Human adipose-derived side population stem cells cultured on demineralized bone matrix for bone tissue engineering

Tissue Engineering - Part A

Volumn 17, Issue 5-6, 2011, Pages 789-798

  Supronowicz, Peter ^a   Gill, Elise ^a   Trujillo, Angelica ^a   Thula, Taili ^a   Zhukauskas, Rasa ^a   Ramos, Thomas ^b   Cobb, Ronald R ^a  

^a RTI Biologics Inc   (United States)

^b PrimeGen Biotech LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; CELL PROLIFERATION; MINERAL RESOURCES; PHOSPHATASES; PROTEINS; STEM CELLS;

ADIPOSE DERIVED STEM CELLS; ADIPOSE TISSUE; ALKALINE PHOSPHATASE ACTIVITY; BONE FORMATION; BONE MATRIX; BONE MORPHOGENETIC PROTEIN-2; BONE REPAIR; BONE TISSUE ENGINEERING; DEMINERALIZED BONE MATRIX; ECTOPIC BONES; EXTRACELLULAR MATRIX PROTEIN; GROWTH FACTOR; HUMAN ADIPOSE; IN-VITRO; MINERAL DEPOSITS; MULTICOMPONENTS; NATURALLY OCCURRING; OSTEOCONDUCTIVE; OSTEOGENIC; RAT MODEL; TISSUE ENGINEERING APPLICATIONS;

TISSUE ENGINEERING;

RATTUS;

ALKALINE PHOSPHATASE; BIOLOGICAL MARKER; CALCIUM;

ADIPOSE TISSUE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BONE; BONE DEVELOPMENT; BONE MATRIX; BONE MINERALIZATION; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; ENZYMOLOGY; HUMAN; MALE; METABOLISM; METHODOLOGY; PHYSIOLOGY; RAT; SIDE POPULATION CELL; STEM CELL; TISSUE ENGINEERING;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE; ANIMALS; BIOLOGICAL MARKERS; BONE AND BONES; BONE MATRIX; CALCIFICATION, PHYSIOLOGIC; CALCIUM; CELL ADHESION; CELL PROLIFERATION; CELLS, CULTURED; HUMANS; MALE; MODELS, BIOLOGICAL; OSTEOGENESIS; RATS; SIDE-POPULATION CELLS; STEM CELLS; TISSUE ENGINEERING;

EID: 79952159983     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0357     Document Type: Article

References (72)

