Rationale Radiation therapy is widely used for cancer treatment but its efficacy is limited by radioresistance and by damages caused to adjacent normal tissues. Active research aims at maximizing tumor eradication while reducing side-effects with theranostic nanoparticles that act as radioenhancers in situ. Ferromagnetic materials have been identified as promising nanotools for image-guided radiotherapy. Here, we investigated the potential of RGD-tagged magnetosomes (magnetosomes@RGD), bacterial biogenic magnetic nanoparticles naturally coated by a biological membrane and genetically engineered to express a RGD peptide, as tumour enhancers to conventional radiotherapy and proton therapy. Methods The potential of native and RGD-functionalized magnetosomes to enhance the effects of ionizing radiations was assessed in a DNA fragmentation assay and in melanoma and colorectal cancer cells using in vitro clonogenic assays. The in vivo radiotherapy enhancement efficacy of the magnetosomes@RGD was explored in preclinical models of melanoma-bearing mice treated with either X-rays or protons. Results Native and RGD-tagged magnetosomes similarly enhanced radiation-induced DNA damage. On cancer cells, both magnetoprobes were able to boost the killing efficacy of radiotherapy, although to a much larger extent with the magnetosomes@RGD enhancing the mortality by 2.5 fold in melanoma cells and by 2.9 fold in colorectal cancer cells. In vivo treatment of melanomabearing mice with magnetosomes@RGD prior to X-rays led to a 65% reduction in tumor development compared to radiotherapy alone (31%). Comparatively, a more effective tumor 3 growth inhibition (77%) was observed in combining RGD-decorated nanoprobes to proton therapy. The radioenhancing potential of magnetosomes@RGD was further evidenced by the DNA damage observed in the nanoscale vicinity of magnetosomes within the treated lesions. Conclusions Our results show efficacy of magnetosomes functionalized with a RGD peptide as tumor radioenhancers to both X-rays and protons in vivo and strengthen the interest of developing biogenic magnetoparticles for multimodal nanomedicine for cancer therapy.
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