In vivo bone formation by progeny of human embryonic stem cells

Stem Cells and Development

Volumn 20, Issue 2, 2011, Pages 269-287

  Kuznetsov, Sergei A ^a   Cherman, Natasha ^a   Robey, Pamela Gehron ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; ALKALINE PHOSPHATASE; ASCORBIC ACID; BONE SIALOPROTEIN; BOVINE SERUM ALBUMIN; CALCIUM PHOSPHATE CERAMIC; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; DEXAMETHASONE; HYDROXYAPATITE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; CHONDROGENESIS; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; FETUS; FIBROBLAST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROGENY; STEM CELL TRANSPLANTATION; TERATOMA;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOCOMPROMISED HOST; KARYOTYPING; MICE; MICE, NUDE; OSTEOBLASTS; OSTEOGENESIS; PREGNANCY; STEM CELL TRANSPLANTATION; TERATOMA;

BOVINAE; MUS;

EID: 78951481817     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0501     Document Type: Article

References (77)

1. Roitberg B. (2003). Improvement in the ability to direct the differentiation of embryonic stem cells. Surg Neurol 60:3-4.
2. Ahn SE, S Kim, KH Park, et al. (2006). Primary bone-derived cells induce osteogenic differentiation without exogenous factors in human embryonic stem cells. Biochem Biophys Res Commun 340:403-408.
3. Arpornmaeklong P, SE Brown, Z Wang and PH Krebsbach. (2009). Phenotypic characterization, osteoblastic differentia-tion, and bone regeneration capacity of human embryonic stem cell-derived mesenchymal stem cells. Stem Cells Dev 18:955-968.
4. Barberi T, LM Willis, ND Socci and L Studer. (2005). Deri-vation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2:e161.
5. Bielby RC, AR Boccaccini, JM Polak and LD Buttery. (2004). In vitro differentiation and in vivo mineralization of osteo-genic cells derived from human embryonic stem cells. Tissue Eng 10:1518-1525.
6. Karner E, C Unger, AJ Sloan, L Ahrlund-Richter, RV Sugars and M Wendel. (2007). Bone matrix formation in osteogenic cultures derived from human embryonic stem cells in vitro. Stem Cells Dev 16:39-52.
7. Karp JM, LS Ferreira, A Khademhosseini, AH Kwon, J Yeh and RS Langer. (2006). Cultivation of human embryonic stem cells without the embryoid body step enhances osteo-genesis in vitro. Stem Cells 24:835-843.
8. Lian Q, E Lye, K Suan Yeo, et al. (2007). Derivation of clin-ically compliant MSCs from CD105 +, CD24-differentiated human ESCs. Stem Cells 25:425-436.
9. Olivier EN, AC Rybicki and EE Bouhassira. (2006). Differ-entiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 24:1914-1922.
10. Sottile V, A Thomson and J McWhir. (2003). In vitro osteo-genic differentiation of human ES cells. Cloning Stem Cells 5:149-155.
11. Bennett JH, CJ Joyner, JT Triffitt and ME Owen. (1991). Adipocytic cells cultured from marrow have osteogenic potential. J Cell Sci 99 (Pt 1):131-139.
12. Castano-Izquierdo H, J Alvarez-Barreto, J van den Dolder, JA Jansen, AG Mikos and VI Sikavitsas. (2007). Pre-culture pe-riod of mesenchymal stem cells in osteogenic media influ-ences their in vivo bone forming potential. J Biomed Mater Res A 82:129-138.
13. De Kok IJ, KC Hicok, RJ Padilla, RG Young and LF Cooper. (2006). Effect of vitamin D pretreatment of human mesen-chymal stem cells on ectopic bone formation. J Oral Implantol 32:103-109.
14. Derubeis AR, M Mastrogiacomo, R Cancedda and R Quarto. (2003). Osteogenic potential of rat spleen stromal cells. Eur J Cell Biol 82:175-181.