1. Caplan, A. I., and Bruder, S. P. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7, 259, 2001.
2. Keating, J. F., and McQueen, M. M. Substitutes for autologous bone graft in orthopaedic trauma. J Bone Joint Surg Br 83, 3, 2001.
3. Khan, S. N., Cammisa, F. P., Jr., Sandhu, H. S., Diwan, A. D., Girardi, F. P., and Lane, J. M. The biology of bone grafting. J Am Acad Orthop Surg 13, 77, 2005.
4. Costantino, P. D., Chaplin, J. M., Wolpoe, M. E., Catalano, P. J., Sen, C., Bederson, J. B., and Govindaraj, S. Applications of fast-setting hydroxyapatite cement: cranioplasty. Otolaryngol Head Neck Surg 123, 409, 2000.
5. Turk, J. B., and Parhiscar, A. BoneSource for craniomaxillofacial reconstruction. Facial Plast Surg 16, 7, 2000.
6. Garbuz, D. S., Masri, B. A., and Czitrom, A. A. Biology of allografting. Orthop Clin North Am 29, 199, 1998.
7. Kubler, N., Michel, C., Zoller, J., Bill, J., Muhling, J., and Reuther, J. Repair of human skull defects using osteoinductive bone alloimplants. J Craniomaxillofac Surg 23, 337, 1995.
8. Mulliken, J. B., Glowacki, J., Kaban, L. B., Folkman, J., and Murray, J. E. Use of demineralized allogeneic bone implants for the correction of maxillocraniofacial deformities. Ann Surg 194, 366, 1981.
9. Rosenthal, R. K., Folkman, J., and Glowacki, J. Demineralized bone implants for nonunion fractures, bone cysts, and fibrous lesions. Clin Orthop Relat Res 364, 61, 1999.
10. Upton, J., Boyajian, M., Mulliken, J. B., and Glowacki, J. The use of demineralized xenogeneic bone implants to correct phalangeal defects: a case report. J Hand Surg [Am] 9, 388, 1984.
11. Bruder, S. P., and Fox, B. S. Tissue engineering of bone. Cell based strategies. Clin Orthop Relat Res (367 Suppl), S68, 1999.
12. Lane, J. M., Yasko, A. W., Tomin, E., Cole, B. J., Waller, S., Browne, M., Turek, T., and Gross, J. Bone marrow and recombinant human bone morphogenetic protein-2 in osseous repair. Clin Orthop Relat Res (361), 216, 1999.
13. De Long, W. G., Jr., Einhorn, T. A., Koval, K., McKee, M., Smith, W., Sanders, R., and Watson, T. Bone grafts and bone graft substitutes in orthopaedic trauma surgery. A critical analysis. J Bone Joint Surg Am 89, 649, 2007.
14. Sampath, T. K., and Reddi, A. H. Homology of bone-inductive proteins from human, monkey, bovine, and rat extracellular matrix. Proc Natl Acad Sci USA 80, 6591, 1983.
15. Schmitt, J. M., Hwang, K., Winn, S. R., and Hollinger, J. O. Bone morphogenetic proteins: an update on basic biology and clinical relevance. J Orthop Res 17, 269, 1999.
16. Edwards, J. T., Diegmann, M. H., and Scarborough, N. L. Osteoinduction of human demineralized bone: characterization in a rat model. Clin Orthop Relat Res (357), 219, 1998.
17. Honsawek, S., Powers, R. M., and Wolfinbarger, L. Extractable bone morphogenetic protein and correlation with induced new bone formation in an in vivo assay in the athymic mouse model. Cell Tissue Bank 6, 13, 2005.
18. Kado, K. E., Gambetta, L. A., and Perlman, M. D. Uses of Grafton for reconstructive foot and ankle surgery. J Foot Ankle Surg 35, 59, 1996.
19. Russell, J., Scarborough, N., and Chesmel, K. Re: ability of commercial demineralized freeze-dried bone allograft to induce new bone formation (1996;67:918-26). J Periodontol 68, 804, 1997.
20. Sandhu, H. S., Khan, S. N., Suh, D. Y., and Boden, S. D. Demineralized bone matrix, bone morphogenetic proteins, and animal models of spine fusion: an overview. Eur Spine J 10 (Suppl 2), S122, 2001.
21. Urist, M. R., and Dowell, T. A. Inductive substratum for osteogenesis in pellets of particulate bone matrix. Clin Orthop Relat Res 61, 61, 1968.
22. Rougraff, B. T., and Kling, T. J. Treatment of active unicameral bone cysts with percutaneous injection of demineralized bone matrix and autogenous bone marrow. J Bone Joint Surg Am 84-A, 921, 2002.
23. Tiedeman, J. J., Connolly, J. F., Strates, B. S., and Lippiello, L. Treatment of nonunion by percutaneous injection of bone marrow and demineralized bone matrix. An experimental study in dogs. Clin Orthop Relat Res (268), 294, 1991.
24. Sikavitsas, V. I., Bancroft, G. N., Holtorf, H. L., Jansen, J. A., and Mikos, A. G. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci USA 100, 14683, 2003.
25. Katz, J. M., Nataraj, C., Jaw, R., Deigl, E., and Bursac, P. Demineralized bone matrix as an osteoinductive biomaterial and in vitro predictors of its biological potential. J Biomed Mater Res B Appl Biomater 89, 127, 2009.
