The tumor suppressor miR-138-5p targets PD-L1 in colorectal cancer

Oncotarget

Volumn 7, Issue 29, 2016, Pages 45370-45384

  Zhao, Lian ^a,b   Yu, Haibo ^c   Yi, Shuijing ^a   Peng, Xiaowei ^d   Su, Peng ^a,b   Xiao, Zhiming ^a   Liu, Rui ^a   Tang, Anliu ^a,b   Li, Xiayu ^a,b   Liu, Fen ^a,b   Shen, Shourong ^a,b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b Hunan Key Laboratory of Nonresolving Inflammation and Cancer   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d HUNAN CANCER HOSPITAL   (China)

Author keywords

Biomarker; Colorectal cancer; miR 138 5p; PD L1; Tumor suppressor

Indexed keywords

MICRORNA; MICRORNA 138 5P; PROGRAMMED DEATH 1 LIGAND 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CD274 PROTEIN, HUMAN; MIRN138 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER STAGING; CANCER TISSUE; CELL CYCLE S PHASE; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INFANT; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN EXPRESSION; PROTEIN TARGETING; ADULT; AGED; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; COLORECTAL TUMOR; FEMALE; GENETICS; MALE; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PROPORTIONAL HAZARDS MODEL; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

ADULT; AGED; ANIMALS; B7-H1 ANTIGEN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICRORNAS; MIDDLE AGED; PROPORTIONAL HAZARDS MODELS;

EID: 84979902959     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9659     Document Type: Article

