دورية أكاديمية

SNAP reverses temozolomide resistance in human glioblastoma multiforme cells through down-regulation of MGMT.

التفاصيل البيبلوغرافية
العنوان: SNAP reverses temozolomide resistance in human glioblastoma multiforme cells through down-regulation of MGMT.
المؤلفون: Tsai CK; Department of Neurology, Tri-Service General Hospital, Taipei, Taiwan., Huang LC; Department of Biochemistry, National Defense Medical Center, Taipei, Taiwan., Wu YP; Department of Biochemistry, National Defense Medical Center, Taipei, Taiwan., Kan IY; Department of Biochemistry, National Defense Medical Center, Taipei, Taiwan., Hueng DY; Department of Neurological Surgery, Tri-Service General Hospital, Taipei, Taiwan.; Department of Biochemistry, National Defense Medical Center, Taipei, Taiwan.; Graduate Institute of Medical Sciences, National Defense Medical Center, Taipei, Taiwan.; Department of Biology and Anatomy, National Defense Medical Center, Taipei, Taiwan.
المصدر: FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2019 Dec; Vol. 33 (12), pp. 14171-14184. Date of Electronic Publication: 2019 Nov 07.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Federation of American Societies for Experimental Biology Country of Publication: United States NLM ID: 8804484 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1530-6860 (Electronic) Linking ISSN: 08926638 NLM ISO Abbreviation: FASEB J Subsets: MEDLINE
أسماء مطبوعة: Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley
Original Publication: [Bethesda, Md.] : The Federation, [c1987-
مواضيع طبية MeSH: Drug Resistance, Neoplasm*, DNA Modification Methylases/*metabolism , DNA Repair Enzymes/*metabolism , Glioblastoma/*drug therapy , S-Nitroso-N-Acetylpenicillamine/*pharmacology , Temozolomide/*pharmacology , Tumor Suppressor Proteins/*metabolism, Animals ; Antineoplastic Agents, Alkylating/pharmacology ; Apoptosis/drug effects ; Biomarkers/blood ; DNA Damage ; DNA Modification Methylases/genetics ; DNA Repair Enzymes/genetics ; Down-Regulation ; Enzyme Inhibitors/pharmacology ; Gene Expression Regulation, Neoplastic/drug effects ; Humans ; Mice ; Mice, Nude ; Neoplasms, Experimental ; Tumor Suppressor Proteins/genetics
مستخلص: Glioblastoma multiforme (GBM) is the most frequently occurring and gravest primary tumor of the CNS in adults. The development of chemoresistance to temozolomide (TMZ), the first-line chemotherapy for GBM, is an important factor contributing to poor treatment outcomes. Down-regulation of O -6-methylguanine-DNA methyltransferase (MGMT) expression in GBM cells is an attractive strategy for overcoming TMZ resistance and improving outcomes. This study revealed that the nitric oxide (NO) donor S -nitroso- N -acetylpenicillamine (SNAP) exerts antitumorigenic effects on TMZ-sensitive and TMZ-resistant (TMZ-R) glioma cells. Pretreatment with SNAP not only induced apoptosis, mitochondrial dysfunction, and hypoxia-inducing factor 1, but also resensitized TMZ-R GBM cells to TMZ through down-regulation of MGMT expression. SNAP acted principally through post-translational modification of p53, phosphorylated N-myc downstream regulated gene 1, and MGMT protein stability in TMZ-R GBM cells. Additionally, when applied together, SNAP and TMZ enhanced the inhibition of tumor growth in vitro and in vivo . This study sheds new light on a potential strategy to overcome TMZ resistance in GBM and thus possesses the potential for prolonging survival of patients with GBM.-Tsai, C.-K., Huang, L.-C., Wu, Y.-P., Kan, I.-Y., Hueng, D.-Y. SNAP reverses temozolomide resistance in human glioblastoma multiforme cells through down-regulation of MGMT.
References: Stupp, R., Mason, W. P., van den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J., Belanger, K., Brandes, A. A., Marosi, C., Bogdahn, U., Curschmann, J. Janzer, R. C., Ludwin, S. K., Gorlia, T., Allgeier, A., Lacombe, D., Cairncross, J. G., Eisenhauer, E., and Mirimanoff, R. O. European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy GroupsNational Cancer Institute of Canada Clinical Trials Group. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987-996.
Hegi, M. E., Diserens, A. C., Gorlia, T., Hamou, M. F., de Tribolet, N., Weller, M., Kros, J. M., Hainfellner, J. A., Mason, W., Mariani, L., Bromberg, J. E., Hau, P., Mirimanoff, R. O., Cairncross, J. G., Janzer, R. C., and Stupp, R. (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352, 997-1003.
