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Tumor-derived extracellular vesicles: reliable tools for Cancer diagnosis and clinical applications

Reza Rahbarghazi, Nasrollah Jabbari, Neda Abbaspour Sani and 8 more

Cell Communication and Signaling · 2019 · Review · CC BY

doi:10.1186/s12964-019-0390-y

Abstract

Background. Studies have recently revealed that almost every type of cells including tumor cells abundantly release small vesicles known as extracellular vesicles (EVs) into the extracellular milieu. EVs carry a repertoire of biological molecules including nucleic acids, proteins, lipids, and carbohydrates and transport their cargo between cells in the vicinity as well as distantly located cells and hence act as messengers of intercellular communication. In this review, we aimed to discuss the tumor-derived exosome biology and the pivotal roles of exosomes in cancer diagnosis and treatment.

Methods. In the present review study, the authors studied several articles over the past two decades published on the kinetics of EVs in tumor environment as well as on the application of these vesicles in cancer diagnosis and therapy.

Results. A growing body of evidence indicates that nucleic acids such as microRNAs (miRNAs) transferring by EVs participate to create a conducive tumor environment. As EV-associated miRNAs are tissue-specific and present in most biological fluids, they hold great potential for clinical application in cancer early diagnosis, prognosis, and treatment response. Furthermore, exosomes can serve as drug delivery vehicles transferring miRNAs as well as therapeutic agents to target cells. These nano-vesicles exhibit ideal properties in comparison with the synthetic carriers that attracted scientist’s attention in the field of nanotechnology medicine. Scientists have employed different strategies to build exosomes-based drug delivery system. In general, two methods (direct engineering and indirect engineering) are being utilized to produce artificial exosomes. Para-clinical data have confirmed the beneficial effects of engineering exosomes in cancer therapy.

Conclusion. Exosomal miRNAs hold great promise for clinical application in early diagnosis and treatment of cancers. In addition, in spite of enthusiastic results obtained by engineered exosomes, however, there is an increasing concern over the use of optimal methods for engineering exosomes and the safety of engineered exosomes in clinical trials is still unclear.

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    Rupp A-K, Rupp C, Keller S, Brase JC, Ehehalt R, Fogel M, Moldenhauer G, Marmé F, Sültmann H, Altevogt P. Loss of EpCAM expression in breast cancer derived serum exosomes: role of proteolytic cleavage. Gynecol Oncol. 2011;122:437-446.

    Not in our library10.1016/j.ygyno.2011.04.035

  94. 94.

    He Y, Deng F, Yang S, Wang D, Chen X, Zhong S, Zhao J, Tang J. Exosomal microRNA: a novel biomarker for breast cancer. Biomark Med. 2018;12:177-188.

    Not in our library10.2217/bmm-2017-0305

  95. 95.
    Increased Exosomal MicroRNA-21 and MicroRNA-146a Levels in the Cervicovaginal Lavage Specimens of Patients with Cervical Cancer · 2014
    No notice
  96. 96.
    Circulating Exosomal microRNAs as Biomarkers of Colon Cancer · 2014
    No notice
  97. 97.
    Exosomes secreted from human colorectal cancer cell lines contain mRNAs, microRNAs and natural antisense RNAs, that can transfer into the human hepatoma HepG2 and lung cancer A549 cell lines · 2012
    No notice
  98. 98.

    Tanaka Y, Kamohara H, Kinoshita K, Kurashige J, Ishimoto T, Iwatsuki M, Watanabe M, Baba H. Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma. Cancer. 2013;119:1159-1167.

    Not in our library10.1002/cncr.27895

  99. 99.

    Manterola L, Guruceaga E, Pérez-Larraya JG, González-Huarriz M, Jauregui P, Tejada S, Diez-Valle R, Segura V, Samprón N, Barrena C. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro-Oncology. 2014;16:520-527.

    Not in our library10.1093/neuonc/not218

  100. 100.
    Exosomal levels of miRNA-21 from cerebrospinal fluids associated with poor prognosis and tumor recurrence of glioma patients · 2015
    No notice
  101. 101.

