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Open Access 01-09-2013 | Review

Membrane trafficking in podocyte health and disease

Author: Agnieszka Swiatecka-Urban

Published in: Pediatric Nephrology | Issue 9/2013

Abstract

Podocytes are highly specialized epithelial cells localized in the kidney glomerulus. The distinct cell signaling events and unique cytoskeletal architecture tailor podocytes to withstand changes in hydrostatic pressure during glomerular filtration. Alteration of glomerular filtration leads to kidney disease and frequently manifests with proteinuria. It has been increasingly recognized that cell signaling and cytoskeletal dynamics are coupled more tightly to membrane trafficking than previously thought. Membrane trafficking coordinates the cross-talk between protein networks and signaling cascades in a spatially and temporally organized fashion and may be viewed as a communication highway between the cell exterior and interior. Membrane trafficking involves transport of cargo from the plasma membrane to the cell interior (i.e., endocytosis) followed by cargo trafficking to lysosomes for degradation or to the plasma membrane for recycling. Yet, recent studies indicate that the conventional classification does not fully reflect the complex and versatile nature of membrane trafficking. While the increasing complexity of elaborate protein scaffolds and signaling cascades is being recognized in podocytes, the role of membrane trafficking is less well understood. This review will focus on the role of membrane trafficking in podocyte health and disease.

Sigismund S, Confalonieri S, Ciliberto A, Polo S, Scita G, Di Fiore PP (2012) Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol Rev 92:273–366PubMedCrossRef

Andersson ER (2012) The role of endocytosis in activating and regulating signal transduction. Cell Mol Life Sci 69:1755–1771PubMedCrossRef

Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10:597–608PubMedCrossRef

Canton I, Battaglia G (2012) Endocytosis at the nanoscale. Chem Soc Rev 41:2718–2739PubMedCrossRef

Gong Q, Huntsman C, Ma D (2008) Clathrin-independent internalization and recycling. J Cell Mol Med 12:126–144PubMedCrossRef

Jovic M, Sharma M, Rahajeng J, Caplan S (2010) The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 25:99–112PubMed

Hopkins CR, Trowbridge IS (1983) Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells. J Cell Biol 97:508–521PubMedCrossRef

Deneka M, Neeft M, Popa I, van Oort M, Sprong H, Oorschot V, Klumperman J, Schu P, van der Sluijs P (2003) Rabaptin-5alpha/rabaptin-4 serves as a linker between rab4 and gamma(1)-adaptin in membrane recycling from endosomes. EMBO J 22:2645–2657PubMedCrossRef

Chua CE, Lim YS, Tang BL (2010) Rab35—a vesicular traffic-regulating small GTPase with actin modulating roles. FEBS Lett 584:1–6PubMedCrossRef

10.

Grant BD, Caplan S (2008) Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9:2043–2052PubMedCrossRef

11.

Traer CJ, Rutherford AC, Palmer KJ, Wassmer T, Oakley J, Attar N, Carlton JG, Kremerskothen J, Stephens DJ, Cullen PJ (2007) SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat Cell Biol 9:1370–1380PubMedCrossRef

12.

Mattila PE, Youker RT, Mo D, Bruns JR, Cresawn KO, Hughey RP, Ihrke G, Weisz OA (2012) Multiple biosynthetic trafficking routes for apically secreted proteins in MDCK cells. Traffic 13:433–442PubMedCrossRef

13.

Luzio JP, Parkinson MD, Gray SR, Bright NA (2009) The delivery of endocytosed cargo to lysosomes. Biochem Soc Trans 37:1019–1021PubMedCrossRef

14.

Haglund K, Dikic I (2012) The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci 125:265–275PubMedCrossRef

15.

Shivas JM, Morrison HA, Bilder D, Skop AR (2010) Polarity and endocytosis: reciprocal regulation. Trends Cell Biol 20:445–452PubMedCrossRef

16.

Haraldsson B, Jeansson M (2009) Glomerular filtration barrier. Curr Opin Nephrol Hypertens 18:331–335PubMedCrossRef

17.

Asanuma K, Mundel P (2003) The role of podocytes in glomerular pathobiology. Clin Exp Nehrol 7:255–259CrossRef

18.

