Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis

Cancer presents a significant public health concern, particularly in the context of metastatic disease. Surgical removal of primary tumors, while essential, can inadvertently heighten the risk of metastasis. Thus, there is a critical need for innovative neoadjuvant therapies capable of curtailing me...

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Main Authors: Léa Bourguignon, Roxann Hétu-Arbour, Tania Charpentier, Marilène Bolduc, Denis Leclerc, Krista M. Heinonen, Alain Lamarre
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:OncoImmunology
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Online Access:https://www.tandfonline.com/doi/10.1080/2162402X.2024.2429846
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author Léa Bourguignon
Roxann Hétu-Arbour
Tania Charpentier
Marilène Bolduc
Denis Leclerc
Krista M. Heinonen
Alain Lamarre
author_facet Léa Bourguignon
Roxann Hétu-Arbour
Tania Charpentier
Marilène Bolduc
Denis Leclerc
Krista M. Heinonen
Alain Lamarre
author_sort Léa Bourguignon
collection DOAJ
description Cancer presents a significant public health concern, particularly in the context of metastatic disease. Surgical removal of primary tumors, while essential, can inadvertently heighten the risk of metastasis. Thus, there is a critical need for innovative neoadjuvant therapies capable of curtailing metastatic progression before or immediately following tumor resection. Addressing this imperative, the papaya mosaic virus nanoparticle (PapMV) has demonstrated potent immunostimulatory capabilities against both viruses and tumors, effectively hindering their proliferation. Our study reveals that PapMV exerts a protective effect against lung metastasis when administered systemically prior to tumor implantation or during the early stages of metastasis in various mouse models of cancer. This anti-tumor effect is initiated by the recruitment of myeloid cells in the lungs. These cells adopt a pro-inflammatory profile, secreting cytokines such as IFN-α, thus fostering a tumor microenvironment inhospitable to tumor progression. Crucially, this protective mechanism hinges on the presence of macrophages before treatment. TLR7 and IFN-I signaling pathways also play pivotal roles in this process. Furthermore, our findings demonstrate that PapMV triggers the activation of the bone marrow emergency response, which accounts for the influx of myeloid cells into the lungs. This study unveils a novel aspect of PapMV’s functionality. By bolstering the immune system, PapMV confers robust protection against metastasis at an early stage of disease progression. This discovery holds promise for therapeutic intervention, particularly as a preemptive measure prior to or just after surgical intervention.
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spelling doaj-art-bb48637c0ce04e7b89fffb27e9da916e2024-12-03T13:49:35ZengTaylor & Francis GroupOncoImmunology2162-402X2024-12-0113110.1080/2162402X.2024.2429846Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesisLéa Bourguignon0Roxann Hétu-Arbour1Tania Charpentier2Marilène Bolduc3Denis Leclerc4Krista M. Heinonen5Alain Lamarre6Centre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, Laval, QC, CanadaCentre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, Laval, QC, CanadaCentre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, Laval, QC, CanadaDepartment of Microbiology, Infectiology and Immunology, Infectious Disease Research Center, Laval University, Quebec City, QC, CanadaDepartment of Microbiology, Infectiology and Immunology, Infectious Disease Research Center, Laval University, Quebec City, QC, CanadaCentre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, Laval, QC, CanadaCentre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, Laval, QC, CanadaCancer presents a significant public health concern, particularly in the context of metastatic disease. Surgical removal of primary tumors, while essential, can inadvertently heighten the risk of metastasis. Thus, there is a critical need for innovative neoadjuvant therapies capable of curtailing metastatic progression before or immediately following tumor resection. Addressing this imperative, the papaya mosaic virus nanoparticle (PapMV) has demonstrated potent immunostimulatory capabilities against both viruses and tumors, effectively hindering their proliferation. Our study reveals that PapMV exerts a protective effect against lung metastasis when administered systemically prior to tumor implantation or during the early stages of metastasis in various mouse models of cancer. This anti-tumor effect is initiated by the recruitment of myeloid cells in the lungs. These cells adopt a pro-inflammatory profile, secreting cytokines such as IFN-α, thus fostering a tumor microenvironment inhospitable to tumor progression. Crucially, this protective mechanism hinges on the presence of macrophages before treatment. TLR7 and IFN-I signaling pathways also play pivotal roles in this process. Furthermore, our findings demonstrate that PapMV triggers the activation of the bone marrow emergency response, which accounts for the influx of myeloid cells into the lungs. This study unveils a novel aspect of PapMV’s functionality. By bolstering the immune system, PapMV confers robust protection against metastasis at an early stage of disease progression. This discovery holds promise for therapeutic intervention, particularly as a preemptive measure prior to or just after surgical intervention.https://www.tandfonline.com/doi/10.1080/2162402X.2024.2429846Cancer immunotherapyemergency myelopoiesismetastasis preventionneoadjuvant therapyvirus-based nanoparticle
spellingShingle Léa Bourguignon
Roxann Hétu-Arbour
Tania Charpentier
Marilène Bolduc
Denis Leclerc
Krista M. Heinonen
Alain Lamarre
Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
OncoImmunology
Cancer immunotherapy
emergency myelopoiesis
metastasis prevention
neoadjuvant therapy
virus-based nanoparticle
title Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
title_full Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
title_fullStr Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
title_full_unstemmed Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
title_short Systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
title_sort systemic administration of a viral nanoparticle neoadjuvant prevents lung metastasis development through emergency myelopoiesis
topic Cancer immunotherapy
emergency myelopoiesis
metastasis prevention
neoadjuvant therapy
virus-based nanoparticle
url https://www.tandfonline.com/doi/10.1080/2162402X.2024.2429846
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