Carboxylated Agarose (CA)-Silk Fibroin (SF) Dual Confluent Matrices Containing Oriented Hydroxyapatite (HA) Crystals: Biomimetic Organic/Inorganic Composites for Tibia Repair

Biomacromolecules

Volumn 17, Issue 7, 2016, Pages 2437-2447

  Hu, Jing Xiao ^a   Ran, Jia Bing ^a   Chen, Si ^a   Jiang, Pei ^a   Shen, Xin Yu ^a   Tong, Hua ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; BIOMIMETICS; BIOMINERALIZATION; CARBOXYLATION; CHEMICAL STABILITY; DEFECTS; DEGRADATION; HYDROXYAPATITE; REPAIR; SCAFFOLDS (BIOLOGY);

BIOLOGICAL PROPERTIES; CELL BEHAVIORS; COMPOSITE SCAFFOLDS; DEGRADATION RATE; LOAD-BEARING BONE REPAIR; ORGANIC MATRIX; ORGANIC/INORGANIC COMPOSITES; PREFERRED ORIENTATIONS;

BONE;

AGAROSE; BIOMIMETIC MATERIAL; HYDROXYAPATITE; NANOROD; NANOSHEET; SILK FIBROIN; FIBROIN; NANOPARTICLE; SEPHAROSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA SHEET; BIODEGRADATION; BIOMINERALIZATION; BONE DEVELOPMENT; BONE REMODELING; BONE TISSUE; CARBOXYLATION; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CHEMICAL COMPOSITION; COMPRESSIVE STRENGTH; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; CRYSTALLIZATION; IN VITRO STUDY; MALE; MOLECULAR WEIGHT; NONHUMAN; OSTEOBLAST; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; RAT; THERMOSTABILITY; TIBIA; YOUNG MODULUS; ANIMAL; BIOMIMETICS; CELL CULTURE; CHEMISTRY; MATERIALS TESTING; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WOUND HEALING;

ANIMALS; BIOMIMETICS; CELLS, CULTURED; DURAPATITE; FIBROINS; MALE; MATERIALS TESTING; NANOPARTICLES; OSTEOGENESIS; RATS; RATS, SPRAGUE-DAWLEY; SEPHAROSE; TIBIA; WOUND HEALING;

EID: 84978906200     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.6b00587     Document Type: Article

References (47)

