The immunogenicity and immunomodulatory function of osteogenic cells differentiated from mesenchymal stem cells

Journal of Immunology

Volumn 176, Issue 5, 2006, Pages 2864-2871

  Liu, Hua ^a   Kemeny, David Michael ^b   Heng, Boon Chin ^a   Ouyang, Hong Wei ^c   Melendez, Alirio J ^d   Cao, Tong ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSFORMING GROWTH FACTOR BETA;

ALLOGENEIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FUNCTION; CELL TYPE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; FEMALE; GRAFT REJECTION; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOMODULATION; IN VITRO STUDY; LYMPHOCYTE CULTURE; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NEW ZEALAND; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; RABBIT; SKIN TRANSPLANTATION; STATISTICAL SIGNIFICANCE; SURVIVAL; TISSUE REGENERATION;

EID: 33644522374     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.5.2864     Document Type: Article

References (46)

1. Kadiyala, S., R. G. Young, M. A. Thiede, and S. P. Bruder. 1997. Culture expanded canine mesanchymal stem cells possess osteochondrogenic potential in vivo and in vitro. Cell. Transplant. 6: 125-134.
2. Pittenger, M. F., A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, J. D. Mosca, M. A. Moorman, D. W. Simonetti, S. Craig, and D. R. Marshak. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
3. Fibbe, W. E. 2002. Mesenchymal stem cells: a potential source for skeletal repair. Ann. Rheum. Dis. 61: ii29-ii31.
4. Ko, O. C., and S. L. Gerson. 2003. Mesenchymal stem cells in allogeneic transplantation. In Allogeneic Stem Cell Transplantation: Clinical Research and Practice. M. J. Laughlin and H. M. Lazarus, eds. Humana Press, Totowa, pp. 151-158.
5. Bruder, S. P., N. Jaiswal, N. S. Ricalton, J. D. Mosca, K. H. Kraus, and S. Kadiyala. 1998. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin. Orthop. 355(Suppl.): S247-S256.
6. Connolly, J. F. 1998. Clinical use of marrow osteoprogenitor cells to stimulate osteogenesis. Clin. Orthop. 355(Suppl.): S257-S266.
7. Quarto, R., M. Mastrogiacomo, R. Cancedda, S. M. Kutepov, V. Mukhachev, A. Lavroukov, E. Kon, and M. Marcacci. 2001. Repair of large bone defects with the use of autologous bone marrow stromal cells. N. Engl. J. Med. 344: 385-386.
8. De Kok, I. J., S. J. Peter, M. Archambault, C. van den Bos, S. Kadiyala, I. Aukhil, and L. F. Cooper. 2003. Investigation of allogeneic mesenchymal stem cell-based alveolar bone formation: preliminary findings. Clin. Oral Impl. Res. 14:481-489.
9. Wong, R. K., E. U. Hagg, A. B. Rabie and D. W. Lau. 2002. Bone induction in clinical orthodontics: a review. Int. J. Adult Orthodon. Orthognath. Surg. 17: 140-149.
10. Bartholomew, A., C. Sturgeon, M. Siatskas, K. Ferrer, K. McIntosh, S. Patil, W. Hardy, S. Devine, D. Ucker, R. Deans, et al. 2002. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30: 42-48.
11. Di Nicola, M., C. Carlo-Stella, M. Magni, M. Milanesi, P. D. Longoni, P. Matteucci, S. Grisanti, A. M. Gianni, and P. D. Longoni. 2002. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99: 3838-3843.
12. Le Blanc, K. 2003. Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy 5: 485-489.
13. Le Blanc, K., L. Tammik, B. Sundberg, S. E. Haynesworth, and O. Ringdén. 2003. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 57: 11-20.
14. Tse, W. T., J. D. Pendleton, W. M. Beyer, M. C. Egalka, and E. C. Guinan. 2003. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implication in transplantation. Transplantation 75: 389-397.
15. Krampera, M., S. Glennie, J. Dyson, D. Scott, R. Laylor, E. Simpson, and F. Dazzi. 2003. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101: 3722-3729.
16. Maitra, B., E. Szekely, K. Gjini, M. J. Laughlin, J. Dennis, S. E. Haynesworth, and O. C. Ko. 2004. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant. 33: 597-604.
17. McManus, P. M., and L. Weiss. 1984. Busulfan-induced chronic bone marrow failure: changes in cortical bone, marrow stromal cells, and adherent cell colonies. Blood 64: 1036-1041.
18. Uhlman, D. L., C. Verfaillie, R. B. Jones, and S. D. Luikart. 1991. BCNU treatment of marrow stromal monolayers reversibly alters haematopoiesis. Br. J. Haematol. 78: 304-309.
19. Rasmusson, I., O. Ringdén, B. Sundberg, and K. Le Blanc. 2003. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76: 1208-1213.
20. Li, Y., H. Hisha, M. Inaba, Z. Lian, C. Yu, M. Kawamura, Y. Yamamoto, N. Nishio, J. Toki, H. Fan, and S. Ikehara. 2000. Evidence for migration of donor bone marrow stromal cells into recipient thymus after bone marrow transplantation plus bone grafts: a role of stromal cells in positive selection. Exp. Hematol. 28: 950-960.
21. Devine, S. M., C. Cobbs, M. Jennings, A. Bartholomew, and R. Hoffman. 2003. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 101: 2999-3001.
