Exosomal circular RNAs in tumor microenvironment: An emphasis on signaling pathways and clinical opportunities

Junshu Li , Wencheng Zhou , Huiling Wang , Meijuan Huang , Hongxin Deng

MedComm ›› 2024, Vol. 5 ›› Issue (12) : e70019

PDF
MedComm ›› 2024, Vol. 5 ›› Issue (12) : e70019 DOI: 10.1002/mco2.70019
REVIEW

Exosomal circular RNAs in tumor microenvironment: An emphasis on signaling pathways and clinical opportunities

Author information +
History +
PDF

Abstract

Exosomes can regulate the malignant progression of tumors by carrying a variety of genetic information and transmitting it to target cells. Recent studies indicate that exosomal circular RNAs (circRNAs) regulate multiple biological processes in carcinogenesis, such as tumor growth, metastasis, epithelial–mesenchymal transition, drug resistance, autophagy, metabolism, angiogenesis, and immune escape. In the tumor microenvironment (TME), exosomal circRNAs can be transferred among tumor cells, endothelial cells, cancer-associated fibroblasts, immune cells, and microbiota, affecting tumor initiation and progression. Due to the high stability and widespread presence of exosomal circRNAs, they hold promise as biomarkers for tumor diagnosis and prognosis prediction in blood and urine. In addition, designing nanoparticles targeting exosomal circRNAs and utilizing exosomal circRNAs derived from immune cells or stem cells provide new strategies for cancer therapy. In this review, we examined the crucial role of exosomal circRNAs in regulating tumor-related signaling pathways and summarized the transmission of exosomal circRNAs between various types of cells and their impact on the TME. Finally, our review highlights the potential of exosomal circRNAs as diagnostic and prognostic prediction biomarkers, as well as suggesting new strategies for clinical therapy.

Keywords

biomarker / circRNA / exosome / tumor microenvironment / tumor therapy

Cite this article

Download citation ▾
Junshu Li, Wencheng Zhou, Huiling Wang, Meijuan Huang, Hongxin Deng. Exosomal circular RNAs in tumor microenvironment: An emphasis on signaling pathways and clinical opportunities. MedComm, 2024, 5(12): e70019 DOI:10.1002/mco2.70019

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Cao M, Li H, Sun D, et al. Cancer burden of major cancers in China: a need for sustainable actions. Cancer Commun. 2020; 40(5): 205-210.

[2]

Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2024; 74(3): 229-263.

[3]

Siegel RL, Giaquinto AN, Jemal A. Cancer statistics, 2024. CA Cancer J Clin. 2024; 74(1): 12-49.

[4]

Schafer EJ, Jemal A, Wiese D, et al. Disparities and trends in genitourinary cancer incidence and mortality in the USA. Eur Urol. 2023; 84(1): 117-126.

[5]

Boehmer U, Chang S, Sanchez NF, et al. Cancer survivors’ health behaviors and outcomes: a population-based study of sexual and gender minorities. J Natl Cancer Inst. 2023; 115(10): 1164-1170.

[6]

Shelton J, Zotow E, Smith L, et al. 25 year trends in cancer incidence and mortality among adults aged 35–69 years in the UK, 1993–2018: retrospective secondary analysis. Bmj. 2024; 384.

[7]

Lin Z, Ji Y, Zhou J, et al. Exosomal circRNAs in cancer: implications for therapy resistance and biomarkers. Cancer Lett. 2023:216245.

[8]

Lauwers E, Wang Y-C, Gallardo R, et al. Hsp90 mediates membrane deformation and exosome release. Mol Cell. 2018; 71(5): 689-702.e9.

[9]

Deng J, Liao S, Chen C, et al. Specific intracellular retention of circSKA3 promotes colorectal cancer metastasis by attenuating ubiquitination and degradation of SLUG. Cell Death Dis. 2023; 14(11): 750.

[10]

Du WW, Yang W, Li X, et al. The circular RNA circSKA3 binds integrin β1 to induce invadopodium formation enhancing breast cancer invasion. Mol Ther. 2020; 28(5): 1287-1298.

[11]

Liu Q-W, He Y, Xu WW. Molecular functions and therapeutic applications of exosomal noncoding RNAs in cancer. Exp Mol Med. 2022; 54(3): 216-225.

[12]

Pisignano G, Michael DC, Visal TH, et al. Going circular: history, present, and future of circRNAs in cancer. Oncogene. 2023; 42(38): 2783-2800.

[13]

Lin H, Wang Y, Wang P, et al. Mutual regulation between N6-methyladenosine (m6A) modification and circular RNAs in cancer: impacts on therapeutic resistance. Mol Cancer. 2022; 21(1): 148.

[14]

Li J, Zhang G, Liu C-G, et al. The potential role of exosomal circRNAs in the tumor microenvironment: insights into cancer diagnosis and therapy. Theranostics. 2022; 12(1): 87.

[15]

Xu H-Z, Lin X-Y, Xu Y-X, et al. An emerging research: the role of hepatocellular carcinoma-derived exosomal circRNAs in the immune microenvironment. Front Immunol. 2023; 14: 1227150.

[16]

De Visser KE, Joyce JA. The evolving tumor microenvironment: from cancer initiation to metastatic outgrowth. Cancer Cell. 2023; 41(3): 374-403.

[17]

Xu Z, Chen Y, Ma L, et al. Role of exosomal non-coding RNAs from tumor cells and tumor-associated macrophages in the tumor microenvironment. Mol Ther. 2022; 30(10): 3133-3154.

[18]

Zhang Y, Luo J, Yang W, et al. CircRNAs in colorectal cancer: potential biomarkers and therapeutic targets. Cell Death Dis. 2023; 14(6): 353.

[19]

Zhou W, Zhou Y, Chen X, et al. Pancreatic cancer-targeting exosomes for enhancing immunotherapy and reprogramming tumor microenvironment. Biomaterials. 2021; 268: 120546.

[20]

Elahi FM, Farwell DG, Nolta JA, et al. Preclinical translation of exosomes derived from mesenchymal stem/stromal cells. Stem Cells. 2020; 38(1): 15-21.

[21]

Greening DW, Xu R, Ale A, et al. Extracellular vesicles as next generation immunotherapeutics. Semin Cancer Biol. 2023; 90: 73-100.

[22]

Liu Z, Wang T, She Y, et al. N 6-methyladenosine-modified circIGF2BP3 inhibits CD8+ T-cell responses to facilitate tumor immune evasion by promoting the deubiquitination of PD-L1 in non-small cell lung cancer. Mol Cancer. 2021; 20: 1-25.

[23]

Hui B, Zhou C, Xu Y, et al. Exosomes secreted by Fusobacterium nucleatum-infected colon cancer cells transmit resistance to oxaliplatin and 5-FU by delivering hsa_circ_0004085. J Nanobiotechnol. 2024; 22(1): 62.

[24]

Yi Q, Yue J, Liu Y, et al. Recent advances of exosomal circRNAs in cancer and their potential clinical applications. J Transl Med. 2023; 21(1): 516.

[25]

Xian J, Su W, Liu L, et al. Identification of three circular RNA cargoes in serum exosomes as diagnostic biomarkers of non–small-cell lung cancer in the chinese population. J Mol Diagn. 2020; 22(8): 1096-1108.

[26]

Li J, Zhang Y, Dong P-Y, et al. A comprehensive review on the composition, biogenesis, purification, and multifunctional role of exosome as delivery vehicles for cancer therapy. Biomed Pharmacother. 2023; 165: 115087.

[27]

Xie H, Yao J, Wang Y, et al. Exosome-transmitted circVMP1 facilitates the progression and cisplatin resistance of non-small cell lung cancer by targeting miR-524-5p-METTL3/SOX2 axis. Drug Deliv. 2022; 29(1): 1257-1271.

[28]

Zeng W, Liu Y, Li WT, et al. CircFNDC3B sequestrates miR-937-5p to derepress TIMP3 and inhibit colorectal cancer progression. Mol Oncol. 2020; 14(11): 2960-2984.

[29]

Wang X, Zhang H, Yang H, et al. Exosome-delivered circRNA promotes glycolysis to induce chemoresistance through the miR-122-PKM2 axis in colorectal cancer. Mol Oncol. 2020; 14(3): 539-555.

