Advances in natural biomaterials for nerve tissue repair

Natural biomaterials are well positioned to play a significant role in the development of the next generation of biomaterials for nervous system repair. These materials are derived from naturally occurring substances and are highly diverse and versatile. They are generally biocompatible and are well tolerated in vivo, and therefore have a high potential to be successful as part of clinical repair strategies in the nervous system. Here we review recent reports on acellular tissue grafts, collagen, hyaluronan, fibrin, and agarose in their use to repair the nervous system. In addition, newly developed advanced fabrication techniques to further develop the next generation natural biomaterials-based therapeutic devices are discussed.

[1]  C. Sarkar,et al.  Effect of bone marrow-derived mononuclear cells on nerve regeneration in the transection model of the rat sciatic nerve , 2009, Journal of Clinical Neuroscience.

[2]  Emma East,et al.  Alignment of astrocytes increases neuronal growth in three-dimensional collagen gels and is maintained following plastic compression to form a spinal cord repair conduit. , 2010, Tissue engineering. Part A.

[3]  J. Shumsky,et al.  Aspiration of a cervical spinal contusion injury in preparation for delayed peripheral nerve grafting does not impair forelimb behavior or axon regeneration , 2008, Experimental Neurology.

[4]  Christine E Schmidt,et al.  Engineering an improved acellular nerve graft via optimized chemical processing. , 2004, Tissue engineering.

[5]  M. Filbin,et al.  Glial inhibition of nerve regeneration in the mature mammalian CNS , 2000, Glia.

[6]  John H. Martin,et al.  Spinal cord bypass surgery with intercostal and spinal accessory nerves: an anatomical feasibility study in human cadavers. , 2012, Journal of neurosurgery. Spine.

[7]  Laura J Suggs,et al.  Three-dimensional culture for expansion and differentiation of mouse embryonic stem cells. , 2006, Biomaterials.

[8]  M. Spector,et al.  Development of hyaluronic acid-based scaffolds for brain tissue engineering. , 2009, Acta biomaterialia.

[9]  S. Woerly,et al.  Evaluation of two cross-linked collagen gels implanted in the transected spinal cord , 1993, Brain Research Bulletin.

[10]  Kozo Takayama,et al.  Release phenomena of insulin from an implantable device composed of a polyion complex of chitosan and sodium hyaluronate. , 2003, Journal of controlled release : official journal of the Controlled Release Society.

[11]  M. Shoichet,et al.  An injectable drug delivery platform for sustained combination therapy. , 2009, Journal of controlled release : official journal of the Controlled Release Society.

[12]  N. Chaverot,et al.  Molecular Mechanism of Systemic Delivery of Neural Precursor Cells to the Brain: Assembly of Brain Endothelial Apical Cups and Control of Transmigration by CD44 , 2008, Stem cells.

[13]  Brent A. Reynolds,et al.  Multipotent CNS Stem Cells Are Present in the Adult Mammalian Spinal Cord and Ventricular Neuroaxis , 1996, The Journal of Neuroscience.

[14]  A. K. Gulati,et al.  Immunogenicity and regenerative potential of acellular nerve allografts to repair peripheral nerve in rats and rabbits , 1994, Acta Neurochirurgica.

[15]  M. Tuszynski,et al.  Axon regeneration through scars and into sites of chronic spinal cord injury , 2007, Experimental Neurology.

[16]  A. Aguayo,et al.  Axonal regeneration after crush injury of rat central nervous system fibres innervating peripheral nerve grafts , 1985, Journal of neurocytology.

[17]  Gordana Vunjak-Novakovic,et al.  Percutaneous Cell Delivery into the Heart Using Hydrogels Polymerizing in Situ , 2009, Cell transplantation.

[18]  Y. Koyama,et al.  Enhancement of peripheral nerve regeneration using bioabsorbable polymer tubes packed with fibrin gel. , 2007, Artificial organs.

