Key role of exosomes derived from M2 macrophages in maintaining cancer cell stemness (Review)
- Authors:
- Weiqiong Zhang
- Ruiping Zhou
- Xin Liu
- Lin You
- Chang Chen
- Xiaoling Ye
- Jie Liu
- Youde Liang
-
Affiliations: Department of Orthopedics, The Fourth Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong 510150, P.R. China, Department of Stomatology, Yantian District People's Hospital, Southern University of Science and Technology, Shenzhen, Guangdong 518081, P.R. China - Published online on: September 14, 2023 https://doi.org/10.3892/ijo.2023.5574
- Article Number: 126
-
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
 |
 |
 |
|
Clevers H: The cancer stem cell: Premises, promises and challenges. Nat Med. 17:313–319. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Nassar D and Blanpain C: Cancer stem cells: Basic concepts and therapeutic Implications. Annu Rev Pathol. 11:47–76. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Dawood S, Austin L and Cristofanilli M: Cancer stem cells: Implications for cancer therapy. Oncology (Williston Park). 28:1101–1107. 11102014.PubMed/NCBI | |
|
Vlashi E and Pajonk F: Cancer stem cells, cancer cell plasticity and radiation therapy. Semin Cancer Biol. 31:28–35. 2015. View Article : Google Scholar | |
|
Walcher L, Kistenmacher AK, Suo H, Kitte R, Dluczek S, Strauß A, Blaudszun AR, Yevsa T, Fricke S and Kossatz-Boehlert U: Cancer stem cells-origins and biomarkers: Perspectives for targeted personalized therapies. Front Immunol. 11:12802020. View Article : Google Scholar : PubMed/NCBI | |
|
Plaks V, Kong N and Werb Z: The cancer stem cell niche: How essential is the niche in regulating stemness of tumor cells? Cell Stem Cell. 16:225–238. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Neophytou CM, Panagi M, Stylianopoulos T and Papageorgis P: The role of tumor microenvironment in cancer metastasis: Molecular mechanisms and therapeutic opportunities. Cancers (Basel). 13:20532021. View Article : Google Scholar : PubMed/NCBI | |
|
Liu J, Geng X, Hou J and Wu G: New insights into M1/M2 macrophages: Key modulators in cancer progression. Cancer Cell Int. 21:3892021. View Article : Google Scholar : PubMed/NCBI | |
|
Kalluri R and LeBleu VS: The biology, function, and biomedical applications of exosomes. Science. 367:eaau69772020. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou B, Xu K, Zheng X, Chen T, Wang J, Song Y, Shao Y and Zheng S: Application of exosomes as liquid biopsy in clinical diagnosis. Signal Transduct Target Ther. 5:1442020. View Article : Google Scholar : PubMed/NCBI | |
|
Nicolini A, Ferrari P and Biava PM: Exosomes and cell communication: From tumour-derived exosomes and their role in tumour progression to the use of exosomal cargo for cancer treatment. Cancers (Basel). 13:8222021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y, Liu Q, Zhang X, Huang H, Tang S, Chai Y, Xu Z, Li M, Chen X, Liu J and Yang C: Recent advances in exosome-mediated nucleic acid delivery for cancer therapy. J Nanobiotechnology. 20:2792022. View Article : Google Scholar : PubMed/NCBI | |
|
Long KB, Collier AI and Beatty GL: Macrophages: Key orchestrators of a tumor microenvironment defined by therapeutic resistance. Mol Immunol. 110:3–12. 2019. View Article : Google Scholar | |
|
Binenbaum Y, Fridman E, Yaari Z, Milman N, Schroeder A, Ben David G, Shlomi T and Gil Z: Transfer of miRNA in macrophage-derived exosomes induces drug resistance in pancreatic adenocarcinoma. Cancer Res. 78:5287–5299. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K, Batte K, Shah P, Wisler J, Eubank TD, Tridandapani S, et al: Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood. 121:984–995. 2013. View Article : Google Scholar : | |
|
Behzadi E, Hosseini HM, Halabian R and Fooladi AAI: Macrophage cell-derived exosomes/staphylococcal enterotoxin B against fibrosarcoma tumor. Microb Pathog. 111:132–138. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Cheng L, Wang Y and Huang L: Exosomes from M1-polarized macrophages potentiate the cancer vaccine by creating a pro-inflammatory microenvironment in the lymph node. Mol Ther. 25:1665–1675. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Batlle E and Clevers H: Cancer stem cells revisited. Nat Med. 23:1124–1134. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Akbar Samadani A, Keymoradzdeh A, Shams S, Soleymanpour A, Elham Norollahi S, Vahidi S, Rashidy-Pour A, Ashraf A, Mirzajani E, Khanaki K, et al: Mechanisms of cancer stem cell therapy. Clin Chim Acta. 510:581–592. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao W, Li Y and Zhang X: Stemness-related markers in cancer. Cancer Transl Med. 3:87–95. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Babaei G, Aziz SG and Jaghi NZZ: EMT, cancer stem cells and autophagy; the three main axes of metastasis. Biomed Pharmacother. 133:1109092021. View Article : Google Scholar | |
