Advances of serum exosome microRNAs in patients with colorectal cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

XUE Yuan ^1,2 , LI Peidong ^1,2 ,  ZHANG Guangjun ^1,2

1. The Second Department of Gastrointestinal Surgery, The Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637000, P. R. China;
2. Institute of Hepatobiliary, Pancreatic, and Intestinal Disease, North Sichuan Medical College, Nanchong, Sichuan 637000, P. R. China;

Corresponding author：

ZHANG Guangjun, Email: zhanggj1977@126.com

Keywords：

colorectal cancer; serum exosome; microRNA; review

DOI：

10.7507/1007-9424.202002049

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the current research progress of serum exosome microRNAs in patients with colorectal cancer.Methods The domestic and foreign literatures related to serum exosome microRNAs of colorectal cancer patients, which had been reported in recent years were collected through literature search. Subsequently, those literatures were used to read and review.Results Exosomes were extracellular vesicles, which contained lipids, proteins, DNA, RNA (mRNA, microRNA, and long non-coding RNA), and other molecules. These vesicles mediated communication between cells by transporting the above molecules. Exosomes in serum were the main carriers of microRNAs in the blood circulation system. Serum exosome microRNAs could affect the proliferation, invasion, and metastasis of colorectal cancer cells, mediate the drug resistance of colorectal cancer cells, and could be used as biomarkers to predict the prognosis of colorectal cancer.Conclusions Serum exosome microRNAs play important role in the occurrence, development, treatment, and diagnosis of colorectal cancer. As a class of biomarker, serum exosome microRNAs have great potential in the early diagnosis and prognostic evaluation of colorectal cancer.

Citation： XUE Yuan, LI Peidong, ZHANG Guangjun. Advances of serum exosome microRNAs in patients with colorectal cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(9): 1169-1174. doi: 10.7507/1007-9424.202002049 Copy

