The function of endocytosis in podocytes

Current Opinion in Nephrology and Hypertension

Volumn 22, Issue 4, 2013, Pages 432-438

  Soda, Keita ^a   Ishibe, Shuta ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endocytosis; Nephrotic syndrome; Podocytes

Indexed keywords

ACTIN; CLATHRIN; DYNAMIN; ENDOPHILIN; NEPHRIN; SYNAPTOJANIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; BASEMENT MEMBRANE; CELL MEMBRANE; ELECTRON MICROSCOPY; ENDOCYTOSIS; HUMAN; NEPHROTIC SYNDROME; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEINURIA; REVIEW; SUMOYLATION; UBIQUITINATION;

ACTIN CYTOSKELETON; ANIMALS; CLATHRIN-COATED VESICLES; COATED PITS, CELL-MEMBRANE; ENDOCYTOSIS; HUMANS; NEPHROTIC SYNDROME; PODOCYTES; PROTEIN TRANSPORT; PROTEINURIA; SIGNAL TRANSDUCTION;

EID: 84879220425     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0b013e3283624820     Document Type: Review

References (83)

1. Jarad G, Miner JH. Update on the glomerular filtration barrier. Curr Opin Nephrol Hypertens 2009; 18:226-232.
2. Kestila M, Lenkkeri U, Mannikko M, et al. Positionally cloned gene for a novel glomerular protein-nephrin-is mutated in congenital nephrotic syndrome. Mol Cell 1998; 1:575-582.
3. Ruotsalainen V, Ljungberg P, Wartiovaara J, et al. Nephrin is specifically located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci U S A 1999; 96:7962-7967.
4. Boute N, Gribouval O, Roselli S, et al. NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 2000; 24:349-354.
5. Has C, Sparta G, Kiritsi D, et al. Integrin alpha3 mutations with kidney, lung, and skin disease. N Engl J Med 2012; 366:1508-1514.
6. Nicolaou N, Margadant C, Kevelam SH, et al. Gain of glycosylation in integrin alpha3 causes lung disease and nephrotic syndrome. J Clin Invest 2012; 122:4375-4387.
7. Kim JM, Wu H, Green G, et al. CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 2003; 300:1298-1300.
8. Kaplan JM, Kim SH, North KN, et al. Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 2000; 24:251-256.
9. Mele C, Iatropoulos P, Donadelli R, et al. MYO1E mutations and childhood familial focal segmental glomerulosclerosis. N Engl J Med 2011; 365:295-306.
10. Genovese G, Tonna SJ, Knob AU, et al. A risk allele for focal segmental glomerulosclerosis in African Americans is located within a region containing APOL1 and MYH9. Kidney Int 2010; 78:698-704.
11. 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.
12. Reiser J, Polu KR, Moller CC, et al. TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 2005; 37:739-744.
13. Rastaldi MP, Armelloni S, Berra S, et al. Glomerular podocytes contain neuron-like functional synaptic vesicles. FASEB J 2006; 20:976-978.
14. Shen K, Fetter RD, Bargmann CI. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 2004; 116:869-881.
15. Boyer O, Nevo F, Plaisier E, et al. INF2 mutations in Charcot-Marie-Tooth disease with glomerulopathy. N Engl J Med 2011; 365:2377-2388.
16. Farquhar MG, Vernier RL, Good RA. An electron microscope study of the glomerulus in nephrosis, glomerulonephritis, and lupus erythematosus. J Exp Med 1957; 106:649-660.
17. Kerjaschki D, Farquhar MG. Immunocytochemical localization of the Heymann nephritis antigen (GP330) in glomerular epithelial cells of normal Lewis rats. J Exp Med 1983; 157:667-686.
18. McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2011; 12:517-533.
19. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 2009; 78:857-902.
20. Ferguson SM, Raimondi A, Paradise S, et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 2009; 17:811-822.
21. Ferguson SM, De Camilli P. Dynamin, a membrane remodeling GTPase. Nat Rev Mol Cell Biol 2012; 13:75-88.
22. Sever S, Altintas MM, Nankoe SR, et al. Proteolytic processing of dynamin by cytoplasmic cathepsin L is a mechanism for proteinuric kidney disease. J Clin Invest 2007; 117:2095-2104.
23. Soda K, Balkin DM, Ferguson SM, et al. Role of dynamin, synaptojanin, and endophilin in podocyte foot processes. J Clin Invest 2012; 122:4401-4411.
24. McPherson PS, Garcia EP, Slepnev VI, et al. A presynaptic inositol-5-phosphatase. Nature 1996; 379:353-357.
25. Cremona O, Di Paolo G, Wenk MR, et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 1999; 99:179-188.
26. Milosevic I, Giovedi S, Lou X, et al. Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 2011; 72:587-601.