26. Andrades, J. A., Santamaria, J. A., Nimni, M. E., and Becerra, J. Selection and amplification of a bone marrow cell population and its induction to the chondro-osteogenic lineage by rhOP-1: an in vitro and in vivo study. Int J Dev Biol 45, 689, 2001.
27. Gordon, J. A., Tye, C. E., Sampaio, A. V., Underhill, T. M., Hunter, G. K., and Goldberg, H. A. Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone 41, 462, 2007.
28. Kon, E., et al. Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J Biomed Mater Res 49, 328, 2000.
29. Mauney, J. R., Jaquiery, C., Volloch, V., Heberer, M., Martin, I., and Kaplan, D. L. In vitro and in vivo evaluation of differentially demineralized cancellous bone scaffolds combined with human bone marrow stromal cells for tissue engineering. Biomaterials 26, 3173, 2005.
30. Petite, H., Viateau, V., Bensaid, W., Meunier, A., de Pollak, C., Bourguignon, M., Oudina, K., Sedel, L., and Guillemin, G. Tissue-engineered bone regeneration. Nat Biotechnol 18, 959, 2000.
31. Hattori, H., et al. Osteogenic potential of human adipose tissue-derived stromal cells as an alternative stem cell source. Cells Tissues Organs 178, 2, 2004.
32. Le Blanc, K., and Ringden, O. Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr Opin Immunol 18, 586, 2006.
33. Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., and Hedrick, M. H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7, 211, 2001.
34. Goodell, M. A., Brose, K., Paradis, G., Conner, A. S., and Mulligan, R. C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183, 1797, 1996.
35. Alvi, A. J., Clayton, H., Joshi, C., Enver, T., Ashworth, A., Vivanco, M. M., Dale, T. C., and Smalley, M. J. Functional and molecular characterisation of mammary side population cells. Breast Cancer Res 5, R1, 2003.
36. Asakura, A., Komaki, M., and Rudnicki, M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68, 245, 2001.
37. Asakura, A., and Rudnicki, M. A. Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 30, 1339, 2002.
38. Leatherman, B. D., and Dornhoffer, J. L. The use of demineralized bone matrix for mastoid cavity obliteration. Otol Neurotol 25, 22; discussion 25-26, 2004.
39. Lin, X., Pena, L. A., Zamora, P. O., Campion, S. L., and Takahashi, K. Augmentation of demineralized bone matrix (DBM) mineralization by a synthetic growth factor mimetic. J Orthop Res 24, 2051, 2006.
40. Shimano, K., Satake, M., Okaya, A., Kitanaka, J., Kitanaka, N., Takemura, M., Sakagami, M., Terada, N., and Tsujimura, T. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am J Pathol 163, 3, 2003.
41. Summer, R., Kotton, D. N., Sun, X., Ma, B., Fitzsimmons, K., and Fine, A. Side population cells and Bcrp1 expression in lung. Am J Physiol Lung Cell Mol Physiol 285, L97, 2003.
42. Welm, B. E., Tepera, S. B., Venezia, T., Graubert, T. A., Rosen, J. M., and Goodell, M. A. Sca-1 (pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 245, 42, 2002.
43. Ramos, T. V., Wang, T., Maki, C. B., Pascual, M., and Izadyar, F. Adipose stem cell side population in the mouse. J Tissue Eng Regen Med 3, 430, 2009.
44. Pacaccio, D. J., and Stern, S. F. Demineralized bone matrix: basic science and clinical applications. Clin Podiatr Med Surg 22, 599, vii, 2005.
45. Schouten, C. C., Hartman, E. H., Spauwen, P. H., and Jansen, J. A. DBM induced ectopic bone formation in the rat: the importance of surface area. J Mater Sci Mater Med 16, 149, 2005.
46. Chen, D., Zhao, M., and Mundy, G. R. Bone morphogenetic proteins. Growth Factors 22, 233, 2004.
47. Puleo, D. A., Holleran, L. A., Doremus, R. H., and Bizios, R. Osteoblast responses to orthopedic implant materials in vitro. J Biomed Mater Res 25, 711, 1991.
48. Voytik-Harbin, S. L., Brightman, A. O., Waisner, B., Lamar, C. H., and Badylak, S. F. Application and evaluation of the alamarBlue assay for cell growth and survival of fibroblasts. In Vitro Cell Dev Biol Anim 34, 239, 1998.
49. Hattori, H., et al. Osteogenic potential of human adipose tissue-derived stromal cells as an alternative stem cell source. Cells Tissues Organs 178, 2, 2004. (Pubitemid 19198635)
50. Ramos, T. V., Wang, T., Supronowicz, P., and Silva, F. Adipose derived satellite stem cell side population in human and mouse. Poster presented as part of the International Society for Stem Cell Research Annual Meeting, Philadelphia, PA, June 11-14, 2008.