[30]

Cheng L, Hill AF. Therapeutically harnessing extracellular vesicles. Nat Rev Drug Discov. 2022; 21(5): 379-399.

[31]

Hendrix A, Lippens L, Pinheiro C, et al. Extracellular vesicle analysis. Nat Rev Method Prime. 2023; 3(1): 56.

[32]

Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020; 367(6478): eaau6977.

[33]

Mashouri L, Yousefi H, Aref AR, et al. Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer. 2019; 18: 1-14.

[34]

Tuo B, Chen Z, Dang Q, et al. Roles of exosomal circRNAs in tumour immunity and cancer progression. Cell Death Dis. 2022; 13(6): 539.

[35]

Yan H, Li Y, Cheng S, et al. Advances in analytical technologies for extracellular vesicles. Anal Chem. 2021; 93(11): 4739-4774.

[36]

Dong J, Zeng Z, Sun R, et al. Specific and sensitive detection of CircRNA based on netlike hybridization chain reaction. Biosens Bioelectron. 2021; 192: 113508.

[37]

Dong J, Zeng Z, Huang Y, et al. Challenges and opportunities for circRNA identification and delivery. Crit Rev Biochem Mol. 2023; 58(1): 19-35.

[38]

Lee JU, Kim WH, Lee HS, et al. Quantitative and specific detection of exosomal miRNAs for accurate diagnosis of breast cancer using a surface-enhanced Raman scattering sensor based on plasmonic head-flocked gold nanopillars. Small. 2019; 15(17): 1804968.

[39]

Van Niel G, d’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018; 19(4): 213-228.

[40]

Marar C, Starich B, Wirtz D. Extracellular vesicles in immunomodulation and tumor progression. Nat Immunol. 2021; 22(5): 560-570.

[41]

Maacha S, Bhat AA, Jimenez L, et al. Extracellular vesicles-mediated intercellular communication: roles in the tumor microenvironment and anti-cancer drug resistance. Mol Cancer. 2019; 18: 1-16.

[42]

Aloi N, Drago G, Ruggieri S, et al. Extracellular vesicles and immunity: at the crossroads of cell communication. Int J Mol Sci. 2024; 25(2): 1205.

[43]

Stoorvogel W, Strous GJ, Geuze HJ, et al. Late endosomes derive from early endosomes by maturation. Cell. 1991; 65(3): 417-427.

[44]

Liu J, Ren L, Li S, et al. The biology, function, and applications of exosomes in cancer. Acta Pharm Sin B. 2021; 11(9): 2783-2797.

[45]

Kogure A, Yoshioka Y, Ochiya T. Extracellular vesicles in cancer metastasis: potential as therapeutic targets and materials. Int J Mol Sci. 2020; 21(12): 4463.

[46]

Vu LT, Gong J, Pham TT, et al. MicroRNA exchange via extracellular vesicles in cancer. Cell Prolif. 2020; 53(11): e12877.

[47]

Wang H-X, Gires O. Tumor-derived extracellular vesicles in breast cancer: from bench to bedside. Cancer Lett. 2019; 460: 54-64.

[48]

Sil S, Dagur RS, Liao K, et al. Strategies for the use of extracellular vesicles for the delivery of therapeutics. J Neuroimmune Pharm. 2020; 15: 422-442.

[49]

Eguchi T, Sheta M, Fujii M, et al. Cancer extracellular vesicles, tumoroid models, and tumor microenvironment. Semin Cancer Biol. 2022; 86: 112-126.

[50]

Adnani L, Spinelli C, Tawil N, et al. Role of extracellular vesicles in cancer-specific interactions between tumour cells and the vasculature. Semin Cancer Biol. 2022; 87: 196-213.

[51]

Zhou E, Li Y, Wu F, et al. Circulating extracellular vesicles are effective biomarkers for predicting response to cancer therapy. EBioMedicine. 2021; 67: 103365.

[52]

Calvo V, Izquierdo M. T lymphocyte and CAR-T cell-derived extracellular vesicles and their applications in cancer therapy. Cells. 2022; 11(5): 790.

[53]

Shi Y, Lu Y, You J. Antigen transfer and its effect on vaccine-induced immune amplification and tolerance. Theranostics. 2022; 12(13): 5888.

[54]

Zhang H, Xie Y, Li W, et al. CD4+ T cell-released exosomes inhibit CD8+ cytotoxic T-lymphocyte responses and antitumor immunity. Cell Mol Immunol. 2011; 8(1): 23-30.

[55]

Martinez-Usatorre A, De Palma M. Dendritic cell cross-dressing and tumor immunity. EMBO Mol Med. 2022; 14(10): e16523.

[56]

Kristensen LS, Andersen MS, Stagsted LV, et al. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019; 20(11): 675-691.

[57]

Zhou W-Y, Cai Z-R, Liu J, et al. Circular RNA: metabolism, functions and interactions with proteins. Mol Cancer. 2020; 19: 1-19.

[58]

Beilerli A, Gareev I, Beylerli O, et al. Circular RNAs as biomarkers and therapeutic targets in cancer. Semin Cancer Biol. 2022; 83: 242-252.

[59]

Li F, Yang Q, He AT, et al. Circular RNAs in cancer: limitations in functional studies and diagnostic potential. Semin Cancer Biol. 2021; 75: 49-61.

[60]

Xu X, Zhang J, Tian Y, et al. CircRNA inhibits DNA damage repair by interacting with host gene. Mol Cancer. 2020; 19: 1-19.

[61]

Conn VM, Gabryelska M, Toubia J, et al. Circular RNAs drive oncogenic chromosomal translocations within the MLL recombinome in leukemia. Cancer Cell. 2023; 41(7): 1309-1326.e10.

[62]

Conn VM, Chinnaiyan AM, Conn SJ. Circular RNA in cancer. Nat Rev Cancer. 2024: 1-17.

[63]

Kristensen LS, Jakobsen T, Hager H, et al. The emerging roles of circRNAs in cancer and oncology. Nat Rev Clin Oncol. 2022; 19(3): 188-206.

[64]

Fu B, Liu W, Zhu C, et al. Circular RNA circBCBM1 promotes breast cancer brain metastasis by modulating miR-125a/BRD4 axis. Int J of Biol Sci. 2021; 17(12): 3104.

[65]

Li H, Jiao W, Song J, et al. circ-hnRNPU inhibits NONO-mediated c-Myc transactivation and mRNA stabilization essential for glycosylation and cancer progression. J Exp Clin Cancer Res. 2023; 42(1): 313.

[66]

Chen C-K, Cheng R, Demeter J, et al. Structured elements drive extensive circular RNA translation. Mol Cell. 2021; 81(20): 4300-4318.e13.

[67]

Zhang F, Jiang J, Qian H, et al. Exosomal circRNA: emerging insights into cancer progression and clinical application potential. J Hematol Oncol. 2023; 16(1): 67.

[68]

Corrado C, Barreca MM, Zichittella C, et al. Molecular mediators of RNA loading into extracellular vesicles. Cells. 2021; 10(12): 3355.

[69]

Teng Y, Ren Y, Hu X, et al. MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nat Commun. 2017; 8(1): 14448.

[70]

He T, Zhang Q, Xu P, et al. Extracellular vesicle-circEHD2 promotes the progression of renal cell carcinoma by activating cancer-associated fibroblasts. Mol Cancer. 2023; 22(1): 117.

[71]

Ghossoub R, Chéry M, Audebert S, et al. Tetraspanin-6 negatively regulates exosome production. Proc Natl Acad Sci USA. 2020; 117(11): 5913-5922.

[72]

Zhou X, Hong Y, Liu Y, et al. Intervening in hnRNPA2B1-mediated exosomal transfer of tumor-suppressive miR-184-3p for tumor microenvironment regulation and cancer therapy. J Nanobiotechnol. 2023; 21(1): 422.

[73]

Yao Y, Chen C, Wang J, et al. Circular RNA circATP9A promotes non-small cell lung cancer progression by interacting with HuR and by promoting extracellular vesicles-mediated macrophage M2 polarization. J Exp Clin Cancer Res. 2023; 42(1): 330.

