Megalin and cubilin: Multifunctional endocytic receptors

Nature Reviews Molecular Cell Biology

Volumn 3, Issue 4, 2002, Pages 258-268

  Christensen, Erik Ilsã ^a   Birn, Henrik ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CUBILIN; MEGALIN;

CELL FUNCTION; CELL MEMBRANE TRANSPORT; ENDOCYTOSIS; HISTORY; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW;

EID: 84984766757     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm778     Document Type: Article

References (132)

1. Saito, A., Pietromonaco, S., Loo, A. K. & Farquhar, M. G. Complete cloning and sequencing of rat gp330/‘megalin’, a distinctive member of the low density lipoprotein receptor gene family. Proc. Nat Acad. Sci. USA 91, 9725-9729 (1994).
2. 2+-binding receptor with potential intracellular signaling properties. Eur. J. Biochem. 239, 132-137 (1996).
3. Korenberg, J. R. et al. Chromosomal localization of human genes for the LDL receptor family member glycoprotein 330 (LRP2) and its associated protein RAP (LRPAP1). Genomics 22, 88-93 (1994).
4. Raychowdhury, R., Niles, J. L., McCluskey, R. T. & Smith, J. A. Autoimmune target in Heymann nephritis is a glycoprotein with homology to the LDL receptor. Science 244, 1163-1165 (1989).
5. Willnow, T E. The low-density lipoprotein receptor gene family: multiple roles in lipid metabolism. J. Mol. Med. 77, 306-315 (1999).
6. Hussain, M. M. Structural, biochemical and signaling properties of the low-density lipoprotein receptor gene family. Front Biosci. 6, D417-D428 (2001).
7. Yochem, J. & Greenwald, I. A gene for a low density lipoprotein receptor-related protein in the nematode Caenofoabditis elegans. Proc. Natl Acad. Sci. USA 90, 4572-4576 (1993).
8. Davis, C. G. et al. Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region. Nature 326, 760-765 (1987).
9. Chen, W. J., Goldstein, J. L. & Brown, M. S. NPXY a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265, 3116-3123 (1990).
10. Willnow, T. E., Nykjær, A. & Herz, J. Lipoprotein receptors: new roles for ancient proteins. Nature Cell Biol. 1, E157-E162 (1999).
11. Orlando, R. A. et al. Identification of the second cluster of ligand-binding repeats in megalin as a site for receptor- ligand interactions. Proc. Natl Acad. Sci. USA 94, 2368-2373 (1997).
12. 12 homeostasis. Proc. Natl Acad. Sci. USA 93, 8612-8617 (1996).
13. Christensen, E. I., Gliemann, J. & Moestrup, S. K. Renal tubule gp330 is a calcium binding receptor for endocytic uptake of protein. J. Histochem. Cytochem. 40, 1481-1490 (1992).
14. Seetharam, B., Christensen, E. I., Moestrup, S. K., Hammond, T. G. & Verroust, P J. Identification of rat yolk sac target protein of teratogenic antibodies, gp280, as intrinsic factor-cobalamin receptor. J. Clin. Invest. 99, 2317-2322 (1997).
15. Moestrup, S. K. et al. The intrinsic factor-vitamin B12 receptor and target of teratogenic antibodies is a megalin- binding peripheral membrane protein with homology to developmental proteins. J. Biol. Chem. 273, 5235-5242 (1998).
16. Kozyraki, R. et al. The human intrinsic factor-vitamin B12 receptor, cubilin: molecular characterization and chromosomal mapping of the gene to 10p within the autosomal recessive megaloblastic anemia (MGA1) region. Blood 91, 3593-3600 (1998).
17. Xu, D., Kozyraki, R., Newman, T. C. & Fyfe, J. C. Genetic evidence of an accessory activity required specifically for cubilin brush-border expression and intrinsic factor-cobalamin absorption. Blood 94, 3604-3606 (1999).
