The endocytic receptor megalin and its associated proteins in proximal tubule epithelial cells

Membranes

Volumn 4, Issue 3, 2014, Pages 333-335

  De, Shankhajit ^a   Kuwahara, Shoji ^a   Saito, Akihiko ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

ARH; Clathrin; CLC 5; Cubilin; Endocytosis; Exosome; Megalin; NHE3; Trafficking

Indexed keywords

CELLS; DISEASES; MOLECULAR BIOLOGY; MOLECULES; PROTEINS;

ARH; CLATHRINS; CLC-5; CUBILIN; ENDOCYTOSIS; EXOSOME; MEGALIN; NHE3; TRAFFICKING;

DIAGNOSIS;

EID: 84904298932     PISSN: None     EISSN: 20770375     Source Type: Journal    
DOI: 10.3390/membranes4030333     Document Type: Article

References (167)

1. Evans, P.R.; Owen, D.J. Endocytosis and vesicle trafficking. Curr. Opin. Struct. Biol. 2002, 12, 814-821.
2. Scita, G.; di Fiore, P.P. The endocytic matrix. Nature 2010, 463, 464-473.
3. Taylor, M.J.; Perrais, D.; Merrifield, C.J. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 2011, 9, e1000604:1-e1000604:23.
4. Maldonado-Báez, L.; Wendland, B. Endocytic adaptors: Recruiters, coordinators and regulators. Trends Cell Biol. 2006, 16, 505-513.
5. Denzer, K.; Kleijmeer, M.J.; Heijnen, H.F.; Stoorvogel, W.; Geuze, H.J. Exosome: From internal vesicle of the multivesicular body to intercellular signaling device. J. Cell. Sci. 2000, 113, 3365-3374.
6. 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 1982, 79, 5557-5561.
7. Kerjaschki, D.; Farquhar, M.G. Immunocytochemical localization of the Heymann nephritis antigen (GP330) in glomerular epithelial cells of normal Lewis rats. J. Exp. Med. 1983, 157, 667-686.
8. 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. Natl. Acad. Sci. USA 1994, 91, 9725-9729.
9. Hjälm, G.; Murray, E.; Crumley, G.; Harazim, W.; Lundgren, S.; Onyango, I.; Ek, B.; Larsson, M.; Juhlin, C.; Hellman, P.; et al. Cloning and sequencing of human gp330, a Ca2+-binding receptor with potential intracellular signaling properties. Eur. J. Biochem. 1996, 239, 132-137.
10. Xia, Y.R.; Bachinsky, D.R.; Smith, J.A.; McCluskey, R.T.; Warden, C.H.; Lusis, A.J. Mapping of the glycoprotein 330 (Gp330) gene to mouse chromosome 2. Genomics 1993, 17, 780-781.
11. 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 1989, 244, 1163-1165.
12. Davis, C.G.; Goldstein, J.L.; Sudhof, T.C.; Anderson, R.G.; Russell, D.W.; Brown, M.S. Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region. Nature 1987, 326, 760-765.
13. Takeda, T.; Yamazaki, H.; Farquhar, M.G. Identification of an apical sorting determinant in the cytoplasmic tail of megalin. Am. J. Physiol. Cell. Physiol. 2003, 284, C1105-C1113.
14. Saito, A.; Sato, H.; Iino, N.; Takeda, T. Physiology and Pathophysiology of Megalin-Mediated Endocytosis in Renal Proximal Tubule Cells. In Advances in Medicine and Biology; Berhardt, L.V., Ed.; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2011; Volume 14, pp. 169-184.
15. Verroust, P.J.; Kozyraki, R.; Hammond, T.G.; Moestrup, S.K.; Christensen, E.I. Physiopathologic role of cubilin and megalin. Adv. Nephrol. Necker. Hosp. 2000, 30, 127-145.
16. Christensen, E.I.; Verroust, P.J.; Nielsen, R. Receptor mediated endocytosis in renal proximal tubule. Pflugers. Arch. 2009, 458, 1039-1048.
17. Prabakaran, T.; Nielsen, R.; Larsen, J.V.; Sørensen, S.S.; Feldt-Rasmussen, U.; Saleem, M.A.; Petersen, C.M.; Verroust, P.J.; Christensen, E.I. Receptor-mediated endocytosis of α-galactosidase A in human podocytes in Fabry disease. Nephrol. Dial. Transplant. 2012, 27, 3156-3159.
18. Chun, J.T.; Wang, L.; Pasinetti, G.M.; Finch, C.E.; Zlokovic, B.V. Glycoprotein 330/megalin (LRP-2) has low prevalence as mRNA and protein in brain microvessels and choroid plexus. Exp. Neurol. 1999, 157, 194-201.
19. Wicher, G.; Larsson, M.; Svenningsen, A.F.; Gyllencreutz, E.; Rask, L.; Aldskogius, H. Low density lipoprotein receptor-related protein-2/megalin is expressed in oligodendrocytes in the mouse spinal cord white matter. J. Neurosci. Res. 2006, 83, 864-873.
20. Bento-Abreu, A.; Velasco, A.; Polo-Hernández, E.; Pérez-Reyes, P.L.; Tabernero, A.; Medina, J.M. Megalin is a receptor for albumin in astrocytes and is required for the synthesis of the neurotrophic factor oleic acid. J. Neurochem. 2008, 106, 1149-1159.
21. Chung, R.S.; Penkowa, M.; Dittmann, J.; King, C.E.; Bartlett, C.; Asmussen, J.W.; Hidalgo, J.; Carrasco, J.; Leung, Y.K.; Walker, A.K. et al. Redefining the role of metallothionein within the injured brain: Extracellular metallothioneins play an important role in the astrocyte-neuron response to injury. J. Biol. Chem. 2008, 283, 15349-15358.
