Bilayered silk/silk-nanoCaP scaffolds for osteochondral tissue engineering: In vitro and in vivo assessment of biological performance

Acta Biomaterialia

Volumn 12, Issue 1, 2015, Pages 227-241

  Yan, Le Ping ^a   Silva Correia, Joana ^a   Oliveira, Mariana B ^a   Vilela, Carlos ^a,b,c   Pereira, Hélder ^a,d   Sousa, Rui A ^a   Mano, João F ^a   Oliveira, Ana L ^a,e   Oliveira, Joaquim M ^a   Reis, Rui L ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c Orthopedic Department   (Portugal)

^d Hospital da Póvoa De Varzim   (Portugal)

^e UNIVERSIDADE CATÓLICA PORTUGUESA   (Portugal)

Author keywords

Bilayered scaffold; Calcium phosphate; Nanocomposite; Osteochondral regeneration; Silk fibroin

Indexed keywords

BONE; CALCIUM PHOSPHATE; SCAFFOLDS (BIOLOGY); TISSUE REGENERATION;

BILAYERED; BILAYERED SCAFFOLDS; CALCIUM PHOSPHATE SCAFFOLDS; IN-VITRO; NANO-CALCIUM PHOSPHATES; OSTEOCHONDRAL DEFECTS; OSTEOCHONDRAL REGENERATIONS; OSTEOCHONDRAL TISSUE ENGINEERING; SILK FIBROIN; VITRO AND IN VIVO;

PHOSPHATASES;

ALKALINE PHOSPHATASE; CALCIUM PHOSPHATE; COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN; MOLECULAR SCAFFOLD; SILK;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE REGENERATION; CARTILAGE; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CELL VIABILITY; CHEMICAL COMPOSITION; CONFORMATION; CONTROLLED STUDY; DNA CONTENT; ENZYMATIC DEGRADATION; EXPERIMENTAL RABBIT; EXTRACELLULAR MATRIX; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; OSSIFICATION; POROSITY; PRIORITY JOURNAL; TISSUE ENGINEERING; WEIGHT REDUCTION; ANIMAL; BONE; CHEMISTRY; PHYSIOLOGY; RABBIT; TISSUE SCAFFOLD;

ORYCTOLAGUS CUNICULUS;

ANIMALS; BONE AND BONES; CALCIUM PHOSPHATES; CARTILAGE; IN VITRO TECHNIQUES; RABBITS; SILK; TISSUE ENGINEERING; TISSUE SCAFFOLDS; X-RAY MICROTOMOGRAPHY;

EID: 84924991609     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.10.021     Document Type: Article

References (57)

