外泌体源性miRNA在肿瘤发生发展中作用的研究进展
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摘要
外泌体作为细胞间信息交流的重要媒介,可携带蛋白质、脂质、核酸等多种信息物质到受体细胞中,使受体细胞产生不同的生化反应进而调节各项生命活动。近年来大量研究表明,外泌体源性miRNA广泛参与包括肿瘤在内的多种疾病的发生发展。为了更好地了解外泌体源性miRNA对肿瘤发生发展的影响,该文综述了外泌体源性miRNA在肿瘤血管生成、上皮-间质转化、免疫调节、转移前微环境、耐药等方面的作用。
Exosomes, the important cell-cell communication players, can carry a variety of signal molecules, such as proteins, lipids, and nucleic acids, into the recipient cells, allowing these cells to produce different biochemical reactions and regulate various life activities. In recent years, accumulating evidence has demonstrated that exosomal miRNAs participate extensively in the occurrence and development of multiple diseases, including tumors. In this review, we summarized the role of exosomal miRNAs in tumor angiogenesis, epithelial-mesenchymal transition,immunoregulation, pre-metastatic niche, and drug resistance to better understand the effects of exosomal miRNAs on the occurrence and development of tumors.
Exosomes, the important cell-cell communication players, can carry a variety of signal molecules, such as proteins, lipids, and nucleic acids, into the recipient cells, allowing these cells to produce different biochemical reactions and regulate various life activities. In recent years, accumulating evidence has demonstrated that exosomal miRNAs participate extensively in the occurrence and development of multiple diseases, including tumors. In this review, we summarized the role of exosomal miRNAs in tumor angiogenesis, epithelial-mesenchymal transition,immunoregulation, pre-metastatic niche, and drug resistance to better understand the effects of exosomal miRNAs on the occurrence and development of tumors.
引文
[1]Couto N,Caja S,Maia J,et al.Exosomes as emerging players in cancer biology.Biochimie,2018,155:2-10
[2]Hammond SM.An overview of microRNAs.Adv Drug Deliv Rev,2015,87:3-14
[3]Ge Q,Zhou Y,Lu J,et al.miRNA in plasma exosome is stable under different storage conditions.Molecules,2014,19:1568-75
[4]Hunter MP,Ismail N,Zhang X,et al.Detection of microRNA expression in human peripheral blood microvesicles.PLoS One,2008,3:e3694
[5]Wang W,Li DB,Li RY,et al.Diagnosis of hyperacute and acute ischaemic stroke:the potential utility of exosomal microRNA-21-5p and microRNA-30a-5p.Cerebrovasc Dis,2018,45:204-12
[6]Garikipati VNS,Shoja-Taheri F,Davis ME,et al.Extracellular vesicles and the application of system biology and computational modeling in cardiac repair.Circ Res,2018,123:188-204
[7]Yu Y,Bai F,Qin N,et al.Non-proximal renal tubulederived urinary exosomal miR-200b as a biomarker of renal fibrosis.Nephron,2018,139:269-82
[8]Demircioglu F,Hodivala-Dilke K.αvβ3 integrin and tumour blood vessels-learning from the past to shape the future.Curr Opin Cell Biol,2016,42:121-7
[9]Land SC,Tee AR.Hypoxia-inducible factor 1αis regulated by the mammalian target of rapamycin(mTOR)via an mTOR signaling motif.J Biol Chem,2007,282:20534-43
[10]Pakravan K,Babashah S,Sadeghizadeh M,et al.MicroRNA-100 shuttled by mesenchymal stem cellderived exosomes suppresses in vitro angiogenesis through modulating the mTOR/HIF-1α/VEGF signaling axis in breast cancer cells.Cell Oncol(Dordr),2017,40:457-70
[11]Umezu T,Ohyashiki K,Kuroda M,et al.Leukemia cell to endothelial cell communication via exosomal miRNAs.Oncogene,2013,32:2747-55
