Influencing Neuroplasticity in Stroke Treatment with Advanced

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Influencing Neuroplasticity in Stroke Treatment with Advanced Advanced Drug Delivery Reviews 148 (2019) 204–218 Contents lists available at ScienceDirect Advanced Drug Delivery Reviews journal homepage: www.elsevier.com/locate/addr Influencing neuroplasticity in stroke treatment with advanced biomaterials-based approaches J.M. Obermeyer a,b,c,E.Hoa,b,c, A. Gracias a,c, M.S. Shoichet a,b,c,d,⁎ a Department of Chemical Engineering and Applied Chemistry, University of Toronto, 200 College Street, Toronto, ON M5S 3E5, Canada b Institute of Biomaterials and Biomedical Engineering, University of Toronto, 164 College Street, Toronto, ON M5S 3G9, Canada c Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, 160 College Street, Toronto, ON M5S 3E1, Canada d Department of Chemistry, University of Toronto, 80 St. George Street, Toronto, ON M5S 3H6, Canada article info abstract Article history: Since the early 1990s, we have known that the adult brain is not static and has the capacity to repair itself. The Received 10 July 2018 delivery of various therapeutic factors and cells have resulted in some exciting pre-clinical and clinical outcomes Received in revised form 5 November 2018 in stroke models by targeting post-injury plasticity to enhance recovery. Developing a deeper understanding of Accepted 17 December 2018 the pathways that modulate plasticity will enable us to optimize delivery strategies for therapeutics and achieve Available online 21 December 2018 more robust effects. Biomaterials are a key tool for the optimization of these potential treatments, owing to their biocompatibility and tunability. In this review, we identify factors and targets that impact plastic processes known to contribute to recovery, discuss the role of biomaterials in enhancing the efficacy of treatment strategies, and suggest combinatorial approaches based on the stage of injury progression. © 2018 Elsevier B.V. All rights reserved. Contents 1. Introduction.............................................................. 205 2. Definingneuroplasticity......................................................... 205 3. Clinicalstrategiesforstroketreatment.................................................. 205 4. Endogenousresponsetostrokeinjury................................................... 206 4.1. Injuryprogression........................................................ 206 4.2. Reactiveastrocytesandtheglialscar................................................ 206 4.3. Brain-derivedneurotrophicfactor................................................. 206 4.4. Additionalendogenousplasticitymodulators............................................ 207 5. Exogenousplasticitymodulators..................................................... 208 5.1. Exogenousbiomolecules..................................................... 208 5.2. Transplantationofexogenouscells................................................. 209 6. Biomaterialsforplasticitymodulation................................................... 210 6.1. Biomaterialsforexogenousfactordelivery............................................. 210 6.1.1. Systemicdeliveryusingnanoparticlebiomaterialformulations................................ 210 6.1.2. Localdeliveryofbiomaterialparticles........................................... 212 6.2. Scaffolds............................................................. 212 6.2.1. Scaffoldsasdeliveryvehicles............................................... 213 6.3. Biomaterialsforcelldelivery.................................................... 213 ⁎ Corresponding author at: Department of Chemical Engineering and Applied Chemistry, University of Toronto, 200 College Street, Toronto, ON M5S 3E5, Canada. E-mail address: [email protected] (M.S. Shoichet). https://doi.org/10.1016/j.addr.2018.12.012 0169-409X/© 2018 Elsevier B.V. All rights reserved. J.M. Obermeyer et al. / Advanced Drug Delivery Reviews 148 (2019) 204–218 205 7. Outlookandfuturedirections...................................................... 214 Acknowledgments.............................................................. 214 References................................................................. 