Dual Role of ROS as Signal and Stress Agents: Iron Tips the Balance in favor of Toxic Effects

Oxidative Medicine and Cellular Longevity

Volumn 2016, Issue , 2016, Pages

  Gammella, Elena ^a   Recalcati, Stefania ^a   Cairo, Gaetano ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; IRON; OXYGEN; PHYSIOLOGY;

AEROBIC CONDITION; HYDROXYL RADICALS; IRON HOMEOSTASIS; MULTIFACETED SYSTEMS; OXIDATIVE DAMAGE; PATHOPHYSIOLOGICAL; REACTIVE OXYGEN SPECIES; STORAGE PROTEINS;

IRON COMPOUNDS;

ANTHRACYCLINE; IRON; REACTIVE OXYGEN METABOLITE;

CARDIOTOXICITY; CELL LEVEL; DEGENERATIVE DISEASE; HUMAN; IRON BALANCE; IRON BLOOD LEVEL; IRON METABOLISM; IRON OVERLOAD; IRON RESPONSIVE ELEMENT; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; ACTIVE TRANSPORT; ANIMAL; METABOLISM;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; HUMANS; IRON; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84960969420     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2016/8629024     Document Type: Review

References (73)

1. B. Halliwell and J. M. C. Gutteridge, "Oxygen toxicity, oxygen radicals, transition metals and disease, " Biochemical Journal, vol. 219, no. 1, pp. 1-14, 1984.
2. D. Trachootham, W. Lu, M. A. Ogasawara, N. R.-D. Valle, and P. Huang, "Redox regulation of cell survival, " Antioxidants and Redox Signaling, vol. 10, no. 8, pp. 1343-1374, 2008.
3. T. Finkel, "Signal transduction by mitochondrial oxidants, " The Journal of Biological Chemistry, vol. 287, no. 7, pp. 4434-4440, 2012.
4. G. Shadel and T. Horvath, "Mitochondrial ROS signaling in organismal homeostasis, " Cell, vol. 163, no. 3, pp. 560-569, 2015.
5. B. Harwell, "Biochemistry of oxidative stress, " Biochemical Society Transactions, vol. 35, no. 5, pp. 1147-1150, 2007.
6. S. J. Dixon, K. M. Lemberg, M. R. Lamprecht et al., "Ferroptosis: an iron-dependent form of nonapoptotic cell death, " Cell, vol. 149, no. 5, pp. 1060-1072, 2012.
7. S. J. Dixon, D. Patel, M. Welsch et al., "Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis, " eLife, vol. 2014, no. 3, 2014.
8. J. P. Friedmann Angeli, M. Schneider, B. Proneth et al., "Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice, " Nature Cell Biology, vol. 16, no. 12, pp. 1180-1191, 2014.
9. M. Gao, P. Monian, N. Quadri, R. Ramasamy, and X. Jiang, "Glutaminolysis and transferrin regulate ferroptosis, "Molecular Cell, vol. 59, no. 2, pp. 298-308, 2015.
10. X. Sun, Z. Ou, R. Chen et al., "Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells, " Hepatology, vol. 63, no. 1, pp. 173-184, 2016.
11. G. Cairo, F. Bernuzzi, and S. Recalcati, "A precious metal: iron, an essential nutrient for all cells, " Genes & Nutrition, vol. 1, no. 1, pp. 25-39, 2006.
12. A. D. Sheftel, A. B. Mason, and P. Ponka, "The long history of iron in the Universe and in health and disease, " Biochimica et Biophysica Acta (BBA)-General Subjects, vol. 1820, no. 3, pp. 161-187, 2012.
13. N. C. Andrews, "Forging a field: the golden age of iron biology, " Blood, vol. 112, no. 2, pp. 219-230, 2008.
14. M. W. Hentze, M. U. Muckenthaler, B. Galy, andC. Camaschella, "Two to tango: regulation of Mammalian iron metabolism, " Cell, vol. 142, no. 1, pp. 24-38, 2010.
15. G. Cairo and S. Recalcati, "Iron-regulatory proteins: molecular biology and pathophysiological implications, " Expert Reviews in Molecular Medicine, vol. 9, no. 33, pp. 1-13, 2007.
16. S. Recalcati, G. Minotti, and G. Cairo, "Iron regulatory proteins: from molecular mechanisms to drug development, " Antioxidants and Redox Signaling, vol. 13, no. 10, pp. 1593-1616, 2010.
17. R. C. Hider and X. Kong, "Iron speciation in the cytosol: an overview, " Dalton Transactions, vol. 42, no. 9, pp. 3220-3229, 2013.
