Physiological importance of endosomal acidification: Potential role in proximal tubulopathies

Current Opinion in Nephrology and Hypertension

Volumn 11, Issue 5, 2002, Pages 527-537

  Marshansky, Vladimir ^a   Ausiello, Dennis A ^a   Brown, Dennis ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

CLC 5; Cubilin; Endosomal acidification; Fanconi syndrome; Kidney proximal tubule; Megalin; Protein reabsorption; Receptor mediated endocytosis; V ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALBUMIN; ALBUMIN RECEPTOR; AMINOGLYCOSIDE DERIVATIVE; APOLIPOPROTEIN; AQUAPORIN 1; BETA 2 MICROGLOBULIN; CADMIUM; CARRIER PROTEIN; CHEMOKINE; CHLORIDE CHANNEL; CLATHRIN; COLECALCIFEROL; CUBILIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; ELECTROLYTE; EPIDERMAL GROWTH FACTOR; GLUCOSE TRANSPORTER; GUANOSINE TRIPHOSPHATASE; HORMONE; MEGALIN; MEMBRANE PROTEIN; PARATHYROID HORMONE; PLASMA PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; POLYPEPTIDE; PROUROKINASE; RECEPTOR; RETINOL BINDING PROTEIN; UNINDEXED DRUG; VITAMIN BINDING PROTEIN;

ABSORPTION; ACIDIFICATION; DISEASE ASSOCIATION; ENDOCYTOSIS; ENDOSOME; ENZYME INHIBITION; FANCONI RENOTUBULAR SYNDROME; GENE MUTATION; HUMAN; KIDNEY FAILURE; KIDNEY PROXIMAL TUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA; REVIEW;

ABSORPTION; ACIDS; ANIMALS; ENDOCYTOSIS; ENDOSOMES; FANCONI SYNDROME; HUMANS; KIDNEY DISEASES; KIDNEY TUBULES, PROXIMAL; PROTEINS; RECEPTORS, CELL SURFACE;

EID: 0036736777     PISSN: 10624821     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041552-200209000-00009     Document Type: Review

References (103)

