Nutrient Sensing and the Oxidative Stress Response

Trends in Endocrinology and Metabolism

Volumn 28, Issue 6, 2017, Pages 449-460

  Luo, Hanzhi ^a   Chiang, Hou Hsien ^a   Louw, Makensie ^a   Susanto, Albert ^b   Chen, Danica ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENERAL AMINO ACID CONTROL NON DEREPRESSIBLE 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN; REACTIVE OXYGEN METABOLITE; SIRTUIN; UNCLASSIFIED DRUG;

AGING; CALORIC RESTRICTION; CARCINOGENESIS; CELL FUNCTION; HUMAN; INNATE IMMUNITY; MALIGNANT NEOPLASM; METABOLIC REGULATION; NONHUMAN; NUTRIENT SENSING; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; STEM CELL; TISSUE DEGENERATION; ANIMAL; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; CALORIC RESTRICTION; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 85019220504     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2017.02.008     Document Type: Review

References (104)

1. McCay, C.M., Crowell, M.F., Prolonging the life span. Sci. Monthly 39 (1934), 405–414.
2. Arumugam, T.V., et al. Age and energy intake interact to modify cell stress pathways and stroke outcome. Ann. Neurol. 67 (2010), 41–52.
3. Colman, R.J., et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325 (2009), 201–204.
4. Godar, R.J., et al. Repetitive stimulation of autophagy–lysosome machinery by intermittent fasting preconditions the myocardium to ischemia–reperfusion injury. Autophagy 11 (2015), 1537–1560.
5. Longo, V.D., Mattson, M.P., Fasting: molecular mechanisms and clinical applications. Cell Metab. 19 (2014), 181–192.
6. Weindruch, R., Walford, R.L., Retardation of aging and disease by dietary restriction. 1988, C.C. Thomas.
7. Sohal, R.S., Weindruch, R., Oxidative stress, caloric restriction, and aging. Science 273 (1996), 59–63.
8. Chen, D., et al. Increase in activity during calorie restriction requires Sirt1. Science, 310, 2005, 1641.
9. Qiu, X., et al. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 12 (2010), 662–667.
10. Someya, S., et al. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143 (2010), 802–812.
11. Balaban, R.S., et al. Mitochondria, oxidants, and aging. Cell 120 (2005), 483–495.
12. Harman, D., Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11 (1956), 298–300.
13. Reczek, C.R., Chandel, N.S., ROS-dependent signal transduction. Curr. Opin. Cell Biol. 33 (2015), 8–13.
14. Chae, Y.C., et al. Landscape of the mitochondrial Hsp90 metabolome in tumours. Nat. Commun., 4, 2013, 2139.
15. Liang, Q., et al. Bioenergetic and autophagic control by Sirt3 in response to nutrient deprivation in mouse embryonic fibroblasts. Biochem. J. 454 (2013), 249–257.
16. Liu, Z., et al. Nutrient deprivation-related OXPHOS/glycolysis interconversion via HIF-1α/C-MYC pathway in U251 cells. Tumour Biol. 37 (2016), 6661–6671.
17. Bruss, M.D., et al. Calorie restriction increases fatty acid synthesis and whole body fat oxidation rates. Am. J. Physiol. Endocrinol. Metab. 298 (2010), E108–E116.
18. Nisoli, E., et al. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310 (2005), 314–317.
19. Schwer, B., Verdin, E., Conserved metabolic regulatory functions of sirtuins. Cell Metab. 7 (2008), 104–112.
20. Hallows, W.C., et al. Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol. Cell 41 (2011), 139–149.
21. Shi, T., et al. SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J. Biol. Chem. 280 (2005), 13560–13567.
22. Bell, E.L., et al. SirT3 suppresses hypoxia inducible factor 1α and tumor growth by inhibiting mitochondrial ROS production. Oncogene 30 (2011), 2986–2996.
23. Brown, K., et al. SIRT3 reverses aging-associated degeneration. Cell Rep. 3 (2013), 319–327.
24. Chen, I.C., et al. Role of SIRT3 in the regulation of redox balance during oral carcinogenesis. Mol. Cancer, 12, 2013, 68.
25. Finley, L.W., et al. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1α destabilization. Cancer Cell 19 (2011), 416–428.
26. Hirschey, M.D., et al. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol. Cell 44 (2011), 177–190.
27. Jang, Y.C., et al. Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD. Aging Cell 11 (2012), 770–782.
28. Jing, E., et al. Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 14608–14613.
29. Traba, J., et al. Fasting and refeeding differentially regulate NLRP3 inflammasome activation in human subjects. J. Clin. Invest. 125 (2015), 4592–4600.
