Mesenchymal stromal cells in rheumatoid arthritis: Biological properties and clinical applications

Current Stem Cell Research and Therapy

Volumn 4, Issue 1, 2009, Pages 61-69

  Kastrinaki, Maria Christina ^a   Papadaki, Helen A ^a  

^a UNIVERSITY OF CRETE   (Greece)

Author keywords

Autoimmune diseases; Bone marrow; Mesenchymal stromal cells (MSCs); Rheumatoid arthritis; Tissue regeneration

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; TUMOR NECROSIS FACTOR ALPHA;

ANTIINFLAMMATORY ACTIVITY; BONE REMODELING; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; FIBROBLAST LIKE SYNOVIOCYTE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOREGULATION; INFLAMMATION; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOCYTE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYNOVIOCYTE; TISSUE REPAIR; ANIMAL; ARTHRITIS; BONE REGENERATION; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; STEM CELL TRANSPLANTATION; STROMA CELL; TISSUE ENGINEERING;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; BONE REGENERATION; CELL DIFFERENTIATION; HUMANS; IMMUNOSUPPRESSION; INFLAMMATION; MESENCHYMAL STEM CELLS; MICE; OSTEOCYTES; STEM CELL TRANSPLANTATION; STROMAL CELLS; TISSUE ENGINEERING;

EID: 67849121971     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157488809787169084     Document Type: Review

References (131)

1. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976; 4: 267-74.
2. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001; 44: 1928-42.
3. Jones EA, English A, Henshaw K, et al. Enumeration and phenotypic characterization of synovial fluid multipotential mesenchymal progenitor cells in inflammatory and degenerative arthritis. Arthritis Rheum 2004; 50: 817-27.
4. Bosch P, Musgrave DS, Lee JY, et al. Osteoprogenitor cells within skeletal muscle. J Orthop Res 2000; 18: 933-44.
5. 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.
6. Dell'Accio F, De Bari C, Luyten FP. Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Exp Cell Res 2003; 287: 16-27.
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. Nakahara H, Goldberg VM, Caplan AI. Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo. J Orthop Res 1991; 9: 465-76.
9. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7: 211-28.
10. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13: 4279-95.
11. Fukuchi Y, Nakajima H, Sugiyama D, Hirose I, Kitamura T, Tsuji K. Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 2004; 22: 649-58.
12. Roubelakis MG, Pappa KI, Bitsika V, et al. Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cells. Stem Cells Dev 2007; 16: 931-52.
13. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004; 103: 1669-75.
14. Lu LL, Liu YJ, Yang SG, et al. Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 2006; 91: 1017-26.
15. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000; 109: 235-42.
16. Martin-Rendon E, Watt SM. Stem cell plasticity. Br J Haematol 2003; 122: 877-91.
17. Zipori D. The stem state: mesenchymal plasticity as a paradigm. Curr Stem Cell Res Ther 2006; 1: 95-102.
18. Owen M. Marrow stromal cells. J Cell Sci Suppl 1985; 10: 63-76.
19. Gronthos S, Simmons PJ. The biology and application of human bone marrow stromal cell precursors. J Hematother 1996; 5: 15-23.
20. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001; 19: 180-92.
21. Delorme B, Charbord P. Culture and characterisation of human bone marrow mesenchymal stem cells. In Hauser H, Fussenegger M, Eds. Methods in molecular medicine, 2nd edn: Tissue Eng. Totowa, New Jersey, USA: Humana Press Inc., 2007, 67-81.
22. Gronthos S, Simmons PJ. The growth factor requirements of STRO-1-positive human bone marrow stromal precursors under serum-deprived conditions in vitro. Blood 1995; 85: 929-40.
23. 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.
24. Haynesworth SE, Baber MA, Caplan AI. Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 1992; 13: 69-80.
25. Barry F, Boynton R, Murphy M, Haynesworth S, Zaia J. The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun 2001; 289: 519-24.
26. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997; 276: 71-4.
27. Conget PA, Minguell JJ. Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol 1999; 181: 67-73.
28. Bruder SP, Ricalton NS, Boynton RE, et al. Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res 1998; 13: 655-63.
29. Xu W, Zhang X, Qian H, et al. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med (Maywood.) 2004; 229: 623-31.
30. Delorme B, Ringe J, Gallay N, et al. Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 2008; 111: 2631-5.
31. Baddoo M, Hill K, Wilkinson R, et al. Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. J Cell Biochem 2003; 89: 1235-49.
32. Jones EA, Kinsey SE, English A, et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 2002; 46: 3349-60.
33. Quirici N, Soligo D, Bossolasco P, Servida F, Lumini C, Deliliers GL. Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 2002; 30: 783-91.
34. Gang EJ, Bosnakovski D, Figueiredo CA, Visser JW, Perlingeiro RCR. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 2008; 109: 1743-51.
35. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-7.
36. Krampera M, Pizzolo G, Aprili G, Franchini M. Mesenchymal stem cells for bone, cartilage, tendon and skeletal muscle repair. Bone 2006; 39: 678-83.
37. 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.
38. Kastrinaki MC, Sidiropoulos P, Roche S, et al. Functional, molecular and proteomic characterisation of bone marrow mesenchymal stem cells in rheumatoid arthritis. Ann Rheum Dis 2008; 67: 741-9.
39. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841-6.
40. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425: 836-41.
41. Dazzi F, Ramasamy R, Glennie S, Jones SP, Roberts I. The role of mesenchymal stem cells in haemopoiesis. Blood Rev 2006; 20: 161-71.
42. Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 2004; 36: 568-84.
43. Otto WR, Rao J. Tomorrow's skeleton staff: mesenchymal stem cells and the repair of bone and cartilage. Cell Prolif 2004; 37: 97-110.
44. Panayi GS, Corrigall VM, Pitzalis C. Pathogenesis of rheumatoid arthritis. The role of T cells and other beasts. Rheum Dis Clin North Am 2001; 27: 317-34.
45. Gabriel SE, Crowson CS, Kremers HM, et al. Survival in rheumatoid arthritis: a population-based analysis of trends over 40 years. Arthritis Rheum 2003; 48: 54-8.
46. Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 2001; 344: 907-16.
47. Elliot MJ, Maini RN, Feldmann M, et al. Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to tumor necrosis factor alpha. Arthritis Rheum 2008; 58: S92-S101.
48. Feldmann M, Maini SR. Role of cytokines in rheumatoid arthritis: an education in pathophysiology and therapeutics. Immunol Rev 2008; 223: 7-19.
49. Ando W, Tateishi K, Hart DA, et al. Cartilage repair using an in vitro generated scaffold-free tissue-engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials 2007; 28: 5462-70.
50. De Bari C, Dell'Accio F. Mesenchymal stem cells in rheumatology: a regenerative approach to joint repair. Clin Sci 2007; 113: 339-48.
51. Dazzi F, van Laar JM, Cope A, Tyndall A. Cell therapy for autoimmune diseases. Arthritis Res Ther 2007; 9: 206.
52. Ando W, Tateishi K, Katakai D, et al. In vitro generation of a scaffold-free tissue-engineered construct (tec) derived from human synovial mesenchymal stem cells: biological and mechanical properties, and further chondrogenic potential. Tissue Eng Part A 2008; 14(12): 2041-49.
53. Yoshikawa H, Myoui A. Bone tissue engineering with porous hydroxyapatite ceramics. J Artif Organs 2005; 8: 131-6.
54. Shi K, Hayashida K, Hashimoto J, Sugamoto K, Kawai H, Yoshikawa H. Hydroxyapatite augmentation for bone atrophy in total ankle replacement in rheumatoid arthritis. J Foot Ankle Surg 2006; 45: 316-21.
55. Watanabe J, Kashii M, Hirao M, et al. Quick-forming hydroxyapatite/agarose gel composites induce bone regeneration. J Biomed Mater Res A 2007; 83: 845-52.
56. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005; 23: 47-55.
57. Marinova-Mutafchieva L, Taylor P, Funa K, Maini RN, Zvaifler NJ. Mesenchymal cells expressing bone morphogenetic protein receptors are present in the rheumatoid arthritis joint. Arthritis Rheum 2000; 43: 2046-55.
58. Marinova-Mutafchieva L, Williams RO, Funa K, Maini RN, Zvaifler NJ. Inflammation is preceded by tumor necrosis factor-dependent infiltration of mesenchymal cells in experimental arthritis. Arthritis Rheum 2002; 46: 507-13.
59. Rattis FM, Voermans C, Reya T. Wnt signaling in the stem cell niche. Curr Opin Hematol 2004; 11: 88-94.
60. Boland GM, Perkins G, Hall DJ, Tuan RS. Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J Cell Biochem 2004; 93: 1210-30.
61. Sheldahl LC, Park M, Malbon CC, Moon RT. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a Gprotein-dependent manner. Curr Biol 1999; 9: 695-8.
62. Sen M, Lauterbach K, El-Gabalawy H, Firestein GS, Corr M, Carson DA. Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc Natl Acad Sci USA 2000; 97: 2791-6.
63. Li X, Makarov SS. An essential role of NF-kappaB in the "tumor-like" phenotype of arthritic synoviocytes. Proc Natl Acad Sci USA 2006; 103: 17432-7.
64. Corr M, Zvaifler NJ. Mesenchymal precursor cells. Ann Rheum Dis 2002; 61: 3-5.
65. 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: 1610-9.
66. Papadaki HA, Kritikos HD, Valatas V, Boumpas DT, Eliopoulos GD. Anemia of chronic disease in rheumatoid arthritis is associated with increased apoptosis of bone marrow erythroid cells: improvement following anti-tumor necrosis factor-alpha antibody therapy. Blood 2002; 100: 474-82.
67. Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum 2002; 46: 704-13.
68. Schonland SO, Lopez C, Widmann T, et al. Premature telomeric loss in rheumatoid arthritis is genetically determined and involves both myeloid and lymphoid cell lineages. Proc. Natl Acad Sci USA 2003; 100: 13471-6.
69. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003; 31: 890-6.
70. Le Blanc K. Mesenchymal stromal cells: Tissue repair and immune modulation. Cytotherapy 2006; 8: 559-61.
71. Noel D, Djouad F, Bouffi C, Mrugala D, Jorgensen C. Multipotent mesenchymal stromal cells and immune tolerance. Leuk Lymphoma 2007; 48: 1283-9.
