Toward understanding renal fanconi syndrome: Step by step advances through experimental models

Contributions to Nephrology

Volumn 169, Issue , 2011, Pages 247-261

  Sirac, Christophe ^a   Bridoux, Frank ^a,b   Essig, Marie ^c   Devuyst, Olivier ^d   Touchard, Guy ^b   Cogné, Michel ^a  

^a UNIVERSITY OF LIMOGES   (France)

^b University of Poitiers   (France)

^c DUPUYTREN UNIVERSITY HOSPITAL   (France)

^d UNIVERSITY OF LOUVAIN MEDICAL SCHOOL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); MEGALIN;

ANIMAL; ARTICLE; DISEASE MODEL; ENDOCYTOSIS; FANCONI RENOTUBULAR SYNDROME; GENETICS; HUMAN; KIDNEY PROXIMAL TUBULE; MOUSE; MOUSE MUTANT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; ENDOCYTOSIS; FANCONI SYNDROME; HUMANS; KIDNEY TUBULES, PROXIMAL; LDL-RECEPTOR RELATED PROTEIN 2; MICE; MICE, KNOCKOUT; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 79551471490     PISSN: 03025144     EISSN: None     Source Type: Book Series    
DOI: 10.1159/000313962     Document Type: Article

References (100)

1. Jacobson HR, Seldin DW: Proximal tubular reabsorption and its regulation. Annu Rev Pharmacol Toxicol 1977;17:623-646.
2. Gonick HC: Pathophysiology of human proximal tubular transport defects. Klin Wochenschr 1982;60:1201-1211.
3. Laski ME, Kurtzman NA: The renal adenosine triphosphatases: functional integration and clinical significance. Miner Electrolyte Metab 1996;22:410-422.
4. Maack T, Johnson V, Kau ST, Figueiredo J, Sigulem D: Renal filtration, transport, and metabolism of low- molecular- weight proteins: a review. Kidney Int 1979;16:251-270.
5. Marshansky V, Bourgoin S, Londono I, Bendayan M, Maranda B, Vinay P: Receptor- mediated endocytosis in kidney proximal tubules: recent advances and hypothesis. Electrophoresis 1997;18:2661-2676.
6. Christensen EI, Birn H, Verroust P, Moestrup SK: Membrane receptors for endocytosis in the renal proximal tubule. Int Rev Cytol 1998;180:237-284. (Pubitemid 28122166)
7. Christensen EI, Verroust PJ, Nielsen R: Receptor- mediated endocytosis in renal proximal tubule. Pflugers Arch 2009;458:1039-1048.
8. Grunfeld JP, Niaudet P, Rotig A: Renal involvement in mitochondrial cytopathies. Nephrol Dial Transplant 1996;11:760-761. (Pubitemid 26148238)
9. Lloyd SE, Pearce SH, Fisher SE, Steinmeyer K, Schwappach B, Scheinman SJ, Harding B, Bolino A, Devoto M, Goodyer P, Rigden SP, Wrong O, Jentsch TJ, Craig IW, Thakker RV: A common molecular basis for three inherited kidney stone diseases. Nature 1996;379:445-449.
10. Thakker RV: Pathogenesis of Dents disease and related syndromes of X- linked nephrolithiasis. Kidney Int 2000;57:787-793.
11. Lowe CU, Terrey M, Mac LE: Organicaciduria, decreased renal ammonia production, hydrophthalmos, and mental retardation; a clinical entity. AMA Am J Dis Child 1952;83:164-184.
12. Lowe M: Structure and function of the Lowe syndrome protein OCRL1. Traffic 2005;6:711-719.
13. Gahl WA, Bashan N, Tietze F, Bernardini I, Schulman JD: Cystine transport is defective in isolated leukocyte lysosomes from patients with cystinosis. Science 1982;217:1263-1265.