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2.	于永扬, 陈海宁, 周总光. 我国结直肠癌的现状、制约瓶颈与反思. 中国普外基础与临床杂志, 2019, 26(8): 897-902.
3.	Chen W, Sun K, Zheng R, et al. Cancer incidence and mortality in China, 2014. Chin J Cancer Res, 2018, 30(1): 1-12.
4.	McDevitt J, Comber H, Walsh PM. Colorectal cancer incidence and survival by sub-site and stage of diagnosis: a population-based study at the advent of national screening. Ir J Med Sci, 2017, 186(1): 113-121.
5.	Singh H, Nugent Z, Demers AA, et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology, 2010, 139(4): 1128-1137.
6.	Locker GY, Hamilton S, Harris J, et al. ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J Clin Oncol, 2006, 24(33): 5313-5327.
7.	Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev, 2013, 32(3-4): 623-642.
8.	Mohammadi S, Yousefi F, Shabaninejad Z, et al. Exosomes and cancer: from oncogenic roles to therapeutic applications. IUBMB Life, 2020, 72(4): 724-748.
9.	Ingenito F, Roscigno G, Affinito A, et al. The role of exo-miRNAs in cancer: a focus on therapeutic and diagnostic applications. Int J Mol Sci, 2019, 20(19): E4687.
10.	Singh R, Pochampally R, Watabe K, et al. Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol Cancer, 2014, 13: 256.
11.	Zhao S, Li J, Zhang G, et al. Exosomal miR-451a functions as a tumor suppressor in hepatocellular carcinoma by targeting LPIN1. Cell Physiol Biochem, 2019, 53(1): 19-35.
12.	Conlan RS, Pisano S, Oliveira MI, et al. Exosomes as reconfigurable therapeutic systems. Trends Mol Med, 2017, 23(7): 636-650.
13.	Soung YH, Ford S, Zhang V, et al. Exosomes in cancer diagnostics. Cancers (Basel), 2017, 9(1): E8.
14.	Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol, 2006, Chapter 3: Unit3.22.
15.	Tovar-Camargo OA, Toden S, Goel A. Exosomal microRNA biomarkers: emerging frontiers in colorectal and other human cancers. Expert Rev Mol Diagn, 2016, 16(5): 553-567.
16.	Savina A, Fader CM, Damiani MT, et al. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic, 2005, 6(2): 131-143.
17.	van Niel G, Raposo G, Candalh C, et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology, 2001, 121(2): 337-349.
18.	Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol, 2002, 2(8): 569-579.
19.	Keller S, Rupp C, Stoeck A, et al. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int, 2007, 72(9): 1095-1102.
20.	Gallo A, Tandon M, Alevizos I, et al. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One, 2012, 7(3): e30679.
21.	Kalluri R. The biology and function of exosomes in cancer. J Clin Invest, 2016, 126(4): 1208-1215.
22.	Zhang L, Zhang S, Yao J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature, 2015, 527(7576): 100-104.
23.	Zhang L, Yu D. Exosomes in cancer development, metastasis, and immunity. Biochim Biophys Acta Rev Cancer, 2019, 1871(2): 455-468.
24.	Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5): 843-854.
25.	Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2): 281-297.
26.	Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A, 2002, 99(24): 15524-15529.
27.	Bhome R, Goh RW, Bullock MD, et al. Exosomal microRNAs derived from colorectal cancer-associated fibroblasts: role in driving cancer progression. Aging (Albany NY), 2017, 9(12): 2666-2694.
28.	Schetter AJ, Okayama H, Harris CC. The role of microRNAs in colorectal cancer. Cancer J, 2012, 18(3): 244-252.
29.	Yan S, Han B, Gao S, et al. Exosome-encapsulated microRNAs as circulating biomarkers for colorectal cancer. Oncotarget, 2017, 8(36): 60149-60158.
30.	Zhao K, Liang G, Sun X, et al. Comparative miRNAome analysis revealed different miRNA expression profiles in bovine sera and exosomes. BMC Genomics, 2016, 17(1): 630.
31.	Li Y, Zheng Q, Bao C, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res, 2015, 25(8): 981-984.
32.	Zhou J, Li XL, Chen ZR, et al. Tumor-derived exosomes in colorectal cancer progression and their clinical applications. Oncotarget, 2017, 8(59): 100781-100790.
33.	Huang X, Yuan T, Liang M, et al. Exosomal miR-1290 and miR-375 as prognostic markers in castration-resistant prostate cancer. Eur Urol, 2015, 67(1): 33-41.
34.	Guiot J, Struman I, Louis E, et al. Exosomal miRNAs in lung diseases: from biologic function to therapeutic targets. J Clin Med, 2019, 8(9): E1345.
35.	Shi Y, Wang Z, Zhu X, et al. Exosomal miR-1246 in serum as a potential biomarker for early diagnosis of gastric cancer. Int J Clin Oncol, 2020, 25(1): 89-99.
