Molecular mechanisms of non-transferrin-bound and transferring-bound iron uptake in primary hippocampal neurons

Journal of Neurochemistry

Volumn 133, Issue 5, 2015, Pages 668-683

  Ji, Changyi ^a   Kosman, Daniel J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

ferrireductase; NTBI; permease; primary hippocampal neurons; TBI; Zip8

Indexed keywords

CARRIER PROTEIN; FERRIC CITRATE FE 59; FERRIC ION; FERROUS ION; IRON; MESSENGER RNA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; NON TRANSFERRIN BOUND IRON; OXIDOREDUCTASE; PROTEIN STEAP2; PROTEIN ZIP14; PROTEIN ZIP8; STROMAL CELL DERIVED RECEPTOR 2; TRANSFERRIN; TRANSFERRIN RECEPTOR; TRANSFERRING BOUND IRON; UNCLASSIFIED DRUG; ZINC ION; IRON BINDING PROTEIN; METAL;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BIOACCUMULATION; BRAIN LEVEL; BRAIN NERVE CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; GENE SILENCING; IN VITRO STUDY; INHIBITION KINETICS; IRON ASSIMILATION; IRON KINETICS; IRON PERMEATION; IRON REDUCTION; IRON TRANSPORT; MOLECULAR BIOLOGY; NONHUMAN; PRIMARY HIPPOCAMPAL NEURON; PRIORITY JOURNAL; PROTEIN CO LOCALIZATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; ANIMAL; CELL MEMBRANE; CYTOLOGY; DRUG EFFECTS; FEMALE; HIPPOCAMPUS; METABOLISM; NERVE CELL; PREGNANCY; PRIMARY CELL CULTURE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; CELL MEMBRANE; FEMALE; HIPPOCAMPUS; IRON; IRON RADIOISOTOPES; IRON-BINDING PROTEINS; METALS; NEURONS; PREGNANCY; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFERRIN;

EID: 84928010413     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13040     Document Type: Article

References (67)

