Aspirin inhibits the SHH/GLI1 signaling pathway and sensitizes malignant glioma cells to temozolomide therapy

Aging

Volumn 9, Issue 4, 2017, Pages 1233-1247

  Ming, Jianguang ^a,b   Sun, Bo ^a,b   Li, Ziwei ^a,b   Lin, Lin ^a,b   Meng, Xiangqi ^a,b   Han, Bo ^a,b   Wang, Ruijia ^a,b   Wu, Pengfei ^a,b   Li, Jianlong ^a,b   Cai, Jinquan ^a,b,c   Jiang, Chuanlu ^a,b,c  

^a HARBIN MEDICAL UNIVERSITY   (China)

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

^c Biopharmaceutical Institute   (China)

Author keywords

Aspirin; DNA damage; Glioma; Hedgehog; Temozolomide

Indexed keywords

ACETYLSALICYLIC ACID; ALKYLATING AGENT; DACARBAZINE; GLI1 PROTEIN, HUMAN; SHH PROTEIN, HUMAN; SONIC HEDGEHOG PROTEIN; TEMOZOLOMIDE; TRANSCRIPTION FACTOR GLI1;

ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BRAIN TUMOR; DNA REPAIR; DRUG EFFECTS; DRUG POTENTIATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE TRANSLOCATION; GLIOMA; HUMAN; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; ASPIRIN; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; DNA REPAIR; DRUG SYNERGISM; EPITHELIAL-MESENCHYMAL TRANSITION; GLIOMA; HEDGEHOG PROTEINS; HUMANS; SIGNAL TRANSDUCTION; TRANSLOCATION, GENETIC; ZINC FINGER PROTEIN GLI1;

EID: 85018975093     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.101224     Document Type: Article

References (44)

1. Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS. CBTRUS Statistical Report: Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 2008-2012. Neuro-oncol. 2015 (Suppl 4); 17:iv1-62. doi: 10.1093/neuonc/nov189.
2. Katoh Y, Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med. 2009; 9:873-86. doi: 10.2174/156652409789105570.
3. Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, Ruiz i Altaba A. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med. 2009; 1:338-51. doi: 10.1002/emmm.200900039.
4. Yamasaki A, Kameda C, Xu R, Tanaka H, Tasaka T, Chikazawa N, Suzuki H, Morisaki T, Kubo M, Onishi H, Tanaka M, Katano M. Nuclear factor kappaBactivated monocytes contribute to pancreatic cancer progression through the production of Shh. Cancer Immunol Immunother. 2010; 59:675-86. doi: 10.1007/s00262-009-0783-7.
5. Wang TP, Hsu SH, Feng HC, Huang RF. Folate deprivation enhances invasiveness of human colon cancer cells mediated by activation of sonic hedgehog signaling through promoter hypomethylation and cross action with transcription nuclear factor-kappa B pathway. Carcinogenesis. 2012; 33:1158-68. doi: 10.1093/carcin/bgs138.
6. Colavito SA, Zou MR, Yan Q, Nguyen DX, Stern DF. Significance of glioma-associated oncogene homolog 1 (GLI1) expression in claudin-low breast cancer and crosstalk with the nuclear factor kappa-light-chainenhancer of activated B cells (NFkappaB) pathway. Breast cancer research. BCR. 2014; 16:444. doi: 10.1186/s13058-014-0444-4.
7. Sarkaria JN, Kitange GJ, James CD, Plummer R, Calvert H, Weller M, Wick W. Mechanisms of chemoresistance to alkylating agents in malignant glioma. Clin Cancer Res. 2008; 14:2900-08. doi: 10.1158/1078-0432.CCR-07-1719.
8. Meng E, Hanna A, Samant RS, Shevde LA. The Impact of Hedgehog Signaling Pathway on DNA Repair Mechanisms in Human Cancer. Cancers (Basel). 2015; 7:1333-48. doi: 10.3390/cancers7030839.
9. Yue W, Zheng X, Lin Y, Yang CS, Xu Q, Carpizo D, Huang H, DiPaola RS, Tan XL. Metformin combined with aspirin significantly inhibit pancreatic cancer cell growth in vitro and in vivo by suppressing antiapoptotic proteins Mcl-1 and Bcl-2. Oncotarget. 2015; 6:21208-24. doi: 10.18632/oncotarget.4126.
10. Zhang Y, Liu L, Fan P, Bauer N, Gladkich J, Ryschich E, Bazhin AV, Giese NA, Strobel O, Hackert T, Hinz U, Gross W, Fortunato F, Herr I. Aspirin counteracts cancer stem cell features, desmoplasia and gemcitabine resistance in pancreatic cancer. Oncotarget. 2015; 6:9999-10015. doi: 10.18632/oncotarget.3171.
11. Gao M, Kong Q, Hua H, Yin Y, Wang J, Luo T, Jiang Y. AMPK-mediated up-regulation of mTORC2 and MCL-1 compromises the anti-cancer effects of aspirin. Oncotarget. 2016; 7:16349-61. doi: 10.18632/oncotarget.7648.
12. Sivak-Sears NR, Schwartzbaum JA, Miike R, Moghadassi M, Wrensch M. Case-control study of use of nonsteroidal antiinflammatory drugs and glioblastoma multiforme. Am J Epidemiol. 2004; 159:1131-39. doi: 10.1093/aje/kwh153.
13. Wan L, Dong H, Xu H, Ma J, Zhu Y, Lu Y, Wang J, Zhang T, Li T, Xie J, Xu B, Xie F, Gao Y, et al. Aspirin, lysine, mifepristone and doxycycline combined can effectively and safely prevent and treat cancer metastasis: prevent seeds from gemmating on soil. Oncotarget. 2015; 6:35157-72. doi: 10.18632/oncotarget.6038.
14. Liao X, Siu MK, Au CW, Wong ES, Chan HY, Ip PP, Ngan HY, Cheung AN. Aberrant activation of hedgehog signaling pathway in ovarian cancers: effect on prognosis, cell invasion and differentiation. Carcinogenesis. 2009; 30:131-40. doi: 10.1093/carcin/bgn230.
15. Du WZ, Feng Y, Wang XF, Piao XY, Cui YQ, Chen LC, Lei XH, Sun X, Liu X, Wang HB, Li XF, Yang DB, Sun Y, et al. Curcumin suppresses malignant glioma cells growth and induces apoptosis by inhibition of SHH/GLI1 signaling pathway in vitro and vivo. CNS Neurosci Ther. 2013; 19:926-36. doi: 10.1111/cns.12163.
16. Benedek IH, Joshi AS, Pieniaszek HJ, King SY, Kornhauser DM. Variability in the pharmacokinetics and pharmacodynamics of low dose aspirin in healthy male volunteers. J Clin Pharmacol. 1995; 35:1181-86. doi: 10.1002/j.1552-4604.1995.tb04044.x.
17. Brighenti E, Giannone FA, Fornari F, Onofrillo C, Govoni M, Montanaro L, Treré D, Derenzini M. Therapeutic dosages of aspirin counteract the IL-6 induced pro-tumorigenic effects by slowing down the ribosome biogenesis rate. Oncotarget. 2016; 7:63226-41. doi: 10.18632/oncotarget.11441.
18. Liu X, Wang X, Du W, Chen L, Wang G, Cui Y, Liu Y, Dou Z, Wang H, Zhang P, Chang L, Yi L, Cai J, Jiang C. Suppressor of fused (Sufu) represses Gli1 transcription and nuclear accumulation, inhibits glioma cell proliferation, invasion and vasculogenic mimicry, improving glioma chemo-sensitivity and prognosis. Oncotarget. 2014; 5:11681-94. doi: 10.18632/oncotarget.2585.
19. Fritz G, Tano K, Mitra S, Kaina B. Inducibility of the DNA repair gene encoding O6-methylguanine-DNA methyltransferase in mammalian cells by DNAdamaging treatments. Mol Cell Biol. 1991; 11:4660-68 doi: 10.1128/MCB.11.9.4660.
20. Yoon JW, Gilbertson R, Iannaccone S, Iannaccone P, Walterhouse D. Defining a role for Sonic hedgehog pathway activation in desmoplastic medulloblastoma by identifying GLI1 target genes. Int J Cancer. 2009; 124:109-19. doi: 10.1002/ijc.23929.
