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Review Open Access

Role of exosomes in pancreatic cancer (Review)

  • Authors:
    • Hao Liu
    • Shishi Qiao
    • Xiaoyue Fan
    • Yufei Gu
    • Yingxuan Zhang
    • Shuai Huang
  • View Affiliations / Copyright

    Affiliations: Department of Hepatobiliary and Pancreatic Surgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, P.R. China, Department of Pathology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, P.R. China
    Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 298
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    Published online on: February 17, 2021
       https://doi.org/10.3892/ol.2021.12559
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Abstract

Pancreatic cancer (PC) is a malignant tumour of the human digestive system that has a poor prognosis. Exosomes contain proteins and nucleic acids, and constitute a class of extracellular vesicles defined as membrane‑bound nanovesicles of endocytic origin, with a diameter of 40‑150 nm. Exosomes are potential diagnostic markers of PC; however, their roles in cancer initiation and progression remain unclear. Previous studies have focused on the molecular mechanisms and functions of exosomes that allow them to accelerate PC cell proliferation, migration and invasion. The present review discusses the interactions between exosomes and the pathophysiology of PC. The potential clinical applications of exosomes are also discussed.
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1 

Siegel RL, Miller KD and Jemal A: Cancer statistics, 2018. CA Cancer J Clin. 68:7–30. 2018. View Article : Google Scholar : PubMed/NCBI

2 

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI

3 

Deplanque G and Demartines N: Pancreatic cancer: Are more chemotherapy and surgery needed? Lancet. 389:985–986. 2017. View Article : Google Scholar : PubMed/NCBI

4 

Théry C: Exosomes: Secreted vesicles and intercellular communications. F1000 Biol Rep. 3:152011. View Article : Google Scholar : PubMed/NCBI

5 

Kalluri R: The biology and function of exosomes in cancer. J Clin Invest. 126:1208–1215. 2016. View Article : Google Scholar : PubMed/NCBI

6 

Vader P, Breakefield XO and Wood MJ: Extracellular vesicles: Emerging targets for cancer therapy. Trends Mol Med. 20:385–393. 2014. View Article : Google Scholar : PubMed/NCBI

7 

Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM and Breakefield XO: Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 10:1470–1476. 2008. View Article : Google Scholar : PubMed/NCBI

8 

Johnstone RM, Adam M, Hammond JR, Orr L and Turbide C: Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 262:9412–9420. 1987. View Article : Google Scholar : PubMed/NCBI

9 

Kowal J, Tkach M and Théry C: Biogenesis and secretion of exosomes. Curr Opin Cell Biol. 29:116–125. 2014. View Article : Google Scholar : PubMed/NCBI

10 

Meehan K and Vella LJ: The contribution of tumour-derived exosomes to the hallmarks of cancer. Crit Rev Clin Lab Sci. 53:121–131. 2016. View Article : Google Scholar : PubMed/NCBI

11 

Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, Chow A, O'Connor STF, Li S, Chin AR, et al: Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol. 17:183–194. 2015. View Article : Google Scholar : PubMed/NCBI

12 

Mu W, Rana S and Zöller M: Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia. 15:875–887. 2013. View Article : Google Scholar : PubMed/NCBI

13 

Sung BH, Ketova T, Hoshino D, Zijlstra A and Weaver AM: Directional cell movement through tissues is controlled by exosome secretion. Nat Commun. 6:71642015. View Article : Google Scholar : PubMed/NCBI

14 

Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G and Amigorena S: Eradication of established murine tumors using a novel cell-free vaccine: Dendritic cell-derived exosomes. Nat Med. 4:594–600. 1998. View Article : Google Scholar : PubMed/NCBI

15 

Abusamra AJ, Zhong Z, Zheng X, Li M, Ichim TE, Chin JL and Min WP: Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis. 35:169–173. 2005. View Article : Google Scholar : PubMed/NCBI

16 

Kamerkar S, LeBleu VS, Sugimoto H, Yang S, Ruivo CF, Melo SA, Lee JJ and Kalluri R: Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature. 546:498–503. 2017. View Article : Google Scholar : PubMed/NCBI

17 

Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, Ostrowski M and Théry C: Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 72:4920–4930. 2012. View Article : Google Scholar : PubMed/NCBI

18 

Bhatia A and Kumar Y: Cellular and molecular mechanisms in cancer immune escape: A comprehensive review. Expert Rev Clin Immunol. 10:41–62. 2014. View Article : Google Scholar : PubMed/NCBI