1. Marshansky V, Bourgoin S, Londono I, et al. Receptor-mediated endocytosis in kidney proximal tubules: recent advances and hypothesis. Electrophoresis 1997; 18:2661-2676.
2. Brown D, Stow JL. Protein trafficking and polarity in kidney epithelium: from cell biology to physiology. Physiol Rev 1996; 76:245-297.
3. +-ATPase and endocytosis in rat kidney cortex. Kidney Int 1998; 53:1713-1726.
4. Marshansky V, Richard M, Bartle J, et al. Regulation of renal albumin reabsorption by endosomal proton transport [Abstract]. J Amer Soc Nephrol 1996; 7:1311.
5. Fisher SE, Black GC, Lloyd SE, et al. Isolation and partial characterization of a chloride channel gene which is expressed in kidney and is a candidate for Dent's disease (an X-linked hereditary nephrolithiasis). Hum Mol Genet 1994; 3:2053-2059.
6. Fisher SE, van Bakel I, Lloyd SE, et al. Cloning and characterization of CLCN5, the human kidney chloride channel gene implicated in Dent disease (an X-linked hereditary nephrolithiasis). Genomics 1995; 29:598-606.
7. Steinmeyer K, Schwappach B, Bens M, et al. Cloning and functional expression of rat CLC-5, a chloride channel related to kidney disease. J Biol Chem 1995; 270:31172-31177.
8. Lloyd SE, Pearce SH, Fisher SE, et al. A common molecular basis for three inherited kidney stone diseases. Nature 1996; 379:445-449.
9. --channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 2000; 408:369-373.
10. Wang SS, Devuyst O, Courtoy PJ, et al. 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.
11. Jentsch TJ, Stein V, Weinreich F, Zdebik AA. Molecular structure and physiological function of chloride channels. Physiol Rev 2002; 82:503-568.
12. Maranda B, Brown D, Bourgoin S, et al. Intra-endosomal pH-sensitive recruitment of the Arf-nucleotide exchange factor ARNO and Arf6 from cytoplasm to proximal tubule endosomes. J Biol Chem 2001; 276:18540-18550.
13. Marshansky V, Maranda B, Bourgoin S, et al. Intraendosomal pH-sensitive recruitment of ARNO and Arf6 to kidney proximal tubules endosomes: the possible link between impaired endosomal acidification and protein reabsorption in Dent's disease and Fanconi syndrome [abstract]. Biochem Cell Biol 2001; 79:678.
14. Christensen EI, Birn H, Verroust P, Moestrup SK. Membrane receptors for endocytosis in the renal proximal tubule. Int Rev Cytol 1998; 180:237-284.
15. Christensen EI, Birn H. Megalin and cubilin: synergistic endocytic receptors in renal proximal tubule. Am J Physiol Renal Physiol 2001; 280:F562-F573.
16. Kerjaschki D, Farquhar MG. The pathogenic antigen of Heymann nephritis is a membrane glycoprotein of the renal proximal tubule brush border. Proc Natl Acad Sci U S A 1982; 79:5557-5581.
17. Saito A, Pietromonaco S, Leo AK, Farquhar MG. Complete cloning and sequencing of rat gp330/"megalin", a distinctive member of the low density lipoprotein receptor gene family. Proc Natl Acad Sci U S A 1994; 91:9725-9729.
18. Raychowdhury R, Niles JL, McCluskey RT, Smith JA. Autoimmune target in Heymann nephritis is a glycoprotein with homology to the LDL receptor. Science 1989; 244:1163-1165.
19. Sahali D, Mulliez N, Chatelet F, 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 Exp Med 1988; 167:213-218.
20. Moestrup SK, Kozyraki R, Kristiansen M, 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 1998; 273:5235-5242.
21. Moestrup SK, Nielsen S, Andreasen P, et al. Epithelial glycoprotein-330 mediates endocytosis of plasminogen activator-plasminogen activator inhibitor type-1 complexes. J Biol Chem 1993; 268:16564-16570.
22. Birn H, Fyfe JC, Jacobsen C, et al. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J Clin Invest 2000; 105:1353-1361.
23. Cui S, Verroust PJ, Moestrup SK, Christensen EI. Megalin/gp330 mediates uptake of albumin in renal proximal tubule. Am J Physiol 1996; 271:F900-F907.
24. Cessac-Guillemet AL, Mounier F, Borot C, et al. Characterization and distribution of albumin binding protein in normal rat kidney. Am J Physiol 1996; 271:F101-F107.