Cabrini, G., Fabbri, E., Lo Nigro, C., Dechecchi, M. C., and Gambari, R. (2015) Regulation of expression of O6-methylguanine-DNA methyltransferase and the treatment of glioblastoma (Review). Int. J. Oncol. 47, 417-428.
Bocangel, D., Sengupta, S., Mitra, S., and Bhakat, K. K. (2009) p53-Mediated down-regulation of the human DNA repair gene O6-methylguanine-DNA methyltransferase (MGMT) via interaction with Sp1 transcription factor. Anticancer Res. 29, 3741-3750.
Weiler, M., Blaes, J., Pusch, S., Sahm, F., Czabanka, M., Luger, S., Bunse, L., Solecki, G., Eichwald, V. Jugold, M., Hodecker, S., Osswald, M., Meisner, C., Hielscher, T., Rübmann, P., Pfenning, P. N., Ronellenfitsch, M., Kempf, T., Schnölzer, M., Abdollahi, A., Lang, F., Bendszus, M., von Deimling, A., Winkler, F., Weller, M., Vajkoczy, P., Platten, M., and Wick, W. (2014) mTOR target NDRG1 confers MGMT-dependent resistance to alkylating chemotherapy. Proc. Natl. Acad. Sci. USA 111, 409-414.
Moncada, S., Palmer, R. M., and Higgs, E. A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142.
Michel, T., and Feron, O. (1997) Nitric oxide synthases: which, where, how, and why? J. Clin. Invest. 100, 2146-2152.
Singh, S., and Gupta, A. K. (2011) Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother. Pharmacol. 67, 1211-1224.
Mocellin, S., Bronte, V., and Nitti, D. (2007) Nitric oxide, a double edged sword in cancer biology: searching for therapeutic opportunities. Med. Res. Rev. 27, 317-352.
Leung, E. L., Fraser, M., Fiscus, R. R., and Tsang, B. K. (2008) Cisplatin alters nitric oxide synthase levels in human ovarian cancer cells: involvement in p53 regulation and cisplatin resistance. Br. J. Cancer 98, 1803-1809.
Janssens, M. Y., Verovski, V. N., Van den Berge, D. L., Monsaert, C., and Storme, G. A. (1999) Radiosensitization of hypoxic tumour cells by S-nitroso-N-acetylpenicillamine implicates a bioreductive mechanism of nitric oxide generation. Br. J. Cancer 79, 1085-1089.
Aranda, E., López-Pedrera, C., De La Haba-Rodriguez, J. R., and Rodriguez-Ariza, A. (2012) Nitric oxide and cancer: the emerging role of S-nitrosylation. Curr. Mol. Med. 12, 50-67.
Riganti, C., Miraglia, E., Viarisio, D., Costamagna, C., Pescarmona, G., Ghigo, D., and Bosia, A. (2005) Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux. Cancer Res. 65, 516-525.
Hickok, J. R., Sahni, S., Mikhed, Y., Bonini, M. G., and Thomas, D. D. (2011) Nitric oxide suppresses tumor cell migration through N-Myc downstream-regulated gene-1 (NDRG1) expression: role of chelatable iron. J. Biol. Chem. 286, 41413-41424.
Tsai, C. K., Huang, L. C., Tsai, W. C., Huang, S. M., Lee, J. T., and Hueng, D. Y. (2018) Overexpression of PLOD3 promotes tumor progression and poor prognosis in gliomas. Oncotarget 9, 15705-15720.
Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S., and Tannenbaum, S. R. (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126, 131-138.
El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell. 75, 817-825.
Huang, S. M., Schönthal, A. H., and Stallcup, M. R. (2001) Enhancement of p53-dependent gene activation by the transcriptional coactivator Zac1. Oncogene 20, 2134-2143.
Esteller, M., Garcia-Foncillas, J., Andion, E., Goodman, S. N., Hidalgo, O. F., Vanaclocha, V., Baylin, S. B., and Herman, J. G. (2000) Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N. Engl. J. Med. 343, 1350-1354.
Tang, Z., Li, C., Kang, B., Gao, G., Li, C., and Zhang, Z. (2017) GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 45 (W1), W98-W102.
Vieira, H., and Kroemer, G. (2003) Mitochondria as targets of apoptosis regulation by nitric oxide. IUBMB Life 55, 613-616.
Poyton, R., and Hendrickson, M. (2015) Crosstalk between nitric oxide and hypoxia-inducible factor signaling pathways: an update. Res. Rep. Biochem. 5, 147-161.
