Research progress of exosomes in gastrointestinal cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YU Kexun ,  CHEN Zihua

Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha 410000, P. R. China;

Corresponding author：

CHEN Zihua, Email: zihuachenxy@126.com

Keywords：

gastrointestinal cancer; exosomes; malignant development; molecular mechanism; invasion and metastasis; tumor microenvironment; biomarker; review

DOI：

10.7507/1007-9424.202002107

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the relationship between exosomes and the occurrence and development of gastrointestinal cancer.Methods Through online database, we collected the literatures about the relationship between exosomes and the development of gastrointestinal cancer at home and abroad, and then made an review.Results Exosomes secreted by gastrointestinal cancer cells were related to tumorigenesis, tumor cell survival, chemoresistance, and early metastasis. Exosomes could play the role of information transmission, and regulation of cell physiology and pathological process in the development of gastrointestinal cancer through a variety of intercellular binding ways, and affectted the occurrence and development of gastrointestinal cancer via epigenetic regulation and tumor related signal transduction mechanism. They had been proved to be biomarkers, targets, and drug carriers for the treatment of gastrointestinalcancer.Conclusion It is a new way to explore the molecular mechanism of exosomes in the development of gastrointestinal cancer.

Citation： YU Kexun, CHEN Zihua. Research progress of exosomes in gastrointestinal cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(11): 1444-1449. doi: 10.7507/1007-9424.202002107 Copy