14. Baum M: The Fanconi syndrome of cystinosis: insights into the pathophysiology. Pediatr Nephrol 1998;12:492-497.
15. Kramer HJ, Gonick HC: Experimental Fanconi syndrome. I. Effect of maleic acid on renal cortical Na- K- ATPase activity and ATP levels. J Lab Clin Med 1970;76:799-808.
16. Gonick H, Indraprasit S, Neustein H, Rosen V: Cadmium- induced experimental Fanconi syndrome. Curr Probl Clin Biochem 1975;4:111-118.
17. Kintzel PE: Anticancer druginduced kidney disorders. Drug Saf 2001;24:19-38.
18. Gonick HC: Nephrotoxicity of cadmium & lead. Indian J Med Res 2008;128:335-352.
19. Maldonado JE, Velosa JA, Kyle RA, Wagoner RD, Holley KE, Salassa RM: Fanconi syndrome in adults. A manifestation of a latent form of myeloma. Am J Med 1975;58:354-364.
20. Messiaen T, Deret S, Mougenot B, Bridoux F, Dequiedt P, Dion JJ, Makdassi R, Meeus F, Pourrat J, Touchard G, Vanhille P, Zaoui P, Aucouturier P, Ronco PM: Adult Fanconi syndrome secondary to light chain gammopathy. Clinicopathologic heterogeneity and unusual features in 11 patients. Medicine (Baltimore) 2000;79:135-154.
21. Leheste JR, Rolinski B, Vorum H, Hilpert J, Nykjaer A, Jacobsen C, Aucouturier P, Moskaug JO, Otto A, Christensen EI, Willnow TE: Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 1999;155:1361-1370.
22. Piwon N, Gunther W, Schwake M, Bosl MR, Jentsch TJ: ClC- 5 Cl- - channel disruption impairs endocytosis in a mouse model for Dents disease. Nature 2000;408:369-373.
23. Wang SS, Devuyst O, Courtoy PJ, Wang XT, Wang H, Wang Y, Thakker RV, Guggino S, Guggino WB: Mice lacking renal chloride channel, CLC- 5, are a model for Dents disease, a nephrolithiasis disorder associated with defective receptor- mediated endocytosis. Hum Mol Genet 2000;9:2937-2945.
24. Herak- Kramberger CM, Brown D, Sabolic I: Cadmium inhibits vacuolar H(+)- ATPase and endocytosis in rat kidney cortex. Kidney Int 1998;53:1713-1726.
25. Rocca A, Khamlichi AA, Touchard G, Mougenot B, Ronco P, Denoroy L, Deret S, Preudhomme JL, Aucouturier P, Cogne M: Sequences of V kappa L subgroup light chains in Fanconis syndrome. Light chain V region gene usage restriction and peculiarities in myeloma- associated Fanconis syndrome. J Immunol 1995;155:3245-3252.
26. Stowe HD, Wilson M, Goyer RA: Clinical and morphologic effects of oral cadmium toxicity in rabbits. Arch Pathol 1972;94:389-405.
27. Yanase M, Orita Y, Okada N, Nakanishi T, Horio M, Ando A, Abe H: Decreased Na+- gradientdependent D- glucose transport in brush- border membrane vesicles from rabbits with experimental Fanconi syndrome. Biochim Biophys Acta 1983;733:95-101.
28. Khalil- Manesh F, Gonick HC, Cohen AH, Alinovi R, Bergamaschi E, Mutti A, Rosen VJ: Experimental model of lead nephropathy. I. Continuous highdose lead administration. Kidney Int 1992;41:1192-1203.
29. Kramer HJ, Gonick HC, Lu E: In vitro inhibition of Na- K- ATPase by trace metals: relation to renal and cardiovascular damage. Nephron 1986;44:329-336.
30. Foreman JW, Bowring MA, Lee J, States B, Segal S: Effect of cystine dimethylester on renal solute handling and isolated renal tubule transport in the rat: a new model of the Fanconi syndrome. Metabolism 1987;36:1185-1191.