|
Das PK, Pillai S, Rakib MA, Khanam JA, Gopalan V, Lam AKY and Islam F: Plasticity of cancer stem cell: Origin and role in disease progression and therapy resistance. Stem Cell Rev Rep. 16:397–412. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Huang T, Song X, Xu D, Tiek D, Goenka A, Wu B, Sastry N, Hu B and Cheng SY: Stem cell programs in cancer initiation, progression, and therapy resistance. Theranostics. 10:8721–8743. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu P and Fan Z: Cancer stem cells and tumorigenesis. Biophys Rep. 4:178–188. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Chen W, Dong J, Haiech J, Kilhoffer MC and Zeniou M: Cancer stem cell quiescence and plasticity as major challenges in cancer therapy. Stem Cells Int. 2016:17409362016. View Article : Google Scholar : PubMed/NCBI | |
|
Yang L, Shi P, Zhao G, Xu J, Peng W, Zhang J, Zhang G, Wang X, Dong Z, Chen F and Cui H: Targeting cancer stem cell pathways for cancer therapy. Signal Transduct Target Ther. 5:82020. View Article : Google Scholar : PubMed/NCBI | |
|
Shi C and Pamer EG: Monocyte recruitment during infection and inflammation. Nat Rev Immunol. 11:762–774. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
van Furth R and Cohn ZA: The origin and kinetics of mononuclear phagocytes. J Exp Med. 128:415–435. 1968. View Article : Google Scholar : PubMed/NCBI | |
|
Epelman S, Lavine KJ and Randolph GJ: Origin and functions of tissue macrophages. Immunity. 41:21–35. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Casanova-Acebes M, Dalla E, Leader AM, LeBerichel J, Nikolic J, Morales BM, Brown M, Chang C, Troncoso L, Chen ST, et al: Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells. Nature. 595:578–584. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Gratchev A, Schledzewski K, Guillot P and Goerdt S: Alternatively activated antigen-presenting cells: Molecular repertoire, immune regulation, and healing. Skin Pharmacol Appl Skin Physiol. 14:272–279. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Orecchioni M, Ghosheh Y, Pramod AB and Ley K: Macrophage polarization: Different gene signatures in M1(LPS+) vs classically and M2(LPS-) vs alternatively activated macrophages. Front Immunol. 10:10842019. View Article : Google Scholar | |
|
Tong Y, Guo YJ, Zhang Q, Bi HX, Kai K and Zhou RY: Combined treatment with dihydrotestosterone and lipopolysaccharide modulates prostate homeostasis by upregulating TNF-α from M1 macrophages and promotes proliferation of prostate stromal cells. Asian J Androl. 24:513–520. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Hu W, Lin J, Lian X, Yu F, Liu W, Wu Y, Fang X, Liang X and Hao W: M2a and M2b macrophages predominate in kidney tissues and M2 subpopulations were associated with the severity of disease of IgAN patients. Clin Immunol. 205:8–15. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Wen Y, Lu X, Ren J, Privratsky JR, Yang B, Rudemiller NP, Zhang J, Griffiths R, Jain MK, Nedospasov SA, et al: KLF4 in macrophages attenuates TNFα-mediated kidney injury and fibrosis. J Am Soc Nephrol. 30:1925–1938. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Loegl J, Hiden U, Nussbaumer E, Schliefsteiner C, Cvitic S, Lang I, Wadsack C, Huppertz B and Desoye G: Hofbauer cells of M2a, M2b and M2c polarization may regulate feto-placental angiogenesis. Reproduction. 152:447–455. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Lurier EB, Dalton D, Dampier W, Raman P, Nassiri S, Ferraro NM, Rajagopalan R, Sarmady M and Spiller KL: Transcriptome analysis of IL-10-stimulated (M2c) macrophages by next-generation sequencing. Immunobiology. 222:847–856. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Q, Ni H, Lan L, Wei X, Xiang R and Wang Y: Fra-1 protooncogene regulates IL-6 expression in macrophages and promotes the generation of M2d macrophages. Cell Res. 20:701–712. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Ferrante CJ, Pinhal-Enfield G, Elson G, Cronstein BN, Hasko G, Outram S and Leibovich SJ: The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin-4 receptor alpha (IL-4Rα) signaling. Inflammation. 36:921–931. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Cassetta L and Pollard JW: Targeting macrophages: Therapeutic approaches in cancer. Nat Rev Drug Discov. 