Redox mechanisms of cardiomyocyte mitochondrial protection

Frontiers in Physiology

Volumn 6, Issue OCT, 2015, Pages

  Bartz, Raquel R ^a   Suliman, Hagir B ^a   Piantadosi, Claude A ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

Author keywords

Heart; Mitochondria; Mitochondrial biogenesis; Nitric oxide synthase; Oxidative stress; Reactive oxygen species (ROS)

Indexed keywords

CARBON MONOXIDE; DNA BINDING PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MITOCHONDRIAL DNA; NITRIC OXIDE; NUCLEAR RESPIRATORY FACTOR 1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NF E2;

BIOGENESIS; CELL PROTECTION; CELL REGENERATION; CELL TRANSPORT; CYTOPLASM; DNA BINDING; GENETIC TRANSCRIPTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HUMAN; MITOPHAGY; NONHUMAN; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEIN FUNCTION; REDOX STRESS; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84946560207     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00291     Document Type: Review

References (97)

1. Alam, J., Stewart, D., Touchard, C., Boinapally, S., Choi, A. M., and Cook, J. L. (1999). Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274, 26071-26078. doi: 10.1074/jbc.274.37.26071.
2. Anand, P., and Stamler, J. S. (2012). Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. J. Mol. Med. 90, 233-244. doi: 10.1007/s00109-012-0878-z.
3. Andersson, U., and Scarpulla, R. C. (2001). Pgc-1-related coactivator, a novel, serum-inducible coactivator of nuclear respiratory factor 1-dependent transcription in mammalian cells. Mol. Cell. Biol. 21, 3738-3749. doi: 10.1128/MCB.21.11.3738-3749.2001.
4. Aon, M. A., Cortassa, S., Marbán, E., and O'Rourke, B. (2003). Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278, 44735-44744. doi: 10.1074/jbc. M302673200.
5. Aon, M. A., Stanley, B. A., Sivakumaran, V., Kembro, J. M., O'Rourke, B., Paolocci, N., et al. (2012). Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study. J. Gen. Physiol. 139, 479-491. doi: 10.1085/jgp.201210772.
6. Balaban, R. S., Nemoto, S., and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495. doi: 10.1016/j.cell.2005.02.001.
7. Broniowska, K. A., and Hogg, N. (2012). The chemical biology of S-nitrosothiols. Antioxid. Redox Signal. 17, 969-980. doi: 10.1089/ars.2012.4590.
8. Buchwalow, I. B., Schulze, W., Kostic, M. M., Wallukat, G., and Morwinski, R. (1997). Intracellular localization of inducible nitric oxide synthase in neonatal rat cardiomyocytes in culture. Acta Histochem. 99, 231-240. doi: 10.1016/S0065-1281(97)80046-3.
9. Cadenas, E., Boveris, A., Ragan, C. I., and Stoppani, A. O. (1977). Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch. Biochem. Biophys. 180, 248-257. doi: 10.1016/0003-9861(77)90035-2.
10. Calì, T., Ottolini, D., Negro, A., and Brini, M. (2013). Enhanced parkin levels favor ER-mitochondria crosstalk and guarantee Ca(2+) transfer to sustain cell bioenergetics. Biochim. Biophys. Acta 1832, 495-508. doi: 10.1016/j.bbadis.2013.01.004.
11. Carraway, M. S., Suliman, H. B., Jones, W. S., Chen, C. W., Babiker, A., and Piantadosi, C. A. (2010). Erythropoietin activates mitochondrial biogenesis and couples red cell mass to mitochondrial mass in the heart. Circ. Res. 106, 1722-1730. doi: 10.1161/CIRCRESAHA.109.214353.
12. Carrodeguas, J. A., Yun, S., Shadel, G. S., Clayton, D. A., and Bogenhagen, D. F. (1996). Functional conservation of yeast mtTFB despite extensive sequence divergence. Gene Expr. 6, 219-230.
13. Carter, R. S., and Avadhani, N. G. (1994). Cooperative binding of GA-binding protein transcription factors to duplicated transcription initiation region repeats of the cytochrome c oxidase subunit IV gene. J. Biol. Chem. 269, 4381-4387.
14. Chang, A. L., Ulrich, A., Suliman, H. B., and Piantadosi, C. A. (2015). Redox regulation of mitophagy in the lung during murine Staphylococcus aureus sepsis. Free Radic. Biol. Med. 78, 179-189. doi: 10.1016/j.freeradbiomed.2014.10.582.
