Polyglycolic acid-hyaluronan scaffolds loaded with bone marrow-derived mesenchymal stem cells show chondrogenic differentiation in vitro and cartilage repair in the rabbit model

Journal of Biomedical Materials Research - Part B Applied Biomaterials

Volumn 101, Issue 7, 2013, Pages 1310-1320

  Patrascu, Jenel M ^a   Krüger, Jan Philipp ^b   Böss, Hademar G ^a   Ketzmar, Anna Katharina ^b   Freymann, Undine ^b   Sittinger, Michael ^c   Notter, Michael ^c   Endres, Michaela ^b,c   Kaps, Christian ^b  

^a VICTOR BABES UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b TRANSTISSUE TECHNOLOGIES GMBH   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

cartilage regeneration; cartilage repair; cell free implant; microfracture; stem cells

Indexed keywords

ARTICULAR CARTILAGE DEFECTS; BONE MARROW-DERIVED MESENCHYMAL STEM CELLS; CARTILAGE REGENERATION; CARTILAGE REPAIR; CELL-FREE; CHONDROGENIC DIFFERENTIATION; GENE EXPRESSION ANALYSIS; MICRO-FRACTURE;

CARTILAGE; CELL CULTURE; DEFECTS; GENE EXPRESSION; HYALURONIC ACID; REPAIR; STEM CELLS; TISSUE;

SCAFFOLDS (BIOLOGY);

AGGRECAN; CARTILAGE OLIGOMERIC MATRIX PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 9; FATTY ACID BINDING PROTEIN 4; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYALURONIC ACID; LINK PROTEIN; POLYGLYCOLIC ACID; TISSUE SCAFFOLD;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE INJURY; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; FREEZE DRYING; GENE EXPRESSION PROFILING; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; ILIAC CREST; IMPLANT; IN VITRO STUDY; MARKER GENE; MESENCHYMAL STEM CELL; MICROFRACTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; RABBIT; TISSUE CULTURE; TISSUE REPAIR;

CARTILAGE REGENERATION; CARTILAGE REPAIR; CELL-FREE IMPLANT; MICROFRACTURE; STEM CELLS;

ADULT; AGED; ANIMALS; BONE MARROW CELLS; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELLS, IMMOBILIZED; FEMALE; HUMANS; HYALURONIC ACID; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; POLYGLYCOLIC ACID; RABBITS; REGENERATION; TISSUE SCAFFOLDS;

EID: 84884208381     PISSN: 15524973     EISSN: 15524981     Source Type: Journal    
DOI: 10.1002/jbm.b.32944     Document Type: Article

References (50)