17:887–904. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N and Coussens LM: CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell. 16:91–102. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J and Condeelis J: A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 64:7022–7029. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Esser S, Lampugnani MG, Corada M, Dejana E and Risau W: Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 111:1853–1865. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Su S, Liu Q, Chen J, Chen J, Chen F, He C, Huang D, Wu W, Lin L, Huang W, et al: A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell. 25:605–620. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Squadrito ML, Baer C, Burdet F, Maderna C, Gilfillan GD, Lyle R, Ibberson M and De Palma M: Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 8:1432–1446. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Kim YB, Ahn YH, Jung JH, Lee YJ, Lee JH and Kang JL: Programming of macrophages by UV-irradiated apoptotic cancer cells inhibits cancer progression and lung metastasis. Cell Mol Immunol. 16:851–867. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Välimäki E, Cypryk W, Virkanen J, Nurmi K, Turunen PM, Eklund KK, Åkerman KE, Nyman TA and Matikainen S: Calpain activity is essential for ATP-driven unconventional vesicle-mediated protein secretion and inflammasome activation in human macrophages. J Immunol. 197:3315–3325. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Qu Y, Franchi L, Nunez G and Dubyak GR: Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol. 179:1913–1925. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Pegtel DM and Gould SJ: Exosomes. Annu Rev Biochem. 88:487–514. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Yang Q, Nanayakkara GK, Drummer C, Sun Y, Johnson C, Cueto R, Fu H, Shao Y, Wang L, Yang WY, et al: Low-intensity ultrasound-induced anti-inflammatory effects are mediated by several new mechanisms including gene induction, immunosuppressor cell promotion, and enhancement of exosome biogenesis and docking. Front Physiol. 8:8182017. View Article : Google Scholar : PubMed/NCBI | |
|
Xu J, Camfield R and Gorski SM: The interplay between exosomes and autophagy-partners in crime. J Cell Sci. 131:jcs2152102018. View Article : Google Scholar | |
|
Babuta M, Furi I, Bala S, Bukong TN, Lowe P, Catalano D, Calenda C, Kodys K and Szabo G: Dysregulated autophagy and lysosome function are linked to exosome production by Micro-RNA 155 in alcoholic liver disease. Hepatology. 70:2123–2141. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Li ZG, Scott MJ, Brzóska T, Sundd P, Li YH, Billiar TR, Wilson MA, Wang P and Fan J: Lung epithelial cell-derived IL-25 negatively regulates LPS-induced exosome release from macrophages. Mil Med Res. 5:242018.PubMed/NCBI | |
|
Brahimi-Horn MC, Chiche J and Pouysségur J: Hypoxia and cancer. J Mol Med (Berl). 85:1301–1307. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Goto Y, Ogawa Y, Tsumoto H, Miura Y, Nakamura TJ, Ogawa K, Akimoto Y, Kawakami H, Endo T, Yanoshita R and Tsujimoto M: Contribution of the exosome-associated form of secreted endoplasmic reticulum aminopeptidase 1 to exosome-mediated macrophage activation. Biochim Biophys Acta Mol Cell Res. 1865:874–888. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Sancho-Albero M, Navascués N, Mendoza G, Sebastián V, Arruebo M, Martín-Duque P and Santamaría J: Exosome origin determines cell targeting and the transfer of therapeutic nanoparticles towards target cells. J Nanobiotechnology. 17:162019. View Article : Google Scholar : PubMed/NCBI | |
|
Lai B, Wang J, Fagenson A, Sun Y, Saredy J, Lu Y, Nanayakkara G, Yang WY, Yu D, Shao Y, et al: Twenty novel disease group-specific and 12 new shared macrophage pathways in eight groups of 34 diseases including 24 inflammatory organ diseases and 10 types of tumors. Front Immunol. 10:26122019. View Article : Google Scholar : PubMed/NCBI | |
|
Bryl R, Piwocka O, Kawka E, Mozdziak P, Kempisty B and Knopik-Skrocka A: Cancer stem cells-the insight into non-coding RNAs. Cells. 11:36992022. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng N, Wang T, Luo Q, Liu Y, Yang J, Zhou Y, Xie G, Ma Y, Yuan X and Shen L: M2 macrophage-derived exosomes suppress tumor intrinsic immunogenicity to confer immunotherapy resistance. Oncoimmunology. 12:22109592023. View Article : Google Scholar : PubMed/NCBI | |
|
