A bioinspired 3D shape olibanum-collagen-gelatin scaffolds with tunable porous microstructure for efficient neural tissue regeneration.


Journal

Biotechnology progress
ISSN: 1520-6033
Titre abrégé: Biotechnol Prog
Pays: United States
ID NLM: 8506292

Informations de publication

Date de publication:
01 2020
Historique:
received: 22 12 2018
revised: 14 07 2019
accepted: 17 09 2019
pubmed: 3 10 2019
medline: 9 6 2021
entrez: 3 10 2019
Statut: ppublish

Résumé

There are a number of procedures for regeneration of injured nerves; however, tissue engineering scaffolds seems to be a promising approach for recovery of the functionality of the injured nerves. Consequently, in this study, olibanum-collagen-gelatin scaffolds were fabricated by freeze-cast technology. For this purpose, the olibanum and collagen were extracted from natural sources. The effect of solidification gradient on microstructure and properties of scaffolds was investigated. Scanning electron microscopy micrographs showed the formation of lamellar-type microstructure in which the average pore size reduced with an increase in freezing rate. According to the results, the prepared scaffolds at lower freezing rate showed a slight reduction in mechanical strength while the swelling and biodegradation ratio were increased due to the presence of larger pores and unidirectional channels. The composition of scaffolds and oriented microstructure improved cellular interaction. In addition, scaffolds with lower freezing rate exhibited promising results in terms of adhesion, spreading, and proliferation. In brief, the synthesized scaffolds at lower solidification rate have the potential for more in vitro and in vivo analyses to regeneration of neural defects.

Identifiants

pubmed: 31576679
doi: 10.1002/btpr.2918
doi:

Substances chimiques

Gelatin 9000-70-8
Collagen 9007-34-5
Frankincense R9XLF1R1WM

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2918

Subventions

Organisme : Alborz University of Medical Sciences
Pays : International

Informations de copyright

© 2019 American Institute of Chemical Engineers.

