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Article

Neoadjuvant Intratumoral Immunotherapy with Cowpea Mosaic Virus Induces Local and Systemic Antitumor Efficacy in Canine Mammary Cancer Patients

by
Guillermo Valdivia
1,†,
Daniel Alonso-Miguel
1,†,
Maria Dolores Perez-Alenza
1,
Anna Barbara Emilia Zimmermann
2,
Evelien Schaafsma
3,
Fred W. Kolling IV
4,
Lucia Barreno
1,
Angela Alonso-Diez
1,
Veronique Beiss
5,
Jessica Fernanda Affonso de Oliveira
5,
María Suárez-Redondo
1,
Steven Fiering
4,6,
Nicole F. Steinmetz
5,7,8,9,10,11,12,
Johannes vom Berg
2,
Laura Peña
1,‡ and
Hugo Arias-Pulido
6,*,‡
1
Department of Animal Medicine, Surgery and Pathology, Mammary Oncology Unit, Veterinary Teaching Hospital, Veterinary Medicine School, Complutense University of Madrid, 28040 Madrid, Spain
2
Institute of Laboratory Animal Science, University of Zurich, 8952 Schlieren, Switzerland
3
Aquila Data Analytics, LLC., Concord, NH 03766, USA
4
Dartmouth Cancer Center, Geisel School of Medicine at Dartmouth, Lebanon, NH 03756, USA
5
Department of NanoEngineering, University of California San Diego, 9500 Gilman Dr., La Jolla, CA 92093, USA
6
Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Lebanon, NH 03756, USA
7
Department of Radiology, University of California San Diego, La Jolla, CA 92093, USA
8
Department of Bioengineering, University of California San Diego, La Jolla, CA 92039, USA
9
Moores Cancer Center, University of California San Diego, La Jolla, CA 92039, USA
10
Center for Nano Immuno-Engineering, University of California San Diego, La Jolla, CA 92039, USA
11
Institute for Materials Discovery and Design, University of California San Diego, La Jolla, CA 92039, USA
12
Center for Engineering in Cancer, Institute for Engineering in Medicine, University of California San Diego, La Jolla, CA 92039, USA
 
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*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
‡
These authors contributed equally to this work.
Cells 2023, 12(18), 2241; https://doi.org/10.3390/cells12182241
Submission received: 17 August 2023 / Revised: 4 September 2023 / Accepted: 6 September 2023 / Published: 8 September 2023
(This article belongs to the Section Cellular Immunology)
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Abstract

The lack of optimal models to evaluate novel agents is delaying the development of effective immunotherapies against human breast cancer (BC). In this prospective open label study, we applied neoadjuvant intratumoral immunotherapy with empty cowpea mosaic virus-like particles (eCPMV) to 11 companion dogs diagnosed with canine mammary cancer (CMC), a spontaneous tumor resembling human BC. We found that two neoadjuvant intratumoral eCPMV injections resulted in tumor reduction in injected tumors in all patients and in noninjected tumors located in the ipsilateral and contralateral mammary chains of injected dogs. Tumor reduction was independent of clinical stage, tumor size, histopathologic grade, and tumor molecular subtype. RNA-seq-based analysis of injected tumors indicated a decrease in DNA replication activity and an increase in activated dendritic cell infiltration in the tumor microenvironment. Immunohistochemistry analysis demonstrated significant intratumoral increases in neutrophils, T and B lymphocytes, and plasma cells. eCPMV intratumoral immunotherapy demonstrated antitumor efficacy without any adverse effects. This novel immunotherapy has the potential for improving outcomes for human BC patients.
Keywords: canine mammary cancer; intratumoral immunotherapy; plant virus; cowpea mosaic virus; nanoparticles; immune cells; tumor microenvironment; patient outcome canine mammary cancer; intratumoral immunotherapy; plant virus; cowpea mosaic virus; nanoparticles; immune cells; tumor microenvironment; patient outcome

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MDPI and ACS Style

Valdivia, G.; Alonso-Miguel, D.; Perez-Alenza, M.D.; Zimmermann, A.B.E.; Schaafsma, E.; Kolling, F.W., IV; Barreno, L.; Alonso-Diez, A.; Beiss, V.; Affonso de Oliveira, J.F.; et al. Neoadjuvant Intratumoral Immunotherapy with Cowpea Mosaic Virus Induces Local and Systemic Antitumor Efficacy in Canine Mammary Cancer Patients. Cells 2023, 12, 2241. https://doi.org/10.3390/cells12182241

AMA Style

Valdivia G, Alonso-Miguel D, Perez-Alenza MD, Zimmermann ABE, Schaafsma E, Kolling FW IV, Barreno L, Alonso-Diez A, Beiss V, Affonso de Oliveira JF, et al. Neoadjuvant Intratumoral Immunotherapy with Cowpea Mosaic Virus Induces Local and Systemic Antitumor Efficacy in Canine Mammary Cancer Patients. Cells. 2023; 12(18):2241. https://doi.org/10.3390/cells12182241

Chicago/Turabian Style

Valdivia, Guillermo, Daniel Alonso-Miguel, Maria Dolores Perez-Alenza, Anna Barbara Emilia Zimmermann, Evelien Schaafsma, Fred W. Kolling, IV, Lucia Barreno, Angela Alonso-Diez, Veronique Beiss, Jessica Fernanda Affonso de Oliveira, and et al. 2023. "Neoadjuvant Intratumoral Immunotherapy with Cowpea Mosaic Virus Induces Local and Systemic Antitumor Efficacy in Canine Mammary Cancer Patients" Cells 12, no. 18: 2241. https://doi.org/10.3390/cells12182241

APA Style

Valdivia, G., Alonso-Miguel, D., Perez-Alenza, M. D., Zimmermann, A. B. E., Schaafsma, E., Kolling, F. W., IV, Barreno, L., Alonso-Diez, A., Beiss, V., Affonso de Oliveira, J. F., Suárez-Redondo, M., Fiering, S., Steinmetz, N. F., vom Berg, J., Peña, L., & Arias-Pulido, H. (2023). Neoadjuvant Intratumoral Immunotherapy with Cowpea Mosaic Virus Induces Local and Systemic Antitumor Efficacy in Canine Mammary Cancer Patients. Cells, 12(18), 2241. https://doi.org/10.3390/cells12182241

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