Agonism of Wnt-β-catenin signalling promotes mesenchymal stem cell (MSC) expansion

Journal of Tissue Engineering and Regenerative Medicine

Volumn 9, Issue 11, 2015, Pages E13-E26

  Hoffman, Michael D ^a   Benoit, Danielle S W ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

6 bromoindirubin 3 oxime; Hydrogel biomaterials; Mesenchymal stem cells; Pluripotency; Proliferation; Regenerative medicine

Indexed keywords

BIOMATERIALS; CELL CULTURE; CELL SIGNALING; GENE EXPRESSION; REGENERATIVE MEDICINE; STEM CELLS; TISSUE REGENERATION;

6-BROMOINDIRUBIN-3′-OXIME; AGONISMS; CATENIN SIGNALING; HYDROGEL BIOMATERIAL; MESENCHYMAL STEM CELL; PLURIPOTENCY; PROLIFERATION; REGENERATIVE MEDICINE; STEM CELL EXPANSION; Β-CATENIN;

HYDROGELS;

6 BROMOINDIRUBIN 3' OXIME; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; UNCLASSIFIED DRUG; WNT PROTEIN; 6-BROMOINDIRUBIN-3'-OXIME; HYDROGEL; INDOLE DERIVATIVE; OXIME;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL FUNCTION; CELL POPULATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; TISSUE REGENERATION; ADIPOGENESIS; AGONISTS; ANIMAL; BONE MARROW CELL; C3H MOUSE; CHEMISTRY; CHONDROCYTE; CYTOLOGY; HYDROLYSIS; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES; REGENERATIVE MEDICINE; WNT SIGNALING PATHWAY;

ADIPOCYTES; ADIPOGENESIS; ANIMALS; BETA CATENIN; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROCYTES; HUMANS; HYDROGELS; HYDROLYSIS; INDOLES; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C3H; OSTEOBLASTS; OXIMES; REGENERATIVE MEDICINE; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84932640878     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1736     Document Type: Article

References (72)