25. Gburek J, Verroust PJ, Willnow TE, et al. Megalin and cubilin are endocytic receptors involved in renal clearance of hemoglobin. J Am Soc Nephrol 2002; 13:423-430.
26. Kozyraki R, Fyfe J, Verroust PJ, et al. Megalin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc Natl Acad Sci U S A 2001; 98:12491-12496.
27. Orlando RA, Rader K, Authier F, et al. Megalin is an endocytic receptor for insulin. J Am Soc Nephrol 1998; 9:1759-1766.
28. Hilpert J, Nykjaer A, Jacobsen C, et al. Megalin antagonizes activation of the parathyroid hormone receptor. J Biol Chem 1999; 274:5620-5625.
29. Christensen EI, Willnow TE. Essential role of megalin in renal proximal tubule for vitamin homeostasis. J Am Soc Nephrol 1999; 10:2224-2236.
30. 3. Cell 1999; 96:507-515.
31. 3. Proc Natl Acad Sci U S A 2001; 98:13895-13900.
32. Christensen EI, Moskaug JO, Vorum H, et al. Evidence for an essential role of megalin in transepithelial transport of retinol. J Am Soc Nephrol 1999; 10:685-695.
33. Marino M, Andrews D, Brown D, McCluskey RT. Transcytosis of retinol-binding protein across renal proximal tubule cells after megalin (gp 330)-mediated endocytosis. J Am Soc Nephrol 2001; 12:637-648.
34. 12 in LLC-PK1 renal proximal tubule cells. J Am Soc Nephrol 2001; 12:1099-1106.
35. 12. Am J Physiol Renal Physiol 2002; 282:F408-F416.
36. 12 receptor, cubilin, is a high-affinity apolipoprotein A-I receptor facilitating endocytosis of high-density lipoprotein. Nat Med 1999; 5:656-661.
37. Schmitz C, Hilpert J, Jacobsen C, et al. Megalin deficiency offers protection from renal aminoglycoside accumulation. J Biol Chem 2002; 277:618-622.
38. Maack T, Johnson V, Kau ST, et al. Renal filtration, transport, and metabolism of low-molecular-weight proteins: a review [Review]. Kidney Int 1979; 16:251-270.
39. Maack T, Park C, Camargo M. Renal filtration, transport and metabolism of proteins. In: Seldin D, Giebisch G, editors. The kidney: physiology and pathophysiology. New York: Raven Press; 1985. pp. 1773-1803.
40. Christensen EI, Birn H. Megalin and cubilin: multifunctional endocytotic receptors. [Review]. Nat Rev Mol Cell Biol 2002; 3:258-268.
41. Fyfe JC, Giger U, Hall CA, et al. Inherited selective intestinal cobalamin malabsorption and cobalamin deficiency in dogs. Pediatr Res 1991; 29:24-31.
42. Fyfe JC, Ramanujam KS, Ramaswamy K, et al. Defective brush-border expression of intrinsic factor-cobalamin receptor in canine inherited intestinal cobalamin malabsorption. J Biol Chem 1991; 266:4489-4494.
43. 12 receptor, cubilin, cause hereditary megaloblastic anaemia 1. Nat Genet 1999; 21:309-313.
44. Broch H, Imerslund O, Monn E, et al. Imerslund-Grasbeck anemia. A long-term follow-up study. Acta Paediatr Scand 1984; 73:248-253.
45. Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 1986; 55:663-700.
46. Mellman I. The importance of being acid: the role of acidification in intracellular membrane traffic. J Exp Biol 1992; 172:39-45.
47. Shi LB, Fushimi K, Bae HR, Verkman AS. Heterogeneity in ATP-dependent acidification in endocytic vesicles from kidney proximal tubule: measurement of pH in individual endocytic vesicles in a cell-free system. Biophys J 1991; 59:1208-1217.
48. Marshansky V, Vinay P. Proton gradient formation in early endosomes from proximal tubules. Biochim Biophys Acta 1996; 1284:171-180.
49. +V-ATPase/proton pump). In: Seldin DW, Giebisch G, editors. The kidney: physiology and pathophysiology, vol. 1. Philadelphia: Lippincott Williams & Wilkins; 2000. pp. 171-191.
50. Sabolic I, Burckhardt G. Characteristics of the proton pump in rat renal cortical endocytotic vesicles. Am J Physiol 1986; 250:F817-F826.
51. Sabolic I, Burckhardt G. Proton ATPase in rat renal cortical endocytotic vesicles. Biochim Biophys Acta 1988; 937:398-410.
