Exome sequencing and in vitro studies identified podocalyxin as a candidate gene for focal and segmental glomerulosclerosis

Kidney International

Volumn 85, Issue 1, 2014, Pages 124-133

  Barua, Moumita ^a,b   Shieh, Eric ^b   Schlondorff, Johannes ^a,b   Genovese, Giulio ^b,c,d   Kaplan, Bernard S ^e   Pollak, Martin R ^a,b  

^a Beth Deaconess Medical Center   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Stanley Center for Psychiatric Research   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

focal segmental glomerulosclerosis; genetic renal disease; glomerular disease

Indexed keywords

EZRIN; PODOCALYXIN; PROTEIN VARIANT;

ADULT; ANIMAL CELL; ARTICLE; AUTOSOMAL DOMINANT DISORDER; AUTOSOMAL DOMINANT INHERITANCE; CELL FUNCTION; CELL SURFACE; CELLULAR DISTRIBUTION; CHILD; CONTROLLED STUDY; DIMERIZATION; EXOME; FOCAL GLOMERULOSCLEROSIS; GENE IDENTIFICATION; GENE PRODUCT; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MONOGENIC DISORDER; NONHUMAN; PEDIGREE; PODOCALYXIN GENE; PODOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RARE DISEASE; SCHOOL CHILD;

ADOLESCENT; ADULT; ANIMALS; CHILD; DOGS; EXOME; FEMALE; GENES, DOMINANT; GENETIC VARIATION; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MALE; MICE; MIDDLE AGED; RABBITS; RATS; SEQUENCE ANALYSIS, DNA; SIALOGLYCOPROTEINS; YOUNG ADULT;

EID: 84891557500     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2013.354     Document Type: Article

References (39)

