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      Exosome-derived microRNAs in cancer metabolism: possible implications in cancer diagnostics and therapy

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          Abstract

          Malignant progression is greatly affected by dynamic cross-talk between stromal and cancer cells. Exosomes are secreted nanovesicles that have key roles in cell–cell communication by transferring nucleic acids and proteins to target cells and tissues. Recently, MicroRNAs (miRs) and their delivery in exosomes have been implicated in physiological and pathological processes. Tumor-delivered miRs, interacting with stromal cells in the tumor microenvironment, modulate tumor progression, angiogenesis, metastasis and immune escape. Altered cell metabolism is one of the hallmarks of cancer. A number of different types of tumor rely on mitochondrial metabolism by triggering adaptive mechanisms to optimize their oxidative phosphorylation in relation to their substrate supply and energy demands. Exogenous exosomes can induce metabolic reprogramming by restoring the respiration of cancer cells and supress tumor growth. The exosomal miRs involved in the modulation of cancer metabolism may be potentially utilized for better diagnostics and therapy.

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          Biogenesis and secretion of exosomes.

          Joanna Kowal, Mercedes Tkach, Clotilde Théry (2014)
          Although observed for several decades, the release of membrane-enclosed vesicles by cells into their surrounding environment has been the subject of increasing interest in the past few years, which led to the creation, in 2012, of a scientific society dedicated to the subject: the International Society for Extracellular Vesicles. Convincing evidence that vesicles allow exchange of complex information fuelled this rise in interest. But it has also become clear that different types of secreted vesicles co-exist, with different intracellular origins and modes of formation, and thus probably different compositions and functions. Exosomes are one sub-type of secreted vesicles. They form inside eukaryotic cells in multivesicular compartments, and are secreted when these compartments fuse with the plasma membrane. Interestingly, different families of molecules have been shown to allow intracellular formation of exosomes and their subsequent secretion, which suggests that even among exosomes different sub-types exist. Copyright © 2014 Elsevier Ltd. All rights reserved.
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            Exosomal microRNA: a diagnostic marker for lung cancer.

            Guilherme Rabinowits, Cicek Gercel-Taylor, Jamie Day … (2009)
            To date, there is no screening test for lung cancer shown to affect overall mortality. MicroRNAs (miRNAs) are a class of small noncoding RNA genes found to be abnormally expressed in several types of cancer, suggesting a role in the pathogenesis of human cancer. We evaluated the circulating levels of tumor exosomes, exosomal small RNA, and specific exosomal miRNAs in patients with and without lung adenocarcinoma, correlating the levels with the American Joint Committee on Cancer (AJCC) disease stage to validate it as an acceptable marker for diagnosis and prognosis in patients with adenocarcinoma of the lung. To date, 27 patients with lung adenocarcinoma AJCC stages I-IV and 9 controls, all aged 21-80 years, were enrolled in the study. Small RNA was detected in the circulating exosomes. The mean exosome concentration was 2.85 mg/mL (95% CI, 1.94-3.76) for the lung adenocarcinoma group versus 0.77 mg/mL (95% CI, 0.68-0.86) for the control group (P < .001). The mean miRNA concentration was 158.6 ng/mL (95% CI, 145.7-171.5) for the lung adenocarcinoma group versus 68.1 ng/mL (95% CI, 57.2-78.9) for the control group (P < .001). Comparisons between peripheral circulation miRNA-derived exosomes and miRNA-derived tumors indicated that the miRNA signatures were not significantly different. The significant difference in total exosome and miRNA levels between lung cancer patients and controls, and the similarity between the circulating exosomal miRNA and the tumor-derived miRNA patterns, suggest that circulating exosomal miRNA might be useful as a screening test for lung adenocarcinoma. No correlation between the exosomal miRNA levels and the stage of disease can be made at this point.
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              Targeting lactate metabolism for cancer therapeutics.

              Joanne R. Doherty, John L. Cleveland (2013)
              Lactate, once considered a waste product of glycolysis, has emerged as a critical regulator of cancer development, maintenance, and metastasis. Indeed, tumor lactate levels correlate with increased metastasis, tumor recurrence, and poor outcome. Lactate mediates cancer cell intrinsic effects on metabolism and has additional non-tumor cell autonomous effects that drive tumorigenesis. Tumor cells can metabolize lactate as an energy source and shuttle lactate to neighboring cancer cells, adjacent stroma, and vascular endothelial cells, which induces metabolic reprogramming. Lactate also plays roles in promoting tumor inflammation and in functioning as a signaling molecule that stimulates tumor angiogenesis. Here we review the mechanisms of lactate production and transport and highlight emerging evidence indicating that targeting lactate metabolism is a promising approach for cancer therapeutics.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Exp Mol Med
                Journal ID (iso-abbrev): Exp. Mol. Med
                Title: Experimental & Molecular Medicine
                Publisher: Nature Publishing Group
                ISSN (Print): 1226-3613
                ISSN (Electronic): 2092-6413
                Publication date (Print): January 2017
                Publication date (Electronic): 20 January 2017
                Publication date PMC-release: 1 January 2017
                Volume: 49
                Issue: 1
                Page: e285
                Affiliations
                [1 ]Department of Clinical and Molecular Sciences, Polytechnic University of Marche , Ancona, Italy
                [2 ]Department of Biochemistry, Dongguk University College of Medicine , Gyeongju, Korea
                [3 ]Mitochondria, Apoptosis and Cancer Research Group, School of Medical Science and Menzies Health Institute Queensland, Griffith University , Southport, Queensland, Australia
                [4 ]Molecular Therapy Group, Institute of Biotechnology, Czech Academy of Sciences , Prague-West, Czech Republic
                Author notes
                [* ]Department of Clinical and Molecular Sciences, Polytechnic University of Marche , via Tronto 10A, 60020 Ancona, Italy. E-mail: m.tomasetti@ 123456univpm.it
                [* ]Mitochondria, Apoptosis and Cancer Research Group, School of Medical Science and Menzies Health Institute Queensland, Griffith University , Southport, Queensland 4222, Australia. E-mail: j.neuzil@ 123456griffith.edu.au
                Article
                Publisher Item ID: emm2016153
                DOI: 10.1038/emm.2016.153
                PMC ID: 5291842
                PubMed ID: 28104913
                SO-VID: 30fe095b-4431-44f9-943c-34f9533ac1b1
                Copyright © Copyright © 2017 The Author(s)
                License:

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                Date received : 11 October 2016
                Date accepted : 24 October 2016
                Categories
                Subject: Review

                ScienceOpen disciplines: Molecular medicine
                Data availability:
                ScienceOpen disciplines: Molecular medicine

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