Blockage of a miR-21/EGFR regulatory feedback loop augments anti-EGFR therapy in glioblastomas

Cancer Letters

Volumn 342, Issue 1, 2014, Pages 139-149

  Zhang, Kai liang ^a,b,c,f   Han, Lei ^a,b,c,f   Chen, Lu yue ^a,b,c,f   Shi, Zhen dong ^a,b,c,f   Yang, Ming ^d   Ren, Yu ^a   Chen, Ling chao ^e,f   Zhang, Jun xia ^a,b,c,f   Pu, Pei yu ^a,b,c,f   Kang, Chun sheng ^a,b,c,f  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b Tianjin Neurological Institute   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

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

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

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

Author keywords

EGFR; Feedback loop; Glioblastoma; MiR 21

Indexed keywords

BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FENOFIBRATE; MICRORNA 21; NIMOTUZUMAB; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN KINASE B; TRANSCRIPTION FACTOR AP 1; VON HIPPEL LINDAU PROTEIN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL INVASION; CELL PROLIFERATION; CONCENTRATION RESPONSE; DRUG EFFICACY; DRUG MECHANISM; FEEDBACK SYSTEM; GLIOBLASTOMA; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING;

EGFR; FEEDBACK LOOP; GLIOBLASTOMA; MIR-21;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BASE SEQUENCE; BETA CATENIN; BINDING SITES; BRAIN NEOPLASMS; CELL LINE, TUMOR; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; PPAR ALPHA; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; TRANSCRIPTION FACTOR AP-1; TUMOR BURDEN; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN; WNT SIGNALING PATHWAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887615282     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.08.043     Document Type: Article

References (42)