31. Guan S, el- Dahr S, Dipp S, Batuman V: Inhibition of Na- K- ATPase activity and gene expression by a myeloma light chain in proximal tubule cells. J Investig Med 1999;47:496-501.
32. Thevenod F, Friedmann JM: Cadmium- mediated oxidative stress in kidney proximal tubule cells induces degradation of Na+/K(+)- ATPase through proteasomal and endo- /lysosomal proteolytic pathways. FASEB J 1999;13:1751-1761.
33. Conner SD, Schmid SL: Regulated portals of entry into the cell. Nature 2003;422:37-44.
34. Christensen EI, Verroust PJ: Megalin and cubilin, role in proximal tubule function and during development. Pediatr Nephrol 2002;17:993 999.
35. Gekle M: Renal tubule albumin transport. Annu Rev Physiol 2005;67:573 594.
36. Faundez V, Hartzell HC: Intracellular chloride channels: determinants of function in the endosomal pathway. Sci STKE 2004;2004: re8.
37. 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. Bio phys J 1991;59:1208 1217.
38. Jentsch TJ: CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit Rev Biochem Mol Biol 2008;43:3 36.
39. Moriyama Y, Nelson N: The purified ATPase from chromaffin granule membranes is an aniondependent proton pump. J Biol Chem 1987;262:9175 9180.
40. Willnow TE, Hilpert J, Armstrong SA, Rohlmann A, Hammer RE, Burns DK, Herz J: Defective forebrain development in mice lacking gp330/ megalin. Proc Natl Acad Sci USA 1996;93:8460 8464.
41. Christensen EI, Birn H: Megalin and cubilin: synergistic endocytic receptors in renal proximal tubule. Am J Physiol Renal Physiol 2001;280:F562 F573.
42. Gburek J, Verroust PJ, Willnow TE, Fyfe JC, Nowacki W, Jacobsen C, Moestrup SK, Christensen EI: Megalin and cubilin are endocytic receptors involved in renal clearance of hemoglobin. J Am Soc Nephrol 2002;13:423 430.
43. Kozyraki R, Fyfe J, Verroust PJ, Jacobsen C, Dautry- Varsat A, Gburek J, Willnow TE, Christensen EI, Moestrup SK: Megalin- dep endent 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.
44. Sousa MM, Norden AG, Jacobsen C, Willnow TE, Christensen EI, Thakker RV, Verroust PJ, Moestrup SK, Saraiva MJ: Evidence for the role of megalin in renal uptake of transthyretin. J Biol Chem 2000;275:38176 38181.
45. Christensen EI, Moskaug JO, Vorum H, Jacobsen C, Gundersen TE, Nykjaer A, Blomhoff R, Willnow TE, Moestrup SK: Evidence for an essential role of megalin in transepithelial transport of retinol. J Am Soc Nephrol 1999;10:685 695.
46. Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, Melsen F, Christensen EI, Willnow TE: An endocytic pathway essential for renal uptake and activation of the steroid 25- (OH) vitamin D3. Cell 1999;96:507 515.
47. Raila J, Willnow TE, Schweigert FJ: Megalin- mediated reuptake of retinol in the kidneys of mice is essential for vitamin A homeostasis. J Nutr 2005;135:2512 2516.
48. Bachmann S, Schlichting U, Geist B, Mutig K, Petsch T, Bacic D, Wagner CA, Kaissling B, Biber J, Murer H, Willnow TE: 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.
49. Nykjaer A, Fyfe JC, Kozyraki R, Leheste JR, Jacobsen C, Nielsen MS, Verroust PJ, Aminoff M, de la Chapelle A, Moestrup SK, Ray R, Gliemann J, Willnow TE, Christensen EI: Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D(3). Proc Natl Acad Sci USA 2001;98:13895 13900.
50. Birn H, Fyfe JC, Jacobsen C, Mounier F, Verroust PJ, Orskov H, Willnow TE, Moestrup SK, Christensen EI: Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J Clin Invest 2000;105:1353 1361.
