Journal of APPLIED BIOMEDICINE
ISSN 1214-0287 (on-line)
ISSN 1214-021X (printed)

Volume 5 (2007), No 3, p 139-150




Chondrogenic differentiation of human bone marrow and adipose tissue-derived mesenchymal stem cells

Lubos Danisovic, Petr Lesny, Vojtech Havlas, Petr Teyssler, Zdenka Syrova, Martin Kopani, Gabriela Fujerikova, Tomas Trc, Eva Sykova, Pavla Jendelova

Address: Pavla Jendelova, Institute of Experimental Medicine ASCR, Videnska 1083, 140 20 Prague 4, Czech Republic
pavla.jendelova@lfmotol.cuni.cz

Received 21st March 2007.
Revised 23rd April 2007.
Published online 3rd May 2007.

Full text article (pdf)
Full text article (html)

SUMMARY
Congenital abnormalities, various diseases and injuries may result in the degeneration of articular cartilage. Recently, stem cell therapy has offered new treatment possibilities for this condition. The aim of our study was to verify the chondrogenic differentiation potential of human bone marrow mesenchymal stem cells (BMSCs) and adipose tissue-derived mesenchymal stem cells (AMSCs) in vitro in the presence or absence of transforming growth factor beta (TGF-beta1). Human BMSCs and AMSCs from healthy donors were collected during orthopaedic surgeries and expanded in vitro to obtain a sufficient quantity of cells; their chondrogenic differentiation was studied in the pellet culture system. Spontaneous chondrogenesis occurred in both BMSC and AMSC pellet cultures and was similar in both TGF-beta1 treated and untreated pellet cultures. BMSC pellets contained more cells with a chondrogenic phenotype. The presence of TGF-beta1 led to a decrease in the levels of collagen type I mRNA and to increased levels of collagen type II mRNA only in the BMSC pellet culture. Our results demonstrate that although both mesenchymal cell types can be used in cartilage tissue engineering, the chondrogenic potential of human BMSCs is higher than that of AMSCs.

KEY WORDS
cartilage; collagen mRNA; mesenchymal stem cell; pellet cell culture; TGF-beta1


REFERENCES
Bosnakovski D, Mizuno M, Kim G, Ishiguro T, Okumura M, Iwanaga T, Kadosawa T, Fujinaga T: Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells in pellet cultural system. Exp Hematol 32:502-509, 2004.

Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T: Isolation and multilineage differentiation of bovine bone marrow mesenchymal stem cells. Cell Tissue Res 319:243-253, 2005.

Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T: Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol Bioeng 93:1152-1163, 2006.

Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L: Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331:889-895, 1994.

Buckwalter JA: Articular cartilage: injuries and potential for healing. J Orthop Sports Phys Ther 28:192-202, 1998.

Collins SD, Baffour R, Waksman R: Cell therapy in myocardial infarction. Cardiovasc Revasc Med 8:43-51, 2007.

Galera P, Redini F, Vivien D, Bonaventure J, Penfornis H, Loyau G, Pujol JP: Effect of transforming growth factor-beta 1 (TGF-beta 1) on matrix synthesis by monolayer cultures of rabbit articular chondrocytes during the dedifferentiation process. Exp Cell Res 200:379-392, 1992.

Gimble J, Guilak F: Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5:362-369, 2003.

Huang JI, Zuk PA, Jones NF, Zhu M, Lorenz HP, Hedrick MH, Benhaim P: Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg 113:585-594, 2004.

Im GI, Jung NH, Tae SK: Chondrogenic differentiation of mesenchymal stem cells isolated from patients in late adulthood: the optimal conditions of growth factors. Tissue Eng 12:527-536, 2006.

Indrawattana N, Chen G, Tadokoro M, Shann LH, Ohgushi H, Tateishi T, Tanaka J, Bunyaratvej A: Growth factor combination for chondrogenic induction from human mesenchymal stem cell. Biochem Biophys Res Commun 320:914-919, 2004.

Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU: In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238:265-272, 1998.

Kosher RA, Kulyk WM, Gay SW: Collagen gene expression during limb cartilage differentiation. J Cell Biol 102:1151-1156, 1986a.

Kosher RA, Gay SW, Kamanitz JR, Kulyk WM, Rodgers BJ, Sai S, Tanaka T, Tanzer ML: Cartilage proteoglycan core protein gene expression during limb cartilage differentiation. Dev Biol 118:112-117, 1986b.

