Iron trafficking inside the brain

Journal of Neurochemistry

Volumn 103, Issue 5, 2007, Pages 1730-1740

  Moos, Torben ^a   Nielsen, Thomas Rosengren ^b   Skjørringe, Tina ^b   Morgan, Evan H ^c  

^a AALBORG UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Astrocyte; Blood brain barrier; Cerebrospinal fluid; Citrate; Divalent metal transporter 1; Endosome; Ferroportin; Transferrin receptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; CERULOPLASMIN; CITRIC ACID; FERROPORTIN 1; IRON; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; TRANSFERRIN; TRANSFERRIN RECEPTOR;

ASTROCYTE; BLOOD; BRAIN; BRAIN CAPILLARY; BRAIN CELL; BRAIN CIRCULATION; BRAIN VENTRICLE; CELL ACTIVITY; CELL SURFACE; CELL TRANSPORT; ENDOCYTOSIS; ENDOTHELIUM CELL; EXTRACELLULAR FLUID; GLIA CELL; HUMAN; INTRACELLULAR SPACE; IRON BINDING CAPACITY; IRON KINETICS; IRON TRANSPORT; MACROGLIA; MEMBRANE BINDING; MICROGLIA; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SHORT SURVEY;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; IRON; MODELS, BIOLOGICAL; NEURONS; RECEPTORS, TRANSFERRIN; TRANSFERRIN;

EID: 36248942024     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04976.x     Document Type: Short Survey

References (93)

1. Abbott N. J., Ronnback L. Hansson E. (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41 53.
2. Angelova-Gateva P. (1980) Iron transferrin receptors in rat and human cerebrum. Agressologie 21, 27 30.
3. Batey R.G., Lai Chung Fong P., Shamir S. Sherlock S. (1980) A non-transferrin-bound serum iron in idiopathic hemochromatosis. Dig. Dis. Sci. 25, 340 346.
4. Beard J. L., Wiesinger J. A., Nan L. I. Connor J. R. (2005) Brain iron uptake in hypotransferrinemic mice: influence of systemic iron status. J. Neurosci. Res. 79, 254 261.
5. Benkovic S. A. Connor J. R. (1993) Ferritin, transferrin, and iron in selected regions of the adult and aged rat brain. J. Comp. Neurol. 338, 97 113.
6. Bickel U., Kang Y. S., Yoshikawa T. Pardridge W. M. (1994) In vivo demonstration of subcellular localization of anti-transferrin receptor monoclonal antibody-colloidal gold conjugate in brain capillary endothelium. J. Histochem. Cytochem. 42, 1493 1497.
7. Bloch B., Popovici T., Levin M. J., Tuil D. Kahn A. (1985) Transferrin gene expression visualized in oligodendrocytes of the rat brain by using in situ hybridization and immunohistochemistry. Proc. Natl Acad. Sci. USA 82, 6706 6710.
8. Bradbury M. (1997) Transport of iron in the blood-brain-cerebrospinal fluid system. J. Neurochem. 69, 443 454.
9. Brightman M. W. Reese T. S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648 677.
10. Brissot P., Wright T. L., Ma W. L. Weisiger R. A. (1985) Efficient clearance of non-transferrin-bound iron by rat liver. Implications for hepatic iron loading in iron overload states. J. Clin. Invest. 76, 1463 1470.
11. Brock J. (1995) Lactoferrin: a multifunctional immunoregulatory protein? Immunol. Today 9, 417 419.
12. Burdo J. R., Menzies S. L., Simpson I. A., Garrick L. M., Garrick M. D., Dolan K. G., Haile D. J., Beard J. L. 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.
13. Burdo J. R., Antonetti D. A., Wolpert E. B. Connor J. R. (2003) Mechanisms and regulation of transferrin and iron transport in a model blood-brain barrier system. Neuroscience 121, 883 890.
