ROS Function in Redox Signaling and Oxidative Stress

Current Biology - Tập 24 Số 10 - Trang R453-R462 - 2014
Michael Schieber1, Navdeep S. Chandel1
1Division of Pulmonary and Critical Care Medicine, Department of Medicine, The Feinberg School of Medicine, Northwestern University, Chicago, IL 60611 USA.

Tóm tắt

Từ khóa


Tài liệu tham khảo

Cross, 1987, Oxygen radicals and human disease, Ann. Int. Med., 107, 526, 10.7326/0003-4819-107-4-526

Finkel, 2011, Signal transduction by reactive oxygen species, J. Cell Biol., 194, 7, 10.1083/jcb.201102095

Wood, 2003, Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling, Science, 300, 650, 10.1126/science.1080405

Kiley, 2004, Exploiting thiol modifications, PLoS Biol., 2, e400, 10.1371/journal.pbio.0020400

Rhee, 2006, Cell signaling. H2O2, a necessary evil for cell signaling, Science, 312, 1882, 10.1126/science.1130481

Finkel, 2012, From sulfenylation to sulfhydration: what a thiolate needs to tolerate, Sci. Signal, 5, pe10, 10.1126/scisignal.2002943

Winterbourn, 2008, Thiol chemistry and specificity in redox signaling, Free Radic Biol. Med., 45, 549, 10.1016/j.freeradbiomed.2008.05.004

Lambeth, 2004, NOX enzymes and the biology of reactive oxygen, Nat. Rev. Immunol., 4, 181, 10.1038/nri1312

Brand, 2010, The sites and topology of mitochondrial superoxide production, Exp. Gerontol., 45, 466, 10.1016/j.exger.2010.01.003

Fridovich, 1997, Superoxide anion radical (O2-.), superoxide dismutases, and related matters, J. Biol. Chem., 272, 18515, 10.1074/jbc.272.30.18515

Chen, 2009, Superoxide is the major reactive oxygen species regulating autophagy, Cell Death Differ., 16, 1040, 10.1038/cdd.2009.49

Dizdaroglu, 2012, Mechanisms of free radical-induced damage to DNA, Free Radic. Res., 46, 382, 10.3109/10715762.2011.653969

Morgan, 2011, Measuring E(GSH) and H(2)O(2) with roGFP2-based redox probes, Free Radic Biol. Med., 51, 1943, 10.1016/j.freeradbiomed.2011.08.035

Murphy, 2012, Mitochondrial thiols in antioxidant protection and redox signaling: distinct roles for glutathionylation and other thiol modifications, Antioxid. Redox Signal., 16, 476, 10.1089/ars.2011.4289

Al-Mehdi, 2012, Perinuclear mitochondrial clustering creates an oxidant-rich nuclear domain required for hypoxia-induced transcription, Sci. Signal., 5, ra47, 10.1126/scisignal.2002712

Thompson, 2011, Rethinking the regulation of cellular metabolism, Cold Spring Harb. Symp. Quant. Biol., 76, 23, 10.1101/sqb.2012.76.010496

Lemmon, 2010, Cell signaling by receptor tyrosine kinases, Cell, 141, 1117, 10.1016/j.cell.2010.06.011

Cantley, 2002, The phosphoinositide 3-kinase pathway, Science, 296, 1655, 10.1126/science.296.5573.1655

Tonks, 2006, Protein tyrosine phosphatases: from genes, to function, to disease, Nat. Rev. Mol. Cell Biol., 7, 833, 10.1038/nrm2039

Wishart, 2002, PTEN and myotubularin phosphatases: from 3-phosphoinositide dephosphorylation to disease, Trends Cell Biol., 12, 579, 10.1016/S0962-8924(02)02412-1

Sundaresan, 1995, Requirement for generation of H2O2 for platelet-derived growth factor signal transduction, Science, 270, 296, 10.1126/science.270.5234.296

Bae, 1997, Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation, J. Biol. Chem., 272, 217, 10.1074/jbc.272.1.217

Adachi, 1996, Mammalian SH2-containing protein tyrosine phosphatases, Cell, 85, 15, 10.1016/S0092-8674(00)81077-6

Lee, 1998, Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor, J. Biol. Chem., 273, 15366, 10.1074/jbc.273.25.15366

Meng, 2002, Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo, Mol. Cell, 9, 387, 10.1016/S1097-2765(02)00445-8

Denu, 1998, Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation, Biochemistry, 37, 5633, 10.1021/bi973035t

Lee, 2002, Reversible inactivation of the tumor suppressor PTEN by H2O2, J. Biol. Chem., 277, 20336, 10.1074/jbc.M111899200