18. T. Moroishi, M. Nishiyama, Y. Takeda, K. Iwai, and K. I. Nakayama, "The FBXL5-IRP2 axis is integral to control of iron metabolism in vivo, " CellMetabolism, vol. 14, no. 3, pp. 339-351, 2011.
19. J. C. Ruiz and R. K. Bruick, "F-box and leucine-rich repeat protein 5 (FBXL5): sensing intracellular iron and oxygen, " Journal of Inorganic Biochemistry, vol. 133, pp. 73-77, 2014.
20. S. Recalcati, E. Gammella, and G. Cairo, "New perspectives on the molecular basis of the interaction between oxygen homeostasis and iron metabolism, " Hypoxia, vol. 3, pp. 93-103, 2015.
21. M. U. Muckenthaler, B. Galy, andM. W. Hentze, "Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network, " Annual Review ofNutrition, vol. 28, pp. 197-213, 2008.
22. N. Wilkinson and K. Pantopoulos, "TheIRP/IRE system in vivo: insights from mouse models, " Frontiers in Pharmacology, vol. 5, article 176, 2014.
23. S. Recalcati, A. Alberghini, A. Campanella et al., "Iron regulatory proteins 1 and 2 in human monocytes, macrophages and duodenum: expression and regulation in hereditary hemochromatosis and iron deficiency, " Haematologica, vol. 91, no. 3, pp. 303-310, 2006.
24. D.-L. Zhang, M. C. Ghosh, andT. A. Rouault, "Thephysiological functions of iron regulatory proteins in iron homeostasis-an update, " Frontiers in Pharmacology, vol. 5, article 124, 2014.
25. G. Cairo, S. Recalcati, A. Pietrangelo, and G. Minotti, "The iron regulatory proteins: targets and modulators of free radical reactions and oxidative damage, " Free Radical Biology and Medicine, vol. 32, no. 12, pp. 1237-1243, 2002.
26. P. Arosio, F. Carmona, R. Gozzelino, F. Maccarinelli, and M. Poli, "The importance of eukaryotic ferritins in iron handling and cytoprotection, " Biochemical Journal, vol. 472, no. 1, pp. 1-15, 2015.
27. C. P. Anderson, M. Shen, R. S. Eisenstein, and E. A. Leibold, "Mammalian ironmetabolismand its control by iron regulatory proteins, " Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, vol. 1823, no. 9, pp. 1468-1483, 2012.
28. K. Pantopoulos, S. K. Porwal, A. Tartakoff, and L. Devireddy, "Mechanisms of mammalian iron homeostasis, " Biochemistry, vol. 51, no. 29, pp. 5705-5724, 2012.
29. L. C. Kühn, "Iron regulatory proteins and their role in controlling iron metabolism, " Metallomics, vol. 7, no. 2, pp. 232-243, 2015.
30. T. A. Rouault, "Iron metabolism in the CNS: implications for neurodegenerative diseases, " Nature Reviews Neuroscience, vol. 14, no. 8, pp. 551-564, 2013.
31. G. Isaya, "Mitochondrial iron-sulfur cluster dysfunction in neurodegenerative disease, " Frontiers in Pharmacology, vol. 5, article 29, 2014.
32. L. Zecca, M. B. H. Youdim, P. Riederer, J. R. Connor, and R. R. Crichton, "Iron, brain ageing and neurodegenerative disorders, " Nature Reviews Neuroscience, vol. 5, no. 11, pp. 863-873, 2004.
33. A. Martelli and H. Puccio, "Dysregulation of cellular iron metabolism in Friedreich ataxia: from primary iron-sulfur cluster deficit tomitochondrial iron accumulation, " Frontiers in Pharmacology, vol. 5, article 130, 2014.
34. V. Campuzano, L. Montermini, M. D. Moltò et al., "Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion, " Science, vol. 271, no. 5254, pp. 1423-1427, 1996.
35. R. A. Vaubel and G. Isaya, "Iron-sulfur cluster synthesis, iron homeostasis and oxidative stress in Friedreich ataxia, "Molecular and Cellular Neuroscience, vol. 55, pp. 50-61, 2013.
36. P. Arosio and S. Levi, "Cytosolic and mitochondrial ferritins in the regulation of cellular iron homeostasis and oxidative damage, " Biochimica et Biophysica Acta (BBA)-General Subjects, vol. 1800, no. 8, pp. 783-792, 2010.