19 

Mateescu B, Kowal EJ, van Balkom BW, Bartel S, Bhattacharyya SN, Buzás EI, Buck AH, de Candia P, Chow FWN, Das S, et al: Obstacles and opportunities in the functional analysis of extracellular vesicle RNA-an ISEV position paper. J Extracell Vesicles. 6:12860952017. View Article : Google Scholar : PubMed/NCBI

20 

Colombo M, Raposo G and Théry C: Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 30:255–289. 2014. View Article : Google Scholar : PubMed/NCBI

21 

Zhang HG and Grizzle WE: Exosomes: A novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am J Pathol. 184:28–41. 2014. View Article : Google Scholar : PubMed/NCBI

22 

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

23 

Hong CS, Funk S and Whiteside TL: Isolation of biologically active exosomes from plasma of patients with cancer. Methods Mol Biol. 1633:257–265. 2017. View Article : Google Scholar : PubMed/NCBI

24 

Xie JX, Fan X, Drummond CA, Majumder R, Xie Y, Chen T, Liu L, Haller ST, Brewster PS, Dworkin LD, et al: MicroRNA profiling in kidney disease: Plasma versus plasma-derived exosomes. Gene. 627:1–8. 2017. View Article : Google Scholar : PubMed/NCBI

25 

Zhou X, Lu Z, Wang T, Huang Z, Zhu W and Miao Y: Plasma miRNAs in diagnosis and prognosis of pancreatic cancer: A miRNA expression analysis. Gene. 673:181–193. 2018. View Article : Google Scholar : PubMed/NCBI

26 

Théry C, Ostrowski M and Segura E: Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 9:581–593. 2009. View Article : Google Scholar : PubMed/NCBI

27 

Madhavan B, Yue S, Galli U, Rana S, Gross W, Müller M, Giese NA, Kalthoff H, Becker T, Büchler MW and Zöller M: Combined evaluation of a panel of protein and miRNA serum-exosome biomarkers for pancreatic cancer diagnosis increases sensitivity and specificity. Int J Cancer. 136:2616–2627. 2015. View Article : Google Scholar : PubMed/NCBI

28 

Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, et al: Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 523:177–182. 2015. View Article : Google Scholar : PubMed/NCBI

29 

Street JM, Koritzinsky EH, Glispie DM, Star RA and Yuen PST: Urine exosomes: An emerging trove of biomarkers. Adv Clin Chem. 78:103–122. 2017. View Article : Google Scholar : PubMed/NCBI

30 

Katsiougiannis S, Chia D, Kim Y, Singh RP and Wong DTW: Saliva exosomes from pancreatic tumor-bearing mice modulate NK cell phenotype and antitumor cytotoxicity. FASEB J. 31:998–1010. 2017. View Article : Google Scholar : PubMed/NCBI

31 

Sun Y, Liu S, Qiao Z, Shang Z, Xia Z, Niu X, Qian L, Zhang Y, Fan L, Cao CX and Xiao H: Systematic comparison of exosomal proteomes from human saliva and serum for the detection of lung cancer. Anal Chim Acta. 982:84–95. 2017. View Article : Google Scholar : PubMed/NCBI

32 

Qin W, Tsukasaki Y, Dasgupta S, Mukhopadhyay N, Ikebe M and Sauter ER: Exosomes in human breast milk promote EMT. Clin Cancer Res. 22:4517–4524. 2016. View Article : Google Scholar : PubMed/NCBI

33 

Mathivanan S, Ji H and Simpson RJ: Exosomes: Extracellular organelles important in intercellular communication. J Proteomics. 73:1907–1920. 2010. View Article : Google Scholar : PubMed/NCBI

34 

van Niel G, Porto-Carreiro I, Simoes S and Raposo G: Exosomes: A common pathway for a specialized function. J Biochem. 140:13–21. 2006. View Article : Google Scholar : PubMed/NCBI

35 

Nazarenko I, Rana S, Baumann A, McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT and Zöller M: Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res. 70:1668–1678. 2010. View Article : Google Scholar : PubMed/NCBI

36 

Raimondo F, Morosi L, Chinello C, Magni F and Pitto M: Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics. 11:709–720. 2011. View Article : Google Scholar : PubMed/NCBI

37 

Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G and Altevogt P: Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol. 107:563–571. 2007. View Article : Google Scholar : PubMed/NCBI

38 

Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, Chen D, Gu J, He X and Huang S: Circular RNA is enriched and stable in exosomes: A promising biomarker for cancer diagnosis. Cell Res. 25:981–984. 2015. View Article : Google Scholar : PubMed/NCBI

39 

Salido-Guadarrama I, Romero-Cordoba S, Peralta-Zaragoza O, Hidalgo-Miranda A and Rodríguez-Dorantes M: MicroRNAs transported by exosomes in body fluids as mediators of intercellular communication in cancer. OncoTargets Ther. 7:1327–1338. 2014.

