Human mesenchymal stem cells modulate allogeneic immune cell responses

Blood

Volumn 105, Issue 4, 2005, Pages 1815-1822

  Aggarwal, Sudeepta ^a   Pittenger, Mark F ^a  

^a OSIRIS THERAPEUTICS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ALLOGENEIC STEM CELL TRANSPLANTATION; ANTIGEN RECOGNITION; ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; EFFECTOR CELL; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPOTENT STEM CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; STATISTICAL ANALYSIS; TH1 CELL; TH2 CELL;

EID: 13544249606     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-04-1559     Document Type: Article

References (74)

1. Urist MR, McLean LF. Osteogenetic potency and new-bone formation by induction in transplants to the anterior chamber of the eye. J Bone Joint Surg Am. 1952;34A:443-476.
2. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970;3:393-403.
3. Owen M, Friedenstein AJ. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp. 1988;136:42-60.
4. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641-650.
5. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI. Characterization of cells with osteogenic potential from human marrow. Bone. 1992; 13:81-88.
6. Pittenger MF, Mackay AM, Beck SC, et al. Multi-lineage potential of adult human mesenchymal stem cells. Science. 1999;284:143-147.
7. Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci. 2000;113:1161-1166.
8. Wakitani S, Saito T, Caplan AI. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve. 1995;18:1417-1426.
9. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000; 61:364-370.
10. Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A. 1999;96:10711-10716.
11. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 2002;105:93-98.
12. Kawada H, Fujita J, Kinjo K, et al. Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Prepublished on August 5, 2004, as DOI 10.1182/blood-2004-04-1488. (Now available as Blood. 2004;104:3581-3587).
13. Kawada H, Fujita J, Kinjo K, et al. Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Prepublished on August 5, 2004, as DOI 10.1182/blood-2004-04-1488. (Now available as Blood. 2004;104:3581-3587).
14. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res. 2004;95:9-20.
15. Pereira RF, O'Hara MD, Laptev AV, et al. 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 U S A. 1998;95:1142-1147.
16. Liechty KW, MacKenzie TC, Shaaban AF, et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med. 2000;6: 1282-1286.
17. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res. 2000;9:841-848.
18. Haynesworth SE, Baber MA, Caplan AI. Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J Cell Physiol. 1996;166: 585-592.
19. Cheng L, Qasba P, Vanguri P, Thiede MA. Human mesenchymal stem cells support megakaryocyte and pro-platelet formation from CD34(+) hematopoietic progenitor cells. J Cell Physiol. 2000;184: 58-69.
20. Cheng L, Hammond H, Ye Z, Zhan X, Dravid G. Human adult marrow cells support prolonged expansion of human embryonic stem cells in culture. Stem Cells. 2003;21:131-142.
21. Tomita S, Li RK, Weisel RD, et al. Autologous transplantation of bone marrow cells improves damaged heart function. Circulation. 1999; 100(suppl II):II247-II256.
22. Shake JG, Gruber PJ, Baumgartner WA, et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg. 2002;73:1919-1925.
23. Noel D, Djouad F, Jorgense C. Regenerative medicine through mesenchymal stem cells for bone and cartilage repair. Curr Opin Investig Drugs. 2002;3:1000-1004.
24. Bruder SP, Kurth AA, Shea M, et al. Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res. 1998;16:155-162.
25. De Kok IJ, Peter SJ, Archambault M, et al. Investigation of allogeneic mesenchymal stem cell-based alveolar bone formation: preliminary findings. Clin Oral Implants Res. 2003;14:481-489.
26. Gao J, Dennis JE, Solchaga LA, et al. Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng. 2001;7:363-371.
27. Awad HA, Boivin GP, Dressler MR, et al. Repair of patellar tendon injuries using a cell-collagen composite. J Orthop Res. 2003;21:420-431.
28. Wakitani S, Goto T, Pineda SJ, et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am. 1994;76:579-592.
29. Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 2003;48:3464-3474.
30. Bittira B, Shum-Tim D, Al-Khaldi A, Chiu RC. Mobilization and homing of bone marrow stromal cells in myocardial infarction. Eur J Cardiothorac Surg. 2003;24:393-398.
31. Mackenzie TC, Flake AW. Human mesenchymal stem cells persist, demonstrate site-specific multipotential differentiation, and are present in sites of wound healing and tissue regeneration after transplantation into fetal sheep. Blood Cells Mol Dis. 2001;27:1-4.
32. Wu GD, Nolta JA, Jin YS, et al. Migration of mesenchymal stem cells to heart allografts during chronic rejection. Transplantation. 2003;75:679-685.
33. Perin EC, Dohmann HF, Borojevic R, et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation. 2003;107:2294-2302.
34. Stamm C, Kleine HD, Westphal B, et al. CABG and bone marrow stem cell transplantation after myocardial infarction. Thorac Cardiovasc Surg. 2004;52:152-158.
35. Britten MB, Abolmaali ND, Assmus B, et al. Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): mechanistic insights from serial contrast-enhanced magnetic resonance imaging. Circulation. 2003;108:2212-2218).
36. Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal NS, Caplan AI. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 1995;16:557-564.
