Best Practice & Research Clinical Rheumatology
Volume 22, Issue 2 , Pages 269-284 , April 2008

Multipotent mesenchymal stromal cells in articular diseases

  • Christian Jorgensen

      Affiliations

    • Corresponding Author InformationCorresponding author. Inserm U844, CHU Saint Eloi, Bâtiment INM, 80 avenue Augustin Fliche, Montpellier F-34091, France.

References 

  1. Jorgensen C, Gordeladze J, Noel D. Tissue engineering through autologous mesenchymal stem cells. Current Opinion in Biotechnology. 2004;15(5):406–410
  2. Djouad F, Bony C, Haupl T, et al. Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Research & Therapy. 2005;7(6):R1304–R1315
  3. Djouad F, Delorme B, Maurice M, et al. Microenvironmental changes during differentiation of mesenchymal stem cells towards chondrocytes. Arthritis Research & Therapy. 2007;9(2):R33
  4. Djouad F, Plence P, Bony C, et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003;102(10):3837–3844
  5. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–317
  6. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell and Tissue Kinetics. 1970;3(4):393–403
  7. Gronthos S, Simmons PJ. The biology and application of human bone marrow stromal cell precursors. Journal of Hematotherapy. 1996;5(1):15–23
  8. Stolzing A, Scutt A. Age-related impairment of mesenchymal progenitor cell function. Aging Cell. 2006;5(3):213–224
  9. Ringden O, Le Blanc K. Allogeneic hematopoietic stem cell transplantation: state of the art and new perspectives. Acta Pathologica, Microbiologica, Et Immunologica Scandinavica. 2005;113(11-12):813–830
  10. Kashiwakura I, Takahashi TA. Fibroblast growth factor and ex vivo expansion of hematopoietic progenitor cells. Leukemia & Lymphoma. 2005;46(3):329–333
  11. Pittenger M, Vanguri P, Simonetti D, Young R. Adult mesenchymal stem cells: potential for muscle and tendon regeneration and use in gene therapy. Journal of Musculoskeletal & Neuronal Interactions. 2002;2(4):309–320
  12. Makino S, Fukuda K, Miyoshi S, et al. Cardiomyocytes can be generated from marrow stromal cells in vitro. The Journal of Clinical Investigation. 1999;103(5):697–705
  13. Phinney DG, Isakova I. Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system. Current Pharmaceutical Design. 2005;11(10):1255–1265
  14. Tropel P, Platet N, Platel JC, et al. Functional neuronal differentiation of bone marrow-derived mesenchymal stem cells. Stem Cells. 2006;24(12):2868–2876
  15. Bhatia R, Hare JM. Mesenchymal stem cells: future source for reparative medicine. Congestive heart failure (Greenwich, Conn.). 2005;11(2):87–91[quiz: 92–93]
  16. Yoshimura H, Muneta T, Nimura A, et al. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell and Tissue Research. 2007;327(3):449–462
  17. Awad HA, Wickham MQ, Leddy HA, et al. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials. 2004;25(16):3211–3222
  18. De Angelis L, Berghella L, Coletta M, et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. The Journal of Cell Biology. 1999;147(4):869–878
  19. Lee OK, Kuo TK, Chen WM, et al. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood. 2004;103(5):1669–1675
  20. Sottile V, Seuwen K. Bone morphogenetic protein-2 stimulates adipogenic differentiation of mesenchymal precursor cells in synergy with BRL 49653 (rosiglitazone). FEBS Letters. 2000;475(3):201–204
  21. Wakitani S, Goto T, Pineda SJ, et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. The Journal of Bone and Joint Surgery. American Volume. 1994;76(4):579–592
  22. Trippel SB, Ghivizzani SC, Nixon AJ. Gene-based approaches for the repair of articular cartilage. Gene Therapy. 2004;11(4):351–359
  23. Shao XX, Hutmacher DW, Ho ST, et al. Evaluation of a hybrid scaffold/cell construct in repair of high-load-bearing osteochondral defects in rabbits. Biomaterials. 2006;27(7):1071–1080
  24. Raghunath J, Salacinski HJ, Sales KM, et al. Advancing cartilage tissue engineering: the application of stem cell technology. Current Opinion in Biotechnology. 2005;16(5):503–509
  25. Li WJ, Tuli R, Okafor C, et al. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials. 2005;26(6):599–609
  26. Gao J, Dennis JE, Solchaga LA, et al. Repair of osteochondral defect with tissue-engineered two-phase composite material of injectable calcium phosphate and hyaluronan sponge. Tissue Engineering. 2002;8(5):827–837
