Efficient transfer of receptor-associated protein (RAP) across the blood-brain barrier

Journal of Cell Science

Volumn 117, Issue 21, 2004, Pages 5071-5078

  Pan, Weihong ^a   Kastin, Abba J ^a   Zankel, Todd C ^b   van Kerkhof, Peter ^c   Terasaki, Tetsuya ^d   Bu, Guojun ^c  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b BIOMARIN PHARMACEUTICAL INC   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

Bloof brain barrier; Drug delivery; LRP; Megalin; Receptor associated protein; Receptor mediated transport

Indexed keywords

IODINE 125; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MEGALIN; RAP PROTEIN; TRANSFERRIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN CAPILLARY; BRAIN HOMOGENATE; BRAIN PERFUSION; BRAIN TISSUE; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CELL STRAIN; CELL TRANSPORT; CONTROLLED STUDY; DRUG TRANSPORT; EPITHELIUM CELL; GENETIC TRANSFECTION; IN VITRO STUDY; MALE; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE; DOGS; ENDOPLASMIC RETICULUM; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; LIGANDS; LINEAR MODELS; MICE; NEOPLASM PROTEINS; PERFUSION; PROTEIN BINDING; RECEPTORS, LDL; TIME FACTORS; TRANSFECTION; TRANSFERRIN;

ANIMALIA;

EID: 8744266243     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01381     Document Type: Article

References (44)

