Potential of Agarose/Silk Fibroin Blended Hydrogel for in Vitro Cartilage Tissue Engineering

ACS Applied Materials and Interfaces

Volumn 8, Issue 33, 2016, Pages 21236-21249

  Singh, Yogendra Pratap ^a   Bhardwaj, Nandana ^b   Mandal, Biman B ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI   (India)

^b INSTITUTE OF ADVANCED STUDY IN SCIENCE AND TECHNOLOGY   (India)

Author keywords

agarose; cartilage; non mulberry silk; silk fibroin; tissue engineering

Indexed keywords

BIODEGRADATION; BIOMATERIALS; CARTILAGE; COLLAGEN; DEPOSITION; FIELD EMISSION MICROSCOPES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; GLYCOPROTEINS; MACROPHAGES; METALS; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; PORE SIZE; SCANNING ELECTRON MICROSCOPY; TISSUE; TISSUE ENGINEERING;

AGAROSE; CARTILAGE TISSUE ENGINEERING; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; IMMUNOHISTOCHEMICAL ANALYSIS; NON-MULBERRY SILK; SILK FIBROIN; SULFATED GLYCOSAMINOGLYCANS; TUMOR NECROSIS FACTOR ALPHA;

HYDROGELS;

BIOMATERIAL; FIBROIN; SEPHAROSE;

ANIMAL; BOMBYX; CARTILAGE; CHEMISTRY; HYDROGEL; MOUSE; TISSUE ENGINEERING; TISSUE SCAFFOLD;

ANIMALS; BIOCOMPATIBLE MATERIALS; BOMBYX; CARTILAGE; FIBROINS; HYDROGELS; MICE; SEPHAROSE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84983528621     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b08285     Document Type: Article

References (70)

