Exosomes: A rising star in breast cancer (Review)
- Authors:
- Lingxia Wang
- Bo Wang
- Huiyan Wen
- Jiahui Mao
- Yang Ren
- Huan Yang
-
Affiliations: Department of Clinical Laboratory, The Second Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215004, P.R. China, Department of Oncology, The Second Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215004, P.R. China, Department of Central Laboratory, The Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu 212000, P.R. China - Published online on: June 9, 2020 https://doi.org/10.3892/or.2020.7638
- Pages: 407-423
This article is mentioned in:
Abstract
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 136:E359–E386. 2015. View Article : Google Scholar : PubMed/NCBI | |
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2017. CA Cancer J Clin. 67:7–30. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sempere LF, Keto J and Fabbri M: Exosomal MicroRNAs in breast cancer towards diagnostic and therapeutic applications. Cancers (Basel). 9(pii): E712017. View Article : Google Scholar : PubMed/NCBI | |
Bardelli A and Pantel K: Liquid biopsies, what we do not know (Yet). Cancer Cell. 31:172–179. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kalra H, Drummen GP and Mathivanan S: Focus on extracellular vesicles: Introducing the next small big thing. Int J Mol Sci. 17:1702016. View Article : Google Scholar : PubMed/NCBI | |
Naseri Z, Oskuee RK, Jaafari MR and Forouzandeh Moghadam M: Exosome-mediated delivery of functionally active miRNA-142-3p inhibitor reduces tumorigenicity of breast cancer in vitro and in vivo. Int J Nanomedicine. 13:7727–7747. 2018. View Article : Google Scholar : PubMed/NCBI | |
Tkach M and Théry C: Communication by extracellular vesicles: Where we are and where we need to go. Cell. 164:1226–1232. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Shi H, Yuan X, Jiang P, Qian H and Xu W: Tumor-derived exosomes induce N2 polarization of neutrophils to promote gastric cancer cell migration. Mol Cancer. 17:1462018. View Article : Google Scholar : PubMed/NCBI | |
Jin Y, Chen K, Wang Z, Wang Y, Liu J, Lin L, Shao Y, Gao L, Yin H, Cui C, et al: DNA in serum extracellular vesicles is stable under different storage conditions. BMC Cancer. 16:7532016. View Article : Google Scholar : PubMed/NCBI | |
Li Q, Shao Y, Zhang X, Zheng T, Miao M, Qin L, Wang B, Ye G, Xiao B and Guo J: Plasma long noncoding RNA protected by exosomes as a potential stable biomarker for gastric cancer. Tumour Biol. 36:2007–2012. 2015. View Article : Google Scholar : PubMed/NCBI | |
Street JM, Koritzinsky EH, Glispie DM, Star RA and Yuen PS: Urine exosomes: An emerging trove of biomarkers. Adv Clin Chem. 78:103–122. 2017. View Article : Google Scholar : PubMed/NCBI | |
Nair S, Tang KD, Kenny L and Punyadeera C: Salivary exosomes as potential biomarkers in cancer. Oral Oncol. 84:31–40. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yang H, Fu H, Xu W and Zhang X: Exosomal non-coding RNAs: A promising cancer biomarker. Clin Chem Lab Med. 54:1871–1879. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Xu C, Hua Y, Sun L, Cheng K, Jia Z, Han Y, Dong J, Cui Y and Yang Z: Exosomes play an important role in the process of psoralen reverse multidrug resistance of breast cancer. J Exp Clin Cancer Res. 35:1862016. View Article : Google Scholar : PubMed/NCBI | |
Conte D, Verri C, Borzi C, Suatoni P, Pastorino U, Sozzi G and Fortunato O: Novel method to detect microRNAs using chip-based QuantStudio 3D digital PCR. BMC Genomics. 16:8492015. View Article : Google Scholar : PubMed/NCBI | |
Jeong S, Park J, Pathania D, Castro CM, Weissleder R and Lee H: Integrated magneto-electrochemical sensor for exosome analysis. ACS Nano. 10:1802–1809. 2016. View Article : Google Scholar : PubMed/NCBI | |
Singh CK, Kumar A and Roy SS: Quantitative analysis of the methane gas emissions from municipal solid waste in India. Sci Rep. 8:29132018. View Article : Google Scholar : PubMed/NCBI | |
Deng Z, Rong Y, Teng Y, Zhuang X, Samykutty A, Mu J, Zhang L, Cao P, Yan J, Miller D and Zhang HG: Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis. Oncogene. 36:639–651. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sebolt-Leopold JS and Herrera R: Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat Rev Cancer. 4:937–947. 2004. View Article : Google Scholar : PubMed/NCBI | |
Zhou R, Chen KK, Zhang J, Xiao B, Huang Z, Ju C, Sun J, Zhang F, Lv XB and Huang G: The decade of exosomal long RNA species: An emerging cancer antagonist. Mol Cancer. 17:752018. View Article : Google Scholar : PubMed/NCBI | |