[19]  Christine E Schmidt,et al.  Effects of collagen 1, fibronectin, laminin and hyaluronic acid concentration in multi-component gels on neurite extension , 2007, Journal of biomaterials science. Polymer edition.

[20]  R. U. Margolis,et al.  Distribution and metabolism of glycoproteins and glycosaminoglycans in subcellular fractions of brain. , 1975, Biochemistry.

[21]  B. Sellhaus,et al.  In vitro assessment of axonal growth using dorsal root ganglia explants in a novel three-dimensional collagen matrix. , 2007, Tissue engineering.

[22]  V. Perry,et al.  The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration , 1987, The Journal of experimental medicine.

[23]  J. Fawcett,et al.  Spinal cord repair: from experimental models to human application , 1998, Spinal Cord.

[24]  David L. Wilson,et al.  Effects of a conditioning lesion on bullfrog sciatic nerve regeneration: Analysis of fast axonally transported proteins , 1987, Brain Research.

[25]  T. Bowden,et al.  Enhanced neuronal differentiation in a three‐dimensional collagen‐hyaluronan matrix , 2007, Journal of neuroscience research.

[26]  M. Griffith,et al.  Fibrin glues in combination with mesenchymal stem cells to develop a tissue-engineered cartilage substitute. , 2011, Tissue engineering. Part A.

[27]  Susan E Mackinnon,et al.  Use of Cold-Preserved Allografts Seeded with Autologous Schwann Cells in the Treatment of a Long-Gap Peripheral Nerve Injury , 2007, Plastic and reconstructive surgery.

[28]  M. Longaker,et al.  Studies in fetal wound healing. IV. Hyaluronic acid-stimulating activity distinguishes fetal wound fluid from adult wound fluid. , 1989, Annals of surgery.

[29]  K. Na,et al.  Bone morphogenic protein-2 (BMP-2) loaded nanoparticles mixed with human mesenchymal stem cell in fibrin hydrogel for bone tissue engineering. , 2009, Journal of bioscience and bioengineering.

[30]  Jianzhong Xu,et al.  In vitro evaluation of a fibrin gel antibiotic delivery system containing mesenchymal stem cells and vancomycin alginate beads for treating bone infections and facilitating bone formation. , 2008, Tissue engineering. Part A.

[31]  B. Mcewen,et al.  Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Cindi M Morshead,et al.  Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels. , 2011, Nature materials.

[33]  E Gould,et al.  Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat , 1997, Neuroscience.

[34]  Jason B. Shear,et al.  High‐Resolution Patterning of Hydrogels in Three Dimensions using Direct‐Write Photofabrication for Cell Guidance , 2009 .

[35]  Elizabeth Gould,et al.  Is there a link between adult neurogenesis and learning? , 2006, Hippocampus.

[36]  M. Tuszynski,et al.  The fabrication and characterization of linearly oriented nerve guidance scaffolds for spinal cord injury. , 2004, Biomaterials.

[37]  M. Bates,et al.  Regrowth of axons in lesioned adult rat spinal cord: promotion by implants of cultured Schwann cells , 1994, Journal of neurocytology.

[38]  S. Sakiyama-Elbert,et al.  Tissue-engineered fibrin scaffolds containing neural progenitors enhance functional recovery in a subacute model of SCI. , 2010, Soft matter.

[39]  S. Weiss,et al.  Erythropoietin Regulates the In Vitro and In Vivo Production of Neuronal Progenitors by Mammalian Forebrain Neural Stem Cells , 2001, The Journal of Neuroscience.

[40]  S. Lord Fibrinogen and fibrin: scaffold proteins in hemostasis , 2007, Current opinion in hematology.

[41]  H. Buettner,et al.  Neurite Outgrowth is Directed by Schwann Cell Alignment in the Absence of Other Guidance Cues , 2005, Annals of Biomedical Engineering.

[42]  G. Tobin,et al.  Collagen biosynthesis in healing spinal cord wounds. , 1979, Surgical forum.

