Interaction of micropatterned topographical and biochemical cues to direct neurite growth from spiral ganglion neurons

Truong, Kristy; Leigh, Braden; Vecchi, Joseph T.; Bartholomew, Reid; Xu, Honghui; Guymon, C. Allan; Hansen, Marlan R.

doi:10.1016/j.heares.2021.108315

Cited by 8 publications

(12 citation statements)

References 49 publications

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“…Importantly, the conclusion that microfeature geometry determines neurite turning remains sound since even with the chaotic reorientation occurring, we still see clear and significant differences in our comparisons of interest (figures 2, 3 and supplementary figure 3). That being said, the reorientation of the neurite shafts is an important finding that motivates a reinterpretation of prior studies using fixed neurons to study pathfinding in response to various cues [17,34]. Our data suggest that the growth cone may be consistently navigating a microfeature, but the shaft may reorient bringing it out of the microfeature.…”

Section: Growth Cones Respond To the Topographically Micropatterned S...supporting

confidence: 58%

“…This random nature of growth cone motility has been described previously [56][57][58]. Neurite pathfinding results from an interplay between the strength of the turn cue [17,19], stochastic actin polymerization [58], and signaling from the support cells from the primary culture influencing guidance cues [54]. Within the experimental system used here, these factors result in non-uniform pathfinding observations within each geometric condition, e.g.…”

Section: Growth Cones Respond To the Topographically Micropatterned S...mentioning

confidence: 53%

“…To inform these aims, further work is needed to understand the fundamental behaviors of growth cones as they sense and respond to cues in their environment. Thus, many are studying how neurites grow and turn in response to various cues such as diffusible chemical gradients [10,16], patterned peptide surface coatings [17,18], and engineered surface topography [19][20][21], among others [22], including electrospun scaffolds [23,24]. Though each of these approaches has its optimal uses and limitations, engineered surface topography to direct cell material interactions is particularly appealing for directing neurite growth to improve neural prostheses.…”

Section: Introductionmentioning

confidence: 99%

“…Both topographical and biochemical cues activate similar signaling to direct growth cone guidance behavior [28,29]. Finally, gradual, micron-scale, topographical cues can be engineered to offer similar or even greater influence on neurite guidance compared to biochemical cues [17,18].…”

Section: Introductionmentioning

confidence: 99%

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The geometry of photopolymerized topography influences neurite pathfinding by directing growth cone morphology and migration

Vecchi,

Rhomberg,

Guymon

et al. 2024

J. Neural Eng.

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Objective: Cochlear implants provide auditory perception to those with severe to profound sensorineural hearing loss: however, the quality of sound perceived by users does not approximate natural hearing. This limitation is due in part to the large physical gap between the stimulating electrodes and their target neurons. Therefore, directing the controlled outgrowth of processes from spiral ganglion neurons (SGNs) into close proximity to the electrode array could provide significantly increased hearing function. Approach: For this objective to be properly designed and implemented, the ability and limits of SGN neurites to be guided must first be determined. In this work, we engineer precise topographical microfeatures with angle turn challenges of various geometries to study SGN pathfinding and use live imaging to better understand how neurite growth is guided by these cues. Main Results: We find that the geometry of the angled microfeatures determines the ability of neurites to navigate the angled microfeature turns. SGN neurite pathfinding fidelity is increased by 20 to 70% through minor increases in microfeature amplitude (depth) and by 25% if the angle of the patterned turn is made obtuse. Further, we see that dorsal root ganglion neuron growth cones change their morphology and migration to become more elongated within microfeatures. Our observations also indicate complexities in studying neurite turning. First, as the growth cone pathfinds in response to the various cues, the associated neurite often reorients across the angle topographical microfeatures. Additionally, neurite branching is observed in response to topographical guidance cues, most frequently when turning decisions are most uncertain. Significance: Overall, the multi-angle channel micropatterned substrate is a versatile and efficient system to assess neurite turning and pathfinding in response to topographical cues. These findings represent fundamental principles of neurite pathfinding that will be essential to consider for the design of 3D systems aiming to guide neurite growth in vivo.

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Section: Growth Cones Respond To the Topographically Micropatterned S...supporting

confidence: 58%

Section: Growth Cones Respond To the Topographically Micropatterned S...mentioning

confidence: 53%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The geometry of photopolymerized topography influences neurite pathfinding by directing growth cone morphology and migration

Vecchi,

Rhomberg,

Guymon

et al. 2024

J. Neural Eng.

Self Cite

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“…[23,24] Yet, other examples of ephrin patterns leading to tissue's organization in vitro are scarce. [23,[25][26][27][28] To address the role of ephrins as positional cues in tissue organization, patterning must be applied on proper cellfriendly and biomimetic substrates. In vivo, tissues sit on thin, dense forms of extracellular matrix (ECM) known as the basement membrane (BM), mainly composed of collagen type IV and laminin.…”

Section: Introductionmentioning

confidence: 99%

Ephrin Micropatterns Exogenously Modulate Cell Organization in Organoid‐Derived Intestinal Epithelial Monolayers

Larrañaga

Fernández‐Majada

Ojosnegros

et al. 2022

Adv Materials Inter

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Eph‐ephrin signaling acts as spatial cue to define the tissue boundaries, the axonal growth, or the organization of compartmentalized tissues in vertebrates. By the regulation of tension, adhesion, and repulsion, intermingling of cells expressing the membrane‐tethered ligand and cells expressing the membrane‐tethered receptor is prevented. Despite being surface‐bound, most of the studies addressing Eph‐ephrin interactions use soluble ligands, which lack the spatial component needed to study tissue patterning. Here, it is shown that spatial patterns of ephrin ligands can modulate the organization of the different compartments in organoid‐derived intestinal epithelial monolayers. A modified version of the microcontact printing technique is used to create spatial cues of ephrin ligand on basement membrane surrogates. It is shown that both ligand concentration and cellular density can impact the strength of the repulsive effect triggered by Eph‐ephrin signaling. Finally, it is demonstrated that by using micropatterned ephrin spatial cues one can modify the orientation of intestinal crypts and align them in the direction set by the pattern. The approach presented here is believed to be an excellent tool to study exogenous signal with relevant spatial distribution in vivo.

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The cochlear matrisome: Importance in hearing and deafness

Pressé,

Malgrange,

Delacroix

2024

Matrix Biology

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Interaction of micropatterned topographical and biochemical cues to direct neurite growth from spiral ganglion neurons

Cited by 8 publications

References 49 publications

The geometry of photopolymerized topography influences neurite pathfinding by directing growth cone morphology and migration

The geometry of photopolymerized topography influences neurite pathfinding by directing growth cone morphology and migration

Ephrin Micropatterns Exogenously Modulate Cell Organization in Organoid‐Derived Intestinal Epithelial Monolayers

The cochlear matrisome: Importance in hearing and deafness

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