51. Aminoff M, Carter JE, Chadwick RB, Johnson C, Grasbeck R, Abdelaal MA, Broch H, Jenner LB, Verroust PJ, Moestrup SK, de la Chapelle A, Krahe R: Mutations in CUBN, encoding the intrinsic factor- vitamin B12 receptor, cubilin, cause hereditary megaloblastic anaemia 1. Nat Genet 1999;21:309 313.
52. Wahlstedt- Froberg V, Pettersson T, Aminoff M, Dugue B, Grasbeck R: Proteinuria in cubilin- deficient patients with selective vitamin B12 malabsorption. Pediatr Nephrol 2003;18:417 421.
53. Devuyst O, Jouret F, Auzanneau C, Courtoy PJ: Chloride channels and endocytosis: new insights from Dents disease and ClC- 5 knockout mice. Nephron Physiol 2005;99:p69 p73.
54. Devuyst O, Pirson Y: Genetics of hypercalciuric stone forming diseases. Kidney Int 2007;72:1065 1072.
55. Christensen EI, Devuyst O, Dom G, Nielsen R, Van der Smissen P, Verroust P, Leruth M, Guggino WB, Courtoy PJ: 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.
56. Mellman I: The importance of being acid: the role of acidification in intracellular membrane traffic. J Exp Biol 1992;172:39 45.
57. Hurtado- Lorenzo A, Skinner M, El Annan J, Futai M, Sun- Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V: V- ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 2006;8:124 136.
58. Pontoglio M, Barra J, Hadchouel M, Doyen A, Kress C, Bach JP, Babinet C, Yaniv M: Hepatocyte nuclear factor 1 inactivation results in hepatic dysfunction, phenylketonuria, and renal Fanconi syndrome. Cell 1996; 84:575 585.
59. Cheret C, Doyen A, Yaniv M, Pontoglio M: Hepatocyte nuclear factor 1 alpha controls renal expression of the Npt1- Npt4 anionic transporter locus. J Mol Biol 2002;322:929 941.
60. Pontoglio M, Prie D, Cheret C, Doyen A, Leroy C, Froguel P, Velho G, Yaniv M, Friedlander G: HNF1alpha controls renal glucose reabsorption in mouse and man. EMBO Rep 2000;1:359 365.
61. Janne PA, Suchy SF, Bernard D, MacDonald M, Crawley J, Grinberg A, Wynshaw- Boris A, Westphal H, Nussbaum RL: Functional overlap between murine Inpp5b and Ocrl1 may explain why deficiency of the murine ortholog for OCRL1 does not cause Lowe syndrome in mice. J Clin Invest 1998;101:2042 2053.
62. Cherqui S, Sevin C, Hamard G, Kalatzis V, Sich M, Pequignot MO, Gogat K, Abitbol M, Broyer M, Gubler MC, Antignac C: Intralysosomal cystine accumulation in mice lacking cystinosin, the protein defective in cystinosis. Mol Cell Biol 2002;22:7622-7632.
63. Nevo N, Chol M, Bailleux A, Kalatzis V, Morisset L, Devuyst O, Gubler MC, Antignac C: Renal phenotype of the cystinosis mouse model is dependent upon genetic background. Nephrol Dial Transplant 2010;25:1059-1066.
64. Elsea SH, Lucas RE: The mousetrap: what we can learn when the mouse model does not mimic the human disease. ILAR J 2002;43:66-79.
65. Ronco PM, Mougenot B, Moulin B, Bouiller M, Messiaen T, Aucouturier P: Adult Fanconis syndrome due to monoclonal immunoglobulin light chains: an underdiagnosed disease with unexpected clinical and pathologic heterogeneity in G; in Touchard PA, Hermine O, Ronco P (eds): Monoclonal Gammapathies and the Kidney. Dordrecht, Kluwer Academic Publishers, 2003, pp 75- 86.
