Advertisement

Biomaterials Developments for Brain Tissue Engineering

  • Eduarda P. Oliveira
  • Joana Silva-Correia
  • Rui L. Reis
  • Joaquim M. OliveiraEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1078)

Abstract

The Central Nervous System (CNS) is a highly complex organ that works as the control centre of the body, managing vital and non-vital functions. Neuro-diseases can lead to the degeneration of neural tissue, breakage of the neuronal networks which can affect vital functions and originate cognitive deficits. The complexity of the neural networks, their components and the low regenerative capacity of the CNS are on the basis for the lack of recovery, having the need for therapies that can promote tissue repair and recovery. Most brain processes are mediated through molecules (e.g. cytokines, neurotransmitters) and cells response accordingly and to surrounding cues, either biological or physical, which offers molecule administration and/or cell transplantation a great potential for use in brain recovery. Biomaterials and in particular, of natural-origin are attractive candidates owed to their intrinsic biological cues and biocompatibility and degradability. Through the use of biomaterials, it is possible to protect the cells/molecules from body clearance, enzymatic degradation while maintaining the components in a place of interest. Moreover, by means of combining several components, it is possible to obtain a more targeted and controlled delivery, to image the biomaterial implantation and its degradation over time and tackling simultaneously occurring events (cell death and inflammation) in brain diseases. In this chapter, it is reviewed some brain-affecting diseases and the current developments on tissue engineering approaches for a functional recovery of the brain from those diseases.

Keywords

Brain Biomaterials Cells Molecules Tissue engineering 

References

  1. 1.
    Addington CP, Dharmawaj S, Heffernan JM, Sirianni RW, Stabenfeldt SE (2017) Hyaluronic acid-laminin hydrogels increase neural stem cell transplant retention and migratory response to SDF-1α. Matrix Biol 60–61:206–216.  https://doi.org/10.1016/j.matbio.2016.09.007 CrossRefPubMedGoogle Scholar
  2. 2.
    Ajroud-Driss S, Siddique T (2015) Sporadic and hereditary amyotrophic lateral sclerosis (ALS). Biochim Biophys Acta (BBA) - Mol Basis Dis 1852(4):679–684.  https://doi.org/10.1016/j.bbadis.2014.08.010 CrossRefGoogle Scholar
  3. 3.
    Allaman I, Bélanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34(2):76–87.  https://doi.org/10.1016/j.tins.2010.12.001 CrossRefPubMedGoogle Scholar
  4. 4.
    Amer MH, Rose FRAJ, Shakesheff KM, Modo M, White LJ (2017) Translational considerations in injectable cell-based therapeutics for neurological applications: concepts, progress and challenges. NP J Regen Med 2(1):23.  https://doi.org/10.1038/s41536-017-0028-x CrossRefGoogle Scholar
  5. 5.
    Appel AA, Anastasio MA, Larson JC, Brey EM (2013) Imaging challenges in biomaterials and tissue engineering. Biomaterials 34(28):6615–6630.  https://doi.org/10.1016/j.biomaterials.2013.05.033 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
  7. 7.
    Bloom OE, Morgan JR (2011) Membrane trafficking events underlying axon repair, growth, and regeneration. Mol Cell Neurosci 48(4):339–348.  https://doi.org/10.1016/j.mcn.2011.04.003 CrossRefPubMedGoogle Scholar
  8. 8.
    Boisserand LSB, Kodama T, Papassin J, Auzely R, Moisan A, Rome C, Detante O (2016) Biomaterial applications in cell-based therapy in experimental stroke. Stem Cells Int 2016:1–14.  https://doi.org/10.1155/2016/6810562 CrossRefGoogle Scholar
  9. 9.
    Bozdaǧ Pehlivan S (2013) Nanotechnology-based drug delivery systems for targeting, imaging and diagnosis of neurodegenerative diseases. Pharm Res 30(10):2499–2511.  https://doi.org/10.1007/s11095-013-1156-7 CrossRefGoogle Scholar
  10. 10.