72. Patel SA, Sherman L, Munoz J, Rameshwar P. Immunological properties of mesenchymal stem cells and clinical implications. Arch Immunol Ther Exp (Warsz.) 2008; 56: 1-8.
73. Glennie S, Soeiro I, Dyson PJ, Lam EWF, Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005; 105: 2821-7.
74. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105: 1815-22.
75. Beyth S, Borovsky Z, Mevorach D, et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce Tcell unresponsiveness. Blood 2005; 105: 2214-9.
76. Jiang XX, Zhang Y, Liu B, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005; 105: 4120-6.
77. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 2006; 177: 2080-7.
78. 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-dioxygenase-mediated tryptophan degradation. Blood 2004; 103: 4619-21.
79. Ryan JM, Barry FP, Murphy JM, Mahon BP. Mesenchymal cells avoid allogeneic rejection. J Inflamm (Lond) 2005; 2: 8.
80. 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: 228-34.
81. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003; 75: 389-97.
82. Zheng ZH, Li XY, Ding J, Jia JF, Zhu P. Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. Rheumatology 2008; 47: 22-30.
83. 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: 386-98.
84. Romieu-Mourez R, Francois M, Boivin MN, Stagg J, Galipeau J. Regulation of MHC class II expression and antigen processing in murine and human mesenchymal stromal cells by IFN-gamma, TGF-beta, and cell density. J Immunol 2007; 179: 1549-58.
85. 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.
86. 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.
87. 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.
88. Bocelli-Tyndall C, Bracci L, Spagnoli G, et al. Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and autoimmune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro. Rheumatology 2007; 46: 403-8.
89. Shapiro F, Koide S, Glimcher MJ. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 1993; 75: 532-53.
90. Filipak M, Sparks RL, Tzen CY, Scott RE. Tumor necrosis factor inhibits the terminal event in mesenchymal stem cell differentiation. J Cell Physiol 1988; 137: 367-73.
91. Sitcheran R, Cogswell PC, Baldwin AS. Jr. NF-kappaB mediates inhibition of mesenchymal cell differentiation through a posttranscriptional gene silencing mechanism. Genes Dev 2003; 17: 2368-73.
92. Suzawa M, Takada I, Yanagisawa J, et al. Cytokines suppress adipogenesis and PPAR-gamma function through the TAK1/TAB1/NIK cascade. Nat Cell Biol 2003; 5: 224-30.
93. Lukic IK, Grcevic D, Kovacic N, et al. Alteration of newly induced endochondral bone formation in adult mice without tumour necrosis factor receptor 1. Clin Exp Immunol 2005; 139: 236-44.
94. Okuma-Yoshioka C, Seto H, Kadono Y, et al. Tumor necrosis factor-alpha inhibits chondrogenic differentiation of synovial fibroblasts through p38 mitogen activating protein kinase pathways. Mod Rheumatol 2008; 18(4): 366-78.
95. Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007; 13: 156-63.
96. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C. Canonical Wnt/ beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 2005; 8: 727-38.
97. Day TF, Guo X, Garrett-Beal L, Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 2005; 8: 739-50.
98. Djouad F, Delorme B, Maurice M, et al. Microenvironmental changes during differentiation of mesenchymal stem cells towards chondrocytes. Arthritis Res Ther 2007; 9: R33.
99. Bu R, Borysenko CW, Li Y, Cao L, Sabokbar A, Blair HC. Expression and function of TNF-family proteins and receptors in human osteoblasts. Bone 2003; 33: 760-70.
100. Papadaki HA, Vlahava VM, Kastrinaki MC, Damianaki A, Gemetzi C, Eliopoulos GD. Study of apoptosis and expression pattern of the TNF Receptor Family members in human bone marrow mesenchymal cells. Haematologica Hematol J 2007; 92(s1):358 (abstract 0962).
101. Evans CH, Ghivizzani SC, Gouze E, Rediske JI, Schawarz EM. The 3rd International Meeting on Gene Therapy in Rheumatology and Orthopaedics. Arthritis Res Ther 2005; 7: 273-8.
102. Kumar S, Nagy TR, Ponnazhagan S. Ex vivo mesenchymal stem cell therapy with raav2 encoding bmp-2 enhances bone regeneration in ovariectomized mouse model. Mol Ther 2006; 13: S219.
103. Wang JC, Kanim LEA, Yoo S, Campbell PA, Berk AJ, Lieberman JR. Effect of regional gene therapy with bone morphogenetic protein-2-producing bone marrow cells on spinal fusion in rats. J Bone Joint Surg Am 2003; 85: 905-11.
