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Sensory nerves enhance triple-negative breast cancer migration and metastasis via the axon guidance molecule PlexinB3

Thanh T Le, Samantha L Payne, Maia N Buckwald, Lily A Hayes, View ORCID ProfileChristopher B Burge, View ORCID ProfileMadeleine J Oudin
doi: https://doi.org/10.1101/2021.12.07.471585
Thanh T Le
1Department of Biomedical Engineering, 200 College Avenue, Tufts University, Medford MA 02155, USA
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Samantha L Payne
1Department of Biomedical Engineering, 200 College Avenue, Tufts University, Medford MA 02155, USA
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Maia N Buckwald
1Department of Biomedical Engineering, 200 College Avenue, Tufts University, Medford MA 02155, USA
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Lily A Hayes
1Department of Biomedical Engineering, 200 College Avenue, Tufts University, Medford MA 02155, USA
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Christopher B Burge
2Department of Biology, MIT, Cambridge, MA 02139, USA
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Madeleine J Oudin
1Department of Biomedical Engineering, 200 College Avenue, Tufts University, Medford MA 02155, USA
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  • ORCID record for Madeleine J Oudin
  • For correspondence: madeleine.oudin@tufts.edu
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Abstract

In breast cancer, nerve presence has been correlated with more invasive disease and worse prognosis, yet the mechanisms by which different types of peripheral nerves drive tumor progression remain poorly understood. In this study, we identified sensory nerves as more abundant in human triple-negative breast cancer (TNBC) tumors. Coinjection of sensory neurons isolated from the dorsal root ganglia (DRG) of adult female mice with human TNBC cells in immunocompromised mice increased the number of lung metastases. Direct in vitro co-culture of human TNBC cells with the dorsal root ganglia (DRG) of adult female mice revealed that TNBC cells adhere to sensory neuron fibers leading to an increase in migration speed. Species-specific RNA sequencing revealed that co-culture of TNBC cells with sensory nerves upregulates the expression of genes associated with cell migration and adhesion in cancer cells. We demonstrate that the axon guidance molecule Plexin B3 mediates cancer cell adhesion to and migration on sensory nerves. Together, our results identify a novel mechanism by which nerves contribute to breast cancer migration and metastasis by inducing a shift in TNBC cell gene expression and support the rationale for disrupting neuron-cancer cell interactions to target metastasis.

Significance The presence of nerves in breast tumors has been associated with poor outcome. Understanding the mechanisms by which nerves contribute to tumor progression could help identify novel strategies to target metastatic disease.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 07, 2021.
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Sensory nerves enhance triple-negative breast cancer migration and metastasis via the axon guidance molecule PlexinB3
Thanh T Le, Samantha L Payne, Maia N Buckwald, Lily A Hayes, Christopher B Burge, Madeleine J Oudin
bioRxiv 2021.12.07.471585; doi: https://doi.org/10.1101/2021.12.07.471585
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Sensory nerves enhance triple-negative breast cancer migration and metastasis via the axon guidance molecule PlexinB3
Thanh T Le, Samantha L Payne, Maia N Buckwald, Lily A Hayes, Christopher B Burge, Madeleine J Oudin
bioRxiv 2021.12.07.471585; doi: https://doi.org/10.1101/2021.12.07.471585

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