Immunomodulatory effects of mesenchymal stromal cells in solid organ transplantation

Current Opinion in Organ Transplantation

Volumn 15, Issue 6, 2010, Pages 731-737

  Casiraghi, Federica ^a   Noris, Marina ^a   Remuzzi, Giuseppe ^a  

^a MARIO NEGRI INST PHARMACOL RES   (Italy)

Author keywords

immunomodulation; mesenchymal stromal cells; solid organ transplantation; T cells

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; PROSTAGLANDIN E2; SCATTER FACTOR;

CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL CONTACT; CELL PROLIFERATION; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; IN VITRO STUDY; INHIBITION KINETICS; MAJOR HISTOCOMPATIBILITY COMPLEX; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NONHUMAN; ORGAN TRANSPLANTATION; REVIEW; STROMA CELL; T LYMPHOCYTE;

ANIMALS; HUMANS; IMMUNOMODULATION; IMMUNOSUPPRESSIVE AGENTS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; ORGAN TRANSPLANTATION;

EID: 78649659727     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0b013e328340172c     Document Type: Review

References (97)

1. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968; 6:230-247.
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. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteriafordefining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8:315-317.
4. Campagnoli C, Roberts IA, Kumar S, et al. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001; 98:2396-2402.
5. De Ugarte DA, Morizono K, Elbarbary A, et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003; 174:101-109.
6. Hoogduijn MJ,Crop MJ, Peeters A M, et al. Human heart,spleen, and perirenal fat-derived mesenchymal stem cells have immunomodulatory capacities. Stem Cells Dev 2007; 16:597-604.
7. Arai F, Ohneda O, Miyamoto T, et al. Mesenchymal stem cells in perichon-drium express activated leukocyte cell adhesion molecule and participate in bone marrowformation. J Exp Med 2002; 195:1549-1563.
8. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000; 109:235-242.
9. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Isolation of mesenchymal stemcellsof fetal or maternal originfrom human placenta. Stem Cells 2004; 22:1338-1345
10. In't Anker P S,Scherjon SA, Kleijburg-van derKeur C, et al.Amnioticfluid asa novel source of mesenchymal stem cells for therapeutic transplantation. Blood 2003; 102:1548-1549.
11. Bieback K, Kern S, Kluter H, Eichler H. Critical parametersforthe isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 2004; 22:625-634.
12. Weiss LM, Anderson C, Medicetty S, et al. Immune properties of human umbilicalcord Wharton's jelly-derived cells. Stem Cells 2008;26:2865-2874.
13. Li CD, Zhang WY, Li HL, et al. Mesenchymal stem cells derived from human placenta suppress allogeneic umbilical cord blood lymphocyte proliferation. Cell Res 2005; 15:539-547.
14. Le Blanc K, Tammik C, Rosendahl K, et al. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003; 31:890-896.
15. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mito-genic stimuli. Blood 2002; 99:3838-3843.
16. Tse WT, Pendleton JD, Beyer WM, et al. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003; 75:389-397.
17. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284:143-147.
18. Glennie S, Soeiro I, Dyson PJ, et al. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005; 105:2821-2827.
19. Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106:1755-1761.
20. Batten P, Sarathchandra P, Antoniw JW, et al. Human mesenchymal stem cells induceTcell anergyand downregulateTcell allo-responsesviatheTH2 pathway: relevance to tissue engineering human heart valves. Tissue Eng 2006; 12:2263-2273.
21. Stagg J, Pommey S, Eliopoulos N, Galipeau J. Interferon-gamma-stimulated marrow stromal cells: a new type of non hematopoieticantigen-presenting cell. Blood 2006; 107:2570-2577.
