Anti-inflammatory role and immunomodulation of mesenchymal stem cells in systemic joint diseases: Potential for treatment

Expert Opinion on Therapeutic Targets

Volumn 17, Issue 3, 2013, Pages 243-254

  MacFarlane, Robert J ^a   Graham, Simon Matthew ^a   Davies, Peter S E ^a   Korres, Nectarios ^b   Tsouchnica, Helen ^b   Heliotis, Manolis ^b   Mantalaris, Athanasios ^c,d   Tsiridis, Eleftherios ^b,c  

^a ROYAL LIVERPOOL UNIVERSITY HOSPITAL   (United Kingdom)

^b ARISTOTLE UNIVERSITY MEDICAL SCHOOL   (Greece)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d Division of Surgery   (United Kingdom)

Author keywords

Autoimmune disease; Mesenchymal stem cells; Osteoarthritis; Rheumatoid arthritis; Tumor necrosis factor

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ANTIINFLAMMATORY ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTHROPATHY; B LYMPHOCYTE ACTIVATION; CARTILAGE CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CHONDROGENESIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; IMMUNOMODULATION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; OSTEOARTHRITIS; OSTEOCYTE; PATHOPHYSIOLOGY; PERIARTICULAR JOINT DISEASE; PLURIPOTENT STEM CELL; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION;

ANIMALS; ARTHRITIS; HUMANS; IMMUNOMODULATION; MESENCHYMAL STROMAL CELLS;

EID: 84873900026     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2013.746954     Document Type: Review

References (102)

1. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;2:143-7
2. Roberts S, Genever P, McCaskie A, De Bari C. Prospects of stem cell therapy in osteoarthritis. Regen Med 2011;6(3):351-66
3. Wakitani S, Goto T, Pineda SJ, et al. Mesenchymal cell-based repair of large, full thickness defects in articular cartilage. J Bone Joint Surg Am 1994;76:579-92
4. Lazarus HM, Haynesworth SE, Gerson SL, et al. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant 1995;16:557-64
5. De Bari C, Dell'Accio F, Vandenabeele F, et al. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 2003;160:909-18
6. Jones EA, English A, Henshaw K, et al. Enumeration and phenotypic characterisation of synovial fluid multipotential mesenchymal stem cells in inflammatory and degenerative arthritis. Arthritis Rheum 2004;50:315-17
7. Dowthwaite GP, Bishop JC, Redman SN, et al. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 2004;117:889-97
8. English A, Jones EA, Corscadden D, et al. A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteoarthritis. Rheumatology 2007;46:1676-16
9. De Bari C, Dell'Accio F, Vanlauwe J, et al. Mesenchymal multipotency of adult human periostial cells demonstrated by single cell lineage analysis. Arthritis Rheum 2006;54:1209-21
10. Mohanty ST, Kottam L, Gambardella A, et al. Alterations in the self renewal and differentiation ability of bone marrow mesenchymal stem cells in a mouse model of rheumatoid arthritis. Arthritis Res Ther 2010;12:R149
11. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cell 2001;19:180-92
12. Yagi H, Soto-Gutierrez A, Parekkadan B, et al. Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplant 2010;9:667-9
13. Stute N, Hiltz K, Bubenheim M, et al. Autologous serum for isolation and expansion of human mesenchymal stem cells for clinical use. Exp Haematol 2004;32:1212-25
14. Lange C, Cakiroglu F, Spless AN, et al. Accelerated and safe expansion of human mesenchymal stromal cells in animal-serum free medium for transplantation and regenerative medicine. J cell Physiol 2007;213:18-26
15. Carrancio S, Lopez-Holgado N, Sanchez-Guilo FM, et al. Optimization of mesenchymal stem cell expansion procedures by cell separation and culture condition modification. Exp Haematol 2008;36:1014-21
16. Pittenger M, Vanguri P, Simonetti D, Young R. Adult mesenchymal stem cells: potential for muscle and tendon regeneration and use in gene therapy. J Musculoskelet Neuronal Interact 2002;2:309-20
17. Simmons PJ, Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 1991;78:55-62
18. Da Silva ML, Chagatelles PC, Nardi NB. Mesenchymal stem cells reside in almost all post-natal organs and tissues. J Cell Sci 2006;119:2204-13
19. Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008;3:301-13
20. Slack JMW. Stem cells in Epithelial tissues. Science 2000;287:1431
21. Salingcarnboriboon R, Yoshitake H, Tsuji K, et al. Establishment of tendon-derived cell lines exhibiting pluripotent mesenchymal stem cell-like property. Exp Cell Res 2003;287:289-300
22. Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004;364:149-55
23. Sabatini F, Petecchia L, Tavian M, et al. Human bronchial fibroblasts exhibit a mesenchymal stem cell phenotype and multilineage differentiating potentialities. Lab Invest 2005;85:962-71
24. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003;18:696-704
25. Anjos-Afonso F, Siapati EK, Bonnet D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J Cell Sci 2004;117:5655-64
26. Campagnoli C, Roberts IA, Kumar S, et al. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001;98:2396-402
27. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 2003;102:1548-9
28. In 't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004;22:1338-45
29. In't Anker PS, Noort WA, Scherjon SA, et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 2003;88:845-52
30. Hu Y, Liao L, Wang Q, et al. Isolation and identification of mesenchymal stem cells from human fetal pancreas. J Lab Clin Med 2003;141:342-9
31. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000;109:235-42
32. Mareschi K, Biasin E, Piacibello W, et al. Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Haematologica 2001;86:1099-100
33. Ilancheran S, Moodley Y, Manuelpillai U. Human fetal membranes: a source of stem cells for human tissue regeneration and repair? Placenta 2009;30:2-10
34. Fickert S, Fielder J, Brenner RE. Identification, quantification and isolation of mesenchymal progenitor cells from osteoarthritic synovium by fluorescence automated cell sorting. Osteoarthritis Cartilage 2003;11:790-800
35. Jorgensen C, Djouad F, Bouffi C, et al. Multipotent mesenchymal stromal cells in articular diseases. Best Pract Res Clin Rheumatol 2008;22:269-84
