Human mesenchymal stem cells: Basic biology and clinical applications for bone tissue regeneration

Trends in Stem Cell Biology and Technology

Volumn , Issue , 2009, Pages 177-190

  Abdallah, Basem M ^a   Saeed, Hamid ^a   Kassem, Moustapha ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Bone regeneration; Cell therapy; Human bone marrow derived mesenchymal stem cells; Mesenchymal stem cells

Indexed keywords

EID: 77956060121     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-60327-905-5_12     Document Type: Chapter

References (95)

1. Dominici M, Le BK, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-7 .
2. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001; 19: 180-92 .
3. Dezawa M, Kanno H, Hoshino M, et al. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest 2004; 113: 1701-10 .
4. Luk JM, Wang PP, Lee CK, Wang JH, Fan ST. Hepatic potential of bone marrow stromal cells: development of in vitro co-culture and intra-portal transplantation models. J Immunol Methods 2005; 305: 39-47 .
5. Dexter TM. Haemopoiesis in long-Term bone marrow cultures. A review. Acta Haematol 1979; 62: 299-305 .
6. Friedenstein AJ. Osteogenic stem cells in the bone marrow. Bone Miner 1991; 7: 243-72 .
7. Owen M. Marrow stromal stem cells. J Cell Sci Suppl 1988; 10: 63-76 .
8. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970; 3: 393-403 .
9. Luria EA, Panasyuk AF, Friedenstein AY. Fibroblast colony formation from monolayer cultures of blood cells. Transfusion 1971; 11: 345-9 .
10. Abdallah BM, Haack-Sorensen M, Burns JS, et al. Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite [corrected] extensive proliferation. Biochem Biophys Res Commun 2005; 326: 527-38 .
11. Foster LJ, Zeemann PA, Li C, Mann M, Jensen ON, Kassem M. Differential expression profiling of membrane proteins by quantitative proteomics in a human mesenchymal stem cell line undergoing osteoblast differentiation. Stem Cells 2005; 23: 1367-77 .
12. Kassem M, Mosekilde L, Eriksen EF. 1,25-Dihydroxyvitamin D3 potentiates fluoride-stimulated collagen type I production in cultures of human bone marrow stromal osteoblast-like cells. J Bone Miner Res 1993; 8: 1453-8 .
13. Rickard DJ, Kassem M, Hefferan TE, Sarkar G, Spelsberg TC, Riggs BL. Isolation and characterization of osteoblast precursor cells from human bone marrow. J Bone Miner Res 1996; 11: 312-24 .
14. Kuznetsov SA, Krebsbach PH, Satomura K, et al. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997; 12: 1335-47 .
15. Gronthos S, Graves SE, Ohta S, Simmons PJ. The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 1994; 84: 4164-73 .
16. Stenderup K, Justesen J, Eriksen EF, Rattan SI, Kassem M. Number and proliferative capacity of osteogenic stem cells are maintained during aging and in patients with osteoporosis. J Bone Miner Res 2001; 16: 1120-9 .
17. Sacchetti B, Funari A, Michienzi S, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007; 131: 324-36 .
18. Gronthos S, Zannettino AC, Hay SJ, et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003; 116 (Pt 9): 1827-35 .
19. Delorme B, Ringe J, Gallay N, et al. Specific plasma membrane protein phenotype of cultureamplified and native human bone marrow mesenchymal stem cells. Blood 2008; 111: 2631-5 .
20. Buhring HJ, Battula VL, Treml S, Schewe B, Kanz L, Vogel W. Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 2007; 1106: 262-71.
21. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001; 98: 2615-25 .
22. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002; 418: 41-9 .
23. Olmsted-Davis EA, Gugala Z, Camargo F, et al. Primitive adult hematopoiletic stem cells can function as osteoblast precursors. Proc Natl Acad Sci U S A 2003; 100: 15877-82 .
