Inflammation and toll-like receptor ligation differentially affect the osteogenic potential of human mesenchymal stromal cells depending on their tissue origin

Tissue Engineering - Part A

Volumn 18, Issue 13-14, 2012, Pages 1410-1418

  Raicevic, Gordana ^a   Najar, Mehdi ^a   Pieters, Karlien ^a   De Bruyn, Cecile ^a   Meuleman, Nathalie ^a   Bron, Dominique ^a   Toungouz, Michel ^a,b   Lagneaux, Laurence ^a  

^a JULES BORDET INSTITUTE   (Belgium)

^b ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMINERALIZATION; BONE; CELLS; PATHOLOGY; PHOSPHATASES; TISSUE;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE ACTIVITY; BONE MARROW; CELL TYPES; CELL-BASED; CLINICAL SETTINGS; CYTOKINES; ENZYMATIC ACTIVITIES; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; OSTEOGENIC; OSTEOGENIC DIFFERENTIATION; OSTEOGENIC POTENTIAL; TOLL-LIKE RECEPTORS; UMBILICAL CORDS;

CELL CULTURE;

ALKALINE PHOSPHATASE; BIOLOGICAL MARKER; TLR3 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4;

ADIPOSE TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE MINERALIZATION; CELL MEMBRANE; CELL SEPARATION; CYTOLOGY; ENZYMOLOGY; HUMAN; INFLAMMATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; WHARTON JELLY;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE; BIOLOGICAL MARKERS; BONE MARROW CELLS; CALCIFICATION, PHYSIOLOGIC; CELL MEMBRANE; CELL SEPARATION; HUMANS; INFLAMMATION; MESENCHYMAL STROMAL CELLS; ORGAN SPECIFICITY; OSTEOGENESIS; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; WHARTON JELLY;

EID: 84911808355     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2011.0434     Document Type: Article

References (43)

1. Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W.G., Ross, J., Haug, J., Johnson, T., Feng, J.Q., Harris, S., Wiedemann, L.M., Mishina, Y., and Li, L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836, 2003.
2. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
3. Krampera, M., Glennie, S., Dyson, J., Scott, D., Laylor, R., Simpson, E., and Dazzi, F. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigenspecific T cells to their cognate peptide. Blood 101, 3722, 2003.
4. Aggarwal, S., and Pittenger, M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815, 2005.
5. Uccelli, A., Moretta, L., and Pistoia, V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 36, 2566, 2006.
6. Corcione, A., Benvenuto, F., Ferretti, E., Giunti, D., Cappiello, V., Cazzanti, F., Risso, M., Gualandi, F., Mancardi, G.L., Pistoia, V., and Uccelli, A. Human mesenchymal stem cells modulate B-cell functions. Blood 107, 367, 2006.
7. Le Blanc, K., Gotherstrom, C., Ringden, O., Hassan, M., McMahon, R., Horwitz, E., Anneren, G., Axelsson, O., Nunn, J., Ewald, U., Norden-Lindeberg, S., Jansson, M., Dalton, A., Astrom, E., and Westgren, M. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 79, 1607, 2005.
8. Baksh, D., Yao, R., and Tuan, R.S. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 25, 1384, 2007.
9. Blaha, M., Mericka, P., Zak, P., Stepanova, V., Vavra, L., Maly, J., and Tousovska, K. The risk of infection transmission from blood progenitor cell concentrates. J Hematother Stem Cell Res 12, 161, 2003.
10. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., and Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315, 2006.
11. Najar, M., Raicevic, G., Boufker, H.I., Fayyad-Kazan, H., De Bruyn, C., Meuleman, N., Bron, D., Toungouz, M., and Lagneaux, L. Adipose-tissue-derived and Wharton's jellyderived mesenchymal stromal cells suppress lymphocyte responses by secreting leukemia inhibitory factor. Tissue Eng Part A 16, 3537, 2010.
12. Weiss, M.L., Anderson, C., Medicetty, S., Seshareddy, K.B., Weiss, R.J., VanderWerff, I., Troyer, D., and McIntosh, K.R. Immune properties of human umbilical cord Wharton's jelly-derived cells. Stem Cells 26, 2865, 2008.
13. Raicevic, G., Rouas, R., Najar, M., Stordeur, P., Boufker, H.I., Bron, D., Martiat, P., Goldman, M., Nevessignsky, M.T., and Lagneaux, L. Inflammation modifies the pattern and the function of Toll-like receptors expressed by human mesenchymal stromal cells. Hum Immunol 71, 235, 2010.
14. Liotta, F., Angeli, R., Cosmi, L., Fili, L., Manuelli, C., Frosali, F., Mazzinghi, B., Maggi, L., Pasini, A., Lisi, V., Santarlasci, V., Consoloni, L., Angelotti, M.L., Romagnani, P., Parronchi, P., Krampera, M., Maggi, E., Romagnani, S., and Annunziato, F. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells 26, 279, 2008.
15. Lombardo, E., DelaRosa, O., Mancheno-Corvo, P., Menta, R., Ramirez, C., and Buscher, D. Toll-like receptor-mediated signaling in human adipose-derived stem cells: implications for immunogenicity and immunosuppressive potential. Tissue Eng Part A 15, 1579, 2009.
16. Kawai, T., and Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11, 373, 2010.
17. Akira, S., and Sato, S. Toll-like receptors and their signaling mechanisms. Scand J Infect Dis 35, 555, 2003.
18. Raicevic, G., Najar, M., Stamatopoulos, B., De Bruyn, C., Meuleman, N., Bron, D., Toungouz, M., and Lagneaux, L. The source of human mesenchymal stromal cells influences their TLR profile as well as their functional properties. Cell Immunol 270, 207, 2011.
19. Najar, M., Raicevic, G., Id Boufker, H., Stamatopoulos, B., De Bruyn, C., Meuleman, N., Bron, D., Toungouz, M., and Lagneaux, L. Modulated expression of adhesion molecules and galectin-1: role during mesenchymal stromal cell immunoregulatory functions. Exp Hematol 38, 922, 2010.
20. De Bruyn, C.X., Najar, M., Raicevic, G., Meuleman, N., Pieters, K., Stamatopoulos, B., Delforge, A., Bron, D., and Lagneaux, L. A rapid, simple and reproducible method for the isolation of mesenchymal stromal cells from Wharton's jelly without enzymatic treatment. Stem Cells Dev 20, 547, 2011.
21. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7, 211, 2001.
22. Hwa, C.H., Bae, Y.C., and Jung, J.S. Role of toll-like receptors on human adipose-derived stromal cells. Stem Cells 24, 2744, 2006.
23. St Onge, M., Dumas, A., Michaud, A., Laflamme, C., Dussault, A.A., and Pouliot, M. Impact of anti-inflammatory agents on the gene expression profile of stimulated human neutrophils: unraveling endogenous resolution pathways. PLoS One 4, e4902, 2009.
