Clostridium botulinum neurotoxin A induces apoptosis and mitochondrial oxidative stress via activation of TRPM2 channel signaling pathway in neuroblastoma and glioblastoma tumor cells

References

• Ji X, Wang H, Zhu J, et al. Correlation of Nrf2 and HIF-1α in glioblastoma and their relationships to clinicopathologic features and survival. Neurol Res. 2013;35(10):1044–1050.
   PubMed Web of Science ®Google Scholar
• Bhatti P, Stewart PA, Hutchinson A, et al. Lead exposure, polymorphisms in genes related to oxidative stress, and risk of adult brain tumors. Cancer Epidemiol Biomarkers Prev. 2009;18(6):1841–1848.
   PubMed Web of Science ®Google Scholar
• Paquette K, Coltin H, Boivin A, et al. Cancer risk in children and young adults born preterm: A systematic review and meta-analysis. PLoS One. 2019;14(1):e0210366.
   PubMed Web of Science ®Google Scholar
• Incekara F, Koene S, Vincent A, et al. Association between supratotal glioblastoma resection and patient survival: a systematic review and meta-analysis. World Neurosurg. 2019;127:617–624.
   PubMed Web of Science ®Google Scholar
• Eyüpoglu IY, Savaskan NE. Epigenetics in brain tumors: HDACs take center stage. Curr Neuropharmacol. 2016;14(1):48–54.
   PubMed Web of Science ®Google Scholar
• Nazıroğlu M. New molecular mechanisms on the activation of TRPM2 channels by oxidative stress and ADP-ribose. Neurochem Res. 2007;32(11):1990–2001.
   PubMed Web of Science ®Google Scholar
• Nazıroğlu M, Tokat S, Demirci S. Role of melatonin on electromagnetic radiation-induced oxidative stress and Ca2+ signaling molecular pathways in breast cancer. J Recept Signal Transduct Res. 2012;32(6):290–297.
   PubMed Web of Science ®Google Scholar
• Ishii M, Oyama A, Hagiwara T, et al. Facilitation of H2O2-induced A172 human glioblastoma cell death by insertion of oxidative stress-sensitive TRPM2 channels. Anticancer Res. 2007;27(6B):3987–3992.
   PubMed Web of Science ®Google Scholar
• Hantute-Ghesquier A, Haustrate A, Prevarskaya N, et al. TRPM family channels in cancer. Pharmaceuticals (Basel). 2018;11(2):58.
   Google Scholar
• Chen SJ, Zhang W, Tong Q, et al. Role of TRPM2 in cell proliferation and susceptibility to oxidative stress. Am J Physiol, Cell Physiol. 2013;304(6):C548–560.
   PubMed Web of Science ®Google Scholar
• Hara Y, Wakamori M, Ishii M, et al. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell. 2002;9(1):163–173.
   PubMed Web of Science ®Google Scholar
• Nazıroğlu M, Lückhoff A. A calcium influx pathway regulated separately by oxidative stress and ADP-Ribose in TRPM2 channels: single channel events. Neurochem Res. 2008;33(7):1256–1262.
   PubMed Web of Science ®Google Scholar
• Gökçe Kütük S, Gökçe G, Kütük M, et al. Curcumin enhances cisplatin-induced human laryngeal squamous cancer cell death through activation of TRPM2 channel and mitochondrial oxidative stress. Sci Rep. 2019;9(1):17784.
   PubMedGoogle Scholar
• Ertilav K, Nazıroğlu M, Ataizi ZS, et al. Selenium enhances the apoptotic efficacy of docetaxel through activation of TRPM2 channel in DBTRG glioblastoma cells. Neurotox Res. 2019;35(4):797–808.
   PubMed Web of Science ®Google Scholar
• Öz A, Çelik Ö. Curcumin inhibits oxidative stress-induced TRPM2 channel activation, calcium ion entry and apoptosis values in SH-SY5Y neuroblastoma cells: Involvement of transfection procedure. Mol Membr Biol. 2016;33(3-5):76–88.
   PubMed Web of Science ®Google Scholar
• Li X, Jiang LH. A critical role of the transient receptor potential melastatin 2 channel in a positive feedback mechanism for reactive oxygen species-induced delayed cell death. J Cell Physiol. 2019;234(4):3647–3660.
   PubMed Web of Science ®Google Scholar
• Özkaya D, Nazıroğlu M. Curcumin diminishes cisplatin-induced apoptosis and mitochondrial oxidative stress through inhibition of TRPM2 channel signaling pathway in mouse optic nerve. J Recept Signal Transduct Res. 2020;5:1–12.
   Google Scholar
• Sillar JR, Germon ZP, DeIuliis GN, et al. The role of reactive oxygen species in acute myeloid leukaemia. Int J Mol Sci. 2019;20(23):E6003.
   PubMed Web of Science ®Google Scholar
• Patil S, Willett O, Thompkins T, et al. Botulinum toxin: Pharmacology and therapeutic roles in pain states. Curr Pain Headache Rep. 2016;20(3):15.
   PubMed Web of Science ®Google Scholar
• Oh HM, Chung ME. Botulinum toxin for neuropathic pain: a review of the literature. Toxins (Basel). 2015;7(8):3127–3154.
   PubMed Web of Science ®Google Scholar
• Karsenty G, Rocha J, Chevalier S, et al. Botulinum toxin type A inhibits the growth of LNCaP human prostate cancer cells in vitro and in vivo. Prostate. 2009;69(11):1143–1150.