40 

Medina PP, Nolde M and Slack FJ: OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature. 467:86–90. 2010. View Article : Google Scholar : PubMed/NCBI

41 

Schutters K and Reutelingsperger C: Phosphatidylserine targeting for diagnosis and treatment of human diseases. Apoptosis. 15:1072–1082. 2010. View Article : Google Scholar : PubMed/NCBI

42 

Beloribi S, Ristorcelli E, Breuzard G, Silvy F, Bertrand-Michel J, Beraud E, Verine A and Lombardo D: Exosomal lipids impact notch signaling and induce death of human pancreatic tumoral SOJ-6 cells. PLoS One. 7:e474802012. View Article : Google Scholar : PubMed/NCBI

43 

Beloribi-Djefaflia S, Siret C and Lombardo D: Exosomal lipids induce human pancreatic tumoral MiaPaCa-2 cells resistance through the CXCR4-SDF-1α signaling axis. Oncoscience. 2:15–30. 2014. View Article : Google Scholar : PubMed/NCBI

44 

Zhang Y, Yang J, Li H, Wu Y, Zhang H and Chen W: Tumor markers CA19-9, CA242 and CEA in the diagnosis of pancreatic cancer: A meta-analysis. Int J Clin Exp Med. 8:11683–11691. 2015.PubMed/NCBI

45 

Frebourg T, Bercoff E, Manchon N, Senant J, Basuyau JP, Breton P, Janvresse A, Brunelle P and Bourreille J: The evaluation of CA 19-9 antigen level in the early detection of pancreatic cancer. A prospective study of 866 patients. Cancer. 62:2287–2290. 1988. View Article : Google Scholar : PubMed/NCBI

46 

Awad W, Adamczyk B, Ornros J, Karlsson NG, Mani K and Logan DT: Structural aspects of N-glycosylations and the C-terminal region in human glypican-1. J Biol Chem. 290:22991–23008. 2015. View Article : Google Scholar : PubMed/NCBI

47 

Aikawa T, Whipple CA, Lopez ME, Gunn J, Young A, Lander AD and Korc M: Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells. J Clin Invest. 118:89–99. 2008. View Article : Google Scholar : PubMed/NCBI

48 

Frampton AE, Prado MM, Lopez-Jimenez E, Fajardo-Puerta AB, Jawad ZAR, Lawton P, Giovannetti E, Habib NA, Castellano L, Stebbing J, et al: Glypican-1 is enriched in circulating-exosomes in pancreatic cancer and correlates with tumor burden. Oncotarget. 9:19006–19013. 2018. View Article : Google Scholar : PubMed/NCBI

49 

Joshi GK, Deitz-McElyea S, Liyanage T, Lawrence K, Mali S, Sardar R and Korc M: Label-Free nanoplasmonic-based short noncoding RNA sensing at attomolar concentrations allows for quantitative and highly specific assay of MicroRNA-10b in biological fluids and circulating exosomes. ACS Nano. 9:11075–11089. 2015. View Article : Google Scholar : PubMed/NCBI

50 

Taller D, Richards K, Slouka Z, Senapati S, Hill R, Go DB and Chang HC: On-chip surface acoustic wave lysis and ion-exchange nanomembrane detection of exosomal RNA for pancreatic cancer study and diagnosis. Lab Chip. 15:1656–1666. 2015. View Article : Google Scholar : PubMed/NCBI

51 

Xu YF, Hannafon BN, Zhao YD, Postier RG and Ding WQ: Plasma exosome miR-196a and miR-1246 are potential indicators of localized pancreatic cancer. Oncotarget. 8:77028–77040. 2017. View Article : Google Scholar : PubMed/NCBI

