MicroRNA-566 activates EGFR signaling and its inhibition sensitizes glioblastoma cells to nimotuzumab

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Zhang, Kai Liang ^a,b,c,d,h   Zhou, Xuan ^a   Han, Lei ^a,b,c,h   Chen, Lu Yue ^a,b,c,h   Chen, Ling Chao ^e,h   Shi, Zhen Dong ^a,b,c,h   Yang, Ming ^f   Ren, Yu ^a   Yang, Jing Xuan ^d   Frank, Thomas S ^d   Zhang, Chuan Bao ^g,h   Zhang, Jun Xia ^a,b,c,h   Pu, Pei Yu ^a,b,c,h   Zhang, Jian Ning ^a,b,c,h   Jiang, Tao ^g,h   Wagner, Eric J ^d   Li, Min ^d   Kang, Chun Sheng ^a,b,c,h  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b Tian Jin Normal University   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e THE SECOND AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

^f INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^g CAPITAL MEDICAL UNIVERSITY   (China)

^h Chinese Glioma Cooperative Group (CGCG)   (China)

Author keywords

Combination therapy; EGFR; Glioblastoma; miR 566; Nimotuzumab

Indexed keywords

BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MICRORNA; MICRORNA 566; NIMOTUZUMAB; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL INVASION; CELL NUCLEUS; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOPLASM; G1 PHASE CELL CYCLE CHECKPOINT; GENE OVEREXPRESSION; GENE TARGETING; GLIOBLASTOMA CELL LINE; GLIOMA CELL LINE; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; MICE, NUDE; MICRORNAS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSFECTION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84899582313     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-63     Document Type: Article

References (43)

1. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. Journal of Neurosurgery 2001, 95:190-198.
2. Rich JN, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BK, Dobra A, Dressman HK, Bigner DD, Nevins JR, West M. Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 2005, 65:4051-4058. 10.1158/0008-5472.CAN-04-3936, 15899794.
3. Zhu VF, Yang J, Lebrun DG, Li M. Understanding the role of cytokines in Glioblastoma Multiforme pathogenesis. Cancer Lett 2012, 316:139-150. 10.1016/j.canlet.2011.11.001, 22075379.
4. Smith JS, Tachibana I, Passe SM, Huntley BK, Borell TJ, Iturria N, O'Fallon JR, Schaefer PL, Scheithauer BW, James CD, Buckner JC, Jenkins RB. PTEN mutation, EGFR amplification, and outcome in patients with anaplastic astrocytoma and glioblastoma multiforme. J Natl Cancer Inst 2001, 93:1246-1256. 10.1093/jnci/93.16.1246, 11504770.
5. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, Settleman J, Haber DA. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004, 350:2129-2139. 10.1056/NEJMoa040938, 15118073.
6. Chakravarti A, Chakladar A, Delaney MA, Latham DE, Loeffler JS. The epidermal growth factor receptor pathway mediates resistance to sequential administration of radiation and chemotherapy in primary human glioblastoma cells in a RAS-dependent manner. Cancer Res 2002, 62:4307-4315.
7. Schulte JH, Horn S, Schlierf S, Schramm A, Heukamp LC, Christiansen H, Buettner R, Berwanger B, Eggert A. MicroRNAs in the pathogenesis of neuroblastoma. Cancer Lett 2009, 274:10-15. 10.1016/j.canlet.2008.06.010, 18639376.
8. Zhou X, Ren Y, Moore L, Mei M, You Y, Xu P, Wang B, Wang G, Jia Z, Pu P, Zhang W, Kang C. Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab Invest 2010, 90:144-155. 10.1038/labinvest.2009.126, 20048743.
9. Chen L, Han L, Zhang K, Shi Z, Zhang J, Zhang A, Wang Y, Song Y, Li Y, Jiang T, Pu P, Jiang C, Kang C. VHL regulates the effects of miR-23b on glioma survival and invasion via suppression of HIF-1alpha/VEGF and beta-catenin/Tcf-4 signaling. Neuro Oncol 2012, 14:1026-1036. 10.1093/neuonc/nos122, 3408255, 22649212.
10. Chen L, Li H, Han L, Zhang K, Wang G, Wang Y, Liu Y, Zheng Y, Jiang T, Pu P, Jiang C, Kang C. Expression and function of miR-27b in human glioma. Oncol Rep 2011, 26:1617-1621.
11. Chen L, Zhang W, Yan W, Han L, Zhang K, Shi Z, Zhang J, Wang Y, Li Y, Yu S, Pu P, Jiang C, Jiang T, Kang C. The putative tumor suppressor miR-524-5p directly targets Jagged-1 and Hes-1 in glioma. Carcinogenesis 2012, 33:2276-2282. 10.1093/carcin/bgs261, 22871495.
12. Zhang W, Zhang J, Yan W, You G, Bao Z, Li S, Kang C, Jiang C, You Y, Zhang Y, Chen CC, Song SW, Jiang T. Whole-genome microRNA expression profiling identifies a 5-microRNA signature as a prognostic biomarker in Chinese patients with primary glioblastoma multiforme. Cancer 2013, 119:814-824. 10.1002/cncr.27826, 22990979.
13. Wang XF, Shi ZM, Wang XR, Cao L, Wang YY, Zhang JX, Yin Y, Luo H, Kang CS, Liu N, Jiang T, You YP. MiR-181d acts as a tumor suppressor in glioma by targeting K-ras and Bcl-2. J Cancer Res Clin Oncol 2012, 138:573-584. 10.1007/s00432-011-1114-x, 22207524.
14. Baffa R, Fassan M, Volinia S, O'Hara B, Liu CG, Palazzo JP, Gardiman M, Rugge M, Gomella LG, Croce CM, Rosenberg A. MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J Pathol 2009, 219:214-221. 10.1002/path.2586, 19593777.
15. Dudziec E, Miah S, Choudhry HM, Owen HC, Blizard S, Glover M, Hamdy FC, Catto JW. Hypermethylation of CpG islands and shores around specific microRNAs and mirtrons is associated with the phenotype and presence of bladder cancer. Clin Cancer Res 2011, 17:1287-1296. 10.1158/1078-0432.CCR-10-2017, 21138856.
16. Sarkar FH, Li Y, Wang Z, Kong D, Ali S. Implication of microRNAs in drug resistance for designing novel cancer therapy. Drug Resist Updat 2010, 13:57-66. 10.1016/j.drup.2010.02.001, 2883024, 20236855.
17. Weidhaas JB, Babar I, Nallur SM, Trang P, Roush S, Boehm M, Gillespie E, Slack FJ. MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res 2007, 67:11111-11116. 10.1158/0008-5472.CAN-07-2858, 18056433.
18. Zhang JX, Qian D, Wang FW, Liao DZ, Wei JH, Tong ZT, Fu J, Huang XX, Liao YJ, Deng HX, Zeng YX, Xie D, Mai SJ. MicroRNA-29c enhances the sensitivities of human nasopharyngeal carcinoma to cisplatin-based chemotherapy and radiotherapy. Cancer Lett 2013, 329:91-98. 10.1016/j.canlet.2012.10.033, 23142283.
19. Weiss GJ, Bemis LT, Nakajima E, Sugita M, Birks DK, Robinson WA, Varella-Garcia M, Bunn PA, Haney J, Helfrich BA, Kato H, Hirsch FR, Franklin WA. EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines. Ann Oncol 2008, 19:1053-1059. 10.1093/annonc/mdn006, 18304967.
20. Papagiannakopoulos T, Shapiro A, Kosik KS. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 2008, 68:8164-8172. 10.1158/0008-5472.CAN-08-1305, 18829576.
21. Kanno H, Sato H, Yokoyama TA, Yoshizumi T, Yamada S. The VHL tumor suppressor protein regulates tumorigenicity of U87-derived glioma stem-like cells by inhibiting the JAK/STAT signaling pathway. Int J Oncol 2013, 42:881-886.
22. Behrens J. One hit, two outcomes for VHL-mediated tumorigenesis. Nat Cell Biol 2008, 10:1127-1128. 10.1038/ncb1008-1127, 18830218.
23. Zhang K, Zhang J, Han L, Pu P, Kang C. Wnt/beta-catenin signaling in glioma. J Neuroimmune Pharmacol 2012, 7:740-749. 10.1007/s11481-012-9359-y, 22454041.
