Skip to main content
Top
Published in: Arthritis Research & Therapy 1/2007

01-02-2007 | Meeting report

Immunomodulatory properties of mesenchymal stem cells: a review based on an interdisciplinary meeting held at the Kennedy Institute of Rheumatology Division, London, UK, 31 October 2005

Authors: Alan Tyndall, Ulrich A Walker, Andrew Cope, Francesco Dazzi, Cosimo De Bari, Willem Fibbe, Serena Guiducci, Simon Jones, Christian Jorgensen, Katarina Le Blanc, Frank Luyten, Dennis McGonagle, Ivan Martin, Chiara Bocelli-Tyndall, Giuseppina Pennesi, Vito Pistoia, Constantino Pitzalis, Antonio Uccelli, Nico Wulffraat, Marc Feldmann

Published in: Arthritis Research & Therapy | Issue 1/2007

Login to get access

Abstract

Multipotent mesenchymal stromal cells isolated from bone marrow and other sites are currently being studied to determine their potential role in the pathogenesis and/or management of autoimmune diseases. In vitro studies have shown that they exhibit a dose-dependent antiproliferative effect on T and B lymphocytes, dendritic cells, natural killer cells and various B cell tumour lines – an effect that is both cell contact and soluble factor dependent. Animal models of autoimmune disease treated with multipotent mesenchymal stromal cells have mostly exhibited a positive clinical response, as have a limited number of patients suffering from acute graft versus host disease. This review summarizes the findings of a 1-day meeting devoted to the subject with the aim of coordinating efforts.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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. 2004, 363: 1439-1441. 10.1016/S0140-6736(04)16104-7.CrossRefPubMed 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. 2004, 363: 1439-1441. 10.1016/S0140-6736(04)16104-7.CrossRefPubMed
2.
go back to reference Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F: Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 2005, 105: 2821-2827. 10.1182/blood-2004-09-3696.CrossRefPubMed Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F: Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 2005, 105: 2821-2827. 10.1182/blood-2004-09-3696.CrossRefPubMed
3.
go back to reference Ohata J, Zvaifler NJ, Nishio M, Boyle DL, Kalled SL, Carson DA, Kipps TJ: Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. J Immunol. 2005, 174: 864-870.CrossRefPubMed Ohata J, Zvaifler NJ, Nishio M, Boyle DL, Kalled SL, Carson DA, Kipps TJ: Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. J Immunol. 2005, 174: 864-870.CrossRefPubMed
4.
go back to reference Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, Noel D, Jorgensen C: Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003, 102: 3837-3844. 10.1182/blood-2003-04-1193.CrossRefPubMed Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, Noel D, Jorgensen C: Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003, 102: 3837-3844. 10.1182/blood-2003-04-1193.CrossRefPubMed
5.
go back to reference Nauta AJ, Westerhuis G, Kruisselbrink AB, Lurvink EG, Willemze R, Fibbe WE: Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a non-myeloablative setting. Blood. 2006, 108: 2114-2120. 10.1182/blood-2005-11-011650.PubMedCentralCrossRefPubMed Nauta AJ, Westerhuis G, Kruisselbrink AB, Lurvink EG, Willemze R, Fibbe WE: Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a non-myeloablative setting. Blood. 2006, 108: 2114-2120. 10.1182/blood-2005-11-011650.PubMedCentralCrossRefPubMed
6.
go back to reference Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A, the International Society for Cellular Therapy: Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy. 2005, 7: 393-395. 10.1080/14653240500319234.CrossRefPubMed Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A, the International Society for Cellular Therapy: Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy. 2005, 7: 393-395. 10.1080/14653240500319234.CrossRefPubMed
7.