Lee JW, Kim YH, Kim SH, Han SH, Hahn SB: Chondrogenic differentiation of mesenchymal stem cells and its clinical applications. Yonsei Med J 45 (Suppl.):41-47, 2004.

Lyon A, Harding S: The potential of cardiac stem cell therapy for heart failure. Curr Opin Pharmacol 7:164-170, 2007.

Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF: Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4:415-428, 1998.

Mastrogiacomo M, Cancedda R, Quarto R: Effect of different growth factors on the chondrogenic potential of human bone marrow stromal cells. Osteoarthr Cartil 9 (Suppl. A):S36-40, 2001.

Miyazono K: Positive and negative regulation of TGF-beta signaling. J Cell Sci 113:1101-1109, 2000.

Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR: Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147, 1999.

Sakaguchi Y, Sekiya I, Yagishita K, Muneta T: Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52:2521-2529, 2005.

Schmitt B, Ringe J, Haupl T, Notter M, Manz R, Burmester GR, Sittinger M, Kaps C: BMP2 initiates chondrogenic lineage development of adult human mesenchymal stem cells in highdensity culture. Differentiation 71:567-577, 2003.

Schnabel M, Marlovits S, Eckhoff G, Fichtel I, Gotzen L, Vecsei V, Schlegel J: Dedifferentiation-associated changes in morphology and gene expression in primary human articular chondrocytes in cell culture. Osteoarthr Cartil 10:62-70, 2002.

Smith RK, Korda M, Blunn GW, Goodship AE: Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment. Equine Vet J 35:99-102, 2003.

Stott NS, Jiang TX, Chuong CM: Successive formative stages of precartilaginous mesenchymal condensations in vitro: modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 180:314-324, 1999.

Strem BM, Hedrick MH: The growing importance of fat in regenerative medicine. Trends Biotechnol. 23:64-66, 2005.

Tew SR, Kwan AP, Hann A, Thomson BM, Archer CW: The reactions of articular cartilage to experimental wounding: role of apoptosis. Arthritis Rheum 43:215-225, 2000.

Tuli R, Li WJ, Tuan RS: Current state of cartilage tissue engineering. Arthritis Res Ther 5:235-238, 2003.

Wagers AJ, Weissman IL: Plasticity of adult stem cells. Cell 116:639-648, 2004.

Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H, Weber RM, Ewerbeck V, Richter W: Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 48:418-429, 2003.

Yang X, Chen L, Xu X, Li C, Huang C, Deng CX: TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 153:35-46, 2001.

Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228, 2001.
CITED

Thakkar S Ghebes CA, Ahmed M, Kelder C, van Blitterswijk CA, Saris D, Fernandes HAM, Moroni L. Mesenchymal stromal cell-derived extracellular matrix influences gene expression of chondrocytes. Biofabrication. 5, Art No: 025003, 2013.

Tuemmers C, Rebolledo N, Aguilera R. Effect of the application of stem cells for tendon injuries in sporting horses. Arch Med Veterin. 44: 207-215, 2012.

Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Develop. 21: 2724-2752, 2012.

Kaewsuwan S, Song SY, Kim JH, Sung JH. Mimicking the functional niche of adipose-derived stem cells for regenerative medicine. Expert Opin Biol Ther. 12: 1575-1588, 2012.

Danisovic L, Varga I, Polak S. Growth factors and chondrogenic differentiation of mesenchymal stem cells. Tissue Cell. 44: 69-73, 2012.

Hepsibha P, Meenambigai TV, Mangalagowri A, Palanisamy A, Stalin A, Nithya S, Kumanan K. Multipotent Differentiation Potential of Buffalo Adipose Tissue Derived Mesenchymal Stem Cells. Asian J Anim Veterin Adv. 6: 772-788, 2011.

Varga I, Mikusova R, Pospisilova V, Varga I, Galfiova P, Adamkov M, Polak S, Galbavy S. Morphologic heterogeneity of human thymic nonlymphocytic cells. Neuroendocrin Lett. 30: 275-283, 2009.

Gimble JM, Guilak F, Nuttall ME, Sathiskhumar S, Vidal M, Bunnell BA. In vitro differentiation potential of mesenchymal stem cells. Transf Med Hemother. 35: 228-238, 2008.

BACK