22. Le Blanc, K., C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringdén. 2003. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp. Hematol. 31: 890-896.
23. Zhang, W., W. Ge, C. Li, S. You, L. Liao, Q. Han, W. Deng, and R. C. Zhao. 2004. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev. 13: 263-271.
24. Aggarwal, S., and M. F. Pittenger. 2005. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105: 1815-1822.
25. Horwitz, E. M., P. L. Gordon, W. K. Koo, J. C. Marx, M. D. Neel, R. Y. McNall, L. Muul, and T. Hofmann. 2002. 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 99: 8932-8937.
26. Arinzeh, T. L., S. J. Peter, M. P. Archambault, C. van den Bos, S. Gordon, K. Kraus, A. Smith, and S. Kadiyala. 2003. Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect. J. Bone Joint Surg. 85: 1927-1935.
27. Jaiswal, N., S. E. Haynesworth, A. I. Caplan, and S. P. Bruder. 1997. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J. Cell. Biochem. 64: 295-312.
28. Tsubota, S., H. Tsuchiya, Y. Shinokawa, K. Tomita, and H. Minato. 1999. Transplantation of osteoblast-like cells to the distracted callus in rabbits. J. Bone Joint Surg. 81: 125-129.
29. Solchaga, L. A., B. Johnstone, J. U. Yoo, V. M. Goldberg, and A. I. Caplan. 1999. High variability in rabbit bone marrow-derived mesenchymal cell preparation. Cell. Transplant. 8: 511-519.
30. Koyama, N., K. Ohara, H. Yokota, T. Kurome, M. Katayama, F. Hino, I. Kato, and T. Akai. 1991. A one step sandwich enzyme immunoassay for γ-carboxylated osteocalcin using monoclonal antibodies. J. Immunol. Methods 139: 17-23.
31. Yoo, J. U., T. S. Bartheland, K. Nishimura, L. Solchaga, A. I. Caplan, V. M. Goldberg, and B. Johnstone. 1998. The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J. Bone Joint Surg. 80: 1745-1757.
32. Johnstone, B., T. M. Hering, A. I. Caplan, V. M. Goldberg, and J. U. Yoo. 1998. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 238: 265-272.
33. Cao, T., K. H. Ho, and S. H. Teoh. 2004. Scaffold design and in vitro study of ostochondral coculture in a three-dimensional porous polycaprolactone scaffold fabricated by fused deposition modeling. Tissue Eng. 9(Suppl. 1): S103-S112.
34. Ishiko, O., T. Sumi, H. Yoshida, Y. Hyun, and S. Ogita. 2001. Angiogenesis in the adipose tissue of tumor-bearing rabbits treated by cyclic plasma perfusion. Int. J. Oncol. 19: 785-790.
35. Majumdar, M. K., M. Keane-Moore, and D. Buyaner. 2003. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J. Biomed. Sci. 10: 228-241.
36. Junger, W. G., D. B. Hoyt, F. C. Liu, W. H. Loomis, and R. Coimbra. 1996. Immunosuppression after endotoxin shock: the result of multiple antiinflammatory factors. J. Trauma 40: 702-709.
37. Kunz, C. R., M. R. Jadus, G. D. Kukes, F. Kramer, V. N. Nguyen, and S. A. Sasse. 2004. Intrapleural injection of transforming growth factor-β antibody inhibits pleural fibrosis in empyema. Chest 126: 1636-1644.
38. Sasse, S. A., M. R. Jadus, and G. D. Kukes. 2003. Pleural fluid transforming growth factor-β1 correlates with pleural fibrosis in experimental empyema. Am. J. Respir. Crit. Care Med. 168: 700-705.
39. Ashton, B. A., T. D. Allen, C. R. Howlett, C. C. Eaglesom, A. Hattori, and M. Owen. 1980. Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vitro. Clin. Orthod. Res. 151: 294-307.
40. Johnson, K. A., C. R. Howlett, C. R. Bellenger, and P. Armati-Gulson. 1988. Osteogenesis by canine and rabbit bone marrow in diffusion chambers. Calcif. Tissue Int. 42: 113-118.
41. Binet, I., and K. J. Wood. 2003. In vivo models of inflammation: immune rejection and skin transplantation in vivo. In Methods in Molecular Biology, Vol. 225: Inflammation Protocols. P. G. Winyard and D. A. Willoughby, eds. Humana Press, Totowa, pp. 239-248.
42. Reyes-Botella, C., M. J. Montes, M. F. Vallecillo-Capilla, E. G. Olivares, and C. Ruiz. 2000. Expression of molecules involved in antigen presentation and T cell activalion (HLA-DR, CD80, CD86, CD44 and CD54) by cultured human osleoblasts. J. Periodontol. 71: 614-617.
43. Skjødt, H., T. Møller, and S. F. Freiesleben. 1989. Human osteoblast-like cells expressing MHC class II determinants stimulate allogeneic and autologous peripheral blood mononuclear cells and function as antigen-presenting cells. Immunology 68: 416-420.
44. Gruber, H. E. 1991. Bone and the immune system. Proc. Soc. Exp. Biol. Med. 197: 219-225.
45. Marriott, I., D. L. Gray, S. L. Tranguch, V. G. Fowler, Jr., M. Stryjewski, L. Scott Levin, M. C. Hudson, and K. L. Bost. 2004. Osteoblasts express the inflammatory cytokine interleukin-6 in a murine model of Staphylococcus aureus osteomyelitis and infected human bone tissue. Am. J. Pathol. 164: 1399-1406.
46. Reyes-Botella, C., M. J. Montes, M. F. Vallecillo-Capilla, E. G. Olivares, and C. Ruiz. 2002. Antigenic phenotype of cultured human osteoblast-like cells. Cell. Physlol. Biochem. 12: 359-364.