Transferrin and transferrin receptor function in brain barrier systems

Cellular and Molecular Neurobiology

Volumn 20, Issue 1, 2000, Pages 77-95

  Moos, Torben ^a   Morgan, Evan H ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Blood brain barrier; Blood CSF barrier; Iron; Transferrin; Transferrin receptor

Indexed keywords

IRON BINDING PROTEIN; TRANSFERRIN; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; CELL MEMBRANE TRANSPORT; CEREBROSPINAL FLUID; GLIA CELL; IRON TRANSPORT; NERVE CELL; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CEREBROSPINAL FLUID; ION TRANSPORT; IRON; ORGANELLES; RATS; RECEPTORS, TRANSFERRIN; TRANSFERRIN;

ANIMALIA;

EID: 0033961913     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006948027674     Document Type: Article

References (115)

1. Aizenman, Y., and de Vellis, J. (1987). Brain neurons develop in a serum and glial free environment: Effects of transferrin, insulin, insulin-like growth factor-I and thyroid hormone on neuronal survival, growth and differentiation. Brain Res. 406:32-42.
2. Aizenman, Y., Weichsel, M. E., and de Vellis, J. (1986). Changes in insulin and transferrin requirements of pure brain neuronal cultures during embryonic development. Proc. Natl. Acad. Sci. USA 83:2263-2266.
3. Aldred, A. R., Dickson, P. W., Marley, P. D., and Schreiber, G. (1987). Distribution of transferrin synthesis in the brain and other tissues in the rat. J. Biol. Chem. 262:5293-5297.
4. Angelova-Gateva, P. (1979). Iron transferrin receptors in rat and human cerebrum. Agressologie 21:27-30.
5. Baker, E., and Morgan, E. H. (1994). Iron transport. In Brock, J. H., Halliday, J. W., Pippard, M. J., and Powell, L. W. (eds.), Iron Metabolism in Health and Disease, Saunders, London, pp. 63-95.
6. Banks, W. A., Kastin, A. J., Fasold, M. B., Barrera, C. M., and Augereau, G. (1988). Studies of the slow bidirectional transport of iron and transferrin across the blood-brain barrier. Brain Res. Bull. 21:881-885.
7. Barakat-Walter, I., Deloulme, J. C., Sensenbrenner, M., and Labourdette, G. (1991). Proliferation of chick embryo neuroblasts grown in the presence of horse serum requires exogenous transferrin. J. Neurosci. Res. 28:391-398.
8. Bartlett, W. P., Li, X.-S., and Connor, J. R. (1991). Expression of transferrin mRNA in the CNS of normal and jimpy mice. J. Neurochem. 57:318-322.
9. Bell, J. D., Brown, J. C. C., Sadler, P. J., Macleod, A. F., Sönksen, P. H., Hughes, R. D., and Williams, R. (1987). High resolution proton nuclear magnetic resonance studies of human cerebrospinal fluid. Clin. Sci. 72:563-570.
10. Bickel, V., Kank, Y.-S., Yoshikawa, T., and 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.
11. Bloch, B., Povovici, T., Levin, M. J., Tuil, D., and 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.
12. Bloch, B., Popovici, T. M., Chouham, S., Levin, M. J., Tuil, D., and Kahn, A. (1987). Transferrin gene expression in choroid plexus of the adult rat brain. Brain Res. Bull. 18:573-576.
13. Bowen, B., and Morgan, E. H. (1987). Anemia of the Belgrade rat: Evidence for defective membrane transport of iron. Blood 70:38-44.
14. Brightman, M. W. (1965). The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. I. Ependymal distribution. J. Cell. Biol. 26:99-123.
15. Broadwell, R. D. (1989). Transcytosis of macromolecules through the blood-brain barrier: A cell biological perspective and critical appraisal. Acta Neuropathol. 79:117-128.
16. Broadwell, R. D., Balin, B. J., Salcman, M., and Kaplan, R. S. (1983). Blood-brain barrier? Yes or no. Proc. Natl. Acad. Sci. USA 80:7352-7356.
