Vps34 deficiency reveals the importance of endocytosis for podocyte homeostasis

Journal of the American Society of Nephrology

Volumn 24, Issue 5, 2013, Pages 727-743

  Bechtel, Wibke ^a   Helmstädter, Martin ^a,b   Balica, Jan ^a   Hartleben, Björn ^a   Kiefer, Betina ^a   Hrnjic, Fatima ^a   Schell, Christoph ^a,b   Kretz, Oliver ^b   Liu, Shuya ^a,b   Geist, Felix ^a   Kerjaschki, Dontscho ^c   Walz, Gerd ^a,b   Huber, Tobias B ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL 3 KINASE; PODOCIN; RAB PROTEIN; RAB7 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL COMPARTMENTALIZATION; CELL DEGENERATION; CELL PROLIFERATION; CELL VACUOLE; CONTROLLED STUDY; DISEASE SEVERITY; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; ENDOSOME; GLOMERULAR FILTRATION BARRIER; GLOMERULOSCLEROSIS; HOMEOSTASIS; INTRACELLULAR SPACE; MOUSE; NONHUMAN; PHENOTYPE; PHOSPHATIDYLINOSITOL 3 KINASE DEFICIENCY; PODOCYTE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEINURIA; SCAR FORMATION; SIGNAL TRANSDUCTION;

EID: 84877097595     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012070700     Document Type: Article

References (61)

