Immunomodulation of delayed-type hypersensitivity responses by mesenchymal stem cells is associated with bystander T cell apoptosis in the draining lymph node

Journal of Immunology

Volumn 185, Issue 7, 2010, Pages 4022-4029

  Lim, Jong Hyung ^a   Kim, Jung Sik ^a   Yoon, Il Hee ^a   Shin, Jun Seop ^a   Nam, Hye Young ^a   Yang, Seung Ha ^a   Kim, Sang Joon ^a   Park, Chung Gyu ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CD3 ANTIGEN; NITRIC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; B LYMPHOCYTE; BYSTANDER EFFECT; CELL COUNT; CELL MIGRATION; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; GERMINAL CENTER; IMMUNE RESPONSE; IMMUNOMODULATION; LYMPH NODE CELL; LYMPHOCYTIC INFILTRATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; ANIMAL; ARTICLE; C57BL MOUSE; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; LYMPH NODE; METABOLISM; NEUTROPHIL CHEMOTAXIS; NICK END LABELING; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; BYSTANDER EFFECT; CELL SEPARATION; CHEMOTAXIS, LEUKOCYTE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HYPERSENSITIVITY, DELAYED; IMMUNOMODULATION; IN SITU NICK-END LABELING; LYMPH NODES; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NITRIC OXIDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 77958139165     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902723     Document Type: Review

References (37)