15. Chau, C. M., Evans, M. J., and Scarpulla, R. C. (1992). Nuclear respiratory factor 1 activation sites in genes encoding the gamma-subunit of ATP synthase, eukaryotic initiation factor 2 alpha, and tyrosine aminotransferase. Specific interaction of purified NRF-1 with multiple target genes. J. Biol. Chem. 267, 6999-7006.
16. Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L., and Lesnefsky, E. J. (2003). Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278, 36027-36031. doi: 10.1074/jbc. M304854200.
17. Cherry, A. D., Suliman, H. B., Bartz, R. R., and Piantadosi, C. A. (2014). Peroxisome proliferator-activated receptor gamma co-activator 1-alpha as a critical co-activator of the murine hepatic oxidative stress response and mitochondrial biogenesis in Staphylococcus aureus sepsis. J. Biol. Chem. 289, 41-52. doi: 10.1074/jbc. M113.512483.
18. Cortassa, S., O'Rourke, B., and Aon, M. A. (2014). Redox-optimized ROS balance and the relationship between mitochondrial respiration and ROS. Biochim. Biophys. Acta 1837, 287-295. doi: 10.1016/j.bbabio.2013.11.007.
19. Dairaghi, D. J., Shadel, G. S., and Clayton, D. A. (1995). Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim. Biophys. Acta 1271, 127-134. doi: 10.1016/0925-4439(95)00019-Z.
20. Darvekar, S. R., Elvenes, J., Brenne, H. B., Johansen, T., and Sjøttem, E. (2014). SPBP is a sulforaphane induced transcriptional coactivator of NRF2 regulating expression of the autophagy receptor p62/SQSTM1. PLoS ONE 9:e85262. doi: 10.1371/journal.pone.0085262.
21. Dorn, G. W. II. (2015). Mitochondrial dynamism and heart disease: changing shape and shaping change. EMBO Mol. Med. 7, 865-877. doi: 10.15252/emmm.201404575.
22. Ekstrand, M. I., Falkenberg, M., Rantanen, A., Park, C. B., Gaspari, M., Hultenby, K., et al. (2004). Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 13, 935-944. doi: 10.1093/hmg/ddh109.
23. Evans, M. J., and Scarpulla, R. C. (1990). NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 4, 1023-1034. doi: 10.1101/gad.4.6.1023.
24. Falkenberg, M., Gaspari, M., Rantanen, A., Trifunovic, A., Larsson, N. G., and Gustafsson, C. M. (2002). Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 31, 289-294. doi: 10.1038/ng909.
25. Favreau, L. V., and Pickett, C. B. (1995). The rat quinone reductase antioxidant response element. Identification of the nucleotide sequence required for basal and inducible activity and detection of antioxidant response element-binding proteins in hepatoma and non-hepatoma cell lines. J. Biol. Chem. 270, 24468-24474. doi: 10.1074/jbc.270.41.24468.
26. Ferrari, R., Cargnoni, A., Curello, S., Boffa, G. M., and Ceconi, C. (1989). Effects of iloprost (ZK 36374) on glutathione status during ischaemia and reperfusion of rabbit isolated hearts. Br. J. Pharmacol. 98, 678-684. doi: 10.1111/j.1476-5381.1989.tb12643.x.
27. Fisher-Wellman, K. H., Mattox, T. A., Thayne, K., Katunga, L. A., La Favor, J. D., Neufer, P. D., et al. (2013). Novel role for thioredoxin reductase-2 in mitochondrial redox adaptations to obesogenic diet and exercise in heart and skeletal muscle. J. Physiol. (Lond). 591, 3471-3486. doi: 10.1113/jphysiol.2013.254193.
28. Fujita, K., Maeda, D., Xiao, Q., and Srinivasula, S. M. (2011). Nrf2-mediated induction of p62 controls Toll-like receptor-4-driven aggresome-like induced structure formation and autophagic degradation. Proc. Natl. Acad. Sci. U.S.A. 108, 1427-1432. doi: 10.1073/pnas.1014156108.
29. Garnier, A., Fortin, D., Deloménie, C., Momken, I., Veksler, V., and Ventura-Clapier, R. (2003). Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J. Physiol. (Lond). 551, 491-501. doi: 10.1113/jphysiol.2003.045104.
