaklis N.P. Anagnou 2007 Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cells Stem Cells Dev. 16 931 952
54. P.V. Guillot C. Gotherstrom J. Chan H. Kurata N.M. Fisk 2007 Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC Stem Cells 25 646 654
55. C. Martinez T.J. Hofmann R. Marino M. Dominici E.M. Horwitz 2007 Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs Blood 109 4245 4248
56. D.H. Kwak K. Yu S.M. Kim D.H. Lee S.M. Kim J.U. Jung J.W. Seo N. Kim S. Lee K.Y. Jung H.K. You H.A. Kim Y.K. Choo 2006 Dynamic changes of gangliosides expression during the differentiation of embryonic and mesenchymal stem cells into neural cells Exp. Mol. Med. 38 668 676
57. A. Varki T. Angata 2006 Siglecs-the major subfamily of I-type lectins Glycobiology 16 1R 27R
58. S.D. Rosen 1999 Endothelial ligands for L-selectin: from lymphocyte recirculation to allograft rejection Am. J. Pathol. 155 1013 1020
59. B. Muller C. Prante M. Gastens J. Kuhn K. Kleesiek C. Gotting 2008 Increased levels of xylosyltransferase I correlate with the mineralization of the extracellular matrix during osteogenic differentiation of mesenchymal stem cells Matrix Biol. 27 139 149
60. F. Liu L. Malaval J.E. Aubin 2003 Global amplification polymerase chain reaction reveals novel transitional stages during osteoprogenitor differentiation J. Cell Sci. 116 1787 1796
61. R.J. Midura D.J. McQuillan K.J. Benham L.W. Fisher V.C. Hascall 1990 A rat osteogenic cell line (UMR 106-01) synthesizes a highly sulfated form of bone sialoprotein J. Biol. Chem. 265 5285 5291
62. J. Zaia R. Boynton D. Heinegard F. Barry 2001 Posttranslational modifications to human bone sialoprotein determined by mass spectrometry Biochemistry 40 12983 12991
63. K. Ley 2003 The role of selectins in inflammation and disease Trends Mol. Med. 9 263 268
64. J.L. Magnani 2004 The discovery, biology, and drug development of sialyl Lea and sialyl Lex Arch. Biochem. Biophys. 426 122 131
65. A. Hidalgo P.S. Frenette 2005 Enforced fucosylation of neonatal CD34+ cells generates selectin ligands that enhance the initial interactions with microvessels but not homing to bone marrow Blood 105 567 575
66. L. Xia J.M. McDaniel T. Yago A. Doeden R.P. McEver 2004 Surface fucosylation of human cord blood cells augments binding to P-selectin and E-selectin and enhances engraftment in bone marrow Blood 104 3091 3096
67. R. Sackstein J.S. Merzaban D.W. Cain N.M. Dagia J.A. Spencer C.P. Lin R. Wohlgemuth 2008 Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone Nat. Med. 14 181 187
68. B. Ruster S. Gottig R.J. Ludwig R. Bistrian S. Muller E. Seifried J. Gille R. Henschler 2006 Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells Blood 108 3938 3944
69. P.P. Wilkins R.P. McEver R.D. Cummings 1996 Structures of the O-glycans on P-selectin glycoprotein ligand-1 from HL-60 cells J. Biol. Chem. 271 18732 18742
70. M. Lenter A. Levinovitz S. Isenmann D. Vestweber 1994 Monospecific and common glycoprotein ligands for E- and P-selectin on myeloid cells J. Cell Biol. 125 471 481
71. C.J. Dimitroff J.Y. Lee R.C. Fuhlbrigge R. Sackstein 2000 A distinct glycoform of CD44 is an L-selectin ligand on human hematopoietic cells Proc. Natl. Acad. Sci. U S A 97 13841 13846
72. T. Hennet D. Chui J.C. Paulson J.D. Marth 1998 Immune regulation by the ST6Gal sialyltransferase Proc. Natl. Acad. Sci. USA 95 4504 4509
73. M. Takahata N. Iwasaki H. Nakagawa Y. Abe T. Watanabe M. Ito T. Majima A. Minami 2007 Sialylation of cell surface glycoconjugates is essential for osteoclastogenesis Bone 41 77 86
74. J.J. Priatel D. Chui N. Hiraoka C.J. Simmons K.B. Richardson D.M. Page M. Fukuda N.M. Varki J.D. Marth 2000 The ST3Gal-I sialyltransferase controls CD8+ T lymphocyte homeostasis by modulating O-glycan biosynthesis Immunity 12 273 283
75. T.P. Skelton C. Zeng A. Nocks I. Stamenkovic 1998 Glycosylation provides both stimulatory and inhibitory effects on cell surface and soluble CD44 binding to hyaluronan J. Cell Biol. 140 431 446