Intercellular transfer of multidrug resistance mediated by extracellular vesicles

Anxiang Yang , Hui Sun , Xiaokun Wang

Cancer Drug Resistance ›› 2024, Vol. 7 : 36

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Cancer Drug Resistance ›› 2024, Vol. 7 :36 DOI: 10.20517/cdr.2024.84
review-article

Intercellular transfer of multidrug resistance mediated by extracellular vesicles

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Abstract

Multidrug resistance (MDR) poses a formidable obstacle in cancer treatment, enabling cancer cells to evade the cytotoxic effects of chemotherapeutic drugs through various mechanisms. These mechanisms include intrinsic resistance, which is present prior to treatment, and acquired resistance, which develops after exposure to chemotherapy agents. Small membrane-bound vesicles, known as extracellular vesicles (EVs), are crucial in intercellular signaling as they transport bioactive molecules that can modify the characteristics and functions of recipient cells. Recent research highlights EVs as pivotal players in fostering drug resistance. This review focuses on the intercellular transfer of MDR from donor cells to susceptible recipient cells through specific cargo in EVs, such as ATP-binding cassette (ABC) transporter proteins, nucleic acids, and other regulatory factors. Additionally, the features of intercellular communication mediated by EVs are also discussed. Gaining insight into these mechanisms is essential for developing strategies to counteract resistance and improve the effectiveness of cancer treatments.

Keywords

Multidrug resistance / extracellular vesicles / intercellular transfer / intercellular communication / ABC transporter

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Anxiang Yang, Hui Sun, Xiaokun Wang. Intercellular transfer of multidrug resistance mediated by extracellular vesicles. Cancer Drug Resistance, 2024, 7: 36 DOI:10.20517/cdr.2024.84

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References

[1]

György B,Pásztói M.Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles.Cell Mol Life Sci2011;68:2667-88 PMCID:PMC3142546

[2]

Gurung S,Touramanidou L.The exosome journey: from biogenesis to uptake and intracellular signalling.Cell Commun Signal2021;19:47 PMCID:PMC8063428

[3]

Skog J,van Rijn S.Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers.Nat Cell Biol2008;10:1470-6 PMCID:PMC3423894

[4]

Peinado H,Lavotshkin S.Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET.Nat Med2012;18:883-91 PMCID:PMC3645291

[5]

Ratajczak J,Kucia M.Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery.Leukemia2006;20:847-56

[6]

Minciacchi VR,Di Vizio D.Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes.Semin Cell Dev Biol2015;40:41-51 PMCID:PMC4747631

[7]

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

[8]

Yang Q,Gu J.Extracellular vesicles in cancer drug resistance: roles, mechanisms, and implications.Adv Sci2022;9:e2201609 PMCID:PMC9731723

[9]

Wang D,Xu F.Cisplatin-resistant NSCLC cells induced by hypoxia transmit resistance to sensitive cells through exosomal PKM2.Theranostics2021;11:2860-75 PMCID:PMC7806469

[10]

Marar C,Wirtz D.Extracellular vesicles in immunomodulation and tumor progression.Nat Immunol2021;22:560-70 PMCID:PMC9389600

[11]

Gould SJ.As we wait: coping with an imperfect nomenclature for extracellular vesicles.J Extracell Vesicles2013;2:20389 PMCID:PMC3760635

[12]

Hessvik NP.Current knowledge on exosome biogenesis and release.Cell Mol Life Sci2018;75:193-208 PMCID:PMC5756260

[13]

Théry C,Aikawa E.Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines.J Extracell Vesicles2018;7:1535750 PMCID:PMC6322352

[14]

Bayraktar R,Calin GA.Cell-to-cell communication: microRNAs as hormones.Mol Oncol2017;11:1673-86 PMCID:PMC5709614

[15]

Battistelli M.Apoptotic bodies: particular extracellular vesicles involved in intercellular communication.Biology2020;9:21 PMCID:PMC7168913

[16]

Pavlyukov MS,Bastola S.Apoptotic cell-derived extracellular vesicles promote malignancy of glioblastoma via intercellular transfer of splicing factors.Cancer Cell2018;34:119-35.e10 PMCID:PMC6048596