[74]

Pan Z, Zhao R, Li B, et al. EWSR1-induced circNEIL3 promotes glioma progression and exosome-mediated macrophage immunosuppressive polarization via stabilizing IGF2BP3. Mol Cancer. 2022; 21(1): 16.

[75]

Ma R-J, Ma C, Hu K, et al. Molecular mechanism, regulation, and therapeutic targeting of the STAT3 signaling pathway in esophageal cancer. Int J Oncol. 2022; 61(3): 1-21.

[76]

Ashrafizadeh M, Mohan CD, Rangappa S, et al. Noncoding RNAs as regulators of STAT3 pathway in gastrointestinal cancers: roles in cancer progression and therapeutic response. Med Res Rev. 2023; 43(5): 1263-1321.

[77]

Liu S, Li W, Liang L, et al. The regulatory relationship between transcription factor STAT3 and noncoding RNA. Cell Mol Biol Lett. 2024; 29(1): 4.

[78]

Li C-J, Li D-G, Liu E-J, et al. Circ8199 encodes a protein that inhibits the activity of OGT by JAK2-STAT3 pathway in esophageal squamous cell carcinoma. Am J Cancer Res. 2023; 13(3): 1107.

[79]

Hashemi M, Nadafzadeh N, Imani MH, et al. Targeting and regulation of autophagy in hepatocellular carcinoma: revisiting the molecular interactions and mechanisms for new therapy approaches. Cell Commun Signal. 2023; 21(1): 32.

[80]

Song J, Liu Q, Han L, et al. Hsa_circ_0009092/miR-665/NLK signaling axis suppresses colorectal cancer progression via recruiting TAMs in the tumor microenvironment. J Exp Clin Cancer Res. 2023; 42(1): 319.

[81]

Zheng X, Huang M, Xing L, et al. The circRNA circSEPT9 mediated by E2F1 and EIF4A3 facilitates the carcinogenesis and development of triple-negative breast cancer. Mol Cancer. 2020; 19: 1-22.

[82]

Wu S, Lu J, Zhu H, et al. A novel axis of circKIF4A-miR-637-STAT3 promotes brain metastasis in triple-negative breast cancer. Cancer Lett. 2024; 581: 216508.

[83]

Li Z, Ruan Y, Zhang H, et al. Tumor-suppressive circular RNAs: mechanisms underlying their suppression of tumor occurrence and use as therapeutic targets. Cancer Sci. 2019; 110(12): 3630-3638.

[84]

Zhang Y, Li C, Liu X, et al. circHIPK3 promotes oxaliplatin-resistance in colorectal cancer through autophagy by sponging miR-637. EBioMedicine. 2019; 48: 277-288.

[85]

Yin H, Tang Q, Xia H, et al. Targeting RAF dimers in RAS mutant tumors: from biology to clinic. Acta Pharm Sin B. 2024; 14(5): 1895-1923.

[86]

Klomp JE, Diehl JN, Klomp JA, et al. Determining the ERK-regulated phosphoproteome driving KRAS-mutant cancer. Science. 2024; 384(6700): eadk0850.

[87]

Timofeev O, Giron P, Lawo S, et al. ERK pathway agonism for cancer therapy: evidence, insights, and a target discovery framework. NPJ Precis Oncol. 2024; 8(1): 70.

[88]

Meier C, La Rocca G, Nawrot V, et al. Erk inhibition as a promising therapeutic strategy for high IL-8-secreting and low SPTAN1-expressing colorectal cancer. Int J Mol Sci. 2024; 25(11): 5658.

[89]

Klomp JA, Klomp JE, Stalnecker CA, et al. Defining the KRAS-and ERK-dependent transcriptome in KRAS-mutant cancers. Science. 2024; 384(6700): eadk0775.

[90]

Dong L, Choi H, Budhu S, et al. Intermittent MEK inhibition with GITR co-stimulation rescues T-cell function for increased efficacy with CTLA-4 blockade in solid tumor models. Cancer Immunol Res. 2024; 12(10): 1392-1408.

[91]

Lee S, Rauch J, Kolch W. Targeting MAPK signaling in cancer: mechanisms of drug resistance and sensitivity. Int J Mol Sci. 2020; 21(3): 1102.

[92]

Du J, Lan T, Liao H, et al. CircNFIB inhibits tumor growth and metastasis through suppressing MEK1/ERK signaling in intrahepatic cholangiocarcinoma. Mol Cancer. 2022; 21(1): 18.

[93]

Cui Y, Wu X, Jin J, et al. CircHERC1 promotes non-small cell lung cancer cell progression by sequestering FOXO1 in the cytoplasm and regulating the miR-142-3p-HMGB1 axis. Mol Cancer. 2023; 22(1): 179.

[94]

Shen Y, Zhang N, Chai J, et al. CircPDIA4 induces gastric cancer progression by promoting ERK1/2 activation and enhancing biogenesis of oncogenic circRNAs. Cancer Res. 2023; 83(4): 538-552.

[95]

Lyu Y, Tan B, Li L, et al. A novel protein encoded by circUBE4B promotes progression of esophageal squamous cell carcinoma by augmenting MAPK/ERK signaling. Cell Death Dis. 2023; 14(6): 346.

[96]

Zhang F, Wei D, Xie S, et al. CircZCCHC2 decreases pirarubicin sensitivity and promotes triple-negative breast cancer development via the miR-1200/TPR axis. Iscience. 2024; 27(3).

[97]

Huang W, Hu X, He X, et al. TRIM29 facilitates gemcitabine resistance via MEK/ERK pathway and is modulated by circRPS29/miR-770–5p axis in PDAC. Drug Resist Update. 2024; 74: 101079.

[98]

Liu S, Wang Y, Wang T, et al. CircPCNXL2 promotes tumor growth and metastasis by interacting with STRAP to regulate ERK signaling in intrahepatic cholangiocarcinoma. Mol Cancer. 2024; 23(1): 35.

[99]

Revathidevi S, Munirajan AK. Akt in cancer: mediator and more. Semin Cancer Biol. 2019; 59: 80-91.

[100]

Pal I, Mandal M. PI3K and Akt as molecular targets for cancer therapy: current clinical outcomes. Acta Pharmacol Sin. 2012; 33(12): 1441-1458.

[101]

Li P, Huang D, Gu X. Exploring the dual role of circRNA and PI3K/AKT pathway in tumors of the digestive system. Biomed Pharmacother. 2023; 168: 115694.

[102]

Yan S, Chen L, Zhuang H, et al. HDAC inhibition sensitize hepatocellular carcinoma to lenvatinib via suppressing AKT activation. Int J Biol Sci. 2024; 20(8): 3046.

[103]

Huang B, Ren J, Ma Q, et al. A novel peptide PDHK1-241aa encoded by circPDHK1 promotes ccRCC progression via interacting with PPP1CA to inhibit AKT dephosphorylation and activate the AKT-mTOR signaling pathway. Mol Cancer. 2024; 23(1): 34.

[104]

Zhao D, Dong Y, Duan M, et al. Circadian gene ARNTL initiates circGUCY1A2 transcription to suppress non-small cell lung cancer progression via miR-200c-3p/PTEN signaling. J Exp Clin Cancer Res. 2023; 42(1): 229.

[105]

Ma Z, Chen H, Xia Z, et al. Energy stress-induced circZFR enhances oxidative phosphorylation in lung adenocarcinoma via regulating alternative splicing. J Exp Clin Cancer Res. 2023; 42(1): 169.

[106]

Liao W, Du J, Li L, et al. CircZNF215 promotes tumor growth and metastasis through inactivation of the PTEN/AKT pathway in intrahepatic cholangiocarcinoma. J Exp Clin Cancer Res. 2023; 42(1): 125.

[107]

Zhang C, Yu Z, Yang S, et al. ZNF460-mediated circRPPH1 promotes TNBC progression through ITGA5-induced FAK/PI3K/AKT activation in a ceRNA manner. Mol Cancer. 2024; 23(1): 33.

[108]

Li Y, Wang Z, Yang J, et al. CircTRIM1 encodes TRIM1-269aa to promote chemoresistance and metastasis of TNBC via enhancing CaM-dependent MARCKS translocation and PI3K/AKT/mTOR activation. Mol Cancer. 2024; 23(1): 102.