36.	Dai G, Yao X, Zhang Y, et al. Colorectal cancer cell-derived exosomes containing miR-10b regulate fibroblast cells via the PI3K/Akt pathway. Bull Cancer, 2018, 105(4): 336-349.
37.	Xu Y, Shen L, Li F, et al. microRNA-16-5p-containing exosomes derived from bone marrow-derived mesenchymal stem cells inhibit proliferation, migration, and invasion, while promoting apoptosis of colorectal cancer cells by downregulating ITGA2. J Cell Physiol, 2019, 234(11): 21380-21394.
38.	Cheng WC, Liao TT, Lin CC, et al. RAB27B-activated secretion of stem-like tumor exosomes delivers the biomarker microRNA-146a-5p, which promotes tumorigenesis and associates with an immunosuppressive tumor microenvironment in colorectal cancer. Int J Cancer, 2019, 145(8): 2209-2224.
39.	Zaharie F, Muresan MS, Petrushev B, et al. Exosome-carried microRNA-375 inhibits cell progression and dissemination viaBcl-2 blocking in colon cancer. J Gastrointestin Liver Dis, 2015, 24(4): 435-443.
40.	Peng ZY, Gu RH, Yan B. Downregulation of exosome-encapsulated miR-548c-5p is associated with poor prognosis in colorectal cancer. J Cell Biochem, 2018, [Epub ahead of print].
41.	Hu HY, Yu CH, Zhang HH, et al. Exosomal miR-1229 derived from colorectal cancer cells promotes angiogenesis by targeting HIPK2. Int J Biol Macromol, 2019, 132: 470-477.
42.	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.
43.	Tsukamoto M, Iinuma H, Yagi T, et al. Circulating exosomal microRNA-21 as a biomarker in each tumor stage of colorectal cancer. Oncology, 2017, 92(6): 360-370.
44.	Teng Y, Ren Y, Hu X, et al. MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nat Commun, 2017, 8: 14448.
45.	Takano Y, Masuda T, Iinuma H, et al. Circulating exosomal microRNA-203 is associated with metastasis possibly via inducing tumor-associated macrophages in colorectal cancer. Oncotarget, 2017, 8(45): 78598-78613.
46.	Tang Y, Zhao Y, Song X, et al. Tumor-derived exosomal miRNA-320d as a biomarker for metastatic colorectal cancer. J Clin Lab Anal, 2019, 33(9): e23004.
47.	Monzo M, Santasusagna S, Moreno I, et al. Exosomal microRNAs isolated from plasma of mesenteric veins linked to liver metastases in resected patients with colon cancer. Oncotarget, 2017, 8(19): 30859-30869.
48.	Ogata-Kawata H, Izumiya M, Kurioka D, et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One, 2014, 9(4): e92921.
49.	Ye H, Hao H, Wang J, et al. miR-203 as a novel biomarker for the diagnosis and prognosis of colorectal cancer: a systematic review and meta-analysis. Onco Targets Ther, 2017, 10: 3685-3696.
50.	Ji L, Wei Y, Jiang T, et al. Correlation of Nrf2, NQO1, MRP1, cmyc and p53 in colorectal cancer and their relationships to clinicopathologic features and survival. Int J Clin Exp Pathol, 2014, 7(3): 1124-1131.
51.	Yagi T, Iinuma H, Hayama T, et al. Plasma exosomal microRNA-125b as a monitoring biomarker of resistance to mFOLFOX6-based chemotherapy in advanced and recurrent colorectal cancer patients. Mol Clin Oncol, 2019, 11(4): 416-424.
52.	Jin G, Liu Y, Zhang J, et al. A panel of serum exosomal microRNAs as predictive markers for chemoresistance in advanced colorectal cancer. Cancer Chemother Pharmacol, 2019, 84(2): 315-325.
53.	Quinn TP, Nguyen T, Lee SC, et al. Cancer as a tissue anomaly: classifying tumor transcriptomes based only on healthy data. Front Genet, 2019, 10: 599.
54.	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.
55.	Liu X, Pan B, Sun L, et al. Circulating exosomal miR-27a and miR-130a act as novel diagnostic and prognostic biomarkers of colorectal cancer. Cancer Epidemiol Biomarkers Prev, 2018, 27(7): 746-754.
56.	Liu C, Eng C, Shen J, et al. Serum exosomal miR-4772-3p is a predictor of tumor recurrence in stage Ⅱ and Ⅲ colon cancer. Oncotarget, 2016, 7(46): 76250-76260.
57.	Yan S, Jiang Y, Liang C, et al. Exosomal miR-6803-5p as potential diagnostic and prognostic marker in colorectal cancer. J Cell Biochem, 2018, 119(5): 4113-4119.
58.	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.
59.	Yu B, Du Q, Li H, et al. Diagnostic potential of serum exosomal colorectal neoplasia differentially expressed long non-coding RNA (CRNDE-p) and microRNA-217 expression in colorectal carcinoma. Oncotarget, 2017, 8(48): 83745-83753.
60.	Slaby O. Non-coding RNAs as biomarkers for colorectal cancer screening and early detection. Adv Exp Med Biol, 2016, 937: 153-170.