Leslie, 2003, Redox regulation of PI 3-kinase signalling via inactivation of PTEN, EMBO J., 22, 5501, 10.1093/emboj/cdg513

Choi, 2005, Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II, Nature, 435, 347, 10.1038/nature03587

Kwon, 2004, Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors, Proc. Natl. Acad. Sci. USA, 101, 16419, 10.1073/pnas.0407396101

Woo, 2010, Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling, Cell, 140, 517, 10.1016/j.cell.2010.01.009

Connor, 2005, Mitochondrial H2O2 regulates the angiogenic phenotype via PTEN oxidation, J. Biol. Chem., 280, 16916, 10.1074/jbc.M410690200

Hanahan, 2011, Hallmarks of cancer: the next generation, Cell, 144, 646, 10.1016/j.cell.2011.02.013

Cairns, 2011, Regulation of cancer cell metabolism, Nat. Rev. Cancer, 11, 85, 10.1038/nrc2981

Szatrowski, 1991, Production of large amounts of hydrogen peroxide by human tumor cells, Cancer Res., 51, 794

Ames, 1993, Oxidants, antioxidants, and the degenerative diseases of aging, Proc. Natl. Acad. Sci. USA, 90, 7915, 10.1073/pnas.90.17.7915

Gao, 2007, HIF-dependent antitumorigenic effect of antioxidants in vivo, Cancer Cell, 12, 230, 10.1016/j.ccr.2007.08.004

Irani, 1997, Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts, Science, 275, 1649, 10.1126/science.275.5306.1649

Weinberg, 2010, Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity, Proc. Natl. Acad. Sci. USA, 107, 8788, 10.1073/pnas.1003428107

Sullivan, 2013, The Proto-oncometabolite fumarate binds glutathione to amplify ROS-dependent signaling, Mol. Cell, 51, 236, 10.1016/j.molcel.2013.05.003

Ishikawa, 2008, ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis, Science, 320, 661, 10.1126/science.1156906

Woo, 2012, Mitochondrial genome instability and ROS enhance intestinal tumorigenesis in APC(Min/+) mice, Am. J. Pathol., 180, 24, 10.1016/j.ajpath.2011.10.003

Ben-Neriah, 2011, Inflammation meets cancer, with NF-kappaB as the matchmaker, Nat. Immunol., 12, 715, 10.1038/ni.2060

Schreck, 1991, Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1, EMBO J., 10, 2247, 10.1002/j.1460-2075.1991.tb07761.x

Gorrini, 2013, Modulation of oxidative stress as an anticancer strategy. Nat. Rev, Drug Discov., 12, 931, 10.1038/nrd4002

Trachootham, 2006, Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate, Cancer Cell, 10, 241, 10.1016/j.ccr.2006.08.009

Nogueira, 2008, Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis, Cancer Cell, 14, 458, 10.1016/j.ccr.2008.11.003

Sporn, 2012, NRF2 and cancer: the good, the bad and the importance of context, Nat. Rev. Cancer, 12, 564, 10.1038/nrc3278

Jaramillo, 2013, The emerging role of the Nrf2-Keap1 signaling pathway in cancer, Genes Dev., 27, 2179, 10.1101/gad.225680.113

DeNicola, 2011, Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis, Nature, 475, 106, 10.1038/nature10189

Cao, 2009, Prdx1 inhibits tumorigenesis via regulating PTEN/AKT activity, EMBO J., 28, 1505, 10.1038/emboj.2009.101

Neumann, 2003, Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression, Nature, 424, 561, 10.1038/nature01819

Budanov, 2004, Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD, Science, 304, 596, 10.1126/science.1095569

Sablina, 2005, The antioxidant function of the p53 tumor suppressor, Nat. Med., 11, 1306, 10.1038/nm1320

Li, 2012, Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence, Cell, 149, 1269, 10.1016/j.cell.2012.04.026

Cheung, 2012, Mitochondrial localization of TIGAR under hypoxia stimulates HK2 and lowers ROS and cell death, Proc. Natl. Acad. Sci. USA, 109, 20491, 10.1073/pnas.1206530109

Bensaad, 2006, TIGAR, a p53-inducible regulator of glycolysis and apoptosis, Cell, 126, 107, 10.1016/j.cell.2006.05.036

Dansen, 2008, Unravelling the tumor-suppressive functions of FOXO proteins, Trends Cell Biol., 18, 421, 10.1016/j.tcb.2008.07.004

Gatenby, 2004, Why do cancers have high aerobic glycolysis?, Nat. Rev. Cancer, 4, 891, 10.1038/nrc1478