66. Engle RL Jr, Wallis LA: Multiple myeloma and the adult Fanconi syndrome. I. Report of a case with crystal- like deposits in the tumor cells and in the epithelial cells of the kidney. Am J Med 1957;22:5-23.
67. Sirota JH, Hamerman D: Renal function studies in a adult subject with the Fanconi syndrome. Am J Med 1954;16:138-152.
68. Thorner PS, Bedard YC, Fernandes BJ: Lambda- light- chain nephropathy with Fanconis syndrome. Arch Pathol Lab Med 1983;107:654-657.
69. Orfila C, Lepert JC, Modesto A, Bernadet P, Suc JM: Fanconis syndrome, kappa light- chain myeloma, non- amyloid fibrils and cytoplasmic crystals in renal tubular epithelium. Am J Nephrol 1991;11:345-349.
70. Truong LD, Mawad J, Cagle P, Mattioli C: Cytoplasmic crystals in multiple myeloma- associated Fanconis syndrome. A morphological study including immunoelectron microscopy. Arch Pathol Lab Med 1989;113: 781-785.
71. Lacy MQ, Gertz MA: Acquired Fanconis syndrome associated with monoclonal gammopathies. Hematol Oncol Clin North Am 1999;13:1273-1280.
72. Bridoux F, Sirac C, Hugue V, Decourt C, Thierry A, Quellard N, Abou- Ayache R, Goujon JM, Cogne M, Touchard G: Fanconis syndrome induced by a monoclonal Vkappa3 light chain in Waldenstroms macroglobulinemia. Am J Kidney Dis 2005;45:749-757.
73. Decourt C, Bridoux F, Touchard G, Cogne M: A monoclonal V kappa l light chain responsible for incomplete proximal tubulopathy. Am J Kidney Dis 2003;41:497-504.
74. Bate KL, Clouston D, Packham D, Ratnaike S, Ebeling PR: Lambda light chain induced nephropathy: a rare cause of the Fanconi syndrome and severe osteomalacia. Am J Kidney Dis 1998;32:E3.
75. Isobe T, Kametani F, Shinoda T: V- domain deposition of lambda Bence Jones protein in the renal tubular epithelial cells in a patient with the adult Fanconi syndrome with myeloma. Amyloid 1998;5:117-120.
76. Aucouturier P, Bauwens M, Khamlichi AA, Denoroy L, Spinelli S, Touchard G, Preudhomme JL, Cogne M: Monoclonal Ig L chain and L chain V domain fragment crystallization in myeloma- associated Fanconis syndrome. J Immunol 1993;150:3561-3568.
77. Decourt C, Rocca A, Bridoux F, Vrtovsnik F, Preudhomme JL, Cogne M, Touchard G: Mutational analysis in murine models for myelomaassociated Fanconis syndrome or cast myeloma nephropathy. Blood 1999;94:3559-3566.
78. Deret S, Denoroy L, Lamarine M, Vidal R, Mougenot B, Frangione B, Stevens FJ, Ronco PM, Aucouturier P: Kappa light chain- associated Fanconis syndrome: molecular analysis of monoclonal immunoglobulin light chains from patients with and without intracellular crystals. Protein Eng 1999;12:363-369.
79. Leboulleux M, Lelongt B, Mougenot B, Touchard G, Makdassi R, Rocca A, Noel LH, Ronco PM, Aucouturier P: Protease resistance and binding of Ig light chains in myelomaassociated tubulopathies. Kidney Int 1995;48:72-79.
80. El Hamel C TA, Trouillas P, Bridoux F, Carrion C, Quellard N, Goujon JM, Aldigier C, Gombert JM, Cogne M, Touchard G: Crystal- storing histiocytosis with renal Fanconi syndrome: pathological and molecular characteristics compared with classical myeloma- associated Fanconi syndrome. Nephrol Dial Transplant 2010, E- pub ahead of print.
81. Klassen RB, Allen PL, Batuman V, Crenshaw K, Hammond TG: Light chains are a ligand for megalin. J Appl Physiol 2005;98:257-263.