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2.	Bijlsma MF, Sadanandam A, Tan P, et al. Molecular subtypes in cancers of the gastrointestinal tract. Nat Rev Gastroenterol Hepatol, 2017, 14(6): 333-342.
3.	Molina-Castro S, Pereira-Marques J, Figueiredo C, et al. Gastric cancer: basic aspects. Helicobacter, 2017, 22(Suppl 1): e12412.
4.	Liu X, Meltzer SJ. Gastric cancer in the era of precision medicine. Cell Mol Gastroenterol Hepatol, 2017, 3(3): 348-358.
5.	Zhang Z, Li G, Qiu H, et al. The novel notch-induced long noncoding RNA LUNAR1 determines the proliferation and prognosis of colorectal cancer. Sci Rep, 2019, 9(1): 19915.
6.	Steinbichler TB, Dudás J, Riechelmann H, et al. The role of exosomes in cancer metastasis. Semin Cancer Biol, 2017, 44: 170-181.
7.	Ogorevc E, Kralj-Iglic V, Veranic P. The role of extracellular vesicles in phenotypic cancer transformation. Radiol Oncol, 2013, 47(3): 197-205.
8.	Hannafon BN, Ding WQ. Intercellular communication by exosome-derived micrornas in cancer. Int J Mol Sci, 2013, 14(7): 14240-14269.
9.	Baghaei K, Tokhanbigli S, Asadzadeh H, et al. Exosomes as a novel cell-free therapeutic approach in gastrointestinal diseases. J Cell Physiol, 2019, 234(7): 9910-9926.
10.	Raab-Traub N, Dittmer DP. Viral effects on the content and function of extracellular vesicles. Nat Rev Microbiol, 2017, 15(9): 559-572.
11.	Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19): 9412-9420.
12.	Simpson RJ, Lim JW, Moritz RL, et al. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics, 2009, 6(3): 267-283.
13.	Wahlgren J, De L Karlson T, Brisslert M, et al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res, 2012, 40(17): e130.
14.	Gowda R, Robertson BM, Iyer S, et al. The role of exosomes in metastasis and progression of melanoma. Cancer Treat Rev, 2020, 85: 101975.
15.	Carvalho J, Oliveira C. Extracellular vesicles-powerful markers of cancer evolution. Front Immunol, 2015, 5: 685.
16.	Tschuschke M, Kocherova I, Bryja A, et al. Inclusion biogenesis, methods of isolation and clinical application of human cellular exosomes. J Clin Med, 2020, 9(2): 436.
17.	Nakase I, Noguchi K, Aoki A, et al. Arginine-rich cell-penetrating peptide-modified extracellular vesicles for active macropinocytosis induction and efficient intracellular delivery. Sci Rep, 2017, 7(1): 1991.
18.	Sarko DK, McKinney CE. Exosomes: origins and therapeutic potential for neurodegenerative disease. Front Neurosci, 2017, 11: 82.
19.	Zhou Y, Tian T, Zhu Y, et al. Exosomes transfer among different species cells and mediating miRNAs delivery. J Cell Biochem, 2017, 118(12): 4267-4274.
20.	Lan B, Zeng S, Grützmann R, et al. The role of exosomes in pancreatic cancer. Int J Mol Sci, 2019, 20(18): 4332.
21.	Ge Q, Zhou Y, Lu J, et al. miRNA in plasma exosome is stable under different storage conditions. Molecules, 2014, 19(2): 1568-1575.
22.	Dejima H, Iinuma H, Kanaoka R, et al. Exosomal microRNA in plasma as a non-invasive biomarker for the recurrence of non-small cell lung cancer. Oncol Lett, 2017, 13(3): 1256-1263.
23.	Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6): 654-659.
24.	Soung YH, Ford S, Zhang V, et al. Exosomes in cancer diagnostics. Cancers (Basel), 2017, 9(1): 8.
25.	Kalluri R. The biology and function of exosomes in cancer. J Clin Invest, 2016, 126(4): 1208-1215.
26.	Logozzi M, Mizzoni D, Angelini DF, et al. Microenvironmental pH and exosome levels interplay in human cancer cell lines of different histotypes. Cancers (Basel), 2018, 10(10): 370.
27.	Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature, 2018, 560(7718): 382-386.
28.	Gougelet A. Exosomal microRNAs as a potential therapeutic strategy in hepatocellular carcinoma. World J Hepatol, 2018, 10(11): 785-789.
29.	Figueroa J, Phillips LM, Shahar T, et al. Exosomes from glioma-associated mesenchymal stem cells increase the tumorigenicity of glioma stem-like cells via transfer of miR-1587. Cancer Res, 2017, 77(21): 5808-5819.
30.	Guo W, Gao Y, Li N, et al. Exosomes: new players in cancer (review). Oncol Rep, 2017, 38(2): 665-675.
31.	Wang J, Ni J, Beretov J, et al. Exosomal microRNAs as liquid biopsy biomarkers in prostate cancer. Crit Rev Oncol Hematol, 2020, 145: 102860.
32.	Xiao Y, Zhong J, Zhong B, et al. Exosomes as potential sources of biomarkers in colorectal cancer. Cancer Lett, 2020, 476: 13-22.
33.	Xie F, Zhou X, Fang M, et al. Extracellular vesicles in cancer immune microenvironment and cancer immunotherapy. Adv Sci (Weinh), 2019, 6(24): 1901779.
34.	Roma-Rodrigues C, Fernandes AR, Baptista PV. Exosome in tumour microenvironment: overview of the crosstalk between normal and cancer cells. Biomed Res Int, 2014, 2014: 179486.
35.	Stec M, Szatanek R, Baj-Krzyworzeka M, et al. Interactions of tumour-derived micro(nano)vesicles with human gastric cancer cells. J Transl Med, 2015, 13: 376.
36.	Li W, Gao YQ. MiR-217 is involved in the carcinogenesis of gastric cancer by down-regulating CDH1 expression. Kaohsiung J Med Sci, 2018, 34(7): 377-384.