22. 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. 2001, 281, E900-E907.
23. Erranz, B.; Miquel, J.F.; Argraves, W.S.; Barth, J.L.; Pimentel, F.; Marzolo, M.P. Megalin and cubilin expression in gallbladder epithelium and regulation by bile acids. J. Lipid Res. 2004, 45, 2185-2198.
24. Lundgren, S.; Hjälm, G.; Hellman, P.; Ek, B.; Juhlin, C.; Rastad, J.; Klareskog, L.; Åkerström, G.; Rask, L. A protein involved in calcium sensing of the human parathyroid and placental cytotrophoblast cells belonging to the LDL-receptor superfamily. Exp. Cell Res. 1994, 212, 344-350.
25. Lundgren, S.; Carling, T.; Hjälm, G.; Juhlin, C.; Rastad, J.; Pihlgren, U.; Rask, L.; Akerström, G.; Hellman, P. Tissue distribution of human gp330/megalin, a putative Ca2+-sensing protein. J. Histochem. Cytochem. 1997, 45, 383-392.
26. Argraves, W.S.; Morales, C.R. Immunolocalization of cubilin, megalin, apolipoprotein J, and apolipoprotein A-I in the uterus and oviduct. Mol. Reprod. Dev. 2004, 69, 419-427.
27. Leheste, J.R.; Rolinski, B.; Vorum, H.; Hilpert, J.; Nykjaer, A.; Jacobsen, C.; Aucouturier, P.; Moskaug, J.O.; Otto, A.; Christensen, E.I.; et al. Megalin knockout mice as an animal model of low molecular weight proteinuria. Am. J. Pathol. 1999, 155, 1361-1370.
28. Kantarci, S.; Al-Gazali, L.; Hill, R.S.; Donnai, D.; Black, G.C.; Bieth, E.; Chassaing, N.; Lacombe, D.; Devriendt, K.; et al. Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat. Genet. 2007, 39, 957-959.
29. Pober, B.R.; Longoni, M.; Noonan, K.M. A Review of Donnai-Barrow and Facio-oculoacousticorenal (DB/FOAR) Syndrome: Clinical features and differential diagnosis. Birth Defects Res. A Clin. Mol. Teratol. 2009, 85, 76-81.
30. McCarthy, R.A.; Barth, J.L.; Chintalapudi, M.R.; Knaak, C.; Argraves, W.S. Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 2002, 277, 25660-25667.
31. Orlando, R.A.; Rader, K.; Authier, F.; Yamazaki, H.; Posner, B.I.; Bergeron, J.J.; Farquhar, M.G. Megalin is an endocytic receptor for insulin. J. Am. Soc. Nephrol. 1998, 9, 1759-1766.
32. Cui, S.; Verroust, P.J.; Moestrup, S.K.; Christensen, E.I. Megalin/gp330 mediates uptake of albumin in renal proximal tuble. Am. J. Physiol. Renal. Physiol. 1996, 271, F900-F907.
33. Gburek, J.; Verroust, P.J.; Willnow, T.E.; Fyfe, J.C.; Nowacki, W.; Jacobsen, C.; Moestrup, S.K.; Christensen, E.I. Megalin and cubilin are endocytic receptors involved in renal clearance of hemoglobin. J. Am. Soc. Nephrol. 2002, 13, 423-430.
34. Nykjaer, A.; Dragun, D.; Walther, D.; Vorum, H.; Jacobsen, C.; Herz, J.; Melsen, F.; Christensen, E.I.; Willnow, T.E. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 1999, 96, 507-515.
35. Christensen, E.I.; Moskaug, J.O.; Vorum, H.; Jacobsen, C.; Gundersen, T.E.; Nykjaer, A.; Blomhoff, R.; Willnow, T.E.; Moestrup, S.K. Evidence for an essential role of megalin in transepithelial transport of retinol. J. Am. Soc. Nephrol. 1999, 10, 685-695.
36. Saito, A.; Kazama, J.J.; Iino, N.; Cho, K.; Sato, N.; Yamazaki, H.; Oyama, Y.; Takeda, T.; Orlando, R.A.; Shimizu, F. Bioengineered implantation of megalin-expressing cells: A potential intracorporeal therapeutic model for uremic toxin protein clearance in renal failure. J. Am. Soc. Nephrol. 2003, 14, 2025-2032.
37. Saito, A.; Nagai, R.; Tanuma, A.; Hama, H.; Cho, K.; Takeda, T.; Yoshida, Y.; Toda, T.; Shimizu, F.; Horiuchi, S.; Gejyo, F. Role of megalin in endocytosis of advanced glycation end products: Implications for a novel protein binding to both megalin and advanced glycation end products. J. Am. Soc. Nephrol. 2003, 14, 1123-1131.
38. Batuman, V.; Guan, S. Receptor-mediated endocytosis of immunoglobulin light chains by renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 1997, 272, F521-F530.
39. Klassen, R.B.; Allen, P.L.; Batuman, V.; Crenshaw, K.; Hammond, T.G. Light chains are a ligand for megalin. J. Appl. Physiol. 2005, 98, 257-263.
40. Sengul, S.; Erturk, S.; Khan, A.M.; Batuman, V. Receptor-Associated Protein blocks internalization and cytotoxicity of Myeloma Light Chain in cultured human proximal tubular cells. PLoS One 2013, 8, e70276:1-e70276:8.
41. Moestrup, S.K.; Cui, S.; Vorum, H.; Bregengård, C.; Bjørn, S.E.; Norris, K.; Gliemann, J.; Christensen, E.I. Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J. Clin. Invest. 1995, 96, 1404-1413.
42. Christensen, E.I.; Birn, H.; Storm, T.; Weyer, K.; Nielsen, R. Endocytic receptors in the renal proximal tubule. Physiology 2012, 27, 223-236.
