Changes in glycosaminoglycan structure on differentiation of human embryonic stem cells towards mesoderm and endoderm lineages

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 6, 2014, Pages 1993-2003

  Gasimli, Leyla ^a   Hickey, Anne Marie ^a   Yang, Bo ^b   Li, Guoyun ^b   Dela Rosa, Mitche ^c   Nairn, Alison V ^c   Kulik, Michael J ^d   Dordick, Jonathan S ^a,e   Moremen, Kelley W ^c   Dalton, Stephen ^d   Linhardt, Robert J ^a,b,e  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b Research Rensselaer Polytechnic Institute   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d Department of Biochemistry and Molecular Biology University of Georgia ^*  (United States)

^e RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Embryonic; Glycosaminoglycan; Hepatocytes; Proteoglycans; Splanchnic mesoderm; Stem cells

Indexed keywords

6 O SULFOTRANSFERASE 2; 6 O SULFOTRANSFERASE 3; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; N DEACETYLASE N SULFOTRANSFERASE 1; SULFOTRANSFERASE; UNCLASSIFIED DRUG; AGGRECAN; AGRIN; BIGLYCAN; BREVICAN; CD74 ANTIGEN; DECORIN; FIBROMODULIN; GLYPICAN 1; GLYPICAN 3; HERMES ANTIGEN; LUMICAN; NEUROCAN; PERLECAN; SYNDECAN 1; SYNDECAN 2; SYNDECAN 3; SYNDECAN 4; THROMBOMODULIN; VERSICAN;

ARTICLE; CARBOHYDRATE ANALYSIS; CELL DIFFERENTIATION; CELL FATE; CHEMICAL MODIFICATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; GENE; GENE EXPRESSION; GLYCOSAMINOGLYCAN METABOLISM; HS6ST2 GENE; HS6ST3 GENE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; LIVER CELL; MESODERM; NDST1 GENE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; CELL LINEAGE; GENETIC TRANSCRIPTION; MULTIPOTENT STEM CELL; PLURIPOTENT STEM CELL LINE; PROTEIN EXPRESSION;

EMBRYONIC; GLYCOSAMINOGLYCAN; HEPATOCYTES; PROTEOGLYCANS; SPLANCHNIC MESODERM; STEM CELLS;

CELL DIFFERENTIATION; CELL LINEAGE; EMBRYONIC STEM CELLS; ENDODERM; GLYCOSAMINOGLYCANS; HEPATOCYTES; HUMANS; MESODERM; PROTEOGLYCANS;

EID: 84897424280     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.01.007     Document Type: Article

References (50)