14. Cheepsunthorn P., Palmer C. Connor J. R. (1998) Cellular distribution of ferritin subunits in postnatal rat brain. J. Comp. Neurol. 400, 73 86.
15. Copp A. J., Estibeiro J. P., Brook F. A. Downs K. M. (1992) Exogenous transferrin is taken up and localized by the neurulation-stage mouse embryo in vitro. Dev. Biol. 153, 312 323.
16. Crowe A. Morgan E. H. (1992) Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res. 592, 8 16.
17. Davson H. Segal M. B. (1969) Effect of cerebrospinal fluid on volume of distribution of extracellular markers. Brain 92, 131 136.
18. De Arriba Zerpa G. A., Saleh M. C., Fernandez P. M., Guillou F., Espinosa de los Monteros A., de Vellis J., Zakin M. M. Baron B. (2000) Alternative splicing prevents transferrin secretion during differentiation of a human oligodendrocyte cell line. J. Neurosci. Res. 61, 388 395.
19. Dexter D. T., Wells F. R., Agid F., Agid Y., Lees A. J., Jenner P. Marsden C. D. (1987) Increased nigral iron content in postmortem parkinsonian brain. Lancet 2, 1219 1220.
20. Dunford H. B. (1987) Free radicals in iron-containing systems. Free Radic. Biol. Med. 3, 405 421.
21. 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.
22. Fillebeen C., Descamps L., Dehouck M.-P., Fenart L., Benaissa M., Spik G., Cecchelli R. Pierce A. (1999) Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier. J. Biol. Chem. 274, 7011 7017.
23. Gosk S., Vermehren C., Storm G. Moos T. (2004) Targeting anti-transferrin receptor antibody (OX26) and OX26-conjugated liposomes to brain capillary endothelial cells using in situ perfusion. J. Cereb. Blood Flow Metab. 24, 1193 1204.
24. Gunshin H., Mackenzie B., Berger U. V., Gunshin Y., Romero M. F., Boron W. F., Nussberger S., Gollan J. L. Hediger M. A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482 488.
25. Guthrie P. B., Knappenberger J., Segal M., Charles A. C. Kater S. B. (1999) ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520 528.
26. Hansen T. M., Nielsen H., Bernth N. Moos T. (1999) Expression of ferritin protein and subunit mRNAs in normal and iron deficient rat brain. Mol. Brain Res. 65, 186 197.
27. Hua Y., Nakamura T., Keep R. F., Wu J., Schallert T., Hoff J. T. Xi G. (2006) Long-term effects of experimental intracerebral hemorrhage: the role of iron. J. Neurosurg. 104, 305 312.
28. Huang E., Ong W. Y. Connor J. R. (2004) Distribution of divalent metal transporter-1 in the monkey basal ganglia. Neurosci. 128, 487 496.
29. Huang E., Ong W. Y., Go M. L. Connor J. R. (2006) Upregulation of iron regulatory proteins and divalent metal transporter-1 isoforms in the rat hippocampus after kainate induced neuronal injury. Exp. Brain Res. 170, 376 386.
30. Jefferies W. A., Brandon M. R., Hunt S. V., Williams A. F., Gatter K. C. Mason D. Y. (1984) Transferrin receptor on endothelium of brain capillaries. Nature 312, 162 163.
31. Jeong S. Y. David S. (2006) Age-related changes in iron homeostasis and cell death in the cerebellum of ceruloplasmin-deficient mice. J. Neurosci. 26, 9810 9819.
32. Kacem K., Lacombe P., Seylaz J. Bonvento G. (1998) Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 23, 1 10.
33. Kawabata H., Yang R., Hirama T., Vuong P. T., Kawano S., Gombart A. F. Koeffler H. P. (1999) Molecular cloning of transferrin receptor 2. A new member of the transferrin receptor-like family. J. Biol. Chem. 274, 20826 20832.
34. Kawamata T., Tooyama I., Yamada T., Walker D. G. McGeer P. L. (1993) Lactoferrin immunocytochemistry in Alzheimer and normal human brain. Am. J. Pathol. 142, 1574 1585.
