Improvements in biomaterial matrices for neural precursor cell transplantation

  • Nolan Skop
  • Frances Calderon
  • Cheul Cho
  • Chirag Gandhi
  • Steven Levison
Keywords: Tissue engineering, Neural stem cells, Scaffold, Biomaterials, CNS, Brain injury, TBI, Stroke, Transplantation, Review

Abstract

Progress is being made in developing neuroprotective strategies for traumatic brain injuries; however, there will never be a therapy that will fully preserve neurons that are injured from moderate to severe head injuries. Therefore, to restore neurological function, regenerative strategies will be required. Given the limited regenerative capacity of the resident neural precursors of the CNS, many investigators have evaluated the regenerative potential of transplanted precursors. Unfortunately, these precursors do not thrive when engrafted without a biomaterial scaffold. In this article we review the types of natural and synthetic materials that are being used in brain tissue engineering applications for traumatic brain injury and stroke. We also analyze modifications of the scaffolds including immobilizing drugs, growth factors and extracellular matrix molecules to improve CNS regeneration and functional recovery. We conclude with a discussion of some of the challenges that remain to be solved towards repairing and regenerating the brain.

Downloads

Download data is not yet available.

References

Langer R, Vacanti JP: Tissue engineering. Science. 1993, 260 (5110): 920-926.

PubMedGoogle Scholar

Kim IY, Seo SJ, Moon HS, Yoo MK, Park IY, Kim BC, Cho CS: Chitosan and its derivatives for tissue engineering applications. Biotechnol Adv. 2008, 26 (1): 1-21.

PubMedGoogle Scholar

Centers for Disease Control and Prevention (CDC), N.C.f.I.P.a.C: Report to Congress on mild traumatic brain injury in the United States: steps to prevent a serious public health problem. 2003, Centers for Disease Control and Prevention

Google Scholar

Faul M, Likang X, Wald MM, Coronado VG: Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. 2010, Centers for Disease Control and Prevention, National Center for Injury Prevention and Control

Google Scholar

Smith DH, Chen XH, Pierce JE, Wolf JA, Trojanowski JQ, Graham DI, McIntosh TK: Progressive atrophy and neuron death for one year following brain trauma in the rat. J Neurotrauma. 1997, 14 (10): 715-727.

PubMedGoogle Scholar

Cortez SC, McIntosh TK, Noble LJ: Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res. 1989, 482 (2): 271-282.

PubMedGoogle Scholar

Hicks R, Soares H, Smith D, McIntosh T: Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol (Berl). 1996, 91 (3): 236-246.

Google Scholar

Colicos MA, Dixon CE, Dash PK: Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res. 1996, 739 (1–2): 111-119.

PubMedGoogle Scholar

Dietrich WD, Alonso O, Halley M: Early microvascular and neuronal consequences of traumatic brain injury: a light and electron microscopic study in rats. J Neurotrauma. 1994, 11 (3): 289-301.

PubMedGoogle Scholar

Silver J, Miller JH: Regeneration beyond the glial scar. Nat Rev Neurosci. 2004, 5 (2): 146-156.

PubMedGoogle Scholar

Morganti-Kossmann MC, Satgunaseelan L, Bye N, Kossmann T: Modulation of immune response by head injury. Injury. 2007, 38 (12): 1392-1400.

PubMedGoogle Scholar

Molcanyi M, Riess P, Bentz K, Maegele M, Hescheler J, Schafke B, Trapp T, Neugebauer E, Klug N, Schafer U: Trauma-associated inflammatory response impairs embryonic stem cell survival and integration after implantation into injured rat brain. J Neurotrauma. 2007, 24 (4): 625-637.

PubMedGoogle Scholar

(CDC), C.f.D.C.a.P: Injury Prevention & Control: Traumatic Brain Injury. 2014, Available from: http://www.cdc.gov/ncipc/factsheets/tbi.htm

Google Scholar

Crompton KE, Goud JD, Bellamkonda RV, Gengenbach TR, Finkelstein DI, Horne MK, Forsythe JS: Polylysine-functionalised thermoresponsive chitosan hydrogel for neural tissue engineering. Biomaterials. 2007, 28 (3): 441-449.

PubMedGoogle Scholar

Clinic M: Traumatic Brain Injury, Treatments and Drugs. 2014,http://www.mayoclinic.org/diseases-conditions/traumatic-brain-injury/basics/treatment/con-20029302,

Google Scholar

America, B.I.A.o: Living With Brain Injury: Treatment. 2014,http://www.biausa.org/brain-injury-treatment.htm,

Google Scholar

Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G: Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell. 2011, 8 (5): 566-579.

PubMedCentralPubMedGoogle Scholar

Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z: Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci. 2009, 29 (14): 4408-4419.

PubMedGoogle Scholar

Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A: Corridors of migrating neurons in the human brain and their decline during infancy. Nature. 2011, 478 (7369): 382-386.

PubMedCentralPubMedGoogle Scholar

Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O: Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med. 2002, 8 (9): 963-970.

PubMedGoogle Scholar

Yang Z, Levison SW: Perinatal Hypoxic/Ischemic Brain Injury Induces Persistent Production of Striatal Neurons from Subventricular Zone Progenitors. Dev Neurosci. 2007, 29 (4–5): 331-340.

PubMedGoogle Scholar

Yang Z, You Y, Levison SW: Neonatal hypoxic/ischemic brain injury induces production of calretinin-expressing interneurons in the striatum. J Comp Neurol. 2008, 511 (1): 19-33.

PubMedCentralPubMedGoogle Scholar

Salman H, Ghosh P, Kernie SG: Subventricular zone neural stem cells remodel the brain following traumatic injury in adult mice. J Neurotrauma. 2004, 21 (3): 283-292.

PubMedGoogle Scholar

Sundholm-Peters NL, Yang HK, Goings GE, Walker AS, Szele FG: Subventricular zone neuroblasts emigrate toward cortical lesions. J Neuropathol Exp Neurol. 2005, 64 (12): 1089-1100.

PubMedGoogle Scholar

Svendsen CN, Smith AG: New prospects for human stem-cell therapy in the nervous system. Trends Neurosci. 1999, 22 (8): 357-364.

PubMedGoogle Scholar

Snyder EY, Park KI, Flax JD, Liu S, Rosario CM, Yandava BD, Aurora S: Potential of neural "stem-like" cells for gene therapy and repair of the degenerating central nervous system. Adv Neurol. 1997, 72: 121-132.

