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Identifying a molecular phenotype for bone marrow stromal cells with in vivo bone-forming capacity

  1. Kenneth H Larsen1,
  2. Casper M Frederiksen1,
  3. Jorge S Burns1,
  4. Basem M Abdallah1,
  5. Moustapha Kassem1,2,*

Article first published online: 14 DEC 2009

DOI: 10.1359/jbmr.091018

Issue

Journal of Bone and Mineral Research

Journal of Bone and Mineral Research

Volume 25, Issue 4, pages 796–808, April 2010

Additional Information

How to Cite

Larsen, K. H., Frederiksen, C. M., Burns, J. S., Abdallah, B. M. and Kassem, M. (2010), Identifying a molecular phenotype for bone marrow stromal cells with in vivo bone-forming capacity. J Bone Miner Res, 25: 796–808. doi: 10.1359/jbmr.091018

Author Information

  1. 1

    Laboratory for Molecular Endocrinology (KMEB), Department of Endocrinology, University Hospital of Odense and Medical Biotechnology Center, University of Southern Denmark, Odense C, Denmark

  2. 2

    Stem Cell Unit, Department of Anatomy, College of Medicine, King Saud University, KSA

*University Department of Endocrinology and Metabolism, University Hospital of Odense, Kloevervaenget 6, 4th floor, DK-5000 Odense C, Denmark.

Publication History

  1. Issue published online: 9 APR 2010
  2. Article first published online: 14 DEC 2009
  3. Accepted manuscript online: 27 JAN 2010 12:00AM EST
  4. Manuscript Accepted: 9 OCT 2009
  5. Manuscript Revised: 8 JUL 2009
  6. Manuscript Received: 2 OCT 2008