37.	Wu L, Zhang X, Zhang B, et al. Exosomes derived from gastric cancer cells activate NF-κB pathway in macrophages to promote cancer progression. Tumour Biol, 2016, 37(9): 12169-12180.
38.	Deng G, Qu J, Zhang Y, et al. Gastric cancer-derived exosomes promote peritoneal metastasis by destroying the mesothelial barrier. FEBS Lett, 2017, 591(14): 2167-2179.
39.	Zhang X, Shi H, Yuan X, et al. Tumor-derived exosomes induce N2 polarization of neutrophils to promote gastric cancer cell migration. Mol Cancer, 2018, 17(1): 146.
40.	Wang J, Guan X, Zhang Y, et al. Exosomal miR-27a derived from gastric cancer cells regulates the transformation of fibroblasts into cancer-associated fibroblasts. Cell Physiol Biochem, 2018, 49(3): 869-883.
41.	Yen EY, Miaw SC, Yu JS, et al. Exosomal TGF-β1 is correlated with lymphatic metastasis of gastric cancers. Am J Cancer Res, 2017, 7(11): 2199-2208.
42.	Shimoda A, Ueda K, Nishiumi S, et al. Exosomes as nanocarriers for systemic delivery of the Helicobacter Pylori virulence factor CagA. Sci Rep, 2016, 6: 18346.
43.	Soda N, Rehm BHA, Sonar P, et al. Advanced liquid biopsy technologies for circulating biomarker detection. J Mater Chem B, 2019, 7(43): 6670-6704.
44.	Huang Z, Zhu D, Wu L, et al. Six serum-based miRNAs as potential diagnostic biomarkers for gastric cancer. Cancer Epidemiol Biomarkers Prev, 2017, 26(2): 188-196.
45.	Tokuhisa M, Ichikawa Y, Kosaka N, et al. Exosomal miRNAs from peritoneum lavage fluid as potential prognostic biomarkers of peritoneal metastasis in gastric cancer. PLoS One, 2015, 10(7): e0130472.
46.	Abak A, Abhari A, Rahimzadeh S. Exosomes in cancer: small vesicular transporters for cancer progression and metastasis, biomarkers in cancer therapeutics. PeerJ, 2018, 6: e4763.
47.	Zheng P, Chen L, Yuan X, et al. Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res, 2017, 36(1): 53.
48.	Wang X, Zhang H, Bai M, et al. Exosomes serve as nanoparticles to deliver anti-miR-214 to reverse chemoresistance to cisplatin in gastric cancer. Mol Ther, 2018, 26(3): 774-783.
49.	Liu F, Bu Z, Zhao F, et al. Increased T-helper 17 cell differentiation mediated by exosome-mediated microRNA-451 redistribution in gastric cancer infiltrated T cells. Cancer Sci, 2018, 109(1): 65-73.
50.	Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol, 2015, 40: 41-51.
51.	Wang M, Su Z, Amoah Barnie P. Crosstalk among colon cancer-derived exosomes, fibroblast-derived exosomes, and macrophage phenotypes in colon cancer metastasis. Int Immunopharmacol, 2020, 81: 106298.
52.	Liu X, Chen X, Zeng K, et al. DNA-methylation-mediated silencing of miR-486-5p promotes colorectal cancer proliferation and migration through activation of PLAGL2/IGF2/β-catenin signal pathways. Cell Death Dis, 2018, 9(10): 1037.
53.	Zhou MK, Liu XJ, Zhao ZG, et al. MicroRNA-100 functions as a tumor suppressor by inhibiting Lgr5 expression in colon cancer cells. Mol Med Rep, 2015, 11(4): 2947-2952.
54.	Harada T, Yamamoto H, Kishida S, et al. Wnt5b-associated exosomes promote cancer cell migration and proliferation. Cancer Sci, 2017, 108(1): 42-52.
55.	Huang Z, Feng Y. Exosomes derived from hypoxic colorectal cancer cells promote angiogenesis through Wnt4-inducedβ-Catenin signaling in endothelial cells. Oncol Res, 2017, 25(5): 651-661.
56.	Whiteside TL. Exosomes carrying immunoinhibitory proteins and their role in cancer. Clin Exp Immunol, 2017, 189(3): 259-267.
57.	Gastpar R, Gehrmann M, Bausero MA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res, 2005, 65(12): 5238-5247.
58.	Liu H, Liu Y, Sun P, et al. Colorectal cancer-derived exosomal miR-106b-3p promotes metastasis by down-regulating DLC-1 expression. Clin Sci (Lond), 2020, 134(4): 419-434.
59.	Wang J, Yan F, Zhao Q, et al. Circulating exosomal miR-125a-3p as a novel biomarker for early-stage colon cancer. Sci Rep, 2017, 7(1): 4150.
60.	Cha DJ, Franklin JL, Dou Y, et al. KRAS-dependent sorting of miRNA to exosomes. Elife, 2015, 4: e07197.
61.	Fu F, Jiang W, Zhou L, et al. Circulating exosomal miR-17-5p and miR-92a-3p predict pathologic stage and grade of colorectal cancer. Transl Oncol, 2018, 11(2): 221-232.
62.	Kurywchak P, Kalluri R. An evolving function of DNA-containing exosomes in chemotherapy-induced immune response. Cell Res, 2017, 27(6): 722-723.
63.	Karaayvaz M, Pal T, Song B, et al. Prognostic significance of miR-215 in colon cancer. Clin Colorectal Cancer, 2011, 10(4): 340-347.
64.	Senfter D, Holzner S, Kalipciyan M, et al. Loss of miR-200 family in 5-fluorouracil resistant colon cancer drives lymphendothelial invasiveness in vitro. Hum Mol Genet, 2015, 24(13): 3689-3698.
65.	Matsumura T, Sugimachi K, Iinuma H, et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br J Cancer, 2015, 113(2): 275-281.
66.	Zhang J, Li S, Li L, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics, 2015, 13(1): 17-24.
67.	Kahn S, Liao Y, Du X, et al. Exosomal microRNAs in milk from mothers delivering preterm infants survive in vitro digestion and are taken up by human intestinal cells. Mol Nutr Food Res, 2018, 62(11): e1701050.

