Adipose tissue-derived multipotent stromal cells have a higher immunomodulatory capacity than their bone marrow-derived counterparts

Stem Cells Translational Medicine

Volumn 2, Issue 6, 2013, Pages 455-463

  Melief, Sara M ^a   Zwaginga, Jaap Jan ^a,b   Fibbe, Willem E ^a   Roelofs, Helene ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Center for Clinical Transfusion Reseach Sanquin LUMC   (Netherlands)

Author keywords

Adult human bone marrow; Bone marrow; Bone marrow stromal cells; Cellular therapy; Immunosuppression; Marrow stromal stem cells; Mesenchymal stem cells

Indexed keywords

3 (4, 5 DIMETHYL 2 THIAZOLYL) 2, 5 DIPHENYLTETRAZOLIUM BROMIDE; ALKALINE PHOSPHATASE; CD45 ANTIGEN; CYTOKINE; INDOLEAMINE 2, 3 DIOXYGENASE; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ADULT; ARTICLE; BONE MARROW; CELL ASSAY; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL THERAPY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DONOR; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOMODULATION; IMMUNOPHENOTYPING; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; MESENCHYMAL STEM CELL; MONOCYTE; MULTIPOTENT STEM CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA CELL;

EID: 84878753775     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2012-0184     Document Type: Article

References (54)

1. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells: The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
2. 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.
3. Marigo I, Dazzi F. The immunomodulatory properties of mesenchymal stem cells. Semin Immunopathol 2011;33:593-602.
4. 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.
5. Djouad F, Charbonnier LM, Bouffi C et al. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Stem Cells 2007;25: 2025-2032.
6. Corcione A, Benvenuto F, Ferretti E et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006;107:367-372.
7. Sotiropoulou PA, Perez SA, Gritzapis AD et al. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006;24:74-85.
8. 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/ suppressive phenotype. Haematologica 2005; 90:516-525.
9. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
10. Crop M, Baan CC, Korevaar SS et al. Human adipose tissue-derived mesenchymal stem cells induce explosive T-cell proliferation. Stem Cells Dev 2010;19:1843-1853.
11. 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+ regulatory T cells. Clin Exp Immunol 2009;156:149-160.
12. Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L. MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: Central role of MSC-derived prostaglandin E2. Blood 2009;113:6576-6583.
13. Meisel R, Zibert A, Laryea M et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxyge-nase-mediated tryptophan degradation. Blood 2004;103:4619-4621.
14. Fu S, Zhang N, Yopp AC et al. TGF-beta Induces Foxp3 + T-regulatory cells from CD4+CD25- precursors. Am J Transplant 2004; 4:1614-1627.
15. Bartholomew A, Sturgeon C, Siatskas M et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Experimental Hematology 2002;30:42-48.
16. Yanez R, Lamana ML, Garcia-Castro J et al. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-ver-sus-host disease. Stem Cells 2006;24:2582-2591.
17. Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005;106:1755-1761.
18. Ball LM, Bernardo ME, Roelofs H et al. Cotransplantation of ex vivo expanded mesen-chymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem-cell transplantation. Blood 2007;110:2764-2767.
19. Le Blanc K, Frassoni F, Ball L et al. Mesenchy-mal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 2008;371:1579-1586.
20. Ciccocioppo R, Bernardo ME, Sgarella A et al. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011;60:788-798.
21. Ra JC, Shin IS, Kim SH et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev 2011;20:1297-1308.
22. Fang B, Song Y, Liao L et al. Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant Proc 2007;39:3358-3362.
23. Bernardo ME, Locatelli F, Fibbe WE. Mes-enchymal stromal cells. Ann NY Acad Sci 2009; 1176:101-117.
24. Strioga M, Viswanathan S, Darinskas A et al. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev 2012;21:2724-2752.
25. Hass R, Kasper C, Bohm S, Jacobs R. Different populations and sources of human mes-enchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011;9:12.
26. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007;100:1249-1260.
27. Izadpanah R, Trygg C, Patel B et al. Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 2006;99:1285-1297.
28. Lee RH, Kim B, Choi I et al. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 2004 2004; 14:311-324.
29. Kern S, Eichler H, Stoeve J et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006;24:1294-1301.
30. Najar M, Raicevic G, Boufker HI et al. Mesenchymal stromal cells use PGE2 to modulate activation and proliferation of lymphocyte subsets: Combined comparisonofadipose tissue, Wharton's jelly and bone marrow sources. Cell Immunol 2010;264:171-179.
31. Wagner W, Wein F, Seckinger A et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005;33:1402-1416.
32. Puissant B, Barreau C, Bourin P et al. Im-munomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005;129:118-129.
33. Torensma R, Prins HJ, Schrama E et al. The impact of cell source, culture methodology, culture location and individual donors on gene expression profiles of bone marrow-derived and adipose-derived stromal cells. Stem Cells Dev 2013;22:1086-1096.
34. Ivanova-Todorova E, Bochev I, Mourd-jeva M et al. Adipose tissue-derived mesenchy-mal stem cells are more potent suppressors of dendritic cells differentiation compared to bone marrow-derived mesenchymal stem cells. Immunol Lett 2009;126:37-42.
35. Niemeyer P, Kornacker M, Mehlhorn A et al. Comparison of immunological properties of bone marrow stromal cells and adipose tissue-derived stem cells before and after osteogenic differentiation in vitro. Tissue Eng 2007;13: 111-121.
36. Yoo KH, Jang IK, Lee MW et al. Comparison of immunomodulatory properties of mes-enchymal stem cells derived from adult human tissues. Cell Immunol 2009;259:150-156.
37. D'Ippolito G, Schiller PC, Ricordi C et al. Age-related osteogenic potentialofmesenchy-mal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 1999;14: 1115-1122.
38. Maijenburg MW, Kleijer M, Vermeul K et al. The composition of the mesenchymal stro-mal cell compartment in human bone marrow changes during development and aging. Haematologica 2012;97:179-183.
39. Zuk PA, Zhu M, Ashjian P et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002;13:4279-4295.
40. Dicker A, Le Blanc K, Astrom G, van HV, Gotherstrom C, Blomqvist L et al. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res 2005;308:283-290.
41. Mitchell JB, McIntosh K, Zvonic S et al. Immunophenotype of human adipose-derived cells: Temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 2006;24:376-385.
42. Gronthos S, Franklin DM, Leddy HA et al. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001;189:54-63.
43. Traktuev DO, Merfeld-Clauss S, Li J et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesen-chymal surface markers, reside in a periendo-thelial location, and stabilize endothelial networks. Circ Res 2008;102:77-85.
44. Miranville A, Heeschen C, Sengenes C et al. Improvement of postnatal neovasculariza-tion by human adipose tissue-derived stem cells. Circulation 2004;110:349-355.
45. Suga H, Matsumoto D, Eto H et al. Functional implications of CD34 expression in human adipose-derived stem/progenitor cells. Stem Cells Dev 2009;18:1201-1210.
46. Francois M, Romieu-Mourez R, Li M, Galipeau J. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Mol Ther 2012;20: 187-195.
47. Melief SM, Geutskens SB, Fibbe W et al. Multipotent stromal cells skew monocytes towards an anti-inflammatory IL-10 producing phenotype by production of IL-6. Haemato-logica 2013 [Epub ahead of print].
48. de Waal Malefyt R, Abrams J, Bennett B et al. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: An autoregu-latory role of IL-10 produced by monocytes. J Exp Med 1991;174:1209-1220.
49. Chomarat P, Banchereau J, Davoust J et al. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol 2000;1:510-514.
50. Patel SA, Meyer JR, Greco SJ et al. Mesenchymal stem cells protect breast cancer cells through regulatory T cells: Role of mesenchymal stem cell-derived TGF-/3. J Immunol 2010; 184:5885-5894.
51. Yanez R, Oviedo A, Aldea M et al. Prostaglandin E2 plays a key role in the immunosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res 2010;316:3109-3123.
52. Gieseke F, Bohringer J, Bussolari R et al. Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells. Blood 2010;116:3770-3779.
53. Najar M, Raicevic G, Id BH et al. Modulated expression of adhesion molecules and galectin-1: Role during mesenchymal stromal cell immunoregulatory functions. Exp Hematol 2010;38:922-932.
54. 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.