[17]

Poon IKH,Jiang L.Moving beyond size and phosphatidylserine exposure: evidence for a diversity of apoptotic cell-derived extracellular vesicles in vitro.J Extracell Vesicles2019;8:1608786 PMCID:PMC6493268

[18]

Dieudé M,Turgeon J.The 20S proteasome core, active within apoptotic exosome-like vesicles, induces autoantibody production and accelerates rejection.Sci Transl Med2015;7:318ra200

[19]

Escola JM,Stoorvogel W,Yoshie O.Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes.J Biol Chem1998;273:20121-7

[20]

Tkach M,Théry C.Why the need and how to approach the functional diversity of extracellular vesicles.Philos Trans R Soc Lond B Biol Sci2018;373:20160479 PMCID:PMC5717434

[21]

Andreu Z.Tetraspanins in extracellular vesicle formation and function.Front Immunol2014;5:442 PMCID:PMC4165315

[22]

Yanatori I,Dhekne HS,Kishi F.CD63 is regulated by iron via the IRE-IRP system and is important for ferritin secretion by extracellular vesicles.Blood2021;138:1490-503 PMCID:PMC8667049

[23]

Yoshioka Y,Kosaka N,Kato T.Comparative marker analysis of extracellular vesicles in different human cancer types.J Extracell Vesicles2013;2:20424 PMCID:PMC3760642

[24]

Keerthikumar S,Ariyaratne D.ExoCarta: a web-based compendium of exosomal cargo.J Mol Biol2016;428:688-92 PMCID:PMC4783248

[25]

Pathan M,Chitti SV.Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles.Nucleic Acids Res2019;47:D516-9 PMCID:PMC6323905

[26]

Skotland T,Llorente A.Lipids in exosomes: current knowledge and the way forward.Prog Lipid Res2017;66:30-41

[27]

Pegtel DM.Exosomes.Annu Rev Biochem2019;88:487-514

[28]

Donoso-Quezada J,González-Valdez J.The role of lipids in exosome biology and intercellular communication: Function, analytics and applications.Traffic2021;22:204-20 PMCID:PMC8361711

[29]

Dixson AC,Di Vizio D.Context-specific regulation of extracellular vesicle biogenesis and cargo selection.Nat Rev Mol Cell Biol2023;24:454-76 PMCID:PMC10330318

[30]

van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles.Nat Rev Mol Cell Biol2018;19:213-28

[31]

Del Conde I, Shrimpton CN, Thiagarajan P, López JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation.Blood2005;106:1604-11

[32]

Wilson KF,Antonyak MA.Rho GTPases and their roles in cancer metabolism.Trends Mol Med2013;19:74-82 PMCID:PMC3607349

[33]

Milman N,Gil Z.Exosomes and their role in tumorigenesis and anticancer drug resistance.Drug Resist Updat2019;45:1-12

[34]

Colombo M,Théry C.Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles.Annu Rev Cell Dev Biol2014;30:255-89

[35]

Zhang X,Shi H,Qian H.Exosomes in cancer: small particle, big player.J Hematol Oncol2015;8:83 PMCID:PMC4496882

[36]

Mulcahy LA,Carter DRF.Routes and mechanisms of extracellular vesicle uptake.J Extracell Vesicles2014;3:24641 PMCID:PMC4122821

[37]

Antebi YE,Elowitz MB.An operational view of intercellular signaling pathways.Curr Opin Syst Biol2017;1:16-24 PMCID:PMC5665397

[38]

Fu W,Liu S.CAR exosomes derived from effector CAR-T cells have potent antitumour effects and low toxicity.Nat Commun2019;10:4355 PMCID:PMC6761190

[39]

Al-Nedawi K,Micallef J.Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells.Nat Cell Biol2008;10:619-24

[40]

Li F,Sun R.EGFR-rich extracellular vesicles derived from highly metastatic nasopharyngeal carcinoma cells accelerate tumour metastasis through PI3K/AKT pathway-suppressed ROS.J Extracell Vesicles2020;10:e12003 PMCID:PMC7710133

[41]