35. Ke Y., Chang Y. Z., Duan X. L., Du J. R., Zhu L., Wang K., Yang X. D., Ho K. P. Qian Z. M. (2005) Age-dependent and iron-independent expression of two mRNA isoforms of divalent metal transporter 1 in rat brain. Neurobiol. Aging 26, 739 748.
36. Klomp L. W., Farhangrazi Z. S., Dugan L. L. Gitlin J. D. (1996) Ceruloplasmin gene expression in the murine central nervous system. J. Clin. Invest. 98, 207 215.
37. Leveugle B., Spik G., Perl D. P., Bouras C., Fillit H. M. Hof P. R. (1994) The iron-binding protein lactoferrin is present in pathological lesions in a variety of neurodegenerative disorders: a comparative immunological analysis. Brain Res. 650, 20 31.
38. Levy J. E., Jin O., Fujiwara Y., Kuo F. Andrews N. C. (1999) Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat. Genet. 21, 396 399.
39. Mato M., Ookawara S. Namiki T. (1989) Studies on the vasculogenesis in rat cerebral cortex. Anat. Rec. 224, 355 364.
40. McKie A. T., Marciani P., Rolfs A. et al. (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell 5, 299 309.
41. Milby K., Oke A. Adams R. N. (1982) Detailed mapping of ascorbate distribution in rat brain. Neurosci. Lett. 28, 169 174.
42. Milligan C. E., Cunningham T. J. Levitt P. (1991) Differential immunochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain. J. Comp. Neurol. 314, 125 135.
43. Montana V., Malarkey E. B., Verderio C., Matteoli M. Parpura V. (2006) Vesicular transmitter release from astrocytes. Glia 54, 700 715.
44. Moos T. (1995) Developmental profile of non-heme iron distribution in the rat brain during ontogenesis. Dev. Brain Res. 87, 203 213.
45. Moos T. (2003) Delivery of transferrin and immunoglobulins to the ventricular system of the rat. Front. Biosci. 8, 102 109.
46. Moos T. Hoyer P. E. (1996) Detection of plasma proteins in CNS neurons: conspicuous influence of tissue-processing parameters and the utilization of serum for blocking nonspecific reactions. J. Histochem. Cytochem. 44, 591 603.
47. 125I]transferrin injected into the ventricular system of the rat. Brain Res. 790, 115 128.
48. Moos T. Morgan E. H. (1998b) Evidence for low molecular weight, non-transferrin-bound iron in rat brain and cerebrospinal fluid. J. Neurosci. Res. 54, 486 494.
49. Moos T. Morgan E. H. (2000) Transferrin and transferrin receptor function in brain barrier systems. Cell. Mol. Neurobiol. 20, 77 95.
50. Moos T. Morgan E. H. (2001) Restricted transport of OX26 through the blood-brain barrier in the rat. J. Neurochem. 79, 119 129.
51. Moos T. Morgan E. H. (2004) The significance of the mutated divalent metal transporter (DMT1) on iron transport into the Belgrade rat brain. J. Neurochem. 88, 233 245.
52. Moos T. Rosengren Nielsen T. (2006) Ferroportin in the postnatal rat brain: implications for axonal transport and neuronal export of iron. Semin. Pediatr. Neurol. 13, 49 57.
53. Moos T., Oates P. S. Morgan E. H. (1998) Expression of the neuronal transferrin receptor is age dependent and susceptible to iron deficiency. J. Comp. Neurol. 398, 420 430.
54. Moos T., Trinder D. Morgan E. H. (2000) Cellular distribution of ferric iron, ferritin, transferrin and divalent metal transporter (DMT1) in substantia nigra and basal ganglia of normal and β2-microglobulin deficient mouse brain. Cell. Mol. Biol. 46, 549 561.