30. Yu, W., et al. Loss of SIRT3 Provides Growth Advantage for B Cell Malignancies. J. Biol. Chem. 291 (2016), 3268–3279.
31. Cheng, A., et al. Mitochondrial SIRT3 Mediates Adaptive Responses of Neurons to Exercise and Metabolic and Excitatory Challenges. Cell Metab. 23 (2016), 128–142.
32. Tao, R., et al. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 40 (2010), 893–904.
33. Shin, J., et al. Reversible acetylation of metabolic enzymes celebration: SIRT2 and p300 join the party. Mol. Cell 43 (2011), 3–5.
34. Boily, G., et al. SirT1 regulates energy metabolism and response to caloric restriction in mice. PLoS One, 3, 2008, e1759.
35. Herranz, D., Serrano, M., SIRT1: recent lessons from mouse models. Nat. Rev. Cancer 10 (2010), 819–823.
36. Kume, S., et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 120 (2010), 1043–1055.
37. Brunet, A., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004), 2011–2015.
38. Kops, G.J., et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419 (2002), 316–321.
39. Greer, E.L., Brunet, A., Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C elegans. Aging Cell 8 (2009), 113–127.
40. Greer, E.L., et al. An AMPK–FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr. Biol. 17 (2007), 1646–1656.
41. Johnson, E.C., et al. Altered metabolism and persistent starvation behaviors caused by reduced AMPK function in Drosophila. PLoS One, 5, 2010, e12799.
42. Schulz, T.J., et al. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6 (2007), 280–293.
43. Johnson, S.C., et al. mTOR is a key modulator of ageing and age-related disease. Nature 493 (2013), 338–345.
44. Kapahi, P., et al. With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab. 11 (2010), 453–465.
45. Mirzaei, H., et al. Protein and amino acid restriction, aging and disease: from yeast to humans. Trends Endocrinol. Metab. 25 (2014), 558–566.
46. 2 resistance elicited by caloric restriction require the peroxiredoxin Tsa1 in Saccharomyces cerevisiae. Mol. Cell 43 (2011), 823–833.
47. Hardie, D.G., et al. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13 (2012), 251–262.
48. Efeyan, A., et al. Nutrient-sensing mechanisms and pathways. Nature 517 (2015), 302–310.
49. Hinnebusch, A.G., Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59 (2005), 407–450.
50. Jeon, S.M., et al. AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 485 (2012), 661–665.
51. Saito, Y., et al. AMPK protects leukemia-initiating cells in myeloid leukemias from metabolic stress in the bone marrow. Cell Stem Cell 17 (2015), 585–596.
52. Chen, C., et al. TSC–mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J. Exp. Med. 205 (2008), 2397–2408.
53. Ravindran, R., et al. The amino acid sensor GCN2 controls gut inflammation by inhibiting inflammasome activation. Nature 531 (2016), 523–527.
54. Laplante, M., Sabatini, D.M., mTOR signaling in growth control and disease. Cell 149 (2012), 274–293.
55. Morita, M., et al. mTORC1 controls mitochondrial activity and biogenesis through 4E-BP-dependent translational regulation. Cell Metab. 18 (2013), 698–711.
56. Chen, Y., et al. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 12 (2011), 534–5341.
57. Alexander, A., et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 4153–4158.
58. Hawley, S.A., et al. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab. 11 (2010), 554–565.
59. Zmijewski, J.W., et al. Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J. Biol. Chem. 285 (2010), 33154–33164.
60. Perez, V.I., et al. Is the oxidative stress theory of aging dead?. Biochim. Biophys. Acta 1790 (2009), 1005–1014.
61. Hanzen, S., et al. Lifespan control by redox-dependent recruitment of chaperones to misfolded proteins. Cell 166 (2016), 140–151.
62. Nobrega-Pereira, S., G6PD protects from oxidative damage and improves healthspan in mice. Nat. Commun., 7, 2016, 10894.
63. Kubben, N., et al. Repression of the antioxidant NRF2 pathway in premature aging. Cell 165 (2016), 1361–1374.
64. Campisi, J., Cancer and ageing: rival demons?. Nat. Rev. Cancer 3 (2003), 339–349.
65. Anastasiou, D., et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 334 (2011), 1278–1283.
66. Jiang, L., et al. Reductive carboxylation supports redox homeostasis during anchorage-independent growth. Nature 532 (2016), 255–258.
67. Kaur, A., et al. sFRP2 in the aged microenvironment drives melanoma metastasis and therapy resistance. Nature 532 (2016), 250–254.