Le MTN,Guo C.miR-200-containing extracellular vesicles promote breast cancer cell metastasis.J Clin Invest2014;124:5109-28 PMCID:PMC4348969

[42]

Melo SA,O’Connell JT.Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis.Cancer Cell2014;26:707-21 PMCID:PMC4254633

[43]

Qin X,Zhou L.Cisplatin-resistant lung cancer cell-derived exosomes increase cisplatin resistance of recipient cells in exosomal miR-100-5p-dependent manner.Int J Nanomedicine2017;12:3721-33 PMCID:PMC5439933

[44]

Mikamori M,Eguchi H.MicroRNA-155 controls exosome synthesis and promotes gemcitabine resistance in pancreatic ductal adenocarcinoma.Sci Rep2017;7:42339 PMCID:PMC5309735

[45]

Wei F,Zhou T.Exosomes derived from gemcitabine-resistant cells transfer malignant phenotypic traits via delivery of miRNA-222-3p.Mol Cancer2017;16:132 PMCID:PMC5526308

[46]

Zhang H,Li W,Xiong S.CD4+ T cell-released exosomes inhibit CD8+ cytotoxic T-lymphocyte responses and antitumor immunity.Cell Mol Immunol2011;8:23-30 PMCID:PMC4002994

[47]

Ying W,Bandyopadhyay G.Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity.Cell2017;171:372-84.e12

[48]

Chen JJ,Zhao J.Potential roles of exosomal microRNAs as diagnostic biomarkers and therapeutic application in Alzheimer’s disease.Neural Plast2017;2017:7027380 PMCID:PMC5523215

[49]

Morel L,Higashimori H.Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1.J Biol Chem2013;288:7105-16 PMCID:PMC3591620

[50]

Poe AJ.Exosomes as agents of change in the cardiovascular system.J Mol Cell Cardiol2017;111:40-50 PMCID:PMC5600701

[51]

Leroyer AS,Lesèche G.Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques.J Am Coll Cardiol2007;49:772-7

[52]

Boulanger CM,Rautou PE.Extracellular vesicles in coronary artery disease.Nat Rev Cardiol2017;14:259-72

[53]

Chen X,Wang X,Zhu Q.Exosomes derived from hypoxic epithelial ovarian cancer deliver microRNA-940 to induce macrophage M2 polarization.Oncol Rep2017;38:522-8

[54]

Zhao S,Guan B.Tumor-derived exosomal miR-934 induces macrophage M2 polarization to promote liver metastasis of colorectal cancer.J Hematol Oncol2020;13:156 PMCID:PMC7678301

[55]

Qiu S,Lu C.Gastric cancer-derived exosomal miR-519a-3p promotes liver metastasis by inducing intrahepatic M2-like macrophage-mediated angiogenesis.J Exp Clin Cancer Res2022;41:296 PMCID:PMC9549645

[56]

Hosseini R,Yousefi H.The roles of tumor-derived exosomes in altered differentiation, maturation and function of dendritic cells.Mol Cancer2021;20:83 PMCID:PMC8170799

[57]

Zhang PF,Huang XY.Cancer cell-derived exosomal circUHRF1 induces natural killer cell exhaustion and may cause resistance to anti-PD1 therapy in hepatocellular carcinoma.Mol Cancer2020;19:110 PMCID:PMC7320583

[58]

Greening DW,Chen M.Secreted primary human malignant mesothelioma exosome signature reflects oncogenic cargo.Sci Rep2016;6:32643 PMCID:PMC5015102

[59]

Zhao H,Baddour J.Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism.Elife2016;5:e10250 PMCID:PMC4841778

[60]

Al-Nedawi K,Kerbel RS,Rak J.Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR.Proc Natl Acad Sci U S A2009;106:3794-9 PMCID:PMC2656159

[61]

Wu Q,Nie Y,Fan D.Multi-drug resistance in cancer chemotherapeutics: mechanisms and lab approaches.Cancer Lett2014;347:159-66

[62]

Mansoori B,Davudian S,Baradaran B.The different mechanisms of cancer drug resistance: a brief review.Adv Pharm Bull2017;7:339-48 PMCID:PMC5651054

[63]