Goldvaser H, Gutkin A, Beery E, Edel Y, Nordenberg J, Wolach O, Rabizadeh E, Uziel O and Lahav M: Characterisation of blood-derived exosomal hTERT mRNA secretion in cancer patients: A potential pan-cancer marker. Br J Cancer. 117:353–357. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, Yu Y, Chow A, O'Connor ST, Chin AR, et al: Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 25:501–515. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez M, Silva J, Herrera A, Herrera M, Peña C, Martín P, Gil-Calderón B, Larriba MJ, Coronado MJ, Soldevilla B, et al: Exosomes enriched in stemness/metastatic-related mRNAS promote oncogenic potential in breast cancer. Oncotarget. 6:40575–40587. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yan LX, Wu QN, Zhang Y, Li YY, Liao DZ, Hou JH, Fu J, Zeng MS, Yun JP, Wu QL, et al: Knockdown of miR-21 in human breast cancer cell lines inhibits proliferation, in vitro migration and in vivo tumor growth. Breast Cancer Res. 13:R22011. View Article : Google Scholar : PubMed/NCBI | |
Hannafon BN, Carpenter KJ, Berry WL, Janknecht R, Dooley WC and Ding WQ: Exosome-mediated microRNA signaling from breast cancer cells is altered by the anti-angiogenesis agent docosahexaenoic acid (DHA). Mol Cancer. 14:1332015. View Article : Google Scholar : PubMed/NCBI | |
Bi TL, Sun JJ, Tian YZ and Zhou YF: Research progress of relationship between exosomes and breast cancer. Sheng Li Xue Bao. 68:352–358. 2016.(In Chinese). PubMed/NCBI | |
Chen D, Sun Y, Yuan Y, Han Z, Zhang P, Zhang J, You MJ, Teruya-Feldstein J, Wang M, Gupta S, et al: miR-100 induces epithelial-mesenchymal transition but suppresses tumorigenesis, migration and invasion. PLoS Genet. 10:e10041772014. View Article : Google Scholar : PubMed/NCBI | |
Wang W, Yuan X, Xu A, Zhu X, Zhan Y, Wang S and Liu M: Human cancer cells suppress behaviors of endothelial progenitor cells through miR-21 targeting IL6R. Microvasc Res. 120:21–28. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chow A, Zhou W, Liu L, Fong MY, Champer J, Van Haute D, Chin AR, Ren X, Gugiu BG, Meng Z, et al: Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB. Sci Rep. 4:57502014. View Article : Google Scholar : PubMed/NCBI | |
Kong X, Zhang J, Li J, Shao J and Fang L: MiR-130a-3p inhibits migration and invasion by regulating RAB5B in human breast cancer stem cell-like cells. Biochem Biophys Res Commun. 501:486–493. 2018. View Article : Google Scholar : PubMed/NCBI | |
Clayton A and Tabi Z: Exosomes and the MICA-NKG2D system in cancer. Blood Cells Mol Dis. 34:206–213. 2005. View Article : Google Scholar : PubMed/NCBI | |
Vallabhaneni KC, Penfornis P, Dhule S, Guillonneau F, Adams KV, Mo YY, Xu R, Liu Y, Watabe K, Vemuri MC and Pochampally R: Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites. Oncotarget. 6:4953–4967. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhu S, Si ML, Wu H and Mo YY: MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem. 282:14328–14336. 2007. View Article : Google Scholar : PubMed/NCBI | |
Melo SA, Sugimoto H, O'Connell JT, Kato N, Villanueva A, Vidal A, Qiu L, Vitkin E, Perelman LT, Melo CA, et al: Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell. 26:707–721. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ma L, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682–688. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ochieng J, Pratap S, Khatua AK and Sakwe AM: Anchorage-independent growth of breast carcinoma cells is mediated by serum exosomes. Exp Cell Res. 315:1875–1888. 2009. View Article : Google Scholar : PubMed/NCBI | |
Brandes AA, Franceschi E, Tosoni A, Hegi ME and Stupp R: Epidermal growth factor receptor inhibitors in neuro-oncology: Hopes and disappointments. Clin Cancer Res. 14:957–960. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zhong S, Li W, Chen Z, Xu J and Zhao J: MiR-222 and miR-29a contribute to the drug-resistance of breast cancer cells. Gene. 531:8–14. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li X, Liu X, Xu W, Zhou P, Gao P, Jiang S, Lobie PE and Zhu T: c-MYC-regulated miR-23a/24-2/27a cluster promotes mammary carcinoma cell invasion and hepatic metastasis by targeting Sprouty2. J Biol Chem. 288:18121–18133. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li X, Wu Y, Liu A and Tang X: Long non-coding RNA UCA1 enhances tamoxifen resistance in breast cancer cells through a miR-18a-HIF1α feedback regulatory loop. Tumour Biol. 37:14733–14743. 2016. View Article : Google Scholar : PubMed/NCBI | |
Giglio S, Cirombella R, Amodeo R, Portaro L, Lavra L and Vecchione A: MicroRNA miR-24 promotes cell proliferation by targeting the CDKs inhibitors p27Kip1 and p16INK4a. J Cell Physiol. 228:2015–2023. 2013. View Article : Google Scholar : PubMed/NCBI | |