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ and Lötvall JO: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 9:654–659. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Roy S: miRNA in macrophage development and function. Antioxid Redox Signal. 25:795–804. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Li H, Jiang T, Li MQ, Zheng XL and Zhao GJ: Transcriptional regulation of macrophages polarization by MicroRNAs. Front Immunol. 9:11752018. View Article : Google Scholar : PubMed/NCBI | |
|
Yao Q, Song Z, Wang B and Zhang JA: Emerging roles of microRNAs in the metabolic control of immune cells. Cancer Lett. 433:10–17. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
McDonald MK, Tian Y, Qureshi RA, Gormley M, Ertel A, Gao R, Aradillas Lopez E, Alexander GM, Sacan A, Fortina P and Ajit SK: Functional significance of macrophage-derived exosomes in inflammation and pain. Pain. 155:1527–1539. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ma YS, Wu TM, Ling CC, Yu F, Zhang J, Cao PS, Gu LP, Wang HM, Xu H, Li L, et al: M2 macrophage-derived exosomal microRNA-155-5p promotes the immune escape of colon cancer by downregulating ZC3H12B. Mol Ther Oncolytics. 20:484–498. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Lan J, Sun L, Xu F, Liu L, Hu F, Song D, Hou Z, Wu W, Luo X, Wang J, et al: M2 macrophage-derived exosomes promote cell migration and invasion in colon cancer. Cancer Res. 79:146–158. 2019. View Article : Google Scholar | |
|
Yoshikawa T, Fukuda A, Omatsu M, Namikawa M, Sono M, Fukunaga Y, Masuda T, Araki O, Nagao M, Ogawa S, et al: Brg1 is required to maintain colorectal cancer stem cells. J Pathol. 255:257–269. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Yang Y, Guo Z, Chen W, Wang X, Cao M, Han X, Zhang K, Teng B, Cao J, Wu W, et al: M2 macrophage-derived exosomes promote angiogenesis and growth of pancreatic ductal adenocarcinoma by targeting E2F2. Mol Ther. 29:1226–1238. 2021. View Article : Google Scholar : | |
|
Xie D, Pei Q, Li J, Wan X and Ye T: Emerging role of E2F family in cancer stem cells. Front Oncol. 11:7231372021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang K, Li YJ, Peng LJ, Gao HF, Liu LM and Chen H: M2 macrophage-derived exosomal miR-193b-3p promotes progression and glutamine uptake of pancreatic cancer by targeting TRIM62. Biol Direct. 18:12023. View Article : Google Scholar : PubMed/NCBI | |
|
Li X, Xu H, Yi J, Dong C, Zhang H, Wang Z, Miao L and Zhou W: miR-365 secreted from M2 Macrophage-derived extracellular vesicles promotes pancreatic ductal adenocarcinoma progression through the BTG2/FAK/AKT axis. J Cell Mol Med. 25:4671–4683. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Thakur R, Trivedi R, Rastogi N, Singh M and Mishra DP: Inhibition of STAT3, FAK and Src mediated signaling reduces cancer stem cell load, tumorigenic potential and metastasis in breast cancer. Sci Rep. 5:101942015. View Article : Google Scholar : PubMed/NCBI | |
|
Yin Z, Ma T, Huang B, Lin L, Zhou Y, Yan J, Zou Y and Chen S: Macrophage-derived exosomal microRNA-501-3p promotes progression of pancreatic ductal adenocarcinoma through the TGFBR3-mediated TGF-β signaling pathway. J Exp Clin Cancer Res. 38:3102019. View Article : Google Scholar | |
|
Katoh M and Katoh M: WNT signaling and cancer stemness. Essays Biochem. 66:319–331. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Tang Q, Chen J, Di Z, Yuan W, Zhou Z, Liu Z, Han S, Liu Y, Ying G, Shu X and Di M: TM4SF1 promotes EMT and cancer stemness via the Wnt/β-catenin/SOX2 pathway in colorectal cancer. J Exp Clin Cancer Res. 39:2322020. View Article : Google Scholar | |
|
Chang J, Li H, Zhu Z, Mei P, Hu W, Xiong X and Tao J: microRNA-21-5p from M2 macrophage-derived extracellular vesicles promotes the differentiation and activity of pancreatic cancer stem cells by mediating KLF3. Cell Biol Toxicol. 38:577–590. 2022. View Article : Google Scholar : | |
|
Guan B, Dai X, Zhu Y and Geng Q: M2 macrophage-derived exosomal miR-1911-5p promotes cell migration and invasion in lung adenocarcinoma by down-regulating CELF2-activated ZBTB4 expression. Anticancer Drugs. 34:238–247. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Song S, Zhao Y, Wang X, Tong X, Chen X and Xiong Q: M2 macrophages-derived exosomal miR-3917 promotes the progression of lung cancer via targeting GRK6. Biol Chem. 404:41–57. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Le Q, Yao W, Chen Y, Yan B, Liu C, Yuan M, Zhou Y and Ma L: GRK6 regulates ROS response and maintains hematopoietic stem cell self-renewal. Cell Death Dis. 7:e24782016. View Article : Google Scholar : PubMed/NCBI | |
|
