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IGF-1-enhanced miR-513a-5p signaling desensitizes glioma cells to temozolomide by targeting the NEDD4L-inhibited Wnt/β-catenin pathway


Autoři: Ku-Chung Chen aff001;  Peng-Hsu Chen aff001;  Kuo-Hao Ho aff001;  Chwen-Ming Shih aff001;  Chih-Ming Chou aff001;  Chia-Hsiung Cheng aff001;  Chin-Cheng Lee aff003
Působiště autorů: Graduate Institute of Medical Sciences, College of Medicine, Taipei Medical University, Taipei, Taiwan aff001;  Department of Biochemistry and Molecular Cell Biology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan aff002;  Department of Pathology and Laboratory Medicine, Shin Kong Wu Ho-Su Memorial Hospital, Taipei, Taiwan aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225913

Souhrn

Temozolomide (TMZ) is a first-line alkylating agent for glioblastoma multiforme (GBM). Clarifying the mechanisms inducing TMZ insensitivity may be helpful in improving its therapeutic effectiveness against GBM. Insulin-like growth factor (IGF)-1 signaling and micro (mi)RNAs are relevant in mediating GBM progression. However, their roles in desensitizing GBM cells to TMZ are still unclear. We aimed to identify IGF-1-mediated miRNA regulatory networks that elicit TMZ insensitivity for GBM. IGF-1 treatment attenuated TMZ cytotoxicity via WNT/β-catenin signaling, but did not influence glioma cell growth. By miRNA array analyses, 93 upregulated and 148 downregulated miRNAs were identified in IGF-1-treated glioma cells. miR-513a-5p from the miR-513a-2 gene locus was upregulated by IGF-1-mediated phosphoinositide 3-kinase (PI3K) signaling. Its elevated levels were also observed in gliomas versus normal cells, in array data of The Cancer Genome Atlas (TCGA), and the GSE61710, GSE37366, and GSE41032 datasets. In addition, lower levels of neural precursor cell-expressed developmentally downregulated 4-like (NEDD4L), an E3 ubiquitin protein ligase that inhibits WNT signaling, were found in gliomas by analyzing cells, arrays, and RNA sequencing data of TCGA glioma patients. Furthermore, a negative correlation was identified between miR-513a-5p and NEDD4L in glioma. NEDD4L was also validated as a direct target gene of miR-513a-5p, and it was reduced by IGF-1 treatment. Overexpression of NEDD4L inhibited glioma cell viability and reversed IGF-1-repressed TMZ cytotoxicity. In contrast, miR-513a-5p significantly affected NEDD4L-inhibited WNT signaling and reduced TMZ cytotoxicity. These findings demonstrate a distinct role of IGF-1 signaling through miR-513a-5p-inhibited NEDD4L networks in influencing GBM's drug sensitivity to TMZ.

Klíčová slova:

Glioblastoma multiforme – Glioma – Glioma cells – Hyperexpression techniques – Microarrays – MicroRNAs – MTT assay – Polymerase chain reaction


Zdroje

1. Wilson TA, Karajannis MA, Harter DH. Glioblastoma multiforme: State of the art and future therapeutics. Surg Neurol Int. 2014;5:64. Epub 2014/07/06. doi: 10.4103/2152-7806.132138 [pii]. 24991467; PubMed Central PMCID: PMC4078454.

2. Urbanska K, Sokolowska J, Szmidt M, Sysa P. Glioblastoma multiforme—an overview. Contemp Oncol (Pozn). 2014;18(5):307–12. Epub 2014/12/06. doi: 10.5114/wo.2014.40559 [pii]. 25477751; PubMed Central PMCID: PMC4248049.

3. Trojan J, Cloix JF, Ardourel MY, Chatel M, Anthony DD. Insulin-like growth factor type I biology and targeting in malignant gliomas. Neuroscience. 2007;145(3):795–811. doi: 10.1016/j.neuroscience.2007.01.021 17320297.

4. Schlenska-Lange A, Knupfer H, Lange TJ, Kiess W, Knupfer M. Cell proliferation and migration in glioblastoma multiforme cell lines are influenced by insulin-like growth factor I in vitro. Anticancer research. 2008;28(2A):1055–60. 18507054.