Chen WX, Cai YQ, Lv MM, Chen L, Zhong SL, Ma TF, Zhao JH and Tang JH: Exosomes from docetaxel-resistant breast cancer cells alter chemosensitivity by delivering microRNAs. Tumour Biol. 35:9649–9659. 2014. View Article : Google Scholar : PubMed/NCBI | |
He Y, Deng F, Yang S, Wang D, Chen X, Zhong S, Zhao J and Tang J: Exosomal microRNA: A novel biomarker for breast cancer. Biomark Med. 12:177–188. 2018. View Article : Google Scholar : PubMed/NCBI | |
Shen H, Li L, Yang S, Wang D, Zhong S, Zhao J and Tang J: MicroRNA-29a contributes to drug-resistance of breast cancer cells to adriamycin through PTEN/AKT/GSK3β signaling pathway. Gene. 593:84–90. 2016. View Article : Google Scholar : PubMed/NCBI | |
Xu CG, Yang MF, Ren YQ, Wu CH and Wang LQ: Exosomes mediated transfer of lncRNA UCA1 results in increased tamoxifen resistance in breast cancer cells. Eur Rev Med Pharmacol Sci. 20:4362–4368. 2016.PubMed/NCBI | |
Matula Z, Németh A, Lőrincz P, Szepesi Á, Brózik A, Buzás EI, Lőw P, Német K, Uher F and Urbán VS: The role of extracellular vesicle and tunneling nanotube-mediated intercellular cross-talk between mesenchymal stem cells and human peripheral T cells. Stem Cells Dev. 25:1818–1832. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ono M, Kosaka N, Tominaga N, Yoshioka Y, Takeshita F, Takahashi RU, Yoshida M, Tsuda H, Tamura K and Ochiya T: Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal. 7:ra632014. View Article : Google Scholar : PubMed/NCBI | |
Wei Y, Li M, Cui S, Wang D, Zhang CY, Zen K and Li L: Shikonin inhibits the proliferation of human breast cancer cells by reducing tumor-derived exosomes. Molecules. 21(pii): E7772016. View Article : Google Scholar : PubMed/NCBI | |
Gorczynski RM, Zhu F, Chen Z, Kos O and Khatri I: A comparison of serum miRNAs influencing metastatic growth of EMT6 vs 4THM tumor cells in wild-type and CD200R1KO mice. Breast Cancer Res Treat. 162:255–266. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wei Y, Lai X, Yu S, Chen S, Ma Y, Zhang Y, Li H, Zhu X, Yao L and Zhang J: Exosomal miR-221/222 enhances tamoxifen resistance in recipient ER-positive breast cancer cells. Breast Cancer Res Treat. 147:423–431. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Zhang S, Yao J, Lowery FJ, Zhang Q, Huang WC, Li P, Li M, Wang X, Zhang C, et al: Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 527:100–104. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bovy N, Blomme B, Frères P, Dederen S, Nivelles O, Lion M, Carnet O, Martial JA, Noël A, Thiry M, et al: Endothelial exosomes contribute to the antitumor response during breast cancer neoadjuvant chemotherapy via microRNA transfer. Oncotarget. 6:10253–10266. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA, Greco SJ, Bryan M, Patel PS and Rameshwar P: Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res. 71:1550–1560. 2011. View Article : Google Scholar : PubMed/NCBI | |
O'Brien K, Lowry MC, Corcoran C, Martinez VG, Daly M, Rani S, Gallagher WM, Radomski MW, MacLeod RA and O'Driscoll L: miR-134 in extracellular vesicles reduces triple-negative breast cancer aggression and increases drug sensitivity. Oncotarget. 6:32774–32789. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhang G, Zhang W, Li B, Stringer-Reasor E, Chu C, Sun L, Bae S, Chen D, Wei S, Jiao K, et al: MicroRNA-200c and microRNA- 141 are regulated by a FOXP3-KAT2B axis and associated with tumor metastasis in breast cancer. Breast Cancer Res. 19:732017. View Article : Google Scholar : PubMed/NCBI | |
Singh R, Pochampally R, Watabe K, Lu Z and Mo YY: Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol Cancer. 13:2562014. View Article : Google Scholar : PubMed/NCBI | |
Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, Chow A, O'Connor ST, Li S, Chin AR, et al: Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol. 17:183–194. 2015. View Article : Google Scholar : PubMed/NCBI | |
Gernapudi R, Yao Y, Zhang Y, Wolfson B, Roy S, Duru N, Eades G, Yang P and Zhou Q: Targeting exosomes from preadipocytes inhibits preadipocyte to cancer stem cell signaling in early-stage breast cancer. Breast Cancer Res Treat. 150:685–695. 2015. View Article : Google Scholar : PubMed/NCBI | |
Di Modica M, Regondi V, Sandri M, Iorio MV, Zanetti A, Tagliabue E, Casalini P and Triulzi T: Breast cancer-secreted miR-939 downregulates VE-cadherin and destroys the barrier function of endothelial monolayers. Cancer Lett. 384:94–100. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tominaga N, Kosaka N, Ono M, Katsuda T, Yoshioka Y, Tamura K, Lötvall J, Nakagama H and Ochiya T: Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun. 6:67162015. View Article : Google Scholar : PubMed/NCBI | |
