Type of uromodulin mutation and allelic status influence onset and severity of uromodulinassociated kidney disease in mice

Human Molecular Genetics

Volumn 22, Issue 20, 2013, Pages 4148-4163

  Kemter, Elisabeth ^a   Prueckl, Petra ^a   Sklenak, Stefanie ^a   Rathkolb, Birgit ^a,b   Habermann, Felix A ^c   Hans, Wolfgang ^b   Gailus durner, Valérie ^b   Fuchs, Helmut ^b   De Angelis, Martin Hrabě ^b,d   Wolf, Eckhard ^a   Aigner, Bernhard ^a   Wanke, Ruediger ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c Histology and Embryology   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATIN; TAMM HORSFALL GLYCOPROTEIN; UREA; URIC ACID;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DISEASE SEVERITY; DISULFIDE BOND; ENDOPLASMIC RETICULUM; FEMALE; FIBROSING ALVEOLITIS; GENE MUTATION; HENLE LOOP; HUMAN; IN VIVO STUDY; INFLAMMATORY CELL; KIDNEY CELL; KIDNEY CONCENTRATING CAPACITY; KIDNEY DISEASE; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; UREA BLOOD LEVEL; URIC ACID URINE LEVEL; ZYGOSITY;

AGE OF ONSET; ALLELES; ANIMALS; BODY WEIGHT; CYSTATINS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GENETIC HETEROGENEITY; GENOTYPE; GOUT; HUMANS; HYPERURICEMIA; KIDNEY; KIDNEY DISEASES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, MUTANT STRAINS; PHENOTYPE; POINT MUTATION; UREA; URIC ACID; UROMODULIN;

EID: 84884733381     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt263     Document Type: Article

References (55)

