The role of iron and reactive oxygen species in cell death (original) (raw)

• Frey, P.A. & Reed, G.H. The ubiquity of iron. ACS Chem. Biol. 7, 1477–1481 (2012).
  Article CAS PubMed Google Scholar
• Lambeth, J.D. & Neish, A.S. Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu. Rev. Pathol. doi:10.1146/annurev-pathol-012513-104651 (2013).
• Kell, D.B. Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases. BMC Med. Genomics 2, 2 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Petrat, F., de Groot, H., Sustmann, R. & Rauen, U. The chelatable iron pool in living cells: a methodically defined quantity. Biol. Chem. 383, 489–502 (2002).
  Article CAS PubMed Google Scholar
• Kurz, T., Eaton, J.W. & Brunk, U.T. The role of lysosomes in iron metabolism and recycling. Int. J. Biochem. Cell Biol. 43, 1686–1697 (2011).
  Article CAS PubMed Google Scholar
• Carlioz, A. & Touati, D. Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J. 5, 623–630 (1986).
  Article CAS PubMed PubMed Central Google Scholar
• Imlay, J.A. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11, 443–454 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Flint, D.H., Tuminello, J.F. & Emptage, M.H. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 268, 22369–22376 (1993).
  CAS PubMed Google Scholar
• Esposito, L.A., Melov, S., Panov, A., Cottrell, B.A. & Wallace, D.C. Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. USA 96, 4820–4825 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Melov, S. et al. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. USA 96, 846–851 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Li, Y. et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11, 376–381 (1995).
  Article CAS PubMed Google Scholar
• Brennan, A.M. et al. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12, 857–863 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Farrow, M.A. et al. Clostridium difficile toxin B–induced necrosis is mediated by the host epithelial cell NADPH oxidase complex. Proc. Natl. Acad. Sci. USA 110, 18674–18679 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Seaver, L.C. & Imlay, J.A. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183, 7173–7181 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Park, S., You, X. & Imlay, J.A. Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx− mutants of Escherichia coli. Proc. Natl. Acad. Sci. USA 102, 9317–9322 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Jang, S. & Imlay, J.A. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 282, 929–937 (2007).
  Article CAS PubMed Google Scholar
• Jang, S. & Imlay, J.A. Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol. Microbiol. 78, 1448–1467 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Anjem, A. & Imlay, J.A. Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J. Biol. Chem. 287, 15544–15556 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Sobota, J.M. & Imlay, J.A. Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc. Natl. Acad. Sci. USA 108, 5402–5407 (2011).
  Article PubMed PubMed Central Google Scholar
• Cvetkovic, A. et al. Microbial metalloproteomes are largely uncharacterized. Nature 466, 779–782 (2010).
  Article CAS PubMed Google Scholar
• Antunes, F., Cadenas, E. & Brunk, U.T. Apoptosis induced by exposure to a low steady-state concentration of H2O2 is a consequence of lysosomal rupture. Biochem. J. 356, 549–555 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Hamacher-Brady, A. et al. Artesunate activates mitochondrial apoptosis in breast cancer cells via iron-catalyzed lysosomal reactive oxygen species production. J. Biol. Chem. 286, 6587–6601 (2011).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Heo, J.M. et al. A stress-responsive system for mitochondrial protein degradation. Mol. Cell 40, 465–480 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Madeo, F., Frohlich, E. & Frohlich, K.U. A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139, 729–734 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Braun, R.J. et al. Crucial mitochondrial impairment upon CDC48 mutation in apoptotic yeast. J. Biol. Chem. 281, 25757–25767 (2006).
  Article CAS PubMed Google Scholar
• Madeo, F. et al. Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145, 757–767 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Bartolome, F. et al. Pathogenic VCP mutations induce mitochondrial uncoupling and reduced ATP levels. Neuron 78, 57–64 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Raimundo, N. et al. Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell 148, 716–726 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Chae, S. et al. A systems approach for decoding mitochondrial retrograde signaling pathways. Sci. Signal. 6, rs4 (2013).