1. 王锡山. 中美结直肠癌流行病学特征及防诊治策略的对比分析. 中华结直肠疾病电子杂志, 2017, 6(6): 447-453.
2. 于永扬, 陈海宁, 周总光. 我国结直肠癌的现状、制约瓶颈与反思. 中国普外基础与临床杂志, 2019, 26(8): 897-902.
3. Chen W, Sun K, Zheng R, et al. Cancer incidence and mortality in China, 2014. Chin J Cancer Res, 2018, 30(1): 1-12.
4. McDevitt J, Comber H, Walsh PM. Colorectal cancer incidence and survival by sub-site and stage of diagnosis: a population-based study at the advent of national screening. Ir J Med Sci, 2017, 186(1): 113-121.
5. Singh H, Nugent Z, Demers AA, et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology, 2010, 139(4): 1128-1137.
6. Locker GY, Hamilton S, Harris J, et al. ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J Clin Oncol, 2006, 24(33): 5313-5327.
7. Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev, 2013, 32(3-4): 623-642.
8. Mohammadi S, Yousefi F, Shabaninejad Z, et al. Exosomes and cancer: from oncogenic roles to therapeutic applications. IUBMB Life, 2020, 72(4): 724-748.
9. Ingenito F, Roscigno G, Affinito A, et al. The role of exo-miRNAs in cancer: a focus on therapeutic and diagnostic applications. Int J Mol Sci, 2019, 20(19): E4687.
10. Singh R, Pochampally R, Watabe K, et al. Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol Cancer, 2014, 13: 256.
11. Zhao S, Li J, Zhang G, et al. Exosomal miR-451a functions as a tumor suppressor in hepatocellular carcinoma by targeting LPIN1. Cell Physiol Biochem, 2019, 53(1): 19-35.
12. Conlan RS, Pisano S, Oliveira MI, et al. Exosomes as reconfigurable therapeutic systems. Trends Mol Med, 2017, 23(7): 636-650.
13. Soung YH, Ford S, Zhang V, et al. Exosomes in cancer diagnostics. Cancers (Basel), 2017, 9(1): E8.
14. Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol, 2006, Chapter 3: Unit3.22.
15. Tovar-Camargo OA, Toden S, Goel A. Exosomal microRNA biomarkers: emerging frontiers in colorectal and other human cancers. Expert Rev Mol Diagn, 2016, 16(5): 553-567.
16. Savina A, Fader CM, Damiani MT, et al. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic, 2005, 6(2): 131-143.
17. van Niel G, Raposo G, Candalh C, et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology, 2001, 121(2): 337-349.
18. Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol, 2002, 2(8): 569-579.
19. Keller S, Rupp C, Stoeck A, et al. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int, 2007, 72(9): 1095-1102.
20. Gallo A, Tandon M, Alevizos I, et al. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One, 2012, 7(3): e30679.
21. Kalluri R. The biology and function of exosomes in cancer. J Clin Invest, 2016, 126(4): 1208-1215.
22. Zhang L, Zhang S, Yao J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature, 2015, 527(7576): 100-104.
23. Zhang L, Yu D. Exosomes in cancer development, metastasis, and immunity. Biochim Biophys Acta Rev Cancer, 2019, 1871(2): 455-468.
24. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5): 843-854.
25. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2): 281-297.
26. Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A, 2002, 99(24): 15524-15529.
27. Bhome R, Goh RW, Bullock MD, et al. Exosomal microRNAs derived from colorectal cancer-associated fibroblasts: role in driving cancer progression. Aging (Albany NY), 2017, 9(12): 2666-2694.
28. Schetter AJ, Okayama H, Harris CC. The role of microRNAs in colorectal cancer. Cancer J, 2012, 18(3): 244-252.
29. Yan S, Han B, Gao S, et al. Exosome-encapsulated microRNAs as circulating biomarkers for colorectal cancer. Oncotarget, 2017, 8(36): 60149-60158.
30. Zhao K, Liang G, Sun X, et al. Comparative miRNAome analysis revealed different miRNA expression profiles in bovine sera and exosomes. BMC Genomics, 2016, 17(1): 630.
31. Li Y, Zheng Q, Bao C, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res, 2015, 25(8): 981-984.
32. Zhou J, Li XL, Chen ZR, et al. Tumor-derived exosomes in colorectal cancer progression and their clinical applications. Oncotarget, 2017, 8(59): 100781-100790.
33. Huang X, Yuan T, Liang M, et al. Exosomal miR-1290 and miR-375 as prognostic markers in castration-resistant prostate cancer. Eur Urol, 2015, 67(1): 33-41.
34. Guiot J, Struman I, Louis E, et al. Exosomal miRNAs in lung diseases: from biologic function to therapeutic targets. J Clin Med, 2019, 8(9): E1345.
35. Shi Y, Wang Z, Zhu X, et al. Exosomal miR-1246 in serum as a potential biomarker for early diagnosis of gastric cancer. Int J Clin Oncol, 2020, 25(1): 89-99.