[109]

Lei K, Liang R, Liang J, et al. CircPDE5A-encoded novel regulator of the PI3K/AKT pathway inhibits esophageal squamous cell carcinoma progression by promoting USP14-mediated de-ubiquitination of PIK3IP1. J Exp Clin Cancer Res. 2024; 43(1): 124.

[110]

Xue C, Li G, Zheng Q, et al. The functional roles of the circRNA/Wnt axis in cancer. Mol Cancer. 2022; 21(1): 108.

[111]

Li Y, Wang Z, Su P, et al. circ-EIF6 encodes EIF6-224aa to promote TNBC progression via stabilizing MYH9 and activating the Wnt/beta-catenin pathway. Mol Ther. 2022; 30(1): 415-430.

[112]

Alimohammadi M, Gholinezhad Y, Mousavi V, et al. Circular RNAs: novel actors of Wnt signaling pathway in lung cancer progression. EXCLI J. 2023; 22: 645.

[113]

Peng Y, Xu Y, Zhang X, et al. A novel protein AXIN1-295aa encoded by circAXIN1 activates the Wnt/β-catenin signaling pathway to promote gastric cancer progression. Mol Cancer. 2021; 20: 1-19.

[114]

Krishnamurthy N, Kurzrock R. Targeting the Wnt/beta-catenin pathway in cancer: update on effectors and inhibitors. Cancer Treat Rev. 2018; 62: 50-60.

[115]

Li Y, Kong Y, An M, et al. ZEB1-mediated biogenesis of circNIPBL sustains the metastasis of bladder cancer via Wnt/β-catenin pathway. J Exp Clin Cancer Res. 2023; 42(1): 191.

[116]

Wu M, Qiu Q, Zhou Q, et al. circFBXO7/miR-96-5p/MTSS1 axis is an important regulator in the Wnt signaling pathway in ovarian cancer. Mol Cancer. 2022; 21(1): 137.

[117]

Xu S, Luo C, Chen D, et al. circMMD reduction following tumor treating fields inhibits glioblastoma progression through FUBP1/FIR/DVL1 and miR-15b-5p/FZD6 signaling. J Exp Clin Cancer Res. 2023; 42(1): 64.

[118]

Wang Z, Sun A, Yan A, et al. Circular RNA MTCL1 promotes advanced laryngeal squamous cell carcinoma progression by inhibiting C1QBP ubiquitin degradation and mediating beta-catenin activation. Mol Cancer. 2022; 21(1): 92.

[119]

Zhu Q, Hu Y, Jiang W, et al. Circ-CCT2 activates wnt/β-catenin signaling to facilitate hepatoblastoma development by stabilizing PTBP1 mRNA. Cell Mol Gastroenterol. 2024; 17(2): 175-197.

[120]

Kovall RA, Gebelein B, Sprinzak D, et al. The canonical Notch signaling pathway: structural and biochemical insights into shape, sugar, and force. Dev Cell. 2017; 41(3): 228-241.

[121]

Meurette O, Mehlen P. Notch signaling in the tumor microenvironment. Cancer Cell. 2018; 34(4): 536-548.

[122]

Ferreira A, Aster JC. Notch signaling in cancer: complexity and challenges on the path to clinical translation. Semin Cancer Biol. 2022; 85: 95-106.

[123]

Kunze B, Wein F, Fang H-Y, et al. Notch signaling mediates differentiation in Barrett’s esophagus and promotes progression to adenocarcinoma. Gastroenterology. 2020; 159(2): 575-590.

[124]

Capaccione KM, Pine SR. The Notch signaling pathway as a mediator of tumor survival. Carcinogenesis. 2013; 34(7): 1420-1430.

[125]

Ai J, Zhang W, Deng W, et al. A hsa_circ_001726 axis regulated by E2F6 contributes to metastasis of hepatocellular carcinoma. BMC Cancer. 2024; 24(1): 14.

[126]

Chen L, Yang X, Zhao J, et al. Circ_0008532 promotes bladder cancer progression by regulation of the miR-155-5p/miR-330-5p/MTGR1 axis. J Exp Clin Cancer Res. 2020; 39: 1-12.

[127]

Buratin A, Borin C, et al. CircFBXW7 in patients with T-cell ALL: depletion sustains MYC and NOTCH activation and leukemia cell viability. Exp Hematol Oncol. 2023; 12(1): 12.

[128]

Chen J, Hei R, Chen C, et al. CircCRIM1 suppresses osteosarcoma progression via sponging miR146a-5p and targeting NUMB. Am J Cancer Res. 2023; 13(8): 3463.

[129]

Long F, Lin Z, Li L, et al. Comprehensive landscape and future perspectives of circular RNAs in colorectal cancer. Mol Cancer. 2021; 20(1): 26.

[130]

Wang S, Dong Y, Gong A, et al. Exosomal circRNAs as novel cancer biomarkers: challenges and opportunities. Int J Biol Sci. 2021; 17(2): 562.

[131]

Xie G, Lei B, Yin Z, et al. Circ MTA2 drives gastric cancer progression through suppressing MTA2 degradation via interacting with UCHL3. Int J Mol Sci. 2024; 25(5): 2817.

[132]

Wang H, Tang Z, Duan J, et al. Cancer-released exosomal circular RNA circ_0008717 promotes cell tumorigenicity through microRNA-1287-5p/P21-activated kinase 2 (PAK2) axis in non-small cell lung cancer. Bioengineered. 2022; 13(4): 8937-8949.

[133]

Wang Y, Zou R, Li D, et al. Exosomal circSTRBP from cancer cells facilitates gastric cancer progression via regulating miR-1294/miR-593-3p/E2F2 axis. J Cell Mol Med. 2024; 28(8): e18217.

[134]

Li B, Chen J, Wu Y, et al. Decrease of circARID1A retards glioblastoma invasion by modulating miR-370-3p/TGFBR2 pathway. Int J Biol Sci. 2022; 18(13): 5123.

[135]

Luo A, Liu H, Huang C, et al. Exosome-transmitted circular RNA circ-LMO7 facilitates the progression of osteosarcoma by regulating miR-21-5p/ARHGAP24 axis. Cancer Biol Ther. 2024; 25(1): 2343450.

[136]

Zhang C, Wei G, Zhu X, et al. Exosome-delivered circSTAU2 inhibits the progression of gastric cancer by targeting the miR-589/CAPZA1 Axis. Int J Nanomed. 2023: 127-142.

[137]

Luo Y, Zhu Q, Xiang S, et al. Downregulated circPOKE promotes breast cancer metastasis through activation of the USP10-Snail axis. Oncogene. 2023; 42(44): 3236-3251.

[138]

Chen C, Liu Y, Liu L, et al. Exosomal circTUBGCP4 promotes vascular endothelial cell tipping and colorectal cancer metastasis by activating Akt signaling pathway. J Exp Clin Cancer Res. 2023; 42(1): 46.

[139]

Hong W, Du K, Zhang Q, et al. Tanreqing suppresses the proliferation and migration of non-small cell lung cancer cells by mediating the inactivation of the HIF1α signaling pathway via exosomal circ-WDR78. J Biomol Struct Dyn. 2024: 1-12.

[140]

Ghafouri I, Pakravan K, Razmara E, et al. Colorectal cancer-secreted exosomal circ_001422 plays a role in regulating KDR expression and activating mTOR signaling in endothelial cells by targeting miR-195-5p. J Cancer Res Clin. 2023; 149(13): 12227-12240.

[141]

Mao Y, Wang J, Wang Y, et al. Hypoxia induced exosomal Circ-ZNF609 promotes pre-metastatic niche formation and cancer progression via miR-150-5p/VEGFA and HuR/ZO-1 axes in esophageal squamous cell carcinoma. Cell Death Discov. 2024; 10(1): 133.

[142]

Miao Z, Zhao X, Liu X. Exosomal circCOL1A2 from cancer cells accelerates colorectal cancer progression via regulating miR-665/LASP1 signal axis. Eur J Pharmacol. 2023; 950: 175722.

[143]

Jiang W, Yu Y, Ou J, et al. Exosomal circRNA RHOT1 promotes breast cancer progression by targeting miR-204-5p/PRMT5 axis. Cancer Cell Int. 2023; 23(1): 260.