22. Romieu-Mourez R, Francois M, Boivin MN, et al. Regulation of MHC class II expression and antigen processing in murine and human mesenchymal stromal cells by IFN-gamma, TGF-beta, and cell density. J Immunol 2007; 179:1549-1558.
23. Morandi F, Raffaghello L, Bianchi G, et al. Immunogenicity of human me-senchymal stem cells in HLA-class I-restricted T-cell responses against viral ortumor-associated antigens. Stem Cells 2008; 26:1275-1287.
24. Francois M, Romieu-Mourez R, Stock-Martineau S, et al. Mesenchymal stromal cells cross-present soluble exogenous antigens as part of their antigen-presenting cell properties. Blood 2009; 114:2632-2638.
25. Nauta AJ, Westerhuis G, Kruisselbrink A B, et al. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood 2006; 108:2114-2120.
26. Eliopoulos N, Stagg J, Lejeune L, et al. Allogeneic marrow stromal cells are immune rejected by MHC class I-and class II-mismatched recipient mice. Blood 2005; 106:4057-4065.
27. Zangi L, Margalit R, Reich-Zeliger S, et al. Direct imaging of immune rejection and memory induction by allogeneic mesenchymal stromal cells. Stem Cells 2009; 27:2865-2874.
28. 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.
29. Le Blanc K, Tammik L, Sundberg B, et al. 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.
30. Bartholomew A, Sturgeon C, Siatskas M, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002; 30:42-48.
31. Inoue S, Popp FC, Koehl GE, et al. Immunomodulatory effects of mesench-ymal stem cells in a rat organ transplant model. Transplantation 2006; 81:1589-1595.
32. Djouad F, Plence P, Bony C, et al. Immunosuppressive effect of mesenchymal stem cellsfavorstumorgrowth inallogeneic animals. Blood 2003; 102:3837-3844.
33. Augello A, Tasso R, Negrini SM, et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 2005; 35:1482-1490.
34. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allo-geneic immune cell responses. Blood 2005; 105:1815-1822.
35. Krampera M, Cosmi L, Angeli R, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006; 24:386-398.
36. 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.
37. Krampera M, Glennie S, Dyson J, et al. 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.
38. Karlsson H, Samarasinghe S, Ball LM, et al. Mesenchymal stem cells exert differential effects on alloantigen and virus-specific T-cell responses. Blood 2008; 112:532-541.
39. Liu XJ, Zhang JF, Sun B, et al. Reciprocal effect of mesenchymal stem cell on experimental autoimmune encephalomyelitis is mediated by transforming growth factor-beta and interleukin-6. Clin Exp Immunol 2009; 158:37-44.
40. Meisel R, Zibert A, Laryea M, et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryp-tophan degradation. Blood 2004; 103:4619-4621.
41. Sato K,Ozaki K, Oh I, et al. Nitric oxide playsacritical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 2007; 109:228-234.
42. Potian JA, Aviv H, Ponzio NM, et al. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol 2003; 171:3426-3434.
43. Beyth S, Borovsky Z, Mevorach D, et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005; 105:2214-2219.
44. Nasef A, Chapel A, Mazurier C, et al. Identification of IL-10 and TGF-beta transcripts involved in the inhibition of T-lymphocyte proliferation during cell contactwith human mesenchymal stem cells. Gene Exp 2007; 13:217-226.
45. Ren G, Zhang L, Zhao X, et al. Mesenchymal stem cell-mediated immuno-suppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008; 2:141-150.
46. Chabannes D, Hill M, Merieau E, et al. A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Blood 2007; 110:3691-3694.
47. Nasef A, Mathieu N, Chapel A, et al. Immunosuppressive effects of mesench-ymal stem cells: involvement of HLA-G. Transplantation 2007; 84:231-237.
48. Selmani Z, Naji A, Zidi I, et al. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Stem Cells 2008; 26:212-222.