52 

Takahasi K, Iinuma H, Wada K, Minezaki S, Kawamura S, Kainuma M, Ikeda Y, Shibuya M, Miura F and Sano K: Usefulness of exosome-encapsulated microRNA-451a as a minimally invasive biomarker for prediction of recurrence and prognosis in pancreatic ductal adenocarcinoma. J Hepatobiliary Pancreat Sci. 25:155–161. 2018. View Article : Google Scholar : PubMed/NCBI

53 

Que R, Ding G, Chen J and Cao L: Analysis of serum exosomal microRNAs and clinicopathologic features of patients with pancreatic adenocarcinoma. World J Surg Oncol. 11:2192013. View Article : Google Scholar : PubMed/NCBI

54 

Yan Y, Fu G and Ming L: Role of exosomes in pancreatic cancer. Oncol Lett. 15:7479–7488. 2018.PubMed/NCBI

55 

Machida T, Tomofuji T, Maruyama T, Yoneda T, Ekuni D, Azuma T, Miyai H, Mizuno H, Kato H, Tsutsumi K, et al: miR1246 and miR4644 in salivary exosome as potential biomarkers for pancreatobiliary tract cancer. Oncol Rep. 36:2375–2381. 2016. View Article : Google Scholar : PubMed/NCBI

56 

Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al: Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 17:816–826. 2015. View Article : Google Scholar : PubMed/NCBI

57 

Tsukamoto M, Iinuma H, Yagi T, Matsuda K and Hashiguchi Y: Circulating exosomal MicroRNA-21 as a biomarker in each tumor stage of colorectal cancer. Oncology. 92:360–370. 2017. View Article : Google Scholar : PubMed/NCBI

58 

Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A and Kalluri R: Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem. 289:3869–3875. 2014. View Article : Google Scholar : PubMed/NCBI

59 

Sessa F, Bonato M, Bisoni D, Ranzani GN and Capella C: Ki-ras and p53 gene mutations in pancreatic ductal carcinoma: A relationship with tumor phenotype and survival. Eur J Histochem. 42:Spec No. 67–76. 1998.PubMed/NCBI

60 

Charrier A, Chen R, Chen L, Kemper S, Hattori T, Takigawa M and Brigstock DR: Connective tissue growth factor (CCN2) and microRNA-21 are components of a positive feedback loop in pancreatic stellate cells (PSC) during chronic pancreatitis and are exported in PSC-derived exosomes. J Cell Commun Signal. 8:147–156. 2014. View Article : Google Scholar : PubMed/NCBI

61 

Pang W, Su J, Wang Y, Feng H, Dai X, Yuan Y, Chen X and Yao W: Pancreatic cancer-secreted miR-155 implicates in the conversion from normal fibroblasts to cancer-associated fibroblasts. Cancer Sci. 106:1362–1369. 2015. View Article : Google Scholar : PubMed/NCBI

62 

Richards KE, Zeleniak AE, Fishel ML, Wu J, Littlepage LE and Hill R: Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene. 36:1770–1778. 2017. View Article : Google Scholar : PubMed/NCBI

63 

von Ahrens D, Bhagat TD, Nagrath D, Maitra A and Verma A: The role of stromal cancer-associated fibroblasts in pancreatic cancer. J Hematol Oncol. 10:762017. View Article : Google Scholar : PubMed/NCBI

64 

Wu DM, Wen X, Han XR, Wang S, Wang YJ, Shen M, Fan SH, Zhang ZF, Shan Q, Li MQ, et al: Bone marrow mesenchymal stem cell-derived exosomal MicroRNA-126-3p inhibits pancreatic cancer development by targeting ADAM9. Mol Ther Nucleic Acids. 16:229–245. 2019. View Article : Google Scholar : PubMed/NCBI

65 

Yang J, Zhang Z, Zhang Y, Ni X, Zhang G, Cui X, Liu M, Xu C, Zhang Q, Zhu H, et al: ZIP4 promotes muscle wasting and cachexia in mice with orthotopic pancreatic tumors by stimulating RAB27B-regulated release of extracellular vesicles from cancer cells. Gastroenterology. 156:722–734. 2019. View Article : Google Scholar : PubMed/NCBI

66 

Yu Z, Zhao S, Ren L, Wang L, Chen Z, Hoffman RM and Zhou J: Pancreatic cancer-derived exosomes promote tumor metastasis and liver pre-metastatic niche formation. Oncotarget. 8:63461–63483. 2017. View Article : Google Scholar : PubMed/NCBI