1. Altamura S., and, Muckenthaler M. U., (2009) Iron toxicity in diseases of aging: Alzheimer's disease, Parkinson's disease and atherosclerosis. J. Alzheimers Dis. 16, 879-895.
2. Anderson G. J., and, Vulpe C. D., (2009) Mammalian iron transport. Cell. Mol. Life Sci. 66, 3241-3261.
3. Berczi A., Su D., Lakshminarasimhan M., Vargas A., and, Asard H., (2005) Heterologous expression and site-directed mutagenesis of an ascorbate-reducible cytochrome b561. Arch. Biochem. Biophys. 443, 82-92.
4. Besecker B., Bao S., Bohacova B., Papp A., Sadee W., and, Knoell D. L., (2008) The human zinc transporter SLC39A8 (Zip8) is critical in zinc-mediated cytoprotection in lung epithelia. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L1127-L1136.
5. Bleijenberg B. G., Van Eijk H. G., and, Leijnse B., (1971) The determination of non-heme iron and transferrin in cerebrospinal fluid. Clin. Chim. Acta 31, 277-281.
6. Bradbury M. W., (1997) Transport of iron in the blood-brain-cerebrospinal fluid system. J. Neurochem. 69, 443-454.
7. Burdo J. R., and, Connor J. R., (2003) Brain iron uptake and homeostatic mechanisms: an overview. Biometals 16, 63-75.
8. Burdo J. R., Menzies S. L., Simpson I. A., Garrick L. M., Garrick M. D., Dolan K. G., Haile D. J., Beard J. L., and, Connor J. R., (2001) Distribution of divalent metal transporter 1 and metal transport protein 1 in the normal and Belgrade rat. J. Neurosci. Res. 66, 1198-1207.
9. Cheah J. H., Kim S. F., Hester L. D., Clancy K. W., Patterson S. E., 3rd, Papadopoulos V., and, Snyder S. H., (2006) NMDA receptor-nitric oxide transmission mediates neuronal iron homeostasis via the GTPase Dexras1. Neuron 51, 431-440.
10. 2+ homeostasis in neurons from experimental and modeling studies. Am. J. Physiol. Cell Physiol. 294, C726-C742.
11. Del Principe D., Menichelli A., and, Colistra C., (1989) The ceruloplasmin and transferrin system in cerebrospinal fluid of acute leukemia patients. Acta Paediatr. Scand. 78, 327-328.
12. Ding D., Salvi R., and, Roth J. A., (2014) Cellular localization and developmental changes of Zip8, Zip14 and transferrin receptor 1 in the inner ear of rats. Biometals 27, 731-744.
13. Faucheux B. A., Nillesse N., Damier P., et al,. (1995) Expression of lactoferrin receptors is increased in the mesencephalon of patients with Parkinson disease. Proc. Natl Acad. Sci. USA 92, 9603-9607.
14. Fillebeen C., Descamps L., Dehouck M. P., Fenart L., Benaissa M., Spik G., Cecchelli R., and, Pierce A., (1999) Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier. J. Biol. Chem. 274, 7011-7017.
15. Fretham S. J., Carlson E. S., Wobken J., Tran P. V., Petryk A., and, Georgieff M. K., (2012) Temporal manipulation of transferrin-receptor-1-dependent iron uptake identifies a sensitive period in mouse hippocampal neurodevelopment. Hippocampus 22, 1691-1702.
16. Gaasch J. A., Lockman P. R., Geldenhuys W. J., Allen D. D., and, Van der Schyf C. J., (2007) Brain iron toxicity: differential responses of astrocytes, neurons, and endothelial cells. Neurochem. Res. 32, 1196-1208.
17. Garrick M. D., Kuo H. C., Vargas F., Singleton S., Zhao L., Smith J. J., Paradkar P., Roth J. A., and, Garrick L. M., (2006a) Comparison of mammalian cell lines expressing distinct isoforms of divalent metal transporter 1 in a tetracycline-regulated fashion. Biochem. J. 398, 539-546.
18. Garrick M. D., Singleton S. T., Vargas F., et al,. (2006b) DMT1: which metals does it transport? Biol. Res. 39, 79-85.
19. Girijashanker K., He L., Soleimani M., Reed J. M., Li H., Liu Z., Wang B., Dalton T. P., and, Nebert D. W., (2008) Slc39a14 gene encodes ZIP14, a metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol. Pharmacol. 73, 1413-1423.
20. Gutteridge J. M., (1992) Ferrous ions detected in cerebrospinal fluid by using bleomycin and DNA damage. Clin. Sci. 82, 315-320.
21. Haeger P., Alvarez A., Leal N., Adasme T., Nunez M. T., and, Hidalgo C., (2010) Increased hippocampal expression of the divalent metal transporter 1 (DMT1) mRNA variants 1B and +IRE and DMT1 protein after NMDA-receptor stimulation or spatial memory training. Neurotox. Res. 17, 238-247.