1. Mano JF, Reis RL. Osteochondral defects: present situation and tissue engineering approaches. J Tissue Eng Regener Med 2007;1:261-73.
2. Martin I, Miot S, Barbero A, Jakob M, Wendt D. Osteochondral tissue engineering. J Biomech 2007;40:750-65.
3. Gomoll AH, Madry H, Knutsen G, van Dijk N, Seil R, Brittberg M, et al. The subchondral bone in articular cartilage repair: current problems in the surgical management. Knee Surg Sports Traumatol Arthrosc 2010;18:434-47.
4. Weil Jr L. Biologics in foot and ankle surgery. Foot Ankle Spec 2011;4:249-52.
5. Zengerink M, Struijs PA, Tol JL, van Dijk CN. Treatment of osteochondral lesions of the talus: a systematic review. Knee Surg Sports Traumatol Arthrosc 2010;18:238-46.
6. Bitton R. The economic burden of osteoarthritis. Am J Manag Care 2009;15:S230-5.
7. Panseri S, Russo A, Cunha C, Bondi A, Di Martino A, Patella S, et al. Osteochondral tissue engineering approaches for articular cartilage and subchondral bone regeneration. Knee Surg Sports Traumatol Arthrosc 2012;20:1182-91.
8. Langer R, Vacanti JP. Tissue engineering. Science 1993;260:920-6.
9. Wang X, Wenk E, Zhang X, Meinel L, Vunjak-Novakovic G, Kaplan DL. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. J Control Release 2009;134:81-90.
10. Shao XX, Hutmacher DW, Ho ST, Goh JC, Lee EH. Evaluation of a hybrid scaffold/cell construct in repair of high-load-bearing osteochondral defects in rabbits. Biomaterials 2006;27:1071-80.
11. Zhang W, Chen J, Tao J, Hu C, Chen L, Zhao H, et al. The promotion of osteochondral repair by combined intra-articular injection of parathyroid hormone-related protein and implantation of a bi-layer collagen-silk scaffold. Biomaterials 2013;34:6046-57.
12. Minas T, Gomoll AH, Rosenberger R, Royce RO, Bryant T. Increased failure rate of autologous chondrocyte implantation after previous treatment with marrow stimulation techniques. Am J Sports Med 2009;37:902-8.
13. O'Shea TM, Miao X. Bilayered scaffolds for osteochondral tissue engineering. Tissue Eng Part B Rev 2008;14:447-64.
14. Oliveira JM, Rodrigues MT, Silva SS, Malafaya PB, Gomes ME, Viegas CA, et al. Novel hydroxyapatite/chitosan bilayered scaffold for osteochondral tissue-engineering applications: scaffold design and its performance when seeded with goat bone marrow stromal cells. Biomaterials 2006;27:6123-37.
15. Reyes R, Delgado A, Sanchez E, Fernandez A, Hernandez A, Evora C. Repair of an osteochondral defect by sustained delivery of BMP-2 or TGF-beta1 from a bilayered alginate-PLGA scaffold. J Tissue Eng Regener Med 2014;8:521-33.
16. Guo X, Park H, Liu G, Liu W, Cao Y, Tabata Y, et al. In vitro generation of an osteochondral construct using injectable hydrogel composites encapsulating rabbit marrow mesenchymal stem cells. Biomaterials 2009;30:2741-52.
17. Chen J, Chen H, Li P, Diao H, Zhu S, Dong L, et al. Simultaneous regeneration of articular cartilage and subchondral bone in vivo using MSCs induced by a spatially controlled gene delivery system in bilayered integrated scaffolds. Biomaterials 2011;32:4793-805.
18. Kim K, Lam J, Lu S, Spicer PP, Lueckgen A, Tabata Y, et al. Osteochondral tissue regeneration using a bilayered composite hydrogel with modulating dual growth factor release kinetics in a rabbit model. J Control Release 2013;168:166-78.
19. Mohan N, Dormer NH, Caldwell KL, Key VH, Berkland CJ, Detamore MS. Continuous gradients of material composition and growth factors for effective regeneration of the osteochondral interface. Tissue Eng Part A 2011;17:2845-55.
20. Xue D, Zheng Q, Zong C, Li Q, Li H, Qian S, et al. Osteochondral repair using porous poly(lactide-co-glycolide)/nano-hydroxyapatite hybrid scaffolds with undifferentiated mesenchymal stem cells in a rat model. J Biomed Mater Res A 2010;94:259-70.
21. Kon E, Delcogliano M, Filardo G, Busacca M, Di Martino A, Marcacci M. Novel nano-composite multilayered biomaterial for osteochondral regeneration: a pilot clinical trial. Am J Sports Med 2011;39:1180-90.
22. Joshi N, Reverte-Vinaixa M, Diaz-Ferreiro EW, Dominguez-Oronoz R. Synthetic resorbable scaffolds for the treatment of isolated patellofemoral cartilage defects in young patients: magnetic resonance imaging and clinical evaluation. Am J Sports Med 2012;40:1289-95.
23. Bedi A, Foo LF, Williams Iii RJ, Potter HG. The maturation of synthetic scaffolds for osteochondral donor sites of the knee: An MRI and T2-mapping analysis. Cartilage 2010;1:20-8.
24. Moutos FT, Freed LE, Guilak F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 2007;6:162-7.
25. Kon E, Vannini F, Buda R, Filardo G, Cavallo M, Ruffilli A, et al. How to treat osteochondritis dissecans of the knee: surgical techniques and new trends AAOS exhibit selection. J Bone Joint Surg Am 2012;94, e1(1-8).
26. Yang PJ, Temenoff JS. Engineering orthopedic tissue interfaces. Tissue Eng Part B Rev 2009;15:127-41.