Nathanson DA,Mottahedeh J.Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA.Science2014;343:72-6 PMCID:PMC4049335

[64]

Kreso A,van Galen P.Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer.Science2013;339:543-8 PMCID:PMC9747244

[65]

Arora VK,Murali R.Glucocorticoid receptor confers resistance to antiandrogens by bypassing androgen receptor blockade.Cell2013;155:1309-22 PMCID:PMC3932525

[66]

Gatenby RA,Brown JS.Evolutionary dynamics of cancer prevention.Nat Rev Cancer2010;10:526-7 PMCID:PMC3744108

[67]

Gong J,Jaiswal R,Grau GE.Microparticle drug sequestration provides a parallel pathway in the acquisition of cancer drug resistance.Eur J Pharmacol2013;721:116-25

[68]

Bach DH,Park HJ.The role of exosomes and miRNAs in drug-resistance of cancer cells.Int J Cancer2017;141:220-30

[69]

Sharma A.Chemoresistance in cancer cells: exosomes as potential regulators of therapeutic tumor heterogeneity.Nanomedicine2017;12:2137-48

[70]

Camussi G,Bruno S,Fonsato V.Exosome/microvesicle-mediated epigenetic reprogramming of cells.Am J Cancer Res2011;1:98-110 PMCID:PMC3180104

[71]

Duvivier L,Diaz A.Linking ABC transporters to the hallmarks of cancer.Trends Cancer2024;10:124-34

[72]

Quazi F,Molday RS.ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer.Nat Commun2012;3:925 PMCID:PMC3871175

[73]

Kitai K,Tomohiro T,So T.The lysosomal protein ABCD4 can transport vitamin B12 across liposomal membranes in vitro.J Biol Chem2021;296:100654 PMCID:PMC8113721

[74]

Gerovac M.Control of mRNA translation by versatile ATP-driven machines.Trends Biochem Sci2019;44:167-80

[75]

Moitra K,Dean M.Multidrug efflux pumps and cancer stem cells: insights into multidrug resistance and therapeutic development.Clin Pharmacol Ther2011;89:491-502

[76]

Dong J,Hu C,Qin JJ.Strategies to overcome cancer multidrug resistance (MDR) through targeting P-glycoprotein (ABCB1): an updated review.Pharmacol Ther2023;249:108488

[77]

Amiri-Kordestani L,Kurdziel K,Bates SE.Targeting MDR in breast and lung cancer: discriminating its potential importance from the failure of drug resistance reversal studies.Drug Resist Updat2012;15:50-61 PMCID:PMC3680361

[78]

Levchenko A,Niu X.Intercellular transfer of P-glycoprotein mediates acquired multidrug resistance in tumor cells.Proc Natl Acad Sci U S A2005;102:1933-8 PMCID:PMC545583

[79]

Rafii A,Poupot M.Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumours.PLoS One2008;3:e3894 PMCID:PMC2597737

[80]

Bebawy M,Lee E.Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells.Leukemia2009;23:1643-9

[81]

Corcoran C,O’Brien K.Docetaxel-resistance in prostate cancer: evaluating associated phenotypic changes and potential for resistance transfer via exosomes.PLoS One2012;7:e50999 PMCID:PMC3519481

[82]

Jaiswal R,Dalla PV,Bebawy M.Breast cancer-derived microparticles display tissue selectivity in the transfer of resistance proteins to cells.PLoS One2013;8:e61515 PMCID:PMC3625154

[83]

Lv M,Chen W.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

[84]

Pasquier J,Boulangé-Lecomte C.Different modalities of intercellular membrane exchanges mediate cell-to-cell p-glycoprotein transfers in MCF-7 breast cancer cells.J Biol Chem2012;287:7374-87 PMCID:PMC3293537

[85]

Pokharel D,Lu JF.Proteome analysis of multidrug-resistant, breast cancer-derived microparticles.J Extracell Vesicles2014;3:24384 PMCID:PMC4142226

[86]

Zhou H,Cheng X.Intercellular transfer of P-glycoprotein from the drug resistant human bladder cancer cell line BIU-87 does not require cell-to-cell contact.J Urol2013;190:1069-75

[87]

