Developmental-like bone regeneration by human embryonic stem cell-derived mesenchymal cells

Tissue Engineering - Part A

Volumn 20, Issue 1-2, 2014, Pages 365-377

  Kuhn, Liisa T ^a   Liu, Yongxing ^a   Boyd, Nolan L ^b   Dennis, James E ^c   Jiang, Xi ^a   Xin, Xiaonan ^a   Charles, Lyndon F ^a   Wang, Liping ^a   Aguila, H Leonardo ^a   Rowe, David W ^a   Lichtler, Alexander C ^a   Goldberg, A Jon ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIALS; BONE; CELL GROWTH; CELLS; COMPUTERIZED TOMOGRAPHY; CYTOLOGY; DEFECTS; REPAIR;

BONE REGENERATION; BONE TISSUE ENGINEERING; CHONDROGENIC DIFFERENTIATION; ENDOCHONDRAL OSSIFICATION; HISTOLOGICAL ANALYSIS; HUMAN EMBRYONIC STEM CELLS; HYPERTROPHIC CHONDROCYTES; MESENCHYMAL CELLS;

SCAFFOLDS (BIOLOGY);

BONE SIALOPROTEIN; COLLAGEN; HYDROXYAPATITE; TISSUE SCAFFOLD;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; BONE RADIOGRAPHY; BONE REGENERATION; CALVARIA; CARTILAGE CELL; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EMBRYONIC STEM CELL DERIVED MESENCHYMAL CELL; ENCHONDRAL OSSIFICATION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SKULL DEFECT; VASCULARIZATION;

ADULT; ANIMALS; BONE REGENERATION; CELL DIFFERENTIATION; CELL SHAPE; COLLAGEN; DURAPATITE; EMBRYONIC STEM CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MORPHOGENESIS; OSTEOBLASTS; OSTEOGENESIS; PHENOTYPE; PROSTHESIS IMPLANTATION; REGENERATION; SKULL; STEM CELL TRANSPLANTATION; TISSUE SCAFFOLDS;

EID: 84891511708     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0321     Document Type: Article

References (55)