PubMedGoogle Scholar

McKay RD: Stem cell biology and neurodegenerative disease. Philos Trans R Soc Lond B Biol Sci. 2004, 359 (1445): 851-856.

PubMedCentralPubMedGoogle Scholar

Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J: Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A. 1995, 92 (25): 11879-11883.

PubMedCentralPubMedGoogle Scholar

Martinez-Serrano A, Bjorklund A: Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified neural stem cells. J Neurosci. 1996, 16 (15): 4604-4616.

PubMedGoogle Scholar

Martinez-Serrano A, Fischer W, Bjorklund A: Reversal of age-dependent cognitive impairments and cholinergic neuron atrophy by NGF-secreting neural progenitors grafted to the basal forebrain. Neuron. 1995, 15 (2): 473-484.

PubMedGoogle Scholar

Shihabuddin LS, Brunschwig JP, Holets VR, Bunge MB, Whittemore SR: Induction of mature neuronal properties in immortalized neuronal precursor cells following grafting into the neonatal CNS. J Neurocytol. 1996, 25 (2): 101-111.

PubMedGoogle Scholar

Shihabuddin LS, Hertz JA, Holets VR, Whittemore SR: The adult CNS retains the potential to direct region-specific differentiation of a transplanted neuronal precursor cell line. J Neurosci. 1995, 15 (10): 6666-6678.

PubMedGoogle Scholar

Shihabuddin LS, Holets VR, Whittemore SR: Selective hippocampal lesions differentially affect the phenotypic fate of transplanted neuronal precursor cells. Exp Neurol. 1996, 139 (1): 61-72.

PubMedGoogle Scholar

Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartwieg EA, Cepko CL: Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell. 1992, 68 (1): 33-51.

PubMedGoogle Scholar

Snyder EY, Macklis JD: Multipotent neural progenitor or stem-like cells may be uniquely suited for therapy for some neurodegenerative conditions. Clin Neurosci. 1995, 3 (5): 310-316.

PubMedGoogle Scholar

White LA, Eaton MJ, Castro MC, Klose KJ, Globus MY, Shaw G, Whittemore SR: Distinct regulatory pathways control neurofilament expression and neurotransmitter synthesis in immortalized serotonergic neurons. J Neurosci. 1994, 14 (11 Pt 1): 6744-6753.

PubMedGoogle Scholar

Whittemore SR, Neary JT, Kleitman N, Sanon HR, Benigno A, Donahue RP, Norenberg MD: Isolation and characterization of conditionally immortalized astrocyte cell lines derived from adult human spinal cord. Glia. 1994, 10 (3): 211-226.

PubMedGoogle Scholar

Whittemore SR, White LA: Target regulation of neuronal differentiation in a temperature-sensitive cell line derived from medullary raphe. Brain Res. 1993, 615 (1): 27-40.

PubMedGoogle Scholar

Tate CC, Shear DA, Tate MC, Archer DR, Stein DG, LaPlaca MC: Laminin and fibronectin scaffolds enhance neural stem cell transplantation into the injured brain. J Tissue Eng Regen Med. 2009, 3 (3): 208-217.

PubMedGoogle Scholar

Tate MC, Shear DA, Hoffman SW, Stein DG, Archer DR, LaPlaca MC: Fibronectin promotes survival and migration of primary neural stem cells transplanted into the traumatically injured mouse brain. Cell Transplant. 2002, 11 (3): 283-295.

PubMedGoogle Scholar

Sinden JD, Rashid-Doubell F, Kershaw TR, Nelson A, Chadwick A, Jat PS, Noble MD, Hodges H, Gray JA: Recovery of spatial learning by grafts of a conditionally immortalized hippocampal neuroepithelial cell line into the ischaemia-lesioned hippocampus. Neuroscience. 1997, 81 (3): 599-608.

PubMedGoogle Scholar

Yu H, Cao B, Feng M, Zhou Q, Sun X, Wu S, Jin S, Liu H, Lianhong J: Combinated transplantation of neural stem cells and collagen type I promote functional recovery after cerebral ischemia in rats. Anat Rec (Hoboken). 2010, 293 (5): 911-917.

Google Scholar

Yasuhara T, Matsukawa N, Yu G, Xu L, Mays RW, Kovach J, Deans RJ, Hess DC, Carroll JE, Borlongan CV: Behavioral and histological characterization of intrahippocampal grafts of human bone marrow-derived multipotent progenitor cells in neonatal rats with hypoxic-ischemic injury. Cell Transplant. 2006, 15 (3): 231-238.

PubMedGoogle Scholar

Xiao J, Nan Z, Motooka Y, Low WC: Transplantation of a novel cell line population of umbilical cord blood stem cells ameliorates neurological deficits associated with ischemic brain injury. Stem Cells Dev. 2005, 14 (6): 722-733.

PubMedGoogle Scholar

Wieloch T, Nikolich K: Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol. 2006, 16 (3): 258-264.

PubMedGoogle Scholar

Park KI, Hack MA, Ourednik J, Yandava B, Flax JD, Stieg PE, Gullans S, Jensen FE, Sidman RL, Ourednik V, Snyder EY: Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp Neurol. 2006, 199 (1): 156-178.

PubMedGoogle Scholar

Ourednik V, Ourednik J, Flax JD, Zawada WM, Hutt C, Yang C, Park KI, Kim SU, Sidman RL, Freed CR, Snyder EY: Segregation of human neural stem cells in the developing primate forebrain. Science. 2001, 293 (5536): 1820-1824.

PubMedGoogle Scholar

Ikeda R, Kurokawa MS, Chiba S, Yoshikawa H, Ide M, Tadokoro M, Nito S, Nakatsuji N, Kondoh Y, Nagata K, Hashimoto T, Suzuki N: Transplantation of neural cells derived from retinoic acid-treated cynomolgus monkey embryonic stem cells successfully improved motor function of hemiplegic mice with experimental brain injury. Neurobiol Dis. 2005, 20 (1): 38-48.

PubMedGoogle Scholar

Bachoud-Levi AC, Gaura V, Brugieres P, Lefaucheur JP, Boisse MF, Maison P, Baudic S, Ribeiro MJ, Bourdet C, Remy P, Cesaro P, Hantraye P, Peschanski M: Effect of fetal neural transplants in patients with Huntington's disease 6 years after surgery: a long-term follow-up study. Lancet Neurol. 2006, 5 (4): 303-309.