Faa G, Gerosa C, Fanni D, Monga G, Zaffanello M, Van Eyken P, Fanos V (2012) Morphogenesis and molecular mechanisms involved in human kidney development. J Cell Physiol 227:1257–1268PubMedCrossRef

19.

Schmidt-Ott KM, Yang J, Chen X, Wang H, Paragas N, Mori K, Li JY, Lu B, Costantini F, Schiffer M, Bottinger E, Barasch J (2005) Novel regulators of kidney development from the tips of the ureteric bud. J Am Soc Nephrol 16:1993–2002PubMedCrossRef

20.

Park JS, Valerius MT, McMahon AP (2007) Wnt/beta-catenin signaling regulates nephron induction during mouse kidney development. Development 134:2533–2539PubMedCrossRef

21.

Essafi A, Webb A, Berry RL, Slight J, Burn SF, Spraggon L, Velecela V, Martinez-Estrada OM, Wiltshire JH, Roberts SG, Brownstein D, Davies JA, Hastie ND, Hohenstein P (2011) A wt1-controlled chromatin switching mechanism underpins tissue-specific wnt4 activation and repression. Dev Cell 21:559–574PubMedCrossRef

22.

Surendran K, Boyle S, Barak H, Kim M, Stomberski C, McCright B, Kopan R (2010) The contribution of Notch1 to nephron segmentation in the developing kidney is revealed in a sensitized Notch2 background and can be augmented by reducing Mint dosage. Dev Biol 337:386–395PubMedCrossRef

23.

Musse AA, Meloty-Kapella L, Weinmaster G (2012) Notch ligand endocytosis: mechanistic basis of signaling activity. Semin Cell Dev Biol 23:429–436PubMedCrossRef

24.

Cheng HT, Kim M, Valerius MT, Surendran K, Schuster-Gossler K, Gossler A, McMahon AP, Kopan R (2007) Notch2, but not Notch1, is required for proximal fate acquisition in the mammalian nephron. Development 134:801–811PubMedCrossRef

25.

Bonegio RG, Beck LH, Kahlon RK, Lu W, Salant DJ (2011) The fate of Notch-deficient nephrogenic progenitor cells during metanephric kidney development. Kidney Int 79:1099–1112PubMedCrossRef

26.

Reidy KJ, Villegas G, Teichman J, Veron D, Shen W, Jimenez J, Thomas D, Tufro A (2009) Semaphorin3a regulates endothelial cell number and podocyte differentiation during glomerular development. Development 136:3979–3989PubMedCrossRef

27.

Carcea I, Ma’ayan A, Mesias R, Sepulveda B, Salton SR, Benson DL (2010) Flotillin-mediated endocytic events dictate cell type-specific responses to semaphorin 3A. J Neurosci 30:15317–15329PubMedCrossRef

28.

Welsh GI, Saleem MA (2011) The podocyte cytoskeleton—key to a functioning glomerulus in health and disease. Nat Rev Nephrol 8:14–21PubMedCrossRef

29.

Chao WT, Kunz J (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 583:1337–1343PubMedCrossRef

30.

Marco E, Wedlich-Soldner R, Li R, Altschuler SJ, Wu LF (2007) Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129:411–422PubMedCrossRef

31.

Slaughter BD, Das A, Schwartz JW, Rubinstein B, Li R (2009) Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Dev Cell 17:823–835PubMedCrossRef

32.

Scott RP, Hawley SP, Ruston J, Du J, Brakebusch C, Jones N, Pawson T (2012) Podocyte-specific loss of Cdc42 leads to congenital nephropathy. J Am Soc Nephrol 23:1149–1154PubMedCrossRef

33.

Skouloudaki K, Puetz M, Simons M, Courbard JR, Boehlke C, Hartleben B, Engel C, Moeller MJ, Englert C, Bollig F, Schafer T, Ramachandran H, Mlodzik M, Huber TB, Kuehn EW, Kim E, Kramer-Zucker A, Walz G (2009) Scribble participates in Hippo signaling and is required for normal zebrafish pronephros development. Proc Natl Acad Sci USA 106:8579–8584PubMedCrossRef

34.

Joberty G, Petersen C, Gao L, Macara IG (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531–539PubMedCrossRef

35.

Simons M, Hartleben B, Huber TB (2009) Podocyte polarity signalling. Curr Opin Nephrol Hypertens 18:324–330PubMedCrossRef

36.