5. Sinha S, Koul N, Dixit D, Sharma V, Sen E. IGF-1 induced HIF-1alpha-TLR9 cross talk regulates inflammatory responses in glioma. Cellular signalling. 2011;23(11):1869–75. doi: 10.1016/j.cellsig.2011.06.024 21756999.

6. Denduluri SK, Idowu O, Wang Z, Liao Z, Yan Z, Mohammed MK, et al. Insulin-like growth factor (IGF) signaling in tumorigenesis and the development of cancer drug resistance. Genes & Diseases. 2015;2(1):13–25. doi: 10.1016/j.gendis.2014.10.004 25984556; PubMed Central PMCID: PMC4431759.

7. Quail DF, Bowman RL, Akkari L, Quick ML, Schuhmacher AJ, Huse JT, et al. The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science. 2016;352(6288):aad3018. doi: 10.1126/science.aad3018 27199435.

8. Yin D, Tamaki N, Parent AD, Zhang JH. Insulin-like growth factor-I decreased etoposide-induced apoptosis in glioma cells by increasing bcl-2 expression and decreasing CPP32 activity. Neurological research. 2005;27(1):27–35. doi: 10.1179/016164105X18151 15829155.

9. Shea A, Harish V, Afzal Z, Chijioke J, Kedir H, Dusmatova S, et al. MicroRNAs in glioblastoma multiforme pathogenesis and therapeutics. Cancer medicine. 2016. doi: 10.1002/cam4.775 27282910.

10. Teplyuk NM, Uhlmann EJ, Gabriely G, Volfovsky N, Wang Y, Teng J, et al. Therapeutic potential of targeting microRNA-10b in established intracranial glioblastoma: first steps toward the clinic. EMBO molecular medicine. 2016;8(3):268–87. doi: 10.15252/emmm.201505495 26881967; PubMed Central PMCID: PMC4772951.

11. Hu J, Sun T, Wang H, Chen Z, Wang S, Yuan L, et al. MiR-215 Is Induced Post-transcriptionally via HIF-Drosha Complex and Mediates Glioma-Initiating Cell Adaptation to Hypoxia by Targeting KDM1B. Cancer cell. 2016;29(1):49–60. doi: 10.1016/j.ccell.2015.12.005 26766590; PubMed Central PMCID: PMC4871949.

12. Piwecka M, Rolle K, Belter A, Barciszewska AM, Zywicki M, Michalak M, et al. Comprehensive analysis of microRNA expression profile in malignant glioma tissues. Molecular oncology. 2015;9(7):1324–40. doi: 10.1016/j.molonc.2015.03.007 25864039.

13. Goel P, Manning JA, Kumar S. NEDD4-2 (NEDD4L): the ubiquitin ligase for multiple membrane proteins. Gene. 2015;557(1):1–10. doi: 10.1016/j.gene.2014.11.051 25433090.

14. Harvey KF, Dinudom A, Cook DI, Kumar S. The Nedd4-like protein KIAA0439 is a potential regulator of the epithelial sodium channel. The Journal of biological chemistry. 2001;276(11):8597–601. doi: 10.1074/jbc.C000906200 11244092.

15. Deguchi Y, Nakashima E, Ishikawa F, Sato H, Tamai I, Matsushita R, et al. Peritoneal transport of beta-lactam antibiotics: effects of plasma protein binding and the interspecies relationship. Journal of pharmaceutical sciences. 1988;77(7):559–64. doi: 10.1002/jps.2600770702 3171941.

16. Fotia AB, Ekberg J, Adams DJ, Cook DI, Poronnik P, Kumar S. Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. The Journal of biological chemistry. 2004;279(28):28930–5. doi: 10.1074/jbc.M402820200 15123669.

17. Tanksley JP, Chen X, Coffey RJ. NEDD4L is downregulated in colorectal cancer and inhibits canonical WNT signaling. PloS one. 2013;8(11):e81514. doi: 10.1371/journal.pone.0081514 24312311; PubMed Central PMCID: PMC3842946.

18. Gao C, Pang L, Ren C, Ma T. Decreased expression of Nedd4L correlates with poor prognosis in gastric cancer patient. Medical oncology. 2012;29(3):1733–8. doi: 10.1007/s12032-011-0061-3 21909941.

19. He S, Deng J, Li G, Wang B, Cao Y, Tu Y. Down-regulation of Nedd4L is associated with the aggressive progression and worse prognosis of malignant glioma. Japanese journal of clinical oncology. 2012;42(3):196–201. doi: 10.1093/jjco/hyr195 22217575.