18. Bork, P. & Beckmann, G. The CUB domain. A widespread module in developmentally regulated proteins. J. Mol. Biol. 231, 539-545 (1993).
19. Kristiansen, M. et al. Molecular dissection of the intrinsic factor-vitamin B12 receptor, cubilin, discloses regions important for membrane association and ligand binding. J. Biol. Chem. 274, 20540-20544 (1999).
20. Mishra, V K. & Palgunachari, M. N. Interaction of model class A1, class A2, and class Y amphipathic helical peptides with membranes. Biochemistry 35, 11210-11220 (1996).
21. Mercier, C., Cesbron-Delauw, M. F. & Sibley, L. D. The amphipathic a-helices of the toxoplasma protein GRA2 mediate post-secretory membrane association. J. Cell Sci. 111, 2171-2180 (1998).
22. Li, Y., Smith, T, Grabski, S. & DeWitt, D. L. The membrane association sequences of the prostaglandin endoperoxide synthases-1 and -2 isozymes. J. Biol. Chem. 273, 29830-29837 (1998).
23. Chen, C., Seow, K. T., Guo, K., Yaw, L. P & Lin, S. C. The membrane association domain of RGS16 contains unique amphipathic features that are conserved in RGS4 and RGS5. J. Biol. Chem. 274, 19799-19806 (1999).
24. Bernstein, L. S., Grillo, A. A., Loranger, S. S. & Linder, M. E. RGS4 binds to membranes through an amphipathic a-helix. J. Biol. Chem. 275, 1852-18526 (2000).
25. Ramanujam, K. S., Seetharam, S., Dahms, N. M. & Seetharam, B. Effect of processing inhibitors on cobalamin (vitamin B12) transcytosis in polarized opossum kidney cells. Arch. Biochem. Biophys. 315, 8-15 (1994).
26. Moestrup, S. K. & Verroust, P. J. Megalin- and cubilin- mediated endocytosis of protein-bound vitamins, lipids, and hormones in polarized epithelia. Annu. Rev. Nutr. 21, 407- 428 (2001).
27. Lindblom, A. et al. The intrinsic factor-vitamin B12 receptor, cubilin, is assembled into trimers via a coiled-coil a-helix. J. Biol. Chem. 274, 6374-6380 (1999).
28. Yammani, R. R., Seetharam, S. & Seetharam, B. Identification and characterization of two distinct ligand binding regions of cubilin. J. Biol. Chem. 276, 44777-44784 (2001).
29. Romero, A. et al. The crystal structures of two spermadhesins reveal the CUB domain fold. Nature Struct. Biol. 4, 783-788 (1997).
30. Varela, P F. et al. The 2.4 A resolution crystal structure of boar seminal plasma PSP-I/PSP-II: a zona pellucida-binding glycoprotein heterodimer of the spermadhesin family built by a CUB domain architecture. J. Mol. Biol. 274, 635-649 (1997).
31. Yammani, R. R., Seetharam, S. & Seetharam, B. Cubilin and megalin expression and their interaction in the rat intestine: effect of thyroidectomy. Am. J. Physiol. Endocrinol. Metab. 281, E900-E907 (2001).
32. 12 and binds receptor-associated protein. J. Biol. Chem. 272, 26497-26504 (1997).
33. Levine, J. S., Allen, R. H., Alpers, D. H. & Seetharam, B. Immunocytochemical localization of the intrinsic factor-cobalamin receptor in dog-ileum: distribution of intracellular receptor during cell maturation. J. Cell Biol. 98. 1111-1118 (1984).
34. Kerjaschki, D. & Farquhar, M. G. The pathogenic antigen of Heymann nephritis is a membrane glycoprotein of the renal proximal tubule brush border. Proc. Natl Acad. Sci. USA 79, 5557-5581 (1982).
35. Sahali, D. et al. Characterization of a 280-kD protein restricted to the coated pits of the renal brush border and the epithelial cells of the yolk sac. Teratogenic effect of the specific monoclonal antibodies. J. Eye. Med. 167, 213-218 (1988).