[12]Bao L,You B,Shi S,et al.Metastasis-associated miR-23a from nasopharyngeal carcinoma-derived exosomes mediates angiogenesis by repressing a novel target gene TSGA10.Oncogene,2018,37:2873-89
[13]Kalluri R,Weinberg RA.The basics of epithelialmesenchymal transition.J Clin Invest,2009,119:1420-8
[14]Blackwell RH,Foreman KE,Gupta GN.The role of cancer-derived exosomes in tumorigenicity&epithelialto-mesenchymal transition.Cancers(Basel),2017,9:E105
[15]Donnarumma E,Fiore D,Nappa M,et al.Cancerassociated fibroblasts release exosomal microRNAs that dictate an aggressive phenotype in breast cancer.Oncotarget,2017,8:19592-608
[16]Bhagirath D,Yang TL,Bucay N,et al.microRNA-1246 is an exosomal biomarker for aggressive prostate cancer.Cancer Res,2018,78:1833-44
[17]Ludwig S,Floros T,Theodoraki MN,et al.Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer.Clin Cancer Res,2017,23:4843-54
[18]Chen G,Huang AC,Zhang W,et al.Exosomal PD-L1contributes to immunosuppression and is associated with anti-PD-1 response.Nature,2018,560:382-6
[19]Berchem G,Noman MZ,Bosseler M,et al.Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-βand miR23a transfer.Oncoimmunology,2016,5:e1062968
[20]Zhao G,Miao H,Li X,et al.TGF-β3-induced miR-494inhibits macrophage polarization via suppressing PGE2secretion in mesenchymal stem cells.FEBS Lett,2016,590:1602-13
[21]Ying X,Wu Q,Wu X,et al.Epithelial ovarian cancersecreted exosomal miR-222-3p induces polarization of tumor-associated macrophages.Oncotarget,2016,7:43076-87
[22]Chen X,Ying X,Wang X,et al.Exosomes derived from hypoxic epithelial ovarian cancer deliver microRNA-940to induce macrophage M2 polarization.Oncol Rep,2017,38:522-8
[23]Liu F,Bu Z,Zhao F,et al.Increased T-helper 17 cell differentiation mediated by exosome-mediated microRNA-451redistribution in gastric cancer infiltrated T cells.Cancer Sci,2018,109:65-73
[24]Zhou J,Li X,Wu X,et al.Exosomes released from tumorassociated macrophages transfer miRNAs that induce a Treg/Th17 cell imbalance in epithelial ovarian cancer.Cancer Immunol Res,2018,6:1578-92
[25]Liu Y,Cao X.Characteristics and significance of the premetastatic niche.Cancer Cell,2016,30:668-81
[26]Zeng Z,Li Y,Pan Y,et al.Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis.Nat Commun,2018,9:5395
[27]Hu Y,Li D,Wu A,et al.TWEAK-stimulated macrophages inhibit metastasis of epithelial ovarian cancer via exosomal shuttling of microRNA.Cancer Lett,2017,393:60-7
[28]Li BL,Lu W,Qu JJ,et al.Loss of exosomal miR-148b from cancer-associated fibroblasts promotes endometrial cancer cell invasion and cancer metastasis.J Cell Physiol,2019,234:2943-53
[29]Bliss SA,Sinha G,Sandiford OA,et al.Mesenchymal stem cell-derived exosomes stimulate cycling quiescence and early breast cancer dormancy in bone marrow.Cancer Res,2016,76:5832-44
[30]Gernapudi R,Yao Y,Zhang Y,et al.Targeting exosomes from preadipocytes inhibits preadipocyte to cancer stem cell signaling in early-stage breast cancer.Breast Cancer Res Treat,2015,150:685-95
[31]Fang T,Lv H,Lv G,et al.Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer.Nat Commun,2018,9:191
[32]Cheng Y,Li H,Deng Y,et al.Cancer-associated fibroblasts induce PDL1+neutrophils through the IL6-STAT3pathway that foster immune suppression in hepatocellular carcinoma.Cell Death Dis,2018,9:422