[43]  M. Spector,et al.  Collagen-GAG Substrate Enhances the Quality of Nerve Regeneration through Collagen Tubes up to Level of Autograft , 1998, Experimental Neurology.

[44]  C. Cetrulo,et al.  Hyaluronic acid enhances peripheral nerve regeneration in vivo , 1998, Microsurgery.

[45]  J. Steeves,et al.  Modulating astrogliosis after neurotrauma , 2001, Journal of neuroscience research.

[46]  F. Cui,et al.  Combination of Hyaluronic Acid Hydrogel Scaffold and PLGA Microspheres for Supporting Survival of Neural Stem Cells , 2011, Pharmaceutical Research.

[47]  H D Li,et al.  Hyaluronic acid-poly-D-lysine-based three-dimensional hydrogel for traumatic brain injury. , 2005, Tissue engineering.

[48]  R. Tranquillo,et al.  Guided Neurite Elongation and Schwann Cell Invasion into Magnetically Aligned Collagen in Simulated Peripheral Nerve Regeneration , 1999, Experimental Neurology.

[49]  B. Seckel,et al.  Hyaluronic acid through a new injectable nerve guide delivery system enhances peripheral nerve regeneration in the rat , 1995, Journal of neuroscience research.

[50]  D. Neubauer,et al.  Axonal Regeneration into Acellular Nerve Grafts Is Enhanced by Degradation of Chondroitin Sulfate Proteoglycan , 2001, The Journal of Neuroscience.

[51]  Pico Caroni,et al.  Mechanisms of axon degeneration: From development to disease , 2007, Progress in Neurobiology.

[52]  Song Li,et al.  Bone marrow-derived mesenchymal stem cells in fibrin augment angiogenesis in the chronically infarcted myocardium. , 2009, Regenerative medicine.

[53]  S. Willerth,et al.  The effect of controlled growth factor delivery on embryonic stem cell differentiation inside fibrin scaffolds. , 2008, Stem cell research.

[54]  M. Spector,et al.  An experimental test of stroke recovery by implanting a hyaluronic acid hydrogel carrying a Nogo receptor antibody in a rat model , 2007, Biomedical materials.

[55]  R. U. Margolis,et al.  Expression of hyaluronan and the hyaluronan-binding proteoglycans neurocan, aggrecan, and versican by neural stem cells and neural cells derived from embryonic stem cells , 2010, Brain Research.

[56]  A. Kaye,et al.  Extracellular matrix and the brain: components and function , 2000, Journal of Clinical Neuroscience.

[57]  C. Werner,et al.  Directed growth of adult human white matter stem cell-derived neurons on aligned fibrillar collagen. , 2010, Tissue engineering. Part A.

[58]  Alyssa Panitch,et al.  Influence of cross-linked hyaluronic acid hydrogels on neurite outgrowth and recovery from spinal cord injury. , 2007, Journal of neurosurgery. Spine.

[59]  X. Yu,et al.  A laminin and nerve growth factor-laden three-dimensional scaffold for enhanced neurite extension. , 1999, Tissue engineering.

[60]  Charles H Tator,et al.  Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. , 2006, Biomaterials.

[61]  Paul L. Evans,et al.  Cold preserved nerve allografts: Changes in basement membrane, viability, immunogenicity, and regeneration , 1998, Muscle & nerve.

[62]  Zin Z. Khaing,et al.  Functional characterization of optimized acellular peripheral nerve graft in a rat sciatic nerve injury model , 2011, Neurological research.

[63]  Ravi V Bellamkonda,et al.  Differences between the effect of anisotropic and isotropic laminin and nerve growth factor presenting scaffolds on nerve regeneration across long peripheral nerve gaps. , 2008, Biomaterials.

[64]  T. Dick,et al.  Functional regeneration of respiratory pathways after spinal cord injury , 2011, Nature.

