Growth Factors-mediated Effects on the Differentiation of Human Adipose-derived Stem Cells into Chondrocytes_Journal of Biomedical Engineering

Authors：

YANGWu ,  LIUChang

Department of Orthodontics, School of Stomatology, Jilin University, Changchun 130021, China;

Corresponding author：

LIUChang, Email: lcwztt@gmail.com

Keywords：

human adipose-derived stem cell; chondrogenic induction; growth factor

DOI：

10.7507/1001-5515.20140267

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In recent years, there has been a growing emphasis on use of human adipose-derived stem cells (hADSCs)for cartilage tissue engineering owing to their ability to differentiate into chondrocytes, which is mainly induced by growth factors (GFs). In general, GFs for chondrogenic induction come from the transforming growth factor β (TGF-β) superfamily. To date, the most commonly used GFs for chondrogenes is TGF-β1/3. However, the response of hADSCs to GFs may differ significantly from that of human bone marrow stem cells (hBMSCs). It has been reported that bone morphogenetic protein-6 (BMP-6) treatment induced TGF-β receptor-Ⅰ expression of hADSCs. It seems that these two cell populations varied strongly in their potency to undergo chondrogenesis in the same medium conditions. Here, we provide a concise review on various GFs used in chondrogenic differentiation of hADSCs in vitro.

Citation： YANGWu, LIUChang. Growth Factors-mediated Effects on the Differentiation of Human Adipose-derived Stem Cells into Chondrocytes. Journal of Biomedical Engineering, 2014, 31(6): 1409-1413. doi: 10.7507/1001-5515.20140267 Copy

