Mammalian CORVET is required for fusion and conversion of distinct early endosome subpopulations

Traffic

Volumn 15, Issue 12, 2014, Pages 1366-1389

  Perini, Enrico D ^a   Schaefer, Ramona ^a   Stöter, Martin ^a   Kalaidzidis, Yannis ^a,b   Zerial, Marino ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

APPL1; CORVET; Early endosomes; EEA1; Endocytosis; HOPS; Tethering factor

Indexed keywords

APPL1 PROTEIN; CORE VACUOLE ENDOSOME TETHERING PROTEIN; EARLY ENDOSOME ANTIGEN 1; PROTEIN; RAB PROTEIN; TGFBRAP1 PROTEIN; UNCLASSIFIED DRUG; VPS8 PROTEIN; PROTEIN BINDING; VESICULAR TRANSPORT PROTEIN;

AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BIOINFORMATICS; CELL FUSION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOSOME; HELA CELL LINE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; LIVER CYTOSOL; MAMMAL CELL; MOUSE; NONHUMAN; ORTHOLOGY; PHENOTYPE; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TRANSPORT KINETICS; WESTERN BLOTTING; ANIMAL; GENETICS; HUMAN; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; ENDOSOMES; HELA CELLS; HUMANS; MICE; PROTEIN BINDING; PROTEIN TRANSPORT; VESICULAR TRANSPORT PROTEINS;

EID: 84911428413     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12232     Document Type: Article

References (52)

