Changes of the functional capacity of mesenchymal stem cells due to aging or age-associated disease - Implications for clinical applications and donor recruitment

Transfusion Medicine and Hemotherapy

Volumn 35, Issue 4, 2008, Pages 299-305

  Lepperdinger, Günter ^a   Brunauer, Regina ^a   Gassner, Robert ^b   Jamnig, Angelika ^a   Kloss, Frank ^b   Laschober, Gerhard Thomas ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b UNIVERSITY HOSPITAL INNSBRUCK   (Austria)

Author keywords

Aging; Mesenchymal stem cells

Indexed keywords

ADULT STEM CELL; AGING; CELL CULTURE; HUMAN; MESENCHYMAL STEM CELL; NONHUMAN; REVIEW; TISSUE REGENERATION; TISSUE REPAIR;

EID: 58549096714     PISSN: 16603796     EISSN: None     Source Type: Journal    
DOI: 10.1159/000142373     Document Type: Review

References (83)

1. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A: Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005;7:393-395.
2. Caplan AI: Mesenchymal stem cells. J Orthop Res 1991;9:641-650.
3. Pittenger MF, Mosca JD, McIntosh KR: Human mesenchymal stem cells: progenitor cells for cartilage, bone, fat and stroma. Curr Top Microbiol Immunol 2000;251:3-11.
4. Prockop DJ, Sekiya I, Colter DC: Isolation and characterization of rapidly self-renewing stem cells from cultures of human marrow stromal cells. Cytotherapy 2001;3:393-396.
5. Gronthos S, Graves SE, Ohta S, Simmons PJ: The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 1994;84:4164-4173.
6. Horwitz EM, Keating A: Nonhematopoietic mesenchymal stem cells: what are they? Cytotherapy 2000;2:387-388.
7. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E: Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
8. Rando TA: Stem cells, ageing and the quest for immortality. Nature 2006;441:1080-1086.
9. 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;98:2396-2402.
10. Tsai MS, Lee JL, Chang YJ, Hwang SM: Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Hum Reprod 2004;19:1450-1456.
11. In 't Anker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas F H, Fibbe WE, Kanhai HH: Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004;22:1338-1345.
12. Mareschi K, Biasin E, Piacibello W, Aglietta M, Madon E, Fagioli F: Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Haematologica 2001;86:1099-1100.
13. Gotherstrom C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K: Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica 2005;90:1017-1026.
14. Mirmalek-Sani SH, Tare RS, Morgan SM, Roach HI, Wilson DI, Hanley NA, Oreffo RO: Characterization and multipotentiality of human fetal femur-derived cells: implications for skeletal tissue regeneration. Stem Cells 2006;24:1042-1053.
15. Friedenstein AJ, Piatetzky SI, Petrakova KV: Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 1966;16:381-390.
16. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR: Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
17. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, Bagasra O, Prockop DJ: Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A 1995;92:4857-4861.
18. Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, Gülly C, Gassner R, Lepperdinger G: Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell 2007;6:745-757.
19. Tuli R, Tuli S, Nandi S, Wang ML, Alexander PG, Haleem-Smith H, Hozack WJ, Manner PA, Danielson KG, Tuan RS: Characterization of multipotential mesenchymal progenitor cells derived from human trabecular bone. Stem Cells 2003;21:681-693.
20. Schaffler A, Buchler C: Concise review: adipose tissue-derived stromal cells - basic and clinical implications for novel cell-based therapies. Stem Cells 2007;25:818-827.
21. Nakahara H, Bruder SP, Goldberg VM, Caplan AI: In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin Orthop Relat Res 1990:223-232.
22. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T: Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005;52:2521-2529.
23. Abedin M, Tintut Y, Demer LL: Mesenchymal stem cells and the artery wall. Circ Res 2004;95:671-676.
24. Zhang W, Walboomers, XF, Shi S, Fan M, Jansen JA: Multilineage differentiation potential of stem cells derived from human dental pulp after cryopreservation. Tissue Eng;2006, 12:2813-23.
25. Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S: Adult human dental pulp stem cells differentiate towards functionally active neurons under appropriate environmental cues. Stem Cells, 2008; DOI: 10.1634/stemcells.2007- 0979.
26. Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzl M, Lucas PA, Black AC Jr: Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 2001;264:51-62.
27. Roufosse CA, Direkze NC, Otto WR, Wright NA: Circulating mesenchymal stem cells. Int J Biochem Cell Biol 2004;36:585-597.
28. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K: Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006;24:1294-1301.
29. Guillot PV, O'Donoghue K, Kurata H, Fisk NM: Fetal stem cells: betwixt and between. Semin Reprod Med 2006;24:340-347.
30. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I: Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 2004; 22675-682.
31. Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE: Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J Bone Miner Metab 1999;17: 171-177.
32. Muschler GF, Nitto H, Boehm CA, Easley KA: Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res 2001;19:117-125.
33. Majors AK, Boehm CA, Nitto H, Midura RJ, Muschler GF: Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J Orthop Res 1997;15:546-557.
34. Caplan AI: Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007;213:341-347.
35. Stolzing A, Jones E, McGonagle D, Scutt A: Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 2008;129:163-173.
36. Oreffo RO, Bennett A, Carr AJ, Triffitt JT: Patients with primary osteoarthritis show no change with ageing in the number of osteogenic precursors. Scand J Rheumatol 1998;27:415-424.
37. 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;16:1120-1129.
38. Justesen J, Stenderup K, Eriksen EF, Kassem M: Maintenance of osteoblastic and adipocytic differentiation potential with age and osteoporosis in human marrow stromal cell cultures. Calcif Tissue Int 2002;71:36-44.
39. D'Ippolito G, Schiller PC, Ricordi C, Roos BA, Howard GA: Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 1999;14:1115-1122.
40. Glowacki J: Influence of age on human marrow. Calcif Tissue Int 1995;56(suppl 1):S50-51.
41. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, Benayahu D, Robey PG: Singlecolony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997;12:1335-1347.
42. Muraglia A, Cancedda R, Quarto R: Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000;113:1161-1166.
43. Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS, Glowacki J: Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 2008;7:335-343.
44. Mueller SM, Glowacki J: Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 2001;82:583-590.
45. Bosch P, Musgrave DS, Lee JY, Cummins J, Shuler T, Ghivizzani TC, Evans T, Robbins TD, Huard J: Osteoprogenitor cells within skeletal muscle. J Orthop Res 2000;18:933-944.
46. Collett GD, Canfield AE: Angiogenesis and pericytes in the initiation of ectopic calcification. Circ Res 2005;96:930-938.
47. Eghbali-Fatourechi GZ, Lamsam J, Fraser D, Nagel D, Riggs BL, Khosla S: Circulating osteoblast-lineage cells in humans. N Engl J Med 2005;352: 1959-1966.
48. Gruber R, Koch H, Doll BA, Tegtmeier F, Einhorn TA, Hollinger JO: Fracture healing in the elderly patient. Exp Gerontol 2006;41:1080-1093.
49. Hayflick L, Moorhead PS: The serial cultivation of human diploid cell strains. Exp Cell Res 1961;25:585-621.
50. Campisi J: From cells to organisms: can we learn about aging from cells in culture? Exp Gerontol 2001;36:607-618.
51. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, Peacocke M, Campisi J: A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995;92:9363-9367.
52. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, Jansen-Dürr P, Wlaschek M: p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 2006;5:379-389.
53. Vasile E, Tomita Y, Brown LF, Kocher O, Dvorak HF: Differential expression of thymosin beta-10 by early passage and senescent vascular endothelium is modulated by VPF/VEGF: evidence for senescent endothelial cells in vivo at sites of atherosclerosis. FASEB J 2001;15:458-466.
54. 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. Br J Haematol 1999;107:275-281.
55. 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;33:919-926.
56. Stenderup K, Rosada C, Justesen J, Al-Soubky T, Dagnaes-Hansen F, Kassem M: Aged human bone marrow stromal cells maintaining bone forming capacity in vivo evaluated using an improved method of visualization. Biogerontology 2004;5:107-118.