Cheng XZ,Tang SX.Intercellular transfer of P-glycoprotein mediates the formation of stable multi-drug resistance in human bladder cancer BIU-87 cells.Biol Open2019;8:bio041889 PMCID:PMC6550073

[88]

Zhang F,Zhao Q.Microvesicles mediate transfer of P-glycoprotein to paclitaxel-sensitive A2780 human ovarian cancer cells, conferring paclitaxel-resistance.Eur J Pharmacol2014;738:83-90

[89]

Torreggiani E,Perut F,Baldini N.Multimodal transfer of MDR by exosomes in human osteosarcoma.Int J Oncol2016;49:189-96

[90]

Wang X,Chen L.Chemotherapeutic drugs stimulate the release and recycling of extracellular vesicles to assist cancer cells in developing an urgent chemoresistance.Mol Cancer2019;18:182 PMCID:PMC6907227

[91]

Jaiswal R,Bebawy M.Cellular communication via microparticles: role in transfer of multidrug resistance in cancer.Future Oncol2014;10:655-69

[92]

Norris MD,Marshall GM,Cohn SL.Expression of the gene for multidrug-resistance-associated protein and outcome in patients with neuroblastoma.N Engl J Med1996;334:231-8

[93]

Nooter K,Klijn J,Foekens J.Multidrug resistance protein in recurrent breast cancer.Lancet1997;349:1885-6

[94]

Lu JF,Gong J,Grau GE.Microparticles mediate MRP1 intercellular transfer and the re-templating of intrinsic resistance pathways.Pharmacol Res2013;76:77-83

[95]

Bouvy C,Laloy J,Dogné JM.Transfer of multidrug resistance among acute myeloid leukemia cells via extracellular vesicles and their microRNA cargo.Leuk Res2017;62:70-6

[96]

Taylor NMI,Jackson SM,Stahlberg H.Structure of the human multidrug transporter ABCG2.Nature2017;546:504-9

[97]

Hou YX,Palaniyandi K.Effects of putative catalytic base mutation E211Q on ABCG2-mediated methotrexate transport.Biochemistry2009;48:9122-31 PMCID:PMC2770347

[98]

Robey RW,Polgar O.ABCG2: a perspective.Adv Drug Deliv Rev2009;61:3-13 PMCID:PMC3105088

[99]

Patch AM, Christie EL, Etemadmoghadam D, et al; Australian Ovarian Cancer Study Group. Whole-genome characterization of chemoresistant ovarian cancer. Nature 2015;521:489-94.

[100]

Ifergan I,Assaraf YG.Novel extracellular vesicles mediate an ABCG2-dependent anticancer drug sequestration and resistance.Cancer Res2005;65:10952-8

[101]

Ifergan I,Assaraf YG.Riboflavin concentration within ABCG2-rich extracellular vesicles is a novel marker for multidrug resistance in malignant cells.Biochem Biophys Res Commun2009;380:5-10

[102]

Goler-Baron V.Structure and function of ABCG2-rich extracellular vesicles mediating multidrug resistance.PLoS One2011;6:e16007 PMCID:PMC3025911

[103]

Goler-Baron V,Assaraf YG.Inhibition of the PI3K-Akt signaling pathway disrupts ABCG2-rich extracellular vesicles and overcomes multidrug resistance in breast cancer cells.Biochem Pharmacol2012;83:1340-8

[104]

Gajos-Michniewicz A,Czyz M.MiRNA in melanoma-derived exosomes.Cancer Lett2014;347:29-37

[105]

Bang C.Exosomes: new players in cell-cell communication.Int J Biochem Cell Biol2012;44:2060-4

[106]

Jaiswal R,Sambasivam S.Microparticle-associated nucleic acids mediate trait dominance in cancer.FASEB J2012;26:420-9

[107]

Zhuang L,Liu X.Exosomal miR-21-5p derived from cisplatin-resistant SKOV3 ovarian cancer cells promotes glycolysis and inhibits chemosensitivity of its progenitor SKOV3 cells by targeting PDHA1.Cell Biol Int2021;45:2140-9

[108]

