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      International Journal of Nanomedicine (submit here)

      This international, peer-reviewed Open Access journal by Dove Medical Press focuses on the application of nanotechnology in diagnostics, therapeutics, and drug delivery systems throughout the biomedical field. Sign up for email alerts here.

      105,621 Monthly downloads/views I 7.033 Impact Factor I 10.9 CiteScore I 1.22 Source Normalized Impact per Paper (SNIP) I 1.032 Scimago Journal & Country Rank (SJR)

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      Is Open Access

      Extracellular Vesicles from Akkermansia muciniphila Elicit Antitumor Immunity Against Prostate Cancer via Modulation of CD8 + T Cells and Macrophages

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          Abstract

          Purpose

          Prostate cancer (PCa) is one of the most common malignancies in males. Despite the success of immunotherapy in many malignant cancers, strategies are still needed to improve therapeutic efficacy in PCa. This study aimed to investigate the effects of Akkermansia muciniphila-derived extracellular vesicles ( Akk-EVs) on PCa and elucidate the underlying immune-related mechanism.

          Methods

          Akk-EVs were isolated by ultracentrifugation and intravenously injected to treat syngeneic PCa-bearing immune-competent mice. Immunophenotypic changes in immune cells, such as cytotoxic T lymphocytes and macrophages, were measured via flow cytometry analysis. Histological examination was used to detect morphological changes in major organs after Akk-EVs treatments. In vitro, flow cytometry was performed to confirm the effects of Akk-EVs on the activation of CD8 + T cells. Quantitative PCR and immunofluorescence staining were carried out to test the impact of Akk-EVs on macrophage polarization. Cell counting kit-8 (CCK-8) analysis, colony formation assays, and scratch wound healing assays were conducted to assess the effects of Akk-EVs-treated macrophages on the proliferation and invasion of PCa cells. CCK-8 assays also confirmed the impact of Akk-EVs on the viability of normal cells.

          Results

          Intravenous injection of Akk-EVs in immune-competent mice reduced the tumor burden of PCa without inducing obvious toxicity in normal tissues. This treatment elevated the proportion of granzyme B-positive (GZMB +) and interferon γ-positive (IFN-γ +) lymphocytes in CD8 + T cells and caused macrophage recruitment, with increased tumor-killing M1 macrophages and decreased immunosuppressive M2 macrophages. In vitro, Akk-EVs increased the number of GZMB +CD8 + and IFN-γ +CD8 + T cells and M1-like macrophages. In addition, conditioned medium from Akk-EVs-treated macrophages suppressed the proliferation and invasion of prostate cells. Furthermore, the effective dose of Akk-EVs was well-tolerated in normal cells.

          Conclusion

          Our study revealed the promising prospects of Akk-EVs as an efficient and biocompatible immunotherapeutic agent for PCa treatment.

          Most cited references65

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          Cancer statistics, 2020

          Rebecca Siegel, Kimberly D Miller, Ahmedin Jemal (2020)
          Each year, the American Cancer Society estimates the numbers of new cancer cases and deaths that will occur in the United States and compiles the most recent data on population-based cancer occurrence. Incidence data (through 2016) 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 2017) were collected by the National Center for Health Statistics. In 2020, 1,806,590 new cancer cases and 606,520 cancer deaths are projected to occur in the United States. The cancer death rate rose until 1991, then fell continuously through 2017, resulting in an overall decline of 29% that translates into an estimated 2.9 million fewer cancer deaths than would have occurred if peak rates had persisted. This progress is driven by long-term declines in death rates for the 4 leading cancers (lung, colorectal, breast, prostate); however, over the past decade (2008-2017), reductions slowed for female breast and colorectal cancers, and halted for prostate cancer. In contrast, declines accelerated for lung cancer, from 3% annually during 2008 through 2013 to 5% during 2013 through 2017 in men and from 2% to almost 4% in women, spurring the largest ever single-year drop in overall cancer mortality of 2.2% from 2016 to 2017. Yet lung cancer still caused more deaths in 2017 than breast, prostate, colorectal, and brain cancers combined. Recent mortality declines were also dramatic for melanoma of the skin in the wake of US Food and Drug Administration approval of new therapies for metastatic disease, escalating to 7% annually during 2013 through 2017 from 1% during 2006 through 2010 in men and women aged 50 to 64 years and from 2% to 3% in those aged 20 to 49 years; annual declines of 5% to 6% in individuals aged 65 years and older are particularly striking because rates in this age group were increasing prior to 2013. It is also notable that long-term rapid increases in liver cancer mortality have attenuated in women and stabilized in men. In summary, slowing momentum for some cancers amenable to early detection is juxtaposed with notable gains for other common cancers.
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            Microenvironmental regulation of tumor progression and metastasis.