[65]  S. Sakiyama-Elbert,et al.  Controlled Release of Neurotrophin-3 and Platelet-Derived Growth Factor from Fibrin Scaffolds Containing Neural Progenitor Cells Enhances Survival and Differentiation into Neurons in a Subacute Model of SCI , 2010, Cell transplantation.

[66]  Hideyuki Okano,et al.  Establishment of three-dimensional culture of neural stem/progenitor cells in collagen Type-1 Gel. , 2007, Restorative neurology and neuroscience.

[67]  Jason B Shear,et al.  The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. , 2010, Biomaterials.

[68]  Jerry Silver,et al.  Combining an Autologous Peripheral Nervous System “Bridge” and Matrix Modification by Chondroitinase Allows Robust, Functional Regeneration beyond a Hemisection Lesion of the Adult Rat Spinal Cord , 2006, The Journal of Neuroscience.

[69]  Mary Murphy,et al.  Type II collagen-hyaluronan hydrogel--a step towards a scaffold for intervertebral disc tissue engineering. , 2010, European cells & materials.

[70]  Ravi V Bellamkonda,et al.  Anisotropic scaffolds facilitate enhanced neurite extension in vitro. , 2006, Journal of biomedical materials research. Part A.

[71]  M. Lemay,et al.  Peripheral nerve grafts after cervical spinal cord injury in adult cats , 2010, Experimental Neurology.

[72]  F. Cui,et al.  Viability and differentiation of neural precursors on hyaluronic acid hydrogel scaffold , 2009, Journal of neuroscience research.

[73]  L. Sherman,et al.  Neural stem cell niches: roles for the hyaluronan-based extracellular matrix. , 2011, Frontiers in bioscience.

[74]  K. Tohyama,et al.  Long Acellular Nerve Transplants for Allogeneic Grafting and the Effects of Basic Fibroblast Growth Factor on the Growth of Regenerating Axons in Dogs: A Preliminary Report , 1998, Experimental Neurology.

[75]  Laura J Suggs,et al.  Controlled release of stromal cell-derived factor-1 alpha in situ increases c-kit+ cell homing to the infarcted heart. , 2007, Tissue engineering.

[76]  Xiaolin Liu,et al.  Repair of extended peripheral nerve lesions in rhesus monkeys using acellular allogenic nerve grafts implanted with autologous mesenchymal stem cells , 2007, Experimental Neurology.

[77]  Nicole Brazda,et al.  Pharmacological modification of the extracellular matrix to promote regeneration of the injured brain and spinal cord. , 2009, Progress in brain research.

[78]  G. Brook,et al.  Cell-cell interactions of human neural progenitor-derived astrocytes within a microstructured 3D-scaffold. , 2010, Biomaterials.

[79]  Seung‐Woo Cho,et al.  Basic fibroblast growth factor promotes bone marrow stromal cell transplantation-mediated neural regeneration in traumatic brain injury. , 2007, Biochemical and biophysical research communications.

[80]  V. Falanga,et al.  Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. , 2007, Tissue engineering.

[81]  D. van der Kooy,et al.  In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[82]  Y. Ha,et al.  Chitosan/TPP-Hyaluronic Acid Nanoparticles: A New Vehicle for Gene Delivery to the Spinal Cord , 2012, Journal of biomaterials science. Polymer edition.

[83]  L. Margolis,et al.  Primate embryonic stem cells create their own niche while differentiating in three‐dimensional culture systems , 2006, Cell proliferation.

[84]  M. Akagi,et al.  Bridging a 30-mm nerve defect using collagen filaments. , 2003, Journal of biomedical materials research. Part A.

[85]  M. Longaker,et al.  Hyaluronate metabolism undergoes an ontogenic transition during fetal development: implications for scar-free wound healing. , 1993, Journal of pediatric surgery.

[86]  C. Schmidt,et al.  Optimized acellular nerve graft is immunologically tolerated and supports regeneration. , 2004, Tissue engineering.

[87]  James B Phillips,et al.  Neural tissue engineering: a self-organizing collagen guidance conduit. , 2005, Tissue engineering.