1. Banks, W. A., Robinson, S. M., Verma, S. and Morley, J. E. (2003). Efflux of human and mouse amyloid β proteins 1-40 and 1-42 from brain: impairment in a mouse model of Alzheimer's disease. Neurosci. 121, 487-492.
2. Berryman, D. E. and Bensadoun, A. (1995). Heparan sulfate proteoglycans are primarily responsible for the maintenance of enzyme activity, binding, and degradation of lipoprotein lipase in Chinese hamster ovary cells. J. Biol. Chem. 270, 24524-24531.
3. Blasberg, R. G., Fenstermacher, J. D. and Patlak, C. S. (1983). Transport of α-aminoisobutyric acid across brain capillary and cellular membranes. J. Cereb. Blood Flow Metab. 3, 8-32.
4. Broadwell, R. D., Baker-Cairns, B. J., Friden, P. M., Oliver, C. and Villegas, J. C. (1996). Transcytosis of protein through the mammalian cerebral epithelium and endothelium. III. Receptor-mediated transcytosis through the blood-brain barrier of blood-borne transferrin and antibody against the transferrin receptor. Exp. Neurol. 142 47-65.
5. Bu, G., Maksymovitch, E. A., Geuze, H. and Schwartz, A. L. (1994). Subcellular localization and endocytic function of low density lipoprotein receptor-related protein in human glioblastoma cells. J. Biol. Chem. 269, 29874-29882.
6. Bu, G., Geuze, H. J., Strous, G. J. and Schwartz, A. L. (1995). 39 kDa receptor-associated protein is an ER-resident protein and molecular chaperon for LDL receptor-related protein. EMBO J. 14 2269-2280.
7. Chun, J. J., Wang, L., Pasinetti, G. M., Finch, C. E. and Zlokovic, B. V. (1999). Glycoprotein 330/megalin (LRP-2) has low prevalence as mRNA and protein in brain microvessel and choroid plexus. Exp. Neurol. 157, 194-201.
8. Czekay, R. P., Orlando, R. A., Woodward, L., Lundstrom, M. and Farquhar, M. G. (1997). Endocytic trafficking of megalin/RAP complexes: dissociation of the complexes in late endosomes. Mol. Biol. Cell 8, 517-532.
9. Demeule, M., Poirier, J., Jodoin, J., Bertrand, Y., Desrosiers, R. R., Dagenais, C., Nguyen, T., Lanthier, J., Gabathuler, R., Kennard, M. et al. (2002). High transcytosis of melanotransferrin (p97) across the blood-brain barrier. J. Neurochem. 83, 924-933.
10. Irvine, J. D., Takahashi, L., Lockhart, K., Cheong, J., Tolan, J. W., Selick, H. E. and Grove, J. R. (1999). MDCK (Madin-Darby canine kidney) cells: a tool for membrane permeability screening. J. Pharm. Sci. 88, 28-33.
11. Kastin, A. J., Akerstrom, V. and Pan, W. (2001). Validity of multiple-time regression analysis in measurement of tritiated and iodinated leptin crossing the blood-brain barrier: meaningful controls. Peptides 22, 2127-2136.
12. Kounnas, M. Z., Haudenschild, C. C., Strickland, D. K. and Argraves, W. S. (1994). Immunological localization of glycoprotein 330, low density lipoprotein receptor related protein and 39 kDa receptor associated protein in embryonic mouse tissues. In Vivo 8, 343-351.
13. Li, Y., Marzolo, M. P., van Kerkhof, P., Strous, G. J. and Bu, G. (2000). The YXXL motif, but not the two NPXY motifs, serves as the dominant endocytosis signal for low density lipoprotein receptor-related protein. J. Biol. Chem. 275, 17187-17194.
14. Li, Y., Cam, J. and Bu, G. (2001a). Low-density lipoprotein receptor family. Endocyrosis and signal transduction. Mol. Neurobiol. 23, 53-67.
15. Li, Y., Lu, W., Marzolo, M. P. and Bu, G. (2001b). Differential functions of members of the low density lipoprotein receptor family suggested by their distinct endocytosis rates. J. Biol. Chem. 276, 18000-18006.
16. Marinò, M., Chiovato, L., Lisi, S., Pinchera, A. and McCluskey, R. T. (2001). Binding of the low density lipoprotein receptor-associated protein (RAP) to thyroglobulin (Tg): putative role of RAP in the Tg secretory pathway. Mol. Endocrinol. 15, 1829-1837.
17. Marinò, M., Zheng, G. and McCluskey, R. T. (2003). Megalin (gp330) is an endocytic receptor for thyroglobulin on cultured Fisher rat thyroid cells. J. Biol. Chem. 274, 12898-12904.
18. Marzolo, M. P., Yuseff, M. I., Retamal, C., Donoso, M., Ezquer, F., Farfán, P., Li, Y. and Bu, G. (2003). Differential distribution of low-density lipoprotein-receptor-related protein (LRP) and megalin in polarized epithelial cells is determined by their cytoplasmic domains. Traffic 4, 273-288.
19. Melman, L., Can, Z.-F., Rennke, S., Marzolo, M. P., Wardell, M. R. and Bu, G. (2001). High affinity binding of receptor-associated protein to heparin and low density lipoprotein receptor-related protein requires similar basic amino acid sequence motifs. J. Biol. Chem. 276, 29338-29346.
20. Moos, T. and Morgan, E. H. (2001). Restricted transport of anti-transferrin receptor antibody (OX26) through the blood-brain barrier in the rat. J. Neurochem. 79, 119-129.
21. Morris, C. M., Keith, A. B., Edwardson, J. A. and Pullen, R. G. (1992). Uptake and distribution of iron and transferrin in the adult rat brain. J. Neurochem. 59, 300-306.