1. Rydel JJ, Korbet SM, Borok RZ et al. Focal segmental glomerular sclerosis in adults: presentation, course, and response to treatment. Am J Kidney Dis 1995; 25: 534-542.
2. Korbet SM, Schwartz MM, Lewis EJ. Primary focal segmental glomerulosclerosis: clinical course and response to therapy. Am J Kidney Dis 1994; 23: 773-783. (Pubitemid 24173558)
3. D'Agati VD, Kaskel FJ, Falk RJ. Focal segmental glomerulosclerosis. N Engl J Med 2011; 365: 2398-2411.
4. Kitiyakara C, Eggers P, Kopp JB. Twenty-one-year trend in ESRD due to focal segmental glomerulosclerosis in the United States. Am J Kidney Dis 2004; 44: 815-825. (Pubitemid 39445913)
5. Somlo S, Mundel P. Getting a foothold in nephrotic syndrome. Nat Genet 2000; 24: 333-335. (Pubitemid 30187426)
6. Kerjaschki D, Sharkey DJ, Farquhar MG. Identification and characterization of podocalyxin-The major sialoprotein of the renal glomerular epithelial cell. J Cell Biol 1984; 98: 1591-1596. (Pubitemid 14126988)
7. Dekan G, Gabel C, Farquhar MG. Sulfate contributes to the negative charge of podocalyxin, the major sialoglycoprotein of the glomerular filtration slits. Proc Natl Acad Sci USA 1991; 88: 5398-5402. (Pubitemid 21914752)
8. Schnabel E, Dekan G, Miettinen A et al. Biogenesis of podocalyxin-The major glomerular sialoglycoprotein-in the newborn rat kidney. Eur J Cell Biol 1989; 48: 313-326. (Pubitemid 19127296)
9. Nielsen JS, McNagny KM. The role of podocalyxin in health and disease. J Am Soc Nephrol 2009; 20: 1669-1676.
10. Seiler MW, Rennke HG, Venkatachalam MA et al. Pathogenesis of polycation-induced alterations ('fusion') of glomerular epithelium. Lab Invest 1977; 36: 48-61. (Pubitemid 8021270)
11. Kerjaschki D. Polycation-induced dislocation of slit diaphragms and formation of cell junctions in rat kidney glomeruli: the effects of low temperature, divalent cations, colchicine, and cytochalasin B. Lab Invest 1978; 39: 430-440. (Pubitemid 9095299)
12. Kurihara H, Anderson JM, Kerjaschki D et al. The altered glomerular filtration slits seen in puromycin aminonucleoside nephrosis and protamine sulfate-Treated rats contain the tight junction protein ZO-1. Am J Pathol 1992; 141: 805-816.
13. Andrews PM. Glomerular epithelial alterations resulting from sialic acid surface coat removal. Kidney Int 1979; 15: 376-385. (Pubitemid 10219858)
14. Gelberg H, Healy L, Whiteley H et al. In vivo enzymatic removal of alpha 2-46-linked sialic acid from the glomerular filtration barrier results in podocyte charge alteration and glomerular injury. Lab Invest 1996; 74: 907-920. (Pubitemid 26152660)
15. Doyonnas R, Kershaw DB, Duhme C et al. Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J Exper Med 2001; 194: 13-27. (Pubitemid 32660434)
16. Kavoura E, Gakiopoulou H, Paraskevakou H et al. Immunohistochemical evaluation of podocalyxin expression in glomerulopathies associated with nephrotic syndrome. Hum Pathol 2011; 42: 227-235.
17. Copelovitch L, Guttenberg M, Pollak MR et al. Renin-Angiotensin axis blockade reduces proteinuria in presymptomatic patients with familial FSGS. Pediatr Nephrol 2007; 22: 1779-1784. (Pubitemid 47337436)
18. Kaplan JM, Kim SH, North KN et al. Mutations in ACTN4, encoding alphaactinin- 4, cause familial focal segmental glomerulosclerosis. Nat Genet 2000; 24: 251-256. (Pubitemid 30132192)
19. Weins A, Kenlan P, Herbert S et al. Mutational and Biological Analysis of alpha-Actinin-4 in focal segmental glomerulosclerosis. J Am Soc Nephrol 2005; 16: 3694-3701. (Pubitemid 46211291)
20. Brown EJ, Schlondorff JS, Becker DJ et al. Mutations in the formin gene INF2 cause focal segmental glomerulosclerosis. Nat Genet 2010; 42: 72-76.
21. Winn MP, Conlon PJ, Lynn KL et al. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 2005; 308: 1801-1804. (Pubitemid 40848011)
22. Reiser J, Polu KR, Moller CC et al. TRPC6 is a glomerular slit diaphragmassociated channel required for normal renal function. Nat Genet 2005; 37: 739-744. (Pubitemid 41754891)
23. Michael AF, Blau E, Vernier RL. Glomerular polyanion. Alteration in aminonucleoside nephrosis. Lab Invest 1970; 23: 649-657.
24. Mohos SC, Skoza L. Glomerular sialoprotein. Science 1969; 164: 1519-1521.
25. Wegner B, Al-Momany A, Kulak SC et al. CLIC5A, a component of the ezrin-podocalyxin complex in glomeruli, is a determinant of podocyte integrity. Am J Physiol Renal Physiol 2010; 298: F1492-F1503.
26. Takeda T, McQuistan T, Orlando RA et al. Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 2001; 108: 289-301. (Pubitemid 32656253)
27. Sun H, Schlondorff JS, Brown EJ et al. Rho activation of mDia formins is modulated by an interaction with inverted formin 2 (INF2). Proc Natl Acad Sci USA 2011; 108: 2933-2938.
28. Weins A, Schlondorff JS, Nakamura F et al. Disease-Associated mutant alpha-Actinin-4 reveals a mechanism for regulating its F-Actin-binding affinity. Proc Natl Acad Sci USA 2007; 104: 16080-16085. (Pubitemid 350099367)
29. Pierchala BA, Munoz MR, Tsui CC. Proteomic analysis of the slit diaphragm complex: CLIC5 is a protein critical for podocyte morphology and function. Kidney Int 2010; 78: 868-882.
30. Orlando RA, Takeda T, Zak B et al. The glomerular epithelial cell antiadhesin podocalyxin associates with the actin cytoskeleton through interactions with ezrin. J Am Soc Nephrol 2001; 12: 1589-1598. (Pubitemid 32674420)
31. Fukasawa H, Obayashi H, Schmieder S et al. Phosphorylation of podocalyxin (Ser415) Prevents RhoA and ezrin activation and disrupts its interaction with the actin cytoskeleton. Am J Pathol 2011; 179: 2254-2265.
32. Takeda T, Go WY, Orlando RA et al. Expression of podocalyxin inhibits cell-cell adhesion and modifies junctional properties in Madin-Darby canine kidney cells. Mol Biol Cell 2000; 11: 3219-3232. (Pubitemid 32107095)
33. Yu CY, Chen JY, Lin YY et al. A bipartite signal regulates the faithful delivery of apical domain marker podocalyxin/Gp135. Mol Biol Cell 2007; 18: 1710-1722.
34. Fukasawa H, Obayashi H, Schmieder S et al. Phosphorylation of podocalyxin (Ser415) prevents RhoA and ezrin activation and disrupts its interaction with the actin cytoskeleton. Am J Pathol 2011; 179: 2254-2265.
35. Schmieder S, Nagai M, Orlando RA et al. Podocalyxin activates RhoA and induces actin reorganization through NHERF1 and Ezrin in MDCK cells. J Am Soc Nephrol 2004; 15: 2289-2298. (Pubitemid 39159329)
36. Meder D, Shevchenko A, Simons K et al. Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. J Cell Biol 2005; 168: 303-313. (Pubitemid 40248227)
37. Li H, Durbin R. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 2009; 25: 1754-1760.
38. McKenna A, Hanna M, Banks E et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20: 1297-1303.
39. DePristo MA, Banks E, Poplin R et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genet 2011; 43: 491-498.