43. Seetharam, B.; Levine, J.S.; Ramsey, M.; Alpers, D.H. Purification, properties, and immunochemical localization of a receptor for intrinsic factor-cobalamin complex in the rat kidney. J. Biol. Chem. 1988, 263, 4443-4449.
44. 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. 1997, 99, 2317-2322.
45. Aminoff, M.; Carter, J.E.; Chadwick, R.B.; Johnson, C.; Gräsbeck, R.; Abdelaal, M.A.; Broch, H.; Jenner, L.B.; Verroust, P.J.; Moestrup, S.K. et al. Mutations in CUBN, encoding the intrinsic factor-vitamin B12 receptor, cubilin, cause hereditary megaloblastic anaemia 1. Nat. Genet. 1999, 21, 309-313.
46. Prabakaran, T.; Christensen, E.I.; Nielsen, R.; Verroust, P.J. Cubilin is expressed in rat and human glomerular podocytes. PLoS One 2011, 6, e25065:1-e25065:11.
47. Kristiansen, M.; Kozyraki, R.; Jacobsen, C.; Nexø, E.; Verroust, P.J.; Moestrup, S.K. Molecular dissection of the intrinsic factor-vitamin B12 receptor, cubilin, discloses regions important for membrane association and ligand binding. J. Biol. Chem. 1999, 274, 20540-20544.
48. Kozyraki, R.; Kristiansen, M.; Silahtaroglu, A.; Hansen, C.; Jacobsen, C.; Tommerup, N.; Verroust, P.J.; Moestrup, S.K. 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 1998, 91, 3593-3600.
49. Birn, H.; Fyfe, J.C.; Jacobsen, C.; Mounier, F.; Verroust, P.J.; Orskov, H.; Willnow, T.E.; Moestrup, S.K.; Christensen, E.I. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J. Clin. Invest. 2000, 105, 1353-1361.
50. Kozyraki, R.; Fyfe, J.; Verroust, P.J.; Jacobsen, C.; Dautry-Varsat, A.; Gburek, J.; Willnow, T.E.; Christensen, E.I.; Moestrup, S.K. Megalin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc. Natl. Acad. Sci. USA 2001, 98, 12491-12496.
51. Nykjaer, A.; Fyfe, J.C.; Kozyraki, R.; Leheste, J.R.; Jacobsen, C.; Nielsen, M.S.; Verroust, P.J.; Aminoff, M.; de la Chapelle, A.; Moestrup, S. K. et al. Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D(3). Proc. Natl. Acad. Sci. USA 2001, 98, 13895-13900.
52. Yammani, R.R.; Seetharam, S.; Seetharam, B. Identification and characterization of two distinct ligand binding regions of cubilin. J. Biol. Chem. 2001, 276, 44777-44784.
53. Fyfe, J.C.; Madsen, M.; Højrup, P.; Christensen, E.I.; Tanner, S.M.; de la Chapelle, A.; He, Q.; Moestrup, S.K. The functional cobalamin (vitamin B12)-intrinsic factor receptor is a novel complex of cubilin and amnionless. Blood 2004, 103, 1573-1579.
54. Coudroy, G.; Gburek, J.; Kozyraki, R.; Madsen, M.; Trugnan, G.; Moestrup, S.K.; Verroust, P.J.; Maurice, M. Contribution of cubilin and amnionless to processing and membrane targeting of cubilin-amnionless complex. J. Am. Soc. Nephrol. 2005, 16, 2330-2337.
55. Kalantry, S.; Manning, S.; Haub, O.; Tomihara-Newberger, C.; Lee, H.G.; Fangman, J.; Disteche, C.M.; Manova, K.; Lacy, E. The amnionless gene, essential for mouse gastrulation, encodes a visceral endoderm-specific protein with an extracellular cysteine-rich domain. Nat. Genet. 2001, 27, 412-416.
56. He, Q.; Madsen, M.; Kilkenney, A.; Gregory, B.; Christensen, E.I.; Vorum, H.; Højrup, P.; Schäffer, A.A.; Kirkness, E.F.; et al. Amnionless function is required for cubilin brush-border expression and intrinsic factor-cobalamin (vitamin B12) absorption in vivo. Blood 2005, 106, 1447-1453.
57. Zhang, F.; Zhao, Y.; Chao, Y.; Muir, K.; Han, Z. Cubilin and amnionless mediate protein reabsorption in Drosophila nephrocytes. J. Am. Soc. Nephrol. 2013, 24, 209-216.
58. Preisig, P.A; Rector, F.C., Jr. Role of Na+-H+ antiport in rat proximal tubule NaCl absorption. Am. J. Physiol. Renal Physiol. 1988, 255, F461-F465.
59. Preisig, P.A.; Ives, H.E.; Cragoe, E.J., Jr.; Alpern, R.J.; Rector, F.C., Jr. Role of the Na+/H+ antiporter in rat proximal tubule bicarbonate absorption. J. Clin. Invest. 1987, 80, 970-978.
60. Nagami, G.T. Luminal secretion of ammonia in the mouse proximal tubule perfused in vitro. J. Clin. Invest. 1988, 81, 159-164.
61. Bobulescu, I.A.; Moe, O.W. Luminal Na+/H+ exchange in the proximal tubule. Pflugers. Arch. 2009, 458, 5-21.
62. Pan, W.; Borovac, J.; Spicer, Z.; Hoenderop, J.G.; Bindels, R.J.; Shull, G.E.; Doschak, M.R.; Cordat, E.; Alexander, R.T. The epithelial sodium/proton exchanger, NHE3, is necessary for renal and intestinal calcium (re)absorption. Am. J. Physiol. Renal Physiol. 2012, 302, F943-F956.
