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Patrascu Et Al. Polyglycolic Acid-Hyaluronan Scaffolds Loaded with Bone Marrow-Derived Mesenchymal Stem Cells Show

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Patrascu Et Al. Polyglycolic Acid-Hyaluronan Scaffolds Loaded with Bone Marrow-Derived Mesenchymal Stem Cells Show Polyglycolic acid-hyaluronan scaffolds loaded with bone marrow- derived mesenchymal stem cells show chondrogenic differentiation in vitro and cartilage repair in the rabbit model Jenel M. Patrascu,1* Jan Philipp Kruger,€ 2* Hademar G. Boss,€ 1 Anna-Katharina Ketzmar,2 Undine Freymann,2 Michael Sittinger,3,4 Michael Notter,5 Michaela Endres,2,3 Christian Kaps2 1Department of Orthopaedic Surgery, V. Babes University of Medicine and Pharmacy, Timisoara, Romania 2TransTissue Technologies GmbH, Chariteplatz 1, 10117 Berlin, Germany 3Department of Rheumatology, Tissue Engineering Laboratory, Charite Campus Mitte, Charite - Universitatsmedizin€ Berlin, Chariteplatz 1, 10117, Berlin, Germany 4Berlin-Brandenburg Center for Regenerative Therapies, Charite-Universit atsmedizin€ Berlin, Augustenburger Platz 1, 13353 Berlin 5Department of Hematology and Oncology, Charite-Universitatsmedizin€ Berlin, Hindenburgdamm 30, 12200 Berlin, Germany Received 5 November 2012; revised 28 January 2013; accepted 6 March 2013 Published online 10 May 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/jbm.b.32944 Abstract: In cartilage repair, scaffold-assisted one-step chondrogenic marker genes like type II collagen and formation approaches are used to improve the microfracture (Mfx) tech- of hyaline-like cartilaginous tissue in MSC-laden PGA-HA nique. Since the number of progenitors in Mfx is low and may implants. Histological evaluation of rabbit repair tissue forma- further decrease with age, aim of our study was to analyze the tion after 30 and 45 days showed formation of repair tissue, chondrogenic potential of freeze-dried polyglycolic acid-hyalur- rich in chondrocytic cells and of a hyaline-like appearance. onan (PGA-HA) implants preloaded with mesenchymal Controls showed no articular resurfacing, tissue repair in the stem cells (MSCs) in vitro and in a rabbit articular cartilage subchondral zone and fibrin formation. These results suggest defect model. Human bone marrow-derived MSC from iliac that MSC-laden PGA-HA scaffolds have chondrogenic potential crest were cultured in freeze-dried PGA-HA implants for and are a promising option for stem cell-mediated cartilage chondrogenic differentiation. In a pilot study, implants were regeneration. VC 2013 Wiley Periodicals, Inc. J Biomed Mater Res Part loaded with autologous rabbit MSC and used to cover 5 mm 3 B: Appl Biomater 101B: 1310–1320, 2013. 6 mm full-thickness femoral articular cartilage defects (n 5 4). Untreated defects (n 5 3) served as controls. Gene expression Key Words: cartilage repair, cartilage regeneration, cell-free analysis and histology showed induction of typical implant, microfracture, stem cells How to cite this article: Patrascu JM, Kruger€ JP, Boss€ HG, Ketzmar A-K, Freymann U, Sittinger M, Notter M, Endres M, Kaps C. 2013. Polyglycolic acid-hyaluronan scaffolds loaded with bone marrow-derived mesenchymal stem cells show chondrogenic differentiation in vitro and cartilage repair in the rabbit model. J Biomed Mater Res Part B 2013:101B:1310–1320. INTRODUCTION or Mfxs. In Mfx, repair tissue formation by mesenchymal In cartilage repair, a variety of techniques evolved that aim stem cells (MSCs) may be stimulated by growth and differ- at cartilage resurfacing and=or regeneration. These techni- entiation factors from the subchondral bone and=or the sy- ques comprise debridement, bone marrow stimulation (e.g., novial fluid.5,8,9 Although clinical studies demonstrated that abrasion, drilling, and microfracturing), osteochondral graft- the Mfx technique shows good results in the short and mid- ing or mosaicplasty, and autologous chondrocyte implanta- term with up to 5 years follow-up,10 the repair tissue tion with or without the use of scaffolds.1–5 The induced by Mfxs has been shown to be of mostly fibrocarti- microfracture (Mfx) technique is a frequently used and cost laginous appearance with limited short-term durability.11 effective first-line treatment option for the repair of focal Apparently, the Mfx treatment shows good short-term cartilage defects.6,7 In Mfx, bleeding of the subchondral results, but clinical results may be variable in the mid to bone is induced by the introduction of multiple perforations long terms. Apart from that, the technique may be limited *These authors contributed equally to this work. JPK, UF, ME, and CK are employees of TransTissue Technologies GmbH (TTT). TTT develops scaffold-based cartilage repair treatment strategies and developed the PGA-HA scaffold. CK is consultant of BioTissue AG that distributes the PGA-HA based chondrotissue cartilage implant. MS is consultant of BioTissue Technologies GmbH that produces the PGA-HA scaffold. Correspondence to: C. Kaps; e-mail: [email protected] Contract grant sponsor: European Union, EU-FP7 program; contract grand number: TissueGEN: HEALTH-F4-2011-278955 1310 VC 2013 WILEY PERIODICALS, INC. ORIGINAL RESEARCH REPORT