Baroni S, Romero-Cordoba S, Plantamura I, Dugo M, D'Ippolito E, Cataldo A, Cosentino G, Angeloni V, Rossini A, Daidone MG and Iorio MV: Exosome-mediated delivery of miR-9 induces cancer-associated fibroblast-like properties in human breast fibroblasts. Cell Death Dis. 7:e23122016. View Article : Google Scholar : PubMed/NCBI | |
Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang JD and Song E: Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 10:1172011. View Article : Google Scholar : PubMed/NCBI | |
Dong H, Wang W, Chen R, Zhang Y, Zou K, Ye M, He X, Zhang F and Han J: Exosome-mediated transfer of lncRNA-SNHG14 promotes trastuzumab chemoresistance in breast cancer. Int J Oncol. 53:1013–1026. 2018.PubMed/NCBI | |
Klinke DJ II, Kulkarni YM, Wu Y and Byrne-Hoffman C: Inferring alterations in cell-to-cell communication in HER2+ breast cancer using secretome profiling of three cell models. Biotechnol Bioeng. 111:1853–1863. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zheng Y, Campbell EC, Lucocq J, Riches A and Powis SJ: Monitoring the Rab27 associated exosome pathway using nanoparticle tracking analysis. Exp Cell Res. 319:1706–1713. 2013. View Article : Google Scholar : PubMed/NCBI | |
Bard MP, Hegmans JP, Hemmes A, Luider TM, Willemsen R, Severijnen LA, van Meerbeeck JP, Burgers SA, Hoogsteden HC and Lambrecht BN: Proteomic analysis of exosomes isolated from human malignant pleural effusions. Am J Respir Cell Mol Biol. 31:114–121. 2004. View Article : Google Scholar : PubMed/NCBI | |
Palazzolo G, Albanese NN, DI Cara G, Gygax D, Vittorelli ML and Pucci-Minafra I: Proteomic analysis of exosome-like vesicles derived from breast cancer cells. Anticancer Res. 32:847–860. 2012.PubMed/NCBI | |
Ma X, Chen Z, Hua D, He D, Wang L, Zhang P, Wang J, Cai Y, Gao C, Zhang X, et al: Essential role for TrpC5-containing extracellular vesicles in breast cancer with chemotherapeutic resistance. Proc Natl Acad Sci USA. 111:6389–6394. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kong JN, He Q, Wang G, Dasgupta S, Dinkins MB, Zhu G, Kim A, Spassieva S and Bieberich E: Guggulsterone and bexarotene induce secretion of exosome-associated breast cancer resistance protein and reduce doxorubicin resistance in MDA-MB-231 cells. Int J Cancer. 137:1610–1620. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yang SJ, Wang DD, Li J, Xu HZ, Shen HY, Chen X, Zhou SY, Zhong SL, Zhao JH and Tang JH: Predictive role of GSTP1-containing exosomes in chemotherapy-resistant breast cancer. Gene. 623:5–14. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ning K, Wang T, Sun X, Zhang P, Chen Y, Jin J and Hua D: UCH-L1-containing exosomes mediate chemotherapeutic resistance transfer in breast cancer. J Surg Oncol. 115:932–940. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kesimer M, Scull M, Brighton B, DeMaria G, Burns K, O'Neal W, Pickles RJ and Sheehan JK: Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: A possible role in innate defense. FASEB J. 23:1858–1868. 2009. View Article : Google Scholar : PubMed/NCBI | |
Villarreal L, Méndez O, Salvans C, Gregori J, Baselga J and Villanueva J: Unconventional secretion is a major contributor of cancer cell line secretomes. Mol Cell Proteomics. 12:1046–1060. 2013. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Zeng C, Zhan Y, Wang H, Jiang X and Li W: Aberrant low expression of p85α in stromal fibroblasts promotes breast cancer cell metastasis through exosome-mediated paracrine Wnt10b. Oncogene. 36:4692–4705. 2017. View Article : Google Scholar : PubMed/NCBI | |
Muluhngwi P and Klinge CM: Identification of miRNAs as biomarkers for acquired endocrine resistance in breast cancer. Mol Cell Endocrinol. 456:76–86. 2017. View Article : Google Scholar : PubMed/NCBI | |
Dutta S, Warshall C, Bandyopadhyay C, Dutta D and Chandran B: Interactions between exosomes from breast cancer cells and primary mammary epithelial cells leads to generation of reactive oxygen species which induce DNA damage response, stabilization of p53 and autophagy in epithelial cells. PLoS One. 9:e975802014. View Article : Google Scholar : PubMed/NCBI | |
Wu C and Luo J: Long non-coding RNA (lncRNA) urothelial carcinoma-associated 1 (UCA1) enhances tamoxifen resistance in breast cancer cells via inhibiting mTOR signaling pathway. Med Sci Monit. 22:3860–3867. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gutkin A, Uziel O, Beery E, Nordenberg J, Pinchasi M, Goldvaser H, Henick S, Goldberg M and Lahav M: Tumor cells derived exosomes contain hTERT mRNA and transform nonmalignant fibroblasts into telomerase positive cells. Oncotarget. 7:59173–59188. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gong C, Nie Y, Qu S, Liao JY, Cui X, Yao H, Zeng Y, Su F, Song E and Liu Q: miR-21 induces myofibroblast differentiation and promotes the malignant progression of breast phyllodes tumors. Cancer Res. 74:4341–4352. 2014. View Article : Google Scholar : PubMed/NCBI | |