            Daniela F Quail, Johanna A Joyce (2013)
            Cancers develop in complex tissue environments, which they depend on for sustained growth, invasion and metastasis. Unlike tumor cells, stromal cell types within the tumor microenvironment (TME) are genetically stable and thus represent an attractive therapeutic target with reduced risk of resistance and tumor recurrence. However, specifically disrupting the pro-tumorigenic TME is a challenging undertaking, as the TME has diverse capacities to induce both beneficial and adverse consequences for tumorigenesis. Furthermore, many studies have shown that the microenvironment is capable of normalizing tumor cells, suggesting that re-education of stromal cells, rather than targeted ablation per se, may be an effective strategy for treating cancer. Here we discuss the paradoxical roles of the TME during specific stages of cancer progression and metastasis, as well as recent therapeutic attempts to re-educate stromal cells within the TME to have anti-tumorigenic effects.
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              Understanding the tumor immune microenvironment (TIME) for effective therapy

              Weiping Zou, T. Kevin Howcroft, Elisa C Woodhouse … (2018)
              The clinical successes in immunotherapy have been both astounding and at the same time unsatisfactory. Countless patients with varied tumor types have seen pronounced clinical response with immunotherapeutic intervention; however, many more patients have experienced minimal or no clinical benefit when provided the same treatment. As technology has advanced, so has the understanding of the complexity and diversity of the immune context of the tumor microenvironment and its influence on response to therapy. It has been possible to identify different subclasses of immune environment that have an influence on tumor initiation and response and therapy; by parsing the unique classes and subclasses of tumor immune microenvironment (TIME) that exist within a patient’s tumor, the ability to predict and guide immunotherapeutic responsiveness will improve, and new therapeutic targets will be revealed.
              Article 0 comments Cited 1878 times – based on 0 reviews     Review now
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                Author and article information

                Journal
                Journal ID (nlm-ta): Int J Nanomedicine
                Journal ID (iso-abbrev): Int J Nanomedicine
                Journal ID (publisher-id): ijn
                Journal ID (pmc): intjnano
                Title: International Journal of Nanomedicine
                Publisher: Dove
                ISSN (Print): 1176-9114
                ISSN (Electronic): 1178-2013
                Publication date (Electronic): 20 April 2021
                Publication date Collection: 2021
                Volume: 16
                Pages: 2949-2963
                Affiliations
                [1 ]Department of Orthopedics, Xiangya Hospital, Central South University , Changsha, Hunan, People’s Republic of China
                [2 ]Movement System Injury and Repair Research Center, Xiangya Hospital, Central South University , Changsha, Hunan, People’s Republic of China
                [3 ]Xiangya Nursing School, Central South University , Changsha, Hunan, People’s Republic of China
                [4 ]Department of Urology, The Second Xiangya Hospital, Central South University , Changsha, Hunan, People’s Republic of China
                [5 ]Department of Sports Medicine, Xiangya Hospital, Central South University , Changsha, Hunan, People’s Republic of China
                [6 ]Hunan Key Laboratory of Organ Injury, Aging and Regenerative Medicine , Changsha, Hunan, People’s Republic of China
                [7 ]Hunan Key Laboratory of Bone Joint Degeneration and Injury , Changsha, Hunan, People’s Republic of China
                [8 ]National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University , Changsha, Hunan, People’s Republic of China
                Author notes
                Correspondence: Hui Xie Department of Orthopedics, Xiangya Hospital, Central South University , 87 Xiangya Road, Changsha, Hunan, 410008, People’s Republic of China Email huixie@csu.edu.cn
                Ran Xu Department of Urology, The Second Xiangya Hospital, Central South University , 139 Middle Renmin Road, Changsha, Hunan, 410011, People’s Republic of China Email xuran@csu.edu.cn
                Author information
                http://orcid.org/0000-0002-9626-1664
                http://orcid.org/0000-0003-1058-7717
                http://orcid.org/0000-0003-1387-6696
                http://orcid.org/0000-0002-8526-2637
                Article
                Publisher ID: 304515
                DOI: 10.2147/IJN.S304515
                PMC ID: 8068512
                PubMed ID: 33907401
                SO-VID: 7a4e132a-3cae-4011-9ed1-529078227574
                Copyright © © 2021 Luo et al.
                License:

                This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License ( http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms ( https://www.dovepress.com/terms.php).

                History
                Date received : 29 January 2021
                Date accepted : 15 March 2021
                Page count
                Figures: 5, References: 65, Pages: 15
                Categories
                Subject: Original Research

                ScienceOpen disciplines: Molecular medicine
                Keywords: akkermansia muciniphila,extracellular vesicles,immunotherapy,prostate cancer,cytotoxic t lymphocytes,macrophages
                Data availability:
                ScienceOpen disciplines: Molecular medicine
                Keywords: akkermansia muciniphila, extracellular vesicles, immunotherapy, prostate cancer, cytotoxic t lymphocytes, macrophages

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