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

References

• Tondreau T, Meuleman N, Delforge A, Dejeneffe M, Leroy R, Massy M, et al. Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells. 2005; 23:1105–112.
   PubMed Web of Science ®Google Scholar
• Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001; 7:211–28.
   PubMedGoogle Scholar
• Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM, et al. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 2001; 98:2396–2402.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284:143–7.
   PubMed Web of Science ®Google Scholar
• Keating A. Mesenchymal stromal cells. Curr Opin Hematol. 2006; 13:419–25.
   PubMed Web of Science ®Google Scholar
• Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol. 2008; 36:733–41.
   PubMed Web of Science ®Google Scholar
• Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, et al. 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 Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringdén 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.
   PubMed Web of Science ®Google Scholar
• Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 2003; 101:3722–9.
   PubMed Web of Science ®Google Scholar
• Nasef A, Ashammakhi N, Fouillard L. Immunomodulatory effect of mesenchymal stromal cells: possible mechanisms. Regen Med. 2008; 3:531–46.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringdén O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003; 31:890–6.
   PubMed Web of Science ®Google Scholar
• 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; 149:353–63.
   PubMed Web of Science ®Google Scholar
• Tabera S, Pérez-Simón JA, Díez-Campelo M, Sánchez-Abarca LI, Blanco B, López A, et al. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica. 2008; 93:1301–9.
   PubMed Web of Science ®Google Scholar
• Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, et al. Human mesenchymal stem cells modulate B-cell functions. Blood. 2006; 107:367–72.
   PubMed Web of Science ®Google Scholar
• Rasmusson I, Le Blanc K, Sundberg B, et al. Mesenchymal stem cells stimulate antibody secretion in human B cells. Scand J Immunol. 2007; 65:336–43.
   PubMed Web of Science ®Google Scholar
• Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 2008; 111:1327–33.
   PubMed Web of Science ®Google Scholar
• 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; 177:2080–7.
   PubMed Web of Science ®Google Scholar
• Li YP, Paczesny S, Lauret E, Poirault S, Bordigoni P, Mekhloufi F, 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; 180:1598–608.
   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
• Di Ianni M, Del Papa B, De Ioanni M, Moretti L, Bonifacio E, Cecchini D, et al. Mesenchymal cells recruit and regulate T regulatory cells. Exp Hematol. 2008; 36:309–18.
   PubMed Web of Science ®Google Scholar
• Tondreau T, Lagneaux L, Dejeneffe M, Delforge A, Massy M, Mortier C, et al. Isolation of BM mesenchymal stem cells by plastic adhesion or negative selection: phenotype, proliferation kinetics and differentiation potential. Cytotherapy. 2004; 6:372–9.
   PubMed Web of Science ®Google Scholar
• D'Arena G, Musto P, Cascavilla N, Minervini MM, Di Giorgio G, Maglione A, et al. Inability of activated cord blood T lymphocytes to perform Th1-like and Th2-like responses: implications for transplantation. J Hematother Stem Cell Res. 1999; 8:381–5.
   Google Scholar
• Garcia Vela JA, Delgado I, Bornstein R, Alvarez B, Auray MC, Martin I, et al. Comparative intracellular cytokine production by in vitro stimulated T lymphocytes from human umbilical cord blood (HUCB) and adult peripheral blood (APB). Anal Cell Pathol. 2000; 20:93–8.
   Google Scholar
• Han P, McDonald T, Hodge G. Potential immaturity of the T-cell and antigen-presenting cell interaction in cord blood with particular emphasis on the CD40–CD40 ligand costimulatory pathway. Immunology. 2004; 113:26–34.
   Google Scholar
• Chadburn A, Inghirami G, Knowles DM. The kinetics and temporal expression of T-cell activation-associated antigens CD15 (LeuM1), CD30 (Ki-1), EMA, and CD11c (LeuM5) by benign activated T cells. Hematol Pathol. 1992; 6:193–202.
   PubMedGoogle Scholar
• Smol'nikova VV, Voznyuk AV, Potapnev MP. Cytokine-induced differentiation and proliferation of human T lymphocytes in vitro: effects of interleukin 2 and interleukin 6. Bull Exp Biol Med. 2000; 129:567–70.
   PubMed Web of Science ®Google Scholar
• Yonezawa A, Hori T, Sakaida H, Uchiyama T. SDF-1 has costimulatory effects on human T cells: possible involvement of MAPK (ERK2) activation. Microbiol Immunol. 2000; 44:135–41.
   Google Scholar
• Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003; 102:3837–44.
   PubMed Web of Science ®Google Scholar
• Plumas J, Chaperot L, Richard MJ, Molens JP, Bensa JC, Favrot MC. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia. 2005; 19:1597–604.
   PubMed Web of Science ®Google Scholar
• Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol. 2005; 129:118–29.
   PubMed Web of Science ®Google Scholar
• Wang XN, Sviland L, Ademokun AJ, Dunn J, Cavanagh G, Proctor SJ, et al. Cellular alloreactivity of human cord blood cells detected by T-cell frequency analysis and a human skin explant model. Transplantation. 1998; 66:903–9.
   Google Scholar
• Kurtzberg J. Update on umbilical cord blood transplantation. Curr Opin Pediatr. 2009; 21:22–9.
   PubMed Web of Science ®Google Scholar
• Macmillan ML, Blazar BR, Defor TE, Wagner JE. Transplantation of ex-vivo culture-expanded parental haploidentical mesenchymal stem cells to promote engraftment in pediatric recipients of unrelated donor umbilical cord blood: results of a phase I-II clinical trial. Bone Marrow Transplant.. 2009; 43:447–54.
   PubMed Web of Science ®Google Scholar
• Harris DT, Schumacher MJ, Locascio J, Besencon FJ, Olson GB, DeLuca D, et al. Phenotypic and functional immaturity of human umbilical cord blood T lymphocytes. Proc Natl Acad Sci USA. 1992; 89:10006–10.
   PubMed Web of Science ®Google Scholar
• Li C, Zhang W, Jiang X, Mao N. Human-placenta-derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cells. Cell Tissue Res. 2007; 330:437–46.
   PubMed Web of Science ®Google Scholar
• Fang L, Lange C, Engel M, Zander AR, Fehse B. Sensitive balance of suppressing and activating effects of mesenchymal stem cells on T-cell proliferation. Transplantation. 2006; 82:1370–3.
   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
• 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
• Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, et al. 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
• Chan JL, Tang KC, Patel AP, Bonilla LM, Pierobon N, Ponzio NM, et al. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma. Blood. 2006; 107:4817–24.
   PubMed Web of Science ®Google Scholar
• Magatti M, De Munari S, Vertua E, Gibelli L, Wengler GS, Parolini O. Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem Cells. 2008; 26:182–92.
   PubMed Web of Science ®Google Scholar
• Eddahri F, Denanglaire S, Bureau F, Spolski R, Leonard WJ, Leo O, et al. Interleukin-6/STAT3 signaling regulates the ability of naive T cells to acquire B-cell help capacities. Blood. 2009; 113:2426–33.
   PubMed Web of Science ®Google Scholar
• Traggiai E, Volpi S, Schena F, Gattorno M, Ferlito F, Moretta L, 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; 26:562–9.
   PubMed Web of Science ®Google Scholar
• Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, 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; 26:212–22.
   PubMed Web of Science ®Google Scholar
• Barrett AJ, Le Blanc K. Prophylaxis of acute GVHD: manipulate the graft or the environment?. Best Pract Res Clin Haematol. 2008; 21:165–76.
   Web of Science ®Google Scholar