63. LaPointe, MS.; Sodhi, C.; Sahai, A.; Batlle, D. Na+/H+ exchange activity and NHE-3 expression in renal tubules from the spontaneously hypertensive rat. Kidney Int. 2002, 62, 157-165.
64. Biemesderfer, D.; Nagy, T.; DeGray, B.; Aronson, P.S. Specific association of megalin and the Na+/H+ exchanger isoform NHE3 in the proximal tubule. J. Biol. Chem. 1999, 274, 17518-17524.
65. Biemesderfer, D.; DeGray, B.; Aronson, P.S. Active (9.6 s) and inactive (21 s) oligomers of NHE3 in microdomains of the renal brush border. J. Biol. Chem. 2001, 276, 10161-10167.
66. Schultheis, P.J.; Clarke, L.L.; Meneton, P.; Miller, M.L.; Soleimani, M.; Gawenis, L.R.; Riddle, T.M.; Duffy, J.J.; Doetschman, T.; Wang, T. et al. Renal and intestinal absorptive defects in mice lacking the NHE3 Na+/H+ exchanger. Nat. Genet. 1998, 19, 282-285.
67. Besse-Eschmann, V.; Klisic, J.; Nief, V.; Le Hir, M.; Kaissling, B.; Ambühl, P.M. Regulation of the proximal tubular sodium/proton exchanger NHE3 in rats with Puromycin Aminonucleoside (PAN)-induced nephrotic syndrome. J. Am. Soc. Nephrol. 2002, 13, 2199-2206.
68. Fuster, D.G.; Bobulescu, I.A.; Zhang, J.; Wade, J.; Moe, O.W. Characterization of the regulation of renal Na+/H+ exchanger NHE3 by insulin. Am. J. Physiol. Renal Physiol. 2007, 292, F577-F585.
69. Wesson, D.E. Endothelin role in kidney Acidification. Semin. Nephrol. 2006, 26, 393-398.
70. Uchida, S. In vivo role of CLC chloride channels in the kidney. Am. J. Physiol. Renal Physiol. 2000, 279, F802-F808.
71. Scheel, O.; Zdebik, A.A.; Lourdel, S.; Jentsch, T.J. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 2005, 436, 424-427.
72. Jentsch, T.J. Chloride transport in the kidney: Lessons from human disease and knockout mice. J. Am. Soc. Nephrol. 2005, 16, 1549-1561.
73. Ceol, M.; Tiralongo, E.; Baelde, H.J.; Vianello, D.; Betto, G.; Marangelli, A.; Bonfante, L.; Valente, M.; Della Barbera, M.; D'Angelo, A. et al. Involvement of the tubular ClC-type exchanger ClC-5 in glomeruli of human proteinuric nephropathies. PLoS One 2012, 7, e45605:1-e45605:7.
74. Günther, W.; Lüchow, A.; Cluzeaud, F.; Vandewalle, A.; Jentsch, T.J. ClC-5, the chloride channel mutated in Dent's disease, colocalizes with the proton pump in endocytotically active kidney cells. Proc. Natl. Acad. Sci. USA 1998, 95, 8075-8080.
75. Devuyst, O.; Christie, P.T.; Courtoy, P.J.; Beauwens, R.; Thakker, R.V. Intra-renal and subcellular distribution of the human chloride channel, CLC-5, reveals a pathophysiological basis for Dent's disease. Hum. Mol. Genet. 1999, 8, 247-257.
76. Piwon, N.; Günther, W.; Schwake, M.; Bösl, M.R.; Jentsch, T.J. ClC-5 Cl-channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 2000, 408, 369-373.
77. Hara-Chikuma, M.; Wang, Y.; Guggino, S.E.; Guggino, W.B.; Verkman, A.S. Impaired acidification in early endosomes of ClC-5 deficient proximal tubule. Biochem. Biophys. Res. Commun. 2005, 329, 941-946.
78. Rickheit, G.; Wartosch, L.; Schaffer, S.; Stobrawa, S.M.; Novarino, G.; Weinert, S.; Jentsch, T.J. Role of ClC-5 in renal endocytosis is unique among ClC exchangers and does not require PY-motif-dependent ubiquitylation. J. Biol. Chem. 2010, 285, 17595-17603.
79. Reed, A.A.; Loh, N.Y.; Terryn, S.; Lippiat, J.D.; Partridge, C.; Galvanovskis, J.; Williams, S.E.; Jouret, F.; Wu, F.T.; Courtoy, P.J. CLC-5 and KIF3B interact to facilitate CLC-5 plasma membrane expression, endocytosis, and microtubular transport: Relevance to pathophysiology of Dent's disease. Am. J. Physiol. Renal Physiol. 2010, 298, F365-F380.
80. Hryciw, D.H.; Jenkin, K.A.; Simcocks, A.C.; Grinfeld, E.; McAinch, A.J.; Poronnik, P. The interaction between megalin and ClC-5 is scaffolded by the Na+-H+ exchanger regulatory factor 2 (NHERF2) in proximal tubule cells. Int. J. Biochem. Cell Biol. 2012, 44, 815-823.
81. Christensen, E.I.; Devuyst, O.; Dom, G.; Nielsen, R.; Van der Smissen, P.; Verroust, P.; Leruth, M.; Guggino, W.B.; Courtoy, P.J. Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules. Proc. Natl. Acad. Sci. USA 2003, 100, 8472-8477.
82. Maritzen, T.; Lisi, S.; Botta, R.; Pinchera, A.; Fanelli, G.; Viacava, P.; Marcocci, C.; Marinò, M. ClC-5 does not affect megalin expression and function in the thyroid. Thyroid 2006, 16, 725-730.