1. Hinman, R. S.; Hunt, M. A.; Creaby, M. W.; Wrigley, T. V.; McManus, F. J.; Bennell, K. L. Hip Muscle Weakness in Individuals with Medial Knee Osteoarthritis Arthritis Care Res. 2010, 62, 1190-1193 10.1002/acr.20199
2. Piscitelli, P.; Iolascon, G.; Di Tanna, G.; Bizzi, E.; Chitano, G.; Argentiero, A.; Neglia, C.; Giolli, L.; Distante, A.; Gimigliano, R. Socioeconomic Burden of Total Joint Arthroplasty for Symptomatic Hip and Knee Osteoarthritis in the Italian Population: A 5-Year Analysis Based on Hospitalization Records Arthritis Care Res. 2012, 64, 1320-1327 10.1002/acr.21706
3. Wang, Y.; Kim, U.-J.; Blasioli, D. J.; Kim, H.-J.; Kaplan, D. L. In Vitro Cartilage Tissue Engineering with 3D Porous Aqueous-Derived Silk Scaffolds and Mesenchymal Stem Cells Biomaterials 2005, 26, 7082-7094 10.1016/j.biomaterials.2005.05.022
4. Redman, S.; Oldfield, S.; Archer, C. Current Strategies for Articular Cartilage Repair Eur. Cells Mater. 2005, 9, 23-32
5. Abdel-Sayed, P.; Pioletti, D. P. Strategies for Improving the Repair of Focal Cartilage Defects Nanomedicine 2015, 10, 2893-2905 10.2217/nnm.15.119
6. Langer, R.; Vacanti, J. Tissue Engineering Science 1993, 260, 920-926 10.1126/science.8493529
7. O'brien, F. J. Biomaterials & Scaffolds for Tissue Engineering Mater. Today 2011, 14, 88-95 10.1016/S1369-7021(11)70058-X
8. Lee, K. Y.; Mooney, D. J. Hydrogels for Tissue Engineering Chem. Rev. 2001, 101, 1869-1880 10.1021/cr000108x
9. Wang, H. Y.; Zhang, Y. Q. Processing Silk Hydrogel and Its Applications in Biomedical Materials Biotechnol. Prog. 2015, 31, 630-640 10.1002/btpr.2058
10. Bellamkonda, R.; Ranieri, J. P.; Bouche, N.; Aebischer, P. Hydrogel-Based Three-Dimensional Matrix for Neural Cells J. Biomed. Mater. Res. 1995, 29, 663-671 10.1002/jbm.820290514
11. Selmi, T.; Verdonk, P.; Chambat, P.; Dubrana, F.; Potel, J.-F.; Barnouin, L.; Neyret, P. Autologous Chondrocyte Implantation in a Novel Alginate-Agarose Hydrogel: Outcome at Two Years J. Bone Jt. Surg., Br. Vol. 2008, 90, 597-604 10.1302/0301-620X.90B5.20360
12. Buschmann, M. D.; Gluzband, Y. A.; Grodzinsky, A. J.; Hunziker, E. B. Mechanical Compression Modulates Matrix Biosynthesis in Chondrocyte/Agarose Culture J. Cell Sci. 1995, 108, 1497-1508
13. Francioli, S. E.; Candrian, C.; Martin, K.; Heberer, M.; Martin, I.; Barbero, A. Effect of Three-Dimensional Expansion and Cell Seeding Density on the Cartilage-Forming Capacity of Human Articular Chondrocytes in Type II Collagen Sponges J. Biomed. Mater. Res., Part A 2010, 95, 924-931 10.1002/jbm.a.32917
14. Yodmuang, S.; McNamara, S. L.; Nover, A. B.; Mandal, B. B.; Agarwal, M.; Kelly, T. A.; Chao, P. H.; Hung, C.; Kaplan, D. L.; Vunjak-Novakovic, G. Silk Microfiber-Reinforced Silk Hydrogel Composites for Functional Cartilage Tissue Repair Acta Biomater. 2015, 11, 27-36 10.1016/j.actbio.2014.09.032
15. Lima, E. G.; Bian, L.; Ng, K. W.; Mauck, R. L.; Byers, B. A.; Tuan, R. S.; Ateshian, G. A.; Hung, C. T. The Beneficial Effect of Delayed Compressive Loading on Tissue-Engineered Cartilage Constructs Cultured with TGF-β3 Osteoarthr. Cartil. 2007, 15, 1025-1033 10.1016/j.joca.2007.03.008