    Broguiere N, Isenmann L, Zenobi-Wong M (2016) Novel enzymatically cross-linked hyaluronan hydrogels support the formation of 3D neuronal networks. Biomaterials 99:47–55.  https://doi.org/10.1016/j.biomaterials.2016.04.036 CrossRefPubMedGoogle Scholar
  11. 11.
    Broussalis E, Killer M, McCoy M, Harrer A, Trinka E, Kraus J (2012) Current therapies in ischemic stroke. Part A. Recent developments in acute stroke treatment and in stroke prevention. Drug Discov Today 17(7–8):296–309.  https://doi.org/10.1016/j.drudis.2011.11.005 CrossRefPubMedGoogle Scholar
  12. 12.
    Carter R, Aldridge S, Page M, Parker S, Frith CD, Frith U, Shulman MB (2014) The human brain book: an illustrated guide to its structure, function, and disorders (Carter R, Page M, eds) (Rev ed). DK Publishing, New YorkGoogle Scholar
  13. 13.
    Chen S, Zeng L, Hu Z (2014) Progressing haemorrhagic stroke: categories, causes, mechanisms and managements. J Neurol 261(11):2061–2078.  https://doi.org/10.1007/s00415-014-7291-1 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Cheng AY, García AJ (2013) Engineering the matrix microenvironment for cell delivery and engraftment for tissue repair. Curr Opin Biotechnol 24(5):864–871.  https://doi.org/10.1016/j.copbio.2013.04.005 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Cheng TY, Chen MH, Chang WH, Huang MY, Wang TW (2013) Neural stem cells encapsulated in a functionalized self-assembling peptide hydrogel for brain tissue engineering. Biomaterials 34(8):2005–2016.  https://doi.org/10.1016/j.biomaterials.2012.11.043 CrossRefGoogle Scholar
  16. 16.
    Clark AR, Carter AB, Hager LE, Price EM (2016) In vivo neural tissue engineering: cylindrical biocompatible hydrogels that create new neural tracts in the adult mammalian brain. Stem Cells Dev 25(15):1109–1118.  https://doi.org/10.1089/scd.2016.0069 CrossRefPubMedGoogle Scholar
  17. 17.
    David S, Kroner A (2015) Inflammation and secondary damage after spinal cord injury. In: Neural regeneration. Elsevier.  https://doi.org/10.1016/B978-0-12-801732-6.00016-1 CrossRefGoogle Scholar
  18. 18.
    Delcroix GJR, Schiller PC, Benoit JP, Montero-Menei CN (2010) Adult cell therapy for brain neuronal damages and the role of tissue engineering. Biomaterials 31(8):2105–2120.  https://doi.org/10.1016/j.biomaterials.2009.11.084 CrossRefGoogle Scholar
  19. 19.
    Dexter DT, Jenner P (2013) Parkinson disease: from pathology to molecular disease mechanisms. Free Radic Biol Med 62:132–144.  https://doi.org/10.1016/j.freeradbiomed.2013.01.018 CrossRefPubMedGoogle Scholar
  20. 20.
    Dhar S, Reddy EM, Prabhune A, Pokharkar V, Shiras A, Prasad BLV (2011) Cytotoxicity of sophorolipid-gellan gum-gold nanoparticle conjugates and their doxorubicin loaded derivatives towards human glioma and human glioma stem cell lines. Nanoscale 3(2):575–580.  https://doi.org/10.1039/C0NR00598C CrossRefPubMedGoogle Scholar
  21. 21.
    Dong G-C, Kuan C-Y, Subramaniam S, Zhao J-Y, Sivasubramaniam S, Chang H-Y, Lin F-H (2015) A potent inhibition of oxidative stress induced gene expression in neural cells by sustained ferulic acid release from chitosan based hydrogel. Mater Sci Eng C 49:691–699.  https://doi.org/10.1016/j.msec.2015.01.030 CrossRefGoogle Scholar
  22. 22.
