Transport of iron in the blood-brain-cerebrospinal fluid system

Journal of Neurochemistry

Volumn 69, Issue 2, 1997, Pages 443-454

  Bradbury, M W B ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Blood brain barrier; Cerebrospinal fluid; Iron; Iron transport; Transferrin; Transferrin receptors

Indexed keywords

ASCORBIC ACID; FERRIC CHLORIDE; FERRITIN; IODINE 125; IRON; IRON 59; TRANSFERRIN; TRANSFERRIN RECEPTOR;

BINDING SITE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; GLIA CELL; HUMAN; IRON TRANSPORT; MALE; MEMBRANE TRANSPORT; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; REVIEW; VASCULAR ENDOTHELIUM;

ARACHNOIDEA;

EID: 0030739637     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69020443.x     Document Type: Review

References (121)

1. 65Zn transport into brain and other soft tissues of the rat. J. Physiol. (Lond.) 423, 40P.
2. Aldred A. R., Dickson P. W., Marley P. D., and Schreiber G. (1987) Distribution of transferrin in brain and other tissues of the rat. J. Biol. Chem. 262, 5293-5297.
3. Beard J. L., Connor J. R., and Jones B. C. (1993) Iron in brain. Nutr. Rev. 51, 157-170.
4. Bell J. E., Fryer A. A., Collins M., Marshall T., Jones P. W., Strange R., and Hume R. (1991) Developmental profile of plasma proteins in human cerebrospinal fluid and blood. Neuropathol. Appl. Neurobiol. 17, 441-456.
5. Ben-Shachar D., Eshel B. A., Riederer P., and Youdim M. B. H. (1992) Role of iron and iron chelation in dopaminergic-induced neurodegeneration: implications for Parkinson's disease. Ann. Neurol. 32, S105-S110.
6. 3 uptake. J. Neurochem. 62, 1112-1118.
7. Bickel U., Yoshikawa I., Landaw E. M., Paull K. P., and Pardridge W. M. (1993) Pharmacologic effects in vivo in brain by vector-mediated peptide drug delivery. Proc. Natl. Acad. Sci. USA 90, 2618-2622.
8. Bleijenberg B. G., Van Eijk H. G., and Leijnse B. (1979) The determination of nonheme iron and transferrin in cerebrospinal fluid. Clin. Chim. Acta 31, 277-281.
9. Bloch B., Popovici T., Levin M., Tull D., and Kahn A. (1985) Transferrin gene expression visualized in oligodendrocytes of a rat brain by using in situ hybridizations and immunohistochemistry. Proc. Natl. Acad. Sci. USA 481, 142-160.
10. Bradbury M. W. B. (1979) The Concept of a Blood-Brain Barrier. John Wiley, Chichester.
11. Bradbury M. W. B. (1992) Trace metal transport at the blood-brain barrier, in Handbook for Experimental Pharmacology, Vol. 103: Physiology and Pharmacology of the Blood-Brain Barrier (Bradbury M. W. B., ed), pp. 263-278. Springer-Verlag, Berlin.
12. 2+ into brain during cerebrovascular perfusion in the anaesthetized rat. J. Physiol. (Lond.) 479, 37P.
13. Bradbury M. W. B. (1996) Observations from the anaesthetized rabbit, pertinent to the mechanism of iron transport into brain. J. Physiol. (Lond.) 491, 30P.
14. Breuer W., Epsztejn S., and Cabantchik Z. I. (1995) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J. Biol. Chem. 270, 24209-24215.
15. Brissot P., Wright T. L., Ma W. L., and Weiseger 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.
16. Broadwell R. D. (1989) Transcytosis of macromolecules through the blood-brain barrier: a cell biological perspective and critical appraisal. Acta Neuropathol. 79, 117-128.
17. Broadwell R. D., Baker-Cairns B. J., Friden P. M., Oliver C., and Villegas J. C. (1996) Transcytosis through mammalian cerebral epithelium and endothelium. Part III. Receptor-mediated endocytosis at the blood-brain barrier of blood-borne transferrin and antibody against the transferrin receptor. Exp. Neurol. 142, 47-65.
