A disease-causing mutation illuminates the protein membrane topology of the kidney-expressed prohibitin homology (PHB) domain protein podocin

Journal of Biological Chemistry

Volumn 289, Issue 16, 2014, Pages 11262-11271

  Schurek, Eva Maria ^a   Völker, Linus A ^a   Tax, Judit ^a   Lamkemeyer, Tobias ^b   Rinschen, Markus M ^a   Ungrue, Denise ^b   Kratz III, John E ^c   Sirianant, Lalida ^d   Kunzelmann, Karl ^d   Chalfie, Martin ^d   Schermer, Bernhard ^a,b   Benzing, Thomas ^a,b   Höhne, Martin ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TOPOLOGY;

HAIRPIN-LIKE; KIDNEY DISEASE; MEMBRANE TOPOLOGY; PODOCIN; PROLINE RESIDUES; PROTEIN MEMBRANE; STOMATIN;

PROTEINS;

CHOLESTEROL; PODOCIN; PROLINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6;

ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; DEGLYCOSYLATION; GENETIC SCREENING; GENETIC TRANSFECTION; HEK293 CELL LINE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; KIDNEY DISEASE; LIPID RAFT; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEMBRANE STRUCTURE; MUTANT; MUTATION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; VOLTAGE CLAMP TECHNIQUE; WILD TYPE;

CAENORHABDITIS ELEGANS; CHOLESTEROL-BINDING PROTEIN; GLYCOSYLATION; LIPID RAFT; MEMBRANE TOPOLOGY; PHB DOMAIN; PODOCIN; PROTEIN CONFORMATION; STEROID-RESISTANT NEPHROTIC SYNDROME; STOMATIN FAMILY PROTEINS;

AMINO ACID SUBSTITUTION; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; CELL MEMBRANE; CHOLESTEROL; GLOMERULAR FILTRATION BARRIER; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MICE; MUTATION, MISSENSE; NEPHROTIC SYNDROME; PROTEIN STRUCTURE, TERTIARY;

EID: 84898961246     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.521773     Document Type: Article

References (38)