51. de Girolamo, L., Sartori, M. F., Albisetti, W., and Brini, A. T. Osteogenic differentiation of human adipose-derived stem cells: comparison of two different inductive media. J Tissue Eng Regen Med 1, 154, 2007.
52. Challen, G. A., Bertoncello, I., Deane, J. A., Ricardo, S. D., and Little, M. H. Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J Am Soc Nephrol 17, 1896, 2006.
53. Challen, G. A., and Little, M. H. A side order of stem cells: the SP phenotype. Stem Cells 24, 3, 2006.
54. Aubin, J. E., Liu, F., Malaval, L., and Gupta, A. K. Osteoblast and chondroblast differentiation. Bone 17 (2 Suppl), 77S, 1995.
55. Gurevitch, O., Kurkalli, B. G., Prigozhina, T., Kasir, J., Gaft, A., and Slavin, S. Reconstruction of cartilage, bone, and hematopoietic microenvironment with demineralized bone matrix and bone marrow cells. Stem Cells 21, 588, 2003.
56. Wang, J. C., Alanay, A., Mark, D., Kanim, L. E., Campbell, P. A., Dawson, E. G., and Lieberman, J. R. A comparison of commercially available demineralized bone matrix for spinal fusion. Eur Spine J 16, 1233, 2007.
57. Wozniak, M., Fausto, A., Carron, C. P., Meyer, D. M., and Hruska, K. A. Mechanically strained cells of the osteoblast lineage organize their extracellular matrix through unique sites of alphavbeta3-integrin expression. J Bone Miner Res 15, 1731, 2000.
58. Hessle, L., Johnson, K. A., Anderson, H. C., Narisawa, S., Sali, A., Goding, J. W., Terkeltaub, R., and Millan, J. L. Tissuenonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci USA 99, 9445, 2002.
59. Pietrzak, W. S., Perns, S. V., Keyes, J., Woodell-May, J., and McDonald, N. M. Demineralized bone matrix graft: a scientific and clinical case study assessment. J Foot Ankle Surg 44, 345, 2005.
60. Stein, G. S., Lian, J. B., and Owen, T. A. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J 4, 3111, 1990.
61. Bancroft, G. N., Sikavitsas, V. I., van den Dolder, J., Sheffield, T. L., Ambrose, C. G., Jansen, J. A., and Mikos, A. G. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA 99, 12600, 2002.
62. Datta, N., Holtorf, H. L., Sikavitsas, V. I., Jansen, J. A., and Mikos, A. G. Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials 26, 971, 2005.
63. Dworetzky, S. I., Fey, E. G., Penman, S., Lian, J. B., Stein, J. L., and Stein, G. S. Progressive changes in the protein composition of the nuclear matrix during rat osteoblast differentiation. Proc Natl Acad Sci USA 87, 4605, 1990.
64. Lian, J. B., and Stein, G. S. Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation. Crit Rev Oral Biol Med 3, 269, 1992.
65. Mizuno, M., Imai, T., Fujisawa, R., Tani, H., and Kuboki, Y. Bone sialoprotein (BSP) is a crucial factor for the expression of osteoblastic phenotypes of bone marrow cells cultured on type I collagen matrix. Calcif Tissue Int 66, 388, 2000.
66. Yamate, T., Mocharla, H., Taguchi, Y., Igietseme, J. U., Manolagas, S. C., and Abe, E. Osteopontin expression by osteoclast and osteoblast progenitors in the murine bone marrow: demonstration of its requirement for osteoclastogenesis and its increase after ovariectomy. Endocrinology 138, 3047, 1997.
67. Lee, J. H., Rhie, J. W., Oh, D. Y., and Ahn, S. T. Osteogenic differentiation of human adipose tissue-derived stromal cells (hASCs) in a porous three-dimensional scaffold. Biochem Biophys Res Commun 370, 456, 2008.
68. Bruder, S. P., Jaiswal, N., Ricalton, N. S., Mosca, J. D., Kraus, K. H., and Kadiyala, S. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res (355 Suppl), S247, 1998.
69. Yao, K. L., Todescan, R., Jr., and Sodek, J. Temporal changes in matrix protein synthesis and mRNA expression during mineralized tissue formation by adult rat bone marrow cells in culture. J Bone Miner Res 9, 231, 1994.
70. Imitola, J., Comabella, M., Chandraker, A. K., Dangond, F., Sayegh, M. H., Snyder, E. Y., and Khoury, S. J. Neural stem/progenitor cells express costimulatory molecules that are differentially regulated by inflammatory and apoptotic stimuli. Am J Pathol 164, 1615, 2004.
71. Vilalta, M., et al. Dual luciferase labelling for non-invasive bioluminescence imaging of mesenchymal stromal cell chondrogenic differentiation in demineralized bone matrix scaffolds. Biomaterials 30, 4986, 2009.
72. Zhao, Y., Lin, H., Zhang, J., Chen, B., Sun, W., Wang, X., Zhao, W., Xiao, Z., and Dai, J. Crosslinked three-dimensional demineralized bone matrix for the adipose-derived stromal cell proliferation and differentiation. Tissue Eng Part A 15, 13, 2009.