16. Benya, P. D.; Shaffer, J. D. Dedifferentiated Chondrocytes Reexpress the Differentiated Collagen Phenotype when Cultured in Agarose Gels Cell 1982, 30, 215-224 10.1016/0092-8674(82)90027-7
17. Buschmann, M. D.; Gluzband, Y. A.; Grodzinsky, A. J.; Kimura, J. H.; Hunziker, E. B. Chondrocytes in Agarose Culture Synthesize a Mechanically Functional Extracellular Matrix J. Orthop. Res. 1992, 10, 745-758 10.1002/jor.1100100602
18. Chao, P. H. G.; Yodmuang, S.; Wang, X.; Sun, L.; Kaplan, D. L. Vunjak-Novakovic, G. Silk Hydrogel for Cartilage Tissue Engineering J. Biomed. Mater. Res., Part B 2010, 95, 84-90 10.1002/jbm.b.31686
19. Gruber, H. E.; Fisher, E. C., Jr; Desai, B.; Stasky, A. A.; Hoelscher, G.; Hanley, E. N., Jr Human Intervertebral Disc Cells from the Annulus: Three-Dimensional Culture in Agarose or Alginate and Responsiveness to TGF-β1 Exp. Cell Res. 1997, 235, 13-21 10.1006/excr.1997.3647
20. Hunter, C. J.; Levenston, M. E. Maturation and Integration of Tissue-Engineered Cartilages within an In Vitro Defect Repair Model Tissue Eng. 2004, 10, 736-746 10.1089/1076327041348310
21. Doulabi, A. H.; Mequanint, K.; Mohammadi, H. Blends and Nanocomposite Biomaterials for Articular Cartilage Tissue Engineering Materials 2014, 7, 5327-5355 10.3390/ma7075327
22. Bhat, S.; Tripathi, A.; Kumar, A. Supermacroprous Chitosan-Agarose-Gelatin Cryogels: In Vitro Characterization and In Vivo Assessment for Cartilage Tissue Engineering J. R. Soc., Interface 2011, 8, 540-554 10.1098/rsif.2010.0455
23. Vepari, C.; Kaplan, D. L. Silk as a Biomaterial Prog. Polym. Sci. 2007, 32, 991-1007 10.1016/j.progpolymsci.2007.05.013
24. Rockwood, D. N.; Preda, R. C.; Yücel, T.; Wang, X.; Lovett, M. L.; Kaplan, D. L. Materials Fabrication from Bombyx Mori Silk Fibroin Nat. Protoc. 2011, 6, 1612-1631 10.1038/nprot.2011.379
25. Meinel, L.; Hofmann, S.; Karageorgiou, V.; Kirker-Head, C.; McCool, J.; Gronowicz, G.; Zichner, L.; Langer, R.; Vunjak-Novakovic, G.; Kaplan, D. L. The Inflammatory Responses to Silk Films In Vitro and In Vivo Biomaterials 2005, 26, 147-155 10.1016/j.biomaterials.2004.02.047
26. Mandal, B. B.; Grinberg, A.; Seok Gil, E.; Panilaitis, B.; Kaplan, D. L. High-Strength Silk Protein Scaffolds for Bone Repair Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 7699-7704 10.1073/pnas.1119474109
27. Altman, G. H.; Horan, R. L.; Lu, H. H.; Moreau, J.; Martin, I.; Richmond, J. C.; Kaplan, D. L. Silk Matrix for Tissue Engineered Anterior Cruciate Ligaments Biomaterials 2002, 23, 4131-4141 10.1016/S0142-9612(02)00156-4
28. Kang, J. H.; Gimble, J. M.; Kaplan, D. L. In Vitro 3D Model for Human Vascularized Adipose Tissue Tissue Eng., Part A 2009, 15, 2227-2236 10.1089/ten.tea.2008.0469
29. Wang, Y.; Blasioli, D. J.; Kim, H.-J.; Kim, H. S.; Kaplan, D. L. Cartilage Tissue Engineering with Silk Scaffolds and Human Articular Chondrocytes Biomaterials 2006, 27, 4434-4442 10.1016/j.biomaterials.2006.03.050
