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Reversible Photothermal Modulation of Electrical Activity of Excitable Cells using Polydopamine Nanoparticles.

ABSTRACT: Advances in the design and synthesis of nanomaterials with desired biophysicochemical properties can be harnessed to develop non-invasive neuromodulation technologies. Here, the reversible modulation of the electrical activity of neurons and cardiomyocytes is demonstrated using polydopamine (PDA) nanoparticles as photothermal nanotransducers. In addition to their broad light absorption and excellent photothermal activity, PDA nanoparticles are highly biocompatible and biodegradable, making them excellent candidates for both in vitro and in vivo applications. The modulation of the activity (i.e., spike rate of the neurons and beating rate of cardiomyocytes) of excitable cells can be finely controlled by varying the excitation power density and irradiation duration. Under optimal conditions, reversible suppression (≈100%) of neural activity and reversible enhancement (two-fold) in the beating rate of cardiomyocytes is demonstrated. To improve the ease of interfacing of photothermal transducers with these excitable cells and enable spatial localization of the photothermal stimulus, a collagen/PDA nanoparticle foam is realized, which can be used as an "add-on patch" for photothermal stimulation. The non-genetic optical neuromodulation approach using biocompatible and biodegradable nanoparticles represents a minimally invasive method for controlling the activity of excitable cells with potential applications in nano-neuroscience and engineering.

SUBMITTER: Gholami Derami H

PROVIDER: S-EPMC8363531 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Reversible Photothermal Modulation of Electrical Activity of Excitable Cells using Polydopamine Nanoparticles.

Gholami Derami Hamed H Gupta Prashant P Weng Kuo-Chan KC Seth Anushree A Gupta Rohit R Silva Jonathan R JR Raman Baranidharan B Singamaneni Srikanth S

Advanced materials (Deerfield Beach, Fla.) 20210703 32

Advances in the design and synthesis of nanomaterials with desired biophysicochemical properties can be harnessed to develop non-invasive neuromodulation technologies. Here, the reversible modulation of the electrical activity of neurons and cardiomyocytes is demonstrated using polydopamine (PDA) nanoparticles as photothermal nanotransducers. In addition to their broad light absorption and excellent photothermal activity, PDA nanoparticles are highly biocompatible and biodegradable, making them ...[more]

PMID: 34216406

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Project description:Photothermal therapy (PTT) can be an effective antitumor therapy, but it may not completely eliminate tumor cells, leading to the risk of recurrence or metastasis. Here we describe nanocarriers that allow combination therapy involving PTT and immunotherapy. Nanocarriers are prepared by coating Al2O3 nanoparticles with non-toxic, biodegradable polydopamine, which shows high photothermal efficiency. A near-infrared laser irradiation can kill the majority of tumor tissues, resulting in the release of tumor-associated antigens. The Al2O3 within the nanoparticles, together with CpG, acts as an adjuvant to trigger robust cell-mediated immune responses that can help eliminate the residual tumor cells and reduce the risk of tumor recurrence. Methods: The characteristics and photothermal performance of polydopamine-coated Al2O3 nanoparticles were examined after one-step preparation. Then we studied their internalization, photothermal toxicity and immunostimulatory activity in vitro. For in vivo experiments, these nanocarriers were injected directly into B16F10 melanoma allografts in mice to ensure specific localization. After photothermal irradiation on day 0, mice were subcutaneously injected with CpG adjuvant on day 1, 3 and 5. Tumor volumes and number of living mice were recorded every two days. Moreover, various immune responses induced by our combined therapy were tested for mechanism research. Results: 50% of mice after our combined treatment successfully achieved the goal of tumor eradication, and survived for 120 days, which was the end point of the experiment. Mechanism studies demonstrated the combined therapy efficiently led to dendritic cell maturation, resulting in the secretion of antibodies and cytokines as well as the proliferation of splenocytes and lymphocytes for anti-tumor immunotherapy. Conclusion: Taken together, these results demonstrated the promise of our combined photothermal therapy and immunotherapy for tumor shrinkage, which merited further research.

Project description:BackgroundAdoptive T cell therapy (ATCT) has been successful in treating hematological malignancies and is currently under investigation for solid-tumor therapy. In contrast to existing chimeric antigen receptor (CAR) T cell and/or antigen-specific T cell approaches, which require known targets, and responsive to the need for targeting a broad repertoire of antigens in solid tumors, we describe the first use of immunostimulatory photothermal nanoparticles to generate tumor-specific T cells.MethodsSpecifically, we subject whole tumor cells to Prussian blue nanoparticle-based photothermal therapy (PBNP-PTT) before culturing with dendritic cells (DCs), and subsequent stimulation of T cells. This strategy differs from previous approaches using tumor cell lysates because we use nanoparticles to mediate thermal and immunogenic cell death in tumor cells, rendering them enhanced antigen sources.ResultsIn proof-of-concept studies using two glioblastoma (GBM) tumor cell lines, we first demonstrated that when PBNP-PTT was administered at a "thermal dose" targeted to induce the immunogenicity of U87 GBM cells, we effectively expanded U87-specific T cells. Further, we found that DCs cultured ex vivo with PBNP-PTT-treated U87 cells enabled 9- to 30-fold expansion of CD4+ and CD8+ T cells. Upon co-culture with target U87 cells, these T cells secreted interferon-ɣ in a tumor-specific and dose-dependent manner (up to 647-fold over controls). Furthermore, T cells manufactured using PBNP-PTT ex vivo expansion elicited specific cytolytic activity against target U87 cells (donor-dependent 32-93% killing at an effector to target cell (E:T) ratio of 20:1) while sparing normal human astrocytes and peripheral blood mononuclear cells from the same donors. In contrast, T cells generated using U87 cell lysates expanded only 6- to 24-fold and killed 2- to 3-fold less U87 target cells at matched E:T ratios compared with T cell products expanded using the PBNP-PTT approach. These results were reproducible even when a different GBM cell line (SNB19) was used, wherein the PBNP-PTT-mediated approach resulted in a 7- to 39-fold expansion of T cells, which elicited 25-66% killing of the SNB19 cells at an E:T ratio of 20:1, depending on the donor.ConclusionsThese findings provide proof-of-concept data supporting the use of PBNP-PTT to stimulate and expand tumor-specific T cells ex vivo for potential use as an adoptive T cell therapy approach for the treatment of patients with solid tumors.

Dataset Information

Reversible Photothermal Modulation of Electrical Activity of Excitable Cells using Polydopamine Nanoparticles.

Publications

Reversible Photothermal Modulation of Electrical Activity of Excitable Cells using Polydopamine Nanoparticles.

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