1. Bruder, S.P., Kurth, A.A., Shea, M., Hayes, W.C., Jaiswal, N., and Kadiyala, S. Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res 16, 155, 1998.
2. Fleming, J.E., Jr., Cornell, C.N., and Muschler, G.F. Bone cells and matrices in orthopedic tissue engineering. Orthop Clin N Am 31, 357, 2000.
3. Chanda, D., Kumar, S., and Ponnazhagan, S. Therapeutic potential of adult bone marrow-derived mesenchymal stem cells in diseases of the skeleton. J Cell Biochem 111, 249, 2010.
4. Abumaree, M., Al Jumah, M., Pace, R.A., and Kalionis, B. Immunosuppressive properties of mesenchymal stem cells. Stem Cell Rev 8, 375, 2012.
5. Cuomo, A.V., Virk, M., Petrigliano, F., Morgan, E.F., and Lieberman, J.R. Mesenchymal stem cell concentration and bone repair: potential pitfalls from bench to bedside. J Bone Joint Surg 91, 1073, 2009.
6. Meijer, G.J., de Bruijn, J.D., Koole, R., and van Blitterswijk, C.A. Cell-based bone tissue engineering. PLoS Med 4, e9, 2007.
7. Siddappa, R., Licht, R., van Blitterswijk, C., and de Boer, J. Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J Orthop Res 25, 1029, 2007.
8. Gamradt, S.C., and Lieberman, J.R. Genetic modification of stem cells to enhance bone repair. Ann Biomed Eng 32, 136, 2004.
9. Sarugaser, R., Lickorish, D., Baksh, D., Hosseini, M.M., and Davies, J.E. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23, 220, 2005.
10. Baba, K., Yamazaki, Y., Ishiguro, M., Kumazawa, K., Aoyagi, K., Ikemoto, S., et al. Osteogenic potential of human umbilical cord-derived mesenchymal stromal cells cultured with umbilical cord blood-derived fibrin: a preliminary study. J Craniomaxillofac Surg pii: S1010-5182(13)00040-1, 2013.
11. Liu, G., Li, Y., Sun, J., Zhou, H., Zhang, W., Cui, L., et al. In vitro and in vivo evaluation of osteogenesis of human umbilical cord blood-derived mesenchymal stem cells on partially demineralized bone matrix. Tissue Eng Part A 16, 971, 2010.
12. Barberi, T., Willis, L.M., Socci, N.D., and Studer, L. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2, e161, 2005.
13. Carpenter, M.K., Rosler, E., and Rao, M.S. Characterization and differentiation of human embryonic stem cells. Cloning Stem Cells 5, 79, 2003.
14. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145, 1998.
15. Trounson, A. Human embryonic stem cells: mother of all cell and tissue types. Reprod Biomed Online 4 Suppl 1, 58, 2002.
16. Arpornmaeklong, P., Brown, S.E., Wang, Z., and Krebsbach, P.H. Phenotypic characterization, osteoblastic differentiation, and bone regeneration capacity of human embryonic stem cell-derived mesenchymal stem cells. Stem Cells Dev 18, 955, 2009.
17. Bielby, R.C., Boccaccini, A.R., Polak, J.M., and Buttery, L.D. In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 10, 1518, 2004.
18. Both, S.K., van Apeldoorn, A.A., Jukes, J.M., Englund, M.C., Hyllner, J., van Blitterswijk, C.A., et al. Differential boneforming capacity of osteogenic cells from either embryonic stem cells or bone marrow-derived mesenchymal stem cells. J Tissue Eng Regen Med 5, 180, 2011.
19. Harkness, L., Mahmood, A., Ditzel, N., Abdallah, B.M., Nygaard, J.V., and Kassem, M. Selective isolation and differentiation of a stromal population of human embryonic stem cells with osteogenic potential. Bone 48, 231, 2011.
20. Hwang, N.S., Varghese, S., Lee, H.J., Zhang, Z., Ye, Z., Bae, J., et al. In vivo commitment and functional tissue regeneration using human embryonic stem cell-derived mesenchymal cells. Proc Natl Acad Sci U S A 105, 20641, 2008.
21. Kim, S., Kim, S.S., Lee, S.H., Eun Ahn, S., Gwak, S.J., Song, J.H., et al. In vivo bone formation from human embryonic stem cell-derived osteogenic cells in poly(d,l-lacticco- glycolic acid)/hydroxyapatite composite scaffolds. Biomaterials 29, 1043, 2008.
22. Kopher, R.A., Penchev, V.R., Islam, M.S., Hill, K.L., Khosla, S., and Kaufman, D.S. Human embryonic stem cell-derived CD34 + cells function as MSC progenitor cells. Bone 47, 718, 2010.
23. Kuznetsov, S.A., Cherman, N., and Robey, P.G. In vivo bone formation by progeny of human embryonic stem cells. Stem Cells Dev 20, 269, 2011.
24. Marolt, D., Campos, I.M., Bhumiratana, S., Koren, A., Petridis, P., Zhang, G., et al. Engineering bone tissue from human embryonic stem cells. Proc Natl Acad Sci U S A 109, 8705, 2012.
25. Undale, A., Fraser, D., Hefferan, T., Kopher, R.A., Herrick, J., Evans, G.L., et al. Induction of fracture repair by mesenchymal cells derived from human embryonic stem cells or bone marrow. J Orthop Res 29, 1804, 2011.
26. Arpornmaeklong, P., Wang, Z., Pressler, M.J., Brown, S.E., and Krebsbach, P.H. Expansion and characterization of human embryonic stem cell-derived osteoblast-like cells. Cell Reprogram 12, 377, 2010.
27. Gawlitta, D., Farrell, E., Malda, J., Creemers, L.B., Alblas, J., and Dhert, W.J. Modulating endochondral ossification of multipotent stromal cells for bone regeneration. Tissue Eng Part B Rev 16, 385, 2010.
28. Oliveira, S.M., Mijares, D.Q., Turner, G., Amaral, I.F., Barbosa, M.A., and Teixeira, C.C. Engineering endochondral bone: in vivo studies. Tissue Eng Part A 15, 635, 2009.
29. Scotti, C., Tonnarelli, B., Papadimitropoulos, A., Scherberich, A., Schaeren, S., Schauerte, A., et al. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci U S A 107, 7251, 2010.
