MIR-29a Regulates Radiosensitivity in Human Intestinal Cells by Targeting PTEN Gene

Radiation Research

Volumn 186, Issue 3, 2016, Pages 292-301

  Wang, Juan ^a   Xu, Jinping ^a   Fu, Jiamei ^a   Yuan, Dexiao ^a   Guo, Fei ^a   Zhou, Cuiping ^a   Shao, Chunlin ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; MESSENGER RNA; MICRORNA; MICRORNA 29A; MICRORNA 33B; MICRORNA 378; MICRORNA 92A; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; STAT1 PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG; MIRN29 MICRORNA, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PTEN PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CANCER RESISTANCE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CRYPT CELL; GENE EXPRESSION; GENE TARGETING; HCT116 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; INTESTINE CELL; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; RADIATION RESPONSE; RADIOSENSITIVITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; INTESTINE; METABOLISM; RADIATION TOLERANCE; TUMOR CELL LINE;

CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTESTINES; MICRORNAS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RADIATION TOLERANCE; SIGNAL TRANSDUCTION;

EID: 84988651256     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR14428.1     Document Type: Article

References (69)

1. Yang Y, Gu X, Zhou M, Xiang J, Chen Z. Serum microRNAs: A new diagnostic method for colorectal cancer. Biomed Rep 2013; 1:495-8.
2. Ciorba MA, Stenson WF. Probiotic therapy in radiation-induced intestinal injury and repair. Ann N Y Acad Sci 2009; 1165:190-4.
3. Gavazzi C, Bhoori S, Lovullo S, Cozzi G, Mariani L. Role of home parenteral nutrition in chronic radiation enteritis. Am J Gastroenterol 2006; 101:374-9.
4. Matthews MA, Watkins D, Darbyshire A, Carson WE, Besner GE. Heparin-binding EGF-like growth factor (HB-EGF) protects the intestines from radiation therapy-induced intestinal injury. J Pediatr Surg 2013; 48:1316-22.
5. Pan Y, Zhou C, Yuan D, Zhang J, Shao C. Radiation exposure promotes hepatocarcinoma cell invasion through epithelial mesenchymal transition mediated by H2S/CSE pathway. Radiat Res 2016; 185:96-105.
6. Hussein MR, Abu-Dief EE, Kamel E, Abou El-Ghait AT, Abdulwahed SR, Ahmad MH. Melatonin and roentgen irradiation-induced acute radiation enteritis in Albino rats: an animal model. Cell Biol Int 2008; 32:1353-61.
7. Gurtler A, Hauptmann M, Pautz S, Kulka U, Friedl AA, Lehr S, et al. The inter-individual variability outperforms the intra-individual variability of differentially expressed proteins prior and post irradiation in lymphoblastoid cell lines. Arch Physiol Biochem 2014; 120:198-207.
8. Xu W, Chen J, Xu L, Li H, Guo X. Acute radiation enteritis caused by dose-dependent radiation exposure in dogs: experimental research. Exp Biol Med (Maywood) 2014; 239:1543-56.
9. Iizuka D, Imaoka T, Nishimura M, Kawai H, Suzuki F, Shimada Y. Aberrant microRNA expression in radiation-induced rat mammary cancer: the potential role of miR-194 overexpression in cancer cell proliferation. Radiat Res 2013; 179:151-9.
10. Zhu Y, Zhang X, Ding X, Wang H, Chen X, Zhao H, et al. miR-27 inhibits adipocyte differentiation via suppressing CREB expression. Acta Biochim Biophys Sin (Shanghai) 2014; 46:590-6.
11. Xu H, Liu C, Zhang Y, Guo X, Liu Z, Luo Z, et al. Let-7b-5p regulates proliferation and apoptosis in multiple myeloma by targeting IGF1R. Acta Biochim Biophys Sin (Shanghai) 2014; 46:965-72.