55. Moos T., Skjoerringe T., Gosk S. Morgan E. H. (2006) Brain capillary endothelial cells mediate iron transport into the brain by segregating iron from transferrin without the involvement of divalent metal transporter 1. J. Neurochem. 98, 1946 1958.
56. Morgan E. H. (1977) Iron exchange between transferrin molecules mediated by phosphate compounds and other cell metabolites. Biochim. Biophys. Acta 499, 169 177.
57. Morgan E. H. (1979) Studies on the mechanism of iron release from transferrin. Biochim. Biophys. Acta 580, 312 326.
58. Morgan E. (1981) Transferrin, biochemistry, physiology and clinical significance. Mol. Aspects Med. 4, 1 123.
59. Morgan E. H. (1983) Effect of pH and iron content of transferrin on its binding to reticulocyte receptors. Biochim. Biophys. Acta 762, 498 502.
60. Morgan E. H. (1999) Iron and transition metal transport in the brain, in Brain Barrier Systems, Alfred Benzon Symposium 45 (Paulson O., Knudsen G.M., Moos T. Svejgaard A., eds pp. 357 366. Munksgaard, Copenhagen.
61. Morgan E. H. Moos T. (2002) Mechanism and developmental changes in iron transport across the blood-brain barrier. Dev. Neurosci. 24, 106 113.
62. Neary J. T., Rathbone M. P., Cattabeni F., Abbracchio M. P. Burnstock G. (1996) Trophic action of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurol. Sci. 19, 13 18.
63. Patel B. N. David S. (1997) A novel glycosylphosphatidylinositol-anchored form of ceruloplasmin is expressed by mammalian astrocytes. J. Biol. Chem. 272, 20185 20190.
64. Petroff O. A., Yu R. K. Ogino T. (1986) High-resolution proton magnetic resonance analysis of human cerebrospinal fluid. J. Neurosci. 47, 1270 1276.
65. Roberts R. L., Fine R. E. Sandra A. (1993) Receptor-mediated endocytosis of transferrin at the blood-brain barrier. J. Cell Sci. 104, 521 532.
66. Rouault T. A. (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2, 406 414.
67. Rouault T. A. Cooperman S. (2006) Brain iron metabolism. Semin. Pediatr. Neurol. 13, 142 148.
68. Russo N., Edwards M., Andrews T., O'Brien M. Bhatia K. P. (2004) Hereditary haemochromatosis is unlikely to cause movement disorders-a critical review. J. Neurol. 251, 849 852.
69. Savman K., Nilsson U. A., Thoresen M. Kjellmer I. (2005) Non-protein-bound iron in brain interstitium of newborn pigs after hypoxia. Dev. Neurosci. 27, 176 184.
70. Schipper H. M., Bernier L., Mehindate K. Frankel D. (1999) Mitochondrial iron sequestration in dopamine-challenged astroglia; role of heme oxygenase-1 and the permeability transition pore. J. Neurochem. 72, 1802 1811.
71. Shin E. J., Suh S. K., Lim Y. K. et al. (2005) Ascorbate attenuates trimethyltin-induced oxidative burden and neuronal degeneration in the rat hippocampus by maintaining glutathione homeostasis. Neuroscience 133, 715 727.
72. Siddapappa A. J., Rao R. B., Wobken J. D., Liebold E. A., Connor J. R. 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.
73. Siddapappa A. J., Rao R. B., Wobken J. D., Kasperson K., Liebold E. A., Connor J. R. 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.
74. Siebert P. D. Huang B. C. (1997) Identification of an alternative form of human lactoferrin mRNA that is expressed differentially in normal tissues and tumor-derived cell lines. Proc. Natl Acad. Sci. USA 94, 2198 2203.
75. Sofic E., Riederer P., Heinsen H., Beckmann H., Reynolds G. P., Hebenstreit G. Youdim M. B. (1988) Increased iron (III) and total iron content in post mortem substantia nigra of parkinsonian brain. J. Neural. Transm. 74, 199 205.