1. Hinkes, B. G., Mucha, B., Vlangos, C. N., Gbadegesin, R., Liu, J., Hasselbacher, K., Hangan, D., Ozaltin, F., Zenker, M., and Hildebrandt, F. (2007) Nephrotic syndrome in the first year of life. Two thirds of cases are caused by mutations in 4 genes (NPHS1, NPHS2, WT1, and LAMB2). Pediatrics 119, e907-e919
2. Boute, N., Gribouval, O., Roselli, S., Benessy, F., Lee, H., Fuchshuber, A., Dahan, K., Gubler, M.-C., Niaudet, P., and Antignac, C. (2000) NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat. Genet. 24, 349-354
3. Weber, S., Gribouval, O., Esquivel, E. L., Morinière, V., Tête, M.-J., Legendre, C., Niaudet, P., and Antignac, C. (2004) NPHS2 mutation analysis shows genetic heterogeneity of steroid-resistant nephrotic syndrome and lowpost-transplant recurrence. Kidney Int. 66, 571-579
4. Ozer, E. A., Aksu, N., Erdogan, H., Yavascan, O., Kara, O., Gribouval, O., Gubler, M.-C., and Antignac, C. (2004) A novel NPHS2 gene mutation in Turkish children with familial steroid-resistant nephrotic syndrome. Nephrology 9, 310-312
5. Caridi, G., Perfumo, F., and Ghiggeri, G. M. (2005) NPHS2 (Podocin) mutations in nephrotic syndrome. Clinical spectrum and fine mechanisms. Pediatr. Res. 57, 54R-61R
6. Haraldsson, B., Nyström, J., and Deen, W. M. (2008) Properties of the glomerular barrier and mechanisms of proteinuria. Physiol. Rev. 88, 451-487
7. Pavenstädt, H., Kriz, W., and Kretzler, M. (2003) Cell biology of the glomerular podocyte. Physiol. Rev. 83, 253-307
8. Benzing, T. (2004) Signaling at the slit diaphragm. J. Am. Soc. Nephrol. 15, 1382-1391
9. Kestilä, M., Lenkkeri, U., Männikkö, M., Lamerdin, J., McCready, P., Putaala, H., Ruotsalainen, V., Morita, T., Nissinen, M., Herva, R., Kashtan, C. E., Peltonen, L., Holmberg, C., Olsen, A., and Tryggvason, K. (1998) Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol. Cell 1, 575-582
10. Schwarz, K., Simons, M., Reiser, J., Saleem, M. A., Faul, C., Kriz, W., Shaw, A. S., Holzman, L. B., and Mundel, P. (2001) Podocin, a raft-associated component of the glomerular slit diaphragm, interacts with CD2AP and nephrin. J. Clin. Invest. 108, 1621-1629
11. Roselli, S., Gribouval, O., Boute, N., Sich, M., Benessy, F., Attié, T., Gubler, M.-C., and Antignac, C. (2002) Podocin localizes in the kidney to the slit diaphragm area. Am. J. Pathol. 160, 131-139
12. Winn, M. P., Conlon, P. J., Lynn, K. L., Farrington, M. K., Creazzo, T., Hawkins, A. F., Daskalakis, N., Kwan, S. Y., Ebersviller, S., Burchette, J. L., Pericak-Vance, M. A., Howell, D. N., Vance, J. M., and Rosenberg, P. B. (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308, 1801-1804
13. Reiser, J., Polu, K. R., Möller, C. C., Kenlan, P., Altintas, M. M., Wei, C., Faul, C., Herbert, S., Villegas, I., Avila-Casado, C., McGee, M., Sugimoto, H., Brown, D., Kalluri, R., Mundel, P., Smith, P. L., Clapham, D. E., and Pollak, M. R. (2005) TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat. Genet. 37, 739-744
14. Huber, T. B., Schermer, B., Müller, R. U., Höhne, M., Bartram, M., Calixto, A., Hagmann, H., Reinhardt, C., Koos, F., Kunzelmann, K., Shirokova, E., Krautwurst, D., Harteneck, C., Simons, M., Pavenstädt, H., Kerjaschki, D., Thiele, C., Walz, G., Chalfie, M., and Benzing, T. (2006) Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels. Proc. Natl. Acad. Sci. 103, 17079-17086
15. Hiebl-Dirschmied, C. M., Entler, B., Glotzmann, C., Maurer-Fogy, I., Stratowa, C., and Prohaska, R. (1991) Cloning and nucleotide sequence of cDNA encoding human erythrocyte band 7 integral membrane protein. Biochim. Biophys. Acta 1090, 123-124
16. Browman, D. T., Hoegg, M. B., and Robbins, S. M. (2007) The SPFH domain-containing proteins. More than lipid raft markers. Trends Cell Biol. 17, 394-402
17. Huber, T. B., Simons, M., Hartleben, B., Sernetz, L., Schmidts, M., Gundlach, E., Saleem, M. A., Walz, G., and Benzing, T. (2003) Molecular basis of the functional podocin-nephrin complex. Mutations in the NPHS2 gene disrupt nephrin targeting to lipid raft microdomains. Hum. Mol. Genet. 12, 3397-3405
