You have full text access to this OnlineOpen article

Age-related impairment of mesenchymal progenitor cell function

  1. Alexandra Stolzing1,
  2. Andrew Scutt1,2

Article first published online: 26 APR 2006

DOI: 10.1111/j.1474-9726.2006.00213.x

Issue

Aging Cell

Aging Cell

Volume 5, Issue 3, pages 213–224, June 2006

Additional Information

How to Cite

Stolzing, A. and Scutt, A. (2006), Age-related impairment of mesenchymal progenitor cell function. Aging Cell, 5: 213–224. doi: 10.1111/j.1474-9726.2006.00213.x

Author Information

  1. 1

    Centre for Biomaterials and Tissue Engineering, Department of Engineering Materials, and

  2. 2

    Division of Clinical Sciences South, University of Sheffield, North Campus, Sheffield S37HQ, UK

* A. Stolzing, University of Sheffield, North Campus, Kroto Research Institute, Broad Lane, Sheffield S3 7HQ, UK. Tel.: 01142225931; fax: 01142225945; e-mail: stolzing@gmail.com

Publication History

  1. Issue published online: 26 APR 2006
  2. Article first published online: 26 APR 2006
  3. Accepted for publication 9 February 2006

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (473K)

References

  • Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815–1822.
  • Artandi SE, Attardi LD (2005) Pathways connecting telomeres and p53 in senescence, apoptosis, and cancer. Biochem. Biophys. Res. Commun. 331, 881–890.
  • Banfi A, Bianchi G, Notaro R, Luzzatto L, Cancedda R, Quarto R (2002) Replicative aging and gene expression in long-term cultures of human bone marrow stromal cells. Tissue Eng. 8, 901–910.
  • Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I (2004) Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22, 675–682.
    Direct Link:
  • Bentley SA (1982) Bone marrow connective tissue and the haemopoietic microenvironment. Br. J. Haematol. 50, 1–6.
    Direct Link:
  • Bergman RJ, Gazit D, Kahn AJ, Gruber H, McDougall S, Hahn TJ (1996) Age-related changes in osteogenic stem cells in mice. J. Bone Miner Res. 11, 568–577.
    Direct Link:
  • Brockbank KG, Ploemacher RE, Van Peer CM (1983) An in vitro analysis of murine hemopoietic fibroblastoid progenitors and fibroblastoid cell function during aging. Mech. Ageing Dev. 22, 11–21.
  • Buege JA, Aust. SD (1978) Microsomal lipid peroxidation. Meth. Enzymol. 52, 302–310.
  • Buss H, Chan TP, Sluis KB, Domigan NM, Winterbourn CC (1997) Protein carbonyl measurement by a sensitive ELISA method. Free Radic. Biol. Med. 23, 361–366.
  • Campisi J (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120, 513–522.
  • Chen LC, Pace JL, Russell SW, Morrison DC (1996) Altered regulation of inducible nitric oxide synthase expression in macrophages from senescent mice. Infect. Immun. 64, 4288–4298.
  • Colter DC, Sekiya I, Prockop DJ (2001) Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl Acad. Sci. U S A 98, 7841–7845.
  • Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575–1577.
  • D’Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC (2004) Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J. Cell Sci. 117, 2971–2981.
  • Davies J, Chambers TJ (2004) Parathyroid hormone activates adhesion in bone marrow stromal precursor cells. J. Endocrinol. 180, 505–513.
  • De Haan JB, Crack PJ, Flentjar N, Iannello RC, Hertzog PJ, Kola I (2003) An imbalance in antioxidant defense affects cellular function: the pathophysiological consequences of a reduction in antioxidant defense in the glutathione peroxidase-1 (Gpx1) knockout mouse. Redox Rep. 8, 69–79.
  • Deans RJ, Moseley AB (2000) Mesenchymal stem cells: biology and potential clinical uses. Exp. Hematol. 28, 875–884.
  • Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, Dimmeler S (2004) Antioxidative stress-associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104, 3591–3597.