[144]

Liu L, Liao R, Wu Z, et al. Hepatic stellate cell exosome-derived circWDR25 promotes the progression of hepatocellular carcinoma via the miRNA-4474-3P-ALOX-15 and EMT axes. BioSci Trends. 2022; 16(4): 267-281.

[145]

Sang H, Zhang W, Peng L, et al. Exosomal circRELL1 serves as a miR-637 sponge to modulate gastric cancer progression via regulating autophagy activation. Cell Death Dis. 2022; 13(1): 56.

[146]

Wang X, Dong F-L, Wang Y-Q, et al. Exosomal circTGFBR2 promotes hepatocellular carcinoma progression via enhancing ATG5 mediated protective autophagy. Cell Death Dis. 2023; 14(7): 451.

[147]

Song H, Zhao Z, Ma L, et al. Novel exosomal circEGFR facilitates triple negative breast cancer autophagy via promoting TFEB nuclear trafficking and modulating miR-224-5p/ATG13/ULK1 feedback loop. Oncogene. 2024: 1-16.

[148]

Liu Y, Ma L, Hua F, et al. Exosomal circCARM1 from spheroids reprograms cell metabolism by regulating PFKFB2 in breast cancer. Oncogene. 2022; 41(14): 2012-2025.

[149]

Lin J, Wang X, Zhai S, et al. Hypoxia-induced exosomal circPDK1 promotes pancreatic cancer glycolysis via c-myc activation by modulating miR-628-3p/BPTF axis and degrading BIN1. J Hematol Oncol. 2022; 15(1): 128.

[150]

Huang C, Zhou Y, Feng X, et al. Delivery of engineered primary tumor-derived exosomes effectively suppressed the colorectal cancer chemoresistance and liver metastasis. ACS Nano. 2023; 17(11): 10313-10326.

[151]

Chen Y, Liu H, Zou J, et al. Exosomal circ_0091741 promotes gastric cancer cell autophagy and chemoresistance via the miR-330-3p/TRIM14/Dvl2/Wnt/β-catenin axis. Hum Cell. 2023; 36(1): 258-275.

[152]

Zhang Y, Tan X, Lu Y. Exosomal transfer of circ_0006174 contributes to the chemoresistance of doxorubicin in colorectal cancer by depending on the miR-1205/CCND2 axis. J Physiol Biochem. 2022; 78(1): 39-50.

[153]

Culy CR, Clemett D, Wiseman LR. Oxaliplatin: a review of its pharmacological properties and clinical efficacy in metastatic colorectal cancer and its potential in other malignancies. Drugs. 2000; 60: 895-924.

[154]

Pan Z, Zheng J, Zhang J, et al. A novel protein encoded by exosomal CircATG4B induces oxaliplatin resistance in colorectal cancer by promoting autophagy. Adv Sci. 2022; 9(35): 2204513.

[155]

Wu Y, Xu M, Feng Z, et al. AUF1-induced circular RNA hsa_circ_0010467 promotes platinum resistance of ovarian cancer through miR-637/LIF/STAT3 axis. Cell Mol Life Sci. 2023; 80(9): 256.

[156]

Chen Z, Xu Z, Wang Q, et al. Exosome-delivered circRNA circSYT15 contributes to cisplatin resistance in cervical cancer cells through the miR-503-5p/RSF1 axis. Cell Cycle. 2023; 22(20): 2211-2228.

[157]

Gong J, Han G, Chen Z, et al. CircDCAF8 promotes the progression of hepatocellular carcinoma through miR-217/NAP1L1 Axis, and induces angiogenesis and regorafenib resistance via exosome-mediated transfer. J Transl Med. 2024; 22(1): 1-20.

[158]

Dong F-L, Xu Z-Z, Wang Y-Q, et al. Exosome-derived circUPF2 enhances resistance to targeted therapy by redeploying ferroptosis sensitivity in hepatocellular carcinoma. J Nanobiotechnol. 2024; 22(1): 298.

[159]

Xia W, Chen W, Ni C, et al. Chemotherapy-induced exosomal circBACH1 promotes breast cancer resistance and stemness via miR-217/G3BP2 signaling pathway. Breast Cancer Res. 2023; 25(1): 85.

[160]

Wang X, Chen T, Li C, et al. CircRNA-CREIT inhibits stress granule assembly and overcomes doxorubicin resistance in TNBC by destabilizing PKR. J Hematol Oncol. 2022; 15(1): 122.

[161]

Wei S-L, Ye J-J, Sun L, et al. Exosome-derived circKIF20B suppresses gefitinib resistance and cell proliferation in non-small cell lung cancer. Cancer Cell Int. 2023; 23(1): 129.

[162]

Lu L, Zeng Y, Yu Z, et al. EIF4a3-regulated circRABL2B regulates cell stemness and drug sensitivity of lung cancer via YBX1-dependent downregulation of MUC5AC expression. Int J Biol Sci. 2023; 19(9): 2725.

[163]

Luo X, Li Y, Hua Z, et al. Exosomes-mediated tumor metastasis through reshaping tumor microenvironment and distant niche. J Control Release. 2023; 353: 327-336.

[164]

Elhanani O, Ben-Uri R, Keren L. Spatial profiling technologies illuminate the tumor microenvironment. Cancer Cell. 2023; 41(3): 404-420.

[165]

Toninelli M, Rossetti G, Pagani M. Charting the tumor microenvironment with spatial profiling technologies. Trends Cancer. 2023; 9(12): 1085-1096.

[166]

Marangon D, Lecca D. Exosomal non-coding RNAs in glioma progression: insights into tumor microenvironment dynamics and therapeutic implications. Front Cell Dev Biol. 2023; 11: 1275755.

[167]

Tsoumakidou M. The advent of immune stimulating CAFs in cancer. Nat Rev Cancer. 2023; 23(4): 258-269.

[168]

Kim S-J, Khadka D, Seo JH. Interplay between solid tumors and tumor microenvironment. Front Immunol. 2022; 13: 882718.

[169]

Li Y, Zheng X, Wang J, et al. Exosomal circ-AHCY promotes glioblastoma cell growth via Wnt/β-catenin signaling pathway. Ann Clin Transl Neur. 2023; 10(6): 865-878.

[170]

Dai W, Wu X, Li J, et al. Hedgehog-Gli1-derived exosomal circ-0011536 mediates peripheral neural remodeling in pancreatic cancer by modulating the miR-451a/VGF axis. J Exp Clin Cancer Res. 2023; 42(1): 329.

[171]

Ding L, Zheng Q, Lin Y, et al. Exosome-derived circTFDP2 promotes prostate cancer progression by preventing PARP1 from caspase-3-dependent cleavage. Clin Transl Med. 2023; 13(1): e1156.

[172]

Chen L, Guo P, He Y, et al. HCC-derived exosomes elicit HCC progression and recurrence by epithelial-mesenchymal transition through MAPK/ERK signalling pathway. Cell Death Dis. 2018; 9(5): 513.

[173]

Huang X-Y, Huang Z-L, Huang J, et al. Exosomal circRNA-100338 promotes hepatocellular carcinoma metastasis via enhancing invasiveness and angiogenesis. J Exp Clin Cancer Res. 2020; 39: 1-16.

[174]

Zhang H, Yue X, Chen Z, et al. Define cancer-associated fibroblasts (CAFs) in the tumor microenvironment: new opportunities in cancer immunotherapy and advances in clinical trials. Mol Cancer. 2023; 22(1): 159.

[175]

Öhlund D, Handly-Santana A, Biffi G, et al. Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. J Exp Med. 2017; 214(3): 579-596.

[176]

Fang Z, Meng Q, Xu J, et al. Signaling pathways in cancer-associated fibroblasts: recent advances and future perspectives. Cancer Commun. 2023; 43(1): 3-41.

[177]

Kennel KB, Bozlar M, De Valk AF, et al. Cancer-associated fibroblasts in inflammation and antitumor immunity. Clin Cancer Res. 2023; 29(6): 1009-1016.

[178]

Ye F, Liang Y, Wang Y, et al. Cancer-associated fibroblasts facilitate breast cancer progression through exosomal circTBPL1-mediated intercellular communication. Cell Death Dis. 2023; 14(7): 471.