104. Wright VJ, Peng H, Usas A, et al. BMP4-expressing muscle-derived stem cells differentiate into osteogenic lineage and improve bone healing in immunocompetent mice. Mol Ther 2002; 6: 169-78.
105. Kawamura K, Chu CR, Sobajima S, et al. Adenoviral-mediated transfer of TGF-beta1 but not IGF-1 induces chondrogenic differentiation of human mesenchymal stem cells in pellet cultures. Exp Hematol 2005; 33: 865-72.
106. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004; 363: 1439-41.
107. Ringden O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006; 81: 1390-7.
108. Ishida T, Inaba M, Hisha H, et al. Requirement of donor-derived stromal cells in the bone marrow for successful allogeneic bone marrow transplantation. Complete prevention of recurrence of autoimmune diseases in MRL/MP-Ipr/Ipr mice by transplantation of bone marrow plus bones (stromal cells) from the same donor. J Immunol 1994; 152: 3119-27.
109. Zappia E, Casazza S, Pedemonte E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106: 1755-61.
110. Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007; 56: 1175-86.
111. Tyndall A, Walker UA, Cope A, et al. Immunomodulatory properties of mesenchymal stem cells: a review based on an interdisciplinary meeting held at the Kennedy Institute of Rheumatology Division, London, UK, 31 October 2005. Arthritis Res Ther 2007; 9: 301.
112. Chen Y, Shao JZ, Xiang LX, Dong XJ, Zhang GR. Mesenchymal stem cells: A promising candidate in regenerative medicine. Int J Biochem Cell Biol 2008; 40: 815-20.
113. Granero-Molto F, Weis JA, Longobardi L, Spagnoli A. Role of mesenchymal stem cells in regenerative medicine: application to bone and cartilage repair. Expert Opin Biol Ther 2008; 8: 255-68.
114. Ikehara S. A novel method of bone marrow transplantation (BMT) for intractable autoimmune diseases. J Autoimmun 2008; 30: 108-15.
115. Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol 2008; 36: 733-41.
116. Kumar S, Chanda D, Ponnazhagan S. Therapeutic potential of genetically modified mesenchymal stem cells. Gene Ther 2008; 15: 711-5.
117. Kwan MD, Slater BJ, Wan DC, Longaker MT. Cell-based therapies for skeletal regenerative medicine. Hum Mol Genet 2008; 17: R93-R98.
118. Ozawa K, Sato K, Oh I, et al. Cell and gene therapy using mesenchymal stem cells (MSCs). J Autoimmun 2008; 30: 121-7.
119. Roobrouck VD, Ulloa-Montoya F, Verfaillie CM. Self-renewal and differentiation capacity of young and aged stem cells. Exp Cell Res 2008; 314: 1937-44.
120. Siddappa R, Fernandes H, Liu J, van Blitterswijk C, de Boer J. The response of human mesenchymal stem cells to osteogenic signals and its impact on bone tissue engineering. Curr Stem Cell Res Ther 2007; 2: 209-20.
121. Slater BJ, Kwan MD, Gupta DM, Panetta NJ, Longaker MT. Mesenchymal cells for skeletal tissue engineering. Expert Opin Biol Ther 2008; 8: 885-93.
122. Fickert S, Fiedler J, Brenner RE. Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Res Ther 2004; 6: R422-R432.
123. 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: R1304-15.
124. Banfi A, Bianchi G, Notaro R, Luzzatto L, Cancedda R, Quarto R. Replicative aging and gene expression in long-term cultures of human bone marrow stromal cells. Tissue Eng 2002; 8: 901-10.
125. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 2004; 32: 414-25.
126. Rubio D, Garcia-Castro J, Martin MC, et al. Spontaneous human adult stem cell transformation. Cancer Res 2005; 65: 3035-9.
127. Tolar J, Nauta AJ, Osborn MJ, et al. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 2007; 25: 371-9.
128. Aslan H, Zilberman Y, Kandel L, et al. Osteogenic differentiation of noncultured immunoisolated bone marrow-derived CD105+ cells. Stem Cells 2006; 24: 1728-37.
129. Gronthos S, Graves SE, Simmons PJ. Isolation, purification and in vitro manipulation of human bone marrow stromal precursor cells. In: Beresford JN, Owen ME, eds. Marrow stromal cell culture. Cambridge, UK: Cambridge University Press 1998: 26-42.
130. Kastrinaki MC, Andreakou I, Charbord P, Papadaki HA. Isolation of human bone marrow mesenchymal stem cells using different membrane markers: comparison of colony/cloning efficiency, differentiation potential and molecular profile. Tissue Eng Part C 2008; In press.
131. Majumdar MK, Banks V, Peluso DP, Morris EA. Isolation, characterization, and chondrogenic potential of human bone marrow-derived multipotential stromal cells. J Cell Physiol 2000; 185: 98-106.