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      Minimally invasive injection of biomimetic Nano@Microgel for in situ ovarian cancer treatment through enhanced photodynamic reactions and photothermal combined therapy

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          Abstract

          Photodynamic therapy (PDT) induces immunogenic cell death (ICD) by producing reactive oxygen species (ROS), making it an ideal method for cancer treatment. However, the extremely lower level of oxygen, short half-life of produced ROS, and limited photosensitizers accumulating in the tumor site via intravenous administration are the main reasons that limit the further application of PDT. To address these issues, we loaded the photosensitizer porphine (THPP) into biomimetic gold nanorod-mesoporous silica core-shell nanoparticles (Au-MSN NPs) to prepare Au@MSN/THPP@CM NPs. We then seeded the NPs together with catalase (CAT) into a gelatin methacryloyl (GelMA) microgel matrix to form Au@MSN-Ter/THPP@CM@GelMA/CAT microspheres consisting of biomimetic nano@microgel. The NPs and biomimetic nano@microgel exhibited enhanced photodynamic (PD) reaction and excellent photothermal conversion ability. Moreover, we further conjugated an endoplasmic reticulum (ER) targeting ligand Tosyl Ethylenediamine (Ter) on the surface of Au-MSN NPs. The results showed that both Au@MSN-Ter/THPP@CM NPs and the finally formed Au@MSN-Ter/THPP@CM@GelMA/CAT biomimetic nano@microgel induced precise and prolonged ER stress through photodynamic reactions, which stimulated the exposure of the proapoptotic calreticulin (CRT) on the cell membrane and increased the release of high mobility group box 1 (HMGB1) form the nucleus in SKOV3 cells under near-infrared (NIR) laser irradiation. Additionally, a single dose of the nano@microgel delivered through minimally invasive injection generated a significant anti-tumor effect in the SKOV3 cell line-derived orthotopic ovarian cancer mouse model through a PD and PT combination therapy. This study offers a new strategy for enhanced PDT and provides a PD/PT synergistic treatment method for ovarian cancer.

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          Highlights

          • •

            An intratumorally injectable biomimetic nano@microgel for ovary cancer therapy is developed.

          • •

            The combination of enhanced photodynamic and photothermal therapy can be realized.

          • •

            The microgel exhibits sustained drug release and excellent tumor retention ability.

          • •

            The microgel can be used for ER targeted photosensitizer administration.

          • •

            The microgel can trigger ICD through enhanced photodynamic reactions.

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          Cancer Statistics, 2021

          Rebecca Siegel, Kimberly D Miller, Hannah Fuchs … (2021)
          Each year, the American Cancer Society estimates the numbers of new cancer cases and deaths in the United States and compiles the most recent data on population-based cancer occurrence. Incidence data (through 2017) were collected by the Surveillance, Epidemiology, and End Results Program; the National Program of Cancer Registries; and the North American Association of Central Cancer Registries. Mortality data (through 2018) were collected by the National Center for Health Statistics. In 2021, 1,898,160 new cancer cases and 608,570 cancer deaths are projected to occur in the United States. After increasing for most of the 20th century, the cancer death rate has fallen continuously from its peak in 1991 through 2018, for a total decline of 31%, because of reductions in smoking and improvements in early detection and treatment. This translates to 3.2 million fewer cancer deaths than would have occurred if peak rates had persisted. Long-term declines in mortality for the 4 leading cancers have halted for prostate cancer and slowed for breast and colorectal cancers, but accelerated for lung cancer, which accounted for almost one-half of the total mortality decline from 2014 to 2018. The pace of the annual decline in lung cancer mortality doubled from 3.1% during 2009 through 2013 to 5.5% during 2014 through 2018 in men, from 1.8% to 4.4% in women, and from 2.4% to 5% overall. This trend coincides with steady declines in incidence (2.2%-2.3%) but rapid gains in survival specifically for nonsmall cell lung cancer (NSCLC). For example, NSCLC 2-year relative survival increased from 34% for persons diagnosed during 2009 through 2010 to 42% during 2015 through 2016, including absolute increases of 5% to 6% for every stage of diagnosis; survival for small cell lung cancer remained at 14% to 15%. Improved treatment accelerated progress against lung cancer and drove a record drop in overall cancer mortality, despite slowing momentum for other common cancers.
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            Immunogenic cell death in cancer and infectious disease

