Functional and phenotypic alteration of intrasplenic lymphocytes affected by mesenchymal stem cells in a murine allosplenocyte transfusion model

Cell Transplantation

Volumn 16, Issue 1, 2007, Pages 85-95

  Li, Hong ^a   Guo, Zi Kuan ^a   Li, Xiu Sen ^a   Hou, Chun Mei ^a   Tang, Pei Hsien ^a   Mao, Ning ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

Immunomodulation; In vivo; Lymphocyte subsets; Mesenchymal stem cells; Murine model

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ALLOGENEIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GRAFT VERSUS HOST REACTION; IMMUNOMODULATION; IN VIVO STUDY; INTESTINE; LIVER; LUNG PARENCHYMA; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; SPLEEN; SPLEEN LYMPHOCYTE; SURVIVAL TIME; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL;

MURINAE; MUS;

EID: 34047143246     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/000000007783464470     Document Type: Article

References (59)

1. Aggarwal, S.; Pittenger, M. F. Human mesenchymal stem cells modulate allogeneic immune responses. Blood 105(4):1815-1822; 2005.
2. Allers, C.; Sierralta, W. D.; Neubauer, S,; Rivera, F.; Minguell, J, J.; Conget, P. A, Dynamic of distribution of human bone marrow-derived mesenchymal stem cells after transplantation into adult unconditioned mice. Transplantation 78(4):503-508; 2004.
3. Anjos-Afonso, F.; Siapati, E. K.; Bonnet, D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J. Cell Sci. 117(Pt. 23):5655-5664; 2004.
4. Bartholomew, A.; Sturgeon, C.; Siatskas, M.; Ferrer, K.; McIntosh, K.; Patil, S.; Hardy, W.; Devine, S.; Ucker, D.; Deans, R.; Moseley, A.; Hoffman, R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30(1):42-48; 2002.
5. Beilhack, A.; Schulz, S.; Baker, J.; Beilhack, G. F.; Wieland, C. B.; Herman, E. I.; Baker, E. M.; Cao, Y. A.; Contag, C. H.; Negrin, R. S. In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood 106(3): 1113-1122; 2005.
6. Bendiksen, S.; Rekvig, O. P. Interleukin-2, but not interleukin-15, is required to terminate experimentally induced clonal T-cell anergy. Scand. J. Immunol. 60(l-2):64-73; 2004.
7. Bluestone, J. A.; Abbas, A. K. Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3(3):253-257; 2003.
8. Chatila, T. A. Role of regulatory T cells in human diseases. J. Allergy Clin. Immunol. 116(5):949-959; 2005.
9. Chapel, A.; Bertho, J. M.; Bensidhoum, M.; Fouillard, L.; Young, R. G.; Prick, J.; Demarquay, C.; Cuvelier, F.; Mathieu, E.; Trompier, F.; Dudoignon, N.; Germain, C.; Mazurier, C.; Aigueperse, J.; Borneman, J.; Gorin, N. C.; Gourmelon, P.; Thierry, D. 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(12):1028-1038; 2003.
10. Colson, Y. L.; Christopher, K.; Glickman, J.; Taylor, K. N.; Wright, R.; Perkins, D. L. Absence of clinical GvHD and the in vivo induction of regulatory T cells following facilitating cell transplantation. Blood 104(12): 3829-3835; 2004.
11. Dazzi, F.; Ramasamy, R.; Glennie, S.; Jones, S. P.; Roberts, I. The role of mesenchymal stem cells in haemopoiesis. Blood Rev. 20(3):161-171; 2006.