18. Huber, T. B., and Benzing, T. (2005) The slit diaphragm. A signaling platform to regulate podocyte function. Curr. Opin. Nephrol. Hypertens. 14, 211-216
19. Schermer, B., and Benzing, T. (2009) Lipid-protein interactions along the slit diaphragm of podocytes. J. Am. Soc. Nephrol. 20, 473-478
20. Ekim, M., Ozçakar, Z. B., Acar, B., Yüksel, S., Yalçnkaya, F., Tulunay, O., Ensari, A., and Erbay, B. (2004) Three siblings with steroid-resistant nephrotic syndrome: New NPHS2 mutations in a Turkish family. Am. J. Kidney Dis. 44, e22-e24
21. Berdeli, A., Mir, S., Yavascan, O., Serdaroglu, E., Bak, M., Aksu, N., Oner, A., Anarat, A., Donmez, O., Yildiz, N., Sever, L., Tabel, Y., Dusunsel, R., Sonmez, F., and Cakar, N. (2007) NPHS2 (podicin) mutations in Turkish children with idiopathic nephrotic syndrome. Pediatr. Nephrol. 22, 2031-2040
22. Zhang, S., Arnadottir, J., Keller, C., Caldwell, G. A., Yao, C. A., and Chalfie, M. (2004) MEC-2 is recruited to the putative mechanosensory complex in C. elegans touch receptor neurons through its stomatin-like domain. Curr. Biol. 14, 1888-1896
23. Bouchireb, K., Boyer, O., Gribouval, O., Nevo, F., Huynh-Cong, E., Morinière, V., Campait, R., Ars, E., Brackman, D., Dantal, J., Eckart, P., Gigante, M., Lipska, B. S., Liutkus, A., Megarbane, A., Mohsin, N., Ozaltin, F., Saleem, M. A., Schaefer, F., Soulami, K., Torra, R., Garcelon, N., Mollet, G., Dahan, K., and Antignac, C. (2014) NPHS2 mutations in steroid-resistant nephrotic syndrome. A mutation update and the associated phenotypic spectrum. Hum. Mutat. 35, 178-186
24. Huber, T. B., Kottgen, M., Schilling, B., Walz, G., and Benzing, T. (2001) Interaction with podocin facilitates nephrin signaling. J. Biol. Chem. 276, 41543-41546
25. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji. An open-source platform for biological-image analysis. Nat. Methods 9, 676-682
26. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micropurification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906
27. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability- based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
28. Letunic, I., Doerks, T., and Bork, P. (2012) SMART 7. Recent updates to the protein domain annotation resource. Nucleic Acids Res. 40, D302-D305
29. Edgar, R. C. (2004) MUSCLE. Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
30. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., and Barton, G. J. (2009) Jalview Version 2. A multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191
31. Kadurin, I., Huber, S., and Gründer, S. (2009) A single conserved proline residue determines the membrane topology of stomatin. Biochem. J. 418, 587-594
32. Eckhardt, M., Fewou, S. N., Ackermann, I., and Gieselmann, V. (2002) N-glycosylation is required for full enzymic activity of the murine galactosylceramide sulphotransferase. Biochem. J. 368, 317-324
33. Rho, S., Lee, H. M., Lee, K., and Park, C.-S. (2000) Effects of mutation at a conserved N-glycosylation site in the bovine retinal cyclic nucleotidegated ion channel. FEBS Lett. 478, 246-252
34. Roselli, S., Moutkine, I., Gribouval, O., Benmerah, A., and Antignac, C. (2004) Plasma membrane targeting of podocin through the classical exocytic pathway. Effect of NPHS2 mutations. Traffic 5, 37-44
35. Goodman, M. B., Ernstrom, G. G., Chelur, D. S., O'Hagan, R., Yao, C. A., and Chalfie, M. (2002) MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation. Nature 415, 1039-1042
36. Völker, L. A., Schurek, E.-M., Rinschen, M. M., Tax, J., Schutte, B. A., Lamkemeyer, T., Ungrue, D., Schermer, B., Benzing, T., and Höhne, M. (2013) Characterization of a short isoform of the kidney protein podocin in human kidney. BMC Nephrol. 14, 102
37. Anderson, M., Kim, E. Y., Hagmann, H., Benzing, T., and Dryer, S. E. (2013) Opposing effects of podocin on the gating of podocyte TRPC6 channels evoked by membrane stretch or diacylglycerol. Am. J. Physiol. Cell Physiol. 305, C276-289
38. Brand, J., Smith, E. S., Schwefel, D., Lapatsina, L., Poole, K., Omerbašić, D., Kozlenkov, A., Behlke, J., Lewin, G. R., and Daumke, O. (2012) A stomatin dimer modulates the activity of acid-sensing ion channels. EMBO J. 31, 3635-3646