Nelson WJ (2009) Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. Cold Spring Harb Perspect Biol 1:a000513PubMedCrossRef

37.

Schluter MA, Pfarr CS, Pieczynski J, Whiteman EL, Hurd TW, Fan S, Liu CJ, Margolis B (2009) Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol Biol Cell 20:4652–4663PubMedCrossRef

38.

Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P (2007) Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17:428–437PubMedCrossRef

39.

Steed E, Balda MS, Matter K (2010) Dynamics and functions of tight junctions. Trends Cell Biol 20:142–149PubMedCrossRef

40.

Tang VW, Brieher WM (2012) alpha-Actinin-4/FSGS1 is required for Arp2/3-dependent actin assembly at the adherens junction. J Cell Biol 196:115–130PubMedCrossRef

41.

Kestila M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K (1998) Positionally cloned gene for a novel glomerular protein—nephrin—is mutated in congenital nephrotic syndrome. Mol Cell 1:575–582PubMedCrossRef

42.

Wartiovaara J, Ofverstedt LG, Khoshnoodi J, Zhang J, Makela E, Sandin S, Ruotsalainen V, Cheng RH, Jalanko H, Skoglund U, Tryggvason K (2004) Nephrin strands contribute to a porous slit diaphragm scaffold as revealed by electron tomography. J Clin Invest 114:1475–1483PubMed

43.

Benigni A, Gagliardini E, Tomasoni S, Abbate M, Ruggenenti P, Kalluri R, Remuzzi G (2004) Selective impairment of gene expression and assembly of nephrin in human diabetic nephropathy. Kidney Int 65:2193–2200PubMedCrossRef

44.

Shono A, Tsukaguchi H, Kitamura A, Hiramoto R, Qin XS, Doi T, Iijima K (2009) Predisposition to relapsing nephrotic syndrome by a nephrin mutation that interferes with assembly of functioning microdomains. Hum Mol Genet 18:2943–2956PubMedCrossRef

45.

Huber TB, Simons M, Hartleben B, Sernetz L, Schmidts M, Gundlach E, Saleem MA, Walz G, 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 12:3397–3405PubMedCrossRef

46.

Roselli S, Moutkine I, Gribouval O, Benmerah A, Antignac C (2004) Plasma membrane targeting of podocin through the classical exocytic pathway: effect of NPHS2 mutations. Traffic 5:37–44PubMedCrossRef

47.

Morrow IC, Parton RG (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6:725–740PubMedCrossRef

48.

Otto GP, Nichols BJ (2011) The roles of flotillin microdomains—endocytosis and beyond. J Cell Sci 124:3933–3940PubMedCrossRef

49.

Zhao F, Zhang J, Liu YS, Li L, He YL (2011) Research advances on flotillins. Virol J 8:479PubMedCrossRef

50.

Li H, Lemay S, Aoudjit L, Kawachi H, Takano T (2004) SRC-family kinase Fyn phosphorylates the cytoplasmic domain of nephrin and modulates its interaction with podocin. J Am Soc Nephrol 15:3006–3015PubMedCrossRef

51.

Qin XS, Tsukaguchi H, Shono A, Yamamoto A, Kurihara H, Doi T (2009) Phosphorylation of nephrin triggers its internalization by raft-mediated endocytosis. J Am Soc Nephrol 20:2534–2545PubMedCrossRef

52.

Quack I, Woznowski M, Potthoff SA, Palmer R, Konigshausen E, Sivritas S, Schiffer M, Stegbauer J, Vonend O, Rump LC, Sellin L (2011) PKC alpha mediates beta-arrestin2-dependent nephrin endocytosis in hyperglycemia. J Biol Chem 286:12959–12970PubMedCrossRef

53.

Waters AM, Wu MY, Huang YW, Liu GY, Holmyard D, Onay T, Jones N, Egan SE, Robinson LA, Piscione TD (2012) Notch promotes dynamin-dependent endocytosis of nephrin. J Am Soc Nephrol 23:27–35PubMedCrossRef

54.

Quack I, Rump LC, Gerke P, Walther I, Vinke T, Vonend O, Grunwald T, Sellin L (2006) beta-Arrestin2 mediates nephrin endocytosis and impairs slit diaphragm integrity. Proc Natl Acad Sci USA 103:14110–14115PubMedCrossRef

55.