1. Short, A. R.; Koralla, D.; Deshmukh, A.; Wissel, B.; Stocker, B.; Calhoun, M.; Dean, D.; Winter, J. O. Hydrogels that allow and facilitate bone repair, remodeling, and regeneration J. Mater. Chem. B 2015, 3, 7818-7830 10.1039/C5TB01043H
2. He, F.; Chen, Y.; Li, J.; Lin, B.; Ouyang, Y.; Yu, B.; Xia, Y.; Yu, B.; Ye, J. Improving bone repair of femoral and radial defects in rabbit by incorporating PRP into PLGA/CPC composite scaffold with unidirectional pore structure J. Biomed. Mater. Res., Part A 2015, 103, 1312-1324 10.1002/jbm.a.35248
3. Chatzinikolaidou, M.; Rekstyte, S.; Danilevicius, P.; Pontikoglou, C.; Papadaki, H.; Farsari, M.; Vamvakaki, M. Adhesion and growth of human bone marrow mesenchymal stem cells on precise-geometry 3D organic-inorganic composite scaffolds for bone repair Mater. Sci. Eng., C 2015, 48, 301-309 10.1016/j.msec.2014.12.007
4. Liu, X.; Wei, D.; Zhong, J.; Ma, M.; Zhou, J.; Peng, X.; Ye, Y.; Sun, G.; He, D. Electrospun Nanofibrous P(DLLA-CL) Balloons as Calcium Phosphate Cement Filled Containers for Bone Repair: in Vitro and in Vivo Studies ACS Appl. Mater. Interfaces 2015, 7, 18540-18552 10.1021/acsami.5b04868
5. Curtin, C. M.; Tierney, E. G.; McSorley, K.; Cryan, S.-A.; Duffy, G. P.; O'Brien, F. J. Combinatorial Gene Therapy Accelerates Bone Regeneration: Non-Viral Dual Delivery of VEGF and BMP2 in a Collagen-Nanohydroxyapatite Scaffold Adv. Healthcare Mater. 2015, 4, 223-227 10.1002/adhm.201400397
6. David, F.; Levingstone, T. J.; Schneeweiss, W.; de Swarte, M.; Jahns, H.; Gleeson, J. P.; O'Brien, F. J. Enhanced bone healing using collagen-hydroxyapatite scaffold implantation in the treatment of a large multiloculated mandibular aneurysmal bone cyst in a thoroughbred filly J. Tissue Eng. Regener. Med. 2015, 9, 1193-1199 10.1002/term.2006
7. Ding, G.-J.; Zhu, Y.-J.; Qi, C.; Lu, B.-Q.; Chen, F.; Wu, J. Porous hollow microspheres of amorphous calcium phosphate: soybean lecithin templated microwave-assisted hydrothermal synthesis and application in drug delivery J. Mater. Chem. B 2015, 3, 1823-1830 10.1039/C4TB01862A
8. Huebsch, N.; Lippens, E.; Lee, K.; Mehta, M.; Koshy, S. T.; Darnell, M. C.; Desai, R. M.; Madl, C. M.; Xu, M.; Zhao, X.; Chaudhuri, O.; Verbeke, C.; Kim, W. S.; Alim, K.; Mammoto, A.; Ingber, D. E.; Duda, G. N.; Mooney, D. J. Matrix elasticity of void-forming hydrogels controls transplanted-stem-cell-mediated bone formation Nat. Mater. 2015, 14, 1269-1277 10.1038/nmat4407
9. Kutikov, A. B.; Skelly, J. D.; Ayers, D. C.; Song, J. Templated Repair of Long Bone Defects in Rats with Bioactive Spiral-Wrapped Electrospun Amphiphilic Polymer/Hydroxyapatite Scaffolds ACS Appl. Mater. Interfaces 2015, 7, 4890-4901 10.1021/am508984y
10. Quan, C.; Tang, Y.; Liu, Z.; Rao, M.; Zhang, W.; Liang, P.; Wu, N.; Zhang, C.; Shen, H.; Jiang, Q. Effect of modification degree of nanohydroxyapatite on biocompatibility and mechanical property of injectable poly(methyl methacrylate)-based bone cement J. Biomed. Mater. Res., Part B 2016, 104, 576-584 10.1002/jbm.b.33428
11. Dhivya, S.; Saravanan, S.; Sastry, T.; Selvamurugan, N. Nanohydroxyapatite-reinforced chitosan composite hydrogel for bone tissue repair in vitro and in vivo J. Nanobiotechnol. 2015, 13, 40 10.1186/s12951-015-0099-z
12. Yang, M.; Zhou, G.; Shuai, Y.; Wang, J.; Zhu, L.; Mao, C. Ca2+-induced self-assembly of Bombyx mori silk sericin into a nanofibrous network-like protein matrix for directing controlled nucleation of hydroxylapatite nano-needles J. Mater. Chem. B 2015, 3, 2455-2462 10.1039/C4TB01944J
13. Jahan, K.; Tabrizian, M. Composite biopolymers for bone regeneration enhancement in bony defects Biomater. Sci. 2016, 4, 25-39 10.1039/C5BM00163C