  • Devine SM, Hoffman R (2000) Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr. Opin. Hematol. 7, 358–363.
  • Digirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ (1999) 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. 107, 275–281.
    Direct Link:
  • Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linsken M, Rubelj I, Pereira-Smith O (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl Acad. Sci. U S A 92, 9363–9367.
  • Dobson KR, Reading L, Haberey M, Marine X, Scutt A (1999) Centrifugal isolation of bone marrow from bone: an improved method for the recovery and quantitation of bone marrow osteoprogenitor cells from rat tibiae and femurae. Calcif Tissue Int. 65, 411–413.
  • Erben RG, Bromm S, Stangassinger M (1998) Therapeutic efficacy of 1alpha,25-dihydroxyvitamin D3 and calcium in osteopenic ovariectomized rats: evidence for a direct anabolic effect of 1alpha,25-dihydroxyvitamin D3 on bone. Endocrinology 139, 4319–4328.
  • Foreman KE, Tang J (2003) Molecular mechanisms of replicative senescence in endothelial cells. Exp. Gerontol. 38, 1251–1257.
  • Friedenstein AJ (1976) Precursor cells of mechanocytes. Int. Rev. Cytol. 47, 327–359.
  • Gieche J, Mehlhase J, Licht A, Zacke T, Sitte N, Grune T (2001) Protein oxidation and proteolysis in RAW264.7 macrophages: effects of PMA activation. Biochim. Biophys. Acta 1538, 321–328.
  • Globerson A (1997) Thymocytopoiesis in aging: the bone marrow-thymus axis. Arch. Gerontol. Geriatr. 24, 141–155.
  • Gregory CD, Devitt A (2004) The macrophage and the apoptotic cell: an innate immune interaction viewed simplistically? Immunology 113, 1–14.
    Direct Link:
  • Grinnemo KH, Mansson A, Dellgren G, Klingberg D, Wardell E, Drvota V, Tammik C, Holgersson J, Ringden O, Sylven C, Le Blanc K (2004) Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium. J. Thorac. Cardiovasc. Surg. 127, 1293–1300.
  • Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298–300.
  • He T, Peterson TE, Holmuhamedov EL, Terzic A, Caplice NM, Oberley LW, Katusic ZS (2004) Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler Thromb. Vasc. Biol. 24, 2021–2027.
  • Hitchon CA, El-Gabalawy HS (2004) Oxidation in rheumatoid arthritis. Arthritis Res. Ther. 6, 265–278.
  • Hoffman R, Tong J, Brandt J, Traycoff C, Bruno E, McGuire BW, Gordon MS, McNiece I, Srour EF (1993) The in vitro and in vivo effects of stem cell factor on human hematopoiesis. Stem Cells 11 (Suppl. 2), 76–82.
  • Huang H, Manton KG (2004) The role of oxidative damage in mitochondria during aging: a review. Front. Biosci. 9, 1100–1117.
  • Hung SC, Chen NJ, Hsieh SL et al. (2002) Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells 20, 249–258.
    Direct Link:
  • Inoue M, Sato EF, Nishikawa M, Park AM, Kira Y, Imada I, Utsumi K (2003) Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr. Med. Chem. 10, 2495–2505.
  • Itahana K, Campisi J, Dimri GP (2004) Mechanisms of cellular senescence in human and mouse cells. Biogerontology 5, 1–10.
  • Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR (2002) A stem cell molecular signature. Science 298, 601–604.
  • Jung K, Henke W (1996) Developmental changes of antioxidant enzymes in kidney and liver from rats. Free Radic. Biol. Med. 20, 613–617.
  • Kadiyala S, Young RG, Thiede MA, Bruder SP (1997) Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro. Cell Transplant 6, 125–134.
  • Kirkwood TB, Franceschi C (1992) Is aging as complex as it would appear? New perspectives in aging research. Ann. N. Y. Acad. Sci. 663, 412–417.
    Direct Link:
  • Kuznetsov SA, Friedenstein AJ, Robey PG (1997) Factors required for bone marrow stromal fibroblast colony formation in vitro. Br. J. Haematol. 97, 561–570.
    Direct Link:
  • Li JM, Shah AM (2004) Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1014–R1030.
  • De Magalhaes JP (2004) From cells to ageing: a review of models and mechanisms of cellular senescence and their impact on human ageing. Exp. Cell Res. 300, 1–10.