27. Gallop JL, Jao CC, Kent HM, et al. Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 2006; 25:2898-2910.
28. Inoki K, Mori H, Wang J, et al. mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 2011; 121:2181-2196.
29. Harris DP, Vogel P, Wims M, et al. Requirement for class II phosphoinositide 3-kinase C2alpha in maintenance of glomerular structure and function. Mol Cell Biol 2011; 31:63-80.
30. Prabakaran T, Nielsen R, Larsen JV, et al. Receptor-mediated endocytosis of alpha-galactosidase A in human podocytes in Fabry disease. PLoS One 2011; 6:e25065.
31. Ceol M, Tiralongo E, Baelde HJ, et al. Involvement of the tubular ClC-type exchanger ClC-5 in glomeruli of human proteinuric nephropathies. PLoS One 2012; 7:e45605.
32. Faul C, Asanuma K, Yanagida-Asanuma E, et al. Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 2007; 17:428-437.
33. Verma R, Kovari I, Soofi A, et al. Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J Clin Invest 2006; 116:1346-1359.
34. Jones N, Blasutig IM, Eremina V, et al. Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 2006; 440:818-823.
35. Asanuma K, Yanagida-Asanuma E, Faul C, et al. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat Cell Biol 2006; 8:485-491.
36. Yaddanapudi S, Altintas MM, Kistler AD, et al. CD2AP in mouse and human podocytes controls a proteolytic program that regulates cytoskeletal structure and cellular survival. J Clin Invest 2011; 121:3965-3980.
37. Galletta BJ, Mooren OL, Cooper JA. Actin dynamics and endocytosis in yeast and mammals. Curr Opin Biotechnol 2010; 21:604-610.
38. Berro J, Sirotkin V, Pollard TD. Mathematical modeling of endocytic actin patch kinetics in fission yeast: disassembly requires release of actin filament fragments. Mol Biol Cell 2010; 21:2905-2915.
39. Sirotkin V, Berro J, Macmillan K, et al. Quantitative analysis of the mechanism of endocytic actin patch assembly and disassembly in fission yeast. Mol Biol Cell 2010; 21:2894-2904.
40. Boulant S, Kural C, Zeeh JC, et al. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 2011; 13:1124-1131.
41. Taylor MJ, Perrais D, Merrifield CJ. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 2011; 9:e1000604.
42. Taylor MJ, Lampe M, Merrifield CJ. A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 2012; 10:e1001302.
43. Yarar D, Waterman-Storer CM, Schmid SL. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 2005; 16:964-975.
44. Gu C, Yaddanapudi S, Weins A, et al. Direct dynamin-actin interactions regulate the actin cytoskeleton. EMBO J 2010; 29:3593-3606.
45. Krueger EW, Orth JD, Cao H, McNiven MA. A dynamin-cortactin-Arp2/3 complex mediates actin reorganization in growth factor-stimulated cells. Mol Biol Cell 2003; 14:1085-1096.
46. Merrifield CJ, Qualmann B, Kessels MM, Almers W. Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited tosites of clathrin-mediated endocytosis in cultured fibroblasts. Eur J Cell Biol 2004; 83:13-18.
47. Perera RM, Zoncu R, Lucast L, et al. Two synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages. Proc Natl Acad Sci U S A 2006; 103:19332-19337.
48. Krendel M, Osterweil EK, Mooseker MS. Myosin 1E interacts with synapto-janin-1 and dynamin and is involved in endocytosis. FEBS Lett 2007; 581:644-650.
49. Krendel M, Kim SV, Willinger T, et al. Disruption of Myosin 1e promotes podocyte injury. J Am Soc Nephrol 2009; 20:86-94.
50. Welsch T, Endlich N, Gokce G, et al. Association of CD2AP with dynamic actin on vesicles in podocytes. Am J Physiol Renal Physiol 2005; 289: F1134-F1143.
51. Fawcett JP, Georgiou J, Ruston J, et al. Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc Natl Acad Sci U S A 2007; 104:20973-20978.
52. Zhu J, Sun N, Aoudjit L, et al. Nephrin mediates actin reorganization via phosphoinositide 3-kinase in podocytes. Kidney Int 2008; 73:556-566.
53. Quaggin SE, Kreidberg JA. Development of the renal glomerulus: good neighbors and good fences. Development 2008; 135:609-620.
54. Liu G, Kaw B, Kurfis J, et al. Neph1 and nephrin interaction in the slit diaphragm is an important determinant of glomerular permeability. J Clin Invest 2003; 112:209-221.
55. Barletta GM, Kovari IA, Verma RK, et al. Nephrin and Neph1 co-localize at the podocyte foot process intercellular junction and form cis hetero-oligomers. J Biol Chem 2003; 278:19266-19271.