  27. Frosch KH, Drengk A, Krause P, et al. Stem cell-coated titanium implants for the partial joint resurfacing of the knee. Biomaterials. 2006;27(12):2542–2549
  28. Wang DW, Fermor B, Gimble JM, et al. Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. Journal of Cellular Physiology. 2005;204(1):184–191
  29. Lefebvre V, Behringer RR, de Crombrugghe B. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis and Cartilage. 2001;9(Suppl A):S69–S75
  30. Akiyama H, Chaboissier MC, Martin JF, et al. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes & Development. 2002;16(21):2813–2828
  31. Ikeda T, Kamekura S, Mabuchi A, et al. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis & Rheumatism. 2004;50(11):3561–3573
  32. Furumatsu T, Tsuda M, Taniguchi N, et al. Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/p300 recruitment. The Journal of Biological Chemistry. 2005;280(9):8343–8350
  33. Kawakami Y, Tsuda M, Takahashi S, et al. Transcriptional coactivator PGC-1alpha regulates chondrogenesis via association with Sox9. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(7):2414–2419
  34. Murtaugh LC, Zeng L, Chyung JH, Lassar AB. The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMP-dependent axial chondrogenesis. Developmental Cell. 2001;1(3):411–422
  35. Rodrigo I, Hill RE, Balling R, et al. Pax1 and Pax9 activate Bapx1 to induce chondrogenic differentiation in the sclerotome. Development. 2003;130(3):473–482
  36. Li L, Cserjesi P, Olson EN. Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Developmental Biology. 1995;172(1):280–292
  37. Srivastava D, Cserjesi P, Olson EN. A subclass of bHLH proteins required for cardiac morphogenesis. Science. 1995;270(5244):1995–1999
  38. Wolf C, Thisse C, Stoetzel C, et al. The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Developmental Biology. 1991;143(2):363–373
  39. Bounpheng MA, Morrish TA, Dodds SG, Christy BA. Negative regulation of selected bHLH proteins by eHAND. Experimental Cell Research. 2000;257(2):320–331
  40. Spicer DB, Rhee J, Cheung WL, Lassar AB. Inhibition of myogenic bHLH and MEF2 transcription factors by the bHLH protein Twist. Science. 1996;272(5267):1476–1480
  41. Liu Y, Watanabe H, Nifuji A, et al. Overexpression of a single helix-loop-helix-type transcription factor, scleraxis, enhances aggrecan gene expression in osteoblastic osteosarcoma ROS17/2.8 cells. The Journal of Biological Chemistry. 1997;272(47):29880–29885
  42. Wilson-Rawls J, Rhee JM, Rawls A. Paraxis is a basic helix-loop-helix protein that positively regulates transcription through binding to specific E-box elements. The Journal of Biological Chemistry. 2004;279(36):37685–37692
  43. Goldring MB, Tsuchimochi K, Ijiri K. The control of chondrogenesis. Journal of Cellular Biochemistry. 2006;97(1):33–44
  44. Johnstone B, Hering TM, Caplan AI, et al. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Experimental Cell Research. 1998;238(1):265–272
  45. Barry F, Boynton RE, Liu B, Murphy JM. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Experimental Cell Research. 2001;268(2):189–200
  46. Li WG, Xu XX. The expression of N-cadherin, fibronectin during chondrogenic differentiation of MSC induced by TGF-beta(1). Chinese Journal of Traumatology. 2005;8(6):349–351
  47. Goessler UR, Bugert P, Bieback K, et al. In-vitro analysis of the expression of TGFbeta -superfamily-members during chondrogenic differentiation of mesenchymal stem cells and chondrocytes during dedifferentiation in cell culture. Cellular & Molecular Biology Letters. 2005;10(2):345–362
  48. Jin EJ, Park JH, Lee SY, et al. Wnt-5a is involved in TGF-beta3-stimulated chondrogenic differentiation of chick wing bud mesenchymal cells. International Journal of Biochemistry & Cell Biology. 2006;38(2):183–195
  49. Brunet LJ, Mc Mahon JA, Mc Mahon AP, Harland RM. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science. 1998;280:1455–1457
  50. Hills RL, Belanger LM, Morris EA. Bone morphogenetic protein 9 is a potent anabolic factor for juvenile bovine cartilage, but not adult cartilage. Journal of Orthopaedic Research. 2005;23(3):611–617