36. Seetharam, B., Levine, J. S., Ramasamy, M. & Alpers, D. H. Purification, properties, and immunochemical localization of a receptor for intrinsic factor-cobalamin complex in the rat kidney. J. Biol. Chem. 263, 4443-4449 (1988).
37. Chatelet, F., Brianti, E., Ronco, P., Roland, J. & Verroust, P Ultrastructural localization by monoclonal antibodies of brush border antigens expressed by glomeruli. I. Renal distribution. Am. J. Pathol. 122, 500-511 (1986).
38. Doxsey, S., Kerjaschki, D. & Farquhar, M. G. A large membrane glycoprotein (gp330) is a resident of coated pits of serveral absorptive epithelia. J. Cell Biol. Abstr. 98, 178a (1984).
39. Chatelet, F., Brianti, E., Ronco, P., Roland, J. & Verroust, P Ultrastructural localization by monoclonal antibodies of brush border antigens expressed by glomeruli. II. Extrarenal distribution. Am. J. Pathol. 122, 512-519 (1986).
40. 2+ in cytotrophoblast cells of human placenta. J. Biol. Chem. 265, 8275-8279 (1990).
41. Sahali, D. et al. Coexpression in humans by kidney and fetal envelopes of a 280 kDa-coated pit-restricted protein. Similarity with the murine target of teratogenic antibodies. Am. J. Pathol. 140, 33-44 (1992).
42. Kounnas, M. Z., Haudenschild, C. C., Strickland, D. K. & Argraves, W. S. 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 (1994).
43. Zheng, G. et al. 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 (1994).
44. Juhlin, C. et al. Monoclonal antibodies with exclusive reactivity against parathyroid cells and tubule cells of the kidney. Proc. Natl Acad. Sci. USA 84, 2990-2994 (1987).
45. 2+- sensor/receptor function in rat placenta and uterus. J. Reprod. Immunol. 16, 199-205 (1989).
46. Mizuta, K et al. Ultrastructural localization of megalin in the rat cochlear duct. Hear Res. 129, 83-91 (1999).
47. Sahali, D. et al. Comparative immunochemistry and ontogeny of two closely related coated pit proteins. The 280-kd target of teratogenic antibodies and the 330-kd target of nephritogenic antibodies. Am. J. Pathol. 142, 1654-1667 (1993).
48. Kerjaschki, D., Noronha Blob, L., Sacktor B. & Farquhar, M. G. Microdomains of distinctive glycoprotein composition in the kidney proximal tubule brush border. J. Cell Biol. 98, 1505-1513 (1984).
49. Christensen, E. I., Birn, H., Verroust, P. & Moestrup, S. K. Membrane receptors for endocytosis in the renal proximal tubule. Int. Rev. Cytol. 180, 237-284 (1998).
50. Bu, G., Geuze, H. J., Strous, G. J. & Schwartz, A. L. 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J. 14, 2269-2280 (1995).
51. Bu, G., Rennke, S. & Geuze, H. J. ERD2 proteins mediate ER retention of the HNEL signal of LRP's receptor- associated protein (RAP). J. Cel Sci. 110, 65-73 (1997).
52. Willnow, T. E., Armstrong, S. A., Hammer, R. E. & Herz, J. Functional expression of low density lipoprotein receptor- related protein is controlled by receptor-associated protein in vivo. Proc. Natl Acad. Sci. USA 92, 4537-4541 (1995).
53. Willnow, T. E. et al. RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytic receptors. EMBO J. 15. 2632-2639 (1996).
54. Willnow, T. E. Receptor-associated protein (RAP): a specialized chaperone for endocytic receptors. Biol. Chem. 379, 1025-1031 (1998).
55. Bu, G. & Rennke, S. Receptor-associated protein is a folding chaperone for low density lipoprotein receptor-related protein. J. Biol. Chem. 271, 22218-22224 (1996).
