Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T01:09:22.111Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative Assessment of Oral Mesenchymal Stem Cells Isolated from Healthy and Diseased Tissues

Published online by Cambridge University Press:  28 August 2015

Emöke Páll ,
Adrian Florea ,
Olga Soriţău ,
Mihai Cenariu ,
Adrian S. Petruţiu  and
Alexandra Roman
Emöke Páll
Affiliation:
Department of Reproduction, Obstetrics and Veterinary Gynecology, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine, 3-5 Mănăştur St., 400372 Cluj-Napoca, Romania Department of Periodontology, Faculty of Dental Medicine, “Iuliu Haţieganu” University of Medicine and Pharmacy, 15 V. Babeş St., 400012 Cluj-Napoca, Romania
Adrian Florea*
Affiliation:
Department of Cell and Molecular Biology, Faculty of Medicine, “Iuliu Haţieganu” University of Medicine and Pharmacy, 6 L. Pasteur St., 400349 Cluj-Napoca, Romania
Olga Soriţău
Affiliation:
Laboratory of Radiotherapy, Tumor and Radiobiology, Prof. Dr. “Ion Chiricuţă” Oncology Institute, 34-36 I. Creangă St., 400015 Cluj-Napoca, Romania
Mihai Cenariu
Affiliation:
Department of Reproduction, Obstetrics and Veterinary Gynecology, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine, 3-5 Mănăştur St., 400372 Cluj-Napoca, Romania
Adrian S. Petruţiu
Affiliation:
Department of Periodontology, Faculty of Dental Medicine, “Iuliu Haţieganu” University of Medicine and Pharmacy, 15 V. Babeş St., 400012 Cluj-Napoca, Romania
Alexandra Roman
Affiliation:
Department of Periodontology, Faculty of Dental Medicine, “Iuliu Haţieganu” University of Medicine and Pharmacy, 15 V. Babeş St., 400012 Cluj-Napoca, Romania
*
*Corresponding authors. aflorea@umfcluj.ro; adrian_a_florea@yahoo.com
Get access

Abstract

The aim of the present study was to isolate human mesenchymal stem cells (MSCs) from palatal connective and periodontal granulation tissues and to comparatively evaluate their properties. MSCs were isolated using the explant culture method. Adherence to plastic, specific antigen makeup, multipotent differentiation potential, functionality, and ultrastructural characteristics were investigated. The frequency of colony-forming unit fibroblasts for palatal-derived mesenchymal stem cells (pMSCs) was significantly higher than that of granulation tissue-derived mesenchymal stem cells (gtMSCs). A significantly higher population doubling time and lower migration potential were recorded for gtMSCs than for pMSCs. Both cell lines were positive for CD105, CD73, CD90, CD44, and CD49f, and negative for CD34, CD45, and HLA-DR, but the level of expression was different. MSCs from both sources were relatively uniform in their ultrastructure. Generally, both cell lines possessed a large, irregular-shaped euchromatic nucleus, and cytoplasm rich in mitochondria, lysosomes, and endoplasmic reticulum. The periphery of the plasma membrane displayed many small filopodia. MSCs from both cell lines were successfully differentiated into osteogenic, adiopogenic, and chondrogenic lineages. Both healthy and diseased tissues may be considered as valuable sources of MSCs for regenerative medicine owing to the high acceptance and fewer complications during harvesting.