15. Mendes SC, JM Tibbe, M Veenhof, et al. (2004). Relation between in vitro and in vivo osteogenic potential of cultured human bone marrow stromal cells. J Mater Sci Mater Med 15:1123-1128.
16. Sabatini F, L Petecchia, M Tavian, V Jodon de Villeroche, GA Rossi and D Brouty-Boye. (2005). Human bronchial fibro-blasts exhibit a mesenchymal stem cell phenotype and mul-tilineage differentiating potentialities. Lab Invest 85:962-971.
17. Sacchetti B, A Funari, S Michienzi, et al. (2007). Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell131:324-336.
18. Sudo K, M Kanno, K Miharada, et al. (2007). Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells 25:1610-1617.
19. Kim S, SS Kim, SH Lee, et al. (2008). In vivo bone formation from human embryonic stem cell-derived osteogenic cells in poly(d,l-lactic-co-glycolic acid)/hydroxyapatite composite scaffolds. Biomaterials 29:1043-1053.
20. Tremoleda JL, NR Forsyth, NS Khan, et al. (2008). Bone tissue formation from human embryonic stem cells in vivo. Cloning Stem Cells 10:119-132.
21. Kuznetsov SA, PH Krebsbach, K Satomura, et al. (1997). Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 12:1335-1347.
22. Krebsbach PH, SA Kuznetsov, K Satomura, RV Emmons, DW Rowe and PG Robey. (1997). Bone formation in vivo: com-parison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63:1059-1069.
23. Mankani MH, SA Kuznetsov, B Fowler, A Kingman and PG Robey. (2001). In vivo bone formation by human bone marrow stromal cells: effect of carrier particle size and shape. Biotechnol Bioeng 72:96-107.
24. Das AK and R Pal. (2010). Induced pluripotent stem cells (iPSCs): the emergence of a new champion in stem cell technology-driven biomedical applications. J Tissue Eng Regen Med [Epub ahead of print].
25. Friedenstein AJ, RK Chailakhyan and UV Gerasimov. (1987). Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 20: 263-272.
26. Mankani MH, SA Kuznetsov, B Shannon, et al. (2006). Canine cranial reconstruction using autologous bone mar-row stromal cells. Am J Pathol 168:542-550.
27. Bianco P, M Riminucci, S Gronthos and PG Robey. (2001). Bone marrow stromal stem cells: nature, biology, and po-tential applications. Stem Cells 19:180-192.
28. Bradbeer JN, M Riminucci and P Bianco. (1994). Giemsa as a fluorescent stain for mineralized bone. J Histochem Cyto-chem 42:677-680.
29. De Carvalho HF and SR Taboga. (1996). Fluorescence and confocal laser scanning microscopy imaging of elastic fibers in hematoxylin-eosin stained sections. Histochem Cell Biol 106:587-592.
30. Kasten P, J Vogel, R Luginbuhl, et al. (2005). Ectopic bone formation associated with mesenchymal stem cells in a re-sorbable calcium deficient hydroxyapatite carrier. Biomater-ials 26:5879-5889.
31. Mendes SC, JM Tibbe, M Veenhof, et al. (2002). Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age. Tissue Eng 8:911-920.
32. Song IH, AI Caplan and JE Dennis. (2009). In vitro dexa-methasone pretreatment enhances bone formation of human mesenchymal stem cells in vivo. J Orthop Res 27:916-921.
33. Yamanouchi K, K Satomura, Y Gotoh, et al. (2001). Bone formation by transplanted human osteoblasts cultured within collagen sponge with dexamethasone in vitro. J Bone Miner Res 16:857-867.
34. Kim CH, SL Cheng and GS Kim. (1999). Effects of dexameth-asone on proliferation, activity, and cytokine secretion of nor-mal human bone marrow stromal cells: possible mechanisms of glucocorticoid-induced bone loss. J Endocrinol162:371-379.