12. Deng, W.; Han, Q.; Liao, L.; Li, C.; Ge, W.; Zhao, Z.; You, S.; Deng, H.; Zhao, R. C. Allogeneic bone marrow-derived flk-1+Sca-1- mesenchymal stem cells leads to stable mixed chimerism and donor-specific tolerance. Exp. Hematol. 32(9):861-867; 2004.
13. Deng, W.; Han, Q.; Liao, L.; You, S.; Deng, H.; Zhao, R. C. Effects of allogeneic bone marrow-derived mesenchymal stem cells on T and B lymphocytes from BXSB mice. DNA Cell Biol. 24(7):458-463; 2005.
14. Devine, S. M.; Cobbs, C.; Jennings, M.; Bartholomew, A.; Hoffman, R. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 101(8):2999-3001; 2003.
15. Di Nicola, M.; Carlo-Stella, C.; Magni, M.; Milanesi, M.; Longoni, P. D.; Matteucci, P.; Grisanti, S.; Gianni, A. M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99(10):3838-3843; 2002.
16. Dicker, A.; Le Blanc, K.; Astrom, G.; van Harmelen, V.; Gotherstrom, C.; Blomqvist, L.; Arner, P.; Ryden, M. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp. Cell Res. 308(2): 283-290; 2005.
17. Duan, H. F.; Wu, C. T.; Wu, D. L.; Lu, Y.; Lu, H. J.; Ha, X. Q.; Zhang, Q. W.; Wang, H.; Jia, X. X.; Wang, L. S. Treatment of myocardial ischemia with bone marrow-derived mesenchymal stem cells overexpressing hepatocyte growth factor. Mol. Ther. 8(3):467-474; 2003.
18. Ermann, J.; Szanya, V.; Ford, G. S.; Paragas, V.; Fathman, C. G.; Lejon, K. CD4+CD25+ T cells facilitate the induction of T cell anergy. J. Immnol. 167(8):4271-4275; 2001.
19. Fantini, M. C.; Becker, C.; Tubbe, I.; Nikolaev, A.; Lehr, H. A.; Galle, P. R.; Neurath, M. F. TGF-β induced Foxp3+ regulatory T cells suppress Th1-mediated experimental colitis. Gut 55(5):671-680; 2006.
20. Fontenot, J. D.; Rasmussen, J. P.; Gavin, M. A.; Rudensky, A. Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6(11):1142-1151; 2005.
21. Friedenstein, A. J.; Chailakhjan, R. K.; Lalykina, K. S. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 3(4):393-403; 1970.
22. Fu, S.; Zhang, N.; Yopp, A. C.; Chen, D.; Mao, M.; Chen, D.; Zhang, H.; Ding, Y.; Bromberg, J. S. TGF-beta induces Foxp3 + T-regulatory cells from CD4+ CD25- precursors. Am. J. Transplant. 4(10):1614-1627; 2004.
23. Gao, J.; Dennis, J. E.; Muzic, R. F.; Lundberg, M.; Caplan, A. I. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 169(1):12-20; 2001.
24. Giulietti, A.; Overbergh, L.; Valckx, D.; Decallonne, B.; Bouillon, R.; Mathieu, C. An overview of real-time quantitative PCR: Applications to quantify cytokine gene expression. Methods 25(4):386-401; 2001.
25. Guo, Z. K.; Li, H.; Li, X. S.; Yu, X. D.; Wang, H. X.; Tang, P. X.; Mao, N. In vitro characteristics and in vivo immunosuppressive activity of compact bone-derived murine mesenchymal progenitor cells. Stem Cells 24(4):992-1000; 2006.
26. Guo, Z. K.; Yang, J. Q.; Liu, X. D.; Li, X. S.; Hou, C. M.; Tang, P. H.; Mao, N. Biological features of mesenchymal stem cells from human bone marrow. Chin. Med. J. 114(6):950-953;2001.
27. Hoffmann, P.; Ermann, J.; Edinger, M.; Fathmann, C. G.; Strober, S. Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J. Exp. Med. 196(3): 389-399; 2002.