52. Sabolic I, Burckhardt G. ATP-driven proton transport in vesicles from the kidney cortex. Methods Enzymol 1990; 191:505-520.
53. Uchida S. In vivo role of CLC chloride channels in the kidney. Am J Physiol Renal Physiol 2000; 279:F802-F808.
54. Bae HR, Verkman AS. Protein kinase A regulates chloride conductance in endocytic vesicles from proximal tubule. Nature 1990; 348:637-639.
55. Gunther W, Luchow A, Cluzeaud F, et al. CIC-5, the chloride channel mutated in Dent's disease, colocalizes with the proton pump in endocytotically active kidney cells. Proc Natl Acad Sci U S A 1998; 95:8075-8080.
56. Luyckx VA, Goda FO, Mount DB, et al. Intrarenal and subcellular localization of rat CLC5. Am J Physiol 1998; 275:F761-F769.
57. +-ATPase. Am J Physiol 1999; 277:F957-F965.
58. Marshansky V, Fleser A, Noel J, et al. Isolation of heavy endosomes from dog proximal tubules in suspension. J Membr Biol 1996; 153:59-73.
59. Wills NK, Fong P. CIC chloride channels in epithelia: recent progress and remaining puzzles. News Physiol Sci 2001; 16:161-166.
60. - indicator: evidence for chloride accumulation during acidification. J Biol Chem 2002; 277:5506-5513.
61. +-ATPases - nature's most versatile proton pumps. Nat Rev Mol Cell Biol 2002; 3:94-103.
62. + exchanger isoform NHE3 in the proximal tubule. J Biol Chem 1999; 274:17518-17524.
63. + exchanger isoform NHE3 and dipeptidyl peptidase IV in the renal proximal tubule. J Biol Chem 2001; 276:46671-46677.
64. Biemesderfer D, DeGray B, Aronson PS. 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.
65. + exchanger-3 isoform. J Biol Chem 2002; 277:11090-11096.
66. Bergeron M, Gougoux A, Vinay P. The renal Fanconi syndrome. In: Scriver C, Beaudet A, Sly W, editors. The metabolic and molecular bases of inherited disease, vol. 3. New York: McGraw-Hill; 1995. pp. 3691-3716.
67. Bergeron M, Gougoux A, Noel J, Parent L. The renal Fanconi syndrome. In: Scriver CR, Beaudet AL, et al., editors. The metabolic and molecular bases of inherited disease, 8th edn. New York: McGraw-Hill; 2001. pp. 5023-5038.
68. Bonnardeaux A, Bichet DG. Inherited disorders of the renal tubule. In: Brenner BM, editor. The kidney, vol. 2, 6th edn. Philadelphia: W. B. Saunders; 2000. pp. 1656-1698.
69. Thakker RV. Pathogenesis of Dent's disease and related syndromes of X-linked nephrolithiasis. Kidney Int 2000; 57:787-793.
70. Lowe C, Terrey M, MacLachlan E. Organic aciduria, decreased renal ammonia production, hydrophthalmos and mental retardation: a clinical entity. Am J Dis Child 1952; 83:164-184.
71. Nussbaum RL, Orrison BM, Janne PA, et al. Physical mapping and genomic structure of the Lowe syndrome gene OCRL1. Hum Genet 1997; 99:145-150.
72. Adams RG, Harrison JF, Scott P. The development of cadmium-induced proteinuria, impaired renal function, and osteomalacia in alkaline battery workers. Q J Med 1969; 38:425-443.
73. Kim YK, Choi JK, Kim JS, Park YS. Changes in renal function in cadmium-intoxicated rats. Pharmacol Toxicol 1988; 63:342-350.
74. Kim KR, Lee HY, Kim CK, Park YS. Alteration of renal amino acid transport system in cadmium-intoxicated rats. Toxicol Appl Pharmacol 1990; 106:102-111.
75. Lee HY, Kim KR, Park YS. Transport kinetics of glucose and alanine in renal brush-border membrane vesicles of cadmium-intoxicated rabbits. Pharmacol Toxicol 1991; 69:390-395.
76. Ahn DW, Park YS. Transport of inorganic phosphate in renal cortical brush-border membrane vesicles of cadmium-intoxicated rats. Toxicol Appl Pharmacol 1995; 133:239-243.
77. Herak-Kramberger CM, Spindler B, Biber J, et al. Renal type II Na/Pi-cotransporter is strongly impaired whereas the Na/sulphate-cotransporter and aquaporin 1 are unchanged in cadmium-treated rats. Pflugers Arch 1996; 432:336-344.
78. +ATPase-mediated acidification in the rat epididymis. Biol Reprod 2000; 63:599-606.
79. Sabolic I, Herak-Kramberger CM, Brown D. Subchronic cadmium treatment affects the abundance and arrangement of cytoskeletal proteins in rat renal proximal tubule cells. Toxicology 2001; 165:205-216.
