ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition

Nature Chemical Biology - Tập 13 Số 1 - Trang 91-98 - 2017
Sebastian Doll1, Bettina Proneth1, Yulia Y. Tyurina2, Elena Panzilius3, Sho Kobayashi1, Irina Ingold1, Martin Irmler4, Johannes Beckers4, Michaela Aichler5, Axel Walch5, Holger Prokisch6, Dietrich Trümbach1, Gaowei Mao2, Feng Qu2, Hülya Bayır2, Joachim Füllekrug7, Christina Scheel3, Wolfgang Wurst1, Joel Schick1, Valerian E. Kagan2, Josè Pedro Friedmann Angeli1, Marcus Conrad1
1Institute of Developmental Genetics, Helmholtz Zentrum München, Neuherberg, Germany
2Department of Environmental and Occupational Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
3Institute of Stem Cell Biology, Helmholtz Zentrum München, Neuherberg, Germany
4Institute of Experimental Genetics, Helmholtz Zentrum München, Neuherberg, Germany
5Institute of Pathology, Helmholtz Zentrum München, Neuherberg, Germany
6Institute of Human Genetics, Helmholtz Zentrum München, Neuherberg, Germany
7Department of Gastroenterology, University of Heidelberg, Heidelberg, Germany

Tóm tắt

Từ khóa


Tài liệu tham khảo

Conrad, M., Angeli, J.P., Vandenabeele, P. & Stockwell, B.R. Regulated necrosis: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 15, 348–366 (2016).

Friedmann Angeli, J.P. et al. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat. Cell Biol. 16, 1180–1191 (2014).

Matsushita, M. et al. T cell lipid peroxidation induces ferroptosis and prevents immunity to infection. J. Exp. Med. 212, 555–568 (2015).

Yang, W.S. et al. Regulation of ferroptotic cancer cell death by GPX4. Cell 156, 317–331 (2014).

Linkermann, A. et al. Synchronized renal tubular cell death involves ferroptosis. Proc. Natl. Acad. Sci. USA 111, 16836–16841 (2014).

Jiang, L. et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature 520, 57–62 (2015).

Dolma, S., Lessnick, S.L., Hahn, W.C. & Stockwell, B.R. Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 3, 285–296 (2003).

Dixon, S.J. et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149, 1060–1072 (2012).

Ishii, T., Sugita, Y. & Bannai, S. Regulation of glutathione levels in mouse spleen lymphocytes by transport of cysteine. J. Cell. Physiol. 133, 330–336 (1987).

Ursini, F., Maiorino, M., Valente, M., Ferri, L. & Gregolin, C. Purification from pig liver of a protein which protects liposomes and biomembranes from peroxidative degradation and exhibits glutathione peroxidase activity on phosphatidylcholine hydroperoxides. Biochim. Biophys. Acta 710, 197–211 (1982).

Yang, W.S. & Stockwell, B.R. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem. Biol. 15, 234–245 (2008).

Dixon, S.J. et al. Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. eLife 3, e02523 (2014).

Louandre, C. et al. Iron-dependent cell death of hepatocellular carcinoma cells exposed to sorafenib. Int. J. Cancer 133, 1732–1742 (2013).

Hayano, M., Yang, W.S., Corn, C.K., Pagano, N.C. & Stockwell, B.R. Loss of cysteinyl-tRNA synthetase (CARS) induces the transsulfuration pathway and inhibits ferroptosis induced by cystine deprivation. Cell Death Differ. 23, 270–278 (2016).

Seiler, A. et al. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 8, 237–248 (2008).

Koike-Yusa, H., Li, Y., Tan, E.P., Velasco-Herrera, Mdel.C. & Yusa, K. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat. Biotechnol. 32, 267–273 (2014).

Wortmann, M. et al. Combined deficiency in glutathione peroxidase 4 and vitamin E causes multiorgan thrombus formation and early death in mice. Circ. Res. 113, 408–417 (2013).

Canli, Ö. et al. Glutathione peroxidase 4 prevents necroptosis in mouse erythroid precursors. Blood 127, 139–148 (2016).

Soupene, E., Fyrst, H. & Kuypers, F.A. Mammalian acyl-CoA:lysophosphatidylcholine acyltransferase enzymes. Proc. Natl. Acad. Sci. USA 105, 88–93 (2008).

Yamanaka, K. et al. A novel fluorescent probe with high sensitivity and selective detection of lipid hydroperoxides in cells. RSC Advances 2, 7894–7900 (2012).

Dixon, S.J. et al. Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chem. Biol. 10, 1604–1609 (2015).

Yin, H., Xu, L. & Porter, N.A. Free radical lipid peroxidation: mechanisms and analysis. Chem. Rev. 111, 5944–5972 (2011).

Pratt, D.A., Mills, J.H. & Porter, N.A. Theoretical calculations of carbon-oxygen bond dissociation enthalpies of peroxyl radicals formed in the autoxidation of lipids. J. Am. Chem. Soc. 125, 5801–5810 (2003).