76. 13C]NMR spectroscopy of cultured neurons and astrocytes. Neurosci. Lett. 128, 235 239.
77. Strahan M. E., Crowe A. Morgan E. H. (1992) Iron uptake in relation to transferrin degradation in brain and other tissues of rats. Am. J. Physiol. 263, R924 R929.
78. Sturrock A., Alexander J., Lamb J., Craven C. M. Kaplan J. (1990) Characterization of a transferrin-independent uptake system for iron in HeLa cells. J. Biol. Chem. 265, 3139 3145.
79. Szentistvanyi I., Patlak C. S., Ellis R. A. Cserr H. F. (1984) Drainage of interstitial fluid from different regions of rat brain. Am. J. Physiol. 246, F835 F844.
80. Takeda A., Devenyi A. Connor J. R. (1998) Evidence for non-transferrin-mediated uptake and release of iron and manganese in glial cell cultures from hypotransferrinemic mice. J. Neurosci. Res. 51, 454 462.
81. Takeda A., Tataksuka K., Connor J. R. Oku N. (2001) Abnormal iron accumulation in the brain of hypotransferrinemic mice. Brain Res. 912, 154 161.
82. Taylor E. M. Morgan E. H. (1990) Developmental changes in transferrin and iron uptake by the brain in the rat. Dev. Brain Res. 55, 35 42.
83. Taylor E. M., Crowe A. Morgan E. H. (1991) Transferrin and iron uptake by the brain: Effects of altered iron status. J. Neurochem. 57, 1584 1592.
84. 2-microglobulin in cerebrospinal fluid. Elevated levels in patients with acute cerebrovascular lesions as indices of inflammation. Stroke 12, 40 46.
85. Tsutsumi M., Skinner M. K. Sanders-Bush E. (1989) Transferrin gene expression and synthesis by cultured choroid plexus epithelial cells. Regulation by serotonin and cyclic adenosine 3',5'-monophosphate. J. Biol. Chem. 264, 9626 9631.
86. 59Fe uptake into brain and cerebrospinal fluid and the influence thereon of antibodies against the transferrin receptor. J. Neurochem. 60, 106 113.
87. Van Gelder W., Huijskes-Heins M. I., van Dijk J. P., Cleton-Soeteman M. I. van Eijk H. G. (1995) Quantification of different transferrin receptor pools in primary cultures of porcine blood-brain barrier endothelial cells. J. Neurochem. 64, 2708 2715.
88. Van Gelder W., Cleton-Soeteman M. I., Huijskes-Heins M. I., van Run P. R. van Eijk H. G. (1997) Transcytosis of 6.6-nm gold-labeled transferrin: an ultrastructural study in cultured porcine blood-brain barrier endothelial cells. Brain Res. 746, 105 116.
89. Vargas J. D., Herpers B., McKie A. T., Gledhill S., McDonnell J., van den Heuvel M., Davies K. E. Ponting C. P. (2003) Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases. Biochim. Biophys. Acta 1651, 116 123.
90. Visser C. C., Voorwinden L. H., Crommelin D. J., Danhof M. de Boer A. G. (2004) Characterization and modulation of the transferrin receptor on brain capillary endothelial cells. Pharm. Res. 21, 761 769.
91. Wessling-Resnick M. (2006) Iron Imports. III. Transfer of iron from mucosa into circulation. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G1 G6.
92. Wu L. J., Leenders A. G., Cooperman S., Meyron-Holtz E., Smith S., Land W., Tsai R. Y., Berger U. V., Sheng Z. H. Rouault T. A. (2004) Expression of the iron transporter ferroportin in synaptic vesicles and the blood-brain barrier. Brain Res. 1001, 108 117.
93. Xu J. Ling E. A. (1994) Studies of the ultrastructure and permeability of the blood-brain barrier in the developing corpus callosum in postnatal rat brain using electron dense tracers. J. Anat. 184, 227 237.