PubMedGoogle Scholar

Bliss TM, Kelly S, Shah AK, Foo WC, Kohli P, Stokes C, Sun GH, Ma M, Masel J, Kleppner SR, Schallert T, Palmer T, Steinberg GK: Transplantation of hNT neurons into the ischemic cortex: cell survival and effect on sensorimotor behavior. J Neurosci Res. 2006, 83 (6): 1004-1014.

PubMedGoogle Scholar

Bakshi A, Shimizu S, Keck CA, Cho S, LeBold DG, Morales D, Arenas E, Snyder EY, Watson DJ, McIntosh TK: Neural progenitor cells engineered to secrete GDNF show enhanced survival, neuronal differentiation and improve cognitive function following traumatic brain injury. Eur J Neurosci. 2006, 23 (8): 2119-2134.

PubMedGoogle Scholar

Boockvar JA, Schouten J, Royo N, Millard M, Spangler Z, Castelbuono D, Snyder E, O'Rourke D, McIntosh T: Experimental traumatic brain injury modulates the survival, migration, and terminal phenotype of transplanted epidermal growth factor receptor-activated neural stem cells. Neurosurgery. 2005, 56 (1): 163-171. discussion 171

PubMedGoogle Scholar

Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, Snyder EY: Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol. 1998, 16 (11): 1033-1039.

PubMedGoogle Scholar

Seyfried D, Ding J, Han Y, Li Y, Chen J, Chopp M: Effects of intravenous administration of human bone marrow stromal cells after intracerebral hemorrhage in rats. J Neurosurg. 2006, 104 (2): 313-318.

PubMedGoogle Scholar

Mahmood A, Lu D, Yi L, Chen JL, Chopp M: Intracranial bone marrow transplantation after traumatic brain injury improving functional outcome in adult rats. J Neurosurg. 2001, 94 (4): 589-595.

PubMedGoogle Scholar

Mahmood A, Lu D, Qu C, Goussev A, Chopp M: Long-term recovery after bone marrow stromal cell treatment of traumatic brain injury in rats. J Neurosurg. 2006, 104 (2): 272-277.

PubMedGoogle Scholar

Mahmood A, Lu D, Qu C, Goussev A, Chopp M: Human marrow stromal cell treatment provides long-lasting benefit after traumatic brain injury in rats. Neurosurgery. 2005, 57 (5): 1026-1031. discussion 1026–31

PubMedCentralPubMedGoogle Scholar

Mahmood A, Lu D, Chopp M: Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma. 2004, 21 (1): 33-39.

PubMedGoogle Scholar

Lu J, Moochhala S, Moore XL, Ng KC, Tan MH, Lee LK, He B, Wong MC, Ling EA: Adult bone marrow cells differentiate into neural phenotypes and improve functional recovery in rats following traumatic brain injury. Neurosci Lett. 2006, 398 (1–2): 12-17.

PubMedGoogle Scholar

Lu D, Li Y, Mahmood A, Wang L, Rafiq T, Chopp M: Neural and marrow-derived stromal cell sphere transplantation in a rat model of traumatic brain injury. J Neurosurg. 2002, 97 (4): 935-940.

PubMedGoogle Scholar

Li Y, McIntosh K, Chen J, Zhang C, Gao Q, Borneman J, Raginski K, Mitchell J, Shen L, Zhang J, Lu D, Chopp M: Allogeneic bone marrow stromal cells promote glial-axonal remodeling without immunologic sensitization after stroke in rats. Exp Neurol. 2006, 198 (2): 313-325.

PubMedGoogle Scholar

Dezawa M, Hoshino M, Ide C: Treatment of neurodegenerative diseases using adult bone marrow stromal cell-derived neurons. Expert Opin Biol Ther. 2005, 5 (4): 427-435.

PubMedGoogle Scholar

Chen Q, Long Y, Yuan X, Zou L, Sun J, Chen S, Perez-Polo JR, Yang K: Protective effects of bone marrow stromal cell transplantation in injured rodent brain: synthesis of neurotrophic factors. J Neurosci Res. 2005, 80 (5): 611-619.

PubMedGoogle Scholar

Hodges H, Veizovic T, Bray N, French SJ, Rashid TP, Chadwick A, Patel S, Gray JA: Conditionally immortal neuroepithelial stem cell grafts reverse age-associated memory impairments in rats. Neuroscience. 2000, 101 (4): 945-955.

PubMedGoogle Scholar

Hodges H, Sowinski P, Virley D, Nelson A, Kershaw TR, Watson WP, Veizovic T, Patel S, Mora A, Rashid T, French SJ, Chadwick A, Gray JA, Sinden JD: Functional reconstruction of the hippocampus: fetal versus conditionally immortal neuroepithelial stem cell grafts. Novartis Found Symp. 2000, 231: 53-65. discussion 65–9

PubMedGoogle Scholar

Hodges H, Sowinski P, Fleming P, Kershaw TR, Sinden JD, Meldrum BS, Gray JA: Contrasting effects of fetal CA1 and CA3 hippocampal grafts on deficits in spatial learning and working memory induced by global cerebral ischaemia in rats. Neuroscience. 1996, 72 (4): 959-988.

PubMedGoogle Scholar

Vink R, McIntosh TK: Pharmacological and physiological effects of magnesium on experimental traumatic brain injury. Magnes Res. 1990, 3 (3): 163-169.

PubMedGoogle Scholar

McIntosh TK, Vink R, Soares H, Hayes R, Simon R: Effect of noncompetitive blockade of N-methyl-D-aspartate receptors on the neurochemical sequelae of experimental brain injury. J Neurochem. 1990, 55 (4): 1170-1179.

PubMedGoogle Scholar

Keirstead HS, Ben-Hur T, Rogister B, O'Leary MT, Dubois-Dalcq M, Blakemore WF: Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J Neurosci. 1999, 19 (17): 7529-7536.

PubMedGoogle Scholar

Buzsaki G, Smith A, Berger S, Fisher LJ, Gage FH: Petit mal epilepsy and parkinsonian tremor: hypothesis of a common pacemaker. Neuroscience. 1990, 36 (1): 1-14.

PubMedGoogle Scholar

Philips MF, Mattiasson G, Wieloch T, Bjorklund A, Johansson BB, Tomasevic G, Martinez-Serrano A, Lenzlinger PM, Sinson G, Grady MS, McIntosh TK:Neuroprotective and behavioral efficacy of nerve growth factor-transfected hippocampal progenitor cell transplants after experimental traumatic brain injury. J Neurosurg. 2001, 94 (5): 765-774.

