Receptor Interacting Protein 3 is Required for Arsenite-mediated Necroptosis
Keywords:
Arsenite, Heat shock protein 90, programmed necrosis, receptor interacting protein 3Abstract
Arsenic compounds such as sodium arsenite (SA) and arsenic trioxide (ATO) are toxic to human. Primarily, we pursued to outline the cell death modes caused by arsenic compounds and to address what proteins would be responsible for arsenite-induced cytotoxicity. Both SA and ATO substantially exhibited cytotoxic activity in L929 cells. Necrostatin-1 (Nec-1) treatment significantly protected cell death mediated by arsenic compounds, suggesting that cells are committed to die in a programmed necrotic way. A geldanamycin analog DMAG destabilized receptor interacting protein 3 (RIP3) and concomitantly protected cells from SA toxicity. Using interfering RNAs, we eventually found that RIP3 was responsible for its antagonizing effects on SA. Therefore, it is proposed that arsenic compounds execute necroptotic cell death of L929 via a RIP3 dependent pathway.
References
. P. B. Tchounwou, J. A. Centeno, and A. K. Patlolla, "Arsenic toxicity, mutagenesis, and carcinogenesis--a health risk assessment and management approach," Mol Cell Biochem, vol. 255, pp. 47-55, Jan. 2004.
. S. Kann, C. Estes, J. F. Reichard, M. Y. Huang, M. A. Sartor, S. Schwemberger, et al., "Butylhydroquinone protects cells genetically deficient in glutathione biosynthesis from arsenite-induced apoptosis without significantly changing their prooxidant status," Toxicol Sci, vol. 87, pp. 365-84, Oct. 2005.
. A. H. Smith, C. Hopenhayn-Rich, M. N. Bates, H. M. Goeden, I. Hertz-Picciotto, H. M. Duggan, et al., "Cancer risks from arsenic in drinking water," Environ Health Perspect, vol. 97, pp. 259-67, Jul. 1992.
. T. G. Rossman, A. N. Uddin, and F. J. Burns, "Evidence that arsenite acts as a cocarcinogen in skin cancer," Toxicol Appl Pharmacol, vol. 198, pp. 394-404, Aug 1. 2004.
. A. Hernandez-Zavala, E. Cordova, L. M. Del Razo, M. E. Cebrian, and E. Garrido, "Effects of arsenite on cell cycle progression in a human bladder cancer cell line," Toxicology, vol. 207, pp. 49-57, Feb 1. 2005.
. M. J. McCabe, Jr., K. P. Singh, S. A. Reddy, B. Chelladurai, J. G. Pounds, J. J. Reiners, Jr., et al., "Sensitivity of myelomonocytic leukemia cells to arsenite-induced cell cycle disruption, apoptosis, and enhanced differentiation is dependent on the inter-relationship between arsenic concentration, duration of treatment, and cell cycle phase," J Pharmacol Exp Ther, vol. 295, pp. 724-33, Nov. 2000.
. M. Marin, S. Golem, K. M. Rose, S. L. Kozak, and D. Kabat, "Human immunodeficiency virus type 1 Vif functionally interacts with diverse APOBEC3 cytidine deaminases and moves with them between cytoplasmic sites of mRNA metabolism," J Virol, vol. 82, pp. 987-98, Jan. 2008.
. P. Zhang, "On arsenic trioxide in the clinical treatment of acute promyelocytic leukemia," Leuk Res Rep, vol. 7, pp. 29-32, 2017.
. J. McCafferty-Grad, N. J. Bahlis, N. Krett, T. M. Aguilar, I. Reis, K. P. Lee, et al., "Arsenic trioxide uses caspase-dependent and caspase-independent death pathways in myeloma cells," Mol Cancer Ther, vol. 2, pp. 1155-64, Nov. 2003.
. R. Chowdhury, S. Chowdhury, P. Roychoudhury, C. Mandal, and K. Chaudhuri, "Arsenic induced apoptosis in malignant melanoma cells is enhanced by menadione through ROS generation, p38 signaling and p53 activation," Apoptosis, vol. 14, pp. 108-23, Jan. 2009.
. X. Li, X. Ding, and T. E. Adrian, "Arsenic trioxide induces apoptosis in pancreatic cancer cells via changes in cell cycle, caspase activation, and GADD expression," Pancreas, vol. 27, pp. 174-9, Aug. 2003.