Shenoy SK, Lefkowitz RJ (2003) Trafficking patterns of beta-arrestin and G protein-coupled receptors determined by the kinetics of beta-arrestin deubiquitination. J Biol Chem 278:14498–14506PubMedCrossRef

56.

Shukla AK, Xiao K, Lefkowitz RJ (2011) Emerging paradigms of beta-arrestin-dependent seven transmembrane receptor signaling. Tremds Boochem Sci 36:457–469CrossRef

57.

Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447PubMedCrossRef

58.

Tossidou I, Teng B, Menne J, Shushakova N, Park JK, Becker JU, Modde F, Leitges M, Haller H, Schiffer M (2010) Podocytic PKC-alpha is regulated in murine and human diabetes and mediates nephrin endocytosis. PLoS One 5:e10185PubMedCrossRef

59.

Menne J, Meier M, Park JK, Boehne M, Kirsch T, Lindschau C, Ociepka R, Leitges M, Rinta-Valkama J, Holthofer H, Haller H (2006) Nephrin loss in experimental diabetic nephropathy is prevented by deletion of protein kinase C alpha signaling in-vivo. Kidney Int 70:1456–1462PubMedCrossRef

60.

Kawachi H, Miyauchi N, Suzuki K, Han GD, Orikasa M, Shimizu F (2006) Role of podocyte slit diaphragm as a filtration barrier. Nephrology 11:274–281PubMedCrossRef

61.

Watanabe S, Take H, Takeda K, Yu ZX, Iwata N, Kajigaya S (2000) Characterization of the CIN85 adaptor protein and identification of components involved in CIN85 complexes. Biophys Res Commun 278:167–174CrossRef

62.

Tossidou I, Teng B, Drobot L, Meyer-Schwesinger C, Worthmann K, Haller H, Schiffer M (2010) CIN85/RukL is a novel binding partner of nephrin and podocin and mediates slit diaphragm turnover in podocytes. J Biol Chem 285:25285–25295PubMedCrossRef

63.

Tossidou I, Niedenthal R, Klaus M, Teng B, Worthmann K, King BL, Peterson KJ, Haller H, Schiffer M (2012) CD2AP regulates SUMOylation of CIN85 in podocytes. Mol Cell Biol 32:1068–1079PubMedCrossRef

64.

Lehtonen S, Zhao F, Lehtonen E (2002) CD2-associated protein directly interacts with the actin cytoskeleton. Am J Physiol 283:F734–F743

65.

Gaidos G, Soni S, Oswald DJ, Toselli PA, Kirsch KH (2007) Structure and function analysis of the CMS/CIN85 protein family identifies actin-bundling properties and heterotypic-complex formation. J Cell Sci 120:2366–2377PubMedCrossRef

66.

Take H, Watanabe S, Takeda K, Yu ZX, Iwata N, Kajigaya S (2000) Cloning and characterization of a novel adaptor protein, CIN85, that interacts with c-Cbl. Biochem Biophys Res Commun 268:321–328PubMedCrossRef

67.

Havrylov S, Redowicz MJ, Buchman VL (2010) Emerging roles of Ruk/CIN85 in vesicle-mediated transport, adhesion, migration and malignancy. Traffic 11:721–731PubMedCrossRef

68.

Fukasawa H, Bornheimer S, Kudlicka K, Farquhar MG (2009) Slit diaphragms contain tight junction proteins. J Am Soc Nephrol 20:1491–1503PubMedCrossRef

69.

Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6:622–634PubMedCrossRef

70.

de Beco S, Amblard F, Coscoy S (2012) New insights into the regulation of E-cadherin distribution by endocytosis. Int Rev Cell Mol Biol 295:63–108PubMedCrossRef

71.

Caswell PT, Vadrevu S, Norman JC (2009) Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10:843–853PubMedCrossRef

72.

Kreidberg JA, Symons JM (2000) Integrins in kidney development, function, and disease. Am J Physiol Renal Physiol 279:F233–F242PubMed

73.

Reiser J, Oh J, Shirato I, Asanuma K, Hug A, Mundel TM, Honey K, Ishidoh K, Kominami E, Kreidberg JA, Tomino Y, Mundel P (2004) Podocyte migration during nephrotic syndrome requires a coordinated interplay between cathepsin L and alpha3 integrin. J Biol Chem 279:34827–34832PubMedCrossRef

74.