    Dutta RC, Dutta AK (2009) Cell-interactive 3D-scaffold; advances and applications. Biotechnol Adv 27(4):334–339.  https://doi.org/10.1016/j.biotechadv.2009.02.002 CrossRefPubMedGoogle Scholar
  23. 23.
    Elliott Donaghue I, Tam R, Sefton MV, Shoichet MS (2014) Cell and biomolecule delivery for tissue repair and regeneration in the central nervous system. J Control Release 190:219–227.  https://doi.org/10.1016/j.jconrel.2014.05.040 CrossRefPubMedGoogle Scholar
  24. 24.
    Forstmann BU, Wagenmakers EJ (2015) An introduction to model-based cognitive neuroscience. In: Forstmann BU, Wagenmakers E-J (eds) An introduction to model-based cognitive neuroscience. Springer New York, New York.  https://doi.org/10.1007/978-1-4939-2236-9 CrossRefGoogle Scholar
  25. 25.
    George PM, Steinberg GK (2015) Novel stroke therapeutics: unraveling stroke pathophysiology and its impact on clinical treatments. Neuron 87:297–309.  https://doi.org/10.1016/j.neuron.2015.05.041 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Gwon K, Kim E, Tae G (2017) Heparin-hyaluronic acid hydrogel in support of cellular activities of 3D encapsulated adipose derived stem cells. Acta Biomater 49:284–295.  https://doi.org/10.1016/j.actbio.2016.12.001 CrossRefPubMedGoogle Scholar
  27. 27.
    Haidet-Phillips AM, Maragakis NJ (2015) Neural and glial progenitor transplantation as a neuroprotective strategy for amyotrophic lateral sclerosis (ALS). Brain Res 1628:343–350.  https://doi.org/10.1016/j.brainres.2015.06.035 CrossRefPubMedGoogle Scholar
  28. 28.
    Haim LB, Rowitch DH (2016) Functional diversity of astrocytes in neural circuit regulation. Nat Rev Neurosci 18(1):31–41.  https://doi.org/10.1038/nrn.2016.159 CrossRefPubMedGoogle Scholar
  29. 29.
    Hamby ME, Sofroniew MV (2010) Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 7(4):494–506.  https://doi.org/10.1016/j.nurt.2010.07.003 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Harris JP, Struzyna LA, Murphy PL, Adewole DO, Kuo E, Cullen DK (2016) Advanced biomaterial strategies to transplant preformed micro-tissue engineered neural networks into the brain. J Neural Eng 13(1):16019.  https://doi.org/10.1088/1741-2560/13/1/016019 CrossRefGoogle Scholar
  31. 31.
    Harvey AR, Lovett SJ, Majda BT, Yoon JH, Wheeler LPG, Hodgetts SI (2014) Neurotrophic factors for spinal cord repair: which, where, how and when to apply, and for what period of time? Brain Res 1619:1–36.  https://doi.org/10.1016/j.brainres.2014.10.049 CrossRefGoogle Scholar
  32. 32.
    Huang S, Li J, Han L, Liu S, Ma H, Huang R, Jiang C (2011) Dual targeting effect of Angiopep-2-modified, DNA-loaded nanoparticles for glioma. Biomaterials 32(28):6832–6838.  https://doi.org/10.1016/j.biomaterials.2011.05.064 CrossRefPubMedGoogle Scholar
  33. 33.
    Islam MT (2016) Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol Res 6412(November):1–10.  https://doi.org/10.1080/01616412.2016.1251711 CrossRefGoogle Scholar
  34. 34.
    Ivana J, Nina K, Radovan K (2013) Glioma and glioblastoma – how much do we (not) know? Mol Clin Oncol 1(6):935–941.  https://doi.org/10.3892/mco.2013.172 CrossRefGoogle Scholar
  35. 35.