18. Cavanagh M. E., Cornelis M., Dziegielewska K. M., Luft A. J., Lai P. C., Lorschieder F. L., and Saunders N. R. (1982) Proteins in cerebrospinal fluid and plasma of fetal pigs during development. Dev. Neurosci. 5, 492-502.
19. Chen Q., Connor J. R., and Beard J. L. (1995) Brain, iron, transferrin and ferritin concentrations are altered in developing iron-deficient rats. J. Nutr. 125, 1529-1535.
20. Connor J. R. and Benkovic S. A. (1992) Iron regulation in the brain: histochemical, biochemical, and molecular considerations. Ann. Neurol. 32, S51-S61.
21. Connor J. R., Snyder B. S., Beard J. L., Fine R. E., and Mufson E. J. (1992a) Regional distribution of iron and iron regulatory proteins in the brain in aging and Alzheimer's disease. J. Neurosci. Res. 31, 327-335.
22. Connor J. R., Menzies S. L., St. Martin S. M., and Mufson E. J. (1992b) A histochemical study of iron, transferrin, and ferritin in Alzheimer diseased brains. J. Neurosci. Res. 31, 75-83.
23. Crichton R. R. (1991) Inorganic Biochemistry of Iron Metabolism. Ellis Horwood, New York.
24. Crowe A. and Morgan E. H. (1992) Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res. 592, 8-16.
25. Dallman P. R. and Spirito R. A. (1977) Brain iron in the rat: extremely slow turnover in normal rats may explain long-lasting effects of early iron deficiency. J. Nutr. 107, 1075-1081.
26. Dallman P. R., Simes M. A., and Manies E. C. (1975) Persistent deficiency following short term iron deprivation in the young rat. Br. J. Haematol. 31, 209-215.
27. Davson H., Welch K., and Segal M. B. (1987) Physiology and Pathophysiology of the Cerebrospinal Fluids. Churchill Livingstone, Edinburgh.
28. Del Principe D., Menichelli A., and Colistra C. (1989) The ceruloplasmin and transferrin systems in cerebrospinal fluid in acute leukaemia patients. Acta Paediatr. Scand. 78, 327-328.
29. Dwork A. J., Schon E. A., and Herbert J. (1988) Non-identical distribution of transferrin and ferric iron in human brain. Neuroscience 27, 333-345.
30. Dziegielewska K. M. and Saunders N. R. (1982) Transferrin in fetal sheep cerebrospinal fluid and plasma during gestation. Comp. Biochem. Physiol. 73A, 327-329.
31. Dziegielewska K. M., Evans C. A. N., New H., Reynolds M. L., and Saunders N. R. (1984a) Synthesis of plasma proteins by rat fetal brain and choroid plexus. Int. J. Dev. Neurosci. 2, 215-222.
32. Dziegielewska K. M., Reynolds M. L., Sarantis M. E. P., and Saunders N. R. (1984b) Plasma proteins in fetal sheep brain: correlation of immuno-chemical distribution and local synthesis. J. Physiol. (Lond.) 353, 48P.
33. El-Yazigi A., Al-Saleh I., and Al-Meftz O. (1986) Concentrations of iron, molybdenum, arsenic and lithium in cerebrospinal fluid of patients with brain tumours. Clin. Chem. 32, 2187-2190.
34. Fatemi S. J. A., Kadir F. H. A., and Moore G. R. (1991) Aluminium transport in blood-serum. Binding of aluminium by human transferrin in the presence of human albumin and citrate. Biochem. J. 280, 527-532.
35. 125I-ferrotransferrin binding sites in the mesencephalon of control subjects and patients with Parkinson's disease. J. Neurochem. 60, 2338-2341.
36. Felgenhauer K. (1974) Protein size and cerebrospinal fluid. Klin. Wochenschr. 52, 1158-1164.
37. Fishman J. B., Rubin J. B., Handrahan J. V., Connor J. R., and Fine R. E. (1987) Receptor-mediated transcytosis of transferrin across the blood-brain barrier. J. Neurosci. Res. 18, 299-304.
