Efficient differentiation of human pluripotent stem cells into mesenchymal stem cells by modulating intracellular signaling pathways in a feeder/serum-free system

Stem Cells and Development

Volumn 21, Issue 7, 2012, Pages 1165-1175

  Tran, Ngoc Tung ^a   Trinh, Quynh Mai ^a   Lee, Gyun Min ^a   Han, Yong Mahn ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; 6 BROMOINDIRUBIN 3' OXIME; ACTIVIN A; ALPHA TUBULIN; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; COLLAGEN TYPE 1; COMPLEMENTARY DNA; ENDOGLIN; NOGGIN; OCTAMER TRANSCRIPTION FACTOR 4; OSTEOCALCIN; OXIME DERIVATIVE; RNA; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; FEEDER FREE CULTURE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; OSTEOBLAST; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTIVINS; ADIPOCYTES; ANTIGENS, CD; BONE MORPHOGENETIC PROTEIN 4; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CULTURE MEDIA, SERUM-FREE; DRUG SYNERGISM; GENE EXPRESSION PROFILING; HUMANS; INDOLES; INDUCED PLURIPOTENT STEM CELLS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STEM CELLS; OSTEOBLASTS; OXIMES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84860204390     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0346     Document Type: Article

References (57)

1. Friedenstein AJ, JF Gorskaja and NN Kulagina. (1976). Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4:267-274.
2. Fukuchi Y, H Nakajima, D Sugiyama, I Hirose, T Kitamura and K Tsuji. (2004). Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22:649-658.
3. Javazon EH, KJ Beggs and AW Flake. (2004). Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 32:414-425.
4. Kassis I, L Zangi, R Rivkin, L Levdansky, S Samuel, G Marx and R Gorodetsky. (2006). Isolation of mesenchymal stem cells from G-CSF-mobilized human peripheral blood using fibrin microbeads. Bone Marrow Transplant 37:967-976.
5. Wang HS, SC Hung, ST Peng, CC Huang, HM Wei, YJ Guo, YS Fu, MC Lai and CC Chen. (2004). Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem Cells 22:1330-1337.
6. Hung SC, H Cheng, CY Pan, MJ Tsai, LS Kao and HL Ma. (2002). In vitro differentiation of size-sieved stem cells into electrically active neural cells. Stem Cells 20:522-529.
7. Sanchez-Ramos J, S Song, F Cardozo-Pelaez, C Hazzi, T Stedeford, A Willing, TB Freeman, S Saporta, W Janssen, et al. (2000). Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164:247-256.
8. Kadivar M, S Khatami, Y Mortazavi, MA Shokrgozar, M Taghikhani and M Soleimani. (2006). In vitro cardiomyogenic potential of human umbilical vein-derived mesenchymal stem cells. Biochem Biophys Res Commun 340:639-647.
9. Reyes M, T Lund, T Lenvik, D Aguiar, L Koodie and CM Verfaillie. (2001). Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98:2615-2625.
10. Kang XQ, WJ Zang, LJ Bao, DL Li, TS Song, XL Xu and XJ Yu. (2005). Fibroblast growth factor-4 and hepatocyte growth factor induce differentiation of human umbilical cord blood-derived mesenchymal stem cells into hepatocytes. World J Gastroenterol 11:7461-7465.
11. Klyushnenkova E, JD Mosca, V Zernetkina, MK Majumdar, KJ Beggs, DW Simonetti, RJ Deans and KR McIntosh. (2005). T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci 12:47-57.
12. Lee RH, B Kim, I Choi, H Kim, HS Choi, K Suh, YC Bae and JS Jung. (2004). Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 14:311-324.
13. Madonna R, YJ Geng and R De Caterina. (2009). Adipose tissue-derived stem cells: characterization and potential for cardiovascular repair. Arterioscler Thromb Vasc Biol 29: 1723-1729.
14. Le Blanc K, I Rasmusson, B Sundberg, C Gotherstrom, M Hassan, M Uzunel and O Ringden. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439-1441.
15. Baksh D, L Song and RS Tuan. (2004). Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 8:301-316.
16. Digirolamo CM, D Stokes, D Colter, DG Phinney, R Class and DJ Prockop. (1999). Propagation and senescence of human marrow stromal cells in culture: a simple colonyforming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 107:275-281.
17. Kretlow JD, YQ Jin,WLiu, WJ Zhang, TH Hong, G Zhou, LS Baggett, AG Mikos and Y Cao. (2008). Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol 9:60.
18. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
19. Stenderup K, J Justesen, C Clausen and M Kassem. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919-926.
20. Wagner W, S Bork, P Horn, D Krunic, T Walenda, A Diehlmann, V Benes, J Blake, FX Huber, et al. (2009). Aging and replicative senescence have related effects on human stem and progenitor cells. PLoS One 4:e5846.
21. Greber B, H Lehrach and J Adjaye. (2007). Fibroblast growth factor 2 modulates transforming growth factor beta signaling in mouse embryonic fibroblasts and human ESCs (hESCs) to support hESC self-renewal. Stem Cells 25:455-464.
22. James D, AJ Levine, D Besser and A Hemmati-Brivanlou. (2005). TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132:1273-1282.
23. Rho JY, K Yu, JS Han, JI Chae, DB Koo, HS Yoon, SY Moon, KK Lee and YM Han. (2006). Transcriptional profiling of the developmentally important signalling pathways in human embryonic stem cells. Hum Reprod 21:405-412.
24. Sato N, L Meijer, L Skaltsounis, P Greengard and AH Brivanlou. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10:55-63.