go back to reference De Bari C, Dell'Accio F, Vanlauwe J, Eyckmans J, Khan IM, Archer CW, Jones EA, McGonagle D, Mitsiadis TA, Pitzalis C, et al: Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum. 2006, 54: 1209-1221. 10.1002/art.21753.CrossRefPubMed De Bari C, Dell'Accio F, Vanlauwe J, Eyckmans J, Khan IM, Archer CW, Jones EA, McGonagle D, Mitsiadis TA, Pitzalis C, et al: Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum. 2006, 54: 1209-1221. 10.1002/art.21753.CrossRefPubMed
8.
go back to reference Barry F, Boynton R, Murphy M, Haynesworth S, Zaia J: The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun. 2001, 289: 519-524. 10.1006/bbrc.2001.6013.CrossRefPubMed Barry F, Boynton R, Murphy M, Haynesworth S, Zaia J: The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun. 2001, 289: 519-524. 10.1006/bbrc.2001.6013.CrossRefPubMed
9.
go back to reference Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA: Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol. 1974, 2: 83-92.PubMed Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA: Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol. 1974, 2: 83-92.PubMed
10.
go back to reference Nakahara H, Dennis JE, Bruder SP, Haynesworth SE, Lennon DP, Caplan AI: In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp Cell Res. 1991, 195: 492-503. 10.1016/0014-4827(91)90401-F.CrossRefPubMed Nakahara H, Dennis JE, Bruder SP, Haynesworth SE, Lennon DP, Caplan AI: In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp Cell Res. 1991, 195: 492-503. 10.1016/0014-4827(91)90401-F.CrossRefPubMed
11.
go back to reference Sampath TK, Nathanson MA, Reddi AH: In vitro transformation of mesenchymal cells derived from embryonic muscle into cartilage in response to extracellular matrix components of bone. Proc Natl Acad Sci USA. 1984, 81: 3419-3423. 10.1073/pnas.81.11.3419.PubMedCentralCrossRefPubMed Sampath TK, Nathanson MA, Reddi AH: In vitro transformation of mesenchymal cells derived from embryonic muscle into cartilage in response to extracellular matrix components of bone. Proc Natl Acad Sci USA. 1984, 81: 3419-3423. 10.1073/pnas.81.11.3419.PubMedCentralCrossRefPubMed
12.
go back to reference Nathanson MA: Bone matrix-directed chondrogenesis of muscle in vitro. Clin Orthop Relat Res. 1985, 200: 142-158.PubMed Nathanson MA: Bone matrix-directed chondrogenesis of muscle in vitro. Clin Orthop Relat Res. 1985, 200: 142-158.PubMed
13.
go back to reference De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP: Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001, 44: 1928-1942. 10.1002/1529-0131(200108)44:8<1928::AID-ART331>3.0.CO;2-P.CrossRefPubMed De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP: Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001, 44: 1928-1942. 10.1002/1529-0131(200108)44:8<1928::AID-ART331>3.0.CO;2-P.CrossRefPubMed
14.
go back to reference Jones EA, English A, Henshaw K, Kinsey SE, Markham AF, Emery P, McGonagle D: Enumeration and phenotypic characterization of synovial fluid multipotential mesenchymal progenitor cells in inflammatory and degenerative arthritis. Arthritis Rheum. 2004, 50: 817-827. 10.1002/art.20203.CrossRefPubMed Jones EA, English A, Henshaw K, Kinsey SE, Markham AF, Emery P, McGonagle D: Enumeration and phenotypic characterization of synovial fluid multipotential mesenchymal progenitor cells in inflammatory and degenerative arthritis. Arthritis Rheum. 2004, 50: 817-827. 10.1002/art.20203.CrossRefPubMed
15.
go back to reference Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM: Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 2001, 98: 2396-2402. 10.1182/blood.V98.8.2396.CrossRefPubMed Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM: Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 2001, 98: 2396-2402. 10.1182/blood.V98.8.2396.CrossRefPubMed
16.
go back to reference Erices A, Conget P, Minguell JJ: Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol. 2000, 109: 235-242. 10.1046/j.1365-2141.2000.01986.x.CrossRefPubMed Erices A, Conget P, Minguell JJ: Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol. 2000, 109: 235-242. 10.1046/j.1365-2141.2000.01986.x.CrossRefPubMed
17.