80. Baus M, Medjugorac-Popovski M, Brown D, et al. In colchicine-treated rats, cellular distribution of AQP-1 in convoluted and straight proximal tubule segments is differently affected. Pflugers Arch 2000; 439:321-330.
81. Miura K, Inokawa M, Imura N. Effects of methylmercury and some metal ions on microtubule networks in mouse glioma cells and in vitro tubulin polymerization. Toxicol Appl Pharmacol 1984; 73:218-231.
82. Perrino BA, Chou IN. Role of calmodulin in cadmium-induced microtubule disassembly. Cell Biol Int Rep 1986; 10:565-573.
83. Lloyd SE, Pearce SH, Gunther W, et al. Idiopathic low molecular weight proteinuria associated with hypercalciuric nephrocalcinosis in Japanese children is due to mutations of the renal chloride channel (CLCN5). J Clin Invest 1997; 99:967-974.
84. Akuta N, Lloyd SE, Igarashi T, et al. Mutations of CLCN5 in Japanese children with idiopathic low molecular weight proteinuria, hypercalciuria and nephrocalcinosis. Kidney Int 1997; 52:911-916.
85. Reinhart SC, Norden AG, Lapsley M, et al. Characterization of carrier females and affected males with X-linked recessive nephrolithiasis. J Am Soc Nephrol 1995; 5:1451-1461.
86. Yu AS. Role of CLC-5 in the pathogenesis of hypercalciuria: recent insights from transgenic mouse models. Curr Opin Nephrol Hypertens 2001; 10:415-420.
87. Luyckx VA, Leclercq B, Dowland LK, Yu AS. Diet-dependent hypercalciuria in transgenic mice with reduced CLC5 chloride channel expression. Proc Natl Acad Sci U S A 1999; 96:12174-12179.
88. Leheste JR, Rolinski B, Vorum H, et al. Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 1999; 155:1361-1370.
89. Zhai XY, Nielsen R, Birn H, et al. Cubilin- and megalin-mediated uptake of albumin in cultured proximal tubule cells of opossum kidney. Kidney Int 2000; 58:1523-1533.
90. Norden AG, Scheinman SJ, Deschodt-Lanckman MM, et al. Tubular proteinuria defined by a study of Dent's (CLCN5 mutation) and other tubular diseases. Kidney Int 2000; 57:240-249.
91. Norden AG, Lapsley M, Lee PJ, et al. Glomerular protein sieving and implications for renal failure in Fanconi syndrome. Kidney Int 2001; 60:1885-1892.
92. Norden AG, Lapsley M, Igarashi T, et al. Urinary megalin deficiency implicates abnormal tubular endocytic function in Fanconi syndrome. J Am Soc Nephrol 2002; 13:125-133.
93. Xu D, Kozyraki R, Newman TC, Fyfe JC. Genetic evidence of an accessory activity required specifically for cubilin brush-border expression and intrinsic factor-cobalamin absorption. Blood 1999; 94:3604-3606.
94. Davis CG, Goldstein JL, Sudhof TC, et al. Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region. Nature 1987; 326:760-765.
95. Marshansky V, El Annan J, Yu AS, et al. Possible role of Arf6 small GTPase in pathogenesis of Dent's disease and Fanconi syndrome [Abstract]. FASEB J 2002; 16:A844.
96. +-ATPase. J Membr Biol 1992; 125:231-241.
97. Zeuzem S, Feick P, Zimmermann P, et al. Intravesicular acidification correlates with binding of ADP-ribosylation factor to microsomal membranes. Proc Natl Acad Sci U S A 1992; 89:6619-6623.
98. Clague MJ, Urbe S, Aniento F, Gruenberg J. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 1994; 269:21-24.
99. Aniento F, Gruenberg J. Membrane transport from early to late endosomes. Cold Spring Harb Symp Quant Biol 1995; 60:205-209.
100. Aniento F, Gu F, Parton RG, Gruenberg J. An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 1996; 133:29-41.
101. Gu F, Gruenberg J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J Biol Chem 2000; 275:8154-8160.
102. Blackstock WP, Weir MP. Proteomics: quantitative and physical mapping of cellular proteins. Trends Biotechnol 1999; 17:121-127.
103. Rowley A, Choudhary JS, Marzioch M, et al. Applications of protein mass spectrometry in cell biology. Methods 2000; 20:383-397.