Semenza, 2012, Hypoxia-inducible factors in physiology and medicine, Cell, 148, 399, 10.1016/j.cell.2012.01.021

Kaelin, 2008, Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway, Mol. Cell, 30, 393, 10.1016/j.molcel.2008.04.009

Semenza, 2012, Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy, Trends Pharmacol. Sci., 33, 207, 10.1016/j.tips.2012.01.005

Chandel, 2000, Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing, J. Biol. Chem., 275, 25130, 10.1074/jbc.M001914200

Bell, 2007, The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production, J. Cell Biol., 177, 1029, 10.1083/jcb.200609074

Horak, 2010, Negative feedback control of HIF-1 through REDD1-regulated ROS suppresses tumorigenesis, Proc. Natl. Acad. Sci. USA, 107, 4675, 10.1073/pnas.0907705107

Ma, 2009, Antitumorigenesis of antioxidants in a transgenic Rac1 model of Kaposi's sarcoma, Proc. Natl. Acad. Sci. USA, 106, 8683, 10.1073/pnas.0812688106

Bell, 2011, SirT3 suppresses hypoxia inducible factor 1α and tumor growth by inhibiting mitochondrial ROS production, Oncogene, 30, 2986, 10.1038/onc.2011.37

Finley, 2011, SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization, Cancer Cell, 19, 416, 10.1016/j.ccr.2011.02.014

Bjelakovic, 2007, Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis, JAMA, 297, 842, 10.1001/jama.297.8.842

Raj, 2011, Selective killing of cancer cells by a small molecule targeting the stress response to ROS, Nature, 475, 231, 10.1038/nature10167

Glasauer, 2014, Targeting SOD1 reduces experimental non-small-cell lung cancer, J. Clin. Invest., 124, 117, 10.1172/JCI71714

Shaw, 2011, Selective killing of K-ras mutant cancer cells by small molecule inducers of oxidative stress, Proc. Natl. Acad. Sci. USA, 108, 8773, 10.1073/pnas.1105941108

West, 2011, Mitochondria in innate immune responses, Nat. Rev. Immunol., 11, 389, 10.1038/nri2975

Kaminski, 2013, Mitochondria as oxidative signaling organelles in T-cell activation: physiological role and pathological implications, Archivum immunologiae et therapiae experimentalis, 61, 367, 10.1007/s00005-013-0235-0

Mittal, 2014, Reactive Oxygen Species in Inflammation and Tissue Injury, Antioxid. Redox Signal., 20, 1126, 10.1089/ars.2012.5149

Iwasaki, 2010, Regulation of adaptive immunity by the innate immune system, Science, 327, 291, 10.1126/science.1183021

West, 2006, Recognition and signaling by toll-like receptors, Annu. Rev. Cell Dev. Biol., 22, 409, 10.1146/annurev.cellbio.21.122303.115827

Takeuchi, 2009, Innate immunity to virus infection, Immunol. Rev., 227, 75, 10.1111/j.1600-065X.2008.00737.x

Chen, 2010, Sterile inflammation: sensing and reacting to damage, Nat. Rev. Immunol., 10, 826, 10.1038/nri2873

Chandel, 2000, Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin, J. Immunol., 165, 1013, 10.4049/jimmunol.165.2.1013

Wang, 1994, Effect of the NADPH oxidase inhibitor apocynin on septic lung injury in guinea pigs, Am. J. Respir. Crit. Care Med., 150, 1449, 10.1164/ajrccm.150.5.7952574

West, 2011, TLR signalling augments macrophage bactericidal activity through mitochondrial ROS, Nature, 472, 476, 10.1038/nature09973

Tal, 2009, Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling, Proc. Natl. Acad. Sci. USA, 106, 2770, 10.1073/pnas.0807694106

Moore, 2008, Regulation of mitochondrial antiviral signaling pathways, Immunity, 28, 735, 10.1016/j.immuni.2008.05.005

Allen, 2009, The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA, Immunity, 30, 556, 10.1016/j.immuni.2009.02.005

Cruz, 2007, ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages, J. Biol. Chem., 282, 2871, 10.1074/jbc.M608083200

Tschopp, 2010, NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production?, Nat. Rev. Immunol., 10, 210, 10.1038/nri2725

Nakahira, 2011, Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome, Nat. Immunol., 12, 222, 10.1038/ni.1980

Dostert, 2008, Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica, Science, 320, 674, 10.1126/science.1156995

Bulua, 2011, Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS), J. Exp. Med., 208, 519, 10.1084/jem.20102049

Chaudhri, 1986, Effect of antioxidants on primary alloantigen-induced T cell activation and proliferation, J. Immunol., 137, 2646, 10.4049/jimmunol.137.8.2646