go back to reference Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC, Jung JS: Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem. 2004, 14: 311-324. 10.1159/000080341.CrossRefPubMed Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC, Jung JS: Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem. 2004, 14: 311-324. 10.1159/000080341.CrossRefPubMed
18.
go back to reference Djouad F, Bony C, Haupl T, Uze G, Lahlou N, Louis-Plence P, Apparailly F, Canovas F, Reme T, Sany J, et al: Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res Ther. 2005, 7: R1304-R1315. 10.1186/ar1827.PubMedCentralCrossRefPubMed Djouad F, Bony C, Haupl T, Uze G, Lahlou N, Louis-Plence P, Apparailly F, Canovas F, Reme T, Sany J, et al: Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res Ther. 2005, 7: R1304-R1315. 10.1186/ar1827.PubMedCentralCrossRefPubMed
19.
go back to reference Gotherstrom C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K: Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica. 2005, 90: 1017-1026.PubMed Gotherstrom C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K: Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica. 2005, 90: 1017-1026.PubMed
20.
go back to reference Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O: Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol. 2003, 57: 11-20. 10.1046/j.1365-3083.2003.01176.x.CrossRefPubMed Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O: Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol. 2003, 57: 11-20. 10.1046/j.1365-3083.2003.01176.x.CrossRefPubMed
21.
go back to reference Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, et al: Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002, 30: 42-48. 10.1016/S0301-472X(01)00769-X.CrossRefPubMed Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, et al: Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002, 30: 42-48. 10.1016/S0301-472X(01)00769-X.CrossRefPubMed
22.
go back to reference Maitra B, Szekely E, Gjini K, Laughlin MJ, Dennis J, Haynesworth SE, Koc ON: Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant. 2004, 33: 597-604. 10.1038/sj.bmt.1704400.CrossRefPubMed Maitra B, Szekely E, Gjini K, Laughlin MJ, Dennis J, Haynesworth SE, Koc ON: Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant. 2004, 33: 597-604. 10.1038/sj.bmt.1704400.CrossRefPubMed
23.
go back to reference Maccario R, Podesta M, Moretta A, Cometa A, Comoli P, Montagna D, Daudt L, Ibatici A, Piaggio G, Pozzi S, et al: Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica. 2005, 90: 516-525.PubMed Maccario R, Podesta M, Moretta A, Cometa A, Comoli P, Montagna D, Daudt L, Ibatici A, Piaggio G, Pozzi S, et al: Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica. 2005, 90: 516-525.PubMed
24.
go back to reference 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. 2003, 101: 3722-3729. 10.1182/blood-2002-07-2104.CrossRefPubMed 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. 2003, 101: 3722-3729. 10.1182/blood-2002-07-2104.CrossRefPubMed
25.
go back to reference Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, Risso M, Gualandi F, Mancardi GL, Pistoia V, et al: Human mesenchymal stem cells modulate B cell functions. Blood. 2006, 107: 367-372. 10.1182/blood-2005-07-2657.CrossRefPubMed Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, Risso M, Gualandi F, Mancardi GL, Pistoia V, et al: Human mesenchymal stem cells modulate B cell functions. Blood. 2006, 107: 367-372. 10.1182/blood-2005-07-2657.CrossRefPubMed
26.
go back to reference Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE: Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol. 2006, 177: 2080-2087.CrossRefPubMed Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE: Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol. 2006, 177: 2080-2087.CrossRefPubMed
27.
go back to reference Ramaswamy R, Fazekasoz H, Lam EW, Soeiro I, Lombardi G, Dazzi F: Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation. 2007, 83: 71-76. 10.1097/01.tp.0000244572.24780.54.CrossRef Ramaswamy R, Fazekasoz H, Lam EW, Soeiro I, Lombardi G, Dazzi F: Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation. 2007, 83: 71-76. 10.1097/01.tp.0000244572.24780.54.CrossRef
28.