1. S. He, D. Nakada, and S.J. Morrison Mechanisms of stem cell self-renewal Annu. Rev. Cell Dev. Biol. 25 2009 377 406
2. L.A. Boyer, T.I. Lee, M.F. Cole, S.E. Johnstone, S.S. Levine, J.P. Zucker, M.G. Guenther, R.M. Kumar, H.L. Murray, R.G. Jenner, D.K. Gifford, D.A. Melton, R. Jaenisch, and R.A. Young Core transcriptional regulatory circuitry in human embryonic stem cells Cell 122 2005 947 956
3. J. Kim, J. Chu, X. Shen, J. Wang, and S.H. Orkin An extended transcriptional network for pluripotency of embryonic stem cells Cell 132 2008 1049 1061
4. X. Chen, H. Xu, P. Yuan, F. Fang, M. Huss, V.B. Vega, E. Wong, Y.L. Orlov, W. Zhang, J. Jiang, Y.H. Loh, H.C. Yeo, Z.X. Yeo, V. Narang, K.R. Govindarajan, B. Leong, A. Shahab, Y. Ruan, G. Bourque, W.K. Sung, N.D. Clarke, C.L. Wei, and H.H. Ng Integration of external signaling pathways with the core transcriptional network in embryonic stem cells Cell 133 2008 1106 1117
5. A. Marson, S.S. Levine, M.F. Cole, G.M. Frampton, T. Brambrink, S. Johnstone, M.G. Guenther, W.K. Johnston, M. Wernig, J. Newman, J.M. Calabrese, L.M. Dennis, T.L. Volkert, S. Gupta, J. Love, N. Hannett, P.A. Sharp, D.P. Bartel, R. Jaenisch, and R.A. Young Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells Cell 134 2008 521 533
6. L. He, J.M. Thomson, M.T. Hemann, E. Hernando-Monge, D. Mu, S. Goodson, S. Powers, C. Cordon-Cardo, S.W. Lowe, G.J. Hannon, and S.M. Hammond A microRNA polycistron as a potential human oncogene Nature 435 2005 828 833
7. Y. Wang, S. Baskerville, A. Shenoy, J.E. Babiarz, L. Baehner, and R. Blelloch Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation Nat. Genet. 40 2008 1478 1483
8. Z. Lichner, E. Pall, A. Kerekes, E. Pallinger, P. Maraghechi, Z. Bosze, and E. Gocza The miR-290-295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells Differentiation 81 2011 11 24
9. Y. Tay, J. Zhang, A.M. Thomson, B. Lim, and I. Rigoutsos MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation Nature 455 2008 1124 1128
10. C. Melton, R.L. Judson, and R. Blelloch Opposing microRNA families regulate self-renewal in mouse embryonic stem cells Nature 463 2010 621 626
11. M. Ly, T.N. Laremore, and R.J. Linhardt Proteoglycomics: recent progress and future challenges OMICS 14 2010 389 399
12. A.D. Lander, and S.B. Selleck The elusive functions of proteoglycans: in vivo veritas J. Cell Biol. 148 2000 227 232
13. L. Kjellen, and U. Lindahl Proteoglycans: structures and interactions Annu. Rev. Biochem. 60 1991 443 475
14. M. Bernfield, M. Gotte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, and M. Zako Functions of cell surface heparan sulfate proteoglycans Annu. Rev. Biochem. 68 1999 729 777
15. A. Yoneda, and J.R. Couchman Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans Matrix Biol. 22 2003 25 33
16. R.J. Linhardt, and T. Toida Role of glycosaminoglycans in cellular communication Acc. Chem. Res. 37 2004 431 438
17. J.D. Esko, K. Kimata, and U. Lindahl Proteoglycans and sulfated glycosaminoglycans A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, M.E. Etzler, Essentials of Glycobiology 2nd ed. 2009 Cold Spring Harbor NY 229 248
18. A. Horowitz, M. Murakami, Y. Gao, and M. Simons Phosphatidylinositol-4,5- bisphosphate mediates the interaction of syndecan-4 with protein kinase C Biochemistry 38 1999 15871 15877
19. E.S. Oh, A. Woods, S.T. Lim, A.W. Theibert, and J.R. Couchman Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity J. Biol. Chem. 273 1998 10624 10629
20. L. Gasimli, R.J. Linhardt, and J.S. Dordick Proteoglycans in stem cells Biotechnol. Appl. Biochem. 59 2012 65 76
21. M. Inatani, F. Irie, A.S. Plump, M. Tessier-Lavigne, and Y. Yamaguchi Mammalian brain morphogenesis and midline axon guidance require heparan sulfate Science 302 2003 1044 1046
22. S. Kuriyama, and R. Mayor A role for Syndecan-4 in neural induction involving ERK- and PKC-dependent pathways Development 136 2009 575 584
23. A.V. Nairn, A. Kinoshita-Toyoda, H. Toyoda, J. Xie, K. Harris, S. Dalton, M. Kulik, J.M. Pierce, T. Toida, K.W. Moremen, and R.J. Linhardt Glycomics of proteoglycan biosynthesis in murine embryonic stem cell differentiation J. Proteome Res. 6 2007 4374 4387
24. C.E. Johnson, B.E. Crawford, M. Stavridis, G. Ten Dam, A.L. Wat, G. Rushton, C.M. Ward, V. Wilson, T.H. van Kuppevelt, J.D. Esko, A. Smith, J.T. Gallagher, and C.L. Merry Essential alterations of heparan sulfate during the differentiation of embryonic stem cells to Sox1-enhanced green fluorescent protein-expressing neural progenitor cells Stem Cells 25 2007 1913 1923
25. L. Bu, X. Jiang, S. Martin-Puig, L. Caron, S. Zhu, Y. Shao, D.J. Roberts, P.L. Huang, I.J. Domian, and K.R. Chien Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages Nature 460 2009 113 117
26. C.N. Medine, B. Lucendo-Villarin, W. Zhou, C.C. West, and D.C. Hay Robust generation of hepatocyte-like cells from human embryonic stem cell populations J. Vis. Exp. 56 2011 e2969
