Download PDF
CC BY-NC-ND 4.0 · Eur J Dent 2009; 03(03): 240-249
DOI: 10.1055/s-0039-1697439
Original Article
Dental Investigation Society

“Opening” The Mesenchymal Stem Cell Tool Box

Fares Zeidán-Chuliá
a   Medical Biochemistry and Developmental Biology, Institute of Biomedicine, University of Helsinki, Finland
,
Mami Noda
b   Laboratory of Pathophysiology, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan
› Author Affiliations
Further Information

Publication History

Publication Date:
27 September 2019 (online)

Also available at
  PDF Download Permissions and Reprints

ABSTRACT

Adult mesenchymal stem cells (MSCs) are adherent stromal cells able to self-renew and differentiate into a wide variety of cells and tissues. MSCs can be obtained from distinct tissue sources and have turned out to be successfully manipulated in vitro. As adult stem cells, MSCs are less tumorigenic than their embryonic correlatives and posses another unique characteristic which is their almost null immunogenicity. Moreover, these cells seem to be immunosuppressive in vitro. These facts together with others became MSCs a promising subject of study for future approaches in bioengineering and cell-based therapy. On the other hand, new strategies to achieve long-term integration as well as efficient differentiation of these cells at the area of the lesion are still challenging, and the signalling pathways ruling these processes are not completely well characterized. In this review, we are going summarize the general landscape and current status of the MSC tool as well as their wide potential in tissue engineering, from neuronal to tooth replacement. Highlights and pitfalls for further clinical applications will be discussed. (Eur J Dent 2009;3:240-249)

Key words:

Adult mesenchymal stem cell - Dental pulp - Differentiation - Cell-based therapy - Tissue engineering - Tooth replacement
 

