Mesenchymal stromal cells from donors varying widely in age are of equal cellular fitness after in vitro expansion under hypoxic conditions

References

• Friedenstein AJ, Piatetzky S, II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol. 1966;16(3):381–90.
   PubMedGoogle Scholar
• Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976;4(5):267–74.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–74.
   PubMed Web of Science ®Google Scholar
• Caplan AI, Bruder SP. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med. 2001;7(6):259–64.
   PubMed Web of Science ®Google Scholar
• Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol. 2008;36(6):733–41.
   PubMed Web of Science ®Google Scholar
• Lazennec G, Jorgensen C. Concise review: adult multipotent stromal cells and cancer: risk or benefit? Stem Cells. 2008;26(6):1387–94.
   PubMed Web of Science ®Google Scholar
• 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(1):27–35.
   PubMed Web of Science ®Google Scholar
• Dryden GW. Overview of stem cell therapy for Crohn's disease. Expert Opin Biol Ther. 2009;9(7):841–7.
   PubMed Web of Science ®Google Scholar
• 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;22(5):675–82.
   PubMed Web of Science ®Google Scholar
• Banfi A, Muraglia A, Dozin B, Mastrogiacomo M, Cancedda R, Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp Hematol. 2000; 28(6):707–15.
   PubMed Web of Science ®Google Scholar
• Stolzing A, Jones E, McGonagle D, Scutt A. Age–related changes inhuman bone marrow–derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev. 2008;129(3):163–73.
   PubMed Web of Science ®Google Scholar
• Garinis GA, van der Horst GT, Vijg J, Hoeijmakers JH. DNA damage and ageing: new–age ideas for an age–old problem. Nat Cell Biol. 2008;10(11):1241–7.
   PubMed Web of Science ®Google Scholar
• Zhang ZX, Guan LX, Zhang K, Wang S, Cao PC, Wang YH, . Cytogenetic analysis of human bone marrow–derived mesenchymal stem cells passaged in vitro. Cell Biol Int. 2007;31(6):645–8.
   PubMed Web of Science ®Google Scholar
• Rubio D, Garcia–Castro J, Martin MC, de la Fuente R, Cigudosa JC, Lloyd AC, . Spontaneous human adult stem cell transformation. Cancer Res. 2005;65(8):3035–9.
   PubMed Web of Science ®Google Scholar
• Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, . Sarcoma derived from cultured mesenchymal stem cells. Stem Cells. 2007;25(2):371–9.
   PubMed Web of Science ®Google Scholar
• Guillot PV, Gotherstrom C, Chan J, Kurata H, Fisk NM. Human first–trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells. 2007;25(3):646–54.
   PubMed Web of Science ®Google Scholar
• Rosova I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells. 2008;26(8):2173–82.
   PubMed Web of Science ®Google Scholar
• Krinner A, Zscharnack M, Bader A, Drasdo D, Galle J. Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif. 2009;42(4): 471–84.
   PubMed Web of Science ®Google Scholar
• Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, . Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell. 2007;6(6):745–57.
   PubMed Web of Science ®Google Scholar
• Grant JD, Broccoli D, Muquit M, Manion FJ, Tisdall J, Ochs MF. Telometric: a tool providing simplified, reproducible measurements of telomeric DNA from constant field agarose gels. Biotechniques. 2001;31(6):1314–6, 8.
   PubMed Web of Science ®Google Scholar
• Mageed AS, Pietryga DW, DeHeer DH, West RA. Isolation of large numbers of mesenchymal stem cells from the washings of bone marrow collection bags: characterization of fresh mesenchymal stem cells. Transplantation. 2007;83(8): 1019–26.
   PubMed Web of Science ®Google Scholar
• Capelli C, Salvade A, Pedrini O, Barbui V, Gotti E, Borleri G, . The washouts of discarded bone marrow collection bags and filters are a very abundant source of hMSCs. Cytotherapy. 2009;11(4):403–13.
