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Alpha-Synuclein Aggregates Associated with Mitochondria in Tunnelling Nanotubes

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Abstract

The interaction of α-synuclein with mitochondria in both typical and atypical Parkinson’s disease is a critical component of degeneration. The mechanism of cell-to-cell propagation of pathological α-synuclein in synucleinopathies is unclear. Intercellular exchange of mitochondria along tunnelling nanotubes has been described in other diseases, such as cancer; however, its role in synucleinopathies is unknown. Pathological α-synuclein species have been demonstrated previously to move from cell to cell via tunnelling nanotubes. This process was further explored using co-culture and monoculture systems to determine if α-synuclein binds to migrating mitochondria within tunnelling nanotubes. Super-resolution analysis via stimulated emission depletion microscopy showed interaction between α-synuclein with the mitochondrial outer membrane and the presence of alpha-synuclein associated with mitochondria in tunnelling nanotubes between 1321N1, differentiated THP-1 and SH-SY5Y cell types. siRNA knockdown of Miro1, a critical protein-bridging mitochondria to the motor adaptor complex, had no effect on mitochondrial density or α-synuclein association with mitochondria in tunnelling nanotubes. The results show that α-synuclein aggregates associate with mitochondria in intercellular tunnelling nanotubes, suggesting that mitochondria-mediated α-synuclein transfer between cells may contribute to cell-to-cell spread of α-synuclein aggregates and disease propagation.

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Abbreviations

CNS:

Central nervous system

dH2O:

Deionised H2O

DMEM:

Dulbecco’s modified Eagle medium

FACS:

Fluorescence-activated cell sorting

MSA:

Multiple system atrophy

NGS:

Normal goat serum

NHS:

Normal Horse serum

PBS:

Phosphate-buffered saline

PD:

Parkinson’s disease

PMA:

Phorbol-12-myristate-13-acetate

RIPA:

Radioimmunoprecipitation assay

ROS:

Reactive oxygen species

RT:

Room temperature

SDS:

Sodium dodecyl sulfate

siRNA:

Silencer RNA

STED:

Stimulated emission depletion

TnTs:

Tunnelling nanotubes

TOM:

Translocase of outer membrane receptor

WB:

Western blot

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Acknowledgements

We gratefully acknowledge Marie Olšinová and the Imaging Methods Core Facility at BIOCEV, institution supported by the MEYS CR (Large RI Project LM2018129 Czech-Bioimaging) and ERDF (project no. CZ.02.1.01/0.0/0.0/16_013/0001775) for their support with obtaining imaging data presented in this paper.

Funding

This study is financially supported by Griffith University and BIOCEV. JN was supported in part by grant 20-05942S from the Czech Science Foundation.

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  1. School of Medical Science, Griffith University, Gold Coast, Queensland, 4222, Australia

    Dario Valdinocci, Jiri Neuzil & Dean L. Pountney

  2. Institute of Biotechnology (BIOCEV), Czech Academy of Sciences, Prague-West, Czech Republic

    Jaromira Kovarova & Jiri Neuzil

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  1. Dario Valdinocci
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Valdinocci, D., Kovarova, J., Neuzil, J. et al. Alpha-Synuclein Aggregates Associated with Mitochondria in Tunnelling Nanotubes. Neurotox Res 39, 429–443 (2021). https://doi.org/10.1007/s12640-020-00285-y

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