1. Hart, T.C., Gorry, M.C., Hart, P.S., Woodard, A.S., Shihabi, Z., Sandhu, J., Shirts, B., Xu, L., Zhu, H., Barmada, M.M. et al. (2002) Mutations of the UMOD gene are responsible for medullary cystic kidney disease 2 and familial juvenile hyperuricaemic nephropathy. J. Med. Genet., 39, 882-892.
2. Scolari, F., Caridi, G., Rampoldi, L., Tardanico, R., Izzi, C., Pirulli, D., Amoroso, A., Casari, G. and Ghiggeri, G.M. (2004) Uromodulin storage diseases: clinical aspects and mechanisms. Am. J. Kidney Dis., 44, 987-999.
3. Zaucke, F., Boehnlein, J.M., Steffens, S., Polishchuk, R.S., Rampoldi, L., Fischer, A., Pasch, A., Boehm, C.W., Baasner, A., Attanasio,M.et al. (2010) Uromodulin is expressed in renal primary cilia and UMODmutations result in decreased ciliary uromodulin expression. Hum. Mol. Genet., 19, 1985-1997.
4. Rampoldi, L., Scolari, F., Amoroso, A., Ghiggeri, G. and Devuyst, O. (2011) The rediscovery of uromodulin (Tamm-Horsfall protein): from tubulointerstitial nephropathy to chronic kidney disease. Kidney Int., 80, 338-347.
5. Bollee, G., Dahan, K., Flamant, M., Moriniere, V., Pawtowski, A., Heidet, L., Lacombe, D., Devuyst, O., Pirson, Y., Antignac, C. et al. (2011) Phenotype and outcome in hereditary tubulointerstitial nephritis secondary to UMOD mutations. Clin. J. Am. Soc. Nephrol., 6, 2429-2438.
6. Rampoldi, L., Caridi, G., Santon, D., Boaretto, F., Bernascone, I., Lamorte, G., Tardanico, R., Dagnino, M., Colussi, G., Scolari, F. et al. (2003) Allelism of MCKD, FJHN and GCKD caused by impairment of uromodulin export dynamics. Hum. Mol. Genet., 12, 3369-3384.
7. Bleyer, A.J., Zivna, M. and Kmoch, S. (2011) Uromodulin-associated kidney disease. Nephron Clin. Pract., 118, c31-c36.
8. Nasr, S.H., Lucia, J.P., Galgano, S.J., Markowitz, G.S. and D'Agati, V.D. (2008) Uromodulin storage disease. Kidney Int., 73, 971-976.
9. Vylet'al, P., Kublova, M., Kalbacova, M., Hodanova, K., Baresova, V., Stiburkova, B., Sikora, J., Hulkova, H., Zivny, J., Majewski, J. et al. (2006) Alterations of uromodulin biology: a common denominator of the genetically heterogeneous FJHN/MCKD syndrome. Kidney Int., 70, 1155-1169.
10. Smith, G.D., Robinson, C., Stewart, A.P., Edwards, E.L., Karet, H.I., Norden, A.G., Sandford, R.N. and Karet Frankl, F.E. (2011) Characterization of a recurrent in-frame UMOD indel mutation causing late-onset autosomal dominant end-stage renal failure. Clin. J. Am. Soc. Nephrol., 6, 2766-2774.
11. Williams, S.E., Reed, A.A., Galvanovskis, J., Antignac, C., Goodship, T., Karet, F.E., Kotanko, P., Lhotta, K., Moriniere, V., Williams, P. et al. (2009) Uromodulin mutations causing familial juvenile hyperuricaemicnephropathy lead to protein maturation defects and retention in the endoplasmic reticulum. Hum. Mol. Genet., 18, 2963-2974.
12. Tamm, I. and Horsfall, F.L. Jr. (1950) Characterization and separation of an inhibitor of viral hemagglutination present in urine. Proc. Soc. Exp. Biol. Med., 74, 106-108.
13. Pennica, D., Kohr, W.J., Kuang, W.J., Glaister, D., Aggarwal, B.B., Chen, E.Y. and Goeddel, D.V. (1987) Identification of human uromodulin as the Tamm-Horsfall urinary glycoprotein. Science, 236, 83-88.
14. Hoyer, J.R., Sisson, S.P. and Vernier, R.L. (1979) Tamm-Horsfall glycoprotein: ultrastructural immunoperoxidase localization in rat kidney. Lab. Invest., 41, 168-173.
15. Van Rooijen, J.J., Voskamp, A.F., Kamerling, J.P. and Vliegenthart, J.F. (1999) Glycosylation sites and site-specific glycosylation in human Tamm-Horsfall glycoprotein. Glycobiology, 9, 21-30.
16. Serafini-Cessi, F., Malagolini, N. and Cavallone, D. (2003) Tamm-Horsfall glycoprotein: biology and clinical relevance. Am. J. Kidney Dis., 42, 658-676.
17. Bachmann, S., Mutig, K., Bates, J., Welker, P., Geist, B., Gross, V., Luft, F.C., Alenina, N., Bader, M., Thiele, B.J. et al. (2005) Renal effects of Tamm-Horsfall protein (uromodulin) deficiency in mice. Am. J. Physiol. Renal Physiol., 288, F559-F567.
18. Raffi, H., Bates, J.M., Laszik, Z. and Kumar, S. (2006) Tamm-Horsfall protein knockout mice do not develop medullary cystic kidney disease. Kidney Int., 69, 1914-1915.