37. A. Campanella, G. Isaya, H. A. O'Neill et al., "The expression of human mitochondrial ferritin rescues respiratory function in frataxin-deficient yeast, " HumanMolecular Genetics, vol. 13, no. 19, pp. 2279-2288, 2004.
38. Z. I. Cabantchik, "Labile iron in cells and body fluids: physiology, pathology, and pharmacology, " Frontiers in Pharmacology, vol. 5, article 45, 2014.
39. G. Minotti, P. Menna, E. Salvatorelli, G. Cairo, and L. Gianni, "Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity, " Pharmacological Reviews, vol. 56, no. 2, pp. 185-229, 2004.
40. P. Menna, S. Recalcati, G. Cairo, and G. Minotti, "An introduction to the metabolic determinants of anthracycline cardiotoxicity, " Cardiovascular Toxicology, vol. 7, no. 2, pp. 80-85, 2007.
41. E. Gammella, S. Recalcati, I. Rybinska, P. Buratti, and G. Cairo, "Iron-induced damage in cardiomyopathy: oxidativedependent and independent mechanisms, " Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 230182, 10 pages, 2015.
42. G. Minotti, G. Cairo, and E. Monti, "Role of iron in anthracycline cardiotoxicity: new tunes for an old song" The FASEB Journal, vol. 13, no. 2, pp. 199-212, 1999.
43. M. ?St?erba, O. Popelová, A. Vávrová et al., "Oxidative stress, redox signaling, and metal chelation in anthracycline cardiotoxicity and pharmacological cardioprotection, " Antioxidants and Redox Signaling, vol. 18, no. 8, pp. 899-929, 2013.
44. F. Bernuzzi, S. Recalcati, A. Alberghini, and G. Cairo, "Reactive oxygen species-independent apoptosis in doxorubicintreatedH9c2 cardiomyocytes: role for heme oxygenase-1 downmodulation, " Chemico-Biological Interactions, vol. 177, no. 1, pp. 12-20, 2009.
45. R. D. Spagnuolo, S. Recalcati, L. Tacchini, and G. Cairo, "Role of hypoxia-inducible factors in the dexrazoxane-mediated protection of cardiomyocytes from doxorubicin-induced toxicity, " British Journal of Pharmacology, vol. 163, no. 2, pp. 299-312, 2011.
46. G. Minotti, R. Ronchi, E. Salvatorelli, P. Menna, and G. Cairo, "Doxorubicin irreversibly inactivates iron regulatory proteins 1 and 2 in cardiomyocytes: evidence for distinct metabolic pathways and implications for iron-mediated cardiotoxicity of antitumor therapy, " Cancer Research, vol. 61, no. 23, pp. 8422-8428, 2001.
47. G. Corna, P. Santambrogio, G. Minotti, and G. Cairo, "Doxorubicin paradoxically protects cardiomyocytes against ironmediated toxicity: role of reactive oxygen species and ferritin, " The Journal of Biological Chemistry, vol. 279, no. 14, pp. 13738-13745, 2004.
48. G. Corna, B. Galy, M. W. Hentze, and G. Cairo, "IRP1-independent alterations of cardiac iron metabolism in doxorubicin-treated mice, " Journal of Molecular Medicine, vol. 84, no. 7, pp. 551-560, 2006.
49. M. C. Asensio-López, J. Sánchez-Más, D. A. Pascual-Figal et al., "Involvement of ferritin heavy chain in the preventive effect of metformin against doxorubicin-induced cardiotoxicity, " Free Radical Biology and Medicine, vol. 57, pp. 188-200, 2013.
50. J. C. Kwok and D. R. Richardson, "Examination of the mechanism( s) involved in doxorubicin-mediated iron accumulation in ferritin: studies using metabolic inhibitors, protein synthesis inhibitors, and lysosomotropic agents, " Molecular Pharmacology, vol. 65, no. 1, pp. 181-195, 2004.
51. J. Drysdale, P. Arosio, R. Invernizzi et al., "Mitochondrial ferritin: a newplayer in iron metabolism, " Blood Cells, Molecules &Diseases, vol. 29, no. 3, pp. 376-383, 2002.
52. Y. Ichikawa, M. Ghanefar, M. Bayeva et al., "Cardiotoxicity of doxorubicin is mediated through mitochondrial iron accumulation, " The Journal of Clinical Investigation, vol. 124, no. 2, pp. 617-630, 2014.