Jahani-Asl, A., and Bonni, A. (2013) iNOS: a potential therapeutic target for malignant glioma. Curr. Mol. Med. 13, 1241-1249.
Ookawa, S., Wanibuchi, M., Kataoka-Sasaki, Y., Sasaki, M., Oka, S., Ohtaki, S., Noshiro, S., Komatsu, K., Akiyama, Y., Mikami, T., Mikuni, N., Kocsis, J. D., and Honmou, O. (2018) Digital polymerase chain reaction quantification of SERPINA1 predicts prognosis in high-grade glioma. World Neurosurg. 111, e783-e789.
Xu, S., Shao, Q. Q., Sun, J. T., Yang, N., Xie, Q., Wang, D. H., Huang, Q. B., Huang, B., Wang, X. Y., Li, X. G., and Qu, X. (2013) Synergy between the ectoenzymes CD39 and CD73 contributes to adenosinergic immunosuppression in human malignant gliomas. Neuro-oncol. 15, 1160-1172.
Salimian Rizi, B., Achreja, A., and Nagrath, D. (2017) Nitric oxide: the forgotten child of tumor metabolism. Trends Cancer 3, 659-672.
Dai, C., and Gu, W. (2010) p53 post-translational modification: deregulated in tumorigenesis. Trends Mol. Med. 16, 528-536.
Brüne, B., and Schneiderhan, N. (2003) Nitric oxide evoked p53-accumulation and apoptosis. Toxicol. Lett. 139, 119-123.
Kitamura, Y., Kamoshima, W., Shimohama, S., Nomura, Y., and Taniguchi, T. (1998) Nitric oxide donor-induced p53-sensitive cell death is enhanced by Bcl-2 reduction in human neuroblastoma cells. Neurochem. Int. 32, 93-102.
Wang, X., Michael, D., de Murcia, G., and Oren, M. (2002) p53 activation by nitric oxide involves down-regulation of Mdm2. J. Biol. Chem. 277, 15697-15702.
Schneiderhan, N., Budde, A., Zhang, Y., and Brüne, B. (2003) Nitric oxide induces phosphorylation of p53 and impairs nuclear export. Oncogene 22, 2857-2868.
Kitagaki, J., Yang, Y., Saavedra, J. E., Colburn, N. H., Keefer, L. K., and Perantoni, A. O. (2009) Nitric oxide prodrug JS-K inhibits ubiquitin E1 and kills tumor cells retaining wild-type p53. Oncogene 28, 619-624.
Van Meir, E. G., Kikuchi, T., Tada, M., Li, H., Diserens, A. C., Wojcik, B. E., Huang, H. J., Friedmann, T., de Tribolet, N., and Cavenee, W. K. (1994) Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Res. 54, 649-652.
Kang, K. B., Zhu, C., Yong, S. K., Gao, Q., and Wong, M. C. (2009) Enhanced sensitivity of celecoxib in human glioblastoma cells: induction of DNA damage leading to p53-dependent G1 cell cycle arrest and autophagy. Mol. Cancer 8, 66.
Bouaoun, L., Sonkin, D., Ardin, M., Hollstein, M., Byrnes, G., Zavadil, J., and Olivier, M. (2016) TP53 variations in human cancers: new lessons from the IARC TP53 database and genomics data. Hum. Mutat. 37, 865-876.
Chao, J. I., Kuo, P. C., and Hsu, T. S. (2004) Down-regulation of survivin in nitric oxide-induced cell growth inhibition and apoptosis of the human lung carcinoma cells. J. Biol. Chem. 279, 20267-20276.
Garbán, H. J., and Bonavida, B. (2001) Nitric oxide inhibits the transcription repressor Yin-Yang 1 binding activity at the silencer region of the Fas promoter: a pivotal role for nitric oxide in the up-regulation of Fas gene expression in human tumor cells. J. Immunol. 167, 75-81.
Binabaj, M. M., Bahrami, A., Shahid Sales, S., Joodi, M., Joudi Mashhad, M., Hassanian, S. M., Anvari, K., and Avan, A. (2018) The prognostic value of MGMT promoter methylation in glioblastoma: a meta-analysis of clinical trials. J. Cell. Physiol. 233, 378-386.
Srivenugopal, K. S., Shou, J., Mullapudi, S. R., Lang, F. F., Jr., Rao, J. S., and Ali-Osman, F. (2001) Enforced expression of wild-type p53 curtails the transcription of the O(6)-methylguanine-DNA methyltransferase gene in human tumor cells and enhances their sensitivity to alkylating agents. Clin. Cancer Res. 7, 1398-1409.