56. Birn, H., Vorum, H., Verroust, P. J., Moestrup, S. K. & Christensen, E. I. Receptor-associated protein is important for normal processing of megalin in kidney proximal tubules. J.Am. Soc. Nephrol. 11, 191-202 (2000).
57. Takeda, T, Orlando, R. A. & Farquhar, M. G. Identification of apical sorting determinants in the cytoplasmic tail of megalin. J.Am. Soc. Nephrol. 12, Abstr. 60A-61A (2001).
58. Bravo, D. A., Gleason, J. B., Sanchez, R. I., Roth, R. A. & Fuller, R. S. Accurate and efficient cleavage of the human insulin proreceptor by the human proprotein-processing protease furin. Characterization and kinetic parameters using the purified, secreted soluble protease expressed by a recombinant baculovirus. J. Biol. Chem. 269, 25830-25837
59. Willnow, T. E., Moehring, J. M., Inocencio, N. M., Moehring, T. J. & Herz, J. The low-density-lipoprotein receptor-related protein (LRP) is processed by furin in vivo and in vitro. Biochem. J. 313, 71-76 (1996).
60. Baricault, L., Galceran, M., Ronco, P M., Trugnan, G. & Verroust, P Unusual processing of gp280, a protein associated with the intermicrovillar areas of yolk sac epithelial cells: plasma membrane delivery of immature protein. Biochem. Biophys. Res. Commun. 212, 353-359
61. Xu, D. & Fyfe, J. C. Cubilin expression and posttranslational modification in the canine gastrointestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G748-G756 (2000).
62. Fyfe, J. C., Ramanujam, K. S., Ramaswamy, K., Patterson, D. F. & Seetharam, B. Defective brush-border expression of intrinsic factor-cobalamin receptor in canine inherited intestinal cobalamin malabsorption. J. Biol. Chem. 266, 4489-4494 (1991).
63. Fyfe, J. C. et al. Inherited selective intestinal cobalamin malabsorption and cobalamin deficiency in dogs. Pediatr. Res. 29, 24-31 (1991).
64. Zhao, J., Oleinikov, A. V, Oleinikova, I. & Makker, S. P Functional characterization of rat gp600/megalin promoter: combination of proximal Sp1 site and JCV repeat is important in rat gp600/megalin promoter activation. Gene 265, 123-131 (2001).
65. Stefansson, S., Chappell, D. A., Argraves, K. M., Strickland, D. K. & Argraves, W. S. Glycoprotein 330/low density lipoprotein receptor-related protein-2 mediates endocytosis of low density lipoproteins via interaction with apolipoprotein B100. J. Biol. Chem. 270, 19417-19421 (1995).
66. Liu, W. et al. Regulation of gp330/megalin expression by vitamins A and D. Eur. J. Clin. invest. 28, 100-107 (1998).
67. Hammad, S. M. et al. Cubilin, the endocytic receptor for intrinsic factor-vitamin B(12) complex, mediates high-density lipoprotein holoparticle endocytosis. Proc. Natl Acad. Sci. USA 96, 10158-10163 (1999).
68. Makker, S. P., Widstrom, R. & Huang, J. Transcription and translation of gp600 and receptor-associated protein (RAP) in active Heymann nephritis. Am. J. Pathol. 146, 1481-1487 (1995).
69. LaFerla, F M., Troncoso, J. C., Strickland, D. K., Kawas, C. H. & Jay, G. Neuronal cell death in Alzheimer's disease correlates with apoE uptake and intracellular Ap stabilization. J. Clin. invest. 100, 310-320 (1997).
70. Thakker, R. V. The role of renal chloride channel mutations in kidney stone disease and nephrocalcinosis. Curr. Opin. Nephrol. Hypertens. 7, 385-388 (1998).
71. Piwon, N., Gunther, W., Schwake, M., Bosl, M. R. & Jentsch, T. J. CIC-5 Cl channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408, 369-373 (2000).
72. Juhlin, C. et al. Hyperparathyroidism is associated with reduced expression of a parathyroid calcium receptor mechanism defined by monoclonal antiparathyroid antibodies. Endocrinology 122, 2999-3001 (1988).
