Mitochondrial ferritin in the regulation of brain iron homeostasis and neurodegenerative diseases

Frontiers in Pharmacology

Volumn 5 FEB, Issue , 2014, Pages

  Gao, Guofen ^a   Chang, Yan Zhong ^a  

^a HEBEI NORMAL UNIVERSITY   (China)

Author keywords

Brain; Iron; Mitochondrial ferritin; Neurodegenerative diseases; Oxidative damage

Indexed keywords

AMYLOID BETA PROTEIN; FERRITIN; FRATAXIN; MITOCHONDRIAL FERRITIN; OXIDOPAMINE; REACTIVE OXYGEN METABOLITE; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; APOPTOSIS; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; FRIEDREICH ATAXIA; HUMAN; IRON BALANCE; IRON METABOLISM; IRON OVERLOAD; IRON STORAGE; IRON TRANSPORT; MITOCHONDRION; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PARKINSON DISEASE; PATHOGENESIS; PROTEIN LOCALIZATION; RESTLESS LEGS SYNDROME; REVIEW;

EID: 84895536249     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00019     Document Type: Review

References (70)

1. Anderson, G. J., and Wang, F. (2012). Essential but toxic: controlling the flux of iron in the body. Clin. Exp. Pharmacol. Physiol. 39, 719-724. doi: 10.1111/j.1440-1681.2011.05661.x.
2. Arosio, P., Ingrassia, R., and Cavadini, P. (2009). Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim. Biophys. Acta 1790, 589-599. doi: 10.1016/j.bbagen.2008.09.004.
3. Arosio, P., and Levi, S. (2002). Ferritin, iron homeostasis, and oxidative damage. Free Radic. Biol. Med. 33, 457-463. doi: 10.1016/S0891-5849(02)00842-0.
4. Berg, D., and Hochstrasser, H. (2006). Iron metabolism in Parkinsonian syndromes. Mov. Disord. 21, 1299-1310. doi: 10.1002/mds.21020.
5. Bou-Abdallah, F., Santambrogio, P., Levi, S., Arosio, P., and Chasteen, N. D. (2005). Unique iron binding and oxidation properties of human mitochondrial ferritin: a comparative analysis with Human H-chain ferritin. J. Mol. Biol. 347, 543-554. doi: 10.1016/j.jmb.2005.01.007.
6. Bradbury, M. W. (1997). Transport of iron in the blood-brain-cerebrospinal fluid system. J. Neurochem. 69, 443-454. doi: 10.1046/j.1471-4159.1997.69020443.x.
7. Campanella, A., Isaya, G., O'neill, H. A., Santambrogio, P., Cozzi, A., Arosio, P., et al. (2004). The expression of human mitochondrial ferritin rescues respiratory function in frataxin-deficient yeast. Hum. Mol. Genet. 13, 2279-2288. doi: 10.1093/hmg/ddh232.
8. Campanella, A., Rovelli, E., Santambrogio, P., Cozzi, A., Taroni, F., and Levi, S. (2009). Mitochondrial ferritin limits oxidative damage regulating mitochondrial iron availability: hypothesis for a protective role in Friedreich ataxia. Hum. Mol. Genet. 18, 1-11. doi: 10.1093/hmg/ddn308.
9. Cazzola, M., Invernizzi, R., Bergamaschi, G., Levi, S., Corsi, B., Travaglino, E., et al. (2003). Mitochondrial ferritin expression in erythroid cells from patients with sideroblastic anemia. Blood 101, 1996-2000. doi: 10.1182/blood-2002-07-2006.
10. Connor, J. R., Boyer, P. J., Menzies, S. L., Dellinger, B., Allen, R. P., Ondo, W. G., et al. (2003). Neuropathological examination suggests impaired brain iron acquisition in restless legs syndrome. Neurology 61, 304-309. doi: 10.1212/01.WNL.0000078887.16593.12.
11. Connor, J. R., Wang, X. S., Patton, S. M., Menzies, S. L., Troncoso, J. C., Earley, C. J., et al. (2004). Decreased transferrin receptor expression by neuromelanin cells in restless legs syndrome. Neurology 62, 1563-1567. doi: 10.1212/01.WNL.0000123251.60485.AC.
12. Corsi, B., Cozzi, A., Arosio, P., Drysdale, J., Santambrogio, P., Campanella, A., et al. (2002). Human mitochondrial ferritin expressed in HeLa cells incorporates iron and affects cellular iron metabolism. J. Biol. Chem. 277, 22430-22437. doi: 10.1074/jbc.M105372200.
13. Crichton, R. R., Dexter, D. T., and Ward, R. J. (2011). Brain iron metabolism and its perturbation in neurological diseases. J. Neural. Transm. 118, 301-314. doi: 10.1007/s00702-010-0470-z.
