Predictive value of exosomes and their cargo in drug response/resistance of breast cancer patients

Heidi Schwarzenbach , Peter B. Gahan

Cancer Drug Resistance ›› 2020, Vol. 3 ›› Issue (1) : 63 -82.

PDF
Cancer Drug Resistance ›› 2020, Vol. 3 ›› Issue (1) :63 -82. DOI: 10.20517/cdr.2019.90
Review
review-article

Predictive value of exosomes and their cargo in drug response/resistance of breast cancer patients

Author information +
History +
PDF

Abstract

Exosomes are small extracellular vesicles engaged in intercellular communication in both healthy and tumor cells. When released by the primary tumor, they transfer their cargo including nucleic acids, proteins, and lipids to target cells, thus modulating the character and fate of the recipient cells. By propagating their oncogenic content, exosomes are able to promote tumor progression, angiogenesis, metastases, and drug resistance. Their functions as delivery vehicles of biological material make exosomes promising biomarkers for the early prediction of disease progression and drug resistance in breast cancer, as well as for therapeutic targeting of molecules to treat this deadly disease. In the present review, we accentuate the relevance of exosomes as vehicles of prognostic and predictive markers and target molecules, and describe their potential therapeutic applications as drug cargo suppliers. We made an extensive literature research to clarify the association of their cargo, including exosomal DNA and RNA molecules, with the propagation of drug resistance.

Keywords

Breast cancer / exosomes / exosomal DNA / mRNA / non-coding RNAs / microRNAs / lncRNAs

Cite this article

Download citation ▾
Heidi Schwarzenbach, Peter B. Gahan. Predictive value of exosomes and their cargo in drug response/resistance of breast cancer patients. Cancer Drug Resistance, 2020, 3(1): 63-82 DOI:10.20517/cdr.2019.90

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Dasari S.Cisplatin in cancer therapy: molecular mechanisms of action..Eur J Pharmacol2014;740:364-78 PMCID:PMC4146684

[2]

Garutti M,Bartoletti M,Gerratana L.Platinum salts in patients with breast cancer: a focus on predictive factors..Int J Mol Sci2019;20: PMCID:PMC6678596

[3]

Farha NG.Docetaxel. In: StatPearls [Internet].2020;Treasure Island (FL)StatPearls Publishing

[4]

Stage TB,Kroetz DL.Clinical pharmacokinetics of paclitaxel monotherapy: an updated literature review..Clin Pharmacokinet2018;57:7-19

[5]

Johnson-Arbor K.Doxorubicin. In: StatPearls [Internet].2020;Treasure Island (FL)StatPearls Publishing

[6]

Khasraw M,Dang C.Epirubicin: is it like doxorubicin in breast cancer? A clinical review..Breast2012;21:142-9

[7]

Li J,Shao Z.Fulvestrant in the treatment of hormone receptor-positive/human epidermal growth factor receptor 2-negative advanced breast cancer: a review..Cancer Med2019;8:1943-57 PMCID:PMC6536994

[8]

Zhao D,Chu M.Prolonged low-dose infusion for gemcitabine: a systematic review..Onco Targets Ther2019;12:4859-68 PMCID:PMC6593688

[9]

Voigtlaender M,Trepel M.Lapatinib..Recent Results Cancer Res2018;211:19-44

[10]

Roshan MH,Pace NP.Metformin as an adjuvant in breast cancer treatment..SAGE Open Med2019;7:2050312119865114 PMCID:PMC6637843

[11]

Bochum S,Martens UM.Olaparib..Recent Results Cancer Res2018;211:217-33

[12]

Farrar MC.Tamoxifen. In: StatPearls [Internet].2020;Treasure Island (FL)StatPearls Publishing

[13]

Mazzotta M,Barchiesi G,Tomao F.Long-term safety and real-world effectiveness of trastuzumab in breast cancer..J Clin Med2019;8: PMCID:PMC6406268

[14]

Moudi M,Yien CY.Vinca alkaloids..Int J Prev Med2013;4:1231-5 PMCID:PMC3883245

[15]