38. Fleming J. and Joshi J. G. (1987) Ferritin: isolation of aluminum-ferritin complex from brain. Proc. Natl. Acad. Sci. USA 84, 7866-7870.
39. Friden P. M., Walus L. R., Musso G. F., Taylor M. A., Malfroy B., and Starzyk R. M. (1991) Anti-transferrin receptor antibody and antibody-drug conjugates across the blood-brain barrier. Proc. Natl. Acad. Sci. USA 88, 4771-4775.
40. Friden P. M., Walus L. R., Watson P., Doctrow S. R., Kozarich J. W., Backman C., Bergman H., Hoffer B., Bloom P., and Granholm A. C. (1993) Blood-brain barrier penetration and in vivo activity of an NGF conjugate. Science 259, 373-377.
41. Gelman B. B. (1995) Iron in CNS disease. J. Neuropathol. Exp. Neurol. 54, 477-486.
42. Gelman B. B., Rodriguez-Wolf M. G., Wen J., Kumar S., Campbell G. A., and Herzog N. (1992) Siderotic cerebral macrophages in the acquired immune-deficiency syndrome. Arch. Pathol. Lab. Med. 116, 509-516.
43. Gerber M. R. and Conner J. R. (1989) Do oligodendrocytes mediate iron regulation in the human brain? Ann. Neurol. 26, 95-98.
44. Gerlach M., Ben-Shachar D., Riederer P., and Youdim M. B. H. (1994) Altered brain metabolism of iron as a cause of neurodegenerative disease. J. Neurochem. 63, 793-807.
45. Giometto B., Bozza F., Argentiero V., Gallo P., Pagni S., Piccinno M. G., and Travolato B. (1990) Transferrin receptor in rat central nervous system. An immunohistochemical study. J. Neurol. Sci. 98, 81-90.
46. Gruener N., Gozlan O., Goldstein T., Davis J., Besner I., and Iancu T. C. (1991) Iron, transferrin and ferritin in cerebrospinal fluid of children. Clin. Chem. 37, 263-265.
47. Gutteridge J. M. C. (1992) Ferrous ions detected in cerebrospinal fluid by using bleomycin and DNA damage. Clin. Sci. 82, 315-320.
48. Gutteridge J. M. C. (1994) Hydroxyl radicals, iron, oxidative stress and neurodegeneration. Ann. NY Acad. Sci. 738, 201-213.
49. Haerer A. F. (1971) Citrate and alpha-ketoglutarate in cerebrospinal fluid and blood. Neurology (Minneap.) 21, 1059-1065.
50. Hallgren B. and Sourander P. (1958) The effect of age on the non haemin iron in the human brain. J. Neurochem. 3, 41-51.
51. Hershey C. O., Hershey L. A., Varnes A., Vibhakar S. D., Lavin P., and Strain W. H. (1983) Cerebrospinal fluid trace element content in dementia: clinical, radiologic and pathologic correlations. Neurology 33, 1350-1353.
52. Hill J. H. (1988) The distribution of iron in brain, in Topics in Neurochemistry and Neuropharmacology, Vol. 2: Brain Iron: Neurochemical and Behavioural Aspects (Youdim M. B. H., ed), pp. 1-24. Taylor and Francis, London.
53. Hill J. M. and Switzer R. C. (1984) The regional distribution and cellular localization of iron in the rat brain. Neuroscience 11, 595-603.
54. Huebers H. A. and Finch C. A. (1987) The physiology of transferrin and transferrin receptors. Physiol. Rev. 67, 520-582.
55. Jefferies W. A., Brandon M. R., Hunt S. V., Williams A. F., Gatter K. C., and Mason D. Y. (1984) Transferrin receptor on endothelium of brain capillaries. Nature 312, 162-163.
56. Kalaria R. N., Sromek S. M., Grahovac I., and Harik S. I. (1992) Transferrin receptors of rat and human brain and cerebral microvessels and their status in Alzheimer's disease. Brain Res. 585, 87-93.