14. Subramaniam, S.; Fang, Y.-H.; Sivasubramanian, S.; Lin, F.-H.; Lin, C.-p. Hydroxyapatite-calcium sulfate-hyaluronic acid composite encapsulated with collagenase as bone substitute for alveolar bone regeneration Biomaterials 2016, 74, 99-108 10.1016/j.biomaterials.2015.09.044
15. Dinjaski, N.; Kaplan, D. L. Recombinant protein blends: silk beyond natural design Curr. Opin. Biotechnol. 2016, 39, 1-7 10.1016/j.copbio.2015.11.002
16. Xie, J.; Peng, C.; Zhao, Q.; Wang, X.; Yuan, H.; Yang, L.; Li, K.; Lou, X.; Zhang, Y. Osteogenic differentiation and bone regeneration of iPSC-MSCs supported by a biomimetic nanofibrous scaffold Acta Biomater. 2016, 29, 365-379 10.1016/j.actbio.2015.10.007
17. Gentile, P.; Nandagiri, V. K.; Daly, J.; Chiono, V.; Mattu, C.; Tonda-Turo, C.; Ciardelli, G.; Ramtoola, Z. Localised controlled release of simvastatin from porous chitosan-gelatin scaffolds engrafted with simvastatin loaded PLGA-microparticles for bone tissue engineering application Mater. Sci. Eng., C 2016, 59, 249-257 10.1016/j.msec.2015.10.014
18. Pina, S.; Oliveira, J. M.; Reis, R. L. Natural-Based Nanocomposites for Bone Tissue Engineering and Regenerative Medicine: A Review Adv. Mater. 2015, 27, 1143-1169 10.1002/adma.201403354
19. Denry, I.; Kuhn, L. T. Design and characterization of calcium phosphate ceramic scaffolds for bone tissue engineering Dent. Mater. 2016, 32, 43-53 10.1016/j.dental.2015.09.008
20. Aizenberg, J.; Fratzl, P. New Materials through Bioinspiration and Nanoscience Adv. Funct. Mater. 2013, 23, 4398-4399 10.1002/adfm.201302690
21. Wegst, U. G. K.; Bai, H.; Saiz, E.; Tomsia, A. P.; Ritchie, R. O. Bioinspired structural materials Nat. Mater. 2014, 14, 23-36 10.1038/nmat4089
22. Diegmueller, J. J.; Cheng, X.; Akkus, O. Modulation of hydroxyapatite nanocrystal size and shape by polyelectrolytic peptides Cryst. Growth Des. 2009, 9, 5220-5226 10.1021/cg900750z
23. Coleman, R. J.; Jack, K. S.; Perrier, S. b.; Grøndahl, L. Hydroxyapatite mineralization in the presence of anionic polymers Cryst. Growth Des. 2013, 13, 4252-4259 10.1021/cg400447e
24. Huang, X.; Liu, X.; Liu, S.; Zhang, A.; Lu, Q.; Kaplan, D. L.; Zhu, H. Biomineralization regulation by nano-sized features in silk fibroin proteins: Synthesis of water-dispersible nano-hydroxyapatite J. Biomed. Mater. Res., Part B 2014, 102, 1720-1729 10.1002/jbm.b.33157
25. Amici, E.; Clark, A. H.; Normand, V.; Johnson, N. B. Interpenetrating network formation in agarose-sodium gellan gel composites Carbohydr. Polym. 2001, 46, 383-391 10.1016/S0144-8617(00)00342-8
26. Hu, J.; Zhu, Y.; Tong, H.; Shen, X.; Chen, L.; Ran, J. A detailed study of homogeneous agarose/hydroxyapatite nanocomposites for load-bearing bone tissue Int. J. Biol. Macromol. 2016, 82, 134-143 10.1016/j.ijbiomac.2015.09.077
27. Yixue, S.; Bin, C.; Yuan, G.; Chaoxi, W.; Lingmin, Z.; Peng, C.; Xiaoying, W.; Shunqing, T. Modification of agarose with carboxylation and grafting dopamine for promotion of its cell-adhesiveness Carbohydr. Polym. 2013, 92, 2245-2251 10.1016/j.carbpol.2012.12.003
28. Forget, A.; Pique, R. A.; Ahmadi, V.; Lüdeke, S.; Shastri, V. P. Mechanically Tailored Agarose Hydrogels through Molecular Alloying with β-Sheet Polysaccharides Macromol. Rapid Commun. 2015, 36, 196-203 10.1002/marc.201400353
29. Hu, J.-x.; Cai, X.; Mo, S.-b.; Chen, L.; Shen, X.-y. Fabrication and characterization of chitosan-silk fibroin/hydroxyapatite composites via in situ precipitation for bone tissue engineering Chin. J. Polym. Sci. 2015, 33, 1661-1671 10.1007/s10118-015-1710-3