67 

Sceneay J, Smyth MJ and Möller A: The pre-metastatic niche: Finding common ground. Cancer Metastasis Rev. 32:449–464. 2013. View Article : Google Scholar : PubMed/NCBI

68 

Nielsen SR, Quaranta V, Linford A, Emeagi P, Rainer C, Santos A, Ireland L, Sakai T, Sakai K, Kim YS, et al: Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis. Nat Cell Biol. 18:549–560. 2016. View Article : Google Scholar : PubMed/NCBI

69 

Dey A, Allen J and Hankey-Giblin PA: Ontogeny and polarization of macrophages in inflammation: Blood monocytes versus tissue macrophages. Front Immunol. 5:6832015. View Article : Google Scholar : PubMed/NCBI

70 

Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Mark MT, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al: Tumour exosome integrins determine organotropic metastasis. Nature. 527:329–335. 2015. View Article : Google Scholar : PubMed/NCBI

71 

Matsushita H, Yang YM, Pandol SJ and Seki E: Exosome migration inhibitory factor as a marker and therapeutic target for pancreatic cancer. Gastroenterology. 150:1033–1035. 2016. View Article : Google Scholar : PubMed/NCBI

72 

Milane L, Singh A, Mattheolabakis G, Suresh M and Amiji MM: Exosome mediated communication within the tumor microenvironment. J Control Release. 219:278–294. 2015. View Article : Google Scholar : PubMed/NCBI

73 

Syn N, Wang L, Sethi G, Thiery JP and Goh BC: Exosome-mediated metastasis: From epithelial-mesenchymal transition to escape from immunosurveillance. Trends Pharmacol Sci. 37:606–617. 2016. View Article : Google Scholar : PubMed/NCBI

74 

Steinbichler TB, Dudás J, Riechelmann H and Skvortsova II: The role of exosomes in cancer metastasis. Semin Cancer Biol. 44:170–181. 2017. View Article : Google Scholar : PubMed/NCBI

75 

Ackerman D and Simon MC: Hypoxia, lipids, and cancer: Surviving the harsh tumor microenvironment. Trends Cell Biol. 24:472–478. 2014. View Article : Google Scholar : PubMed/NCBI

76 

Lewis CE and Pollard JW: Distinct role of macrophages in different tumor microenvironments. Cancer Res. 66:605–612. 2006. View Article : Google Scholar : PubMed/NCBI

77 

King HW, Michael MZ and Gleadle JM: Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer. 12:4212012. View Article : Google Scholar : PubMed/NCBI

78 

Semenza GL: Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene. 29:625–634. 2010. View Article : Google Scholar : PubMed/NCBI

79 

Löfstedt T, Fredlund E, Holmquist-Mengelbier L, Pietras A, Ovenberger M, Poellinger L and Påhlman S: Hypoxia inducible factor-2alpha in cancer. Cell Cycle. 6:919–926. 2007. View Article : Google Scholar : PubMed/NCBI

80 

Singh A, Talekar M, Raikar A and Amiji M: Macrophage-targeted delivery systems for nucleic acid therapy of inflammatory diseases. J Control Release. 190:515–530. 2014. View Article : Google Scholar : PubMed/NCBI

81 

Wang J, Cao Z, Zhang XM, Nakamura M, Sun M, Hartman J, Harris RA, Sun Y and Cao Y: Novel mechanism of macrophage-mediated metastasis revealed in a zebrafish model of tumor development. Cancer Res. 75:306–315. 2015. View Article : Google Scholar : PubMed/NCBI

82 

Wang X, Luo G, Zhang K, Cao J, Huang C, Jiang T, Liu B, Su L and Qiu Z: Hypoxic tumor-derived exosomal miR-301a mediates M2 macrophage polarization via PTEN/PI3Kγ to promote pancreatic cancer metastasis. Cancer Res. 78:4586–4598. 2018. View Article : Google Scholar : PubMed/NCBI

83 

Li Z, Yanfang W, Li J, Jiang P, Peng T, Chen K, Zhao X, Zhang Y, Zhen P, Zhu J and Li X: Tumor-released exosomal circular RNA PDE8A promotes invasive growth via the miR-338/MACC1/MET pathway in pancreatic cancer. Cancer Lett. 432:237–250. 2018. View Article : Google Scholar : PubMed/NCBI