Zijlstra A.Size matters in nanoscale communication..Nat Cell Biol2018;20:228-30 PMCID:PMC6652179

[16]

Yu X,Fries JW.Exosomes as miRNA carriers: formation-function-future..Int J Mol Sci2016;17: PMCID:PMC5187828

[17]

Guescini M,Stocchi V.Astrocytes and Glioblastoma cells release exosomes carrying mtDNA..J Neural Transm (Vienna)2010;117:1-4

[18]

Thakur BK,Becker A,Huang Y.Double-stranded DNA in exosomes: a novel biomarker in cancer detection..Cell Res2014;24:766-9 PMCID:PMC4042169

[19]

Sansone P,Kurelac I,Amato LB.Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer..Proc Natl Acad Sci U S A2017;114:E9066-75 PMCID:PMC5664494

[20]

Kalluri R.Discovery of double-stranded genomic DNA in circulating exosomes..Cold Spring Harb Symp Quant Biol2016;81:275-80

[21]

Huang X,Tschannen M,Jacob H.Characterization of human plasma-derived exosomal RNAs by deep sequencing..BMC Genomics2013;14:319 PMCID:PMC3653748

[22]

Simons M.Exosomes--vesicular carriers for intercellular communication..Curr Opin Cell Biol2009;21:575-81

[23]

Cai J,Ren HM,He DF.Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells..J Mol Cell Biol2013;5:227-38 PMCID:PMC3733418

[24]

Zong WX,White E.Mitochondria and cancer..Mol Cell2016;61:667-76 PMCID:PMC4779192

[25]

Wang J,Qiu Y,Cai J.Cell adhesion-mediated mitochondria transfer contributes to mesenchymal stem cell-induced chemoresistance on T cell acute lymphoblastic leukemia cells..J Hematol Oncol2018;11:11 PMCID:PMC5778754

[26]

Schwarzenbach H.MicroRNA shuttle from cell-to-cell by exosomes and its impact in cancer..Noncoding RNA2019;5: PMCID:PMC6468647

[27]

Kim KM,Mustapic M,Gorospe M.RNA in extracellular vesicles..Wiley Interdiscip Rev RNA2017;8: PMCID:PMC5474163

[28]

Malumbres M,Sotillo R,Odajima J.Driving the cell cycle to cancer..Adv Exp Med Biol2003;532:1-11

[29]

Serra F,Quaquarini E,Sottotetti F.Palbociclib in metastatic breast cancer: current evidence and real-life data..Drugs Context2019;8:212579 PMCID:PMC6668507

[30]

Del Re M,Crucitta S,Rofi E.Overexpression of TK1 and CDK9 in plasma-derived exosomes is associated with clinical resistance to CDK4/6 inhibitors in metastatic breast cancer patients..Breast Cancer Res Treat2019;178:57-62

[31]

Boelens MC,Nabet BY,Qiu Y.Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways..Cell2014;159:499-513 PMCID:PMC4283810

[32]

Zeromski J,Boruczkowski M,Kowala-Piaskowska A.Significance and role of pattern recognition receptors in malignancy..Arch Immunol Ther Exp (Warsz)2019;67:133-41 PMCID:PMC6509067

[33]

Zhang Y.STAT1 in cancer: friend or foe?.Discov Med2017;24:19-29

[34]

Brzozowa-Zasada M,Michalski M,Kurek J.Notch and its oncogenic activity in human malignancies..Eur Surg2017;49:199-209 PMCID:PMC5653712

[35]

Wang X,Hua Y,Cheng K.Exosomes play an important role in the process of psoralen reverse multidrug resistance of breast cancer..J Exp Clin Cancer Res2016;35:186 PMCID:PMC5131502

[36]

Panno ML.Effects of psoralens as anti-tumoral agents in breast cancer cells..World J Clin Oncol2014;5:348-58 PMCID:PMC4127606

[37]

Verderio C,Giussani P.Role of sphingolipids in the biogenesis and biological activity of extracellular vesicles..J Lipid Res2018;59:1325-40 PMCID:PMC6071771

[38]