  Article CAS PubMed Google Scholar
• Kagan, V.E. et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 1, 223–232 (2005).
  Article CAS PubMed Google Scholar
• Ji, J. et al. Lipidomics identifies cardiolipin oxidation as a mitochondrial target for redox therapy of brain injury. Nat. Neurosci. 15, 1407–1413 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Jiang, J. et al. Interplay between bax, reactive oxygen species production, and cardiolipin oxidation during apoptosis. Biochem. Biophys. Res. Commun. 368, 145–150 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ricci, J.E. et al. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117, 773–786 (2004).
  Article CAS PubMed Google Scholar
• Huai, J. et al. TNFa-induced lysosomal membrane permeability (LMP) is downstream of MOMP and triggered by caspase-mediated p75 cleavage and ROS formation. J. Cell Sci. 126, 4015–4025 (2013).
  Article CAS PubMed Google Scholar
• Garcia-Perez, C. et al. Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling. Proc. Natl. Acad. Sci. USA 109, 4497–4502 (2012).
  Article PubMed PubMed Central Google Scholar
• Degterev, A. et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112–119 (2005).
  Article CAS PubMed Google Scholar
• Linkermann, A. et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc. Natl. Acad. Sci. USA 110, 12024–12029 (2013).
  Article PubMed PubMed Central Google Scholar
• Zhang, D.W. et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325, 332–336 (2009).
  Article CAS PubMed Google Scholar
• Vercammen, D. et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187, 1477–1485 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Shulga, N. & Pastorino, J.G. GRIM-19–mediated translocation of STAT3 to mitochondria is necessary for TNF-induced necroptosis. J. Cell Sci. 125, 2995–3003 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, Y.S., Morgan, M.J., Choksi, S. & Liu, Z.G. TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol. Cell 26, 675–687 (2007).
  Article CAS PubMed Google Scholar
• Yazdanpanah, B. et al. Riboflavin kinase couples TNF receptor 1 to NADPH oxidase. Nature 460, 1159–1163 (2009).
  Article CAS PubMed Google Scholar
• Xie, C. et al. Distinct roles of basal steady-state and induced H-ferritin in tumor necrosis factor–induced death in L929 cells. Mol. Cell. Biol. 25, 6673–6681 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Dixon, S.J. et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149, 1060–1072 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Yagoda, N. et al. RAS-RAF-MEK–dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864–868 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Gout, P.W., Buckley, A.R., Simms, C.R. & Bruchovsky, N. Sulfasalazine, a potent suppressor of lymphoma growth by inhibition of the xc− cystine transporter: a new action for an old drug. Leukemia 15, 1633–1640 (2001).
  Article CAS PubMed Google Scholar
• Murphy, T.H., Miyamoto, M., Sastre, A., Schnaar, R.L. & Coyle, J.T. Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2, 1547–1558 (1989).
  Article CAS PubMed Google Scholar
• Wolpaw, A.J. et al. Modulatory profiling identifies mechanisms of small molecule–induced cell death. Proc. Natl. Acad. Sci. USA 108, E771–E780 (2011).
  Article PubMed PubMed Central Google Scholar
• Shaw, A.T. et al. Selective killing of K-ras mutant cancer cells by small molecule inducers of oxidative stress. Proc. Natl. Acad. Sci. USA 108, 8773–8778 (2011).
  Article PubMed PubMed Central Google Scholar
• Siddiq, A. et al. Selective inhibition of hypoxia-inducible factor (HIF) prolyl-hydroxylase 1 mediates neuroprotection against normoxic oxidative death via HIF- and CREB-independent pathways. J. Neurosci. 29, 8828–8838 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Li, Y., Maher, P. & Schubert, D. A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion. Neuron 19, 453–463 (1997).
  Article CAS PubMed Google Scholar
• Abeysinghe, R.D. et al. The environment of the lipoxygenase iron binding site explored with novel hydroxypyridinone iron chelators. J. Biol. Chem. 271, 7965–7972 (1996).