1. Friedenstein, A. J., I. I. Piatetzky-Shapiro, and K. V. Petrakova. 1966. Osteogenesis in transplants of bone marrow cells. J. Embryol. Exp. Morphol. 16:381-390.
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. Pereira, R. F., M. D. O'Hara, A. V. Laptev, K. W. Halford, M. D. Pollard, R. Class, D. Simon, K. Livezey, and D. J. Prockop. 1998. Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc. Natl. Acad. Sci. USA 95:1142-1147.
4. Kopen, G. C., D. J. Prockop, and D. G. Phinney. 1999. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. USA 96:10711-10716.
5. Koç, O. N., S. L. Gerson, B. W. Cooper, S. M. Dyhouse, S. E. Haynesworth, A. I. Caplan, and H. M. Lazarus. 2000. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J. Clin. Oncol. 18:307-316.
6. Le Blanc, K., I. Rasmusson, B. Sundberg, C. Götherström, M. Hassan, M. Uzunel, and O. Ringdén. 2004. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439-1441.
7. Sasaki, M., R. Abe, Y. Fujita, S. Ando, D. Inokuma, and H. Shimizu. 2008. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J. Immunol. 180:2581-2587.
8. Glennie, S., I. Soeiro, P. J. Dyson, E. W. Lam, and F. Dazzi. 2005. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105:2821-2827.
9. Corcione, A., F. Benvenuto, E. Ferretti, D. Giunti, V. Cappiello, F. Cazzanti, M. Risso, F. Gualandi, G. L. Mancardi, V. Pistoia, and A. Uccelli. 2006. Human mesenchymal stem cells modulate B-cell functions. Blood 107:367-372.
10. Ramasamy, R., H. Fazekasova, E. W. Lam, I. Soeiro, G. Lombardi, and F. Dazzi. 2007. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation 83:71-76.
11. Spaggiari, G. M., A. Capobianco, S. Becchetti, M. C. Mingari, and L. Moretta. 2006. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 107:1484-1490.
12. Di Nicola, M., C. Carlo-Stella, M. Magni, M. Milanesi, P. D. Longoni, P. Matteucci, S. Grisanti, and A. M. Gianni. 2002. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838-3843.
13. Sato, K., K. Ozaki, I. Oh, A. Meguro, K. Hatanaka, T. Nagai, K. Muroi, and K. Ozawa. 2007. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109:228-234.
14. Aggarwal, S., and M. F. Pittenger. 2005. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815-1822.
15. Meisel, R., A. Zibert, M. Laryea, U. Göbel, W. Däubener, and D. Dilloo. 2004. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase-mediated tryptophan degradation. Blood 103:4619-4621.
16. Zappia, E., S. Casazza, E. Pedemonte, F. Benvenuto, I. Bonanni, E. Gerdoni, D. Giunti, A. Ceravolo, F. Cazzanti, F. Frassoni, et al. 2005. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106:1755-1761.
17. Gerdoni, E., B. Gallo, S. Casazza, S. Musio, I. Bonanni, E. Pedemonte, R. Mantegazza, F. Frassoni, G. Mancardi, R. Pedotti, and A. Uccelli. 2007. Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann. Neurol. 61:219-227.
18. Xu, G., L. Zhang, G. Ren, Z. Yuan, Y. Zhang, R. C. Zhao, and Y. Shi. 2007. Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Res. 17:240-248.
19. Plumas, J., L. Chaperot, M. J. Richard, J. P. Molens, J. C. Bensa, and M. C. Favrot. 2005. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 19:1597-1604.
20. Benvenuto, F., S. Ferrari, E. Gerdoni, F. Gualandi, F. Frassoni, V. Pistoia, G. Mancardi, and A. Uccelli. 2007. Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells 25:1753-1760.
21. Raffaghello, L., G. Bianchi, M. Bertolotto, F. Montecucco, A. Busca, F. Dallegri, L. Ottonello, and V. Pistoia. 2008. Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche. Stem Cells 26:151-162.
22. Ren, G., L. Zhang, X. Zhao, G. Xu, Y. Zhang, A. I. Roberts, R. C. Zhao, and Y. Shi. 2008. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2:141-150.
23. Yang, S. H., M. J. Park, I. H. Yoon, S. Y. Kim, S. H. Hong, J. Y. Shin, H. Y. Nam, Y. H. Kim, B. Kim, and C. G. Park. 2009. Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10. Exp. Mol. Med. 41:315-324.
24. Varona, R., R. Villares, L. Carramolino, I. Goya, A. Zaballos, J. Gutiérrez, M. Torres, C. Martínez-A, and G. Márquez. 2001. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J. Clin. Invest. 107: R37-R45.
25. Garrigue, J. L., J. F. Nicolas, R. Fraginals, C. Benezra, H. Bour, and D. Schmitt. 1994. Optimization of the mouse ear swelling test for in vivo and in vitro studies of weak contact sensitizers. Contact Dermat. 30:231-237.
26. Gao, J., J. E. Dennis, R. F. Muzic, M. Lundberg, and A. I. Caplan. 2001. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs (Print) 169:12-20.
27. 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.
28. Von Lüttichau, I., M. Notohamiprodjo, A. Wechselberger, C. Peters, A. Henger, C. Seliger, R. Djafarzadeh, R. Huss, and P. J. Nelson. 2005. Human adult CD34-progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev. 14:329-336.
29. Malorny, U., M. Goebeler, J. Gutwald, J. Roth, and C. Sorg. 1990. Differences in migration inhibitory factor production by C57Bl/6 and BALB/c mice in allergic and irritant contact dermatitis. Int. Arch. Allergy Appl. Immunol. 92:356-360.
30. Vadas, M. A., J. F. Miller, J. Gamble, and A. Whitelaw. 1975. A radioisotopic method to measure delayed type hypersensitivity in the mouse. I. Studies in sensitized and normal mice. Int. Arch. Allergy Appl. Immunol. 49:670-692.
31. Wang, B., H. Fujisawa, L. Zhuang, I. Freed, B. G. Howell, S. Shahid, G. M. Shivji, T. W. Mak, and D. N. Sauder. 2000. CD4+ Th1 and CD8+ type 1 cytotoxic T cells both play a crucial role in the full development of contact hypersensitivity. J. Immunol. 165:6783-6790.
32. Djouad, F., V. Fritz, F. Apparailly, P. Louis-Plence, C. Bony, J. Sany, C. Jorgensen, and D. Noël. 2005. Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum. 52:1595-1603.
33. Ohtaki, H., J. H. Ylostalo, J. E. Foraker, A. P. Robinson, R. L. Reger, S. Shioda, and D. J. Prockop. 2008. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc. Natl. Acad. Sci. USA 105:14638-14643.
34. Németh, K., A. Leelahavanichkul, P. S. Yuen, B. Mayer, A. Parmelee, K. Doi, P. G. Robey, K. Leelahavanichkul, B. H. Koller, J. M. Brown, et al. 2009. Bone marrow stromal cells attenuate sepsis via prostaglandin E (2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 15:42-49.
35. Eisen, H. N., L. Orris, and S. Belman. 1952. Elicitation of delayed allergic skin reactions with haptens; the dependence of elicitation on hapten combination with protein. J. Exp. Med. 95:473-487.
36. Mouiseddine, M., S. François, A. Semont, A. Sache, B. Allenet, N. Mathieu, J. Frick, D. Thierry, and A. Chapel. 2007. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br. J. Radiol. 80 (Spec No 1): S49-S55.
37. Chapel, A., J. M. Bertho, M. Bensidhoum, L. Fouillard, R. G. Young, J. Frick, C. Demarquay, F. Cuvelier, E. Mathieu, F. Trompier, et al. 2003. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J. Gene Med. 5:1028-1038.