SOD2 and the Mitochondrial UPR: Partners Regulating Cellular Phenotypic Transitions

Trends in Biochemical Sciences

Volumn 41, Issue 7, 2016, Pages 568-577

  He, Chenxia ^a   Hart, Peter C ^a   Germain, Doris ^b   Bonini, Marcelo G ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; SIRTUIN 3; SIRTUIN 7; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; SUPEROXIDE DISMUTASE;

CELL COMMUNICATION; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL HYPOXIA; CELL ORGANELLE; CELL SPECIFICITY; CELL SURVIVAL; ENZYME ACTIVITY; ENZYME REGULATION; GLYCOLYSIS; MITOCHONDRION; NONHUMAN; PHENOTYPE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY CHAIN; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; HUMAN; METABOLISM;

ANIMALS; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA; PHENOTYPE; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; UNFOLDED PROTEIN RESPONSE;

EID: 84970028289     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.04.004     Document Type: Review

References (68)

1. 1 Shaughnessy, D.T., et al. Mitochondria, energetics, epigenetics, and cellular responses to stress. Environ. Health Perspect. 122 (2014), 1271–1278.
2. 2 Chandel, N.S., Evolution of mitochondria as signaling organelles. Cell Metab. 22 (2015), 204–206.
3. 3 Simon, M.C., Coming up for air: HIF-1 and mitochondrial oxygen consumption. Cell Metab. 3 (2006), 150–151.
4. 4 Shadel, G.S., Horvath, T.L., Mitochondrial ROS signaling in organismal homeostasis. Cell 163 (2015), 560–569.
5. 5 Lee, C., et al. The mitochondrial-derived peptide MOTS-c promotes metabolic homeostasis and reduces obesity and insulin resistance. Cell Metab. 21 (2015), 443–454.
6. 6 Guo, B., et al. Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature 423 (2003), 456–461.
7. 2 regulates the angiogenic phenotype via PTEN oxidation. J. Biol. Chem. 280 (2005), 16916–16924.
8. 8 Lee, S.R., et al. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273 (1998), 15366–15372.
9. 9 Borutaite, V., Brown, G.C., Caspases are reversibly inactivated by hydrogen peroxide. FEBS Lett. 500 (2001), 114–118.
10. 10 He, B.J., et al. Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat. Med. 17 (2011), 1610–1618.
11. 11 Hart, P.C., et al. Caveolin-1 regulates cancer cell metabolism via scavenging Nrf2 and suppressing MnSOD-driven glycolysis. Oncotarget 7 (2015), 308–322.
12. 12 Hart, P.C., et al. MnSOD upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signalling in cancer. Nat. Commun., 6, 2015, 6053.
13. 13 Sun, Y., et al. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ. Res. 105 (2009), 676–685.
14. 14 Demasi, M., et al. 20 S proteasome from Saccharomyces cerevisiae is responsive to redox modifications and is S-glutathionylated. J. Biol. Chem. 278 (2003), 679–685.
15. 2 via an antioxidant response element. FASEB J. 19 (2005), 2085–2087.
16. 16 Huang, L.E., et al. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J. Biol. Chem. 271 (1996), 32253–32259.
17. 17 Zhang, J., et al. Hydrogen peroxide activates NFκB and the interleukin-6 promoter through NFκB-inducing kinase. Antioxid. Redox Signal. 3 (2001), 493–504.
18. 18 De Bock, K., et al. Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154 (2013), 651–663.
19. 19 Kuppusamy, K.T., et al. Let-7 family of microRNA is required for maturation and adult-like metabolism in stem cell-derived cardiomyocytes. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), E2785–E2794.
20. 20 Sperber, H., et al. The metabolome regulates the epigenetic landscape during naive-to-primed human embryonic stem cell transition. Nat. Cell Biol. 17 (2015), 1523–1535.
21. 21 Folmes, C.D., et al. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab. 14 (2011), 264–271.
22. 22 Panopoulos, A.D., et al. The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res. 22 (2012), 168–177.
23. 23 Zhang, J., et al. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J. 30 (2011), 4860–4873.
24. 24 Boveris, A., Cadenas, E., Mitochondrial production of superoxide anions and its relationship to the antimycin insensitive respiration. FEBS Lett. 54 (1975), 311–314.
25. 25 Cadenas, E., et al. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch. Biochem. Biophys. 180 (1977), 248–257.
26. 26 Chouchani, E.T., et al. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515 (2014), 431–435.
27. 27 Buettner, G.R., The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Arch. Biochem. Biophys. 300 (1993), 535–543.
28. 28 Bonini, M.G., et al. Redox control of enzymatic functions: the electronics of life's circuitry. IUBMB Life., 2014, 10.1002/iub.1258 Published online March 26, 2014.
29. 29 Ochocki, J.D., Simon, M.C., Nutrient-sensing pathways and metabolic regulation in stem cells. J. Cell Biol. 203 (2013), 23–33.
30. 30 DeNicola, G.M., Cantley, L.C., Cancer's fuel choice: new flavors for a picky eater. Mol. Cell 60 (2015), 514–523.