Chen WX,Qian Q,Peng WT.Analysis of miRNA signature differentially expressed in exosomes from adriamycin-resistant and parental human breast cancer cells..Biosci Rep2018;38: PMCID:PMC6240718

[39]

O’Brien K,Corcoran C,Daly M.miR-134 in extracellular vesicles reduces triple-negative breast cancer aggression and increases drug sensitivity..Oncotarget2015;6:32774-89 PMCID:PMC4741729

[40]

Santos JC,Sarian LO,Ribeiro ML.Exosome-mediated breast cancer chemoresistance via miR-155 transfer..Sci Rep2018;8:829 PMCID:PMC5770414

[41]

Stevic I,Weber K,Karn T.Specific microRNA signatures in exosomes of triple-negative and HER2-positive breast cancer patients undergoing neoadjuvant therapy within the GeparSixto trial..BMC Med2018;16:179 PMCID:PMC6178264

[42]

Chen WX,Lv MM,Zhong SL.Exosomes from docetaxel-resistant breast cancer cells alter chemosensitivity by delivering microRNAs..Tumour Biol2014;35:9649-59

[43]

Chen WX,Lv MM,Zhao JH.Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs..PloS One2014;9:e95240 PMCID:PMC3989268

[44]

Wei Y,Yu S,Ma Y.Exosomal miR-221/222 enhances tamoxifen resistance in recipient ER-positive breast cancer cells..Breast Cancer Res Treat2014;147:423-31

[45]

Yu DD,Zhang XH,Chen WX.Exosomes from adriamycin-resistant breast cancer cells transmit drug resistance partly by delivering miR-222..Tumour Biol2016;37:3227-35

[46]

Wang B,Ye M,Ma L.Cisplatin-resistant MDA-MB-231 cell-derived exosomes increase the resistance of recipient cells in an exosomal miR-423-5p-dependent manner..Curr Drug Metab2019;20:804-14

[47]

Bovy N,Freres P,Nivelles O.Endothelial exosomes contribute to the antitumor response during breast cancer neoadjuvant chemotherapy via microRNA transfer..Oncotarget2015;6:10253-66 PMCID:PMC4496353

[48]

Zhong SL,Wang DD,Shen HY.MicroRNA expression profiles of drug-resistance breast cancer cells and their exosomes..Oncotarget2016;7:19601-9 PMCID:PMC4991404

[49]

Li Y,Sang Y,Zhang H.MiR-770 suppresses the chemo-resistance and metastasis of triple negative breast cancer via direct targeting of STMN1..Cell Death Dis2018;9:14 PMCID:PMC5849036

[50]

Li XJ,Tang JH.Exosomal microRNA MiR-1246 promotes cell proliferation, invasion and drug resistance by targeting CCNG2 in breast cancer..Cell Physiol Biochem2017;44:1741-8

[51]

Shen M,Ruan X,Cao M.Chemotherapy-induced extracellular vesicle miRNAs promote breast cancer stemness by targeting ONECUT2..Cancer Res2019;79:3608-21

[52]

Chen WX,Qian Q,Peng WT.D Rhamnose β-hederin reverses chemoresistance of breast cancer cells by regulating exosome-mediated resistance transmission..Biosci Rep2018;38: PMCID:PMC6165836

[53]

Ozawa PMM,Cavalli IJ,de Souza Fonseca Ribeiro EM.Extracellular vesicles from triple-negative breast cancer cells promote proliferation and drug resistance in non-tumorigenic breast cells..Breast Cancer Res Treat2018;172:713-23 PMCID:PMC6245099

[54]

Dillon RL,Muller WJ.The phosphatidyl inositol 3-kinase signaling network: implications for human breast cancer..Oncogene2007;26:1338-45

[55]

Giltnane JM.Rationale for targeting the Ras/MAPK pathway in triple-negative breast cancer..Discov Med2014;17:275-83

[56]

Milani M.Targeting tumour hypoxia in breast cancer..Eur J Cancer2008;44:2766-73

[57]

Pak SH,Park JH,Darvin P.Hypoxia upregulates Hsp90alpha expression via STAT5b in cancer cells..Int J Oncol2012;41:161-8

[58]

