Scale invariant disordered nanotopography promotes hippocampal neuron development and maturation with involvement of mechanotransductive pathways

Carsten Schulte, Maddalena Ripamonti, Elisa Maffioli, Martino A. Cappelluti, Simona Nonnis, Luca Puricelli, Jacopo Lamanna, Claudio Piazzoni, Alessandro Podestà, Cristina Lenardi, Gabriella Tedeschi, Antonio Malgaroli, Paolo Milani

Research output: Contribution to journalArticle

Abstract

The identification of biomaterials which promote neuronal maturation up to the generation of integrated neural circuits is fundamental for modern neuroscience. The development of neural circuits arises from complex maturative processes regulated by poorly understood signaling events,often guided by the extracellular matrix (ECM). Here we report that nanostructured zirconia surfaces,produced by supersonic cluster beam deposition of zirconia nanoparticles and characterized by ECM-like nanotopographical features,can direct the maturation of neural networks. Hippocampal neurons cultured on such cluster-assembled surfaces displayed enhanced differentiation paralleled by functional changes. The latter was demonstrated by single-cell electrophysiology showing earlier action potential generation and increased spontaneous postsynaptic currents compared to the neurons grown on the featureless unnaturally flat standard control surfaces. Label-free shotgun proteomics broadly confirmed the functional changes and suggests furthermore a vast impact of the neuron/nanotopography interaction on mechanotransductive machinery components,known to control physiological in vivo ECM-regulated axon guidance and synaptic plasticity. Our results indicate a potential of cluster-assembled zirconia nanotopography exploitable for the creation of efficient neural tissue interfaces and cell culture devices promoting neurogenic events,but also for unveiling mechanotransductive aspects of neuronal development and maturation.
Original languageEnglish
Article number267
Pages (from-to)-
JournalFrontiers in Cellular Neuroscience
Volume10
Issue numberNOV2016
DOIs
Publication statusPublished - Nov 18 2016

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Extracellular Matrix
Neurons
Synaptic Potentials
Neuronal Plasticity
Electrophysiology
Firearms
Biocompatible Materials
Neurosciences
Proteomics
Nanoparticles
Action Potentials
Cell Culture Techniques
Equipment and Supplies
zirconium oxide
Axon Guidance

Keywords

  • Biomaterial
  • Integrin adhesion complex
  • Mechanotransduction
  • Neuronal cell adhesion molecules
  • Neuronal differentiation
  • Neuronal network maturation
  • Proteomics
  • Synaptic activity

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience

Cite this

Scale invariant disordered nanotopography promotes hippocampal neuron development and maturation with involvement of mechanotransductive pathways. / Schulte, Carsten; Ripamonti, Maddalena; Maffioli, Elisa; Cappelluti, Martino A.; Nonnis, Simona; Puricelli, Luca; Lamanna, Jacopo; Piazzoni, Claudio; Podestà, Alessandro; Lenardi, Cristina; Tedeschi, Gabriella; Malgaroli, Antonio; Milani, Paolo.

In: Frontiers in Cellular Neuroscience, Vol. 10, No. NOV2016, 267, 18.11.2016, p. -.

Research output: Contribution to journalArticle

Schulte, C, Ripamonti, M, Maffioli, E, Cappelluti, MA, Nonnis, S, Puricelli, L, Lamanna, J, Piazzoni, C, Podestà, A, Lenardi, C, Tedeschi, G, Malgaroli, A & Milani, P 2016, 'Scale invariant disordered nanotopography promotes hippocampal neuron development and maturation with involvement of mechanotransductive pathways', Frontiers in Cellular Neuroscience, vol. 10, no. NOV2016, 267, pp. -. https://doi.org/10.3389/fncel.2016.00267
Schulte, Carsten ; Ripamonti, Maddalena ; Maffioli, Elisa ; Cappelluti, Martino A. ; Nonnis, Simona ; Puricelli, Luca ; Lamanna, Jacopo ; Piazzoni, Claudio ; Podestà, Alessandro ; Lenardi, Cristina ; Tedeschi, Gabriella ; Malgaroli, Antonio ; Milani, Paolo. / Scale invariant disordered nanotopography promotes hippocampal neuron development and maturation with involvement of mechanotransductive pathways. In: Frontiers in Cellular Neuroscience. 2016 ; Vol. 10, No. NOV2016. pp. -.
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