  • REFERENCES

  • 1 Preston SL , Alison MR , Forbes SJ, Direkze NC, Poulsom R, Wright NA. The new stem cell biology: something for everyone. J Clin Pathol: Mol Pathol 2003;56:86-96.
  • 2 Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
  • 3 Nakagami H, Morishita R, Maeda K, Kikuchi Y, Ogihara T, Kaneda Y. Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 2006;13:77-81.
  • 4 Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003;100:5807-5812.
  • 5 Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004;103:1669-1675.
  • 6 da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006;119:2204-2213.
  • 7 Meirelles Lda S, Nardi NB. Methodology, biology and clinical applications of mesenchymal stem cells. Front Biosci 2009;14:4281-4298.
  • 8 Haniffa MA, Collin MP, Buckley CD, Dazzi F. Mesenchymal stem cells: the fibroblasts� new clothes? Haematologica 2009;94:258-263.
  • 9 Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A; the International Society for Cellular Therapy. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005;7:393-395.
  • 10 Valtieri M, Sorrentino A. The mesenchymal stromal cell contribution to homeostasis. J Cell Physiol 2008;217:296-300.
  • 11 Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
  • 12 Takahashi K, Tanabe K, Ohnuki M, Ichisaka T, Tomoda K Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
  • 13 Yamanaka S. A fresh look to iPS cells. Cell 2009;137:13-17.
  • 14 Zhou H, Wu S, Joo J, Zhu S, Han D, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer H, Duan L, Ding S. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009, doi:10.1016/j. stem.2009.04.005.
  • 15 Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 2006;36:2566-2573.
  • 16 Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
  • 17 Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res 2006;312:2169-2179.
  • 18 Chang CJ, Yen ML, Chen YC Chien CC, Huang HI, Bai CH, Yen BL. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-��. Stem Cells 2006;24:2466-2477.
  • 19 Le Blanc K, Tammik C, Rosendhal K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003;31:890-896.
  • 20 Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, Galun E, Rachmilewitz J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005;105:2214-2219.
  • 21 Rasmusson I, Ringden O, Sundberg B, Le Blanc K. -Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 2003; 76:1208-1213.
  • 22 Taivan M, Zheng B, Oberlin E, Crisan M, Sun B, Huard J, Peault B. The vascular wall as a source of stem cells. Ann NY Acad Sci 2005;1044:41-50.
  • 23 Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S. The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 2005;8:191-199.
  • 24 Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005;33:1402-1416. Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S. Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 2008;26:1787-1795.
  • 26 Zhang W, Walboomers XF, Van Kuppevelt TH, Daamen WF, Van Damme PA, Bian Z, Jansen JA. In vivo evaluation of human dental pulp stem cells differentiated towards multiple lineages. J Tissue Eng Regen Med 2008;2:117-125.
  • 27 Bieback K, Kern S, Koca�mer A, Ferlik K, Bugert P. Comparing mesenchymal stromal cells from different human tissues: bone marrow, adipose tissue and umbilical cord blood. Biomed Mater Eng 2008;18:S71-S76.
  • 28 Mitsiadis TA, Rahiotis C. Parallels between tooth development and repair: conserved molecular mechanisms following carious and dental injury. J Dent Res 2004;83:896-902.
  • 29 Arana-Chavez VE, Massa LF. Odontoblast: the cells forming and maintaining dentine. Int J Biochem Cell Biol 2004;36:1367-1373.
  • 30 Murray PE, About I, Franquin JC, Remusat M, Smith AJ. Restorative pulpal and repair responses. J Am Dent Assoc 2001;132:482-491.
  • 31 Huang GT, Sonoyama W, Liu Y, Liu H, Wang S, Shi S. The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. J Endod 2008;34:645-651.
  • 32 Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 2000;97:13625-13630.
  • 33 Wei X, Ling J, Wu L, Liu L, Xiao Y. Expression of mineralization markers in dental pulp cells. J Endod 2007;33:703-708.
  • 34 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.
