Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model

Inducing immunogenic cell death (ICD) during cancer therapy is a major challenge that might significantly improve patient survival. The purpose of this study was to develop a theranostic nanocarrier, capable both of conveying a cytotoxic thermal dose when mediating photothermal therapy (PTT) after i...

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Main Authors: Ailton Antonio Sousa-Junior, Francyelli Mello-Andrade, João Victor Ribeiro Rocha, Tácio Gonçalves Hayasaki, Juliana Santana de Curcio, Lívia do Carmo Silva, Ricardo Costa de Santana, Eliana Martins Lima, Cléver Gomes Cardoso, Elisângela de Paula Silveira-Lacerda, Sebastião Antonio Mendanha, Andris Figueiroa Bakuzis
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Pharmaceutics
Subjects:
Online Access:https://www.mdpi.com/1999-4923/15/3/943
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author Ailton Antonio Sousa-Junior
Francyelli Mello-Andrade
João Victor Ribeiro Rocha
Tácio Gonçalves Hayasaki
Juliana Santana de Curcio
Lívia do Carmo Silva
Ricardo Costa de Santana
Eliana Martins Lima
Cléver Gomes Cardoso
Elisângela de Paula Silveira-Lacerda
Sebastião Antonio Mendanha
Andris Figueiroa Bakuzis
author_facet Ailton Antonio Sousa-Junior
Francyelli Mello-Andrade
João Victor Ribeiro Rocha
Tácio Gonçalves Hayasaki
Juliana Santana de Curcio
Lívia do Carmo Silva
Ricardo Costa de Santana
Eliana Martins Lima
Cléver Gomes Cardoso
Elisângela de Paula Silveira-Lacerda
Sebastião Antonio Mendanha
Andris Figueiroa Bakuzis
author_sort Ailton Antonio Sousa-Junior
collection DOAJ
description Inducing immunogenic cell death (ICD) during cancer therapy is a major challenge that might significantly improve patient survival. The purpose of this study was to develop a theranostic nanocarrier, capable both of conveying a cytotoxic thermal dose when mediating photothermal therapy (PTT) after its intravenous delivery, and of consequently inducing ICD, improving survival. The nanocarrier consists of red blood cell membranes (RBCm) embedding the near-infrared dye IR-780 (IR) and camouflaging Mn-ferrite nanoparticles (RBCm-IR-Mn). The RBCm-IR-Mn nanocarriers were characterized by size, morphology, surface charge, magnetic, photophysical, and photothermal properties. Their photothermal conversion efficiency was found to be size- and concentration-dependent. Late apoptosis was observed as the cell death mechanism for PTT. Calreticulin and HMGB1 protein levels increased for in vitro PTT with temperature around 55 °C (ablative regime) but not for 44 °C (hyperthermia), suggesting ICD elicitation under ablation. RBCm-IR-Mn were then intravenously administered in sarcoma S180-bearing Swiss mice, and in vivo ablative PTT was performed five days later. Tumor volumes were monitored for the subsequent 120 days. RBCm-IR-Mn-mediated PTT promoted tumor regression in 11/12 animals, with an overall survival rate of 85% (11/13). Our results demonstrate that the RBCm-IR-Mn nanocarriers are great candidates for PTT-induced cancer immunotherapy.
