Assessment of a preclinical model for studying the survival and engraftment of human stem cell derived osteogenic cell populations following orthotopic implantation

Journal of Musculoskeletal Neuronal Interactions

Volumn 12, Issue 4, 2012, Pages 241-253

  Tremoleda, J L ^b,d   Khan, N S ^d   Mann, V ^a,d   Racey, S N ^c,d   Martin, A J ^d   Simpson, A H W R ^d   Noble, B S ^a,d  

^a UNIVERSITY OF SUFFOLK   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NORTHUMBRIA UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Bone regeneration; Calvarial model; Osteoprogenitors; Stem cells; Transplantation

Indexed keywords

ADULT ANIMAL; ADULT STEM CELL; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEFECT; BONE MARROW; BONE REGENERATION; CALVARIA; CELL SURVIVAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENGRAFTMENT; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; OSTEOPROGENITOR CELL; RAT; STEM CELL; STEM CELL TRANSPLANTATION; STRAIN DIFFERENCE; STROMA CELL; WILD TYPE;

ANIMALS; EMBRYONIC STEM CELLS; HUMANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; RATS; RATS, SPRAGUE-DAWLEY; STEM CELL TRANSPLANTATION;

EID: 84870832508     PISSN: 11087161     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Bolland BJ, Tilly S, New AM, Dunlop DG, Oreffo RO. Adult Mesenchymal stem cells and impacting grafting a new clinical paradigm shift. Expert Dev Med Devices 2007;4:393-404.
2. Cancedda R, Dozin B, Giannoni P, Quarto R. Tissue engineering and cell therapy of cartilage and bone. Matrix Biol 2003;22:81-91.
3. Dimitriou R, Jones E, McGonagle D, Giannoudis PV. Bone regeneration: current concepts and future directions. BMC Med 2011;31;9:66.
4. Bianco P, Robey PG. Stem cells in tissue engineering. Nature 2001;414:118-121.
5. Mendes SC, Tibbe JM, Veenhof M, Bakker K, Both S, Platenburg PP, Oner FC, de Bruijn JD, van Blitterswijk CA. Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age. Tissue Eng 2002;8:911-920.
6. Horwitz EM, Gordon PL, Koo WW, Marx JC, Neel M, McNall RY, Muul L, Hofmann T. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci USA 2002;99:8932-8937.
7. Meijer GJ, de Bruijn JD, Koole R, van Blitterswijk CA. Cell based bone tissue engineering in jaw defects. Biomaterials 2008;29:3053-3061.
8. Friedenstein AJ, Piatetzky-Shapiro II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morpho 1966;16:381-390.
9. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhacher V, Lavroukov A, Kon E, Marcacci M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 2001;344:385-386.
10. Muschler GF, Nitto H, Matsukura Y, Boehm C, Valdevit A, Kambic H, Davros W, Powell K, Easley K. Spine fusion using cell matrix composites enriched in bone marrow-derived cells. Clin Orthop Relat Res 2003;407:102-118.
11. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cells in vitro. BMC Cell Biol 2006;7:14.
12. Sottile V, Thomson A, McWhir J. In vitro osteogenic differentiation of human ES cells. Cloning Stem Cells 2003; 5:149-155.
13. Bielby RC, Boccaccini AR, Polak JM, Buttery LD. In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 2004;10:1518-1525.
14. Tremoleda JL, NR Forsyth, Khan N, Wojtacha D, Christodoulou I, Tye BJ, Racey SN, Collishaw S, Sottile V, Thompson AJ, Simpson AH, Noble BS, McWhir J. Bone tissue formation from human embryonic stem cells in vivo. Cloning Stem Cells 2008;10:119-132.
15. Kim S, Kim SS, Lee SH, Ahn SE, Gwak SJ, Song JH, Kim BS, Chung HM. In vivo bone formation from human embryonic stem cell-derived osteogenic cells in poly (d,L-lactic-co-glycolic acid)/hydroxyapatite composite scaffolds. Biomaterials 2008;29:1043-1053.
16. Arpornmaeklong P, Brown SE, Wang Z, Krebsbach PH. Phenotypic characterization, osteoblastic differentiation, and bone regeneration capacity of human embryonic stem cell-derived mesenchymal stem cells. Stem Cells Dev 2009;18:955-968.
