The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model.

Abraham Lin; Joey De Backer; Delphine Quatannens; Bart Cuypers; Hanne Verswyvel; Edgar Cardenas De La Hoz; Bart Ribbens; Vasiliki Siozopoulou; Jonas Van Audenaerde; Elly Marcq; Filip Lardon; Kris Laukens; Steve Vanlanduit; Evelien Smits; Annemie Bogaerts

doi:10.1002/btm2.10314

The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model.

Abraham Lin, Joey De Backer, Delphine Quatannens, Bart Cuypers, Hanne Verswyvel, Edgar Cardenas De La Hoz, Bart Ribbens, Vasiliki Siozopoulou, Jonas Van Audenaerde, Elly Marcq, Filip Lardon, Kris Laukens, Steve Vanlanduit, Evelien Smits, Annemie Bogaerts

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

22 Citations (Scopus)

Abstract

Melanoma remains a deadly cancer despite significant advances in immune checkpoint blockade and targeted therapies. The incidence of melanoma is also growing worldwide, which highlights the need for novel treatment options and strategic combination of therapies. Here, we investigate non-thermal plasma (NTP), an ionized gas, as a promising, therapeutic option. In a melanoma mouse model, direct treatment of tumors with NTP results in reduced tumor burden and prolonged survival. Physical characterization of NTP treatment in situ reveals the deposited NTP energy and temperature associated with therapy response, and whole transcriptome analysis of the tumor identified several modulated pathways. NTP treatment also enhances the cancer-immunity cycle, as immune cells in both the tumor and tumor-draining lymph nodes appear more stimulated to perform their anti-cancer functions. Thus, our data suggest that local NTP therapy stimulates systemic, anti-cancer immunity. We discuss, in detail, how these fundamental insights will help direct the translation of NTP technology into the clinic and inform rational combination strategies to address the challenges in melanoma therapy.

Original language	English
Article number	e10314
Number of pages	18
Journal	Bioengineering & translational medicine
Volume	7
Issue number	3
DOIs	https://doi.org/10.1002/btm2.10314
Publication status	Published - Sept 2022
Externally published	Yes

Bibliographical note

Funding Information:
The authors would like to thank and acknowledge Christophe Hermans, Ho Wa Lau, and Hilde Lambrechts for their help with sectioning and preparing the IHC slides. The authors would also like to thank Dani Banner for designing the ergonomic NTP applicator handle and Hasan Baysal for 3D printing the pieces used in this experiment. We would also like to thank several patrons, as part of this research was funded by donations from different donors, including Dedert Schilde vzw, Mr Willy Floren, and the Vereycken family. Some of the resources and services used in this work were provided by the VSC (Flemish Supercomputer Center) and funded by the Research Foundation ‐ Flanders (FWO) and the Flemish Government. The FWO fellowships and grants that funded this work also include: 12S9218N (Abraham Lin), 12S9221N (Abraham Lin), G044420N (Abraham Lin, Annemie Bogaert, and Steve Vanlanduit), 1S76421N (Delphine Quatannens), and 1S67621N (Hanne Verswyvel). Figure 7 was created with BioRender.com .

Funding Information:
The authors would like to thank and acknowledge Christophe Hermans, Ho Wa Lau, and Hilde Lambrechts for their help with sectioning and preparing the IHC slides. The authors would also like to thank Dani Banner for designing the ergonomic NTP applicator handle and Hasan Baysal for 3D printing the pieces used in this experiment. We would also like to thank several patrons, as part of this research was funded by donations from different donors, including Dedert Schilde vzw, Mr Willy Floren, and the Vereycken family. Some of the resources and services used in this work were provided by the VSC (Flemish Supercomputer Center) and funded by the Research Foundation - Flanders (FWO) and the Flemish Government. The FWO fellowships and grants that funded this work also include: 12S9218N (Abraham Lin), 12S9221N (Abraham Lin), G044420N (Abraham Lin, Annemie Bogaert, and Steve Vanlanduit), 1S76421N (Delphine Quatannens), and 1S67621N (Hanne Verswyvel). Figure 7 was created with BioRender.com.

Publisher Copyright:
© 2022 The Authors. Bioengineering & Translational Medicine published by Wiley Periodicals LLC on behalf of American Institute of Chemical Engineers.