  • 35 Le Blanc K, Pittenger M. Mesenchymal stem cells: progress toward promise. Cytotherapy 2005;7:36-45.
  • 36 Caplan AI. Why are MSCs therapeutic? New data: new insight. J Pathol 2009;217:318-324.
  • 37 Moioli EK, Clark PA, Xin X, Lal S, Mao JJ. Matrices and scaffolds for drug delivery in dental, oral and craniofacial tissue engineering. Adv Drug Deliv Rev 2007;59:308-324.
  • 38 Oh S, Brammer KS, Li YS, Teng D, Engler AJ, Chien S, Jin S. Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci USA 2009;106:2130-2135.
  • 39 Tuan RS, Boland G, Tuli R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 2003;5:32-45.
  • 40 Zietlow R, Lane EL, Dunnett SB, Rosser AE. Human stem cells for CNS repair. Cell Tissue Res 2008;331:301-322.
  • 41 Rosser AE, Zietlow R, Dunnett SB. Stem cell transplantation for neurodegenerative diseases. Curr Opin Neurol 2007;20:668-692.
  • 42 Chen J, Li Y, Wang L, Lu M, Zhang X, Chopp M. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 2001;189:49-57.
  • 43 Mazzini L, Fagioli F, Boccaletti R, Mareschi K, Oliveri G, Oliveri C, Pastore I, Marasso R, Madon E. Stem cell therapy in amyotrophic lateral sclerosis: a methodological approach in humans. Amyotroph Lateral Scler Other Motor Neuron Disord 2003;4:158-161.
  • 44 Leme RJ, Chadi G. Distant microglial and astroglial activation secondary to experimental spinal cord lesion. Arq Neuropsiquiatr 2001;59:483-492.
  • 45 KarnezisT, Mandemakers W, McQualter JL, Zheng B, Ho PP, Jordan KA, Murray BM, Barres B, Tessier-Lavigne M, Bernard CC. The neurite outgrowth inhibitor Nogo A is involved in autoimmune-mediated demyelination. Nat Neurosci 2004;7:736-744.
  • 46 Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA 2002;99:2199-2204.
  • 47 Breitbach M, Bostani T, Roell W, Xia Y, Dewald O, Nygren JM, Fries JW, Tiemann K, Bohlen H, Hescheler J, Welz A, Bloch W, Jacobsen SE, Fleischmann BK. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 2007;110:1362-1369.
  • 48 Kale S, Karihaloo A, Clark PR, Kashgarian M, Krause DS, Cantley LG. Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J Clin Invest 2003;112:42-49.
  • 49 Gupta S, Verfaillie C, Chmielewski D, Kim Y, Rosenberg ME. A role for extrarenal cells in the regeneration following acute renal failure. Kidney Int 2002;62:1285-1290.
  • 50 Poulsom R, Forbes SJ, Hodivala-Dilke K, Ryan E, Wyles S, Navaratnarasah S, Jeffery R, Hunt T, Alison M, Cook T, Pusey C, Wright NA. Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 2001;195:229-235.
  • 51 Morigi M, Introna M, Imberti B, Corna D, Abbate M, Rota C, Rottoli D, Benigni A, Perico N, Zoja C, Rambaldi A, Remuzzi A, Remuzzi G. Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 2008;26:2075-2082.
  • 52 Herrera MB, Bussolati B, Bruno S, Morando L, Mauriello-Romanazzi G, Sanavio F, Stamenkovic I, Biancone L, Camussi G. Exogenous mesenchymal stem cells localize to the kidney by means of CD44 following acute tubular injury. Kidney Int 2007;72:430-441.
  • 53 Ninichuk V, Gross O, Segerer S, Hoffmann R, Radomska E, Buchstaller A, Huss R, Akis N, Schl�ndorff D, Anders HJ. Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int 2006;70:121-129.
  • 54 Rosa SB, Voltarelli JC, Chies JA, Pranke P. The use of stem cells for the treatment of autoimmune diseases. Braz J Med Biol Res 2007;40:1579-1597.
  • 55 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.
  • 56 Gazdag AR, Lane JM, Glaser D, Forster RA. Alternatives to Autogenous Bone Graft: Efficacy and Indications. J Am Acad Orthop Surg 1995;3:1-8.
  • 57 M�ller I, Lymperi S, Dazzi F. Mesenchymal stem cell therapy for degenerative inflammatory disorders. Curr Opin Organ Transplant 2008; 13:639-644.
  • 58 Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084.
  • 59 Tsuchiya H, Sugiura F, Ishiguro N. Chondrogenesis enhanced by overexpression of sox9 gene in mouse bone marrow-derived mesenchymal stem cells. Biochem Biophys Res Commun 2003;301:338-343.
  • 60 Ling L, Nurcombe V, Cool SM. Wnt signaling controls the fate of mesenchymal stem cells. Gene 2009;433:1-7.
  • 61 Baksh D, Tuan RS. Canonical and non-canonical Wnts differentially affect the development potential of primary isolate of human bone marrow mesenchymal stem cells. J Cell Physiol 2007;212:817-826.