1. Farquhar MG, Vernier RL, Good RA: An electron microscope study of the glomerulus in nephrosis, glomerulonephritis, and lupus erythematosus. J Exp Med 106: 649-660, 1957
2. Farquhar MG, Palade GE: Segregation of ferritin in glomerular protein absorption droplets. J Biophys Biochem Cytol 7: 297-304, 1960
3. Farquhar MG, Palade GE: Glomerular permeability. II. Ferritin transfer across the glomerular capillary wall in nephrotic rats. J Exp Med 114: 699-716, 1961
4. Farquhar MG, Wissig SL, Palade GE: Glomerular permeability. I. Ferritin transfer across the normal glomerular capillary wall. J Exp Med 113: 47-66, 1961
5. Caulfield JP, Farquhar MG: The permeability of glomerular capillaries to graded dextrans. Identification of the basement membrane as the primary filtration barrier. J Cell Biol 63: 883-903, 1974
6. Vogt A, Bockhorn H, Kozima K, Sasaki M: Electron microscopic localization of the nephrotoxic antibody in the glomeruli of the rat after intravenous application of purified nephritogenic antibody-ferritin conjugates. J Exp Med 127: 867-878, 1968
7. Venkatachalam MA, Cotran RS, Karnovsky MJ: An ultrastructural study of glomerular permeability in aminonucleoside nephrosis using catalase as a tracer protein. J Exp Med 132: 1168-1180, 1970
8. Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V, Maschke U, Purfürst B, Schneider W, Rump LC, Luft FC, Dechend R, Bader M, Huber TB, Nguyen G, Muller DN: Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 22: 2193-2202, 2011
9. Marsh M, McMahon HT: The structural era of endocytosis. Science 285: 215-220, 1999 (Pubitemid 29329987)
10. McMahon HT, Boucrot E: Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533, 2011
11. Rastaldi MP, Armelloni S, Berra S, Calvaresi N, Corbelli A, Giardino LA, Li M, Wang GQ, Fornasieri A, Villa A, Heikkila E, Soliymani R, Boucherot A, Cohen CD, Kretzler M, Nitsche A, Ripamonti M, Malgaroli A, Pesaresi M, Forloni GL, Schlöndorff D, Holthofer H, D'Amico G: Glomerular podocytes contain neuron-like functional synaptic vesicles. FASEB J 20: 976-978, 2006
12. Prabakaran T, Nielsen R, Larsen JV, Sørensen SS, Feldt-Rasmussen U, Saleem MA, Petersen CM, Verroust PJ, Christensen EI: Receptor-mediated endocytosis of α-galactosidase A in human podocytes in Fabry disease. PLoS One 6: e25065, 2011
13. Longatti A, Tooze SA: Vesicular traf ficking and autophagosome formation. Cell Death Differ 16: 956-965, 2009
14. Tooze SA, Yoshimori T: The origin of the autophagosomal membrane. Nat Cell Biol 12: 831-835, 2010
15. Balla T: Phosphoinositide-derived messengers in endocrine signaling. J Endocrinol 188: 135-153, 2006
16. Herman PK, Emr SD: Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol Cell Biol 10: 6742-6754, 1990 (Pubitemid 120004619)
17. Backer JM: The regulation and function of Class III PI3Ks: Novel roles for Vps34. Biochem J 410: 1-17, 2008
18. Juhász G, Hill JH, Yan Y, Sass M, Baehrecke EH, Backer JM, Neufeld TP: The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 181: 655-666, 2008 (Pubitemid 351717512)
19. Cheung PC, Trinkle-Mulcahy L, Cohen P, Lucocq JM: Characterization of a novel phosphatidylinositol 3-phosphate-binding protein containing two FYVE fingers in tandem that is targeted to the Golgi. Biochem J 355: 113-121, 2001 (Pubitemid 32304241)
20. Lemmon SK, Traub LM: Sorting in the endosomal system in yeast and animal cells. Curr Opin Cell Biol 12: 457-466, 2000 (Pubitemid 30453597)
21. Odorizzi G, Babst M, Emr SD: Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci 25: 229-235, 2000 (Pubitemid 30236220)
22. Simonsen A, Stenmark H: PX domains: Attracted by phosphoinositides. Nat Cell Biol 3: E179-E182, 2001 (Pubitemid 32734239)
23. Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip SC, Waterfield MD, Backer JM, Zerial M: Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1: 249-252, 1999 (Pubitemid 129500945)
24. Lindmo K, Stenmark H: Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 119: 605-614, 2006
25. Eskelinen EL: Maturation of autophagic vacuoles in Mammalian cells. Autophagy 1: 1-10, 2005
26. Odorizzi G, Babst M, Emr SD: Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95: 847-858, 1998 (Pubitemid 29014464)
27. Kihara A, Noda T, Ishihara N, Ohsumi Y: Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152: 519-530, 2001 (Pubitemid 34280235)
28. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT: Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685-701, 2008
29. Walker S, Chandra P, Manifava M, Axe E, Ktistakis NT: Making autophagosomes: Localized synthesis of phosphatidylinositol 3-phosphate holds the clue. Autophagy 4: 1093-1096, 2008
30. Zhou X, Wang L, Hasegawa H, Amin P, Han BX, Kaneko S, He Y, Wang F: Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc Natl Acad Sci U S A 107: 9424-9429, 2010
31. Jaber N, Dou Z, Chen JS, Catanzaro J, Jiang YP, Ballou LM, Selinger E, Ouyang X, Lin RZ, Zhang J, Zong WX: Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc Natl Acad Sci U S A 109: 2003-2008, 2012
32. Stopkova P, Saito T, Papolos DF, Vevera J, Paclt I, Zukov I, Bersson YB, Margolis BA, Strous RD, Lachman HM: Identification of PIK3C3 promoter variant associated with bipolar disorder and schizophrenia. Biol Psychiatry 55: 981-988, 2004 (Pubitemid 38581913)
33. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB: Podocyte-specific expression of cre recombinase in transgenic mice. Genesis 35: 39-42, 2003 (Pubitemid 36150980)
34. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T: p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171: 603-614, 2005 (Pubitemid 41668720)
35. Rusten TE, Stenmark H: p62, an autophagy hero or culprit? Nat Cell Biol 12: 207-209, 2010
36. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L: A global double-fluorescent Cre reporter mouse. Genesis 45: 593-605, 2007 (Pubitemid 350013057)
37. Hartleben B, Gödel M, Meyer-Schwesinger C, Liu S, Ulrich T, Köbler S, Wiech T, Grahammer F, Arnold SJ, Lindenmeyer MT, Cohen CD, Pavenstädt H, Kerjaschki D, Mizushima N, Shaw AS, Walz G, Huber TB: Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest 120: 1084-1096, 2010
38. Olkkonen VM, Stenmark H: Role of Rab GTPases in membrane traffic. Int Rev Cytol 176: 1-85, 1997 (Pubitemid 27395619)
39. Simonsen A, Lippé R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H: EEA1 links PI(3) K function to Rab5 regulation of endosome fusion. Nature 394: 494-498, 1998 (Pubitemid 28373962)
40. Stenmark H, Parton RG, Steele-Mortimer O, Lütcke A, Gruenberg J, Zerial M: Inhibition of rab5GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13: 1287-1296, 1994 (Pubitemid 24090209)
41. Vernier RL, Farquhar MG, Brunson JG, Good RA: Chronic renal disease in children; correlation of clinical findings with morphologic characteristics seen by light and electron microscopy. AMA J Dis Child 96: 306-343, 1958
42. Venkatachalam MA, Karnovsky MJ, Cotran RS: Glomerular permeability. Ultrastructural studies in experimental nephrosis using horseradish peroxidase as a tracer. J Exp Med 130: 381-399, 1969
43. Feldman JD, Fisher ER: Renal lesions of aminonucleoside nephrosis as revealed by electron microscopy. Lab Invest 8: 371-385, 1959
44. Rantala I: Glomerular epithelial cell endocytosis of immune deposits in the nephrotic rat. An ultrastructural immunoperoxidase study. Nephron 29: 239-244, 1981
45. Sharon Z, Schwartz MM, Pauli BU, Lewis EJ: Kinetics of glomerular visceral epithelial cell phagocytosis. Kidney Int 14: 526-529, 1978 (Pubitemid 9068295)
46. Kim JM, Wu H, Green G, Winkler CA, Kopp JB, Miner JH, Unanue ER, Shaw AS: CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 300: 1298-1300, 2003 (Pubitemid 36618242)
47. Harris DP, Vogel P, Wims M, Moberg K, Humphries J, Jhaver KG, DaCosta CM, Shadoan MK, Xu N, Hansen GM, Balakrishnan S, Domin J, Powell DR, Oravecz T: Requirement for class II phosphoinositide 3-kinase C2alpha in maintenance of glomerular structure and function. Mol Cell Biol 31: 63-80, 2011
48. Stenmark H, Aasland R, Driscoll PC: The phosphatidylinositol 3-phosphate-binding FYVE finger. FEBS Lett 513: 77-84, 2002 (Pubitemid 34242982)
49. Byfield MP, Murray JT, Backer JM: hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082, 2005 (Pubitemid 41368357)
50. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, Gulati P, Byfield MP, Backer JM, Natt F, Bos JL, Zwartkruis FJ, Thomas G: Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci U S A 102: 14238-14243, 2005 (Pubitemid 41429682)
51. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, Mi N, Zhao Y, Liu Z, Wan F, Hailey DW, Oorschot V, Klumperman J, Baehrecke EH, Lenardo MJ: Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465: 942-946, 2010
52. Cinà DP, Onay T, Paltoo A, Li C, Maezawa Y, De Arteaga J, Jurisicova A, Quaggin SE: Inhibition of MTOR disrupts autophagic flux in podocytes. J Am Soc Nephrol 23: 412-420, 2012
53. Pavenstädt H, Kriz W, Kretzler M: Cell biology of the glomerular podocyte. Physiol Rev 83: 253-307, 2003 (Pubitemid 36459882)
54. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE: Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111: 707-716, 2003 (Pubitemid 36278589)
55. Guan F, Villegas G, Teichman J, Mundel P, Tufro A: Autocrine VEGF-A system in podocytes regulates podocin and its interaction with CD2AP. Am J Physiol Renal Physiol 291: F422-F428, 2006 (Pubitemid 44148132)
56. Weavers H, Prieto-Sánchez S, Grawe F, Garcia-López A, Artero R, Wilsch-Bräuninger M, Ruiz-Gómez M, Skaer H, Denholm B: The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm. Nature 457: 322-326, 2009
57. Denholm B, Skaer H: Bringing together components of the fly renal system. Curr Opin Genet Dev 19: 526-532, 2009
58. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N: Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889, 2006
59. Raij L, Azar S, Keane W: Mesangial immune injury, hypertension, and progressive glomerular damage in Dahl rats. Kidney Int 26: 137-143, 1984 (Pubitemid 14017051)
60. van den Berg JG, van den Bergh Weerman MA, Assmann KJ, Weening JJ, Florquin S: Podocyte foot process effacement is not correlated with the level of proteinuria in human glomerulopathies. Kidney Int 66: 1901-1906, 2004
61. Takemoto M, Asker N, Gerhardt H, Lundkvist A, Johansson BR, Saito Y, Betsholtz C: A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 161: 799-805, 2002 (Pubitemid 34988366)