[179]

Jiang Q, Lei Z, Wang Z, et al. Tumor-associated fibroblast-derived exosomal circDennd1b promotes pituitary adenoma progression by modulating the miR-145-5p/ONECUT2 axis and activating the MAPK pathway. Cancers. 2023; 15(13): 3375.

[180]

Yang C, Zhang Y, Yan M, et al. Exosomes derived from cancer-associated fibroblasts promote tumorigenesis, metastasis and chemoresistance of colorectal cancer by upregulating circ_0067557 to target Lin28. BMC Cancer. 2024; 24(1): 64.

[181]

Nilsson I, Bahram F, Li X, et al. VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J. 2010; 29(8): 1377-1388.

[182]

Bautch VL. Endothelial cells form a phalanx to block tumor metastasis. Cell. 2009; 136(5): 810-812.

[183]

Coso S, Bovay E, Petrova TV. Pressing the right buttons: signaling in lymphangiogenesis. Blood. 2014; 123(17): 2614-2624.

[184]

Sheldon H, Heikamp E, Turley H, et al. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood. 2010; 116(13): 2385-2394.

[185]

Bovy N, Blomme B, Frères P, et al. Endothelial exosomes contribute to the antitumor response during breast cancer neoadjuvant chemotherapy via microRNA transfer. Oncotarget. 2015; 6(12): 10253.

[186]

Maes H, Olmeda D, Soengas MS, et al. Vesicular trafficking mechanisms in endothelial cells as modulators of the tumor vasculature and targets of antiangiogenic therapies. FEBS J. 2016; 283(1): 25-38.

[187]

Shen X, Kong S, Ma S, et al. Hsa_circ_0000437 promotes pathogenesis of gastric cancer and lymph node metastasis. Oncogene. 2022; 41(42): 4724-4735.

[188]

Thommen DS, Schumacher TN. T cell dysfunction in cancer. Cancer Cell. 2018; 33(4): 547-562.

[189]

Reina-Campos M, Scharping NE, Goldrath AW. CD8+ T cell metabolism in infection and cancer. Nat Rev Immunol. 2021; 21(11): 718-738.

[190]

Hashimoto M, Kamphorst AO, Im SJ, et al. CD8 T cell exhaustion in chronic infection and cancer: opportunities for interventions. Annu Rev Med. 2018; 69: 301-318.

[191]

Park J, Hsueh P-C, Li Z, et al. Microenvironment-driven metabolic adaptations guiding CD8+ T cell anti-tumor immunity. Immunity. 2023; 56(1): 32-42.

[192]

Dolina JS, Van Braeckel-Budimir N, Thomas GD, et al. CD8+ T cell exhaustion in cancer. Front Immunol. 2021; 12: 715234.

[193]

Wang J, Zhao X, Wang Y, et al. circRNA-002178 act as a ceRNA to promote PDL1/PD1 expression in lung adenocarcinoma. Cell Death Dis. 2020; 11(1): 32.

[194]

Chen S-W, Zhu S-Q, Pei X, et al. Cancer cell-derived exosomal circUSP7 induces CD8+ T cell dysfunction and anti-PD1 resistance by regulating the miR-934/SHP2 axis in NSCLC. Mol Cancer. 2021; 20: 1-18.

[195]

Luo Y-H, Yang Y-P, Chien C-S, et al. Circular RNA hsa_circ_0000190 facilitates the tumorigenesis and immune evasion by upregulating the expression of soluble PD-L1 in non-small-cell lung cancer. Int J Mol Sci. 2021; 23(1): 64.

[196]

Hu Z, Chen G, Zhao Y, et al. Exosome-derived circCCAR1 promotes CD8+ T-cell dysfunction and anti-PD1 resistance in hepatocellular carcinoma. Mol Cancer. 2023; 22(1): 55.

[197]

Lu J-C, Zhang P-F, Huang X-Y, et al. Amplification of spatially isolated adenosine pathway by tumor–macrophage interaction induces anti-PD1 resistance in hepatocellular carcinoma. J Hematol Oncol. 2021; 14: 1-20.

[198]

Yang C, Wu S, Mou Z, et al. Exosome-derived circTRPS1 promotes malignant phenotype and CD8+ T cell exhaustion in bladder cancer microenvironments. Mol Ther. 2022; 30(3): 1054-1070.

[199]

Shan F, Somasundaram A, Bruno TC, et al. Therapeutic targeting of regulatory T cells in cancer. Trends Cancer. 2022; 8(11): 944-961.

[200]

Li C, Jiang P, Wei S, et al. Regulatory T cells in tumor microenvironment: new mechanisms, potential therapeutic strategies and future prospects. Mol Cancer. 2020; 19: 1-23.

[201]

Alvisi G, Termanini A, Soldani C, et al. Multimodal single-cell profiling of intrahepatic cholangiocarcinoma defines hyperactivated Tregs as a potential therapeutic target. J Hepatol. 2022; 77(5): 1359-1372.

[202]

Huang M, Huang X, Huang N. Exosomal circGSE1 promotes immune escape of hepatocellular carcinoma by inducing the expansion of regulatory T cells. Cancer Sci. 2022; 113(6): 1968-1983.

[203]

Chen Y, Li Z, Liang J, et al. CircRNA has_circ_0069313 induced OSCC immunity escape by miR-325-3p-Foxp3 axes in both OSCC cells and Treg cells. Aging (Albany NY). 2022; 14(10): 4376.

[204]

Li C, Xu X, Wei S, et al. Tumor-associated macrophages: potential therapeutic strategies and future prospects in cancer. J Immunother Cancer. 2021; 9(1).

[205]

Vinogradov S, Warren G, Wei X. Macrophages associated with tumors as potential targets and therapeutic intermediates. Nanomedicine. 2014; 9(5): 695-707.

[206]

Xu M, Zhou C, Weng J, et al. Tumor associated macrophages-derived exosomes facilitate hepatocellular carcinoma malignance by transferring lncMMPA to tumor cells and activating glycolysis pathway. J Exp Clin Cancer Res. 2022; 41(1): 253.

[207]

Lu Y, Han G, Zhang Y, et al. M2 macrophage-secreted exosomes promote metastasis and increase vascular permeability in hepatocellular carcinoma. Cell Commun Signal. 2023; 21(1): 299.

[208]

Ran X-M, Yang J, Wang Z-Y, et al. M2 macrophage-derived exosomal circTMCO3 acts through miR-515-5p and ITGA8 to enhance malignancy in ovarian cancer. Commun Biol. 2024; 7(1): 583.

[209]

Wang L, Yi X, Xiao X, et al. Exosomal miR-628-5p from M1 polarized macrophages hinders m6A modification of circFUT8 to suppress hepatocellular carcinoma progression. Cell Mol Biol Lett. 2022; 27(1): 106.

[210]

Chen M, Cao C, Ma J. Tumor-related exosomal circ_0001715 promotes lung adenocarcinoma cell proliferation and metastasis via enhancing M2 macrophage polarization by regulating triggering receptor expressed on myeloid cells-2. Thorac Cancer. 2024; 15(3): 227-238.

[211]

Zhang L, Zhang J, Li P, et al. Exosomal hsa_circ_0004658 derived from RBPJ overexpressed-macrophages inhibits hepatocellular carcinoma progression via miR-499b-5p/JAM3. Cell Death Dis. 2022; 13(1): 32.

[212]

Shi L, Cao Y, Yuan W, et al. Exosomal circRNA BTG2 derived from RBP-J overexpressed-macrophages inhibits glioma progression via miR-25-3p/PTEN. Cell Death Dis. 2022; 13(5): 506.

[213]

Deng C, Huo M, Chu H, et al. Exosome circATP8A1 induces macrophage M2 polarization by regulating the miR-1-3p/STAT6 axis to promote gastric cancer progression. Mol Cancer. 2024; 23(1): 49.

[214]

Zhang Y, Guo J, Zhang L, et al. CircASPH enhances exosomal STING to facilitate M2 macrophage polarization in colorectal cancer. Inflamm Bowel Dis. 2023; 29(12): 1941-1956.

[215]

Zhou B, Mo Z, Lai G, et al. Targeting tumor exosomal circular RNA cSERPINE2 suppresses breast cancer progression by modulating MALT1-NF-κB-IL-6 axis of tumor-associated macrophages. J Exp Clin Canc Res. 2023; 42(1): 48.

