Iron handling in hippocampal neurons: Activity-dependent iron entry and mitochondria-mediated neurotoxicity

Aging Cell

Volumn 10, Issue 1, 2011, Pages 172-183

  Pelizzoni, Ilaria ^a,b   Macco, Romina ^a,c   Morini, Marco Francesco ^a,d   Zacchetti, Daniele ^a,b   Grohovaz, Fabio ^a,b,c   Codazzi, Franca ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Calcium; Hippocampal neurons; Iron; Mitochondria; Neurotoxicity; Oxidative stress

Indexed keywords

CALCIUM; CALCIUM ION; FERROUS ION; INTRACELLULAR CALCIUM SENSING PROTEIN; IRON; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NON TRANSFERRIN BOUND IRON; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; HIPPOCAMPUS; IRON OVERLOAD; IRON STORAGE; IRON TRANSPORT; NERVE CELL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CELL CULTURE TECHNIQUES; CELL DEATH; CELLS, CULTURED; HIPPOCAMPUS; ION TRANSPORT; IRON; IRON METABOLISM DISORDERS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, N-METHYL-D-ASPARTATE; SINGLE-CELL ANALYSIS;

EID: 78651299328     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00652.x     Document Type: Article

References (54)

1. Altamura S, Muckenthaler MU (2009) Iron toxicity in diseases of aging: Alzheimer's disease, parkinson's disease and atherosclerosis. J. Alzheimers Dis. 16, 879-895.
2. Andersen JK (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat. Med. 10 (Suppl.), S18-S25.
3. Andrews NC (1999) The iron transporter DMT1. Int. J. Biochem. Cell Biol. 31, 991-994.
4. Atlante A, Calissano P, Bobba A, Giannattasio S, Marra E, Passarella S (2001) Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett. 497, 1-5.
5. Benarroch EE (2009) Brain iron homeostasis and neurodegenerative disease. Neurology 72, 1436-1440.
6. Bradbury MW (1997) Transport of iron in the blood-brain-cerebrospinal fluid system. J. Neurochem. 69, 443-454.
7. Bralet J, Schreiber L, Bouvier C (1992) Effect of acidosis and anoxia on iron delocalization from brain homogenates. Biochem. Pharmacol. 43, 979-983.
8. Breuer W, Epsztejn S, Cabantchik ZI (1996) Dynamics of the cytosolic chelatable iron pool of K562 cells. FEBS Lett. 382, 304-308.
9. Britigan BE, Rasmussen GT, Cox CD (1998) Binding of iron and inhibition of iron-dependent oxidative cell injury by the "calcium chelator" 1, 2-bis(2-aminophenoxy)ethane N, N, N', N'-tetraacetic acid (BAPTA). Biochem. Pharmacol. 55, 287-295.
10. Cabantchik ZI, Glickstein H, Milgram P, Breuer W (1996) A fluorescence assay for assessing chelation of intracellular iron in a membrane model system and in mammalian cells. Anal. Biochem. 233, 221-227.
11. Chang YZ, Ke Y, Du JR, Halpern GM, Ho KP, Zhu L, Gu XS, Xu YJ, Wang Q, Li LZ, Wang CY, Qian ZM (2006) Increased divalent metal transporter 1 expression might be associated with the neurotoxicity of L-DOPA. Mol. Pharmacol. 69, 968-974.
12. Cheah JH, Kim SF, Hester LD, Clancy KW, Patterson SE 3rd, Papadopoulos V, Snyder SH (2006) NMDA receptor-nitric oxide transmission mediates neuronal iron homeostasis via the GTPase Dexras1. Neuron 51, 431-440.
13. Codazzi F, Di Cesare A, Chiulli N, Albanese A, Meyer T, Zacchetti D, Grohovaz F (2006) Synergistic control of protein kinase cgamma activity by ionotropic and metabotropic glutamate receptor inputs in hippocampal neurons. J. Neurosci. 26, 3404-3411.
14. Du F, Qian ZM, Zhu L, Wu XM, Yung WH, Tsim TY, Ke Y (2009) L-DOPA neurotoxicity is mediated by up-regulation of DMT1-IRE expression. PLoS ONE 4, e4593.