73. Willnow, T. E. et al. Defective forebrain development in mice lacking gp330/megalin. Proc. Natl Acad. Sci. USA 93, 8460-8464 (1996).
74. Leheste, J. R. et al. Megalin knockout mice as an animal model of low molecular weight proteinuria. Am. J. Pathol. 155, 1361-1370 (1999).
75. Aminoff, M. et al. Mutations in CUBN, encoding the intrinsic factor-vitamin B12 receptor, cubilin, cause hereditary megaloblastic anaemia 1. Nature Genet. 21, 309-313 (1999).
76. Hammad, S. M., Barth, J. L., Knaak, C. & Argraves, W S. Megalin acts in concert with cubilin to mediate endocytosis of high density lipoproteins. J. Biol. Chem. 275, 12003-12008 (2000).
77. Nykjær, A. et al. Purified a2-macroglobulin receptor/LDL receptor-related protein binds uroklnase-plasmlnogen activator inhibitor type-1 complex. Evidence that the a2- macroglobulin receptor mediates cellular degradation of urokinase receptor-bound complexes. J. Biol. Chem. 267, 14543-14546 (1992).
78. + exchanger isoform NHE3 in the proximal tubule. J. Biol. Chem. 274, 17518-17524 (1999).
79. Christensen, E. I. et al. Evidence for an essential role of megalin in transepithelial transport of retinol. J. Am. Soc. Nephrol. 10, 68-695 (1999).
80. Birn, H. et al. Megalin is essential for renal proximal tubule reabsorption and accumulation of transcobalamin-B(12). Am. J. Physiol. Renal Physiol. 282, F408-F416 (2002).
81. Nykjær, A. et al. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96, 507-515 (1999).
82. Nykjær, A. et al. Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25-(OH) vitamin D3 Proc. Natl Acad. Sci. USA 98, 13895-13900 (2001).
83. Mendel, C. M. The free hormone hypothesis: a physiologically based mathematical model. Endocrinol. Rev. 10, 232-274 (1989).
84. Kozyraki, R. et al. Megalin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc. Natl Acad. Sci. USA 98, 12491-12496 (2001).
85. 125I-labelled rat transferrin by early organogenesis rat conceptuses in vitro. Placenta 18, 553-562 (1997).
86. Gburek, J. et al. Megalin and cubilin are endocytic receptors involved in renal clearance of hemoglobin. J. Am. Soc. Nephrol. 13, 423-430 (2002).
87. Gunshin, H. et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488 (1997).
88. Young, S. P. Inhibition of endosome fusion in primary hepatocytes prevents asialoglycoprotein degradation but not uptake of transferrin iron demonstrating that intracellular iron release occurs from early endosomes. FEBS Lett. 466. 135-138 (2000).
89. Abboud, S. & Haile, D. J. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275, 19906-19912 (2000).
90. Ruggenenti, P. & Remuzzi, G. The role of protein traffic in the progression of renal diseases. Annu. Rev. Med. 51, 315-327 (2000).
91. Kozyraki, R. et al. The intrinsic factor-vitamin B12 receptor, cubilin, is a high-affinity apolipoprotein A-I receptor facilitating endocytosis of high-density lipoprotein. Nature Med. 5, 656-661 (1999).
92. Glass, C., Pittman, R. C., Civen, M. & Steinberg, D. Uptake of high-density lipoprotein-associated apoprotein A-I and cholesterol esters by 16 tissues of the rat in vivo and by adrenal cells and hepatocytes in vitro. J. Biol. Chem. 260, 744-750 (1985).
93. Glass, C. K., Pittman, R. C., Keller, G. A. & Steinberg, D. Tissue sites of degradation of apoprotein A-I in the rat. J. Biol. Chem. 258, 7161-7167 (1983).
94. Zheng, G., Marino, M., Zhao, J. & McCluskey, R. T. Megalin (gp330): a putative endocytic receptor for thyroglobulin (Tg). frdocrinology 139, 1462-1465 (1998).
