Carbon monoxide and mitochondria-modulation of cell metabolism, redox response and cell death

Frontiers in Physiology

Volumn 6, Issue FEB, 2015, Pages

  Almeida, Ana S ^a,b,c   Figueiredo Pereira, Cláudia ^a   Vieira, Helena L A ^a,c  

^a NOVA MEDICAL SCHOOL   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

Author keywords

Carbon monoxide; Cytochrome c oxidase; Gasotransmitters; Mitochondria; Mitochondrial biogenesis; Mitochondrial metabolism; Programmed cell death; Reactive oxygen species

Indexed keywords

CARBON MONOXIDE; CYTOCHROME C OXIDASE; ION CHANNEL; REACTIVE OXYGEN METABOLITE;

BIOGENESIS; CELL DEATH; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CELL METABOLISM; CELL PROTECTION; ENZYME ACTIVITY; HUMAN; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; REDOX STRESS; SHORT SURVEY; SIGNAL TRANSDUCTION;

EID: 84926506367     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00033     Document Type: Short Survey

References (51)

1. Ajioka, R. S., Phillips, J. D., and Kushner, J. P. (2006). Biosynthesis of heme in mammals. Biochim. Biophys. Acta 1763, 723-736. doi: 10.1016/j.bbamcr.2006.05.005
2. Almeida, A. S., Queiroga, C. S. F., Sousa, M. F. Q., Alves, P. M., and Vieira, H. L. A. (2012). Carbon monoxide modulates apoptosis by reinforcing oxidative metabolism in astrocytes: role of Bcl-2. J. Biol. Chem. 287, 10761-10770. doi: 10.1074/jbc.M111.306738
3. Bilban, M., Haschemi, A., Wegiel, B., Chin, B. Y., Wagner, O., and Otterbein, L. E. (2008). Heme oxygenase and carbon monoxide initiate homeostatic signaling. J. Mol. Med. 86, 267-279. doi: 10.1007/s00109-007-0276-0
4. Boczkowski, J., Poderoso, J. J., and Motterlini, R. (2006). CO-metal interaction: vital signaling from a lethal gas. Trends Biochem. Sci. 31, 614-621. doi: 10.1016/j.tibs.2006.09.001
5. Brown, S. D., and Piantadosi, C. A. (1990). In vivo binding of carbon monoxide to cytochrome c oxidase in rat brain. J. Appl. Physiol. 68, 604-610.
6. Chance, B., Erecinska, M., and Wagner, M. (1970). Mitochondrial responses to carbon monoxide toxicity. Ann. N.Y. Acad. Sci. 174, 193-204. doi: 10.1111/j.1749-6632.1970.tb49786.x
7. Chin, B. Y., Jiang, G., Wegiel, B., Wang, H. J., Macdonald, T., Zhang, X. C., et al. (2007). Hypoxia-inducible factor 1alpha stabilization by carbon monoxide results in cytoprotective preconditioning. Proc. Natl. Acad. Sci. U.S.A. 104, 5109-5114. doi: 10.1073/pnas.0609611104
8. Dallas, M. L., Boyle, J. P., Milligan, C. J., Sayer, R., Kerrigan, T. L., McKinstry, C., et al. (2011). Carbon monoxide protects against oxidant-induced apoptosis via inhibition of Kv2.1. FASEB J. 25, 1519-1530. doi: 10.1096/fj.10-173450
9. Dallas, M. L., Scragg, J. L., and Peers, C. (2009). Inhibition of L-type Ca(2+) channels by carbon monoxide. Adv. Exp. Med. Biol. 648, 89-95. doi: 10.1007/978-90-481-2259-2_10
10. D'Amico, G., Lam, F., Hagen, T., and Moncada, S. (2006). Inhibition of cellular respiration by endogenously produced carbon monoxide. J. Cell Sci. 119, 2291-2298. doi: 10.1242/jcs.02914
11. Di Noia, M. A., Van Driesche, S., Palmieri, F., Yang, L.-M., Quan, S., Goodman, A. I., et al. (2006). Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J. Biol. Chem. 281, 15687-15693. doi: 10.1074/jbc.M510595200
12. Dore, S., Takahashi, M., Ferris, C. D., Zakhary, R., Hester, L. D., Guastella, D., et al. (1999). Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl. Acad. Sci. U.S.A. 96, 2445-2450. doi: 10.1073/pnas.96.5.2445
13. Fukuda, R., Zhang, H., Kim, J. W., Shimoda, L., Dang, C. V., and Semenza, G. L. (2007). HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129, 111-122. doi: 10.1016/j.cell.2007.01.047
14. Galluzzi, L., Kepp, O., and Kroemer, G. (2012). Mitochondria: master regulators of danger signalling. Nat. Rev. Mol. Cell Biol. 13, 780-788. doi: 10.1038/nrm3479