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Lin, A., De Backer, J., Quatannens, D., Cuypers, B., Verswyvel, H., Cardenas De La Hoz, E., Ribbens, B., Siozopoulou, V., Van Audenaerde, J., Marcq, E., Lardon, F., Laukens, K., Vanlanduit, S., Smits, E., & Bogaerts, A. (2022). The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model. Bioengineering & translational medicine, 7(3), Article e10314. https://doi.org/10.1002/btm2.10314

@article{7f6c60ff2fc94be5a74bf6145454f96a,

title = "The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model.",

abstract = "Melanoma remains a deadly cancer despite significant advances in immune checkpoint blockade and targeted therapies. The incidence of melanoma is also growing worldwide, which highlights the need for novel treatment options and strategic combination of therapies. Here, we investigate non-thermal plasma (NTP), an ionized gas, as a promising, therapeutic option. In a melanoma mouse model, direct treatment of tumors with NTP results in reduced tumor burden and prolonged survival. Physical characterization of NTP treatment in situ reveals the deposited NTP energy and temperature associated with therapy response, and whole transcriptome analysis of the tumor identified several modulated pathways. NTP treatment also enhances the cancer-immunity cycle, as immune cells in both the tumor and tumor-draining lymph nodes appear more stimulated to perform their anti-cancer functions. Thus, our data suggest that local NTP therapy stimulates systemic, anti-cancer immunity. We discuss, in detail, how these fundamental insights will help direct the translation of NTP technology into the clinic and inform rational combination strategies to address the challenges in melanoma therapy.",

author = "Abraham Lin and {De Backer}, Joey and Delphine Quatannens and Bart Cuypers and Hanne Verswyvel and {Cardenas De La Hoz}, Edgar and Bart Ribbens and Vasiliki Siozopoulou and {Van Audenaerde}, Jonas and Elly Marcq and Filip Lardon and Kris Laukens and Steve Vanlanduit and Evelien Smits and Annemie Bogaerts",

note = "Funding Information: The authors would like to thank and acknowledge Christophe Hermans, Ho Wa Lau, and Hilde Lambrechts for their help with sectioning and preparing the IHC slides. The authors would also like to thank Dani Banner for designing the ergonomic NTP applicator handle and Hasan Baysal for 3D printing the pieces used in this experiment. We would also like to thank several patrons, as part of this research was funded by donations from different donors, including Dedert Schilde vzw, Mr Willy Floren, and the Vereycken family. Some of the resources and services used in this work were provided by the VSC (Flemish Supercomputer Center) and funded by the Research Foundation ‐ Flanders (FWO) and the Flemish Government. The FWO fellowships and grants that funded this work also include: 12S9218N (Abraham Lin), 12S9221N (Abraham Lin), G044420N (Abraham Lin, Annemie Bogaert, and Steve Vanlanduit), 1S76421N (Delphine Quatannens), and 1S67621N (Hanne Verswyvel). Figure 7 was created with BioRender.com . Funding Information: The authors would like to thank and acknowledge Christophe Hermans, Ho Wa Lau, and Hilde Lambrechts for their help with sectioning and preparing the IHC slides. The authors would also like to thank Dani Banner for designing the ergonomic NTP applicator handle and Hasan Baysal for 3D printing the pieces used in this experiment. We would also like to thank several patrons, as part of this research was funded by donations from different donors, including Dedert Schilde vzw, Mr Willy Floren, and the Vereycken family. Some of the resources and services used in this work were provided by the VSC (Flemish Supercomputer Center) and funded by the Research Foundation - Flanders (FWO) and the Flemish Government. The FWO fellowships and grants that funded this work also include: 12S9218N (Abraham Lin), 12S9221N (Abraham Lin), G044420N (Abraham Lin, Annemie Bogaert, and Steve Vanlanduit), 1S76421N (Delphine Quatannens), and 1S67621N (Hanne Verswyvel). Figure 7 was created with BioRender.com. Publisher Copyright: {\textcopyright} 2022 The Authors. Bioengineering & Translational Medicine published by Wiley Periodicals LLC on behalf of American Institute of Chemical Engineers.",

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doi = "10.1002/btm2.10314",

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Lin, A, De Backer, J, Quatannens, D, Cuypers, B, Verswyvel, H, Cardenas De La Hoz, E, Ribbens, B, Siozopoulou, V, Van Audenaerde, J, Marcq, E, Lardon, F, Laukens, K, Vanlanduit, S, Smits, E & Bogaerts, A 2022, 'The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model.', Bioengineering & translational medicine, vol. 7, no. 3, e10314. https://doi.org/10.1002/btm2.10314

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T1 - The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model.