go back to reference Aggarwal S, Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005, 105: 1815-1822. 10.1182/blood-2004-04-1559.CrossRefPubMed Aggarwal S, Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005, 105: 1815-1822. 10.1182/blood-2004-04-1559.CrossRefPubMed
29.
go back to reference 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. 2003, 76: 1208-1213. 10.1097/01.TP.0000082540.43730.80.CrossRefPubMed 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. 2003, 76: 1208-1213. 10.1097/01.TP.0000082540.43730.80.CrossRefPubMed
30.
go back to reference Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L: 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. 2006, 107: 1484-1490. 10.1182/blood-2005-07-2775.CrossRefPubMed Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L: 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. 2006, 107: 1484-1490. 10.1182/blood-2005-07-2775.CrossRefPubMed
31.
go back to reference Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M: Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells. 2006, 24: 74-85. 10.1634/stemcells.2004-0359.CrossRefPubMed Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M: Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells. 2006, 24: 74-85. 10.1634/stemcells.2004-0359.CrossRefPubMed
32.
go back to reference Poggi A, Prevosto C, Massaro AM, Negrini S, Urbani S, Pierri I, Saccardi R, Gobbi M, Zocchi MR: Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: role of NKp30 and NKG2D receptors. J Immunol. 2005, 175: 6352-6360.CrossRefPubMed Poggi A, Prevosto C, Massaro AM, Negrini S, Urbani S, Pierri I, Saccardi R, Gobbi M, Zocchi MR: Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: role of NKp30 and NKG2D receptors. J Immunol. 2005, 175: 6352-6360.CrossRefPubMed
33.
go back to reference Rasmusson I, Ringden O, Sundberg B, Le Blanc K: Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res. 2005, 305: 33-41. 10.1016/j.yexcr.2004.12.013.CrossRefPubMed Rasmusson I, Ringden O, Sundberg B, Le Blanc K: Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res. 2005, 305: 33-41. 10.1016/j.yexcr.2004.12.013.CrossRefPubMed
34.
go back to reference Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM: Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002, 99: 3838-3843. 10.1182/blood.V99.10.3838.CrossRefPubMed Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM: Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002, 99: 3838-3843. 10.1182/blood.V99.10.3838.CrossRefPubMed
35.
go back to reference 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. 2004, 60: 307-315. 10.1111/j.0300-9475.2004.01483.x.CrossRefPubMed 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. 2004, 60: 307-315. 10.1111/j.0300-9475.2004.01483.x.CrossRefPubMed
36.
go back to reference Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, Keskin DB, Marshall B, Chandler P, Antonia SJ, Burgess R, et al: Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science. 2002, 297: 1867-1870. 10.1126/science.1073514.CrossRefPubMed Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, Keskin DB, Marshall B, Chandler P, Antonia SJ, Burgess R, et al: Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science. 2002, 297: 1867-1870. 10.1126/science.1073514.CrossRefPubMed
37.
go back to reference Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D: Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004, 103: 4619-4621. 10.1182/blood-2003-11-3909.CrossRefPubMed Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D: Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004, 103: 4619-4621. 10.1182/blood-2003-11-3909.CrossRefPubMed
38.
go back to reference 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. 10.1097/01.TP.0000045055.63901.A9.CrossRefPubMed 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. 10.1097/01.TP.0000045055.63901.A9.CrossRefPubMed
39.
go back to reference Belladonna ML, Grohmann U, Guidetti P, Volpi C, Bianchi R, Fioretti MC, Schwarcz R, Fallarino F, Puccetti P: Kynurenine pathway enzymes in dendritic cells initiate tolerogenesis in the absence of functional IDO. J Immunol. 2006, 177: 130-137.CrossRefPubMed Belladonna ML, Grohmann U, Guidetti P, Volpi C, Bianchi R, Fioretti MC, Schwarcz R, Fallarino F, Puccetti P: Kynurenine pathway enzymes in dendritic cells initiate tolerogenesis in the absence of functional IDO. J Immunol. 2006, 177: 130-137.CrossRefPubMed
40.