84 

Takikawa T, Masamune A, Yoshida N, Hamada S, Kogure T and Shimosegawa T: Exosomes derived from pancreatic stellate cells: MicroRNA signature and effects on pancreatic cancer cells. Pancreas. 46:19–27. 2017. View Article : Google Scholar : PubMed/NCBI

85 

Chen D, Wu X, Xia M, Wu F, Ding J, Jiao Y, Zhan Q and An F: Upregulated exosomic miR-23b-3p plays regulatory roles in the progression of pancreatic cancer. Oncol Rep. 38:2182–2188. 2017. View Article : Google Scholar : PubMed/NCBI

86 

Kurahara H, Shinchi H, Mataki Y, Maemura K, Noma H, Kubo F, Sakoda M, Ueno S, Natsugoe S and Takao S: Significance of M2-polarized tumor-associated macrophage in pancreatic cancer. J Surg Res. 167:e211–e219. 2011. View Article : Google Scholar : PubMed/NCBI

87 

Di Caro G, Cortese N, Castino GF, Grizzi F, Gavazzi F, Ridolfi C, Capretti G, Mineri R, Todoric J, Zerbi A, et al: Dual prognostic significance of tumour-associated macrophages in human pancreatic adenocarcinoma treated or untreated with chemotherapy. Gut. 65:1710–1720. 2016. View Article : Google Scholar : PubMed/NCBI

88 

Szczepanski MJ, Szajnik M, Welsh A, Whiteside TL and Boyiadzis M: Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1. Haematologica. 96:1302–1309. 2011. View Article : Google Scholar : PubMed/NCBI

89 

Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS and Albelda SM: Polarization of tumor-associated neutrophil phenotype by TGF-beta: ‘N1’ versus ‘N2’ TAN. Cancer Cell. 16:183–194. 2009. View Article : Google Scholar : PubMed/NCBI

90 

Benson DD, Meng X, Fullerton DA, Moore EE, Lee JH, Ao L, Silliman CC and Barnett CC Jr: Activation state of stromal inflammatory cells in murine metastatic pancreatic adenocarcinoma. Am J Physiol Regul Integr Comp Physiol. 302:R1067–R1075. 2012. View Article : Google Scholar : PubMed/NCBI

91 

Galdiero MR, Bonavita E, Barajon I, Garlanda C, Mantovani A and Jaillon S: Tumor associated macrophages and neutrophils in cancer. Immunobiology. 218:1402–1410. 2013. View Article : Google Scholar : PubMed/NCBI

92 

Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y and Hiraoka N: Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer. 108:914–923. 2013. View Article : Google Scholar : PubMed/NCBI

93 

Hiraoka N, Onozato K, Kosuge T and Hirohashi S: Prevalence of FOXP3+ regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its premalignant lesions. Clin Cancer Res. 12:5423–5434. 2006. View Article : Google Scholar : PubMed/NCBI

94 

Szajnik M, Czystowska M, Szczepanski MJ, Mandapathil M and Whiteside TL: Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS One. 5:e114692010. View Article : Google Scholar : PubMed/NCBI

95 

Wada J, Onishi H, Suzuki H, Yamasaki A, Nagai S, Morisaki T and Katano M: Surface-bound TGF-beta1 on effusion-derived exosomes participates in maintenance of number and suppressive function of regulatory T-cells in malignant effusions. Anticancer Res. 30:3747–3757. 2010.PubMed/NCBI

96 

Ding G, Zhou L, Qian Y, Fu M, Chen J, Chen J, Xiang J, Wu Z, Jiang G and Cao L: Pancreatic cancer-derived exosomes transfer miRNAs to dendritic cells and inhibit RFXAP expression via miR-212-3p. Oncotarget. 6:29877–29888. 2015. View Article : Google Scholar : PubMed/NCBI

97 

Zhou M, Chen J, Zhou L, Chen W, Ding G and Cao L: Pancreatic cancer derived exosomes regulate the expression of TLR4 in dendritic cells via miR-203. Cell Immunol. 292:65–69. 2014. View Article : Google Scholar : PubMed/NCBI

98 

Nagathihalli NS, Castellanos JA, Shi C, Beesetty Y, Reyzer ML, Caprioli R, Chen X, Walsh AJ, Skala MC, Moses HL and Merchant NB: Signal transducer and activator of transcription 3, mediated remodeling of the tumor microenvironment results in enhanced tumor drug delivery in a mouse model of pancreatic cancer. Gastroenterology. 149:1932–1943, e1939. 2015. View Article : Google Scholar : PubMed/NCBI

