Immunomodulatory role of EV-derived non-coding RNA in lung cancer

Patrizia Ghidotti , Ilaria Petraroia , Orazio Fortunato , Francesca Pontis

Extracellular Vesicles and Circulating Nucleic Acids ›› 2023, Vol. 4 ›› Issue (1) : 59 -71.

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Extracellular Vesicles and Circulating Nucleic Acids ›› 2023, Vol. 4 ›› Issue (1) :59 -71. DOI: 10.20517/evcna.2022.42
Review

Immunomodulatory role of EV-derived non-coding RNA in lung cancer

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Abstract

Lung cancer is the deadliest cancer worldwide, primarily because of its metastatic spread. Extracellular vesicles (EVs) are small lipid-bilayer particles released by almost all types of cells. EVs play fundamental roles in cell-cell communication and cell-environment interactions by carrying proteins, nucleic acids such as DNA and RNA (mRNAs, lncRNAs, and miRNAs), and other bioactive molecules that are able to influence the behaviour of recipient cells. EVs have been described as key players in the modulation of tumour progression and the anticancer immune response. In this review, we highlight current knowledge on the role of non-coding RNAs in the modulation of the immune response, focusing on lung cancer. Since EVs are fundamental cell-to-cell mediators, we discuss the current knowledge on the immunomodulatory properties of tumour-derived EVs and, in particular, their ncRNA cargo during the different phases of lung cancer development and progression.

Keywords

Extracellular vesicles / microRNA / lung cancer / immune cells

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Patrizia Ghidotti, Ilaria Petraroia, Orazio Fortunato, Francesca Pontis. Immunomodulatory role of EV-derived non-coding RNA in lung cancer. Extracellular Vesicles and Circulating Nucleic Acids, 2023, 4(1): 59-71 DOI:10.20517/evcna.2022.42

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References

[1]

Siegel RL,Fuchs HE.Cancer statistics, 2022.CA Cancer J Clin2022;72:7-33

[2]

Goldstraw P,Crowley J.International Association for the Study of Lung Cancer Staging and Prognostic Factors Committee, Advisory Boards and Participating InstitutionsInternational Association for the Study of Lung Cancer Staging and Prognostic Factors Committee Advisory Boards and Participating InstitutionsThe IASLC Lung Cancer Staging Project: proposals for revision of the TNM stage groupings in the forthcoming (Eighth) edition of the TNM classification for lung cancer.J Thorac Oncol2016;11:39-51

[3]

Duma N,Molina JR.Non-small cell lung cancer: epidemiology, screening, diagnosis, and treatment.Mayo Clin Proc2019;94:1623-40

[4]

Hirsch FR,Mulshine JL.Lung cancer: current therapies and new targeted treatments.Lancet2017;389:299-311

[5]

Tartarone A,Di Micco C.Beyond conventional: the new horizon of targeted therapy for the treatment of advanced non small cell lung cancer.Front Oncol2021;11:632256 PMCID:PMC8176852

[6]

Takeda M.First- and second-generation EGFR-TKIs are all replaced to osimertinib in chemo-naive EGFR mutation-positive non-small cell lung cancer?.Int J Mol Sci2019;20:146 PMCID:PMC6337322

[7]

Grant MJ,Goldberg SB.Selecting the optimal immunotherapy regimen in driver-negative metastatic NSCLC.Nat Rev Clin Oncol2021;18:625-44

[8]

Reck M,Robinson AG.Five-year outcomes with pembrolizumab versus chemotherapy for metastatic non-small-cell lung cancer with PD-L1 tumor proportion score ≥ 50.J Clin Oncol2021;39:2339-49 PMCID:PMC8280089

[9]

Altorki NK,Gao D.The lung microenvironment: an important regulator of tumour growth and metastasis.Nat Rev Cancer2019;19:9-31 PMCID:PMC6749995

[10]

Barbazán J.Cancer associated fibroblasts: Is the force the path to the dark side?.Curr Opin Cell Biol2019;56:71-9

[11]

Kargl J,Yang GH.Neutrophils dominate the immune cell composition in non-small cell lung cancer.Nat Commun2017;8:14381 PMCID:PMC5296654

[12]

Maia J,Strano Moraes MC,Costa-Silva B.Exosome-based cell-cell communication in the tumor microenvironment.Front Cell Dev Biol2018;6:18 PMCID:PMC5826063

[13]