57. Kaneko Y., Kitamoto T., Tateishi J., and Yamaguchi K. (1989) Ferritin immunochemistry as a marker for microglia. Acta Neuropathol. 79, 129-136.
58. Kjellin K. G. (1966) Determination of the iron content in cerebrospinal fluid. J. Neurochem. 13, 413-422.
59. Lamoureux G., Jolicoeur R., Giard N., St.-Hilaire M., and Duplantis F. (1975) Cerebrospinal fluid proteins in multiple sclerosis. Neurology 25, 537-552.
60. Leenders K. L., Antonini A., Schwarzbach R., Smith-Jones P., Reist H., Ben-Shachar D., Youdim M., and Henn V. (1994) Blood to brain iron uptake in one rhesus monkey using Fe-52 citrate and positron emission tomography (PET). J. Neural Transm. Suppl. 43, 123-132.
61. LeVine S. M. and Macklin W. B. (1990) Iron-enriched oligodendrocytes; a reexamination of their spatial distribution. J. Neurosci. Res. 26, 508-512.
62. +-ATPase from reticulocyte endosomes reconstituted into liposomes acts as an iron transporter. J. Biol. Chem. 269, 10242-10246.
63. +-ATPase. Biochemistry 34, 5130-5136.
64. Martell A. E. and Smith R. M. (1977) Critical Stability Constants, Vol. 3: Other Organic Ligands. Plenum, New York.
65. Martell A. E. and Smith R. M. (1982) Critical Stability Constants, Vol. 5: First Supplement. Plenum, New York.
66. May W. S. and Cuatrecasas P. (1985) Transferrin receptor: its biological significance. J. Membr. Biol. 88, 205-215.
67. Mefford I. N., Oke A. F., and Adams R. N. (1981) Regional distribution of ascorbate in human brain. Brain Res. 212, 223-226.
68. Milby K., Oke A., and Adams R. N. (1982) Detailed mapping of ascorbate distribution in rat brain. Neurosci. Lett. 28, 169-174.
69. Morris C. M., Candy J. M., Court J. A., Whitford C. A., and Edwardson J. A. (1987) The role of transferrin in the uptake of aluminium and manganese by the IMR32 neuroblastoma cell line. Biochem. Soc. Trans. 15, 498.
70. Morris C. M., Candy J. M., Oakley A. E., Bloxham C. A., and Edwardson J. A. (1992a) Histochemical distribution of non-haem iron in the human brain. Acta Anat. (Basel) 144, 235-257.
71. Morris C. M., Candy J. M., Bloxham C. A., and Edwardson J. A. (1992b) Immunocytochemical localization of transferrin in the human brain. Acta Anat. (Basel) 143, 14-18.
72. Morris C. M., Keith A. B., Edwardson J. A., and Pullen R. G. L. (1992c) Uptake and distribution of iron and transferrin in the adult rat brain. J. Neurochem. 59, 300-306.
73. Morris C. M., Candy J. M., Omar S., Bloxham C. A., and Edwardson J. A. (1994) Transferrin receptors in the parkinsonian midbrain. Neuropathol. Appl. Neurobiol. 20, 468-472.
74. Mundigl O., Matteoli M., Daniell L., Thomas-Roetz A., Metcalf A., Jahn R., and De Camilli P. (1993) Synaptic vesicle proteins and early endosomes in cultured hippocampal neurones; differential effects of brefeldin A in axon and dendrites. J. Cell Biol. 122, 1207-1221.
75. Munro H. (1993) The ferritin genes: their response to iron status. Nutr. Rev. 51, 65-73.
76. 55Fe and effect of calcium deficiency. J. Neurochem. 58, 898-902.
77. Murphy V. A., Wadhwani K. C., Smith Q. R., and Rapoport S. I. (1991) Saturable transport of manganese (II) across the rat blood-brain barrier. J. Neurochem. 57, 948-954.
78. New H., Dziegielewska K. M., and Saunders N. R. (1983) Transferrin in fetal rat brain and cerebrospinal fluid. Int. J. Dev. Neurosci. 1, 369-373.