   PubMed Web of Science ®Google Scholar
• Glees P, Hasan M. Lipofuscin in neuronal aging and diseases. Norm Pathol Anat (Stuttg). 1976;32:1–68.
   PubMedGoogle Scholar
• Ksiazek K. A comprehensive review on mesenchymal stem cell growth and senescence. Rejuvenation Res. 2009;12(2): 105–16.
   PubMed Web of Science ®Google Scholar
• Kasper G, Mao L, Geissler S, Draycheva A, Trippens J, Kuhnisch J, . Insights into mesenchymal stem cell aging: involvement of antioxidant defense and actin cytoskeleton. Stem Cells. 2009;27(6):1288–97.
   PubMed Web of Science ®Google Scholar
• Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, . Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet. 1995;11(4):376–81.
   PubMed Web of Science ®Google Scholar
• Lee JA, Song HY, Ju SM, Lee SJ, Kwon HJ, Eum WS, . Differential regulation of inducible nitric oxide synthase and cyclooxygenase–2 expression by superoxide dismutase in lipopolysaccharide stimulated RAW 264.7 cells. Exp Mol Med. 2009;41(9):629–37.
   PubMed Web of Science ®Google Scholar
• Chung HY, Cesari M, Anton S, Marzetti E, Giovannini S, Seo AY, . Molecular inflammation: underpinnings of aging and age–related diseases. Ageing Res Rev. 2009;8(1): 18–30.
   PubMed Web of Science ®Google Scholar
• Saini A, Sei Y. Age–related impairment of early and late events of signal transduction in mouse immune cells. Life Sci. 1993;52(22):1759–65.
   PubMed Web of Science ®Google Scholar
• Badawi AF, Liu Y, Eldeen MB, Morrow W, Razak ZR, Maradeo M, . Age–associated changes in the expression pattern of cyclooxygenase–2 and related apoptotic markers in the cancer susceptible region of rat prostate. Carcinogenesis. 2004;25(9):1681–8.
   PubMed Web of Science ®Google Scholar
• Naik AA, Xie C, Zuscik MJ, Kingsley P, Schwarz EM, Awad H, . Reduced COX–2 expression in aged mice is associated with impaired fracture healing. J Bone Miner Res. 2009;24(2):251–64.
   PubMed Web of Science ®Google Scholar
• Han JH, Roh MS, Park CH, Park KC, Cho KH, Kim KH, . Selective COX–2 inhibitor, NS–398, inhibits the replicative senescence of cultured dermal fibroblasts. Mech Ageing Dev. 2004;125(5):359–66.
   PubMed Web of Science ®Google Scholar
• Lee CH, Yoo KY, Choi JH, Park OK, Hwang IK, Kang IJ, . Cyclooxygenase–2 immunoreactivity and protein level in the gerbil hippocampus during normal aging. Neurochem Res. 2010;35(1):99–106.
   PubMed Web of Science ®Google Scholar
• Tajima T, Murata T, Aritake K, Urade Y, Hirai H, Nakamura M, . Lipopolysaccharide induces macrophage migration via prostaglandin D(2) and prostaglandin E(2). J Pharmacol Exp Ther. 2008;326(2):493–501.
   PubMed Web of Science ®Google Scholar
• Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter–Kochanek K, Jansen–Durr P, . p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell. 2006;5(5):379–89.
   PubMed Web of Science ®Google Scholar
• Scaffidi P, Misteli T. Lamin A–dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol. 2008;10(4):452–9.
   PubMed Web of Science ®Google Scholar
• Worman HJ, Fong LG, Muchir A, Young SG. Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest. 2009;119(7):1825–36.
   PubMed Web of Science ®Google Scholar
• McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, Collins FS, . The mutant form of lamin A that causes Hutchinson–Gilford progeria is a biomarker of cellular aging in human skin. PLoS One. 2007;2(12):e1269.
   Web of Science ®Google Scholar
• Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell–cycle control causing specific inhibition of cyclin D/CDK4. Nature. 1993;366(6456):704–7.
