CD90 + Human Dermal Stromal Cells Are Potent Inducers of FoxP3 + Regulatory T Cells

Journal of Investigative Dermatology

Volumn 135, Issue 1, 2015, Pages 130-141

  Pfisterer, Karin ^a,c   Lipnik, Karoline M ^b   Hofer, Erhard ^b   Elbe Bürger, Adelheid ^a  

^a Universitatsklinik fur Dermatologie   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADAPALENE; ALPHA SMOOTH MUSCLE ACTIN; CD133 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; ENDOGLIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; STAGE SPECIFIC EMBRYO ANTIGEN 4; T LYMPHOCYTE RECEPTOR; THY 1 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL CONTACT; CELL DENSITY; CELL DIFFERENTIATION; CELL LINEAGE; CELLULAR DISTRIBUTION; CYTOKINE RELEASE; DERMAL MICROVASCULAR ENDOTHELIAL CELL; EMBRYO; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MALE; MESENCHYMAL STROMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SKIN CELL; UPREGULATION; CELL PROLIFERATION; CELL SEPARATION; COCULTURE; CYTOLOGY; DERMIS; ENDOTHELIUM CELL; HEK293 CELL LINE; HOMEOSTASIS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; PREPUCE; PRIMARY CELL CULTURE; STROMA CELL;

ANTIGENS, CD28; ANTIGENS, THY-1; CELL PROLIFERATION; CELL SEPARATION; COCULTURE TECHNIQUES; DERMIS; ENDOTHELIAL CELLS; FORESKIN; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HOMEOSTASIS; HUMANS; IMMUNOPHENOTYPING; MALE; PRIMARY CELL CULTURE; STROMAL CELLS; T-LYMPHOCYTES, REGULATORY;

EID: 84925862714     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.309     Document Type: Article

References (77)