    Janowski M, Wagner D-C, Boltze J (2015) Stem cell–based tissue replacement after stroke: factual necessity or notorious fiction? Stroke 46(8):2354–2363.  https://doi.org/10.1161/STROKEAHA.114.007803 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Johnstone VPA, Shultz SR, Yan EB, O’Brien TJ, Rajan R (2014) The acute phase of mild traumatic brain injury is characterized by a distance-dependent neuronal hypoactivity. J Neurotrauma 31(22):1881–1895.  https://doi.org/10.1089/neu.2014.3343 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O et al (2011) Amyotrophic lateral sclerosis. Lancet 377(9769):942–955.  https://doi.org/10.1016/S0140-6736(10)61156-7 CrossRefGoogle Scholar
  38. 38.
    Knight VB, Serrano EE (2017) Hydrogel scaffolds promote neural gene expression and structural reorganization in human astrocyte cultures. Peer J 5:e2829.  https://doi.org/10.7717/peerj.2829 CrossRefPubMedGoogle Scholar
  39. 39.
    Koh E, Jung YC, Woo H-M, Kang B-J (2017) Injectable alginate-microencapsulated canine adipose tissue-derived mesenchymal stem cells for enhanced viable cell retention. J Vet Med Sci 79(3):492–501.  https://doi.org/10.1292/jvms.16-0456 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Koivisto JT, Joki T, Parraga JE, Pääkkönen R, Ylä-Outinen L, Salonen L et al (2017) Bioamine-crosslinked gellan gum hydrogel for neural tissue engineering. Biomed Mater 12(2):25014.  https://doi.org/10.1088/1748-605X/aa62b0 CrossRefGoogle Scholar
  41. 41.
    Koss KM, Churchward MA, Nguyen AT, Yager JY, Todd KG, Unsworth LD (2016) Brain biocompatibility and microglia response towards engineered self-assembling (RADA)4nanoscaffolds. Acta Biomater 35:127–137.  https://doi.org/10.1016/j.actbio.2016.02.001 CrossRefPubMedGoogle Scholar
  42. 42.
    Lee H, McKeon RJ, Bellamkonda RV (2010) Sustained delivery of thermostabilized chABC enhances axonal sprouting and functional recovery after spinal cord injury. Proc Natl Acad Sci U S A 107(8):3340–3345.  https://doi.org/10.1073/pnas.0905437106 CrossRefPubMedGoogle Scholar
  43. 43.
    Li X, Han J, Zhao Y, Ding W, Wei J, Han S et al (2015) Functionalized collagen scaffold neutralizing the myelin-inhibitory molecules promoted neurites outgrowth in vitro and facilitated spinal cord regeneration in vivo. ACS Appl Mater Interfaces 7(25):13960–13971.  https://doi.org/10.1021/acsami.5b03879 CrossRefPubMedGoogle Scholar
  44. 44.
    Li X, Katsanevakis E, Liu X, Zhang N, Wen X (2012) Engineering neural stem cell fates with hydrogel design for central nervous system regeneration. Prog Polym Sci 37(8):1105–1129.  https://doi.org/10.1016/j.progpolymsci.2012.02.004 CrossRefGoogle Scholar
  45. 45.
    Liang Y, Bar-Shir A, Song X, Gilad AA, Walczak P, Bulte JWM (2015) Label-free imaging of gelatin-containing hydrogel scaffolds. Biomaterials 42(18):144–150.  https://doi.org/10.1016/j.biomaterials.2014.11.050 CrossRefPubMedGoogle Scholar
  46. 46.
    Lim TC, Spector M (2017) Biomaterials for enhancing CNS repair. Transl Stroke Res 8(1):57–64.  https://doi.org/10.1007/s12975-016-0470-x CrossRefPubMedGoogle Scholar
  47. 47.
    Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A et al (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109.  https://doi.org/10.1007/s00401-007-0243-4 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK et al (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131(6):803–820.  https://doi.org/10.1007/s00401-016-1545-1 CrossRefGoogle Scholar
  49. 49.
    Mazibuko Z, Choonara YE, Kumar P, Du Toit LC, Modi G, Naidoo D, Pillay V (2015) A review of the potential role of nano-enabled drug delivery technologies in amyotrophic lateral sclerosis: lessons learned from other neurodegenerative disorders. J Pharm Sci 104(4):1213–1229.  https://doi.org/10.1002/jps.24322 CrossRefPubMedGoogle Scholar
  50. 50.