30. Jukes, J.M., Both, S.K., Leusink, A., Sterk, L.M., van Blitterswijk, C.A., and de Boer, J. Endochondral bone tissue engineering using embryonic stem cells. Proc Natl Acad Sci U S A 105, 6840, 2008.
31. Lenas, P., Moos, M., and Luyten, F.P. Developmental engineering: a new paradigm for the design and manufacturing of cell-based products. Part I: from three-dimensional cell growth to biomimetics of in vivo development. Tissue Eng Part B Rev 15, 381, 2009.
32. Hwang, N.S., Varghese, S., Lee, J.H., Zhang, Z., and Elisseeff, J. Biomaterials directed in vivo osteogenic differentiation of mesenchymal cells derived from human embryonic stem cells. Tissue Eng Part A 19, 1723, 2013.
33. Boyd, N.L., Robbins, K.R., Dhara, S.K., West, F.D., and Stice, S.L. Human embryonic stem cell-derived mesoderm-like epithelium transitions to mesenchymal progenitor cells. Tissue Eng Part A 15, 1897, 2009.
34. Kuhn, L.T., Liu, Y., Advincula, M., Wang, Y.H., Maye, P., and Goldberg, A.J. A nondestructive method for evaluating in vitro osteoblast differentiation on biomaterials using osteoblast- specific fluorescence. Tissue Eng Part C Methods 16, 1357, 2010.
35. Neen, D., Noyes, D., Shaw, M., Gwilym, S., Fairlie, N., and Birch, N. Healos and bone marrow aspirate used for lumbar spine fusion: a case controlled study comparing healos with autograft. Spine 31, E636, 2006.
36. Gang, E.J., Bosnakovski, D., Figueiredo, C.A., Visser, J.W., and Perlingeiro, R.C. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109, 1743, 2007.
37. Riekstina, U., Cakstina, I., Parfejevs, V., Hoogduijn, M., Jankovskis, G., Muiznieks, I., et al. Embryonic stem cell marker expression pattern in human mesenchymal stem cells derived from bone marrow, adipose tissue, heart and dermis. Stem Cell Rev 5, 378, 2009.
38. Boskey, A.L., and Roy, R. Cell culture systems for studies of bone and tooth mineralization. Chem Rev 108, 4716, 2008.
39. Siggelkow, H., Rebenstorff, K., Kurre, W., Niedhart, C., Engel, I., Schulz, H., et al. Development of the osteoblast phenotype in primary human osteoblasts in culture: comparison with rat calvarial cells in osteoblast differentiation. J Cell Biochem 75, 22, 1999.
40. Rai, B., Lin, J.L., Lim, Z.X., Guldberg, R.E., Hutmacher, D.W., and Cool, S.M. Differences between in vitro viability and differentiation and in vivo bone-forming efficacy of human mesenchymal stem cells cultured on PCL-TCP scaffolds. Biomaterials 31, 7960, 2010.
41. Levi, B., Nelson, E.R., Li, S., James, A.W., Hyun, J.S., Montoro, D.T., et al. Dura mater stimulates human adiposederived stromal cells to undergo bone formation in mouse calvarial defects. Stem Cells 29, 1241, 2011.
42. Bianco, P., Fisher, L.W., Young, M.F., Termine, J.D., and Robey, P.G. Expression of bone sialoprotein (BSP) in developing human tissues. Calcifi Tissue Int 49, 421, 1991.
43. Gerstenfeld, L.C., and Shapiro, F.D. Expression of bonespecific genes by hypertrophic chondrocytes: implication of the complex functions of the hypertrophic chondrocyte during endochondral bone development. J Cell Biochem 62, 1, 1996.
44. Leboy, P.S., Vaias, L., Uschmann, B., Golub, E., Adams, S.L., and Pacifici, M. Ascorbic acid induces alkaline phosphatase, type X collagen, and calcium deposition in cultured chick chondrocytes. J Biol Chem 264, 17281, 1989.
45. Cooper, L.F., Harris, C.T., Bruder, S.P., Kowalski, R., and Kadiyala, S. Incipient analysis of mesenchymal stem-cellderived osteogenesis. J Dental Res 80, 314, 2001.
46. Tremoleda, J.L., Forsyth, N.R., Khan, N.S., Wojtacha, D., Christodoulou, I., Tye, B.J., et al. Bone tissue formation from human embryonic stem cells in vivo. Cloning Stem Cells 10, 119, 2008.
47. Arinzeh, T.L., Tran, T., McAlary, J., and Daculsi, G. A comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem-cell-induced bone formation. Biomaterials 26, 3631, 2005.
48. Haynesworth, S.E., Goshima, J., Goldberg, V.M., and Caplan, A.I. Characterization of cells with osteogenic potential from human marrow. Bone 13, 81, 1992.
49. Krebsbach, P.H., Kuznetsov, S.A., Satomura, K., Emmons, R.V., Rowe, D.W., and Robey, P.G. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63, 1059, 1997.
50. Lonza Walkersville, I. Clonetics Endothelial Cell Medium Products. www.lonza.com. #CC-26-8, 2011.
51. Boyd, N.L., Nunes, S.S., Jokinen, J.D., Krishnan, L., Chen, Y., Smith, K.H., et al. Microvascular mural cell functionality of human embryonic stem cell-derived mesenchymal cells. Tissue Eng Part A 17, 1537, 2011.
52. Boyd, N.L., Nunes, S.S., Krishnan, L., Jokinen, J.D., Ramakrishnan, V.M., Bugg, A.R., et al. Dissecting the role of human embryonic stem cell-derived mesenchymal cells in human umbilical vein endothelial cell network stabilization in three-dimensional environments. Tissue Eng Part A 19, 211, 2013.
53. Cruess, R.L., and Dumont, J. Healing of Bone, Tendon, and Ligament. Philadelphia, PA: JB Lippincott, 1975.
54. Tortelli, F., Tasso, R., Loiacono, F., and Cancedda, R. The development of tissue-engineered bone of different origin through endochondral and intramembranous ossification following the implantation of mesenchymal stem cells and osteoblasts in a murine model. Biomaterials 31, 242, 2010.
55. Horwitz, E.M., and Prather, W.R. Cytokines as the major mechanism of mesenchymal stem cell clinical activity: expanding the spectrum of cell therapy. Isr Med Assoc J 11, 209, 2009.