Derivation of stromal (Skeletal and Mesenchymal) stem-like cells from human embryonic stem cells

Stem Cells and Development

Volumn 21, Issue 17, 2012, Pages 3114-3124

  Mahmood, Amer ^a,b   Harkness, Linda ^b   Abdallah, Basem M ^b   Elsafadi, Mona ^a   Al Nbaheen, May S ^a   Aldahmash, Abdullah ^a,b   Kassem, Moustapha ^a,b  

^a KING KHALID UNIVERSITY HOSPITAL   (Saudi Arabia)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; CALCIUM PHOSPHATE; CD44V ANTIGEN; CD56 ANTIGEN; CD63 ANTIGEN; CD71 ANTIGEN; ENDOGLIN; HYDROXYAPATITE; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ARTICLE; BONE TISSUE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; EX VIVO STUDY; FEMALE; HUMAN; IN VIVO CULTURE; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELL LINE; CHONDROCYTES; EMBRYONIC STEM CELLS; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MESODERM; MICE; MICE, INBRED NOD; MICE, SCID; MUSCLE, SKELETAL; OSTEOBLASTS; OSTEOGENESIS; TERATOMA; VIMENTIN;

MUS;

EID: 84869041528     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0035     Document Type: Article

References (60)

1. Abdallah BM and Kassem M. (2008). Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther 15:109-116.
2. Stenderup K, Justesen J, Clausen C and Kassem M. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919-926. (Pubitemid 37543568)
3. Barberi T, Willis LM, Socci ND and Studer L. (2005). Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2:e161.
4. Barberi T, Bradbury M, Dincer Z, Panagiotakos G, Socci ND and Studer L. (2007). Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med 13:642-648. (Pubitemid 46828477)
5. Lian Q, Lye E, Suan Yeo K, Khia Way Tan E, Salto-Tellez M, Liu TM, Palanisamy N, El Oakley RM, Lee EH, Lim B and Lim SK. (2007). Derivation of Clinically Compliant MSCs from CD105 +, CD24-Differentiated Human ESCs. Stem Cells 25:425-436. (Pubitemid 46232798)
6. Trivedi P and Hematti P. (2007). Simultaneous generation of CD34 + primitive hematopoietic cells and CD73 + mesenchymal stem cells from human embryonic stem cells cocultured with murine OP9 stromal cells. Exp Hematol 35:146-154. (Pubitemid 46014371)
7. Mahmood A, Harkness L, Schroder HD, Abdallah BM and Kassem M. (2010). Enhanced differentiation of human embryonic stem cells to mesenchymal progenitors by inhibition of TGF-beta/activin/nodal signaling using SB-431542. J Bone Miner Res 25:1216-1233.
8. Hyslop LA, Armstrong L, Stojkovic M and Lako M. (2005). Human embryonic stem cells: biology and clinical implications. Expert Rev Mol Med 7:1-21.
9. Itskovitz-Eldor J, Schuldiner M, Karsenti D, Eden A, Yanuka O, Amit M, Soreq H and Benvenisty N. (2000). Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 6:88-95.
10. Cai J, Chen J, Liu Y, Miura T, Luo Y, Loring JF, Freed WJ, Rao MS and Zeng X. (2006). Assessing self-renewal and differentiation in human embryonic stem cell lines. Stem Cells 24:516-530. (Pubitemid 44464756)
11. Olivier EN, Rybicki AC and Bouhassira EE. (2006). Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 24:1914-1922. (Pubitemid 44474167)
12. Bielby RC, Boccaccini AR, Polak JM and Buttery LDK. (2004). In Vitro Differentiation and In Vivo Mineralization of Osteogenic Cells Derived from Human Embryonic Stem Cells. Tissue Eng 10:1518-1525. (Pubitemid 39557855)
13. Sottile V and Seuwen K. (2000). Bone morphogenetic protein-2 stimulates adipogenic differentiation of mesenchymal precursor cells in synergy with BRL 49653 (rosiglitazone). FEBS Lett 475:201-204. (Pubitemid 30408453)
14. Cowan CA, Klimanskaya I, McMahon J, Atienza J, Witmyer J, Zucker JP, Wang S, Morton CC, McMahon AP, Powers D and Melton DA. (2004). Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 350:1353-1356. (Pubitemid 38375373)
15. Larsen KH, Frederiksen CM, Burns JS, Abdallah BM, and Kassem M. (2010). Identifying a molecular phenotype for bone marrow stromal cells with in vivo bone-forming capacity. J Bone Miner Res 25:796-808.
16. Simonsen JL, Rosada C, Serakinci N, Justesen J, Stenderup K, Rattan SI, Jensen TG and Kassem M. (2002). Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 20: 592-596. (Pubitemid 34595153)
17. Abdallah BM, Ditzel N and Kassem M. (2008). Assessment of bone formation capacity using in vivo transplantation assays: procedure and tissue analysis. Methods Mol Biol 455:89-100.