82. Plans V, Rickheit G, Jentsch TJ: Physiological roles of CLC Cl(- )/H (+) exchangers in renal proximal tubules. Pflugers Arch 2009;458:23-37.
83. Batuman V, Sastrasinh M, Sastrasinh S: Light chain effects on alanine and glucose uptake by renal brush border membranes. Kidney Int 1986;30:662-665.
84. Batuman V, Dreisbach AW, Cyran J: Light- chain binding sites on renal brush- border membranes. Am J Physiol 1990;258:F1259-F1265.
85. Batuman V, Guan S: Receptormediated endocytosis of immunoglobulin light chains by renal proximal tubule cells. Am J Physiol 1997;272:F521-F530.
86. Batuman V, Verroust PJ, Navar GL, Kaysen JH, Goda FO, Campbell WC, Simon E, Pontillon F, Lyles M, Bruno J, Hammond TG: Myeloma light chains are ligands for cubilin (gp280). Am J Physiol 1998;275:F246-F254.
87. Sanders PW, Herrera GA, Galla JH: Human Bence Jones protein toxicity in rat proximal tubule epithelium in vivo. Kidney Int 1987;32:851-861.
88. Sanders PW, Herrera GA, Chen A, Booker BB, Galla JH: Differential nephrotoxicity of low molecular weight proteins including Bence Jones proteins in the perfused rat nephron in vivo. J Clin Invest 1988;82:2086-2096.
89. 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.
90. Sengul S, Zwizinski C, Simon EE, Kapasi A, Singhal PC, Batuman V: Endocytosis of light chains induces cytokines through activation of NFkappaB in human proximal tubule cells. Kidney Int 2002;62:1977-1988.
91. Wang PX, Sanders PW: Immunoglobulin light chains generate hydrogen peroxide. J Am Soc Nephrol 2007;18:1239-1245.
92. Khamlichi AA, Rocca A, Touchard G, Aucouturier P, Preudhomme JL, Cogne M: Role of light chain variable region in mye loma with light chain deposition disease: evidence from an experimental model. Blood 1995;86:3655-3659.
93. Chauveau C, Decourt C, Cogne M: Insertion of the IgH locus 3 regulatory palindrome in expression vectors warrants sure and efficient expression in stable B cell transfectants. Gene 1998;222:279-285.
94. Khamlichi AA, Rocca A, Cogne M: The effect of intron sequences on expression levels of Ig cDNAs. Gene 1994;150:387-390.
95. Sirac C, Bridoux F, Carrion C, Devuyst O, Fernandez B, Goujon JM, El Hamel C, Aldigier JC, Touchard G, Cogne M: Role of the monoclonal kappa chain V domain and reversibility of renal damage in a transgenic model of acquired Fanconi syndrome. Blood 2006;108:536-543.
96. Bernard AM, Thielemans NO, Lauwerys RR: Urinary protein 1 or Clara cell protein: a new sensitive marker of proximal tubular dysfunction. Kidney Int Suppl 1994;47:S34-S37.
97. Batuman V, Guan S, ODonovan R, Puschett JB: Effect of myeloma light chains on pho sphate and glucose transport in renal pro ximal tubule cells. Ren Physiol Biochem 1994;17:294-300.
98. Nicastri AL, Brandao de Almeida Prado MJ, Sesso A, Brandao de Almeida Prado EB: Defective proximal tubule lysosomal acidification by Bence Jones proteins. An immunoelectron microscopy study. Exp Nephrol 1998;6:514-521.
99. Ma CX, Lacy MQ, Rompala JF, Dispenzieri A, Rajkumar SV, Greipp PR, Fonseca R, Kyle RA, Gertz MA: Acquired Fanconi syndrome is an indolent disorder in the absence of overt multiple myeloma. Blood 2004;104:40-42.
100. Devuyst O, Guggino WB: Chloride channels in the kidney: lessons learned from knockout animals. Am J Physiol Renal Physiol 2002; 283:F1176-F1191.