30. Gauthier, L. D., Greenstein, J. L., Cortassa, S., O'Rourke, B., and Winslow, R. L. (2013). A computational model of reactive oxygen species and redox balance in cardiac mitochondria. Biophys. J. 105, 1045-1056. doi: 10.1016/j.bpj.2013.07.006.
31. Ghafourifar, P., Schenk, U., Klein, S. D., and Richter, C. (1999). Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J. Biol. Chem. 274, 31185-31188. doi: 10.1074/jbc.274.44.31185.
32. Giulivi, C., Poderoso, J. J., and Boveris, A. (1998). Production of nitric oxide by mitochondria. J. Biol. Chem. 273, 11038-11043. doi: 10.1074/jbc.273.18.11038.
33. Gleyzer, N., Vercauteren, K., and Scarpulla, R. C. (2005). Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol. Cell. Biol. 25, 1354-1366. doi: 10.1128/MCB.25.4.1354-1366.2005.
34. Haga, S., Ozawa, T., Yamada, Y., Morita, N., Nagashima, I., Inoue, H., et al. (2014). p62/SQSTM1 plays a protective role in oxidative injury of steatotic liver in a mouse hepatectomy model. Antioxid. Redox Signal. 21, 2515-2530. doi: 10.1089/ars.2013.5391.
35. Hamacher-Brady, A., Brady, N. R., and Gottlieb, R. A. (2006). Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J. Biol. Chem. 281, 29776-29787. doi: 10.1074/jbc. M603783200.
36. Hickson-Bick, D. L., Jones, C., and Buja, L. M. (2008). Stimulation of mitochondrial biogenesis and autophagy by lipopolysaccharide in the neonatal rat cardiomyocyte protects against programmed cell death. J. Mol. Cell. Cardiol. 44, 411-418. doi: 10.1016/j.yjmcc.2007.10.013.
37. Hogg, N., Broniowska, K. A., Novalija, J., Kettenhofen, N. J., and Novalija, E. (2007). Role of S-nitrosothiol transport in the cardioprotective effects of S-nitrosocysteine in rat hearts. Free Radic. Biol. Med. 43, 1086-1094. doi: 10.1016/j.freeradbiomed.2007.06.016.
38. Holmqvist, B., and Ekström, P. (1997). Subcellular localization of neuronal nitric oxide synthase in the brain of a teleost; an immunoelectron and confocal microscopical study. Brain Res. 745, 67-82. doi: 10.1016/S0006-8993(96)01128-6.
39. Huang, C., Andres, A. M., Ratliff, E. P., Hernandez, G., Lee, P., and Gottlieb, R. A. (2011). Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS ONE 6:e20975. doi: 10.1371/journal.pone.0020975.
40. Ide, T., Tsutsui, H., Kinugawa, S., Utsumi, H., Kang, D., Hattori, N., et al. (1999). Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ. Res. 85, 357-363. doi: 10.1161/01.RES.85.4.357.
41. Iqbal, M., Cohen, R. I., Marzouk, K., and Liu, S. F. (2002). Time course of nitric oxide, peroxynitrite, and antioxidants in the endotoxemic heart. Crit. Care Med. 30, 1291-1296. doi: 10.1097/00003246-200206000-00021.
42. Irwin, M. W., Mak, S., Mann, D. L., Qu, R., Penninger, J. M., Yan, A., et al. (1999). Tissue expression and immunolocalization of tumor necrosis factor-alpha in postinfarction dysfunctional myocardium. Circulation 99, 1492-1498. doi: 10.1161/01.CIR.99.11.1492.
43. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., et al. (1997). An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322. doi: 10.1006/bbrc.1997.6943.
44. Itoh, K., Ishii, T., Wakabayashi, N., and Yamamoto, M. (1999a). Regulatory mechanisms of cellular response to oxidative stress. Free Radic. Res. 31, 319-324. doi: 10.1080/10715769900300881.
45. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., et al. (1999b). Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86. doi: 10.1101/gad.13.1.76.
46. Jaloszynski, P., Murata, S., Shinkai, Y., Takahashi, S., Kumagai, Y., Nishimura, S., et al. (2007). Dysfunction of Nrf2 decreases KBrO3-induced oxidative DNA damage in Ogg1-null mice. Biochem. Biophys. Res. Commun. 364, 966-971. doi: 10.1016/j.bbrc.2007.10.123.
47. Jennings, R. B., and Ganote, C. E. (1976). Mitochondrial structure and function in acute myocardial ischemic injury. Circ. Res. 38, I80-I91.