Kagan, V.E. Oxidized arachidonic and adrenic phosphatidylethanolamines navigate cells to ferroptosis. Nat. Chem. Biol. http://dx.doi.org/nchembio.2238 (2016).

Timmerman, L.A. et al. Glutamine sensitivity analysis identifies the xCT antiporter as a common triple-negative breast tumor therapeutic target. Cancer Cell 24, 450–465 (2013).

Kim, J.H., Lewin, T.M. & Coleman, R.A. Expression and characterization of recombinant rat Acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J. Biol. Chem. 276, 24667–24673 (2001).

Gale, E.A. Lessons from the glitazones: a story of drug development. Lancet 357, 1870–1875 (2001).

Küch, E.M. et al. Differentially localized acyl-CoA synthetase 4 isoenzymes mediate the metabolic channeling of fatty acids towards phosphatidylinositol. Biochim. Biophys. Acta 1841, 227–239 (2014).

Van Horn, C.G. et al. Characterization of recombinant long-chain rat acyl-CoA synthetase isoforms 3 and 6: identification of a novel variant of isoform 6. Biochemistry 44, 1635–1642 (2005).

Brash, A.R. Arachidonic acid as a bioactive molecule. J. Clin. Invest. 107, 1339–1345 (2001).

Orlando, U.D. et al. Acyl-CoA synthetase-4, a new regulator of mTOR and a potential therapeutic target for enhanced estrogen receptor function in receptor-positive and -negative breast cancer. Oncotarget 6, 42632–42650 2015).

Wu, X. et al. ACSL4 promotes prostate cancer growth, invasion and hormonal resistance. Oncotarget 6, 44849–44863 (2015).

Wu, X. et al. Long chain fatty acyl-CoA synthetase 4 is a biomarker for and mediator of hormone resistance in human breast cancer. PLoS One 8, e77060 (2013).

Monaco, M.E. et al. Expression of long-chain fatty acyl-CoA synthetase 4 in breast and prostate cancers is associated with sex steroid hormone receptor negativity. Transl. Oncol. 3, 91–98 (2010).

Hudis, C.A. & Gianni, L. Triple-negative breast cancer: an unmet medical need. Oncologist 16 (Suppl. 1), 1–11 (2011).

Jin, J. et al. Neuroprotective effects of PPAR-γ agonist rosiglitazone in N171-82Q mouse model of Huntington's disease. J. Neurochem. 125, 410–419 (2013).

Heneka, M.T., Fink, A. & Doblhammer, G. Effect of pioglitazone medication on the incidence of dementia. Ann. Neurol. 78, 284–294 (2015).

Belfort, R. et al. A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N. Engl. J. Med. 355, 2297–2307 (2006).

Aithal, G.P. et al. Randomized, placebo-controlled trial of pioglitazone in nondiabetic subjects with nonalcoholic steatohepatitis. Gastroenterology 135, 1176–1184 (2008).

Han, L. et al. Rosiglitazone promotes white matter integrity and long-term functional recovery after focal cerebral ischemia. Stroke 46, 2628–2636 (2015).

Culman, J. et al. Treatment of rats with pioglitazone in the reperfusion phase of focal cerebral ischemia: a preclinical stroke trial. Exp. Neurol. 238, 243–253 (2012).

Rennings, A.J. et al. Rosiglitazone reduces ischaemia-reperfusion injury in patients with the metabolic syndrome. Eur. Heart J. 31, 983 (2010).

Wu, J.S. et al. Ligand-activated peroxisome proliferator-activated receptor-gamma protects against ischemic cerebral infarction and neuronal apoptosis by 14-3-3 epsilon upregulation. Circulation 119, 1124–1134 (2009).

Kuboki, S. et al. Peroxisome proliferator-activated receptor-γ protects against hepatic ischemia/reperfusion injury in mice. Hepatology 47, 215–224 (2008).

Tietze, F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502–522 (1969).

Bannai, S. & Ishii, T. Transport of cystine and cysteine and cell growth in cultured human diploid fibroblasts: effect of glutamate and homocysteate. J. Cell. Physiol. 112, 265–272 (1982).

Roveri, A., Maiorino, M. & Ursini, F. Enzymatic and immunological measurements of soluble and membrane-bound phospholipid-hydroperoxide glutathione peroxidase. Methods Enzymol. 233, 202–212 (1994).

Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819–823 (2013).

Brinkman, E.K., Chen, T., Amendola, M. & van Steensel, B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res. 42, e168 (2014).

Mannes, A.M., Seiler, A., Bosello, V., Maiorino, M. & Conrad, M. Cysteine mutant of mammalian GPx4 rescues cell death induced by disruption of the wild-type selenoenzyme. FASEB J. 25, 2135–2144 (2011).

Haack, T.B. et al. ELAC2 mutations cause a mitochondrial RNA processing defect associated with hypertrophic cardiomyopathy. Am. J. Hum. Genet. 93, 211–223 (2013).

Bornkamm, G.W. et al. Stringent doxycycline-dependent control of gene activities using an episomal one-vector system. Nucleic Acids Res. 33, e137 (2005).