17. Kuznetov SA, Cherman N, Robey PG. In vivo bone formation by progeny of human embryonic stem cells. Stem Cells and Development 2011;20:269-287.
18. Muschler GF, Raut VP, Patterson TE, Wenke JC, Hollinger JO. The design and use of animal modets for translational research in bone tissue engineering and regenerative medicine. Tissue Engineering part B 2010; 16:123-145.
19. Mankani MH, Kuznetsov SA, Wolfe RM, Marshall GW, Robey PG. In vivo bone formation by human bone marrow stromal cells: reconstruction of the mouse calvarium and mandible. Stem Cells 2006;24:2140-2149.
20. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-1147.
21. Löser P, Schirm J, Guhr A, Wobus AM, Kurtz A. Human Embryonic Stem Cell Lines and Their Use in International Research. Stem Cells 2010;28:240-246.
22. Xu C, Inokuma MS, Denham J, Gods K, Kundu P, Gold JP, Carpenter MK. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001; 19:971-974.
23. McWhir J, Wojtacha D, Thomson A. Routine culture and differentiation of human embryonic stem cells. Methods Mol Biol 2006;331:77-90.
24. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI. Characterization of cells with osteogenic potential from human marrow. Bone 1992;13:81-88.
25. Gurevith O, Kurkalli BG, Prigozhina T, Gaft A, Slavin S. Reconstruction of cartilage, bone, and hematopoietic microenvironment with demineralised bone matrix and bone marrow. Stem Cells 2003;21:588-597.
26. Newsome PN, Johannessen I, Boyle S, Dalakas E, McAulay KA, Samuel K, Rae F, Forrester L, Turner ML, Hayes PC, Harrison DJ, Bickmore WA, Plevris JN. Human cord blood-derived cells can differentiate into hepatocytes in the mouse liver with no evidence of cellular fusion. Gastroenterology 2003;124:1891-1900.
27. Weidner N, Semple JP, Welch WR. Tumour angiogenesis and metastasis-correlation in invasive breast carcinoma. N Engl J Med 1991;324:1-8.
28. Noble BS, Stevens H, Loveridge N, Reeve J. Identification of apoptotic changes in osteocytes in normal and pathological human bone. Bone 1997;20:273-282.
29. Bills CE, Eisenberg H, Pallante SL. Complexes of organic acids with calcium phosphate: the von Kossa stain as a clue to the composition of bone mineral. Johns Hopkins Med J 1971;128:194-207.
30. Walsh WR, Walton M, Bruce W, Yan Y, Gillies RM, Svehla M. Cell structure and biology of bone and cartilage. In Handbook of histology methods for bone and cartilage. 2003, Ed An YH, Martin KL Humana press.
31. Yew TL, Huang TF, Ma HL, Hsu YT, Tsai CC, Chiang CC, Chen WM, Hung SC. Scale-up of MSC under hypoxic conditions for allogeneic transplantation and enhancing bony regeneration in a rabbit calvarial defect model. J Orthop Res 2012;30:1213-1214.
32. Krebsbach PH, Mankani Mh, Satomura K, Kuznetsov SA, Robey PG. Repair of craniotomy defects using bone marrow stromal cells. Transplantation 1998;10:1272-278.
33. Shang Q, Wang Z, Liu W, Shi Y, Cui L, Cao Y. Tissueengineered bone repair of sheep cranial defects with autologous bone marrow stromal cells. J Craniofac Surg 2001;12(6):586-593.
34. Frey-Vasconcells J, Whittlesey KJ, Baum E, Feigal EG. Translation of stem cell research: points to consider in designing preclinical animal studies. Stem Cells Translational Medicine 2012;1:1-6.
35. Muschler GF, Raut VP, Patterson TE, Wenke JC, Hollinger JO. The design and use of animal models for translational research in bone tissue engineering and regenerative medicine. Tissue Eng Part B Rev 2010;16:123-145.
36. Vos JG, Berkvens JM, Kruijt BC. The athymic nude rat. I. Morphology of lymphoid and endocrine organs. Clin Immunol Immunopathol 1980;15:213-228.
37. Geng YJ, Wu Q, Muszynsky M, Hansson GK, Libby P. Apoptosis of vascular smooth muscle cells induced by in vitro stimulation with interferon-gamma, tumor necrosis factor-alpha, and interleukin-1 beta. Arterioscler Thromb Vasc Biol 1996;16:19-27.