14. Deane, R., Zheng, W., and Zlokovic, B. V. (2004). Brain capillary endothelium and choroid plexus epithelium regulate transport of transferrin-bound and free iron into the rat brain. J. Neurochem. 88, 813-820. doi: 10.1046/j.1471-4159.2003.02221.x.
15. Drysdale, J., Arosio, P., Invernizzi, R., Cazzola, M., Volz, A., Corsi, B., et al. (2002). Mitochondrial ferritin: a new player in iron metabolism. Blood Cells Mol. Dis. 29, 376-383. doi: 10.1006/bcmd.2002.0577.
16. Eaton, J. W., and Qian, M. (2002). Molecular bases of cellular iron toxicity. Free Radic. Biol. Med. 32, 833-840. doi: 10.1016/S0891-5849(02)00772-4.
17. Ford, G. C., Harrison, P. M., Rice, D. W., Smith, J. M., Treffry, A., White, J. L., et al. (1984). Ferritin: design and formation of an iron-storage molecule. Philos. Trans. R. Soc. Lond. B Biol. Sci. 304, 551-565. doi: 10.1098/rstb.1984.0046.
18. Foury, F., and Roganti, T. (2002). Deletion of the mitochondrial carrier genes MRS3 and MRS4 suppresses mitochondrial iron accumulation in a yeast frataxin-deficient strain. J. Biol. Chem. 277, 24475-24483. doi: 10.1074/jbc.M111789200.
19. Godau, J., Schweitzer, K. J., Liepelt, I., Gerloff, C., and Berg, D. (2007). Substantia nigra hypoechogenicity: definition and findings in restless legs syndrome. Mov. Disord. 22, 187-192. doi: 10.1002/mds.21230.
20. Halliwell, B. (1992). Reactive oxygen species and the central nervous system. J. Neurochem. 59, 1609-1623. doi: 10.1111/j.1471-4159.1992.tb10990.x.
21. Han, J., Day, J. R., Connor, J. R., and Beard, J. L. (2003). Gene expression of transferrin and transferrin receptor in brains of control vs. iron-deficient rats. Nutr. Neurosci. 6, 1-10.
22. Harrison, P. M., and Arosio, P. (1996). The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275, 161-203. doi: 10.1016/0005-2728(96)00022-9.
23. Langlois d'Estaintot, B., Santambrogio, P., Granier, T., Gallois, B., Chevalier, J. M., Precigoux, G., et al. (2004). Crystal structure and biochemical properties of the human mitochondrial ferritin and its mutant Ser144Ala. J. Mol. Biol. 340, 277-293. doi: 10.1016/j.jmb.2004.04.036.
24. Lee, D. W., Andersen, J. K., and Kaur, D. (2006). Iron dysregulation and neurodegeneration: the molecular connection. Mol. Interv. 6, 89-97. doi: 10.1124/mi.6.2.6.
25. Leipuviene, R., and Theil, E. C. (2007). The family of iron responsive RNA structures regulated by changes in cellular iron and oxygen. Cell. Mol. Life Sci. 64, 2945-2955. doi: 10.1007/s00018-007-7198-4.
26. Levi, S., and Arosio, P. (2004). Mitochondrial ferritin. Int. J. Biochem. Cell Biol. 36, 1887-1889. doi: 10.1016/j.biocel.2003.10.020.
27. Levi, S., Corsi, B., Bosisio, M., Invernizzi, R., Volz, A., Sanford, D., et al. (2001). A human mitochondrial ferritin encoded by an intronless gene. J. Biol. Chem. 276, 24437-24440. doi: 10.1074/jbc.C100141200.
28. Levi, S., and Rovida, E. (2009). The role of iron in mitochondrial function. Biochim. Biophys. Acta 1790, 629-636. doi: 10.1016/j.bbagen.2008.09.008.
29. Lin, M. T., and Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795. doi: 10.1038/nature05292.
30. Lozoff, B., Jimenez, E., Hagen, J., Mollen, E., and Wolf, A. W. (2000). Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics 105, E51. doi: 10.1542/peds.105.4.e51.
31. Marques, F., Falcao, A. M., Sousa, J. C., Coppola, G., Geschwind, D., Sousa, N., et al. (2009). Altered iron metabolism is part of the choroid plexus response to peripheral inflammation. Endocrinology 150, 2822-2828. doi: 10.1210/en.2008-1610.
32. Meyron-Holtz, E. G. (2004). Mammalian tissue oxygen levels modulate iron-regulatory protein activities in vivo. Science 306, 2087-2090. doi: 10.1126/science.1103786.
33. Mills, E., Dong, X. P., Wang, F., and Xu, H. (2010). Mechanisms of brain iron transport: insight into neurodegeneration and CNS disorders. Future Med. Chem. 2, 51-64. doi: 10.4155/fmc.09.140.
