Endoplasmic reticulum stress-inducing drugs sensitize glioma cells to temozolomide through downregulation of MGMT, MPG, and Rad51

Neuro-Oncology

Volumn 18, Issue 8, 2016, Pages 1109-1119

  Xipell, Enric ^a   Aragón, Tomás ^b   Martínez Velez, Naiara ^a   Vera, Beatriz ^a   Idoate, Miguel Angel ^c   Martínez Irujo, Juan José ^d   Garzón, Antonia García ^d   Gonzalez Huarriz, Marisol ^a   Acanda, Arlet M ^a   Jones, Chris ^e   Lang, Frederick F ^f   Fueyo, Juan ^f   Gomez Manzano, Candelaria ^f   Alonso, Marta M ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c Universidad Pública de Navarra   (Spain)

^d UNIVERSITY OF NAVARRA   (Spain)

^e INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

DNA damage; ER stress; Glioblastoma; Salinomycin; Temozolomide

Indexed keywords

DNA GLYCOSYLTRANSFERASE; HISTONE H2AX; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; N METHYLPURINE DNA GLYCOSYLASE; RAD51 PROTEIN; SALINOMYCIN; TEMOZOLOMIDE; THAPSIGARGIN; UNCLASSIFIED DRUG; ALKYLATING AGENT; DACARBAZINE; DNA LIGASE; DNA METHYLTRANSFERASE; DNA-3-METHYLADENINE GLYCOSIDASE II; MGMT PROTEIN, HUMAN; PYRAN DERIVATIVE; TUMOR SUPPRESSOR PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CHEMOSENSITIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; LONG TERM SURVIVAL; MOUSE; MTT ASSAY; MULTIPLE CYCLE TREATMENT; NONHUMAN; OVERALL SURVIVAL; PROTEIN EXPRESSION; TREATMENT DURATION; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN TUMOR; CELL SURVIVAL; DRUG EFFECTS; GLIOBLASTOMA; METABOLISM; SURVIVAL ANALYSIS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; DACARBAZINE; DNA DAMAGE; DNA GLYCOSYLASES; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; GLIOBLASTOMA; HUMANS; MICE; PYRANS; RAD51 RECOMBINASE; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEINS;

EID: 84982124664     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/now022     Document Type: Article