31. 31 Chandel, N.S., et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci.U.S.A. 95 (1998), 11715–11720.
32. 32 Brunelle, J.K., et al. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 1 (2005), 409–414.
33. 33 Ding, Y., et al. Endogenous hydrogen peroxide regulates glutathione redox via nuclear factor erythroid 2-related factor 2 downstream of phosphatidylinositol 3-kinase during muscle differentiation. Am. J. Pathol. 172 (2008), 1529–1541.
34. 34 Kobayashi, M., et al. The antioxidant defense system Keap1–Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol. Cell. Biol. 29 (2009), 493–502.
35. 35 Jung, Y., et al. Dynein light chain LC8 negatively regulates NF-κB through the redox-dependent interaction with IκBα. J. Biol. Chem. 283 (2008), 23863–23871.
36. 2-mediated activation of NFκB-inducing kinase. J. Biol. Chem. 281 (2006), 1495–1505.
37. 37 Mathieu, J., et al. HIF induces human embryonic stem cell markers in cancer cells. Cancer Res. 71 (2011), 4640–4652.
38. 38 Lee, K.E., Simon, M.C., From stem cells to cancer stem cells: HIF takes the stage. Curr. Opin. Cell Biol. 24 (2012), 232–235.
39. 39 Karin, M., NF-κB as a critical link between inflammation and cancer. Cold Spring Harb. Perspect. Biol., 1, 2009, a000141.
40. 40 Iliopoulos, D., et al. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 1397–1402.
41. 41 Korkaya, H., et al. Regulation of cancer stem cells by cytokine networks: attacking cancer's inflammatory roots. Clin. Cancer Res. 17 (2011), 6125–6129.
42. 42 Jang, J., et al. Nrf2, a regulator of the proteasome, controls self-renewal and pluripotency in human embryonic stem cells. Stem Cells 32 (2014), 2616–2625.
43. 43 Katajisto, P., et al. Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348 (2015), 340–343.
44. 2 formation. Free Radic. Biol. Med. 42 (2007), 1465–1469.
45. 45 Zhao, Q., et al. A mitochondrial specific stress response in mammalian cells. EMBO J. 21 (2002), 4411–4419.
46. 46 Benedetti, C., et al. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 174 (2006), 229–239.
47. 47 Haynes, C.M., et al. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 13 (2007), 467–480.
48. mt. Mol. Cell 58 (2015), 123–133.
49. 49 Liu, Z., Butow, R.A., Mitochondrial retrograde signaling. Annu. Rev. Genet. 40 (2006), 159–185.
50. 50 Jovaisaite, V., et al. The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J. Exp. Biol. 217 (2014), 137–143.
51. 51 Bennett, C.F., et al. Activation of the mitochondrial unfolded protein response does not predict longevity in Caenorhabditis elegans. Nat. Commun., 5, 2014, 3483.
52. +/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 154 (2013), 430–441.
53. 53 Papa, L., Germain, D., SirT3 regulates the mitochondrial unfolded protein response. Mol. Cell. Biol. 34 (2014), 699–710.
54. 54 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, 41–52.
55. 55 Jin, S.M., Youle, R.J., The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 9 (2013), 1750–1757.
56. 56 Papa, L., Germain, D., Estrogen receptor mediates a distinct mitochondrial unfolded protein response. J. Cell Sci. 124 (2011), 1396–1402.
57. 57 Rimmele, P., et al. Mitochondrial metabolism in hematopoietic stem cells requires functional FOXO3. EMBO Rep. 16 (2015), 1164–1176.
58. 58 Mohrin, M., et al. Stem cell aging. A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science 347 (2015), 1374–1377.
59. 59 Semenza, G.L., Hypoxia-inducible factors in physiology and medicine. Cell 148 (2012), 399–408.
60. 60 Majmundar, A.J., et al. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40 (2010), 294–309.
61. 61 Chandel, N.S., et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275 (2000), 25130–25138.
62. 62 Zou, X., et al. MnSOD acetylation and dys-regulation, due to loss of SIRT3 activity, promotes a Luminal B-like breast carcinogenic permissive phenotype. Antioxid. Redox Signal., 2016, 10.1089/ars.2016.6641 Published online April 15, 2016.
63. 63 Zhu, Y., et al. Exploring the electrostatic repulsion model in the role of Sirt3 in directing MnSOD acetylation status and enzymatic activity. Free Radic. Biol. Med. 53 (2012), 828–833.
64. 64 Ozden, O., et al. Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging (Albany NY) 3 (2011), 102–107.
65. 65 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.
66. 66 Jin, C., et al. CDK4-mediated MnSOD activation and mitochondrial homeostasis in radioadaptive protection. Free Radic. Biol. Med. 81 (2015), 77–87.
67. 67 Ansenberger-Fricano, K., et al. The peroxidase activity of mitochondrial superoxide dismutase. Free Radic. Biol. Med. 54 (2013), 116–124.
68. 68 Ganini, D., et al. Iron incorporation into MnSOD A (bacterial Mn-dependent superoxide dismutase) leads to the formation of a peroxidase/catalase implicated in oxidative damage to bacteria. Biochim. Biophys. Acta 1850 (2015), 1795–1805.