Keywords

mesenchymal stem cellspalategranulation tissuedifferentiationultrastructure
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 21 , Supplement 5 , October 2015 , pp. 1249 - 1263
Copyright
© Microscopy Society of America 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al Battah, F., De Kock, J., Vanhaecke, T. & Rogiers, V. (2011). Current status of human adipose-derived stem cells: Differentiation into hepatocyte-like cells. Sci World J 11, 1568–1581.Google Scholar
Alongi, D.J., Yamaza, T., Song, Y., Fouad, A.F., Romberg, E.E., Shi, S., Tuan, R.S. & Huang, G.T. (2010). Stem/progenitor cells from inflamed human dental pulp retain tissue regeneration potential. Regen Med 5, 617–631.CrossRefGoogle ScholarPubMed
Armitage, G.C. (1999). Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4, 1–6.Google Scholar
Bakopoulou, A., Leyhausen, G., Volk, J., Tsiftsoglou, A., Garefis, P., Koidis, P. & Geurtsen, W. (2011). Assessment of the impact of two different isolation methods on the osteo/odontogenic differentiation potential of human dental stem cells derived from deciduous teeth. Calcif Tissue Int 88, 130–141.Google Scholar
Bieback, K., Kern, S., Klüter, H. & Eichler, H. (2004). Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 22, 625–634.Google Scholar
Bobis, S., Jarocha, D. & Majka, M. (2006). Mesenchymal stem cells: Characteristics and clinical applications. Folia Histochem Cytobiol 44, 215–230.Google ScholarPubMed
Boiret, N., Rapatel, C., Veyrat-Masson, R., Guillouard, L., Guérin, J.-J., Pigeon, P., Descamps, S., Boisgard, S. & Berger, M.G. (2005). Characterization of nonexpanded mesenchymal progenitor cells from normal adult human bone marrow. Exp Hematol 33, 219–225.CrossRefGoogle ScholarPubMed
Caplan, A.I. (1991). Mesenchymal stem cells. J Orthop Res 9, 641–650.CrossRefGoogle ScholarPubMed
Castro-Malaspina, H., Gay, R.E., Resnick, G., Kapoor, N., Meyers, P., Chiarieri, D., Mckenzie, S., Broxmeyer, H.E. & Moore, M.A. (1980). Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 56, 289–301.Google Scholar
Chen, F.M., Sun, H.H., Lu, H. & Yu, Q. (2012). Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials 33, 6320–6344.CrossRefGoogle ScholarPubMed
Chen, S.C., Marino, V., Gronthos, S. & Bartold, P.M. (2006). Location of putative stem cells in human periodontal ligament. J Periodontal Res 41, 547–553.Google Scholar
Csaki, C., Matis, U., Mobasheri, A., Ye, H. & Shakibaei, M. (2007). Chondrogenesis, osteogenesis and adipogenesis of canine mesenchymal stem cells: A biochemical, morphological and ultrastructural study. Histochem Cell Biol 128, 507–520.Google Scholar
Danisovic, L., Varga, I., Polak, S., Ulicna, M., Bohmer, D. & Vojtassak, J. (2008). Morphology of in vitro expanded human muscle—derived stem cells. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 152, 235–238.Google Scholar
Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D.J. & Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315–317.CrossRefGoogle ScholarPubMed
Estrela, C., De Alencar, A.H.G., Kitten, G.T., Vencio, E.F. & Gava, E. (2011). Mesenchymal stem cells in the dental tissues: Perspectives for tissue regeneration. Braz Dent J 22, 91–98.Google Scholar
Florea, A. & Crăciun, C. (2013). Bee venom induced in vivo ultrastructural reactions of cells involved in the bone marrow erythropoiesis and of circulating red blood cells. Microsc Microanal 19, 393–405.Google Scholar
