Podocyte-specific overexpression of wild type or mutant Trpc6 in mice is sufficient to cause glomerular disease

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-11

  Krall, Paola ^a,b   Canales, Cesar P ^a,c   Kairath, Pamela ^a,b   Carmona Mora, Paulina ^a,c   Molina, Jessica ^a   Carpio, J Daniel ^b   Ruiz, Phillip ^c   Mezzano, Sergio A ^b   Li, Jing ^c   Wei, Changli ^c   Reiser, Jochen ^c   Young, Juan I ^a,c   Walz, Katherina ^a,c  

^a CENTRO DE ESTUDIOS CIENTÍFICOS CECS   (Chile)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, MOUSE;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FOCAL GLOMERULOSCLEROSIS; GENE OVEREXPRESSION; HISTOPATHOLOGY; MALE; MOUSE; MUTANT; NONHUMAN; PODOCYTE; RISK FACTOR; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CBA MOUSE; CELL LINE; DISEASE MODEL; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MUTATION;

MUS; MUS MUSCULUS;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MUTATION; ORGAN SPECIFICITY; PODOCYTES; TRPC CATION CHANNELS;

EID: 77958473430     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012859     Document Type: Article

References (44)

1. Kitiyakara C, Kopp JB, Eggers P (2003) Trends in the epidemiology of focal segmental glomerulosclerosis. Semin Nephrol 23: 172-182.
2. Thomas DB (2009) Focal segmental glomerulosclerosis: a morphologic diagnosis in evolution. Arch Pathol Lab Med 133: 217-223.
3. D'Agati VD (2008) The spectrum of focal segmental glomerulosclerosis: new insights. Curr Opin Nephrol Hypertens 17: 271-281.
4. Reiser J, Kriz W, Kretzler M, Mundel P (2000) The glomerular slit diaphragm is a modified adherens junction. J Am Soc Nephrol 11: 1-8.
5. D'Agati VD (2008) Podocyte injury in focal segmental glomerulosclerosis: Lessons from animal models (a play in five acts). Kidney Int 73: 399-406.
6. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, et al. (2000) NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 24: 349-354.
7. Monteiro EJ, Pereira AC, Pereira AB, Krieger JE, Mastroianni-Kirsztajn G (2006) NPHS2 mutations in adult patients with primary focal segmental glomerulosclerosis. J Nephrol 19: 366-371.
8. Kaplan JM, Kim SH, North KN, Rennke H, Correia LA, et al. (2000) Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 24: 251-256.
9. Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, et al. (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308: 1801-1804.
10. Reiser J, Polu KR, Möller CC, Kenlan P, Altintas MM, et al. (2005) TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 37: 739-744.
11. Brown EJ, Schlöndorff JS, Becker DJ, Tsukaguchi H, Tonna SJ, Uscinski AL, Higgs HN, Henderson JM, Pollak MR (2010) Mutations in the formin gene INF2 cause focal segmental glomerulosclerosis. Nat Genet 42: 72-76.
12. Kopp JB, Smith MW, Nelson GW, Johnson RC, Freedman BI, et al. (2008) MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis. Nat Genet 40: 1175-1184.
13. Montell C, Birnbaumer L, Flockerzi V (2002) The TRP channels, a remarkably functional family. Cell 108: 595-598.
14. Clapham DE (2003) TRP channels as cellular sensors. Nature 426: 517-524.
15. Eder P, Poteser M, Romanin C, Groschner K (2005) Na(+) entry and modulation of Na(+)/Ca(2+) exchange as a key mechanism of TRPC signaling. Pflugers Arch 451: 99-104.
16. Estacion M, Sinkins WG, Jones SW, Applegate MA, Schilling WP (2006) Human TRPC6 expressed in HEK 293 cells forms non-selective cation channels with limited Ca2+ permeability. J Physiol 572: 359-377.
17. Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, et al. (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397: 259-263.
18. Okada T, Inoue R, Yamazaki K, Maeda A, Kurosaki T, et al. (1999) Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. Ca(2+)-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J Biol Chem 274: 27359-27370.
19. Heeringa SF, Möller CC, Du J, Yue L, Hinkes B, et al. (2009) A novel TRPC6 mutation that causes childhood FSGS. Plos One 4: e7771.
20. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB (2002) Two gene fragments that direct podocyte-specific expression in transgenic mice. J Am Soc Nephrol 13: 1561-1567.
21. Shigehara T, Zaragoza C, Kitiyakara C, Takahashi H, Lu H, et al. (2003) Inducible podocyte-specific gene expression in transgenic mice. J Am Soc Nephrol 14: 1998-2003.
22. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB (2003) Podocyte-specific expression of cre recombinase in transgenic mice. Genesis 35: 39-42.
23. El-Aouni C, Herbach N, Blattner SM, Henger A, Rastaldi MP, et al. (2006) Podocyte-specific deletion of integrin-linked kinase results in severe glomerular basement membrane alterations and progressive glomerulosclerosis. J Am Soc Nephrol 17: 1334-1344.
24. Juhila J, Roozendaal R, Lassila M, Verbeek SJ, Holthofer H (2006) Podocyte cell-specific expression of doxycycline inducible Cre recombinase in mice. J Am Soc Nephrol 17: 648-654.
25. Kajiyama H, Titus S, Austin CP, Chiotos K, Matsumoto T, et al. (2008) Tetracycline-inducible gene expression in conditionally immortalized mouse podocytes. Am J Nephrol 29: 153-163.
26. Boulay G, Zhu X, Peyton M, Jiang M, Hurst R, et al. (1997) Cloning and expression of a novel mammalian homolog of Drosophila transient receptor potential (Trp) involved in calcium entry secondary to activation of receptors coupled by the Gq class of G protein. J Biol Chem 272: 29672-29680.
27. Spassova M, Hewavitharana T, Xu W, Soboloff J, Gill D (2006) A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci USA 103: 16586-16591.
28. Mundel P, Heid HW, Mundel TM, Krüger M, Reiser J, et al. (1997) Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 139: 193-204.
29. Kriz W, Lemley KV (1999) The role of the podocyte in glomerulosclerosis. Curr Opin Nephrol Hypertens 8: 489-497.
30. Santín S, Ars E, Rossetti S, Salido E, Silva I, et al. (2009) TRPC6 mutational analysis in a large cohort of patients with focal segmental glomerulosclerosis. Nephrol Dial Transplant 24: 3089-3096.
31. Möller CC, Wei C, Altintas MM, Li J, Greka A, et al. (2007) Induction of TRPC6 channel in acquired forms of proteinuric kidney disease. J Am Soc Nephrol 18: 29-36.
32. Yu Y, Fantozzi I, Remillard CV, Landsberg JW, Kunichika N, et al. (2004) Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proc Natl Acad Sci 101: 13861-13866.
33. Michaud JL, Lemieux LI, Dubé M, Vanderhyden BC, Robertson SJ, et al. (2003) Focal and segmental glomerulosclerosis in mice with podocyte-specific expression of mutant alpha-actinin-4. J Am Soc Nephrol 14: 1200-1211.
34. Huber TB, Kwoh C, Wu H, Asanuma K, Gödel M, et al. (2006) Bigenic mouse models of focal segmental glomerulosclerosis involving pairwise interaction of CD2AP, Fyn, and synaptopodin. J Clin Invest 116: 1337-1345.
35. Pollak MR (2003) The genetic basis of FSGS and steroid-resistant nephrosis. Semin Nephrol 23: 141-146.
36. Fogo AB (2003) Animal models of FSGS: lessons for pathogenesis and treatment. Semin Nephrol 23: 161-171.
37. Roselli S, Heidet L, Sich M, Henger A, Kretzler M, et al. (2004) Early glomerular filtration defect and severe renal disease in podocin-deficient mice. Mol Cell Biol 24: 550-560.
38. Putaala H, Soininen R, Kilpelainen P, Wartiovaara J, Tryggvason K (2001) The murine nephrin gene is specifically expressed in kidney, brain and pancreas: inactivation of the gene leads to massive proteinuria and neonatal death. Hum Mol Genet 10: 1-8.
39. Donoviel DB, Freed DD, Vogel H, Potter DG, Hawkins E, et al. (2001) Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol Cell Biol 21: 4829-4836.
40. Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, et al. (1999) Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 286: 312-315.
41. Yu CC, Yen TS, Lowell CA, DeFranco AL (2001) Lupus-like kidney disease in mice deficient in the Src family tyrosine kinases Lyn and Fyn. Curr Biol 11: 34-38.
42. Schlöndorff J, Del Camino D, Carrasquillo R, Lacey V, Pollak MR (2009) TRPC6 mutations associated with focal segmental glomerulosclerosis cause constitutive activation of NFAT-dependent transcription. Am J Physiol Cell Physiol 296: C558-569.
43. Faul C, Donnelly M, Merscher-Gomez S, Chang YH, Franz S, et al. (2008) The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat Med 14: 931-938.
44. Crowley SD, Vasievich MP, Ruiz P, Gould SK, Parsons KK, et al. (2009) Glomerular type 1 angiotensin receptors augment kidney injury and inflammation in murine autoimmune nephritis. J Clin Invest 119: 943-953.