    Migliaresi Claudio MA (2014) Scaffolds for tissue engineering – biological design, materials, and fabrication. Pan Stanford Publishing, Singapore.  https://doi.org/10.4032/9789814463218 CrossRefGoogle Scholar
  51. 51.
    Nih LR, Carmichael ST, Segura T (2016) Hydrogels for brain repair after stroke: an emerging treatment option. Curr Opin Biotechnol 40:155–163.  https://doi.org/10.1016/j.copbio.2016.04.021 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Noback CR, Strominger NL, Demarest RJ, Ruggiero DA (2005) The human nervous system – structure and function (Catanese T, ed) (6th edn). Humana Press. Retrieved from https://link.springer.com/content/pdf/10.1007%2F978-1-59259-730-7.pdf
  53. 53.
    Nowinski WL (2011) Introduction to brain anatomy. In: Miller K (ed) Biomechanics of the brain, biological and medical physics, biomedical engineering, vol 27. Springer New York, New York, pp 5–40.  https://doi.org/10.1007/978-1-4419-9997-9_2 CrossRefGoogle Scholar
  54. 54.
    Oliveira E, Assunção-Silva RC, Ziv-Polat O, Gomes ED, Teixeira FG, Silva NA, Shahar A, Salgado AJ (2017) Influence of different ECM-like hydrogels on neurite outgrowth induced by adipose tissue-derived stem cells. Stem Cells Int 2017(3):1–10.  https://doi.org/10.1155/2017/6319129 Google Scholar
  55. 55.
    Omuro A (2013) Glioblastoma and other malignant gliomas. JAMA 310(17):1842.  https://doi.org/10.1001/jama.2013.280319 CrossRefPubMedGoogle Scholar
  56. 56.
    Placone AL, McGuiggan PM, Bergles DE, Guerrero-Cazares H, Quiñones-Hinojosa A, Searson PC (2015) Human astrocytes develop physiological morphology and remain quiescent in a novel 3D matrix. Biomaterials 42:134–143.  https://doi.org/10.1016/j.biomaterials.2014.11.046 CrossRefPubMedGoogle Scholar
  57. 57.
    Purves D (2004). Neuroscience third edition. Vascular (vol 3). http://doi.org/978-0878937257
  58. 58.
    Rassu G, Soddu E, Cossu M, Brundu A, Cerri G, Marchetti N et al (2015) Solid microparticles based on chitosan or methyl-β-cyclodextrin: a first formulative approach to increase the nose-to-brain transport of deferoxamine mesylate. J Control Release 201(2):68–77.  https://doi.org/10.1016/j.jconrel.2015.01.025 CrossRefPubMedGoogle Scholar
  59. 59.
    Re DB, Le Verche V, Yu C, Amoroso MW, Politi KA, Phani S et al (2014) Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 81(5):1001–1008.  https://doi.org/10.1016/j.neuron.2014.01.011 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Re F, Gregori M, Masserini M (2012) Nanotechnology for neurodegenerative disorders. Maturitas 73(1):45–51.  https://doi.org/10.1016/j.maturitas.2011.12.015 CrossRefPubMedGoogle Scholar
  61. 61.
    Rinaldi F, Motti D, Ferraiuolo L, Kaspar BK (2016) High content analysis in amyotrophic lateral sclerosis. Mol Cell Neurosci 80:180–191.  https://doi.org/10.1016/j.mcn.2016.12.001 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Roqué PJ, Costa LG (2017) Co-culture of neurons and microglia. In Current protocols in toxicology (pp 11.24.1–11.24.17).  https://doi.org/10.1002/cptx.32
  63. 63.
    Sandilyan MB, Dening T (2015) Brain function, disease and dementia. Nurs Stand 29(39):36–42.  https://doi.org/10.7748/ns.29.39.36.e9425 CrossRefPubMedGoogle Scholar
  64. 64.