17. Broadwell, R. D., Baker-Cairns, B., Friden, P. M., Oliver, C., and Villegas, J. C. (1996). Transcytosis of protein through the mammalian cerebral epithelium and endothelium. Exp. Neurol. 142:47-65.
18. Connor, J. R., and Fine, R. E. (1986). The distribution of transferrin immunoreactivity in the rat central nervous system. Brain Res. 368:319-328.
19. Connor, J. R., and Fine, R. E. (1987). Development of transferrin-positive oligodendrocytes in the rat central nervous system. J. Neurosci. Res. 17:51-59.
20. Connor, J. R., Phillips, T. M., Lakshman, M. R., Barron, K. D., Fine, R. E., and Csiza, C. K. (1987). Regional variation in the levels of transferrin in the CNS of normal and myelin-deficient rats. J. Neurochem. 49:1523-1529.
21. Crowe, A., and Morgan, E. H. (1992). Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res. 592:8-16.
22. Crowe, A., and Morgan, E. H. (1994). Effects of chelators on iron uptake and release by the brain in the rat. Neurochem. Res. 19:71-76.
23. Cserr, H. F., Cooper, D. N., Suri, P. K., and Patlak, C. S. (1981). Efflux of radiolabelled polyethylene glycols and albumin from rat brain. Am. J. Physiol. 240:F319-F328.
24. Descamps, L., Dehouck, M.-P., Torpier, G., and Cecchelli, R. (1996). Receptor mediated transcytosis of transferrin through blood-brain barrier endothelial cells. Am. J. Physiol. 270:H1149-H1158.
25. Dickson, P. W., Alred, A. R., Marley, P. D., Guo-Fen, T., Howlett, G. J., and Schreiber, G. (1985). High prealbumin and transferrin mRNA levels in the choroid plexus of rat brain. Biochem. Biophys. Res. Commun. 127:890-895.
26. Dion, T. L., Markelonis, G. J., Oh, T. H., Bregman, B. S., Pugh, M. A., Hobbs, S. L., and Kim, Y. C. (1988). Immunocytochemical localization of transferrin and mitochondrial malate dehydrogenase in the developing nervous system of the rat. Dev. Neurosci. 10:152-164.
27. Dunker, R. O., Harris, A. B., and Jenkins, D. P. (1976). Kinetics of horseradish peroxidase migration through cerebral cortex. Brain Res. 118:199-217.
28. Dwork, A. J., Schon, E. A., and Herbert, J. (1988). Nonidentical distribution of transferrin and ferric iron in human brain. Neuroscience 27:333-345.
29. Dwork, A. J., Lawler, G., Zybert, P. A., Durkin, M., Osman, M., Willson, N., and Barkai, A. I. (1990). An autoradiographic study of the uptake and distribution of iron by the brain of the young rat. Brain Res. 518:31-39.
30. Dziegielewska, K. M., Evans, C. A. N., Malinowska, D. H., Møllgård, K., Reynolds, M. L., and Saunders, N. R. (1980). Blood-cerebrospinal fluid transfer of plasma proteins during fetal development in the sheep. J. Physiol. 300:457-465.
31. Dziegielewska, K. M., Evans, C. A. N., New, H., Reynolds, M. L., and Saunders, N. R. (1984). Synthesis of plasma proteins by rat fetal brain and choroid plexus. Int. J. Dev. Neurosci. 2:215-222.
32. Ekblom, P., and Thesloff, I. (1995). The role of transferrin and extracellular matrix components in kidney development. Modern Cell Biol. 4:85-127.
33. Espinosa de los Monteros, A., and Foucard, B. (1987). Effect of iron and transferrin on pure oligodendrocytes in culture; Characterization of a high-affinity transferrin receptor at different ages. Dev. Brain. Res. 35:123-130.
34. Espinosa de los Monteros, A., Chiappelli, F., Fisher, R. S., and de Vellis, J. (1988). Transferrin: An early marker of oligodendrocytes in culture. Int. J. Dev. Neurosci. 6:167-175.
