Immunosuppression by mesenchymal stem cells: Mechanisms and clinical applications

Stem Cell Research and Therapy

Volumn 1, Issue 1, 2010, Pages

  Ghannam, Soufiane ^a,b   Bouffi, Carine ^a,b   Djouad, Farida ^a,b   Jorgensen, Christian ^a,b,c   Noël, Danièle ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c LAPEYRONIE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; GLYCOPROTEIN P 15095; HEME OXYGENASE 1; INDOLEAMINE 2,3 DIOXYGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROSTAGLANDIN E2; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ACUTE GRAFT VERSUS HOST DISEASE; ADVANCED CANCER; ALLERGIC ENCEPHALOMYELITIS; ALLOGENEIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; AUTOIMMUNITY; B LYMPHOCYTE; BREAST CANCER; CELL HOMING; CELL INTERACTION; CYTOKINE RELEASE; DIABETES MELLITUS; ENGRAFTMENT; GRAFT REJECTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; TARGET CELL; THERAPY EFFECT;

ANIMALS; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; GRAFT VS HOST DISEASE; HUMANS; IMMUNOSUPPRESSION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; NEUTROPHILS; PERIPHERAL TOLERANCE; TRANSPLANTATION IMMUNOLOGY;

EID: 77958467862     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt2     Document Type: Review

References (67)

1. Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases. Djouad F Bouffi C Ghannam S Noel D, Jorgensen C,, Nat Rev Rheumatol 2009 5 392 399 10.1038/nrrheum.2009.104 19568253
2. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. da Silva Meirelles L Chagastelles PC Nardi NB,, J Cell Sci 2006 119 2204 2213 10.1242/jcs.02932 16684817 (Pubitemid 43960310)
3. Multilineage potential of adult human mesenchymal stem cells. Pittenger MF Mackay AM, Beck SC Jaiswal RK, Douglas R Mosca JD, Moorman MA Simonetti DW, Craig S Marshak DR, Science 1999 284 143 147 10.1126/science.284.5411.143 10102814 (Pubitemid 29282067)
4. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Dominici M Le Blanc K, Mueller I Slaper-Cortenbach I, Marini F Krause D, Deans R Keating A, Prockop D Horwitz E, Cytotherapy 2006 8 315 317 10.1080/14653240600855905 16923606 (Pubitemid 44269669)
5. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Krampera M Cosmi L, Angeli R Pasini A, Liotta F Andreini A, Santarlasci V Mazzinghi B, Pizzolo G Vinante F, Romagnani P Maggi E, Romagnani S Annunziato F, Stem Cells 2006 24 386 398 10.1634/stemcells.2005- 0008 16123384 (Pubitemid 44464808)
6. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Ren G Zhang L, Zhao X Xu G, Zhang Y Roberts AI, Zhao RC Shi Y, Cell Stem Cell 2008 2 141 150 10.1016/j.stem.2007.11. 014 18371435 (Pubitemid 351181031)
7. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Polchert D Sobinsky J Douglas G Kidd M, Moadsiri A Reina E, Genrich K Mehrotra S, Setty S Smith B, Bartholomew A,, Eur J Immunol 2008 38 1745 1755 10.1002/eji.200738129 18493986
8. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Meisel R Zibert A, Laryea M Gobel U, Daubener W Dilloo D, Blood 2004 103 4619 4621 10.1182/blood-2003-11-3909 15001472 (Pubitemid 38745993)
9. Functional alteration of the lymphoma stromal cell niche by the cytokine context: role of indoleamine-2,3 dioxygenase. Maby-El Hajjami H Ame-Thomas P, Pangault C Tribut O, DeVos J Jean R, Bescher N Monvoisin C, Dulong J Lamy T, Fest T Tarte K, Cancer Res 2009 69 3228 3237 10.1158/0008-5472.CAN-08-3000 19276371
10. Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Ryan JM Barry F, Murphy JM Mahon BP, Clin Exp Immunol 2007 149 353 363 10.1111/j.1365-2249.2007.03422.x 17521318 (Pubitemid 47063057)
11. Human multipotent mesenchymal stromal cells inhibit proliferation of PBMCs independently of IFNR1 signaling and IDO expression. Gieseke F Schutt B Viebahn S Koscielniak E, Friedrich W Handgretinger R, Muller I,, Blood 2007 110 2197 2200 10.1182/blood-2007-04-083162 17522338 (Pubitemid 47443941)
12. 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. Opitz CA Litzenburger UM Lutz C Lanz TV, Tritschler I Koppel A, Tolosa E Hoberg M, Anderl J Aicher WK, Weller M Wick W, Platten M,, Stem Cells 2009 27 909 919 10.1002/stem.7 19353519
13. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Djouad F Charbonnier LM Bouffi C Louis-Plence P, Bony C Apparailly F, Cantos C Jorgensen C, Noel D,, Stem Cells 2007 25 2025 2032 10.1634/stemcells.2006-0548 17510220
14. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Ren G Su J Zhang L Zhao X, Ling W L'Huillie A, Zhang J Lu Y, Roberts AI Ji W, Zhang H Rabson AB, Shi Y,, Stem Cells 2009 27 1954 1962 10.1002/stem.118 19544427
15. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Sato K Ozaki K, Oh I Meguro A, Hatanaka K Nagai T, Muroi K Ozawa K, Blood 2007 109 228 234 10.1182/blood-2006-02-002246 16985180 (Pubitemid 46053063)
16. Human mesenchymal stem cells modulate allogeneic immune cell responses. Aggarwal S Pittenger MF, Blood 2005 105 1815 1822 10.1182/blood-2004-04-1559 15494428
17. 2-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nemeth K Leelahavanichkul A, Yuen PS Mayer B, Parmelee A Doi K, Robey PG Leelahavanichkul K, Koller BH Brown JM, Hu X Jelinek I, Star RA Mezey E, Nat Med 2009 15 42 49 10.1038/nm.1905 19098906
18. 2. Spaggiari GM Abdelrazik H, Becchetti F Moretta L, Blood 2009 113 6576 6583 10.1182/blood-2009-02-203943 19398717
19. Human mesenchymal stem cells inhibit differentiation and function of monocytederived dendritic cells. Jiang XX Zhang Y Liu B Zhang SX, Wu Y Yu XD, Mao N,, Blood 2005 105 4120 4126 10.1182/blood-2004-02-0586 15692068 (Pubitemid 40656164)
20. Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche. Raffaghello L Bianchi G, Bertolotto M Montecucco F, Busca A Dallegri F, Ottonello L Pistoia V, Stem Cells 2008 26 151 162 10.1634/stemcells.2007-0416 17932421
21. The role of IL-6 in inhibition of lymphocyte apoptosis by mesenchymal stem cells. Xu G Zhang Y Zhang L Ren G, Shi Y,, Biochem Biophys Res Commun 2007 361 745 750 10.1016/j.bbrc.2007.07.052 17678624 (Pubitemid 47238033)
22. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Di Nicola M Carlo-Stella C, Magni M Milanesi M, Longoni PD Matteucci P, Grisanti S Gianni AM, Blood 2002 99 3838 3843 10.1182/blood.V99.10.3838 11986244 (Pubitemid 34534559)
23. A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Chabannes D Hill M, Merieau E Rossignol J, Brion R Soulillou JP, Anegon I Cuturi MC, Blood 2007 110 3691 3694 10.1182/blood-2007-02-075481 17684157 (Pubitemid 350159638)
24. Leukemia inhibitory factor: role in human mesenchymal stem cells mediated immunosuppression. Nasef A Mazurier C, Bouchet S Francois S, Chapel A Thierry D, Gorin NC Fouillard L, Cell Immunol 2008 253 16 22 10.1016/j.cellimm.2008.06. 002 18639869