18. Abdallah BM and Kassem M. (2009). The use of mesenchymal (skeletal) stem cells for treatment of degenerative diseases: current status and future perspectives. J Cell Physiol 218:9-12.
19. Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A and Simmons PJ. (2003). Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116:1827-1835. (Pubitemid 36582169)
20. Minguell JJ, Erices A and Conget P. (2001). Mesenchymal Stem Cells. Exp Biol Med 226:507-520. (Pubitemid 32524497)
21. Stenderup K, Rosada C, Justesen J, Al-Soubky T, gnaes-Hansen F and Kassem M. (2004). Aged human bone marrow stromal cells maintaining bone forming capacity in vivo evaluated using an improved method of visualization. Biogerontology 5:107-118. (Pubitemid 39137527)
22. Coucouvanis E and Martin GR. (1999). BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126:535-546. (Pubitemid 29082040)
23. Abe K, Niwa H, Iwase K, Takiguchi M, Mori M, Abe SI, Abe K and Yamamura KI. (1996). Endoderm-specific gene expression in embryonic stem cells differentiated to embryoid bodies. Exp Cell Res 229:27-34. (Pubitemid 26423931)
24. Coucouvanis E and Martin GR. (1995). Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83:279-287.
25. Conley BJ, Trounson AO and Mollard R. (2004). Human embryonic stem cells form embryoid bodies containing visceral endoderm-like derivatives. Fetal Diagn Ther 19:218-223. (Pubitemid 38469315)
26. Keller G. (2005). Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 19:1129-1155. (Pubitemid 40696181)
27. Hwang NS, Varghese S, Lee HJ, Zhang Z, Ye Z, Bae J, Cheng L and Elisseeff J. (2008). In vivo commitment and functional tissue regeneration using human embryonic stem cell-derived mesenchymal cells. Proc Natl Acad Sci U S A 105: 20641-20646.
28. Olivares-Navarrete R, Raines AL, Hyzy SL, Park JH, Hutton DL, Cochran DL, Boyan BD and Schwartz Z. (2012). Osteoblast maturation and new bone formation in response to titanium implant surface features are reduced with age. J Bone Miner Res. [Epub ahead of print]; DOI: 10.002/jbmr .1628.
29. Buttery L, Bielby R, Howard D and Shakesheff K. (2011). Osteogenic differentiation of embryonic stem cells in 2D and 3D culture. Methods Mol Biol 695:281-308.
30. Boyd NL, Dhara SK, Rekaya R, Godbey EA, Hasneen K, Rao RR, West FD, III, Gerwe BA and Stice SL. (2007). BMP4 Promotes Formation of Primitive Vascular Networks in Human Embryonic Stem Cell-Derived Embryoid Bodies. Exp Biol Med 232:833-843. (Pubitemid 46827826)
31. Harkness L, Mahmood A, Ditzel N, Abdallah BM, Nygaard JV and Kassem M. (2011). Selective isolation and differentiation of a stromal population of human embryonic stem cells with osteogenic potential. Bone 48:231-241.
32. Ullmann U, In't Veld P, Gilles C, Sermon K, De Rycke M, Van de Velde H, Van Steirteghem A and Liebaers I. (2007). Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions. Mol Hum Reprod 13:21-32. (Pubitemid 44942721)
33. Karp JM, Ferreira LS, Khademhosseini A, Kwon AH, Yeh J and Langer RS. (2006). Cultivation of human embryonic stem cells without the embryoid body step enhances osteogenesis in vitro. Stem Cells 24:835-843. (Pubitemid 44464716)
34. Vodyanik MA, Bork JA, Thomson JA and Slukvin II. (2005). Human embryonic stem cell-derived CD34 + cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 105:617-626. (Pubitemid 40070744)
35. Inanc B, Elcin AE and Elcin YM. (2007). Effect of osteogenic induction on the in vitro differentiation of human embryonic stem cells cocultured with periodontal ligament fibroblasts. Artif Organs 31:792-800. (Pubitemid 350131991)
36. Karner E, Unger C, Sloan AJ, hrlund-Richter L, Sugars RV and Wendel M. (2007). Bone matrix formation in osteogenic cultures derived from human embryonic stem cells in vitro. Stem Cells Dev 16:39-52. (Pubitemid 46362591)
37. Karner E, Unger C, Cerny R, hrlund-Richter L, Ganss B, Dilber MS and Wendel M. (2008). Differentiation of human embryonic stem cells into osteogenic or hematopoietic lineages: a dose-dependent effect of osterix over-expression. J Cell Physiol 218:323-333.
38. Kawaguchi J, Mee PJ and Smith AG. (2005). Osteogenic and chondrogenic differentiation of embryonic stem cells in response to specific growth factors. Bone 36:758-769. (Pubitemid 40616010)