99 

Lobb RJ, van Amerongen R, Wiegmans A, Ham S, Larsen JE and Möller A: Exosomes derived from mesenchymal non-small cell lung cancer cells promote chemoresistance. Int J Cancer. 141:614–620. 2017. View Article : Google Scholar : PubMed/NCBI

100 

Santos JC, da Silva Lima N, Sarian LO, Matheu A, Ribeiro ML and Derchain SFM: Exosome-mediated breast cancer chemoresistance via miR-155 transfer. Sci Rep. 8:8292018. View Article : Google Scholar : PubMed/NCBI

101 

Li J, Yang X, Guan H, Mizokami A, Keller ET, Xu X, Liu X, Tan J, Hu L, Lu Y and Zhang J: Exosome-derived microRNAs contribute to prostate cancer chemoresistance. Int J Oncol. 49:838–846. 2016. View Article : Google Scholar : PubMed/NCBI

102 

Zheng P, Chen L, Yuan X, Luo Q, Liu Y, Xie G, Ma Y and Shen L: Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res. 36:532017. View Article : Google Scholar : PubMed/NCBI

103 

Wang M, Qiu R, Yu S, Xu X, Li G, Gu R, Tan C, Zhu W and Shen B: Paclitaxelresistant gastric cancer MGC803 cells promote epithelialtomesenchymal transition and chemoresistance in paclitaxelsensitive cells via exosomal delivery of miR1555p. Int J Oncol. 54:326–338. 2019.PubMed/NCBI

104 

Marques-Rocha JL, Garcia-Lacarte M, Samblas M, Bressan J, Martínez JA and Milagro FI: Regulatory roles of miR-155 and let-7b on the expression of inflammation-related genes in THP-1 cells: Effects of fatty acids. J Physiol Biochem. 74:579–589. 2018. View Article : Google Scholar : PubMed/NCBI

105 

Patel GK, Khan MA, Bhardwaj A, Srivastava SK, Zubair H, Patton MC, Singh S, Khushman M and Singh AP: Exosomes confer chemoresistance to pancreatic cancer cells by promoting ROS detoxification and miR-155-mediated suppression of key gemcitabine-metabolising enzyme, DCK. Br J Cancer. 116:609–619. 2017. View Article : Google Scholar : PubMed/NCBI

106 

Mikamori M, Yamada D, Eguchi H, Hasegawa S, Kishimoto T, Tomimaru Y, Asaoka T, Noda T, Wada H, Kawamoto K, et al: MicroRNA-155 controls exosome synthesis and promotes gemcitabine resistance in pancreatic ductal adenocarcinoma. Sci Rep. 7:423392017. View Article : Google Scholar : PubMed/NCBI

107 

Asuncion Valenzuela MM, Castro I, Gonda A, Diaz Osterman CJ, Jutzy JM, Aspe JR, Khan S, Neidigh JW and Wall NR: Cell death in response to antimetabolites directed at ribonucleotide reductase and thymidylate synthase. Onco Targets Ther. 8:495–507. 2015.PubMed/NCBI

108 

Fan J, Wei Q, Koay EJ, Liu Y, Ning B, Bernard PW, Zhang N, Han H, Katz MH, Zhao Z and Hu Y: Chemoresistance transmission via exosome-mediated EphA2 transfer in pancreatic cancer. Theranostics. 8:5986–5994. 2018. View Article : Google Scholar : PubMed/NCBI

109 

van den Boorn JG, Schlee M, Coch C and Hartmann G: SiRNA delivery with exosome nanoparticles. Nat Biotechnol. 29:325–326. 2011. View Article : Google Scholar : PubMed/NCBI

110 

Buscail L: Pancreatic cancer: Exosomes for targeting KRAS in the treatment of pancreatic cancer. Nat Rev Gastroenterol Hepatol. 14:636–638. 2017. View Article : Google Scholar : PubMed/NCBI

111 

Christianson HC, Svensson KJ, van Kuppevelt TH, Li JP and Belting M: Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci USA. 110:17380–17385. 2013. View Article : Google Scholar : PubMed/NCBI

112 

Fares J, Kashyap R and Zimmermann P: Syntenin: Key player in cancer exosome biogenesis and uptake? Cell Adh Migr. 11:124–126. 2017. View Article : Google Scholar : PubMed/NCBI