1. Awad HA, Zhang X, Reynolds DG, et al. 2007; Recent advances in gene delivery for structural bone allografts. Tissue Eng 13: 1973-1985.
2. Ball SG, Shuttleworth CA, Kielty CM. 2007; Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J Cell Biol 177: 489-500.
3. Banfi A, Muraglia A, Dozin B, et al. 2000; Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp Hematol 28: 707-715.
4. Baxter MA, Wynn RF, Jowitt SN, et al. 2004; Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22: 675-682.
5. Becker AJ, Mc CE, Till JE. 1963; Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197: 452-454.
6. Benoit DS, Tripodi MC, Blanchette JO, et al. 2007a; Integrin-linked kinase production prevents anoikis in human mesenchymal stem cells. J Biomed Mater Res A 81: 259-268.
7. Benoit DSW, Anseth KS. 2005; Heparin functionalized PEG gels that modulate protein adsorption for hMSC adhesion and differentiation. Acta Biomater 1: 461-470.
8. Benoit DSW, Collins SD, Anseth KS. 2007b; Multifunctional hydrogels that promote osteogenic human mesenchymal stem cell differentiation through stimulation and sequestering of bone morphogenic protein 2. Adv Funct Mater 17: 2085-2093.
9. Benoit DSW, Durney AR, Anseth KS. 2006a; Manipulations in hydrogel degradation behavior enhance osteoblast function and mineralized tissue formation, Tissue Eng 12: 1663-1673.
10. Benoit DSW, Durney AR, Anseth KS. 2007c; The effect of heparin-functionalized PEG hydrogels on three-dimensional human mesenchymal stem cell osteogenic differentiation. Biomaterials 28: 66-77.
11. Benoit DSW, Nuttelman CR, Collins SD, et al. 2006b; Synthesis and characterization of a fluvastatin-releasing hydrogel delivery system to modulate hMSC differentiation and function for bone regeneration. Biomaterials 27: 6102-6110.
12. Benoit DSW, Schwartz MP, Durney AR, et al. 2008; Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater 7: 816-823.
13. Biechele TL, Moon RT. 2008; Assaying β-catenin/TCF transcription with β-catenin/TCF transcription-based reporter constructs. Methods Mol Biol 468: 99-110.
14. Bilkovski R, Schulte DM, Oberhauser F, et al. 2010; Role of WNT-5a in the determination of human mesenchymal stem cells into preadipocytes. J Biol Chem 285: 6170-6178.
15. Bonab MM, Alimoghaddam K, Talebian F, et al. 2006; Aging of mesenchymal stem cell in vitro. BMC Cell Biol 7: 14.
16. Bonewald LF, Dallas SL. 1994; Role of active and latent transforming growth factor β in bone formation. J Cell Biochem 55: 350-357.
17. Bork S, Pfister S, Witt H, et al. 2010; DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell 9: 54-63.
18. Bowers RR, Lane MD. 2008; Wnt signaling and adipocyte lineage commitment. Cell Cycle 7: 1191-1196.
19. Brack AS, Conboy MJ, Roy S, et al. 2007; Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317: 807-810.
20. Bruder SP, Jaiswal N, Haynesworth SE. 1997; Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64: 278-294.
21. Chen S, Do JT, Zhang Q, et al. 2006; Self-renewal of embryonic stem cells by a small molecule. Proc Natl Acad Sci USA 103: 17266-17271.
22. Elisseeff J, Puleo C, Yang F, et al. 2005; Advances in skeletal tissue engineering with hydrogels. Orthod Craniofac Res 8: 150-161.
23. Fairbanks BD, Schwartz MP, Bowman CN, et al. 2009; Photoinitiated polymerization of PEG-diacrylate with lithium phenyl-2, 4, 6-trimethylbenzoylphosphinate: polymerization rate and cytocompatibility. Biomaterials 30: 6702-6707.
24. Fierro F, Illmer T, Jing D, et al. 2007; Inhibition of platelet-derived growth factor receptor-β by imatinib mesylate suppresses proliferation and alters differentiation of human mesenchymal stem cells in vitro. Cell Prolif 40: 355-366.
25. Fre S, Pallavi SK, Huyghe M, et al. 2009; Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc Natl Acad Sci USA 106: 6309-6314.
26. Jaiswal N, Haynesworth SE, Caplan AI, et al. 1997; Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64: 295-312.
27. Kashyap V, Rezende NC, Scotland KB, et al. 2009; Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 18: 1093-1108.
28. Kasten P, Beyen I, Egermann M, et al. 2008; Instant stem cell therapy: characterization and concentration of human mesenchymal stem cells in vitro. Eur Cell Mater 16: 47-55.
29. Kelly KF, Ng DY, Jayakumaran G, et al. 2011; β-catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 8: 214-227.
30. Krause U, Harris S, Green A, et al. 2010; Pharmaceutical modulation of canonical Wnt signaling in multipotent stromal cells for improved osteoinductive therapy. Proc Natl Acad Sci USA 107: 4147-4152.
31. Kwon C, Cheng P, King IN, et al. 2011; Notch post-translationally regulates β-catenin protein in stem and progenitor cells. Nat Cell Biol 13: 1244-1251.
32. Lin CC, Anseth KS. 2009; PEG hydrogels for the controlled release of biomolecules in regenerative medicine. Pharm Res 26: 631-643.
33. Lin-Gibson S, Bencherif S, Cooper JA, et al. 2004; Synthesis and characterization of PEG dimethacrylates and their hydrogels. Biomacromolecules 5: 1280-1287.
34. Liu GZ, Vijayakumar S, Grumolato L, et al. 2009; Canonical Wnts function as potent regulators of osteogenesis by human mesenchymal stem cells. J Cell Biol 185: 67-75.
35. Luu HH, Song WX, Luo X, et al. 2007; Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells. J Orthop Res 25: 665-677.
36. Mackay AM, Beck SC, Murphy JM, et al. 1998; Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4: 415-428.