  Article CAS PubMed Google Scholar
• Tan, S., Schubert, D. & Maher, P. Oxytosis: A novel form of programmed cell death. Curr. Top. Med. Chem. 1, 497–506 (2001).
  Article CAS PubMed Google Scholar
• Zaman, K. et al. Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J. Neurosci. 19, 9821–9830 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Tan, S., Wood, M. & Maher, P. Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J. Neurochem. 71, 95–105 (1998).
  Article CAS PubMed Google Scholar
• Tobaben, S. et al. Bid-mediated mitochondrial damage is a key mechanism in glutamate-induced oxidative stress and AIF-dependent cell death in immortalized HT-22 hippocampal neurons. Cell Death Differ. 18, 282–292 (2011).
  Article CAS PubMed Google Scholar
• Henke, N. et al. The plasma membrane channel ORAI1 mediates detrimental calcium influx caused by endogenous oxidative stress. Cell Death Dis. 4, e470 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Volpe, J.J., Kinney, H.C., Jensen, F.E. & Rosenberg, P.A. The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int. J. Dev. Neurosci. 29, 423–440 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Sato, H. et al. Distribution of cystine/glutamate exchange transporter, system xc−, in the mouse brain. J. Neurosci. 22, 8028–8033 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hentze, M.W., Muckenthaler, M.U., Galy, B. & Camaschella, C. Two to tango: regulation of mammalian iron metabolism. Cell 142, 24–38 (2010).
  Article CAS PubMed Google Scholar
• Puccio, H. et al. Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 27, 181–186 (2001).
  Article CAS PubMed Google Scholar
• Eaton, J.W. & Qian, M. Molecular bases of cellular iron toxicity. Free Radic. Biol. Med. 32, 833–840 (2002).
  Article CAS PubMed Google Scholar
• Silva-Gomes, S. et al. Transcription factor NRF2 protects mice against dietary iron–induced liver injury by preventing hepatocytic cell death. J. Hepatol. doi:10.1016/j.jhep.2013.09.004 (2013).
• Torti, S.V. & Torti, F.M. Iron and cancer: more ore to be mined. Nat. Rev. Cancer 13, 342–355 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Kruer, M.C. The neuropathology of neurodegeneration with brain iron accumulation. Int. Rev. Neurobiol. 110, 165–194 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Lei, P. et al. Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat. Med. 18, 291–295 (2012).
  Article CAS PubMed Google Scholar
• Duce, J.A. et al. Iron-export ferroxidase activity of b-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 142, 857–867 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Kaur, D. et al. Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson's disease. Neuron 37, 899–909 (2003).
  Article CAS PubMed Google Scholar
• Guzman, J.N. et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468, 696–700 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Allen, G.F., Toth, R., James, J. & Ganley, I.G. Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. doi:10.1038/embor.2013.168 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, Y. et al. Dexras1, a small GTPase, is required for glutamate-NMDA neurotoxicity. J. Neurosci. 33, 3582–3587 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Cheah, J.H. et al. NMDA receptor–nitric oxide transmission mediates neuronal iron homeostasis via the GTPase Dexras1. Neuron 51, 431–440 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Vaseva, A.V. et al. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149, 1536–1548 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, X. & Lemasters, J.J. Translocation of iron from lysosomes to mitochondria during ischemia predisposes to injury after reperfusion in rat hepatocytes. Free Radic. Biol. Med. 63, 243–253 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Uchiyama, A. et al. Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress–induced hepatocellular injury. Hepatology 48, 1644–1654 (2008).
  Article CAS PubMed Google Scholar
• Li, L., Chen, O.S., McVey Ward, D. & Kaplan, J. CCC1 is a transporter that mediates vacuolar iron storage in yeast. J. Biol. Chem. 276, 29515–29519 (2001).