Références

Gu X, Ding F, Williams DF. Neural tissue engineering options for peripheral nerve regeneration. Biomaterials. 2014;35(24):6143-6156. https://doi.org/10.1016/j.biomaterials.2014.04.064.
Ghorbani F, Zamanian A, Nojehdehian H. Effects of pore orientation on in-vitro properties of retinoic acid-loaded PLGA/gelatin scaffolds for artificial peripheral nerve application. Mater Sci Eng C Mater Biol Appl. 2017;77:159-172. https://doi.org/10.1016/j.msec.2017.03.175.
Siriwardane ML. The Extraction of Type I Collagne and the Fabrication of Multi-Filament Embedded Hydrogels for Guided Nerve Regeneration. MSc Thesis. New Jersey Institute of Technology, USA, 2008.
Schmidt CE, Leach JB. Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng. 2003;5(1):293-347. https://doi.org/10.1146/annurev.bioeng.5.011303.120731.
Asthana A, White CM, Douglass M, Kisaalita WS. Evaluation of cellular adhesion and organization in different microporous polymeric scaffolds. Biotechnol Prog. 2018;34(2):505-514. https://doi.org/10.1002/btpr.2627.
Raynes JK, Domigan LJ, Pearce FG, Gerrard JA. Immobilization of tobacco etch virus (TEV) protease on a high surface area protein nanofibril scaffold. Biotechnol Prog. 2018;34(6):1506-1512. https://doi.org/10.1002/btpr.2670.
Ahani E, Montazer M, Toliyat T, Mahmoudi Rad M, Harifi T. Preparation of nano cationic liposome as carrier membrane for polyhexamethylene biguanide chloride through various methods utilizing higher antibacterial activities with low cell toxicity. J Microencapsul. 2017;34(2):121-131. https://doi.org/10.1080/02652048.2017.1296500.
Hollister SJ. Porous scaffold design for tissue engineering. Nat Mater. 2005;4(7):518-524. https://doi.org/10.1038/nmat1421.
Wang X, Wang H, Lu M, Teng R, Du X. Facile synthesis of phenyl-modified magnetic graphene/mesoporous silica with hierarchical bridge-pore structure for efficient adsorption of pesticides. Mater Chem Phys. 2017;198:393-400. https://doi.org/10.1016/j.matchemphys.2016.12.017.
Francis NL, Hunger PM, Donius AE, Wegst UGK, Wheatley MA. Strategies for neurotrophin-3 and chondroitinase ABC release from freeze-cast chitosan-alginate nerve-guidance scaffolds. J Tissue Eng Regen Med. 2017;11(1):285-294. https://doi.org/10.1002/term.1912.
Ahani E, Montazer M, Toliyat T, Mahmoudi Rad M. A novel biocompatible antibacterial product: nanoliposomes loaded with poly(hexamethylene biguanide chloride). J Bioact Compat Polym. 2017;32(3):242-262. https://doi.org/10.1177/0883911516675367.
Hsu S, Chang W-C, Yen C-T. Novel flexible nerve conduits made of water-based biodegradable polyurethane for peripheral nerve regeneration. J Biomed Mater Res A. 2017;105(5):1383-1392. https://doi.org/10.1002/jbm.a.36022.
Meng ZX, Zheng W, Li L, Zheng YF. Fabrication, characterization and in vitro drug release behavior of electrospun PLGA/chitosan nanofibrous scaffold. Mater Chem Phys. 2011;125(3):606-611. https://doi.org/10.1016/j.matchemphys.2010.10.010.
Stokols S, Tuszynski MH. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials. 2006;27(3):443-451. https://doi.org/10.1016/j.biomaterials.2005.06.039.
Zeng X, Ma Y, Chen Y, et al. Autocrine fibronectin from differentiating mesenchymal stem cells induces the neurite elongation in vitro and promotes nerve fiber regeneration in transected spinal cord injury. J Biomed Mater Res A. 2016;104(8):1902-1911. https://doi.org/10.1002/jbm.a.35720.
Kriebel A, Hodde D, Kuenzel T, Engels J, Brook G, Mey J. Cell-free artificial implants of electrospun fibres in a three-dimensional gelatin matrix support sciatic nerve regeneration in vivo. J Tissue Eng Regen Med. 2017;11(12):3289-3304. https://doi.org/10.1002/term.2237.
Farjah GH, Dolatkhah MA, Pourheidar B, Heshmatian B. The effect of cerebro-spinal fluid in collagen guide channel on sciatic nerve regeneration in rat. Turk Neurosurg. 2017;3(27):1-7. https://doi.org/10.5137/1019-5149.JTN.16004-15.2.