  • Majors AK, Boehm CA, Nitto H, Midura RJ, Muschler GF (1997) Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J. Orthop. Res. 15, 546–557.
    Direct Link:
  • Makino N, Sasaki K, Hashida K, Sakakura Y (2004) A metabolic model describing the H2O2 elimination by mammalian cells including H2O2 permeation through cytoplasmic and peroxisomal membranes: comparison with experimental data. Biochim. Biophys. Acta 1673, 149–159.
  • Martinez ME, Del Campo MT, Medina S, Sanchez M, Sanchez-Cabezudo MJ, Esbrit P, Martinez P, Moreno I, Rodrigo A, Garces MV, Munuera L (1999) Influence of skeletal site of origin and donor age on osteoblastic cell growth and differentiation. Calcif Tissue Int. 64, 280–286.
  • Mates JM, Sanchez-Jimenez F (1999) Antioxidant enzymes and their implications in pathophysiologic processes. Front. Biosci. 4, D339–D345.
  • Merker K, Stolzing A, Grune T (2001) Proteolysis, caloric restriction and aging. Mech. Ageing Dev. 122, 595–615.
  • Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin. Orthop. Relat. Res. 80, 147–154.
  • Michiels C, Raes M, Toussaint O, Remacle J (1994) Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic. Biol. Med. 17, 235–248.
  • Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F (2002) Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum. 46, 704–713.
    Direct Link:
  • Nakahara H, Dennis JE, Bruder SP, Haynesworth SE, Lennon DP, Caplan AI (1991) In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp. Cell Res. 195, 492–503.
  • Nishida S, Yamaguchi A, Tanizawa T, Endo N, Mashiba T, Uchiyama Y, Suda T, Yoshiki S, Takahashi HE (1994) Increased bone formation by intermittent parathyroid hormone administration is due to the stimulation of proliferation and differentiation of osteoprogenitor cells in bone marrow. Bone 15, 717–723.
  • Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE (1999) Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J. Bone Miner. Metab. 17, 171–177.
  • Oreffo RO, Bord S, Triffitt JT (1998) Skeletal progenitor cells and ageing human populations. Clin. Sci. (Lond.) 94, 549–555.
  • Pelicano H, Carney D, Huang P (2004) ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 7, 97–110.
  • Pelicci PG (2004) Do tumor-suppressive mechanisms contribute to organism aging by inducing stem cell senescence? J. Clin. Invest. 113, 4–7.
  • Pendergrass WR, Li Y, Jiang D, Fei RG, Wolf NS (1995) Caloric restriction: conservation of cellular replicative capacity in vitro accompanies life-span extension in mice. Exp. Cell Res. 217, 309–316.
  • Piacibello W, Gammaitoni L, Pignochino Y (2005) Proliferative senescence in hematopoietic stem cells during ex-vivo expansion. Folia. Histochem. Cytobiol. 43, 197–202.
  • Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143–147.
  • Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A (2003) Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes 52, 2795–2804.
  • Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA (2002) ‘Stemness’: transcriptional profiling of embryonic and adult stem cells. Science 298, 597–600.
  • Rao MS, Mattson MP (2001) Stem cells and aging: expanding the possibilities. Mech. Ageing Dev. 122, 713–734.
  • Ringe J, Kaps C, Schmitt B, Buscher K, Bartel J, Smolian H, Schultz O, Burmester GR, Haupl T, Sittinger M (2002) Porcine mesenchymal stem cells. Induction of distinct mesenchymal cell lineages. Cell Tissue Res. 307, 321–327.
  • Scutt A, Bertram P (1995) Bone marrow cells are targets for the anabolic actions of prostaglandin E2 on bone: induction of a transition from nonadherent to adherent osteoblast precursors. J. Bone Miner. Res. 10, 474–487.
    Direct Link:
  • Scutt A, Kollenkirchen U, Bertram P (1996a) Effect of age and ovariectomy on fibroblastic colony-forming unit numbers in rat bone marrow. Calcif. Tissue Int. 59, 309–310.