48. Kanai, A. J., Pearce, L. L., Clemens, P. R., Birder, L. A., VanBibber, M. M., Choi, S. Y., et al. (2001). Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc. Natl. Acad. Sci. U.S.A. 98, 14126-14131. doi: 10.1073/pnas.241380298.
49. Kane, J. J., Murphy, M. L., Bissett, J. K., deSoyza, N., Doherty, J. E., and Straub, K. D. (1975). Mitochondrial function, oxygen extraction, epicardial S-T segment changes and tritiated digoxin distribution after reperfusion of ischemic myocardium. Am. J. Cardiol. 36, 218-224. doi: 10.1016/0002-9149(75)90530-5.
50. Kelly, D. P., and Scarpulla, R. C. (2004). Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368. doi: 10.1101/gad.1177604.
51. Kolamunne, R. T., Dias, I. H., Vernallis, A. B., Grant, M. M., and Griffiths, H. R. (2013). Nrf2 activation supports cell survival during hypoxia and hypoxia/reoxygenation in cardiomyoblasts; the roles of reactive oxygen and nitrogen species. Redox Biol. 1, 418-426. doi: 10.1016/j.redox.2013.08.002.
52. Laguens, R. P., and Gómez-Dumm, C. L. (1967). Fine structure of myocardial mitochondria in rats after exercise for one-half to two hours. Circ. Res. 21, 271-279. doi: 10.1161/01.RES.21.3.271.
53. Lancel, S., Hassoun, S. M., Favory, R., Decoster, B., Motterlini, R., and Neviere, R. (2009). Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis. J. Pharmacol. Exp. Ther. 329, 641-648. doi: 10.1124/jpet.108.148049.
54. Larsson, N. G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., et al. (1998). Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18, 231-236. doi: 10.1038/ng0398-231.
55. Lin, J., Puigserver, P., Donovan, J., Tarr, P., and Spiegelman, B. M. (2002). Peroxisome proliferator-activated receptor gamma coactivator 1beta (PGC-1beta), a novel PGC-1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 277, 1645-1648. doi: 10.1074/jbc. C100631200.
56. Liu, A., Fang, H., Wei, W., Dirsch, O., and Dahmen, U. (2014). Ischemic preconditioning protects against liver ischemia/reperfusion injury via heme oxygenase-1-mediated autophagy. Crit. Care Med. 42, e762-e771. doi: 10.1097/CCM.0000000000000659.
57. Loeper, J., Goy, J., Klein, J. M., Dufour, M., Bedu, O., Loeper, S., et al. (1991a). The evolution of oxidative stress indicators in the course of myocardial ischemia. Free Radic. Res. Commun. 12-13(Pt 2), 675-680. doi: 10.3109/10715769109145846.
58. Loeper, J., Goy, J., Rozensztajn, L., Bedu, O., and Moisson, P. (1991b). Lipid peroxidation and protective enzymes during myocardial infarction. Clin. Chim. Acta 196, 119-125. doi: 10.1016/0009-8981(91)90064-J.
59. Maines, M. D. (1988). Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2, 2557-2568.
60. Maulik, N., Sharma, H. S., and Das, D. K. (1996). Induction of the haem oxygenase gene expression during the reperfusion of ischemic rat myocardium. J. Mol. Cell. Cardiol. 28, 1261-1270. doi: 10.1006/jmcc.1996.0116.
61. McBride, A. G., Borutaité, V., and Brown, G. C. (1999). Superoxide dismutase and hydrogen peroxide cause rapid nitric oxide breakdown, peroxynitrite production and subsequent cell death. Biochim. Biophys. Acta 1454, 275-288. doi: 10.1016/S0925-4439(99)00046-0.
62. Mokranjac, D., and Neupert, W. (2009). Thirty years of protein translocation into mitochondria: unexpectedly complex and still puzzling. Biochim. Biophys. Acta 1793, 33-41. doi: 10.1016/j.bbamcr.2008.06.021.
63. Murphy, M. P. (2009). How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13. doi: 10.1042/BJ20081386.
64. Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorati, C., et al. (2003). Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299, 896-899. doi: 10.1126/science.1079368.
65. Nisoli, E., Falcone, S., Tonello, C., Cozzi, V., Palomba, L., Fiorani, M., et al. (2004). Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc. Natl. Acad. Sci. U.S.A. 101, 16507-16512. doi: 10.1073/pnas.0405432101.