1. Fu DG. Epigenetic alterations in gastric cancer (review). Mol Med Rep, 2015, 12(3): 3223-3230.
2. Bijlsma MF, Sadanandam A, Tan P, et al. Molecular subtypes in cancers of the gastrointestinal tract. Nat Rev Gastroenterol Hepatol, 2017, 14(6): 333-342.
3. Molina-Castro S, Pereira-Marques J, Figueiredo C, et al. Gastric cancer: basic aspects. Helicobacter, 2017, 22(Suppl 1): e12412.
4. Liu X, Meltzer SJ. Gastric cancer in the era of precision medicine. Cell Mol Gastroenterol Hepatol, 2017, 3(3): 348-358.
5. Zhang Z, Li G, Qiu H, et al. The novel notch-induced long noncoding RNA LUNAR1 determines the proliferation and prognosis of colorectal cancer. Sci Rep, 2019, 9(1): 19915.
6. Steinbichler TB, Dudás J, Riechelmann H, et al. The role of exosomes in cancer metastasis. Semin Cancer Biol, 2017, 44: 170-181.
7. Ogorevc E, Kralj-Iglic V, Veranic P. The role of extracellular vesicles in phenotypic cancer transformation. Radiol Oncol, 2013, 47(3): 197-205.
8. Hannafon BN, Ding WQ. Intercellular communication by exosome-derived micrornas in cancer. Int J Mol Sci, 2013, 14(7): 14240-14269.
9. Baghaei K, Tokhanbigli S, Asadzadeh H, et al. Exosomes as a novel cell-free therapeutic approach in gastrointestinal diseases. J Cell Physiol, 2019, 234(7): 9910-9926.
10. Raab-Traub N, Dittmer DP. Viral effects on the content and function of extracellular vesicles. Nat Rev Microbiol, 2017, 15(9): 559-572.
11. Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19): 9412-9420.
12. Simpson RJ, Lim JW, Moritz RL, et al. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics, 2009, 6(3): 267-283.
13. Wahlgren J, De L Karlson T, Brisslert M, et al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res, 2012, 40(17): e130.
14. Gowda R, Robertson BM, Iyer S, et al. The role of exosomes in metastasis and progression of melanoma. Cancer Treat Rev, 2020, 85: 101975.
15. Carvalho J, Oliveira C. Extracellular vesicles-powerful markers of cancer evolution. Front Immunol, 2015, 5: 685.
16. Tschuschke M, Kocherova I, Bryja A, et al. Inclusion biogenesis, methods of isolation and clinical application of human cellular exosomes. J Clin Med, 2020, 9(2): 436.
17. Nakase I, Noguchi K, Aoki A, et al. Arginine-rich cell-penetrating peptide-modified extracellular vesicles for active macropinocytosis induction and efficient intracellular delivery. Sci Rep, 2017, 7(1): 1991.
18. Sarko DK, McKinney CE. Exosomes: origins and therapeutic potential for neurodegenerative disease. Front Neurosci, 2017, 11: 82.
19. Zhou Y, Tian T, Zhu Y, et al. Exosomes transfer among different species cells and mediating miRNAs delivery. J Cell Biochem, 2017, 118(12): 4267-4274.
20. Lan B, Zeng S, Grützmann R, et al. The role of exosomes in pancreatic cancer. Int J Mol Sci, 2019, 20(18): 4332.
21. Ge Q, Zhou Y, Lu J, et al. miRNA in plasma exosome is stable under different storage conditions. Molecules, 2014, 19(2): 1568-1575.
22. Dejima H, Iinuma H, Kanaoka R, et al. Exosomal microRNA in plasma as a non-invasive biomarker for the recurrence of non-small cell lung cancer. Oncol Lett, 2017, 13(3): 1256-1263.
23. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6): 654-659.
24. Soung YH, Ford S, Zhang V, et al. Exosomes in cancer diagnostics. Cancers (Basel), 2017, 9(1): 8.
25. Kalluri R. The biology and function of exosomes in cancer. J Clin Invest, 2016, 126(4): 1208-1215.