30. Park, S. Y.; Ki, C. S.; Park, Y. H.; Jung, H. M.; Woo, K. M.; Kim, H. J. Electrospun Silk Fibroin Scaffolds with Macropores for Bone Regeneration: An In Vitro and In Vivo Study Tissue Eng., Part A 2010, 16, 1271-1279 10.1089/ten.tea.2009.0328
31. Lovett, M.; Eng, G.; Kluge, J.; Cannizzaro, C.; Vunjak-Novakovic, G.; Kaplan, D. L. Tubular Silk Scaffolds for Small Diameter Vascular Grafts Organogenesis 2010, 6, 217-224 10.4161/org.6.4.13407
32. Mauney, J. R.; Nguyen, T.; Gillen, K.; Kirker-Head, C.; Gimble, J. M.; Kaplan, D. L. Engineering Adipose-Like Tissue In Vitro and In Vivo Utilizing Human Bone Marrow and Adipose-Derived Mesenchymal Stem Cells with Silk Fibroin 3D Scaffolds Biomaterials 2007, 28, 5280-5290 10.1016/j.biomaterials.2007.08.017
33. Chen, C.-H.; Liu, J. M.-J.; Chua, C.-K.; Chou, S.-M.; Shyu, V. B.-H.; Chen, J.-P. Cartilage Tissue Engineering with Silk Fibroin Scaffolds Fabricated by Indirect Additive Manufacturing Technology Materials 2014, 7, 2104-2119 10.3390/ma7032104
34. Saha, S.; Kundu, B.; Kirkham, J.; Wood, D.; Kundu, S. C.; Yang, X. B. Osteochondral Tissue Engineering In Vivo: A Comparative Study using Layered Silk Fibroin Scaffolds from Mulberry and Non-mulberry Silkworms PLoS One 2013, 8, e80004 10.1371/journal.pone.0080004
35. Kar, S.; Talukdar, S.; Pal, S.; Nayak, S.; Paranjape, P.; Kundu, S. Silk Gland Fibroin from Indian Muga Silkworm Antheraea Assama as Potential Biomaterial Tissue Eng. Regener. Med. 2013, 10, 200-210 10.1007/s13770-012-0008-6
36. Bhardwaj, N.; Rajkhowa, R.; Wang, X.; Devi, D. Milled Non-Mulberry Silk Fibroin Microparticles as Biomaterial for Biomedical Applications Int. J. Biol. Macromol. 2015, 81, 31-40 10.1016/j.ijbiomac.2015.07.049
37. Gupta, A.; Mita, K.; Arunkumar, K. P.; Nagaraju, J. Molecular Architecture of Silk Fibroin of Indian Golden Silkmoth, Antheraea Assama Sci. Rep. 2015, 5, 12706 10.1038/srep12706
38. Loeser, R. F. Integrins and Chondrocyte-Matrix Interactions in Articular Cartilage Matrix Biol. 2014, 39, 11-16 10.1016/j.matbio.2014.08.007
39. Mandal, B. B.; Das, S.; Choudhury, K.; Kundu, S. C. Implication of Silk Film RGD Availability and Surface Roughness on Cytoskeletal Organization and Proliferation of Primary Rat Bone Marrow Cells Tissue Eng., Part A 2010, 16, 2391-2403 10.1089/ten.tea.2009.0206
40. Talukdar, B.; Saikia, M.; Handique, P. J.; Devi, D. Effect of Organic Solvents on Tensile Strength of Muga Silk Produced by Antheraea Assamensis Int. J. Pure. Appl. Sci. Technol. 2011, 7, 81-86
41. Bhardwaj, N.; Singh, Y. P.; Devi, D.; Kandimalla, R.; Kotoky, J.; Mandal, B. B. Potential of Silk Fibroin/Chondrocyte Constructs of Muga Silkworm Antheraea Assamensis for Cartilage Tissue Engineering J. Mater. Chem. B 2016, 4, 3670-3684 10.1039/C6TB00717A
42. Gupta, P.; Kumar, M.; Bhardwaj, N.; Kumar, J. P.; Krishnamurthy, C.; Nandi, S. K.; Mandal, B. B. Mimicking Form and Function of Native Small Diameter Vascular Conduits using Mulberry and Non-Mulberry Patterned Silk Films ACS Appl. Mater. Interfaces 2016, 8, 15874-15888 10.1021/acsami.6b00783