Wang M,Ding H,Li P.Emerging function and clinical values of exosomal MicroRNAs in cancer.Mol Ther Nucleic Acids2019;16:791-804 PMCID:PMC6545365

[14]

Dai J,Zhong S.Exosomes: key players in cancer and potential therapeutic strategy.Signal Transduct Target Ther2020;5:145 PMCID:PMC7406508

[15]

Palucka AK.The basis of oncoimmunology.Cell2016;164:1233-47 PMCID:PMC4788788

[16]

Peng D,Nagarsheth N.Epigenetic silencing of TH1-type chemokines shapes tumour immunity and immunotherapy.Nature2015;527:249-53 PMCID:PMC4779053

[17]

Vesely MD,Schreiber RD.Natural innate and adaptive immunity to cancer.Annu Rev Immunol2011;29:235-71

[18]

Liu Y.Cancer and innate immune system interactions: translational potentials for cancer immunotherapy.J Immunother2012;35:299-308 PMCID:PMC3331796

[19]

Schreiber RD,Smyth MJ.Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion.Science2011;331:1565-70

[20]

Pardoll DM.The blockade of immune checkpoints in cancer immunotherapy.Nat Rev Cancer2012;12:252-64 PMCID:PMC4856023

[21]

Lavin Y,Leader A.Innate immune landscape in early lung adenocarcinoma by paired single-cell analyses.Cell2017;169:750-765.e17 PMCID:PMC5737939

[22]

Durrans A,Gupta R.Identification of reprogrammed myeloid cell transcriptomes in NSCLC.PLoS One2015;10:e0129123 PMCID:PMC4457876

[23]

Kim N,Lee K.Single-cell RNA sequencing demonstrates the molecular and cellular reprogramming of metastatic lung adenocarcinoma.Nat Commun2020;11:2285 PMCID:PMC7210975

[24]

Anastasiadou E,Slack FJ.Non-coding RNA networks in cancer.Nat Rev Cancer2018;18:5-18 PMCID:PMC6337726

[25]

Esteller M.Non-coding RNAs in human disease.Nat Rev Genet2011;12:861-74

[26]

Wu KL,Lien CT,Hung AJ.The roles of microRNA in lung cancer.Int J Mol Sci2019;20:1611 PMCID:PMC6480472

[27]

Li Z.Therapeutic targeting of microRNAs: current status and future challenges.Nat Rev Drug Discov2014;13:622-38

[28]

Nana-Sinkam SP.Clinical applications for microRNAs in cancer.Clin Pharmacol Ther2013;93:98-104

[29]

Slack FJ.The role of non-coding RNAs in oncology.Cell2019;179:1033-55 PMCID:PMC7347159

[30]

Chen L,Goswami S.Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression.Nat Commun2014;5:5241 PMCID:PMC4212319

[31]

Fujita Y,Hagiwara K.The clinical relevance of the miR-197/CKS1B/STAT3-mediated PD-L1 network in chemoresistant non-small-cell lung cancer.Mol Ther2015;23:717-27 PMCID:PMC4395779

[32]

Tang D,Wu Y.The miR-3127-5p/p-STAT3 axis up-regulates PD-L1 inducing chemoresistance in non-small-cell lung cancer.J Cell Mol Med2018;22:3847-56 PMCID:PMC6050495

[33]

Sage AP,Marshall EA.Assessment of long non-coding RNA expression reveals novel mediators of the lung tumour immune response.Sci Rep2020;10:16945 PMCID:PMC7547676

[34]

Sun Y.TCF-4 regulated lncRNA-XIST promotes M2 polarization of macrophages and is associated with lung cancer.Onco Targets Ther2019;12:8055-62 PMCID:PMC6781636

[35]

Li Z,Guo J,Xie D.GNAS-AS1/miR-4319/NECAB3 axis promotes migration and invasion of non-small cell lung cancer cells by altering macrophage polarization.Funct Integr Genomics2020;20:17-28

[36]

Tian X,Wang T.Corrigendum: long non-coding RNA HOXA transcript antisense RNA myeloid-specific 1-HOXA1 axis downregulates the immunosuppressive activity of myeloid-derived suppressor cells in lung cancer.Front Immunol2019;10:2929 PMCID:PMC6985904

[37]

Wu J,Li KS,Zhang PF.Circular RNA drives resistance to anti-PD-1 immunotherapy by regulating the miR-30a-5p/SOX4 axis in non-small cell lung cancer.Cancer Drug Resist2022;5:261-70 PMCID:PMC9255236