26. Logozzi M, Mizzoni D, Angelini DF, et al. Microenvironmental pH and exosome levels interplay in human cancer cell lines of different histotypes. Cancers (Basel), 2018, 10(10): 370.
27. Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature, 2018, 560(7718): 382-386.
28. Gougelet A. Exosomal microRNAs as a potential therapeutic strategy in hepatocellular carcinoma. World J Hepatol, 2018, 10(11): 785-789.
29. Figueroa J, Phillips LM, Shahar T, et al. Exosomes from glioma-associated mesenchymal stem cells increase the tumorigenicity of glioma stem-like cells via transfer of miR-1587. Cancer Res, 2017, 77(21): 5808-5819.
30. Guo W, Gao Y, Li N, et al. Exosomes: new players in cancer (review). Oncol Rep, 2017, 38(2): 665-675.
31. Wang J, Ni J, Beretov J, et al. Exosomal microRNAs as liquid biopsy biomarkers in prostate cancer. Crit Rev Oncol Hematol, 2020, 145: 102860.
32. Xiao Y, Zhong J, Zhong B, et al. Exosomes as potential sources of biomarkers in colorectal cancer. Cancer Lett, 2020, 476: 13-22.
33. Xie F, Zhou X, Fang M, et al. Extracellular vesicles in cancer immune microenvironment and cancer immunotherapy. Adv Sci (Weinh), 2019, 6(24): 1901779.
34. Roma-Rodrigues C, Fernandes AR, Baptista PV. Exosome in tumour microenvironment: overview of the crosstalk between normal and cancer cells. Biomed Res Int, 2014, 2014: 179486.
35. Stec M, Szatanek R, Baj-Krzyworzeka M, et al. Interactions of tumour-derived micro(nano)vesicles with human gastric cancer cells. J Transl Med, 2015, 13: 376.
36. Li W, Gao YQ. MiR-217 is involved in the carcinogenesis of gastric cancer by down-regulating CDH1 expression. Kaohsiung J Med Sci, 2018, 34(7): 377-384.
37. Wu L, Zhang X, Zhang B, et al. Exosomes derived from gastric cancer cells activate NF-κB pathway in macrophages to promote cancer progression. Tumour Biol, 2016, 37(9): 12169-12180.
38. Deng G, Qu J, Zhang Y, et al. Gastric cancer-derived exosomes promote peritoneal metastasis by destroying the mesothelial barrier. FEBS Lett, 2017, 591(14): 2167-2179.
39. Zhang X, Shi H, Yuan X, et al. Tumor-derived exosomes induce N2 polarization of neutrophils to promote gastric cancer cell migration. Mol Cancer, 2018, 17(1): 146.
40. Wang J, Guan X, Zhang Y, et al. Exosomal miR-27a derived from gastric cancer cells regulates the transformation of fibroblasts into cancer-associated fibroblasts. Cell Physiol Biochem, 2018, 49(3): 869-883.
41. Yen EY, Miaw SC, Yu JS, et al. Exosomal TGF-β1 is correlated with lymphatic metastasis of gastric cancers. Am J Cancer Res, 2017, 7(11): 2199-2208.
42. Shimoda A, Ueda K, Nishiumi S, et al. Exosomes as nanocarriers for systemic delivery of the Helicobacter Pylori virulence factor CagA. Sci Rep, 2016, 6: 18346.
43. Soda N, Rehm BHA, Sonar P, et al. Advanced liquid biopsy technologies for circulating biomarker detection. J Mater Chem B, 2019, 7(43): 6670-6704.
44. Huang Z, Zhu D, Wu L, et al. Six serum-based miRNAs as potential diagnostic biomarkers for gastric cancer. Cancer Epidemiol Biomarkers Prev, 2017, 26(2): 188-196.
45. Tokuhisa M, Ichikawa Y, Kosaka N, et al. Exosomal miRNAs from peritoneum lavage fluid as potential prognostic biomarkers of peritoneal metastasis in gastric cancer. PLoS One, 2015, 10(7): e0130472.
46. Abak A, Abhari A, Rahimzadeh S. Exosomes in cancer: small vesicular transporters for cancer progression and metastasis, biomarkers in cancer therapeutics. PeerJ, 2018, 6: e4763.