go back to reference Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB: Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med. 2002, 196: 459-468. 10.1084/jem.20020121.PubMedCentralCrossRefPubMed Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB: Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med. 2002, 196: 459-468. 10.1084/jem.20020121.PubMedCentralCrossRefPubMed
41.
go back to reference 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. 10.1016/S0301-472X(03)00110-3.CrossRefPubMed 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. 10.1016/S0301-472X(03)00110-3.CrossRefPubMed
42.
go back to reference Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, Deans RJ, McIntosh KR: T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci. 2005, 12: 47-57. 10.1007/s11373-004-8183-7.CrossRefPubMed Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, Deans RJ, McIntosh KR: T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci. 2005, 12: 47-57. 10.1007/s11373-004-8183-7.CrossRefPubMed
43.
go back to reference Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, Marshak DR, Flake AW: Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med. 2000, 6: 1282-1286. 10.1038/81395.CrossRefPubMed Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, Marshak DR, Flake AW: Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med. 2000, 6: 1282-1286. 10.1038/81395.CrossRefPubMed
44.
go back to reference Bocelli-Tyndall C, Bracci L, Spagnoli G, Braccini A, Bouchenaki M, Ceredig R, Pistoia V, Martin I, Tyndall A: Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and autoimmune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro. Rheumatology (Oxford). 2006. Bocelli-Tyndall C, Bracci L, Spagnoli G, Braccini A, Bouchenaki M, Ceredig R, Pistoia V, Martin I, Tyndall A: Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and autoimmune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro. Rheumatology (Oxford). 2006.
45.
go back to reference Eyckmans J, Luyten FP: Species specificity of ectopic bone formation using periosteum-derived mesenchymal progenitor cells. Tissue Eng. 2006, 12: 2203-2213. 10.1089/ten.2006.12.2203.CrossRefPubMed Eyckmans J, Luyten FP: Species specificity of ectopic bone formation using periosteum-derived mesenchymal progenitor cells. Tissue Eng. 2006, 12: 2203-2213. 10.1089/ten.2006.12.2203.CrossRefPubMed
46.
go back to reference Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, Markham AF, Jack A, Emery P, McGonagle D: Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002, 46: 3349-3360. 10.1002/art.10696.CrossRefPubMed Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, Markham AF, Jack A, Emery P, McGonagle D: Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002, 46: 3349-3360. 10.1002/art.10696.CrossRefPubMed
47.
go back to reference Braccini A, Wendt D, Jaquiery C, Jakob M, Heberer M, Kenins L, Wodnar-Filipowicz A, Quarto R, Martin I: Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells. 2005, 23: 1066-1072. 10.1634/stemcells.2005-0002.CrossRefPubMed Braccini A, Wendt D, Jaquiery C, Jakob M, Heberer M, Kenins L, Wodnar-Filipowicz A, Quarto R, Martin I: Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells. 2005, 23: 1066-1072. 10.1634/stemcells.2005-0002.CrossRefPubMed
48.
go back to reference Bocelli-Tyndall C, Barbero A, Candrian C, Ceredig R, Tyndall A, Martin I: Human articular chondrocytes suppress in vitro proliferation of anti-CD3 activated peripheral blood mononuclear cells. J Cell Physiol. 2006, 209: 732-734. 10.1002/jcp.20789.CrossRefPubMed Bocelli-Tyndall C, Barbero A, Candrian C, Ceredig R, Tyndall A, Martin I: Human articular chondrocytes suppress in vitro proliferation of anti-CD3 activated peripheral blood mononuclear cells. J Cell Physiol. 2006, 209: 732-734. 10.1002/jcp.20789.CrossRefPubMed
49.
go back to reference Murphy JM, Fink DJ, Hunziker EB, Barry FP: Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 2003, 48: 3464-3474. 10.1002/art.11365.CrossRefPubMed Murphy JM, Fink DJ, Hunziker EB, Barry FP: Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 2003, 48: 3464-3474. 10.1002/art.11365.CrossRefPubMed
50.