Jiang X, Ma J, Wei Q, et al. Effect of frankincense extract on nerve recovery in the rat sciatic nerve damage model. Evid Based Complement Alternat Med. 2016;2016:1-8. https://doi.org/10.1155/2016/3617216.
Agenor A, Dvoracek L, Leu A, et al. Hyaluronic acid/carboxymethyl cellulose directly applied to transected nerve decreases axonal outgrowth. J Biomed Mater Res B Appl Biomater. 2017;105(3):568-574. https://doi.org/10.1002/jbm.b.33576.
Roth AD, Elmer J, Harris DR, et al. Hemoglobin regulates the migration of glioma cells along poly(ε-caprolactone)-aligned nanofibers. Biotechnol Prog. 2014;30(5):1214-1220. https://doi.org/10.1002/btpr.1950.
Gumera CB. New Materials and Scaffold Fabrication Method for Nerve Tissue Engineering [dissertation]. Georgia Institute of Technology; 2009.
Paino CL, Bunge MB. Induction of axon growth into schwann cell implants grafted into lesioned adult rat spinal cord. Exp Neurol. 1991;114(2):254-257. https://doi.org/10.1016/0014-4886(91)90043-C.
Madaghiele M, Sannino A, Yannas IV, Spector M. Collagen-based matrices with axially oriented pores. J Biomed Mater Res A. 2008;85(3):757-767. https://doi.org/10.1002/jbm.a.31517.
Ghorbani F, Zamanian A, Behnamghader A, Daliri Joupari M. A novel pathway for in situ synthesis of modified gelatin microspheres by silane coupling agents as a bioactive platform. J Appl Polym Sci. 2018;135(41):46739. https://doi.org/10.1002/app.46739.
Zhang X, Zeng Y, Zhang W, Wang J, Wu J, Li J. Co-transplantation of neural stem cells and NT-3-overexpressing Schwann cells in transected spinal cord. J Neurotrauma. 2007;24(12):1863-1877. https://doi.org/10.1089/neu.2007.0334.
Lee D-Y, Choi B-H, Park J-H, et al. Nerve regeneration with the use of a poly(l-lactide-co-glycolic acid)-coated collagen tube filled with collagen gel. J Craniomaxillofac Surg. 2006;34(1):50-56. https://doi.org/10.1016/j.jcms.2005.07.011.
Panda S. Formulation and evaluation of zidovudine loaded olibanum resin microcapsules: exploring the use of natural resins as biodegradable polymeric materials for controlled release. Asian J Pharm Clin Res. 2013;6(3):191-196.
Manjula BS, Srinatha A, Sridhar BK. Evaluation of hydrophilic polymers and their combinations in formulation of sustained-release matrix tablets of water-soluble drug. Indian J Pharm Educ Res. 2014;48(3):48-59. https://doi.org/10.5530/ijper.48.3.7.
Ammon HPT. Medical use of incense (Olibanum) in different historical periods HPT Ammon. Phytomedicine. 2008;15:541-546.
Choi O-B, Park J-H, Lee YJ, et al. Olibanum extract inhibits vascular smooth muscle cell migration and proliferation in response to platelet-derived growth factor. Korean J Physiol Pharmacol. 2009;13:107-113.
Zamanian A, Farhangdoust S, Yasaei M, Khorami M, Hafezi M. The effect of particle size on the mechanical and microstructural properties of freeze-casted macroporous hydroxyapatite scaffolds. Int J Appl Ceram Technol. 2014;11(1):12-21. https://doi.org/10.1111/ijac.12031.
Giesche H. Mercury porosimetry: a general (practical) overview. Part Part Syst Charact. 2006;23(1):9-19. https://doi.org/10.1002/ppsc.200601009.
Arabi N, Zamanian A, Rashvand SN, Ghorbani F. The tunable porous structure of gelatin-bioglass nanocomposite scaffolds for bone tissue engineering applications: physicochemical, mechanical, and in-vitro properties. Macromol Mater Eng. 2018;303(3):1700539. https://doi.org/10.1002/mame.201700539.
Aidun A, Zamanian A, Ghorbani F. Novel bioactive porous starch-siloxane matrix for bone regeneration: physicochemical, mechanical, and in vitro properties. Biotechnol Appl Biochem. 2019;66(1):43-52. https://doi.org/10.1002/bab.1694.
Ghorbani F, Zamanian A. Oxygen-plasma treatment-induced surface engineering of biomimetic polyurethane nanofibrous scaffolds for gelatin-heparin immobilization. e-Polymers. 2018;18(3):275-285. https://doi.org/10.1515/epoly-2017-0185.