1.	FREYRIA A M, MALLEIN-GERIN F. Chondrocytes or adult stem cells for cartilage repair:the indisputable role of growth factors[J]. Injury, 2012, 43(3):259-265.
2.	INUI A, IWAKURA T, REDDI A H, et al. Human stem cells and articular cartilage regeneration[J]. Cells, 2012, 1(4):994-1009.
3.	ACHARYA C, ADESIDA A, ZAJAC P, et al. Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation[J]. J Cell Physiol, 2012, 227(1):88-97.
4.	JUNG Y, BAUER G, NOLTA J A. Concise review:induced pluripotent stem cell-derived mesenchymal stem cells:progress toward safe clinical products[J]. Stem Cells, 2012, 30(1):42-47.
5.	ZUK P A, ZHU M, MIZUNO H, et al. Multilineage cells from human adipose tissue:implications for cell-based therapies[J]. Tissue Eng, 2001, 7(2):211-228.
6.	HENNIG T, LORENZ H, THIEL A, et al. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFβ receptor and BMP profile and is overcome by BMP-6[J]. J Cell Physiol, 2007, 211(3):682-691.
7.	ESTES B T, WU A W, STORMS R W, et al. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells[J]. J Cell Physiol, 2006, 209(3):987-995.
8.	ESTES B T, WU A W, GUILAK F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6[J]. Arthritis Rheum, 2006, 54(4):1222-1232.
9.	MEHLHORN A T, NIEMEYER P, KAISER S, et al. Differential expression pattern of extracellular matrix molecules during chondrogenesis of mesenchymal stem cells from bone marrow and adipose tissue[J]. Tissue Eng, 2006, 12(10):2853-2862.
10.	JUNGMANN P M, MEHLHORN A T, SCHMAL H, et al. Nanomechanics of human adipose-derived stem cells:small GTPases impact chondrogenic differentiation[J]. Tissue Eng Part A, 2012, 18(9-10):1035-1044.
11.	YOON I S, CHUNG C W, SUNG J H, et al. Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold[J]. J Biosci Bioeng, 2011, 112(4):402-408.
12.	HWANG N S, IM S G, WU P B, et al. Chondrogenic priming adipose-mesenchymal stem cells for cartilage tissue regeneration[J]. Pharm Res, 2011, 28(6):1395-1405.
13.	YU B, YU D, CAO L, et al. Simulated microgravity using a rotary cell culture system promotes chondrogenesis of human adipose-derived mesenchymal stem cells via the p38 MAPK pathway[J]. Biochem Biophys Res Commun, 2011, 414(2):412-418.
14.	ZHANG Z, KANG Y, ZHANG Z, et al. Expression of microRNAs during chondrogenesis of human adipose-derived stem cells[J]. Osteoarthritis Cartilage, 2012, 20(12):1638-1646.
15.	KIM H J, PARK S H, DURHAM J, et al. In vitro chondrogenic differentiation of human adipose-derived stem cells with silk scaffolds[J]. Journal of Tissue Engineering, 2012, 3(1):2041731412466405.
16.	WU L, PRINS H J, HELDER M N, et al. Trophic effects of mesenchymal stem cells in chondrocyte co-cultures are independent of culture conditions and cell sources[J]. Tissue Eng Part A, 2012, 18(15-16):1542-1551.
17.	HAMID A A, IDRUS R B, SAIM A B, et al. Characterization of human adipose-derived stem cells and expression of chondrogenic genes during induction of cartilage differentiation[J]. Clinics (Sao Paulo), 2012, 67(2):99-106.
18.	SUKARTO A, YU C, FLYNN L E, et al. Co-delivery of adipose-derived stem cells and growth factor-loaded microspheres in RGD-grafted N-methacrylate glycol chitosan gels for focal chondral repair[J]. Biomacromolecules, 2012, 13(8):2490-2502.