1. Rusten TE, Haglund K, Stenmark H. Aberrant receptor signaling and trafficking as mechanisms in oncogenesis. Crit Rev Oncog 2007;13:39-74.
2. Mosesson Y, Mills GB, Yarden Y. Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 2008;8:835-850.
3. Nixon RA. The role of autophagy in neurodegenerative disease. Nat Med 2013;19:983-997.
4. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005;122:735-749.
5. Foret L, Dawson JE, Villaseñor R, Collinet C, Deutsch A, Brusch L, Zerial M, Kalaidzidis Y, Jülicher F. A general theoretical framework to infer endosomal network dynamics from quantitative image analysis. Curr Biol 2012;22:1381-1390.
6. Del Conte-Zerial P, Brusch L, Rink JC, Collinet C, Kalaidzidis Y, Zerial M, Deutsch A. Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol Syst Biol 2008;4:206.
7. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
8. Pfeffer S, Aivazian D. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 2004;5:886-896.
9. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A. Rab GTPases at a glance. J Cell Sci 2008;121:246.
10. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009;10:513-525.
11. Whyte JRC, Munro S. Vesicle tethering complexes in membrane traffic. J Cell Sci 2002;115:2627-2637.
12. Yu I-M, Hughson FM. Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 2010;26:137-156.
13. 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 1998;394:494-498.
14. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 1999;397:621-625.
15. Mills IG, Jones AT, Clague MJ. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol 1998;8:881-884.
16. Peplowska K, Markgraf DF, Ostrowicz CW, Bange G, Ungermann C. The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Cell 2007;12:739-750.
17. Balderhaar HJ, Lachmann J, Yavavli E, Bröcker C, Lürick A, Ungermann C. The CORVET complex promotes tethering and fusion of Rab5/Vps21-positive membranes. Proc Natl Acad Sci USA 2013;2013:1-6.
18. Cabrera M, Arlt H, Epp N, Lachmann J, Griffith J, Perz A, Reggiori F, Ungermann C. Functional separation of endosomal fusion factors and the class C core vacuole/endosome tethering (CORVET) complex in endosome biogenesis. J Biol Chem 2013;288:5166-5175.
19. Hickey CM, Wickner W. HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Mol Biol Cell 2010;21:2297-2305.
20. Bröcker C, Kuhlee A, Gatsogiannis C, kleine Balderhaar HJ, Hönscher C, Engelbrecht-Vandré S, Ungermann C, Raunser S. Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc Natl Acad Sci USA 2012;109:1991-1996.
21. Ostrowicz CW, Bröcker C, Ahnert F, Nordmann M, Lachmann J, Peplowska K, Perz A, Auffarth K, Engelbrecht-Vandré S, Ungermann C. Defined subunit arrangement and rab interactions are required for functionality of the HOPS tethering complex. Traffic 2010;11:1334-1346.
22. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A. Identification of the switch in early-to-late endosome transition. Cell 2010;141:497-508.
23. Nordmann M, Cabrera M, Perz A, Bröcker C, Ostrowicz C, Engelbrecht-Vandré S, Ungermann C. The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 2010;20:1654-1659.
24. Epp N, Rethmeier R, Krämer L, Ungermann C. Membrane dynamics and fusion at late endosomes and vacuoles - Rab regulation, multisubunit tethering complexes and SNAREs. Eur J Cell Biol 2011;90:779-785.
25. Caplan S. Human Vam6p promotes lysosome clustering and fusion in vivo. J Cell Biol 2001;154:109-122.
26. Huizing M, Didier A, Walenta J, Anikster Y, Gahl WA, Krämer H. Molecular cloning and characterization of human VPS18, VPS 11, VPS16, and VPS33. Gene 2001;264:241-247.
27. Kim S, Wairkar YP, Daniels RW, DiAntonio A. The novel endosomal membrane protein Ema interacts with the class C Vps-HOPS complex to promote endosomal maturation. J Cell Biol 2010;188:717-734.
28. Nickerson DP, Brett CL, Merz AJ. Vps-C complexes: gatekeepers of endolysosomal traffic. Biol Cell 2010;21:543-551.
29. Pols MS, ten Brink C, Gosavi P, Oorschot V, Klumperman J. The HOPS proteins hVps41 and hVps39 are required for homotypic and heterotypic late endosome fusion. Traffic 2013;14:219-232.
30. Solinger JA, Spang A. Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J 2013;280:2743-2757.
31. Richardson SCW, Winistorfer SC, Poupon V, Luzio JP, Piper RC. Mammalian late vacuole protein sorting orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol Biol Cell 2004;15:1197-1210.
32. Zlatic SA, Tornieri K, L'hernault SW, Faundez V. Clathrin-dependent mechanisms modulate the subcellular distribution of class C Vps/HOPS tether subunits in polarized and non-polarized cells. Mol Biol Cell 2011;22:1699-715.
33. Messler S, Kropp S, Episkopou V, Felici A, Würthner J, Lemke R, Jerabek-Willemsen M, Willecke R, Scheu S, Pfeffer K, Wurthner JU. The TGF-β signaling modulators TRAP1/TGFBRAP1 and VPS39/Vam6/TLP are essential for early embryonic development. Immunobiology 2011;216:343-350.
34. Charng MJ, Zhang D, Kinnunen P, Schneider MD. A novel protein distinguishes between quiescent and activated forms of the type I transforming growth factor beta receptor. J Biol Chem 1998;273:9365-9368.
35. Klinger CM, Klute MJ, Dacks JB. Comparative genomic analysis of multi-subunit tethering complexes demonstrates an ancient pan-eukaryotic complement and sculpting in apicomplexa. PLoS One 2013;8:e76278.
36. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004;116:445-456.
37. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 2009;136:1110-1121.
38. Miaczynska M, Kalaidzidis I, Olchowik M, Hupalowska A, Parton RG, Kalaidzidis Y, Zerial M. APPL endosomes are not obligatory endocytic intermediates but act as stable cargo sorting compartments. (submitted).
39. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389-3402.
40. Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, Yu Y-K. Protein database searches using compositionally adjusted substitution matrices. FEBS J 2005;272:5101-5109.
41. 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 1999;1:249-252.
42. Gorvel JP, Chavrier P, Zerial M, Gruenberg J. rab5 controls early endosome fusion in vitro. Cell 1991;64:915-925.
43. Ohya T, Miaczynska M, Coskun U, Lommer B, Runge A, Drechsel D, Kalaidzidis Y, Zerial M. Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 2009;459:1091-1097.
44. Poser I, Sarov M, Hutchins JRA, Hériché J-K, Toyoda Y, Pozniakovsky A, Weigl D, Nitzsche A, Hegemann B, Bird AW, Pelletier L, Kittler R, Hua S, Naumann R, Augsburg M, et al. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat Methods 2008;5:409-415.
45. Collinet C, Stöter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, Habermann B, Buchholz F, Henschel R, Mueller MS, Nagel WE, Fava E, Kalaidzidis Y, Zerial M. Systems survey of endocytosis by multiparametric image analysis. Nature 2010;464:243-249.
46. Wurthner JU, Frank DB, Felici A, Green HM, Cao Z, Schneider MD, McNally JG, Lechleider RJ, Roberts AB. Transforming growth factor-beta receptor-associated protein 1 is a Smad4 chaperone. J Biol Chem 2001;276:19495-19502.
47. Macé G, Miaczynska M, Zerial M, Nebreda AR. Phosphorylation of EEA1 by p38 MAP kinase regulates mu opioid receptor endocytosis. EMBO J 2005;24:3235-3246.
48. Christoforidis S, Zerial M. Purification and identification of novel Rab effectors using affinity chromatography. Methods 2000;20:403-410.
49. Horiuchi H, Lippé R, McBride HM, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M, Zerial M. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 1997;90:1149-1159.
50. Gilleron J, Querbes W, Zeigerer A, Borodovsky A, Marsico G, Schubert U, Manygoats K, Seifert S, Andree C, Stöter M, Epstein-Barash H, Zhang L, Koteliansky V, Fitzgerald K, Fava E, et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat Biotechnol 2013;31:638-646.
51. Zeigerer A, Gilleron J, Bogorad RL, Marsico G, Nonaka H, Seifert S, Epstein-Barash H, Kuchimanchi S, Peng CG, Ruda VM, Del Conte-Zerial P, Hengstler JG, Kalaidzidis Y, Koteliansky V, Zerial M. Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 2012;485:465-470.
52. Zhu G, Salazar G, Zlatic SA, Fiza B, Doucette MM, Heilman CJ, Levey AI, Faundez V, L'hernault SW. SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery. Mol Biol Cell 2009;20:1223-1240.