  51. Palmer GD, Steinert A, Pascher A, et al. Gene-induced chondrogenesis of primary mesenchymal stem cells in vitro. Molecular Therapy. 2005;12(2):219–228
  52. Wozney JM. The bone morphogenetic protein family and osteogenesis. Molecular Reproduction and Development. 1992;32(2):160–167
  53. Gafni Y, Pelled G, Zilberman Y, et al. Gene therapy platform for bone regeneration using an exogenously regulated, AAV-2-based gene expression system. Molecular Therapy. 2004;9(4):587–595
  54. Knippenberg M, Helder MN, Zandieh Doulabi B, et al. Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochemical and Biophysical Research. 2006;342(3):902–908
  55. Hatakeyama Y, Nguyen J, Wang X, et al. Smad signaling in mesenchymal and chondroprogenitor cells. The Journal of Bone and Joint Surgery. American Volume. 2003;85-A(Suppl. 3):13–18
  56. Chhabra A, Zijerdi D, Zhang J, et al. BMP-14 deficiency inhibits long bone fracture healing: a biochemical, histologic, and radiographic assessment. Journal of Orthopaedic Trauma. 2005;19(9):629–634
  57. Liu Z, Xu J, Colvin JS, Ornitz DM. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes & Development. 2002;16(7):859–869
  58. Enomoto-Iwamoto M, Nakamura T, Aikawa T, et al. Hedgehog proteins stimulate chondrogenic cell differentiation and cartilage formation. Journal of Bone and Mineral Research. 2000;15(9):1659–1668
  59. Davidson D, Blanc A, Filion D, et al. Fibroblast growth factor (FGF) 18 signals through FGF receptor 3 to promote chondrogenesis. The Journal of Biological Chemistry. 2005;280(21):20509–20515
  60. Mizuta H, Kudo S, Nakamura E, et al. Active proliferation of mesenchymal cells prior to the chondrogenic repair response in rabbit full-thickness defects of articular cartilage. Osteoarthritis and Cartilage. 2004;12(7):586–596
  61. Stevens MM, Marini RP, Martin I, Langer R. Prasad Shastri V. FGF-2 enhances TGF-beta1-induced periosteal chondrogenesis. Journal of Orthopaedic Research. 2004;22(5):1114–1119
  62. Baddoo M, Hill K, Wilkinson R, et al. Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. Journal of Cellular Biochemistry. 2003;89(6):1235–1249
  63. Boyden LM, Mao J, Belsky J, et al. High bone density due to a mutation in LDL-receptor-related protein 5. The New England Journal of Medicine. 2002;346(20):1513–1521
  64. Guo X, Day TF, Jiang X, et al. Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes & Development. 2004;18(19):2404–2417
  65. Church V, Nohno T, Linker C, et al. Wnt regulation of chondrocyte differentiation. Journal of Cell Science. 2002;115(Pt 24):4809–4818
  66. Rudnicki JA, Brown AM. Inhibition of chondrogenesis by Wnt gene expression in vivo and in vitro. Developmental Biology. 1997;185(1):104–118
  67. Tufan AC, Daumer KM, DeLise AM, Tuan RS. AP-1 transcription factor complex is a target of signals from both WnT-7a and N-cadherin-dependent cell-cell adhesion complex during the regulation of limb mesenchymal chondrogenesis. Experimental Cell Research. 2002;273(2):197–203
  68. Fischer L, Boland G, Tuan RS. Wnt-3A enhances bone morphogenetic protein-2-mediated chondrogenesis of murine C3H10T1/2 mesenchymal cells. The Journal of Biological Chemistry. 2002;277(34):30870–30878
  69. Hwang SG, Yu SS, Lee SW, Chun JS. Wnt-3a regulates chondrocyte differentiation via c-Jun/AP-1 pathway. FEBS Letters. 2005;579(21):4837–4842
  70. Le Blanc K, Tammik C, Rosendahl K, et al. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Experimental Hematology. 2003;31(10):890–896
  71. 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(3):389–397
  72. Potian JA, Aviv H, Ponzio NM, et al. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. Journal of Immunology (Baltimore, Md.: 1950). 2003;171(7):3426–3434
  73. 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(12):4817–4824
  74. Stagg J, Pommey S, Eliopoulos N, Galipeau J. Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood. 2006;107(6):2570–2577
  75. 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. 2002;27:27
  76. Bartholomew A, Sturgeon C, Siatskas M, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Experimental Hematology. 2002;30(1):42–48
  77. Glennie S, Soeiro I, Dyson PJ, et al. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 2005;105(7):2821–2827
  78. Corcione A, Benvenuto F, Ferretti E, et al. Human mesenchymal stem cells modulate B-cell functions. Blood. 2006;107(1):367–372