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spelling doaj.art-dac3f4eff5e7464d92dd4f33c698f9012023-11-17T13:16:35ZengMDPI AGPharmaceutics1999-49232023-03-0115394310.3390/pharmaceutics15030943Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma ModelAilton Antonio Sousa-Junior0Francyelli Mello-Andrade1João Victor Ribeiro Rocha2Tácio Gonçalves Hayasaki3Juliana Santana de Curcio4Lívia do Carmo Silva5Ricardo Costa de Santana6Eliana Martins Lima7Cléver Gomes Cardoso8Elisângela de Paula Silveira-Lacerda9Sebastião Antonio Mendanha10Andris Figueiroa Bakuzis11Institute of Physics, Federal University of Goias, Goiania 74690-900, GO, BrazilBiological Sciences Institute, Federal University of Goias, Goiania 74045-155, GO, BrazilInstitute of Physics, Federal University of Goias, Goiania 74690-900, GO, BrazilFarmaTec, School of Pharmacy, Federal University of Goias, Goiania 74690-631, GO, BrazilBiological Sciences Institute, Federal University of Goias, Goiania 74045-155, GO, BrazilBiological Sciences Institute, Federal University of Goias, Goiania 74045-155, GO, BrazilInstitute of Physics, Federal University of Goias, Goiania 74690-900, GO, BrazilFarmaTec, School of Pharmacy, Federal University of Goias, Goiania 74690-631, GO, BrazilBiological Sciences Institute, Federal University of Goias, Goiania 74045-155, GO, BrazilBiological Sciences Institute, Federal University of Goias, Goiania 74045-155, GO, BrazilInstitute of Physics, Federal University of Goias, Goiania 74690-900, GO, BrazilInstitute of Physics, Federal University of Goias, Goiania 74690-900, GO, BrazilInducing immunogenic cell death (ICD) during cancer therapy is a major challenge that might significantly improve patient survival. The purpose of this study was to develop a theranostic nanocarrier, capable both of conveying a cytotoxic thermal dose when mediating photothermal therapy (PTT) after its intravenous delivery, and of consequently inducing ICD, improving survival. The nanocarrier consists of red blood cell membranes (RBCm) embedding the near-infrared dye IR-780 (IR) and camouflaging Mn-ferrite nanoparticles (RBCm-IR-Mn). The RBCm-IR-Mn nanocarriers were characterized by size, morphology, surface charge, magnetic, photophysical, and photothermal properties. Their photothermal conversion efficiency was found to be size- and concentration-dependent. Late apoptosis was observed as the cell death mechanism for PTT. Calreticulin and HMGB1 protein levels increased for in vitro PTT with temperature around 55 °C (ablative regime) but not for 44 °C (hyperthermia), suggesting ICD elicitation under ablation. RBCm-IR-Mn were then intravenously administered in sarcoma S180-bearing Swiss mice, and in vivo ablative PTT was performed five days later. Tumor volumes were monitored for the subsequent 120 days. RBCm-IR-Mn-mediated PTT promoted tumor regression in 11/12 animals, with an overall survival rate of 85% (11/13). Our results demonstrate that the RBCm-IR-Mn nanocarriers are great candidates for PTT-induced cancer immunotherapy.https://www.mdpi.com/1999-4923/15/3/943thermal nanomedicinecancernear-infrared dyebiomimetic nanoparticlesS180 cells
spellingShingle Ailton Antonio Sousa-Junior
Francyelli Mello-Andrade
João Victor Ribeiro Rocha
Tácio Gonçalves Hayasaki
Juliana Santana de Curcio
Lívia do Carmo Silva
Ricardo Costa de Santana
Eliana Martins Lima
Cléver Gomes Cardoso
Elisângela de Paula Silveira-Lacerda
Sebastião Antonio Mendanha
Andris Figueiroa Bakuzis
Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model
Pharmaceutics
thermal nanomedicine
cancer
near-infrared dye
biomimetic nanoparticles
S180 cells
title Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model
title_full Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model
title_fullStr Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model
title_full_unstemmed Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model
title_short Immunogenic Cell Death Photothermally Mediated by Erythrocyte Membrane-Coated Magnetofluorescent Nanocarriers Improves Survival in Sarcoma Model
title_sort immunogenic cell death photothermally mediated by erythrocyte membrane coated magnetofluorescent nanocarriers improves survival in sarcoma model
topic thermal nanomedicine
cancer
near-infrared dye
biomimetic nanoparticles
S180 cells
url https://www.mdpi.com/1999-4923/15/3/943
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