36. Jones EA, Kinsey SE, English A, et al. Isolation and characterisation of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 2002;46:3349-60
37. Sachetti B, Funari A. Michienzi, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organise a haematopoietic microenvironment. Cell 2007;131:324-36
38. Majumdar MK, Keane-Moore M, Buyaner D, et al. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci 2003;10:228-41
39. Le Blanc K, Tammik L, Sundberg B, et al. Mesenchymal stem cells inhibit 55. and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003;57:11-20
40. Djouad F, Bony C, Haupl T, et al. Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res Ther 2005;7:1304-15
41. Noel D, Caton D, Roche S, et al. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp Cell Res 2008;314:1575-84
42. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res 2007;100:1249-60
43. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell based therapies. Tissue Eng 2001;72:211-28
44. Frith J, Genever P. Transcriptional control of mesenchymal stem cell differentiation. Transf Med Hemother 2008;35:216-27
45. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 1997;64:295-312
46. Zhou G, Zheng Q, Engin F, et al. Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc Natl Acad Sci USA 2006;103:19004-9
47. Cheng A, Genever PG. SOX9 determines RUNX transactivity by directing intracellular degradation. J Miner Res 2010;25(12):2404-13
48. de Crombrugghe B, Lefebvre V, Behringer RR, et al. Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 2000;19:389-94
49. Ren G, Zhiang L, Zhao X, et al. Mesenchymal stem cell mediated immunosuppression occurs via concerted interaction of chemokines and nitric oxide. Cell Stem Cell 2008;2:141-50
50. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or non-specific mitogenic stimuli. Blood 2002;99:3838-43
51. Le Blanc K, Rasmusson I, Gotherstrom C, et al. Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2-receptor) and CD38 on phytohaemagglutinin-activiated lymphocytes. Scand J Imunol 2004;60:307-15
52. Maccario R, Podesta M, Moretta A, 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 regulatory/suppressive phenotype. Haematologica 2005;90:516-25
53. Mougiakakos D, Jitschin R, Johansson CC, et al. The impact of inflammatory licensing on heme oxygenase-1-mediated induction of regulatory T cells by human mesenchymal stem cells. Blood 2011;117:4826-35
54. Ghannam S, Pene J, Torcy-Moquet G, et al. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 2010;185:302-12
55. Bouffi C, Djouad F, Mathieu M, et al. Mulitpotent mesenchymal stromal cells and rheumatoid arthritis: risk or benefit? Rheumatology 2009;49:1185-9
56. Selmani Z, Naji A, Zidi I, 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 Cell 2008;26:212-22
57. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res 2006;312:2169-79
58. Liu CH, Hwang SM. Cytokine interactions in mesenchymal stem cells from cord blood. Cytokine 2005;32:270-9
59. Pevsner-Fischer M, Morad V, Cohen-Svady M, et al. Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood 2007;109:1422-43
60. Tomchuck SL, Zwezdaryk KJ, Coffelt SB, et al. Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cell 2008;26:99-107
61. Chen L, Zhang W, Yue H, et al. Effects of human mesenchymal stem cells on the differentiation of dendritic stem cells from CD34+ cells. Stem Cells Dev 2007;16:719-31
62. Jiang XX, Zhang Y, Liu B. Human mesenchymal stem cells inhibit differentiation and function of monocyte derived dendritic cells. Blood 2005;105:4120-6
63. Nauta AJ, Kruisselbrink AB, Lurvink E, et al. Mesenchymal stem cells inhibit generation and function of both CD34 +-derived and monocyte derived dendritic cells. J Immunol 2006;177:2080-7
64. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-22
65. Corcione A, Benvenuto F, Ferretti E, et al. Human mesenchymal stem cells modulate B cell functions. Blood 2006;107:367-72
66. Abdelrazik H, Spaggiari GM, Chiossone L, Moretta L. Mesenchymal stem cells expanded in human platelet lysate display a decreased inhibitory capacity on T-and NK-cell proliferation and function. Eur J Immunol 2011;41:3281-90
67. Spaggiari GM, Capobianco A, Abdelrazik H, et al. 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
68. Spaggiari GM, Capobianco A, Becchetti S, et al. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006;107:1484-90
69. Sotiropoulou PA, Perez SA, Gritzapis AD, et al. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006;24:74-85
70. 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
71. English K, Barry FP, Field-Corbett CP, Mahon BP. IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett 2007;110:91-100
72. Tse WT, Pendleton JD, Beyer WM, et al. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003;75:389-97
73. 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;101:3722-9