214 1. Introduction initiated, strengthening these synapses to make information transfer more efficient for processes that are frequently used. This concept, orig- Increases in metabolic risk factors such as obesity and diabetes inally introduced in 1973 by Bliss and Lomo [21], has helped to explain mellitus, in conjunction with the ageing population, have made stroke why repetitive use and coordination of neural pathways is crucial to the second most common cause of death and the third leading cause memory formation and skill development. Early studies by Levy and of adult disability worldwide [1]. To add insult to injury, advancements Steward furthered this understanding, showing that LTP has coopera- in stroke treatment are severely lacking. Tissue plasminogen activator tive and associative properties. A strong input will induce cooperative (tPA) remains the sole clinically-used therapeutic for patients present- LTP by recruiting many excitatory synapses to fire together. Associative ing with ischemic stroke. Since the first use of tPA for stroke treatment LTP occurs when simultaneous activation of two separate inputs, one in 1996 [2], the only significant standard of care improvement has strong and one weak, induces LTP in the weak input that would not ex- been to widen the timeframe for administration of this drug via perienceLTPonitsown[22], as is the case in Pavlovian fear conditioning endovascular thrombectomy (ET) in large-vessel occlusions [3]. ET has [23]. Though N-methyl-D-aspartate (NMDA) receptor-dependent LTP in dramatically increased the population eligible to receive tPA and limits hippocampal CA1 neurons has been the most heavily investigated form, the extent of the damage, but it does not address the chronic aspects LTP takes on different characteristics depending on the area of the brain of the illness. Rehabilitation therapy remains the gold standard for man- in which it is observed [24]. Advances in optogenetics are shedding light agement of memory loss and functional deficits that affect stroke pa- on the mechanisms that contribute to long-term memory formation tients, yet it only restores partial function in most cases [4]. and have enabled the deactivation and reactivation of associative mem- The inherent plasticity of the brain could be the key to pushing past ories in a mouse model [25]. this stagnation in stroke therapy innovation. By developing strategies Confining the definition of neuroplasticity to alterations in existing that support and augment natural reparative mechanisms, we can neural and glial cells oversimplifies this phenomenon by neglecting to take advantage of the existing architecture of the brain to achieve acknowledge other contributing factors. Neurogenesis, angiogenesis, more robust long-term changes. Biomaterials have been fundamental and changes in the extracellular matrix (ECM) occur in conjunction to these strategies, owing to their versatility and tunability. These bio- with alterations to existing neural and glial cells. Adult neural stem compatible, and often biodegradable, materials typically serve as the ve- cells, located in the subventricular zone of the lateral ventricles and hicles for sustained therapeutic factor release and cell delivery [5,6]. the subgranular zone of the dentate gyrus, can be stimulated to rejuve- nate neural circuitry or mitigate the effects of injury [26,27]. With in- creased or decreased usage of particular regions of the brain, demands 2. Defining neuroplasticity for oxygen and nutrients fluctuate, dictating the required degree of vas- cularization and initiating angiogenesis [18,28]. The ECM must accom- Neuroplasticity is a broad term that encompasses any changes in modate and support all of these architectural changes, and so will be nervous system structure, function or connections made in response catabolized and restructured accordingly [29]. As a multi-faceted and to external or internal stimuli [7]. In order to affect neuroplasticity in a complex phenomenon, neuroplasticity offers many opportunities for beneficial way, it is important to recognize that these changes happen therapeutic intervention. on several different levels, often simultaneously. At the highest level, global plasticity is a rewiring of entire neural systems and can result from major traumatic injury. When large regions of tissue are compro- 3. Clinical strategies for stroke treatment mised, compensatory mechanisms recruit the remaining tissue to take on functions that would otherwise be lost. This has been observed Stroke is generally broken down into two main types: hemorrhagic both in animal models [8] and in humans [9,10]. There is evidence of and ischemic. Hemorrhagic stroke is caused by blood vessels rupturing both ipsilesional [11] and contralesional [12] tissues taking on this func- and is often fatal. The loss of blood supply combined with increased in- tionality, though it remains unclear precisely what determines the re- tracranial pressure and infiltration of inflammatory cytokines and ma- distribution to one hemisphere over the other [13]. There is also an trix metalloproteinases typically results in severe and rapid tissue ongoing debate surrounding which of these two scenarios is preferred damage [30]. In ischemic stroke, a blockage such as a blood clot ob- when developing intervention strategies, or whether the goal should structs blood flow to one or more areas, interrupting the supply
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