PubMedGoogle Scholar

Wong AM, Hodges H, Horsburgh K: Neural stem cell grafts reduce the extent of neuronal damage in a mouse model of global ischaemia. Brain Res. 2005, 1063 (2): 140-150.

PubMedGoogle Scholar

Perri BR, Smith DH, Murai H, Sinson G, Saatman KE, Raghupathi R, Bartus RT, McIntosh TK: Metabolic quantification of lesion volume following experimental traumatic brain injury in the rat. J Neurotrauma. 1997, 14 (1): 15-22.

PubMedGoogle Scholar

Modo M, Rezaie P, Heuschling P, Patel S, Male DK, Hodges H: Transplantation of neural stem cells in a rat model of stroke: assessment of short-term graft survival and acute host immunological response. Brain Res. 2002, 958 (1): 70-82.

PubMedGoogle Scholar

McIntosh TK, Smith DH, Voddi M, Perri BR, Stutzmann JM: Riluzole, a novel neuroprotective agent, attenuates both neurologic motor and cognitive dysfunction following experimental brain injury in the rat. J Neurotrauma. 1996, 13 (12): 767-780.

PubMedGoogle Scholar

Riess P, Zhang C, Saatman KE, Laurer HL, Longhi LG, Raghupathi R, Lenzlinger PM, Lifshitz J, Boockvar J, Neugebauer E, Snyder EY, McIntosh TK: Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery. 2002, 51 (4): 1043-1052. discussion 1052–4

PubMedGoogle Scholar

Riess P, Molcanyi M, Bentz K, Maegele M, Simanski C, Carlitscheck C, Schneider A, Hescheler J, Bouillon B, Schafer U, Neugebauer E: Embryonic stem cell transplantation after experimental traumatic brain injury dramatically improves neurological outcome, but may cause tumors. J Neurotrauma. 2007, 24 (1): 216-225.

PubMedGoogle Scholar

Hoane MR, Becerra GD, Shank JE, Tatko L, Pak ES, Smith M, Murashov AK: Transplantation of neuronal and glial precursors dramatically improves sensorimotor function but not cognitive function in the traumatically injured brain. J Neurotrauma. 2004, 21 (2): 163-174.

PubMedGoogle Scholar

Gao J, Prough DS, McAdoo DJ, Grady JJ, Parsley MO, Ma L, Tarensenko YI, Wu P: Transplantation of primed human fetal neural stem cells improves cognitive function in rats after traumatic brain injury. Exp Neurol. 2006, 201 (2): 281-292.

PubMedGoogle Scholar

Alvarez-Dolado M, Calcagnotto ME, Karkar KM, Southwell DG, Jones-Davis DM, Estrada RC, Rubenstein JL, Alvarez-Buylla A, Baraban SC: Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain. J Neurosci. 2006, 26 (28): 7380-7389.

PubMedCentralPubMedGoogle Scholar

Richardson RM, Singh A, Sun D, Fillmore HL, Dietrich DW, Bullock MR: Stem cell biology in traumatic brain injury: effects of injury and strategies for repair. J Neurosurg. 2010, 112 (5): 1125-1138.

PubMedGoogle Scholar

Sanberg PR, Eve DJ, Cruz LE, Borlongan CV: Neurological disorders and the potential role for stem cells as a therapy. Br Med Bull. 2012, 101: 163-181.

PubMedCentralPubMedGoogle Scholar

Shindo T, Matsumoto Y, Wang Q, Kawai N, Tamiya T, Nagao S: Differences in the neuronal stem cells survival, neuronal differentiation and neurological improvement after transplantation of neural stem cells between mild and severe experimental traumatic brain injury. J Med Invest. 2006, 53 (1–2): 42-51.

PubMedGoogle Scholar

Wallenquist U, Brannvall K, Clausen F, Lewen A, Hillered L, Forsberg-Nilsson K: Grafted neural progenitors migrate and form neurons after experimental traumatic brain injury. Restor Neurol Neurosci. 2009, 27 (4): 323-334.

PubMedGoogle Scholar

Harting MT, Sloan LE, Jimenez F, Baumgartner J, Cox CS: Subacute neural stem cell therapy for traumatic brain injury. J Surg Res. 2009, 153 (2): 188-194.

PubMedCentralPubMedGoogle Scholar

Ma H, Yu B, Kong L, Zhang Y, Shi Y: Transplantation of neural stem cells enhances expression of synaptic protein and promotes functional recovery in a rat model of traumatic brain injury. Mol Med Rep. 2011, 4 (5): 849-856.

PubMedGoogle Scholar

Shear DA, Tate MC, Archer DR, Hoffman SW, Hulce VD, Laplaca MC, Stein DG: Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Res. 2004, 1026 (1): 11-22.

PubMedGoogle Scholar

Sun D, Gugliotta M, Rolfe A, Reid W, McQuiston AR, Hu W, Young H: Sustained survival and maturation of adult neural stem/progenitor cells after transplantation into the injured brain. J Neurotrauma. 2011, 28 (6): 961-972.

PubMedCentralPubMedGoogle Scholar

Skop NB: A Multifunctional Microsphere Scaffold to Deliver Neural Precursors for Traumatic Brain Injury Repair. 2013, U.S.A: p. Ph.D. Thesis. Rutgers The State University of NJ

Google Scholar

Mo L, Yang Z, Zhang A, Li X: The repair of the injured adult rat hippocampus with NT-3-chitosan carriers. Biomaterials. 2010, 31 (8): 2184-2192.

PubMedGoogle Scholar

Meredith JE, Fazeli B, Schwartz MA: The extracellular matrix as a cell survival factor. Mol Biol Cell. 1993, 4 (9): 953-961.

PubMedCentralPubMedGoogle Scholar

Ingber DE: Extracellular matrix as a solid-state regulator in angiogenesis: identification of new targets for anti-cancer therapy. Semin Cancer Biol. 1992, 3 (2): 57-63.

PubMedGoogle Scholar

Aplin AE, Howe AK, Juliano RL: Cell adhesion molecules, signal transduction and cell growth. Curr Opin Cell Biol. 1999, 11 (6): 737-744.

PubMedGoogle Scholar

Aplin AE, Juliano RL: Integrin and cytoskeletal regulation of growth factor signaling to the MAP kinase pathway. J Cell Sci. 1999, 112 (Pt 5): 695-706.