    Silva NA, Moreira J, Ribeiro-Samy S, Gomes ED, Tam RY, Shoichet MS et al (2013) Modulation of bone marrow mesenchymal stem cell secretome by ECM-like hydrogels. Biochimie 95(12):2314–2319.  https://doi.org/10.1016/j.biochi.2013.08.016 CrossRefPubMedGoogle Scholar
  65. 65.
    Silva Adaya D, Aguirre-Cruz L, Guevara J, Ortiz-Islas E (2017) Nanobiomaterials’ applications in neurodegenerative diseases. J Biomater Appl 31(7):953–984.  https://doi.org/10.1177/0885328216659032 CrossRefPubMedGoogle Scholar
  66. 66.
    Snaidero N, Simons M (2014) Myelination at a glance. J Cell Sci 127(Pt 14):2999–3004.  https://doi.org/10.1242/jcs.151043 CrossRefPubMedGoogle Scholar
  67. 67.
    So K-F, Xu X-M (2015) Advances and challenges for neural regeneration research. In: XIAO-MING K-FS, XU X-M (eds) Neural regeneration, 1st edn. Elsevier, pp 3–17.  https://doi.org/10.1016/B978-0-12-801732-6.00001-X CrossRefGoogle Scholar
  68. 68.
    Soichet MS, Tate CC, Baumann MD, LaPlaca MC (2008). Strategies for regeneration and repair in the injured central nervous system. In: Indwelling neural implants, Chapter 8.  https://doi.org/10.1258/ebm.2011.010367 CrossRefGoogle Scholar
  69. 69.
    Squire LR, Bloom FE, Spitzer NC, Lac Sdu, Ghosh A, Berg D (2008) Fundamental neuroscience, vol 8, p 1127. Retrieved from http://books.google.com/books?id=AEmEn-_hD9IC&pgis=1
  70. 70.
    Stanwick JC, Baumann MD, Shoichet MS (2012) Enhanced neurotrophin-3 bioactivity and release from a nanoparticle-loaded composite hydrogel. J Control Release 160(3):666–675.  https://doi.org/10.1016/j.jconrel.2012.03.024 CrossRefPubMedGoogle Scholar
  71. 71.
    Tam RY, Fuehrmann T, Mitrousis N, Shoichet MS (2013) Regenerative therapies for central nervous system diseases: a biomaterials approach. Neuropsychopharmacology 39(1):169–188.  https://doi.org/10.1038/npp.2013.237 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Tivnan A, Heilinger T, Ramsey JM, O’Connor G, Pokorny JL, Sarkaria JN et al (2017) Anti-GD2-ch14.18/CHO coated nanoparticles mediate glioblastoma (GBM)-specific delivery of the aromatase inhibitor, Letrozole, reducing proliferation, migration and chemoresistance in patient-derived GBM tumor cells. Oncotarget 8(10):16605–16620.  https://doi.org/10.18632/oncotarget.15073 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Tuszynski MH, Steward O (2012) Concepts and methods for the study of axonal regeneration in the CNS. Neuron 74(5):777–791.  https://doi.org/10.1016/j.neuron.2012.05.006.Concepts CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Ulrich TA, de Juan Pardo EM, Kumar S (2009) The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 69(10):4167–4174.  https://doi.org/10.1158/0008-5472.CAN-08-4859 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Venugopal C, Chandanala S, Prasad HC, Nayeem D, Bhonde RR, Dhanushkodi A (2017) Regenerative therapy for hippocampal degenerative diseases: lessons from preclinical studies. J Tissue Eng Regen Med 11(2):321–333.  https://doi.org/10.1002/term.2052 CrossRefPubMedGoogle Scholar
  76. 76.
    Vieira S, da Silva Morais A, Silva-Correia J, Oliveira JM, Reis RL (2017) Natural-based hydrogels: from processing to applications. In: Encyclopedia of polymer science and technology. Wiley, Hoboken, pp 1–27.  https://doi.org/10.1002/0471440264.pst652 CrossRefGoogle Scholar
  77. 77.
    Walker PA (2010) Advances in progenitor cell therapy using scaffolding constructs for central nervous system injury. Cell 5(3):283–300.  https://doi.org/10.1007/s12015-009-9081-1.Advances CrossRefGoogle Scholar
  78. 78.
