Mesenchymal stromal cells derived from CD271⁺ bone marrow mononuclear cells exert potent allosuppressive properties

References

• Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res. 2006;312:2169–79.
   PubMed Web of Science ®Google Scholar
• Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol. 2006;36:2566–73.
   PubMed Web of Science ®Google Scholar
• Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110:3499–506.
   PubMed Web of Science ®Google Scholar
• Di NM, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, . Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99:3838–43.
   PubMed Web of Science ®Google Scholar
• Le BK, 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.
   Google Scholar
• 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;171:3426–34.
   PubMed Web of Science ®Google Scholar
• 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;75:389–97.
   PubMed Web of Science ®Google Scholar
• Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, . Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002;30:42–8.
   PubMed Web of Science ®Google Scholar
• Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, . Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003;102:3837–44.
   PubMed Web of Science ®Google Scholar
• Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, . Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 2003;101:3722–9.
   PubMed Web of Science ®Google Scholar
• Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR, . Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci. 2003;10:228–41.
   PubMed Web of Science ®Google Scholar
• 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;105:2821–7.
   PubMed Web of Science ®Google Scholar
• Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, . Human mesenchymal stem cells modulate B-cell functions. Blood. 2006;107:367–72.
   PubMed Web of Science ®Google Scholar
• 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;107:1484–90.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Rasmusson I, Gotherstrom C, Seidel C, Sundberg B, Sundin M, . Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes. Scand J Immunol. 2004;60:307–15.
   PubMed Web of Science ®Google Scholar
• 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;103:4619–21.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815–22.
   PubMed Web of Science ®Google Scholar
• Yanez R, Oviedo A, Aldea M, Bueren JA, Lamana ML. Prostaglandin E2 plays a key role in the immunosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res. 2010;316:3109–23.
   PubMed Web of Science ®Google Scholar
• Najar M, Raicevic G, Boufker HI, Fayyad KH, De BC, Meuleman N, . Mesenchymal stromal cells use PGE2 to modulate activation and proliferation of lymphocyte subsets: combined comparison of adipose tissue, Wharton's jelly and bone marrow sources. Cell Immunol. 2010;264:171–9.
   PubMed Web of Science ®Google Scholar
• Selmani Z, Naji A, Gaiffe E, Obert L, Tiberghien P, Rouas-Freiss N, . HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation. 2009;87:S62–6.
   Web of Science ®Google Scholar
• Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, . Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood. 2007;109:228–34.
   PubMed Web of Science ®Google Scholar
• Maccario R, Podesta M, Moretta A, Cometa A, Comoli P, Montagna D, . 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;90:516–25.
   PubMed Web of Science ®Google Scholar
• Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, . Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 2005;105:2214–19.
   PubMed Web of Science ®Google Scholar
• Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C, Deliliers GL. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol. 2002;30:783–91.
   PubMed Web of Science ®Google Scholar
• Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, . Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002;46:3349–60.
   PubMed Web of Science ®Google Scholar
• Jones E, English A, Churchman SM, Kouroupis D, Boxall SA, Kinsey S, . Large-scale extraction and characterization of CD271+ multipotential stromal cells from trabecular bone in health and osteoarthritis: implications for bone regeneration strategies based on uncultured or minimally cultured multipotential stromal cells. Arthritis Rheum. 2010;62:1944–54.
   PubMedGoogle Scholar
• Kuci S, Kuci Z, Kreyenberg H, Deak E, Putsch K, Huenecke S, . CD271 antigen defines a subset of multipotent stromal cells with immunosuppressive and lymphohematopoietic engraftment-promoting properties. Haematologica. 2010;95: 651–59.
   PubMed Web of Science ®Google Scholar
• Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, . Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–17.
   PubMed Web of Science ®Google Scholar
• Daheshia M, Yao JQ. The bone marrow lesion in osteoarthritis. Rheumatol Int. 2011;31:143–8.
   Google Scholar
• Jimenez-Boj E, Redlich K, Turk B, Hanslik-Schnabel B, Wanivenhaus A, Chott A, . Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J Immunol. 2005;175:2579–88.
   PubMed Web of Science ®Google Scholar
• Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, . Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+ CD25high FOXP3+ regulatory T cells. Stem Cells. 2008;26:212–22.
   PubMed Web of Science ®Google Scholar
• Sheng H, Wang Y, Jin Y, Zhang Q, Zhang Y, Wang L, . A critical role of IFNgamma in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Res. 2008;18:846–57.
   PubMed Web of Science ®Google Scholar
• Djouad F, Fritz V, Apparailly F, Louis-Plence P, Bony C, Sany J, . Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum. 2005;52:1595–603.
   PubMed Web of Science ®Google Scholar
• Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, . Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells. 2006;24:386–98.
   PubMed Web of Science ®Google Scholar
• Prevosto C, Zancolli M, Canevali P, Zocchi MR, Poggi A. Generation of CD4+ or CD8+ regulatory T cells upon mesenchymal stem cell–lymphocyte interaction. Haematologica. 2007;92:881–8.
   PubMedGoogle Scholar
• Hoffmann P, Eder R, Boeld TJ, Doser K, Piseshka B, Andreesen R, . Only the CD45RA+ subpopulation of CD4+ CD25high T cells gives rise to homogeneous regulatory T-cell lines upon in vitro expansion. Blood. 2006;108: 4260–7.
   PubMed Web of Science ®Google Scholar
• Ermann J, Hoffmann P, Edinger M, Dutt S, Blankenberg FG, Higgins JP, . Only the CD62L+ subpopulation of CD4+ CD25+ regulatory T cells protects from lethal acute GVHD. Blood. 2005;105:2220–6.
   PubMed Web of Science ®Google Scholar
• Lu SY, Liu KY, Liu DH, Xu LP, Huang XJ. High frequencies of CD62L(+) naive regulatory T cells in allografts are associated with a low risk of acute graft-versus-host disease following unmanipulated allogeneic haematopoietic stem cell transplantation. Clin Exp Immunol. 2011;165:264–77.
   Google Scholar