    Molina-Pinelo S, Suárez R, Pastor MD, Nogal A, Márquez-Martín E, Martín-Juan J, Carnero A, Paz-Ares L. Association between the miRNA signatures in plasma and bronchoalveolar fluid in respiratory pathologies. Dis Markers. 2012;32:221-230.

    Not in our library10.1155/2012/873749

  102. 102.

    Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110:13-21.

    Not in our library10.1016/j.ygyno.2008.04.033

  103. 103.

    Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009;10:42-46.

    Not in our library10.3816/clc.2009.n.006

  104. 104.
    Molecular characterization of exosome-like vesicles from breast cancer cells · 2014
    No notice
  105. 105.
    Increased serum levels of circulating exosomal microRNA-373 in receptor-negative breast cancer patients · 2014
    No notice
  106. 106.

    Matsumura T, Sugimachi K, Iinuma H, Takahashi Y, Kurashige J, Sawada G, Ueda M, Uchi R, Ueo H, Takano Y. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br J Cancer. 2015;113:275.

    Not in our library10.1038/bjc.2015.201

  107. 107.

    Samsonov R, Shtam T, Burdakov V, Glotov A, Tsyrlina E, Berstein L, Nosov A, Evtushenko V, Filatov M, Malek A. Lectin-induced agglutination method of urinary exosomes isolation followed by mi-RNA analysis: application for prostate cancer diagnostic. Prostate. 2016;76:68-79.

    Not in our library10.1002/pros.23101

  108. 108.

    Kumar MS, Erkeland SJ, Pester RE, Chen CY, Ebert MS, Sharp PA, Jacks T. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci U S A. 2008;105:3903-3908.

    Not in our library10.1073/pnas.0712321105

  109. 109.

    Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012;119:756-766.

    Not in our library10.1182/blood-2011-02-338004

  110. 110.

    Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133-144.

    Not in our library10.1016/j.molcel.2010.06.010

  111. 111.

    Yu B, Kim HW, Gong M, Wang J, Millard RW, Wang Y, Ashraf M, Xu M. Exosomes secreted from GATA-4 overexpressing mesenchymal stem cells serve as a reservoir of anti-apoptotic microRNAs for cardioprotection. Int J Cardiol. 2015;182:349-360.

    Not in our library10.1016/j.ijcard.2014.12.043

  112. 112.

    S-i O, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013;21:185-191.

    Not in our library10.1038/mt.2012.180

  113. 113.

    Kosaka N, Takeshita F, Yoshioka Y, Hagiwara K, Katsuda T, Ono M, Ochiya T. Exosomal tumor-suppressive microRNAs as novel cancer therapy:“exocure” is another choice for cancer treatment. Adv Drug Deliv Rev. 2013;65:376-382.

    Not in our library10.1016/j.addr.2012.07.011

  114. 114.
    Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma · 2015
    No notice
  115. 115.

    Didiot M-C, Hall LM, Coles AH, Haraszti RA, Godinho BM, Chase K, Sapp E, Ly S, Alterman JF, Hassler MR. Exosome-mediated delivery of hydrophobically modified siRNA for huntingtin mRNA silencing. Mol Ther. 2016;24:1836-1847.

    Not in our library10.1038/mt.2016.126

  116. 116.

    Mukherjee B. Editorial (thematic issue:“Nanosize drug delivery system”). Curr Pharm Biotechnol. 2013;14:1221.

    Not in our library10.2174/138920101415140804121008

  117. 117.

    Leonard R, Williams S, Tulpule A, Levine A, Oliveros S. Improving the therapeutic index of anthracycline chemotherapy: focus on liposomal doxorubicin (Myocet™). Breast. 2009;18:218-224.

    Not in our library10.1016/j.breast.2009.05.004

  118. 118.

    Petrelli F, Borgonovo K, Barni S. Targeted delivery for breast cancer therapy: the history of nanoparticle-albumin-bound paclitaxel. Expert Opin Pharmacother. 2010;11:1413-1432.

    Not in our library10.1517/14656561003796562

  119. 119.

    Kanada M, Bachmann MH, Hardy JW, Frimannson DO, Bronsart L, Wang A, Sylvester MD, Schmidt TL, Kaspar RL, Butte MJ. Differential fates of biomolecules delivered to target cells via extracellular vesicles. Proc Natl Acad Sci U. S A. 2015;112:E1433-E1442.

    Not in our library10.1073/pnas.1418401112

  120. 120.

    Royo F, Falcon-Perez JM. Liver extracellular vesicles in health and disease. J Extracell Vesicles. 2012;1:18825.

    Not in our library10.3402/jev.v1i0.18825

  121. 121.

    Drommelschmidt K, Serdar M, Bendix I, Herz J, Bertling F, Prager S, Keller M, Ludwig A-K, Duhan V, Radtke S. Mesenchymal stem cell-derived extracellular vesicles ameliorate inflammation-induced preterm brain injury. Brain Behav Immun. 2017;60:220-232.

    Not in our library10.1016/j.bbi.2016.11.011

  122. 122.
    Mesenchymal Stromal Cell‐Derived Extracellular Vesicles Protect the Fetal Brain After Hypoxia‐Ischemia · 2016
    Not checked
  123. 123.

    Xitong D, Xiaorong Z. Targeted therapeutic delivery using engineered exosomes and its applications in cardiovascular diseases. Gene. 2016;575:377-384.

    Not in our library10.1016/j.gene.2015.08.067

  124. 124.

    Rupert DL, Claudio V, Lässer C, Bally M. Methods for the physical characterization and quantification of extracellular vesicles in biological samples. Biochim Biophys Acta Gen Subj. 1861;2017:3164-3179.

    Not in our library10.1016/j.bbagen.2016.07.028

  125. 125.

    Zhuang X, Xiang X, Grizzle W, Sun D, Zhang S, Axtell RC, Ju S, Mu J, Zhang L, Steinman L. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther. 2011;19:1769-1779.

    Not in our library10.1038/mt.2011.164

  126. 126.

    Sun D, Zhuang X, Xiang X, Liu Y, Zhang S, Liu C, Barnes S, Grizzle W, Miller D, Zhang H-G. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther. 2010;18:1606-1614.

    Not in our library10.1038/mt.2010.105

  127. 127.

    Fuhrmann G, Serio A, Mazo M, Nair R, Stevens MM. Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins. J Control Release. 2015;205:35-44.

    Not in our library10.1016/j.jconrel.2014.11.029

  128. 128.

    Kim MS, Haney MJ, Zhao Y, Mahajan V, Deygen I, Klyachko NL, Inskoe E, Piroyan A, Sokolsky M, Okolie O. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine. 2016;12:655-664.

    Not in our library10.1016/j.nano.2015.10.012

  129. 129.

    Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011;29:341.

    Not in our library10.1038/nbt.1807

  130. 130.
    Exosomes are natural carriers of exogenous siRNA to human cells in vitro · 2013
    No notice
  131. 131.

    Wahlgren J, Karlson TDL, Brisslert M, Vaziri Sani F, Telemo E, Sunnerhagen P, Valadi H. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res. 2012;40:e130.

    Not in our library10.1093/nar/gks463

  132. 132.

    Lamichhane TN, Jeyaram A, Patel DB, Parajuli B, Livingston NK, Arumugasaamy N, Schardt JS, Jay SM. Oncogene knockdown via active loading of small RNAs into extracellular vesicles by sonication. Cell Mol Bioeng. 2016;9:315-324.

    Not in our library10.1007/s12195-016-0457-4

  133. 133.

    Lamichhane TN, Raiker RS, Jay SM. Exogenous DNA loading into extracellular vesicles via electroporation is size-dependent and enables limited gene delivery. Mol Pharm. 2015;12:3650-3657.

