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

14 Citations (Scopus)

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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

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

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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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title = "The glycocalyx affects the mechanotransductive perception of the topographical microenvironment",

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.].",

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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AU - Chighizola, Matteo

AU - Dini, Tania

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

PY - 2022/12

Y1 - 2022/12

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

KW - focal adhesion

KW - force loading

KW - glycocalyx

KW - integrin adhesion complexes

KW - mechanotransduction

KW - molecular clutch

KW - nanostructured cell microenvironment

KW - nanotopography

U2 - 10.1186/s12951-022-01585-5

DO - 10.1186/s12951-022-01585-5

M3 - Article

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AN - SCOPUS:85138144342

SN - 1477-3155

VL - 20

JO - Journal of Nanobiotechnology

JF - Journal of Nanobiotechnology

M1 - 418

ER -

The glycocalyx affects the mechanotransductive perception of the topographical microenvironment

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Keywords

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