19.	YUMOTO K, THOMAS P S, LANE J, et al. TGF-β-activated kinase 1(Tak1) mediates agonist-induced Smad activation and linker region phosphorylation in embryonic craniofacial neural crest-derived cells[J]. J Biol Chem, 2013, 288(19):13467-13480.
20.	BAHNEY C S, LUJAN T J, HSU C W, et al. Visible light photoinitiation of mesenchymal stem cell-laden bioresponsive hydrogels[J]. Eur Cell Mater, 2011, 22:43-55.
21.	PUETZER J L, PETITTE J N, LOBOA E G. Comparative review of growth factors for induction of three-dimensionalin vitro chondrogenesisin human mesenchymal stem cells isolated from bone marrow and adipose tissue[J]. Tissue Eng Part B Rev, 2010, 16(4):435-444.
22.	BIAN L, ZHAI D Y, TOUS E, et al. Enhanced MSC chondrogenesis following delivery of TGF-β3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo[J]. Biomaterials, 2011, 32(27):6425-6434.
23.	GUPTA M S, COOPER E S, NICOLL S B. Transforming growth factor-beta 3 stimulates cartilage matrix elaboration by human marrow-derived stromal cells encapsulated in photocrosslinked carboxymethylcellulose hydrogels:potential for nucleus pulposus replacement[J]. Tissue Eng Part A, 2011, 17(23-24):2903-2910.
24.	KEMMIS C M, VAHDATI A, WEISS H E, et al. Bone morphogenetic protein 6 drives both osteogenesis and chondrogenesis in murine adipose-derived mesenchymal cells depending on culture conditions[J]. Biochem Biophys Res Commun, 2010, 401(1):20-25.
25.	PARK J S, YANG H N, WOO D G, et al. The promotion of chondrogenesis, osteogenesis, and adipogenesis of human mesenchymal stem cells by multiple growth factors incorporated into nanosphere-coated microspheres[J]. Biomaterials, 2011, 32(1):28-38.
26.	WELTER J F, SOLCHAGA L A, BASKARAN H, et al. Chondrogenesis from human mesenchymal stem cells:role of culture conditions[M]//HAYAT M A. Stem cells and cancer stem cells, Volume 5:Therapeutic applications in disease and injury. Dordrecht:Springer Netherlands, 2012, 5:269-280.
27.	HILDNER F, PETERBAUER A, WOLBANK S, et al. FGF-2 abolishes the chondrogenic effect of combined BMP-6 and TGF-beta in human adipose derived stem cells[J]. J Biomed Mater Res A, 2010, 94(3):978-987.
28.	MUELLER M B, FISCHER M, ZELLNER J, et al. Effect of parathyroid hormone-related protein in an in vitro hypertrophy model for mesenchymal stem cell chondrogenesis[J]. Int Orthop, 2013, 37(5):945-951.
29.	INDRAWATTANA N, CHEN G, TADOKORO M, et al. Growth factor combination for chondrogenic induction from human mesenchymal stem cell[J]. Biochem Biophys Res Commun, 2004, 320(3):914-919.
30.	NARCISI R, SIGNORILE L, VERHAAR J A, et al. TGFβ inhibition during expansion phase increases the chondrogenic re-differentiation capacity of human articular chondrocytes[J]. Osteoarthritis Cartilage, 2012, 20(10):1152-1160.
31.	VAN DER KRAAN P M. Transforming growth factor-beta induced chrondrogenic differentiation of bone marrow-derived mesenchymal stem cells:role of Smad signaling pathways[M]//HAYAT M A. Stem cells and cancer stem cells, Volume 10:Therapeutic applications in disease and injury. Dordrecht:Springer Netherlands, 2013, 10:85-91.