34. Moos, T., Rosengren Nielsen, T., Skjorringe, T., and Morgan, E. H. (2007). Iron trafficking inside the brain. J. Neurochem. 103, 1730-1740. doi: 10.1111/j.1471-4159.2007.04976.x.
35. Morris, C. M., Candy, J. M., Oakley, A. E., Bloxham, C. A., and Edwardson, J. A. (1992). Histochemical distribution of non-haem iron in the human brain. Acta Anat. (Basel) 144, 235-257. doi: 10.1159/000147312.
36. Nicolas, G., Chauvet, C., Viatte, L., Danan, J. L., Bigard, X., Devaux, I., et al. (2002). The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J. Clin. Invest. 110, 1037-1044.
37. Nie, G., Sheftel, A. D., Kim, S. F., and Ponka, P. (2005). Overexpression of mitochondrial ferritin causes cytosolic iron depletion and changes cellular iron homeostasis. Blood 105, 2161-2167. doi: 10.1182/blood-2004-07-2722.
38. Ondo, W. G. (2005). Restless legs syndrome. Curr. Neurol. Neurosci. Rep. 5, 266-274. doi: 10.1007/s11910-005-0071-7.
39. Pandolfo, M. (2002). Iron metabolism and mitochondrial abnormalities in Friedreich ataxia. Blood Cells Mol. Dis. 29, 536-547; discussion 548-552. doi: 10.1006/bcmd.2002.0591.
40. Paradkar, P. N., Zumbrennen, K. B., Paw, B. H., Ward, D. M., and Kaplan, J. (2009). Regulation of mitochondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2. Mol. Cell. Biol. 29, 1007-1016. doi: 10.1128/MCB.01685-08.
41. Park, C. H., Valore, E. V., Waring, A. J., and Ganz, T. (2001). Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J. Biol. Chem. 276, 7806-7810. doi: 10.1074/jbc.M008922200.
42. Parkinson, J. (2002). An essay on the shaking palsy. 1817. J. Neuropsychiatry Clin. Neurosci. 14, 223-236; discussion 222. doi: 10.1176/appi.neuropsych.14.2.223.
43. Pollitt, E. (1999). Early iron deficiency anemia and later mental retardation. Am. J. Clin. Nutr. 69, 4-5.
44. Ponka, P. (1997). Tissue-specific regulation of iron metabolism and heme synthesis: distinct control mechanisms in erythroid cells. Blood 89, 1-25.
45. Ramey, G., Deschemin, J. C., Durel, B., Canonne-Hergaux, F., Nicolas, G., and Vaulont, S. (2010). Hepcidin targets ferroportin for degradation in hepatocytes. Haematologica 95, 501-504. doi: 10.3324/haematol.2009.014399.
46. Rouault, T. A. (2006). The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2, 406-414. doi: 10.1038/nchembio807.
47. Santambrogio, P., Biasiotto, G., Sanvito, F., Olivieri, S., Arosio, P., and Levi, S. (2007). Mitochondrial ferritin expression in adult mouse tissues. J. Histochem. Cytochem. 55, 1129-1137. doi: 10.1369/jhc.7A7273.2007.
48. Schmidauer, C., Sojer, M., Seppi, K., Stockner, H., Hogl, B., Biedermann, B., et al. (2005). Transcranial ultrasound shows nigral hypoechogenicity in restless legs syndrome. Ann. Neurol. 58, 630-634. doi: 10.1002/ana.20572.
49. Schmucker, S., and Puccio, H. (2010). Understanding the molecular mechanisms of Friedreich's ataxia to develop therapeutic approaches. Hum. Mol. Genet. 19, R103-R110. doi: 10.1093/hmg/ddq165.
50. Selkoe, D. J. (1996). Amyloid beta-protein and the genetics of Alzheimer's disease. J. Biol. Chem. 271, 18295-18298.
51. Selkoe, D. J. (2000). Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann. N. Y. Acad. Sci. 924, 17-25. doi: 10.1111/j.1749-6632.2000.tb05554.x.
52. Selkoe, D. J. (2001). Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766.
53. Shi, Z. H., Nie, G., Duan, X. L., Rouault, T., Wu, W. S., Ning, B., et al. (2010). Neuroprotective mechanism of mitochondrial ferritin on 6-hydroxydopamine-induced dopaminergic cell damage: implication for neuroprotection in Parkinson's disease. Antioxid. Redox Signal. 13, 783-796. doi: 10.1089/ars.2009.3018.