74. Hemeda H, Jakob M, Ludwig AK. Interferon-gamma and tumor necrosis factor-alpha differentially affect cytokine expression and migration properties of mesenchymal stem cells. Stem Cells Dev 2010;19:693-706
75. Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS ONE 2010;5:e9016
76. Chan JL, Tang KC, Patel AP, 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
77. Sheng H, Wang Y, Jin Y, et al. A critical role of IFNgamma in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Res 2008;18:846-57
78. Alsalameh S, Amin R, Gemba T, Lotz M. Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis Rheum 2004;50:1522-32
79. Murphy JM, Dixon K, Beck S, et al. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum 2002;46:704-13
80. Pretzel D, Linss S, Rochler S, et al. Relative percentage and zonal distribution of mesenchymal progenitor cells in human osteoarthritic and normal cartilage. Arthritis Res Ther 2011;13:R64
81. Koelling S, Kruegel L, Imer M, et al. Migratory chondrogenic progenitor cells from repair tissue during the later stages of human osteoarthritis. Cell Stem Cell 2009;4:324-35
82. Mor A, Abramson SB, Pillinger MH. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clin Immunol 2005;115:118-28
83. Fox DA. The role of T cells in the immunopathogenesis of rheumatoid arthritis: new perspectives. Arthritis Rheum 1997;40:598-609
84. Papadaki HA, Kritikos HD, Gemetzi C, et al. Bone marrow progenitor cell reserve and function and stromal cell function are defective in rheumatoid arthritis: evidence for a tumor necrosis factor alpha-mediated effect. Blood 2002;99:1610-19
85. Marinova-Mutafchieva L, Williams RO, Funa K, et al. Inflammation is preceded by tumor necrosis factor-dependent infiltration of mesenchymal cells in experimental arthritis. Arthritis Rheum 2002;46:507-13
86. Morimoto D, Kuroda S, Kizawa T, et al. Equivalent osteoblastic differentiation function of human mesenchymal stem cells from rheumatoid arthritis in comparison with osteoarthritis. Rheumatology 2009;48:643-9
87. Skalska U, Kontny E, Prochorec-Sobieszek M, Maslinski W. Intra-articular adipose-derived mesenchymal stem cells from rheumatoid arthritis patients maintain the function of chondrogenic differentiation. Rheumatology 2012. [Epub ahead of print]
88. Yanez R, Lamana ML, Garcia-Castro J, et al. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006;24:2582-91
89. Ho JH, Tseng TC, Ma WH, et al. Multiple intravenous transplantations of mesenchymal stem cells effectively restore long-term blood glucose homeostasis by hepatic enlargement and beta cell differentiation in streptozosin induced diabetic mice. Cell Transplant 2011. [Epub ahead of print]
90. Choi EW, Shin IS, Park SY, et al. Reversal of serologic, immunologic, and histologic dysfunction in mice with systemic lupus erythematosus by long-term serial adipose tissue-derived mesenchymal stem cell transplantation. Arthritis Rheum 2012;64:243-53
91. Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005;106:1755-61
92. Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for the treatment of steroid resistant, severe, acute, graft versus host disease: a phase II study. Lancet 2008;371:1579-86
93. Djouad F, Fritz V, Apparailly F, et al. Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum 2005;52:1595-603
94. Augello A, Tasso R, Negrini SM, et al. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007;56:1175-86
95. Zhou B, Yuan Z, Zhou Y, et al. Administering human adipose derived mesenchymal stem cells to prevent and treat experimental arthritis. Clin Immunol 2011;141:328-37
96. Choi JJ, Yoo SA, Park SJ, et al. Mesenchymal stem cells overexpressing interleukin-10 attenuate collagen-induced arthritis in mice. Clin Exp Immunol 2008;153:269-76
97. Ra JC, Kang SK, Shin IS, et al. Stem cell treatment for patients with autoimmune disease by systemic infusion of culture-expanded autologous adipose tissue derived mesenchymal stem cells. J Transl Med 2011;21:181
98. Ra JC, Shin IS, Kim SH, et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cell Dev 2011;20:1297-308
99. Bhosale AM, Kuiper JH, Johnson WE, et al. Mid-term to long-term longitudinal outcome of autologous chondrocyte implantation in the knee joint: a multilevel analysis. Am J Sports Med 2009;37:131S-8S
100. Park SH, Park SR, Chung SI, et al. Tissue-engineered cartilage using fibrin/hyaluronan composite gel and its in vivo implantation. Artif Organs 2005;29:838-45
101. Shi J, Zhang X, Zeng X, et al. One-step articular cartilage repair: combination of in situ bone marrow stem cells with cell-free poly(L-lactic-co-glycolic acid) in a rabbit model. Orthopaedics 2012;35:e665-71
102. Koh YG, Choi YJ. Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis. Knee 2012. [Epub ahead of print]