Chondrogenic differentiation of bone marrow-derived mesenchymal stromal cells via biomimetic and bioactive poly-ε-caprolactone scaffolds

Journal of Biomedical Materials Research - Part A

Volumn 101 A, Issue 6, 2013, Pages 1620-1628

  Schagemann, J C ^a,b   Paul, S ^a   Casper, M E ^b   Rohwedel, J ^c   Kramer, J ^c   Kaps, C ^d   Mittelstaedt, H ^a   Fehr, M ^e   Reinholz, G G ^b  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF LÜBECK   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

hyaluronan; mesenchymal stem cells; poly caprolactone; regenerative medicine; tissue engineering; transforming growth factor 1

Indexed keywords

CAPROLACTONE; HYALURONAN; MESENCHYMAL STEM CELL; REGENERATIVE MEDICINE; TRANSFORMING GROWTH FACTORS;

BIOMIMETICS; BONE; CELL CULTURE; FLOWCHARTING; GENE EXPRESSION; HYALURONIC ACID; NANOFIBERS; POLYMERASE CHAIN REACTION; TISSUE; TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

AGGRECAN; BIOMIMETIC MATERIAL; BOVINE SERUM ALBUMIN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; HYALURONIC ACID; MOLECULAR SCAFFOLD; POLYCAPROLACTONE; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; BONE MARROW CELL; CARTILAGE CELL; CARTILAGE MATRIX; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STROMA CELL; MOLECULAR WEIGHT; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION;

AGED; AGED, 80 AND OVER; AGGRECANS; ALKALINE PHOSPHATASE; ANIMALS; BIOLOGICAL MARKERS; BIOMIMETIC MATERIALS; CATTLE; CELL DIFFERENTIATION; CHONDROGENESIS; COLLAGEN TYPE I; COLLAGEN TYPE II; DNA; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; NANOFIBERS; OSTEOCALCIN; OSTEOPONTIN; POLYESTERS; TISSUE SCAFFOLDS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84876287301     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.34457     Document Type: Article

References (45)