References (56)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA: a cancer journal for clinicians. 2012; 62:10-29.
2. Gellad ZF, Provenzale D. Colorectal cancer: national and international perspective on the burden of disease and public health impact. Gastroenterology. 2010; 138:2177-90.
3. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116:281-97.
4. Yu X, Li Z. The role of microRNAs expression in laryngeal cancer. Oncotarget. 2015; 6:23297-305. doi: 10.18632/ oncotarget.4195.
5. Lee SH, Jung YD, Choi YS, Lee YM. Targeting of RUNX3 by miR-130a and miR-495 cooperatively increases cell proliferation and tumor angiogenesis in gastric cancer cells. Oncotarget. 2015; 6:33269-78. doi: 10.18632/ oncotarget.5037.
6. Kim HS, Lee KS, Bae HJ, Eun JW, Shen Q, Park SJ, Shin WC, Yang HD, Park M, Park WS, Kang YK, Nam SW. MicroRNA-31 functions as a tumor suppressor by regulating cell cycle and epithelial-mesenchymal transition regulatory proteins in liver cancer. Oncotarget. 2015; 6:8089-102. doi: 10.18632/oncotarget.3512.
7. Liu Y, Wang Y, Sun X, Mei C, Wang L, Li Z, Zha X. miR-449a promotes liver cancer cell apoptosis by downregulation of Calpain6 and POU2F1. Oncotarget. 2015; 7:13491-501. doi: 10.18632/oncotarget.4821.
8. Zheng H, Ma R, Wang Q, Zhang P, Li D, Wang Q, Wang J, Li H, Liu H, Wang Z. MiR-625-3p promotes cell migration and invasion via inhibition of SCAI in colorectal carcinoma cells. Oncotarget. 2015; 6:27805-15. doi: 10.18632/ oncotarget.4738.
9. Li W, Chang J, Wang S, Liu X, Peng J, Huang D, Sun M, Chen Z, Zhang W, Guo W, Li J. miRNA-99b-5p suppresses liver metastasis of colorectal cancer by down-regulating mTOR. Oncotarget. 2015; 6:24448-62. doi: 10.18632/ oncotarget.4423.
10. Ma F, Song H, Guo B, Zhang Y, Zheng Y, Lin C, Wu Y, Guan G, Sha R, Zhou Q, Wang D, Zhou X, Li J, et al. MiR-361-5p inhibits colorectal and gastric cancer growth and metastasis by targeting staphylococcal nuclease domain containing-1. Oncotarget. 2015; 6:17404-16. doi: 10.18632/ oncotarget.3744.
11. Fang L, Li H, Wang L, Hu J, Jin T, Wang J, Yang BB. MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget. 2014; 5:2974-87 doi: 10.18632/oncotarget.1614.
12. Smith AR, Marquez RT, Tsao WC, Pathak S, Roy A, Ping J, Wilkerson B, Lan L, Meng W, Neufeld KL, Sun XF, Xu L. Tumor suppressive microRNA-137 negatively regulates Musashi-1 and colorectal cancer progression. Oncotarget. 2015; 6:12558-73. doi: 10.18632/oncotarget.3726.
13. Huang Z, Huang S, Wang Q, Liang L, Ni S, Wang L, Sheng W, He X, Du X. MicroRNA-95 promotes cell proliferation and targets sorting Nexin 1 in human colorectal carcinoma. Cancer research. 2011; 71:2582-89.
14. Jahid S, Sun J, Edwards RA, Dizon D, Panarelli NC, Milsom JW, Sikandar SS, Gumus ZH, Lipkin SM. miR-23a promotes the transition from indolent to invasive colorectal cancer. Cancer discovery. 2012; 2:540-53.
15. Wang Z, Wei W, Sarkar FH. miR-23a, a critical regulator of "migR"ation and metastasis in colorectal cancer. Cancer discovery. 2012; 2:489-91.
16. Ma F, Song H, Guo B, Zhang Y, Zheng Y, Lin C, Wu Y, Guan G, Sha R, Zhou Q, Wang D, Zhou X, Li J, et al. MiR-361-5p inhibits colorectal and gastric cancer growth and metastasis by targeting staphylococcal nuclease domain containing-1. Oncotarget. 2015; 6:17404-16. doi: 10.18632/ oncotarget.3744.
17. Ma Y, Zhang P, Wang F, Zhang H, Yang J, Peng J, Liu W, Qin H. miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut. 2012; 61:1447-53.
18. Zhang XF, Li KK, Gao L, Li SZ, Chen K, Zhang JB, Wang D, Tu RF, Zhang JX, Tao KX, Wang G, Zhang XD. miR-191 promotes tumorigenesis of human colorectal cancer through targeting C/EBPbeta. Oncotarget. 2015; 6:4144-58. doi: 10.18632/oncotarget.2864.
19. Zhang C, Liu J, Wang X, Wu R, Lin M, Laddha SV, Yang Q, Chan CS, Feng Z. MicroRNA-339-5p inhibits colorectal tumorigenesis through regulation of the MDM2/ p53 signaling. Oncotarget. 2014; 5:9106-17. doi: 10.18632/ oncotarget.2379.
20. Sun Y, Shen S, Liu X, Tang H, Wang Z, Yu Z, Li X, Wu M. MiR-429 inhibits cells growth and invasion and regulates EMT-related marker genes by targeting Onecut2 in colorectal carcinoma. Molecular and cellular biochemistry. 2014; 390:19-30.