. Y. F. Mu, Y. H. Chen, M. M. Chang, Y. C. Chen, and B. M. Huang, "Arsenic compounds induce apoptosis through caspase pathway activation in MA-10 Leydig tumor cells," Oncol Lett, vol. 18, pp. 944-954, Jul. 2019.
. Y. Akao, Y. Nakagawa, and K. Akiyama, "Arsenic trioxide induces apoptosis in neuroblastoma cell lines through the activation of caspase 3 in vitro," FEBS Lett, vol. 455, pp. 59-62, Jul 16. 1999.
. W. Qian, J. Liu, J. Jin, W. Ni, and W. Xu, "Arsenic trioxide induces not only apoptosis but also autophagic cell death in leukemia cell lines via up-regulation of Beclin-1," Leuk Res, vol. 31, pp. 329-39, Mar. 2007.
. W. Zhang, K. Ohnishi, K. Shigeno, S. Fujisawa, K. Naito, S. Nakamura, et al., "The induction of apoptosis and cell cycle arrest by arsenic trioxide in lymphoid neoplasms," Leukemia, vol. 12, pp. 1383-91, Sep. 1998.
. T. Suzuki, K. Ishibashi, A. Yumoto, K. Nishio, and Y. Ogasawara, "Utilization of arsenic trioxide as a treatment of cisplatin-resistant non-small cell lung cancer PC-9/CDDP and PC-14/CDDP cells," Oncol Lett, vol. 10, pp. 805-809, Aug. 2015.
. C. Scholz, T. Wieder, L. Starck, F. Essmann, K. Schulze-Osthoff, B. Dorken, et al., "Arsenic trioxide triggers a regulated form of caspase-independent necrotic cell death via the mitochondrial death pathway," Oncogene, vol. 24, pp. 1904-13, Mar 10. 2005.
. V. Selvaraj, M. Y. Armistead, M. Cohenford, and E. Murray, "Arsenic trioxide (As(2)O(3)) induces apoptosis and necrosis mediated cell death through mitochondrial membrane potential damage and elevated production of reactive oxygen species in PLHC-1 fish cell line," Chemosphere, vol. 90, pp. 1201-9, Jan. 2013.
. G. Majno and I. Joris, "Apoptosis, oncosis, and necrosis. An overview of cell death," Am J Pathol, vol. 146, pp. 3-15, Jan. 1995.
. S. L. Fink and B. T. Cookson, "Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells," Infect Immun, vol. 73, pp. 1907-16, Apr. 2005.
. D. E. Christofferson and J. Yuan, "Necroptosis as an alternative form of programmed cell death," Curr Opin Cell Biol, vol. 22, pp. 263-8, Apr. 2010.
. S. Y. Park, J. H. Shim, and Y. S. Cho, "Distinctive roles of receptor-interacting protein kinases 1 and 3 in caspase-independent cell death of L929," Cell Biochem Funct, vol. 32, pp. 62-9, Jan. 2014.
. A. Degterev, J. Hitomi, M. Germscheid, I. L. Ch'en, O. Korkina, X. Teng, et al., "Identification of RIP1 kinase as a specific cellular target of necrostatins," Nat Chem Biol, vol. 4, pp. 313-21, May. 2008.
. A. Degterev, J. L. Maki, and J. Yuan, "Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase," Cell Death Differ, vol. 20, p. 366, Feb. 2013.
. D. Tang, R. Kang, T. V. Berghe, P. Vandenabeele, and G. Kroemer, "The molecular machinery of regulated cell death," Cell Res, vol. 29, pp. 347-364, May. 2019.
. Y. S. Cho, S. Challa, D. Moquin, R. Genga, T. D. Ray, M. Guildford, et al., "Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation," Cell, vol. 137, pp. 1112-23, Jun 12. 2009.
. S. Fulda, A. M. Gorman, O. Hori, and A. Samali, "Cellular stress responses: cell survival and cell death," Int J Cell Biol, vol. 2010, p. 214074, 2010.
. A. Shrestha, I. Mehdizadeh Gohari, and B. A. McClane, "RIP1, RIP3, and MLKL Contribute to Cell Death Caused by Clostridium perfringens Enterotoxin," mBio, vol. 10, Dec 17. 2019.