79. Núñez M.-T., Gaete V., Watkins J. A., and Glass J. (1990) Mobilization of iron from endocytic vesicles. The effects of acidification and reduction. J. Biol. Chem. 265, 6688-6692.
80. O'Halloran T. V. (1993) Transition metals in control of gene expression. Science 261, 715-725.
81. Olanow C. W. (1992) An introduction to the free radical hypothesis in Parkinson's disease. Ann. Neurol. 32, S2-S9.
82. Pardridge W. M., Eisenberg J., and Yang J. (1987) Human blood-brain barrier transferrin receptor. Metabolism 36, 892-893.
83. Pardridge W. M., Buciak J. L., and Friden P. M. (1991) Selective transport of an anti-transferrin receptor antibody through the blood-brain barrier in vivo. J. Pharmacol. Exp. Ther. 259, 66-70.
84. Patino M. M. and Walden W. E. (1992) Cloning of a functional cDNA for the rabbit ferritin in RNA repressor protein. J. Biol. Chem. 267, 19011-19016.
85. Patlak C. S., Blasberg R. G., and Fenstermacher J. D. (1983) Graphical evaluation of blood-brain transfer constants from multiple-time uptake data. J. Cereb. Blood Flow Metab. 3, 1-7.
86. Pountney D. J., Raja K. B., Bothwood M. J., Wrigglesworth J. M., and Simpson R. J. (1996) Mucosal surface reductase activity in mouse duodenum. Biometals 9, 15-20.
87. 54Mn in the anaesthetized rat. J. Physiol. (Lond.) 446, 507P.
88. 65Zn uptake from blood into brain in the rat. J. Neurochem. 56, 485-489.
89. Qian Z. M. and Tang P. L. (1995) Mechanisms of iron uptake by mammalian cells. Biochim. Biophys. Acta 1269, 205-214.
90. Rabin O., Hegedus L., Bourre J.-M., and Smith Q. R. (1993) Rapid brain uptake of manganese(II) across the blood-brain barrier. J. Neurochem. 61, 509-517.
91. Raja K. B., Simpson R. J., and Peters T. J. (1992) Investigation of a role for reduction in ferric iron uptake by mouse duodenum. Biochim. Biophys. Acta 1135, 141-146.
92. Raub T. J. and Newton C. R. (1991) Recycling kinetics and transcytosis of transferrin in primary cultures of bovine brain microvessel endothelial cells. J. Cell. Physiol. 149, 141-145.
93. Ridge B. D., Fairhurst E., Chadwick D., and Reynolds E. H. (1976) Ascorbic acid concentration in human plasma and cerebrospinal fluid. Proc. Nutr. Soc. 35, 57A-58A.
94. Riederer P., Sofic E., Rausch W.-D., Schmidt B., Reynolds G. P., Jellinger K., and Youdim M. B. H. (1989) Transition metals, ferritin, glutathione and ascorbic acid in parkinsonian brains. J. Neurochem. 52, 515-520.
95. Roberts R., Sandra A., Siek G. C., Lucas J. J., and Fine R. E. (1992) Studies of the mechanism of iron transport across the blood-brain barrier. Ann. Neurol. 32, S43-S50.
96. Roberts R. L., Fine R. E., and Sandra A. (1993) Receptor-mediated endocytosis of transferrin at the blood-brain barrier. J. Cell Sci. 104, 521-532.
97. Roskams A. J. I. and Connor J. R. (1994) Iron, transferrin and ferritin in the rat brain during development and aging. J. Neurochem. 63, 709-716.
98. 125I-labeled β-amyloid peptide A beta 1-40 through the blood-brain barrier and binding to Alzheimer disease amyloid of the A beta 1-40/vector complex. Proc. Natl. Acad. Sci. USA 92, 10227-10231.
99. 125I] transferrin through the rat blood-brain barrier. Brain Res. 683, 164-171.