20. Hsieh A, Ellsworth R, Hsieh D. Hedgehog/GLI1 regulates IGF dependent malignant behaviors in glioma stem cells. Journal of cellular physiology. 2011;226(4):1118–27. doi: 10.1002/jcp.22433 20857406.

21. Weinstein JN, Myers TG, O'Connor PM, Friend SH, Fornace AJ Jr., Kohn KW, et al. An information-intensive approach to the molecular pharmacology of cancer. Science. 1997;275(5298):343–9. doi: 10.1126/science.275.5298.343 8994024.

22. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120(1):15–20. doi: 10.1016/j.cell.2004.12.035 15652477.

23. Vanamala J, Reddivari L, Radhakrishnan S, Tarver C. Resveratrol suppresses IGF-1 induced human colon cancer cell proliferation and elevates apoptosis via suppression of IGF-1R/Wnt and activation of p53 signaling pathways. BMC cancer. 2010;10:238. doi: 10.1186/1471-2407-10-238 20504360; PubMed Central PMCID: PMC2891636.

24. Yi GZ, Liu YW, Xiang W, Wang H, Chen ZY, Xie SD, et al. Akt and beta-catenin contribute to TMZ resistance and EMT of MGMT negative malignant glioma cell line. Journal of the neurological sciences. 2016;367:101–6. doi: 10.1016/j.jns.2016.05.054 27423571.

25. Weroha SJ, Haluska P. The insulin-like growth factor system in cancer. Endocrinology and metabolism clinics of North America. 2012;41(2):335–50, vi. doi: 10.1016/j.ecl.2012.04.014 22682634; PubMed Central PMCID: PMC3614012.

26. Zhang M, Liu J, Li M, Zhang S, Lu Y, Liang Y, et al. Insulin-like growth factor 1/insulin-like growth factor 1 receptor signaling protects against cell apoptosis through the PI3K/AKT pathway in glioblastoma cells. Experimental and therapeutic medicine. 2018;16(2):1477–82. doi: 10.3892/etm.2018.6336 30116397; PubMed Central PMCID: PMC6090237.

27. Chen HX, Sharon E. IGF-1R as an anti-cancer target—trials and tribulations. Chinese journal of cancer. 2013;32(5):242–52. doi: 10.5732/cjc.012.10263 23601239; PubMed Central PMCID: PMC3845553.

28. Zamykal M, Martens T, Matschke J, Gunther HS, Kathagen A, Schulte A, et al. Inhibition of intracerebral glioblastoma growth by targeting the insulin-like growth factor 1 receptor involves different context-dependent mechanisms. Neuro-oncology. 2015;17(8):1076–85. doi: 10.1093/neuonc/nou344 25543125; PubMed Central PMCID: PMC4490867.

29. Zhou Q. BMS-536924, an ATP-competitive IGF-1R/IR inhibitor, decreases viability and migration of temozolomide-resistant glioma cells in vitro and suppresses tumor growth in vivo. OncoTargets and therapy. 2015;8:689–97. doi: 10.2147/OTT.S80047 25897243; PubMed Central PMCID: PMC4396459.

30. Suwala AK, Koch K, Rios DH, Aretz P, Uhlmann C, Ogorek I, et al. Inhibition of Wnt/beta-catenin signaling downregulates expression of aldehyde dehydrogenase isoform 3A1 (ALDH3A1) to reduce resistance against temozolomide in glioblastoma in vitro. Oncotarget. 2018;9(32):22703–16. doi: 10.18632/oncotarget.25210 29854309; PubMed Central PMCID: PMC5978259.

31. Wickstrom M, Dyberg C, Milosevic J, Einvik C, Calero R, Sveinbjornsson B, et al. Wnt/beta-catenin pathway regulates MGMT gene expression in cancer and inhibition of Wnt signalling prevents chemoresistance. Nature communications. 2015;6:8904. doi: 10.1038/ncomms9904 26603103; PubMed Central PMCID: PMC4674781.

32. Suwala AK, Hanaford A, Kahlert UD, Maciaczyk J. Clipping the Wings of Glioblastoma: Modulation of WNT as a Novel Therapeutic Strategy. Journal of neuropathology and experimental neurology. 2016;75(5):388–96. doi: 10.1093/jnen/nlw013 26979081.