[216]

Sun Z, Xu Y, Shao B, et al. Exosomal circPOLQ promotes macrophage M2 polarization via activating IL-10/STAT3 axis in a colorectal cancer model. J Immunother Cancer. 2024; 12(5).

[217]

Zhang Y, Wang X, Liu W, et al. CircGLIS3 promotes gastric cancer progression by regulating the miR-1343-3p/PGK1 pathway and inhibiting vimentin phosphorylation. J Transl Med. 2024; 22(1): 251.

[218]

Lu C, Shi W, Hu W, et al. Endoplasmic reticulum stress promotes breast cancer cells to release exosomes circ_0001142 and induces M2 polarization of macrophages to regulate tumor progression. Pharmacol Res. 2022; 177: 106098.

[219]

Wang D, Wang S, Jin M, et al. Hypoxic exosomal circPLEKHM1-mediated crosstalk between tumor cells and macrophages drives lung cancer metastasis. Adv Sci. 2024:2309857.

[220]

Katopodi T, Petanidis S, Domvri K, et al. Kras-driven intratumoral heterogeneity triggers infiltration of M2 polarized macrophages via the circHIPK3/PTK2 immunosuppressive circuit. Sci Rep. 2021; 11(1): 15455.

[221]

Myers JA, Miller JS. Exploring the NK cell platform for cancer immunotherapy. Nat Rev Clin Oncol. 2021; 18(2): 85-100.

[222]

Wu S-Y, Fu T, Jiang Y-Z, et al. Natural killer cells in cancer biology and therapy. Mol Cancer. 2020; 19: 1-26.

[223]

Lamers-Kok N, Panella D, Georgoudaki A-M, et al. Natural killer cells in clinical development as non-engineered, engineered, and combination therapies. J Hematol Oncol. 2022; 15(1): 164.

[224]

Vivier E, Rebuffet L, Narni-Mancinelli E, et al. Natural killer cell therapies. Nature. 2024; 626(8000): 727-736.

[225]

Bald T, Krummel MF, Smyth MJ, et al. The NK cell-cancer cycle: advances and new challenges in NK cell-based immunotherapies. Nat Immunol. 2020; 21(8): 835-847.

[226]

Zhang P-F, Gao C, Huang X-Y, et al. Cancer cell-derived exosomal circUHRF1 induces natural killer cell exhaustion and may cause resistance to anti-PD1 therapy in hepatocellular carcinoma. Mol Cancer. 2020; 19: 1-15.

[227]

Lasser SA, Arkhypov I, et al. Myeloid-derived suppressor cells in cancer and cancer therapy. Nat Rev Clin Oncol. 2024; 21(2): 147-164.

[228]

Hegde S, Leader AM, Merad M. MDSC: markers, development, states, and unaddressed complexity. Immunity. 2021; 54(5): 875-884.

[229]

Gao F, Xu Q, Tang Z, et al. Exosomes derived from myeloid-derived suppressor cells facilitate castration-resistant prostate cancer progression via S100A9/circMID1/miR-506-3p/MID1. J Transl Med. 2022; 20(1): 346.

[230]

Liu X, Zhao S, Sui H, et al. MicroRNAs/LncRNAs modulate MDSCs in tumor microenvironment. Front Oncol. 2022; 12: 772351.

[231]

Zhou X, Fang D, Liu H, et al. PMN-MDSCs accumulation induced by CXCL1 promotes CD8+ T cells exhaustion in gastric cancer. Cancer Lett. 2022; 532: 215598.

[232]

Pettinella F, Mariotti B, Lattanzi C, et al. Surface CD52, CD84, and PTGER2 mark mature PMN-MDSCs from cancer patients and G-CSF-treated donors. Cell Rep Med. 2024; 5(2).

[233]

Zhang R, Dong M, Tu J, et al. PMN-MDSCs modulated by CCL20 from cancer cells promoted breast cancer cell stemness through CXCL2-CXCR2 pathway. Signal Transduct Target Ther. 2023; 8(1): 97.

[234]

Shi X, Pang S, Zhou J, et al. Bladder-cancer-derived exosomal circRNA_0013936 promotes suppressive immunity by up-regulating fatty acid transporter protein 2 and down-regulating receptor-interacting protein kinase 3 in PMN-MDSCs. Mol Cancer. 2024; 23(1): 52.

[235]

Xiong S, Dong L, Cheng L. Neutrophils in cancer carcinogenesis and metastasis. J Hematol Oncol. 2021; 14: 1-17.

[236]

Jaillon S, Ponzetta A, Di Mitri D, et al. Neutrophil diversity and plasticity in tumour progression and therapy. Nat Rev Cancer. 2020; 20(9): 485-503.

[237]

Aroca-Crevillén A, Vicanolo T, Ovadia S, et al. Neutrophils in physiology and pathology. Annu Rev Pathol-Mech. 2024; 19(1): 227-259.

[238]

Que H, Fu Q, Lan T, et al. Tumor-associated neutrophils and neutrophil-targeted cancer therapies. BBA-Rev Cancer. 2022; 1877(5): 188762.

[239]

Liu S, Wu W, Du Y, et al. The evolution and heterogeneity of neutrophils in cancers: origins, subsets, functions, orchestrations and clinical applications. Mol Cancer. 2023; 22(1): 148.

[240]

Shaul ME, Fridlender ZG. Tumour-associated neutrophils in patients with cancer. Nat Rev Clin Oncol. 2019; 16(10): 601-620.

[241]

Shang A, Gu C, Wang W, et al. Exosomal circPACRGL promotes progression of colorectal cancer via the miR-142-3p/miR-506-3p-TGF-β1 axis. Mol Cancer. 2020; 19: 1-15.

[242]

Park EM, Chelvanambi M, Bhutiani N, et al. Targeting the gut and tumor microbiota in cancer. Nat Med. 2022; 28(4): 690-703.

[243]

Yang L, Li A, Wang Y, et al. Intratumoral microbiota: roles in cancer initiation, development and therapeutic efficacy. Signal Transduct Target Ther. 2023; 8(1): 35.

[244]

Sepich-Poore GD, Zitvogel L, Straussman R, et al. The microbiome and human cancer. Science. 2021; 371(6536): eabc4552.

[245]

Garrett WS. Cancer and the microbiota. Science. 2015; 348(6230): 80-86.

[246]

Zang X, Wang R, Wang Z, et al. Exosomal circ50547 as a potential marker and promotor of gastric cancer progression via miR-217/HNF1B axis. Transl Oncol. 2024; 45: 101969.

[247]

Huang X-j, Wang Y, Wang H-t, et al. Exosomal hsa_circ_000200 as a potential biomarker and metastasis enhancer of gastric cancer via miR-4659a/b-3p/HBEGF axis. Cancer Cell Int. 2023; 23(1): 151.

[248]

Chen Z, Ma X, Chen Z, et al. Exosome-transported circ_0061407 and circ_0008103 play a tumour-repressive role and show diagnostic value in non-small-cell lung cancer. J Transl Med. 2024; 22(1): 427.

[249]

Li X, Lin Y-L, Shao J-K, et al. Plasma exosomal hsa_circ_0079439 as a novel biomarker for early detection of gastric cancer. World J Gastroenterol. 2023; 29(22): 3482.

[250]

Liu Q, Li S. Exosomal circRNAs: novel biomarkers and therapeutic targets for urinary tumors. Cancer Lett. 2024:216759.

[251]

Gopikrishnan M, Ashour HM, Pintus G, et al. Therapeutic and diagnostic applications of exosomal circRNAs in breast cancer. Funct Integr Genomic. 2023; 23(2): 184.

[252]

Zheng R, Zhang K, Tan S, et al. Exosomal circLPAR1 functions in colorectal cancer diagnosis and tumorigenesis through suppressing BRD4 via METTL3-eIF3h interaction. Mol Cancer. 2022; 21(1): 49.

[253]

Zhou H, Huang X, Yang X, et al. CircRAPGEF5 promotes the proliferation and metastasis of lung adenocarcinoma through the miR-1236-3p/ZEB1 axis and serves as a potential biomarker. Int J Biol Sci. 2022; 18(5): 2116.