21. Thomas AA, Brennan CW, DeAngelis LM, Omuro AM. Emerging therapies for glioblastoma. JAMA Neurol. 2014; 71:1437-44. doi: 10.1001/jamaneurol.2014.1701.
22. Villavicencio EH, Walterhouse DO, Iannaccone PM. The sonic hedgehog-patched-gli pathway in human development and disease. Am J Hum Genet. 2000; 67:1047-54. doi: 10.1016/S0002-9297(07)62934-6.
23. Mimeault M, Batra SK. Frequent deregulations in the hedgehog signaling network and cross-talks with the epidermal growth factor receptor pathway involved in cancer progression and targeted therapies. Pharmacol Rev. 2010; 62:497-524. doi: 10.1124/pr.109.002329.
24. Santoni M, Burattini L, Nabissi M, Morelli MB, Berardi R, Santoni G, Cascinu S. Essential role of Gli proteins in glioblastoma multiforme. Curr Protein Pept Sci. 2013; 14:133-40. doi: 10.2174/1389203711314020005.
25. Ryan KE, Chiang C. Hedgehog secretion and signal transduction in vertebrates. J Biol Chem. 2012; 287:17905-13. doi: 10.1074/jbc.R112.356006.
26. Ding H, Xu Y, Gao D, Wang L. Glioma-associated oncogene homolog 1 promotes epithelialmesenchymal transition in human renal tubular epithelial cell. Am J Transl Res. 2016; 8:662-69.
27. Scheurer ME, El-Zein R, Thompson PA, Aldape KD, Levin VA, Gilbert MR, Weinberg JS, Bondy ML. Longterm anti-inflammatory and antihistamine medication use and adult glioma risk. Cancer Epidemiol Biomarkers Prev. 2008; 17:1277-81. doi: 10.1158/1055-9965.EPI-07-2621.
28. Rothwell PM, Fowkes FG, Belch JF, Ogawa H, Warlow CP, Meade TW. Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet. 2011; 377:31-41. doi: 10.1016/S0140-6736(10)62110-1.
29. Mitrugno A, Sylman JL, Ngo AT, Pang J, Sears RC, Williams CD, McCarty OJ. Aspirin therapy reduces the ability of platelets to promote colon and pancreatic cancer cell proliferation: implications for the oncoprotein c-MYC. Am J Physiol Cell Physiol. 2017; 312:C176-89. doi: 10.1152/ajpcell.00196.2016.
30. Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, Ohlfest JR, Okada H. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 2011; 71:2664-74. doi: 10.1158/0008-5472.CAN-10-3055.
31. Shi ZD, Qian XM, Liu CY, Han L, Zhang KL, Chen LY, Zhang JX, Pu PY, Yuan XB, Kang CS, and Chinese Glioma Cooperative Group (CGCG). Aspirin-/TMZcoloaded microspheres exert synergistic antiglioma efficacy via inhibition of β-catenin transactivation. CNS Neurosci Ther. 2013; 19:98-108. doi: 10.1111/cns.12041.
32. Kim SR, Bae MK, Kim JY, Wee HJ, Yoo MA, Bae SK. Aspirin induces apoptosis through the blockade of IL-6-STAT3 signaling pathway in human glioblastoma A172 cells. Biochem Biophys Res Commun. 2009; 387:342-47. doi: 10.1016/j.bbrc.2009.07.022.
33. Wang Z, Zhang S, Siu TL, Huang S. Glioblastoma multiforme formation and EMT: role of FoxM1 transcription factor. Curr Pharm Des. 2015; 21:1268-71 doi: 10.2174/1381612821666141211115949.
34. Auffinger B, Morshed R, Tobias A, Cheng Y, Ahmed AU, Lesniak MS. Drug-loaded nanoparticle systems and adult stem cells: a potential marriage for the treatment of malignant glioma? Oncotarget. 2013; 4:378-96. doi: 10.18632/oncotarget.937.
35. Liang P, Shi H, Zhu W, Gui Q, Xu Y, Meng J, Guo X, Gong Z, Chen H. Silver nanoparticles enhance the sensitivity of temozolomide on human glioma cells. Oncotarget. 2017; 8:7533-39.
36. Zahreddine HA, Culjkovic-Kraljacic B, Assouline S, Gendron P, Romeo AA, Morris SJ, Cormack G, Jaquith JB, Cerchietti L, Cocolakis E, Amri A, Bergeron J, Leber B, et al. The sonic hedgehog factor GLI1 imparts drug resistance through inducible glucuronidation. Nature. 2014; 511:90-93. doi: 10.1038/nature13283.
37. Amable L, Fain J, Gavin E, Reed E. Gli1 contributes to cellular resistance to cisplatin through altered cellular accumulation of the drug. Oncol Rep. 2014; 32:469-74 doi: 10.3892/or.2014.3257.
38. Kasperczyk H, Baumann B, Debatin KM, Fulda S. Characterization of sonic hedgehog as a novel NFkappaB target gene that promotes NF-kappaBmediated apoptosis resistance and tumor growth in vivo. FASEB J. 2009; 23:21-33. doi: 10.1096/fj.08-111096.
39. Wu ZH, Miyamoto S. Many faces of NF-κB signaling induced by genotoxic stress. J Mol Med (Berl). 2007; 85:1187-202. doi: 10.1007/s00109-007-0227-9.
40. Caporali S, Levati L, Graziani G, Muzi A, Atzori MG, Bonmassar E, Palmieri G, Ascierto PA, D'Atri S. NF-κB is activated in response to temozolomide in an AKTdependent manner and confers protection against the growth suppressive effect of the drug. J Transl Med. 2012; 10:252. doi: 10.1186/1479-5876-10-252.
41. Habraken Y, Piette J. NF-kappaB activation by doublestrand breaks. Biochem Pharmacol. 2006; 72:1132-41 doi: 10.1016/j.bcp.2006.07.015.
42. Nogueira L, Ruiz-Ontañon P, Vazquez-Barquero A, Moris F, Fernandez-Luna JL. The NFκB pathway: a therapeutic target in glioblastoma. Oncotarget. 2011; 2:646-53. doi: 10.18632/oncotarget.322.
43. Zhang Y, Zhang X, Wang X, Gan L, Yu G, Chen Y, Liu K, Li P, Pan J, Wang J, Qin S. Inhibition of LDH-A by lentivirus-mediated small interfering RNA suppresses intestinal-type gastric cancer tumorigenicity through the downregulation of Oct4. Cancer Lett. 2012; 321:45-54. doi: 10.1016/j.canlet.2012.03.013.
44. Li J, Cai J, Zhao S, Yao K, Sun Y, Li Y, Chen L, Li R, Zhai X, Zhang J, Jiang C. GANT61, a GLI inhibitor, sensitizes glioma cells to the temozolomide treatment. J Exp Clin Cancer Res. 2016; 35:184. doi: 10.1186/s13046-016-0463-3.