   PubMed Web of Science ®Google Scholar
• Shibata KR, Aoyama T, Shima Y, Fukiage K, Otsuka S, Furu M, . Expression of the p16INK4 A gene is associated closely with senescence of human mesenchymal stem cells and is potentially silenced by DNA methylation during in vitro expansion. Stem Cells. 2007;25(9):2371–82.
   PubMed Web of Science ®Google Scholar
• Stolzing A, Scutt A. Age–related impairment of mesenchymal progenitor cell function. Aging Cell. 2006;5(3):213–24.
   PubMed Web of Science ®Google Scholar
• Sethe S, Scutt A, Stolzing A. Aging of mesenchymal stem cells. Ageing Res Rev. 2006;5(1):91–116.
   PubMed Web of Science ®Google Scholar
• Roura S, Farre J, Soler–Botija C, Llach A, Hove–Madsen L, Cairo JJ, . Effect of aging on the pluripotential capacity of human CD105(+) mesenchymal stem cells. Eur J Heart Fail. 2006;8(6):555–63.
   PubMed Web of Science ®Google Scholar
• Mohyeddin Bonab M, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Mesenchymal stem cell and in vitro Aging. BMC Cell Biol. 2006;7(1):14.
   PubMedGoogle Scholar
• Fehrer C, Laschober G, Lepperdinger G. Aging of murine mesenchymal stem cells. Ann N Y Acad Sci. 2006;1067: 235–42.
   PubMed Web of Science ®Google Scholar
• Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 2006;7:14.
   PubMed Web of Science ®Google Scholar
• Kim J, Kang JW, Park JH, Choi Y, Choi KS, Park KD, . Biological characterization of long–term cultured human mesenchymal stem cells. Arch Pharm Res. 2009;32(1): 117–26.
   PubMed Web of Science ®Google Scholar
• Sun L, Akiyama K, Zhang H, Yamaza T, Hou Y, Zhao S, . Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells. 2009;27(6):1421–32.
   PubMed Web of Science ®Google Scholar
• Kebriaei P, Isola L, Bahceci E, Holland K, Rowley S, McGuirk J, . Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft–versus–host disease. Biol Blood Marrow Transplant. 2009;15(7):804–11.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, . Mesenchymal stem cells for treatment of steroid–resistant, severe, acute graft –versus–host disease: a phase II study. Lancet. 2008;371(9624):1579–86.
   PubMed Web of Science ®Google Scholar
• Hung SC, Pochampally RR, Hsu SC, Sanchez C, Chen SC, Spees J, . Short–term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS One. 2007; 2(5):e416.
   Web of Science ®Google Scholar
• Stolzing A, Scutt A. Effect of reduced culture temperature on antioxidant defences of mesenchymal stem cells. Free Radic Biol Med. 2006;41(2):326–38.
   PubMed Web of Science ®Google Scholar
• Annabi B, Lee YT, Turcotte S, Naud E, Desrosiers RR, Champagne M, . Hypoxia promotes murine bone–marrow–derived stromal cell migration and tube formation. Stem Cells. 2003;21(3):337–47.
   PubMed Web of Science ®Google Scholar
• Minamino T, Mitsialis SA, Kourembanas S. Hypoxia extends the life span of vascular smooth muscle cells through telomerase activation. Mol Cell Biol. 2001;21(10):3336–42.
   PubMed Web of Science ®Google Scholar
• Poulios E, Trougakos IP, Chondrogianni N, Gonos ES. Exposure of human diploid fibroblasts to hypoxia extends proliferative life span. Ann N Y Acad Sci. 2007;1119:9–19.
   PubMed Web of Science ®Google Scholar
• Mueller LP, Luetzkendorf J, Mueller T, Reichelt K, Simon H, Schmoll HJ. Presence of mesenchymal stem cells in human bone marrow after exposure to chemotherapy: evidence of resistance to apoptosis induction. Stem Cells. 2006; 24(12):2753–65.
   PubMed Web of Science ®Google Scholar