[38]

Yang J,Wang B.Circular RNA CHST15 sponges miR-155-5p and miR-194-5p to promote the immune escape of lung cancer cells mediated by PD-L1.Front Oncol2021;11:595609 PMCID:PMC7991744

[39]

Mathieu M,Lavieu G.Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication.Nat Cell Biol2019;21:9-17

[40]

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

[41]

Niel G,Clayton A,Raposo G.Challenges and directions in studying cell-cell communication by extracellular vesicles.Nat Rev Mol Cell Biol2022;23:369-82

[42]

Peinado H,Matei IR.Pre-metastatic niches: organ-specific homes for metastases.Nat Rev Cancer2017;17:302-17

[43]

Becker A,Weiss JM,Peinado H.Extracellular vesicles in cancer: cell-to-cell mediators of metastasis.Cancer Cell2016;30:836-48 PMCID:PMC5157696

[44]

Jella KK,Li Z,Buchwald ZS.Exosomes, their biogenesis and role in inter-cellular communication, tumor microenvironment and cancer immunotherapy.Vaccines (Basel)2018;6:69 PMCID:PMC6313856

[45]

Zhang L,He Z,Li H.Multi-functional extracellular vesicles: potentials in cancer immunotherapy.Cancer Lett2022;551:215934

[46]

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

[47]

Serratì S,Di Fonte R.Circulating extracellular vesicles expressing PD1 and PD-L1 predict response and mediate resistance to checkpoint inhibitors immunotherapy in metastatic melanoma.Mol Cancer2022;21:20 PMCID:PMC8764806

[48]

Chen G,Zhang W.Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response.Nature2018;560:382-6 PMCID:PMC6095740

[49]

Zhang W,Wang B.ICAM-1-mediated adhesion is a prerequisite for exosome-induced T cell suppression.Dev Cell2022;57:329-343.e7 PMCID:PMC8881799

[50]

Ohue Y.Regulatory T (Treg) cells in cancer: can Treg cells be a new therapeutic target?.Cancer Sci2019;110:2080-9 PMCID:PMC6609813

[51]

Nakazawa Y,Koizumi H,Nakahashi-Oda C.Tumor-derived extracellular vesicles regulate tumor-infiltrating regulatory T cells via the inhibitory immunoreceptor CD300a.Elife2021;10 PMCID:PMC8577836

[52]

Swatler J,Brewinska-Olchowik M.4-1BBL-containing leukemic extracellular vesicles promote immunosuppressive effector regulatory T cells.Blood Adv2022;6:1879-94 PMCID:PMC8941461

[53]

Haderk F,Iskar M.Tumor-derived exosomes modulate PD-L1 expression in monocytes.Sci Immunol2017;2:eaah5509

[54]

Vignard V,Marec N.MicroRNAs in tumor exosomes drive immune escape in melanoma.Cancer Immunol Res2020;8:255-67

[55]

Shinohara H,Kumazaki M.Regulated polarization of tumor-associated macrophages by miR-145 via colorectal cancer-derived extracellular vesicles.J Immunol2017;199:1505-15

[56]

Xun J,Gao R.Cancer-derived exosomal miR-138-5p modulates polarization of tumor-associated macrophages through inhibition of KDM6B.Theranostics2021;11:6847-59 PMCID:PMC8171095

[57]

Zhang C,Gao Y.Radiated glioblastoma cell-derived exosomal circ_0012381 induce M2 polarization of microglia to promote the growth of glioblastoma by CCL2/CCR2 axis.J Transl Med2022;20:388 PMCID:PMC9441045

[58]

Menay F,De Toro J.Exosomes isolated from ascites of T-Cell lymphoma-bearing mice expressing surface CD24 and HSP-90 induce a tumor-specific immune response.Front Immunol2017;8:286 PMCID:PMC5352668

[59]

Daßler-Plenker J,van den Boorn JG.RIG-I activation induces the release of extracellular vesicles with antitumor activity.Oncoimmunology2016;5:e1219827 PMCID:PMC5087302

[60]

Ma J,Zhang H.Mechanisms by which dendritic cells present tumor microparticle antigens to CD8+ T cells.Cancer Immunol Res2018;6:1057-68

[61]

Okoye IS,Pelly VS.MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells.Immunity2014;41:89-103 PMCID:PMC4104030

[62]