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References

  • 1
    Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008; 2: 313–319.
  • 2
    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.
  • 3
    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: 1453–1458.
    Direct Link:
  • 4
    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: 1335–1347.
    Direct Link:
  • 5
    Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284: 143–147.
  • 6
    Abdallah BM, Kassem M. Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther. 2008; 15: 109–116.
  • 7
    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: 385–386.
  • 8
    Robey PG, Bianco P. The use of adult stem cells in rebuilding the human face. J Am Dent Assoc. 2006; 137: 961–972.
  • 9
    Parfitt AM. Bone forming cells in clinical conditions. In: HallBK, ed. In Bone, The Osteoblast and Osteocyte. London: Telford Press; 1991: 351–426.
  • 10
    Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003; 425: 841–846.
  • 11
    Aubin JE, Triffitt JT. Mesenchymal stem cells and osteoblast differentiation. In: BilezikianJP, RaiszLG, RodanGA, eds. The Principles of Bone Biology, 2nd edition. San Diego, CA: Academic Press; 2002: 59–81.
  • 12
    Rodan GA, Noda M. Gene expression in osteoblastic cells. Crit Rev Eukaryot Gene Expr. 1991; 1: 85–98.
  • 13
    Abdallah BM, Ditzel N, Kassem M. Assessment of bone formation capacity using in vivo transplantation assays: procedure and tissue analysis. Methods Mol Biol. 2008; 455: 89–100.
  • 14
    Dennis JE, Konstantakos EK, Arm D, Caplan AI. In vivo osteogenesis assay: a rapid method for quantitative analysis. Biomaterials. 1998; 19: 1323–1328.
  • 15
    Mankani MH, Kuznetsov SA, Fowler B, Kingman A, Robey PG. In vivo bone formation by human bone marrow stromal cells: effect of carrier particle size and shape. Biotechnol Bioeng. 2001; 72: 96–107.
    Direct Link:
  • 16
    Stenderup K, Rosada C, Justesen J, Al-Soubky T, Gnaes-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.
  • 17
    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–R1315.
  • 18
    Qi H, Aguiar DJ, Williams SM, La PA, Pan W, Verfaillie CM. Identification of genes responsible for osteoblast differentiation from human mesodermal progenitor cells. Proc Natl Acad Sci USA. 2003; 100: 3305–3310.
  • 19
    Scheideler M, Elabd C, Zaragosi LE, et al. Comparative transcriptomics of human multipotent stem cells during adipogenesis and osteoblastogenesis. BMC Genomics. 2008; 9: 340.
  • 20
    Schilling T, Noth U, Klein-Hitpass L, Jakob F, Schutze N. Plasticity in adipogenesis and osteogenesis of human mesenchymal stem cells. Mol Cell Endocrinol. 2007; 271: 1–117.
  • 21
    Song L, Webb NE, Song Y, Tuan RS. Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells. 2006; 24: 1707–1718.
    Direct Link:
  • 22
    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: 527–538.
  • 23
    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: 592–596.
  • 24
    Qiu W, Andersen TE, Bollerslev J, Mandrup S, Abdallah BM, Kassem M. Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells. J Bone Miner Res. 2007; 22: 1720–1731.
    Direct Link:
  • 25
    Frederiksen CM, Knudsen S, Laurberg S, Orntoft TF. Classification of Dukes' B and C colorectal cancers using expression arrays. J Cancer Res Clin Oncol. 2003; 129: 263–271.
  • 26
    Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003; 31.
  • 27
    Al-Shahrour F, Minguez P, Vaquerizas JM, Conde L, Dopazo J. BABELOMICS: a suite of Web tools for functional annotation and analysis of groups of genes in high-throughput experiments. Nucleic Acids Res. 2005; 33.
  • 28
    Gollner H, Dani C, Phillips B, Philipsen S, Suske G. Impaired ossification in mice lacking the transcription factor Sp3. Mech Dev. 2001; 106: 77–83.
  • 29
    Chan YM, Bonnemann CG, Lidov HG, Kunkel LM. Molecular organization of sarcoglycan complex in mouse myotubes in culture. J Cell Biol. 1998; 143: 2033–2044.
  • 30
    Liu LA, Engvall E. Sarcoglycan isoforms in skeletal muscle. J Biol Chem. 1999; 274: 38171–38176.
  • 31
    Heyninck K, Beyaert R. Crosstalk between NF-κB-activating and apoptosis-inducing proteins of the TNF-receptor complex. Mol Cell Biol Res Commun. 2001; 4.
  • 32
    Hildebrand A, Romaris M, Rasmussen LM, et al. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor β. Biochem J. 1994; 302: 527–534.
  • 33
    Corsi A, Xu T, Chen XD, et al. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res. 2002; 17: 1180–1189.
    Direct Link:
  • 34
