LRIG1 enhances the radiosensitivity of radioresistant human glioblastoma U251 cells via attenuation of the EGFR/Akt signaling pathway

International Journal of Clinical and Experimental Pathology

Volumn 8, Issue 4, 2015, Pages 3580-3590

  Yang, Ji An ^a   Liu, Bao Hui ^a   Shao, Ling Min ^a   Guo, Zhen Tao ^a   Yang, Qian ^a   Wu, Li Quan ^a   Ji, Bao Wei ^a   Zhu, Xiao Nan ^a   Zhang, Shen Qi ^a   Li, Cheng Jun ^a   Chen, Qian Xue ^a  

^a RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

Author keywords

apoptosis; EGFR signaling; Glioblastoma; LRIG1; Radiosensitivity; H2AX

Indexed keywords

EID: 84935472423     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (34)

1. Goodenberger ML, Jenkins RB. Genetics of adult glioma. Cancer Genetics 2012; 205: 613-621.
2. Ohgaki H, Dessen P, Jourde B, Horstmann S, Nishikawa T, Di Patre PL, Burkhard C, Schüler D, Probst-Hensch NM, Maiorka PC, Baeza N, Pisani P, Yonekawa Y, Yasargil MG, Lütolf UM, Kleihues P. Genetic pathways to glioblastoma: a population-based study. Cancer Res 2004; 64: 6892-6899.
3. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Jan-zer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, MirimanoffRO; European Organisation for Research and Treatment of Cancer Brain Tumor and Radio-therapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma. New Engl J Med 2005; 352: 987-996.
4. Wang Y, Jiang T. Understanding high grade glioma: Molecular mechanism, therapy and comprehensive management. Cancer Lett 2013; 331: 139-146.
5. Carlsson SK, Brothers SP, Wahlestedt C. Emer-ging treatment strategies for glioblastoma multiforme. EMBO Mol Med 2014; 6: 1359-1370.
6. Omuro A. Glioblastoma and other malignant gliomas. JAMA 2013; 310: 1842.
7. Atkins RJ, Ng W, Stylli SS, Hovens CM, Kaye AH. Repair mechanisms help glioblastoma resist treatment. J Clin Neurosci 2015; 22: 14-20.
8. Nilsson J, Vallbo C, Guo D, Golovleva I, Hallberg B, Henriksson R, Hedman H. Cloning, characterization, and expression of human LIG1. Biochem Bioph Res Co 2001; 284: 1155-1161.
9. Hedman H, Nilsson J, Guo D, Henriksson R. Is LRIG1 a tumour suppressor gene at chromosome 3p14.3? Acta Oncol 2002; 41: 352-354.
10. Thomasson M, Hedman H, Guo D, Ljungberg B, Henriksson R. LRIG1 and epidermal growth factor receptor in renal cell carcinoma: a quantitative RT-PCR and immunohistochemical analysis. Brit J Cancer 2003; 89: 1285-1289.
11. Nagata M, Nakamura T, Sotozono C, Inatomi T, Yokoi N, Kinoshita S. LRIG1 as a Potential Novel Marker for Neoplastic Transformation in Ocular Surface Squamous Neoplasia. PLoS One 2014; 9: e93164.
12. Wu X, Hedman H, Bergqvist M, Bergström S, Henriksson R, Gullbo J, Lennartsson J, Hes-selius P, Ekman S. Expression of EGFR and LRIG proteins in oesophageal carcinoma with emphasis on patient survival and cellular chemosensitivity. Acta Oncol 2012; 51: 69-76.
13. Sheu JJ, Lee CC, Hua CH, Li CI, Lai MT, Lee SC, Cheng J, Chen CM, Chan C, Chao SC, Chen JY, Chang JY, Lee CH. LRIG1 modulates aggressiveness of head and neck cancers by regulating EGFR-MAPK-SPHK1 signaling and extracellular matrix remodeling. Oncogene 2013; 33: 1375-1384.
14. Johansson M, Oudin A, Tiemann K, Bernard A, Golebiewska A, Keunen O, Fack F, Stieber D, Wang B, Hedman H, Niclou SP. The soluble form of the tumor suppressor Lrig1 potently inhibits in vivo glioma growth irrespective of EGF receptor status. Neuro-Oncology 2013; 15: 1200-1211.
15. Lu L, Teixeira VH, Yuan Z, Graham TA, Ende-sfelder D, Kolluri K, Al-Juffali N, Hamilton N, Nicholson AG, Falzon M, Kschischo M, Swanton C, Wright NA, Carroll B, Watt FM, George JP, Jensen KB, Giangreco A, Janes SM. LRIG1 regulates cadherin-dependent contact inhibition directing epithelial homeostasis and pre-invasive squamous cell carcinoma development. J Pathol 2013; 229: 608-620.
16. Desoubzdanne D, Claparols C, Martins-Fro-ment N, Zedde C, Balayssac S, Gilard V, Tercé F, Martino R, Malet-Martino M. Analysis of hydrophilic and lipophilic choline compounds in radioresistant and radiosensitive glioblastoma cell lines by HILIC-ESI-MS/MS. Anal Bioanal Chem 2010; 398: 2723-2730.