28. Jiang, X. X.; Zhang, Y.; Liu, B.; Zhang, S. X.; Wu, Y.; Yu, X. D.; Mao, N. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105(10):4120-4126; 2005.
29. Johnstone, B.; Hering, T. M.; Caplan, A. I.; Goldberg, V. M.; Yoo, J. U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 238(l):265-272; 1998.
30. Kadiyala, S.; Young, R. G.; Thiede, M. A.; Bruder, S. P. Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro. Cell Transplant. 6(2):125-134; 1997.
31. Keilholz, U.; Dummer, R.; Welters, H.; Brado, B.; Galm, F.; Matheiowetz, P.; Hunstein, W. A modified cytotoxicity assay with high sensitivity. Scand. J. Clin. Lab. Invest. 50(8):879-884; 1990.
32. Korngold, R.; Sprent, J. Surface markers of T cells causing lethal graft-vs-host disease to class I vs class II H-2 differences. J. Immunol. 135(5):3004-3010; 1985.
33. Krampera, M.; Glennie, S.; Dyson, J.; Scott, D.; Laylor, R.; Simpson, E.; Dazzi, F. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101 (9):3722-3729; 2003.
34. Le Blanc, K.; Rasmusson, I.; Gotherstrom, C.; Seidel, C.; Sundberg, B.; Sundin, M.; Rosendahl, K.; Tammik, C.; Ringden, O. Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes. Scand. J. Immunol. 60(3):307-315; 2004.
35. Le Blanc, K.; Rasmusson, I.; Sundberg, B.; Gotherstrom, C.; Hassan, M.; Uzunel, M.; Ringden, O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363(9419): 1439-1441; 2004.
36. Le Blanc, K.; Tammik, L.; Sundberg, B.; Haynesworth, S. E.; Ringden, O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 57(1):11-20; 2003.
37. Li, X. C.; Zand, M. S.; Li, Y.; Zheng, X. X.; Strom, T. B. On histocompatibility barriers, Th1 to Th2 immune deviation, and the nature of the allograft responses. J. Immnol. 161(5):2241-2247; 1998.
38. Maerten, P.; Shen, C.; Bullens, D. M.; Van Assche, G.; Van Gool, S.; Geboes, K.; Rutgeerts, P.; Ceuppens, J. L. Effects of interleukin 4 on CD25+CD4+ regulatory T cell function. J. Autoimmun. 25(2): 112-120; 2005.
39. Maggi, E.; Cosmi, L.; Liotta, F.; Romagnani, P.; Romagnani, S.; Annunziato, F. Thymic regulatory T cells. Autoimmun. Rev. 4(8):579-586; 2005.
40. Majumdar, M. K.; Keane-Moore, M.; Buyaner, D.; Hardy, W. B.; Moorman, M. A.; McIntosh, K. R.; Mosca, J. D. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J. Biomed. Sci. 10(2):228-241;2003.
41. Martin, D. R.; Cox, N. R.; Hathcock, T. L.; Niemeyer, G. P.; Baker, H. J. Isolation and characterization of multipotential mesenchymal stem cells from feline bone marrow. Exp. Hematol. 30(8):879-886; 2002.
42. Mosca, J. D.; Hendricks, J. K.; Buyaner, D.; Davis-Sproul, J.; Chuang, L. C.; Majumdar, M. K.; Chopra, R.; Barry, F.; Murphy, M.; Thiede, M. A.; Junker, U.; Rigg, R. J.; Forestell, S. P.; Bohnlein, E.; Storb, R.; Sandmaier, B. M. Mesenchymal stem cells as vehicles for gene delivery. Clin. Orthop. Relat. Res. 379(Suppl.):S71-90; 2000.
43. Muguruma, Y.; Yahata, T.; Miyatake, H.; Sato, T.; Uno, T.; Itoh, J.; Kato, S.; Ito, M.; Hotta, T.; Ando, K. Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment. Blood 107(5): 1878-1887; 2005.
44. Peister, A.; Mellad, J. A.; Larson, B. L.; Hall, B. M.; Gibson, L. F.; Prockop, D. J. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103(5): 1662-1668; 2004.