  Article CAS PubMed Google Scholar
• Lin, H., Li, L., Jia, X., Ward, D.M. & Kaplan, J. Genetic and biochemical analysis of high iron toxicity in yeast: iron toxicity is due to the accumulation of cytosolic iron and occurs under both aerobic and anaerobic conditions. J. Biol. Chem. 286, 3851–3862 (2011).
  Article CAS PubMed Google Scholar
• Holmes-Hampton, G.P., Jhurry, N.D., McCormick, S.P. & Lindahl, P.A. Iron content of Saccharomyces cerevisiae cells grown under iron-deficient and iron-overload conditions. Biochemistry 52, 105–114 (2013).
  Article CAS PubMed Google Scholar
• Li, L., Bagley, D., Ward, D.M. & Kaplan, J. Yap5 is an iron-responsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol. Cell. Biol. 28, 1326–1337 (2008).
  Article CAS PubMed Google Scholar
• Lee, Y.J. et al. Sphingolipid signaling mediates iron toxicity. Cell Metab. 16, 90–96 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Breslow, D.K. et al. Orm family proteins mediate sphingolipid homeostasis. Nature 463, 1048–1053 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Kelso, G.F. et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J. Biol. Chem. 276, 4588–4596 (2001).
  Article CAS PubMed Google Scholar
• McManus, M.J., Murphy, M.P. & Franklin, J.L. The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer's disease. J. Neurosci. 31, 15703–15715 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Lowes, D.A., Webster, N.R., Murphy, M.P. & Galley, H.F. Antioxidants that protect mitochondria reduce interleukin-6 and oxidative stress, improve mitochondrial function, and reduce biochemical markers of organ dysfunction in a rat model of acute sepsis. Br. J. Anaesth. 110, 472–480 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Wipf, P. et al. Mitochondrial targeting of selective electron scavengers: synthesis and biological analysis of hemigramicidin-TEMPO conjugates. J. Am. Chem. Soc. 127, 12460–12461 (2005).
  Article CAS PubMed Google Scholar
• Xun, Z. et al. Targeting of XJB-5–131 to mitochondria suppresses oxidative DNA damage and motor decline in a mouse model of Huntington's disease. Cell Rep. 2, 1137–1142 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• DeNicola, G.M. et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475, 106–109 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Son, J. et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature 496, 101–105 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Maddocks, O.D. et al. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 493, 542–546 (2013).
  Article CAS PubMed Google Scholar
• Trachootham, D., Alexandre, J. & Huang, P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov. 8, 579–591 (2009).
  Article CAS PubMed Google Scholar
• Pei, S. et al. Targeting aberrant glutathione metabolism to eradicate human acute myelogenous leukemia cells. J. Biol. Chem. doi:10.1074/jbc.M113.511170 (2013).
• Trachootham, D. et al. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by b-phenylethyl isothiocyanate. Cancer Cell 10, 241–252 (2006).
  Article CAS PubMed Google Scholar
• Raj, L. et al. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475, 231–234 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Diehn, M. et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458, 780–783 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Kohanski, M.A., Dwyer, D.J., Hayete, B., Lawrence, C.A. & Collins, J.J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797–810 (2007).
  Article CAS PubMed Google Scholar
• Liu, Y. & Imlay, J.A. Cell death from antibiotics without the involvement of reactive oxygen species. Science 339, 1210–1213 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, S. et al. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat. Med. 18, 1639–1642 (2012).
  Article CAS PubMed Google Scholar
• Cochemé, H.M. et al. Measurement of H2O2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix. Cell Metab. 13, 340–350 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Albrecht, S.C., Barata, A.G., Grosshans, J., Teleman, A.A. & Dick, T.P. In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab. 14, 819–829 (2011).
  Article CAS PubMed Google Scholar
• Au-Yeung, H.Y., Chan, J., Chantarojsiri, T. & Chang, C.J. Molecular imaging of labile iron(II) pools in living cells with a turn-on fluorescent probe. J. Am. Chem. Soc. 135, 15165–15173 (2013).
  Article CAS PubMed Google Scholar