Baglio SR, Rooijers K, Koppers-Lalic D, Verweij FJ, Pérez Lanzón M, Zini N, Naaijkens B, Perut F, Niessen HW, Baldini N and Pegtel DM: Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species. Stem Cell Res Ther. 6:1272015. View Article : Google Scholar : PubMed/NCBI | |
Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A and Lund AH: Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem. 283:1026–1033. 2008. View Article : Google Scholar : PubMed/NCBI | |
Si ML, Zhu S, Wu H, Lu Z, Wu F and Mo YY: miR-21-mediated tumor growth. Oncogene. 26:2799–2803. 2007. View Article : Google Scholar : PubMed/NCBI | |
Yu DD, Lv MM, Chen WX, Zhong SL, Zhang XH, Chen L, Ma TF, Tang JH and Zhao JH: Role of miR-155 in drug resistance of breast cancer. Tumour Biol. 36:1395–1401. 2015. View Article : Google Scholar : PubMed/NCBI | |
Maji S, Chaudhary P, Akopova I, Nguyen PM, Hare RJ, Gryczynski I and Vishwanatha JK: Exosomal annexin II promotes angiogenesis and breast cancer metastasis. Mol Cancer Res. 15:93–105. 2017. View Article : Google Scholar : PubMed/NCBI | |
Menck K, Klemm F, Gross JC, Pukrop T, Wenzel D and Binder C: Induction and transport of Wnt 5a during macrophage-induced malignant invasion is mediated by two types of extracellular vesicles. Oncotarget. 4:2057–2066. 2013. View Article : Google Scholar : PubMed/NCBI | |
Nabet BY, Qiu Y, Shabason JE, Wu TJ, Yoon T, Kim BC, Benci JL, DeMichele AM, Tchou J, Marcotrigiano J and Minn AJ: Exosome RNA unshielding couples stromal activation to pattern recognition receptor signaling in cancer. Cell. 170:352–366.e13. 2017. View Article : Google Scholar : PubMed/NCBI | |
Donnarumma E, Fiore D, Nappa M, Roscigno G, Adamo A, Iaboni M, Russo V, Affinito A, Puoti I, Quintavalle C, et al: Cancer-associated fibroblasts release exosomal microRNAs that dictate an aggressive phenotype in breast cancer. Oncotarget. 8:19592–19608. 2017. View Article : Google Scholar : PubMed/NCBI | |
Jung KO, Youn H, Lee CH, Kang KW and Chung JK: Visualization of exosome-mediated miR-210 transfer from hypoxic tumor cells. Oncotarget. 8:9899–9910. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lee JK, Park SR, Jung BK, Jeon YK, Lee YS, Kim MK, Kim YG, Jang JY and Kim CW: Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One. 8:e842562013. View Article : Google Scholar : PubMed/NCBI | |
Pakravan K, Babashah S, Sadeghizadeh M, Mowla SJ, Mossahebi-Mohammadi M, Ataei F, Dana N and Javan M: MicroRNA-100 shuttled by mesenchymal stem cell-derived exosomes suppresses in vitro angiogenesis through modulating the mTOR/HIF-1α/VEGF signaling axis in breast cancer cells. Cell Oncol (Dordr). 40:457–470. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen WX, Zhong SL, Ji MH, Pan M, Hu Q, Lv MM, Luo Z, Zhao JH and Tang JH: MicroRNAs delivered by extracellular vesicles: An emerging resistance mechanism for breast cancer. Tumour Biol. 35:2883–2892. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen WX, Liu XM, Lv MM, Chen L, Zhao JH, Zhong SL, Ji MH, Hu Q, Luo Z, Wu JZ and Tang JH: Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs. PLoS One. 9:e952402014. View Article : Google Scholar : PubMed/NCBI | |
Dong Y, Pan Q, Jiang L, Chen Z, Zhang F, Liu Y, Xing H, Shi M, Li J, Li X, et al: Tumor endothelial expression of P-glycoprotein upon microvesicular transfer of TrpC5 derived from adriamycin-resistant breast cancer cells. Biochem Biophys Res Commun. 446:85–90. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ma X, Cai Y, He D, Zou C, Zhang P, Lo CY, Xu Z, Chan FL, Yu S, Chen Y, et al: Transient receptor potential channel TRPC5 is essential for P-glycoprotein induction in drug-resistant cancer cells. Proc Natl Acad Sci USA. 109:16282–16287. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sansone P, Savini C, Kurelac I, Chang Q, Amato LB, Strillacci A, Stepanova A, Iommarini L, Mastroleo C, Daly L, et al: Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc Natl Acad Sci USA. 114:E9066–E9075. 2017. View Article : Google Scholar : PubMed/NCBI | |
Challagundla KB, Wise PM, Neviani P, Chava H, Murtadha M, Xu T, Kennedy R, Ivan C, Zhang X, Vannini I, et al: Exosome-mediated transfer of microRNAs within the tumor microenvironment and neuroblastoma resistance to chemotherapy. J Natl Cancer Inst. 107(pii): djv1352015.PubMed/NCBI | |