24. Lodie TA, Blickarz CE, Devarakonda TJ, et al. Systematic analysis of reportedly distinct populations of multipotent bone marrow-derived stem cells reveals a lack of distinction. Tissue Eng 2002; 8: 739-51 .
25. Kuznetsov SA, Mankani MH, Gronthos S, Satomura K, Bianco P, Robey PG. Circulating skeletal stem cells. J Cell Biol 2001; 153: 1133-40 .
26. Rosada C, Justesen J, Melsvik D, Ebbesen P, Kassem M. The human umbilical cord blood: a potential source for osteoblast progenitor cells. Calcif Tissue Int 2003; 72: 135-42 .
27. De Bari C, DellAccio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001; 44: 1928-42 .
28. Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001; 189: 54-63 .
29. 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. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-Trimester fetal blood, liver, and bone marrow. Blood 2001; 98: 2396-402 .
31. Gronthos S, Robey PG, Boyde A, Shi S. Human dental pulp stem cells (DPSCs): characterization and developmental potential. J Bone Miner Res 2001; 16: S265 .
32. Otaki S, Ueshima S, Shiraishi K, et al. Mesenchymal progenitor cells in adult human dental pulp and their ability to form bone when transplanted into immunocompromised mice. Cell Biol Int 2007; 31: 1191-7 .
33. Miura M, Gronthos S, Zhao M, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 2003; 100: 5807-12 .
34. 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 .
35. Wagner W, Wein F, Seckinger A, et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005; 33: 1402-16 .
36. Yamada Y, Fujimoto A, Ito A, Yoshimi R, Ueda M. Cluster analysis and gene expression profiles: a cDNA microarray system-based comparison between human dental pulp stem cells (hDPSCs) and human mesenchymal stem cells (hMSCs) for tissue engineering cell therapy. Biomaterials 2006; 27: 3766-81 .
37. Kassem M, Ankersen L, Eriksen EF, Clark BF, Rattan SI. Demonstration of cellular aging and senescence in serially passaged long-Term cultures of human trabecular osteoblasts. Osteoporos Int 1997; 7: 514-24 .
38. DiGirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate 6. Br J Haematol 1999; 107: 275-81 .
39. Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003; 33: 919-26 .
40. Rattan SIS. Aging outside the body: usefulness of the Hayflick system. In: Kaul SC, Wadhwa R, editors. Aging of cells in and outside the body. Kluwer, London, 2003: 1-8 .
41. Simonsen JL, Rosada C, Serakinci N, et al. Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 2002; 20: 592-6 .
42. Zimmermann S, Voss M, Kaiser S, Kapp U, Waller CF, Martens UM. Lack of telomerase activity in human mesenchymal stem cells. Leukemia 2003; 17: 1146-9.
43. Mckee JA, Banik SSR, Boyer MJ, et al. Human arteries engineered in vitro. EMBO Rep 2003; 4: 633-8 .
44. Serakinci N, Guldberg P, Burns JS, et al. Adult human mesenchymal stem cell as a target for neoplastic transformation. Oncogene 2004; 23: 5095-8 .
45. Serakinci N, Hoare SF, Kassem M, Atkinson SP, Keith WN. Telomerase promoter reprogramming and interaction with general transcription factors in the human mesenchymal stem cell. Regen Med 2006; 1: 125-31 .
46. Krebsbach PH, Kuznetsov SA, Satomura K, Emmons RV, Rowe DW, Robey PG. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 1997; 63: 1059-69 .
47. Abdallah BM, Haack-Sorensen M, Fink T, Kassem M. Inhibition of osteoblast differentiation but not adipocyte differentiation of mesenchymal stem cells by sera obtained from aged females. Bone 2006; 39: 181-8 .
48. Luu HH, Song WX, Luo X, et al. Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells. J Orthop Res 2007; 25: 665-77 .