83. Wrong, O.M.; Norden, A.G.; Feest, T.G. Dent's disease; a familial proximal renal tubular syndrome with low-molecular-weight proteinuria, hypercalciuria, nephrocalcinosis, metabolic bone disease, progressive renal failure and a marked male predominance. Q.J.M. 1994, 87, 473-493.
84. Lloyd, S.E.; Pearce, S.H.; Fisher, S.E.; Steinmeyer, K.; Schwappach, B.; Scheinman, S.J.; Harding, B.; Bolino, A.; Devoto, M.; Goodyer, P.; et al. A common molecular basis for three inherited kidney stone diseases. Nature 1996, 379, 445-449.
85. Wang, S.S.; Devuyst, O.; Courtoy, P.J.; Wang, X.T.; Wang, H.; Wang, Y.; Thakker, R.V.; Guggino, S.; Guggino, W.B. Mice lacking renal chloride channel, CLC-5, are a model for Dent's disease, a nephrolithiasis disorder associated with defective receptor-mediated endocytosis. Hum. Mol. Genet. 2000, 9, 2937-2945.
86. Devuyst, O.; Jouret, F.; Auzanneau, C.; Courtoy, P.J. Chloride channels and endocytosis: New insights from Dent's disease and ClC-5 knockout mice. Nephron Physiol. 2005, 99, 69-73.
87. Tanuma, A.; Sato, H.; Takeda, T.; Hosojima, M.; Obayashi, H.; Hama, H.; Iino, N.; Hosaka, K.; Kaseda, R.; Imai, N. et al. Functional characterization of a novel missense CLCN5 mutation causing alterations in proximal tubular endocytic machinery in Dent's disease. Nephron Physiol. 2007, 107, 87-97.
88. Devuyst, O.; Thakker, R.V. Dent's disease. Orphanet. J. Rare Dis. 2010, 5, 28:1-28:8.
89. Addis, M.; Meloni, C.; Tosetto, E.; Ceol, M.; Cristofaro, R.; Melis, M.A.; Vercelloni, P.; Del Prete, D.; Marra, G.; Anglani, F. An atypical Dent's disease phenotype caused by co-inheritance of mutations at CLCN5 and OCRL genes. Eur. J. Hum. Genet. 2013, 21, 687-690.
90. Miyamoto, K.; Tatsumi, S.; Segawa, H.; Ohkido, I.; Takeda, E. Identification and functional analysis of three isoforms for the Na+-dependent phosphate co-transporter (NaPi-2) in rat kidney. Nephrol. Dial. Transplant. 2000, 15, 31-33.
91. Beck, L.; Karaplis, A.C.; Amizuka, N.; Hewson, A.S.; Ozawa, H.; Tenenhouse, H.S. Targeted inactivation of Npt2 in mice leads to severe renal phosphate wasting, hypercalciuria, and skeletal abnormalities. Proc. Natl. Acad. Sci. USA 1998, 95, 5372-5377.
92. Marks, J.; Debnam, E.S.; Unwin, R.J. Phosphate homeostasis and the renal-gastrointestinal axis. Am. J. Physiol. Renal Physiol. 2010, 299, F285-F296.
93. Hernando, N.; Gisler, S.M.; Pribanic, S.; Deliot, N.; Capuano, P.; Wagner, C.A.; Moe, O.W.; Biber, J.; Murer, H. NaPi-IIa and interacting partners. J. Physiol. 2005, 567, 21-26.
94. Bachmann, S.; Schlichting, U.; Geist, B.; Mutig, K.; Petsch, T.; Bacic, D.; Wagner, C.A.; Kaissling, B.; Biber, J.; Murer, H. et al. Kidney-specific inactivation of the megalin gene impairs trafficking of renal inorganic sodium phosphate cotransporter (NaPi-IIa). J. Am. Soc. Nephrol. 2004, 15, 892-900.
95. Riquier, A.D.; Lee, D.H.; McDonough, A.A. Renal NHE3 and NaPi2 partition into distinct membrane domains. Am. J. Physiol. Cell Physiol. 2009, 296, C900-C910.
96. Tanimura, A.; Yamada, F.; Saito, A.; Ito, M.; Kimura, T.; Anzai, N.; Horie, D.; Yamamoto, H.; Miyamoto, K.; Taketani, Y.; et al. Analysis of different complexes of type IIa sodium dependent phosphate transporter in rat renal cortex using blue-native polyacrylamide gel electrophoresis. J. Med. Invest. 2011, 58, 140-147.
97. Lanaspa, M.A.; Caldas, Y.A.; Breusegem, S.Y.; Andrés-Hernando, A.; Cicerchi, C.; Levi, M.; Sorribas, V. Inorganic phosphate modulates the expression of the NaPi-2a transporter in the trans-golgi network and the interaction with PIST in the proximal tubule. Biomed. Res. Int. 2013, 2013, 513932:1-513932:9.
98. Gattineni, J.; Bates, C.; Twombley, K.; Dwarakanath, V.; Robinson, M.L.; Goetz, R.; Mohammadi, M.; Baum, M. FGF23 decreases renal NaPi-2a and NaPi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am. J. Physiol. Renal Physiol. 2009, 297, F282-F291.
99. Roopenian, D.C.; Akilesh, S. FcRn: The neonatal Fc receptor comes of age. Nat. Rev. Immunol. 2007, 7, 715-725.
100. Simister, N.E.; Mostov, K.E. An Fc receptor structurally related to MHC class I antigens. Nature 1989, 337, 184-187.
101. Burmeister, W.P.; Huber, A.H.; Bjorkman, P.J. Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature 1994, 372, 379-383.
102. Chaudhury, C.; Mehnaz, S.; Robinson, J.M.; Hayton, W.L.; Pearl, D.K.; Roopenian, D.C.; Anderson, C.L. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J. Exp. Med. 2003, 197, 315-322.