Cho JA, Park H, Lim EH and Lee KW: Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol. 40:130–138. 2012.PubMed/NCBI | |
Berrondo C, Flax J, Kucherov V, Siebert A, Osinski T, Rosenberg A, Fucile C, Richheimer S and Beckham CJ: Expression of the long non-coding RNA HOTAIR correlates with disease progression in bladder cancer and is contained in bladder cancer patient urinary exosomes. PLoS One. 11:e01472362016. View Article : Google Scholar : PubMed/NCBI | |
Dong L, Lin W, Qi P, Xu MD, Wu X, Ni S, Huang D, Weng WW, Tan C, Sheng W, et al: Circulating long RNAs in serum extracellular vesicles: Their characterization and potential application as biomarkers for diagnosis of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 25:1158–1166. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bhan A, Soleimani M and Mandal SS: Long noncoding RNA and cancer: A new paradigm. Cancer Res. 77:3965–3981. 2017. View Article : Google Scholar : PubMed/NCBI | |
Dragomir M, Chen B and Calin GA: Exosomal lncRNAs as new players in cell-to-cell communication. Transl Cancer Res. 7 (Suppl 2):S243–S252. 2018. View Article : Google Scholar : PubMed/NCBI | |
Momen-Heravi F, Getting SJ and Moschos SA: Extracellular vesicles and their nucleic acids for biomarker discovery. Pharmacol Ther. 192:170–187. 2018. View Article : Google Scholar : PubMed/NCBI | |
Halvaei S, Daryani S, Eslami-S Z, Samadi T, Jafarbeik-Iravani N, Bakhshayesh TO, Majidzadeh-A K and Esmaeili R: Exosomes in cancer liquid biopsy: A focus on breast cancer. Mol Ther Nucleic Acids. 10:131–141. 2018. View Article : Google Scholar : PubMed/NCBI | |
Hannafon BN, Trigoso YD, Calloway CL, Zhao YD, Lum DH, Welm AL, Zhao ZJ, Blick KE, Dooley WC and Ding WQ: Plasma exosome microRNAs are indicative of breast cancer. Breast Cancer Res. 18:902016. View Article : Google Scholar : PubMed/NCBI | |
Shi W, Gerster K, Alajez NM, Tsang J, Waldron L, Pintilie M, Hui AB, Sykes J, P'ng C, Miller N, et al: MicroRNA-301 mediates proliferation and invasion in human breast cancer. Cancer Res. 71:2926–2937. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ma F, Zhang J, Zhong L, Wang L, Liu Y, Wang Y, Peng L and Guo B: Upregulated microRNA-301a in breast cancer promotes tumor metastasis by targeting PTEN and activating Wnt/β-catenin signaling. Gene. 535:191–197. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lettlova S, Brynychova V, Blecha J, Vrana D, Vondrusova M, Soucek P and Truksa J: MiR-301a-3p suppresses estrogen signaling by directly inhibiting ESR1 in ERα positive breast cancer. Cell Physiol Biochem. 46:2601–2615. 2018. View Article : Google Scholar : PubMed/NCBI | |
Mihelich BL, Dambal S, Lin S and Nonn L: miR-182, of the miR-183 cluster family, is packaged in exosomes and is detected in human exosomes from serum, breast cells and prostate cells. Oncol Lett. 12:1197–1203. 2016. View Article : Google Scholar : PubMed/NCBI | |
Sueta A, Yamamoto Y, Tomiguchi M, Takeshita T, Yamamoto-Ibusuki M and Iwase H: Differential expression of exosomal miRNAs between breast cancer patients with and without recurrence. Oncotarget. 8:69934–69944. 2017. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez-Martinez A, de Miguel-Pérez D, Ortega FG, García-Puche JL, Robles-Fernández I, Exposito J, Martorell-Marugan J, Carmona-Sáez P, Garrido-Navas MDC, Rolfo C, et al: Exosomal miRNA profile as complementary tool in the diagnostic and prediction of treatment response in localized breast cancer under neoadjuvant chemotherapy. Breast Cancer Res. 21:212019. View Article : Google Scholar : PubMed/NCBI | |
Stevic I, Müller V, Weber K, Fasching PA, Karn T, Marmé F, Schem C, Stickeler E, Denkert C, van Mackelenbergh M, et al: Specific microRNA signatures in exosomes of triple-negative and HER2-positive breast cancer patients undergoing neoadjuvant therapy within the GeparSixto trial. BMC Med. 16:1792018. View Article : Google Scholar : PubMed/NCBI | |
Joyce DP, Kerin MJ and Dwyer RM: Exosome-encapsulated microRNAs as circulating biomarkers for breast cancer. Int J Cancer. 139:1443–1448. 2016. View Article : Google Scholar : PubMed/NCBI | |
Eichelser C, Stückrath I, Müller V, Milde-Langosch K, Wikman H, Pantel K and Schwarzenbach H: Increased serum levels of circulating exosomal microRNA-373 in receptor-negative breast cancer patients. Oncotarget. 5:9650–9663. 2014. View Article : Google Scholar : PubMed/NCBI | |
Cuk K, Zucknick M, Madhavan D, Schott S, Golatta M, Heil J, Marmé F, Turchinovich A, Sinn P, Sohn C, et al: Plasma microRNA panel for minimally invasive detection of breast cancer. PLoS One. 8:e767292013. View Article : Google Scholar : PubMed/NCBI | |