Pourheydar B, Soleimani Asl S, Azimzadeh M, Rezaei Moghadam A, Marzban A, Mehdizadeh M. Neuroprotective effects of bone marrow mesenchymal stem cells on bilateral common carotid arteries occlusion model of cerebral ischemia in rat. Behav Neurol. 2016;2016:1-10. https://doi.org/10.1155/2016/2964712.
Deville S. Freezing Colloids: Observations, Principles, Control, and Use. Cham, Switzerland: Springer International Publishing; 2017.
Deville S. Freeze-casting of porous biomaterials: structure, properties and opportunities. Materials. 2010;3(3):1913-1927. https://doi.org/10.3390/ma3031913.
Deville S. Freeze casting of porous ceramics: a review of current achievements and issues. Adv Eng Mater. 2008;10(3):155-169. https://doi.org/10.1002/adem.200700270.
Arabi N, Zamanian A. Effect of cooling rate and gelatin concentration on the microstructural and mechanical properties of ice template gelatin scaffolds. Biotechnol Appl Biochem. 2013;60(6):573-579. https://doi.org/10.1002/bab.1120.
O'Brien F. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials. 2004;25(6):1077-1086. https://doi.org/10.1016/S0142-9612(03)00630-6.
Tamaddon M, Burrows M, Ferreira SA, et al. Monomeric, porous type II collagen scaffolds promote chondrogenic differentiation of human bone marrow mesenchymal stem cells in vitro. Sci Rep. 2017;7:43519. https://doi.org/10.1038/srep43519.
Farhangdoust S, Zamanian A, Yasaei M, Khorami M. The effect of processing parameters and solid concentration on the mechanical and microstructural properties of freeze-casted macroporous hydroxyapatite scaffolds. Mater Sci Eng C Mater Biol Appl. 2013;33(1):453-460. https://doi.org/10.1016/j.msec.2012.09.013.
Nakamatsu J, Torres FG, Troncoso OP, Min-Lin Y, Boccaccini AR. Processing and characterization of porous structures from chitosan and starch for tissue engineering scaffolds. Biomacromolecules. 2006;7(12):3345-3355. https://doi.org/10.1021/bm0605311.
Horst DJ, Tebcherani SM, Kubaski ET, De Almeida Vieira R. Bioactive potential of 3D-printed oleo-gum-resin disks: B. papyrifera, C. myrrha, and S. benzoin loading nanooxides - TiO2, P25, Cu2O, and MoO3. Bioinorg Chem Appl. 2017;2017:6398167. https://doi.org/10.1155/2017/6398167.
Mohanty S, Krishna MG. Proximate analysis and standardization of plant exudates: gum olibanum and gum dikamali. Int J Pharm Sci Rev Res. 2014;24(1):172-176.
Lee EJ, Lee JH, Shin YC, et al. Graphene oxide-decorated PLGA/collagen hybrid fiber sheets for application to tissue engineering scaffolds. Biomater Res. 2014;18(1):18-24.
Ghorbani F, Zamanian A, Behnamghader A, Joupari MD. Microwave-induced rapid formation of biomimetic hydroxyapatite coating on gelatin-siloxane hybrid microspheres in 10X-SBF solution. e-Polymers. 2018;18(3):247-255. https://doi.org/10.1515/epoly-2017-0196.
Sharifi E, Azami M, Kajbafzadeh AM, et al. Preparation of a biomimetic composite scaffold from gelatin/collagen and bioactive glass fibers for bone tissue engineering. Mater Sci Eng C. 2016;59:533-541. https://doi.org/10.1016/j.msec.2015.09.037.
Nguyen T-H, Lee B-T. Fabrication and characterization of cross-linked gelatin electro-spun nano-fibers. J Biomed Sci Eng. 2010;3(12):1117-1124. https://doi.org/10.4236/jbise.2010.312145.
O'Brien FJ. Biomaterials & scaffolds for tissue engineering. Mater Today. 2011;14(3):88-95. https://doi.org/10.1016/S1369-7021(11)70058-X.
Gefen A, Margulies SS. Are in vivo and in situ brain tissues mechanically similar? J Biomech. 2004;37(9):1339-1352. https://doi.org/10.1016/j.jbiomech.2003.12.032.
Bakshi A, Fisher O, Dagci T, Himes BT, Fischer I, Lowman A. Mechanically engineered hydrogel scaffolds for axonal growth and angiogenesis after transplantation in spinal cord injury. J Neurosurg Spine. 2004;1(3):322-329. https://doi.org/10.3171/spi.2004.1.3.0322.