Lei J, Chen P, Zhang F, Zhang N, Zhu J, Wang X and Jiang T: M2 macrophages-derived exosomal microRNA-501-3p promotes the progression of lung cancer via targeting WD repeat domain 82. Cancer Cell Int. 21:912021. View Article : Google Scholar : PubMed/NCBI | |
|
Wei K, Ma Z, Yang F, Zhao X, Jiang W, Pan C, Li Z, Pan X, He Z, Xu J, et al: M2 macrophage-derived exosomes promote lung adenocarcinoma progression by delivering miR-942. Cancer Lett. 526:205–216. 2022. View Article : Google Scholar | |
|
Yu JM, Sun W, Wang ZH, Liang X, Hua F, Li K, Lv XX, Zhang XW, Liu YY, Yu JJ, et al: TRIB3 supports breast cancer stemness by suppressing FOXO1 degradation and enhancing SOX2 transcription. Nat Commun. 10:57202019. View Article : Google Scholar : PubMed/NCBI | |
|
Firat E and Niedermann G: FoxO proteins or loss of functional p53 maintain stemness of glioblastoma stem cells and survival after ionizing radiation plus PI3K/mTOR inhibition. Oncotarget. 7:54883–54896. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Yang X, Cai S, Shu Y, Deng X, Zhang Y, He N, Wan L, Chen X, Qu Y and Yu S: Exosomal miR-487a derived from m2 macrophage promotes the progression of gastric cancer. Cell Cycle. 20:434–444. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Cui HY, Rong JS, Chen J, Guo J, Zhu JQ, Ruan M, Zuo RR, Zhang SS, Qi JM and Zhang BH: Exosomal microRNA-588 from M2 polarized macrophages contributes to cisplatin resistance of gastric cancer cells. World J Gastroenterol. 27:6079–6092. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Xu DD, Zhou PJ, Wang Y, Zhang L, Fu WY, Ruan BB, Xu HP, Hu CZ, Tian L, Qin JH, et al: Reciprocal activation between STAT3 and miR-181b regulates the proliferation of esophageal cancer stem-like cells via the CYLD pathway. Mol Cancer. 15:402016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao G, Ding L, Yu H, Wang W, Wang H, Hu Y, Qin L, Deng G, Xie B, Li G and Qi L: M2-like tumor-associated macrophages transmit exosomal miR-27b-3p and maintain glioblastoma stem-like cell properties. Cell Death Discov. 8:3502022. View Article : Google Scholar : PubMed/NCBI | |
|
Tian B, Zhou L, Wang J and Yang P: miR-660-5p-loaded M2 macrophages-derived exosomes augment hepatocellular carcinoma development through regulating KLF3. Int Immunopharmacol. 101:1081572021. View Article : Google Scholar : PubMed/NCBI | |
|
Li X and Tang M: Exosomes released from M2 macrophages transfer miR-221-3p contributed to EOC progression through targeting CDKN1B. Cancer Med. 9:5976–5988. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Liu W, Long Q, Zhang W, Zeng D, Hu B, Liu S and Chen L: miRNA-221-3p derived from M2-polarized tumor-associated macrophage exosomes aggravates the growth and metastasis of osteosarcoma through SOCS3/JAK2/STAT3 axis. Aging (Albany NY). 13:19760–19775. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Yuan Y, Wang Z, Chen M, Jing Y, Shu W, Xie Z, Li Z, Xu J, He F, Jiao P, et al: Macrophage-derived exosomal miR-31-5p promotes oral squamous cell carcinoma tumourigenesis through the large tumor suppressor 2-mediated hippo signalling pathway. J Biomed Nanotechnol. 17:822–837. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Li Z, Wang Y, Zhu Y, Yuan C, Wang D, Zhang W, Qi B, Qiu J, Song X, Ye J, et al: The Hippo transducer TAZ promotes epithelial to mesenchymal transition and cancer stem cell maintenance in oral cancer. Mol Oncol. 9:1091–1105. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Yao J, Wang Z, Cheng Y, Ma C, Zhong Y, Xiao Y, Gao X and Li Z: M2 macrophage-derived exosomal microRNAs inhibit cell migration and invasion in gliomas through PI3K/AKT/mTOR signaling pathway. J Transl Med. 19:992021. View Article : Google Scholar : PubMed/NCBI | |
|
Gao XF, He HQ, Zhu XB, Xie SL and Cao Y: LncRNA SNHG20 promotes tumorigenesis and cancer stemness in glioblastoma via activating PI3K/Akt/mTOR signaling pathway. Neoplasma. 66:532–542. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Gao Y, Lin L, Li T, Yang J and Wei Y: The role of miRNA-223 in cancer: Function, diagnosis and therapy. Gene. 616:1–7. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Haneklaus M, Gerlic M, O'Neill LA and Masters SL: miR-223: Infection, inflammation and cancer. J Intern Med. 274:215–226. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu X, Shen H, Yin X, Yang M, Wei H, Chen Q, Feng F, Liu Y, Xu W and Li Y: Macrophages derived exosomes deliver miR-223 to epithelial ovarian cancer cells to elicit a chemoresistant phenotype. J Exp Clin Cancer Res. 38:812019. View Article : Google Scholar : PubMed/NCBI | |
|
Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang JD and Song E: Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer. 10:1172011. View Article : Google Scholar : PubMed/NCBI | |
|
Aucher A, Rudnicka D and Davis DM: MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J Immunol. 191:6250–6260. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Bhan A, Soleimani M and Mandal SS: Long noncoding RNA and cancer: A new paradigm. Cancer Res. 77:3965–3981. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Peng WX, Koirala P and Mo YY: LncRNA-mediated regulation of cell signaling in cancer. Oncogene. 36:5661–5667. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Chen F, Chen J, Yang L, Liu J, Zhang X, Zhang Y, Tu Q, Yin D, Lin D, Wong PP, et al: Extracellular vesicle-packaged HIF-1α-stabilizing lncRNA from tumour-associated macrophages regulates aerobic glycolysis of breast cancer cells. Nat Cell Biol. 21:498–510. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Q, Han Z, Zhu Y, Chen J and Li W: Role of hypoxia inducible factor-1 in cancer stem cells (Review). Mol Med Rep. 23:172021. | |
|
Yin Z, Zhou Y, Ma T, Chen S, Shi N, Zou Y, Hou B and Zhang C: Down-regulated lncRNA SBF2-AS1 in M2 macrophage-derived exosomes elevates miR-122-5p to restrict XIAP, thereby limiting pancreatic cancer development. J Cell Mol Med. 24:5028–5038. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Gao Z, Wang Q, Ji M, Guo X, Li L and Su X: Exosomal lncRNA UCA1 modulates cervical cancer stem cell self-renewal and differentiation through microRNA-122-5p/SOX2 axis. J Transl Med. 19:2292021. View Article : Google Scholar : PubMed/NCBI | |
|
Xu M, Zhou C, Weng J, Chen Z, Zhou Q, Gao J, Shi G, Ke A, Ren N, Sun H and Shen Y: Tumor associated macrophages-derived exosomes facilitate hepatocellular carcinoma malignance by transferring lncMMPA to tumor cells and activating glycolysis pathway. J Exp Clin Cancer Res. 41:2532022. View Article : Google Scholar : PubMed/NCBI | |
|
Gelardi ELM, Colombo G, Picarazzi F, Ferraris DM, Mangione A, Petrarolo G, Aronica E, Rizzi M, Mori M, La Motta C and Garavaglia S: A selective competitive inhibitor of aldehyde dehydrogenase 1A3 hinders cancer cell growth, invasiveness and stemness in vitro. Cancers (Basel). 13:3562021. View Article : Google Scholar : PubMed/NCBI | |
|
Guo Y, Sun W, Gao W, Li L, Liang Y, Mei Z, Liu B and Wang R: Long noncoding RNA H19 derived from M2 tumor-associated macrophages promotes bladder cell autophagy via stabilizing ULK1. J Oncol. 2022:34654592022. View Article : Google Scholar : PubMed/NCBI | |
|
Ren J, Ding L, Zhang D, Shi G, Xu Q, Shen S, Wang Y, Wang T and Hou Y: Carcinoma-associated fibroblasts promote the stemness and chemoresistance of colorectal cancer by transferring exosomal lncRNA H19. Theranostics. 8:3932–3948. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Shima H, Kida K, Adachi S, Yamada A, Sugae S, Narui K, Miyagi Y, Nishi M, Ryo A, Murata S, et al: Lnc RNA H19 is associated with poor prognosis in breast cancer patients and promotes cancer stemness. Breast Cancer Res Treat. 170:507–516. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wang F, Rong L, Zhang Z, Li M, Ma L, Ma Y, Xie X, Tian X and Yang Y: LncRNA H19-derived miR-675-3p promotes epithelial-mesenchymal transition and stemness in human pancreatic cancer cells by targeting the STAT3 pathway. J Cancer. 11:4771–4782. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang F, Sang Y, Chen D, Wu X, Wang X, Yang W and Chen Y: M2 macrophage-derived exosomal long non-coding RNA AGAP2-AS1 enhances radiotherapy immunity in lung cancer by reducing microRNA-296 and elevating NOTCH2. Cell Death Dis. 12:4672021. View Article : Google Scholar : PubMed/NCBI | |
|
Mi X, Xu R, Hong S, Xu T, Zhang W and Liu M: M2 macrophage-derived exosomal lncRNA AFAP1-AS1 and MicroRNA-26a affect cell migration and metastasis in esophageal cancer. Mol Ther Nucleic Acids. 22:779–790. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Huang W, Zhong Z, Luo C, Xiao Y, Li L, Zhang X, Yang L, Xiao K, Ning Y, Chen L, et al: The miR-26a/AP-2α/Nanog signaling axis mediates stem cell self-renewal and temozolomide resistance in glioma. Theranostics. 9:5497–5516. 2019. View Article : Google Scholar : | |
|
Xin L, Zhou LQ, Liu C, Zeng F, Yuan YW, Zhou Q, Li SH, Wu Y, Wang JL, Wu DZ and Lu H: Transfer of LncRNA CRNDE in TAM-derived exosomes is linked with cisplatin resistance in gastric cancer. EMBO Rep. 22:e521242021. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng J, Li XD, Wang P, Liu XB, Xue YX, Hu Y, Li Z, Li ZQ, Wang ZH and Liu YH: CRNDE affects the malignant biological characteristics of human glioma stem cells by negatively regulating miR-186. Oncotarget. 6:25339–25355. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Feng Z, Meng S, Zhou H, Xu Z, Tang Y, Li P, Liu C, Huang Y and Wu M: Functions and potential applications of circular RNAs in cancer stem cells. Front Oncol. 9:5002019. View Article : Google Scholar : PubMed/NCBI | |