12. Li M, Li J, Ding X, He M, Cheng SY. microRNA and cancer. AAPS J 2010; 12:309-17.
13. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116:281-97.
14. Qiu L, Zhang W, Tan EK, Zeng L. Deciphering the function and regulation of microRNAs in Alzheimer's disease and Parkinson's disease. ACS Chem Neurosci 2014; 5:884-94.
15. Pan ZW, Lu YJ, Yang BF. MicroRNAs: a novel class of potential therapeutic targets for cardiovascular diseases. Acta Pharmacol Sin 2010; 31:1-9.
16. Xiao H, Xiao W, Cao J, Li H, Guan W, Guo X, et al. miR-206 functions as a novel cell cycle regulator and tumor suppressor in clear-cell renal cell carcinoma. Cancer Lett 2016; 374:107-16.
17. Yang XD, Xu XH, Zhang SY, Wu Y, Xing CG, Ru G, et al. Role of miR-100 in the radioresistance of colorectal cancer cells. Am J Cancer Res 2015; 5:545-59.
18. Wang J, He J, Su F, Ding N, Hu W, Yao B, et al. Repression of ATR pathway by miR-185 enhances radiation-induced apoptosis and proliferation inhibition. Cell Death Dis 2013; 4:e699.
19. Zhou S, Ye W, Ren J, Shao Q, Qi Y, Liang J, et al. MicroRNA-381 increases radiosensitivity in esophageal squamous cell carcinoma. Am J Cancer Res 2015; 5:267-77.
20. Chen L, Xiao H, Wang ZH, Huang Y, Liu ZP, Ren H, et al. miR-29a suppresses growth and invasion of gastric cancer cells in vitro by targeting VEGF-A. BMB Rep 2014; 47:39-44.
21. Wang S, Zan J, Wu M, Zhao W, Li Z, Pan Y, et al. miR-29a promotes scavenger receptor A expression by targeting QKI (quaking) during monocyte-macrophage differentiation. Biochem Biophys Res Commun 2015; 464:1-6.
22. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A 2012; 109:E2110-6.
23. Ramzy I, Hasaballah M, Marzaban R, Shaker O, Soliman ZA. Evaluation of microRNAs-29a, 92a and 145 in colorectal carcinoma as candidate diagnostic markers: An Egyptian pilot study. Clin Res Hepatol Gastroenterol 2015; 39:508-15.
24. Nagano H, Tomimaru Y, Eguchi H, Hama N, Wada H, Kawamoto K, et al. MicroRNA-29a induces resistance to gemcitabine through the Wnt/beta-catenin signaling pathway in pancreatic cancer cells. Int J Oncol 2013; 43:1066-72.
25. Fu J, Tang W, Du P, Wang G, Chen W, Li J, et al. Identifying microRNA-mRNA regulatory network in colorectal cancer by a combination of expression profile and bioinformatics analysis. BMC Syst Biol 2012; 6:68.
26. Kara M, Yumrutas O, Ozcan O, Celik OI, Bozgeyik E, Bozgeyik I, et al. Differential expressions of cancer-associated genes and their regulatory miRNAs in colorectal carcinoma. Gene 2015; 567:81-6.
27. Tang W, Zhu Y, Gao J, Fu J, Liu C, Liu Y, et al. MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br J Cancer 2014; 110:450-8.
28. Zhong S, Li W, Chen Z, Xu J, Zhao J. MiR-222 and miR-29a contribute to the drug-resistance of breast cancer cells. Gene 2013; 531:8-14.
29. Li X, Lin G, Wu B, Zhou X, Zhou K. Overexpression of PTEN induces cell growth arrest and apoptosis in human breast cancer ZR-75-1 cells. Acta Biochim Biophys Sin (Shanghai) 2007; 39:745-50.
30. Zhou XP, Gimm O, Hampel H, Niemann T, Walker MJ, Eng C. Epigenetic PTEN silencing in malignant melanomas without PTEN mutation. Am J Pathol 2000; 157:1123-8.
31. Perrone F, Lampis A, Orsenigo M, Di Bartolomeo M, Gevorgyan A, Losa M, et al. PI3KCA/PTEN deregulation contributes to impaired responses to cetuximab in metastatic colorectal cancer patients. Ann Oncol 2009; 20:84-90.
32. Inaba N, Kimura M, Fujioka K, Ikeda K, Somura H, Akiyoshi K, et al. The effect of PTEN on proliferation and drug-, and radiosensitivity in malignant glioma cells. Anticancer Res 2011; 31:1653-8.