He G,Wei S.Exosomes in the hypoxic TME: from release, uptake and biofunctions to clinical applications.Mol Cancer2022;21:19 PMCID:PMC8762953

[63]

Berchem G,Bosseler M.Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-β and miR23a transfer.Oncoimmunology2016;5:e1062968 PMCID:PMC4839360

[64]

Fan X,Qin T.Exosome miR-27a-3p secreted from adipocytes targets ICOS to promote antitumor immunity in lung adenocarcinoma.Thorac Cancer2020;11:1453-64 PMCID:PMC7262893

[65]

Peng XX,Wu X.Correlation of plasma exosomal microRNAs with the efficacy of immunotherapy in EGFR/ALK wild-type advanced non-small cell lung cancer.J Immunother Cancer2020;8:e000376 PMCID:PMC7057418

[66]

Pontis F,Mensah M.Circulating extracellular vesicles from individuals at high-risk of lung cancer induce pro-tumorigenic conversion of stromal cells through transfer of miR-126 and miR-320.J Exp Clin Cancer Res2021;40:237 PMCID:PMC8293562

[67]

Cortez MA,Valdecanas D.PDL1 regulation by p53 via miR-34.J Natl Cancer Inst2016;108:djv303 PMCID:PMC4862407

[68]

Xie WB,Wu KG.MiR-140 expression regulates cell proliferation and targets PD-L1 in NSCLC.Cell Physiol Biochem2018;46:654-63

[69]

Yin Y,Chen X.Tumor-secreted miR-214 induces regulatory T cells: a major link between immune evasion and tumor growth.Cell Res2014;24:1164-80 PMCID:PMC4185347

[70]

Fan T,He J.Exosome-derived LncRNAs in lung cancer.Front Oncol2020;10:1728 PMCID:PMC7538687

[71]

Wang S,Zhu R,Zhao RC.Lung cancer exosomes initiate global long non-coding RNA changes in mesenchymal stem cells.Int J Oncol2016;48:681-9

[72]

Conway EM,Kung SH.Macrophages, inflammation, and lung cancer.Am J Respir Crit Care Med2016;193:116-30

[73]

Chen J,Zhang H.Macrophages reprogrammed by lung cancer microparticles promote tumor development via release of IL-1β.Cell Mol Immunol2020;17:1233-44 PMCID:PMC7784894

[74]

Lv J,Ma R.Long Noncoding RNA FGD5-AS1 knockdown decrease viability, migration, and invasion of non-small cell lung cancer (NSCLC) cells by regulating the microRNA-944/MACC1 axis.Technol Cancer Res Treat2021;20:1533033821990090 PMCID:PMC7887693

[75]

Ni J,Li J.Correction: tumour-derived exosomal lncRNA-SOX2OT promotes bone metastasis of non-small cell lung cancer by targeting the miRNA-194-5p/RAC1 signalling axis in osteoclasts.Cell Death Dis2021;12:1131 PMCID:PMC8648893

[76]

Zhou R,Wang W.Circular RNAs (circRNAs) in cancer.Cancer Lett2018;425:134-42

[77]

Li Y,Bao C.Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis.Cell Res2015;25:981-4 PMCID:PMC4528056

[78]

Hussen BM,Hama Faraj GS.Exosomal circular RNA: a signature for lung cancer progression.Cancer Cell Int2022;22:378 PMCID:PMC9714134

[79]

Hong W,Jiang J,Gao X.Circular RNA circ-CPA4/ let-7 miRNA/PD-L1 axis regulates cell growth, stemness, drug resistance and immune evasion in non-small cell lung cancer (NSCLC).J Exp Clin Cancer Res2020;39:149 PMCID:PMC7397626

[80]

Wang J,Wang Y.circRNA-002178 act as a ceRNA to promote PDL1/PD1 expression in lung adenocarcinoma.Cell Death Dis2020;11:32 PMCID:PMC6965119

[81]

Katopodi T,Domvri K.Kras-driven intratumoral heterogeneity triggers infiltration of M2 polarized macrophages via the circHIPK3/PTK2 immunosuppressive circuit.Sci Rep2021;11:15455 PMCID:PMC8322174

[82]

Liu Y,Song X.Exosomal circPVT1 derived from lung cancer promotes the progression of lung cancer by targeting miR-124-3p/EZH2 axis and regulating macrophage polarization.Cell Cycle2022;21:514-30 PMCID:PMC8942510

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