100. Smith R. M. and Martell A. E. (1989) Critical Stability Constants, Vol. 6: Second Supplement. Plenum, New York.
101. Spector R. (1977) Vitamin homeostasis in the central nervous system. N. Engl. J. Med. 296, 1393-1398.
102. Spector R. and Lorenzo A. V. (1974) Specificity of ascorbic acid transport system in the central nervous system. Am. J. Physiol. 226, 1468-1473.
103. Strahan M. E., Crowe A., and Morgan E. H. (1992) Iron uptake in relation to transferrin degradation in brain and other tissues of rats. Am. J. Physiol. 263, R924-R929.
104. Suárez N. and Eriksson H. (1993) Receptor-mediated endocytosis of a manganese complex of transferrin into neuroblastoma (SHSY5Y) cells in culture. J. Neurochem. 61, 127-131.
105. Swaiman K. F. and Machen V. L. (1984) Iron uptake by mammalian cortical neurones. Ann. Neurol. 16, 66-70.
106. Taylor E. M. (1993) Transfer of Iron Across Cellular Barriers. Ph.D. Thesis, London University.
107. Taylor E. M. and Morgan E. H. (1990) Developmental changes in transferrin and iron uptake by the brain in the rat. Dev. Brain Res. 55, 35-42.
108. Taylor E. M., Crowe A., and Morgan E. H. (1991) Transferrin and iron uptake by the brain: effects of altered iron status. J. Neurochem. 57, 1584-1592.
109. Theil E. C. (1987) Ferritin: structure, gene regulation, and cellular function in animals, plants and microorganisms. Annu. Rev. Biochem. 56, 289-315.
110. Tu G.-F., Achen M. G., and Aldred A. R. (1991) The distribution of cerebral expression of the transferrin gene is species-specific. J. Biol. Chem. 266, 6201-6208.
111. 59Fe uptake into brain and cerebrospinal fluid and the influence thereon of antibodies against the transferrin receptor. J. Neurochem. 60, 106-113.
112. Ule G., Völkl A., and Berlet H. (1974) Spurenelemente im menschlichen Gehirn II. Kupfer-, Zink, Calcium-und Magnesiumkonzentration in 13 verschiedenen Hirnregionen während der 4. bis 8. Lebensdekade im Vergleich zum Hirneisen. Z. Neurol. 206, 117-128.
113. Völkl A. and Ule G. (1972) Spurenelemente im menschlichen Gehirn. Altersabhängikeit der Eisenkonzentration in 13 verschiedenen Hirnregionen. Z. Neurol. 202, 331-338.
114. Vorbrodt A. W. (1989) Ultracytochemical characterization of anionic sites in the wall of brain capillaries. J. Neurocytol. 18, 359-368.
115. Wagner-Recio M., Toews A. D., and Morell P. (1991) Tellurium blocks cholesterol synthesis by inhibiting squalene metabolism: preferential vulnerability to this metabolic block leads to peripheral nervous system demyelination. J. Neurochem. 57, 1891-1901.
116. r iron isolated from guinea pig reticulocytes as AMP-Fe and ATP-Fe complexes. Biochem. J. 261, 787-792.
117. Weaver J. and Pollack S. (1990) Two types of receptors for iron on mitochondria. Biochem. J. 271, 463-466.
118. Wong R. P. K. and Bradbury M. W. B. (1975) Permeability of the blood-brain barrier to calcium in adrenal deficiency. Brain Res. 84, 361-364.
119. Wrigglesworth J. M. and Baum H. (1988) Iron-dependent enzymes in the brain, in Topics in Neurochemistry and Neuropharmacology, Vol. 2: Brain Iron Neurochemical and Behavioural Aspects (Youdim M. B. H., ed), pp. 25-66. Taylor and Francis, London.
120. Yoshikawa R. and Pardridge W. M. (1992) Biotin delivery to brain with a covalent conjugate of avidin and a monoclonal antibody to the transferrin receptor. J. Pharmacol. Exp. Ther. 263, 897-903.
121. Yu Y., Radisky E., and Leibold E. A. (1992) The iron-responsive element binding protein. Purification, cloning and regulation in rat liver. J. Biol. Chem. 267, 19005-19010.