1. Li WJ, Danielson KG, Alexander PG, Tuan RS,. Biological response of chondrocytes cultured in three-dimensional nanofibrous poly(epsilon- caprolactone) scaffolds. J Biomed Mater Res A 2003; 67: 1105-1114.
2. Hutmacher DW,. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000; 21: 2529-2543.
3. Li WJ, Tuli R, Okafor C, Derfoul A, Danielson KG, Hall DJ, Tuan RS,. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 2005; 26: 599-609.
4. Li WJ, Jiang YJ, Tuan RS,. Chondrocyte phenotype in engineered fibrous matrix is regulated by fiber size. Tissue Eng 2006; 12: 1775-1785.
5. Assoian RK, Komoriya A, Meyers CA, Miller DM, Sporn MB,. Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization. J Biol Chem 1983; 258: 7155-7160.
6. Seyedin SM, Thomas TC, Thompson AY, Rosen DM, Piez KA,. Purification and characterization of two cartilage-inducing factors from bovine demineralized bone. Proc Natl Acad Sci U S A 1985; 82: 2267-2271.
7. Millan FA, Denhez F, Kondaiah P, Akhurst RJ,. Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 1991; 111: 131-143.
8. Hiramatsu K, Iwai T, Yoshikawa H, Tsumaki N,. Expression of dominant negative TGF-beta receptors inhibits cartilage formation in conditional transgenic mice. J Bone Miner Metab 2011; 29: 493-500.
9. Hiraki Y, Inoue H, Hirai R, Kato Y, Suzuki F,. Effect of transforming growth factor beta on cell proliferation and glycosaminoglycan synthesis by rabbit growth-plate chondrocytes in culture. Biochim Biophys Acta 1988; 969: 91-99.
10. O'Driscoll SW, Recklies AD, Poole AR,. Chondrogenesis in periosteal explants. An organ culture model for in vitro study. J Bone Joint Surg Am 1994; 76: 1042-1051.
11. Joyce ME, Roberts AB, Sporn MB, Bolander ME,. Transforming growth factor-beta and the initiation of chondrogenesis and osteogenesis in the rat femur. J Cell Biol 1990; 110: 2195-2207.
12. Critchlow MA, Bland YS, Ashhurst DE,. The effects of age on the response of rabbit periosteal osteoprogenitor cells to exogenous transforming growth factor-beta 2. J Cell Sci 1994; 107: 499-516.
13. Reinholz GG, Fitzsimmons JS, Casper ME, Ruesink TJ, Chung HW, Schagemann JC, O'Driscoll SW,. Rejuvenation of periosteal chondrogenesis using local growth factor injection. Osteoarthritis Cartilage 2009; 17: 723-734.
14. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU,. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998; 238: 265-272.
15. Schagemann JC, Chung HW, Mrosek EH, O'Driscoll SW, Reinholz GG,. Glycosaminoglycans and proteoglycans. In:, Wnek G, Bowlin G, editors. Encyclopedia of Biomaterials and Biomedical Engineering. New York: Informa HealthCare; 2008. p 1195-1209.
16. Knudson W, Loeser RF,. CD44 and integrin matrix receptors participate in cartilage homeostasis. Cell Mol Life Sci 2002; 59: 36-44.
17. Schagemann JC, Chung HW, Mrosek EH, Stone JJ, Fitzsimmons JS, O'Driscoll SW, Reinholz GG,. Poly-epsilon-caprolactone/gel hybrid scaffolds for cartilage tissue engineering. J Biomed Mater Res A 93: 454-463.
18. Abe M, Takahashi M, Nagano A,. The effect of hyaluronic acid with different molecular weights on collagen crosslink synthesis in cultured chondrocytes embedded in collagen gels. J Biomed Mater Res A 2005; 75: 494-499.
19. Brun P, Abatangelo G, Radice M, Zacchi V, Guidolin D, Daga Gordini D, Cortivo R,. Chondrocyte aggregation and reorganization into three-dimensional scaffolds. J Biomed Mater Res 1999; 46: 337-346.
20. Schagemann JC, Kurz H, Casper ME, Stone JS, Dadsetan M, Yu-Long S, Mrosek EH, Fitzsimmons JS, O'Driscoll SW, Reinholz GG,. The effect of scaffold composition on the early structural characteristics of chondrocytes and expression of adhesion molecules. Biomaterials 31: 2798-2805.
21. Kramer J, Bohrnsen F, Lindner U, Behrens P, Schlenke P, Rohwedel J,. In vivo matrix-guided human mesenchymal stem cells. Cell Mol Life Sci 2006; 63: 616-626.
22. Endres M, Neumann K, Haupl T, Erggelet C, Ringe J, Sittinger M, Kaps C,. Synovial fluid recruits human mesenchymal progenitors from subchondral spongious bone marrow. J Orthop Res 2007; 25: 1299-1307.
23. Schagemann JC, Erggelet C, Chung HW, Lahm A, Kurz H, Mrosek EH,. Cell-laden and cell-free biopolymer hydrogel for the treatment of osteochondral defects in a sheep model. Tissue Eng 2009; 15: 75-82.
24. Mrosek E, Erggelet C, McDonald JA, Kurz H,. Hyaluronan synthases in normal and regenerating joint cartilage. Cells Tissues Organs 2003; 173: 93-104.