go back to reference Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, McCarville ME, Orchard PJ, Pyeritz RE, Brenner MK: Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood. 2001, 97: 1227-1231. 10.1182/blood.V97.5.1227.CrossRefPubMed Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, McCarville ME, Orchard PJ, Pyeritz RE, Brenner MK: Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood. 2001, 97: 1227-1231. 10.1182/blood.V97.5.1227.CrossRefPubMed
51.
go back to reference Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, et al: Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999, 5: 309-313. 10.1038/6529.CrossRefPubMed Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, et al: Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999, 5: 309-313. 10.1038/6529.CrossRefPubMed
52.
go back to reference Le Blanc K, Gotherstrom C, Ringden O, Hassan M, McMahon R, Horwitz E, Anneren G, Axelsson O, Nunn J, Ewald U, et al: Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation. 2005, 79: 1607-1614. 10.1097/01.TP.0000159029.48678.93.CrossRefPubMed Le Blanc K, Gotherstrom C, Ringden O, Hassan M, McMahon R, Horwitz E, Anneren G, Axelsson O, Nunn J, Ewald U, et al: Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation. 2005, 79: 1607-1614. 10.1097/01.TP.0000159029.48678.93.CrossRefPubMed
53.
go back to reference De Bari C, Dell'Accio F, Vandenabeele F, Vermeesch JR, Raymackers JM, Luyten FP: Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol. 2003, 160: 909-918. 10.1083/jcb.200212064.PubMedCentralCrossRefPubMed De Bari C, Dell'Accio F, Vandenabeele F, Vermeesch JR, Raymackers JM, Luyten FP: Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol. 2003, 160: 909-918. 10.1083/jcb.200212064.PubMedCentralCrossRefPubMed
54.
go back to reference Devine SM, Bartholomew AM, Mahmud N, Nelson M, Patil S, Hardy W, Sturgeon C, Hewett T, Chung T, Stock W, et al: Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol. 2001, 29: 244-255. 10.1016/S0301-472X(00)00635-4.CrossRefPubMed Devine SM, Bartholomew AM, Mahmud N, Nelson M, Patil S, Hardy W, Sturgeon C, Hewett T, Chung T, Stock W, et al: Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol. 2001, 29: 244-255. 10.1016/S0301-472X(00)00635-4.CrossRefPubMed
55.
go back to reference Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J: Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood. 2005, 106: 4057-4065. 10.1182/blood-2005-03-1004.CrossRefPubMed Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J: Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood. 2005, 106: 4057-4065. 10.1182/blood-2005-03-1004.CrossRefPubMed
56.
go back to reference Sudres M, Norol F, Trenado A, Gregoire S, Charlotte F, Levacher B, Lataillade JJ, Bourin P, Holy X, Vernant JP, et al: Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol. 2006, 176: 7761-7767.CrossRefPubMed Sudres M, Norol F, Trenado A, Gregoire S, Charlotte F, Levacher B, Lataillade JJ, Bourin P, Holy X, Vernant JP, et al: Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol. 2006, 176: 7761-7767.CrossRefPubMed
57.
go back to reference Ringden O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lonnies H, Marschall HU, Dlugosz A, Szakos A, Hassan Z, et al: Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006, 81: 1390-1397. 10.1097/01.tp.0000214462.63943.14.CrossRefPubMed Ringden O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lonnies H, Marschall HU, Dlugosz A, Szakos A, Hassan Z, et al: Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006, 81: 1390-1397. 10.1097/01.tp.0000214462.63943.14.CrossRefPubMed
58.
go back to reference Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, et al: Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005, 106: 1755-1761. 10.1182/blood-2005-04-1496.CrossRefPubMed Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, et al: Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005, 106: 1755-1761. 10.1182/blood-2005-04-1496.CrossRefPubMed
59.