22. Holmes-Hampton G. P., Chakrabarti M., Cockrell A. L., McCormick S. P., Abbott L. C., Lindahl L. S., and, Lindahl P. A., (2012) Changing iron content of the mouse brain during development. Metallomics 4, 761-770.
23. Illing A. C., Shawki A., Cunningham C. L., and, Mackenzie B., (2012) Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1. J. Biol. Chem. 287, 30485-30496.
24. Inman R. S., and, Wessling-Resnick M., (1993) Characterization of transferrin-independent iron transport in K562 cells. J. Biol. Chem. 268, 8521-8528.
25. Kaech S., and, Banker G., (2006) Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415.
26. Lambe T., Simpson R. J., Dawson S., et al,. (2009) Identification of a Steap3 endosomal targeting motif essential for normal iron metabolism. Blood 113, 1805-1808.
27. Lane D. J., Robinson S. R., Czerwinska H., Bishop G. M., and, 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.
28. Latunde-Dada G. O., Simpson R. J., and, McKie A. T., (2008) Duodenal cytochrome B expression stimulates iron uptake by human intestinal epithelial cells. J. Nutr. 138, 991-995.
29. Lee D. W., and, Andersen J. K., (2010) Iron elevations in the aging Parkinsonian brain: a consequence of impaired iron homeostasis? J. Neurochem. 112, 332-339.
30. 2+ uptake by the ZIP8 HCO3-dependent symporter: kinetics, electrogenicity and trafficking. Biochem. Biophys. Res. Commun. 365, 814-820.
31. Liuzzi J. P., Aydemir F., Nam H., Knutson M. D., and, Cousins R. J., (2006) Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells. Proc. Natl Acad. Sci. USA 103, 13612-13617.
32. Macia E., Ehrlich M., Massol R., Boucrot E., Brunner C., and, Kirchhausen T., (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850.
33. Mackenzie B., Takanaga H., Hubert N., Rolfs A., and, Hediger M. A., (2007) Functional properties of multiple isoforms of human divalent metal-ion transporter 1 (DMT1). Biochem. J. 403, 59-69.
34. MacKenzie E. L., Iwasaki K., and, Tsuji Y., (2008) Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid. Redox Signal. 10, 997-1030.
35. McCarthy R. C., and, Kosman D. J., (2012) Mechanistic analysis of iron accumulation by endothelial cells of the BBB. Biometals 25, 665-675.
36. McCormick S. P., Chakrabarti M., Cockrell A. L., Park J., Lindahl L. S., and, Lindahl P. A., (2013) Low-molecular-mass metal complexes in the mouse brain. Metallomics 5, 232-241.
37. McKie A. T., Barrow D., Latunde-Dada G. O., et al,. (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291, 1755-1759.
38. Moos T., and, Morgan E. H., (1998) Evidence for low molecular weight, non-transferrin-bound iron in rat brain and cerebrospinal fluid. J. Neurosci. Res. 54, 486-494.
39. Moos T., and, Morgan E. H., (2004a) The metabolism of neuronal iron and its pathogenic role in neurological disease: review. Ann. N. Y. Acad. Sci. 1012, 14-26.
40. Moos T., and, Morgan E. H., (2004b) The significance of the mutated divalent metal transporter (DMT1) on iron transport into the Belgrade rat brain. J. Neurochem. 88, 233-245.
41. Oakhill J. S., Marritt S. J., Gareta E. G., Cammack R., and, McKie A. T., (2008) Functional characterization of human duodenal cytochrome b (Cybrd1): redox properties in relation to iron and ascorbate metabolism. Biochim. Biophys. Acta 1777, 260-268.
42. Ohgami R. S., Campagna D. R., Greer E. L., et al,. (2005) Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat. Genet. 37, 1264-1269.
43. Ohgami R. S., Campagna D. R., McDonald A., and, Fleming M. D., (2006) The Steap proteins are metalloreductases. Blood 108, 1388-1394.
44. Oshiro S., Nakajima H., Markello T., Krasnewich D., Bernardini I., and, Gahl W. A., (1993) Redox, transferrin-independent, and receptor-mediated endocytosis iron uptake systems in cultured human fibroblasts. J. Biol. Chem. 268, 21586-21591.
45. Pelizzoni I., Macco R., Morini M. F., Zacchetti D., Grohovaz F., and, Codazzi F., (2011) Iron handling in hippocampal neurons: activity-dependent iron entry and mitochondria-mediated neurotoxicity. Aging Cell 10, 172-183.