Ma H, Togawa A, Soda K, Zhang J, Lee S, Ma M, Yu Z, Ardito T, Czyzyk J, Diggs L, Joly D, Hatakeyama S, Kawahara E, Holzman L, Guan JL, Ishibe S (2010) Inhibition of podocyte FAK protects against proteinuria and foot process effacement. J Am Soc Nephrol 21:1145–1156PubMedCrossRef

75.

Takeda T, Go WY, Orlando RA, Farquhar MG (2000) Expression of podocalyxin inhibits cell-cell adhesion and modifies junctional properties in Madin-Darby canine kidney cells. Mol Biol Cell 11:3219–3232PubMedCrossRef

76.

Yu CY, Chen JY, Lin YY, Shen KF, Lin WL, Chien CL, ter Beest MB, Jou TS (2007) A bipartite signal regulates the faithful delivery of apical domain marker podocalyxin/Gp135. Mol Biol Cell 18:1710–1722PubMedCrossRef

77.

Takeda T, McQuistan T, Orlando RA, Farquhar MG (2001) Loss of glomerular foot processes is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 108:289–301PubMed

78.

Kavoura E, Gakiopoulou H, Paraskevakou H, Marinaki S, Agrogiannis G, Stofas A, Boletis I, Patsouris E, Lazaris AC (2011) Immunohistochemical evaluation of podocalyxin expression in glomerulopathies associated with nephrotic syndrome. Hum Pathol 42:227–235PubMedCrossRef

79.

Kerjaschki D (2001) Caught flat-footed: podocyte damage and the molecular bases of focal glomerulosclerosis. J Clin Invest 108:1583–1587PubMed

80.

Ohashi E, Tanabe K, Henmi Y, Mesaki K, Kobayashi Y, Takei K (2011) Receptor sorting within endosomal trafficking pathway is facilitated by dynamic actin filaments. PLoS One 6:e19942PubMedCrossRef

81.

Tanabe K, Ohashi E, Henmi Y, Takei K (2011) Receptor sorting and actin dynamics at early endosomes. Commun Integr Biol 4:742–744PubMed

82.

Welsch T, Endlich N, Gokce G, Doroshenko E, Simpson JC, Kriz W, Shaw AS, Endlich K (2005) Association of CD2AP with dynamic actin on vesicles in podocytes. Am J Physiol Renal Physiol 289:F1134–F1143PubMedCrossRef

83.

Kim JM, Wu H, Green G, Winkler CA, Kopp JB, Miner JH, Unanue ER, Shaw AS (2003) CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 300:1298–1300PubMedCrossRef

84.

Patrie KM, Drescher AJ, Welihinda A, Mundel P, Margolis B (2002) Interaction of two actin-binding proteins, synaptopodin and alpha-actinin-4, with the tight junction protein MAGI-1. J Bio Chem 277:30183–30190CrossRef

85.

Prabakaran T, Nielsen R, Larsen JV, Sorensen SS, Feldt-Rasmussen U, Saleem MA, Petersen CM, Verroust PJ, Christensen EI (2011) Receptor-mediated endocytosis of alpha-galactosidase A in human podocytes in Fabry disease. PLoS One 6:e25065PubMedCrossRef

86.

Yan Q, Sun W, Kujala P, Lotfi Y, Vida TA, Bean AJ (2005) CART: an Hrs/actinin-4/BERP/myosin V protein complex required for efficient receptor recycling. Mol Biol Cell 16:2470–2482PubMedCrossRef

87.

Khurana S, Chakraborty S, Lam M, Liu Y, Su YT, Zhao X, Saleem MA, Mathieson PW, Bruggeman LA, Kao HY (2012) Familial Focal Segmental Glomerulosclerosis (FSGS)-linked alpha-Actinin 4 (ACTN4) protein mutants lose ability to activate transcription by nuclear hormone receptors. J Biol Chem 287:12027–12035PubMedCrossRef

88.

Asparuhova MB, Gelman L, Chiquet M (2009) Role of the actin cytoskeleton in tuning cellular responses to external mechanical stress. Scand J Med Sci Sports 19:490–499PubMedCrossRef

89.

Asanuma K, Yanagida-Asanuma E, Faul C, Tomino Y, Kim K, Mundel P (2006) Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat Cell Biol 8:485–491PubMedCrossRef

90.