33. Rychahou PG, Jackson LN, Silva SR, Rajaraman S, Evers BM. Targeted molecular therapy of the PI3K pathway: therapeutic significance of PI3K subunit targeting in colorectal carcinoma. Ann Surg 2006; 243:833-44.
34. Atreya CE, Sangale Z, Xu N, Matli MR, Tikishvili E, Welbourn W, et al. PTEN expression is consistent in colorectal cancer primaries and metastases and associates with patient survival. Cancer Med 2013; 2:496-506.
35. Sorby LA, Kleiveland CR, Andersen SN, Bukholm IR, Jacobsen MB. The endothelin axis in the metastatic process of colon carcinoma. Anticancer Res 2011; 31:861-9.
36. Wang J, Yu M, Xiao L, Xu S, Yi Q, Jin W. Radiosensitizing effect of oleanolic acid on tumor cells through the inhibition of GSH synthesis in vitro. Oncol Rep 2013; 30:917-24.
37. Zhao L, Bode AM, Cao Y, Dong Z. Regulatory mechanisms and clinical perspectives of miRNA in tumor radiosensitivity. Carcinogenesis 2012; 33:2220-7.
38. Ma W, Yu J, Qi X, Liang L, Zhang Y, Ding Y, et al. Radiationinduced microRNA-622 causes radioresistance in colorectal cancer cells by down-regulating Rb. Oncotarget 2015; 6:15984-94.
39. Dreilich M, Wanders A, Brattstrom D, Bergstrom S, Hesselius P, Wagenius G, et al. HER-2 overexpression (3+) in patients with squamous cell esophageal carcinoma correlates with poorer survival. Dis Esophagus 2006; 19:224-31.
40. Barata JT. The impact of PTEN regulation by CK2 on PI3Kdependent signaling and leukemia cell survival. Adv Enzyme Regul 2011; 51:37-49.
41. Madoux F, Koenig M, Nelson E, Chowdhury S, Cameron M, Mercer B, et al., Modulators of STAT transcription factors for the targeted therapy of cancer (STAT3 Activators). Probe reports from the NIH Molecular Libraries Program; Bethesda, MD; National Center for Biotechnology Information (US) 2010. (http://bit.ly/29Q5ZBM)
42. Macdonald NJ, Delderfield SM, Zhang W, Taglialatela G. Tumour necrosis factor-alpha- vs. growth factor deprivation-promoted cell death: distinct converging pathways. Aging Cell 2003; 2:245-56.
43. Wang H, Wu Q, Liu Z, Luo X, Fan Y, Liu Y, et al. Downregulation of FAP suppresses cell proliferation and metastasis through PTEN/PI3K/AKT and Ras-ERK signaling in oral squamous cell carcinoma. Cell Death Dis 2014; 5:e1155.
44. Li H, Gao Q, Guo L, Lu SH. The PTEN/PI3K/Akt pathway regulates stem-like cells in primary esophageal carcinoma cells. Cancer Biol Ther 2011; 11:950-8.
45. Czochor JR, Glazer PM. microRNAs in cancer cell response to ionizing radiation. Antioxid Redox Signal 2014; 21:293-312.
46. Sun Y, Xing X, Liu Q, Wang Z, Xin Y, Zhang P, et al. Hypoxiainduced autophagy reduces radiosensitivity by the HIF-1alpha/miR-210/Bcl-2 pathway in colon cancer cells. Int J Oncol 2015; 46:750-6.
47. Bandres E, Bitarte N, Arias F, Agorreta J, Fortes P, Agirre X, et al. microRNA-451 regulates macrophage migration inhibitory factor production and proliferation of gastrointestinal cancer cells. Clin Cancer Res 2009; 15:2281-90.
48. Zhang Y, Zheng L, Huang J, Gao F, Lin X, He L, et al. MiR-124 Radiosensitizes human colorectal cancer cells by targeting PRRX1. PLoS One 2014; 9:e93917.
49. Muniyappa MK, Dowling P, Henry M, Meleady P, Doolan P, Gammell P, et al. MiRNA-29a regulates the expression of numerous proteins and reduces the invasiveness and proliferation of human carcinoma cell lines. Eur J Cancer 2009; 45:3104-18.