15. Esposito BP, Epsztejn S, Breuer W, Cabantchik ZI (2002) A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal. Biochem. 304, 1-18.
16. Fariss MW, Chan CB, Patel M, Van Houten B, Orrenius S (2005) Role of mitochondria in toxic oxidative stress. Mol. Interv. 5, 94-111.
17. Fleming MD, Trenor CC 3rd, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 16, 383-386.
18. Gaasch JA, Geldenhuys WJ, Lockman PR, Allen DD, Van der Schyf CJ (2007a) Voltage-gated calcium channels provide an alternate route for iron uptake in neuronal cell cultures. Neurochem. Res. 32, 1686-1693.
19. Gaasch JA, Lockman PR, Geldenhuys WJ, Allen DD, Van der Schyf CJ (2007b) Brain iron toxicity: differential responses of astrocytes, neurons, and endothelial cells. Neurochem. Res. 32, 1196-1208.
20. Galaris D, Mantzaris M, Amorgianiotis C (2008) Oxidative stress and aging: the potential role of iron. Hormones (Athens) 7, 114-122.
21. Galy B, Ferring-Appel D, Kaden S, Gröne HJ, Hentze MW (2008) Iron regulatory proteins are essential for intestinal function and control key iron absorption molecules in the duodenum. Cell Metab. 7, 79-85.
22. Garrick LM, Dolan KG, Romano MA, Garrick MD (1999) Non-transferrin-bound iron uptake in belgrade and normal rat erythroid cells. J. Cell. Physiol. 178, 349-358.
23. Giorgio M, Trinei M, Migliaccio E, Pelicci PG (2007) Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8, 722-728.
24. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488.
25. Hentze MW, Muckenthaler MU, Andrews NC (2004) Balancing acts: molecular control of mammalian iron metabolism. Cell 117, 285-297.
26. Keelan J, Allen NJ, Antcliffe D, Pal S, Duchen MR (2001) Quantitative imaging of glutathione in hippocampal neurons and glia in culture using monochlorobimane. J. Neurosci. Res. 66, 873-884.
27. Kress GJ, Dineley KE, Reynolds IJ (2002) The relationship between intracellular free iron and cell injury in cultured neurons, astrocytes, and oligodendrocytes. J. Neurosci. 22, 5848-5855.
28. Lane DJ, Robinson SR, Czerwinska H, Bishop GM, Lawen A (2010) Two routes of iron accumulation in astrocytes: ascorbate-dependent ferrous iron uptake via the divalent metal transporter (DMT1) plus an independent route for ferric iron. Biochem. J. 432, 123-132.
29. Lipscomb DC, Gorman LG, Traystman RJ, Hurn PD (1998) Low molecular weight iron in cerebral ischemic acidosis in vivo. Stroke 29, 487-493.
30. Lis A, Barone TA, Paradkar PN, Plunkett RJ, Roth JA (2004) Expression and localization of different forms of DMT1 in normal and tumor astroglial cells. Brain Res. Mol. Brain Res. 122, 62-70.
31. Ma YS, Wu SB, Lee WY, Cheng JS, Wei YH (2009) Response to the increase of oxidative stress and mutation of mitochondrial DNA in aging. Biochim. Biophys. Acta 1790, 1021-1029.
32. MacKenzie EL, Iwasaki K, Tsuji Y (2008) Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid. Redox Signal. 10, 997-1030.
33. Madsen E, Gitlin JD (2007) Copper and iron disorders of the brain. Annu. Rev. Neurosci. 30, 317-337.
34. Mills E, Dong XP, Wang F, Xu H (2010) Mechanisms of brain iron transport: insight into neurodegeneration and CNS disorders. Future Med. Chem. 2, 51.
35. Molina JA, Jimenez-Jimenez FJ, Aguilar MV, Meseguer I, Mateos-Vega CJ, Gonzalez-Munoz MJ, de Bustos F, Porta J, Orti-Pareja M, Zurdo M, Barrios E, Martinez-Para MC (1998) Cerebrospinal fluid levels of transition metals in patients with alzheimer's disease. J. Neural Transm. 105, 479-488.