Wu C, Horowitz A (2011) Membrane traffic as a coordinator of cell migration and junction remodeling. Commun Integr Biol 4:703–705PubMed

91.

Marzesco AM, Dunia I, Pandjaitan R, Recouvreur M, Dauzonne D, Benedetti EL, Louvard D, Zahraoui A (2002) The small GTPase Rab13 regulates assembly of functional tight junctions in epithelial cells. Mol Biol Cell 13:1819–1831PubMedCrossRef

92.

Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, Diaspro A, Lanzetti L, Scita G, Di Fiore PP (2008) Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134:135–147PubMedCrossRef

93.

Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12:218–222PubMedCrossRef

94.

Greka A, Mundel P (2011) Balancing calcium signals through TRPC5 and TRPC6 in podocytes. J Am Soc Nephrol 22:1969–1980PubMedCrossRef

95.

Tian D, Jacobo SM, Billing D, Rozkalne A, Gage SD, Anagnostou T, Pavenstadt H, Hsu HH, Schlondorff J, Ramos A, Greka A (2011) Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci Signal 3:ra77CrossRef

96.

van de Graaf SF, Hoenderop JG, Bindels RJ (2006) Regulation of TRPV5 and TRPV6 by associated proteins. Am J Physiol Renal Physiol 290:F1295–F1302PubMedCrossRef

97.

Toro CA, Arias LA, Brauchi S (2011) Sub-cellular distribution and translocation of TRP channels. Curr Pharm Biotechnol 12:12–23PubMedCrossRef

98.

Kim BJ, Jeon JH, Kim SJ, So I (2007) Role of calmodulin and myosin light chain kinase in the activation of carbachol-activated cationic current in murine ileal myocytes. Can J Physiol Pharmacol 85:1254–1262PubMedCrossRef

99.

Shi J, Mori E, Mori Y, Mori M, Li J, Ito Y, Inoue R (2004) Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cells. J Physiol 561:415–432PubMedCrossRef

100.

Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE (2004) Rapid vesicular translocation and insertion of TRP channels. Nature Cell Biol 6:709–720PubMedCrossRef

101.

van de Graaf SF, Chang Q, Mensenkamp AR, Hoenderop JG, Bindels RJ (2006) Direct interaction with Rab11a targets the epithelial Ca2+ channels TRPV5 and TRPV6 to the plasma membrane. Mol Cell Biol 26:303–312PubMedCrossRef

102.

Huber TB, Schermer B, Benzing T (2007) Podocin organizes ion channel-lipid supercomplexes: implications for mechanosensation at the slit diaphragm. Nephron 106:e27–e31PubMed

103.

Duttmann M, Togashi Y, Yanagida T, Mikhailov AS (2012) Myosin-V as a mechanical sensor: an elastic network study. Biophys J 102:542–551PubMedCrossRef

104.

Cheney RE, Rodriguez OC (2001) Cell biology. A switch to release the motor. Science 293:1263–1264PubMedCrossRef

105.

Karcher RL, Roland JT, Zappacosta F, Huddleston MJ, Annan RS, Carr SA, Gelfand VI (2001) Cell cycle regulation of myosin-V by calcium/calmodulin-dependent protein kinase II. Science 293:1317–1320PubMedCrossRef

106.

Huber TB, Hartleben B, Kim J, Schmidts M, Schermer B, Keil A, Egger L, Lecha RL, Borner C, Pavenstadt H, Shaw AS, Walz G, Benzing T (2003) Nephrin and CD2AP associate with phosphoinositide 3-OH kinase and stimulate AKT-dependent signaling. Mol Cell Biol 23:4917–4928PubMedCrossRef

107.

Mellor P, Furber LA, Nyarko JN, Anderson DH (2012) Multiple roles for the p85alpha isoform in the regulation and function of PI3K signalling and receptor trafficking. Biochem J 441:23–37PubMedCrossRef

108.

Zhu J, Sun N, Aoudjit L, Li H, Kawachi H, Lemay S, Takano T (2008) Nephrin mediates actin reorganization via phosphoinositide 3-kinase in podocytes. Kidney Int 73:556–566PubMedCrossRef

109.