35. Choi KM, YK Seo, HH Yoon, et al. (2008). Effect of ascorbic acid on bone marrow-derived mesenchymal stem cell pro-liferation and differentiation. J Biosci Bioeng 105:586-594.
36. Turgeman G, DD Pittman, R Muller, et al. (2001). Engineered human mesenchymal stem cells: a novel platform for skeletal cell mediated gene therapy. J Gene Med 3:240-251.
37. Pradel W, U Eckelt and G Lauer. (2006). Bone regeneration after enucleation of mandibular cysts: comparing autoge-nous grafts from tissue-engineered bone and iliac bone. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 101:285-290.
38. Schmelzeisen R, R Schimming and M Sittinger. (2003). Making bone: implant insertion into tissue-engineered bone for maxillary sinus floor augmentation-a preliminary report. J Craniomaxillofac Surg 31:34-39.
39. Arinzeh TL, T Tran, J McAlary and G Daculsi. (2005). A comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem-cell-induced bone formation. Biomaterials 26:3631-3638.
40. Daga A, A Muraglia, R Quarto, R Cancedda and G Corte. (2002). Enhanced engraftment of EPO-transduced human bone marrow stromal cells transplanted in a 3D matrix in non-conditioned NOD/SCID mice. Gene Ther 9:915-921.
41. Harris CT, LF Cooper. (2004). Comparison of bone graft matrices for human mesenchymal stem cell-directed osteo-genesis. J Biomed Mater Res A 68:747-755.
42. Khlusov IA, AV Karlov, YP Sharkeev, et al. (2005). Osteo-genic potential of mesenchymal stem cells from bone mar-row in situ: role of physicochemical properties of artificial surfaces. Bull Exp Biol Med 140:144-152.
43. Mastrogiacomo M, A Muraglia, V Komlev, et al. (2005). Tissue engineering of bone: search for a better scaffold. Or-thod Craniofac Res 8:277-284.
44. Warren SM, RK Nacamuli, HM Song and MT Longaker. (2004). Tissue-engineered bone using mesenchymal stem cells and a biodegradable scaffold. J Craniofac Surg 15:34-37.
45. Kuznetsov SA, AJ Friedenstein and PG Robey. (1997). Fac-tors required for bone marrow stromal fibroblast colony formation in vitro. Br J Haematol 97:561-570.
46. Perez-Sanchez MJ, E Ramirez-Glindon, M Lledo-Gil, JL Calvo-Guirado and C Perez-Sanchez. (2009). Biomaterials for bone regeneration. Med Oral Patol Oral Cir Bucal15:e517-e522.
47. Schopper C, F Ziya-Ghazvini, W Goriwoda, et al. (2005). HA/TCP compounding of a porous CaP biomaterial improves bone formation and scaffold degradation\a long-term histo-logical study. J Biomed Mater Res B Appl Biomater 74:458-467.
48. Burns JS, PL Rasmussen, KH Larsen, HD Schroder and M Kassem. (2010). Parameters in 3D "Osteospheroids" of telo-merized human mesenchymal (stromal) stem cells grown on osteoconductive scaffolds that predict in vivo bone forming potential. Tissue Eng Part A 16:2331-2342.
49. Aubin JE. (1998). Bone stem cells. J Cell Biochem Suppl 30-31:73-82.
50. Viguet-Carrin S, P Garnero and PD Delmas. (2006). The role of collagen in bone strength. Osteoporos Int 17:319-336.
51. Chevallier N, F Anagnostou, S Zilber, et al. (2009). Osteo-blastic differentiation of human mesenchymal stem cells with platelet lysate. Biomaterials 31:270-278.
52. Schroeder TM, ED Jensen and JJ Westendorf. (2005). Runx2: a master organizer of gene transcription in developing and maturing osteoblasts. Birth Defects Res C Embryo Today 75: 213-225.
53. Millan JL. (2006). Alkaline phosphatases: structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2:335-341.
54. Orimo H. (2010). The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J Nippon Med Sch 77:4-12.