15. Gozzelino, R., Jeney, V., and Soares, M. P. (2010). Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol. 50, 323-354. doi: 10.1146/annurev.pharmtox.010909.105600
16. Iacono, L. L., Boczkowski, J., Zini, R., Salouage, I., Berdeaux, A., Motterlini, R., et al. (2011). A carbon monoxide-releasing molecule (CORM-3) uncouples mitochondrial respiration and modulates the production of reactive oxygen species. Free Radic. Biol. Med. 50, 1556-1564. doi: 10.1016/j.freeradbiomed.2011.02.033
17. Iheagwara, K. N., Thom, S. R., Deutschman, C. S., and Levy, R. J. (2007). Myocardial cytochrome oxidase activity is decreased following carbon monoxide exposure. Biochim. Biophys. Acta 1772, 1112-1116. doi: 10.1016/j.bbadis.2007.06.002
18. Kim, H. S., Loughran, P. A., Rao, J., Billiar, T. R., and Zuckerbraun, B. S. (2008). Carbon monoxide activates NF-kappaB via ROS generation and Akt pathways to protect against cell death of hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G146-G152. doi: 10.1152/ajpgi.00105.2007
19. Kroemer, G., Galluzzi, L., and Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99-163. doi: 10.1152/physrev.00013.2006
20. Lakkisto, P., Kyto, V., Forsten, H., Siren, J. M., Segersvard, H., Voipio-Pulkki, L. M., et al. (2010). Heme oxygenase-1 and carbon monoxide promote neovascularization after myocardial infarction by modulating the expression of HIF-1alpha, SDF-1alpha and VEGF-B. Eur. J. Pharmacol. 635, 156-164. doi: 10.1016/j.ejphar.2010.02.050
21. 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
22. Li, M. H., Cha, Y. N., and Surh, Y. J. (2006). Carbon monoxide protects PC12 cells from peroxynitrite-induced apoptotic death by preventing the depolarization of mitochondrial transmembrane potential. Biochem. Biophys. Res. Commun. 342, 984-990. doi: 10.1016/j.bbrc.2006.02.046
23. Long, R., Salouage, I., Berdeaux, A., Motterlini, R., and Morin, D. (2014). CORM-3, a water soluble CO-releasing molecule, uncouples mitochondrial respiration via interaction with the phosphate carrier. Biochim. Biophys. Acta 1837, 201-209. doi: 10.1016/j.bbabio.2013.10.002
24. MacGarvey, N. C., Suliman, H. B., Bartz, R. R., Fu, P., Withers, C. M., Welty-Wolf, K. E., et al. (2012). Activation of mitochondrial biogenesis by heme oxygenase-1-mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis. Am. J. Respir. Crit. Care Med. 185, 851-861. doi: 10.1164/rccm.201106-1152OC
25. Motterlini, R., and Otterbein, L. E. (2010). The therapeutic potential of carbon monoxide. Nat. Rev. Drug Discov. 9, 728-743. doi: 10.1038/nrd3228
26. Naon, D., and Scorrano, L. (2014). At the right distance: ER-mitochondria juxtaposition in cell life and death. Biochim. Biophys. Acta 1843, 2184-2194. doi: 10.1016/j.bbamcr.2014.05.011
27. Peers, C., Boyle, J. P., Scragg, J. L., Dallas, M. L., Al-Owais, M. M., Hettiarachichi, N. T., et al. (2014). Diverse mechanisms underlying the regulation of ion channels by carbon monoxide. Br. J. Pharmacol. doi: 10.1111/bph.12760. [Epub ahead of print].
28. 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
29. Piantadosi, C. A., and Suliman, H. B. (2012). Redox regulation of mitochondrial biogenesis. Free Radic. Biol. Med. 53, 2043-2053. doi: 10.1016/j.freeradbiomed.2012.09.014
30. Queiroga, C. S., Almeida, A. S., Alves, P. M., Brenner, C., and Vieira, H. L. (2011). Carbon monoxide prevents hepatic mitochondrial membrane permeabilization. BMC Cell Biol. 12:10. doi: 10.1186/1471-2121-12-10
31. Queiroga, C. S., Almeida, A. S., Martel, C., Brenner, C., Alves, P. M., and Vieira, H. L. (2010). Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilisation and apoptosis. J. Biol. Chem. 285, 17077-17088. doi: 10.1074/jbc.M109.065052
32. Queiroga, C. S. F., Almeida, A. S., and Vieira, H. L. A. (2012). Carbon monoxide targeting mitochondria. Biochem. Res. Int. 2012, 1-9. doi: 10.1155/2012/749845