27. Grayson WL, Chao PH, Marolt D, Kaplan DL, Vunjak-Novakovic G. Engineering custom-designed osteochondral tissue grafts. Trends Biotechnol 2008;26:181-9.
28. Yan LP, Wang YJ, Ren L, Wu G, Caridade SG, Fan JB, et al. Genipin-cross-linked collagen/chitosan biomimetic scaffolds for articular cartilage tissue engineering applications. J Biomed Mater Res A 2010;95A:465-75.
29. Vepari C, Kaplan DL. Silk as a biomaterial. Prog Polym Sci 2007;32:991-1007.
30. Kim UJ, Park J, Joo Kim H, Wada M, Kaplan DL. Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 2005;26:2775-85.
31. Oliveira AL, Sun L, Kim HJ, Hu X, Rice W, Kluge J, et al. Aligned silk-based 3-D architectures for contact guidance in tissue engineering. Acta Biomater 2012;8:1530-42.
32. Correia C, Bhumiratana S, Yan LP, Oliveira AL, Gimble JM, Rockwood D, et al. Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater 2012;8:2483-92.
33. Kundu B, Kundu SC. Osteogenesis of human stem cells in silk biomaterial for regenerative therapy. Prog Polym Sci 2010;35:1116-27.
34. Fuchs S, Jiang X, Schmidt H, Dohle E, Ghanaati S, Orth C, et al. Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells. Biomaterials 2009;30:1329-38.
35. Dorozhkin SV, Epple M. Biological and medical significance of calcium phosphates. Angew Chem Int Ed 2002;41:3130-46.
36. Salgado AJ, Coutinho OP, Reis RL. Bone tissue engineering: state of the art and future trends. Macromol Biosci 2004;4:743-65.
37. Yan LP, Oliveira JM, Oliveira AL, Caridade SG, Mano JF, Reis RL. Macro/microporous silk fibroin scaffolds with potential for articular cartilage and meniscus tissue engineering applications. Acta Biomater 2012;8:289-301.
38. Yan LP, Silva-Correia J, Correia C, Caridade SG, Fernandes EM, Sousa RA, et al. Bioactive macro/micro porous silk fibroin/nano-sized calcium phosphate scaffolds with potential for bone-tissue-engineering applications. Nanomed (London) 2013;8:359-78.
39. Yan LP, Salgado AJ, Oliveira JM, Oliveira AL, Reis RL. De novo bone formation on macro/microporous silk and silk/nano-sized calcium phosphate scaffolds. J Bioact Compat Polym 2013;28:439-52.
40. Yan LP, Oliveira JM, Oliveira AL, Reis RL. Silk fibroin/nano-CaP bilayered scaffolds for osteochondral tissue engineering. Key Eng Mater 2014;587:245-8.
41. Jin HJ, Park J, Karageorgiou V, Kim UJ, Valluzzi R, Cebe P, et al. Water-stable silk films with reduced b-sheet content. Adv Funct Mater 2005;15:1241-7.
42. Oliveira JM, Silva SS, Malafaya PB, Rodrigues MT, Kotobuki N, Hirose M, et al. Macroporous hydroxyapatite scaffolds for bone tissue engineering applications: Physicochemical characterization and assessment of rat bone marrow stromal cell viability. J Biomed Mater Res A 2009;91A:175-86.
43. th European Conference on Biomaterials. Nantes, 27 September-1 October 2006.
44. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005;26:5474-91.
45. Khanarian NT, Jiang J, Wan LQ, Mow VC, Lu HH. A hydrogel-mineral composite scaffold for osteochondral interface tissue engineering. Tissue Eng Part A 2012;18:533-45.
46. Nazarov R, Jin HJ, Kaplan DL. Porous 3-D scaffolds from regenerated silk fibroin. Biomacromolecules 2004;5:718-26.
47. Marolt D, Augst A, Freed LE, Vepari C, Fajardo R, Patel N, et al. Bone and cartilage tissue constructs grown using human bone marrow stromal cells, silk scaffolds and rotating bioreactors. Biomaterials 2006;27:6138-49.
48. Bhardwaj N, Kundu SC. Silk fibroin protein and chitosan polyelectrolyte complex porous scaffolds for tissue engineering applications. Carbohydr Polym 2011;85:325-33.
49. Wang TW, Spector M. Development of hyaluronic acid-based scaffolds for brain tissue engineering. Acta Biomater 2009;5:2371-84.
50. Liu X, Smith LA, Hu J, Ma PX. Biomimetic nanofibrous gelatin/apatite composite scaffolds for bone tissue engineering. Biomaterials 2009;30:2252-8.
51. Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000;21:2529-43.
52. Mandal BB, Grinberg A, Seok Gil E, Panilaitis B, Kaplan DL. High-strength silk protein scaffolds for bone repair. Proc Natl Acad Sci USA 2012;109:7699-704.
53. Collins AM, Skaer NJV, Gheysens T, Knight D, Bertram C, Roach HI, et al. Bone-like resorbable silk-based scaffolds for load-bearing osteoregenerative applications. Adv Mater 2009;21:75-8.
54. McMahon LA, O'Brien FJ, Prendergast PJ. Biomechanics and mechanobiology in osteochondral tissues. Regener Med 2008;3:743-59.
55. Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL, Chen JS, et al. Silk-based biomaterials. Biomaterials 2003;24:401-16.
56. Oliveira JM, Kotobuki N, Tadokoro M, Hirose M, Mano JF, Reis RL, et al. Ex vivo culturing of stromal cells with dexamethasone-loaded carboxymethylchitosan/poly(amidoamine) dendrimer nanoparticles promotes ectopic bone formation. Bone 2010;46:1424-35.
57. Zhang Y, Wu C, Friis T, Xiao Y. The osteogenic properties of CaP/silk composite scaffolds. Biomaterials 2010;31:2848-56.