56. Fukasawa H, Bornheimer S, Kudlicka K, Farquhar MG. Slit diaphragms contain tight junction proteins. J Am Soc Nephrol 2009; 20:1491-1503.
57. Huber TB, Hartleben B, Kim J, et al. Nephrin and CD2AP associate with phosphoinositide 3-OH kinase and stimulate AKT-dependent signaling. Mol Cell Biol 2003; 23:4917-4928.
58. Huber TB, Kottgen M, Schilling B, et al. Interaction with podocin facilitates nephrin signaling. J Biol Chem 2001; 276:41543-41546.
59. Schwarz K, Simons M, Reiser J, et al. Podocin, a raft-associated component of the glomerular slit diaphragm, interacts with CD2AP and nephrin. J Clin Invest 2001; 108:1621-1629.
60. Nishibori Y, Liu L, Hosoyamada M, et al. Disease-causing missense mutations in NPHS2 gene alter normal nephrin trafficking to the plasma membrane. Kidney Int 2004; 66:1755-1765.
61. Tossidou I, Teng B, Menne J, et al. Podocytic PKC-alpha is regulated in murine and human diabetes and mediates nephrin endocytosis. PLoS One 2010; 5:e10185.
62. Qin XS, Tsukaguchi H, Shono A, et al. Phosphorylation of nephrin triggers its internalization by raft-mediated endocytosis. J Am Soc Nephrol 2009; 20:2534-2545.
63. Quack I, Rump LC, Gerke P, et al. beta-Arrestin2 mediates nephrin endocy-tosis and impairs slit diaphragm integrity. Proc Natl Acad Sci U S A 2006; 103:14110-14115.
64. Quack I, Woznowski M, Potthoff SA, et al. PKC alpha mediates beta-arrestin2-dependent nephrin endocytosis in hyperglycemia. J Biol Chem 2011; 286: 12959-12970.
65. Tossidou I, Niedenthal R, Klaus M, et al. CD2AP regulates SUMOylation of CIN85 in podocytes. Mol Cell Biol 2012; 32:1068-1079.
66. Waters AM, Wu MY, Huang YW, et al. Notch promotes dynamin-dependent endocytosis of nephrin. J Am Soc Nephrol 2012; 23:27-35.
67. Wasik AA, Polianskyte-Prause Z, Dong MQ, et al. Septin 7 forms a complex with CD2AP and nephrin and regulates glucose transporter trafficking. Mol Biol Cell 2012; 23:3370-3379.
68. Jeon J, Leibiger I, Moede T, et al. Dynamin-mediated Nephrin phosphorylation regulates glucose-stimulated insulin release in pancreatic beta cells. J Biol Chem 2012; 287:28932-28942.
69. Zhuang S, Shao H, Guo F, et al. Sns and Kirre, the Drosophila orthologs of Nephrin and Neph1, direct adhesion, fusion and formation of a slit diaphragmlike structure in insect nephrocytes. Development 2009; 136:2335-2344.
70. Balklava Z, Pant S, Fares H, Grant BD. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 2007; 9:1066-1073.
71. Hartleben B, Schweizer H, Lubben P, et al. Neph-Nephrin proteins bind the Par3-Par6-atypical protein kinase C (aPKC) complex to regulate podocyte cell polarity. J Biol Chem 2008; 283:23033-23038.
72. Hirose T, Satoh D, Kurihara H, et al. An essential role of the universal polarity protein, aPKClambda, on the maintenance of podocyte slit diaphragms. PLoS One 2009; 4:e4194.
73. Scott RP, Hawley SP, Ruston J, et al. Podocyte-specific loss of Cdc42 leads to congenital nephropathy. J Am Soc Nephrol 2012; 23:1149-1154.
74. Kreidberg JA, Donovan MJ, Goldstein SL, et al. Alpha 3 beta 1 integrin has a crucial roleinkidney and lung organogenesis. Development 1996; 122:3537-3547.
75. Pozzi A, Jarad G, Moeckel GW, et al. Beta1 integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol 2008; 316: 288-301.
76. Tian D, Jacobo SM, Billing D, et al. Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci Signal 2010; 3:ra77.
77. Riediger F, Quack I, Qadri F, et al. Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 2011; 22:2193-2202.
78. Oshima Y, Kinouchi K, Ichihara A, et al. Prorenin receptor is essential for normal podocyte structure and function. J Am Soc Nephrol 2011; 22:2203-2212.
79. Hartleben B, Godel M, Meyer-Schwesinger C, et al. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest 2010; 120:1084-1096.
80. Cina DP, Onay T, Paltoo A, et al. Inhibition of MTOR disrupts autophagic flux in podocytes. J Am Soc Nephrol 2012; 23:412-420.
81. Chen J, Chen MX, Fogo AB, et al. mVps34 deletion in podocytes causes glomerulosclerosis by disrupting intracellular vesicle trafficking. J Am Soc Nephrol 2013; 24:198-207.
82. Jin J, Sison K, Li C, et al. Soluble FLT1 binds lipid microdomains in podocytes to control cell morphology and glomerular barrier function. Cell 2012; 151:384-399.
83. Akilesh S, Huber TB, Wu H, et al. Podocytes use FcRn to clear IgG from the glomerular basement membrane. Proc Natl Acad Sci U S A 2008; 105:967-972.