66. Ozawa, K., Komatsubara, A. T., Nishimura, Y., Sawada, T., Kawafune, H., Tsumoto, H., et al. (2013). S-nitrosylation regulates mitochondrial quality control via activation of parkin. Sci. Rep. 3:2202. doi: 10.1038/srep02202.
67. Palmeira, C. M., Serrano, J., Kuehl, D. W., and Wallace, K. B. (1997). Preferential oxidation of cardiac mitochondrial DNA following acute intoxication with doxorubicin. Biochim. Biophys. Acta 1321, 101-106. doi: 10.1016/S0005-2728(97)00055-8.
68. Paolocci, N., Biondi, R., Bettini, M., Lee, C. I., Berlowitz, C. O., Rossi, R., et al. (2001). Oxygen radical-mediated reduction in basal and agonist-evoked NO release in isolated rat heart. J. Mol. Cell. Cardiol. 33, 671-679. doi: 10.1006/jmcc.2000.1334.
69. Piantadosi, C. A. (2012). Regulation of mitochondrial processes by protein S-nitrosylation. Biochim. Biophys. Acta 1820, 712-721. doi: 10.1016/j.bbagen.2011.03.008.
70. Piantadosi, C. A., Carraway, M. S., Babiker, A., and Suliman, H. B. (2008). Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ. Res. 103, 1232-1240. doi: 10.1161/01.RES.0000338597.71702.ad.
71. Prestera, T., Talalay, P., Alam, J., Ahn, Y. I., Lee, P. J., and Choi, A. M. (1995). Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: regulation by upstream antioxidant-responsive elements (ARE). Mol. Med. 1, 827-837.
72. Rushmore, T. H., Morton, M. R., and Pickett, C. B. (1991). The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266, 11632-11639.
73. Scarpulla, R. C. (1997). Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomembr. 29, 109-119. doi: 10.1023/A:1022681828846.
74. Scarpulla, R. C. (2002). Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim. Biophys. Acta 1576, 1-14. doi: 10.1016/S0167-4781(02)00343-3.
75. Shadel, G. S., and Clayton, D. A. (1996). Isolation and characterization of vertebrate mitochondrial transcription factor A homologs. Meth. Enzymol. 264, 149-158. doi: 10.1016/S0076-6879(96)64016-6.
76. Sharma, H. S., Maulik, N., Gho, B. C., Das, D. K., and Verdouw, P. D. (1996). Coordinated expression of heme oxygenase-1 and ubiquitin in the porcine heart subjected to ischemia and reperfusion. Mol. Cell. Biochem. 157, 111-116. doi: 10.1007/BF00227888.
77. Signorile, A., Micelli, L., De Rasmo, D., Santeramo, A., Papa, F., Ficarella, R., et al. (2014). Regulation of the biogenesis of OXPHOS complexes in cell transition from replicating to quiescent state: involvement of PKA and effect of hydroxytyrosol. Biochim. Biophys. Acta 1843, 675-684. doi: 10.1016/j.bbamcr.2013.12.017.
78. Song, M., Mihara, K., Chen, Y., Scorrano, L., and Dorn, G. W. II. (2015). Mitochondrial fission and fusion factors reciprocally orchestrate mitophagic culling in mouse hearts and cultured fibroblasts. Cell Metab. 21, 273-285. doi: 10.1016/j.cmet.2014.12.011.
79. Stamler, J. S., Lamas, S., and Fang, F. C. (2001). Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106, 675-683. doi: 10.1016/S0092-8674(01)00495-0.
80. Stanley, B. A., Sivakumaran, V., Shi, S., McDonald, I., Lloyd, D., Watson, W. H., et al. (2011). Thioredoxin reductase-2 is essential for keeping low levels of H(2)O(2) emission from isolated heart mitochondria. J. Biol. Chem. 286, 33669-33677. doi: 10.1074/jbc. M111.284612.
81. Stepkowski, T. M., and Kruszewski, M. K. (2011). Molecular cross-talk between the NRF2/KEAP1 signaling pathway, autophagy, and apoptosis. Free Radic. Biol. Med. 50, 1186-1195. doi: 10.1016/j.freeradbiomed.2011.01.033.
82. Strohecker, A. M., and White, E. (2014). Autophagy promotes BrafV600E-driven lung tumorigenesis by preserving mitochondrial metabolism. Autophagy 10, 384-385. doi: 10.4161/auto.27320.