Rodríguez-Martínez A,Ortega FG,Robles-Fernández I.Exosomal miRNA profile as complementary tool in the diagnostic and prediction of treatment response in localized breast cancer under neoadjuvant chemotherapy..Breast Cancer Res2019;21:21 PMCID:PMC6366103

[59]

Muller V,Steinbach B,von Minckwitz G.Changes in serum levels of miR-21, miR-210, and miR-373 in HER2-positive breast cancer patients undergoing neoadjuvant therapy: a translational research project within the Geparquinto trial..Breast Cancer Res Treat2014;147:61-8

[60]

Liu F,Lv L.TGF-beta1 acts through miR-155 to down-regulate TP53INP1 in promoting epithelial-mesenchymal transition and cancer stem cell phenotypes..Cancer Lett2015;359:288-98

[61]

Li X,Xu W,Gao P.c-MYC-regulated miR-23a/24-2/27a cluster promotes mammary carcinoma cell invasion and hepatic metastasis by targeting Sprouty2..J Biol Chem2013;288:18121-33 PMCID:PMC3689956

[62]

Zhong S,Chen Z,Zhao J.MiR-222 and miR-29a contribute to the drug-resistance of breast cancer cells..Gene2013;531:8-14

[63]

Hu Q,Zhong SL,Ma TF.MicroRNA-452 contributes to the docetaxel resistance of breast cancer cells..Tumour Biol2014;35:6327-34

[64]

Abbastabar M,Azizian K,Tehrani SS.Multiple functions of p27 in cell cycle, apoptosis, epigenetic modification and transcriptional regulation for the control of cell growth: a double-edged sword protein..DNA Repair (Amst)2018;69:63-72

[65]

Sherr CJ.D-type cyclins..Trends Biochem Sci1995;20:187-90

[66]

Rana S,Senzer N.Stathmin 1: a novel therapeutic target for anticancer activity..Expert Rev Anticancer Ther2008;8:1461-70

[67]

Ahmed S,Matthews J.FOXA1 is essential for aryl hydrocarbon receptor-dependent regulation of cyclin G2..Mol Cancer Res2012;10:636-48

[68]

Chen WX,Pan M,Zhu YL.D Rhamnose beta-Hederin against human breast cancer by reducing tumor-derived exosomes..Oncol Lett2018;16:5172-8 PMCID:PMC6144302

[69]

Mao L,Chen WX,Yu DD.Exosomes decrease sensitivity of breast cancer cells to adriamycin by delivering microRNAs..Tumour Biol2016;37:5247-56

[70]

Braune EB,Lendahl U.Notch and Wnt dysregulation and its relevance for breast cancer and tumor initiation..Biomedicines2018;6: PMCID:PMC6315509

[71]

Tang S,Tang Y,Zou T.Overexpression of serum exosomal HOTAIR is correlated with poor survival and poor response to chemotherapy in breast cancer patients..J Biosci2019;44:

[72]

Zheng Z,Xing P,Xie B.Increased expression of exosomal AGAP2-AS1 (AGAP2 Antisense RNA 1) in breast cancer cells inhibits trastuzumab-induced cell cytotoxicity..Med Sci Monit2019;25:2211-20 PMCID:PMC6446658

[73]

Dong H,Chen R,Zou K.Exosome-mediated transfer of lncRNASNHG14 promotes trastuzumab chemoresistance in breast cancer..Int J Oncol2018;53:1013-26 PMCID:PMC6065402

[74]

Xu CG,Ren YQ,Wang LQ.Exosomes mediated transfer of lncRNA UCA1 results in increased tamoxifen resistance in breast cancer cells..Eur Rev Med Pharmacol Sci2016;20:4362-8

[75]

Kang MH.Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy..Clin Cancer Res2009;15:1126-32 PMCID:PMC3182268

[76]

Adams JM.Modified nucleosides and bizarre 5’-termini in mouse myeloma messenger-rna..P Aust Biochem Soc1975;8:104

[77]

Dominissini D,Schwartz S,Ungar L.Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq..Nature2012;485:201-6

[78]