33. Ye P, Hu Q, Liu H, Yan Y, D'Ercole A J. beta-catenin mediates insulin-like growth factor-I actions to promote cyclin D1 mRNA expression, cell proliferation and survival in oligodendroglial cultures. Glia. 2010;58(9):1031–41. doi: 10.1002/glia.20984 20235220; PubMed Central PMCID: PMC2917840.

34. Verras M, Sun Z. Beta-catenin is involved in insulin-like growth factor 1-mediated transactivation of the androgen receptor. Molecular endocrinology. 2005;19(2):391–8. doi: 10.1210/me.2004-0208 15514031.

35. Desbois-Mouthon C, Cadoret A, Blivet-Van Eggelpoel MJ, Bertrand F, Cherqui G, Perret C, et al. Insulin and IGF-1 stimulate the beta-catenin pathway through two signalling cascades involving GSK-3beta inhibition and Ras activation. Oncogene. 2001;20(2):252–9. doi: 10.1038/sj.onc.1204064 11313952.

36. Jia B, Liu W, Gu J, Wang J, Lv W, Zhang W, et al. MiR-7-5p suppresses stemness and enhances temozolomide sensitivity of drug-resistant glioblastoma cells by targeting Yin Yang 1. Experimental cell research. 2019;375(1):73–81. doi: 10.1016/j.yexcr.2018.12.016 30586549.

37. Chen Y, Li R, Pan M, Shi Z, Yan W, Liu N, et al. MiR-181b modulates chemosensitivity of glioblastoma multiforme cells to temozolomide by targeting the epidermal growth factor receptor. Journal of neuro-oncology. 2017;133(3):477–85. doi: 10.1007/s11060-017-2463-3 28501897.

38. Muti P, Donzelli S, Sacconi A, Hossain A, Ganci F, Frixa T, et al. MiRNA-513a-5p inhibits progesterone receptor expression and constitutes a risk factor for breast cancer: the hOrmone and Diet in the ETiology of breast cancer prospective study. Carcinogenesis. 2018;39(2):98–108. doi: 10.1093/carcin/bgx126 29126102.

39. Donovan P, Poronnik P. Nedd4 and Nedd4-2: ubiquitin ligases at work in the neuron. The international journal of biochemistry & cell biology. 2013;45(3):706–10. doi: 10.1016/j.biocel.2012.12.006 23262292.

40. Ding Y, Zhang Y, Xu C, Tao QH, Chen YG. HECT domain-containing E3 ubiquitin ligase NEDD4L negatively regulates Wnt signaling by targeting dishevelled for proteasomal degradation. The Journal of biological chemistry. 2013;288(12):8289–98. doi: 10.1074/jbc.M112.433185 23396981; PubMed Central PMCID: PMC3605647.

41. Yan J, Du F, Li SD, Yuan Y, Jiang JY, Li S, et al. AUF1 modulates TGF-beta signal in renal tubular epithelial cells via post-transcriptional regulation of Nedd4L expression. Biochimica et biophysica acta Molecular cell research. 2018;1865(1):48–56. doi: 10.1016/j.bbamcr.2017.10.001 28986222.

42. Qu MH, Han C, Srivastava AK, Cui T, Zou N, Gao ZQ, et al. miR-93 promotes TGF-beta-induced epithelial-to-mesenchymal transition through downregulation of NEDD4L in lung cancer cells. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine. 2016;37(4):5645–51. doi: 10.1007/s13277-015-4328-8 26581907.

43. Zhu JY, Heidersbach A, Kathiriya IS, Garay BI, Ivey KN, Srivastava D, et al. The E3 ubiquitin ligase Nedd4/Nedd4L is directly regulated by microRNA 1. Development. 2017;144(5):866–75. doi: 10.1242/dev.140368 28246214; PubMed Central PMCID: PMC5374346.

44. Guarnieri AL, Towers CG, Drasin DJ, Oliphant MUJ, Andrysik Z, Hotz TJ, et al. The miR-106b-25 cluster mediates breast tumor initiation through activation of NOTCH1 via direct repression of NEDD4L. Oncogene. 2018;37(28):3879–93. doi: 10.1038/s41388-018-0239-7 29662198; PubMed Central PMCID: PMC6043359.


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