    Reinboth B, Hanssen E, Cleary EG, Gibson MA. Molecular interactions of biglycan and decorin with elastic fiber components: biglycan forms a ternary complex with tropoelastin and microfibril-associated glycoprotein 1. J Biol Chem. 2002; 277: 3950–3957.
  • 35
    Trask BC, Trask TM, Broekelmann T, Mecham RP. The microfibrillar proteins MAGP-1 and fibrillin-1 form a ternary complex with the chondroitin sulfate proteoglycan decorin. Mol Biol Cell. 2000; 11: 1499–1507.
  • 36
    Raouf A, Ganss B, McMahon C, Vary C, Roughley PJ, Seth A. Lumican is a major proteoglycan component of the bone matrix. Matrix Biol. 2002; 21.
  • 37
    Raouf A, Seth A. Discovery of osteoblast-associated genes using cDNA microarrays. Bone. 2002; 30: 463–471.
  • 38
    Kim MS, Kim SS, Jung ST, et al. Expression and purification of enzymatically active forms of the human lysyl oxidase-like protein 4. J Biol Chem. 2003; 278: 52071–52074.
  • 39
    Maki JM, Sormunen R, Lippo S, Kaarteenaho-Wiik R, Soininen R, Myllyharju J. Lysyl oxidase is essential for normal development and function of the respiratory system and for the integrity of elastic and collagen fibers in various tissues. Am J Pathol. 2005; 167: 927–936.
  • 40
    Wakitani S, Saito T, Caplan AI. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve. 1995; 18: 1417–1426.
    Direct Link:
  • 41
    Wewer UM, Ibaraki K, Schjorring P, Durkin ME, Young MF, Albrechtsen R. A potential role for tetranectin in mineralization during osteogenesis. J Cell Biol. 1994; 127: 1767–1775.
  • 42
    Potter LR, Bbey-Hosch S, Dickey DM. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev. 2006; 27: 47–72.
  • 43
    Matsukawa N, Grzesik WJ, Takahashi N, et al. The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc Natl Acad Sci USA. 1999; 96: 7403–7408.
  • 44
    Jaubert J, Jaubert F, Martin N, et al. Three new allelic mouse mutations that cause skeletal overgrowth involve the natriuretic peptide receptor C gene (Npr3). Proc Natl Acad Sci USA. 1999; 96: 10278–10283.
  • 45
    Hagiwara H, Inoue A, Yamaguchi A, et al. cGMP produced in response to ANP and CNP regulates proliferation and differentiation of osteoblastic cells. Am J Physiol. 1996; 270: C1311–C1318.
  • 46
    Simonet WS, Lacey DL, Dunstan CR, et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997; 89: 309–319.
  • 47
    Simeone A, Acampora D, Pannese M, et al. Cloning and characterization of two members of the vertebrate Dlx gene family. Proc Natl Acad Sci USA. 1994; 91: 2250–2254.
  • 48
    Lee MH, Kim YJ, Yoon WJ, et al. Dlx5 specifically regulates Runx2 type II expression by binding to homeodomain-response elements in the Runx2 distal promoter. J Biol Chem. 2005; 280: 35579–35587.
  • 49
    Puppin C, Fabbro D, Dima M, et al. High periostin expression correlates with aggressiveness in papillary thyroid carcinomas. J Endocrinol. 2008; 197: 401–408.
  • 50
    Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD. Periostin secreted by epithelial ovarian carcinoma is a ligand for α(V)β(3) and α(V)β(5) integrins and promotes cell motility. Cancer Res. 2002; 62: 5358–5364.
  • 51
    Takeshita S, Kikuno R, Tezuka K, Amann E. Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J. 1993; 294: 271–278.
  • 52
    Rios H, Koushik SV, Wang H, et al. Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol. 2005; 25: 11131–11144.
  • 53
    Coutu DL, Wu JH, Monette A, Rivard GE, Blostein MD, Galipeau J. Periostin: a member of a novel family of vitamin K–dependent proteins is expressed by mesenchymal stromal cells. J Biol Chem. 2008; 283: 17991–18001.
  • 54
    Theill LE, Boyle WJ, Penninger JM. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu Rev Immunol. 2002; 20: 795–823.
  • 55
    Mann GN, Jacobs TW, Buchinsky FJ, et al. Interferon-γ causes loss of bone volume in vivo and fails to ameliorate cyclosporin A–induced osteopenia. Endocrinology. 1994; 135: 1077–1083.
  • 56
    Nanes M, Rubin J, Titus L, Hendy G, Catherwood B. Interferon-γ inhibits 1,25-dihydroxyvitamin D3–stimulated synthesis of bone GLA protein in rat osteosarcoma cells by a pretranslational mechanism. Endocrinology. 1990; 127: 588–594.
  • 57
    Takayanagi H, Sato K, Takaoka A, Taniguchi T. Interplay between interferon and other cytokine systems in bone metabolism. Immunol Rev. 2005; 208: 181–193.
    Direct Link:
  • 58
    Sacchetti B, Funari A, Michienzi S, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007; 131: 324–336.
  • 59
    Liu F, Malaval L, Aubin JE. Global amplification polymerase chain reaction reveals novel transitional stages during osteoprogenitor differentiation. J Cell Sci. 2003; 116: 1787–1796.
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