[33]Dai G,Yao X,Zhang Y,et al.Colorectal cancer cellderived exosomes containing miR-10b regulate fibroblast cells via the PI3K/Akt pathway.Bull Cancer,2018,105:336-49
[34]Liu Y,Zhang J,Sun X,et al.Down-regulation of miR-29b in carcinoma associated fibroblasts promotes cell growth and metastasis of breast cancer.Oncotarget,2017,8:39559-70
[35]Whiteside TL.Exosome and mesenchymal stem cell cross-talk in the tumor microenvironment.Semin Immunol,2018,35:69-79
[36]McBride J,Rodriguez-Menocal L,Guzman W,et al.Bone marrow mesenchymal stem cell-derived CD63 exosomes transport Wnt3a exteriorly and enhance dermal fibroblast proliferation,migration,and angiogenesis in vitro.Stem Cells Dev,2017,26:1384-98
[37]Ma M,Chen S,Liu Z,et al.miRNA-221 of exosomes originating from bone marrow mesenchymal stem cells promotes oncogenic activity in gastric cancer.Onco Targets Ther,2017,10:4161-71
[38]Hashimoto K,Ochi H,Sunamura S,et al.Cancer-secreted hsa-miR-940 induces an osteoblastic phenotype in the bone metastatic microenvironment via targeting ARHGAP1 and FAM134A.Proc Natl Acad Sci USA,2018,115:2204-9
[39]Hsu YL,Hung JY,Chang WA,et al.Hypoxic lung cancersecreted exosomal miR-23a increased angiogenesis and vascular permeability by targeting prolyl hydroxylase and tight junction protein ZO-1.Oncogene,2017,36:4929-42
[40]Casadei L,Calore F,Creighton CJ,et al.Exosome-derived miR-25-3p and miR-92a-3p stimulate liposarcoma progression.Cancer Res,2017,77:3846-56
[41]Parimon T,Brauer R,Schlesinger SY,et al.Syndecan-1controls lung tumorigenesis by regulating miRNAs packaged in exosomes.Am J Pathol,2018,188:1094-103
[42]Kumar B,Garcia M,Weng L,et al.Acute myeloid leukemia transforms the bone marrow niche into a leukemia-permissive microenvironment through exosome secretion.Leukemia,2018,32:575-87
[43]Qin X,Yu S,Xu X,et al.Comparative analysis of microRNA expression profiles between A549,A549/DDPand their respective exosomes.Oncotarget,2017,8:42125-35
[44]Yuwen DL,Sheng BB,Liu J,et al.MiR-146a-5p level in serum exosomes predicts therapeutic effect of cisplatin in non-small cell lung cancer.Eur Rev Med Pharmacol Sci,2017,21:2650-8
[45]Wu H,Zhou J,Mei S,et al.Circulating exosomal microRNA-96 promotes cell proliferation,migration and drug resistance by targeting LMO7.J Cell Mol Med,2017,21:1228-36
[46]Wei F,Ma C,Zhou T,et al.Exosomes derived from gemcitabine-resistant cells transfer malignant phenotypic traits via delivery of miRNA-222-3p.Mol Cancer,2017,16:132
[47]Fu X,Liu M,Qu S,et al.Exosomal microRNA-32-5p induces multidrug resistance in hepatocellular carcinoma via the PI3K/Akt pathway.J Exp Clin Cancer Res,2018,37:52
[48]Fu X,Wen H,Jing L,et al.MicroRNA-155-5p promotes hepatocellular carcinoma progression by suppressing PTEN through the PI3K/Akt pathway.Cancer Sci,2017,108:620-31
[49]Fornari F,Pollutri D,Patrizi C,et al.In hepatocellular carcinoma miR-221 modulates sorafenib resistance through inhibition of caspase-3-mediated apoptosis.Clin Cancer Res,2017,23:3953-65
[50]Zheng P,Chen L,Yuan X,et al.Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells.J Exp Clin Cancer Res,2017,36:53
[51]Wang X,Zhang H,Bai M,et al.Exosomes serve as nanoparticles to deliver anti-miR-214 to reverse chemoresistance to cisplatin in gastric cancer.Mol Ther,2018,26:774-83