Koldemir O, Özgür E and Gezer U: Accumulation of GAS5 in exosomes is a marker of apoptosis induction. Biomed Rep. 6:358–362. 2017. View Article : Google Scholar : PubMed/NCBI | |
Moon PG, Lee JE, Cho YE, Lee SJ, Jung JH, Chae YS, Bae HI, Kim YB, Kim IS, Park HY and Baek MC: Identification of developmental endothelial locus-1 on circulating extracellular vesicles as a novel biomarker for early breast cancer detection. Clin Cancer Res. 22:1757–1766. 2016. View Article : Google Scholar : PubMed/NCBI | |
Moon PG, Lee JE, Cho YE, Lee SJ, Chae YS, Jung JH, Kim IS, Park HY and Baek MC: Fibronectin on circulating extracellular vesicles as a liquid biopsy to detect breast cancer. Oncotarget. 7:40189–40199. 2016. View Article : Google Scholar : PubMed/NCBI | |
Higginbotham JN, Demory Beckler M, Gephart JD, Franklin JL, Bogatcheva G, Kremers GJ, Piston DW, Ayers GD, McConnell RE, Tyska MJ and Coffey RJ: Amphiregulin exosomes increase cancer cell invasion. Curr Biol. 21:779–786. 2011. View Article : Google Scholar : PubMed/NCBI | |
Khan S, Bennit HF, Turay D, Perez M, Mirshahidi S, Yuan Y and Wall NR: Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer. 14:1762014. View Article : Google Scholar : PubMed/NCBI | |
Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, et al: Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 523:177–182. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rupp AK, Rupp C, Keller S, Brase JC, Ehehalt R, Fogel M, Moldenhauer G, Marmé F, Sültmann H and Altevogt P: Loss of EpCAM expression in breast cancer derived serum exosomes: Role of proteolytic cleavage. Gynecol Oncol. 122:437–446. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lim LH and Pervaiz S: Annexin 1: The new face of an old molecule. FASEB J. 21:968–975. 2007. View Article : Google Scholar : PubMed/NCBI | |
Galindo-Hernandez O, Villegas-Comonfort S, Candanedo F, González-Vázquez MC, Chavez-Ocaña S, Jimenez-Villanueva X, Sierra-Martinez M and Salazar EP: Elevated concentration of microvesicles isolated from peripheral blood in breast cancer patients. Arch Med Res. 44:208–214. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kooijmans SA, Vader P, van Dommelen SM, van Solinge WW and Schiffelers RM: Exosome mimetics: A novel class of drug delivery systems. Int J Nanomedicine. 7:1525–1541. 2012.PubMed/NCBI | |
Kahlert C and Kalluri R: Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl). 91:431–437. 2013. View Article : Google Scholar : PubMed/NCBI | |
Marleau AM, Chen CS, Joyce JA and Tullis RH: Exosome removal as a therapeutic adjuvant in cancer. J Transl Med. 10:1342012. View Article : Google Scholar : PubMed/NCBI | |
Kumar D, Gupta D, Shankar S and Srivastava RK: Biomolecular characterization of exosomes released from cancer stem cells: Possible implications for biomarker and treatment of cancer. Oncotarget. 6:3280–3291. 2015. View Article : Google Scholar : PubMed/NCBI | |
Shen Y, Ye YF, Ruan LW, Bao L, Wu MW and Zhou Y: Inhibition of miR-660-5p expression suppresses tumor development and metastasis in human breast cancer. Genet Mol Res. 16:2017. View Article : Google Scholar | |
Zhang P, Zhou H, Lu K, Lu Y, Wang Y and Feng T: Exosome-mediated delivery of MALAT1 induces cell proliferation in breast cancer. Onco Targets Ther. 11:291–299. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yeo RW, Lai RC, Zhang B, Tan SS, Yin Y, The BJ and Lim SK: Mesenchymal stem cell: An efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev. 65:336–341. 2013. View Article : Google Scholar : PubMed/NCBI | |
Rani S, Ryan AE, Griffin MD and Ritter T: Mesenchymal stem cell-derived extracellular vesicles: Toward cell-free therapeutic applications. Mol Ther. 23:812–823. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T, et al: Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 21:185–191. 2013. View Article : Google Scholar : PubMed/NCBI | |
de Jong OG, Kooijmans SAA, Murphy DE, Jiang L, Evers MJW, Sluijter JPG, Vader P and Schiffelers RM: Drug delivery with extracellular vesicles: From imagination to innovation. Acc Chem Res. 52:1761–1770. 2019. View Article : Google Scholar : PubMed/NCBI | |
Iyengar P, Combs TP, Shah SJ, Gouon-Evans V, Pollard JW, Albanese C, Flanagan L, Tenniswood MP, Guha C, Lisanti MP, et al: Adipocyte-secreted factors synergistically promote mammary tumorigenesis through induction of anti-apoptotic transcriptional programs and proto-oncogene stabilization. Oncogene. 22:6408–6423. 2003. View Article : Google Scholar : PubMed/NCBI | |
Yao Y and Zhou Q: A novel antiestrogen agent Shikonin inhibits estrogen-dependent gene transcription in human breast cancer cells. Breast Cancer Res Treat. 121:233–240. 2010. View Article : Google Scholar : PubMed/NCBI | |