46. Pelizzoni I., Zacchetti D., Smith C. P., Grohovaz F., and, Codazzi F., (2012) Expression of divalent metal transporter 1 in primary hippocampal neurons: reconsidering its role in non-transferrin-bound iron influx. J. Neurochem. 120, 269-278.
47. Pinilla-Tenas J. J., Sparkman B. K., Shawki A., et al,. (2011) Zip14 is a complex broad-scope metal-ion transporter whose functional properties support roles in the cellular uptake of zinc and nontransferrin-bound iron. Am. J. Physiol. Cell Physiol. 301, C862-C871.
48. Qian Z. M., and, Ke Y., (2007) Brain iron metabolism: neurobiology and neurochemistry. Prog. Neurobiol. 83, 149-173.
49. Salazar J., Mena N., Hunot S., et al,. (2008) Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease. Proc. Natl Acad. Sci. USA 105, 18578-18583.
50. Savman K., Nilsson U. A., Thoresen M., and, Kjellmer I., (2005) Non-protein-bound iron in brain interstitium of newborn pigs after hypoxia. Dev. Neurosci. 27, 176-184.
51. 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.
52. Siddappa A. J., Rao R. B., Wobken J. D., Casperson K., Leibold E. A., Connor J. R., and, Georgieff M. K., (2003) Iron deficiency alters iron regulatory protein and iron transport protein expression in the perinatal rat brain. Pediatr. Res. 53, 800-807.
53. Sturrock A., Alexander J., Lamb J., Craven C. M., and, Kaplan J., (1990) Characterization of a transferrin-independent uptake system for iron in HeLa cells. J. Biol. Chem. 265, 3139-3145.
54. Tabuchi M., Tanaka N., Nishida-Kitayama J., Ohno H., and, Kishi F., (2002) Alternative splicing regulates the subcellular localization of divalent metal transporter 1 isoforms. Mol. Biol. Cell 13, 4371-4387.
55. Tabuchi M., Yanatori I., Kawai Y., and, Kishi F., (2010) Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J. Cell Sci. 123, 756-766.
56. Thorstensen K., (1988) Hepatocytes and reticulocytes have different mechanisms for the uptake of iron from transferrin. J. Biol. Chem. 263, 16837-16841.
57. Thorstensen K., and, Romslo I., (1988) Uptake of iron from transferrin by isolated rat hepatocytes. A redox-mediated plasma membrane process? J. Biol. Chem. 263, 8844-8850.
58. Todorich B., Zhang X., and, Connor J. R., (2011) H-ferritin is the major source of iron for oligodendrocytes. Glia 59, 927-935.
59. Tsubaki M., Takeuchi F., and, Nakanishi N., (2005) Cytochrome b561 protein family: expanding roles and versatile transmembrane electron transfer abilities as predicted by a new classification system and protein sequence motif analyses. Biochim. Biophys. Acta 1753, 174-190.
60. Tulpule K., Robinson S. R., Bishop G. M., and, Dringen R., (2010) Uptake of ferrous iron by cultured rat astrocytes. J. Neurosci. Res. 88, 563-571.
61. Vargas J. D., Herpers B., McKie A. T., Gledhill S., McDonnell J., van den Heuvel M., Davies K. E., and, Ponting C. P., (2003) Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases. Biochim. Biophys. Acta 1651, 116-123.
62. Wang B., Schneider S. N., Dragin N., et al,. (2007) Enhanced cadmium-induced testicular necrosis and renal proximal tubule damage caused by gene-dose increase in a Slc39a8-transgenic mouse line. Am. J. Physiol. Cell Physiol. 292, C1523-C1535.
63. Wang C. Y., Jenkitkasemwong S., Duarte S., Sparkman B., Shawki A., Mackenzie B., and, Knutson M. D., (2012) ZIP8 is an iron and zinc transporter whose cell-surface expression is upregulated by cellular iron loading. J. Biol. Chem. 287, 34032-34043.
64. Wyman S., Simpson R. J., McKie A. T., and, Sharp P. A., (2008) Dcytb (Cybrd1) functions as both a ferric and a cupric reductase in vitro. FEBS Lett. 582, 1901-1906.
65. 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.
66. Zhang D. L., Su D., Berczi A., Vargas A., and, Asard H., (2006) An ascorbate-reducible cytochrome b561 is localized in macrophage lysosomes. Biochim. Biophys. Acta 1760, 1903-1913.
67. Zhao N., Gao J., Enns C. A., and, Knutson M. D., (2010) ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J. Biol. Chem. 285, 32141-32150.