54. Shvartsman, M., Kikkeri, R., Shanzer, A., and Cabantchik, Z. I. (2007). Non-transferrin-bound iron reaches mitochondria by a chelator-inaccessible mechanism: biological and clinical implications. Am. J. Physiol. Cell Physiol. 293, C1383-C1394. doi: 10.1152/ajpcell.00054.2007.
55. Siddappa, A. J., Rao, R. B., Wobken, J. D., Leibold, E. A., Connor, J. R., and Georgieff, M. K. (2002). Developmental changes in the expression of iron regulatory proteins and iron transport proteins in the perinatal rat brain. J. Neurosci. Res. 68, 761-775. doi: 10.1002/jnr.10246.
56. Siddappa, A. M., Georgieff, M. K., Wewerka, S., Worwa, C., Nelson, C. A., and Deregnier, R. A. (2004). Iron deficiency alters auditory recognition memory in newborn infants of diabetic mothers. Pediatr. Res. 55, 1034-1041. doi: 10.1203/01.pdr.0000127021.38207.62.
57. Skjorringe, T., Moller, L. B., and Moos, T. (2012). Impairment of interrelated iron-and copper homeostatic mechanisms in brain contributes to the pathogenesis of neurodegenerative disorders. Front. Pharmacol. 3:169. doi: 10.3389/fphar.2012.00169.
58. Snyder, A. M., Wang, X., Patton, S. M., Arosio, P., Levi, S., Earley, C. J., et al. (2009). Mitochondrial ferritin in the substantia nigra in restless legs syndrome. J. Neuropathol. Exp. Neurol. 68, 1193-1199. doi: 10.1097/NEN.0b013e3181bdc44f.
59. Sugawara, N., Ikeda, T., Sugawara, C., Kohgo, Y., Kato, J., and Takeichi, N. (1992). Regional distribution of copper, zinc and iron in the brain in Long-Evans Cinnamon (LEC) rats with a new mutation causing hereditary hepatitis. Brain Res. 588, 287-290. doi: 10.1016/0006-8993(92)91587-5.
60. Theil, E. C. (1987). Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu. Rev. Biochem. 56, 289-315. doi: 10.1146/annurev.bi.56.070187.001445.
61. Torti, F. M., and Torti, S. V. (2002). Regulation of ferritin genes and protein. Blood 99, 3505-3516. doi: 10.1182/blood.V99.10.3505.
62. Ueda, F., Raja, K. B., Simpson, R. J., Trowbridge, I. S., and Bradbury, M. W. (1993). Rate of 59Fe uptake into brain and cerebrospinal fluid and the influence thereon of antibodies against the transferrin receptor. J. Neurochem. 60, 106-113. doi: 10.1111/j.1471-4159.1993.tb05828.x.
63. Wang, L., Yang, H., Zhao, S., Sato, H., Konishi, Y., Beach, T. G., et al. (2011). Expression and localization of mitochondrial ferritin mRNA in Alzheimer's disease cerebral cortex. PLoS ONE 6:e22325. doi: 10.1371/journal.pone.0022325.
64. Wang, S. M., Fu, L. J., Duan, X. L., Crooks, D. R., Yu, P., Qian, Z. M., et al. (2010). Role of hepcidin in murine brain iron metabolism. Cell. Mol. Life Sci. 67, 123-133. doi: 10.1007/s00018-009-0167-3.
65. Wu, W. S., Zhao, Y. S., Shi, Z. H., Chang, S. Y., Nie, G. J., Duan, X. L., et al. (2013). Mitochondrial ferritin attenuates beta-amyloid-induced neurotoxicity: reduction in oxidative damage through the Erk/P38 mitogen-activated protein kinase pathways. Antioxid. Redox Signal. 18, 158-169. doi: 10.1089/ars.2011.4285.
66. Yang, H., Yang, M., Guan, H., Liu, Z., Zhao, S., Takeuchi, S., et al. (2013). Mitochondrial ferritin in neurodegenerative diseases. Neurosci. Res. 77, 1-7. doi: 10.1016/j.neures.2013.07.005.
67. Zecca, L., Youdim, M. B., Riederer, P., Connor, J. R., and Crichton, R. R. (2004). Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci. 5, 863-873. doi: 10.1038/nrn1537.
68. Zechel, S., Huber-Wittmer, K., and Von Bohlen Und Halbach, O. (2006). Distribution of the iron-regulating protein hepcidin in the murine central nervous system. J. Neurosci. Res. 84, 790-800. doi: 10.1002/jnr.20991.
69. Zhang, Y., Dawson, V. L., and Dawson, T. M. (2000). Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiol. Dis. 7, 240-250. doi: 10.1006/nbdi.2000.0319.
70. Zheng, W., and Monnot, A. D. (2012). Regulation of brain iron and copper homeostasis by brain barrier systems: implication in neurodegenerative diseases. Pharmacol. Ther. 133, 177-188. doi: 10.1016/j.pharmthera.2011.10.006.