[52]Wang M,Qiu R,Yu S,et al.Paclitaxelresistant gastric cancer MGC803 cells promote epithelialtomesenchymal transition and chemoresistance in paclitaxelsensitive cells via exosomal delivery of miR1555p.Int J Oncol,2019,54:326-38
[53]Patel GK,Khan MA,Bhardwaj A,et al.Exosomes confer chemoresistance to pancreatic cancer cells by promoting ROS detoxification and miR-155-mediated suppression of key gemcitabine-metabolising enzyme,DCK.Br J Cancer,2017,116:609-19
[54]Binenbaum Y,Fridman E,Yaari Z,et al.Transfer of miRNA in macrophage-derived exosomes induces drug resistance in pancreatic adenocarcinoma.Cancer Res,2018,78:5287-99
[55]Mikamori M,Yamada D,Eguchi H,et al.MicroRNA-155controls exosome synthesis and promotes gemcitabine resistance in pancreatic ductal adenocarcinoma.Sci Rep,2017,7:42339
[2]Hammond SM.An overview of microRNAs.Adv Drug Deliv Rev,2015,87:3-14
[3]Ge Q,Zhou Y,Lu J,et al.miRNA in plasma exosome is stable under different storage conditions.Molecules,2014,19:1568-75
[4]Hunter MP,Ismail N,Zhang X,et al.Detection of microRNA expression in human peripheral blood microvesicles.PLoS One,2008,3:e3694
[5]Wang W,Li DB,Li RY,et al.Diagnosis of hyperacute and acute ischaemic stroke:the potential utility of exosomal microRNA-21-5p and microRNA-30a-5p.Cerebrovasc Dis,2018,45:204-12
[6]Garikipati VNS,Shoja-Taheri F,Davis ME,et al.Extracellular vesicles and the application of system biology and computational modeling in cardiac repair.Circ Res,2018,123:188-204
[7]Yu Y,Bai F,Qin N,et al.Non-proximal renal tubulederived urinary exosomal miR-200b as a biomarker of renal fibrosis.Nephron,2018,139:269-82
[8]Demircioglu F,Hodivala-Dilke K.αvβ3 integrin and tumour blood vessels-learning from the past to shape the future.Curr Opin Cell Biol,2016,42:121-7
[9]Land SC,Tee AR.Hypoxia-inducible factor 1αis regulated by the mammalian target of rapamycin(mTOR)via an mTOR signaling motif.J Biol Chem,2007,282:20534-43
[10]Pakravan K,Babashah S,Sadeghizadeh M,et al.MicroRNA-100 shuttled by mesenchymal stem cellderived exosomes suppresses in vitro angiogenesis through modulating the mTOR/HIF-1α/VEGF signaling axis in breast cancer cells.Cell Oncol(Dordr),2017,40:457-70
[11]Umezu T,Ohyashiki K,Kuroda M,et al.Leukemia cell to endothelial cell communication via exosomal miRNAs.Oncogene,2013,32:2747-55
[12]Bao L,You B,Shi S,et al.Metastasis-associated miR-23a from nasopharyngeal carcinoma-derived exosomes mediates angiogenesis by repressing a novel target gene TSGA10.Oncogene,2018,37:2873-89
[13]Kalluri R,Weinberg RA.The basics of epithelialmesenchymal transition.J Clin Invest,2009,119:1420-8
[14]Blackwell RH,Foreman KE,Gupta GN.The role of cancer-derived exosomes in tumorigenicity&epithelialto-mesenchymal transition.Cancers(Basel),2017,9:E105
[15]Donnarumma E,Fiore D,Nappa M,et al.Cancerassociated fibroblasts release exosomal microRNAs that dictate an aggressive phenotype in breast cancer.Oncotarget,2017,8:19592-608
[16]Bhagirath D,Yang TL,Bucay N,et al.microRNA-1246 is an exosomal biomarker for aggressive prostate cancer.Cancer Res,2018,78:1833-44
[17]Ludwig S,Floros T,Theodoraki MN,et al.Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer.Clin Cancer Res,2017,23:4843-54