1. Akbar AN, Taams LS, Salmon M et al. (2003) The peripheral generation of CD4 CD25 regulatory T cells. Immunology 109:319-25
2. Allan SE, Crome SQ, Crellin NK et al. (2007) Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 19:345-54
3. Azukizawa H, Dohler A, Kanazawa N et al. (2011) Steady state migratory RelB langerin dermal dendritic cells mediate peripheral induction of antigen-specific CD4 CD25 Foxp3 regulatory T cells. Eur J Immunol 41:1420-34
4. Baecher-Allan C, Wolf E, Hafler DA (2006) MHC class II expression identifies functionally distinct human regulatory T cells. J Immunol 176:4622-31
5. Beriou G, Constantino CM, Ashley CW et al. (2009) IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 113: 4240-9
6. Bocelli-Tyndall C, Bracci L, Schaeren S et al. (2009) Human bone marrow mesenchymal stem cells and chondrocytes promote and/or suppress the in vitro proliferation of lymphocytes stimulated by interleukins 2, 7 and 15. Ann Rheum Dis 68:1352-9
7. Bouffi C, Bony C, Courties G et al. (2010) IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One 5:e1424
8. Campioni D, Rizzo R, Stignani M et al. (2009) A decreased positivity for CD90 on human mesenchymal stromal cells (MSCs) is associated with a loss of immunosuppressive activity by MSCs. Cytometry B Clin Cytom 76:225-30
9. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9:641-50
10. Chamberlain G, Fox J, Ashton B et al. (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25:2739-49
11. Chen W, Jin W, Hardegen N et al. (2003) Conversion of peripheral CD4 CD25 naive T cells to CD4CD25 regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198:1875-86
12. Clark RA, Chong B, Mirchandani N et al. (2006) The vast majority of CLA T cells are resident in normal skin. J Immunol 176:4431-9
13. Clark RA, Huang SJ, Murphy GF et al. (2008) Human squamous cell carcinomas evade the immune response by down-regulation of vascular E-selectin and recruitment of regulatory T cells. J Exp Med 205:2221-34
14. Clark RA (2010) Skin-resident T cells: the ups and downs of on site immunity. J Invest Dermatol 130:362-70
15. Conrad C, Niess H, Huss R et al. (2009) Multipotent mesenchymal stem cells acquire a lymphendothelial phenotype and enhance lymphatic regeneration in vivo. Circulation 119:281-9
16. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV et al. (2007) A functionally specialized population of mucosal CD103 DCs induces Foxp3 regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204:1757-64
17. d'Hennezel E, Yurchenko E, Sgouroudis E et al. (2011) Single-cell analysis of the human T regulatory population uncovers functional heterogeneity and instability within FOXP3 cells. J Immunol 186:6788-97
18. da Silva ML, Caplan AI, Nardi NB (2008) In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26:2287-99
19. da Silva ML, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204-13
20. Davidson TS, Dipaolo RJ, Anderson J et al. (2007) Cutting edge: IL-2 is essential for TGF-beta-mediated induction of FoxP3 T regulatory cells. J Immunol 178:4022-6
21. Di Ianni M, Del Papa B, De Ioanni M et al. (2008) Mesenchymal cells recruit and regulate T regulatory cells. Exp Hematol 36:309-18
22. Dominici M, Le BK, Mueller I et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-7
23. Dudda JC, Perdue N, Bachtanian E et al. (2008) Foxp3 regulatory T cells maintain immune homeostasis in the skin. J Exp Med 205:1559-65
24. Duhen T, Duhen R, Lanzavecchia A et al. (2012) Functionally distinct subsets of human FOXP3 Treg cells that phenotypically mirror effector Th cells. Blood 119:4430-40
25. Engela AU, Baan CC, Dor FJ et al. (2012) On the interactions between mesenchymal stem cells and regulatory T cells for immunomodulation in transplantation. Front Immunol 3:126
26. English K (2013) Mechanisms of mesenchymal stromal cell immunomodulation. Immunol Cell Biol 91:19-26
27. English K, Ryan JM, Tobin L et al. (2009) Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4CD25High forkhead box P3 regulatory T cells. Clin Exp Immunol 156:149-60
28. Fernandes KJ, McKenzie IA, Mill P et al. (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6:1082-93
29. Golovina TN, Mikheeva T, Suhoski MM et al. (2008) CD28 costimulation is essential for human T regulatory expansion and function. J Immunol 181:2855-68
30. Gruschwitz M, Muller PU, Sepp N et al. (1990) Transcription and expression of transforming growth factor type beta in the skin of progressive systemic sclerosis: a mediator of fibrosis? J Invest Dermatol 94:197-203
31. Gruschwitz MS, Hornstein OP (1992) Expression of transforming growth factor type beta on human epidermal dendritic cells. J Invest Dermatol 99:114-6
32. Guo F, Iclozan C, Suh WK et al. (2008) CD28 controls differentiation of regulatory T cells from naive CD4 T cells. J Immunol 181:2285-91
33. Haniffa MA, Wang XN, Holtick U et al. (2007) Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol 179:1595-604
34. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057-61
35. Hsu WT, Lin CH, Chiang BL et al. (2013) Prostaglandin E2 potentiates mesenchymal stem cell-induced IL-10IFN-gCD4 regulatory T cells to control transplant arteriosclerosis. J Immunol 190:2372-780
36. Hunt DP, Morris PN, Sterling J et al. (2008) A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26:163-72
37. Jones BJ, McTaggart SJ (2008) Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol 36:733-41
38. Kaporis HG, Guttman-Yassky E, Lowes MA et al. (2007) Human basal cell carcinoma is associated with Foxp3 T cells in a Th2 dominant microenvironment. J Invest Dermatol 127:2391-8
39. Kmieciak M, Gowda M, Graham L et al. (2009) Human T cells express CD25 and Foxp3 upon activation and exhibit effector/memory phenotypes without any regulatory/suppressor function. J Transl Med 7:89
