Cellular mechanisms and physiological consequences of redox-dependent signalling

Nature Reviews Molecular Cell Biology

Volumn 15, Issue 6, 2014, Pages 411-421

  Holmström, Kira M ^a   Finkel, Toren ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYSTEINE; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

AGING; BIOLOGICAL ACTIVITY; CARCINOGENESIS; CELL FATE; HUMAN; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; METABOLIC REGULATION; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REVIEW; SELF CONCEPT; SIGNAL TRANSDUCTION; STEM CELL;

AGING; ANIMALS; CELL PHYSIOLOGICAL PHENOMENA; HUMANS; NEOPLASMS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84901316606     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3801     Document Type: Review

References (119)

1. Harman, D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300 (1956).
2. 2 for platelet-derived growth factor signal transduction. Science 270, 296-299 (1995).
3. Bae, Y. S. et al. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272, 217-221 (1997). (Pubitemid 27021147)
4. 2 accumulation for cell signaling. Cell 140, 517-528 (2010).
5. Murphy, M. P. How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13 (2009).
6. Jensen, P. K. Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron-transport particles. I. pH dependency and hydrogen peroxide formation. Biochim. Biophys. Acta 122, 157-166 (1966).
7. Brand, M. D. The sites and topology of mitochondrial superoxide production. Exp. Gerontol. 45, 466-472 (2010).
8. Mailloux, R. J. & Harper, M. E. Mitochondrial proticity and ROS signaling: lessons from the uncoupling proteins. Trends Endocrinol. Metab. 23, 451-458 (2012).
9. Sena, L. A. & Chandel, N. S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48, 158-167 (2012).
10. Chandel, N. S. et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl Acad. Sci. USA 95, 11715-11720 (1998). (Pubitemid 28460480)
11. Nemoto, S., Takeda, K., Yu, Z. X., Ferrans, V. J. & Finkel, T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol. Cell. Biol. 20, 7311-7318 (2000).
12. Hampton, M. B., Kettle, A. J. & Winterbourn, C. C. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92, 3007-3017 (1998). (Pubitemid 28492304)
13. Lo, Y. Y. & Cruz, T. F. Involvement of reactive oxygen species in cytokine and growth factor induction of c-fos expression in chondrocytes. J. Biol. Chem. 270, 11727-11730 (1995).
14. Rajagopalan, S. et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J. Clin. Invest. 97, 1916-1923 (1996).
15. Sundaresan, M. et al. Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem. J. 318, 379-382 (1996). (Pubitemid 26305933)
16. phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J. Biol. Chem. 271, 23317-23321 (1996). (Pubitemid 26314775)
17. Suh, Y. A. et al. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82 (1999).
18. Aguirre, J. & Lambeth, J. D. Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic. Biol. Med. 49, 1342-1353 (2010).
19. phox causes vestibular and immune defects in mice. J. Clin. Invest. 118, 1176-1185 (2008). (Pubitemid 351364624)
20. Dixon, S. J. & Stockwell, B. R. The role of iron and reactive oxygen species in cell death. Nature Chem. Biol. 10, 9-17 (2014).
21. 2-dependent, reversible inactivation of peroxiredoxin III in mitochondria. Mol. Cell 46, 584-594 (2012).
22. Truong, T. H. & Carroll, K. S. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51, 9954-9965 (2012).
23. Meng, T. C., Fukada, T. & Tonks, N. K. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399 (2002). (Pubitemid 34195563)
24. Denu, J. M. & Tanner, K. G. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37, 5633-5642 (1998). (Pubitemid 28241948)
25. Paulsen, C. E. et al. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nature Chem. Biol. 8, 57-64 (2012).
26. Frijhoff, J., Dagnell, M., Godfrey, R. & Ostman, A. Regulation of protein tyrosine phosphatase oxidation in cell adhesion and migration. Antioxid. Redox Signal 20, 1994-2010 (2014).
27. Leslie, N. R. et al. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 22, 5501-5510 (2003). (Pubitemid 37279959)