83. Suliman, H. B., Carraway, M. S., Ali, A. S., Reynolds, C. M., Welty-Wolf, K. E., and Piantadosi, C. A. (2007a). The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy. J. Clin. Invest. 117, 3730-3741. doi: 10.1172/jci32967.
84. Suliman, H. B., Carraway, M. S., Tatro, L. G., and Piantadosi, C. A. (2007b). A new activating role for CO in cardiac mitochondrial biogenesis. J. Cell Sci. 120, 299-308. doi: 10.1242/jcs.03318.
85. Suliman, H. B., Sweeney, T. E., Withers, C. M., and Piantadosi, C. A. (2010). Co-regulation of nuclear respiratory factor-1 by NFkappaB and CREB links LPS-induced inflammation to mitochondrial biogenesis. J. Cell Sci. 123, 2565-2575. doi: 10.1242/jcs.064089.
86. Suliman, H. B., Welty-Wolf, K. E., Carraway, M., Tatro, L., and Piantadosi, C. A. (2004). Lipopolysaccharide induces oxidative cardiac mitochondrial damage and biogenesis. Cardiovasc. Res. 64, 279-288. doi: 10.1016/j.cardiores.2004.07.005.
87. Sun, J., Nguyen, T., Aponte, A. M., Menazza, S., Kohr, M. J., Roth, D. M., et al. (2015). Ischaemic preconditioning preferentially increases protein S-nitrosylation in subsarcolemmal mitochondria. Cardiovasc. Res. 106, 227-236. doi: 10.1093/cvr/cvv044.
88. Supinski, G. S., Murphy, M. P., and Callahan, L. A. (2009). MitoQ administration prevents endotoxin-induced cardiac dysfunction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R1095-R1102. doi: 10.1152/ajpregu.90902.2008.
89. Turrens, J. F., Alexandre, A., and Lehninger, A. L. (1985). Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 237, 408-414. doi: 10.1016/0003-9861(85)90293-0.
90. Unuma, K., Aki, T., Funakoshi, T., Yoshida, K., and Uemura, K. (2013a). Cobalt protoporphyrin accelerates TFEB activation and lysosome reformation during LPS-induced septic insults in the rat heart. PLoS ONE 8:e56526. doi: 10.1371/journal.pone.0056526.
91. Unuma, K., Aki, T., Matsuda, S., Funakoshi, T., Yoshida, K., and Uemura, K. (2013b). Inducer of heme oxygenase-1 cobalt protoporphyrin accelerates autophagy and suppresses oxidative damages during lipopolysaccharide treatment in rat liver. Hepatol. Res. 43, 91-96. doi: 10.1111/j.1872-034X.2012.01049.x.
92. Vercauteren, K., Gleyzer, N., and Scarpulla, R. C. (2008). PGC-1-related coactivator complexes with HCF-1 and NRF-2beta in mediating NRF-2(GABP)-dependent respiratory gene expression. J. Biol. Chem. 283, 12102-12111. doi: 10.1074/jbc. M710150200.
93. Vettor, R., Valerio, A., Ragni, M., Trevellin, E., Granzotto, M., Olivieri, M., et al. (2014). Exercise training boosts eNOS-dependent mitochondrial biogenesis in mouse heart: role in adaptation of glucose metabolism. Am. J. Physiol. Endocrinol. Metab. 306, E519-E528. doi: 10.1152/ajpendo.00617.2013.
94. Virbasius, J. V., and Scarpulla, R. C. (1994). Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Natl. Acad. Sci. U.S.A. 91, 1309-1313. doi: 10.1073/pnas.91.4.1309.
95. West, M. B., Rokosh, G., Obal, D., Velayutham, M., Xuan, Y. T., Hill, B. G., et al. (2008). Cardiac myocyte-specific expression of inducible nitric oxide synthase protects against ischemia/reperfusion injury by preventing mitochondrial permeability transition. Circulation 118, 1970-1978. doi: 10.1161/CIRCULATIONAHA.108.791533.
96. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., et al. (1999). Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124. doi: 10.1016/S0092-8674(00)80611-X.
97. Zhao, Y., Zhang, L., Qiao, Y., Zhou, X., Wu, G., Wang, L., et al. (2013). Heme oxygenase-1 prevents cardiac dysfunction in streptozotocin-diabetic mice by reducing inflammation, oxidative stress, apoptosis and enhancing autophagy. PLoS ONE 8:e75927. doi: 10.1371/journal.pone.0075927.