35. Espinosa de los Monteros, A., Kumar, S., Scully, S., Cole, R., and de Vellis, J. (1990). Transferrin gene expression and secretion by rat brain cells in vitro. J. Neurosci. Res. 25:576-580.
36. Espinosa de los Monteros, A., Sawaya, B. E., Guillou, F., Zakin, M. M., de Vellis, J., and Schaeffer, E. (1994). Brain-specific expression of the human transferrin gene. Similar elements govern expression in oligodendrocytes and a neuronal cell line. J. Biol. Chem. 269:24504-24510.
37. Farcich, E., and Morgan, E. H. (1992). Diminished iron acquisition by cells and tissues of Belgrade laboratory rats. Am. J. Physiol. 262:R220-R224.
38. 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.
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 cross the blood-brain barrier. Proc. Natl. Acad. Sci. USA 88:4771-4775.
40. Friden, P. M., Olson, T. S., Obar, R., Walus, L. R., and Putney, S. D. (1996). Characterization, receptor mapping and blood-brain barrier transcytosis of antibodies to the human transferrin receptor. J. Pharmacol. Exp. Ther. 2:1491-1498.
41. Gerber, M. R., and Connor, J. R. (1989). Do oligodendrocytes mediate iron regulation in the human brain? Ann. Neurol. 26:95-98.
42. Giometto, B., Bozza, F., Argentiero, V., Gallow, P., Pagni, S., Piccinno, M. G., and Tavolato, B. (1990). Transferrin receptors in the rat central nervous system. An immunocytochemical study. J. Neurol. Sci. 98:81-90.
43. Gocht, A., Keith, A. B., Candy, J. M., and Morris, C. M. (1993). Iron uptake in the brain of myelin-deficient rats. Neurosci. Lett. 154:187-190.
44. Graeber, M. B., Raivich, G., and Kreutzberg, G. W. (1989). Increase of transferrin receptors and iron uptake in regenerating motor neurons. J. Neurosci. Res. 23:342-345.
45. Harford, J., Rouault, T. A., and Klausner, R. D. (1994). The control of cellular iron homeostasis. In Brock, J. H., Halliday, J. W., Pippard, M. J., and Powell, L. W. (eds.), Iron Metabolism in Health and Disease, Saunders, London, pp. 123-149.
46. Harris, D. C., and Aisen, P. (1989). Physical biochemistry of the transferrins. In Loehr, T. W. (ed.), Iron Carriers and Iron Proteins, VCH, New York, pp. 239-371.
47. Hill, J. M., Ruff, M. R., Weber, R. J., and Pert, C. B. (1985). Transferrin receptors in rat brain: Neuropeptide-like pattern and relationship to iron distribution. Proc. Natl. Acad. Sci. USA 82:4553-4557.
48. Idzerda, R. L., Huebers, H., Finch, C. A., and McKnight, G. S. (1986). Rat transferrin gene expression: Tissue-specific regulation by iron deficiency. Proc. Natl. Acad. Sci. USA 83:3723-3727.
49. 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.
50. Jordan, S. M., and Morgan, E. H. (1969). Plasma protein synthesis by tissue slices from pregnant and lactating rats. Biochim. Biophys. Acta 174:373-349.
51. Kalaria, R. N., Sromek, S. M., Grahovac, I., and Harik, S. I. (1992). Transferrin receptors in rat and human brain and cerebral microvessels and their status in Alzheimer's disease. Brain Res. 585:87-93.
52. Kaur, C., and Ling, E. A. (1995). Transient expression of transferrin receptors and localisation of iron in amoeboid microglia in postnatal rats. J. Anat. 186:165-173.
53. Kennard, M. L., Richardson, D. R., Gabathuler, R., Ponka, P., and Jefferies, W. A. (1995). A novel iron uptake mechanism mediated by GPI-anchored human p97. EMBO J. 17:4178-4186.
54. Kennard, M. L., Feldman, H., Yamada, T., and Jefferies, W. A. (1996). Serum levels of the iron binding protein p97 are elevated in alzheimer's disease. Nature Med. 2:1230-1235.