103. Chaudhury, C.; Brooks, C.L.; Carter, D.C.; Robinson, J.M.; Anderson, C.L. Albumin binding to FcRn: Distinct from the FcRn-IgG interaction. Biochemistry 2006, 45, 4983-4990.
104. Nagai, J.; Sato, K.; Yumoto, R.; Takano, M. Megalin/cubilin-mediated uptake of FITC-labeled IgG by OK kidney epithelial cells. Drug Metab. Pharmacokinet. 2011, 26, 474-485.
105. Haymann, J.P.; Levraud, J.P.; Bouet, S.; Kappes, V.; Hagege, J.; Nguyen, G.; Xu, Y.; Rondeau, E.; Sraer, J.D. Characterization and localization of the neonatal Fc receptor in adult human kidney. J. Am. Soc. Nephrol. 2000, 11, 632-639.
106. Akilesh, S.; Huber, T.B.; Wu, H.; Wang, G.; Hartleben, B.; Kopp, J.B.; Miner, J.H.; Roopenian, D.C.; Unanue, E.R.; Shaw, A.S. Podocytes use FcRn to clear IgG from the glomerular basement membrane. Proc. Natl. Acad. Sci. USA 2008, 105, 967-972.
107. Sarav, M.; Wang, Y.; Hack, B.K.; Chang, A.; Jensen, M.; Bao, L.; Quigg, R.J. Renal FcRn reclaims albumin but facilitates elimination of IgG. J. Am. Soc. Nephrol. 2009, 20, 1941-1952.
108. Tenten, V.; Menzel, S.; Kunter, U.; Sicking, E.M.; van Roeyen, C.R.; Sanden, S.K.; Kaldenbach, M.; Boor, P.; Fuss, A.; Uhlig, S. et al. Albumin is recycled from the primary urine by tubular transcytosis. J. Am. Soc. Nephrol. 2013, 24, 1966-1980.
109. Christensen, E.I.; Birn, H. Tubular handling of albumin-degradation or salvation? Nat. Rev. Nephrol. 2013, 9, 700-702.
110. Gotthardt, M.; Trommsdorff, M.; Nevitt, M.F.; Shelton, J.; Richardson, J.A.; Stockinger, W.; Nimpf, J.; Herz, J. Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem. 2000, 275, 25616-25624.
111. Larsson, M.; Hjalm, G.; Sakwe, A.M.; Engstrom, A.; Hoglund, A.S.; Larsson, E.; Robinson, R.C.; Sundberg, C.; Rask, L. Selective interaction of megalin with postsynaptic density-95 (PSD-95)-like membrane-associated guanylate kinase (MAGUK) proteins. Biochem. J. 2003, 373, 381-391.
112. Lou, X.; McQuistan, T.; Orlando, R.A.; Farquhar, M.G. GAIP, GIPC and Galphai3 are concentrated in endocytic compartments of proximal tubule cells: Putative role in regulating megalin's function. J. Am. Soc. Nephrol. 2002, 13, 918-927.
113. Petersen, H.H.; Hilpert, J.; Militz, D.; Zandler, V.; Jacobsen, C.; Roebroek, A.J.; Willnow, T.E. Functional interaction of megalin with the megalin binding protein (MegBP), a novel tetratrico peptide repeat-containing adaptor molecule. J. Cell Sci. 2003, 116, 453-461.
114. Rader, K.; Orlando, R.A.; Lou, X.; Farquhar, M.G. Characterization of ANKRA, a novel ankyrin repeat protein that interacts with the cytoplasmic domain of megalin. J. Am. Soc. Nephrol. 2000, 11, 2167-2178.
115. 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. 1990, 265, 3116-3123.
116. Nagai, M.; Meerloo, T.; Takeda, T.; Farquhar, M.G. The adaptor protein ARH escorts megalin to and through endosomes. Mol. Biol. Cell. 2003, 14, 4984-4996.
117. Oleinikov, A.V.; Zhao, J.; Makker, S.P. Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem. J. 2000, 347, 613-621.
118. Traub, L.M. Tickets to ride: Selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 2009, 10, 583-596.
119. Nagai, J.; Christensen, E.I.; Morris, S.M.; Willnow, T.E.; Cooper, J.A.; Nielsen, R. Mutually-dependent localization of megalin and Dab2 in the renal proximal tubule. Am. J. Physiol. Renal Physiol. 2005, 289, F569-F576.
120. Maurer, M.E.; Cooper, J.A. Endocytosis of megalin by visceral endoderm cells requires the Dab2 adaptor protein. J. Cell Sci. 2005, 118, 5345-5355.
121. Maurer, M.E.; Cooper, J.A. The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J. Cell Sci. 2006, 119, 4235-4246.
122. Hasson, T. Myosin VI: Two distinct roles in endocytosis. J. Cell Sci. 2003, 116, 3453-3461.
123. Avraham, K.B.; Hasson, T.; Steel, K.P.; Kingsley, D.M.; Russell, L.B.; Mooseker, M.S.; Copeland, N.G.; Jenkins, N.A. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat. Genet. 1995, 11, 369-375.
124. Hosaka, K.; Takeda, T.; Iino, N.; Hosojima, M.; Sato, H.; Kaseda, R.; Yamamoto, K.; Kobayashi, A.; Gejyo, F.; Saito, A. Megalin and nonmuscle myosin heavy chain IIA interact with the adaptor protein Disabled-2 in proximal tubule cells. Kidney Int. 2009, 75, 1308-1315.
125. Kelley, M.J.; Jawien, W.; Ortel, T.L.; Korczak, J.F. Mutation of MYH9, encoding non-muscle myosin heavy chain A, in May-Hegglin anomaly. Nat. Genet. 2000, 26, 106-108.