            Lorenzo Galluzzi, Aitziber Buqué, Oliver Kepp … (2016)
            Initiation of an adaptive immune response depends on the detection of both antigenic epitopes and adjuvant signals. Infectious pathogens and cancer cells often avoid immune detection by limiting the release of danger signals from dying cells. When is cell death immunogenic and what are the pathophysiological implications of this process?
            Article 0 comments Cited 820 times – based on 0 reviews     Review now
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              Immunogenic cell death and DAMPs in cancer therapy.

              Dmitri V. Krysko, Abhishek D. Garg, Agnieszka Kaczmarek … (2012)
              Although it was thought that apoptotic cells, when rapidly phagocytosed, underwent a silent death that did not trigger an immune response, in recent years a new concept of immunogenic cell death (ICD) has emerged. The immunogenic characteristics of ICD are mainly mediated by damage-associated molecular patterns (DAMPs), which include surface-exposed calreticulin (CRT), secreted ATP and released high mobility group protein B1 (HMGB1). Most DAMPs can be recognized by pattern recognition receptors (PRRs). In this Review, we discuss the role of endoplasmic reticulum (ER) stress and reactive oxygen species (ROS) in regulating the immunogenicity of dying cancer cells and the effect of therapy-resistant cancer microevolution on ICD.
              Article 0 comments Cited 771 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Tingyan Shi
                Xian Shen
                Hongbo Zhang
                Journal
                Journal ID (nlm-ta): Mater Today Bio
                Journal ID (iso-abbrev): Mater Today Bio
                Title: Materials Today Bio
                Publisher: Elsevier
                ISSN (Electronic): 2590-0064
                Publication date PMC-release: 18 May 2023
                Publication date Collection: June 2023
                Publication date (Electronic): 18 May 2023
                Volume: 20
                Electronic Location Identifier: 100663
                Affiliations
                [a ]Joint Centre of Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China
                [b ]Department of General Surgery, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China
                [c ]Ovarian Cancer Program, Department of Gynecologic Oncology, Zhongshan Hospital, Fudan University, Shanghai, 200032, China
                [d ]Southern Medical University Affiliated Fengxian Hospital, Shanghai, 201499, China
                [e ]Pharmaceutical Sciences Laboratory, Åbo Akademi University, Turku, 20520, Finland
                [f ]Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, 20520, Finland
                [g ]Longgang District People's Hospital of Shenzhen, Shenzhen, 518172, China
                Author notes
                [∗ ]Corresponding author. Joint Centre of Translational Medicine, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China. hongbo.zhang@ 123456abo.fi
                [∗∗ ]Corresponding author. shenxian@ 123456wmu.edu.cn
                [∗∗∗ ]Corresponding author. shi.tingyan@ 123456zs-hospital.sh.cn
                [1]

                These authors contributed equally to this work.

                Article
                Publisher Item ID: S2590-0064(23)00123-0 Publisher ID: 100663
                DOI: 10.1016/j.mtbio.2023.100663
                PMC ID: 10232889
                SO-VID: 5ebe8f4b-41af-4029-8bdd-4f090ca1cfa8
                Copyright © © 2023 The Authors
                License:

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 19 January 2023
                Date revision received : 8 May 2023
                Date accepted : 10 May 2023
                Categories
                Subject: Full Length Article

                Keywords: gelatin methacryloyl,photodynamic treatment,photothermal treatment,immunogenic cell death,biomimetic nano@microgel
                Data availability:
                Keywords: gelatin methacryloyl, photodynamic treatment, photothermal treatment, immunogenic cell death, biomimetic nano@microgel

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