PubMedGoogle Scholar

Stichel CC, Muller HW: The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res. 1998, 294 (1): 1-9.

PubMedGoogle Scholar

Brazel CY, Alaythan AA, Felling RJ, Calderon F, Levison SW: Molecular Features of Neural Stem Cells Enable their Enrichment Using Pharmacological Inhibitors of Survival-Promoting Kinases. J Neurochem. 2013, 128 (3): 376-390.

PubMedCentralPubMedGoogle Scholar

Nisbet DR, Crompton KE, Horne MK, Finkelstein DI, Forsythe JS: Neural tissue engineering of the CNS using hydrogels. J Biomed Mater Res B Appl Biomater. 2008, 87 (1): 251-263.

PubMedGoogle Scholar

Ta HT, Dass CR, Dunstan DE: Injectable chitosan hydrogels for localised cancer therapy. J Control Release. 2008, 126 (3): 205-216.

PubMedGoogle Scholar

Peng HT, Shek PN: Development of in situ-forming hydrogels for hemorrhage control. J Mater Sci Mater Med. 2009, 20 (8): 1753-1762.

PubMedGoogle Scholar

Banerjee A, Arha M, Choudhary S, Ashton RS, Bhatia SR, Schaffer DV, Kane RS: The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials. 2009, 30 (27): 4695-4699.

PubMedCentralPubMedGoogle Scholar

Brannvall K, Bergman K, Wallenquist U, Svahn S, Bowden T, Hilborn J, Forsberg-Nilsson K: Enhanced neuronal differentiation in a three-dimensional collagen-hyaluronan matrix. J Neurosci Res. 2007, 85 (10): 2138-2146.

PubMedGoogle Scholar

Engler AJ, Sen S, Sweeney HL, Discher DE: Matrix elasticity directs stem cell lineage specification. Cell. 2006, 126 (4): 677-689.

PubMedGoogle Scholar

Flanagan LA, Ju YE, Marg B, Osterfield M, Janmey PA: Neurite branching on deformable substrates. Neuroreport. 2002, 13 (18): 2411-2415.

PubMedCentralPubMedGoogle Scholar

Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA: Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J. 2006, 90 (8): 3012-3018.

PubMedCentralPubMedGoogle Scholar

Hynes SR, Rauch MF, Bertram JP, Lavik EB: A library of tunable poly(ethylene glycol)/poly(L-lysine) hydrogels to investigate the material cues that influence neural stem cell differentiation. J Biomed Mater Res A. 2009, 89 (2): 499-509.

PubMedGoogle Scholar

Saha K, Keung AJ, Irwin EF, Li Y, Little L, Schaffer DV, Healy KE: Substrate modulus directs neural stem cell behavior. Biophys J. 2008, 95 (9): 4426-4438.

PubMedCentralPubMedGoogle Scholar

Seidlits SK, Khaing ZZ, Petersen RR, Nickels JD, Vanscoy JE, Shear JB, Schmidt CE: The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials. 2010, 31 (14): 3930-3940.

PubMedGoogle Scholar

Lo CM, Wang HB, Dembo M, Wang YL: Cell movement is guided by the rigidity of the substrate. Biophys J. 2000, 79 (1): 144-152.

PubMedCentralPubMedGoogle Scholar

Wang S, Roy NS, Benraiss A, Goldman SA: Promoter-based isolation and fluorescence-activated sorting of mitotic neuronal progenitor cells from the adult mammalian ependymal/subependymal zone. Dev Neurosci. 2000, 22 (1–2): 167-176.

PubMedGoogle Scholar

Balgude AP, Yu X, Szymanski A, Bellamkonda RV: Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials. 2001, 22 (10): 1077-1084.

PubMedGoogle Scholar

Willits RK, Skornia SL: Effect of collagen gel stiffness on neurite extension. J Biomater Sci Polym Ed. 2004, 15 (12): 1521-1531.

PubMedGoogle Scholar

Lamoreux P, R.E.B.a.S.R.H: Direct evidence that growth cones pull. Nature. 1989, 340 (6229): 159-162.

Google Scholar

Kai D, Prabhakaran MP, Stahl B, Eblenkamp M, Wintermantel E, Ramakrishna S: Mechanical properties and in vitro behavior of nanofiber-hydrogel composites for tissue engineering applications. Nanotechnology. 2012, 23 (9): 095705-

PubMedGoogle Scholar

Barbucci R: Hydrogels: Biological Properties and Applications, Volume XII. 2009, 200-

Google Scholar

Sinha VR, Singla AK, Wadhawan S, Kaushik R, Kumria R, Bansal K, Dhawan S: Chitosan microspheres as a potential carrier for drugs. Int J Pharm. 2004, 274 (1–2): 1-33.

PubMedGoogle Scholar

Leipzig ND, Shoichet MS: The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials. 2009, 30 (36): 6867-6878.

PubMedGoogle Scholar

Nicholas AP, McInnis C, Gupta KB, Snow WW, Love DF, Mason DW, Ferrell TM, Staas JK, Tice TR: The fate of biodegradable microspheres injected into rat brain. Neurosci Lett. 2002, 323 (2): 85-88.

PubMedGoogle Scholar

Emerich DF, Tracy MA, Ward KL, Figueiredo M, Qian R, Henschel C, Bartus RT: Biocompatibility of poly (DL-lactide-co-glycolide) microspheres implanted into the brain. Cell Transplant. 1999, 8 (1): 47-58.

PubMedGoogle Scholar

Kou JH, Emmett C, Shen P, Aswani S, Iwamoto T, Vaghefi F, Sanders L, Cain G: Bioerosion and biocompatibility of poly(d,llactic-co-glycolic acid) implants in brain. J Control Release. 1997, 43: 123-130.

Google Scholar

Wong DY, Hollister SJ, Krebsbach PH, Nosrat C: Poly(epsilon-caprolactone) and poly (L-lactic-co-glycolic acid) degradable polymer sponges attenuate astrocyte response and lesion growth in acute traumatic brain injury. Tissue Eng. 2007, 13 (10): 2515-2523.

PubMedGoogle Scholar

Nisbet DR, Crompton KE, Nisbet DR, Horne MK, Finkelstein DI, Forsythe JS: Review: Neural Tissue Engineering of the CNS Using Hydrogels. J Biomed Mater Res B. 2007, 87 (1): 251-263.