[254]

Yang X, Xia J, Peng C, et al. Expression of plasma exosomal circLPAR1 in patients with gastric cancer and its clinical application value. Am J Cancer Res. 2023; 13(9): 4269.

[255]

Wei Y, Fu J, Zhang H, et al. N6-methyladenosine modification promotes hepatocarcinogenesis through circ-CDYL-enriched and EpCAM-positive liver tumor-initiating exosomes. Iscience. 2023; 26(10).

[256]

Hussen BM, Abdullah ST, Abdullah SR, et al. Exosomal non-coding RNAs: blueprint in colorectal cancer metastasis and therapeutic targets. Noncoding RNA Res. 2023; 8(4): 615-632.

[257]

Yue X, Lan F, Liu W. Serum exosomal circCCDC66 as a potential diagnostic and prognostic biomarker for pituitary adenomas. Front Oncol. 2023; 13: 1268778.

[258]

Li P, Xu Z, Liu T, et al. Circular RNA sequencing reveals serum exosome circular RNA panel for high-grade astrocytoma diagnosis. Clin Chem. 2022; 68(2): 332-343.

[259]

Tang X, Deng Z, Ding P, et al. A novel protein encoded by circHNRNPU promotes multiple myeloma progression by regulating the bone marrow microenvironment and alternative splicing. J Exp Clin Cancer Res. 2022; 41(1): 85.

[260]

Wen N, Peng D, Xiong X, et al. Cholangiocarcinoma combined with biliary obstruction: an exosomal circRNA signature for diagnosis and early recurrence monitoring. Signal Transduct Target Ther. 2024; 9(1): 107.

[261]

Guo X, Gao C, Yang D-H, et al. Exosomal circular RNAs: a chief culprit in cancer chemotherapy resistance. Drug Resist Update. 2023; 67: 100937.

[262]

Zhang Z, Li X, Wang Y, et al. Involvement of inflammasomes in tumor microenvironment and tumor therapies. J Hematol Oncol. 2023; 16(1): 24.

[263]

Shang Z, Luo Z, Wang Y, et al. CircHIPK3 contributes to cisplatin resistance in gastric cancer by blocking autophagy-dependent ferroptosis. J Cell Physiol. 2023; 238(10): 2407-2424.

[264]

Ma J, Chen C, Fan Z, et al. CircEGFR reduces the sensitivity of pirarubicin and regulates the malignant progression of triple-negative breast cancer via the miR-1299/EGFR axis. Int J Biol Macromol. 2023; 244: 125295.

[265]

Gao J, Ao Y-Q, Zhang L-X, et al. Exosomal circZNF451 restrains anti-PD1 treatment in lung adenocarcinoma via polarizing macrophages by complexing with TRIM56 and FXR1. J Exp Clin Cancer Res. 2022; 41(1): 295.

[266]

Xu Y, Han J, Zhang X, et al. Exosomal circRNAs in gastrointestinal cancer: role in occurrence, development, diagnosis and clinical application. Oncol Rep. 2024; 51(2): 1-14.

[267]

Tang C, He X, Jia L, et al. Circular RNAs in glioma: molecular functions and pathological implications. Noncoding RNA Res. 2023; 9(1): 105-115.

[268]

Li Y, Hu J, Wang M, et al. Exosomal circPABPC1 promotes colorectal cancer liver metastases by regulating HMGA2 in the nucleus and BMP4/ADAM19 in the cytoplasm. Cell Death Discov. 2022; 8(1): 335.

[269]

Chen C, Yu H, Han F, et al. Tumor-suppressive circRHOBTB3 is excreted out of cells via exosome to sustain colorectal cancer cell fitness. Mol Cancer. 2022; 21(1): 46.

[270]

Barile L, Vassalli G. Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Therapeut. 2017; 174: 63-78.

[271]

Lu Q, Kou D, Lou S, et al. Nanoparticles in tumor microenvironment remodeling and cancer immunotherapy. J Hematol Oncol. 2024; 17(1): 16.

[272]

Liao W, Du Y, Zhang C, et al. Exosomes: the next generation of endogenous nanomaterials for advanced drug delivery and therapy. Acta Biomater. 2019; 86: 1-14.

[273]

Shu G, Lu X, Pan Y, et al. Exosomal circSPIRE1 mediates glycosylation of E-cadherin to suppress metastasis of renal cell carcinoma. Oncogene. 2023; 42(22): 1802-1820.

[274]

Chen J, Wang H, Xu J, et al. CircZFR promotes colorectal cancer progression via stabilizing BCLAF1 and regulating the miR-3127-5p/RTKN2 axis. Sci China Life Sci. 2024: 1-18.

[275]

Guo Z, Zhang Y, Xu W, et al. Engineered exosome-mediated delivery of circDIDO1 inhibits gastric cancer progression via regulation of MiR-1307-3p/SOCS2 axis. J Transl Med. 2022; 20(1): 326.

[276]

Geng X, Zhang Y, Lin X, et al. Exosomal circWDR62 promotes temozolomide resistance and malignant progression through regulation of the miR-370-3p/MGMT axis in glioma. Cell Death Dis. 2022; 13(7): 596.

[277]

Hao X, Zhang Y, Shi X, et al. CircPAK1 promotes the progression of hepatocellular carcinoma via modulation of YAP nucleus localization by interacting with 14-3-3ζ. J Exp Clin Cancer Res. 2022; 41(1): 281.

[278]

Ye D, Gong M, Deng Y, et al. Roles and clinical application of exosomal circRNAs in the diagnosis and treatment of malignant tumors. J Transl Med. 2022; 20(1): 161.

[279]

Lyu K, Tang B, Huang B, et al. Exosomal circPVT1 promotes angiogenesis in laryngeal cancer by activating the Rap1b-VEGFR2 signaling pathway. Carcinogenesis. 2024:bgae030.

[280]

Liu X, Guo Q, Gao G, et al. Exosome-transmitted circCABIN1 promotes temozolomide resistance in glioblastoma via sustaining ErbB downstream signaling. J Nanobiotechnol. 2023; 21(1): 45.

[281]

Zhang X, Xu Y, Ma L, et al. Essential roles of exosome and circRNA_101093 on ferroptosis desensitization in lung adenocarcinoma. Cancer Commun. 2022; 42(4): 287-313.

[282]

Zhang Z, Gao Z, Fang H, et al. Therapeutic importance and diagnostic function of circRNAs in urological cancers: from metastasis to drug resistance. Cancer Metast Rev. 2024: 1-22.

[283]

Wang X, Wang G, Wu Z, et al. Exosomal circ-PTPN22 and circ-ADAMTS6 mark T cell exhaustion and neutrophil extracellular traps in Asian intrahepatic cholangiocarcinoma. Mol Ther Nucl Acids. 2023; 31: 151-163.

[284]

Du A, Yang Q, Sun X, et al. Exosomal circRNA-001264 promotes AML immunosuppression through induction of M2-like macrophages and PD-L1 overexpression. Int Immunopharmacol. 2023; 124: 110868.

[285]

Li Y, Jiang B, Zeng L, et al. Adipocyte-derived exosomes promote the progression of triple-negative breast cancer through circCRIM1-dependent OGA activation. Environ Res. 2023; 239: 117266.

[286]

Yuan Z, Xiong B, Liu L, et al. Exosomal circ_0037104 derived from Hu-MSCs inhibits cholangiocarcinoma progression by sponging miR-620 and targeting AFAP1. J Biochem Mol Toxicol. 2024; 38(2): e23656.

[287]

Nicot C. RNA-seq reveals novel CircRNAs involved in breast cancer progression and patient therapy response. Mol Cancer. 2020; 19(1): 76.

[288]

Shi Z-X, Chen Z-C, Zhong J-Y, et al. High-throughput and high-accuracy single-cell RNA isoform analysis using PacBio circular consensus sequencing. Nat Commun. 2023; 14(1): 2631.

[289]

Hansen TB, Venø MT, Damgaard CK, et al. Comparison of circular RNA prediction tools. Nucleic Acids Res. 2016; 44(6): e58-e58.

RIGHTS & PERMISSIONS

2024 The Author(s). MedComm published by Sichuan International Medical Exchange & Promotion Association (SCIMEA) and John Wiley & Sons Australia, Ltd.

AI Summary AI Mindmap
PDF

148

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/