References (44)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987-996
2. Reardon DA, Rich JN, Friedman HS, et al. Recent advances in the treatment of malignant astrocytoma. J Clin Oncol. 2006;24(8): 1253-1265
3. Stupp R, Gander M, Leyvraz S, et al. Current and future developments in the use of temozolomide for the treatment of brain tumours. Lancet Oncol. 2001;2(9):552-560
4. Ochs K, Kaina B. Apoptosis induced by DNA damage O6-methylguanine is Bcl-2 and caspase-9/3 regulated and Fas/ caspase-8 independent. Cancer Res. 2000;60(20):5815-5824
5. Agnihotri S, Gajadhar AS, Ternamian C, et al. Alkylpurine-DNA-N-glycosylase confers resistance to temozolomide in xenograft models of glioblastoma multiforme and is associated with poor survival in patients. J Clin Invest. 2012;122(1):253-266
6. Hegi ME, Diserens AC, Godard S, et al. Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res. 2004; 10(6):1871-1874
7. Clarke HJ, Chambers JE, Liniker E, et al. Endoplasmic reticulum stress in malignancy. Cancer Cell. 2014;25(5):563-573
8. Vincenz L, Jager R, O'Dwyer M, et al. Endoplasmic reticulum stress and the unfolded protein response: targeting the Achilles heel of multiple myeloma. Mol Cancer Ther. 2013;12(6):831-843
9. Tsai YC, Weissman AM. The unfolded protein response, degradation from endoplasmic reticulum and cancer. Genes Cancer. 2010;1(7):764-778
10. Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci. 2007; 32(10):469-476
11. Bonifacino JS, Weissman AM. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol. 1998;14:19-57
12. Yamamori T, Meike S, Nagane M, et al. ER stress suppresses DNA double-strand break repair and sensitizes tumor cells to ionizing radiation by stimulating proteasomal degradation of Rad51. FEBS Lett. 2013;587(20):3348-3353
13. Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138(4):645-659
14. Li T, Su L, Zhong N, et al. Salinomycin induces cell death with autophagy through activation of endoplasmic reticulum stress in human cancer cells. Autophagy. 2013;9(7):1057-1068
15. Yue W, Hamai A, Tonelli G, et al. Inhibition of the autophagic flux by salinomycin in breast cancer stem-like/progenitor cells interferes with their maintenance. Autophagy. 2013;9(5): 714-729
16. Kim JH, Yoo HI, Kang HS, et al. Salinomycin sensitizes antimitotic drugs-treated cancer cells by increasing apoptosis via the prevention of G2 arrest. Biochem Biophys Res Commun. 2012; 418(1):98-103
17. Boehmerle W, Endres M. Salinomycin induces calpain and cytochrome c-mediated neuronal cell death. Cell Death Dis. 2011;2:e168
18. Zhou J, Li P, Xue X, et al. Salinomycin induces apoptosis in cisplatin-resistant colorectal cancer cells by accumulation of reactive oxygen species. Toxicol Lett. 2013;222(2):139-145
19. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64(19):7011-7021
20. Mahoney DJ, Lefebvre C, Allan K, et al. Virus-tumor interactome screen reveals ER stress response can reprogram resistant cancers for oncolytic virus-triggered caspase-2 cell death. Cancer Cell. 2011;20(4):443-456
21. Alonso MM, Jiang H, Yokoyama T, et al. Delta-24-RGD in combination with RAD001 induces enhanced anti-glioma effect via autophagic cell death. Mol Ther. 2008;16(3):487-493
22. Lal S, Lacroix M, Tofilon P, et al. An implantable guide-screw system for brain tumor studies in small animals. J Neurosurg. 2000;92(2):326-333
23. Thastrup O, Cullen PJ, Drobak BK, et al. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A. 1990;87(7):2466-2470
24. Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8(4):445-544
25. Mitani M, Yamanishi T, Miyazaki Y, et al. Salinomycin effects on mitochondrial ion translocation and respiration. Antimicrob Agents Chemother. 1976;9(4):655-660
26. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334(6059): 1081-1086
27. Oslowski CM, Urano F. Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods Enzymol. 2011;490:71-92
28. Aragon T, van Anken E, Pincus D, et al. Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature. 2009; 457(7230):736-740
29. Torres-Quiroz F, Garcia-Marques S, Coria R, et al. The activity of yeast Hog1 MAPK is required during endoplasmic reticulum stress induced by tunicamycin exposure. J Biol Chem. 2010; 285(26):20088-20096
30. Kolb PS, Ayaub EA, Zhou W, et al. The therapeutic effects of 4-phenylbutyric acid in maintaining proteostasis. Int J Biochem Cell Biol. 2015;61:45-52
31. Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010; 70(2):440-446
32. Lagas JS, Sparidans RW, vanWaterschoot RA, et al. P-glycoprotein limits oral availability, brain penetration, and toxicity of an anionic drug, the antibiotic salinomycin. Antimicrob Agents Chemother. 2008;52(3):1034-1039
33. Wang M, Kaufman RJ. The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat Rev Cancer. 2014;14(9):581-597
34. Pyrko P, Schonthal AH, Hofman FM, et al. The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res. 2007;67(20): 9809-9816
35. Zhang LH, Yang XL, Zhang X, et al. Association of elevated GRP78 expression with increased astrocytoma malignancy via Akt and ERK pathways. Brain Res. 2011;1371:23-31
36. Lee HK, Xiang C, Cazacu S, et al. GRP78 is overexpressed in glioblastomas and regulates glioma cell growth and apoptosis. Neuro Oncol. 2008;10(3):236-243
37. Lin CJ, Lee CC, Shih YL, et al. Inhibition of mitochondria-and endoplasmic reticulum stress-mediated autophagy augments temozolomide-induced apoptosis in glioma cells. PLoS One. 2012;7(6):e38706
38. Yoshimoto K, Mizoguchi M, Hata N, et al. Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Front Oncol. 2012;2: 186
39. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005; 352(10):997-1003
40. Liu X, Han EK, Anderson M, et al. Acquired resistance to combination treatment with temozolomide and ABT-888 is mediated by both base excision repair and homologous recombination DNA repair pathways. Mol Cancer Res. 2009; 7(10):1686-1692
41. Short SC, Giampieri S, Worku M, et al. Rad51 inhibition is an effective means of targeting DNA repair in glioma models and CD133+ tumor-derived cells. Neuro Oncol. 2011;13(5):487-499
42. Costanzo V. Brca2, Rad51 and Mre11: performing balancing acts on replication forks. DNA Repair (Amst). 2011;10(10):1060-1065
43. Shinsato Y, Furukawa T, Yunoue S, et al. Reduction of MLH1 and PMS2 confers temozolomide resistance and is associated with recurrence of glioblastoma. Oncotarget. 2013;4(12):2261-2270
44. Agnihotri S, Burrell K, Buczkowicz P, et al. ATM regulates 3-methylpurine-DNA glycosylase and promotes therapeutic resistance to alkylating agents. Cancer Discov. 2014;4(10): 1198-1213