Google Scholar

Zuidema JM, Pap MM, Jaroch DB, Morrison FA, Gilbert RJ: Fabrication and characterization of tunable polysaccharide hydrogel blends for neural repair. Acta Biomater. 2011, 7 (4): 1634-1643.

PubMedGoogle Scholar

Elias PZ, Spector M: Implantation of a collagen scaffold seeded with adult rat hippocampal progenitors in a rat model of penetrating brain injury. J Neurosci Methods. 2012, 209 (1): 199-211.

PubMedGoogle Scholar

Jin K, Mao X, Xie L, Galvan V, Lai B, Wang Y, Gorostiza O, Wang X, Greenberg DA: Transplantation of human neural precursor cells in Matrigel scaffolding improves outcome from focal cerebral ischemia after delayed postischemic treatment in rats. J Cereb Blood Flow Metab. 2010, 30 (3): 534-544.

PubMedCentralPubMedGoogle Scholar

Liang Y, Walczak P, Bulte JW: The survival of engrafted neural stem cells within hyaluronic acid hydrogels. Biomaterials. 2013, 34 (22): 5521-5529.

PubMedCentralPubMedGoogle Scholar

Wang JY, Liou AK, Ren ZH, Zhang L, Brown BN, Cui XT, Badylak SF, Cai YN, Guan YQ, Leak RK, Chen J, Ji X, Chen L: Neurorestorative effect of urinary bladder matrix-mediated neural stem cell transplantation following traumatic brain injury in rats. CNS Neurol Disord Drug Targets. 2013, 12 (3): 413-425.

PubMedCentralPubMedGoogle Scholar

Park KI, Teng YD, Snyder EY: The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat Biotechnol. 2002, 20 (11): 1111-1117.

PubMedGoogle Scholar

Bible E, Chau DY, Alexander MR, Price J, Shakesheff KM, Modo M: The support of neural stem cells transplanted into stroke-induced brain cavities by PLGA particles. Biomaterials. 2009, 30 (16): 2985-2994.

PubMedGoogle Scholar

Cheng TY, Chen MH, Chang WH, Huang MY, Wang TW: Neural stem cells encapsulated in a functionalized self-assembling peptide hydrogel for brain tissue engineering. Biomaterials. 2013, 34 (8): 2005-2016.

PubMedGoogle Scholar

Aliabadi HM, Lavasanifar A: Polymeric micelles for drug delivery. Expert Opin Drug Deliv. 2006, 3 (1): 139-162.

PubMedGoogle Scholar

de Boer R, Knight AM, Spinner RJ, Malessy MJ, Yaszemski MJ, Windebank AJ: In vitro and in vivo release of nerve growth factor from biodegradable poly-lactic-co-glycolic-acid microspheres. J Biomed Mater Res A. 2010, 95 (4): 1067-1073.

PubMedCentralPubMedGoogle Scholar

Kerkhoff H, Jennekens FG: Peripheral nerve lesions: the neuropharmacological outlook. Clin Neurol Neurosurg. 1993, 95 (Suppl): S103-S108.

PubMedGoogle Scholar

Maxwell DJ, Hicks BC, Parsons S, Sakiyama-Elbert SE: Development of rationally designed affinity-based drug delivery systems. Acta Biomater. 2005, 1 (1): 101-113.

PubMedGoogle Scholar

Pean JM, Venier-Julienne MC, Boury F, Menei P, Denizot B, Benoit JP: NGF release from poly(D,L-lactide-co-glycolide) microspheres. Effect of some formulation parameters on encapsulated NGF stability. J Control Release. 1998, 56 (1–3): 175-187.

PubMedGoogle Scholar

Taylor SJ, McDonald JW, Sakiyama-Elbert SE: Controlled release of neurotrophin-3 from fibrin gels for spinal cord injury. J Control Release. 2004, 98 (2): 281-294.

PubMedGoogle Scholar

Yoshimura N, Bennett NE, Hayashi Y, Ogawa T, Nishizawa O, Chancellor MB, de Groat WC, Seki S: Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats. J Neurosci. 2006, 26 (42): 10847-10855.

PubMedGoogle Scholar

Andrieu-Soler C, Aubert-Pouessel A, Doat M, Picaud S, Halhal M, Simonutti M, Venier-Julienne MC, Benoit JP, Behar-Cohen F: Intravitreous injection of PLGA microspheres encapsulating GDNF promotes the survival of photoreceptors in the rd1/rd1 mouse. Mol Vis. 2005, 11: 1002-1011.

PubMedGoogle Scholar

Fu AS, Thatiparti TR, Saidel GM, von Recum HA: Experimental studies and modeling of drug release from a tunable affinity-based drug delivery platform. Ann Biomed Eng. 2011, 39 (9): 2466-2475.

PubMedGoogle Scholar

Grondin R, Gash DM: Glial cell line-derived neurotrophic factor (GDNF): a drug candidate for the treatment of Parkinson's disease. J Neurol. 1998, 245 (11 Suppl 3): P35-P42.

PubMedGoogle Scholar

Moore AM, Wood MD, Chenard K, Hunter DA, Mackinnon SE, Sakiyama-Elbert SE, Borschel GH: Controlled delivery of glial cell line-derived neurotrophic factor enhances motor nerve regeneration. J Hand Surg [Am]. 2010, 35 (12): 2008-2017.

Google Scholar

Willerth SM, Sakiyama-Elbert SE: Approaches to neural tissue engineering using scaffolds for drug delivery. Adv Drug Deliv Rev. 2007, 59 (4–5): 325-338.

PubMedCentralPubMedGoogle Scholar

Wood MD, Moore AM, Hunter DA, Tuffaha S, Borschel GH, Mackinnon SE, Sakiyama-Elbert SE: Affinity-based release of glial-derived neurotrophic factor from fibrin matrices enhances sciatic nerve regeneration. Acta Biomater. 2009, 5 (4): 959-968.

PubMedCentralPubMedGoogle Scholar

Agterberg MJ, Versnel H, van Dijk LM, de Groot JC, Klis SF: Enhanced survival of spiral ganglion cells after cessation of treatment with brain-derived neurotrophic factor in deafened guinea pigs. J Assoc Res Otolaryngol. 2009, 10 (3): 355-367.