1. 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 1994; 331 (14): 889-895.
2. Hubbard MJ,. Articular debridement versus washout for degeneration of the medial femoral condyle. A five-year study. J Bone Joint Surg Br 1996; 78 (2): 217-219.
3. Kreuz PC, Muller S, Freymann U, Erggelet C, Niemeyer P, Kaps C, Hirschmuller A,. Repair of focal cartilage defects with scaffold-assisted autologous chondrocyte grafts: Clinical and biomechanical results 48 months after transplantation. Am J Sports Med 2011; 39 (8): 1697-1705.
4. Matsusue Y, Yamamuro T, Hama H,. Arthroscopic multiple osteochondral transplantation to the chondral defect in the knee associated with anterior cruciate ligament disruption. Arthroscopy 1993; 9 (3): 318-321.
5. Steadman JR, Rodkey WG, Briggs KK, Rodrigo JJ,. The microfracture technic in the management of complete cartilage defects in the knee joint. Orthopade 1999; 28 (1): 26-32.
6. Steadman JR, Briggs KK, Rodrigo JJ, Kocher MS, Gill TJ, Rodkey WG,. Outcomes of microfracture for traumatic chondral defects of the knee: Average 11-year follow-up. Arthroscopy 2003; 19 (5): 477-484.
7. Steadman JR, Rodkey WG, Rodrigo JJ,. Microfracture: Surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res 2001 (391 Suppl): S362-S369.
8. 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 (10): 1299-1307.
9. Shapiro F, Koide S, Glimcher MJ,. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 1993; 75 (4): 532-553.
10. Kreuz PC, Erggelet C, Steinwachs MR, Krause SJ, Lahm A, Niemeyer P, Ghanem N, Uhl M, Sudkamp N,. Is microfracture of chondral defects in the knee associated with different results in patients aged 40 years or younger? Arthroscopy 2006; 22 (11): 1180-1186.
11. Gudas R, Kalesinskas RJ, Kimtys V, Stankevicius E, Toliusis V, Bernotavicius G, Smailys A,. A prospective randomized clinical study of mosaic osteochondral autologous transplantation versus microfracture for the treatment of osteochondral defects in the knee joint in young athletes. Arthroscopy 2005; 21 (9): 1066-1075.
12. Dhollander AA, Verdonk PC, Lambrecht S, Almqvist KF, Elewaut D, Verbruggen G, Verdonk R,. The combination of microfracture and a cell-free polymer-based implant immersed with autologous serum for cartilage defect coverage. Knee Surg Sports Traumatol Arthrosc 2011.
13. Gille J, Schuseil E, Wimmer J, Gellissen J, Schulz AP, Behrens P,. Mid-term results of autologous matrix-induced chondrogenesis for treatment of focal cartilage defects in the knee. Knee Surg Sports Traumatol Arthrosc 2010; 18 (11): 1456-1464.
14. Patrascu JM, Freymann U, Kaps C, Poenaru DV,. Repair of a post-traumatic cartilage defect with a cell-free polymer-based cartilage implant: A follow-up at two years by MRI and histological review. J Bone Joint Surg Br 2010; 92 (8): 1160-1163.
15. Zantop T, Petersen W,. Arthroscopic implantation of a matrix to cover large chondral defect during microfracture. Arthroscopy 2009; 25 (11): 1354-1360.
16. Erggelet C, Endres M, Neumann K, Morawietz L, Ringe J, Haberstroh K, Sittinger M, Kaps C,. Formation of cartilage repair tissue in articular cartilage defects pretreated with microfracture and covered with cell-free polymer-based implants. J Orthop Res 2009; 27 (10): 1353-1360.
17. Siclari A, Mascaro G, Gentili C, Cancedda R, Boux E,. A cell-free scaffold-based cartilage repair provides improved function hyaline-like repair at one year. Clin Orthop Relat Res 2012; 470 (3): 910-919.
18. Chen H, Hoemann CD, Sun J, Chevrier A, McKee MD, Shive MS, Hurtig M, Buschmann MD,. Depth of subchondral perforation influences the outcome of bone marrow stimulation cartilage repair. J Orthop Res 2011; 29 (8): 1178-1184.
19. Chen H, Sun J, Hoemann CD, Lascau-Coman V, Ouyang W, McKee MD, Shive MS, Buschmann MD,. Drilling and microfracture lead to different bone structure and necrosis during bone-marrow stimulation for cartilage repair. J Orthop Res 2009; 27 (11): 1432-1438.
20. Caplan AI,. The mesengenic process. Clin Plast Surg 1994; 21 (3): 429-435.
21. Kaul G, Cucchiarini M, Remberger K, Kohn D, Madry H,. Failed cartilage repair for early osteoarthritis defects: A biochemical, histological and immunohistochemical analysis of the repair tissue after treatment with marrow-stimulation techniques. Knee Surg Sports Traumatol Arthrosc 2012; 20 (11): 2315-2324.
22. de Girolamo L, Bertolini G, Cervellin M, Sozzi G, Volpi P,. Treatment of chondral defects of the knee with one step matrix-assisted technique enhanced by autologous concentrated bone marrow: In vitro characterisation of mesenchymal stem cells from iliac crest and subchondral bone. Injury 2010; 41 (11): 1172-1177.
23. Shi J, Zhang X, Zeng X, Zhu J, Pi Y, Zhou C, Ao Y,. One-step articular cartilage repair: Combination of in situ bone marrow stem cells with cell-free poly(l -lactic-co-glycolic acid) scaffold in a rabbit model. Orthopedics 2012; 35 (5): e665-e671.
24. Cavallo C, Desando G, Columbaro M, Ferrari A, Zini N, Facchini A, Grigolo B,. Chondrogenic differentiation of bone marrow concentrate grown onto a hylauronan scaffold: Rationale for its use in the treatment of cartilage lesions J Biomed Mater Res A 2012 [Epub ahead of print].
25. Xie X, Wang Y, Zhao C, Guo S, Liu S, Jia W, Tuan RS, Zhang C,. Comparative evaluation of MSCs from bone marrow and adipose tissue seeded in PRP-derived scaffold for cartilage regeneration. Biomaterials 2012; 33 (29): 7008-7018.