28. Kwon, J. et al. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc. Natl Acad. Sci. USA 101, 16419-16424 (2004). (Pubitemid 39557728)
29. Savitsky, P. A. & Finkel, T. Redox regulation of Cdc25C. J. Biol. Chem. 277, 20535-20540 (2002). (Pubitemid 34967353)
30. Jeong, W., Bae, S. H., Toledano, M. B. & Rhee, S. G. Role of sulfiredoxin as a regulator of peroxiredoxin function and regulation of its expression. Free Radic. Biol. Med. 53, 447-456 (2012).
31. Wood, Z. A., Poole, L. B. & Karplus, P. A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653 (2003). (Pubitemid 36520591)
32. Edgar, R. S. et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459-464 (2012).
33. Chen, K., Kirber, M. T., Xiao, H., Yang, Y. & Keaney, J. F. Jr. Regulation of ROS signal transduction by NADPH oxidase 4 localization. J. Cell Biol. 181, 1129-1139 (2008). (Pubitemid 351915488)
34. Drazic, A. & Winter, J. The physiological role of reversible methionine oxidation. Biochim. Biophys. Acta http://dx.doi.org/10.1016/j.bbapap. 2014.01.001 (2014).
35. Erickson, J. R. et al. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133, 462-474 (2008). (Pubitemid 351608692)
36. Hung, R. J., Spaeth, C. S., Yesilyurt, H. G. & Terman, J. R. SelR reverses Mical-mediated oxidation of actin to regulate F-actin dynamics. Nature Cell Biol. 15, 1445-1454 (2013).
37. Lee, B. C. et al. MsrB1 and MICALs regulate actin assembly and macrophage function via reversible stereoselective methionine oxidation. Mol. Cell 51, 397-404 (2013).
38. Xanthoudakis, S. & Curran, T. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J. 11, 653-665 (1992).
39. Lee, C. et al. Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nature Struct. Mol. Biol. 11, 1179-1185 (2004).
40. Putker, M. et al. Redox-dependent control of FOXO/DAF-16 by transportin-1. Mol. Cell 49, 730-742 (2013).
41. Taguchi, K., Motohashi, H. & Yamamoto, M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16, 123-140 (2011).
42. Scherz-Shouval, R. & Elazar, Z. Monitoring starvation-induced reactive oxygen species formation. Methods Enzymol. 452, 119-130 (2009).
43. Scherz-Shouval, R. et al. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 26, 1749-1760 (2007). (Pubitemid 46624042)
44. Zhang, J. et al. A tuberous sclerosis complex signalling node at the peroxisome regulates mTORC1 and autophagy in response to ROS. Nature Cell Biol. 15, 1186-1196 (2013).
45. Ha, E. M., Oh, C. T., Bae, Y. S. & Lee, W. J. A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847-850 (2005). (Pubitemid 41567342)
46. Kumar, A. et al. Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J. 26, 4457-4466 (2007). (Pubitemid 350036625)
47. Jones, R. M. et al. Symbiotic lactobacilli stimulate gut epithelial proliferation via Nox-mediated generation of reactive oxygen species. EMBO J. 32, 3017-3028 (2013).
48. Neish, A. S. et al. Prokaryotic regulation of epithelial responses by inhibition of IκB-α ubiquitination. Science 289, 1560-1563 (2000).
49. Lee, W. J. Bacterial-modulated host immunity and stem cell activation for gut homeostasis. Genes Dev. 23, 2260-2265 (2009).
50. West, A. P. et al. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472, 476-480 (2011).
51. Bulua, A. C. et al. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J. Exp. Med. 208, 519-533 (2011).
52. Tal, M. C. et al. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl Acad. Sci. USA 106, 2770-2775 (2009).
53. Zhou, R., Yazdi, A. S., Menu, P. & Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225 (2011).
54. Sena, L. A. et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225-236 (2013).
55. Zhang, Y. et al. ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res. 23, 898-914 (2013).
56. Kobayashi, C. I. & Suda, T. Regulation of reactive oxygen species in stem cells and cancer stem cells. J. Cell. Physiol. 227, 421-430 (2012).
57. Urao, N. & Ushio-Fukai, M. Redox regulation of stem/progenitor cells and bone marrow niche. Free Radic. Biol. Med. 54, 26-39 (2013).
58. Ito, K. et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431, 997-1002 (2004). (Pubitemid 39434422)