go back to reference Djouad F, Fritz V, Apparailly F, Louis-Plence P, Bony C, Sany J, Jorgensen C, Noel D: Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum. 2005, 52: 1595-1603. 10.1002/art.21012.CrossRefPubMed Djouad F, Fritz V, Apparailly F, Louis-Plence P, Bony C, Sany J, Jorgensen C, Noel D: Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum. 2005, 52: 1595-1603. 10.1002/art.21012.CrossRefPubMed
60.
go back to reference Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG: Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA. 2003, 100: 8407-8411. 10.1073/pnas.1432929100.PubMedCentralCrossRefPubMed Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG: Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA. 2003, 100: 8407-8411. 10.1073/pnas.1432929100.PubMedCentralCrossRefPubMed
61.
go back to reference Horwitz EM: Dkk-1-mediated expansion of adult stem cells. Trends Biotechnol. 2004, 22: 386-388. 10.1016/j.tibtech.2004.05.006.CrossRefPubMed Horwitz EM: Dkk-1-mediated expansion of adult stem cells. Trends Biotechnol. 2004, 22: 386-388. 10.1016/j.tibtech.2004.05.006.CrossRefPubMed
62.
go back to reference Doucet C, Ernou I, Zhang Y, Llense JR, Begot L, Holy X, Lataillade JJ: Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J Cell Physiol. 2005, 205: 228-236. 10.1002/jcp.20391.CrossRefPubMed Doucet C, Ernou I, Zhang Y, Llense JR, Begot L, Holy X, Lataillade JJ: Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J Cell Physiol. 2005, 205: 228-236. 10.1002/jcp.20391.CrossRefPubMed
63.
go back to reference 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.PubMed 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.PubMed
64.
go back to reference Del Papa N, Quirici N, Soligo D, Scavullo C, Cortiana M, Borsotti C, Maglione W, Comina DP, Vitali C, Fraticelli P, et al: Bone marrow endothelial progenitors are defective in systemic sclerosis. Arthritis Rheum. 2006, 54: 2605-2615. 10.1002/art.22035.CrossRefPubMed Del Papa N, Quirici N, Soligo D, Scavullo C, Cortiana M, Borsotti C, Maglione W, Comina DP, Vitali C, Fraticelli P, et al: Bone marrow endothelial progenitors are defective in systemic sclerosis. Arthritis Rheum. 2006, 54: 2605-2615. 10.1002/art.22035.CrossRefPubMed
65.
go back to reference Kern S, Eichler H, Stoeve J, Kluter H, Bieback K: Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006, 24: 1294-1301. 10.1634/stemcells.2005-0342.CrossRefPubMed Kern S, Eichler H, Stoeve J, Kluter H, Bieback K: Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006, 24: 1294-1301. 10.1634/stemcells.2005-0342.CrossRefPubMed
66.
go back to reference Griffith LM, Pavletic SZ, Tyndall A, Bredeson CN, Bowen JD, Childs RW, Gratwohl A, van Laar JM, Mayes MD, Martin R, et al: Feasibility of allogeneic hematopoietic stem cell transplantation for autoimmune disease: position statement from a National Institute of Allergy and Infectious Diseases and National Cancer Institute-Sponsored International Workshop, Bethesda, MD, March 12 and 13, 2005. Biol Blood Marrow Transplant. 2005, 11: 862-870. 10.1016/j.bbmt.2005.07.009.CrossRefPubMed Griffith LM, Pavletic SZ, Tyndall A, Bredeson CN, Bowen JD, Childs RW, Gratwohl A, van Laar JM, Mayes MD, Martin R, et al: Feasibility of allogeneic hematopoietic stem cell transplantation for autoimmune disease: position statement from a National Institute of Allergy and Infectious Diseases and National Cancer Institute-Sponsored International Workshop, Bethesda, MD, March 12 and 13, 2005. Biol Blood Marrow Transplant. 2005, 11: 862-870. 10.1016/j.bbmt.2005.07.009.CrossRefPubMed
67.
go back to reference Xu W, Zhang X, Qian H, Zhu W, Sun X, Hu J, Zhou H, Chen Y: Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med (Maywood). 2004, 229: 623-631. Xu W, Zhang X, Qian H, Zhu W, Sun X, Hu J, Zhou H, Chen Y: Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med (Maywood). 2004, 229: 623-631.