53. F. Maccarinelli, E. Gammella, M. Asperti et al., "Mice lacking mitochondrial ferritin are more sensitive to doxorubicinmediated cardiotoxicity, " Journal ofMolecularMedicine, vol. 92, no. 8, pp. 859-869, 2014.
54. S. Gulec, G. J. Anderson, and J. F. Collins, "Mechanistic and regulatory aspects of intestinal iron absorption, " The American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 307, no. 4, pp. G397-G409, 2014.
55. J. E. Levy, O. Jin, Y. Fujiwara, F. Kuo, andN. C. Andrews, "Transferrin receptor is necessary for development of erythrocytes and the nervous system, " Nature Genetics, vol. 21, no. 4, pp. 396-399, 1999.
56. E. Gammella, F. Maccarinelli, P. Buratti, S. Recalcati, and G. Cairo, "The role of iron in anthracycline cardiotoxicity, " Frontiers in Pharmacology, vol. 5, article 25, 2014.
57. T. Ganz, "Systemic iron homeostasis, " Physiological Reviews, vol. 93, no. 4, pp. 1721-1741, 2013.
58. A. Pietrangelo, "Pathogens, metabolic adaptation, and human diseases-an iron-thrifty genetic model, " Gastroenterology, vol. 149, no. 4, pp. 834-838, 2015.
59. A. Pietrangelo, "Hepcidin in human iron disorders: therapeutic implications, " Journal of Hepatology, vol. 54, no. 1, pp. 173-181, 2011.
60. E. Nemeth, M. S. Tuttle, J. Powelson et al., "Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization, " Science, vol. 306, no. 5704, pp. 2090-2093, 2004.
61. C. Camaschella, "Iron-deficiency anemia, " The New England Journal of Medicine, vol. 373, no. 5, pp. 485-486, 2015.
62. A. Kim and E. Nemeth, "New insights into iron regulation and erythropoiesis, " Current Opinion in Hematology, vol. 22, no. 3, pp. 199-205, 2015.
63. L. Kautz, G. Jung, E. V. Valore, S. Rivella, E. Nemeth, and T. Ganz, "Identification of erythroferrone as an erythroid regulator of iron metabolism, " Nature Genetics, vol. 46, no. 7, pp. 678-684, 2014.
64. J. P. Liuzzi, F. Aydemir, H. Nam, M. D. Knutson, and R. J. Cousins, "Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells, " Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 37, pp. 13612-13617, 2006.
65. S. Ludwiczek, I. Theurl, M. U. Muckenthaler et al., "Ca2+ channel blockers reverse iron overload by a new mechanism via divalent metal transporter-1, " Nature Medicine, vol. 13, no. 4, pp. 448-454, 2007.
66. G. Y. Oudit, H. Sun, M. G. Trivieri et al., "L-type Ca2+ channels provide a major pathway for iron entry into cardiomyocytes in iron-overload cardiomyopathy, " Nature Medicine, vol. 9, no. 9, pp. 1187-1194, 2003.
67. P. Venditti, L. Di Stefano, and S. Di Meo, "Mitochondrial metabolism of reactive oxygen species, " Mitochondrion, vol. 13, no. 2, pp. 71-82, 2013.
68. A. Pietrangelo, "Hereditary hemochromatosis: pathogenesis, diagnosis, and treatment, " Gastroenterology, vol. 139, no. 2, pp. 393. e1-408. e2, 2010.
69. G. Sebastiani and K. Pantopoulos, "Disorders associated with systemic or local iron overload: from pathophysiology to clinical practice, " Metallomics, vol. 3, no. 10, pp. 971-986, 2011.
70. R. E. Fleming and P. Ponka, "Iron overload in human disease, " The New England Journal of Medicine, vol. 366, no. 4, pp. 348-359, 2012.
71. J. B. Porter and M. Garbowski, "The pathophysiology of transfusional iron overload, " Hematology/Oncology Clinics of North America, vol. 28, no. 4, pp. 683-701, 2014.
72. V. Berdoukas, T. D. Coates, and Z. I. Cabantchik, "Iron and oxidative stress in cardiomyopathy in thalassemia, " Free Radical Biology and Medicine, vol. 88, pp. 3-9, 2015.
73. J. M. C. Gutteridge and B. Halliwell, "Antioxidants: molecules, medicines, and myths, " Biochemical and Biophysical Research Communications, vol. 393, no. 4, pp. 561-564, 2010.