49. Sioud M, Mobergslien A, Boudabous A, Floisand Y. Evidence forthe involve-ment of galectin-3 in mesenchymal stem cell suppression of allogeneic T-cell proliferation. Scand J Immunol 2010; 71:267-274.
50. Ren G, Su J, Zhang L, et al. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 2009; 27:1954-1962.
51. Maccario R, Podesta M, Moretta A, 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/suppres-sive phenotype. Haematologica 2005; 90:516-525.
52. English K, Ryan JM, Tobin L, et al. Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25(High) forkhead box P3+regulatoryTcells. Clin Exp Immunol 2009; 156:149-160.
53. Renner P, Eggenhofer E, Rosenauer A, et al. Mesenchymal stem cells require a sufficient, ongoing immune response to exert their immunosuppressive function. Transplant Proc 2009; 41:2607-2611.
54. Ryan JM, Barry F, Murphy JM, Mahon BP. Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 2007; 149:353-363.
55. English K, Barry FP, Field-Corbett CP, Mahon BP. IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett 2007; 110:91-100.
56. Sheng H, Wang Y, Jin Y, et al. A critical role of IFNgamma in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Res 2008; 18:846-857.
57. Oh I, Ozaki K, Sato K, et al. Interferon-gamma and NF-kappaB mediate nitric oxide production by mesenchymal stromal cells. Biochem Biophys Res Commun 2007; 355:956-962.
58. 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.
59. Suva D, Passweg J, Arnaudeau S, et al. In vitro activated human T lympho-cytes very efficiently attach to allogenic multipotent mesenchymal stromal cells and transmigrate underthem. J Cell Physiol 2008; 214:588-594.
60. Quaedackers ME, Baan CC, Weimar W, Hoogduijn MJ. Cell contact inter-action between adipose-derived stromal cells and allo-activated T lympho-cytes. Eur J Immunol 2009; 39:3436-3446.
61. Jiang XX, Zhang Y, Liu B, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005; 105:4120-4126.
62. Djouad F, Charbonnier LM, Bouffi C, et al. Mesenchymal stem cells inhibitthe differentiation of dendritic cells through an interleukin-6-dependent mechan-ism. Stem Cells 2007; 25:2025-2032.
63. Nauta AJ, Kruisselbrink AB, Lurvink E, et al. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 2006; 177:2080-2087.
64. Li YP, Paczesny S, Lauret E, et al. Human mesenchymal stem cells license adult CD34+ hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathway. J Immunol 2008; 180:1598-1608.
65. Zhang W, Ge W, Li C, et al. Effects of mesenchymal stem cells on differ-entiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 2004; 13:263-271.
66. Zhang B, Liu R, Shi D, et al. Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population. Blood 2009; 113:46-57.
67. Wang Q, Sun B, Wang D, et al. Murine bone marrow mesenchymal stem cells cause mature dendritic cells to promote T-cell tolerance. Scand J Immunol 2008; 68:607-615.
68. Corcione A, Benvenuto F, Ferretti E, et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006; 107:367-372.
69. Comoli P, Ginevri F, Maccario R, et al. Human mesenchymal stem cells inhibit antibody production induced in vitro by allostimulation. Nephrol Dial Trans-plant 2008; 23:1196-1202.
70. Tabera S, Perez-Simon JA, Diez-Campelo M, et al.The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica 2008; 93:1301-1309.
71. Rasmusson I, Le Blanc K, Sundberg B, Ringden O. Mesenchymal stem cells stimulate antibody secretion in human B cells. Scand J Immunol 2007; 65:336-343.
72. Traggiai E, Volpi S, Schena F, et al. Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients. Stem Cells 2008; 26:562-569.
73. Spaggiari GM, Capobianco A, Becchetti S, et al. 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.
74. Sotiropoulou PA, Perez SA, Gritzapis AD, et al. Interactions between human mesenchymal stem cellsand natural killercells. Stem Cells 2006; 24:74-85.
75. Spaggiari GM, Capobianco A, Abdelrazik H, et al. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008; 111:1327-1333.