47. Zheng P, Chen L, Yuan X, et al. Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res, 2017, 36(1): 53.
48. Wang X, Zhang H, Bai M, et al. Exosomes serve as nanoparticles to deliver anti-miR-214 to reverse chemoresistance to cisplatin in gastric cancer. Mol Ther, 2018, 26(3): 774-783.
49. Liu F, Bu Z, Zhao F, et al. Increased T-helper 17 cell differentiation mediated by exosome-mediated microRNA-451 redistribution in gastric cancer infiltrated T cells. Cancer Sci, 2018, 109(1): 65-73.
50. Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol, 2015, 40: 41-51.
51. Wang M, Su Z, Amoah Barnie P. Crosstalk among colon cancer-derived exosomes, fibroblast-derived exosomes, and macrophage phenotypes in colon cancer metastasis. Int Immunopharmacol, 2020, 81: 106298.
52. Liu X, Chen X, Zeng K, et al. DNA-methylation-mediated silencing of miR-486-5p promotes colorectal cancer proliferation and migration through activation of PLAGL2/IGF2/β-catenin signal pathways. Cell Death Dis, 2018, 9(10): 1037.
53. Zhou MK, Liu XJ, Zhao ZG, et al. MicroRNA-100 functions as a tumor suppressor by inhibiting Lgr5 expression in colon cancer cells. Mol Med Rep, 2015, 11(4): 2947-2952.
54. Harada T, Yamamoto H, Kishida S, et al. Wnt5b-associated exosomes promote cancer cell migration and proliferation. Cancer Sci, 2017, 108(1): 42-52.
55. Huang Z, Feng Y. Exosomes derived from hypoxic colorectal cancer cells promote angiogenesis through Wnt4-inducedβ-Catenin signaling in endothelial cells. Oncol Res, 2017, 25(5): 651-661.
56. Whiteside TL. Exosomes carrying immunoinhibitory proteins and their role in cancer. Clin Exp Immunol, 2017, 189(3): 259-267.
57. Gastpar R, Gehrmann M, Bausero MA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res, 2005, 65(12): 5238-5247.
58. Liu H, Liu Y, Sun P, et al. Colorectal cancer-derived exosomal miR-106b-3p promotes metastasis by down-regulating DLC-1 expression. Clin Sci (Lond), 2020, 134(4): 419-434.
59. Wang J, Yan F, Zhao Q, et al. Circulating exosomal miR-125a-3p as a novel biomarker for early-stage colon cancer. Sci Rep, 2017, 7(1): 4150.
60. Cha DJ, Franklin JL, Dou Y, et al. KRAS-dependent sorting of miRNA to exosomes. Elife, 2015, 4: e07197.
61. Fu F, Jiang W, Zhou L, et al. Circulating exosomal miR-17-5p and miR-92a-3p predict pathologic stage and grade of colorectal cancer. Transl Oncol, 2018, 11(2): 221-232.
62. Kurywchak P, Kalluri R. An evolving function of DNA-containing exosomes in chemotherapy-induced immune response. Cell Res, 2017, 27(6): 722-723.
63. Karaayvaz M, Pal T, Song B, et al. Prognostic significance of miR-215 in colon cancer. Clin Colorectal Cancer, 2011, 10(4): 340-347.
64. Senfter D, Holzner S, Kalipciyan M, et al. Loss of miR-200 family in 5-fluorouracil resistant colon cancer drives lymphendothelial invasiveness in vitro. Hum Mol Genet, 2015, 24(13): 3689-3698.
65. Matsumura T, Sugimachi K, Iinuma H, et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br J Cancer, 2015, 113(2): 275-281.
66. Zhang J, Li S, Li L, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics, 2015, 13(1): 17-24.
67. Kahn S, Liao Y, Du X, et al. Exosomal microRNAs in milk from mothers delivering preterm infants survive in vitro digestion and are taken up by human intestinal cells. Mol Nutr Food Res, 2018, 62(11): e1701050.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of exosomes in gastrointestinal cancer

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