Use of a capillary alginate gel (Capgel™) to study the three-dimensional development of sensory nerves reveals the formation of a rudimentary perineurium

Anderson, Wesley A.; Willenberg, Alicia; Bosak, Alexander; Willenberg, Bradley J.; Lambert, Stephen

doi:10.1016/j.jneumeth.2018.05.003

Cited by 13 publications

(13 citation statements)

References 21 publications

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“…Capgel™ is a self‐assembling, resorbable biomaterial composed of alginate and gelatin, which contains tunable patent capillary structures (Willenberg, Hamazaki, Meng, Terada, & Batich, ). Characterization of the in vitro nerve bundle formed within Capgel™ showed a structure that was strikingly similar to the in vivo nerve fascicle organization (Anderson, Willenberg, Bosak, Willenberg, & Lambert, ). Here, we describe a novel method to record axonal activity by integrating the in vitro generated three‐dimensional nerve model with the MEA.…”

Section: Introductionmentioning

confidence: 65%

Bundling of axons through a capillary alginate gel enhances the detection of axonal action potentials using microelectrode arrays

George

Anderson

Sommerhage

et al. 2019

J Tissue Eng Regen Med

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Microelectrode arrays (MEAs) have become important tools in high throughput assessment of neuronal activity. However, geometric and electrical constraints largely limit their ability to detect action potentials to the neuronal soma. Enhancing the resolution of these systems to detect axonal action potentials has proved both challenging and complex. In this study, we have bundled sensory axons from dorsal root ganglia through a capillary alginate gel (Capgel™) interfaced with an MEA and observed an enhanced ability to detect spontaneous axonal activity compared with two-dimensional cultures. Moreover, this arrangement facilitated the long-term monitoring of spontaneous activity from the same bundle of axons at a single electrode. Finally, using waveform analysis for cultures treated with the nociceptor agonist capsaicin, we were able to dissect action potentials from multiple axons on an individual electrode, suggesting that this model can reproduce the functional complexity associated with sensory fascicles in vivo. This novel three-dimensional functional model of the peripheral nerve can be used to study the functional complexities of peripheral neuropathies and nerve regeneration as well as being utilized in the development of novel therapeutics. KEYWORDS axonal action potential, capillary alginate gel, dorsal root ganglion, microelectrode array, threedimensional nerve model

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Section: Introductionmentioning

confidence: 65%

Bundling of axons through a capillary alginate gel enhances the detection of axonal action potentials using microelectrode arrays

George

Anderson

Sommerhage

et al. 2019

J Tissue Eng Regen Med

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“…Stiff, laminin-coated glass beads used as a 3D network positioned above an MEA showed variant burst rates and stimulus-evoked responses compared with 2D culture of e18 rat hippocampal neurons (Frega et al 2014). Softer substrates, such as anisotropic alginate-based scaffolds (Anderson et al 2018;George et al 2019) or carbon nanotube-containing PDMS (Bosi et al 2015), have also shown varied activity including capabilities of delineating capsaicin-dependent spikes of peripheral nerve culture and improving overall hippocampal neuron activity, respectively. With 3D systems outperforming 2D, future development should surround exploring further how 3D systems may affect arborization (Kayal et al 2019), synaptic maturation and functional activity, especially in the presence of drugs.…”

Section: Functional Assessmentmentioning

confidence: 99%

“…A rudimentary perineurium has also been achieved within alginate constructs with open capillaries. Coating of these constructs with laminin allowed for nerve outgrowth and enough of a polarizing signal to form perineurial cells marked by tight junction expression and distinct localization around the nerve bundle (Anderson et al 2018).…”

Section: Peripheral Nerve Histoarchitecturementioning

confidence: 99%

“…and 3D bioprinted substrates (Antill-O'Brien et al 2019) in order to recreate aspects of 3D macrostructure or neural connectivity seen in the brain. The peripheral nerve has also seen advancements in growing explant or spheroid cultures within anisotropic materials(Anderson et al 2018;George et al 2019) and growth restrictive hydrogels(Huval et al 2015;Nguyen et al 2019;Sharma et al 2019;Kramer et al 2020), respectively. Ultimately, the inherent qualities of anatomical histoarchitecture should guide the design of microarchitectural features of microphysiological devices.…”

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confidence: 99%

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Advances in 3D neuronal microphysiological systems: towards a functional nervous system on a chip

Anderson

Bosak

Högberg

et al. 2021

In Vitro Cell.Dev.Biol.-Animal

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Microphysiological systems (MPS) designed to study the complexities of the peripheral and central nervous systems have made marked improvements over the years and have allowed researchers to assess in two and three dimensions the functional interconnectivity of neuronal tissues. The recent generation of brain organoids has further propelled the field into the nascent recapitulation of structural, functional, and effective connectivities which are found within the native human nervous system. Herein, we will review advances in culture methodologies, focused especially on those of human tissues, which seek to bridge the gap from 2D cultures to hierarchical and defined 3D MPS with the end goal of developing a robust nervous system-on-a-chip platform. These advances have far-reaching implications within basic science, pharmaceutical development, and translational medicine disciplines.

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“…[19,28,29] Although capillary formation in biopolymers has been studied for more than two decades, their practical applications have been reported by only a few studies. [30,29,31] The main issue that limits their practicality is that their formation is strictly controlled by the 1D diffusion of the gelation agent. To date, no study has demonstrated any control over the shape and orientation of selfassembled capillaries in biopolymer hydrogels.…”

Section: Introductionmentioning

confidence: 99%

Chitosan hydrogel micro-bio-devices with complex capillary patterns via reactive-diffusive self-assembly

et al. 2019

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We present chitosan hydrogel microfluidic devices with self-assembled complex microcapillary patterns, conveniently formed by a diffusion-reaction process. These patterns in chitosan hydrogels are formed by a single-step procedure involving diffusion of a gelation agent into the polymer solution inside a microfluidic channel. By changing the channel geometry, it is demonstrated how to control capillary length, trajectory and branching. Diffusion of nanoparticles (NPs) in the capillary network is used as a model to effectively mimic the transport of nano-objects in vascularized tissues. Gold NPs diffusion is measured locally in the hydrogel chips, and during their two-step transport through the capillaries to the gel matrix and eventually to embedded cell clusters in the gel. In addition, the quantitative analyses reported in this study provide novel opportunities for theoretical investigation of capillary formation and propagation during diffusive gelation of biopolymers.

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Use of a capillary alginate gel (Capgel™) to study the three-dimensional development of sensory nerves reveals the formation of a rudimentary perineurium

Cited by 13 publications

References 21 publications

Bundling of axons through a capillary alginate gel enhances the detection of axonal action potentials using microelectrode arrays

Bundling of axons through a capillary alginate gel enhances the detection of axonal action potentials using microelectrode arrays

Advances in 3D neuronal microphysiological systems: towards a functional nervous system on a chip

Chitosan hydrogel micro-bio-devices with complex capillary patterns via reactive-diffusive self-assembly

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