37. Koc ON, Gerson SL, Cooper BW, et al. 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. 2000;18:307-316.
38. Koc ON, Day J, Nieder M, et al. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant. 2002;30:215-222.
39. Horwitz EM, Gordon PL, Koo WK, et al. 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 U S A. 2002; 99:8932-8937.
40. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004;363:1439-1441.
41. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymai stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol. 2003;57:11-20.
42. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99:3838-3843.
43. Potian JA, Aviv H, Ponzio NM, Harrison JS, Rameshwar P. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol. 2003;171:3426-3434.
44. Majumdar MK, Keane-Moore M, Buyaner D, et al. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci. 2003;10:228-241.
45. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation. 2003;75: 389-397.
46. Deans RJ, Moseley AB. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol. 2000;28:875-884.
47. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31: 890-896.
48. Mahmud N, Pang W, Cobbs C, et al. Studies of the route of administration and role of conditioning with radiation on unrelated allogeneic mis-matched mesenchymal stem cell engraftment in a nonhuman primate model. Exp Hematol. 2004; 32:494-501.
49. Arinzeh TL, Peter SJ, Archambault MP, et al. Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect. J Bone Joint Surg Am. 2003;85-A:1927-1935.
50. Grinnemo KH, Mansson A, Dellgren G, et al. Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium. J Thorac Cardiovasc Surg. 2004; 127:1293-1300.
51. Archambault MP, McIntosh KR, Duty A, Peter SJ. Allogeneic rat mesenchymal stem cells do not elicit an immune response after implantation in immunocompetent recipients [abstract]. Blood. 2000;96:762a. Abstract 3295.
52. Le Blanc K, Rasmusson I, Gotherstrom C, et al. Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes. Scand J Immunol. 2004;60:307-315.
53. Gotherstrom C, Ringden O, Westgren M, Tammik C, Le Blanc K. Immunomodulatory effects of human fetal liver-derived mesenchymal stem cells. Bone Marrow Transplant. 2003;32:265-272.
54. Zhang W, Ge W, Li C, et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev. 2004;13:263-271.
55. Lennon DP, Haynesworth SE, Bruder SP, Jaiswal N, Caplan AI. Human and animal mesenchymal progenitor cells from bone marrow: identification of serum for optimal selection and proliferation. In Vitro Cell Dev Biol. 1996;32:602-611.
56. Dzionek A, Fuchs A, Schmidt P, et al. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol. 2000;165:6037-6046.
57. Obermaier B, Dauer M, Herten J, et al. Development of a new protocol for 2-day generation of mature dendritic cells from human monocytes. Biol Proced Online. 2003;5:197-203.
58. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol. 2002;2:389-400.
59. Papiernik M, Banz A. Natural regulatory CD4 T cells expressing CD25. Microbes Infect. 2001;3: 937-945.
60. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol. 2002;23:144-150.
61. Maldonado-Lopez R, Moser M. Dendritic cell subsets and the regulation of Th1/Th2 responses. Semin Immunol. 2001;13:275-282.
62. Ritter U, Meissner A, Ott J, Korner H. Analysis of the maturation process of dendritic cells deficient for TNF and lymphotoxin-alpha reveals an essential role for TNF. J Leukoc Biol. 2003;74:216-222.
63. Abe K, Yarovinsky FO, Murakami T, et al. Distinct contributions of TNF and LT cytokines to the development of dendritic cells in vitro and their recruitment in vivo. Blood. 2003;101:1477-1483.
64. Elfenbein GJ, Sackstein R. Primed marrow for autologous and allogeneic transplantation: a review comparing primed marrow to mobilized blood and steady-state marrow. Exp Hematol. 2004;32:327-339.
65. Tabbara IA, Kairouz S, Nahleh Z, Mihalcea AM. Current concepts in allogeneic hematopoietic stem cell transplantation. Anticancer Res. 2003; 23:5055-5067.
66. Zeng D, Lan F, Hoffmann P, Strober S. Suppression of graft-versus-host disease by naturally occurring regulatory T cells. Transplantation. 2004; 77:S9-S11.
67. Slavin S. Graft-versus-host disease, the graft-versus-leukemia effect, and mixed chimerism following nonmyeloablative stem cell transplantation. Int J Hematol. 2003;78:195-207.
68. van den Brink MR, Burakoff SJ. Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol. 2002;2:273-281.
69. Bruner RJ, Farag SS. Monoclonal antibodies for the prevention and treatment of graft-versus-host disease. Semin Oncol. 2003;30:509-519.
70. Tsimberidou AM, Giles FJ. TNF-alpha targeted therapeutic approaches in patients with hematologic malignancies. Expert Rev Anticancer Ther. 2002;2:277-286.
71. Meisel R, Zibert A, Laryea M, et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004; 103:4619-4621.
72. Newberry RD, McDonough JS, Stenson WF, Lorenz RG. Spontaneous and continuous cyclo-oxygenase-2-dependent prostaglandin E2 production by stromal cells in the murine small intestine lamina propria: directing the tone of the intestinal immune response. J Immunol. 2001; 166:4465-4472.
73. Tilley SL, Coffman TM, Koller BH. Mixed messages: modulation of inflammation and immune responses by prostaglandins and thromboxanes. J Clin Invest. 2001;108:15-23.
74. Klyushnenkova E, Mosca JD, and McIntosh KR. Human mesenchymal stem cells suppress allogeneic T cell responses in vitro: implications for allogeneic transplantation [abstract]. Blood. 1998; 92(suppl 1, pt 1):642a.