39. Frandsen U, Porneki AD, Floridon C, Abdallah BM and Kassem M. (2007). Activin B mediated induction of Pdx1 in human embryonic stem cell derived embryoid bodies. Biochem Biophys Res Commun 362:568-574. (Pubitemid 47368130)
40. Kim SE, Kim BK, Gil JE, Kim SK and Kim JH. (2007). Comparative analysis of the developmental competence of three human embryonic stem cell lines in vitro. Mol Cells 23:49-56.
41. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, et al. (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015-1024. (Pubitemid 47517637)
42. Sottile V, Thomson A and McWhir J. (2003). In vitro osteogenic differentiation of human ES cells. Cloning Stem Cells 5:149-155. (Pubitemid 36877165)
43. Zur Nieden NI, Kempka G, Rancourt DE and Ahr HJ. (2005). Induction of chondro-, osteo-and adipogenesis in embryonic stem cells by bone morphogenetic protein-2: effect of cofactors on differentiating lineages. BMC Dev Biol 5:1.
44. Gadue P, Huber TL, Paddison PJ and Keller GM. (2006). Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci U S A 103:16806-16811. (Pubitemid 44737334)
45. Kärner E, Backesjo CM, Cedervall J, Sugars RV, Ahrlund-Richter L and Wendel M. (2009). Dynamics of gene expression during bone matrix formation in osteogenic cultures derived from human embryonic stem cells in vitro. Biochim Biophys Acta 1790:110-118.
46. Kuznetsov SA, Mankani MH and Robey PG. (2011). In vivo formation of bone and haematopoietic territories by transplanted human bone marrow stromal cells generated in medium with and without osteogenic supplements. J Tissue Eng Regen Med. [Epub ahead of print]; DOI: 10.1002/term .515.
47. Aldahmash A, Zaher W, Al-Nbaheen M and Kassem M. (2012). Human stromal (mesenchymal) stem cells: basic biology and current clinical use for tissue regeneration. Ann Saudi Med 32:68-77.
48. Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S and Keller G. (2007). Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109:2679-2687. (Pubitemid 46482058)
49. Gilbert SF. (2000). Developmental Biology. Sinauer Associates, Sunderland, MA.
50. Wheatley SC, Isacke CM and Crossley PH. (1993). Restricted expression of the hyaluronan receptor, CD44, during postimplantation mouse embryogenesis suggests key roles in tissue formation and patterning. Development 119:295-306. (Pubitemid 23293177)
51. Pignolo RJ and Kassem M. (2011). Circulating osteogenic cells: implications for injury, repair, and regeneration. J Bone Miner Res 26:1685-1693.
52. Brown SE, Tong W and Krebsbach PH. (2009). The derivation of mesenchymal stem cells from human embryonic stem cells. Cells Tissues Organs 189:256-260.
53. Qiu W, Andersen TE, Bollerslev J, Mandrup S, Abdallah BM and Kassem M. (2007). Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells. J Bone Miner Res 22:1720-1731. (Pubitemid 351235138)
54. Harkness L, Taipaleenmaki H, Mahmood A, Frandsen U, Saamanen AM, Kassem M and Abdallah BM. (2009). Isolation and differentiation of chondrocytic cells derived from human embryonic stem cells using dlk1/FA1 as a novel surface marker. Stem Cell Rev 5:353-368.
55. Jukes JM, Both SK, Leusink A, Sterk LM, van Blitterswijk CA and de BJ. (2008). Endochondral bone tissue engineering using embryonic stem cells. Proc Natl Acad Sci U S A 105: 6840-6845. (Pubitemid 351754492)
56. Prokhorova TA, Harkness LM, Frandsen U, Ditzel N, Burns JS, Schroeder HD and Kassem M. (2008). Teratoma Formation by Human Embryonic Stem Cells is site-dependent and enhanced by the presence of Matrigel. Stem Cells Dev 18: 47-54.
57. Blum B and Benvenisty N. (2007). Clonal analysis of human embryonic stem cell differentiation into teratomas. Stem Cells 25:1924-1930. (Pubitemid 47258170)
58. Leor J, Gerecht S, Cohen S, Miller L, Holbova R, Ziskind A, Shachar M, Feinberg MS, Guetta E and Itskovitz-Eldor J. (2007). Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart 93:1278-1284. (Pubitemid 47492921)
59. Brederlau A, Correia AS, Anisimov SV, Elmi M, Paul G, Roybon L, Morizane A, Bergquist F, Riebe I, et al. (2006). Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells 24:1433-1440. (Pubitemid 44464659)
60. Bourne S, Polak JM, Hughes SP and Buttery LD. (2004). Osteogenic differentiation of mouse embryonic stem cells: differential gene expression analysis by cDNA microarray and purification of osteoblasts by cadherin-11 magnetically activated cell sorting. Tissue Eng 10:796-806. (Pubitemid 38880398)