27. B. Li, H. Liu, Z. Zhang, H.E. Stansfield, J.S. Dordick, and R.J. Linhardt Analysis of glycosaminoglycans in stem cell glycomics Methods Mol. Biol. 690 2011 285 300
28. A.V. Nairn, W.S. York, K. Harris, E.M. Hall, J.M. Pierce, and K.W. Moremen Regulation of glycan structures in animal tissues: transcript profiling of glycan-related genes J. Biol. Chem. 283 2008 17298 17313
29. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29 2001 e45
30. F. Zhang, P. Sun, E. Munoz, L. Chi, S. Sakai, T. Toida, H. Zhang, S. Mousa, and R.J. Linhardt Microscale isolation and analysis of heparin from plasma using an anion-exchange spin column Anal. Biochem. 353 2006 284 286
31. D. Shaya, A. Tocilj, Y. Li, J. Myette, G. Venkataraman, R. Sasisekharan, and M. Cygler Crystal structure of heparinase II from Pedobacter heparinus and its complex with a disaccharide product J. Biol. Chem. 281 2006 15525 15535
32. E. Yoshida, S. Arakawa, T. Matsunaga, S. Toriumi, S. Tokuyama, K. Morikawa, and Y. Tahara Cloning, sequencing, and expression of the gene from bacillus circulans that codes for a heparinase that degrades both heparin and heparan sulfate Biosci. Biotechnol. Biochem. 66 2002 1873 1879
33. B. Yang, A. Weyers, J.Y. Baik, E. Sterner, S. Sharfstein, S.A. Mousa, F. Zhang, J.S. Dordick, and R.J. Linhardt Ultra-performance ion-pairing liquid chromatography with on-line electrospray ion trap mass spectrometry for heparin disaccharide analysis Anal. Biochem. 415 2011 59 66
34. J. Dahlstrand, L.B. Zimmerman, R.D. McKay, and U. Lendahl Characterization of the human nestin gene reveals a close evolutionary relationship to neurofilaments J. Cell Sci. 103 Pt 2 1992 589 597
35. E.D. Wederell, M. Bilenky, R. Cullum, N. Thiessen, M. Dagpinar, A. Delaney, R. Varhol, Y. Zhao, T. Zeng, B. Bernier, M. Ingham, M. Hirst, G. Robertson, M.A. Marra, S. Jones, and P.A. Hoodless Global analysis of in vivo Foxa2-binding sites in mouse adult liver using massively parallel sequencing Nucleic Acids Res. 36 2008 4549 4564
36. G.P. Hayhurst, Y.H. Lee, G. Lambert, J.M. Ward, and F.J. Gonzalez Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis Mol. Cell. Biol. 21 2001 1393 1403
37. K. Sugahara, and H. Kitagawa Heparin and heparan sulfate biosynthesis IUBMB Life 54 2002 163 175
38. K. Hirano, T.H. Van Kuppevelt, and S. Nishihara The transition of mouse pluripotent stem cells from the naive to the primed state requires Fas signaling through 3-O sulfated heparan sulfate structures recognized by the HS4C3 antibody Biochem. Biophys. Res. Commun. 430 2013 1175 1181
39. L. Zhang, R. Lawrence, B.A. Frazier, and J.D. Esko CHO glycosylation mutants: proteoglycans Methods Enzymol. 416 2006 205 221
40. M. Dolhnikoff, J. Morin, P.J. Roughley, and M.S. Ludwig Expression of lumican in human lungs Am. J. Respir. Cell Mol. Biol. 19 1998 582 587
41. P.K. Cornuet, T.C. Blochberger, and J.R. Hassell Molecular polymorphism of lumican during corneal development Invest. Ophthalmol. Vis. Sci. 35 1994 870 877
42. R.A. Graham, T.C. Li, I.D. Cooke, and J.D. Aplin Keratan sulphate as a secretory product of human endometrium: cyclic expression in normal women Hum. Reprod. 9 1994 926 930
43. L. Olsson, M. Stigson, R. Perris, J.M. Sorrell, and J. Lofberg Distribution of keratan sulphate and chondroitin sulphate in wild type and white mutant axolotl embryos during neural crest cell migration Pigment Cell Res. 9 1996 5 17
44. R. Droguett, C. Cabello-Verrugio, C. Riquelme, and E. Brandan Extracellular proteoglycans modify TGF-beta bio-availability attenuating its signaling during skeletal muscle differentiation Matrix Biol. 25 2006 332 341
45. L. Gasimli, H.E. Stansfield, A.V. Nairn, H. Liu, J.L. Paluh, B. Yang, J.S. Dordick, K.W. Moremen, and R.J. Linhardt Structural remodeling of proteoglycans upon retinoic acid-induced differentiation of NCCIT cells Glycoconj. J. 30 2013 497 510
46. J. Filmus, M. Capurro, and J. Rast Glypicans Genome Biol. 9 2008 224
47. M. Abrink, M. Grujic, and G. Pejler Serglycin is essential for maturation of mast cell secretory granule J. Biol. Chem. 279 2004 40897 40905
48. B.P. Schick, H.C. Ho, K.C. Brodbeck, C.W. Wrigley, and J. Klimas Serglycin proteoglycan expression and synthesis in embryonic stem cells Biochim. Biophys. Acta 1593 2003 259 267
49. K. Hirano, N. Sasaki, T. Ichimiya, T. Miura, T.H. Van Kuppevelt, and S. Nishihara 3-O-sulfated heparan sulfate recognized by the antibody HS4C3 contribute to the differentiation of mouse embryonic stem cells via Fas signaling PLoS ONE 7 2012 e43440
50. T.G. Fernandes, S.J. Kwon, S.S. Bale, M.Y. Lee, M.M. Diogo, D.S. Clark, J.M. Cabral, and J.S. Dordick Three-dimensional cell culture microarray for high-throughput studies of stem cell fate Biotechnol. Bioeng. 106 2010 106 118