55. Blum B and N Benvenisty. (2009). The tumorigenicity of diploid and aneuploid human pluripotent stem cells. Cell Cycle 8:3822-3830.
56. Ganss B, RH Kim and J Sodek. (1999). Bone sialoprotein. Crit Rev Oral Biol Med 10:79-98.
57. Ogata Y. (2008). Bone sialoprotein and its transcriptional regulatory mechanism. J Periodontal Res 43:127-135.
58. Larsen KH, CM Frederiksen, JS Burns, BM Abdallah and M Kassem. (2010). Identifying a molecular phenotype for bone marrow stromal cells with in vivo bone forming capacity. J Bone Miner Res 25:796-808.
59. Barry F, RE Boynton, B Liu and JM Murphy. (2001). Chon-drogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components. Exp Cell Res 268:189-200.
60. Hyc A, A Osiecka-Iwan, J Jozwiak and S Moskalewski. (2001). The morphology and selected biological properties of articular cartilage. Orthop Traumatol Rehabil 3:151-162.
61. Mwale F, D Stachura, P Roughley and J Antoniou. (2006). Limitations of using aggrecan and type X collagen as markers of chondrogenesis in mesenchymal stem cell differentiation. J Orthop Res 24:1791-1798.
62. Tew SR, AD Murdoch, RP Rauchenberg and TE Hard-ingham. (2008). Cellular methods in cartilage research: pri-mary human chondrocytes in culture and chondrogenesis in human bone marrow stem cells. Methods 45:2-9.
63. Mallon BS, KY Park, KG Chen, RS Hamilton and RD McKay. (2006). Toward xeno-free culture of human embryonic stem cells. Int J Biochem Cell Biol 38:1063-1075.
64. Draper JS, K Smith, P Gokhale, et al. (2004). Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 22:53-54.
65. Przyborski SA. (2005). Differentiation of human embryonic stem cells after transplantation in immune-deficient mice. Stem Cells 23:1242-1250.
66. Thomson JA, J Itskovitz-Eldor, SS Shapiro, et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
67. Brivanlou AH, FH Gage, R Jaenisch, T Jessell, D Melton and J Rossant. (2003). Stem cells. Setting standards for human embryonic stem cells. Science 300:913-916.
68. Hwang WS, YJ Ryu, JH Park, et al. (2004). Evidence of a pluripotent human embryonic stem cell line derived from a cloned blastocyst. Science 303:1669-1674.
69. Lees JG, SA Lim, T Croll, et al. (2007). Transplantation of 3D scaffolds seeded with human embryonic stem cells: biolog-ical features of surrogate tissue and teratoma-forming po-tential. Regen Med 2:289-300.
70. Li Z, M Leung, R Hopper, R Ellenbogen and M Zhang. (2010). Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds. Biomaterials 31:404-412.
71. Abelev GI and TL Eraiser. (1999). Cellular aspects of alpha-fetoprotein reexpression in tumors. Semin Cancer Biol 9: 95-107.
72. Lazarevich NL. (2000). Molecular mechanisms of alpha-fetoprotein gene expression. Biochemistry (Mosc) 65:117-133.
73. Carrell RW. (2004). What we owe to alpha(1)-antitrypsin and to Carl-Bertil Laurell. COPD 1:71-84.
74. Schweizer J, PE Bowden, PA Coulombe, et al. (2006). New consensus nomenclature for mammalian keratins. J Cell Biol 174:169-174.
75. Perrot R, R Berges, A Bocquet and J Eyer. (2008). Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Mol Neurobiol 38:27-65.
76. Amit M, MK Carpenter, MS Inokuma, et al. (2000). Clonally derived human embryonic stem cell lines maintain plur-ipotency and proliferative potential for prolonged periods of culture. Dev Biol 227:271-278.
77. Jukes JM, SK Both, A Leusink, LM Sterk, CA van Blitterswijk and J de Boer. (2008). Endochondral bone tissue engineering using embryonic stem cells. Proc Natl Acad Sci USA 105: 6840-6845.