25. Vallier L, D Reynolds and RA Pedersen. (2004). Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev Biol 275:403-421.
26. Xu RH, X Chen, DS Li, R Li, GC Addicks, C Glennon, TP Zwaka and JA Thomson. (2002). BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20:1261-1264.
27. Zhang P, J Li, Z Tan, C Wang, T Liu, L Chen, J Yong, W Jiang, X Sun, et al. (2008). Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood 111:1933-1941.
28. McLean AB, KA D'Amour, KL Jones, M Krishnamoorthy, MJ Kulik, DM Reynolds, AM Sheppard, H Liu, Y Xu, EE Baetge and S Dalton. (2007). Activin a efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 25:29-38.
29. Chambers SM, CA Fasano, EP Papapetrou, M Tomishima, M Sadelain and L Studer. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27:275-280.
30. Park SW, Y Jun Koh, J Jeon, YH Cho, MJ Jang, Y Kang, MJ Kim, C Choi, Y Sook Cho, et al. (2010). Efficient differentiation of human pluripotent stem cells into functional CD34 + progenitor cells by combined modulation of the MEK/ERK and BMP4 signaling pathways. Blood 116:5762-5772.
31. Evseenko D, Y Zhu, K Schenke-Layland, J Kuo, B Latour, S Ge, J Scholes, G Dravid, X Li, WR MacLellan and GM Crooks. (2010). Mapping the first stages of mesoderm commitment during differentiation of human embryonic stem cells. Proc Natl Acad Sci U S A 107:13742-13747.
32. Kattman SJ, AD Witty, M Gagliardi, NC Dubois, M Niapour, A Hotta, J Ellis and G Keller. (2011). Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8:228-240.
33. Ferreira LS, S Gerecht, HF Shieh, NWatson,MA Rupnick, SM Dallabrida, G Vunjak-Novakovic and R Langer. (2007). Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 101:286-294.
34. Pick M, L Azzola, A Mossman, EG Stanley and AG Elefanty. (2007). Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. 25:2206-2214.
35. Barberi T, LM Willis, ND Socci and L Studer. (2005). Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2:e161.
36. Olivier EN, AC Rybicki and EE Bouhassira. (2006). Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 24:1914-1922.
37. Trivedi P and P Hematti. (2008). Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp Hematol 36:350-359.
38. Vodyanik MA, J Yu, X Zhang, S Tian, R Stewart, JA Thomson and II Slukvin. (2010). A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 7:718-729.
39. Lian Q, E Lye, K Suan Yeo, E Khia Way Tan, M Salto-Tellez, TM Liu, N Palanisamy, RM El Oakley, EH Lee, B Lim and SK Lim. (2007). Derivation of clinically compliant MSCs from CD105 +, CD24- differentiated human ESCs. Stem Cells 25:425-436.
40. Lian Q, Y Zhang, J Zhang, HK Zhang, X Wu, Y Zhang, FF Lam, S Kang, JC Xia, et al. (2010). Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 121:1113-1123.
41. Lee JE, MS Kang, MH Park, SH Shim, TK Yoon, HM Chung and DR Lee. (2010). Evaluation of 28 human embryonic stem cell lines for use as unrelated donors in stem cell therapy: implications of HLA and ABO genotypes. Cell Transplant 19:1383-1395.
42. Xu C,MSInokuma, JDenham,KGolds, P Kundu, JDGold and MK Carpenter. (2001). Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19:971-974.
43. Dreesen O and AH Brivanlou. (2007). Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev 3:7-17.
44. Heasley LE and BE Petersen. (2004). Signalling in stem cells: meeting on signal transduction determining the fate of stem cells. EMBO Rep 5:241-244.
45. Katoh M and M Katoh. (2007). WNT signaling pathway and stem cell signaling network. Clin Cancer Res 13:4042-4045.
46. Nusse R, C Fuerer, W Ching, K Harnish, C Logan, A Zeng, D ten Berge and Y Kalani. (2008). Wnt signaling and stem cell control. Cold Spring Harb Symp Quant Biol 73:59-66.
47. Okita K and S Yamanaka. (2006). Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr Stem Cell Res Ther 1:103-111.
48. Valdimarsdottir G and C Mummery. (2005). Functions of the TGFbeta superfamily in human embryonic stem cells. APMIS 113:773-789.
49. Amit M, C Shariki, V Margulets and J Itskovitz-Eldor. (2004). Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod 70:837-845.
50. D'Amour KA, AD Agulnick, S Eliazer, OG Kelly, E Kroon and EE Baetge. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23:1534-1541.
51. Parashurama N, Y Nahmias, CH Cho, D van Poll, AW Tilles, F Berthiaume and ML Yarmush. (2008). Activin alters the kinetics of endoderm induction in embryonic stem cells cultured on collagen gels. Stem Cells 26:474-484.
52. Hao J, TG Li, X Qi, DF Zhao and GQ Zhao. (2006). Wnt/ beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Dev Biol 290:81-91.
53. Gadue P, TL Huber, PJ Paddison and GM Keller. (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.
54. Lindsley RC, JG Gill, M Kyba, TL Murphy and KM Murphy. (2006). Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 133:3787-3796.
55. Oldershaw RA, MA Baxter, ET Lowe, N Bates, LM Grady, F Soncin, DR Brison, TE Hardingham and SJ Kimber. (2010). Directed differentiation of human embryonic stem cells toward chondrocytes. Nat Biotechnol 28:1187-1194.
56. Sumi T, N Tsuneyoshi, N Nakatsuji and H Suemori. (2008). Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/ beta-catenin, Activin/Nodal and BMP signaling. Development 135:2969-2979.
57. Tada S, T Era, C Furusawa, H Sakurai, S Nishikawa, M Kinoshita, K Nakao, T Chiba and S Nishikawa. (2005). Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132:4363-4374.