55. Kuhn, L. Schulman, H., and Ponka, P. (1990). Iron-transferrin requirements and transferrin receptor expression in proliferating cells. In Ponka, P., Schulman, H., and Woodworth, R. C. (eds.), Iron Transport and Storage, CRC Press, Boca Raton; FL, pp. 149-191.
56. Levin, M. J., Tuil, D., Uzan, G., Dreyfus, J.-C., and Kahn, A. (1984). Expression of transferrin gene during development of non-hepatic tissues. High levels of transferrin mRNA in fetal muscle and adult brain. Biochem. Biophys. Res. Commun. 122:212-217.
57. Lim, B.-C., McArdle, H. J., and Morgan, E. H. (1987). Transferrin-receptor interaction and iron uptake by reticulocytes of vertebrate animals - A comparative study. J. Comp. Physiol. 157:363-371.
58. Markelonis, G. J., Oh, T. H., Park, L. P., Cha, C. Y., Sofia, C. A., Kim, J. W., and Azari, P. (1985a). Synthesis of transferrin receptor by cultures of embryonic chicken spinal neurons. J. Cell Biol. 100:8-17.
59. Markelonis, G. J., Oh, T. H., Park, L. P., Azari, P., and Max, S. R. (1985b). Receptor-mediated uptake of labelled transferrin by embryonic chicken dorsal root ganglion neurons in culture. Int. J. Dev. Neurosci. 3:257-266.
60. Markelonis, G. J., Oh, T. H., Dion, T. L., Bregman, B. S., Pugh, M. A., Royal, G. M., Kim, Y. C., and Hobbs, S. L. (1988). Localization of transferrin within the developing vertebrate nervous system. Rev. Neurol. (Paris) 144:648-655.
61. Mash, D. C., Pablo, J., Flynn, D. D., Efange, S. M. N., and Weiner, W. J. (1990). Characterization and distribution of transferrin receptors in the rat brain. J. Neurochem. 55:1972-1979.
62. Mesher, A. L., and Munaim, S. I. (1988). Transferrin and the growth-promoting effect of nerves. Int. Rev. Cytol. 110:1-26.
63. Møllgård, K., Jacobsen, M., Jacobsen, G. K., Clausen, P. P., and Saunders, N. R. (1979). Immunohistochemical evidence for an intracellular localization of plasma proteins in human foetal choroid plexus and brain. Neurosci. Lett. 14:85-90.
64. Møllgård K., Reynolds, M., Jacobsen, M., Dziegielewska, K. M., and Saunders, N. R. (1984). Differential immunocytochemical staining for fetuin and transferrin in the developing cortical plate. J. Neurocytol. 13:497-502.
65. Møllgård, K., Stagaard, M., and Saunders, N. R. (1987). Cellular distribution of transferrin immunoreactivity in the developing brain. Neurosci. Lett. 78:35-40.
66. Møllgård, K. Dziegielewska, K. M., Saunders, N. R., Zakut, H., and Soreq, H. (1988). Synthesis and localization of plasma proteins in the developing human brain. Integrity of the fetal blood-brain barrier to endogenous proteins of hepatic origin. Dev. Biol. 128:207-221.
67. Moos, T. (1995a). Age-dependent uptake and retrograde axonal transport of exogenous albumin and transferrin in rat motor neurons. Brain Res. 672:14-23.
68. Moos, T. (1995b). Increased accumulation of transferrin by motor neurons of the mouse mutant progressive motor neuronopathy (pmn/pmn). J. Neurocytol. 24:389-398.
69. Moos, T., and Höyer, P. E. (1996). Detection of plasma proteins in CNS neurons: conspicious influence of tissue-processing parameters and the utilization of serum for blocking nonspecific reactions. J. Histochem. Cytochem. 44:591-603.
70. 125I]transferrin injected into the ventricular system of the rat. Brain Res. 790:115-128.