45. Phinney, D. G.; Kopen, G.; Isaacson, R. L.; Prockop, D. J. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J. Cell Biochem. 72(4): 570-585; 1999.
46. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Misca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult mesenchymal stem cells. Science 284(5411):143-147; 1999.
47. Rasmusson, I.; Ringden, O.; Sundberg, B.; Le Blanc, K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76(8):1208-1213; 2003.
48. Rieger, K.; Loddenkemper, C.; Maul, J.; Fietz, T.; Wolff, D.; Terpe, H.; Steiner, B.; Berg, E.; Miehlke, S.; Bornhauser, M.; Schneider, T.; Zeitz, M.; Stein, H.; Thiel, E.; Duchmann, R.; Uharek, L. Mucosal FOXP3+ regulatory T cells are numerically deficient in acute and chronic GvHD. Blood 107(4): 1717-1723; 2006.
49. Ryan, J. M.; Barry, F. P.; Murphy, J. M.; Mahon, B. P. Mesenchymal stem cells avoid allogeneic rejection. J. Inflamm. (Lond.) 26(l):2-8; 2005.
50. Skapenko, A.; Kalden, J. R.; Lipsky, P. E.; Schulze-Koops, H. The IL-4 receptor alpha-chain-binding cytokines, IL-4 and IL-13, induce forkhead box P3-expressing CD25+CD4+ regulatory T cells from CD25-CD4+ precursors. J. Immunol. 175(9):6107-6116; 2005.
51. Sotiropoulou, P. A.; Perez, S. A.; Gritzapis, A. D.; Baxevanis, C. N.; Papamichail, M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 24(1):74-85; 2006.
52. Sun, S. K.; Guo, Z. K.; Xiao, X. R.; Li, B.; Liu, X. D.; Tang, P. H.; Mao, N. Isolation of mouse mesenchymal progenitors by a novel and reliable method. Stem Cells 21(3):527-535; 2003.
53. Taylor, P. A.; Lees, C. J.; Blazar, B. R. The infusion of ex vivo activated and expanded CD4+CD25+ immune regulatory cells inhibits graft-versus-host disease lethality. Blood 99(10):3493-3499; 2002.
54. Tse, W. T.; Pendleton, J. D.; Beyer, W. M.; Egalka, M. C.; Guinan, E. C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: Implications in transplantation. Transplantation 75(3):389-397; 2003.
55. Tuli, R.; Tuli, S.; Nandi, S.; Wang, M. L.; Alexander, P. G.; Haleem-Smith, H.; Hozack, W. J.; Manner, P. A.; Danielson, K. G.; Tuan, R. S. Characterization of multipotential mesenchymal progenitor cells derived from human trabecular bone. Stem Cells 21(6):681-693; 2003.
56. Wagner, W.; Wein, F.; Seckinger, A.; Frankhauser, M.; Wirkner, U.; Krause, U.; Blake, J.; Schwager, C.; Eckstein, V.; Ansorge, W.; Ho, A. D. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, andumbilical cord blood. Exp. Hematol. 33(11):1402-1416; 2005.
57. Wakitani, S.; Saito, T.; Caplan, A. I. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18(12):1417-1426; 1995.
58. Zappia, E.; Casazza, S.; Pedemonte, E.; Benvenuto, F.; Bonanni, I.; Gerdoni, E.; Giunti, D.; Ceravolo, A.; Cazzanti, F.; Frassoni, F.; Mancardi, G.; Uccelli, A. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106(5):1755-1761;2005.
59. Zhang, Y.; Li, C. D.; Jiang, Y. X.; Li, H. L.; Tang, P. H.; Mao, N. Comparison of mesenchymal stem cells from human placenta and bone marrow. Chin. Med. J. 117(6):882-887; 2004.