Cho JA, Yeo DJ, Son HY, Kim HW, Jung DS, Ko JK, Koh JS, Kim YN and Kim CW: Exosomes: A new delivery system for tumor antigens in cancer immunotherapy. Int J Cancer. 114:613–622. 2005. View Article : Google Scholar : PubMed/NCBI | |
Tan A, De La Peña H and Seifalian AM: The application of exosomes as a nanoscale cancer vaccine. Int J Nanomedicine. 5:889–900. 2010.PubMed/NCBI | |
Wu CY, Du SL, Zhang J, Liang AL and Liu YJ: Exosomes and breast cancer: A comprehensive review of novel therapeutic strategies from diagnosis to treatment. Cancer Gene Ther. 24:6–12. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kalluri R: The biology and function of exosomes in cancer. J Clin Invest. 126:1208–1215. 2016. View Article : Google Scholar : PubMed/NCBI | |
Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM and Breakefield XO: Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 10:1470–1476. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tanaka Y, Kamohara H, Kinoshita K, Kurashige J, Ishimoto T, Iwatsuki M, Watanabe M and Baba H: Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma. Cancer. 119:1159–1167. 2013. View Article : Google Scholar : PubMed/NCBI | |
Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al: Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 17:816–826. 2015. View Article : Google Scholar : PubMed/NCBI | |
Castillo J, Bernard V, San Lucas FA, Allenson K, Capello M, Kim DU, Gascoyne P, Mulu FC, Stephens BM, Huang J, et al: Surfaceome profiling enables isolation of cancer-specific exosomal cargo in liquid biopsies from pancreatic cancer patients. Ann Oncol. 29:223–229. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang P, Wang L, Fang Y, Zheng D, Lin T and Wang H: Label-free exosomal detection and classification in rapid discriminating different cancer types based on specific Raman phenotypes and multivariate statistical analysis. Molecules. 24(pii): E29472019. View Article : Google Scholar : PubMed/NCBI | |
Larssen P, Wik L, Czarnewski P, Eldh M, Löf L, Ronquist KG, Dubois L, Freyhult E, Gallant CJ, Oelrich J, et al: Tracing cellular origin of human exosomes using multiplex proximity extension assays. Mol Cell Proteomics. 16:502–511. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wu D, Yan J, Shen X, Sun Y, Thulin M, Cai Y, Wik L, Shen Q, Oelrich J1, Qian X, et al: Profiling surface proteins on individual exosomes using a proximity barcoding assay. Nat Commun. 10:38542019. View Article : Google Scholar : PubMed/NCBI | |
Chen C, Zong S, Liu Y, Wang Z, Zhang Y, Chen B and Cui Y: Profiling of exosomal biomarkers for accurate cancer identification: Combining DNA-PAINT with machine-learning-based classification. Small. 15:e19010142019. View Article : Google Scholar : PubMed/NCBI | |
Shimomura A, Shiino S, Kawauchi J, Takizawa S, Sakamoto H, Matsuzaki J, Ono M, Takeshita F, Niida S, Shimizu C, et al: Novel combination of serum microRNA for detecting breast cancer in the early stage. Cancer Sci. 107:326–334. 2016. View Article : Google Scholar : PubMed/NCBI | |
Roccaro AM, Sacco A, Maiso P, Azab AK, Tai YT, Reagan M, Azab F, Flores LM, Campigotto F, Weller E, et al: BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest. 123:1542–1555. 2013. View Article : Google Scholar : PubMed/NCBI | |
Schwarzenbach H: The clinical relevance of circulating, exosomal miRNAs as biomarkers for cancer. Expert Rev Mol Diagn. 15:1159–1169. 2015. View Article : Google Scholar : PubMed/NCBI | |
Takahashi Y, Nishikawa M, Shinotsuka H, Matsui Y, Ohara S, Imai T and Takakura Y: Visualization and in vivo tracking of the exosomes of murine melanoma B16-BL6 cells in mice after intravenous injection. J Biotechnol. 165:77–84. 2013. View Article : Google Scholar : PubMed/NCBI | |
Smyth T, Kullberg M, Malik N, Smith-Jones P, Graner MW and Anchordoquy TJ: Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release. 199:145–155. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bala S, Csak T, Momen-Heravi F, Lippai D, Kodys K, Catalano D, Satishchandran A, Ambros V and Szabo G: Biodistribution and function of extracellular miRNA-155 in mice. Sci Rep. 5:107212015. View Article : Google Scholar : PubMed/NCBI | |
Tian T, Wang Y, Wang H, Zhu Z and Xiao Z: Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J Cell Biochem. 111:488–496. 2010. View Article : Google Scholar : PubMed/NCBI | |
Grange C, Tapparo M, Bruno S, Chatterjee D, Quesenberry PJ, Tetta C and Camussi G: Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging. Int J Mol Med. 33:1055–1063. 2014. View Article : Google Scholar : PubMed/NCBI |