43. Maličev, E.; Kregar-Velikonja, N.; Barlič, A.; Alibegović, A.; Drobnič, M. Comparison of Articular and Auricular Cartilage as a Cell Source for the Autologous Chondrocyte Implantation J. Orthop. Res. 2009, 27, 943-948 10.1002/jor.20833
44. Mandal, B. B.; Park, S.-H.; Gil, E. S.; Kaplan, D. L. Multilayered Silk Scaffolds for Meniscus Tissue Engineering Biomaterials 2011, 32, 639-651 10.1016/j.biomaterials.2010.08.115
45. Mandal, B. B.; Kundu, S. A Novel Method for Dissolution and Stabilization of Non-Mulberry Silk Gland Protein Fibroin using Anionic Surfactant Sodium Dodecyl Sulfate Biotechnol. Bioeng. 2008, 99, 1482-1489 10.1002/bit.21699
46. Whitley, C.; Ridnour, M.; Draper, K.; Dutton, C.; Neglia, J. Diagnostic Test for Mucopolysaccharidosis. I. Direct Method for Quantifying Excessive Urinary Glycosaminoglycan Excretion Clin. Chem. 1989, 35, 374-379
47. Tullberg-Reinert, H.; Jundt, G. In Situ Measurement of Collagen Synthesis by Human Bone Cells with a Sirius Red-Based Colorimetric Microassay: Effects of Transforming Growth Factor β2 and Ascorbic Acid 2-Phosphate Histochem. Cell Biol. 1999, 112, 271-276 10.1007/s004180050447
48. Wang, L.; Stegemann, J. P. Extraction of High Quality RNA from Polysaccharide Matrices using Cetlytrimethylammonium Bromide Biomaterials 2010, 31, 1612-1618 10.1016/j.biomaterials.2009.11.024
49. Bhardwaj, N.; Kundu, S. C. Chondrogenic Differentiation of Rat Mscs on Porous Scaffolds of Silk Fibroin/Chitosan Blends Biomaterials 2012, 33, 2848-2857 10.1016/j.biomaterials.2011.12.028
50. Bhardwaj, N.; Nguyen, Q. T.; Chen, A. C.; Kaplan, D. L.; Sah, R. L.; Kundu, S. C. Potential of 3-D Tissue Constructs Engineered from Bovine Chondrocytes/Silk Fibroin-Chitosan for In Vitro Cartilage Tissue Engineering Biomaterials 2011, 32, 5773-5781 10.1016/j.biomaterials.2011.04.061
51. Lien, S. M.; Ko, L. Y.; Huang, T. J. Effect of Pore Size on ECM Secretion and Cell Growth in Gelatin Scaffold for Articular Cartilage Tissue Engineering Acta Biomater. 2009, 5, 670-679 10.1016/j.actbio.2008.09.020
52. Liao, J.; Qu, Y.; Chu, B.; Zhang, X.; Qian, Z. Biodegradable CSMA/PECA/Graphene Porous Hybrid Scaffold for Cartilage Tissue Engineering Sci. Rep. 2015, 5, 9879 10.1038/srep09879
53. Cao, Z.; Gilbert, R. J.; He, W. Simple Agarose-Chitosan Gel Composite System for Enhanced Neuronal Growth in Three Dimensions Biomacromolecules 2009, 10, 2954-2959 10.1021/bm900670n
54. Wang, X.; Kluge, J. A.; Leisk, G. G.; Kaplan, D. L. Sonication-Induced Gelation of Silk Fibroin for Cell Encapsulation Biomaterials 2008, 29, 1054-1064 10.1016/j.biomaterials.2007.11.003
55. Li, M.; Ogiso, M.; Minoura, N. Enzymatic Degradation Behavior of Porous Silk Fibroin Sheets Biomaterials 2003, 24, 357-365 10.1016/S0142-9612(02)00326-5
56. Horan, R. L.; Antle, K.; Collette, A. L.; Wang, Y.; Huang, J.; Moreau, J. E.; Volloch, V.; Kaplan, D. L.; Altman, G. H. In Vitro Degradation of Silk Fibroin Biomaterials 2005, 26, 3385-3393 10.1016/j.biomaterials.2004.09.020