71. Morgan, E. H. (1981). Transferrin, biochemistry, physiology and clinical significance. Mol. Aspects Med. 4:1-123.
72. Morgan, E. H. (1983). Synthesis and secretion of transferrin. In Glaumann, H., Peters, T., and Redman, C. (eds.), Plasma Protein Secretion by the Liver, Academic Press, London, pp. 331-355.
73. Morgan, E. H. (1996). Iron metabolism and transport. In Zakin, D., and Boyer, T. D. (eds.), Hepatology. A Textbook of Liver Disease, Vol. 1, 3rd ed., Saunders, Philadelphia, pp. 526-554.
74. Morris, C. M., Candy, J. M., Bloxham, C. A., and Edwardson, J. A. (1992a). Immunocytochemical localisation of transferrin in the human brain. Acta Anat. 143:14-18.
75. Morris, C. M., Candy, J. M., Bloxham, C. A., and Edwardson, J. A. (1992b). Distribution of transferrin receptors in relation to cytochrome oxidase activity in the human spinal cord, lower brainstem and cerebellum. J. Neural Sci. 111:158-172.
76. Morris, C. M., Kieth, 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.
77. New, H., Dziegielewska, K. M., and Saunders, N. R. (1983). Transferrin in fetal brain and cerebrospinal fluid. Int. J. Dev. Neurosci. 1:369-373.
78. Oh, T. H., Markelonis, G. J., Royal, G. M., and Brezman, B. S. (1986). Immunocytochemical distribution of transferrin and its receptor in the developing chicken nervous system. Dev. Brain Res. 30:207-220.
79. Ohe, Y. Ishikawa, K., Itoh, Z., and Tatemoto, K. (1996). Cultured leptomeningeal cells secrete cerebrospinal fluid proteins. J. Neurochem. 67:964-971.
80. Orita, T., Akimura, T., Nishizaki, T., Kamiryo, T., Ikeyama, Y., Aoki, H., and Ito, H. (1990). Transferrin receptors in injured brain. Acta. neuropathol. 79:686-688.
81. Ozawa, E. (1989). Transferrin as a muscle trophic factor. Rev. Physiol. Biochem. Pharmacol. 113:90-141.
82. Pardrige, W. M. (1988). Recent advances in blood brain barrier transport. Ann. Rev. Pharmacol. Toxicol. 28:25-39.
83. Pardridge, W. M., Eisenberg, J., and Yang, Y. (1987). Human blood-brain barrier transferrin receptor. Metabolism 36:892-895.
84. 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.
85. Petroff, O. A. C., Yu, R. K., and Ogino, T. (1986). High-resolution proton magnetic resonance analysis of human cerebrospinal fluid. J. Neurochem. 47:1270-1276.
86. Raivich, G., Graeber, M. B., Gehrmann, J., and Kreutzberg, G. W. (1991). Transferrin receptor expression and iron uptake in the injured and regenerating rat sciatic nerve. Eur. J. Neurosci. 3:919-927.
87. Raub, T., and Newton, C. R. (1991). Recycling kinetics and transcytosis of transferrin in primary cultures of bovine brain microvessel endothelial cells. J. Cell. Physiol. 149:141-151.
88. Reynolds, M. L., and Møllgård, K. (1985). The distribution of plasma proteins in the neocortex and early allocortex of the developing sheep brain. Anat. Embryol. 171:41-60.
89. Risau, W., Hallmann, R., and Albrecht, U. (1986). Differentiation-dependent expression of proteins in brain endothelium during development of the blood-brain barrier. Dev. Biol. 117:537-545.
90. Roberts, R., Sandra, A., Siek, G. C., Lucas, J. J., and Fine, R. E. (1992). Studies on the mechanism of iron transport across the blood-brain barrier. Ann. Neurol. 32:543-550.
91. Roberts, R., Fine, R. E., and Sandra, A. (1993). Receptor-mediated endocytosis of transferrin at the blood-brain barrier. J. Cell Sci. 104:521-532.
92. Roskams, A. J. I., and Connor, J. R. (1994). Iron, transferrin and ferritin in the rat brain during development and aging. J. Neurochem. 83:709-716.