1. Prados M.D., Chang S.M., Butowski N., DeBoer R., Parvataneni R., Carliner H., Kabuubi P., Ayers-Ringler J., Rabbitt J., Page M., Fedoroff A., Sneed P.K., Berger M.S., McDermott M.W., Parsa A.T., Vandenberg S., James C.D., Lamborn K.R., Stokoe D., Haas-Kogan D.A. Phase II study of erlotinib plus temozolomide during and after radiation therapy in patients with newly diagnosed glioblastoma multiforme or gliosarcoma. J. Clin. Oncol. 2009, 27:579-584.
2. Farazi T.A., Spitzer J.I., Morozov P., Tuschl T. MiRNAs in human cancer. J. Pathol. 2011, 223:102-115.
3. Gao W., Shen H., Liu L., Xu J., Shu Y. MiR-21 overexpression in human primary squamous cell lung carcinoma is associated with poor patient prognosis. J. Cancer Res. Clin. Oncol. 2011, 137:557-566.
4. Lakomy R., Sana J., Hankeova S., Fadrus P., Kren L., Lzicarova E., Svoboda M., Dolezelova H., Smrcka M., Vyzula R., Michalek J., Hajduch M., Slaby O. MiR-195, miR-196b, miR-181c, miR-21 expression levels and O-6-methylguanine-DNA methyltransferase methylation status are associated with clinical outcome in glioblastoma patients. Cancer Sci. 2011, 102:2186-2190.
5. Gaur A.B., Holbeck S.L., Colburn N.H., Israel M.A. Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol. 2011, 13:580-590.
6. Ziyan W., Shuhua Y., Xiufang W., Xiaoyun L. MicroRNA-21 is involved in osteosarcoma cell invasion and migration. Med. Oncol. 2011, 28:1469-1474.
7. Kim N., Kim H., Jung I., Kim Y., Kim D., Han Y.M. Expression profiles of miRNAs in human embryonic stem cells during hepatocyte differentiation. Hepatol. Res. 2011, 41:170-183.
8. Gabriely G., Wurdinger T., Kesari S., Esau C.C., Burchard J., Linsley P.S., Krichevsky A.M. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol. Cell. Biol. 2008, 28:5369-5380.
9. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005, 65:6029-6033.
10. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., Alexe G., Lawrence M., O'Kelly M., Tamayo P., Weir B.A., Gabriel S., Winckler W., Gupta S., Jakkula L., Feiler H.S., Hodgson J.G., James C.D., Sarkaria J.N., Brennan C., Kahn A., Spellman P.T., Wilson R.K., Speed T.P., Gray J.W., Meyerson M., Getz G., Perou C.M., Hayes D.N. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
11. Haas-Kogan D.A., Prados M.D., Tihan T., Eberhard D.A., Jelluma N., Arvold N.D., Baumber R., Lamborn K.R., Kapadia A., Malec M., Berger M.S., Stokoe D. Epidermal growth factor receptor, protein kinase B/Akt, and glioma response to erlotinib. J. Natl. Cancer Inst. 2005, 97:880-887.
12. Noordhuis M.G., Eijsink J.J., Ten Hoor K.A., Roossink F., Hollema H., Arts H.J., Pras E., Maduro J.H., Reyners A.K., de Bock G.H., Wisman G.B., Schuuring E., van der Zee A.G. Expression of epidermal growth factor receptor (EGFR) and activated EGFR predict poor response to (chemo)radiation and survival in cervical cancer. Clin. Cancer Res. 2009, 15:7389-7397.
13. 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.
14. Toth J., Egervari K., Klekner A., Bognar L., Szanto J., Nemes Z., Szollosi Z. Analysis of EGFR gene amplification, protein over-expression and tyrosine kinase domain mutation in recurrent glioblastoma. Pathol. Oncol. Res. 2009, 15:225-229.
15. Rong Y., Belozerov V.E., Tucker-Burden C., Chen G., Durden D.L., Olson J.J., Van Meir E.G., Mackman N., Brat D.J. Epidermal growth factor receptor and PTEN modulate tissue factor expression in glioblastoma through JunD/activator protein-1 transcriptional activity. Cancer Res. 2009, 69:2540-2549.
16. Lurje G., Lenz H.J. EGFR signaling and drug discovery. Oncology 2009, 77:400-410.
17. Boland W.K., Bebb G. Nimotuzumab: a novel anti-EGFR monoclonal antibody that retains anti-EGFR activity while minimizing skin toxicity. Expert Opin. Biol. Ther. 2009, 9:1199-1206.
18. Verheij M., Vens C., van Triest B. Novel therapeutics in combination with radiotherapy to improve cancer treatment: rationale, mechanisms of action and clinical perspective. Drug Resist. Update 2010, 13:29-43.
19. Pazour G.J. Immunoprecipitation to examine protein complexes. Methods Cell. Biol. 2009, 91:135-142.
20. Kendziorra E., Ahlborn K., Spitzner M., Rave-Frank M., Emons G., Gaedcke J., Kramer F., Wolff H.A., Becker H., Beissbarth T., Ebner R., Ghadimi B.M., Pukrop T., Ried T., Grade M. Silencing of the Wnt transcription factor TCF4 sensitizes colorectal cancer cells to (chemo-) radiotherapy. Carcinogenesis 2011, 32:1824-1831.
21. Korpal M., Lee E.S., Hu G., Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 2008, 283:14910-14914.
22. Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., Waldvogel B., Vannier C., Darling D., zur Hausen A., Brunton V.G., Morton J., Sansom O., Schuler J., Stemmler M.P., Herzberger C., Hopt U., Keck T., Brabletz S., Brabletz T. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell. Biol. 2009, 11:1487-1495.
23. Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Patrawala L., Brown D., Bader A.G. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010, 70:5923-5930.
24. Lu J., He M.L., Wang L., Chen Y., Liu X., Dong Q., Chen Y.C., Peng Y., Yao K.T., Kung H.F., Li X.P. MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res. 2011, 71:225-233.
25. Lucio-Eterovic A.K., Piao Y., de Groot J.F. Mediators of glioblastoma resistance and invasion during antivascular endothelial growth factor therapy. Clin. Cancer Res. 2009, 15:4589-4599.
26. Nguyen Q.D., Smith G., Glaser M., Perumal M., Arstad E., Aboagye E.O. Positron emission tomography imaging of drug-induced tumor apoptosis with a caspase-3/7 specific [18F] -labeled isatin sulfonamide. Proc. Natl. Acad. Sci. USA 2009, 106:16375-16380.
27. Kessenbrock K., Krumbholz M., Schonermarck U., Back W., Gross W.L., Werb Z., Grone H.J., Brinkmann V., Jenne D.E. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 2009, 15:623-625.
28. Jin X., Jeon H.Y., Joo K.M., Kim J.K., Jin J., Kim S.H., Kang B.G., Beck S., Lee S.J., Park A.K., Park W.Y., Choi Y.J., Nam D.H., Kim H. Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation. Cancer Res. 2011, 71:3066-3075.
29. Ziegler D.S., Keating J., Kesari S., Fast E.M., Zawel L., Ramakrishna N., Barnes J., Kieran M.W., Veldhuijzen van Zanten S.E., Kung A.L. A small-molecule IAP inhibitor overcomes resistance to cytotoxic therapies in malignant gliomas in vitro and in vivo. Neuro. Oncol. 2011, 13:820-829.
30. Yuan J., Mehta P.P., Yin M.J., Sun S., Zou A., Chen J., Rafidi K., Feng Z., Nickel J., Engebretsen J., Hallin J., Blasina A., Zhang E., Nguyen L., Sun M., Vogt P.K., McHarg A., Cheng H., Christensen J.G., Kan J.L., Bagrodia S. PF-04691502, a potent and selective oral inhibitor of PI3K and mTOR kinases with antitumor activity. Mol. Cancer Ther. 2011, 10:2189-2199.
31. Sonderegger S., Haslinger P., Sabri A., Leisser C., Otten J.V., Fiala C., Knofler M. Wingless (Wnt)-3A induces trophoblast migration and matrix metalloproteinase-2 secretion through canonical Wnt signaling and protein kinase B/AKT activation. Endocrinology 2010, 151:211-220.
32. Hsieh H.L., Sun C.C., Wu C.B., Wu C.Y., Tung W.H., Wang H.H., Yang C.M. Sphingosine 1-phosphate induces EGFR expression via Akt/NF-kappaB and ERK/AP-1 pathways in rat vascular smooth muscle cells. J. Cell. Biochem. 2008, 103:1732-1746.
33. Zhou J., Wang K.C., Wu W., Subramaniam S., Shyy J.Y., Chiu J.J., Li J.Y., Chien S. MicroRNA-21 targets peroxisome proliferators-activated receptor-alpha in an autoregulatory loop to modulate flow-induced endothelial inflammation. Proc. Natl. Acad. Sci. USA 2011, 108:10355-10360.
34. Yue X., Lan F., Yang W., Yang Y., Han L., Zhang A., Liu J., Zeng H., Jiang T., Pu P., Kang C. Interruption of beta-catenin suppresses the EGFR pathway by blocking multiple oncogenic targets in human glioma cells. Brain Res. 2010, 1366:27-37.
35. Han L., Yue X., Zhou X., Lan F.M., You G., Zhang W., Zhang K.L., Zhang C.Z., Cheng J.Q., Yu S.Z., Pu P.Y., Jiang T., Kang C.S. MicroRNA-21 expression is regulated by beta-catenin/STAT3 pathway and promotes glioma cell invasion by direct targeting RECK. CNS Neurosci. Ther. 2012, 18:573-583.
36. Kefas B., Godlewski J., Comeau L., Li Y., Abounader R., Hawkinson M., Lee J., Fine H., Chiocca E.A., 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.
37. Yin D., Ogawa S., Kawamata N., Leiter A., Ham M., Li D., Doan N.B., Said J.W., Black K.L., Phillip Koeffler H. MiR-34a functions as a tumor suppressor modulating EGFR in glioblastoma multiforme. Oncogene 2013, 32:1155-1163.
38. Chou T.Y., Chiu C.H., Li L.H., Hsiao C.Y., Tzen C.Y., Chang K.T., Chen Y.M., Perng R.P., Tsai S.F., Tsai C.M. Mutation in the tyrosine kinase domain of epidermal growth factor receptor is a predictive and prognostic factor for gefitinib treatment in patients with non-small cell lung cancer. Clin. Cancer Res. 2005, 11:3750-3757.
39. MacDonald T.J., Aguilera D., Kramm C.M. Treatment of high-grade glioma in children and adolescents. Neuro. Oncol. 2011, 13:1049-1058.
40. Ramos T.C., Figueredo J., Catala M., Gonzalez S., Selva J.C., Cruz T.M., Toledo C., Silva S., Pestano Y., Ramos M., Leonard I., Torres O., Marinello P., Perez R., Lage A. Treatment of high-grade glioma patients with the humanized anti-epidermal growth factor receptor (EGFR) antibody h-R3: report from a phase I/II trial. Cancer Biol. Ther. 2006, 5:375-379.
41. Diaz Miqueli A., Rolff J., Lemm M., Fichtner I., Perez R., Montero E. Radiosensitisation of U87MG brain tumours by anti-epidermal growth factor receptor monoclonal antibodies. Br. J. Cancer 2009, 100:950-958.
42. Zhang S., Chen L., Jung E.J., Calin G.A. Targeting microRNAs with small molecules: from dream to reality. Clin. Pharmacol. Ther. 2010, 87:754-758.