    Ward JA, Huang L, Guo H, Ghatak S, Toole BP (2003) Perturbation of hyaluronan interactions inhibits malignant properties of glioma cells. Am J Pathol 162(5):1403–1409.  https://doi.org/10.1016/S0002-9440(10)64273-3 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Winter CC, Katiyar KS, Hernandez NS, Song YJ, Struzyna LA, Harris JP, Kacy Cullen D (2016) Transplantable living scaffolds comprised of micro-tissue engineered aligned astrocyte networks to facilitate central nervous system regeneration. Acta Biomater 38:44–58.  https://doi.org/10.1016/j.actbio.2016.04.021 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Wright KT, El Masri W, Osman A, Roberts S, Chamberlain G, Ashton B a, Johnson WEB (2007) Bone marrow stromal cells stimulate neurite outgrowth over neural proteoglycans (CSPG), myelin associated glycoprotein and Nogo-A. Biochem Biophys Res Commun 354(2):559–566.  https://doi.org/10.1016/j.bbrc.2007.01.013 CrossRefPubMedGoogle Scholar
  81. 81.
    Yamashita T, Chai HL, Teramoto S, Tsuji S, Shimazaki K, Muramatsu S, Kwak S (2013) Rescue of amyotrophic lateral sclerosis phenotype in a mouse model by intravenous AAV9-ADAR2 delivery to motor neurons. EMBO Mol Med 5(11):1710–1719.  https://doi.org/10.1002/emmm.201302935 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Yan LP, Silva-Correia J, Ribeiro VP, Miranda-Gonçalves V, Correia C, da Silva Morais A, Sousa RA, Reis RM, Oliveira AL, Oliveira JM, Reis RL (2016) Tumor growth suppression induced by biomimetic silk fibroin hydrogels. Sci Rep 6(1):31037.  https://doi.org/10.1038/srep31037 Nature Publishing Group
  83. 83.
    Yang L, Shao B, Zhang X, Cheng Q, Lin T, Liu E (2016) Multifunctional upconversion nanoparticles for targeted dual-modal imaging in rat glioma xenograft. J Biomater Appl 31(3):400–410.  https://doi.org/10.1177/0885328216658779 CrossRefPubMedGoogle Scholar
  84. 84.
    Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7(8):617–627.  https://doi.org/10.1038/nrn1956 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Zhu T, Tang Q, Shen Y, Tang H, Chen L, Zhu J (2015) An acellular cerebellar biological scaffold: preparation, characterization, biocompatibility and effects on neural stem cells. Brain Res Bull 113:48–57.  https://doi.org/10.1016/j.brainresbull.2015.03.003 CrossRefPubMedGoogle Scholar
  86. 86.
    Zhu X, Ni S, Xia T, Yao Q, Li H, Wang B et al (2015) Anti-neoplastic cytotoxicity of SN-38-loaded PCL/Gelatin electrospun composite nanofiber scaffolds against human glioblastoma cells in vitro. J Pharm Sci 104(12):4345–4354.  https://doi.org/10.1002/jps.24684 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Eduarda P. Oliveira
    • 1
    • 2
  • Joana Silva-Correia
    • 1
    • 2
  • Rui L. Reis
    • 1
    • 2
    • 3
  • Joaquim M. Oliveira
    • 1
    • 2
    • 3
    Email author
  1. 1.3B’s Research Group, I3Bs – Research Institute on Biomaterials, Biodegradables and Biomimetics, Headquarters of the European Institute of Excellence on Tissue Engineering and Regenerative Medicine, AvePark, Parque de Ciência e Tecnologia, Zona Industrial da GandraUniversity of MinhoGuimarãesPortugal
  2. 2.ICVS/3Bs - PT Government Associate LaboratoryBraga/GuimarãesPortugal
  3. 3.The Discoveries Centre for Regenerative and Precision MedicineHeadquarters at University of MinhoGuimarãesPortugal

Personalised recommendations