[18]Chen G,Huang AC,Zhang W,et al.Exosomal PD-L1contributes to immunosuppression and is associated with anti-PD-1 response.Nature,2018,560:382-6
[19]Berchem G,Noman MZ,Bosseler M,et al.Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-βand miR23a transfer.Oncoimmunology,2016,5:e1062968
[20]Zhao G,Miao H,Li X,et al.TGF-β3-induced miR-494inhibits macrophage polarization via suppressing PGE2secretion in mesenchymal stem cells.FEBS Lett,2016,590:1602-13
[21]Ying X,Wu Q,Wu X,et al.Epithelial ovarian cancersecreted exosomal miR-222-3p induces polarization of tumor-associated macrophages.Oncotarget,2016,7:43076-87
[22]Chen X,Ying X,Wang X,et al.Exosomes derived from hypoxic epithelial ovarian cancer deliver microRNA-940to induce macrophage M2 polarization.Oncol Rep,2017,38:522-8
[23]Liu F,Bu Z,Zhao F,et al.Increased T-helper 17 cell differentiation mediated by exosome-mediated microRNA-451redistribution in gastric cancer infiltrated T cells.Cancer Sci,2018,109:65-73
[24]Zhou J,Li X,Wu X,et al.Exosomes released from tumorassociated macrophages transfer miRNAs that induce a Treg/Th17 cell imbalance in epithelial ovarian cancer.Cancer Immunol Res,2018,6:1578-92
[25]Liu Y,Cao X.Characteristics and significance of the premetastatic niche.Cancer Cell,2016,30:668-81
[26]Zeng Z,Li Y,Pan Y,et al.Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis.Nat Commun,2018,9:5395
[27]Hu Y,Li D,Wu A,et al.TWEAK-stimulated macrophages inhibit metastasis of epithelial ovarian cancer via exosomal shuttling of microRNA.Cancer Lett,2017,393:60-7
[28]Li BL,Lu W,Qu JJ,et al.Loss of exosomal miR-148b from cancer-associated fibroblasts promotes endometrial cancer cell invasion and cancer metastasis.J Cell Physiol,2019,234:2943-53
[29]Bliss SA,Sinha G,Sandiford OA,et al.Mesenchymal stem cell-derived exosomes stimulate cycling quiescence and early breast cancer dormancy in bone marrow.Cancer Res,2016,76:5832-44
[30]Gernapudi R,Yao Y,Zhang Y,et al.Targeting exosomes from preadipocytes inhibits preadipocyte to cancer stem cell signaling in early-stage breast cancer.Breast Cancer Res Treat,2015,150:685-95
[31]Fang T,Lv H,Lv G,et al.Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer.Nat Commun,2018,9:191
[32]Cheng Y,Li H,Deng Y,et al.Cancer-associated fibroblasts induce PDL1+neutrophils through the IL6-STAT3pathway that foster immune suppression in hepatocellular carcinoma.Cell Death Dis,2018,9:422
[33]Dai G,Yao X,Zhang Y,et al.Colorectal cancer cellderived exosomes containing miR-10b regulate fibroblast cells via the PI3K/Akt pathway.Bull Cancer,2018,105:336-49
[34]Liu Y,Zhang J,Sun X,et al.Down-regulation of miR-29b in carcinoma associated fibroblasts promotes cell growth and metastasis of breast cancer.Oncotarget,2017,8:39559-70
[35]Whiteside TL.Exosome and mesenchymal stem cell cross-talk in the tumor microenvironment.Semin Immunol,2018,35:69-79
[36]McBride J,Rodriguez-Menocal L,Guzman W,et al.Bone marrow mesenchymal stem cell-derived CD63 exosomes transport Wnt3a exteriorly and enhance dermal fibroblast proliferation,migration,and angiogenesis in vitro.Stem Cells Dev,2017,26:1384-98
[37]Ma M,Chen S,Liu Z,et al.miRNA-221 of exosomes originating from bone marrow mesenchymal stem cells promotes oncogenic activity in gastric cancer.Onco Targets Ther,2017,10:4161-71