PubMedCentralPubMedGoogle Scholar

Hou S, Tian W, Xu Q, Cui F, Zhang J, Lu Q, Zhao C: The enhancement of cell adherence and inducement of neurite outgrowth of dorsal root ganglia co-cultured with hyaluronic acid hydrogels modified with Nogo-66 receptor antagonist in vitro. Neuroscience. 2006, 137 (2): 519-529.

PubMedGoogle Scholar

Mehrotra S, Lynam D, Maloney R, Pawelec KM, Tuszynski MH, Lee I, Chan C, Sakamoto J: Time Controlled Protein Release from Layer-by-Layer Assembled Multilayer Functionalized Agarose Hydrogels. Adv Funct Mater. 2010, 20 (2): 247-258.

PubMedCentralPubMedGoogle Scholar

Johnson PJ, Parker SR, Sakiyama-Elbert SE: Controlled release of neurotrophin-3 from fibrin-based tissue engineering scaffolds enhances neural fiber sprouting following subacute spinal cord injury. Biotechnol Bioeng. 2009, 104 (6): 1207-1214.

PubMedCentralPubMedGoogle Scholar

Johnson PJ, Tatara A, Shiu A, Sakiyama-Elbert SE: 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. Cell Transplant. 2010, 19 (1): 89-101.

PubMedCentralPubMedGoogle Scholar

Willerth SM, Rader A, Sakiyama-Elbert SE: The effect of controlled growth factor delivery on embryonic stem cell differentiation inside fibrin scaffolds. Stem Cell Res. 2008, 1 (3): 205-218.

PubMedCentralPubMedGoogle Scholar

Asmani MN, Ai J, Amoabediny G, Noroozi A, Azami M, Ebrahimi-Barough S, Navaei-Nigjeh M, Ai A, Jafarabadi M: Three-dimensional culture of differentiated endometrial stromal cells to oligodendrocyte progenitor cells (OPCs) in fibrin hydrogel. Cell Biol Int. 2013, 37 (12): 1340-1349.

PubMedGoogle Scholar

Delgado-Rivera R, Harris SL, Ahmed I, Babu AN, Patel RP, Ayres V, Flowers D, Meiners S: Increased FGF-2 secretion and ability to support neurite outgrowth by astrocytes cultured on polyamide nanofibrillar matrices. Matrix Biol. 2009, 28 (3): 137-147.

PubMedGoogle Scholar

Galderisi U, Peluso G, Di Bernardo G, Calarco A, D'Apolito M, Petillo O, Cipollaro M, Fusco FR, Melone MA: Efficient cultivation of neural stem cells with controlled delivery of FGF-2. Stem Cell Res. 2013, 10 (1): 85-94.

PubMedGoogle Scholar

Keenan TM, Grinager JR, Procak AA, Svendsen CN: In vitro localization of human neural stem cell neurogenesis by engineered FGF-2 gradients. Integr Biol (Camb). 2012, 4 (12): 1522-1531.

Google Scholar

Lam HJ, Patel S, Wang A, Chu J, Li S: In vitro regulation of neural differentiation and axon growth by growth factors and bioactive nanofibers. Tissue Eng Part A. 2010, 16 (8): 2641-2648.

PubMedCentralPubMedGoogle Scholar

Lee YB, Polio S, Lee W, Dai G, Menon L, Carroll RS, Yoo SS: Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture. Exp Neurol. 2010, 223 (2): 645-652.

PubMedGoogle Scholar

Nakajima M, Ishimuro T, Kato K, Ko IK, Hirata I, Arima Y, Iwata H: Combinatorial protein display for the cell-based screening of biomaterials that direct neural stem cell differentiation. Biomaterials. 2007, 28 (6): 1048-1060.

PubMedGoogle Scholar

Yamashita T, Deguchi K, Nagotani S, Abe K: Vascular protection and restorative therapy in ischemic stroke. Cell Transplant. 2011, 20 (1): 95-97.

PubMedGoogle Scholar

Gelain F, Panseri S, Antonini S, Cunha C, Donega M, Lowery J, Taraballi F, Cerri G, Montagna M, Baldissera F, Vescovi A: Transplantation of nanostructured composite scaffolds results in the regeneration of chronically injured spinal cords. ACS Nano. 2011, 5 (1): 227-236.

PubMedGoogle Scholar

Shoichet MS, Tator CH, Poon P, Kang C, Baumann MD: Intrathecal drug delivery strategy is safe and efficacious for localized delivery to the spinal cord. Prog Brain Res. 2007, 161: 385-392.

PubMedGoogle Scholar

Bible E, Qutachi O, Chau DY, Alexander MR, Shakesheff KM, Modo M: Neo-vascularization of the stroke cavity by implantation of human neural stem cells on VEGF-releasing PLGA microparticles. Biomaterials. 2012, 33 (30): 7435-7446.

PubMedCentralPubMedGoogle Scholar

Aktas Y, Andrieux K, Alonso MJ, Calvo P, Gursoy RN, Couvreur P, Capan Y: Preparation and in vitro evaluation of chitosan nanoparticles containing a caspase inhibitor. Int J Pharm. 2005, 298 (2): 378-383.

PubMedGoogle Scholar

Bodmeier R, Chen HG, Paeratakul O: A novel approach to the oral delivery of micro- or nanoparticles. Pharm Res. 1989, 6 (5): 413-417.

PubMedGoogle Scholar

Pan Y, Li YJ, Zhao HY, Zheng JM, Xu H, Wei G, Hao JS, Cui FD: Bioadhesive polysaccharide in protein delivery system: chitosan nanoparticles improve the intestinal absorption of insulin in vivo. Int J Pharm. 2002, 249 (1–2): 139-147.

PubMedGoogle Scholar

Sun D, Bullock MR, McGinn MJ, Zhou Z, Altememi N, Hagood S, Hamm R, Colello RJ: Basic fibroblast growth factor-enhanced neurogenesis contributes to cognitive recovery in rats following traumatic brain injury. Exp Neurol. 2009, 216 (1): 56-65.

PubMedCentralPubMedGoogle Scholar

Yoshimura S, Teramoto T, Whalen MJ, Irizarry MC, Takagi Y, Qiu J, Harada J, Waeber C, Breakefield XO, Moskowitz MA: FGF-2 regulates neurogenesis and degeneration in the dentate gyrus after traumatic brain injury in mice. J Clin Invest. 2003, 112 (8): 1202-1210.

PubMedCentralPubMedGoogle Scholar

Rifkin DB, Moscatelli D: Recent developments in the cell biology of basic fibroblast growth factor. J Cell Biol. 1989, 106: 87-95.