Roundtree IA,Pan T.Dynamic RNA modifications in gene expression regulation..Cell2017;169:1187-200 PMCID:PMC5657247

[79]

Esteller M.The epitranscriptome of noncoding RNAs in cancer..Cancer Discov2017;7:359-68 PMCID:PMC5997407

[80]

Wang X,Gomez A,Yue Y.N6-methyladenosine-dependent regulation of messenger RNA stability..Nature2014;505:117-20 PMCID:PMC3877715

[81]

Wang X,Roundtree IA,Han D.N(6)-methyladenosine modulates messenger RNA translation efficiency..Cell2015;161:1388-99 PMCID:PMC4825696

[82]

Chen T,Zhang Y,Wang M.m(6)A RNA methylation is regulated by microRNAs and promotes reprogramming to pluripotency..Cell Stem Cell2015;16:289-301

[83]

Geula S,Dominissini D,Kol N.Stem cells. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation..Science2015;347:1002-6

[84]

Chen XY,Zhu JS.The role of m(6)A RNA methylation in human cancer..Mol Cancer2019;18:103 PMCID:PMC6540575

[85]

Ma JZ,Zhou CC,Yuan JH.METTL14 suppresses the metastatic potential of hepatocellular carcinoma by modulating N(6) -methyladenosine-dependent primary MicroRNA processing..Hepatology2017;65:529-43

[86]

Lin S,Du P,Gregory RI.The m(6)A methyltransferase METTL3 promotes translation in human cancer cells..Mol Cell2016;62:335-45 PMCID:PMC4860043

[87]

Liu J,Harada BT,Lu Z.m(6)A mRNA methylation regulates AKT activity to promote the proliferation and tumorigenicity of endometrial cancer..Nat Cell Biol2018;20:1074-83 PMCID:PMC6245953

[88]

Cai X,Cao C,Zhang S.HBXIP-elevated methyltransferase METTL3 promotes the progression of breast cancer via inhibiting tumor suppressor let-7g..Cancer Lett2018;415:11-9

[89]

Choi DS,Kim YK.Proteomics, transcriptomics and lipidomics of exosomes and ectosomes..Proteomics2013;13:1554-71

[90]

Zhang Q,Chen Y,Sursal T.Circulating mitochondrial DAMPs cause inflammatory responses to injury..Nature2010;464:104-7 PMCID:PMC2843437

[91]

Ciravolo V,Ghedini GC,Bianchi F.Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy..J Cell Physiol2012;227:658-67

[92]

Hung Y,Lin YZ,Wu WR.The exosomal compartment protects epidermal growth factor receptor from small molecule inhibitors..Biochem Biophys Res Commun2019;510:42-7

[93]

Ning K,Sun X,Chen Y.UCH-L1-containing exosomes mediate chemotherapeutic resistance transfer in breast cancer..J Surg Oncol2017;115:932-40

[94]

Fang Y.Ubiquitin carboxyl-terminal hydrolases: involvement in cancer progression and clinical implications..Cancer Metastasis Rev2017;36:669-82

[95]

Lv MM,Chen WX,Hu Q.Exosomes mediate drug resistance transfer in MCF-7 breast cancer cells and a probable mechanism is delivery of P-glycoprotein..Tumour Biol2014;35:10773-9

[96]

Ma X,He D,Zhang P.Transient receptor potential channel TRPC5 is essential for P-glycoprotein induction in drug-resistant cancer cells..Proc Natl Acad Sci U S A2012;109:16282-7 PMCID:PMC3479621

[97]

Wang T,Lu TX,Jin L.Increasing circulating exosomes-carrying TRPC5 predicts chemoresistance in metastatic breast cancer patients..Cancer Sci2017;108:448-54 PMCID:PMC5378269

[98]

Martinez VG.Neuromedin U: a multifunctional neuropeptide with pleiotropic roles..Clin Chem2015;61:471-82

[99]

Rani S,Shiels L,Breslin S.Neuromedin U: a candidate biomarker and therapeutic target to predict and overcome resistance to HER-tyrosine kinase inhibitors..Cancer Res2014;74:3821-33

[100]