93. Rothenberger, S., Food, M. R., Gabathuler, R., Kennard, M. L., Yamada, T., Yasuhara, O., McGeer, P. L., and Jefferies, W. A. (1996). Coincident expression and distribution of melanotransferrin and transferrin receptor in human brain capillary endothelial cells. Brain Res. 712:117-121.
94. Shin, S.-V., Friden, P., Moran, M., Olson, T., Kang, Y.-S., Pardridge, W. M., and Morrison, S. L. (1995). Transferrin-antibody fusion proteins are effective in brain targeting. Proc. Natl. Acad. Sci. USA 92:2820-2824.
95. 125I] transferrin through the rat blood-brain barrier. Brain Res. 683:164-171.
96. Skinner, M. K., and Griswold, M. D. (1980). Sertoli cells synthesize and secrete transferrin-like proteins. J. Biol. Chem. 255:9523-9525.
97. 13C]NMR spectroscopy of cultured neurons and astrocytes. Neurosci. Lett. 128:235-239.
98. 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.
99. Swaiman, K. F., and Machen, V. L. (1984). Iron uptake by mammalian cortical neurons. Ann. Neurol. 16:66-70.
100. Swaiman, K. F., and Machen, V. L. (1985). Iron uptake by glial cells. Neurochem. Res. 10:1635-1644.
101. Swaiman, K. F., and Machen, V. L. (1986a). Chloroquine reduces neuronal and glial iron uptake. J. Neurochem. 46:652-654.
102. Swaiman, K. F., and Machen, V. L. (1986b). Transferrin binding by mammalian cortical cells. Neurochem. Res. 11:1241-1248.
103. Szentistvanyi, I., Patlak, C. S., Ellis, A., and Cserr, H. (1984). Drainage of interstitial fluid from different regions of rat brain. Am. J. Physiol. 24:F835-F844.
104. 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.
105. Taylor, E. M., and Morgan, E. H. (1991). Role of transferrin in iron uptake by the brain: A comparative study. J. Comp. Physiol. B 161:521-524.
106. 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.
107. Theisen, M., Behringer, R. R., Cadd, G. G. Brinster, R. L., and McKnight, G. S. (1993). A C/EBP-binding site in the transferrin promoter is essential for expression in the liver but not in the brain of transgenic mice. Mol. Cell. Biol. 13:7666-7676.
108. Thomas, T., Schreiber, G., and Javorowski, A. (1989). Developmental patterns of gene expression of secreted proteins in brain and choroid plexus. Dev. Biol. 134:38-47.
109. Thorstensen, K. (1988). Hepatocytes and reticulocytes have different mechanisms for the uptake of iron from transferrin. J. Biol. Chem. 263:16837-16841.
110. Toran-Allerand, C. D. (1980). Coexistence of α-fetoprotein, albumin and transferrin immunoreactivity in neurones of the developing mouse brain. Nature 286:733-735.
111. Tu, G.-F., Achen, M. G., Alred, A. R., Southwell, B. R., and Schreiber, G. (1991). The distribution of cerebral expression of the transferrin gene is species specific. J. Biol. Chem. 266:6201-6208.
112. 59Fe uptake into the brain and cerebrospinal fluid and the influence thereon of antibodies against the transferrin receptor. J. Neurochem. 60:106-113.
113. Wagner, H.-J., Pilgrim, C.-H., and Brandl, J. (1974). Penetration and removal of horseradish peroxidase injected into the cerebrospinal fluid: Role of cerebral perivascular spaces, endothelium and microglia. Acta Neuropathol. 27:199-215.
114. Westergaard, N., Sonnewald, U., Unsgård, G., Peng, L., Hertz, L., and Schousbol, A. (1994). Uptake, release and metabolism of citrate in neurons and astrocytes in primary culture. J. Neurochem. 62:1727-1733.
115. Zahs, K., Bigornia, V., and Deschepper, C. F. (1993). Characterization of "plasma proteins" secreted by cultured rat macroglial cells. Glia 7:121-133.