Fournier, B.P., Ferre, F.C., Couty, L., Lataillade, J.J., Gourven, M., Naveau, A., Coulomb, B., Lafont, A. & Gogly, B. (2010). Multipotent progenitor cells in gingival connective tissue. Tissue Eng Part A 16, 2891–2899.Google Scholar
Gittel, C., Brehm, W., Burk, J., Juelke, H., Staszyk, C. & Ribitsch, I. (2013). Isolation of equine multipotent mesenchymal stromal cells by enzymatic tissue digestion or explant technique: Comparison of cellular properties. BMC Vet Res 9, 221.CrossRefGoogle ScholarPubMed
Goldstein, J., Newbury, D., Joy, D., Lyman, C., Echlin, P., Lifshin, E., Sawyer, L. & Michael, J. (2003). Scanning Electron Microscopy and X-Ray Microanalysis, 3rd ed. New York, NY: Springer Publishing Co.CrossRefGoogle Scholar
Gronthos, S., Mankani, M., Brahim, J., Robey, P.G. & Shi, S. (2000). Postnatal human dental pulp stem cells DPSC in vitro and in vivo. Proc Natl Acad Sci USA 97, 13625–13630.Google Scholar
Hayat, M.A. (2000). Principles and Techniques of Electron Microscopy—Biological Applications, 4th ed. Cambridge, UK: Cambridge University Press.Google Scholar
Huang, G.T.-J., Gronthos, S. & Shi, S. (2009). Mesenchymal stem cells derived from dental tissues vs. those from other sources, their biology and role in regenerative medicine. J Dent Res 88, 792–806.Google Scholar
Hung, T.Y., H.C., Lin, Chan, Y.J. & Yuan, K. (2012). Isolating stromal stem cells from periodontal granulation tissues. Clin Oral Investig 16, 1171–1180.CrossRefGoogle ScholarPubMed
Hürzeler, M.B. & Weng, D. (1999). A single-incision technique to harvest subepithelial connective tissue grafts from the palate. Int J Periodontics Restorative Dent 19, 279–287.Google Scholar
Hyder, A. (2005). Effect of the pancreatic digestion with liberase versus collagenase on the yield, function and viability of neonatal rat pancreatic islets. Cell Biol Int 29, 831–834.CrossRefGoogle ScholarPubMed
Hynes, K., Menicanin, D., Gronthos, S. & Bartold, P.M. (2012). Clinical utility of stem cells for periodontal regeneration. Periodontol 2000 59, 203–227.Google Scholar
Jang, S., Cho, H.H., Cho, Y.B., Park, J.S. & Jeong, H.S. (2010). Functional neural differentiation of human adipose tissue derived stem cells using bFGF and forskolin. BMC Cell Biol 11, 25–30.CrossRefGoogle ScholarPubMed
Karaoz, E., Aksoy, A., Ayhan, S., Sariboyaci, A.E., Kaymaz, F. & Kasap, M. (2009). Characterization of mesenchymal stem cells from rat bone marrow: Ultrastructural properties, differentiation potential and immunophenotypic markers. Histochem Cell Biol 132, 533–546.CrossRefGoogle ScholarPubMed
Ke, C., Chen, J., Guo, Y., Chen, Z.W. & Cai, J. (2015). Migration mechanism of mesenchymal stem cells studied by QD/NSOM. Biochim Biophys Acta 1848, 859–868.Google Scholar
Kirkland, O. (1931). The suppurative periodontal pus pocket; its treatment by the modified flap operation. J Am Dent Assoc 18, 1462–1470.Google Scholar
Latif, N., Sarathchandra, P., Thomas, P.S., Antoniw, J., Batten, P., Chester, A.H., Taylor, P.M. & Yacoub, M.H. (2007). Characterization of structural and signaling molecules by human valve interstitial cells and comparison to human mesenchymal stem cells. J Heart Valve Dis 16, 56–66.Google Scholar
Lee, R.H., Seo, M.J., Pulin, A.A., Gregory, C.A., Ylostalo, J. & Prockop, D.J. (2009). The CD34 like protein PODXL and alpha6-integrin (CD49f) identify early progenitor MSCs with increased clonogenicity and migration to infarcted heart in mice. Blood 113, 816–826.CrossRefGoogle ScholarPubMed