21. Tang JT, Wang JL, Du W, Hong J, Zhao SL, Wang YC, Xiong H, Chen HM, Fang JY. MicroRNA 345, a methylation-sensitive microRNA is involved in cell proliferation and invasion in human colorectal cancer. Carcinogenesis. 2011; 32:1207-15.
22. Zhang H, Tang J, Li C, Kong J, Wang J, Wu Y, Xu E, Lai M. MiR-22 regulates 5-FU sensitivity by inhibiting autophagy and promoting apoptosis in colorectal cancer cells. Cancer letters. 2015; 356:781-90.
23. Zhang J, Fei B, Wang Q, Song M, Yin Y, Zhang B, Ni S, Guo W, Bian Z, Quan C, Liu Z, Wang Y, Yu J, et al. MicroRNA-638 inhibits cell proliferation, invasion and regulates cell cycle by targeting tetraspanin 1 in human colorectal carcinoma. Oncotarget. 2014; 5:12083-96. doi: 10.18632/oncotarget.2499.
24. Long L, Huang G, Zhu H, Guo Y, Liu Y, Huo J. Downregulation of miR-138 promotes colorectal cancer metastasis via directly targeting TWIST2. Journal of translational medicine. 2013; 11:275.
25. Karwacz K, Arce F, Bricogne C, Kochan G, Escors D. PD-L1 co-stimulation, ligand-induced TCR down-modulation and anti-tumor immunotherapy. Oncoimmunology. 2012; 1:86-88.
26. Peng W, Lizee G, Hwu P. Blockade of the PD-1 pathway enhances the efficacy of adoptive cell therapy against cancer. Oncoimmunology. 2013;2:e22691.
27. Schalper KA. PD-L1 expression and tumor-infiltrating lymphocytes: Revisiting the antitumor immune response potential in breast cancer. Oncoimmunology. 2014;3:e29288.
28. Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology. 2012; 1:1223-25.
29. Soria JC, Marabelle A, Brahmer JR, Gettinger S. Immune checkpoint modulation for non-small cell lung cancer. Clinical cancer research. 2015; 21:2256-62.
30. Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer cell. 2015; 27:450-61.
31. Sui X, Ma J, Han W, Wang X, Fang Y, Li D, Pan H, Zhang L. The anticancer immune response of anti-PD-1/PD-L1 and the genetic determinants of response to anti-PD-1/ PD-L1 antibodies in cancer patients. Oncotarget. 2015; 6:19393-404. doi: 10.18632/oncotarget.5107.
32. Zandberg DP, Strome SE. The role of the PD-L1:PD-1 pathway in squamous cell carcinoma of the head and neck. Oral oncology. 2014; 50:627-32.
33. Shi SJ, Wang LJ, Wang GD, Guo ZY, Wei M, Meng YL, Yang AG, Wen WH. B7-H1 expression is associated with poor prognosis in colorectal carcinoma and regulates the proliferation and invasion of HCT116 colorectal cancer cells. PloS one. 2013;8:e76012.
34. Qin T, Zeng YD, Qin G, Xu F, Lu JB, Fang WF, Xue C, Zhan JH, Zhang XK, Zheng QF, Peng RJ, Yuan ZY, Zhang L, et al. High PD-L1 expression was associated with poor prognosis in 870 Chinese patients with breast cancer. Oncotarget. 2015; 6:33972-81. doi: 10.18632/ oncotarget.5583.
35. Tang Y, Fang W, Zhang Y, Hong S, Kang S, Yan Y, Chen N, Zhan J, He X, Qin T, Li G, Tang W, Peng P, et al. The association between PD-L1 and EGFR status and the prognostic value of PD-L1 in advanced non-small cell lung cancer patients treated with EGFR-TKIs. Oncotarget. 2015; 6:14209-19. doi: 10.18632/oncotarget.3694.
36. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136:215-233.
37. Yeh YM, Chuang CM, Chao KC, Wang LH. MicroRNA-138 suppresses ovarian cancer cell invasion and metastasis by targeting SOX4 and HIF-1alpha. International journal of cancer. 2013; 133:867-78.
38. Jin Y, Chen D, Cabay RJ, Wang A, Crowe DL, Zhou X. Role of microRNA-138 as a potential tumor suppressor in head and neck squamous cell carcinoma. International review of cell and molecular biology. 2013; 303:357-85.
39. Liu X, Jiang L, Wang A, Yu J, Shi F, Zhou X. MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer letters. 2009; 286:217-22.
40. Liu X, Lv XB, Wang XP, Sang Y, Xu S, Hu K, Wu M, Liang Y, Liu P, Tang J, Lu WH, Feng QS, Chen LZ, et al. MiR-138 suppressed nasopharyngeal carcinoma growth and tumorigenesis by targeting the CCND1 oncogene. Cell cycle. 2012; 11:2495-506.
41. Yu C, Wang M, Li Z, Xiao J, Peng F, Guo X, Deng Y, Jiang J, Sun C. MicroRNA-138-5p regulates pancreatic cancer cell growth through targeting FOXC1. Cellular oncology. 2015; 38:173-81.