  79. Angoulvant D, Clerc A, Benchalal S, et al. Human mesenchymal stem cells suppress induction of cytotoxic response to alloantigens. Biorheology. 2004;41(3-4):469–476
  80. Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation. 2003;76(8):1208–1213
  81. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4):1815–1822
  82. Poggi A, Prevosto C, Massaro AM, et al. Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: role of NKp30 and NKG2D receptors. Journal of Immunology (Baltimore, Md. : 1950). 2005;175(10):6352–6360
  83. Maitra B, Szekely E, Gjini K, et al. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplantation. 2004;33(6):597–604
  84. 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(4):1484–1490
  85. Groh ME, Maitra B, Szekely E, Koc ON. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Experimental Hematology. 2005;33(8):928–934
  86. Le Blanc K, Tammik L, Sundberg B, et al. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scandinavian Journal of Immunology. 2003;57(1):11–20
  87. Rasmusson I. Immune modulation by mesenchymal stem cells. Experimental Cell Research. 2006;312(12):2169–2179
  88. Jiang XX, Zhang Y, Liu B, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005;105(10):4120–4126
  89. Meisel R, Zibert A, Laryea M, et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004;103(12):4619–4621
  90. Nauta AJ, Kruisselbrink AB, Lurvink E, et al. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. Journal of Immunology (Baltimore, Md. : 1950). 2006;177(4):2080–2087
  91. Krampera M, Cosmi L, Angeli R, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells. 2006;24(2):386–398
  92. 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(10):3838–3843
  93. Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005;106(5):1755–1761
  94. Plumas J, Chaperot L, Richard MJ, et al. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia. 2005;19(9):1597–1604
  95. Albina JE, Abate JA, Henry WL. Nitric oxide production is required for murine resident peritoneal macrophages to suppress mitogen-stimulated T cell proliferation. Role of IFN-gamma in the induction of the nitric oxide-synthesizing pathway. Journal of Immunology (Baltimore, Md. : 1950). 1991;147(1):144–148
  96. Sato K, Ozaki K, Oh I, et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood. 2007;109(1):228–234
  97. 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 a regulatory/suppressive phenotype. Haematologica. 2005;90(4):516–525
  98. 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(5):2214–2219
  99. Djouad F, Charbonnier LM, Bouffi C, et al. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Stem Cells. 2007;25(8):2025–2032
  100. Bartholomew A, Patil S, Mackay A, et al. Baboon mesenchymal stem cells can be genetically modified to secrete human erythropoietin in vivo. Human Gene Therapy. 2001;12(12):1527–1541
  101. 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 & Rheumatism. 2007;56(4):1175–1186
  102. Nauta AJ, Westerhuis G, Kruisselbrink AB, et al. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood. 2006;108(6):2114–2120
  103. Sudres M, Norol F, Trenado A, et al. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. Journal of Immunology (Baltimore, Md. : 1950). 2006;176(12):7761–7767
  104. 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 & Rheumatism. 2005;52(5):1595–1603
  105. Gelse K, von der Mark K, Aigner T, et al. Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis & Rheumatism. 2003;48(2):430–441
  106. Magne D, Vinatier C, Julien M, et al. Mesenchymal stem cell therapy to rebuild cartilage. Trends in Molecular Medicine. 2005;11(11):519–526
  107. Grande DA, Mason J, Light E, Dines D. Stem cells as platforms for delivery of genes to enhance cartilage repair. The Journal of Bone and Joint Surgery. American Volume. 2003;85-A(Suppl. 2):111–116
  108. Mattioli-Belmonte M, Gigante A, Muzzarelli RA, et al. N,N-dicarboxymethyl chitosan as delivery agent for bone morphogenetic protein in the repair of articular cartilage. Medical & Biological Engineering & Computing. 1999;37(1):130–134

PII: S1521-6942(08)00008-9

doi: 10.1016/j.berh.2008.01.005

Best Practice & Research Clinical Rheumatology
Volume 22, Issue 2 , Pages 269-284 , April 2008