Seidlits SK, Khaing ZZ, Petersen RR, et al. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials. 2010;31(14):3930-3940. https://doi.org/10.1016/j.biomaterials.2010.01.125.
Ghazanfari SMH, Zamanian A. Phase transformation, microstructural and mechanical properties of hydroxyapatite/alumina nanocomposite scaffolds produced by freeze casting. Ceram Int. 2013;39(8):9835-9844. https://doi.org/10.1016/j.ceramint.2013.05.096.
Thakur S, Govender PP, Mamo MA, Tamulevicius S, Thakur VK. Recent progress in gelatin hydrogel nanocomposites for water purification and beyond. Vacuum. 2017;1(146):396-408. https://doi.org/10.1016/j.vacuum.2017.05.032.
Rodrigues APH, Pereira IM, de Souza SD, et al. Control of properties of nanocomposites bio-based collagen and cellulose nanocrystals. Cellulose. 2017;24(4):1731-1744. https://doi.org/10.1007/s10570-017-1218-9.
Pasha B, Ramarao N. Evaluation of some natural gums as sustained release carriers in the manufacturing of tablets. Indian J Res Pharm Biotechnol. 2017;5(3):224-228.
Ratanavaraporn J, Damrongsakkul S, Sanchavanakit N, Banaprasert T, Kanokpanont S. Comparison of gelatin and collagen scaffolds for fibroblast cell culture. J Metals Mater Miner. 2006;16(1):31-36.
Aliramaji S, Zamanian A, Mozafari M. Super-paramagnetic responsive silk fibroin/chitosan/magnetite scaffolds with tunable pore structures for bone tissue engineering applications. Mater Sci Eng C. 2017;70:736-744. https://doi.org/10.1016/j.msec.2016.09.039.
Meng ZX, Wang YS, Ma C, Zheng W, Li L, Zheng YF. Electrospinning of PLGA/gelatin randomly-oriented and aligned nanofibers as potential scaffold in tissue engineering. Mater Sci Eng C. 2010;30(8):1204-1210. https://doi.org/10.1016/j.msec.2010.06.018.
Alizadeh M, Abbasi F, Khoshfetrat AB, Ghaleh H. Microstructure and characteristic properties of gelatin/chitosan scaffold prepared by a combined freeze-drying/leaching method. Mater Sci Eng C Mater Biol Appl. 2013;33(7):3958-3967. https://doi.org/10.1016/j.msec.2013.05.039.
Stokols S, Sakamoto J, Breckon C, Holt T, Weiss J, Tuszynski MH. Templated agarose scaffolds support linear axonal regeneration. Tissue Eng. 2006;12(10):2777-2787.
Han X, Pan J. Finite element analysis of degradation of biodegradable medical devices. OA Biotechnol. 2013;2:22-32.
Grover CN, Cameron RE, Best SM. Investigating the morphological, mechanical and degradation properties of scaffolds comprising collagen, gelatin and elastin for use in soft tissue engineering. J Mech Behav Biomed Mater. 2012;10:62-74. https://doi.org/10.1016/j.jmbbm.2012.02.028.
Liu B, Cai S-X, Ma K-W, et al. Fabrication of a PLGA-collagen peripheral nerve scaffold and investigation of its sustained release property in vitro. J Mater Sci Mater Med. 2008;19(3):1127-1132. https://doi.org/10.1007/s10856-007-3224-1.
Zhang F, He C, Cao L, et al. Fabrication of gelatin-hyaluronic acid hybrid scaffolds with tunable porous structures for soft tissue engineering. Int J Biol Macromol. 2011;48(3):474-481. https://doi.org/10.1016/j.ijbiomac.2011.01.012.
Murphy C, Haugh M, O'Brien F. The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials. 2010;31(3):461-466. https://doi.org/10.1016/j.biomaterials.2009.09.063.

Auteurs

Farnaz Ghorbani (F)

Department of Orthopedics, Shanghai Pudong Hospital, Fudan University Pudong Medical Center, Shanghai, China.

Ali Zamanian (A)

Department of Nanotechnology and Advanced Materials, Materials and Energy Research Center, Karaj, Iran.

Fatemeh Kermanian (F)

Department of Anatomy, School of Medicine, Alborz University of Medical Sciences, Karaj, Iran.

Atefeh Shamoosi (A)

Department of Anatomy, School of Medicine, Alborz University of Medical Sciences, Karaj, Iran.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH