Clonal analysis of multipotent stromal cells derived from CD271+ bone marrow mononuclear cells: Functional heterogeneity and different mechanisms of allosuppression

Haematologica

Volumn 98, Issue 10, 2013, Pages 1609-1616

  Kuçi, Zyrafete ^a   Seiberth, Julia ^a   Latifi Pupovci, Hatixhe ^b   Wehner, Sibylle ^a   Stein, Stefan ^c   Grez, Manuel ^c   Bönig, Halvard ^a   Köhl, Ulrike ^d   Klingebiel, Thomas ^a   Bader, Peter ^a   Kuçi, Selim ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF PRISHTINA   (Serbia)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; CD146 ANTIGEN; CD271 ANTIGEN; CELL ANTIGEN; GREEN FLUORESCENT PROTEIN; INDOLEAMINE 2, 3 DIOXYGENASE; INDOMETACIN; PROSTAGLANDIN E2; UNCLASSIFIED DRUG;

ADIPOCYTE; ALLOTYPE SUPPRESSION; ARTICLE; BONE MARROW CELL; CARTILAGE CELL; CELL CLONE; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONAL EVOLUTION; FLUORESCENCE ACTIVATED CELL SORTING; GENE DUPLICATION; GENETIC HETEROGENEITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOMAGNETIC SEPARATION; IMMUNOSUPPRESSIVE TREATMENT; MESENCHYMAL STROMA CELL; MICROSCOPY; MIXED LYMPHOCYTE REACTION; MONONUCLEAR CELL; NORMAL HUMAN; OSTEOBLAST;

BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; HUMANS; IMMUNE TOLERANCE; LEUKOCYTES, MONONUCLEAR; MULTIPOTENT STEM CELLS; NERVE TISSUE PROTEINS; RECEPTORS, NERVE GROWTH FACTOR; STROMAL CELLS;

EID: 84884936600     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2013.092700     Document Type: Article

References (32)

1. Phinney DG. Functional heterogeneity of mesenchymal stem cells: implications for cell therapy. J Cell Biochem. 2012;113(9):2806-12.
2. Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci. 2000;113(Pt 7):1161-6.
3. Lee CC, Christensen JE, Yoder MC, Tarantal AF. Clonal analysis and hierarchy of human bone marrow mesenchymal stem and progenitor cells. Exp Hematol. 2010;38(1):46-54.
4. Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O'Connor KC. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells. 2010;28(4):788-98.
5. Okamoto T, Aoyama T, Nakayama T, Nakamata T, Hosaka T, Nishijo K, et al. Clonal heterogeneity in differentiation potential of immortalized human mesenchymal stem cells. Biochem Biophys Res Commun. 2002;295(2):354-61.
6. Guilak F, Lott KE, Awad HA, Cao Q, Hicok KC, Fermor B, et al. Clonal analysis of the differentiation potential of human adiposederived adult stem cells. J Cell Physiol. 2006;206(1):229-37.
7. Mareddy S, Crawford R, Brooke G, Xiao Y. Clonal isolation and characterization of bone marrow stromal cells from patients with osteoarthritis. Tissue Eng. 2007; 13(4):819-29.
8. Kuci Z, Kuci S, Zircher S, Koller S, Schubert R, Bonig H, et al. Mesenchymal stromal cells derived from CD271(+) bone marrow mononuclear cells exert potent allosuppressive properties. Cytotherapy. 2011; 13(10):1193-204.
9. Kuci S, Kuci Z, Kreyenberg H, Deak E, Putsch K, Huenecke S, et al. CD271 antigen defines a subset of multipotent stromal cells with immunosuppressive and lymphohematopoietic engraftment-promoting properties. Haematologica. 2010;95(4):651-9.
10. Kumar S, Malachowski WP, DuHadaway JB, LaLonde JM, Carroll PJ, Jaller D, et al. Indoleamine 2,3-dioxygenase is the anticancer target for a novel series of potent naphthoquinone-based inhibitors. J Med Chem. 2008;51(6):1706-18.
11. Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8(4):315-7.
12. Hanagata N, Li X. Osteoblast-enriched membrane protein IFITM5 regulates the association of CD9 with an FKBP11-CD81-FPRP complex and stimulates expression of interferon-induced genes. Biochem Biophys Res Commun. 2011;409(3):378-84.
13. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells. 2004;22(3):377-84.
14. Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C, Deliliers GL. Isolation of bone marrow mesenchymal stem cells by antinerve growth factor receptor antibodies. Exp Hematol. 2002;30(7):783-91.
15. Poloni A, Maurizi G, Rosini V, Mondini E, Mancini S, Discepoli G, et al. Selection of CD271(+) cells and human AB serum allows a large expansion of mesenchymal stromal cells from human bone marrow. Cytotherapy. 2009;11(2):153-62.
16. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res. 2006;312(12):2169-79.
17. Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol. 2006; 36(10):2566-73.
18. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110(10):3499-506.
19. 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(10):3838-43.
20. LeBlanc K, Rasmusson I, Gotherstrom C, Seidel C, Sundberg B, Sundin M, et al. Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes. Scand J Immunol. 2004; 60(3):307-15.
21. 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-dioxygenasemediated tryptophan degradation. Blood. 2004;103(12):4619-21.
22. 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(1):33-41.
23. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4): 1815-22.
24. 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(19):3109-23.
25. Najar M, Raicevic G, Boufker HI, Fayyad KH, De Bruyn C, Meuleman N, et al. 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(2):171-9.
26. Selmani Z, Naji A, Gaiffe E, Obert L, Tiberghien P, Rouas-Freiss N, et al. HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation. 2009;87(9 Suppl):S62-S66.
27. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood. 2007; 109(1):228-34.
28. Maccario R, Podesta M, Moretta A, Cometa A, Comoli P, Montagna D, et al. 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(4):516-25.
29. 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(7):3426-34.
30. Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 2005; 105(5):2214-9.
31. Xu G, Zhang L, Ren G, Yuan Z, Zhang Y, Zhao RC, et al. Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Res. 2007;17(3):240-8.
32. Gieseke F, Schutt B, Viebahn S, Koscielniak E, Friedrich W, Handgretinger R, et al. Human multipotent mesenchymal stromal cells inhibit proliferation of PBMCs independently of IFNgammaR1 signaling and IDO expression. Blood. 2007;110(6):2197-200.