22. Orlando, R. A. and Farquhar, M. G. (1993). Identification of a cell line that expresses a cell surface and a soluble form of the gp330/receptor-associated protein (RAP) Heymann nephritis antigenic complex. Proc. Natl. Acad. Sci. USA 90, 4082-4086.
23. Orlando, R. A. and Farquhar, M. G. (1994). Functional domains of the receptor-associated protein (RAP). Proc. Natl. Acad. Sci. USA 91, 3161-3165.
24. Pan, W. and Kastin, A. J. (2000). Interactions of IGF-1 with the blood-brain barrier in vivo and in situ. Neuroendocrinol. 72, 171-178.
25. Pan, W. and Kastin, A. J. (2003). Transport of cytokines and neurotrophins across the BBB and their regulation after spinal cord injury, In Blood-Spinal Cord and Brain Barriers in Health and Disease (ed. H. Shanker and J. Westman), pp. 395-407. San Diego, CA: Academic Press.
26. Pan, W., Banks, W. A. and Kastin, A. J. (1997). Permeability of the blood-brain and blood-spinal cord barriers to interferons. J. Neuroimmunol. 76, 105-111.
27. Pan, W., Banks, W. A. and Kastin, A. J. (1998). Permeability of the blood-brain barrier to neurotrophins. Brain Res. 788, 87-94.
28. Pan, W., Vallance, K. and Kastin, A. J. (1999). TGFα and the blood-brain barrier: accumulation in cerebral vasculature. Exp. Neurol. 160, 454-459.
29. Pan, W., Kastin, A. J. and Brennan, J. M. (2000). Saturable entry of leukemia inhibitory factor from blood to the central nervous system. J. Neuroimmunol. 106, 172-180.
30. Patlak, C. S., Blasberg, R. G. and Fenstermacher, J. D. (1983). Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J. Cereb. Blood Flow Metab. 3, 1-7.
31. Savonen, R., Obermoeller, L. M., Trausch-Azar, J. S., Schwartz, A. L. and Bu, G. (1999). The carboxyl-terminal domain of receptor-associated protein facilitates proper folding and trafficking of the very low density lipoprotein receptor by interaction with the three amino-terminal ligand-binding repeats of the receptor. J. Biol. Chem. 274, 25877-25882.
32. Shayo, M., McLay, R. N., Kastin, A. J. and Banks, W. A. (1997). The putative blood-brain barrier transporter for the β -amyloid binding protein apolipoprotein J is saturated at physiological concentrations. Life Sci. 60, PL115-PL118.
33. 1-40 peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J. Clin. Invest. 106, 1489-1499.
34. 125I]transferrin through the rat blood-brain barrier. Brain Res. 683, 164-171.
35. Ueda, F., Raja, K. B., Simpson, R. J., Trowbridge, I. S. and Bradbury, M. W. (1993). Rate of 59Fe uptake into brain and cerebrospinal fluid and the influence thereon of antibodies against the transferrin receptor. J. Neurochem. 60, 106-113.
36. Veinbergs, I., van Uden, E., Mallory, M., Alford, M., McGiffert, C., DeTeresa, R., Orlando, R. and Masliah, E. (2001). Role of apolipoprotein E receptors in regulating the differential in vivo neurotrophic effects of apolipoprotein E. Exp. Neurol. 170 15-26.
37. Vilhardt, F., Nielsen, M., Sandvig, K. and van Beurs, B. (1999). Urokinase-type plasminogen activator receptor is internalized by different mechanisms in polarized and nonpolarized Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 10, 179-195.
38. Warshawsky, I., Bu, G. and Schwartz, A. L. (1993). 39-kD protein inhibits tissue-type plasminogen activator clearance in vivo. J. Clin. Invest. 92, 937-944.
39. Wilnow, T. E., Hilpert, J., Armstrong, S. A., Rohlmann, A., Hammer, R. E., Burns, D. K. and Herz, J. (1996). Defective forebrain development in mice lacking gp330/megalin. Proc. Natl. Acad. Sci. USA 93, 8460-8464.
40. Yepes, M., Sandkvist, M., Moore, E. G., Bugge, T. H., Strickland, D. K. and Lawrence, D. A. (2003). Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest. 112, 1533-1540.
41. Zhang, W., Riedel, C., Carrasco, N. and Arvan, P. (2002). Polarized trafficking of thyrocyte proteins in MDCK cells. Mol. Cell. Endocrinol. 188, 27-36.
42. Zheng, G., Bachinsky, D. R., Stamenkovic, I., Strickland, D. K., Brown, D., Andres, G. and McCluskey, R. T. (1994). Organ distribution in rats of two members of the low-density lipoprotein receptor gene family, gp330 and LRP/alpha 2MR, and the receptor-associated protein (RAP). J. Histochem. Cytochem. 42 531-542.
43. Zlokovic, B. V., Skundric, D. S., Segal, M. B., Lipovac, M. N., Mackic, J. B. and Davson, H. (1990). A saturable mechanism for transport of immunoglobulin G across the blood-brain barrier of the guinea pig. Exp. Neurol. 107, 263-270.
44. Zlokovic, B. V., Martel, C. L., Matsubara, E., McComb, J. G., Zheng, G., McCluskey, R. T., Frangione, B. and Ghiso, J. (1996). Glycoprotein 330 /megalin: probable role in receptor-mediated transport of apolipoprotein J alone and in a complex with Alzheimer disease amyloid β at the blood-brain and blood-cerebrospinal fluid barriers. Proc. Natl. Acad. Sci. USA 93, 4229-4234.