Bobustuc, G. C., Baker, C. H., Limaye, A., Jenkins, W. D., Pearl, G., Avgeropoulos, N. G., and Konduri, S. D. (2010) Levetiracetam enhances p53-mediated MGMT inhibition and sensitizes glioblastoma cells to temozolomide. Neuro-oncol. 12, 917-927.
Natsume, A., Wakabayashi, T., Ishii, D., Maruta, H., Fujii, M., Shimato, S., Ito, M., and Yoshida, J. (2008) A combination of IFN-beta and temozolomide in human glioma xenograft models: implication of p53-mediated MGMT downregulation. Cancer Chemother. Pharmacol. 61, 653-659.
Harris, L. C., Potter, P. M., Tano, K., Shiota, S., Mitra, S., and Brent, T. P. (1991) Characterization of the promoter region of the human O6-methylguanine-DNA methyltransferase gene. Nucleic Acids Res. 19, 6163-6167.
Hara, E., Takahashi, K., Tominaga, T., Kumabe, T., Kayama, T., Suzuki, H., Fujita, H., Yoshimoto, T., Shirato, K., and Shibahara, S. (1996) Expression of heme oxygenase and inducible nitric oxide synthase mRNA in human brain tumors. Biochem. Biophys. Res. Commun. 224, 153-158.
Loibl, S., Buck, A., Strank, C., von Minckwitz, G., Roller, M., Sinn, H. P., Schini-Kerth, V., Solbach, C., Strebhardt, K., and Kaufmann, M. (2005) The role of early expression of inducible nitric oxide synthase in human breast cancer. Eur. J. Cancer 41, 265-271.
Ekmekcioglu, S., Ellerhorst, J. A., Prieto, V. G., Johnson, M. M., Broemeling, L. D., and Grimm, E. A. (2006) Tumor iNOS predicts poor survival for stage III melanoma patients. Int. J. Cancer 119, 861-866.
Eyler, C. E., Wu, Q., Yan, K., MacSwords, J. M., Chandler-Militello, D., Misuraca, K. L., Lathia, J. D., Forrester, M. T., Lee, J., Stamler, J. S., Goldman, S. A., Bredel, M., McLendon, R. E., Sloan, A. E., Hjelmeland, A. B., and Rich, J. N. (2011) Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell 146, 53-66.
Matsumoto, H., Takahashi, A., and Ohnishi, T. (2007) Nitric oxide radicals choreograph a radioadaptive response. Cancer Res. 67, 8574-8579.
Kim, R. K., Suh, Y., Cui, Y. H., Hwang, E., Lim, E. J., Yoo, K. C., Lee, G. H., Yi, J. M., Kang, S. G., and Lee, S. J. (2013) Fractionated radiation-induced nitric oxide promotes expansion of glioma stem-like cells. Cancer Sci. 104, 1172-1177.
Chang, K., Lee, S. J., Cheong, I., Billiar, T. R., Chung, H. T., Han, J. A., Kwon, Y. G., Ha, K. S., and Kim, Y. M. (2004) Nitric oxide suppresses inducible nitric oxide synthase expression by inhibiting post-translational modification of IkappaB. Exp. Mol. Med. 36, 311-324.
Lu, G., Zhang, R., Geng, S., Peng, L., Jayaraman, P., Chen, C., Xu, F., Yang, J., Li, Q., Zheng, H., Shen, K., Wang, J., Liu, X., Wang, W., Zheng, Z., Qi, C. F., Si, C., He, J. C., Liu, K., Lira, S. A., Sikora, A. G., Li, L., and Xiong, H. (2015) Myeloid cell-derived inducible nitric oxide synthase suppresses M1 macrophage polarization. Nat. Commun. 6, 6676.
فهرسة مساهمة: Keywords: HIF-1; NDRG1; S-nitroso-N-acetylpenicillamine; apoptosis
المشرفين على المادة: 0 (Antineoplastic Agents, Alkylating)
0 (Biomarkers)
0 (Enzyme Inhibitors)
0 (Tumor Suppressor Proteins)
79032-48-7 (S-Nitroso-N-Acetylpenicillamine)
EC 2.1.1.- (DNA Modification Methylases)
EC 2.1.1.63 (MGMT protein, human)
EC 6.5.1.- (DNA Repair Enzymes)
YF1K15M17Y (Temozolomide)
تواريخ الأحداث: Date Created: 20191115 Date Completed: 20200626 Latest Revision: 20220623
رمز التحديث: 20221213
DOI: 10.1096/fj.201901021RR
PMID: 31725331
قاعدة البيانات: MEDLINE
الوصف
تدمد:1530-6860
DOI:10.1096/fj.201901021RR