113 

Pascucci L, Cocce V, Bonomi A, Ami D, Ceccarelli P, Ciusani E, Viganò L, Locatelli A, Sisto F, Doglia AM, et al: Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: A new approach for drug delivery. J Control Release. 192:262–270. 2014. View Article : Google Scholar : PubMed/NCBI

114 

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 : PubMed/NCBI

115 

Oldrini B, Vaquero-Siguero N, Mu Q, Kroon P, Zhang Y, Galán-Ganga M, Bao Z, Wang Z, Liu H, Sa JK, et al: MGMT genomic rearrangements contribute to chemotherapy resistance in gliomas. Nat Commun. 11:38832020. View Article : Google Scholar : PubMed/NCBI

116 

Xu L, Faruqu FN, Liam-Or R, Abed OA, Li D, Venner K, Errington RJ, Summers H, Wang JTW and Al-Jamal KT: Design of experiment (DoE)-driven in vitro and in vivo uptake studies of exosomes for pancreatic cancer delivery enabled by copper-free click chemistry-based labelling. J Extracell Vesicles. 9:17794582020. View Article : Google Scholar : PubMed/NCBI

117 

Zhou Y, Zhou G, Tian C, Jiang W, Jin L, Zhang C and Chen X: Exosome-mediated small RNA delivery for gene therapy. Wiley Interdiscip Rev RNA. 7:758–771. 2016. View Article : Google Scholar : PubMed/NCBI

118 

Papandreou ME and Tavernarakis N: Autophagy and the endo/exosomal pathways in health and disease. Biotechnol J. 12:2017. View Article : Google Scholar : PubMed/NCBI

119 

Pan JH, Zhou H, Zhao XX, Ding H, Li W, Qin L and Pan YL: Role of exosomes and exosomal microRNAs in hepatocellular carcinoma: Potential in diagnosis and antitumour treatments (Review). Int J Mol Med. 41:1809–1816. 2018.PubMed/NCBI

120 

Zhang Y, Liu YT, Tang H, Xie WQ, Yao H, Gu WT, Zheng YZ, Shang HB, Wang Y, Wei YX, et al: Exosome-transmitted lncRNA H19 inhibits the growth of pituitary adenoma. J Clin Endocrinol Metab. 104:6345–6356. 2019. View Article : Google Scholar : PubMed/NCBI

121 

Zhao X, Ren Y, Cui N, Wang X and Cui Y: Identification of key microRNAs and their targets in exosomes of pancreatic cancer using bioinformatics analysis. Medicine (Baltimore). 97:e126322018. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Liu H, Qiao S, Fan X, Gu Y, Zhang Y and Huang S: Role of exosomes in pancreatic cancer (Review). Oncol Lett 21: 298, 2021.
APA
Liu, H., Qiao, S., Fan, X., Gu, Y., Zhang, Y., & Huang, S. (2021). Role of exosomes in pancreatic cancer (Review). Oncology Letters, 21, 298. https://doi.org/10.3892/ol.2021.12559
MLA
Liu, H., Qiao, S., Fan, X., Gu, Y., Zhang, Y., Huang, S."Role of exosomes in pancreatic cancer (Review)". Oncology Letters 21.4 (2021): 298.
Chicago
Liu, H., Qiao, S., Fan, X., Gu, Y., Zhang, Y., Huang, S."Role of exosomes in pancreatic cancer (Review)". Oncology Letters 21, no. 4 (2021): 298. https://doi.org/10.3892/ol.2021.12559
Copy and paste a formatted citation
x
Spandidos Publications style
Liu H, Qiao S, Fan X, Gu Y, Zhang Y and Huang S: Role of exosomes in pancreatic cancer (Review). Oncol Lett 21: 298, 2021.
APA
Liu, H., Qiao, S., Fan, X., Gu, Y., Zhang, Y., & Huang, S. (2021). Role of exosomes in pancreatic cancer (Review). Oncology Letters, 21, 298. https://doi.org/10.3892/ol.2021.12559
MLA
Liu, H., Qiao, S., Fan, X., Gu, Y., Zhang, Y., Huang, S."Role of exosomes in pancreatic cancer (Review)". Oncology Letters 21.4 (2021): 298.
Chicago
Liu, H., Qiao, S., Fan, X., Gu, Y., Zhang, Y., Huang, S."Role of exosomes in pancreatic cancer (Review)". Oncology Letters 21, no. 4 (2021): 298. https://doi.org/10.3892/ol.2021.12559
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