by its indication for relatively small focal defects with an 100 U=mL penicillin, 100 mg=mL streptomycin, and 10% intact defect shoulder surrounding the defect. human serum and transferred to cell culture flasks. Medium Recently, scaffold-assisted one-step approaches evolved was exchanged after 72 h and then every 2 days thereafter. that may improve cartilage repair by enhancing repair tissue Cells were allowed to grow to 90% confluence, detached by formation in microfracturing and may extend the indication 0.05% trypsin–ethylenediaminetetraacetic acid (Biochrom) even to partly unshouldered defects by covering the micro- in phosphate-buffered saline (PBS; Biochrom) and used fractured defect with, for example, porcine collagen scaffolds directly for further analysis. with fibrin12,13 or resorbable polyglycolic acid-hyaluronan (PGA-HA) scaffolds.14,15 PGA-HA scaffolds have been shown Fluorescence-activated cell sorting to recruit MSC into the scaffold and guide them toward car- For characterization of MSC, typical MSC-related cell surface tilage repair, with improvement of cartilage repair tissue antigens were analyzed. MSC (2.5 3 105 cells, passage 0; n formation compared to microfracturing alone.16 Clinically, in 5 3 donors) were washed in PBS=0.5% bovine serum albu- a group of 52 patients, implantation of PGA-HA scaffolds for min and incubated with monoclonal mouse anti-human anti- treatment of cartilage defects improved the patients’ situa- bodies CD34-phycoerythrin (PE), CD45-fluorescein- tion as shown by the Knee injury and Osteoarthritis Out- isothiocyanate (FITC), CD73-PE, CD90-FITC, CD105-FITC, come Score (KOOS) at 1 year follow-up and formed hyaline- and CD166-PE, conjugated with FITC or PE for 15 min on like cartilage tissue as assessed by second-look biopsies.17 ice. Staining of cell surface antigens was analyzed using the However, from the technical and cell biology point of view, fluorescence-activated cell sorting Calibur equipped with variability in the mid- to long-term outcome may be, for CELLQUEST software (Becton Dickinson). Apoptotic cells example, due to different depths of the Mfxs,18 use of the were excluded from analysis using propidium iodide. CD34 drilling or the Mfx procedure19 and maybe more impor- stained cells served as isotypic control. tantly due to a reduced availability of MSC with chondro- genic capacity in the subchondral bone marrow. In Three-dimensional tissue culture of human MSC particular, with increasing age, the number of MSC in the in polymer scaffolds bone marrow is reduced dramatically20 and in early osteo- The chondrotissue matrix was prepared as described previ- arthritis, for instance, there may be a reduced potential of ously.29 In brief, resorbable PGA scaffolds (BioTissue AG, cells to induce hyaline-like cartilage repair.21 To overcome Zurich, Switzerland) of 8 mm 3 8mm3 0.5 mm were these hurdles, the enrichment of scaffolds with autologous immersed with 32 mL hyaluronic acid (HA, OstenilVR ; TRB bone marrow concentrate or cells are currently investigated Chemedica AG, Germany) and subsequently freeze-dried for to improve and=or extend the Mfx technique and=or carti- 16 h using a lyophilisator (Leybold-Heraeus, Germany). MSC lage repair.22,23 A recent report about bone marrow concen- (passage 0, n 5 3 donors) were seeded into the PGA-HA trate has shown that cells within the concentrate grow on scaffolds at a density of 2 3 107 viable cells=mL by resus- the HA-based scaffold and are able to undergo chondrogenic pending 0.64 3 106 cells in 21 mL cell culture medium and differentiation.24 In addition, expanded bone marrow and=or 11 mL fibrinogen (Tissucol, Baxter International). Polymer- adipose derived stem cells have been shown to differentiate ization of the fibrinogen was achieved by adding thrombin along the chondrogenic lineage in, for example, platelet-rich (10%, v=v in PBS; Tissucol) and incubation at 37 C for 15 plasma (PRP)-derived scaffolds, porous poly(ethylene min. glycol) diglycidyl ether-cross-linked HA, poly-L-lactide-co- epsilon-caprolactone (PLCL)/chitosan scaffolds, or RGD- Differentiation of human MSC in polymer scaffolds polyhydroxyalkanoate scaffolds.25–28 We hypothesize that For chondrogenic differentiation, MSC-PGA-HA scaffolds (n bone marrow-derived MSC show chondrogenic differentia- 5 4 per donor; n 5 3 donors) were cultured up to 14 days tion in clinically applicable PGA-HA scaffolds in vitro and in DME medium containing 1% Insulin–Transferrin–Sele- that implantation of these cells in PGA-HA scaffolds into nium 1 1, 1 mM sodium pyruvate, 0.35 mM L-proline, 0.17 full-thickness articular cartilage defects leads to hyaline-like mM L-ascorbic acid-2-phosphate, and 0.1 mM dexamethasone cartilage repair in the rabbit model. (all Sigma-Aldrich, St. Louis, MO) and 10 ng=mL transform- ing growth factor-b3 (TGFB3; Peprotech). MSC-PGA-HA scaf- MATERIALS AND METHODS folds in DME medium without TGFB3 served as controls. Isolation and culture of human MSC Medium was exchanged every 2–3 days. Human adult MSC were isolated from iliac crest bone mar- row aspirates of healthy donors (n 5 11, 3 female, 8 male, Real-time polymerase chain reaction age 43–72).
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