Lencová, E., Broukal, Z. & Dusková, J. (2006). Psychosocial, behavioural and oral health indicators—review of the literature. Prague Med Rep 107, 305–316.Google ScholarPubMed
Liao, J., Al Shahrani, M., Al-Habib, M., Tanaka, T. & Huang, G.T. (2011). Cells isolated from inflamed periapical tissue express mesenchymal stem cell markers and are highly osteogenic. J Endod 37, 1217–1224.Google Scholar
Lin, C.S., Xin, Z.C., Dai, J. & Lue, T.F. (2013). Commonly used mesenchymal stem cell markers and tracking labels: Limitations and challenges. Histol Histopathol 28, 1109–1116.Google Scholar
Lu, H., Xie, C., Zhao, Y.M. & Chen, F.M. (2013). Translational research and therapeutic applications of stem cell transplantation in periodontal regenerative medicine. Cell Transplant 22, 205–229.CrossRefGoogle ScholarPubMed
Lv, F.J., Tuan, R.S., Cheung, K.M. & Leung, V.Y. (2014). Concise review: The surface markers and identity of human mesenchymal stem cells. Stem Cells 32, 1408–1419.CrossRefGoogle ScholarPubMed
Machado, E., Fernandes, M.H. & De Sousa Gomes, P. (2012). Dental stem cells for craniofacial tissue engineering. Oral Surg Oral Med Oral Pathol Oral Radiol 113, 728–733.Google Scholar
Marrelli, M., Paduano, F. & Tatullo, M. (2013). Cells isolated from human periapical cysts express mesenchymal stem cell-like properties. Int J Biol Sci 9, 1070–1078.Google Scholar
Mensing, N., Gasse, H., Hambruch, N., Haeger, J.-D., Pfarrer, C. & Staszyk, C. (2011). Isolation and characterization of multipotent mesenchymal stromal cells from the gingiva and the periodontal ligament of the horse. BMC Vet Res 7, 42.Google Scholar
Mitrano, T.I., Grob, M.S., Carrion, F., Nova-Lamperti, E., Luz, P.A., Fierro, F.S., Quintero, A., Chaparro, A. & Sanz, A. (2010). Culture and characterization of mesenchymal stem cells from human gingival tissue. J Periodontol 81, 917–925.CrossRefGoogle ScholarPubMed
Miura, M., Gronthos, S., Zhao, M., Lu, B., Fisher, L.W., Robey, P.G. & Shi, S. (2003). SHED: Stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 13, 5807–5812.CrossRefGoogle Scholar
Mogilner, A. & Keren, K. (2009). The shape of motile cells. Curr Biol 15, R762–R771.Google Scholar
Morsczeck, C., Gotz, W., Schierholz, J., Zeilhofer, F., Kuhn, U., Mohl, C., Sippel, C. & Hoffmann, K.H. (2005). Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24, 155–165.CrossRefGoogle ScholarPubMed
Nassiri, F., Cusimano, M.D., Scheithauer, B.W., Rotondo, F., Fazio, A., Yousef, G.M., Syro, L.V., Kovacs, K. & Lloyd, R.V. (2011). Endoglin (CD105): A review of its role in angiogenesis and tumor diagnosis, progression and therapy. Anticancer Res 31, 2283–2290.Google Scholar
Nystedt, J., Anderson, H., Tikkanen, J., Pietilä, M., Hirvonen, T., Takalo, R., Heiskanen, A., Satomaa, T., Natunen, S., Lehtonen, S., Hakkarainen, T., Korhonen, M., Laitinen, S., Valmu, L. & Lehenkari, P. (2013). Cell surface structures influence lung clearance rate of systemically infused mesenchymal stromal cells. Stem Cells 31, 317–326.Google Scholar
Orciani, M., Mariggiò, M.A., Morabito, C., Di Benedetto, G. & Di Primio, R. (2010). Functional characterization of calcium-signaling pathways of human skin-derived mesenchymal stem cells. Skin Pharmacol Physiol 23, 124–132.Google Scholar
Park, J.C., Kim, J.M., Jung, I.H., Kim, J.C., Choi, S.H., Cho, C.S. & Kim, C.S. (2011). Isolation and characterization of human periodontal ligament (PDL) stem cells (PDLSCs) from the inflamed PDL tissue: In vitro and in vivo evaluations. J Clin Periodontol 38, 721–731.CrossRefGoogle ScholarPubMed