Google Scholar

Shiba T, Nishimura D, Kawazoe Y, Onodera Y, Tsutsumi K, Nakamura R, Ohshiro M: Modulation of mitogenic activity of fibroblast growth factors by inorganic polyphosphate. J Biol Chem. 2003, 278 (29): 26788-26792.

PubMedGoogle Scholar

Sommer A, Rifkin DB: Interaction of heparin with human basic fibroblast growth factor: protection of the angiogenic protein from proteolytic degradation by a glycosaminoglycan. J Cell Physiol. 1989, 138 (1): 215-220.

PubMedGoogle Scholar

Skop NB, Calderon F, Levison SW, Gandhi CD, Cho CH: Heparin crosslinked chitosan microspheres for the delivery of neural stem cells and growth factors for central nervous system repair. Acta Biomater. 2013, 9 (6): 6834-6843.

PubMedGoogle Scholar

Skop NB, Calderon F, Cho CH, Gandhi CD, Levison SW: Optimizing a multifunctional microsphere scaffold to improve neural precursor cell transplantation for traumatic brain injury repair. J Tissue Eng Regen Med. 2013

Google Scholar

Blits B, Kitay BM, Farahvar A, Caperton CV, Dietrich WD, Bunge MB: Lentiviral vector-mediated transduction of neural progenitor cells before implantation into injured spinal cord and brain to detect their migration, deliver neurotrophic factors and repair tissue. Restor Neurol Neurosci. 2005, 23 (5–6): 313-324.

PubMedGoogle Scholar

Sakata H, Narasimhan P, Niizuma K, Maier CM, Wakai T, Chan PH: Interleukin 6-preconditioned neural stem cells reduce ischaemic injury in stroke mice. Brain. 2012, 135 (Pt 11): 3298-3310.

PubMedCentralPubMedGoogle Scholar

Mahor S, Collin E, Dash BC, Pandit A: Controlled release of plasmid DNA from hyaluronan nanoparticles. Curr Drug Deliv. 2011, 8 (4): 354-362.

PubMedGoogle Scholar

Miao PH, He CX, Hu YL, Tabata Y, Gao JQ, Hu ZJ: Impregnation of plasmid DNA into three-dimensional PLGA scaffold enhances DNA expression of mesenchymal stem cells in vitro. Pharmazie. 2012, 67 (3): 229-232.

PubMedGoogle Scholar

Oh SH, Kim TH, Jang SH, Im GI, Lee JH: Hydrophilized 3D porous scaffold for effective plasmid DNA delivery. J Biomed Mater Res A. 2011, 97 (4): 441-450.

PubMedGoogle Scholar

Xiao B, Wang X, Qiu Z, Ma J, Zhou L, Wan Y, Zhang S: A dual-functionally modified chitosan derivative for efficient liver-targeted gene delivery. J Biomed Mater Res A. 2013, 101 (7): 1888-1897.

PubMedGoogle Scholar

Kim JH, Park JS, Yang HN, Woo DG, Jeon SY, Do HJ, Lim HY, Kim JM, Park KH: The use of biodegradable PLGA nanoparticles to mediate SOX9 gene delivery in human mesenchymal stem cells (hMSCs) and induce chondrogenesis. Biomaterials. 2011, 32 (1): 268-278.

PubMedGoogle Scholar

Capito RM, Spector M: Collagen scaffolds for nonviral IGF-1 gene delivery in articular cartilage tissue engineering. Gene Ther. 2007, 14 (9): 721-732.

PubMedGoogle Scholar

Myon L, Ferri J, Chai F, Blanchemain N, Raoul G: [Oro-maxillofacial bone tissue engineering combining biomaterials, stem cells, and gene therapy]. Rev Stomatol Chir Maxillofac. 2011, 112 (4): 201-211.

PubMedGoogle Scholar

Nie H, Wang CH: Fabrication and characterization of PLGA/HAp composite scaffolds for delivery of BMP-2 plasmid DNA. J Control Release. 2007, 120 (1–2): 111-121.

PubMedGoogle Scholar

Mehta M, Schmidt-Bleek K, Duda GN, Mooney DJ: Biomaterial delivery of morphogens to mimic the natural healing cascade in bone. Adv Drug Deliv Rev. 2012, 64 (12): 1257-1276.

PubMedCentralPubMedGoogle Scholar

Kizjakina K, Bryson JM, Grandinetti G, Reineke TM: Cationic glycopolymers for the delivery of pDNA to human dermal fibroblasts and rat mesenchymal stem cells. Biomaterials. 2012, 33 (6): 1851-1862.

PubMedCentralPubMedGoogle Scholar

McGinn AN, Nam HY, Ou M, Hu N, Straub CM, Yockman JW, Bull DA, Kim SW: Bioreducible polymer-transfected skeletal myoblasts for VEGF delivery to acutely ischemic myocardium. Biomaterials. 2011, 32 (3): 942-949.

PubMedCentralPubMedGoogle Scholar

Thiersch M, Rimann M, Panagiotopoulou V, Ozturk E, Biedermann T, Textor M, Luhmann TC, Hall H: The angiogenic response to PLL-g-PEG-mediated HIF-1alpha plasmid DNA delivery in healthy and diabetic rats. Biomaterials. 2013, 34 (16): 4173-4182.

PubMedGoogle Scholar

Chen F, Wan H, Xia T, Guo X, Wang H, Liu Y, Li X: Promoted regeneration of mature blood vessels by electrospun fibers with loaded multiple pDNA-calcium phosphate nanoparticles. Eur J Pharm Biopharm. 2013, 85 (3 Pt A): 699-710.

PubMedGoogle Scholar

Cholas RH, Hsu HP, Spector M: The reparative response to cross-linked collagen-based scaffolds in a rat spinal cord gap model. Biomaterials. 2012, 33 (7): 2050-2059.

PubMedGoogle Scholar

McConnell SK: Constructing the cerebral cortex: neurogenesis and fate determination. Neuron. 1995, 15 (4): 761-768.

PubMedGoogle Scholar

Zou B, Liu Y, Luo X, Chen F, Guo X, Li X: Electrospun fibrous scaffolds with continuous gradations in mineral contents and biological cues for manipulating cellular behaviors. Acta Biomater. 2012, 8 (4): 1576-1585.

PubMedGoogle Scholar

Published
2019-01-31
Section
Review