30. Li, C.; Vepari, C.; Jin, H.-J.; Kim, H. J.; Kaplan, D. L. Electrospun silk-BMP-2 scaffolds for bone tissue engineering Biomaterials 2006, 27, 3115-3124 10.1016/j.biomaterials.2006.01.022
31. Hu, J.-X.; Ran, J.-B.; Chen, S.; Shen, X.-Y.; Tong, H. Biomineralization-inspired synthesis of chitosan/hydroxyapatite biocomposites based on a novel bilayer rate-controlling model Colloids Surf., B 2015, 136, 457-464 10.1016/j.colsurfb.2015.09.027
32. Vahabzadeh, S.; Roy, M.; Bandyopadhyay, A.; Bose, S. Phase stability and biological property evaluation of plasma sprayed hydroxyapatite coatings for orthopedic and dental applications Acta Biomater. 2015, 17, 47-55 10.1016/j.actbio.2015.01.022
33. Hofmann, S.; Foo, C. W. P.; Rossetti, F.; Textor, M.; Vunjak-Novakovic, G.; Kaplan, D.; Merkle, H.; Meinel, L. Silk fibroin as an organic polymer for controlled drug delivery J. Controlled Release 2006, 111, 219-227 10.1016/j.jconrel.2005.12.009
34. Kim, U.-J.; Park, J.; Kim, H. J.; Wada, M.; Kaplan, D. L. Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin Biomaterials 2005, 26, 2775-2785 10.1016/j.biomaterials.2004.07.044
35. Cai, X.; Chen, L.; Jiang, T.; Shen, X.; Hu, J.; Tong, H. Facile synthesis of anisotropic porous chitosan/hydroxyapatite scaffolds for bone tissue engineering J. Mater. Chem. 2011, 21, 12015-12025 10.1039/c1jm11503k
36. Cüneyt Tas, A. Synthesis of biomimetic Ca-hydroxyapatite powders at 37°C in synthetic body fluids Biomaterials 2000, 21, 1429-1438 10.1016/S0142-9612(00)00019-3
37. Chen, F.; Zhu, Y.-J.; Zhao, X.-Y.; Lu, B.-Q.; Wu, J. Solvothermal synthesis of oriented hydroxyapatite nanorod/nanosheet arrays using creatine phosphate as phosphorus source CrystEngComm 2013, 15, 4527-4531 10.1039/c3ce40115d
38. Díaz, A.; López, T.; Manjarrez, J.; Basaldella, E.; Martínez-Blanes, J. M.; Odriozola, J. A. Growth of hydroxyapatite in a biocompatible mesoporous ordered silica Acta Biomater. 2006, 2, 173-179 10.1016/j.actbio.2005.12.006
39. Kawashita, M.; Nakao, M.; Minoda, M.; Kim, H. M.; Beppu, T.; Miyamoto, T.; Kokubo, T.; Nakamura, T. Apatite-forming ability of carboxyl group-containing polymer gels in a simulated body fluid Biomaterials 2003, 24, 2477-2484 10.1016/S0142-9612(03)00050-4
40. 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
41. Thurber, A. E.; Omenetto, F. G.; Kaplan, D. L. In vivo bioresponses to silk proteins Biomaterials 2015, 71, 145-157 10.1016/j.biomaterials.2015.08.039
42. Garcia-Fuentes, M.; Giger, E.; Meinel, L.; Merkle, H. P. The effect of hyaluronic acid on silk fibroin conformation Biomaterials 2008, 29, 633-642 10.1016/j.biomaterials.2007.10.024
43. Homminga, J.; McCreadie, B. R.; Ciarelli, T. E.; Weinans, H.; Goldstein, S. A.; Huiskes, R. Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level Bone 2002, 30, 759-764 10.1016/S8756-3282(02)00693-2
44. Rezwan, K.; Chen, Q. Z.; Blaker, J. J.; Boccaccini, A. R. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering Biomaterials 2006, 27, 3413-3431 10.1016/j.biomaterials.2006.01.039
45. Li, B.; Aspden, R. M. Composition and mechanical properties of cancellous bone from the femoral head of patients with osteoporosis or osteoarthritis J. Bone Miner. Res. 1997, 12, 641-651 10.1359/jbmr.1997.12.4.641
46. Jämsä, T.; Jalovaara, P.; Peng, Z.; Väänänen, H. K.; Tuukkanen, J. Comparison of three-point bending test and peripheral quantitative computed tomography analysis in the evaluation of the strength of mouse femur and tibia Bone 1998, 23, 155-161 10.1016/S8756-3282(98)00076-3
47. Lin, K. L.; Wu, C. T.; Chang, J. Advances in synthesis of calcium phosphate crystals with controlled size and shape Acta Biomater. 2014, 10, 4071-4102 10.1016/j.actbio.2014.06.017