57. Forsyth NR, Wright WE, Shay JW: Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation 2002;69:188-197.
58. Zimmermann S, Voss M, Kaiser S, Kapp U, Waller CF, Martens UM: Lack of telomerase activity in human mesenchymal stem cells. Leukemia 2003;17:1146-1149.
59. Napolitano MA, Cipollaro M, Cascino A, Melone MA, Giordano A, Galderisi U: Brg1 chromatin remodeling factor is involved in cell growth arrest, apoptosis and senescence of rat mesenchymal stem cells. J Cell Sci 2007;120:2904-2911.
60. Laschober G, Brunauer R, Jamnig A, Fehrer C, Greiderer B, Lepperdinger G: Leptin receptor/CD 295 is upregulated on primary human mesenchymal stem cells of advancing biological age and distinctly marks the subpopulation of dying cells. Exp Gerontol 2008;DOI: 10.1016/j.exger.2008.05.013.
61. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, Moseley A, Hoffman R: Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002;30:42-48.
62. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, Dazzi F: Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003;101:3722-3729.
63. 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;31:890-896.
64. Le Blanc K, Ringden O: Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 2007;262:509-525.
65. Ringden O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lonnies H, Marschall HU, Dlugosz A, Szakos A, Hassan Z, Omazic B, Aschan J, Barkholt L, Le Blanc K: Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006;81:1390-1397.
66. Le Blanc K, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, Uzunel M, Ringden O: Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363:1439-1441.
67. 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: Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008;371:1579-1586.
68. Giordano A, Galderisi U, Marino IR: From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J Cell Physiol 2007;211:27-35.
69. Bolland BJ, Tilley S, New AM, Dunlop DG, Oreffo RO: Adult mesenchymal stem cells and impaction grafting: a new clinical paradigm shift. Expert Rev Med Devices 2007;4:393-404.
70. Abdel-Latif A, Bolli R, Tleyjeh IM, Montori VM, Perin EC, Hornung CA, Zuba-Surma EK, Al-Mallah M, Dawn B: Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis. Arch Intern Med 2007;167:989-997.
71. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK: Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309-313.
72. Chamberlain JR, Deyle DR, Schwarze U, Wang P, Hirata RK, Li Y, Byers PH, Russell DW: Gene targeting of mutant COL1A2 alleles in mesenchymal stem cells from individuals with osteogenesis imperfecta. Mol Ther 2008;16:187-193.
73. Pochampally RR, Horwitz EM, DiGirolamo CM, Stokes DS, Prockop DJ: Correction of a mineralization defect by overexpression of a wild-type cDNA for COL1A1 in marrow stromal cells (MSCs) from a patient with osteogenesis imperfecta: a strategy for rescuing mutations that produce dominant-negative protein defects. Gene Ther 2005;12:1119-1125.
74. Kassem M: Stem cells: potential therapy for age-related diseases. Ann N Y Acad Sci 2006;1067:436-442.
75. Abdallah BM, Kassem M: Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther 2008;15:109-116.
76. Scaffidi P, Misteli T: Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol 2008;10:452-459.
77. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FS: Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003;423: 293-298.
78. Ferretti M, Gassner R, Wang Z, Perera P, Deschner J, Sowa G, Salter RB, Agarwal S: Biomechanical signals suppress proinflammatory responses in cartilage: early events in experimental antigen-induced arthritis J Immunol 2006;177:8757-8766.
79. Creamer P, Hochberg MC: Osteoarthritis. Lancet 1997;350:503-508.
80. Scharstuhl A, Schewe B, Benz K, Gaissmaier C, Buhring HJ, Stoop R: Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology. Stem Cells 2007;25:3244-3251.
81. 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;46:704-713.
82. Rodriguez JP, Garat S, Gajardo H, Pino AM, Seitz G: Abnormal osteogenesis in osteoporotic patients is reflected by altered mesenchymal stem cells dynamics. J Cell Biochem 1999;75:414-423.
83. Halme DG, Kessler DA: FDA regulation of stem-cell-based therapies. N Engl J Med 2006;355:1730-1735.