36. Moos T, Morgan EH (2004) The metabolism of neuronal iron and its pathogenic role in neurological disease. Ann. N Y Acad. Sci. 1012, 14-26.
37. Moos T, Rosengren Nielsen T, Skjorringe T, Morgan EH (2007) Iron trafficking inside the brain. J. Neurochem. 103, 1730-1740.
38. Nicholls DG, Johnson-Cadwell L, Vesce S, Jekabsons M, Yadava N (2007) Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J. Neurosci. Res. 85, 3206-3212.
39. 2+ channels provide a major pathway for iron entry into cardiomyocytes in iron-overload cardiomyopathy. Nat. Med. 9, 1187-1194.
40. Pelizzoni I, Macco R, Zacchetti D, Grohovaz F, Codazzi F (2008) Iron and calcium in the central nervous system: a close relationship in health and sickness. Biochem. Soc. Trans. 36, 1309-1312.
41. Qian ZM, Shen X (2001) Brain iron transport and neurodegeneration. Trends Mol. Med. 7, 103-108.
42. Robb SJ, Robb-Gaspers LD, Scaduto RC Jr, Thomas AP, Connor JR (1999) Influence of calcium and iron on cell death and mitochondrial function in oxidatively stressed astrocytes. J. Neurosci. Res. 55, 674-686.
43. Roth JA, Horbinski C, Feng L, Dolan KG, Higgins D, Garrick MD (2000) Differential localization of divalent metal transporter 1 with and without iron response element in rat PC12 and sympathetic neuronal cells. J. Neurosci. 20, 7595-7601.
44. Salazar J, Mena N, Hunot S, Prigent A, Alvarez-Fischer D, Arredondo M, Duyckaerts C, Sazdovitch V, Zhao L, Garrick LM, Nunez MT, Garrick MD, Raisman-Vozari R, Hirsch EC (2008) Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of parkinson's disease. Proc. Natl. Acad. Sci. USA 105, 18578-18583.
45. Semenova MM, Mäki-Hokkonen AM, Cao J, Komarovski V, Forsberg KM, Koistinaho M, Coffey ET, Courtney MJ (2007) Rho mediates calcium-dependent activation of p38alpha and subsequent excitotoxic cell death. Nat. Neurosci. 10, 436-443.
46. Seo AY, Xu J, Servais S, Hofer T, Marzetti E, Wohlgemuth SE, Knutson MD, Chung HY, Leeuwenburgh C (2008) Mitochondrial iron accumulation with age and functional consequences. Aging Cell 7, 706-716.
47. Shvartsman M, Kikkeri R, Shanzer A, Cabantchik ZI (2007) Non-transferrin-bound iron reaches mitochondria by a chelator-inaccessible mechanism: biological and clinical implications. Am. J. Physiol. Cell Physiol. 293, C1383-C1394.
48. Song N, Jiang H, Wang J, Xie JX (2007) Divalent metal transporter 1 up-regulation is involved in the 6-hydroxydopamine-induced ferrous iron influx. J. Neurosci. Res. 85, 3118-3126.
49. Stankiewicz JM, Brass SD (2009) Role of iron in neurotoxicity: a cause for concern in the elderly? Curr. Opin. Clin. Nutr. Metab. Care 12, 22-29.
50. Su MA, Trenor CC, Fleming JC, Fleming MD, Andrews NC (1998) The G185R mutation disrupts function of the iron transporter Nramp2. Blood 92, 2157-2163.
51. Vargas JD, Herpers B, McKie AT, Gledhill S, McDonnell J, van den Heuvel M, Davies KE, Ponting CP (2003) Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases. Biochim. Biophys. Acta 1651, 116-123.
52. Wu J, Hua Y, Keep RF, Nakamura T, Hoff JT, Xi G (2003) Iron and iron-handling proteins in the brain after intracerebral hemorrhage. Stroke 34, 2964-2969.
53. Wu LJ, Leenders AG, Cooperman S, Meyron-Holtz E, Smith S, Land W, Tsai RY, Berger UV, Sheng ZH, Rouault TA (2004) Expression of the iron transporter ferroportin in synaptic vesicles and the blood-brain barrier. Brain Res. 1001, 108-117.
54. Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR (2004) Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci. 5, 863-873.