[88]  Tetsuji Yamamoto,et al.  Glial and axonal regeneration following spinal cord injury , 2009, Cell adhesion & migration.

[89]  L. Novikova,et al.  Biodegradable fibrin conduit promotes long-term regeneration after peripheral nerve injury in adult rats. , 2010, Journal of plastic, reconstructive & aesthetic surgery : JPRAS.

[90]  Diane Hoffman-Kim,et al.  Topography, cell response, and nerve regeneration. , 2010, Annual review of biomedical engineering.

[91]  Zin Z. Khaing,et al.  High molecular weight hyaluronic acid limits astrocyte activation and scar formation after spinal cord injury , 2011, Journal of neural engineering.

[92]  H. Cameron,et al.  Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus , 1994, Neuroscience.

[93]  R. Uibo,et al.  Soft materials to treat central nervous system injuries: evaluation of the suitability of non-mammalian fibrin gels. , 2009, Biochimica et biophysica acta.

[94]  Wei Zheng,et al.  The promotion of neural progenitor cells proliferation by aligned and randomly oriented collagen nanofibers through β1 integrin/MAPK signaling pathway. , 2011, Biomaterials.

[95]  L Sedel,et al.  A biodegradable fibrin scaffold for mesenchymal stem cell transplantation. , 2003, Biomaterials.

[96]  Charles Tator,et al.  A new paradigm for local and sustained release of therapeutic molecules to the injured spinal cord for neuroprotection and tissue repair. , 2009, Tissue engineering. Part A.

[97]  J. Zimmerberg,et al.  Multilineage Differentiation of Rhesus Monkey Embryonic Stem Cells in Three‐Dimensional Culture Systems , 2003, Stem cells.

[98]  J. Fawcett,et al.  Controlled release of chondroitinase ABC from fibrin gel reduces the level of inhibitory glycosaminoglycan chains in lesioned spinal cord. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[99]  Ashutosh Kumar Singh,et al.  Solid freeform fabrication of designer scaffolds of hyaluronic acid for nerve tissue engineering , 2011, Biomedical microdevices.

[100]  M. Wiberg,et al.  New Fibrin Conduit for Peripheral Nerve Repair , 2008, Journal of reconstructive microsurgery.

[101]  A. Aguayo,et al.  Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. , 1981, The Journal of experimental biology.

[102]  Jeff Sakamoto,et al.  Templated agarose scaffolds support linear axonal regeneration. , 2006, Tissue engineering.

[103]  Cindi M Morshead,et al.  Controlled epi-cortical delivery of epidermal growth factor for the stimulation of endogenous neural stem cell proliferation in stroke-injured brain. , 2011, Biomaterials.

[104]  J. Mcdonald,et al.  Controlled release of neurotrophin-3 from fibrin gels for spinal cord injury. , 2004, Journal of controlled release : official journal of the Controlled Release Society.

[105]  Anumol Jose,et al.  Effect of matrix composition on differentiation of nestin-positive neural progenitors from circulation into neurons , 2010, Journal of neural engineering.

[106]  Xinqiao Jia,et al.  Perlecan domain I-conjugated, hyaluronic acid-based hydrogel particles for enhanced chondrogenic differentiation via BMP-2 release. , 2009, Biomaterials.

[107]  D. Boyd,et al.  FDA approved guidance conduits and wraps for peripheral nerve injury: a review of materials and efficacy. , 2012, Injury.

[108]  U. Bogdahn,et al.  Increasing capillary diameter and the incorporation of gelatin enhance axon outgrowth in alginate-based anisotropic hydrogels. , 2011, Acta biomaterialia.

[109]  J. Weisel Structure of fibrin: impact on clot stability , 2007, Journal of thrombosis and haemostasis : JTH.

[110]  Gavriil Tsechpenakis,et al.  Synergistic angiogenic effect of codelivering fibroblast growth factor 2 and granulocyte-colony stimulating factor from fibrin scaffolds and bone marrow transplantation in critical limb ischemia. , 2011, Tissue engineering. Part A.