Pascucci, L., Mercati, F., Marini, C., Ceccarelli, P., Dall’aglio, C., Pedini, V. & Gargiulo, A. (2010). Ultrastructural morphology of equine adipose-derived mesenchymal stem cells. Histol Histopathol 25, 1277–1285.Google ScholarPubMed
Pasquinelli, G., Tazzari, P., Ricci, F., Vaselli, C., Buzzi, M., Conte, R., Orrico, C., Foroni, L., Stella, A., Alviano, F., Bagnara, G.P. & Lucarelli, E. (2007). Ultrastructural characteristics of human mesenchymal stromal (stem) cells derived from bone marrow and term placenta. Ultrastruct Pathol 31, 23–31.CrossRefGoogle ScholarPubMed
Perry, B.C., Zhou, D., Wu, X., Yang, F.C., Byers, M.A., Chu, T.M., Hockema, J.J., Woods, E.J. & Goebel, W.S. (2008). Collection, cryopreservation, and characterization of human dental pulp-derived mesenchymal stem cells for banking and clinical use. Tissue Eng Part C Methods 14, 149–156.CrossRefGoogle ScholarPubMed
Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S. & Marshak, D.R. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284, 143–147.CrossRefGoogle ScholarPubMed
Roman, A., Soancă, A., Florea, A. & Páll, E. (2013). In vitro characterization of multipotent mesenchymal stromal cells isolated from palatal subepithelial tissue grafts. Microsc Microanal 19, 370–380.CrossRefGoogle ScholarPubMed
Ronay, V., Belibasakis, G.N., Attin, T., Schmidlin, P.R. & Bostanci, N. (2014). Expression of embryonic stem cell markers and osteogenic differentiation potential in cells derived from periodontal granulation tissue. Cell Biol Int 38, 179–186.Google Scholar
Ruedel, A., Hofmeister, S. & Bosserhoff, A.K. (2013). Development of a model system to analyze chondrogenic differentiation of mesenchymal stem cells. Int J Clin Exp Pathol 6, 3042–3048.Google Scholar
Russell, K.C., Phinney, D.G., Lacey, M.R., Barrilleaux, B.L., Meyertholen, K.E. & O’connor, K.C. (2010). In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 28, 788–798.Google Scholar
Sanz, A.R., Carrión, F.S. & Chaparro, A.P. (2015). Mesenchymal stem cells from the oral cavity and their potential value in tissue engineering. Periodontol 2000 67, 251–267.Google Scholar
Seo, B.M., Miura, M., Gronthos, S., Bartold, P.M., Batouli, S., Brahim, J., Young, M., Robey, P.G., Wang, C.Y. & Shi, S. (2004). Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364, 149–155.Google Scholar
Sonoyama, W., Liu, Y., Fang, D., Yamaza, T., Seo, B.M., Zhang, C., Liu, H., Gronthos, S., Wang, C.-Y., Shi, S. & Wang, S. (2006). Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 1, e79.Google Scholar
Spaeth, E., Klopp, A., Dembinski, J., Andreeff, M. & Marini, F. (2008). Inflammation and tumor microenvironments: Defining the migratory itinerary of mesenchymal stem cells. Gene Ther 15, 730–738.CrossRefGoogle ScholarPubMed
Sun, T., Sun, B.C., Ni, C.S., Zhao, X.L., Wang, X.H., Qie, S., Zhang, D.F., Gu, Q., Qi, H. & Zhao, N. (2008). Pilot study on the interaction between B16 melanoma cell-line and bone-marrow derived mesenchymal stem cells. Cancer Lett 263, 35–43.Google Scholar
Totey, S. & Pal, R. (2009). Adult stem cells: A clinical update. Stem Cells 4, 105–121.Google Scholar
Ullah, I., Baregundi Subbarao, R. & Rho, G.J. (2015). Human mesenchymal stem cells—current trends and future prospective. Biosci Rep 35, e00191.CrossRefGoogle Scholar
Wang, H.L., Greenwell, H., Fiorellini, J., Giannobile, W., Offenbacher, S., Salkin, L., Townsend, C., Sheridan, P. & Genco, R.J., Research, Science and Therapy Committee (2005). Periodontal regeneration. J Periodontol 76, 1601–1622.Google ScholarPubMed
Watt, I.M. (2003). The Principles and Practice of Electron Microscopy. Cambridge, UK: Cambridge University Press.Google Scholar
Wennstrom, J.L., Heijl, L. & Lindhe, J. (2008). Periodontal surgery: Access therapy. In Clinical Periodontology and Implant Therapy (5th ed., chapter 25, Lindhe, J., Lang, N. P., & Karring, T (Eds.), pp. 783–822). Blackwell Munksgaard: Oxford.Google Scholar
Widera, D., Grimm, W.D., Moebius, J.M., Mikenberg, I., Piechaczek, C., Gassmann, G., Wolff, N.A., Thevenod, F., Kaltschmidt, C. & Kaltschmidt, B. (2007). Highly efficient neural differentiation of human somatic stem cells, isolated by minimally invasive periodontal surgery. Stem Cells Dev 16, 447–460.Google Scholar
Williams, J.T., Southerland, S.S., Souza, J., Calcutt, A.F. & Cartledge, R.G. (1999). Cells isolated from adult human skeletal muscle capable of differentiating into multiple mesodermal phenotypes. Am Surg 65, 22–26.Google Scholar
Wuchter, P., Boda-Heggemann, J., Straub, B.K., Grund, C., Kuhn, C., Krause, U., Seckinger, A., Peitsch, W.K., Spring, H., Ho, A.D. & Franke, W.W. (2007). Processus and recessus adhaerentes: Giant adherens cell junction systems connect and attract human mesenchymal stem cells. Cell Tissue Res 328, 499–514.Google Scholar
Yazid, F.B., Gnanasegaran, N., Kunasekaran, W., Govindasamy, V. & Musa, S. (2014). Comparison of immunomodulatory properties of dental pulp stem cells derived from healthy and inflamed teeth. Clin Oral Investig 18, 2103–2112.CrossRefGoogle ScholarPubMed
Yu, K.R., Yang, S.R., Jung, J.W., Kim, H., Ko, K., Han, D.W., Park, S.B., Choi, S.W., Kang, S.K., Schöler, H. & Kang, K.S. (2012). CD49f enhances multipotency and maintains stemness through the direct regulation of OCT4 and SOX2. Stem Cells 30, 876–887.Google Scholar
Yu, S., Diao, S., Wang, J., Ding, G., Yang, D. & Fan, Z. (2014). Comparative analysis of proliferation and differentiation potentials of stem cells from inflamed pulp of deciduous teeth and stem cells from exfoliated deciduous teeth. Biomed Res Int 2014, 930907.CrossRefGoogle ScholarPubMed
Zheng, W., Wang, S., Ma, D., Tang, L., Duan, Y. & Jin, Y. (2009). Loss of proliferation and differentiation capacity of aged human periodontal ligament stem cells and rejuvenation by exposure to the young extrinsic environment. Tissue Eng Part A 15, 2363–2371.Google Scholar
Zhidkova, O.V., Petrov, N.S. & Popov, B.V. (2013). Production and characteristics of the growth and marker properties of mesenchymal stem cells of urinary bladder. Zh Evol Biokhim Fiziol 49, 67–77.Google Scholar
Zhu, H., Mitsuhashi, N., Klein, A., Barsky, L.W., Weinberg, K., Barr, M.L., Demetriou, A. & Wu, G.D. (2006). The role of the hyaluronan receptor CD44 in mesenchymal stem cell migration in the extracellular matrix. Stem Cells 24, 928–935.Google Scholar
Zuk, P.A., Zhu, M., Ashijian, P., De Ugarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhaim, P. & Hedrick, M.H. (2002). Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13, 4279–4295.CrossRefGoogle ScholarPubMed
Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P. & Hedrick, M.H. (2001). Multilineage cells from human adipose tissue: Implications for cell based therapies. Tissue Eng 7, 211–228.Google Scholar
Supplementary material: Image

Páll supplementary material

Figure S1

Download Páll supplementary material(Image)
Image 6.3 MB