19. Bernascone, I., Vavassori, S., Di Pentima, A., Santambrogio, S., Lamorte, G., Amoroso, A., Scolari, F., Ghiggeri, G.M., Casari, G., Polishchuk, R. et al. (2006) Defective intracellular trafficking of uromodulin mutant isoforms. Traffic, 7, 1567-1579.
20. Kemter, E., Rathkolb, B., Rozman, J., Hans, W., Schrewe, A., Landbrecht, C., Klaften, M., Ivandic, B., Fuchs, H., Gailus-Durner, V. et al. (2009) Novel missense mutation of uromodulin in mice causes renal dysfunction with alterations in urea handling, energy, and bone metabolism. Am. J. Physiol. Renal Physiol., 297, F1391-F1398.
21. Kottgen, A., Pattaro, C., Boger, C.A., Fuchsberger, C., Olden, M., Glazer, N.L., Parsa, A., Gao, X., Yang, Q., Smith, A.V. et al. (2010) New loci associated with kidney function and chronic kidney disease. Nat. Genet., 42, 376-384.
22. Gudbjartsson, D.F., Holm, H., Indridason, O.S., Thorleifsson, G., Edvardsson, V., Sulem, P., de Vegt, F., d'Ancona, F.C., den Heijer, M., Wetzels, J.F. et al. (2010) Association of variants at UMOD with chronic kidney disease and kidney stones-role of age and comorbid diseases. PLoS genetics, 6, e1001039.
23. Kottgen, A., Glazer, N.L., Dehghan, A., Hwang, S.J., Katz, R., Li, M., Yang, Q., Gudnason, V., Launer, L.J., Harris, T.B. et al. (2009) Multiple loci associated with indices of renal function and chronic kidney disease. Nat. Genet., 41, 712-717.
24. Han, J., Liu, Y., Rao, F., Nievergelt, C.M., O'Connor, D.T., Wang, X., Liu, L., Bu, D., Liang, Y., Wang, F. et al. (2013) Common genetic variants of the human uromodulin gene regulate transcription and predict plasma uric acid levels. Kidney Int., 83, 733-740.
25. Aigner, B., Rathkolb, B., Herbach, N., Kemter, E., Schessl, C., Klaften, M., Klempt, M., Hrabe de Angelis, M., Wanke, R. and Wolf, E. (2007) Screening for increased plasma urea levels in a large-scale ENU mouse mutagenesis project reveals kidney disease models. Am. J. Physiol. Renal Physiol., 292, F1560-F1567.
26. Keays, D.A., Clark, T.G., Campbell, T.G., Broxholme, J. and Valdar, W. (2007) Estimating the number of coding mutations in genotypic and phenotypic driven N-ethyl-N-nitrosourea (ENU) screens: revisited. Mamm. Genome, 18, 123-124.
27. Yang, B. and Bankir, L. (2005) Urea and urine concentrating ability: new insights from studies in mice. Am. J. Physiol. Renal Physiol., 288, F881-F896.
28. Martensson, J., Martling, C.R. and Bell, M. (2012) Novel biomarkers of acute kidney injury and failure: clinical applicability. Br. J. Anaesth., 109, 843-850.
29. Gillece, P., Luz, J.M., Lennarz, W.J., de La Cruz, F.J. and Romisch, K. (1999) Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J. Cell. Biol., 147, 1443-1456.
30. Inagi, R. (2009) Endoplasmic reticulum stress in the kidney as a novel mediator of kidney injury. Nephron Exp. Nephrol., 112, e1-e9.
31. Guerriero, C.J. and Brodsky, J.L. (2012) The delicate balance between secreted protein folding and endoplasmic reticulum-associated degradation in human physiology. Physiol. Rev., 92, 537-576.
32. Vembar, S.S. and Brodsky, J.L. (2008) One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol., 9, 944-957.
33. Jennings, P., Aydin, S., Kotanko, P., Lechner, J., Lhotta, K., Williams, S., Thakker, R.V. and Pfaller, W. (2007) Membrane targeting and secretion of mutant uromodulin in familial juvenile hyperuricemic nephropathy. J. Am. Soc. Nephrol., 18, 264-273.
34. Bleyer, A.J., Hart, T.C., Shihabi, Z., Robins, V. and Hoyer, J.R. (2004) Mutations in the uromodulin gene decrease urinary excretion of Tamm-Horsfall protein. Kidney Int., 66, 974-977.
35. Wolf, M.T., Beck, B.B., Zaucke, F., Kunze, A., Misselwitz, J., Ruley, J., Ronda, T., Fischer, A., Eifinger, F., Licht, C. et al. (2007) The Uromodulin C744G mutation causes MCKD2 and FJHN in children and adults and may be due to a possible founder effect. Kidney Int., 71, 574-581.
36. Waldherr, R., Lennert, T., Weber, H.P., Fodisch, H.J. and Scharer, K. (1982) The nephronophthisis complex. A clinicopathologic study in children. Virchows Arch. A. Pathol. Anat. Histol., 394, 235-254.
37. Gusmano, R., Caridi, G., Marini, M., Perfumo, F., Ghiggeri, G.M., Piaggio, G., Ceccherini, I. and Seri, M. (2002) Glomerulocystic kidney disease in a family. Nephrol. Dial. Transplant., 17, 813-818.