26. Yang Z, Wu Y, Li C, Zhang T, Zou Y, Hui JH, Ge Z, Lee EH,. Improved mesenchymal stem cells attachment and in vitro cartilage tissue formation on chitosan-modified poly(l -lactide-co-epsilon-caprolactone) scaffold. Tissue Eng Part A 2012; 18 (3-4): 242-251.
27. Yoon IS, Chung CW, Sung JH, Cho HJ, Kim JS, Shim WS, Shim CK, Chung SJ, Kim DD,. Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold. J Biosci Bioeng 2011; 112 (4): 402-408.
28. You M, Peng G, Li J, Ma P, Wang Z, Shu W, Peng S, Chen GQ,. Chondrogenic differentiation of human bone marrow mesenchymal stem cells on polyhydroxyalkanoate (PHA) scaffolds coated with PHA granule binding protein PhaP fused with RGD peptide. Biomaterials 2011; 32 (9): 2305-2313.
29. 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 (36): 5570-5580.
30. Chomczynski P,. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 1993; 15 (3): 532-534, 536-537.
31. Neumann K, Dehne T, Endres M, Erggelet C, Kaps C, Ringe J, Sittinger M,. Chondrogenic differentiation capacity of human mesenchymal progenitor cells derived from subchondral cortico-spongious bone. J Orthop Res 2008; 26 (11): 1449-1456.
32. Behrens P,. Matrix-coupled microfracture-A new concept for cartilage defect repair. Arthroskopie 2005; 18: 193-197.
33. Benthien JP, Behrens P,. The treatment of chondral and osteochondral defects of the knee with autologous matrix-induced chondrogenesis (AMIC): Method description and recent developments. Knee Surg Sports Traumatol Arthrosc 2011; 19 (8): 1316-1319.
34. Dhollander AA, De Neve F, Almqvist KF, Verdonk R, Lambrecht S, Elewaut D, Verbruggen G, Verdonk PC,. Autologous matrix-induced chondrogenesis combined with platelet-rich plasma gel: Technical description and a five pilot patients report. Knee Surg Sports Traumatol Arthrosc 2011; 19 (4): 536-542.
35. 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 (6): 431-438.
36. Barry F, Boynton RE, Liu B, Murphy JM,. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: Differentiation-dependent gene expression of matrix components. Exp Cell Res 2001; 268 (2): 189-200.
37. 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 (1): 265-2672.
38. Cals FL, Hellingman CA, Koevoet W, Baatenburg de Jong RJ, van Osch GJ,. Effects of transforming growth factor-beta subtypes on in vitro cartilage production and mineralization of human bone marrow stromal-derived mesenchymal stem cells. J Tissue Eng Regen Med 2012; 6 (1): 68-76.
39. Alves da Silva ML, Martins A, Costa-Pinto AR, Correlo VM, Sol P, Bhattacharya M, Faria S, Reis RL, Neves NM,. Chondrogenic differentiation of human bone marrow mesenchymal stem cells in chitosan-based scaffolds using a flow-perfusion bioreactor. J Tissue Eng Regen Med 2011; 5 (9): 722-732.
40. Bhardwaj N, Kundu SC,. Chondrogenic differentiation of rat MSCs on porous scaffolds of silk fibroin/chitosan blends. Biomaterials 2012; 33 (10): 2848-2857.
41. Izal I, Aranda P, Sanz-Ramos P, Ripalda P, Mora G, Granero-Molto F, Deplaine H, Gomez-Ribelles JL, Ferrer GG, Acosta V, Ochoa I, García-Aznar JM, Andreu EJ, Monleõn-Pradas M, Doblaré M, Prõsper F,. Culture of human bone marrow-derived mesenchymal stem cells on of poly(l -lactic acid) scaffolds: Potential application for the tissue engineering of cartilage. Knee Surg Sports Traumatol Arthrosc 2012 [Epub ahead of print].
42. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI, Goldberg VM,. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 1994; 76 (4): 579-592.
43. Xie J, Han Z, Naito M, Maeyama A, Kim SH, Kim YH, Matsuda T,. Articular cartilage tissue engineering based on a mechano-active scaffold made of poly(l -lactide-co-epsilon-caprolactone): In vivo performance in adult rabbits. J Biomed Mater Res B Appl Biomater 2010; 94 (1): 80-88.
44. Han SH, Kim YH, Park MS, Kim IA, Shin JW, Yang WI, Jee KS, Park KD, Ryu GH, Lee JW,. Histological and biomechanical properties of regenerated articular cartilage using chondrogenic bone marrow stromal cells with a PLGA scaffold in vivo. J Biomed Mater Res A 2008; 87 (4): 850-861.
45. Wakitani S, Okabe T, Horibe S, Mitsuoka T, Saito M, Koyama T, Nawata M, Tensho K, Kato H, Uematsu K, Kuroda R, Kurosaka M, Yoshiya S, Hattori K, Ohgushi H,. Safety of autologous bone marrow-derived mesenchymal stem cell transplantation for cartilage repair in 41 patients with 45 joints followed for up to 11 years and 5 months. J Tissue Eng Regen Med 2011; 5 (2): 146-150.
46. Gigante A, Calcagno S, Cecconi S, Ramazzotti D, Manzotti S, Enea D,. Use of collagen scaffold and autologous bone marrow concentrate as a one-step cartilage repair in the knee: Histological results of second-look biopsies at 1 year follow-up. Int J Immunopathol Pharmacol 2011; 24 (1 Suppl 2): 69-72.
47. 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 (1): 27-35.
48. Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, Ohgushi H, Wakitani S, Kurosaka M,. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 2007; 15 (2): 226-231.
49. Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M,. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 2002; 10 (3): 199-206.
50. Wakitani S, Mitsuoka T, Nakamura N, Toritsuka Y, Nakamura Y, Horibe S,. Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: Two case reports. Cell Transplant 2004; 13 (5): 595-600.