76. Bischoff DS, Zhu JH, Makhijani NS, Yamaguchi DT. Acidic pH stimulates the production of the angiogenic CXC chemokine, CXCL8 (interleukin-8), in human adult mesenchymal stem cells via the extracellular signal-regulated kinase, p38 mitogen-activated protein kinase, and NF-kappaB pathways. J Cell Biochem 2008; 104:1378-1392.
77. Croitoru-Lamoury J, Lamoury FM, Zaunders JJ, et al. Human mesenchymal stem cells constitutively express chemokines and chemokine receptors that can be upregulated by cytokines, IFN-beta, and Copaxone. J Interferon Cytokine Res 2007; 27:53-64.
78. Popp FC, Eggenhofer E, Renner P, et al. Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate. Transpl Immunol 2008; 20:55-60.
79. Zhou HP, Yi DH, Yu SQ, et al. Administration of donor-derived mesenchymal stem cells can prolong the survival of rat cardiac allograft Transplant Proc 2006; 38:3046-3051.
80. Ge W, Jiang J, Baroja ML, et al. Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft tolerance. Am J Transplant 2009; 9:1760-1772.
81. Casiraghi F,Azzollini N, Cassis P, et al. Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. J Immunol 2008; 181:3933-3946.
82. Wang Y, Zhang A, Ye Z, et al. Bone marrow-derived mesenchymal stem cells inhibit acute rejection of rat liverallografts in association with regulatoryT-cell expansion. Transplant Proc 2009; 41:4352-4356.
83. Ding Y, Xu D, Feng G, et al. Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metal-loproteinase-2 and-9. Diabetes 2009; 58:1797-1806.
84. Buron F, Perrin H, Malcus C, et al. Human mesenchymal stem cells and immunosuppressive drug interactions in allogeneic responses: an in vitro study using human cells. Transplant Proc 2009; 41:3347-3352.
85. Le Blanc K, Rasmusson I, Gotherstrom C, et al. Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phyto-haemagglutinin-activated lymphocytes. Scand J Immunol 2004; 60:307-315.
86. Maccario R, Moretta A, Cometa A, et al. Human mesenchymal stem cells and cyclosporin A exert a synergistic suppressive effect on in vitro activation of alloantigen-specific cytotoxic lymphocytes. Biol Blood Marrow Transplant 2005; 11:1031-1032.
87. Hoogduijn MJ, Crop MJ, Korevaar SS, et al. Susceptibility of human mesenchymal stem cells to tacrolimus, mycophenolic acid, and rapamycin. Transplantation 2008; 86:1283-1291.
88. Zhang W, Qin C, Zhou ZM. Mesenchymal stem cells modulate immune responses combined with cyclosporine in a rat renal transplantation model. Transplant Proc 2007; 39:3404-3408.
89. Sbano P, Cuccia A, Mazzanti B, et al. Use of donor bone marrow mesench-ymal stem cells for treatment of skin allograft rejection in a preclinical rat model. Arch Dermatol Res 2008; 300:115-124.
90. Kuo YR, Goto S, Shih HS, et al. Mesenchymal stem cells prolong composite tissue allotransplant survival in a swine model. Transplantation 2009; 87:1769-1777.
91. 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.
92. Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008; 371:1579-1586.
93. Parekkadan B, Tilles AW, Yarmush ML Bone marrow-derived mesenchymal stem cells ameliorate autoimmune enteropathy independently of regulatory T cells. Stem Cells 2008; 26:1913-1919.
94. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesench-ymal stem cells-their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007; 25:2739-2749.
95. Gonzalez MA, Gonzalez-Rey E, Rico L, et al. Treatment of experimental arthritis by inducing immunetolerancewith human adipose-derived mesench-ymal stem cells. Arthritis Rheum 2009; 60:1006-1019.
96. Nemeth K, Keane-Myers A, Brown JM, et al. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of rag-weed-induced asthma. Proc Natl Acad Sci USA 2010; 107:5652-5657.
97. Dahlke MH, Hoogduijn M, Eggenhofer E, et al. Toward MSC in solid organ transplantation: 2008 position paper of the MISOT study group. Transplantation 2009; 88:614-619.