  • 62 Zhou S, Eid K, Glowacki J. Cooperation between TGFbeta and Wnt pathways during chondrocyte and adipocyte differentiation of human marrow stromal cells. J Bone Miner Res 2004;19:463-470.
  • 63 Raghunath J, Salacinski HJ, Sales KM, Butler PE, Seifalian AM. Advancing cartilage tissue engineering: the application of stem cell technology. Curr Opin Biotechnol 2005;16:503-509.
  • 64 Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 2006;367:1747-1757.
  • 65 Fonarow GC. Heart failure: recent advances in prevention and treatment. Rev Cardiovasc Med 2000;1:25-33, 54.
  • 66 Fedak PW, Verma S, Weidel RD, Li RK. Cardiac remodeling and failure: from molecules to man (Part I). Cardiovasc Pathol 2005;14:1-11.
  • 67 Strauer BE, Schannwell CM, Brehm M. Therapeutic potentials of stem cells in cardiac diseases. Minerva Cardioangiol 2009;57:249-267.
  • 68 Laflamme MA, Murry CE. Regenerating the heart. Nat Biotechnol 2005;23:845-856.
  • 69 Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci USA 2001;98:10344-10349.
  • 70 Erices AA, Allers CI. Conget PA, Rojas CV, Minguell JJ. Human cord blood-derived mesenchymal stem cells home and survive in the marrow of immunodeficient mice after systemic infusion. Cell Transplant 2003;12:555-561.
  • 71 Shim WS, Jiang S, Wong P, Tan J, Chua YL, Tan YS, Sin YK, Lim CH, Chua T, Teh M, Liu TC, Sim E. Ex vivo differentiation of human adult bone marrow stem cells into cardiomyocyte-like cells. Biochem Biophys Res Commun 2004;324:481-488.
  • 72 Xu W, Zhang X, Qian H, Zhu W, Sun X, Hu J, Zhou H, Chen Y. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med 2004;229:623-631.
  • 73 Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006;12:459-465.
  • 74 Martin P. Wound healing--aiming for perfect skin regeneration. Science 1997;276:75-81.
  • 75 Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999;341:738-746.
  • 76 Andersen CA, Roukis TS. The diabetic foot. Surg Clin North Am 2007;87:1149-1177.
  • 77 Armstrong DG, Lipsky BA. Diabetic foot infections: stepwise medical and surgical management. Int Wound J 2004;1:123-132.
  • 78 Li H, Fu X, Ouyang Y, Cai C, Wang J, Sun T. Adult bonemarrow-derived mesenchymal stem cells contribute to wound healing of skin appendages. Cell Tissue Res 2006;326:725-736.
  • 79 Liu P, Deng Z, Han S, Liu T, Wen N, Lu W, Geng X, Huang S, Jin Y. Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs 2008;32:925-931.
  • 80 Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007;25:2648-2659.
  • 81 Amar S, Han X. The impact of periodontal infection on systemic diseases. Med Sci Monit 2003; 9(12):RA291-9.
  • 82 Yen AH, Sharpe PT. Regeneration of teeth using stem cellbased tissue engineering. Expert Opin Biol Ther 2006;6:9-16.
  • 83 Duailibi SE, Duailibi MT, Zhang W, Asrican R, Vacanti JP, Yelick PC. Bioengineered dental tissues grown in the rat jaw. J Dent Res 2008;87:745-750.
  • 84 Ferreira CF, Magini RS, Sharpe PT. Biological tooth replacement and repair. J Oral Rehabil 2007;34:933-939.
  • 85 Bianco P, Robey PG. Stem cells in tissue engineering. Nature 2001;414:118-121.
  • 86 Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 2006;27:3413-3431.
  • 87 Yu J, Deng Z, Shi J, Zhai H, Nie X, Zhuang H, Li Y, Jin Y. Differentiation of dental pulp stem cells into regularshaped dentin-pulp complex induced by tooth germ cell conditioned medium. Tissue Eng 2006;12:3097-3105.
  • 88 Gronthos S, Akintoye SO, Wang CY, Shi S. Bone marrow stromal stem cells for tissue engineering. Periodontol 2000 2006;41:188-195.
  • 89 Liu H, Gronthos S, Shi S. Dental pulp stem cells. Methods Enzymol 2006;419:99-113.
  • 90 Hu B, Unda F, Bopp-Kuchler S, Jimenez L Wang XJ, Ha�kel Y, Wang SL, Lesot H. Bone marrow cells can give rise to ameloblast-like cells. J Dent Res 2006;85:416-421.
  • 91 Iohara K, Nakashima M, Ito M, Ishikawa M, Nakasima A, Akamine A. Dentin regeneration by dental pulp stem cell therapy with recombinant human bone morphogenetic protein 2. J Dent Res 2004;83:590-595.
  • 92 Yu J, Wang Y, Deng Z, Tang L, Li Y, Shi J, Jin Y. Odontogenic capability: bone marrow stromal stem cells versus dental pulp stem cells. Biol Cell 2007;99:465-474.
  • 93 Yu J, Shi J, Jin Y. Current approaches and challenges in making a bio-tooth. Tissue Eng Part B Rev 2008;14:307-319.