24. Grimaldi AM, Guida T, D'Attino R, Perrotta E, Otero M, Masala A, Carteni G. Sunitinib: bridging present and future cancer treatment. Ann Oncol 2007, 18(Suppl 6):vi31-34.
25. Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I, Fujita Y, Okinaga S, Hirano H, Yoshimori K, Harada T, Ogura T, Ando M, Miyazawa H, Tanaka T, Saijo Y, Hagiwara K, Morita S, Nukiwa T. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 2010, 362:2380-2388. 10.1056/NEJMoa0909530, 20573926.
26. Zhu H, Cao X, Ali-Osman F, Keir S, Lo HW. EGFR and EGFRvIII interact with PUMA to inhibit mitochondrial translocalization of PUMA and PUMA-mediated apoptosis independent of EGFR kinase activity. Cancer Lett 2010, 294:101-110. 10.1016/j.canlet.2010.01.028, 2875288, 20153921.
27. Nautiyal J, Majumder P, Patel BB, Lee FY, Majumdar AP. Src inhibitor dasatinib inhibits growth of breast cancer cells by modulating EGFR signaling. Cancer Lett 2009, 283:143-151. 10.1016/j.canlet.2009.03.035, 19398150.
28. Dienstmann R, De Dosso S, Felip E, Tabernero J. Drug development to overcome resistance to EGFR inhibitors in lung and colorectal cancer. Mol Oncol 2012, 6:15-26. 10.1016/j.molonc.2011.11.009, 22189054.
29. Lo HW. EGFR-targeted therapy in malignant glioma: novel aspects and mechanisms of drug resistance. Curr Mol Pharmacol 2010, 3:37-52. 10.2174/1874467211003010037, 3606625, 20030624.
30. Murad JP, Lin OA, Espinosa EV, Khasawneh FT. Current and experimental antibody-based therapeutics: insights, breakthroughs, setbacks and future directions. Curr Mol Med 2013, 13:165-178. 10.2174/156652413804486322, 22834842.
31. Engelman JA, Janne PA. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2008, 14:2895-2899. 10.1158/1078-0432.CCR-07-2248, 18483355.
32. Hara F, Aoe M, Doihara H, Taira N, Shien T, Takahashi H, Yoshitomi S, Tsukuda K, Toyooka S, Ohta T, Shimizu N. Antitumor effect of gefitinib ('Iressa') on esophageal squamous cell carcinoma cell lines in vitro and in vivo. Cancer Lett 2005, 226:37-47. 10.1016/j.canlet.2004.12.025, 16004931.
33. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, Lu KV, Yoshimoto K, Huang JH, Chute DJ, Riggs BL, Horvath S, Liau LM, Cavenee WK, Rao PN, Beroukhim R, Peck TC, Lee JC, Sellers WR, Stokoe D, Prados M, Cloughesy TF, Sawyers CL, Mischel PS. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 2005, 353:2012-2024. 10.1056/NEJMoa051918, 16282176.
34. Osio A, Mateus C, Soria JC, Massard C, Malka D, Boige V, Besse B, Robert C. Cutaneous side-effects in patients on long-term treatment with epidermal growth factor receptor inhibitors. Br J Dermatol 2009, 161:515-521. 10.1111/j.1365-2133.2009.09214.x, 19466958.
35. Crombet T, Osorio M, Cruz T, Roca C, del Castillo R, Mon R, Iznaga-Escobar N, Figueredo R, Koropatnick J, Renginfo E, Fernandez E, Alvarez D, Torres O, Ramos M, Leonard I, Perez R, Lage A. Use of the humanized anti-epidermal growth factor receptor monoclonal antibody h-R3 in combination with radiotherapy in the treatment of locally advanced head and neck cancer patients. J Clin Oncol 2004, 22:1646-1654. 10.1200/JCO.2004.03.089, 15117987.
36. Kefas B, Godlewski J, Comeau L, Li Y, Abounader R, Hawkinson M, Lee J, Fine H, Chiocca EA, Lawler S. Purow B: microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res 2008, 68:3566-3572. 10.1158/0008-5472.CAN-07-6639, 18483236.
37. Sorrentino A, Liu CG, Addario A, Peschle C, Scambia G, Ferlini C. Role of microRNAs in drug-resistant ovarian cancer cells. Gynecol Oncol 2008, 111:478-486. 10.1016/j.ygyno.2008.08.017, 18823650.
38. Graziano F, Canestrari E, Loupakis F, Ruzzo A, Galluccio N, Santini D, Rocchi M, Vincenzi B, Salvatore L, Cremolini C, Spoto C, Catalano V, D'Emidio S, Giordani P, Tonini G, Falcone A, Magnani M. Genetic modulation of the Let-7 microRNA binding to KRAS 3'-untranslated region and survival of metastatic colorectal cancer patients treated with salvage cetuximab-irinotecan. Pharmacogenomics J 2010, 10:458-464. 10.1038/tpj.2010.9, 20177422.
39. Slaby O, Lakomy R, Fadrus P, Hrstka R, Kren L, Lzicarova E, Smrcka M, Svoboda M, Dolezalova H, Novakova J, Valik D, Vyzula R, Michalek J. MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 2010, 57:264-269. 10.4149/neo_2010_03_264, 20353279.
40. Auffinger B, Thaci B, Ahmed A, Ulasov I, Lesniak MS. MicroRNA targeting as a therapeutic strategy against glioma. Curr Mol Med 2013, 13:535-542. 10.2174/1566524011313040006, 22934848.
41. Adam L, Zhong M, Choi W, Qi W, Nicoloso M, Arora A, Calin G, Wang H, Siefker-Radtke A, McConkey D, Bar-Eli M, Dinney C. miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res 2009, 15:5060-5072. 10.1158/1078-0432.CCR-08-2245, 19671845.
42. Garofalo M, Romano G, Di Leva G, Nuovo G, Jeon YJ, Ngankeu A, Sun J, Lovat F, Alder H, Condorelli G, Engelman JA, Ono M, Rho JK, Cascione L, Volinia S, Nephew KP, Croce CM. EGFR and MET receptor tyrosine kinase-altered microRNA expression induces tumorigenesis and gefitinib resistance in lung cancers. Nat Med 2012, 18:74-82.
43. Zhang KL, Han L, Chen LY, Shi ZD, Yang M, Ren Y, Chen LC, Zhang JX, Pu PY, Kang CS. Blockage of a miR-21/EGFR regulatory feedback loop augments anti-EGFR therapy in glioblastomas. Cancer Lett 2014, 342:139-149. 10.1016/j.canlet.2013.08.043, 24012640.