25. + regulatory T cells. Selmani Z Naji A, Zidi I Favier B, Gaiffe E Obert L, Borg C Saas P, Tiberghien P Rouas-Freiss N, Carosella ED Deschaseaux F, Stem Cells 2008 26 212 222 10.1634/stemcells.2007-0554 17932417
26. Selected Stro-1-enriched bone marrow stromal cells display a major suppressive effect on lymphocyte proliferation. Nasef A Zhang YZ Mazurier C Bouchet S, Bensidhoum M Francois S, Gorin NC Lopez M, Thierry D Fouillard L, Chapel A,, Int J Lab Hematol 2009 31 9 19 10.1111/j.1751-553X.2007.00997.x 19143868
27. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Djouad F Plence P, Bony C Tropel P, Apparailly F Sany J, Noel D Jorgensen C, Blood 2003 102 3837 3844 10.1182/blood-2003-04-1193 12881305 (Pubitemid 37409409)
28. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Le Blanc K Tammik L Sundberg B Haynesworth SE, Ringden O,, Scand J Immunol 2003 57 11 20 10.1046/j.1365-3083.2003.01176.x 12542793 (Pubitemid 38019084)
29. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Glennie S Soeiro I Dyson PJ Lam EW, Dazzi F,, Blood 2005 105 2821 2827 10.1182/blood-2004-09-3696 15591115 (Pubitemid 40446275)
30. Human mesenchymal stem cells promote survival of T cells in a quiescent state. Benvenuto F Ferrari S, Gerdoni E Gualandi F, Frassoni F Pistoia V, Mancardi G Uccelli A, Stem Cells 2007 25 1753 1760 10.1634/stemcells.2007-0068 17395776 (Pubitemid 47121854)
31. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Rasmusson I Ringden O, Sundberg B Le Blanc K, Transplantation 2003 76 1208 1213 10.1097/01.TP.0000082540.43730.80 14578755 (Pubitemid 37339646)
32. + regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Prevosto C Zancolli M Canevali P Zocchi MR, Poggi A,, Haematologica 2007 92 881 888 10.3324/haematol.11240 17606437 (Pubitemid 350144234)
33. Bone marrow-derived mesenchymal stem cells ameliorate autoimmune enteropathy independently of regulatory T cells. Parekkadan B Tilles AW Yarmush ML,, Stem Cells 2008 26 1913 1919 10.1634/stemcells.2007-0790 18420833
34. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Zappia E Casazza S, Pedemonte E Benvenuto F, Bonanni I Gerdoni E, Giunti D Ceravolo A, Cazzanti F Frassoni F, Mancardi G Uccelli A, Blood 2005 106 1755 1761 10.1182/blood-2005-04-1496 15905186 (Pubitemid 41208591)
35. Mesenchymal stem cells might be used to induce tolerance in heart transplantation. Zhou H Jin Z, Liu J Yu S, Cui Q Yi D, Med Hypotheses 2008 70 785 787 10.1016/j.mehy.2007.08.010 17959317 (Pubitemid 351318087)
36. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. Haniffa MA Wang XN, Holtick U Rae M, Isaacs JD Dickinson AM, Hilkens CM Collin MP, J Immunol 2007 179 1595 1604 17641026
37. Human mesenchymal stem cells modulate B-cell functions. Corcione A Benvenuto F Ferretti E Giunti D, Cappiello V Cazzanti F, Risso M Gualandi F, Mancardi GL Pistoia V, Uccelli A,, Blood 2006 107 367 372 10.1182/blood-2005-07- 2657 16141348 (Pubitemid 43053565)
38. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Tabera S Perez-Simon JA Diez-Campelo M Sanchez-Abarca LI, Blanco B Lopez A, Benito A Ocio E, Sanchez-Guijo FM Canizo C, San Miguel JF,, Haematologica 2008 93 1301 1309 10.3324/haematol.12857 18641017
39. Mesenchymal stem cells suppress B-cell terminal differentiation. Asari S Itakura S Ferreri K Liu CP, Kuroda Y Kandeel F, Mullen Y,, Exp Hematol 2009 37 604 615 10.1016/j.exphem.2009.01.005 19375651
40. Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients. Traggiai E Volpi S Schena F Gattorno M, Ferlito F Moretta L, Martini A,, Stem Cells 2008 26 562 569 10.1634/stemcells. 2007-0528 18024418 (Pubitemid 351413617)
41. +-derived and monocyte-derived dendritic cells. Nauta AJ Kruisselbrink AB Lurvink E Willemze R, Fibbe WE,, J Immunol 2006 177 2080 2087 16887966 (Pubitemid 44200965)
42. Interactions between human mesenchymal stem cells and natural killer cells. Sotiropoulou PA Perez SA Gritzapis AD Baxevanis CN, Papamichail M,, Stem Cells 2006 24 74 85 10.1634/stemcells.2004-0359 16099998
43. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Honczarenko M Le Y, Swierkowski M Ghiran I, Glodek A Silberstein LE, Stem Cells 2005 24 1030 1041 10.1634/stemcells.2005- 0319 16253981
44. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Sordi V Malosio ML, Marchesi F Mercalli A, Melzi R Giordano T, Belmonte N Ferrari G, Leone BE Bertuzzi F, Zerbini G Allavena P, Bonifacio E Piemonti L, Blood 2005 106 419 427 10.1182/blood-2004-09-3507 15784733
45. Mesenchymal stem cell homing: the devil is in the details. Karp JM Leng Teo GS, Cell Stem Cell 2009 4 206 216 10.1016/j.stem.2009.02.001 19265660
46. Safety and complications reporting on the re-implantation of culture-expanded mesenchymal stem cells using autologous platelet lysate technique. Centeno CJ Schultz JR, Cheever M Robinson B, Freeman M Marasco W, Curr Stem Cell Res Ther 2009 19951252
47. Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Tarte K Gaillard J Lataillade JJ Fouillard L, Becker M Mossafa H, Tchirkov A Rouard H, Henry C Splingard M, Dulong J Monnier D, Gourmelon P Gorin NC, Sensebe L,, Blood 2009 20032501
48. Baboon mesenchymal stem cells can be genetically modified to secrete human erythropoietin in vivo. Bartholomew A Patil S Mackay A Nelson M, Buyaner D Hardy W, Mosca J Sturgeon C, Siatskas M Mahmud N, Ferrer K Deans R, Moseley A Hoffman R, Devine SM,, Hum Gene Ther 2001 12 1527 1541 10.1089/10430340152480258 11506695 (Pubitemid 34248288)
49. Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. Casiraghi F Azzollini N Cassis P Imberti B, Morigi M Cugini D, Cavinato RA Todeschini M, Solini S Sonzogni A, Perico N Remuzzi G, Noris M,, J Immunol 2008 181 3933 3946 18768848
50. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. Koc ON Gerson SL Cooper BW Dyhouse SM, Haynesworth SE Caplan AI, Lazarus HM,, J Clin Oncol 2000 18 307 316 10637244 (Pubitemid 30056419)
51. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Nauta AJ Westerhuis G, Kruisselbrink AB Lurvink EG, Willemze R Fibbe WE, Blood 2006 108 2114 2120 10.1182/blood-2005-11-011650 16690970 (Pubitemid 44395028)
52. Immunobiology of human mesenchymal stem cells and future use in hematopoietic stem cell transplantation. Le Blanc K Ringden O, Biol Blood Marrow Transplant 2005 11 321 334 10.1016/j.bbmt.2005.01.005 15846285 (Pubitemid 40542924)
53. Cotransplantation of ex vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem-cell transplantation. Ball LM Bernardo ME, Roelofs H Lankester A, Cometa A Egeler RM, Locatelli F Fibbe WE, Blood 2007 110 2764 2767 10.1182/blood-2007-04-087056 17638847 (Pubitemid 47523204)
54. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Le Blanc K Rasmusson I Sundberg B Gotherstrom C, Hassan M Uzunel M, Ringden O,, Lancet 2004 363 1439 1441 10.1016/S0140-6736(04)16104-7 15121408 (Pubitemid 38586721)
55. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Le Blanc K Frassoni F Ball L Locatelli F, Roelofs H Lewis I, Lanino E Sundberg B, Bernardo ME Remberger M, Dini G Egeler RM, Bacigalupo A Fibbe W, Ringden O,, Lancet 2008 371 1579 1586 10.1016/S0140-6736(08)60690-X 18468541 (Pubitemid 351626841)
56. The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rate in hematologic malignancy patients: outcome of a pilot clinical study. Ning H Yang F, Jiang M Hu L, Feng K Zhang J, Yu Z Li B, Xu C Li Y, Wang J Hu J, Lou X Chen H, Leukemia 2008 22 593 599 10.1038/sj.leu.2405090 18185520 (Pubitemid 351386730)
57. Results of a pilot study on the use of third-party donor mesenchymal stromal cells in cord blood transplantation in adults. Gonzalo-Daganzo R Regidor C, Martin-Donaire T Rico MA, Bautista G Krsnik I, Fores R Ojeda E, Sanjuan I Garcia-Marco JA, Navarro B Gil S, Sanchez R Panadero N, Gutierrez Y Garcia-Berciano M, Perez N Millan I, Cabrera R Fernandez MN, Cytotherapy 2009 11 278 288 10.1080/14653240902807018 19308773
58. Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Djouad F Fritz V, Apparailly F Louis-Plence P, Bony C Sany J, Jorgensen C Noel D, Arthritis Rheum 2005 52 1595 1603 10.1002/art.21012 15880818 (Pubitemid 40663952)
59. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Augello A Tasso R Negrini SM Cancedda R, Pennesi G,, Arthritis Rheum 2007 56 1175 1186 10.1002/art.22511 17393437 (Pubitemid 46608642)
60. Immunosuppressive effects of mesenchymal stem cells in collagen-induced mouse arthritis. Mao F Xu WR Qian H Zhu W, Yan YM Shao QX, Xu HX,, Inflamm Res 2009 59 219 225 10.1007/s00011-009-0090-y 19763787
61. Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Gonzalez MA Gonzalez-Rey E Rico L Buscher D, Delgado M,, Arthritis Rheum 2009 60 1006 1019 10.1002/art.24405 19333946
62. Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. Zheng ZH Li XY Ding J Jia JF, Zhu P,, Rheumatology (Oxford) 2008 47 22 30 10.1093/rheumatology/kem284 18077486 (Pubitemid 350286256)
63. Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. Rafei M Campeau PM, Aguilar-Mahecha A Buchanan M, Williams P Birman E, Yuan S Young YK, Boivin MN Forner K, Basik M Galipeau J, J Immunol 2009 182 5994 6002 10.4049/jimmunol.0803962 19414750
64. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Sun L Akiyama K Zhang H Yamaza T, Hou Y Zhao S, Xu T Le A, Shi S,, Stem Cells 2009 27 1421 1432 10.1002/stem.68 19489103
65. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Lee RH Seo MJ Reger RL Spees JL, Pulin AA Olson SD, Prockop DJ,, Proc Natl Acad Sci USA 2006 103 17438 17443 10.1073/pnas.0608249103 17088535 (Pubitemid 44788987)
66. Mesenchymal stem cells cooperate with bone marrow cells in therapy of diabetes. Urban VS Kiss J Kovacs J Gocza E, Vas V Monostori E, Uher F,, Stem Cells 2008 26 244 253 10.1634/stemcells.2007-0267 17932424
67. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. Fiorina P Jurewicz M, Augello A Vergani A, Dada S La Rosa S, Selig M Godwin J, Law K Placidi C, Smith RN Capella C, Rodig S Adra CN, Atkinson M Sayegh MH, Abdi R, J Immunol 2009 183 993 1004 10.4049/jimmunol.0900803 19561093