   PubMed Web of Science ®Google Scholar
• Bandala C, Perez-Santos JL, Lara-Padilla E, et al. Effect of botulinum toxin A on proliferation and apoptosis in the T47D breast cancer cell line. Asian Pac J Cancer Prev. 2013;14(2):891–894.
   PubMedGoogle Scholar
• Rust A, Leese C, Binz T, et al. Botulinum neurotoxin type C protease induces apoptosis in differentiated human neuroblastoma cells. Oncotarget. 2016;7(22):33220–33228.
   PubMedGoogle Scholar
• Uğuz AC, Öz A, Nazıroğlu M. Curcumin inhibits apoptosis by regulating intracellular calcium release, reactive oxygen species and mitochondrial depolarization levels in SH-SY5Y neuronal cells. J Recept Signal Transduct Res. 2016;36(4):395–401.
   PubMed Web of Science ®Google Scholar
• Oz A, Celik O, Ovey IS. Effects of different doses of curcumin on apoptosis, mitochondrial oxidative stress and calcium influx in DBTRG glioblastoma cells. J Cell Neurosci Oxid Stress. 2017;9:617–629.
   Google Scholar
• Yowler BC, Kensinger RD, Schengrund CL. Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J Biol Chem. 2002;277(36):32815–32819.
   PubMed Web of Science ®Google Scholar
• Rieger AM, Nelson KL, Konowalchuk JD, et al. Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death. J Vis Exp. 2011;50:2597.
   PubMed Web of Science ®Google Scholar
• Joshi DC, Bakowska JC. Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. J Vis Exp. 2011;51:2704.
   Google Scholar
• Carrasco C, Rodríguez BA, Pariente JA. Melatonin as a stabilizer of mitochondrial function: Role in diseases and aging. Turk J Biol. 2015;39:822–831.
   Web of Science ®Google Scholar
• Carrasco C, Nazıroǧlu M, Rodríguez AB, et al. Neuropathic pain: Delving into the oxidative origin and the possible implication of transient receptor potential channels. Front Physiol. 2018;9:95.
   PubMed Web of Science ®Google Scholar
• Nur G, Nazıroğlu M, Deveci HA. Synergic prooxidant, apoptotic and TRPV1 channel activator effects of alpha-lipoic acid and cisplatin in MCF-7 breast cancer cells. J Recept Signal Transduct Res. 2017;37(6):569–577.
   PubMed Web of Science ®Google Scholar
• Kan H, Hu W, Wang Y, et al. NADPH oxidase-derived production of reactive oxygen species is involved in learning and memory impairments in 16-month-old female rats. Mol Med Rep. 2015;12(3):4546–4553.
   PubMed Web of Science ®Google Scholar
• Kowluru RA, Kowluru A, Veluthakal R, et al. TIAM1-RAC1 signalling axis-mediated activation of NADPH oxidase-2 initiates mitochondrial damage in the development of diabetic retinopathy. Diabetologia. 2014;57(5):1047–1056.
   PubMed Web of Science ®Google Scholar
• Bandala C, Terán-Melo JL, Anaya-Ruiz M, et al. Effect of botulinum neurotoxin type A (BoNTA) on the morphology and viability of 3T3 murine fibroblasts. Int J Clin Exp Pathol. 2015;8(8):9458–9462.
   PubMed Web of Science ®Google Scholar
• Thirunavukkarasusx N, Ghosal KJ, Kukreja R, et al. Microarray analysis of differentially regulated genes in human neuronal and epithelial cell lines upon exposure to type A botulinum neurotoxin. Biochem Biophys Res Commun. 2011;405(4):684–690.
   PubMed Web of Science ®Google Scholar
• Gorgal T, Charrua A, Silva JF, et al. Expression of apoptosis-regulating genes in the rat prostate following botulinum toxin type A injection. BMC Urol. 2012;12:1.
   PubMed Web of Science ®Google Scholar
• Nam HJ, Kang JK, Chang JS, et al. Cells transformed by PLC-gamma 1 overexpression are highly sensitive to clostridium difficile toxin A-induced apoptosis and mitotic inhibition. J Microbiol Biotechnol. 2012;22(1):50–57.
   PubMed Web of Science ®Google Scholar
• Tegenge MA, Böhnel H, Gessler F, et al. Neurotransmitter vesicle release from human model neurons (NT2) is sensitive to botulinum toxin A. Cell Mol Neurobiol. 2012;32(6):1021–1029.
   PubMed Web of Science ®Google Scholar
• Proietti S, Nardicchi V, Porena M, et al. Botulinum toxin type-A toxin activity on prostate cancer cell lines. Urologia. 2012;79(2):135–141.
   PubMedGoogle Scholar
• Berliocchi L, Fava E, Leist M, et al. Botulinum neurotoxin C initiates two different programs for neurite degeneration and neuronal apoptosis. J Cell Biol. 2005;168(4):607–618.
   PubMed Web of Science ®Google Scholar
• Kumar R, Zhou Y, Ghosal K, et al. Anti-apoptotic activity of hemagglutinin-33 and botulinum neurotoxin and its implications to therapeutic and countermeasure issues. Biochem Biophys Res Commun. 2012;417(2):726–731.
   PubMed Web of Science ®Google Scholar