  • Scutt A, Bertram P, Brautigam M (1996b) The role of glucocorticoids and prostaglandin E2 in the recruitment of bone marrow mesenchymal cells to the osteoblastic lineage: positive and negative effects. Calcif. Tissue Int. 59, 154–162.
  • Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ (2002) Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20, 530–541.
    Direct Link:
  • Serra V, Grune T, Sitte N, Saretzki G, Von Zglinicki T (2000) Telomere length as a marker of oxidative stress in primary human fibroblast cultures. Ann. N. Y. Acad. Sci. 908, 327–330.
    Direct Link:
  • Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ (2000) Is β-galactosidase staining a marker of senescence in vitro and in vivo? Exp. Cell Res. 257, 162–171.
  • Singh R, Pathak DN (1990) Lipid peroxidation and glutathione peroxidase, glutathione reductase, superoxide dismutase, catalase, and glucose-6-phosphate dehydrogenase activities in FeCl3-induced epileptogenic foci in the rat brain. Epilepsia 31, 15–26.
    Direct Link:
  • Sitte N, Merker K, Grune T (1998) Proteasome-dependent degradation of oxidized proteins in MRC-5 fibroblasts. FEBS Lett. 440, 399–402.
  • Spees JL, Olson SD, Ylostalo J, Lynch PJ, Smith J, Perry A, Peister A, Wang MY, Prockop DJ (2003) Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma. Proc. Natl Acad. Sci. U S A 100, 2397–2402.
  • Stein GS, Lian JB, Owen TA (1990) Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J. 4, 3111–3123.
  • Stenderup K, Justesen J, Clausen C, Kassem M (2003) Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33, 919–926.
  • Stenderup K, Justesen J, Eriksen EF, Rattan SI, Kassem M (2001) Number and proliferative capacity of osteogenic stem cells are maintained during aging and in patients with osteoporosis. J. Bone Miner. Res. 16, 1120–1129.
    Direct Link:
  • Still K, Scutt A (2001) Stimulation of CFU-f formation by prostaglandin E2 is mediated in part by its degradation product, prostaglandin A2. Prostaglandins Other Lipid Mediat. 65, 21–31.
  • Stolzing A, Sethe S, Grune T (2005) Chronically active: activation of microglial proteolysis in ageing and neurodegeneration. Redox. Rep. 10, 207–213.
  • Strubing C, Ahnert-Hilger G, Shan J, Wiedenmann B, Hescheler J, Wobus AM (1995) Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev. 53, 275–287.
  • Tanaka S, Sakai A, Tanaka M, Otomo H, Okimoto N, Sakata T, Nakamura T (2004) Skeletal unloading alleviates the anabolic action of intermittent PTH(1-34) in mouse tibia in association with inhibition of PTH-induced increase in c-fos mRNA in bone marrow cells. J. Bone Miner. Res. 19, 1813–1820.
    Direct Link:
  • Torella D, Rota M, Nurzynska D, Musso E, Monsen A, Shiraishi I, Zias E, Walsh K, Rosenzweig A, Sussman MA, Urbanek K, Nadal-Ginard B, Kajstura J, Anversa P, Leri A (2004) Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ. Res. 94, 514–524.
  • Tsuboi I, Morimoto K, Horie T, Mori KJ (1991) Age-related changes in various hemopoietic progenitor cells in senescence-accelerated (SAM-P) mice. Exp. Hematol. 19, 874–877.
  • Vaziri H, Dragowska W, Allsopp RC, Thomas TE, Harley CB, Lansdorp PM (1994) Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age. Proc. Natl Acad. Sci. U S A 91, 9857–9860.
  • Wautier MP, Massin P, Guillausseau PJ, Huijberts M, Levy B, Boulanger E, Laloi-Michelin M, Wautier JL (2003) N (carboxymethyl) lysine as a biomarker for microvascular complications in type 2 diabetic patients. Diabetes Metab. 29, 44–52.
  • Weinreb M, Grosskopf A, Shir N (1999) The anabolic effect of PGE2 in rat bone marrow cultures is mediated via the EP4 receptor subtype. Am. J. Physiol. 276, E376–E383.
  • Ying QL, Nichols J, Evans EP, Smith AG (2002) Changing potency by spontaneous fusion. Nature 416, 545–548.
View Full Article (HTML) Get PDF (473K)