59. Tothova, Z. et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128, 325-339 (2007). (Pubitemid 46137992)
60. Miyamoto, K. et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1, 101-112 (2007). (Pubitemid 46865800)
61. Kops, G. J. et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419, 316-321 (2002).
62. Nemoto, S. & Finkel, T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295, 2450-2452 (2002). (Pubitemid 34270258)
63. Liu, J. et al. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459, 387-392 (2009).
64. Chatoo, W. et al. The polycomb group gene Bmi1 regulates antioxidant defenses in neurons by repressing p53 pro-oxidant activity. J. Neurosci. 29, 529-542 (2009).
65. Chuikov, S., Levi, B. P., Smith, M. L. & Morrison, S. J. Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nature Cell Biol. 12, 999-1006 (2010).
66. Abbas, H. A. et al. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 7, 606-617 (2010).
67. Le Belle, J. E. et al. 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, 59-71 (2011).
68. Dickinson, B. C., Peltier, J., Stone, D., Schaffer, D. V. & Chang, C. J. Nox2 redox signaling maintains essential cell populations in the brain. Nature Chem. Biol. 7, 106-112 (2011).
69. Morimoto, H. et al. ROS are required for mouse spermatogonial stem cell self-renewal. Cell Stem Cell 12, 774-786 (2013).
70. Owusu-Ansah, E. & Banerjee, U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461, 537-541 (2009).
71. Li, T. S. & Marban, E. Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells. Stem Cells 28, 1178-1185 (2010).
72. Funato, Y., Michiue, T., Asashima, M. & Miki, H. The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-β-catenin signalling through dishevelled. Nature Cell Biol. 8, 501-508 (2006).
73. Kajla, S. et al. A crucial role for Nox 1 in redox-dependent regulation of Wnt-β-catenin signaling. FASEB J. 26, 2049-2059 (2012).
74. Hamanaka, R. B. et al. Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci. Signal 6, ra8 (2013).
75. Duncan, A. W. et al. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nature Immunol. 6, 314-322 (2005). (Pubitemid 41724769)
76. de Keizer, P. L., Burgering, B. M. & Dansen, T. B. Forkhead box o as a sensor, mediator, and regulator of redox signaling. Antioxid. Redox Signal 14, 1093-1106 (2011).
77. Coant, N. et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol. Cell. Biol. 30, 2636-2650 (2010).
78. Schroeder, E. A., Raimundo, N. & Shadel, G. S. Epigenetic silencing mediates mitochondria stress-induced longevity. Cell. Metab. 17, 954-964 (2013).
79. Lee, J. G., Baek, K., Soetandyo, N. & Ye, Y. Reversible inactivation of deubiquitinases by reactive oxygen species In vitro and in cells. Nature Commun. 4, 1568 (2013).
80. Cotto-Rios, X. M., Bekes, M., Chapman, J., Ueberheide, B. & Huang, T. T. Deubiquitinases as a signaling target of oxidative stress. Cell Rep. 2, 1475-1484 (2012).
81. Kulathu, Y. et al. Regulation of A20 and other OTU deubiquitinases by reversible oxidation. Nature Commun. 4, 1569 (2013).
82. The Alpha-Tocopherol Beta Carotene Cancer Prevention Study Group. The effect of vitamin E and β carotene on the incidence of lung cancer and other cancers in male smokers. N. Engl. J. Med. 330, 1029-1035 (1994).
83. Watson, J. Oxidants, antioxidants and the current incurability of metastatic cancers. Open Biol. 3, 120144 (2013).
84. Christofk, H. R. et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233 (2008). (Pubitemid 351380249)
85. Anastasiou, D. et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 334, 1278-1283 (2011).
86. Mathew, R. & White, E. Autophagy, stress, and cancer metabolism: what doesn't kill you makes you stronger. Cold Spring Harb. Symp. Quant. Biol. 76, 389-396 (2011).
87. Bensaad, K., Cheung, E. C. & Vousden, K. H. Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J. 28, 3015-3026 (2009).
88. Mathew, R. et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062-1075 (2009).
89. Lee, I. H. et al. Atg7 modulates p53 activity to regulate cell cycle and survival during metabolic stress. Science 336, 225-228 (2012).