49. Noel D, Gazit D, Bouquet C, et al. Short-Term BMP-2 expression is sufficient for in vivo osteochondral differentiation of mesenchymal stem cells. Stem Cells 2004; 22: 74-85 .
50. Ichida F, Nishimura R, Hata K, et al. Reciprocal roles of MSX2 in regulation of osteoblast and adipocyte differentiation. J Biol Chem 2004; 279: 34015-22 .
51. Kojima H, Uemura T. Strong and rapid induction of osteoblast differentiation by Cbfa1/Til-1 overexpression for bone regeneration. J Biol Chem 2005; 280: 2944-53 .
52. Tang Z, Sahu SN, Khadeer MA, Bai G, Franklin RB, Gupta A. Overexpression of the ZIP1 zinc transporter induces an osteogenic phenotype in mesenchymal stem cells. Bone 2006; 38: 181-98 .
53. Wu L, Wu Y, Lin Y, et al. Osteogenic differentiation of adipose derived stem cells promoted by overexpression of osterix. Mol Cell Biochem 2007; 301: 83-92 .
54. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 2005; 308: 1472-7 .
55. Le BK, 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 .
56. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells 6. Science 1999; 284: 143-7 .
57. Di NM, 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: 3838-43 .
58. 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 .
59. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105: 1815-22 .
60. Bartholomew A, Sturgeon C, Siatskas M, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002; 30: 42-8 .
61. Le BK, 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 .
62. Inoue S, Popp FC, Koehl GE, et al. Immunomodulatory effects of mesenchymal stem cells in a rat organ transplant model. Transplantation 2006; 81: 1589-95 .
63. Lee ST, Jang JH, Cheong JW, et al. Treatment of high-risk acute myelogenous leukaemia by myeloablative chemoradiotherapy followed by co-infusion of T cell-depleted haematopoietic stem cells and culture-expanded marrow mesenchymal stem cells from a related donor with one fully mismatched human leucocyte antigen haplotype. Br J Haematol 2002; 118: 1128-31 .
64. 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 Transplant 2004; 33: 597-604 .
65. Ringden O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapyresistant graft-versus-host disease. Transplantation 2006; 81: 1390-7 .
66. Dean RM, Bishop MR. Graft-versus-host disease: emerging concepts in prevention and therapy. Curr Hematol Rep 2003; 2: 287-94.
67. Goel A, Sangwan SS, Siwach RC, Ali AM. Percutaneous bone marrow grafting for the treatment of tibial non-union. Injury 2005; 36: 203-6 .
68. Hernigou P, Poignard A, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Joint Surg Am 2005; 87: 1430-7 .
69. Kawate K, Yajima H, Ohgushi H, et al. Tissue-engineered approach for the treatment of steroid-induced osteonecrosis of the femoral head: transplantation of autologous mesenchymal stem cells cultured with beta-Tricalcium phosphate ceramics and free vascularized fibula. Artif Organs 2006; 30: 960-2 .
70. Kuroda R, Ishida K, Matsumoto T, et al. Treatment of a full-Thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 2007; 15: 226-31 .
71. Wakitani S, Mitsuoka T, Nakamura N, Toritsuka Y, Nakamura Y, Horibe S. Autologous bone marrow stromal cell transplantation for repair of full-Thickness articular cartilage defects in human patellae: two case reports. Cell Transplant 2004; 13: 595-600 .
72. Kitoh H, Kitakoji T, Tsuchiya H, et al. Transplantation of marrow-derived mesenchymal stem cells and platelet-rich plasma during distraction osteogenesis-A preliminary result of three cases. Bone 2004; 35: 892-8 .
73. Quarto R, Mastrogiacomo M, Cancedda R, et al. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 2001; 344: 385-6 .
74. Ohgushi H, Kotobuki N, Funaoka H, et al. Tissue engineered ceramic artificial joint-ex vivo osteogenic differentiation of patient mesenchymal cells on total ankle joints for treatment of osteoarthritis. Biomaterials 2005; 26: 4654-61 .