95. Marino, M. et al. Role of megalin (gp330) in transcytosis of thyroglobulin by thyroid cells. A novel function in the control of thyroid hormone release. J. Biol. Chem. 275, 7125-7137 (2000).
96. Marino, M. & McCluskey, R. T. Role of thyroglobulin endocytic pathways in the control of thyroid hormone release. Am. J. Physiol. Cell Physiol. 279, C1295-C1306 (2000).
97. Marino, M. et al. Circulating thyroglobulin transcytosed by thyroid cells in complex with secretory components of its endocytic receptor megalin. J. Clin. Endocrinol. Metab. 85. 3458-3467 (2000).
98. Marino, M. et al. Serum antibodies against megalin (GP330) in patients with autoimmune thyroiditis. J. Clin. Endocrinol. Metab. 84, 2468-2474 (1999).
99. Hilpert, J. et al. Megalin antagonizes activation of the parathyroid hormone receptor. J. Biol. Chem. 274, 5620-5625 (1999).
100. Lundgren, S. et al. A protein involved in calcium sensing of the human parathyroid and placental cytotrophoblast cells belongs to the LDL-receptor protein superfamily. Exp. Cell Res. 212, 344-350 (1994).
101. Moestrup, S. K. et al. Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J. Clin. invest. 96, 1404-1413 (1995).
102. Schmitz, C. et al. Megalin deficiency offers protection from renal aminoglycoside accumulation. J. Biol. Chem. 277, 618-622 (2002).
103. Herz, J., Gotthardt, M. & Willnow, T. E. Cellular signalling by lipoprotein receptors. Curr. Opin. Lipidol. 11, 161-166 (2000).
104. Oleinikov, A. V, Zhao, J. & Makker, S. P. Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem. J. 347, 613-621 (2000).
105. Trommsdorff, M., Borg, J. P., Margolis, B. & Herz, J. Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J. Biol. Chem. 273, 33556-33560 (1998).
106. Trommsdorff, M. et al. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689-701 (1999).
107. Kristiansen, M. et al. Cubilin P1297L mutation associated with hereditary megaloblastic anemia 1 causes impaired recognition of intrinsic factor-vitamin B(12) by cubilin. Blood 96, 405-409 (2000).
108. Bu, G. & Marzolo, M. P. Role of rap in the biogenesis of lipoprotein receptors. Trends Cardiovasc. Med. 10. 148-155 (2000).
109. Idriss, J. M. & Jonas, A. J. Vitamin B12 transport by rat liver lysosomal membrane vesicles. J. Biol. Chem. 266, 9438-9441 (1991).
110. Vassiliadis, A., Rosenblatt, D. S., Cooper, B. A. & Bergeron, J. J. Lysosomal cobalamin accumulation in fibroblasts from a patient with an inborn error of cobalamin metabolism (cblF complementation group): visualization by electron microscope radioautography. Eye. Cell Res. 195, 295-302 (1991).
111. Young, S. P. Inhibition of endosome fusion in primary hepatocytes prevents asialoglycoprotein degradation but not uptake of transferrin iron demonstrating that intracellular iron release occurs from early endosomes. FEBS Lett. 466, 135-138 (2000).
112. Marino, M., Andrews, D., Brown, D. & McCluskey, R. T. Transcytosis of retinol-binding protein across renal proximal tubule cells after megalin (gp 330)-mediated endocytosis. J.Am. Soc. Nephrol. 12, 637-648 (2001).
113. Cui, S., Verroust, P. J., Moestrup, S. K. & Christensen, E. I. Megalin/gp330 mediates uptake of albumin in renal proximal tubule. Am. J. Physiol. 271, F900-F907 (1996).
114. Birn, H. et al. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J. Clin. invest. 105, 1353-1361 (2000).
115. Willnow, T. E., Goldstein, J. L., Orth, K., Brown, M. S. & Herz, J. Low density lipoprotein receptor-related protein and gp330 bind similar ligands, including plasminogen activator- inhibitor complexes and lactoferrin, an inhibitor of chylomicron remnant clearance. J. Biol. Chem. 267, 26172-26180 (1992).