90. Ishikawa, K. et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320, 661-664 (2008). (Pubitemid 351928347)
91. Irani, K. et al. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275, 1649-1652 (1997). (Pubitemid 27120541)
92. Johnson, T. M., Yu, Z. X., Ferrans, V. J., Lowenstein, R. A. & Finkel, T. Reactive oxygen species are downstream mediators of p53-dependent apoptosis. Proc. Natl Acad. Sci. USA 93, 11848-11852 (1996). (Pubitemid 26347212)
93. Polyak, K., Xia, Y., Zweier, J. L., Kinzler, K. W. & Vogelstein, B. A model for p53-induced apoptosis. Nature 389, 300-305 (1997). (Pubitemid 27406646)
94. Vigneron, A. & Vousden, K. H. p53, ROS and senescence in the control of aging. Aging 2, 471-474 (2010).
95. Lee, A. C. et al. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J. Biol. Chem. 274, 7936-7940 (1999).
96. De Nicola, G. M. et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475, 106-109 (2011).
97. Gorrini, C., Harris, I. S. & Mak, T. W. Modulation of oxidative stress as an anticancer strategy. Nature Rev. Drug Discov. 12, 931-947 (2013).
98. Balaban, R. S., Nemoto, S. & Finkel, T. Mitochondria, oxidants, and aging. Cell 120, 483-495 (2005). (Pubitemid 40269763)
99. Van Remmen, H. et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genom. 16, 29-37 (2003). (Pubitemid 38420018)
100. Yang, W., Li, J. & Hekimi, S. A. Measurable increase in oxidative damage due to reduction in superoxide detoxification fails to shorten the life span of long-lived mitochondrial mutants of Caenorhabditis elegans. Genetics 177, 2063-2074 (2007). (Pubitemid 350276988)
101. Schriner, S. E. et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308, 1909-1911 (2005). (Pubitemid 40941874)
102. Schulz, T. J. et al. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell. Metab. 6, 280-293 (2007). (Pubitemid 47468090)
103. Zarse, K. et al. Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell. Metab. 15, 451-465 (2012).
104. +/- mice. J. Biol. Chem. 283, 26217-26227 (2008).
105. Liu, X. et al. Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev. 19, 2424-2434 (2005). (Pubitemid 41483690)
106. Ishii, N. et al. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394, 694-697 (1998). (Pubitemid 28389798)
107. Baker, B. M., Nargund, A. M., Sun, T. & Haynes, C. M. Protective coupling of mitochondrial function and protein synthesis via the eIF2α kinase GCN-2. PLoS Genet. 8, e1002760 (2012).
108. Pan, Y., Schroeder, E. A., Ocampo, A., Barrientos, A. & Shadel, G. S. Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell. Metab. 13, 668-678 (2011).
109. Ristow, M. et al. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl Acad. Sci. USA 106, 8665-8670 (2009).
110. 2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix. Cell. Metab. 13, 340-350 (2011).
111. Dikalov, S. I. & Harrison, D. G. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid. Redox Signal 20, 372-382 (2014).
112. Miller, E. W., Albers, A. E., Pralle, A., Isacoff, E. Y. & Chang, C. J. Boronate-based fluorescent probes for imaging cellular hydrogen peroxide. J. Am. Chem. Soc. 127, 16652-16659 (2005). (Pubitemid 41740416)
113. Miller, E. W., Tulyathan, O., Isacoff, E. Y. & Chang, C. J. Molecular imaging of hydrogen peroxide produced for cell signaling. Nature Chem. Biol. 3, 263-267 (2007). (Pubitemid 46625830)
114. Belousov, V. V. et al. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nature Methods 3, 281-286 (2006).
115. 2 with roGFP2-based redox probes. Free Radic. Biol. Med. 51, 1943-1951 (2011).
116. Rhee, S. G., Woo, H. A., Kil, I. S. & Bae, S. H. Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. J. Biol. Chem. 287, 4403-4410 (2012).
117. Reddi, A. R. & Culotta, V. C. SOD1 integrates signals from oxygen and glucose to repress respiration. Cell 152, 224-235 (2013).
118. Bause, A. S. & Haigis, M. C. SIRT3 regulation of mitochondrial oxidative stress. Exp. Gerontol. 48, 634-639 (2013).
119. Miller, E. W., Dickinson, B. C. & Chang, C. J. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl Acad. Sci. USA 107, 15681-15686 (2010).