Laniewski, 2004, Antioxidant treatment reduces expansion and contraction of antigen-specific CD8+ T cells during primary but not secondary viral infection, J. Virol., 78, 11246, 10.1128/JVI.78.20.11246-11257.2004

Sena, 2013, Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling, Immunity, 38, 225, 10.1016/j.immuni.2012.10.020

Kaminski, 2010, Mitochondrial reactive oxygen species control T cell activation by regulating IL-2 and IL-4 expression: mechanism of ciprofloxacin-mediated immunosuppression, J. Immunol., 184, 4827, 10.4049/jimmunol.0901662

Kaminski, 2007, Novel role for mitochondria: protein kinase Ctheta-dependent oxidative signaling organelles in activation-induced T-cell death, Mol. Cell Biol., 27, 3625, 10.1128/MCB.02295-06

Wheeler, 2012, Prolonged production of reactive oxygen species in response to B cell receptor stimulation promotes B cell activation and proliferation, J. Immunol., 189, 4405, 10.4049/jimmunol.1201433

Singh, 2005, The strength of receptor signaling is centrally controlled through a cooperative loop between Ca2+ and an oxidant signal, Cell, 121, 281, 10.1016/j.cell.2005.02.036

Lang, 2013, Reactive oxygen species delay control of lymphocytic choriomeningitis virus, Cell Death Differ., 20, 649, 10.1038/cdd.2012.167

Arsenijevic, 2000, Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production, Nat. Genet., 26, 435, 10.1038/82565

Wang, 2010, Elevated mitochondrial reactive oxygen species generation affects the immune response via hypoxia-inducible factor-1alpha in long-lived Mclk1+/- mouse mutants, J. Immunol., 184, 582, 10.4049/jimmunol.0902352

Kong, 2011, Enhancing Nrf2 pathway by disruption of Keap1 in myeloid leukocytes protects against sepsis, Am. J. Respir. Crit. Care Med., 184, 928, 10.1164/rccm.201102-0271OC

Thimmulappa, 2006, Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis, J. Clin. Invest., 116, 984, 10.1172/JCI25790

Rangasamy, 2005, Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice, J. Exp. Med., 202, 47, 10.1084/jem.20050538

Szakmany, 2012, N-acetylcysteine for sepsis and systemic inflammatory response in adults, Cochrane Database Syst. Rev., 9, CD006616

Harman, 1956, Aging: a theory based on free radical and radiation chemistry, J. Gerontol., 11, 298, 10.1093/geronj/11.3.298

Balaban, 2005, Mitochondria, oxidants, and aging, Cell, 120, 483, 10.1016/j.cell.2005.02.001

Van Raamsdonk, 2010, Reactive oxygen species and aging in Caenorhabditis elegans: causal or casual relationship?, Antioxid. Redox Signal., 13, 1911, 10.1089/ars.2010.3215

Ristow, 2011, Extending life span by increasing oxidative stress, Free Radic. Biol. Med., 51, 327, 10.1016/j.freeradbiomed.2011.05.010

Orr, 1994, Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster, Science, 263, 1128, 10.1126/science.8108730

Mockett, 2010, Expression of multiple copies of mitochondrially targeted catalase or genomic Mn superoxide dismutase transgenes does not extend the life span of Drosophila melanogaster, Free Radic. Biol. Med., 49, 2028, 10.1016/j.freeradbiomed.2010.09.029

Perez, 2009, The overexpression of major antioxidant enzymes does not extend the lifespan of mice, Aging Cell, 8, 73, 10.1111/j.1474-9726.2008.00449.x

Schriner, 2005, Extension of murine life span by overexpression of catalase targeted to mitochondria, Science, 308, 1909, 10.1126/science.1106653

Van Remmen, 2003, Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging, Physiol. Genomics, 16, 29, 10.1152/physiolgenomics.00122.2003

Zhang, 2009, Mice deficient in both Mn superoxide dismutase and glutathione peroxidase-1 have increased oxidative damage and a greater incidence of pathology but no reduction in longevity, J. Gerontol., 64, 1212, 10.1093/gerona/glp132

Van Raamsdonk, 2009, Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans, PLoS Genet., 5, e1000361, 10.1371/journal.pgen.1000361

Hekimi, 2011, Taking a "good" look at free radicals in the aging process, Trends Cell Biol., 21, 569, 10.1016/j.tcb.2011.06.008

Pan, 2011, Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling, Cell Metab., 13, 668, 10.1016/j.cmet.2011.03.018