40. Kupper TS, Fuhlbrigge RC (2004) Immune surveillance in the skin: mechanisms and clinical consequences. Nat Rev Immunol 4:211-22
41. Le Blanc K, Mougiakakos D (2012) Multipotent mesenchymal stromal cells and the innate immune system. Nat Rev Immunol 12:383-96
42. Le Blanc K, Tammik L, Sundberg B et al. (2003) Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 57:11-20
43. Liang S, Alard P, Zhao Y et al. (2005) Conversion of CD4 CD25 cells into CD4 CD25 regulatory T cells in vivo requires B7 costimulation, but not the thymus. J Exp Med 201:127-37
44. Liu W, Putnam AL, Xu-Yu Z et al. (2006) CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4 T reg cells. J Exp Med 203:1701-11
45. Maccario R, Podesta M, Moretta A et al. (2005) 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 90:516-25
46. McClymont SA, Putnam AL, Lee MR et al. (2011) Plasticity of human regulatory T cells in healthy subjects and patients with type 1 diabetes. J Immunol 186:3918-26
47. McMurchy AN, Gillies J, Gizzi MC et al. (2013) A novel function for FOXP3 in humans: intrinsic regulation of conventional T cells. Blood 121:1265-75
48. Mendez-Ferrer S, Michurina TV, Ferraro F et al. (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829-34
49. Miskov-Zivanov N, Turner MS, Kane LP et al. (2013) The duration of T cell stimulation is a critical determinant of cell fate and plasticity. Sci Signal 6:ra97
50. Najar M, Rouas R, Raicevic G et al. (2009) Mesenchymal stromal cells promote or suppress the proliferation of T lymphocytes from cord blood and peripheral blood: the importance of low cell ratio and role of interleukin-6. Cytotherapy 11:570-83
51. Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110:3499-506
52. Nestle FO, Di MP, Qin JZ et al. (2009) Skin immune sentinels in health and disease. Nat Rev Immunol 9:679-91
53. O'Shea JJ, Paul WE (2010) Mechanisms underlying lineage commitment and plasticity of helper CD4 T cells. Science 327:1098-102
54. Pankajakshan D, Kansal V, Agrawal DK (2013) In vitro differentiation of bone marrow derived porcine mesenchymal stem cells to endothelial cells. J Tissue Eng Regen Med. 7:911-20
55. Peled A, Zipori D, Abramsky O et al. (1991) Expression of alpha-smooth muscle actin in murine bone marrow stromal cells. Blood 78:304-9
56. Pesenacker AM, Bending D, Ursu S et al. (2013) CD161 defines the subset of FoxP3 T cells capable of producing proinflammatory cytokines. Blood 121:2647-58
57. Porada CD, Zanjani ED, Almeida-Porad G (2006) Adult mesenchymal stem cells: a pluripotent population with multiple applications. Curr Stem Cell Res Ther 1:365-9
58. Prevosto C, Zancolli M, Canevali P et al. (2007) Generation of CD4 or CD8 regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Haematologica 92:881-8
59. Quirici N, Soligo D, Bossolasco P et al. (2002) Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30:783-91
60. Ramasamy R, Tong CK, Seow HF et al. (2008) The immunosuppressive effects of human bone marrow-derived mesenchymal stem cells target T cell proliferation but not its effector function. Cell Immunol 251: 131-6
61. Roemeling-van RM, Weimar W, Hoogduijn MJ (2012) Mesenchymal stem cells: application for solid-organ transplantation. Curr Opin Organ Transplant 17:55-62
62. Sakaguchi S, Yamaguchi T, Nomura T et al. (2008) Regulatory T cells and immune tolerance. Cell 133:775-87
63. Schuster C, Vaculik C, Fiala C et al. (2009) HLA-DR leukocytes acquire CD1 antigens in embryonic and fetal human skin and contain functional antigen-presenting cells. J Exp Med 206:169-81
64. Semple K, Nguyen A, Yu Y et al. (2011) Strong CD28 costimulation suppresses induction of regulatory T cells from naive precursors through Lck signaling. Blood 117:3096-103
65. Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18: 696-704
66. Skalli O, Pelte MF, Peclet MC et al. (1989) Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 37:315-21
67. Sontheimer RD (1989) Perivascular dendritic macrophages as immunobiological constituents of the human dermal microvascular unit. J Invest Dermatol 93:96S-101S
68. Su J, Chen X, Huang Y et al. (2013) Phylogenetic distinction of iNOS and IDO function in mesenchymal stem cell-mediated immunosuppression in mammalian species. Cell Death and Diff 21:388-96
69. Sugiyama H, Gyulai R, Toichi E et al. (2005) Dysfunctional blood and target tissue CD4CD25high regulatory T cells in psoriasis: mechanism underlying unrestrained pathogenic effector T cell proliferation. J Immunol 174:164-73
70. Thompson LJ, Valladao AC, Ziegler SF (2011) Cutting edge: de novo induction of functional Foxp3 regulatory CD4 T cells in response to tissuerestricted self antigen. J Immunol 186:4551-5
71. Toma JG, McKenzie IA, Bagli D et al. (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23:727-37
72. Vaculik C, Schuster C, Bauer W et al. (2012) Human dermis harbors distinct mesenchymal stromal cell subsets. J Invest Dermatol 132:563-74
73. Watanabe N, Wang YH, Lee HK et al. (2005) Hassall's corpuscles instruct dendritic cells to induce CD4CD25 regulatory T cells in human thymus. Nature 436:1181-5
74. Wetzel A, Chavakis T, Preissner KT et al. (2004) Human Thy-1 (CD90) on activated endothelial cells is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Immunol 172:3850-9
75. Yagi H, Nomura T, Nakamura K et al. (2004) Crucial role of FOXP3 in the development and function of human CD25CD4 regulatory T cells. Int Immunol 16:1643-56
76. Yamazaki S, Bonito AJ, Spisek R et al. (2007) Dendritic cells are specialized accessory cells along with TGF-b for the differentiation of Foxp3 CD4 regulatory T cells from peripheral Foxp3 precursors. Blood 110:4293-302
77. Zhao H, Peehl DM (2009) Tumor-promoting phenotype of CD90hi prostate cancer-associated fibroblasts. Prostate 69:991-1000