33. Queiroga, C. S. F., Vercelli, A., and Vieira, H. L. A. (2014). Carbon monoxide and the CNS: challenges and achievements. Br. J. Pharmacol. doi: 10.1111/bph.12729. [Epub ahead of print].
34. Rhodes, M. A., Carraway, M. S., Piantadosi, C. A., Reynolds, C. M., Cherry, A. D., Wester, T. E., et al. (2009). Carbon monoxide, skeletal muscle oxidative stress, and mitochondrial biogenesis in humans. Am. J. Physiol. Heart Circ. Physiol. 297, H392-H399. doi: 10.1152/ajpheart.00164.2009
35. Rodella, L., Lamon, B. D., Rezzani, R., Sangras, B., Goodman, A. I., Falck, J. R., et al. (2006). Carbon monoxide and biliverdin prevent endothelial cell sloughing in rats with type I diabetes. Free Radic. Biol. Med. 40, 2198-2205. doi: 10.1016/j.freeradbiomed.2006.02.018
36. Romao, C. C., Blattler, W. A., Seixas, J. D., and Bernardes, G. J. (2012). Developing drug molecules for therapy with carbon monoxide. Chem. Soc. Rev. 41, 3571-3583. doi: 10.1039/c2cs15317c
37. Romão, C. C., and Vieira, H. L. A. (2013). "Metal Carbonyls for CO-based Therapies: challenges and successes," in Advances in Organometallic Chemistry and Catalysis ICOMC Silver/Gold Jubilee Book, ed A. J. L. Pombeiro (Wiley-Blackwell), 545-561.
38. Ryter, S. W. (2006). Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86, 583-650. doi: 10.1152/physrev.00011.2005
39. Scragg, J. L., Dallas, M. L., Wilkinson, J. A., Varadi, G., and Peers, C. (2008). Carbon monoxide inhibits l-type Ca2+ channels via redox modulation of key cysteine residues by mitochondrial reactive oxygen species. J. Biol. Chem. 283, 24412-24419. doi: 10.1074/jbc.M803037200
40. Shigezane, J., Kita, T., and Furuya, Y. (1989). Acute and chronic effects of carbon monoxide on mitochondrial function. Igaku Kenkyu 59, 35-45.
41. Sjostrand, T. (1949). Endogenous formation of carbon monoxide in man. Nature 164, 580. doi: 10.1038/164580a0
42. 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
43. 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
44. Taillé, C., El-Benna, J., Lanone, S., Boczkowski, J., and Motterlini, R. (2005). Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle. J. Biol. Chem. 280, 25350-25360. doi: 10.1074/jbc.M503512200
45. Tang, X. D., Xu, R., Reynolds, M. F., Garcia, M. L., Heinemann, S. H., and Hoshi, T. (2003). Haem can bind to and inhibit mammalian calcium-dependent Slo1 BK channels. Nature 425, 531-535. doi: 10.1038/nature02003
46. Tenhunen, R., Marver, H. S., and Schmid, R. (1968). The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl. Acad. Sci. U.S.A. 61, 748-755. doi: 10.1073/pnas.61.2.748
47. Vieira, H. L., Queiroga, C. S., and Alves, P. M. (2008). Preconditioning induced by carbon monoxide provides neuronal protection against Apoptosis. J. Neurochem. 107, 375-384. doi: 10.1111/j.1471-4159.2008.05610.x
48. Wang, X., Wang, Y., Kim, H. P., Nakahira, K., Ryter, S. W., and Choi, A. M. K. (2007). Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J. Biol. Chem. 282, 1718-1726. doi: 10.1074/jbc.M607610200
49. Yeh, P.-Y., Li, C.-Y., Hsieh, C.-W., Yang, Y.-C., Yang, P.-M., and Wung, B. -S. (2014). CO-releasing molecules and increased heme oxygenase-1 induce protein S-glutathionylation to modulate NF-? B activity in endothelial cells. Free Radic. Biol. Med. 70, 1-13. doi: 10.1016/j.freeradbiomed.2014.01.042
50. Zheng, M., Kim, S.-K., Joe, Y., Back, S. H., Cho, H. R., Kim, H. P., et al. (2012). Sensing endoplasmic reticulum stress by protein kinase RNA-like endoplasmic reticulum kinase promotes adaptive mitochondrial DNA biogenesis and cell survival via heme oxygenase-1/carbon monoxide activity. FASEB J. 26, 2558-2568. doi: 10.1096/fj.11-199604
51. Zuckerbraun, B. S., Chin, B. Y., Bilban, M., de Costa d'Avila, J., Rao, J., Billiar, T. R., et al. (2007). Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. FASEB J. 21, 1099-1106. doi: 10.1096/fj.06-6644com