57. You, R.; Xu, Y.; Liu, Y.; Li, X.; Li, M. Comparison of the In Vitro and In Vivo Degradations of Silk Fibroin Scaffolds from Mulberry and Non-mulberry Silkworms Biomed. Mater. 2015, 10, 015003 10.1088/1748-6041/10/1/015003
58. Brown, J.; Lu, C. L.; Coburn, J.; Kaplan, D. L. Impact of Silk Biomaterial Structure on Proteolysis Acta Biomater. 2015, 11, 212-221 10.1016/j.actbio.2014.09.013
59. Baimark, Y.; Srisa-ard, M.; Srihanam, P. Morphology and Thermal Stability of Silk Fibroin/Starch Blended Microparticles eXPRESS Polym. Lett. 2010, 4, 781-789 10.3144/expresspolymlett.2010.94
60. Mahmoud, A. A.; Osman, O.; Eid, K.; Ashkar, E.; Okasha, A.; Atta, D.; Eid, M.; Aziz, Z. A.; Fakhry, A. FTIR Spectroscopy of Natural Bio-Polymers Blends Middle East J. Appl. Sci. 2014, 4, 816-824
61. Forget, A.; Christensen, J.; Lüdeke, S.; Kohler, E.; Tobias, S.; Matloubi, M.; Thomann, R.; Shastri, V. P. Polysaccharide Hydrogels with Tunable Stiffness and Provasculogenic Properties via α-Helix to β-Sheet Switch in Secondary Structure Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 12887-12892 10.1073/pnas.1222880110
62. Le Goff, K. J.; Gaillard, C.; Helbert, W.; Garnier, C.; Aubry, T. Rheological Study of Reinforcement of Agarose Hydrogels by Cellulose Nanowhiskers Carbohydr. Polym. 2015, 116, 117-123 10.1016/j.carbpol.2014.04.085
63. Priya, M. V.; Kumar, R. A.; Sivashanmugam, A.; Nair, S. V.; Jayakumar, R. Injectable Amorphous Chitin-Agarose Composite Hydrogels for Biomedical Applications J. Funct. Biomater. 2015, 6, 849-862 10.3390/jfb6030849
64. Matsiko, A.; Gleeson, J. P.; O'Brien, F. J. Scaffold Mean Pore Size Influences Mesenchymal Stem Cell Chondrogenic Differentiation and Matrix Deposition Tissue Eng., Part A 2015, 21, 486-497 10.1089/ten.tea.2013.0545
65. Han, K. S.; Song, J. E.; Tripathy, N.; Kim, H.; Moon, B. M.; Park, C. H.; Khang, G. Effect of Pore Sizes of Silk Scaffolds for Cartilage Tissue Engineering Macromol. Res. 2015, 23, 1091-1097 10.1007/s13233-015-3156-4
66. Sakai, S.; Hashimoto, I.; Kawakami, K. Synthesis of an Agarose-Gelatin Conjugate for use as a Tissue Engineering Scaffold J. Biosci. Bioeng. 2007, 103, 22-26 10.1263/jbb.103.22
67. Kwon, H.; Sun, L.; Cairns, D. M.; Rainbow, R. S.; Preda, R. C.; Kaplan, D. L.; Zeng, L. The Influence of Scaffold Material on Chondrocytes under Inflammatory Conditions Acta Biomater. 2013, 9, 6563-6575 10.1016/j.actbio.2013.01.004
68. Zhang, Q.; Lu, H.; Kawazoe, N.; Chen, G. Pore Size Effect of Collagen Scaffolds on Cartilage Regeneration Acta Biomater. 2014, 10, 2005-2013 10.1016/j.actbio.2013.12.042
69. Fernández-Cossío, S.; León-Mateos, A.; Sampedro, F. G.; Oreja, M. T. C. Biocompatibility of Agarose Gel as a Dermal Filler: Histologic Evaluation of Subcutaneous Implants Plast. Reconstr. Surg. 2007, 120, 1161-1169 10.1097/01.prs.0000279475.99934.71
70. Panilaitis, B.; Altman, G. H.; Chen, J.; Jin, H. J.; Karageorgiou, V.; Kaplan, D. L. Macrophage Responses to Silk Biomaterials 2003, 24, 3079-3085 10.1016/S0142-9612(03)00158-3