Human mesenchymal stem cells modulate B-cell functions

Blood - Tập 107 Số 1 - Trang 367-372 - 2006
Anna Corcione1, Federica Benvenuto1, Elisa Ferretti1, Debora Giunti1, Valentina Cappiello1, Francesco Cazzanti1, Marco Risso1, Francesca Gualandi1, Gianluigi Mancardi1, Vito Pistoia1, Antonio Uccelli1
1From the Laboratory of Oncology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) G. Gaslini, Genova, Italy; Neuroimmunology Unit, Department of Neurosciences, Ophthalmology and Genetics and Centre of Excellence for Biomedical Research, University of Genova, Italy; Transfusion Medicine, IRCCS G. Gaslini, Genova, Italy; and Department of Haematology, San Martino Hospital, Genoa, Italy

Tóm tắt

Abstract

Human mesenchymal stem cells (hMSCs) suppress T-cell and dendritic-cell function and represent a promising strategy for cell therapy of autoimmune diseases. Nevertheless, no information is currently available on the effects of hMSCs on B cells, which may have a large impact on the clinical use of these cells. hMSCs isolated from the bone marrow and B cells purified from the peripheral blood of healthy donors were cocultured with different B-cell tropic stimuli. B-cell proliferation was inhibited by hMSCs through an arrest in the G0/G1 phase of the cell cycle and not through the induction of apoptosis. A major mechanism of B-cell suppression was hMSC production of soluble factors, as indicated by transwell experiments. hMSCs inhibited B-cell differentiation because IgM, IgG, and IgA production was significantly impaired. CXCR4, CXCR5, and CCR7 B-cell expression, as well as chemotaxis to CXCL12, the CXCR4 ligand, and CXCL13, the CXCR5 ligand, were significantly down-regulated by hMSCs, suggesting that these cells affect chemotactic properties of B cells. B-cell costimulatory molecule expression and cytokine production were unaffected by hMSCs. These results further support the potential therapeutic use of hMSCs in immune-mediated disorders, including those in which B cells play a major role.

Từ khóa


Tài liệu tham khảo

Devine SM, Hoffman R. Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr Opin Hematol. 2000;7: 358-363.

Gordon MY, Riley GP, Watt SM, Greaves MF. Compartmentalization of a haematopoietic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment. Nature. 1987;326: 403-405.

Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284: 143-147.

Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002;418: 41-49.

Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9: 641-650.

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.

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.

Lazarus HM, Koc ON, Devine SM, et al. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol Blood Marrow Transplant. 2005;11: 389-398.

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.

Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T cell anergy. Blood. 2005;106: 1755-1761.

Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105: 1815-1822.

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.

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.

Kierney PC, Dorshkind K. B lymphocyte precursors and myeloid progenitors survive in diffusion chamber cultures but B cell differentiation requires close association with stromal cells. Blood. 1987;70: 1418-1424.

Kurosaka D, LeBien TW, Pribyl JA. Comparative studies of different stromal cell microenvironments in support of human B-cell development. Exp Hematol. 1999;27: 1271-1281.

Bernasconi NL, Onai N, Lanzavecchia A. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood. 2003;101: 4500-4504.

Burt RK. Finding a less toxic stem cell therapy for multiple sclerosis. Blood. 2005;106: 1514-1515.

Campbell JJ, Bowman EP, Murphy K, et al. 6-C-kine (SLC), a lymphocyte adhesion-triggering chemokine expressed by high endothelium, is an agonist for the MIP-3beta receptor CCR7. J Cell Biol. 1998;141: 1053-1059.

Corcione A, Arduino N, Ferretti E, et al. CCL19 and CXCL12 trigger in vitro chemotaxis of human mantle cell lymphoma B cells. Clin Cancer Res. 2004;10: 964-971.

Corcione A, Tortolina G, Bonecchi R, et al. Chemotaxis of human tonsil B lymphocytes to CC chemokine receptor (CCR) 1, CCR2 and CCR4 ligands is restricted to non-germinal center cells. Int Immunol. 2002;14: 883-892.

Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000; 182: 311-322.

Baggiolini M. Chemokines and leukocyte traffic. Nature. 1998;392: 565-568.

Cyster JG. Chemokines and cell migration in secondary lymphoid organs. Science. 1999;286: 2098-2102.

Muller G, Hopken UE, Stein H, Lipp M. Systemic immunoregulatory and pathogenic functions of homeostatic chemokine receptors. J Leukoc Biol. 2002;72: 1-8.

Pistoia V. Production of cytokines by human B cells in health and disease. Immunol Today. 1997; 18: 343-350.

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: 389-397.

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.

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: 2821-2827.

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.

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: 4619-4621.

Tachibana K, Hirota S, Iizasa H, et al. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature. 1998; 393: 591-594.

Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature. 1998;393: 595-599.

Okada T, Ngo VN, Ekland EH, et al. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J Exp Med. 2002;196: 65-75.

Nie Y, Waite J, Brewer F, Sunshine MJ, Littman DR, Zou YR. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J Exp Med. 2004;200: 1145-1156.

Allen CD, Ansel KM, Low C, et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat Immunol. 2004;5: 943-952.

Odendahl M, Mei H, Hoyer BF, et al. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood. 2005;105: 1614-1621.

Hargreaves DC, Hyman PL, Lu TT, et al. A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med. 2001; 194: 45-56.

Ansel KM, Ngo VN, Hyman PL, et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature. 2000;406: 309-314.

Reif K, Ekland EH, Ohl L, et al. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature. 2002; 416: 94-99.

Ma Q, Jones D, Borghesani PR, et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A. 1998; 95: 9448-9453.