38. Wolf, M.T., Mucha, B.E., Attanasio, M., Zalewski, I., Karle, S.M., Neumann, H.P., Rahman, N., Bader, B., Baldamus, C.A., Otto, E. et al. (2003) Mutations of the Uromodulin gene inMCKDtype 2 patients cluster in exon 4, which encodes three EGF-like domains. Kidney Int., 64, 1580-1587.
39. Dahan, K., Devuyst, O., Smaers, M., Vertommen, D., Loute, G., Poux, J.M., Viron, B., Jacquot, C., Gagnadoux, M.F., Chauveau, D. et al. (2003) A cluster of mutations in the UMOD gene causes familial juvenile hyperuricemic nephropathy with abnormal expression of uromodulin. J. Am. Soc. Nephrol., 14, 2883-2893.
40. Benetti, E., Caridi, G., Vella, M.D., Rampoldi, L., Ghiggeri, G.M., Artifoni, L. and Murer, L. (2009) Immature renal structures associated with a novel UMOD sequence variant. Am. J. Kidney Dis., 53, 327-331.
41. Kimura, K., Jin, H., Ogawa, M. and Aoe, T. (2008) Dysfunction of the ER chaperone BiP accelerates the renal tubular injury. Biochem. Biophys. Res. Commun., 366, 1048-1053.
42. Prunotto, M., Budd, D.C., Gabbiani, G., Meier, M., Formentini, I., Hartmann, G., Pomposiello, S. and Moll, S. (2012) Epithelial-mesenchymal crosstalk alteration in kidney fibrosis. J. Pathol., 228, 131-147.
43. Bohle, A., Mackensen-Haen, S. and von Gise, H. (1987) Significance of tubulointerstitial changes in the renal cortex for the excretory function and concentration ability of the kidney: a morphometric contribution. Am. J. Nephrol., 7, 421-433.
44. Choi, H.K., Mount, D.B. and Reginato, A.M. (2005) Pathogenesis of gout. Ann. Intern. Med., 143, 499-516.
45. Rezende-Lima, W., Parreira, K.S., Garcia-Gonzalez, M., Riveira, E., Banet, J.F. and Lens, X.M. (2004) Homozygosity for uromodulin disorders: FJHN and MCKD-type 2. Kidney Int., 66, 558-563.
46. Takiue, Y., Hosoyamada, M., Yokoo, T., Kimura, M., Ochiai, M., Kaneko, K., Ichida, K., Hosoya, T. and Shibasaki, T. (2008) Production and characterization of transgenic mice harboring mutant human UMOD gene. Nucleosides Nucleotides Nucleic Acids, 27, 596-600.
47. Bernascone, I., Janas, S., Ikehata, M., Trudu, M., Corbelli, A., Schaeffer, C., Rastaldi, M.P., Devuyst, O. and Rampoldi, L. (2010) A transgenic mouse model for uromodulin-associated kidney diseases shows specific tubulo-interstitial damage, urinary concentrating defect and renal failure. Hum. Mol. Genet., 19, 2998-3010.
48. Rathkolb, B., Decker, T., Fuchs, E., Soewarto, D., Fella, C., Heffner, S., Pargent, W., Wanke, R., Balling, R., Hrabe de Angelis, M. et al. (2000) The clinical-chemical screen in the Munich ENU Mouse Mutagenesis Project: screening for clinically relevant phenotypes.Mamm.Genome, 11, 543-546.
49. Gailus-Durner, V., Fuchs, H., Adler, T., Aguilar Pimentel, A., Becker, L., Bolle, I., Calzada-Wack, J., Dalke, C., Ehrhardt, N., Ferwagner, B. et al. (2009) Systemic first-line phenotyping. Methods Mol. Biol., 530, 463-509.
50. Liu, Y., El-Achkar, T.M. and Wu, X.R. (2012) Tamm-Horsfall protein regulates circulating and renal cytokines by affecting glomerular filtration rate and acting as a urinary cytokine trap. J. Biol. Chem, 287, 16365-16378.
51. Kemter, E., Rathkolb, B., Bankir, L., Schrewe, A., Hans, W., Landbrecht, C., Klaften, M., Ivandic, B., Fuchs, H., Gailus-Durner, V. et al. (2010) Mutation of the Na+-K+-2Cl- cotransporter NKCC2 in mice is associated with severe polyuria and a urea-selective concentrating defect without hyperreninemia. Am. J. Physiol. Renal Physiol., 298, F1405-F1415. 4162 Human Molecular Genetics, 2013, Vol. 22, No. 20
52. Weibel, E.R. (1979) Stereological Methods. I. Practical Methods for Biological Morphometry. Academic Press, London.
53. Klose R., Kemter, E., Bedke, T., Bittmann, I., Kelsser, B., Endres, R., Pfeffer, K., Schwinzer, R. and Wolf, E. (2005) Expression of biologically active human TRAIL in transgenic pigs. Transplantation, 80, 222-230
54. Schaffer, P., Gombos, E., Meichelbeck, K., Kiss, A., Hart, P.S. and Bleyer, A.J. (2010) Childhood course of renal insufficiency in a family with a uromodulin gene mutation. Pediatr. Nephrol., 25, 1355-1360.
55. Bleyer, A.J., Trachtman, H., Sandhu, J., Gorry, M.C. and Hart, T.C. (2003) Renal manifestations of a mutation in the uromodulin (Tamm Horsfall protein) gene. Am. J. Kidney Dis., 42, E20-E26.