42. Badoual C, Hans S, Merillon N, Van Ryswick C, Ravel P, Benhamouda N, Levionnois E, Nizard M, Si-Mohamed A, Besnier N, Gey A, Rotem-Yehudar R, Pere H, et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-associated head and neck cancer. Cancer research. 2013; 73:128-38.
43. Droeser RA, Hirt C, Viehl CT, Frey DM, Nebiker C, Huber X, Zlobec I, Eppenberger-Castori S, Tzankov A, Rosso R, Zuber M, Muraro MG, Amicarella F, et al. Clinical impact of programmed cell death ligand 1 expression in colorectal cancer. European journal of cancer. 2013; 49:2233-42.
44. Konishi J, Yamazaki K, Azuma M, Kinoshita I, Dosaka-Akita H, Nishimura M. B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clinical cancer research. 2004; 10:5094-100.
45. Ohigashi Y, Sho M, Yamada Y, Tsurui Y, Hamada K, Ikeda N, Mizuno T, Yoriki R, Kashizuka H, Yane K, Tsushima F, Otsuki N, Yagita H, et al. Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clinical cancer research. 2005; 11:2947-53.
46. Kim ST, Ha SY, Lee S, Ahn S, Lee J, Park SH, Park JO, Lim HY, Kang WK, Kim KM, Park YS. The Impact of PD-L1 Expression in Patients with Metastatic GEP-NETs. Journal of Cancer. 2016; 7:484-89.
47. Barrett MT, Anderson KS, Lenkiewicz E, Andreozzi M, Cunliffe HE, Klassen CL, Dueck AC, McCullough AE, Reddy SK, Ramanathan RK, Northfelt DW, Pockaj BA. Genomic amplification of 9p24.1 targeting JAK2, PD-L1, and PD-L2 is enriched in high-risk triple negative breast cancer. Oncotarget. 2015; 6:26483-93. doi: 10.18632/ oncotarget.4494.
48. Gatalica Z, Snyder C, Maney T, Ghazalpour A, Holterman DA, Xiao N, Overberg P, Rose I, Basu GD, Vranic S, Lynch HT, Von Hoff DD, Hamid O. Programmed cell death 1 (PD-1) and its ligand (PD-L1) in common cancers and their correlation with molecular cancer type. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2014; 23:2965-70.
49. Darb-Esfahani S, Kunze CA, Kulbe H, Sehouli J, Wienert S, Lindner J, Budczies J, Bockmayr M, Dietel M, Denkert C, Braicu I, Johrens K. Prognostic impact of programmed cell death-1 (PD-1) and PD-ligand 1 (PD-L1) expression in cancer cells and tumor-infiltrating lymphocytes in ovarian high grade serous carcinoma. Oncotarget. 2016; 7:1486-99. doi: 10.18632/oncotarget.6429
50. Llosa NJ, Cruise M, Tam A, Wicks EC, Hechenbleikner EM, Taube JM, Blosser RL, Fan H, Wang H, Luber BS, Zhang M, Papadopoulos N, Kinzler KW, et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer discovery. 2015; 5:43-51.
51. Rosty C, Williamson EJ, Clendenning M, Walters RJ, Walsh MD, Win AK, Jenkins MA, Hopper JL, Winship I, Southey MC, Giles GG, English DR, Buchanan DD. Re: Microsatellite instability and BRAF mutation testing in colorectal cancer prognostication. Journal of the National Cancer Institute. 2014;106.
52. Lochhead P, Kuchiba A, Imamura Y, Liao X, Yamauchi M, Nishihara R, Qian ZR, Morikawa T, Shen J, Meyerhardt JA, Fuchs CS, Ogino S. Microsatellite instability and BRAF mutation testing in colorectal cancer prognostication. Journal of the National Cancer Institute. 2013; 105:1151-56.
53. Yu H, Lu J, Zuo L, Yan Q, Yu Z, Li X, Huang J, Zhao L, Tang H, Luo Z, Liao Q, Zeng Z, Zhang J, et al. Epstein-Barr virus downregulates microRNA 203 through the oncoprotein latent membrane protein 1: a contribution to increased tumor incidence in epithelial cells. Journal of virology. 2012; 86:3088-99.
54. Breton G, Yassine-Diab B, Cohn L, Boulassel MR, Routy JP, Sekaly RP, Steinman RM. siRNA knockdown of PD-L1 and PD-L2 in monocyte-derived dendritic cells only modestly improves proliferative responses to Gag by CD8(+) T cells from HIV-1-infected individuals. Journal of clinical immunology. 2009; 29:637-45.
55. Chen Z, Liu S, Tian L, Wu M, Ai F, Tang W, Zhao L, Ding J, Zhang L, Tang A. miR-124 and miR-506 inhibit colorectal cancer progression by targeting DNMT3B and DNMT1. Oncotarget. 2015; 6:38139-50. doi: 10.18632/ oncotarget.5709.
56. Rhodes A, Jasani B, Barnes DM, Bobrow LG, Miller KD. Reliability of immunohistochemical demonstration of oestrogen receptors in routine practice: interlaboratory variance in the sensitivity of detection and evaluation of scoring systems. Journal of clinical pathology. 2000; 53:125-30.