AU - Lin, Abraham

AU - De Backer, Joey

AU - Quatannens, Delphine

AU - Cuypers, Bart

AU - Verswyvel, Hanne

AU - Cardenas De La Hoz, Edgar

AU - Ribbens, Bart

AU - Siozopoulou, Vasiliki

AU - Van Audenaerde, Jonas

AU - Marcq, Elly

AU - Lardon, Filip

AU - Laukens, Kris

AU - Vanlanduit, Steve

AU - Smits, Evelien

AU - Bogaerts, Annemie

N1 - Funding Information: The authors would like to thank and acknowledge Christophe Hermans, Ho Wa Lau, and Hilde Lambrechts for their help with sectioning and preparing the IHC slides. The authors would also like to thank Dani Banner for designing the ergonomic NTP applicator handle and Hasan Baysal for 3D printing the pieces used in this experiment. We would also like to thank several patrons, as part of this research was funded by donations from different donors, including Dedert Schilde vzw, Mr Willy Floren, and the Vereycken family. Some of the resources and services used in this work were provided by the VSC (Flemish Supercomputer Center) and funded by the Research Foundation ‐ Flanders (FWO) and the Flemish Government. The FWO fellowships and grants that funded this work also include: 12S9218N (Abraham Lin), 12S9221N (Abraham Lin), G044420N (Abraham Lin, Annemie Bogaert, and Steve Vanlanduit), 1S76421N (Delphine Quatannens), and 1S67621N (Hanne Verswyvel). Figure 7 was created with BioRender.com . Funding Information: The authors would like to thank and acknowledge Christophe Hermans, Ho Wa Lau, and Hilde Lambrechts for their help with sectioning and preparing the IHC slides. The authors would also like to thank Dani Banner for designing the ergonomic NTP applicator handle and Hasan Baysal for 3D printing the pieces used in this experiment. We would also like to thank several patrons, as part of this research was funded by donations from different donors, including Dedert Schilde vzw, Mr Willy Floren, and the Vereycken family. Some of the resources and services used in this work were provided by the VSC (Flemish Supercomputer Center) and funded by the Research Foundation - Flanders (FWO) and the Flemish Government. The FWO fellowships and grants that funded this work also include: 12S9218N (Abraham Lin), 12S9221N (Abraham Lin), G044420N (Abraham Lin, Annemie Bogaert, and Steve Vanlanduit), 1S76421N (Delphine Quatannens), and 1S67621N (Hanne Verswyvel). Figure 7 was created with BioRender.com. Publisher Copyright: © 2022 The Authors. Bioengineering & Translational Medicine published by Wiley Periodicals LLC on behalf of American Institute of Chemical Engineers.

PY - 2022/9

Y1 - 2022/9

N2 - Melanoma remains a deadly cancer despite significant advances in immune checkpoint blockade and targeted therapies. The incidence of melanoma is also growing worldwide, which highlights the need for novel treatment options and strategic combination of therapies. Here, we investigate non-thermal plasma (NTP), an ionized gas, as a promising, therapeutic option. In a melanoma mouse model, direct treatment of tumors with NTP results in reduced tumor burden and prolonged survival. Physical characterization of NTP treatment in situ reveals the deposited NTP energy and temperature associated with therapy response, and whole transcriptome analysis of the tumor identified several modulated pathways. NTP treatment also enhances the cancer-immunity cycle, as immune cells in both the tumor and tumor-draining lymph nodes appear more stimulated to perform their anti-cancer functions. Thus, our data suggest that local NTP therapy stimulates systemic, anti-cancer immunity. We discuss, in detail, how these fundamental insights will help direct the translation of NTP technology into the clinic and inform rational combination strategies to address the challenges in melanoma therapy.

AB - Melanoma remains a deadly cancer despite significant advances in immune checkpoint blockade and targeted therapies. The incidence of melanoma is also growing worldwide, which highlights the need for novel treatment options and strategic combination of therapies. Here, we investigate non-thermal plasma (NTP), an ionized gas, as a promising, therapeutic option. In a melanoma mouse model, direct treatment of tumors with NTP results in reduced tumor burden and prolonged survival. Physical characterization of NTP treatment in situ reveals the deposited NTP energy and temperature associated with therapy response, and whole transcriptome analysis of the tumor identified several modulated pathways. NTP treatment also enhances the cancer-immunity cycle, as immune cells in both the tumor and tumor-draining lymph nodes appear more stimulated to perform their anti-cancer functions. Thus, our data suggest that local NTP therapy stimulates systemic, anti-cancer immunity. We discuss, in detail, how these fundamental insights will help direct the translation of NTP technology into the clinic and inform rational combination strategies to address the challenges in melanoma therapy.

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DO - 10.1002/btm2.10314

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JO - Bioengineering & translational medicine

JF - Bioengineering & translational medicine

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ER -

The effect of local non-thermal plasma therapy on the cancer-immunity cycle in a melanoma mouse model.

Abstract

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