Martinez VG,Salimu J,Clayton A.Resistance to HER2-targeted anti-cancer drugs is associated with immune evasion in cancer cells and their derived extracellular vesicles..Oncoimmunology2017;6:e1362530 PMCID:PMC5706614

[101]

Liu G,Qi F,Lu XA.Specific chemotherapeutic agents induce metastatic behaviour through stromal- and tumour-derived cytokine and angiogenic factor signalling..J Pathol2015;237:190-202

[102]

Keklikoglou I,Guc E,Spring LM.Chemotherapy elicits pro-metastatic extracellular vesicles in breast cancer models..Nat Cell Biol2019;21:190-202 PMCID:PMC6525097

[103]

Grewal T,Conway JRW,Wahba M.Annexin A6-A multifunctional scaffold in cell motility..Cell Adh Migr2017;11:288-304 PMCID:PMC5479450

[104]

Qian BZ,Zhang H,Zhang J.CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis..Nature2011;475:222-5 PMCID:PMC3208506

[105]

Di Pietro G,Rios-Santos F.Glutathione S-transferases: an overview in cancer research..Expert Opin Drug Metab Toxicol2010;6:153-70

[106]

Yang SJ,Li J,Shen HY.Predictive role of GSTP1-containing exosomes in chemotherapy-resistant breast cancer..Gene2017;623:5-14

[107]

Semina SE,Vnukova AA,Evtushenko EG.Exosome-mediated transfer of cancer cell resistance to antiestrogen drugs..Molecules2018;23: PMCID:PMC6017149

[108]

Ediriweera MK,Samarakoon SR.Role of the PI3K/AKT/mTOR signaling pathway in ovarian cancer: biological and therapeutic significance..Semin Cancer Biol2019;59:147-60

[109]

Sliva D.Signaling pathways responsible for cancer cell invasion as targets for cancer therapy..Curr Cancer Drug Targets2004;4:327-36

[110]

Kaufhold S.Central role of Snail1 in the regulation of EMT and resistance in cancer: a target for therapeutic intervention..J Exp Clin Cancer Res2014;33:62 PMCID:PMC4237825

[111]

Kreger BT,Cerione RA.The enrichment of survivin in exosomes from breast cancer cells treated with paclitaxel promotes cell survival and chemoresistance..Cancers (Basel)2016;8: PMCID:PMC5187509

[112]

Rafatmanesh A,Mobasseri N,Mazoochi T.The survivin molecule as a double-edged sword in cellular physiologic and pathologic conditions and its role as a potential biomarker and therapeutic target in cancer..J Cell Physiol2020;235:725-44

[113]

Familtseva A,Tyagi SC.Exosomes: cell-created drug delivery systems..Mol Cell Biochem2019;459:1-6

[114]

Batrakova EV.Using exosomes, naturally-equipped nanocarriers, for drug delivery..J Control Release2015;219:396-405 PMCID:PMC4656109

[115]

Jung KO,Yu JH,Pratx G.Development and MPI tracking of novel hypoxia-targeted theranostic exosomes..Biomaterials2018;177:139-48 PMCID:PMC6019194

[116]

Dong R,Liu H.The evolving role of trastuzumab emtansine (T-DM1) in HER2-positive breast cancer with brain metastases..Crit Rev Oncol Hematol2019;143:20-6

[117]

Barok M,Vereb G,Isola J.Cancer-derived exosomes from HER2-positive cancer cells carry trastuzumab-emtansine into cancer cells leading to growth inhibition and caspase activation..BMC Cancer2018;18:504 PMCID:PMC5930687

[118]

Wang J,Cui M,Lu Z.Exosome is a mechanism of intercellular drug transfer: Application of quantitative pharmacology..J Control Release2017;268:147-58 PMCID:PMC5722714

[119]

Tian Y,Song J,Zhu M.A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy..Biomaterials2014;35:2383-90

[120]

Pittenger MF,Beck SC,Douglas R.Multilineage potential of adult human mesenchymal stem cells..Science1999;284:143-7

[121]

Lou G,Zheng M.Mesenchymal stem cell-derived exosomes as a new therapeutic strategy for liver diseases..Exp Mol Med2017;49:e346 PMCID:PMC5519012