1. FREYRIA A M, MALLEIN-GERIN F. Chondrocytes or adult stem cells for cartilage repair:the indisputable role of growth factors[J]. Injury, 2012, 43(3):259-265.
2. INUI A, IWAKURA T, REDDI A H, et al. Human stem cells and articular cartilage regeneration[J]. Cells, 2012, 1(4):994-1009.
3. ACHARYA C, ADESIDA A, ZAJAC P, et al. Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation[J]. J Cell Physiol, 2012, 227(1):88-97.
4. JUNG Y, BAUER G, NOLTA J A. Concise review:induced pluripotent stem cell-derived mesenchymal stem cells:progress toward safe clinical products[J]. Stem Cells, 2012, 30(1):42-47.
5. ZUK P A, ZHU M, MIZUNO H, et al. Multilineage cells from human adipose tissue:implications for cell-based therapies[J]. Tissue Eng, 2001, 7(2):211-228.
6. HENNIG T, LORENZ H, THIEL A, et al. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFβ receptor and BMP profile and is overcome by BMP-6[J]. J Cell Physiol, 2007, 211(3):682-691.
7. ESTES B T, WU A W, STORMS R W, et al. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells[J]. J Cell Physiol, 2006, 209(3):987-995.
8. ESTES B T, WU A W, GUILAK F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6[J]. Arthritis Rheum, 2006, 54(4):1222-1232.
9. MEHLHORN A T, NIEMEYER P, KAISER S, et al. Differential expression pattern of extracellular matrix molecules during chondrogenesis of mesenchymal stem cells from bone marrow and adipose tissue[J]. Tissue Eng, 2006, 12(10):2853-2862.
10. JUNGMANN P M, MEHLHORN A T, SCHMAL H, et al. Nanomechanics of human adipose-derived stem cells:small GTPases impact chondrogenic differentiation[J]. Tissue Eng Part A, 2012, 18(9-10):1035-1044.
11. YOON I S, CHUNG C W, SUNG J H, et al. Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold[J]. J Biosci Bioeng, 2011, 112(4):402-408.
12. HWANG N S, IM S G, WU P B, et al. Chondrogenic priming adipose-mesenchymal stem cells for cartilage tissue regeneration[J]. Pharm Res, 2011, 28(6):1395-1405.
13. YU B, YU D, CAO L, et al. Simulated microgravity using a rotary cell culture system promotes chondrogenesis of human adipose-derived mesenchymal stem cells via the p38 MAPK pathway[J]. Biochem Biophys Res Commun, 2011, 414(2):412-418.
14. ZHANG Z, KANG Y, ZHANG Z, et al. Expression of microRNAs during chondrogenesis of human adipose-derived stem cells[J]. Osteoarthritis Cartilage, 2012, 20(12):1638-1646.
15. KIM H J, PARK S H, DURHAM J, et al. In vitro chondrogenic differentiation of human adipose-derived stem cells with silk scaffolds[J]. Journal of Tissue Engineering, 2012, 3(1):2041731412466405.
16. WU L, PRINS H J, HELDER M N, et al. Trophic effects of mesenchymal stem cells in chondrocyte co-cultures are independent of culture conditions and cell sources[J]. Tissue Eng Part A, 2012, 18(15-16):1542-1551.
17. HAMID A A, IDRUS R B, SAIM A B, et al. Characterization of human adipose-derived stem cells and expression of chondrogenic genes during induction of cartilage differentiation[J]. Clinics (Sao Paulo), 2012, 67(2):99-106.
18. SUKARTO A, YU C, FLYNN L E, et al. Co-delivery of adipose-derived stem cells and growth factor-loaded microspheres in RGD-grafted N-methacrylate glycol chitosan gels for focal chondral repair[J]. Biomacromolecules, 2012, 13(8):2490-2502.
19. YUMOTO K, THOMAS P S, LANE J, et al. TGF-β-activated kinase 1(Tak1) mediates agonist-induced Smad activation and linker region phosphorylation in embryonic craniofacial neural crest-derived cells[J]. J Biol Chem, 2013, 288(19):13467-13480.
20. BAHNEY C S, LUJAN T J, HSU C W, et al. Visible light photoinitiation of mesenchymal stem cell-laden bioresponsive hydrogels[J]. Eur Cell Mater, 2011, 22:43-55.
21. PUETZER J L, PETITTE J N, LOBOA E G. Comparative review of growth factors for induction of three-dimensionalin vitro chondrogenesisin human mesenchymal stem cells isolated from bone marrow and adipose tissue[J]. Tissue Eng Part B Rev, 2010, 16(4):435-444.
22. BIAN L, ZHAI D Y, TOUS E, et al. Enhanced MSC chondrogenesis following delivery of TGF-β3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo[J]. Biomaterials, 2011, 32(27):6425-6434.
23. GUPTA M S, COOPER E S, NICOLL S B. Transforming growth factor-beta 3 stimulates cartilage matrix elaboration by human marrow-derived stromal cells encapsulated in photocrosslinked carboxymethylcellulose hydrogels:potential for nucleus pulposus replacement[J]. Tissue Eng Part A, 2011, 17(23-24):2903-2910.
24. KEMMIS C M, VAHDATI A, WEISS H E, et al. Bone morphogenetic protein 6 drives both osteogenesis and chondrogenesis in murine adipose-derived mesenchymal cells depending on culture conditions[J]. Biochem Biophys Res Commun, 2010, 401(1):20-25.
25. PARK J S, YANG H N, WOO D G, et al. The promotion of chondrogenesis, osteogenesis, and adipogenesis of human mesenchymal stem cells by multiple growth factors incorporated into nanosphere-coated microspheres[J]. Biomaterials, 2011, 32(1):28-38.
26. WELTER J F, SOLCHAGA L A, BASKARAN H, et al. Chondrogenesis from human mesenchymal stem cells:role of culture conditions[M]//HAYAT M A. Stem cells and cancer stem cells, Volume 5:Therapeutic applications in disease and injury. Dordrecht:Springer Netherlands, 2012, 5:269-280.
27. HILDNER F, PETERBAUER A, WOLBANK S, et al. FGF-2 abolishes the chondrogenic effect of combined BMP-6 and TGF-beta in human adipose derived stem cells[J]. J Biomed Mater Res A, 2010, 94(3):978-987.
28. MUELLER M B, FISCHER M, ZELLNER J, et al. Effect of parathyroid hormone-related protein in an in vitro hypertrophy model for mesenchymal stem cell chondrogenesis[J]. Int Orthop, 2013, 37(5):945-951.
29. INDRAWATTANA N, CHEN G, TADOKORO M, et al. Growth factor combination for chondrogenic induction from human mesenchymal stem cell[J]. Biochem Biophys Res Commun, 2004, 320(3):914-919.
30. NARCISI R, SIGNORILE L, VERHAAR J A, et al. TGFβ inhibition during expansion phase increases the chondrogenic re-differentiation capacity of human articular chondrocytes[J]. Osteoarthritis Cartilage, 2012, 20(10):1152-1160.
31. VAN DER KRAAN P M. Transforming growth factor-beta induced chrondrogenic differentiation of bone marrow-derived mesenchymal stem cells:role of Smad signaling pathways[M]//HAYAT M A. Stem cells and cancer stem cells, Volume 10:Therapeutic applications in disease and injury. Dordrecht:Springer Netherlands, 2013, 10:85-91.

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