68.
go back to reference Vogel W, Grunebach F, Messam CA, Kanz L, Brugger W, Buhring HJ: Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica. 2003, 88: 126-133.PubMed Vogel W, Grunebach F, Messam CA, Kanz L, Brugger W, Buhring HJ: Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica. 2003, 88: 126-133.PubMed
69.
go back to reference Reyes M, Verfaillie CM: Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann N Y Acad Sci. 2001, 938: 231-233. discussion 233–235CrossRefPubMed Reyes M, Verfaillie CM: Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann N Y Acad Sci. 2001, 938: 231-233. discussion 233–235CrossRefPubMed
70.
go back to reference Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR, Mosca JD: Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci. 2003, 10: 228-241. 10.1007/BF02256058.CrossRefPubMed Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR, Mosca JD: Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci. 2003, 10: 228-241. 10.1007/BF02256058.CrossRefPubMed
71.
go back to reference Deans RJ, Moseley AB: Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol. 2000, 28: 875-884. 10.1016/S0301-472X(00)00482-3.CrossRefPubMed Deans RJ, Moseley AB: Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol. 2000, 28: 875-884. 10.1016/S0301-472X(00)00482-3.CrossRefPubMed
72.
go back to reference Bruder SP, Ricalton NS, Boynton RE, Connolly TJ, Jaiswal N, Zaia J, Barry FP: Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res. 1998, 13: 655-663. 10.1359/jbmr.1998.13.4.655.CrossRefPubMed Bruder SP, Ricalton NS, Boynton RE, Connolly TJ, Jaiswal N, Zaia J, Barry FP: Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res. 1998, 13: 655-663. 10.1359/jbmr.1998.13.4.655.CrossRefPubMed
73.
go back to reference Gronthos S, Graves SE, Ohta S, Simmons PJ: The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood. 1994, 84: 4164-4173.PubMed Gronthos S, Graves SE, Ohta S, Simmons PJ: The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood. 1994, 84: 4164-4173.PubMed
74.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
75.
go back to reference Plumas J, Chaperot L, Richard MJ, Molens JP, Bensa JC, Favrot MC: Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia. 2005, 19: 1597-1604. 10.1038/sj.leu.2403871.CrossRefPubMed Plumas J, Chaperot L, Richard MJ, Molens JP, Bensa JC, Favrot MC: Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia. 2005, 19: 1597-1604. 10.1038/sj.leu.2403871.CrossRefPubMed
76.
go back to reference Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K: Nitric oxide plays a critical role in suppression of T cell proliferation by mesenchymal stem cells. Blood. 2006, 109: 228-234.CrossRefPubMed Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K: Nitric oxide plays a critical role in suppression of T cell proliferation by mesenchymal stem cells. Blood. 2006, 109: 228-234.CrossRefPubMed
Metadata
Title
Immunomodulatory properties of mesenchymal stem cells: a review based on an interdisciplinary meeting held at the Kennedy Institute of Rheumatology Division, London, UK, 31 October 2005
Authors
Alan Tyndall
Ulrich A Walker
Andrew Cope
Francesco Dazzi
Cosimo De Bari
Willem Fibbe
Serena Guiducci
Simon Jones
Christian Jorgensen
Katarina Le Blanc
Frank Luyten
Dennis McGonagle
Ivan Martin
Chiara Bocelli-Tyndall
Giuseppina Pennesi
Vito Pistoia
Constantino Pitzalis
Antonio Uccelli
Nico Wulffraat
Marc Feldmann
Publication date
01-02-2007
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2007
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar2103

Other articles of this Issue 1/2007

Arthritis Research & Therapy 1/2007 Go to the issue