|
Yu T, Wang Y, Fan Y, Fang N, Wang T, Xu T and Shu Y: CircRNAs in cancer metabolism: A review. J Hematol Oncol. 12:902019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou P, Chen X, Shi K, Qu H and Xia J: The characteristics, tumorigenicities and therapeutics of cancer stem cells based on circRNAs. Pathol Res Pract. 233:1538222022. View Article : Google Scholar : PubMed/NCBI | |
|
Zhuang Z, Jia L, Li W and Zheng Y: The emerging roles of circular RNAs in regulating the fate of stem cells. Mol Cell Biochem. 476:231–246. 2021. View Article : Google Scholar | |
|
Yu D, Chang Z, Liu X, Chen P, Zhang H and Qin Y: Macrophage-derived exosomes regulate gastric cancer cell oxaliplatin resistance by wrapping circ 0008253. Cell Cycle. 22:705–717. 2023. View Article : Google Scholar | |
|
Chen S, Chen Z, Li Z, Li S, Wen Z, Cao L, Chen Y, Xue P, Li H and Zhang D: Tumor-associated macrophages promote cholangiocarcinoma progression via exosomal Circ_0020256. Cell Death Dis. 13:942022. View Article : Google Scholar : PubMed/NCBI | |
|
Gu X, Shi Y, Dong M, Jiang L, Yang J and Liu Z: Exosomal transfer of tumor-associated macrophage-derived hsa_ circ_0001610 reduces radiosensitivity in endometrial cancer. Cell Death Dis. 12:8182021. View Article : Google Scholar | |
|
Ma J, Huang L, Gao YB, Li MX, Chen LL and Yang L: M2 macrophage facilitated angiogenesis in cutaneous squamous cell carcinoma via circ_TNFRSF21/miR-3619-5p/ROCK axis. Kaohsiung J Med Sci. 38:761–771. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Panis C, Pizzatti L, Souza GF and Abdelhay E: Clinical proteomics in cancer: Where we are. Cancer Let. 382:231–239. 2016. View Article : Google Scholar | |
|
Zhu Y, Chen X, Pan Q, Wang Y, Su S, Jiang C, Li Y, Xu N, Wu L, Lou X and Liu S: A comprehensive proteomics analysis reveals a secretory path- and status-dependent signature of exosomes released from tumor-associated macrophages. J Proteome Res. 14:4319–4331. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
El-Arabey AA, Denizli M, Kanlikilicer P, Bayraktar R, Ivan C, Rashed M, Kabil N, Ozpolat B, Calin GA, Salama SA, et al: GATA3 as a master regulator for interactions of tumor-associated macrophages with high-grade serous ovarian carcinoma. Cell Signal. 68:1095392020. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng P, Luo Q, Wang W, Li J, Wang T, Wang P, Chen L, Zhang P, Chen H, Liu Y, et al: Tumor-associated macrophages-derived exosomes promote the migration of gastric cancer cells by transfer of functional apolipoprotein E. Cell Death Dis. 9:4342018. View Article : Google Scholar : PubMed/NCBI | |
|
Lee HD, Koo BH, Kim YH, Jeon OH and Kim DS: Exosome release of ADAM15 and the functional implications of human macrophage-derived ADAM15 exosomes. FASEB J. 26:3084–3095. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Yu X, Zhang Q, Zhang X, Han Q, Li H, Mao Y, Wang X, Guo H, Irwin DM, Niu G and Tan H: Exosomes from macrophages exposed to apoptotic breast cancer cells promote breast cancer proliferation and metastasis. J Cancer. 10:2892–2906. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Wang M, Zhou L, Yu F, Zhang Y, Li P and Wang K: The functional roles of exosomal long non-coding RNAs in cancer. Cell Mol Life Sci. 76:2059–2076. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Sharma A and Johnson A: Exosome DNA: Critical regulator of tumor immunity and a diagnostic biomarker. J Cell Physiol. 235:1921–1932. 2020. View Article : Google Scholar | |
|
Azambuja JH, Ludwig N, Yerneni SS, Braganhol E and Whiteside TL: Arginase-1+ exosomes from reprogrammed macrophages promote glioblastoma progression. Int J Mol Sci. 21:39902020. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Y, Jin H, Song Y, Huang T, Cao J, Tang Q and Zou Z: Targeting tumor-associated macrophages: A potential treatment for solid tumors. J Cell Physiol. 236:3445–3465. 2021. View Article : Google Scholar | |
|
Pienta KJ, Machiels JP, Schrijvers D, Alekseev B, Shkolnik M, Crabb SJ, Li S, Seetharam S, Puchalski TA, Takimoto C, et al: Phase 2 study of carlumab (CNTO 888), a human monoclonal antibody against CC-chemokine ligand 2 (CCL2), in metastatic castration-resistant prostate cancer. Invest New Drugs. 31:760–768. 2013. View Article : Google Scholar | |
|