[122]

Melzer C,Yang Y,von der Ohe J.Taxol-loaded MSC-derived exosomes provide a therapeutic vehicle to target metastatic breast cancer and other carcinoma cells..Cancers (Basel)2019;11: PMCID:PMC6627807

[123]

Kalimuthu S,Rajendran RL,Oh JM.A new approach for loading anticancer drugs into mesenchymal stem cell-derived exosome mimetics for cancer therapy..Front Pharmacol2018;9:1116 PMCID:PMC6168623

[124]

Gomari H,Soleimani M,Khodashenas S.Targeted delivery of doxorubicin to HER2 positive tumor models..Int J Nanomedicine2019;14:5679-90 PMCID:PMC6662522

[125]

Gomari H,Soleimani M.Targeted cancer therapy using engineered exosome as a natural drug delivery vehicle..Onco Targets Ther2018;11:5753-62 PMCID:PMC6140699

[126]

Wang P,Huang Q,Yao L.Exosomes from M1-polarized macrophages enhance paclitaxel antitumor activity by activating macrophages-mediated inflammation..Theranostics2019;9:1714-27 PMCID:PMC6485189

[127]

Meng X,Milde-Langosch K,Pantel K.Diagnostic and prognostic relevance of circulating exosomal miR-373, miR-200a, miR-200b and miR-200c in patients with epithelial ovarian cancer..Oncotarget2016;7:16923-35 PMCID:PMC4941360

[128]

Marleau AM,Joyce JA.Exosome removal as a therapeutic adjuvant in cancer..J Transl Med2012;10:134 PMCID:PMC3441244

[129]

Wolfers J,Raposo G,Thery C.Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming..Nat Med2001;7:297-303

[130]

Rashed MH,Helal GK,Amero P.Exosomes: from garbage bins to promising therapeutic targets..Int J Mol Sci2017;18: PMCID:PMC5372554

[131]

Li R,Xiang J.Novel EXO-T vaccine using polyclonal CD4(+) T cells armed with HER2-specific exosomes for HER2-positive breast cancer..Onco Targets Ther2018;11:7089-93 PMCID:PMC6200095

[132]

Xie Y,Xu A,Sami A.Heterologous human/rat HER2-specific exosome-targeted T cell vaccine stimulates potent humoral and CTL responses leading to enhanced circumvention of HER2 tolerance in double transgenic HLA-A2/HER2 mice..Vaccine2018;36:1414-22

[133]

Li Z,Lu W,Wang J.Immunotherapeutic interventions of triple negative breast cancer..J Transl Med2018;16:147 PMCID:PMC5977468

[134]

Walker ND,Guiro K,Greco SJ.Exosomes from differentially activated macrophages influence dormancy or resurgence of breast cancer cells within bone marrow stroma..Cell Death Dis2019;10:59 PMCID:PMC6347644

[135]

Schwarzenbach H.Methods for quantification and characterization of microRNAs in cell-free plasma/serum, normal exosomes and tumor-derived exosomes..Transl Cancer Res2018;7 (Suppl 2):253-63

[136]

Livshts MA,Evtushenko EG,Kulemin NA.Isolation of exosomes by differential centrifugation: theoretical analysis of a commonly used protocol..Sci Rep2015;5:17319 PMCID:PMC4663484

[137]

Crowley E,Loupakis F.Liquid biopsy: monitoring cancer-genetics in the blood..Nat Rev Clin Oncol2013;10:472-84

[138]

Perakis S.Emerging concepts in liquid biopsies..BMC Med2017;15:75 PMCID:PMC5382440

[139]

Mimeault M.Molecular biomarkers of cancer stem/progenitor cells associated with progression, metastases, and treatment resistance of aggressive cancers..Cancer Epidemiol Biomarkers Prev2014;23:234-54 PMCID:PMC3977531

[140]

Ostrowski M,Krumeich S,Raposo G.Rab27a and Rab27b control different steps of the exosome secretion pathway..Nat Cell Biol2010;12:19-30

AI Summary AI Mindmap
PDF

136

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/