37. Masckauchan TN, Shawber CJ, Funahashi Y, et al. 2005; Wnt/β-catenin signaling induces proliferation, survival and interleukin-8 in human endothelial cells. Angiogenesis 8: 43-51.
38. McBeath R, Pirone DM, Nelson CM, et al. 2004; Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
39. Meijer L, Skaltsounis AL, Magiatis P, et al. 2003; GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 10: 1255-1266.
40. Murphy JM, Fink DJ, Hunziker EB, et al. 2003; Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48: 3464-3474.
41. Nuttelman CR, Tripodi MC, Anseth KS. 2006; Dexamethasone-functionalized gels induce osteogenic differentiation of encapsulated hMSCs. J Biomed Mater Res A 76: 183-195.
42. Ogawa T, Akazawa T, Tabata Y. 2010; In vitro proliferation and chondrogenic differentiation of rat bone marrow stem cells cultured with gelatin hydrogel microspheres for TGFβ1 release. J Biomater Sci Polym Ed 21: 609-621.
43. Pevsner-Fischer M, Morad V, Cohen-Sfady M, et al. 2007; Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood 109: 1422-1432.
44. Pfaffl MW. 2001; A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
45. Pittenger MF, Mackay AM, Beck SC, et al. 1999; Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
46. Polychronopoulos P, Magiatis P, Skaltsounis AL, et al. 2004; Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases. J Med Chem 47: 935-946.
47. Reinhold MI, Kapadia RM, Liao Z, et al. 2006; The Wnt-inducible transcription factor Twist1 inhibits chondrogenesis. J Biol Chem 281: 1381-1388.
48. Reznikoff CA, Brankow DW, Heidelberger C. 1973; Establishment and characterization of a cloned line of C3H mouse embryo cells sensitive to postconfluence inhibition of division. Cancer Res 33: 3231-3238.
49. Rodrigues M, Griffith LG, Wells A. 2010; Growth factor regulation of proliferation and survival of multipotential stromal cells. Stem Cell Res Ther 1: 32.
50. Roobrouck VD, Ulloa-Montoya F, Verfaillie CM. 2008; Self-renewal and differentiation capacity of young and aged stem cells. Exp Cell Res 314: 1937-1944.
51. Sato N, Meijer L, Skaltsounis L, et al. 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.
52. Sawhney AS, Pathak CP, Hubbell JA. 1993; Bioerodible hydrogels based on photopolymerized poly(ethylene glycol)-co-poly(α-hydroxy acid) diacrylate macromers. Macromolecules 26: 581-587.
53. Shahdadfar A, Fronsdal K, Haug T, et al. 2005; In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells 23: 1357-1366.
54. Shea CM, Edgar CM, Einhorn TA, et al. 2003; BMP treatment of C3H10T1/2 mesenchymal stem cells induces both chondrogenesis and osteogenesis. J Cell Biochem 90: 1112-1127.
55. Sineva GS, Pospelov VA. 2010; Inhibition of GSK3β enhances both adhesive and signalling activities of β-catenin in mouse embryonic stem cells. Biol Cell 102: 549-560.
56. Stewart A, Guan H, Yang K. 2010; BMP-3 promotes mesenchymal stem cell proliferation through the TGFβ/activin signaling pathway. J Cell Physiol 223: 658-666.
57. Tang J, Peng R, Ding J. 2010; The regulation of stem cell differentiation by cell-cell contact on micropatterned material surfaces. Biomaterials 31: 2470-2476.
58. Tang QQ, Lane MD. 2012; Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem 81: 715-736.
59. Tseng AS, Engel FB, Keating MT. 2006; The GSK-3 inhibitor BIO promotes proliferation in mammalian cardiomyocytes. Chem Biol 13: 957-963.
60. Tsutsumi S, Shimazu A, Miyazaki K, et al. 2001; Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 288: 413-419.
61. Vougogiannopoulou K, Ferandin Y, Bettayeb K, et al. 2008; Soluble 3′, 6-substituted indirubins with enhanced selectivity toward glycogen synthase kinase-3 alter circadian period. J Med Chem 51: 6421-6431.
62. Wagner W, Horn P, Castoldi M, et al. 2008; Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 3: 1-12.
63. Wakitani S, Imoto K, Yamamoto T, et al. 2002; Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthr Cartilage 10: 199-206.
64. Wen J, Liu J, Song GQ, et al. 2010; Effects of 6-bromoindirubin-3′-oxime on the maintenance of pluripotency of porcine embryonic germ cells in combination with stem cell factor, leukemia inhibitory factor and fibroblast growth factor. Reproduction 139: 1039-1046.
65. Wu QQ, Chen D, Zuscik MJ, et al. 2008; Overexpression of Smurf2 stimulates endochondral ossification through upregulation of β-catenin. J Bone Miner Res 23: 552-563.
66. Xie C, Reynolds D, Awad H, et al. 2007; Structural bone allograft combined with genetically engineered mesenchymal stem cells as a novel platform for bone tissue engineering. Tissue Eng 13: 435-445.
67. Yi F, Pereira L, Hoffman JA, et al. 2011; Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 13: 762-770.
68. Ying QL, Wray J, Nichols J, et al. 2008; The ground state of embryonic stem cell self-renewal. Nature 453: 519-523.
69. Yu J, Chau KF, Vodyanik MA, et al. 2011; Efficient feeder-free episomal reprogramming with small molecules. PLoS One 6: e17557.
70. Yu J, Vodyanik MA, Smuga-Otto K, et al. 2007; Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
71. Zhang DY, Wang HJ, Tan YZ. 2011; Wnt/β-catenin signaling induces the aging of mesenchymal stem cells through the DNA damage response and the p53/p21 pathway. PLoS One 6: 1-12.
72. Zhao L, Li G, Chan KM, et al. 2009; Comparison of multipotent differentiation potentials of murine primary bone marrow stromal cells and mesenchymal stem cell line C3H10T1/2. Calcif Tissue Int 84: 56-64.