126. Seri, M.; Cusano, R.; Gangarossa, S.; Caridi, G.; Bordo, D.; Lo Nigro, C.; Ghiggeri, G.M.; Ravazzolo, R.; Savino, M.; Del Vecchio, M. et al. Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes. The May-Heggllin/Fechtner Syndrome Consortium. Nat. Genet. 2000, 26, 103-105.
127. Seri, M.; Savino, M.; Bordo, D.; Cusano, R.; Rocca, B.; Meloni, I.; Di, B.; Koivisto, P.A.; Bolognesi, M.; Ghiggeri, G.M. et al. Epstein syndrome: Another renal disorder with mutations in the nonmuscle myosin heavy chain 9 gene. Hum. Genet. 2002, 110, 182-186.
128. Kao, W.H.; Klag, M.J.; Meoni, L.A.; Reich, D.; Berthier-Schaad, Y.; Li, M.; Coresh, J.; Patterson, N.; Tandon, A.; Powe, N.R. et al. MYH9 is associated with nondiabetic end-stage renal disease in African Americans. Nat. Genet. 2008, 40, 1185-1192.
129. Kopp, J.B.; Smith, M.W.; Nelson, G.W.; Johnson, R.C.; Freedman, B.I.; Bowden, D.W.; Oleksyk, T.; McKenzie, L.M.; Kajiyama, H.; Ahuja, T.S. MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis. Nat. Genet. 2008, 40, 1175-1184.
130. Koral, K.; Erkan, E. PKB/Akt partners with Dab2 in albumin Endocytosis. Am. J. Physiol. Renal Physiol. 2012, 302, F1013-F1024.
131. Garcia, C.K.; Wilund, K.; Arca, M.; Zuliani, G.; Fellin, R.; Maioli, M.; Calandra, S.; Bertolini, S.; Cossu, F.; Grishin, N. et al. Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 2001, 292, 1394-1398.
132. Mishra, S.K.; Watkins, S.C.; Traub, L.M. The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc. Natl. Acad. Sci. USA 2002, 99, 16099-16104.
133. He, G.; Gupta, S.; Michaely, P.; Hobbs, H.H.; Cohen, J.C. ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin and AP-2. J. Biol. Chem. 2002, 277, 44044-44049.
134. Lehtonen, S.; Shah, M.; Nielsen, R.; Iino, N.; Ryan, J.J.; Zhou, H.; Farquhar, M.G. The endocytic adaptor protein ARH associates with motor and centrosomal proteins and is involved in centrosome assembly and cytokinesis. Mol. Biol. Cell. 2008, 19, 2949-2961.
135. Shah, M.; Baterina, O.Y., Jr.; Taupin, V.; Farquhar, M.G. ARH directs megalin to the endocytic recycling compartment to regulate its proteolysis and gene expression. J. Cell. Biol. 2013, 202, 113-127.
136. Kang, R.S.; Fölsch, H. ARH cooperates with AP-1B in the exocytosis of LDLR in polarized epithelial cells. J. Cell Biol. 2011, 193, 51-60.
137. Pedersen, G.A.; Chakraborty, S.; Steinhauser, A.L.; Traub, L.M.; Madsen, M. AMN directs endocytosis of the intrinsic factor-vitamin B12 receptor cubam by engaging ARH or Dab2. Traffic 2010, 11, 706-720.
138. Vlassov, A.V.; Magdaleno, S.; Setterquist, R.; Conrad, R. Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 2012, 1820, 940-948.
139. Théry, C.; Zitvogel, L.; Amigorena, S. Exosomes: Composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2, 569-579.
140. Cocucci, E.; Racchetti, G.; Meldolesi, J. Shedding microvesicles: Artifacts no more. Trends Cell Biol. 2009, 19, 43-51.
141. van Niel, G.; Porto-Carreiro, I.; Simoes, S.; Raposo, G. Exosomes: A common pathway for a specialized function. J. Biochem. 2006, 140, 13-21.
142. Valadi, H.; Ekström, K.; Bossios, A.; Sjöstrand, M.; Lee, J.J.; Lötvall, J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9, 654-659.
143. Lv, L.L.; Cao, Y.; Liu, D.; Xu, M.; Liu, H.; Tang, R.N.; Ma, K.L.; Liu, B.C. Isolation and quantification of microRNAs from urinary exosomes/microvesicles for biomarker discovery. Int. J. Biol. Sci. 2013, 9, 1021-1031.
144. Simpson, R.J.; Lim, J.W.; Moritz, R.L.; Mathivanan, S. Exosomes: Proteomic insights and diagnostic potential. Expert. Rev. Proteomics 2009, 6, 267-283.
145. Pisitkun, T.; Shen, R.F.; Knepper, M.A. Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. USA 2004, 101, 13368-13373.
146. Gonzales, P.A.; Pisitkun, T.; Hoffert, J.D.; Tchapyjnikov, D.; Star, R.A.; Kleta, R.; Wang, N.S.; Knepper, M.A. Large-scale proteomics and phosphoproteomics of urinary exosomes. J. Am. Soc. Nephrol. 2009, 20, 363-379.
147. Raimondo, F.; Corbetta, S.; Morosi, L.; Chinello, C.; Gianazza, E.; Castoldi, G.; Di Gioia, C.; Bombardi, C.; Stella, A.; Battaglia, C. Urinary exosomes and diabetic nephropathy: A proteomic approach. Mol. Biosyst. 2013, 9, 1139-1146.
148. Russo, L.M.; del Re, E.; Brown, D.; Lin, H.Y. Evidence for a role of transforming growth factor (TGF)-beta1 in the induction of postglomerular albuminuria in diabetic nephropathy: Amelioration by soluble TGF-beta type II receptor. Diabetes 2007, 56, 380-388.