75. Gangji V, Hauzeur JP. Treatment of osteonecrosis of the femoral head with implantation of autologous bone-marrow cells. Surgical technique. J Bone Joint Surg Am 2005; 87 Suppl 1(Pt 1): 106-12 .
76. Chang CH, Stanton RP, Glutting J. Unicameral bone cysts treated by injection of bone marrow or methylprednisolone. J Bone Joint Surg Br 2002; 84: 407-12 .
77. Stock UA, Vacanti JP. Tissue engineering: Current state and prospects. Annu Rev Med 2001; 52: 443-51 .
78. Bianco P, Robey PG. Stem cells in tissue engineering. Nature 2001; 414: 118-21 .
79. Kon E, Muraglia A, Corsi A, et al. Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones 10. J Biomed Mater Res 2000; 49: 328-37 .
80. Warnke PH, Springer IN, Wiltfang J, et al. Growth and transplantation of a custom vascularised bone graft in a man. Lancet 2004; 364: 766-70 .
81. Ohgushi H, Goldberg VM, Caplan AI. Repair of bone defects with marrow cells and porous ceramic. Experiments in rats 116. Acta Orthop Scand 1989; 60: 334-9 .
82. Bruder SP, Fink DJ, Caplan AI. Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy 172. J Cell Biochem 1994; 56: 283-94 .
83. Diduch DR, Jordan LC, Mierisch CM, Balian G. Marrow stromal cells embedded in alginate for repair of osteochondral defects. Arthroscopy 2000; 16: 571-7 .
84. Lieberman JR, Le LQ, Wu L, et al. Regional gene therapy with a BMP-2-producing murine stromal cell line induces heterotopic and orthotopic bone formation in rodents. J Orthop Res 1998; 16: 330-9 .
85. Gazit D, Turgeman G, Kelley P, et al. Engineered pluripotent mesenchymal cells integrate and differentiate in regenerating bone: a novel cell-mediated gene therapy. J Gene Med 1999; 1: 121-33 .
86. Lee JY, Musgrave D, Pelinkovic D, et al. Effect of bone morphogenetic protein-2-expressing muscle-derived cells on healing of critical-sized bone defects in mice. J Bone Joint Surg Am 2001; 83-A (7): 1032-9 .
87. Laurencin CT, Attawia MA, Lu LQ, et al. Poly(lactide-co-glycolide)/ hydroxyapatite delivery of BMP-2-producing cells: a regional gene therapy approach to bone regeneration. Biomaterials 2001; 22: 1271-7.
88. Moutsatsos IK, Turgeman G, Zhou S, et al. Exogenously regulated stem cell-mediated gene therapy for bone regeneration. Mol Ther 2001; 3: 449-61 .
89. Shen FH, Visger JM, Balian G, Hurwitz SR, Diduch DR. Systemically administered mesenchymal stromal cells transduced with insulin-like growth factor-I localize to a fracture site and potentiate healing. J Orthop Trauma 2002; 16: 651-9 .
90. Peterson B, Zhang J, Iglesias R, et al. Healing of critically sized femoral defects, using genetically modified mesenchymal stem cells from human adipose tissue. Tissue Eng 2005; 11: 120-9 .
91. Hasharoni A, Zilberman Y, Turgeman G, Helm GA, Liebergall M, Gazit D. Murine spinal fusion induced by engineered mesenchymal stem cells that conditionally express bone morphogenetic protein-2. J Neurosurg Spine 2005; 3: 47-52 .
92. Xu XL, Tang T, Dai K, et al. Immune response and effect of adenovirus-mediated human BMP-2 gene transfer on the repair of segmental tibial bone defects in goats. Acta Orthop 2005; 76: 637-46 .
93. Tobita M, Uysal AC, Ogawa R, Hyakusoku H, Mizuno H. Periodontal tissue regeneration with adipose-derived stem cells. Tissue Eng Part A 2008; 14 (6): 945-53 .
94. Horwitz EM, Gordon PL, Koo WKK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci U S A 2002; 99: 8932-7 .
95. Bentzon JF, Stenderup K, Hansen FD, et al. Tissue distribution and engraftment of human mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene. Biochem Biophys Res Commun 2005; 330: 633-40 .