Moisan F, Francisco EB, Brozovic A, Duran GE, Wang YC, Chaturvedi S, Seetharam S, Snyder LA, Doshi P and Sikic BI: Enhancement of paclitaxel and carboplatin therapies by CCL2 blockade in ovarian cancers. Mol Oncol. 8:1231–1239. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Xu F, Wei Y, Tang Z, Liu B and Dong J: Tumor-associated macrophages in lung cancer: Friend or foe? (Review). Mol Med Rep. 22:4107–4115. 2020.PubMed/NCBI | |
|
DiPersio JF, Uy GL, Yasothan U and Kirkpatrick P: Plerixafor. Nat Rev Drug Discov. 8:105–106. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Tannous BA, Poznansky MC and Chen H: CXCR4 antagonist AMD3100 (plerixafor): From an impurity to a therapeutic agent. Pharmacol Res. 159:1050102020. View Article : Google Scholar : PubMed/NCBI | |
|
Hume DA and MacDonald KP: Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood. 119:1810–1820. 2012. View Article : Google Scholar | |
|
Bonapace L, Coissieux MM, Wyckoff J, Mertz KD, Varga Z, Junt T and Bentires-Alj M: Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature. 515:130–133. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Advani R, Flinn I, Popplewell L, Forero A, Bartlett NL, Ghosh N, Kline J, Roschewski M, LaCasce A, Collins GP, et al: CD47 blockade by Hu5F9-G4 and rituximab in non-Hodgkin's lymphoma. N Engl J Med. 379:1711–1721. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Petrova PS, Viller NN, Wong M, Pang X, Lin GH, Dodge K, Chai V, Chen H, Lee V, House V, et al: TTI-621 (SIRPαFc): A CD47-blocking innate immune checkpoint inhibitor with broad antitumor activity and minimal erythrocyte binding. Clin Cancer Res. 23:1068–1079. 2017. View Article : Google Scholar | |
|
Bouwstra R, van Meerten T and Bremer E: CD47-SIRPα blocking-based immunotherapy: Current and prospective therapeutic strategies. Clin Transl Med. 12:e9432022. View Article : Google Scholar | |
|
Zheng JH, Nguyen VH, Jiang SN, Park SH, Tan W, Hong SH, Shin MG, Chung IJ, Hong Y, Bom HS, et al: Two-step enhanced cancer immunotherapy with engineered Salmonella typhimurium secreting heterologous flagellin. Sci Transl Med. 9:eaak95372017. View Article : Google Scholar : PubMed/NCBI | |
|
Yuan D, Zhao Y, Banks WA, Bullock KM, Haney M, Batrakova E and Kabanov AV: Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials. 142:1–12. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li J, Li N and Wang J: M1 macrophage-derived exosome-encapsulated cisplatin can enhance its anti-lung cancer effect. Minerva Med. Apr 8–2020.Epub ahead of print. View Article : Google Scholar | |
|
Kim MS, Haney MJ, Zhao Y, Mahajan V, Deygen I, Klyachko NL, Inskoe E, Piroyan A, Sokolsky M, Okolie O, et al: Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine. 12:655–664. 2016. View Article : Google Scholar | |
|
Bellmunt À M, López-Puerto L, Lorente J and Closa D: Involvement of extracellular vesicles in the macrophage-tumor cell communication in head and neck squamous cell carcinoma. PLoS One. 14:e02247102019. View Article : Google Scholar : PubMed/NCBI | |
|
Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B and Simons M: Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 319:1244–1247. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Wu ATH, Srivastava P, Yadav VK, Tzeng DTW, Iamsaard S, Su EC, Hsiao M and Liu MC: Ovatodiolide, isolated from Anisomeles indica, suppresses bladder carcinogenesis through suppression of mTOR/β-catenin/CDK6 and exosomal miR-21 derived from M2 tumor-associated macrophages. Toxicol Appl Pharmacol. 401:1151092020. View Article : Google Scholar | |
|
Guo J, Wang X, Guo Q, Zhu S, Li P, Zhang S and Min L: M2 macrophage derived extracellular vesicle-mediated transfer of MiR-186-5p promotes colon cancer progression by targeting DLC1. Int J Biol Sci. 18:1663–1676. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Wang P, Li GY, Zhou L, Jiang HL, Yang Y and Wu HT: Exosomes from M2 macrophages promoted glycolysis in FaDu cells by inhibiting PDLIM2 expression to stabilize PFKL. Neoplasma. 69:1041–1053. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Song L, Luan B, Xu Q, Shi R and Wang X: microRNA-155-3p delivered by M2 macrophages-derived exosomes enhances the progression of medulloblastoma through regulation of WDR82. J Transl Med. 20:132022. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Z, Hu J, Ishihara M, Sharrow AC, Flora K, He Y and Wu L: The miRNA-21-5p payload in exosomes from M2 macrophages drives tumor cell aggression via PTEN/Akt signaling in renal cell carcinoma. Int J Mol Sci. 23:30052022. View Article : Google Scholar : PubMed/NCBI |