Coward RJ, Foster RR, Patton D, Ni L, Lennon R, Bates DO, Harper SJ, Mathieson PW, Saleem MA (2005) Nephrotic plasma alters slit diaphragm-dependent signaling and translocates nephrin, Podocin, and CD2 associated protein in cultured human podocytes. J Am Soc Nephrol 16:629–637PubMedCrossRef

110.

Garg P, Rabelink T (2011) Glomerular proteinuria: a complex interplay between unique players. Adv Chronic Kidney Dis 18:233–242PubMedCrossRef

111.

Gigante M, Piemontese M, Gesualdo L, Iolascon A, Aucella F (2011) Molecular and genetic basis of inherited nephrotic syndrome. Int J Nephrol 2011:792195PubMed

112.

Iwano M (2010) EMT and TGF-beta in renal fibrosis. Front Biosci (Schol Ed) 2:229–238CrossRef

113.

El Hindi S, Reiser J (2011) TRPC channel modulation in podocytes-inching toward novel treatments for glomerular disease. Pediatr Nephrol 26:1057–1064PubMedCrossRef

114.

Moller CC, Wei C, Altintas MM, Li J, Greka A, Ohse T, Pippin JW, Rastaldi MP, Wawersik S, Schiavi S, Henger A, Kretzler M, Shankland SJ, Reiser J (2007) Induction of TRPC6 channel in acquired forms of proteinuric kidney disease. J Am Soc Nephrol 18:29–36PubMedCrossRef

115.

Utech M, Mennigen R, Bruewer M (2010) Endocytosis and recycling of tight junction proteins in inflammation. J Biomed Biotechol 2010:e484987

116.

Helal I, Fick-Brosnahan GM, Reed-Gitomer B, Schrier RW (2012) Glomerular hyperfiltration: definitions, mechanisms and clinical implications. Nat Rev Nephrol 8:293–300PubMedCrossRef

117.

Hsu HH, Hoffmann S, Endlich N, Velic A, Schwab A, Weide T, Schlatter E, Pavenstadt H (2008) Mechanisms of angiotensin II signaling on cytoskeleton of podocytes. J Mol Med 86:1379–1394PubMedCrossRef

118.

Ren Z, Liang W, Chen C, Yang H, Singhal PC, Ding G (2012) Angiotensin II induces nephrin dephosphorylation and podocyte injury: role of caveolin-1. Cell Signal 24:443–450PubMedCrossRef

119.

Eto N, Wada T, Inagi R, Takano H, Shimizu A, Kato H, Kurihara H, Kawachi H, Shankland SJ, Fujita T, Nangaku M (2007) Podocyte protection by darbepoetin: preservation of the cytoskeleton and nephrin expression. Kidney Int 72:455–463PubMedCrossRef

120.

Wei C, El Hindi S, Li J, Fornoni A, Goes N, Sageshima J, Maiguel D, Karumanchi SA, Yap HK, Saleem M, Zhang Q, Nikolic B, Chaudhuri A, Daftarian P, Salido E, Torres A, Salifu M, Sarwal MM, Schaefer F, Morath C, Schwenger V, Zeier M, Gupta V, Roth D, Rastaldi MP, Burke G, Ruiz P, Reiser J (2011) Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat Med 17:952–960PubMedCrossRef

121.

Yang H (2010) Nanoparticle-mediated brain-specific drug delivery, imaging, and diagnosis. Pharm Res 27:1759–1771PubMedCrossRef

122.

Eyre J, Ioannou K, Grubb BD, Saleem MA, Mathieson PW, Brunskill NJ, Christensen EI, Topham PS (2007) Statin-sensitive endocytosis of albumin by glomerular podocytes. Am J Physiol Renal Physiol 292:F674–F681PubMedCrossRef

123.

Chiang WC, Geel TM, Altintas MM, Sever S, Ruiters MH, Reiser J (2010) Establishment of protein delivery systems targeting podocytes. PloS O ne 5:e11837CrossRef

Title: Membrane trafficking in podocyte health and disease
Author: Agnieszka Swiatecka-Urban
Publication date: 01-09-2013
Publisher: Springer Berlin Heidelberg
Published in: Pediatric Nephrology / Issue 9/2013
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI: https://doi.org/10.1007/s00467-012-2281-y

At a glance: The STEP trials

Springer Medicine

Membrane trafficking in podocyte health and disease

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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