38. Zou D, Zhang Z, Ye D, Tang A, Deng L, Han W, Zhao J, Wang S, Zhang W, Zhu C, Zhou J, He J, Wang Y, Xu F, Huang Y, Jiang X. Repair of critical-sized rat calvarial defects using genetically engineered bone marrow-derived mesenchymal stem cells overexpressing hypoxia-inducible factor-1α. Stem Cells 2011;29:1380-1390.
39. Hanamura H, Higuchi Y, Nakagawa M, Iwata H, Nagami H, Urist MR. Solubilized bone morphogenetic protein (BMP) from Mouse osteosarcoma and rat demineralised bone matrix. Clin Orthop Relat Res 1980;148:281-290.
40. Damien CJ, Parsons JR, Prewett AB, Rietveld DC, Zimmerman MC. Investigation of an organic delivery system for demineralized bone matrix in a delayed-healing cranial defect model. J Biomed Mater Res 1994;28:553-561.
41. Tiedeman JJ, Garvin KL, Kile TA, Connolly JF. The role of a composite, demineralized bone matrix and bone marrow in the treatment of osseous defects. Orthopedics 1995;18:1153-1158.
42. Acarturk TO and Hollinger J. Commercially available demineralised bone matrix compositions to regenerate calvarial critical-sized bone defects. Plast Reconstr Surg 2006;118:862-873.
43. Wang J and Glimcher MJ. Characterization of matrix-induced osteogenesis in rat calvarial bone defects: I. Differences in the cellular response to demineralised bone matrix implanted in calvarial defects and in subcutaneous sites. Calcif Tissue Int 1999;65:156-165.
44. Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987;20:263-272.
45. Fairchild PJ, Cartland S, Nolan KF, Waldmann H. Embryonic stem cells and the challenge of transplantation tolerance. Trends Immunol 2004;25:465-470.
46. LeBlanc K, Tammik C, Rosendahl K, Zetterberg E, Ringdén O. HLA Expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematology 2003;890-896.
47. Bradley JA, Bolton EM, Pedersen RA. Stem Cell medicine encounters the immune system. Nat Rev Immunol 2002;2:859-871.
48. Tse WT, Pendleton JD, Beyer E, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003;75:389-397.
49. Grinnemo KH, Månsoon A, Dellgren G, Klingberg D, Wardell E, Drvota V, Tammik C, Holgersson J, Ringdén O, Sylvén C, Le Blanc K. Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infracted rat myocardium. J Thorac Cardiovasc Surg 2004; 127:1293-1300.
50. Drukker M, Katz G, Urbach A, et al. Characterization of the expression of MHC proteins in human embryonic stem cells. Proc Natl Acad Sci USA 2002;99:9864-9869.
51. Drukker M, Katchman H, Katz G, Friedman Even-Tov S, Shezen E, Hornstein E, Mandelboim O, Reisner Y, Benvenisty N. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 2006;24:221-229.
52. Swijnenburg RJ, Tanaka M, Vogel H, Baker J, Kofidis T, Gunawan F, Lebl DR, Caffarelli AD, de Bruin JL, Fedoseyeva EV, Robbins RC. Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 2005;112:1166-1172.
53. Greenwald JA, Mehrara BJ, Spector JA, Warren SM, Crisera FE, Fagenholz PJ, Bouletreau PJ, Longaker MT. Regional differentiation of cranial suture-associated dura mater in vivo and in vitro: implications for suture fusion and patency. J Bone Miner Res 2000;15:2413-2430.
54. Cowan CM, Shi Y-Y, Salami OO, Chou YF, Mari C, Thomas R, Quarto N, Contag CH, Wu B, Longaker MT. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nature Biotech 2004;22:560-657.
55. Eyre-Brook AL. The periosteum: its function reassed. Clin Orthop Relat Res;189:300-307.
56. Einhorn TA. The cell and molecular biology of fracture healing. Clin Orthop 1998;355:S7-S21.
57. Hopper RA, Zhang JR, Fournasier VL, Morova-Protzner I, Protzner KF, Pang CY, Forrest CR. Effect of isolation of periosteum and dura on the healing of rabbit calvarial inlay bone grafts. Plast Reconstr Surg 2001;107:454-462.
58. Gossain AK, Santoro TD, Song LS, Capel CC, Sudhakar PV, Matloub HS. Osteogenesis in calvarial defects: contribution of the dura, the pericranium, and the surrounding bone in adult versus infant animals. Plast Reconstr Surg 2003;112:515-527.