17. Wu F, Hu Y, Long J, Zhou YJ, Zhong YH, Liao ZK, Liu SQ, Zhou FX, Zhou YF, Xie CH. Cytotoxicity and radiosensitization effect of TRA-8 on radioresistant human larynx squamous carcinoma cells. Oncol Rep 2009; 21: 461-465.
18. Lee YS, Oh J, Yoon S, Kwon MS, Song CW, Kim KH, Cho MJ, Mollah ML, Je YJ, Kim YD, Kim CD, Lee JH. Differential Gene Expression Profiles of Radioresistant Non-Small-Cell Lung Cancer Cell Lines Established by Fractionated Irradi-ation: Tumor Protein p53-Inducible Protein 3 Confers Sensitivity to Ionizing Radiation. Int J Radiat Oncol Biol Phys 2010; 77: 858-866.
19. Wouters BG, Sy AM, Skarsgard LD. Low-dose hypersensitivity and increased radioresistance in a panel of human tumor cell lines with different radiosensitivity. Radiat Res 1996; 146: 399-413.
20. Bai L, McEachern D, Yang CY, Lu J, Sun H, Wang S. LRIG1 modulates cancer cell sensitivity to Smac mimetics by regulating TNF expression and receptor tyrosine kinase signaling. Cancer Res 2012; 72: 1229-1238.
21. Qi XC, Xie DJ, Yan QF, Wang YR, Zhu YX, Qian C, Yang SX. LRIG1 dictates the chemo-sensitivity of temozolomide (TMZ) in U251 glioblastoma cells via down-regulation of EGFR/topoisomerase-2/Bcl-2. Biochem Biophys Res Commun 2013; 437: 565-572.
22. Fedrigo CA, Grivicich I, Schunemann DP, Che-male IM, Santos D, Jacovas T, Boschetti PS, Jotz GP, Braga Filho A, da Rocha AB. Radi-oresistance of human glioma spheroids and expression of HSP70, p53 and EGFr. Radiation Oncology 2011; 6: 156.
23. Qu YY, Hu SL, Xu XY, Wang RZ, Yu HY, Xu JY, Chen L, Dong GL. Nimotuzumab Enhances the Radiosensitivity of Cancer Cells In Vitro by Inhibiting Radiation-Induced DNA Damage Repair. PLoS One 2013; 8: e70727.
24. Kesari S, Advani SJ, Lawson JD, Kahle KT, Ng K, Carter B, Chen CC. DNA damage response and repair: insights into strategies for radiation sensitization of gliomas. Future Oncology 2011; 7: 1335-1346.
25. von Stechow L, van de Water B, Danen EH. Un-raveling DNA damage response-signaling networks through systems approaches. Arch Toxicol 2013; 87: 1635-1648.
26. Kinner A, Wu W, Staudt C, Iliakis G. Gramma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008; 36: 5678-5694.
27. Hartlerode AJ, Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem J 2009; 423: 157-168.
28. Boehme KA, Kulikov R, Blattner C. p53 stabilization in response to DNA damage requires Akt/PKB and DNA-PK. Proc Natl Acad Sci U S A 2008; 105: 7785-7790.
29. Bozulic L, Surucu B, Hynx D, Hemmings BA. PKBα/Akt1 Acts downstream of DNA-PK in the DNA double-strand break response and promotes survival. Mol Cell 2008; 30: 203-213.
30. Gupta AK, Cerniglia GJ, Mick R, McKenna WG, Muschel RJ. HIV protease inhibitors block Akt signaling and radiosensitize tumor cells both in vitro and In vivo. Cancer Res 2005; 65: 8256-8265.
31. Toulany M, Kehlbach R, Florczak U, Sak A, Wang S, Chen J, Lobrich M, Rodemann HP. Tar-geting of AKT1 enhances radiation toxicity of human tumor cells by inhibiting DNA-PKcs-dependent DNA double-strand break repair. Mol Cancer Ther 2008; 7: 1772-1781.
32. Chang L, Graham PH, Hao J, Ni J, Bucci J, Cozzi PJ, Kearsley JH, Li Y. PI3K/Akt/mTOR pathway inhibitors enhance radiosensitivity in radioresistant prostate cancer cells through inducing apoptosis, reducing autophagy, suppressing NHEJ and HR repair pathways. Cell Death and Disease 2014; 5: e1437.
33. Golding SE, Morgan RN, Adams BR, Hawkins AJ, Povirk LF, Valerie K. Pro-survival AKT and ERK signaling from EGFR and mutant EGFRvIII enhances DNA double-strand break repair in human glioma cells. Cancer Biol Ther 2009; 8: 730-738.
34. Li B, Yuan M, Kim I, Chang C, Bernhard EJ, Shu HG. Mutant epidermal growth factor receptor displays increased signaling through the phosphatidylinositol-3kinase/AKT pathway and promotes radioresistance in cells of astrocytic origin. Oncogene 2004; 23: 4594-4602.