    Not in our library10.1021/acs.molpharmaceut.5b00364

  134. 134.

    Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, Patel T, Piroyan A, Sokolsky M, Kabanov AV. Exosomes as drug delivery vehicles for Parkinson's disease therapy. J Control Release. 2015;207:18-30.

    Not in our library10.1016/j.jconrel.2015.03.033

  135. 135.
    Combined treatment with a pH-sensitive fusogenic peptide and cationic lipids achieves enhanced cytosolic delivery of exosomes · 2015
    No notice
  136. 136.

    Lv L-H, Wan Y-L, Lin Y, Zhang W, Yang M, Li G-L, Lin H-M, Shang C-Z, Chen Y-J, Min J. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem. 2012;287:15874-15885.

    Not in our library10.1074/jbc.m112.340588

  137. 137.

    Pascucci L, Coccè V, Bonomi A, Ami D, Ceccarelli P, Ciusani E, Viganò L, Locatelli A, Sisto F, Doglia SM. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: a new approach for drug delivery. J Control mRelease. 2014;192:262-270.

    Not in our library10.1016/j.jconrel.2014.07.042

  138. 138.

    Lee J, Kim J, Jeong M, Lee H, Goh U, Kim H, Kim B, Park J-H. Liposome-based engineering of cells to package hydrophobic compounds in membrane vesicles for tumor penetration. Nano Lett. 2015;15:2938-2944.

    Not in our library10.1021/nl5047494

  139. 139.

    Lee J, Lee H, Goh U, Kim J, Jeong M, Lee J, Park J-H. Cellular engineering with membrane fusogenic liposomes to produce functionalized extracellular vesicles. ACS Appl Mater Interfaces. 2016;8:6790-6795.

    Not in our library10.1021/acsami.6b01315

  140. 140.
    Targeted exosome-mediated delivery of opioid receptor Mu siRNA for the treatment of morphine relapse · 2015
    No notice
  141. 141.

    Gnecchi M, He H, Noiseux N, Liang OD, Zhang L, Morello F, Mu H, Melo LG, Pratt RE, Ingwall JS. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J. 2006;20:661-669.

    Not in our library10.1096/fj.05-5211com

  142. 142.

    Sheldon H, Heikamp E, Turley H, Dragovic R, Thomas P, Oon CE, Leek R, Edelmann M, Kessler B, Sainson RC. New mechanism for notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood. 2010;116:2385-2394.

    Not in our library10.1182/blood-2009-08-239228

  143. 143.

    Mackie AR, Klyachko E, Thorne T, Schultz KM, Millay M, Ito A, Kamide CE, Liu T, Gupta R, Sahoo S. Sonic hedgehog–modified human CD34+ cells preserve cardiac function after acute myocardial infarction. Circ Res. 2012;111:312-321.

    Not in our library10.1161/circresaha.112.266015

  144. 144.

    Bianco NR, Kim SH, Ruffner MA, Robbins PD. Therapeutic effect of exosomes from indoleamine 2, 3-dioxygenase–positive dendritic cells in collagen-induced arthritis and delayed-type hypersensitivity disease models. Arthritis Rheumatol. 2009;60:380-389.

    Not in our library10.1002/art.24229

  145. 145.

    Akao Y, Nakagawa Y, Hirata I, Iio A, Itoh T, Kojima K, Nakashima R, Kitade Y, Naoe T. Role of anti-oncomirs miR-143 and-145 in human colorectal tumors. Cancer Gene Ther. 2010;17:398.

    Not in our library10.1038/cgt.2009.88

  146. 146.
    Exosomal Signaling during Hypoxia Mediates Microvascular Endothelial Cell Migration and Vasculogenesis · 2013
    No notice
  147. 147.

    Tadokoro H, Umezu T, Ohyashiki K, Hirano T, Ohyashiki JH. Exosomes derived from hypoxic leukemia cells enhance tube formation in endothelial cells. J Biol Chem. 2013;288:34343-34351.

    Not in our library10.1074/jbc.m113.480822

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