[111]  S. Willerth,et al.  Combining Stem Cells and Biomaterial Scaffolds for Constructing Tissues and Cell Delivery , 2008, StemJournal.

[112]  M. Akagi,et al.  Restoration of function after spinal cord transection using a collagen bridge. , 2004, Journal of biomedical materials research. Part A.

[113]  Christina K. Magill,et al.  Processed allografts and type I collagen conduits for repair of peripheral nerve gaps , 2009, Muscle & nerve.

[114]  G. Lundborg,et al.  Regeneration of the rat sciatic nerve into allografts made acellular through chemical extraction , 1998, Brain Research.

[115]  Elizabeth Gould,et al.  How widespread is adult neurogenesis in mammals? , 2007, Nature Reviews Neuroscience.

[116]  M. Tuszynski,et al.  Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. , 2006, Biomaterials.

[117]  A. R. Little,et al.  Astrogliosis in the adult and developing CNS: is there a role for proinflammatory cytokines? , 2001, Neurotoxicology.

[118]  D. Osterhout,et al.  The inhibitory effects of chondroitin sulfate proteoglycans on oligodendrocytes , 2011, Journal of neurochemistry.

[119]  M. Tuszynski,et al.  Regeneration of long-tract axons through sites of spinal cord injury using templated agarose scaffolds. , 2010, Biomaterials.

[120]  D. Lorinson,et al.  The long-term neurocompatibility of human fibrin sealant and equine collagen as biomatrices in experimental spinal cord injury. , 2007, Experimental and toxicologic pathology : official journal of the Gesellschaft fur Toxikologische Pathologie.

[121]  S. Sakiyama-Elbert,et al.  Fibrin-based tissue engineering scaffolds enhance neural fiber sprouting and delay the accumulation of reactive astrocytes at the lesion in a subacute model of spinal cord injury. , 2010, Journal of biomedical materials research. Part A.

[122]  F. Cui,et al.  Implantation of neural stem cells embedded in hyaluronic acid and collagen composite conduit promotes regeneration in a rabbit facial nerve injury model , 2008, Journal of Translational Medicine.

[123]  R. Bellamkonda,et al.  Biomaterials for the central nervous system , 2008, Journal of The Royal Society Interface.

[124]  V. Edgerton,et al.  Improvement of gait patterns in step-trained, complete spinal cord-transected rats treated with a peripheral nerve graft and acidic fibroblast growth factor , 2010, Experimental Neurology.

[125]  David L Kaplan,et al.  Biomaterials for the development of peripheral nerve guidance conduits. , 2012, Tissue engineering. Part B, Reviews.

[126]  M. Fehlings,et al.  Disruption of the hyaluronan‐based extracellular matrix in spinal cord promotes astrocyte proliferation , 2005, Glia.

[127]  M. Wiberg,et al.  Muscle recovery after repair of short and long peripheral nerve gaps using fibrin conduits , 2011, Neuroscience Letters.

[128]  M. Meek,et al.  US Food and Drug Administration/Conformit Europe-Approved Absorbable Nerve Conduits for Clinical Repair of Peripheral and Cranial Nerves , 2008, Annals of plastic surgery.

[129]  P. Haninec,et al.  Laminin molecules in freeze‐treated nerve segments are associated with migrating Schwann cells that display the corresponding α6β1 integrin receptor , 2001, Glia.

[130]  Christine E Schmidt,et al.  Neural tissue engineering: strategies for repair and regeneration. , 2003, Annual review of biomedical engineering.

[131]  Alan R. Johnson Contact inhibition in the failure of mammalian CNS axonal regeneration , 1993, BioEssays : news and reviews in molecular, cellular and developmental biology.

[132]  P Aebischer,et al.  Hydrogel-based three-dimensional matrix for neural cells. , 1995, Journal of biomedical materials research.