The glycocalyx affects the mechanotransductive perception of the topographical microenvironment

Matteo Chighizola; Tania Dini; Stefania Marcotti; Mirko D’Urso; Claudio Piazzoni; Francesca Borghi; Anita Previdi; Laura Ceriani; Claudia Folliero; Brian Stramer; Cristina Lenardi; Paolo Milani; Alessandro Podestà; Carsten Schulte

doi:10.1186/s12951-022-01585-5

The glycocalyx affects the mechanotransductive perception of the topographical microenvironment

Matteo Chighizola, Tania Dini, Stefania Marcotti, Mirko D’Urso, Claudio Piazzoni, Francesca Borghi, Anita Previdi, Laura Ceriani, Claudia Folliero, Brian Stramer, Cristina Lenardi, Paolo Milani, Alessandro Podestà^*, Carsten Schulte^*

^*Corresponding author for this work

Biomedical Engineering

Research output: Contribution to journal › Article › peer-review

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Abstract

The cell/microenvironment interface is the starting point of integrin-mediated mechanotransduction, but many details of mechanotransductive signal integration remain elusive due to the complexity of the involved (extra)cellular structures, such as the glycocalyx. We used nano-bio-interfaces reproducing the complex nanotopographical features of the extracellular matrix to analyse the glycocalyx impact on PC12 cell mechanosensing at the nanoscale (e.g., by force spectroscopy with functionalised probes). Our data demonstrates that the glycocalyx configuration affects spatio-temporal nanotopography-sensitive mechanotransductive events at the cell/microenvironment interface. Opposing effects of major glycocalyx removal were observed, when comparing flat and specific nanotopographical conditions. The excessive retrograde actin flow speed and force loading are strongly reduced on certain nanotopographies upon strong reduction of the native glycocalyx, while on the flat substrate we observe the opposite trend. Our results highlight the importance of the glycocalyx configuration in a molecular clutch force loading-dependent cellular mechanism for mechanosensing of microenvironmental nanotopographical features. Graphical Abstract: [Figure not available: see fulltext.].

Original language	English
Article number	418
Number of pages	20
Journal	Journal of Nanobiotechnology
Volume	20
Early online date	19 Sept 2022
DOIs	https://doi.org/10.1186/s12951-022-01585-5
Publication status	Published - Dec 2022

Funding

We acknowledge the support of the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 812772, project Phys2Biomed, and under FET Open grant agreement No. 801126, project EDIT. BS and SM are funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 681808). PM and CS acknowledge support from the European Union FP7-NMP-2013-LARGE-7 “Future NanoNeeds” programme. CL gratefully acknowledges funding from Miur – PRIN2017, Prot. 2017YH9MRK.

Keywords

adhesion force spectroscopy
atomic force microscopy
colloidal probes
focal adhesion
force loading
glycocalyx
integrin adhesion complexes
mechanotransduction
molecular clutch
nanostructured cell microenvironment
nanotopography

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10.1186/s12951-022-01585-5Licence: CC BY 4.0

Chighizola-etal-JNB-2022-The-glycocalyx-affects-the-mechanotransductive-perception-of-the-topographical-microenvironmentFinal published version, 2.75 MBLicence: CC BY 4.0

Cite this

Chighizola, M., Dini, T., Marcotti, S., D’Urso, M., Piazzoni, C., Borghi, F., Previdi, A., Ceriani, L., Folliero, C., Stramer, B., Lenardi, C., Milani, P., Podestà, A., & Schulte, C. (2022). The glycocalyx affects the mechanotransductive perception of the topographical microenvironment. Journal of Nanobiotechnology, 20, Article 418. https://doi.org/10.1186/s12951-022-01585-5

