Newly discovered neuron-to-glioma communication: new noninvasive therapeutic opportunities on the horizon?

Sprugnoli, Giulia; Golby, Alexandra J.; Santarnecchi, Emiliano

doi:10.1093/noajnl/vdab018

Cited by 8 publications

(7 citation statements)

References 30 publications

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“…Recently, ground-breaking studies demonstrated that tissue of brain and spinal cord tumours, gliomas, are electrically active and integrated into host neural tissue networks ( Venkataramani et al, 2019 ; Venkatesh et al, 2019 ). This paved the way for electro-therapies to target gliomas with desirable effects on plasticity and neuromodulation, similar to that observed in brain stimulation for psychiatric and neurological disease (Reviewed in Sprugnoli et al, 2021 ). Previously, studies found primary-derived glioblastoma cells respond to EF modulation with migration, in a manner highly dependent on the surrounding 2D or 3D microenvironment ( Huang et al, 2016 ).…”

Section: Future Workmentioning

confidence: 71%

Bioelectric Potential in Next-Generation Organoids: Electrical Stimulation to Enhance 3D Structures of the Central Nervous System

O’Hara-Wright

Mobini

Gonzalez‐Cordero

2022

Front. Cell Dev. Biol.

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Pluripotent stem cell-derived organoid models of the central nervous system represent one of the most exciting areas in in vitro tissue engineering. Classically, organoids of the brain, retina and spinal cord have been generated via recapitulation of in vivo developmental cues, including biochemical and biomechanical. However, a lesser studied cue, bioelectricity, has been shown to regulate central nervous system development and function. In particular, electrical stimulation of neural cells has generated some important phenotypes relating to development and differentiation. Emerging techniques in bioengineering and biomaterials utilise electrical stimulation using conductive polymers. However, state-of-the-art pluripotent stem cell technology has not yet merged with this exciting area of bioelectricity. Here, we discuss recent findings in the field of bioelectricity relating to the central nervous system, possible mechanisms, and how electrical stimulation may be utilised as a novel technique to engineer “next-generation” organoids.

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Section: Future Workmentioning

confidence: 71%

Bioelectric Potential in Next-Generation Organoids: Electrical Stimulation to Enhance 3D Structures of the Central Nervous System

O’Hara-Wright

Mobini

Gonzalez‐Cordero

2022

Front. Cell Dev. Biol.

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“…Ideally, new antiglioma therapies should take advantages of the cell-cell interactions in glioma tissues to minimize the damage and improve the efficacy [ 66 ] . For example, in clinical and research settings, noninvasive brain stimulation (NiBS) involves applying magnetic or electrical fields to modify neuronal activity [ 67 ] in order to modulate the behaviors of glioma cells, so as to influence the development of glioma. However, the mechanism of this treatment is still unclear and its efficacy is difficult to predict.…”

Section: Discussionmentioning

confidence: 99%

Biomimetic three-dimensional glioma model printed in vitro for the studies of glioma cells and neurons interactions

Bai¹,

Hao²,

Wang³

et al. 2024

IJB

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The interactions between glioma cells and neurons are important for glioma progression but are rarely mimicked and recapitulated in in vitro three-dimensional (3D) models, which may affect the success rate of relevant drug research and development. In this study, an in vitro bioprinted 3D glioma model consisting of an outer hemispherical shell with neurons and an inner hemisphere with glioma cells is proposed to simulate the natural glioma. This model was produced by extrusion-based 3D bioprinting technology. The cells survival rate, morphology, and intercellular Ca2+ concentration studies were carried out up to 5 days of culturing. It was found that neurons could promote the proliferation of glioma cells around them, associate the morphological changes of glioma cells to be neuron-like, and increase the expression of intracellular Ca2+ of glioma cells. Conversely, the presence of glioma cells could maintain the neuronal survival rate and promote the neurite outgrowth. The results indicated that glioma cells and neurons facilitated each other implying a symbiotic pattern established between two types of cells during the early stage of glioma development, which were seldom found in the present artificial glioma models. The proposed bioprinted glioma model can mimic the natural microenvironment of glioma tissue, provide an in-depth understanding of cell–cell interactions, and enable pathological and pharmacological studies of glioma.

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“…Recent evidence demonstrating that gliomas integrate within functional neuronal networks and proliferate in response to synaptic activity carries significant clinical and therapeutic implications for disease control and post-treatment recovery ( Venkatesh et al, 2019 ; Young et al, 2020a ; Aabedi et al, 2021c ; Krishna et al, 2021a ). For instance, hyper-excitable networks can be targeted with stimulation or other forms of neuromodulation, which may have an impact on tumor progression, though work in this arena is still in its infancy ( Sprugnoli et al, 2021a , b ). Clinical trials of non-invasive high-frequency electrical field application (i.e., tumor treating fields) to glioblastoma has been met with some success, though whether this treatment has effects beyond purely anti-mitotic activity is unclear ( Carrieri et al, 2020 ).…”

Section: Future Directions—impacting Disease Trajectory and Promoting...mentioning

confidence: 99%

Involvement of White Matter Language Tracts in Glioma: Clinical Implications, Operative Management, and Functional Recovery After Injury

et al. 2022

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To achieve optimal survival and quality of life outcomes in patients with glioma, the extent of tumor resection must be maximized without causing injury to eloquent structures. Preservation of language function is of particular importance to patients and requires careful mapping to reveal the locations of cortical language hubs and their structural and functional connections. Within this language network, accurate mapping of eloquent white matter tracts is critical, given the high risk of permanent neurological impairment if they are injured during surgery. In this review, we start by describing the clinical implications of gliomas involving white matter language tracts. Next, we highlight the advantages and limitations of methods commonly used to identify these tracts during surgery including structural imaging techniques, functional imaging, non-invasive stimulation, and finally, awake craniotomy. We provide a rationale for combining these complementary techniques as part of a multimodal mapping paradigm to optimize postoperative language outcomes. Next, we review local and long-range adaptations that take place as the language network undergoes remodeling after tumor growth and surgical resection. We discuss the probable cellular mechanisms underlying this plasticity with emphasis on the white matter, which until recently was thought to have a limited role in adults. Finally, we provide an overview of emerging developments in targeting the glioma-neuronal network interface to achieve better disease control and promote recovery after injury.

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Newly discovered neuron-to-glioma communication: new noninvasive therapeutic opportunities on the horizon?

Cited by 8 publications

References 30 publications

Bioelectric Potential in Next-Generation Organoids: Electrical Stimulation to Enhance 3D Structures of the Central Nervous System

Bioelectric Potential in Next-Generation Organoids: Electrical Stimulation to Enhance 3D Structures of the Central Nervous System

Biomimetic three-dimensional glioma model printed in vitro for the studies of glioma cells and neurons interactions

Involvement of White Matter Language Tracts in Glioma: Clinical Implications, Operative Management, and Functional Recovery After Injury

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