25. Kalwitz G, Andreas K, Endres M, Neumann K, Notter M, Ringe J, Sittinger M, Kaps C,. Chemokine profile of human serum from whole blood: Migratory effects of CXCL-10 and CXCL-11 on human mesenchymal stem cells. Connect Tissue Res 51: 113-122.
26. Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, Herault O, Charbord P, Domenech J,. The in vitro migration capacity of human bone marrow mesenchymal stem cells: Comparison of chemokine and growth factor chemotactic activities. Stem Cells 2007; 25: 1737-1745.
27. Fiedler J, Roderer G, Gunther KP, Brenner RE,. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. J Cell Biochem 2002; 87: 305-312.
28. Erggelet C, Neumann K, Endres M, Haberstroh K, Sittinger M, Kaps C,. Regeneration of ovine articular cartilage defects by cell-free polymer-based implants. Biomaterials 2007; 28: 5570-5580.
29. Bakhshayesh M, Soleimani M, Mehdizadeh M, Katebi M,. Effects of TGF-beta and b-FGF on the potential of peripheral blood-borne stem cells and bone marrow-derived stem cells in wound healing in a murine model. Inflammation 2011; epub ahead of print.
30. Maleski MP, Knudson CB,. Matrix accumulation and retention in embryonic cartilage and in vitro chondrogenesis. Connect Tissue Res 1996; 34: 75-86.
31. Ishida T, Iijima T, Moriyama S, Nakamura C, Kitagawa T, Machinami R,. Intra-articular calcifying synovial sarcoma mimicking synovial chondromatosis. Skeletal Radiol 1996; 25: 766-769.
32. Kujawa MJ, Caplan AI,. Hyaluronic acid bonded to cell-culture surfaces stimulates chondrogenesis in stage 24 limb mesenchyme cell cultures. Dev Biol 1986; 114: 504-518.
33. Kujawa MJ, Carrino DA, Caplan AI,. Substrate-bonded hyaluronic acid exhibits a size-dependent stimulation of chondrogenic differentiation of stage 24 limb mesenchymal cells in culture. Dev Biol 1986; 114: 519-528.
34. Hegewald AA, Ringe J, Bartel J, Kruger I, Notter M, Barnewitz D, Kaps C, Sittinger M,. Hyaluronic acid and autologous synovial fluid induce chondrogenic differentiation of equine mesenchymal stem cells: A preliminary study. Tissue Cell 2004; 36: 431-438.
35. Solchaga LA, Dennis JE, Goldberg VM, Caplan AI,. Hyaluronic acid-based polymers as cell carriers for tissue-engineered repair of bone and cartilage. J Orthop Res 1999; 17: 205-213.
36. DeFail AJ, Chu CR, Izzo N, Marra KG,. Controlled release of bioactive TGF-beta 1 from microspheres embedded within biodegradable hydrogels. Biomaterials 2006; 27: 1579-1585.
37. Pedrozo HA, Schwartz Z, Gomez R, Ornoy A, Xin-Sheng W, Dallas SL, Bonewald LF, Dean DD, Boyan BD,. Growth plate chondrocytes store latent transforming growth factor (TGF)-beta 1 in their matrix through latent TGF-beta 1 binding protein-1. J Cell Physiol 1998; 177: 343-354.
38. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumur M, Fujinag T,. Gene expression profile of bovine bone marrow mesenchymal stem cell during spontaneous chondrogenic differentiation in pellet culture system. Jpn J Vet Res 2006; 53: 127-139.
39. 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 2006; 93: 1152-1163.
40. 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 2004; 320: 914-919.
41. Li WJ, Tuli R, Huang X, Laquerriere P, Tuan RS,. Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials 2005; 26: 5158-5166.
42. Casper ME, Fitzsimmons JS, Stone JJ, Meza AO, Huang Y, Ruesink TJ, O'Driscoll SW, Reinholz GG,. Tissue engineering of cartilage using poly-epsilon-caprolactone nanofiber scaffolds seeded in vivo with periosteal cells. Osteoarthritis Cartilage 2010; 18: 981-991.
43. Meza AO, Fitzsimmons JS, Casper ME, Chen Q, An KN, Ruesink TJ, O'Driscoll SW, Reinholz GG,. Pretreatment of periosteum with TGF-beta1 in situ enhances the quality of osteochondral tissue regenerated from transplanted periosteal grafts in adult rabbits. Osteoarthritis Cartilage 2010; 18: 1183-1191.
44. Cai DZ, Zeng C, Quan DP, Bu LS, Wang K, Lu HD, Li XF,. Biodegradable chitosan scaffolds containing microspheres as carriers for controlled transforming growth factor-beta1 delivery for cartilage tissue engineering. Chin Med J 2007; 120: 197-203.
45. Kempen DH, Kruyt MC, Lu L, Wilson CE, Florschutz AV, Creemers LB, Yaszemski MJ, Dhert WJ,. Effect of autologous bone marrow stromal cell seeding and bone morphogenetic protein-2 delivery on ectopic bone formation in a microsphere/poly(propylene fumarate) composite. Tissue Eng 2009; 15: 587-594.