36. Dai G, Yao X, Zhang Y, et al. Colorectal cancer cell-derived exosomes containing miR-10b regulate fibroblast cells via the PI3K/Akt pathway. Bull Cancer, 2018, 105(4): 336-349.
37. Xu Y, Shen L, Li F, et al. microRNA-16-5p-containing exosomes derived from bone marrow-derived mesenchymal stem cells inhibit proliferation, migration, and invasion, while promoting apoptosis of colorectal cancer cells by downregulating ITGA2. J Cell Physiol, 2019, 234(11): 21380-21394.
38. Cheng WC, Liao TT, Lin CC, et al. RAB27B-activated secretion of stem-like tumor exosomes delivers the biomarker microRNA-146a-5p, which promotes tumorigenesis and associates with an immunosuppressive tumor microenvironment in colorectal cancer. Int J Cancer, 2019, 145(8): 2209-2224.
39. Zaharie F, Muresan MS, Petrushev B, et al. Exosome-carried microRNA-375 inhibits cell progression and dissemination viaBcl-2 blocking in colon cancer. J Gastrointestin Liver Dis, 2015, 24(4): 435-443.
40. Peng ZY, Gu RH, Yan B. Downregulation of exosome-encapsulated miR-548c-5p is associated with poor prognosis in colorectal cancer. J Cell Biochem, 2018, [Epub ahead of print].
41. Hu HY, Yu CH, Zhang HH, et al. Exosomal miR-1229 derived from colorectal cancer cells promotes angiogenesis by targeting HIPK2. Int J Biol Macromol, 2019, 132: 470-477.
42. 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.
43. Tsukamoto M, Iinuma H, Yagi T, et al. Circulating exosomal microRNA-21 as a biomarker in each tumor stage of colorectal cancer. Oncology, 2017, 92(6): 360-370.
44. Teng Y, Ren Y, Hu X, et al. MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nat Commun, 2017, 8: 14448.
45. Takano Y, Masuda T, Iinuma H, et al. Circulating exosomal microRNA-203 is associated with metastasis possibly via inducing tumor-associated macrophages in colorectal cancer. Oncotarget, 2017, 8(45): 78598-78613.
46. Tang Y, Zhao Y, Song X, et al. Tumor-derived exosomal miRNA-320d as a biomarker for metastatic colorectal cancer. J Clin Lab Anal, 2019, 33(9): e23004.
47. Monzo M, Santasusagna S, Moreno I, et al. Exosomal microRNAs isolated from plasma of mesenteric veins linked to liver metastases in resected patients with colon cancer. Oncotarget, 2017, 8(19): 30859-30869.
48. Ogata-Kawata H, Izumiya M, Kurioka D, et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One, 2014, 9(4): e92921.
49. Ye H, Hao H, Wang J, et al. miR-203 as a novel biomarker for the diagnosis and prognosis of colorectal cancer: a systematic review and meta-analysis. Onco Targets Ther, 2017, 10: 3685-3696.
50. Ji L, Wei Y, Jiang T, et al. Correlation of Nrf2, NQO1, MRP1, cmyc and p53 in colorectal cancer and their relationships to clinicopathologic features and survival. Int J Clin Exp Pathol, 2014, 7(3): 1124-1131.
51. Yagi T, Iinuma H, Hayama T, et al. Plasma exosomal microRNA-125b as a monitoring biomarker of resistance to mFOLFOX6-based chemotherapy in advanced and recurrent colorectal cancer patients. Mol Clin Oncol, 2019, 11(4): 416-424.
52. Jin G, Liu Y, Zhang J, et al. A panel of serum exosomal microRNAs as predictive markers for chemoresistance in advanced colorectal cancer. Cancer Chemother Pharmacol, 2019, 84(2): 315-325.
53. Quinn TP, Nguyen T, Lee SC, et al. Cancer as a tissue anomaly: classifying tumor transcriptomes based only on healthy data. Front Genet, 2019, 10: 599.
54. 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.
55. Liu X, Pan B, Sun L, et al. Circulating exosomal miR-27a and miR-130a act as novel diagnostic and prognostic biomarkers of colorectal cancer. Cancer Epidemiol Biomarkers Prev, 2018, 27(7): 746-754.
56. Liu C, Eng C, Shen J, et al. Serum exosomal miR-4772-3p is a predictor of tumor recurrence in stage Ⅱ and Ⅲ colon cancer. Oncotarget, 2016, 7(46): 76250-76260.
57. Yan S, Jiang Y, Liang C, et al. Exosomal miR-6803-5p as potential diagnostic and prognostic marker in colorectal cancer. J Cell Biochem, 2018, 119(5): 4113-4119.
58. 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.
59. Yu B, Du Q, Li H, et al. Diagnostic potential of serum exosomal colorectal neoplasia differentially expressed long non-coding RNA (CRNDE-p) and microRNA-217 expression in colorectal carcinoma. Oncotarget, 2017, 8(48): 83745-83753.
60. Slaby O. Non-coding RNAs as biomarkers for colorectal cancer screening and early detection. Adv Exp Med Biol, 2016, 937: 153-170.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Advances of serum exosome microRNAs in patients with colorectal cancer

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