. T. C. Tsou, S. C. Yeh, E. M. Tsai, F. Y. Tsai, H. R. Chao, and L. W. Chang, "Arsenite enhances tumor necrosis factor-alpha-induced expression of vascular cell adhesion molecule-1," Toxicol Appl Pharmacol, vol. 209, pp. 10-8, Nov 15. 2005.
. V. N. Ivanov, G. Wen, and T. K. Hei, "Sodium arsenite exposure inhibits AKT and Stat3 activation, suppresses self-renewal and induces apoptotic death of embryonic stem cells," Apoptosis, vol. 18, pp. 188-200, Feb. 2013.
. Y. H. Han, H. J. Moon, B. R. You, S. Z. Kim, S. H. Kim, and W. H. Park, "Effects of arsenic trioxide on cell death, reactive oxygen species and glutathione levels in different cell types," Int J Mol Med, vol. 25, pp. 121-8, Jan. 2010.
. Y. Sun, C. Wang, L. Wang, Z. Dai, and K. Yang, "Arsenic trioxide induces apoptosis and the formation of reactive oxygen species in rat glioma cells," Cell Mol Biol Lett, vol. 23, p. 13, 2018.
. S. Wang, Z. Geng, N. Shi, X. Li, and Z. Wang, "Dose-dependent effects of selenite (Se(4+)) on arsenite (As(3+))-induced apoptosis and differentiation in acute promyelocytic leukemia cells," Cell Death Dis, vol. 6, p. e1596, Jan 15. 2015.
. S. Park, H. Shin, and Y. Cho, "Shikonin induces programmed necrosis-like cell death through the formation of receptor interacting protein 1 and 3 complex," Food Chem Toxicol, vol. 55, pp. 36-41, May. 2013.
. J. Sosna, S. Voigt, S. Mathieu, A. Lange, L. Thon, P. Davarnia, et al., "TNF-induced necroptosis and PARP-1-mediated necrosis represent distinct routes to programmed necrotic cell death," Cell Mol Life Sci, vol. 71, pp. 331-48, Jan. 2014.
. M. S. Ricci and W. X. Zong, "Chemotherapeutic approaches for targeting cell death pathways," Oncologist, vol. 11, pp. 342-57, Apr. 2006.
. J. Lewis, A. Devin, A. Miller, Y. Lin, Y. Rodriguez, L. Neckers, et al., "Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation," J Biol Chem, vol. 275, pp. 10519-26, Apr 7. 2000.
. M. A. Kelliher, S. Grimm, Y. Ishida, F. Kuo, B. Z. Stanger, and P. Leder, "The death domain kinase RIP mediates the TNF-induced NF-kappaB signal," Immunity, vol. 8, pp. 297-303, Mar. 1998.
. N. Vanlangenakker, M. J. Bertrand, P. Bogaert, P. Vandenabeele, and T. Vanden Berghe, "TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex I and II members," Cell Death Dis, vol. 2, p. e230, 2011.
. Y. Cho, T. McQuade, H. Zhang, J. Zhang, and F. K. Chan, "RIP1-dependent and independent effects of necrostatin-1 in necrosis and T cell activation," PLoS One, vol. 6, p. e23209, 2011.
. Y. Fu, D. Wang, H. Wang, M. Cai, C. Li, X. Zhang, et al., "TSPO deficiency induces mitochondrial dysfunction, leading to hypoxia, angiogenesis, and a growth-promoting metabolic shift toward glycolysis in glioblastoma," Neuro Oncol, vol. 22, pp. 240-252, Feb 20. 2020.
. D. C. Ellinsworth, "Arsenic, reactive oxygen, and endothelial dysfunction," J Pharmacol Exp Ther, vol. 353, pp. 458-64, Jun. 2015.
. D. K. Jung, G. U. Bae, Y. K. Kim, S. H. Han, W. S. Choi, H. Kang, et al., "Hydrogen peroxide mediates arsenite activation of p70(s6k) and extracellular signal-regulated kinase," Exp Cell Res, vol. 290, pp. 144-54, Oct 15. 2003.
. I. Yajima, M. Y. Kumasaka, S. Ohnuma, N. Ohgami, H. Naito, H. U. Shekhar, et al., "Arsenite-mediated promotion of anchorage-independent growth of HaCaT cells through placental growth factor," J Invest Dermatol, vol. 135, pp. 1147-1156, Apr. 2015.
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