Zhu T,Wang Z.microRNA-301b-3p from mesenchymal stem cells-derived extracellular vesicles inhibits TXNIP to promote multidrug resistance of gastric cancer cells.Cell Biol Toxicol2023;39:1923-37

[109]

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

[110]

Natasha G,Tan A.Exosomes as immunotheranostic nanoparticles.Clin Ther2014;36:820-9

[111]

Munoz JL,Greco SJ,Ligon KL.Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity.Mol Ther Nucleic Acids2013;2:e126 PMCID:PMC4027430

[112]

Cui X,Zhao L.Extracellular vesicles derived from paclitaxel-sensitive nasopharyngeal carcinoma cells deliver miR-183-5p and impart paclitaxel sensitivity through a mechanism involving P-gp.Cell Biol Toxicol2023;39:2953-70

[113]

Ma X,Hua D.Essential role for TrpC5-containing extracellular vesicles in breast cancer with chemotherapeutic resistance.Proc Natl Acad Sci U S A2014;111:6389-94 PMCID:PMC4035923

[114]

Wu S,To KKW.Intercellular transfer of exosomal wild type EGFR triggers osimertinib resistance in non-small cell lung cancer.Mol Cancer2021;20:17 PMCID:PMC7812728

[115]

Vella LJ,Coleman B,Hill AF.Intercellular resistance to BRAF inhibition can be mediated by extracellular vesicle-associated PDGFRβ.Neoplasia2017;19:932-40 PMCID:PMC5678363

[116]

Ji R,Zhang X.Exosomes derived from human mesenchymal stem cells confer drug resistance in gastric cancer.Cell Cycle2015;14:2473-83 PMCID:PMC4613597

[117]

Qu Z,Wu J,Jiang C.Exosomes derived from HCC cells induce sorafenib resistance in hepatocellular carcinoma both in vivo and in vitro.J Exp Clin Cancer Res2016;35:159 PMCID:PMC5045585

[118]

Wojtuszkiewicz A,Kessler FL.Exosomes secreted by apoptosis-resistant acute myeloid leukemia (AML) blasts harbor regulatory network proteins potentially involved in antagonism of apoptosis.Mol Cell Proteomics2016;15:1281-98 PMCID:PMC4824855

[119]

Kreger BT,Cerione RA.The enrichment of survivin in exosomes from breast cancer cells treated with paclitaxel promotes cell survival and chemoresistance.Cancers2016;8:111 PMCID:PMC5187509

[120]

Lopes-Rodrigues V,Mleczko J.Identification of the metabolic alterations associated with the multidrug resistant phenotype in cancer and their intercellular transfer mediated by extracellular vesicles.Sci Rep2017;7:44541 PMCID:PMC5356019

[121]

Sullivan R,Zhang X.The emerging roles of extracellular vesicles as communication vehicles within the tumor microenvironment and beyond.Front Endocrinol2017;8:194 PMCID:PMC5550719

[122]

Xing F,Watabe K.Cancer associated fibroblasts (CAFs) in tumor microenvironment.Front Biosci2010;15:166-79 PMCID:PMC2905156

[123]

Richards KE,Fishel ML,Littlepage LE.Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells.Oncogene2017;36:1770-8 PMCID:PMC5366272

[124]

Hekmatirad S,Moghadamnia AA.Inhibition of exosome release sensitizes U937 cells to PEGylated liposomal doxorubicin.Front Immunol2021;12:692654 PMCID:PMC8212994

[125]

Muralidharan-Chari V,Asimakopoulos AG.Microvesicle removal of anticancer drugs contributes to drug resistance in human pancreatic cancer cells.Oncotarget2016;7:50365-79 PMCID:PMC5226588

[126]

Federici C,Caimi S.Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin.PLoS One2014;9:e88193 PMCID:PMC3916404

[127]

Atai NA,van Veen H.Heparin blocks transfer of extracellular vesicles between donor and recipient cells.J Neurooncol2013;115:343-51 PMCID:PMC3856724

[128]

Yamazaki S,Maruyama A.Uptake of collagen type I via macropinocytosis cause mTOR activation and anti-cancer drug resistance.Biochem Biophys Res Commun2020;526:191-8

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