68. Piskounova, E., et al. Oxidative stress inhibits distant metastasis by human melanoma cells. Nature 527 (2015), 186–191.
69. Yun, J., et al. Vitamin C selectively kills KRAS and BRAF mutant colorectal cancer cells by targeting GAPDH. Science 350 (2015), 1391–1396.
70. Folmes, C.D., et al. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11 (2012), 596–606.
71. Takubo, K., et al. Regulation of the HIF-1α level is essential for hematopoietic stem cells. Cell Stem Cell 7 (2010), 391–402.
72. Takubo, K., et al. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12 (2013), 49–61.
73. Naka, K., et al. TGF-β–FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 463 (2010), 676–680.
74. Mohrin, M., Chen, D., The mitochondrial metabolic checkpoint and aging of hematopoietic stem cells. Curr. Opin. Hematol. 23 (2016), 318–324.
75. Mohrin, M., et al. Stem cell aging: A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science 347 (2015), 1374–1377.
76. Juntilla, M.M., et al. AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115 (2010), 4030–4038.
77. Ito, K., et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431 (2004), 997–1002.
78. Maryanovich, M., et al. The ATM–BID pathway regulates quiescence and survival of haematopoietic stem cells. Nat. Cell Biol. 14 (2012), 535–541.
79. Jung, H., et al. TXNIP maintains the hematopoietic cell pool by switching the function of p53 under oxidative stress. Cell Metab. 18 (2013), 75–85.
80. Miyamoto, K., et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1 (2007), 101–112.
81. Tothova, Z., et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128 (2007), 325–339.
82. Tsai, J.J., et al. Nrf2 regulates haematopoietic stem cell function. Nat. Cell Biol. 15 (2013), 309–316.
83. Shin, J., et al. SIRT7 represses Myc activity to suppress ER stress and prevent fatty liver disease. Cell Rep. 5 (2013), 654–665.
84. Ito, K., et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 12 (2006), 446–451.
85. Paik, J.H., et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5 (2009), 540–553.
86. Renault, V.M., et al. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5 (2009), 527–539.
87. Webb, A.E., et al. FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. Cell Rep. 4 (2013), 477–491.
88. Yeo, H., et al. FoxO3 coordinates metabolic pathways to maintain redox balance in neural stem cells. EMBO J. 32 (2013), 2589–2602.
89. Hochmuth, C., et al. Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8 (2011), 188–199.
90. Owusu-Ansah, E., Banerjee, U., Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461 (2009), 537–541.
91. Burton, N.A., et al. Disparate impact of oxidative host defenses determines the fate of Salmonella during systemic infection in mice. Cell Host Microbe 15 (2014), 72–83.
92. Walch, M., et al. Cytotoxic cells kill intracellular bacteria through granulysin-mediated delivery of granzymes. Cell 157 (2014), 1309–1323.
93. Mills, E.L., et al. Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell 167 (2016), 457–470.
94. van der Heijden, J., Salmonella apidly regulates membrane permeability to survive oxidative stress. MBio, 7, 2016.
95. Vaubourgeix, J., et al. Stressed mycobacteria use the chaperone ClpB to sequester irreversibly oxidized proteins asymmetrically within and between cells. Cell Host Microbe 17 (2015), 178–190.
96. Gomez, J.C., et al. Nrf2 modulates host defense during streptococcus pneumoniae pneumonia in mice. J. Immunol. 197 (2016), 2864–2879.
97. Noubade, R., et al. NRROS negatively regulates reactive oxygen species during host defence and autoimmunity. Nature 509 (2014), 235–239.
98. Kim, H.S., et al. SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17 (2010), 41–52.
99. Sebastián, C., et al. The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism. Cell 151 (2012), 1185–1199.
100. Tonks, N.K., Redox redux: revisiting PTPs and the control of cell signaling. Cell 121 (2005), 667–670.
101. Grivennikov, S.I., et al. Immunity, inflammation, and cancer. Cell 140 (2010), 883–899.
102. Castilho, B.A., et al. Keeping the eIF2 alpha kinase Gcn2 in check. Biochim. Biophys. Acta 1843 (2014), 1948–1968.
103. Finkel, T., et al. Recent progress in the biology and physiology of sirtuins. Nature 460 (2009), 587–591.
104. Viollet, B., et al. AMPK: Lessons from transgenic and knockout animals. Front. Biosci. (Landmark Ed) 14 (2009), 19–44.