Mesquita, 2010, Caloric restriction or catalase inactivation extends yeast chronological lifespan by inducing H2O2 and superoxide dismutase activity, Proc. Natl. Acad. Sci. USA, 107, 15123, 10.1073/pnas.1004432107

Lee, 2010, Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity, Curr. Biol., 20, 2131, 10.1016/j.cub.2010.10.057

Zarse, 2012, Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal, Cell Metab., 15, 451, 10.1016/j.cmet.2012.02.013

Schulz, 2007, Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress, Cell Metab., 6, 280, 10.1016/j.cmet.2007.08.011

Yang, 2010, A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans, PLoS Biol., 8, e1000556, 10.1371/journal.pbio.1000556

Schmeisser, 2013, Role of sirtuins in lifespan regulation is linked to methylation of nicotinamide, Nat. Chem. Biol., 9, 693, 10.1038/nchembio.1352

Lapointe, 2009, Reversal of the mitochondrial phenotype and slow development of oxidative biomarkers of aging in long-lived Mclk1+/- mice, J. Biol. Chem., 284, 20364, 10.1074/jbc.M109.006569

Liu, 2005, Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice, Genes Dev., 19, 2424, 10.1101/gad.1352905

Packer, 1977, Low oxygen concentration extends the lifespan of cultured human diploid cells, Nature, 267, 423, 10.1038/267423a0

Bell, 2007, Mitochondrial reactive oxygen species trigger hypoxia-inducible factor-dependent extension of the replicative life span during hypoxia, Mol. Cell Biol., 27, 5737, 10.1128/MCB.02265-06

Signer, 2013, Mechanisms that regulate stem cell aging and life span, Cell Stem Cell, 12, 152, 10.1016/j.stem.2013.01.001

Ito, 2006, Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells, Nat. Med., 12, 446, 10.1038/nm1388

Janzen, 2006, Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a, Nature, 443, 421, 10.1038/nature05159

Ito, 2004, Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells, Nature, 431, 997, 10.1038/nature02989

D'Souza, 2013, Reducing mitochondrial ROS improves disease-related pathology in a mouse model of ataxia-telangiectasia, Mol. Ther., 21, 42, 10.1038/mt.2012.203

Guo, 2010, ATM activation by oxidative stress, Science, 330, 517, 10.1126/science.1192912

Cosentino, 2011, ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair, EMBO J., 30, 546, 10.1038/emboj.2010.330

Maryanovich, 2012, The ATM-BID pathway regulates quiescence and survival of haematopoietic stem cells, Nat. Cell Biol., 14, 535, 10.1038/ncb2468

Liu, 2009, Bmi1 regulates mitochondrial function and the DNA damage response pathway, Nature, 459, 387, 10.1038/nature08040

Chen, 2008, TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species, J. Exp. Med., 205, 2397, 10.1084/jem.20081297

Tothova, 2007, FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress, Cell, 128, 325, 10.1016/j.cell.2007.01.003

Chuikov, 2010, Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress, Nat. Cell Biol., 12, 999, 10.1038/ncb2101

Juntilla, 2010, AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species, Blood, 115, 4030, 10.1182/blood-2009-09-241000

Owusu-Ansah, 2009, Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation, Nature, 461, 537, 10.1038/nature08313

Tormos, 2011, Mitochondrial complex III ROS regulate adipocyte differentiation, Cell Metab., 14, 537, 10.1016/j.cmet.2011.08.007

Malinska, 2012, Changes in mitochondrial reactive oxygen species synthesis during differentiation of skeletal muscle cells, Mitochondrion, 12, 144, 10.1016/j.mito.2011.06.015

Hamanaka, 2013, Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development, Sci. Signal, 6, ra8, 10.1126/scisignal.2003638

Morimoto, 2013, ROS are required for mouse spermatogonial stem cell self-renewal, Cell Stem Cell, 12, 774, 10.1016/j.stem.2013.04.001

Le Belle, 2011, Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner, Cell Stem Cell, 8, 59, 10.1016/j.stem.2010.11.028

Hom, 2011, The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation, Dev. Cell, 21, 469, 10.1016/j.devcel.2011.08.008

Ahlqvist, 2012, Somatic progenitor cell vulnerability to mitochondrial DNA mutagenesis underlies progeroid phenotypes in Polg mutator mice, Cell Metab., 15, 100, 10.1016/j.cmet.2011.11.012

Raimundo, 2012, Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness, Cell, 148, 716, 10.1016/j.cell.2011.12.027

Ristow, 2009, Antioxidants prevent health-promoting effects of physical exercise in humans, Proc. Natl. Acad. Sci. USA, 106, 8665, 10.1073/pnas.0903485106