116. Sousa, M. M. et al. Evidence for the role of megalin in renal uptake of transthyretin. J. Biol. Chem. 275, 38176-38181 (2000).
117. Kounnas, M. Z. et al. Identification of glycoprotein 330 as an endocytic receptor for apolipoprotein J/clusterin. J. Biol. Chem. 270, 13070-13075 (1995).
118. Moestrup, S. K et al. ß2-glycoprotein-I (apolipoprotein H) and ß2-glycoprotein-I-phospholipid complex harbor a recognition site for the endocytic receptor megalin. J. Clin. invest. 102, 902-909 (1998).
119. Orlando, R. A. et al. Megalin is an endocytic receptor for insulin. J. Am. Soc. Nephrol. 9, 1759-1766 (1998).
120. Chan, W. L. et al. Trichosanthin interacts with and enters cells via LDL receptor family members. Biochem. Biophys. Res. Commun. 270, 453-457 (2000).
121. Stefansson, S. et al. gp330 on type II pneumocytes mediates endocytosis leading to degradation of prourokinase, plasminogen activator inhibitor-1 and urokinaseplasminogen activator inhibitor-1 complex. J. Cell Sci. 108, 2361-2368 (1995).
122. Moestrup, S. K. et al. Epithelial glycoprotein-330 mediates endocytosis of plasminogen activator-plasminogen activator inhibitor type-1 complexes. J. Biol. Chem. 268, 16564-16570 (1993).
123. Kounnas, M. Z., Chappell, D. A., Strickland, D. K. & Argraves, W. S. Glycoprotein 330, a member of the low density lipoprotein receptor family, binds lipoprotein lipase in vitro. J. Biol. Chem. 268, 14176-14181 (1993).
124. Kanalas, J. J. & Makker, S. P. Identification of the rat Heymann nephritis autoantigen (GP330) as a receptor site for plasminogen. J. Biol. Chem. 266, 10825-10829 (1991).
125. Birn, H. et al. Monoclonal Gammapathies and the Kidney (eds Aucouturier, P., Hermine, P., Ronco, P. & Touchard, G.) (Klüwer, The Netherlands, 2002).
126. Batuman, V. et al. Myeloma light chains are ligands for cubilin (gp280). Am. J. Physiol. 275, F24-F254 (1998).
127. Burmeister, R. et al. A two-receptor pathway for catabolism of Clara cell secretory protein in the kidney. J. Biol. Chem. 276, 13295-13301 (2001).
128. Orlando, R. A., Kerjaschki, D., Kurihara, H., Biemesderfer, D. & Farquhar, M. G. gp330 associates with a 44-kDa protein in the rat kidney to form the Heymann nephritis antigenic complex. Proc. Natl Acad. Sci. USA 89, 6698-6702 (1992).
129. Kounnas, M. Z., Argraves, W. S. & Strickland, D. K. The 39- kDa receptor-associated protein interacts with two members of the low density lipoprotein receptor family, a2- macroglobulin receptor and glycoprotein 330. J. Biol. Chem. 267, 21162-21166 (1992).
130. Kanalas, J. J. & Makker, S. P. Analysis of a 45-kDa protein that binds to the Heymann nephritis autoantigen GP330. J. Biol. Chem. 268, 8188-8192 (1993).
131. Heymann, W., Hackel, D. B., Harwood, S., Wilson, S. G. F & Hunter, J. L. P. Production of the nephrotic syndrome in rats by Freund's adjuvants and rat kidney suspensions. Proc. Soc. Exp. Biol. Med. 100, 660-664 (1959).
132. Brent, R. L, Averich, E. & Drapiewski, V A. Production of congenital malformations using tissue antibodies. I. Kidney antisera. Proc. Soc. Exp. Biol. Med. 106, 523-526 (1961).