50. Han YC, Park CY, Bhagat G, Zhang J, Wang Y, Fan JB, et al. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 2010; 207:475-89.
51. Sun XJ, Liu BY, Yan S, Jiang TH, Cheng HQ, Jiang HS, et al. MicroRNA-29a promotes pancreatic cancer growth by inhibiting tristetraprolin. Cell Physiol Biochem 2015; 37:707-18.
52. Yang Z, Wu L, Zhu X, Xu J, Jin R, Li G, et al. MiR-29a modulates the angiogenic properties of human endothelial cells. Biochem Biophys Res Commun 2013; 434:143-9.
53. Han C, Chen X, Zhuang R, Xu M, Liu S, Li Q. miR-29a promotes myocardial cell apoptosis induced by high glucose through downregulating IGF-1. Int J Clin Exp Med 2015; 8:14352-62.
54. Moskwa P, Zinn PO, Choi YE, Shukla SA, Fendler W, Chen CC, et al. A functional screen identifies miRs that induce radioresistance in glioblastomas. Mol Cancer Res 2014; 12:1767-78.
55. Bhatnagar N, Li X, Padi SK, Zhang Q, Tang MS, Guo B. Downregulation of miR-205 and miR-31 confers resistance to chemotherapy-induced apoptosis in prostate cancer cells. Cell Death Dis 2010; 1:e105.
56. Svoboda M, Sana J, Fabian P, Kocakova I, Gombosova J, Nekvindova J, et al. MicroRNA expression profile associated with response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer patients. Radiat Oncol 2012; 7:195.
57. Xue Q, Sun K, Deng HJ, Lei ST, Dong JQ, Li GX. Anti-miRNA-221 sensitizes human colorectal carcinoma cells to radiation by upregulating PTEN. World J Gastroenterol 2013; 19:9307-17.
58. Saito Y, Swanson X, Mhashilkar AM, Oida Y, Schrock R, Branch CD, et al. Adenovirus-mediated transfer of the PTEN gene inhibits human colorectal cancer growth in vitro and in vivo. Gene Ther 2003; 10:1961-9.
59. Jung IL, Kang HJ, Kim KC, Kim IG. PTEN/pAkt/p53 signaling pathway correlates with the radioresponse of non-small cell lung cancer. Int J Mol Med 2010; 25:517-23.
60. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, et al. PTENdeficient intestinal stem cells initiate intestinal polyposis. Nat Genet 2007; 39:189-98.
61. Chun-Zhi Z, Lei H, An-Ling Z, Yan-Chao F, Xiao Y, Guang-Xiu W, et al. MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer 2010; 10:367.
62. Tumaneng K, Schlegelmilch K, Russell RC, Yimlamai D, Basnet H, Mahadevan N, et al. YAP mediates crosstalk between the Hippo and PI(3)K-TOR pathways by suppressing PTEN via miR-29. Nat Cell Biol 2012; 14:1322-9.
63. Myers MP, Stolarov JP, Eng C, Li J, Wang SI, Wigler MH, et al. P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci U S A 1997; 94:9052-7.
64. Ma Y, Xia H, Liu Y, Li M. Silencing miR-21 sensitizes non-small cell lung cancer A549 cells to ionizing radiation through inhibition of PI3K/Akt. Biomed Res Int 2014; 2014:617868.
65. Chang L, Graham PH, Hao J, Bucci J, Cozzi PJ, Kearsley JH, et al. Emerging roles of radioresistance in prostate cancer metastasis and radiation therapy. Cancer Metastasis Rev 2014; 33:469-96.
66. Osaki M, Oshimura M, Ito H. PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis 2004; 9:667-76.
67. Sun H, Lesche R, Li DM, Liliental J, Zhang H, Gao J, et al. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci U S A 1999; 96:6199-204.
68. Zhang Y, Zheng L, Ding Y, Li Q, Wang R, Liu T, et al. MiR-20a Induces cell radioresistance by activating the PTEN/PI3K/Akt signaling pathway in hepatocellular carcinoma. Int J Radiat Oncol Biol Phys 2015; 92:1132-40.
69. Qu C, Liang Z, Huang J, Zhao R, Su C, Wang S, et al. MiR-205 determines the radioresistance of human nasopharyngeal carcinoma by directly targeting PTEN. Cell Cycle 2012; 11:785-96.