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abstract = "The cell/microenvironment interface is the starting point of integrin-mediated mechanotransduction, but many details of mechanotransductive signal integration remain elusive due to the complexity of the involved (extra)cellular structures, such as the glycocalyx. We used nano-bio-interfaces reproducing the complex nanotopographical features of the extracellular matrix to analyse the glycocalyx impact on PC12 cell mechanosensing at the nanoscale (e.g., by force spectroscopy with functionalised probes). Our data demonstrates that the glycocalyx configuration affects spatio-temporal nanotopography-sensitive mechanotransductive events at the cell/microenvironment interface. Opposing effects of major glycocalyx removal were observed, when comparing flat and specific nanotopographical conditions. The excessive retrograde actin flow speed and force loading are strongly reduced on certain nanotopographies upon strong reduction of the native glycocalyx, while on the flat substrate we observe the opposite trend. Our results highlight the importance of the glycocalyx configuration in a molecular clutch force loading-dependent cellular mechanism for mechanosensing of microenvironmental nanotopographical features. Graphical Abstract: [Figure not available: see fulltext.].",

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AU - Marcotti, Stefania

AU - D’Urso, Mirko

AU - Piazzoni, Claudio

AU - Borghi, Francesca

AU - Previdi, Anita

AU - Ceriani, Laura

AU - Folliero, Claudia

AU - Stramer, Brian

AU - Lenardi, Cristina

AU - Milani, Paolo

AU - Podestà, Alessandro

AU - Schulte, Carsten

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N2 - The cell/microenvironment interface is the starting point of integrin-mediated mechanotransduction, but many details of mechanotransductive signal integration remain elusive due to the complexity of the involved (extra)cellular structures, such as the glycocalyx. We used nano-bio-interfaces reproducing the complex nanotopographical features of the extracellular matrix to analyse the glycocalyx impact on PC12 cell mechanosensing at the nanoscale (e.g., by force spectroscopy with functionalised probes). Our data demonstrates that the glycocalyx configuration affects spatio-temporal nanotopography-sensitive mechanotransductive events at the cell/microenvironment interface. Opposing effects of major glycocalyx removal were observed, when comparing flat and specific nanotopographical conditions. The excessive retrograde actin flow speed and force loading are strongly reduced on certain nanotopographies upon strong reduction of the native glycocalyx, while on the flat substrate we observe the opposite trend. Our results highlight the importance of the glycocalyx configuration in a molecular clutch force loading-dependent cellular mechanism for mechanosensing of microenvironmental nanotopographical features. Graphical Abstract: [Figure not available: see fulltext.].

AB - The cell/microenvironment interface is the starting point of integrin-mediated mechanotransduction, but many details of mechanotransductive signal integration remain elusive due to the complexity of the involved (extra)cellular structures, such as the glycocalyx. We used nano-bio-interfaces reproducing the complex nanotopographical features of the extracellular matrix to analyse the glycocalyx impact on PC12 cell mechanosensing at the nanoscale (e.g., by force spectroscopy with functionalised probes). Our data demonstrates that the glycocalyx configuration affects spatio-temporal nanotopography-sensitive mechanotransductive events at the cell/microenvironment interface. Opposing effects of major glycocalyx removal were observed, when comparing flat and specific nanotopographical conditions. The excessive retrograde actin flow speed and force loading are strongly reduced on certain nanotopographies upon strong reduction of the native glycocalyx, while on the flat substrate we observe the opposite trend. Our results highlight the importance of the glycocalyx configuration in a molecular clutch force loading-dependent cellular mechanism for mechanosensing of microenvironmental nanotopographical features. Graphical Abstract: [Figure not available: see fulltext.].

KW - adhesion force spectroscopy

KW - atomic force microscopy

KW - colloidal probes

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KW - force loading

KW - glycocalyx

KW - integrin adhesion complexes

KW - mechanotransduction

KW - molecular clutch

KW - nanostructured cell microenvironment

KW - nanotopography

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VL - 20

JO - Journal of Nanobiotechnology

JF - Journal of Nanobiotechnology

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ER -

The glycocalyx affects the mechanotransductive perception of the topographical microenvironment

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