149. Hosojima, M.; Sato, H.; Yamamoto, K.; Kaseda, R.; Soma, T.; Kobayashi, A.; Kabasawa, H.; Takeyama, A.; Ikuyama, K. et al. Regulation of megalin expression in cultured proximal tubule cells by angiotensin II type 1A receptor- and insulin-mediated signaling cross talk. Endocrinology 2009, 150, 871-878.
150. Takeyama, A.; Sato, H.; Soma-Nagae, T.; Kabasawa, H.; Suzuki, A.; Yamamoto-Kabasawa, K.; Hosojima, M.; Kaneko, R.; Higuchi, F.; Kaseda, R. et al. Megalin is downregulated via LPS-TNF-α-ERK1/2 signaling pathway in proximal tubule cells. Biochem. Biophys. Res. Commun. 2011, 407, 108-112.
151. Cabezas, F.; Lagos, J.; Céspedes, C.; Vio, C.P.; Bronfman, M.; Marzolo, M.P. Megalin/LRP2 expression is induced by peroxisome proliferator-activated receptor -alpha and -gamma: Implications for PPARs' roles in renal function. PLoS One 2011, 6, e16794:1-e16794:17.
152. Reisman, S.A.; Chertow, G.M.; Hebbar, S.; Vaziri, N.D.; Ward, K.W.; Meyer, C.J. Bardoxolone methyl decreases megalin and activates nrf2 in the kidney. J. Am. Soc. Nephrol. 2012, 23, 1663-1673.
153. Zou, Z.; Chung, B.; Nguyen, T.; Mentone, S.; Thomson, B.; Biemesderfer, D. Linking receptor-mediated endocytosis and cell signaling: Evidence for regulated intramembrane proteolysis of megalin in proximal tubule. J. Biol. Chem. 2004, 279, 34302-34310.
154. Li, Y.; Cong, R.; Biemesderfer, D. The COOH terminus of megalin regulates gene expression in opossum kidney proximal tubule cells. Am. J. Physiol. Cell Physiol. 2008, 295, C529-C537.
155. Christ, A.; Terryn, S.; Schmidt, V.; Christensen, E.I.; Huska, M.R.; Andrade-Navarro, M.A.; Hubner, N.; Devuyst, O.; Hammes, A.; Willnow, T.E. The soluble intracellular domain of megalin does not affect renal proximal tubular function in vivo. Kidney Int. 2010, 78, 473-477.
156. Motoyoshi, Y.; Matsusaka, T.; Saito, A.; Pastan, I.; Willnow, T.E.; Mizutani, S.; Ichikawa, I. Megalin contributes to the early injury of proximal tubule cells during nonselective proteinuria. Kidney Int. 2008, 74, 1262-1269.
157. Shalamanova, L.; McArdle, F.; Amara, A.B.; Jackson, M.J.; Rustom, R. Albumin overload induces adaptive responses in human proximal tubular cells through oxidative stress but not via angiotensin II type 1 receptor. Am. J. Physiol. Renal Physiol. 2007, 292, F1846-1857.
158. Morigi, M.; Macconi, D.; Zoja, C.; Donadelli, R.; Buelli, S.; Zanchi, C.; Ghilardi, M.; Remuzzi, G. Protein overload-induced NF-kappaB activation in proximal tubular cells requires H2O2 through a PKC-dependent pathway. J. Am. Soc. Nephrol. 2002, 13, 1179-1189.
159. Burns, W.C.; Kantharidis, P.; Thomas, M.C. The role of tubular epithelial-mesenchymal transition in progressive kidney disease. Cells Tissues Organs 2007, 185, 222-231.
160. Strutz, F.M. EMT and proteinuria as progression factors. Kidney Int. 2009, 75, 475-481.
161. Saito, A.; Takeda, T.; Sato, K.; Hama, H.; Tanuma, A.; Kaseda, R.; Suzuki, Y.; Gejyo, F. Significance of proximal tubular metabolism of advanced glycation end products in kidney diseases. Ann. N. Y. Acad. Sci. 2005, 1043, 637-643.
162. Verbeke, P.; Perichon, M.; Friguet, B.; Bakala, H. Inhibition of nitric oxide synthase activity by early and advanced glycation end products in cultured rabbit proximal tubular epithelial cells. Biochim. Biophys. Acta 2000, 1502, 481-494.
163. Obeid, R.; Shannan, B.; Herrmann, W. Advanced glycation end products overload might explain intracellular cobalamin deficiency in renal dysfunction, diabetes and aging. Med. Hypotheses 2011, 77, 884-848.
164. Sengul, S.; Zwizinski, C.; Batuman, V. Role of MAPK pathways in light chain-induced cytokine production in human proximal tubule cells. Am. J. Physiol. Renal Physiol. 2003, 284, F1245-F1254.
165. Li, M.; Hering-Smith, K.S.; Simon, E.E.; Batuman, V. Myeloma light chains induce epithelial-mesenchymal transition in human renal proximal tubule epithelial cells. Nephrol. Dial. Transplant. 2008, 23, 860-870.
166. Hutchison, C.A.; Batuman, V.; Behrens, J.; Bridoux, F.; Sirac, C.; Dispenzieri, A.; Herrera, G.A.; Lachmann, H.; Sanders, P.W. International Kidney and Monoclonal Gammopathy Research Group. The pathogenesis and diagnosis of acute kidney injury in multiple myeloma. Nat. Rev. Nephrol. 2011, 8, 43-51.
167. Ogasawara, S.; Hosojima, M.; Kaseda, R.; Kabasawa, H.; Yamamoto-Kabasawa, K.; Kurosawa, H.; Sato, H.; Iino, N.; Takeda, T.; Suzuki, Y. et al. Significance of urinary full-length and ectodomain forms of megalin in patients with type 2 diabetes. Diabetes Care 2012, 35, 1112-1118.