24. Mailliard, R.B., Wankowicz-Kalinska, A., Cai, Q., Wesa, A., Hilkens, C.M., Kapsenberg, M.L., Kirkwood, J.M., Storkus, W.J., and Kalinski, P. Alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res 64, 5934, 2004.
25. Daxecker, H., Raab, M., Markovic, S., Karimi, A., Griesmacher, A., and Mueller, M.M. Endothelial adhesion molecule expression in an in vitro model of inflammation. Clin Chim Acta 325, 171, 2002.
26. Id Boufker, H., Lagneaux, L., Najar, M., Piccart, M., Ghanem, G., Body, J.J., and Journe, F. The Src inhibitor dasatinib accelerates the differentiation of human bone marrowderived mesenchymal stromal cells into osteoblasts. BMC Cancer 10, 298, 2010.
27. De Toni, F., Poglio, S., Youcef, A.B., Cousin, B., Pflumio, F., Bourin, P., Casteilla, L., and Laharrague, P. Human adiposederived stromal cells efficiently support hematopoiesis in vitro and in vivo: a key step for therapeutic studies. Stem Cells Dev 20, 2127, 2011.
28. Frank, O., Heim, M., Jakob, M., Barbero, A., Schafer, D., Bendik, I., Dick, W., Heberer, M., and Martin, I. Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem 8, 737, 2002.
29. Ciavarella, S., Dammacco, F., De Matteo, M., Loverro, G., and Silvestris, F. Umbilical cord mesenchymal stem cells: role of regulatory genes in their differentiation to osteoblasts. Stem Cells Dev 18, 1211, 2009.
30. Wang, F.S., Yang, K.D., Wang, C.J., Huang, H.C., Chio, C.C., Hsu, T.Y., and Ou, C.Y. Shockwave stimulates oxygen radical-mediated osteogenesis of the mesenchymal cells from human umbilical cord blood. J Bone Miner Res 19, 973, 2004.
31. Zhang, Z.Y., Teoh, S.H., Chong, M.S., Schantz, J.T., Fisk, N.M., Choolani, M.A., and Chan, J. Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells. Stem Cells 27, 126, 2009.
32. Hsieh, J.Y., Fu, Y.S., Chang, S.J., Tsuang, Y.H., and Wang, H.W. Functional module analysis reveals differential osteogenic and stemness potentials in human mesenchymal stem cells from bone marrow and Wharton's jelly of umbilical cord. Stem Cells Dev 19, 1895, 2010.
33. Kuo, H.C., Chiu, C.C., Chang, W.C., Sheen, J.M., Ou, C.Y., Kuo, H.C., Chen, R.F., Hsu, T.Y., Chang, J.C., Hsaio, C.C., Wang, F.S., Huang, C.C., Huang, H.Y., and Yang, K.D. Use of proteomic differential displays to assess functional discrepancies and adjustments of human bone marrow-and Wharton jelly-derived mesenchymal stem cells. J Proteome Res 10, 1305, 2011.
34. Lacey, D.C., Simmons, P.J., Graves, S.E., and Hamilton, J.A. Proinflammatory cytokines inhibit osteogenic differentiation from stem cells: implications for bone repair during inflammation. Osteoarthritis Cartilage 17, 735, 2009.
35. Prasanna, S.J., Gopalakrishnan, D., Shankar, S.R., and Vasandan, A.B. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS One 5, e9016, 2010.
36. Rifas, L. T-cell cytokine induction of BMP-2 regulates human mesenchymal stromal cell differentiation and mineralization. J Cell Biochem 98, 706, 2006.
37. Rifas, L., Fausto, A., Scott, M.J., Avioli, L.V., and Welgus, H.G. Expression of metalloproteinases and tissue inhibitors of metalloproteinases in human osteoblast-like cells: differentiation is associated with repression of metalloproteinase biosynthesis. Endocrinology 134, 213, 1994.
38. Orimo, H. The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J Nippon Med Sch 77, 4, 2010.
39. Bigdeli, N., de Peppo, G.M., Lenneras, M., Sjovall, P., Lindahl, A., Hyllner, J., and Karlsson, C. Superior osteogenic capacity of human embryonic stem cells adapted to matrix-free growth compared to human mesenchymal stem cells. Tissue Eng Part A 16, 3427, 2010.
40. Marshak-Rothstein, A., and Rifkin, I.R. Immunologically active autoantigens: the role of toll-like receptors in the development of chronic inflammatory disease. Annu Rev Immunol 25, 419, 2007.
41. Baccala, R., Hoebe, K., Kono, D.H., Beutler, B., and Theofilopoulos, A.N. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med 13, 543, 2007.
42. Opitz, C.A., Litzenburger, U.M., Lutz, C., Lanz, T.V., Tritschler, I., Koppel, A., Tolosa, E., Hoberg, M., Anderl, J., Aicher, W.K., Weller, M., Wick, W., and Platten, M. Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells 27, 909, 2009.
43. Stolzing, A., Jones, E., McGonagle, D., and Scutt, A. Agerelated changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 129, 163, 2008.