[38]Hashimoto K,Ochi H,Sunamura S,et al.Cancer-secreted hsa-miR-940 induces an osteoblastic phenotype in the bone metastatic microenvironment via targeting ARHGAP1 and FAM134A.Proc Natl Acad Sci USA,2018,115:2204-9
[39]Hsu YL,Hung JY,Chang WA,et al.Hypoxic lung cancersecreted exosomal miR-23a increased angiogenesis and vascular permeability by targeting prolyl hydroxylase and tight junction protein ZO-1.Oncogene,2017,36:4929-42
[40]Casadei L,Calore F,Creighton CJ,et al.Exosome-derived miR-25-3p and miR-92a-3p stimulate liposarcoma progression.Cancer Res,2017,77:3846-56
[41]Parimon T,Brauer R,Schlesinger SY,et al.Syndecan-1controls lung tumorigenesis by regulating miRNAs packaged in exosomes.Am J Pathol,2018,188:1094-103
[42]Kumar B,Garcia M,Weng L,et al.Acute myeloid leukemia transforms the bone marrow niche into a leukemia-permissive microenvironment through exosome secretion.Leukemia,2018,32:575-87
[43]Qin X,Yu S,Xu X,et al.Comparative analysis of microRNA expression profiles between A549,A549/DDPand their respective exosomes.Oncotarget,2017,8:42125-35
[44]Yuwen DL,Sheng BB,Liu J,et al.MiR-146a-5p level in serum exosomes predicts therapeutic effect of cisplatin in non-small cell lung cancer.Eur Rev Med Pharmacol Sci,2017,21:2650-8
[45]Wu H,Zhou J,Mei S,et al.Circulating exosomal microRNA-96 promotes cell proliferation,migration and drug resistance by targeting LMO7.J Cell Mol Med,2017,21:1228-36
[46]Wei F,Ma C,Zhou T,et al.Exosomes derived from gemcitabine-resistant cells transfer malignant phenotypic traits via delivery of miRNA-222-3p.Mol Cancer,2017,16:132
[47]Fu X,Liu M,Qu S,et al.Exosomal microRNA-32-5p induces multidrug resistance in hepatocellular carcinoma via the PI3K/Akt pathway.J Exp Clin Cancer Res,2018,37:52
[48]Fu X,Wen H,Jing L,et al.MicroRNA-155-5p promotes hepatocellular carcinoma progression by suppressing PTEN through the PI3K/Akt pathway.Cancer Sci,2017,108:620-31
[49]Fornari F,Pollutri D,Patrizi C,et al.In hepatocellular carcinoma miR-221 modulates sorafenib resistance through inhibition of caspase-3-mediated apoptosis.Clin Cancer Res,2017,23:3953-65
[50]Zheng P,Chen L,Yuan X,et al.Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells.J Exp Clin Cancer Res,2017,36:53
[51]Wang X,Zhang H,Bai M,et al.Exosomes serve as nanoparticles to deliver anti-miR-214 to reverse chemoresistance to cisplatin in gastric cancer.Mol Ther,2018,26:774-83
[52]Wang M,Qiu R,Yu S,et al.Paclitaxelresistant gastric cancer MGC803 cells promote epithelialtomesenchymal transition and chemoresistance in paclitaxelsensitive cells via exosomal delivery of miR1555p.Int J Oncol,2019,54:326-38
[53]Patel GK,Khan MA,Bhardwaj A,et al.Exosomes confer chemoresistance to pancreatic cancer cells by promoting ROS detoxification and miR-155-mediated suppression of key gemcitabine-metabolising enzyme,DCK.Br J Cancer,2017,116:609-19
[54]Binenbaum Y,Fridman E,Yaari Z,et al.Transfer of miRNA in macrophage-derived exosomes induces drug resistance in pancreatic adenocarcinoma.Cancer Res,2018,78:5287-99
[55]Mikamori M,Yamada D,Eguchi H,et al.MicroRNA-155controls exosome synthesis and promotes gemcitabine resistance in pancreatic ductal adenocarcinoma.Sci Rep,2017,7:42339
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